From: Subject: Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma : Article : Nature Reviews Cancer Date: Wed, 5 May 2010 18:51:16 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01CAEC83.F1412610" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.5579 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01CAEC83.F1412610 Content-Type: text/html; charset="utf-8" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.nature.com/nrc/journal/v10/n5/full/nrc2818.html =EF=BB=BF Targeting brain = cancer: advances in the molecular pathology of malignant glioma and = medulloblastoma : Article : Nature Reviews Cancer
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Review

Nature Reviews Cancer = 10, 319-331 = (May 2010) | = doi:10.1038/nrc2818

Targeting brain cancer: advances in the molecular pathology = of=20 malignant glioma and medulloblastoma

Jason T. Huse1<= /A>,5<= /A>=20 & Eric C. Holland2<= /A>,3<= /A>,4<= /A>,5<= /A> =20 Ab= out the=20 authors

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Abstract

Malignant brain tumours continue to be the cause of a=20 disproportionate level of morbidity and mortality across a wide range of = individuals. The most common variants in the adult and paediatric = populations =E2=80=94=20 malignant glioma and medulloblastoma, respectively =E2=80=94 have been = the subject of=20 increasingly intensive research over the past two decades that has led = to=20 considerable advances in the understanding of their basic biology and=20 pathogenesis. This Review summarizes these developments in the context = of the=20 evolving notion of molecular pathology and discusses the implications = that this=20 work has on the design of new treatment regimens.

Primary brain tumours consist of a diverse group of = neoplasms that=20 are derived from various different cell lineages. Much like those = arising from=20 other anatomic sites, tumours of the central nervous system (CNS) have=20 historically been classified on the basis of morphological and, more = recently,=20 immunohistochemical features with less emphasis on their underlying = molecular=20 pathogenesis. The past two decades, however, have seen striking advances = in=20 basic brain tumour biology, especially with regard to malignant=20 glioma and medulloblastoma, the most common CNS cancers of adults = and=20 children, respectively. As described more extensively below, malignant = gliomas=20 consist of a broad range of histological entities, the plurality of = which=20 respond poorly to standard therapeutic regimens. For instance, patients = with=20 glioblastoma, the most prevalent and most aggressive glioma variant, = have a=20 median survival of only 15 months1,= =20 2<= /A>.=20 And although radiation and chemotherapy have been more successful in = combating=20 childhood medulloblastoma, with 5-year survival rates now as high as=20 70=E2=80=9380%3<= /A>,=20 the long-term side effectsof these conventional treatment modalities can = be=20 severe.

The detailed molecular characterization of malignant = glioma and=20 medulloblastoma has not only more accurately defined specific = subgroupings in=20 individual morphological categories, but has also laid the groundwork = for the=20 successful augmentation of standard treatment regimens with rationally = designed,=20 targeted therapies. Similarly, and on a more sobering note, increased=20 understanding of the molecular and cellular heterogeneity inherent to = these=20 tumour classes has also emphasized the formidable therapeutic challenges = still=20 remaining.

Morphological = classification

Although microscopic descriptions of brain tumours began = in the=20 early nineteenth century, the classification scheme developed by Bailey = and=20 Cushing4<= /A>=20 in 1926 formed the foundation on which much of modern pathological = diagnosis=20 still rests. Their system proposed that the evolution of CNS neoplasms = from glial=20 or neuronal=20 precursors arrested at particular developmental stages and therefore led = directly to concepts such as histogenesis=20 and cell of origin. Further refinements, most notably by Kernohan5<= /A>=20 and Ringertz6<= /A>,=20 led ultimately to the World Health Organization (WHO) classification, = which was=20 first formalized in 1979 (Ref. 7<= /A>) and=20 updated in 2007 (Ref. 8<= /A>). In=20 addition to a morphological grouping of brain tumours on the basis of = presumed=20 histogenesis, the WHO schemes have been notable for their grading of = individual=20 tumour classes (I, II, III and IV) as a means of reflecting anticipated=20 biological behaviour. In this way, higher grade tumours (grades III and = IV), in=20 the absence of treatment, are expected to follow a more aggressive = clinical=20 course than their lower grade counterparts (grades I and II). = Additionally,=20 although the WHO classification does remain firmly grounded in = morphological=20 criteria, relevant molecular information regarding the different tumour = classes=20 has been integrated over time.

Most gliomas (presumably derived from either mature glia = or their=20 less differentiated precursors (Fi= g.=20 1)) diffusely infiltrate surrounding brain tissue and together = represent a=20 broad diagnostic group, which the WHO divides into astrocytic, = oligodendroglial=20 and mixed (oligoastrocytic) categories8<= /A>=20 (Fi= g.=20 2a). Additionally, the presence of histological features such as = nuclear=20 atypia, increased proliferation, microvascular proliferation and = necrosis=20 typically result in higher grade classification as either anaplastic = glioma or=20 glioblastoma. Glioblastoma is the most malignant variant of diffuse = glioma and,=20 although the generally reliable expression of protein markers such as = glial=20 fibrillary acid protein (GFAP) has = historically placed=20 it in the confines of the astrocytic class, its precise histogenesis = remains=20 unclear despite considerable advances in the understanding of its basic = biology=20 (discussed below). Further complicating matters, it has long been known = that=20 glioblastomas may evolve from lower grade astrocytic neoplasms over time = (secondary glioblastoma), although most of these tumours seem to arise = de novo (primary glioblastoma)9,= =20 1= 0,=20 1= 1,=20 1= 2.


Figure=20 2 | Current World Health Organization (WHO) = classifications for diffuse glioma and medulloblastoma.
a | Schematic showing the = classification of=20 diffuse gliomas of astrocytic and oligodendroglial lineages. = Representative=20 micrographs for each tumour class are given. The hallmark histological = features=20 of glioblastoma, microvascular proliferation (black arrowhead) and=20 pseudopalisading necrosis (black arrows) are also indicated. b | Representative micrographs = of=20 medulloblastoma histological variants. Differentiated nodules (black = arrows) and=20 mitotic figures (black arrowheads) are indicated.

Medulloblastoma is the archetypal primitive = neuroectodermal tumour=20 (PNET), which is thought to arise from immature neuronal precursors in = the=20 cerebellum (Fi= g.=20 1), and is histologically characterized by closely packed small = round blue=20 cells, typically exhibiting notable mitotic activity. Although all=20 medulloblastoma variants carry the most aggressive WHO designation = (grade IV),=20 their distinct morphological features have been associated with = substantial=20 differences in biological behaviour (Fi= g.=20 2b). For instance, the nodular or desmoplastic subtype and closely = related=20 medulloblastoma with extensive nodularity (MBEN) are associated with = relatively=20 favourable prognoses in young children1= 3,=20 1= 4,=20 whereas the large cell/anaplastic variant tends to exhibit a more = aggressive=20 clinical course with a higher incidence of metastatic disease in the=20 neuraxis1= 5,=20 1= 6,=20 1= 7,=20 1= 8.=20 Recent work has demonstrated, perhaps not surprisingly, that many of the = histopathological and clinical distinctions between the aforementioned=20 medulloblastoma and glioma subcategories are grounded in variability at = the=20 molecular level, conclusions that have been further bolstered by = experiments in=20 mouse model systems (Bo= x=20 1).

Bo= x 1 | Modelling brain tumours in mice
  • Fu= ll box=20

Molecular = pathology:=20 diffuse glioma

Numerous molecular abnormalities have been linked with = the=20 underlying biology of diffuse glioma (Fi= g.=20 3). Mutations in the TP53 tumour suppressor gene were first implicated = in=20 gliomagenesis almost 20 years ago owing to the increased development of = gliomas=20 (most commonly astrocytomas) in patients with the rare = cancer-predisposing=20 disorder Li=E2= =80=93Fraumeni=20 syndrome, which is caused by mutations in TP53 (Refs 1= 9, 2= 0).=20 Subsequent investigations found TP53 mutations to = be a=20 frequent characteristic of sporadic low-grade astrocytic tumours and = secondary=20 glioblastomas2= 1.=20 By contrast, primary glioblastomas were initially associated with = genomic=20 amplifications and activating mutations in the epidermal growth factor = receptor=20 (EGFR) locus2= 2,=20 2= 3,=20 2= 4,=20 the most frequent of these being the variant=20 III deletion (vIII) that was found in 20=E2=80=9330% of all primary = glioblastomas=20 and 50=E2=80=9360% of those also exhibiting EGFR=20 amplification2= 5,=20 2= 6.

Figure=20 3 | Schematic of molecular pathways = implicated in the=20 pathogenesis of glioma.
Downstream=20 oncogenic signalling through receptor tyrosine kinases (RTKs) such as = epithelial=20 growth factor receptor (EGFR) and platelet-derived growth factor = receptor=20 (PDGFR) is mediated by the PI3K=E2=80=93AKT=E2=80=93mTOR and = Ras=E2=80=93MAPK networks. Defects in the=20 p53 and RB tumour suppressor pathways are also common. Proteins = exhibiting=20 alterations at the genomic level that define molecular subclasses of = malignant=20 glioma are also indicated: EGFR (red), PDGFR (blue) and NF1 (green). = CDK,=20 cyclin-dependent kinase; NF1, neurofibromin 1; PDK1,=20 3-phosphoinositide-dependent protein kinase 1; PIP2,=20 phosphatidylinositol-4,5-bisphosphate; PIP3,=20 phosphatidylinositol-3,4,5-trisphosphate.

Contemporaneously, a substantial number of = oligodendroglial=20 tumours (60=E2=80=9390%) were found to exhibit a combined loss of = chromosome arms 1p and=20 19q, a genomic abnormality that interestingly predicted less aggressive=20 biological behaviour and a relatively robust response to = chemotherapy2= 7,=20 2= 8,=20 2= 9.=20 Despite the fact that 1p/19q deletion analysis is frequently used in the = diagnosis and management of oligodendroglial neoplasms, the precise = identity of=20 the presumed tumour suppressors resident in these genomic loci remains=20 elusive3= 0.

In more recent years, additional cancer-related genes = and=20 signalling networks have been directly implicated in glioma pathogenesis = (Fi= g.=20 3). The retinoblastoma (Rb)=20 tumour suppressor pathway has been shown to be defective in a = significant number=20 of high-grade gliomas of both astrocytic and oligodendroglial lineage, = whether=20 by inactivating mutations in RB1 itself or amplification of its negative = regulators=20 cyclin-dependent kinase 4 (CDK4) and, less frequently, CDK6 (Refs 3= 1, 3= 2, 3= 3, 3= 4).=20 Analogously, amplification of the p53 antagonists MDM2 and MDM4 have also been found in distinct subsets of = TP53-intact glioblastomas, as have mutations and/or = deletions in=20 the CDKN2A locus that encodes both INK4A and ARF, which = are=20 crucial positive regulators of RB and p53, respectively. Moreover, = recent=20 genome-wide association screens have identified single nucleotide = polymorphisms=20 (SNPs) in the CDKN2A and adjacent CDKN2B loci as risk factors for glioma = development3= 5,=20 3= 6.=20 These studies have also associated SNPs in other genes, such as = regulator of=20 telomere elongation helicase 1 (RTEL1) and telomerase reverse transcriptase (TERT) with increased glioma incidence, providing = the research=20 community with a new set of molecular targets for investigation. These = findings=20 emphasize the importance of perturbed cell cycle regulation through the=20 disruption of the p53 and Rb pathways in glioma pathogenesis. Mouse = modelling=20 has provided further evidence in this regard by demonstrating that = functional=20 loss of either RB or p53 in various experimental contexts can directly = drive=20 glioma formation, decrease disease-free latency and/or increase tumour=20 grade3= 7,=20 3= 8,=20 3= 9,=20 4= 0,=20 4= 1,=20 4= 2,=20 4= 3,=20 4= 4,=20 4= 5,=20 4= 6.

The involvement of receptor tyrosine kinases (RTKs) in = addition to=20 EGFR in gliomagenesis has also been repeatedly demonstrated. Most = notably,=20 enhanced signalling through platelet-derived growth factor = receptor-=CE=B1 (PDGFR=CE=B1) has been found to be a common feature of = low-grade=20 astrocytic and oligodendroglial tumours along with a significant subset = of=20 glioblastoma (discussed below)4= 7,=20 4= 8.=20 Although activating mutations in PDGFRA are = uncommon4= 9,=20 frequent co-expression of both the receptor and its ligand, most = commonly PDGFB, indicates the = potential=20 for autocrine or paracrine loops boosting oncogenic signalling through = the PDGF=20 network. Similar findings regarding hepatocyte growth factor (HGF) and = its RTK=20 MET (also known as = HGFR)=20 have also been reported for glioma5= 0.=20 Therefore, enhanced RTK signalling, whether driven by somatic = mutagenesis or=20 otherwise, seems to be a foundational oncogenic event in the plurality = of=20 malignant gliomas, the effects of which are probably mediated in large = part=20 through oncogenic PI3K=E2=80=93AKT=E2=80=93mTOR and Ras=E2=80=93MAPK = signalling downstream. Underscoring=20 this fact is the not infrequent dysregulation in malignant gliomas of = molecular=20 components in these downstream networks5= 1,=20 5= 2,=20 the most common of which is functional loss of the tumour suppressor PTEN, the primary negative regulator of = PI3K=E2=80=93AKT=E2=80=93mTOR=20 signalling2= 7,=20 5= 3.=20 Mouse modelling has unequivocally verified a central role for RTK = biology in the=20 pathogenesis of malignant glioma, whether signalling is perturbed at the = level=20 of the RTK itself3= 7,=20 3= 8,=20 5= 4,=20 5= 5,=20 5= 6,=20 5= 7,=20 5= 8,=20 5= 9=20 or the downstream effector (such as KRAS and/or = AKT)5= 4,=20 6= 0,=20 6= 1.=20 On arelated note, targeted deletions of the neurofibromatosis=20 type 1-associated tumour suppressor neurofibromin 1 (NF1), a negative regulator of Ras signalling, have = also been=20 shown to drive gliomagenesis in mice4= 1,=20 4= 6,=20 6= 2,=20 6= 3.=20 Finally, PTEN loss seems to uniformly facilitate glioma formation across = several=20 mouse systems3= 7,=20 3= 8,=20 4= 4,=20 5= 8,=20 6= 2.

Integrated genomics and subsequent = advances. The=20 widespread implementation of comparative genomic hybridization (CGH) has = resulted in more comprehensive analyses of the molecular aberrations = underlying=20 gliomagenesis, as well as insights into their biological = heterogeneity6= 4,=20 6= 5,=20 6= 6,=20 6= 7,=20 6= 8,=20 6= 9,=20 7= 0,=20 7= 1.=20 CGH profiling of primary and secondary glioblastomas, for instance, has = shown=20 strikingly distinct patterns of copy number alteration (CNA), while also = demonstrating that secondary glioblastomas themselves consist of two = subgroups=20 in which the clinical progression times differ significantly6= 6.=20 Coupling array CGH with additional genomic techniques has allowed for=20 increasingly robust, unbiased queries into the identities and functional = characteristics of glioma-relevant genes6= 8,=20 6= 9,=20 7= 1.=20 Some efforts have been considerably aided by multi-institutional = cooperative=20 projects such as the cancer genome atlas (TCGA), which has so far = accumulated=20 expression, CNAs and sequencing data from hundreds of histologically = confirmed=20 glioblastomas, with additional samples and testing modalities (such as = global=20 DNA methylation analysis) currently in progress. These studies have = confirmed=20 the importance of the many glioma-associated genes, including those = described=20 above, and precisely quantified the extent to which they harbour = abnormalities=20 such as mutation, amplification and deletion.

In the context of core signalling pathways, striking = patterns=20 emerge. For instance, although the Ras and AKT isoforms themselves are = mutated=20 and amplified, respectively, in only 2% of glioblastomas (2 of 91 and 2 = of 91),=20 components of the Ras=E2=80=93MAPK and PI3K=E2=80=93AKT=E2=80=93mTOR = signalling pathways are affected in=20 the plurality (88%; 80 of 91) of analysed tumours, with PTEN representing the most commonly altered gene in = either=20 pathway (deleted and/or mutated in ~36% (33 of 91) of all cases)6= 8.=20 Intriguingly, mutations and/or deletions in NF1 = are present=20 in 15=E2=80=9318% of sporadic glioblastomas, a much higher number than = previously=20 realized6= 8,=20 7= 1,=20 and they seem to cluster with a specific glioma subtype (discussed = below). The=20 p53 and RB tumour suppressor networks are also disrupted in similarly = high=20 proportions of glioblastoma: 87% (79 of 91) and 78% (71 of=20 91),respectively6= 8.=20 Such data reinforce the importance of these oncogenic molecular pathways = in=20 gliomagenesis, and correlate well with abundant mouse modelling data.=20 Furthermore, computational analyses of the abundant genomic information = have led=20 to the development of more effective prognostic stratification = algorithms7= 2.

Integrated genomic analysis has also facilitated the=20 identification and characterization of additional genes involved in = glioma=20 pathogenesis. Recently, missense mutations in isocitrate dehydrogenase 1 = (IDH1) were found in a significant number of = glioblastomas=20 that tend to occur mostly in younger patients with more protracted = clinical=20 courses7= 1.=20 These point mutations are restricted exclusively to the R132 residue in = the=20 active site region of the protein in which they disrupt hydrogen bonding = with=20 its substrate7= 1,=20 7= 3.=20 Interestingly, a separate group of gliomas harbour mutations in the = IDH1 homologue IDH2 at the analogous residue (R172). Further = investigations=20 have shown that mutations in IDH1 and IDH2 are present in high proportions of grade II and = III=20 astrocytic and oligodendroglial tumours (72=E2=80=93100%) along with = secon-dary=20 glioblastomas (85%), but are largely absent in primaryglioblastomas = (5%)7= 3,=20 7= 4.=20 Additionally, IDH mutations areassociated with = other=20 genomic abnormalities that are typically seen in lower grade diffuse = gliomas,=20 such as TP53 mutation and 1p/19q deletion; they = are also=20 mutually exclusive with EGFR amplification and = chromosome=20 10loss, and multivariate analysis suggests that they are independent = favourable=20 prognostic markers7= 3,=20 7= 5.=20 These findings suggest that, although IDH = mutations=20 probably contribute to the early evolution of low-grade gliomas = (including those=20 that subsequently progress to higher grade lesions), they seem to have = no role=20 in the underlying biology of de novo = glioblastoma, further=20 emphasizingthe fundamental differences in pathogenesis between these two = broad=20 diagnostic categories.

The mechanisms by which mutations in IDH=20 genes mediate gliomagenesis are still largely unknown. However, one = recent study=20 has demonstrated that loss of IDH1 function through point mutation = induces=20 hypoxia inducible factor 1=CE=B1 (HIF1=CE=B1)7= 6,=20 a component of the hypoxia-responsive transcription factor complex that = has been=20 implicated in angiogenesis and tumour growth7= 7.=20 By contrast, another recent report has shown that mutant IDH1 proteins = exhibit a=20 gain-of-function phenotype by generating R(-)-2-hydroxyglutarate (2HG), a toxic metabolite = associated with=20 an increased risk of malignant brain tumours in patients with inherited = errors=20 of 2HG metabolism7= 8.=20 Although much remains to be studied, the identification of IDH mutations in diffuse gliomas, and more recently in = acute=20 myeloid leukaemia7= 9,=20 has provided new therapeutic targets and emphasized the increasingly = compelling=20 link between cancer biology and basic metabolic processes.

Genomics has also revealed connections between = gliomagenesis and=20 microRNA (miRNA) biology. It has recently been shown that amplification = of miR-26a-2 leads to the overexpression of miR-26a in = ~12% of=20 glioblastomas, promoting gliomagenesis through direct repression of = PTEN, RB and=20 MAP3K2 (Refs 8= 0, 8= 1).=20 By contrast, the p53-induced mi= R-34a,=20 which is typically downregulated in glioblastoma, suppresses = gliomagenesis by=20 directly targeting the expression of the aforementioned oncoproteins MET = and=20 CDK6, along with Notch receptor 1and Notch receptor 2, which seem to = have=20 crucial roles in glioma stem cell survival and proliferation (discussed=20 below)8= 2.=20 Several other miRNAs have also been implicated in glioma formation, = including mi= R-21,=20 miR-7, miR-124a, mi= R-137,=20 mi= R-221,=20 mi= R-222=20 and the miR-181 family, with their individual functions reflecting the = wide=20 range of mRNAs targeted by each8= 3.=20 miRNA-based regulation of the numerous molecular pathways involved in=20 gliomagenesis is undoubtedly complex and this active area of research = should=20 produce numerous additional candidates for therapeutic targeting in the = near=20 future.

Transcriptional profiling: glioma = subclasses. The=20 gene expression profiles of malignant gliomas have been the subject of = several=20 published studies. Initial investigations demonstrated that gliomas of = different=20 histological classes exhibit relatively distinct transcriptional = profiles that=20 can outperform conventional morphological analysis8= 4,=20 8= 5.=20 These studies were followed by others that established transcriptional = variance=20 between subgroups of glioblastoma and correlated these findings with = differences=20 in clinical outcome8= 6,=20 8= 7,=20 8= 8.=20 This work not only revealed an unrealized complexity in the underlying = biology=20 of glioblastoma, but also implicated new genes in gliomagenesis, such as = fatty=20 acid binding protein 7 (FABP7) and ASPM8= 7,=20 8= 9.

Other transcriptionally based classification schemes = have=20 uncovered intriguing links between glioma biology and neuroglial = developmental=20 stages8= 8,=20 9= 0,=20 9= 1=20 (Ta= ble=20 1). The first of these segregated a cohort of malignant gliomas, = comprised=20 of both WHO grade III and IV varieties, into three subclasses: = proneural,=20 proliferative and mesenchymal, the gene expression signatures of which = resembled=20 those of fetal and adult brain; haematopoietic stem cells; and various = soft=20 tissues (including bone, synovium, smooth muscle and fetal astrocytes),=20 respectively. Remarkably, nearly all WHO grade III tumours (65 of 73) = fell into=20 the proneural category, along with a subset of glioblastomas occurring = in=20 younger patients with prolonged disease courses. Moreover, recurrent = tumours,=20 although mostly retaining their initial transcriptional = subclassification,=20 seemed to significantly shift their mRNA signatures towards the = mesenchymal=20 profile. On this note, recent work has identified a set of 'master = regulator'=20 transcription factors, the most important of which are signal transducer = and=20 activator of transcription 3 (STAT3) and = CCAAT/enhancer=20 binding protein-=CE=B2 (C/EBP=CE=B2),=20 which seem to mediate the expression of the mesenchymal phenotype and so = enhance=20 glioma aggressiveness9= 2.

Table=20 1 | Molecular subclasses of malignant = glioma from=20 different studies

Additional clustering analysis using transcriptional = data from=20 TCGA has established similar, if not entirely overlapping, patterns in = primary=20 glioblastomas. Proneural-like and mesenchymal-like signatures have been=20 identified along with additional patterns labelled classic and neuronal = (Ta= ble=20 1). Remarkably, integratingthese findings with copy number, = transcriptional,=20 sequencing and proteomic data effectively correlates glioblastoma = subgroups with=20 characteristic disturbances in defined core signalling networks9= 0,=20 9= 1.=20 The classic, proneural and mesenchymal categories are strongly = associated with=20 genomic abnormalities in either EGFR = (25=E2=80=9330%), PDGFR, IDH1 or IDH2=20 (25=E2=80=9330%), or NF1 (30=E2=80=9340%) (Ta= ble=20 1). Interestingly, not all tumours in each group, and in some cases = only a=20 minority, exhibit actual somatic alterations in the relevant = subclass-defining=20 gene. For example, the proneural subclass contains the most tumours with = alterations in PDGFRA and IDH1, but=20 also includes many cases that are characterized by MET=20 amplification and even includes a small number of EGFR-mutated tumours. This kind of transcriptional = grouping=20 suggests that, despite genomic heterogeneity, gliomas with similar = expression=20 profiles are fundamentally driven by alterations in the same basic = signalling=20 networks and may therefore be susceptible to the same class of targeted=20 therapeutics. Indeed, exhaustive western blot analysis seems to confirm = this=20 conjecture9= 0,=20 and robust mouse models of each subclass (Ta= ble=20 1) should provide a valuable resource for further evaluation. = Finally, on a=20 more foundational level, the existence of molecularly defined subgroups = of=20 glioblastoma raises the question of whether these categories actually = represent=20 separate disease entities rather than the expression of minor = variability in a=20 single tumour class, especially if each is fundamentally driven by its = own=20 distinct underlying biology.

Molecular = pathology:=20 medulloblastoma

Numerous investigations have implicated components of = the sonic=20 hedgehog (SHH) = signalling=20 cascade in medulloblastoma pathogenesis9= 3.=20 The binding of SHH to its receptor patched (PTCH1) relieves tonic = inhibition on the downstream effector smoothened (SMO) and allows the = release of=20 the Gli family of transcription factors from inhibitory protein = complexes that=20 typically include suppressor of fused (SUFU) (Fi= g.=20 4). Genomic alterations in components of the SHH signalling pathway, = specifically inactivating mutations of PTCH1 and = SUFU and/or activating mutations of SMO,=20 have been found in ~15% of sporadic medulloblastomas9= 4,=20 9= 5,=20 9= 6,=20 9= 7.=20 Additionally, germline mutations in PTCH1 cause = Gorl= in's=20 syndrome, a rare congenital condition that is characterized by an = increased=20 incidence of several tumour types, including medulloblastoma9= 8.=20 SHH signalling is known to drive proliferation in the granule neuron = precursors=20 of the cerebellum, and pathway dysregulation resulting from genomic = alterations=20 of its components presumably drives medulloblastoma formation through = analogous=20 downstream effects9= 9.=20 Mouse modelling has further demonstrated the sufficiency of SHH = signalling to=20 generate medulloblastomas in multiple cell types in the developing = hindbrain=20 (discussed below)= 100,=20 = 101.=20 On this note, activating the SHH pathway through various genetic = strategies=20 remains the causative mechanism underlying the plurality of mouse=20 medulloblastoma models that have been produced to date= 100,=20 = 101,=20 = 102,=20 = 103,=20 = 104,=20 = 105,=20 = 106,=20 = 107,=20 = 108,=20 = 109,=20 = 110,=20 = 111,=20 = 112,=20 = 113.

Figure=20 4 | The molecular networks implicated in = the=20 pathogenesis of medulloblastoma.
Dysregulated=20 signalling through the sonic hedgehog (SHH) and Wnt pathways has been = implicated=20 in distinct subclasses of medulloblastoma. Specific proteins in the SHH = and Wnt=20 pathways exhibiting alterations at the genomic level are shown in red = and green,=20 respectively. MYC (blue) amplification has been = associated=20 with the large cell/anaplastic medulloblastoma variant. APC, adenomatous = polyposis coli; DSH, dishevelled; FZD, frizzled; GSK3=CE=B2, glycogen = synthase=20 kinase-3=CE=B2; PTCH1, patched; SMO, smoothened; SUFU, suppressor of = fused.

Dysregulation of the Wnt pathway has also been linked to = the=20 development of medulloblastoma. Wnt ligand binds to its receptor = frizzled (FZD)=20 leading to the release of its downstream effector =CE=B2-catenin from = an inhibitory=20 complex that includes the tumour suppressor adenomatous polyposis coli = (APC) and the axin = proteins (Fi= g.=20 4). Subsequent nuclear accumulation of =CE=B2-catenin is thought to = mediate its=20 tumorigenic functions, presumably through the activation of target genes = such as=20 MYC, cyclin D1 (CCND1) and RE1-silencing transcription factor (REST), which have established roles in cellular=20 proliferation, differentiation and inhibition of apoptosis= 114,=20 = 115.=20 Approximately 20% of sporadic medulloblastomas harbour mutations in = APC, AXIN1, AXIN2 or CTNNB1 (which = encodes=20 =CE=B2-catenin)= 116,=20 = 117,=20 = 118,=20 = 119,=20 = 120,=20 and a similarly sized fraction (18%) has separately been shown to = exhibit=20 nuclear =CE=B2-catenin immunostaining= 114.=20 Furthermore, Turcot's=20 syndrome, which is caused by mutations in APC, is=20 characterized by an increased incidence of medulloblastoma and other=20 neuroepithelial tumours. Finally, medulloblastomas that are driven by = increased=20 Wnt signalling, as shown by nuclear =CE=B2-catenin staining, may follow = a relatively=20 favourable clinical course= 121.=20 Although in vivo models of Wnt pathway-driven=20 medulloblastomas have yet to emerge, one group has successfully = generated supratentorial=20 PNETS using, in part, exogenously augmented =CE=B2-catenin = expression= 122.

Loss of chromosome 17p, typically in association with = gain of 17q=20 (forming isochromosome 17q: i(17)(q10)) is the most common genetic = lesion in=20 medulloblastoma, occurring in 30=E2=80=9350% of cases= 123,=20 = 124,=20 = 125,=20 = 126,=20 = 127,=20 = 128,=20 = 129.=20 Although the precise mechanism by which this genomic abnormality = contributes to=20 tumorigenesis and its prognostic importance remain unclear, the common = deletion=20 region of 17p13.2-13.3 includes several confirmed and putative tumour = suppressor=20 genes, including TP53, the loss of which could = presumably=20 facilitate neoplastic behaviour. Germline defects in TP53,=20 resulting in Li=E2=80=93Fraumeni syndrome, have been correlated with = increased=20 medulloblastoma incidence1= 9,=20 and although TP53 mutations in sporadic = medulloblastomas=20 are not particularly common, they seem to confer poor clinical = outcome= 125,=20 = 130.=20 Additionally, Trp53 loss dramatically enhances=20 medulloblastoma formation in SHH pathway-driven mouse models= 112,=20 = 131,=20 = 132.

Genomic amplification of MYCN and MYC characterizes a = subset of=20 clinically aggressive medulloblastomas that tend to exhibit large=20 cell/anaplastic histological features= 130,=20 = 133.=20 It has recently been demonstrated that the oncogenic miRNA cluster, = miR-17=E2=80=9392, is a downstream target of MYC, the = expression of which=20 seems to be associated with a wide range of tumour types= 134.=20 Also, MYC or MYCN overexpression facilitates medulloblastoma formation = in mice,=20 a characteristic shared with other oncoproteins such as AKT, = insulin-like growth=20 factor 2 (IGF2) = and BCL-2 (Refs = 102,=20 = 107,=20 = 110,=20 = 135).

The Erbb family of RTKs, insulin-like growth factor 1 = receptor (IGF1R) and PDGFR have = also been=20 directly implicated in medulloblastoma pathogenesis, with IGF1R and = PDGFR=20 implicated by their association with poor prognosis= 115,=20 = 136.=20 One group has documented ERBB2 overexpression = in a large=20 proportion of medulloblastomas (28%)= 137,=20 in which it is thought to promote tumorigenesis by activating the = Ras=E2=80=93MAPK and=20 AKT pathways and by promoting the expression of pro-metastatic genes = such as=20 S100 calcium binding protein A4 (S100A4), CCL5 (also known as RANTES) = and MAP2K5 (also known as MEK5)= 138,=20 = 139.=20 Additionally, deletion mutants of ERBB4 have been found in childhood = medulloblastomas= 140,=20 and overexpression of Erbb proteins has been correlated with = unfavourable=20 clinical outcome= 141,=20 = 142,=20 = 143.

Transcriptional profiling: medulloblastoma=20 subclasses. As analogous studies have accomplished for glioma, = global=20 transcriptional analyses of medulloblastoma have both emphasized and = better=20 conceptualized the molecular heterogeneity inherent to this cancer type. = Initial=20 efforts in this regard demonstrated gene expression patterns in = medulloblastoma=20 that were distinct from other CNS tumours with similar histological = features,=20 such as supratentorial PNET and atypical=20 teratoid/rhabdoid tumour (AT/RT)= 144.=20 Furthermore, transcriptional profiles were found to be predictive of = clinical=20 outcome and implied tumour cell lineage= 136,=20 = 144.=20 On a separate note, one study found that PDGFR and Ras=E2=80=93MAPK = signalling=20 correlated with metastatic medulloblastoma, supplementing their array = analysis=20 with confirmatory experiments in vitro= 136.

More recently, two integrated genomic investigations = have revealed=20 distinct transcriptional subclasses of medulloblastoma that also harbour = genomic=20 alterations in oncogenic signalling pathways= 145,=20 = 146.=20 Both have identified subgroups centred around dysregulated SHH and Wnt=20 signalling that are also characterized by genomic alterations in=20 pathway-relevant genes (Ta= ble=20 2). More specifically, the SHH-associated group includes all = analysed=20 tumours with mutations in PTCH1 and SUFU, and the Wnt-associated group contains all tumours = with=20 mutations in CTNNB1. Additional subclasses are = less=20 precisely defined but seem to be somewhat distinct with regard to their=20 associated chromosomal abnormalities, patient age distribution and gene=20 expression-related developmental signatures. Interestingly, = medulloblastomas=20 with desmoplastic histology mainly cluster in the SHH group, confirming = an=20 association that has previously been made9= 4.=20 As with similar analyses carried out for glioma, these studies indicate = that=20 transcriptional variation in medulloblastoma may reflect basic = differences in=20 oncogenic signalling, and in this way invite the implementation of=20 subclass-specific targeted therapy.

Table=20 2 | Molecular subclasses in = medulloblastoma*

Cancer stem = cells and=20 cells of origin

Any discussion of molecular and cellular heterogeneity = within=20 individual tumours must include the 'cancer stem cell' (CSC) hypothesis, = which=20 proposes that neoplastic processes are heavily dependent on a small = population=20 of CSCs that possess the distinct properties of self-renewal, = multipotency and=20 resistance to conventional therapy= 147.=20 In this scheme, the CSC pool and its unique characteristics are thought = to=20 contrast sharply with the bulk of tumour cells of which the lineage is = more=20 specified and proliferative capacity presumably more limited. Although=20 considerable controversy still surrounds the existence, behaviour and = even the=20 nomenclature of CSCs, populations of cells with stem-like properties = have been=20 identified across several solid and liquid tumours, including brain=20 cancers= 148,=20 = 149,=20 = 150.

In both human glioblastomas and medulloblastomas, the = expression=20 of the neural stem cell marker CD133 (also known as = prominin=20 1) has been associated with both tumour initiation capacity and=20 radioresistance= 149,=20 = 150,=20 = 151,=20 = 152.=20 Initial reports indicated that as few as 100 CD133+ cells = collected=20 from either glioblastoma or medulloblastoma could form xenografted = tumours in=20 immunocompromised mice, in sharp contrast to the 105=20 CD133=E2=88=92 cells required for the same phenotype= 150.=20 Although more recent investigations have called into question the unique = tumour-initiating properties of the CD133+ = subpopulation= 153,=20 = 154,=20 CD133 expression has been linked with poor clinical outcome= 155.=20 Furthermore, it has been argued that the discordant results between = studies=20 regarding the stem-like properties of the CD133+ compartment = could be=20 attributed to differences in the handling and culture of primary tissue = samples,=20 factors that dramatically alter both the biological behaviour of tumour = cells=20 and their expression of surface markers such as CD133 (Ref. = 155).=20 It also remains to be seen whether CD133 expression by stem-like cells = is=20 dependent on the molecular subclass of the brain tumour in question.

Related to these ideas is the increasing evidence that = CSCs=20 require a specialized microenvironment for the maintenance of their=20 characteristics= 156,=20 similar in many ways to normal, non-neoplastic stem cell populations. = Indeed, it=20 has been known for some time that stem cells in the adult brain reside=20 specifically in the subgranular zone (SGZ) of the hippocampus and the=20 sub-ventricular zone (SVZ)= 157,=20 = 158,=20 where underlying capillary networks seem to provide both the signals and = nourishment that are required for their support= 159.=20 It has recently been shown that CSCs from various brain tumours, = including=20 glioblastoma and medulloblastoma, exist in a perivascular=20 niche that is analogous to that of their non-neoplastic = counterparts= 160.=20 Stem-like cells from human brain tumours migrate towards, and intimately = interact with, endothelial cells in three-dimensional co-cultures. = Furthermore,=20 transplantation of these brain tumour CSCswith endothelial cells = enhances=20 orthotopic tumour formation in immunocompromised mice, but endothelial = cell=20 depletion in xenografts hinders their growth= 160.=20 Additional work has demonstrated that CD133+ cells from = glioblastomas=20 secrete high levels of vascular endothelial growth factor (VEGF), which = further=20 supports an interactive, functional relationship between brain tumour = CSCs and=20 the surrounding microvasculature= 161.

Various proteins and signalling cascades that are = involved in both=20 tumorigenesis and the maintenance of non-neoplastic stem cell pools have = been=20 implicated in the biology of brain tumour CSCs. These include many of = the=20 signalling pathways discussed above along with the transcription factors = OCT4 (also known as = POU5F1),=20 oligodendrocyte lineage transcription factor 2 (OLIG2) and BMI1 (Ref. = 162).=20 Recent work suggests that the SHH pathway may have an important role in = the=20 establishment of the CSC niche in gliomas. Abundant SHH is secreted by=20 perivascular astrocytes in human and mouse glioblastomas and downstream = Gli=20 activity correlates well with tumour grade= 163.=20 Similarly, molecular cues responsive to cellular hypoxia, particularly = the=20 actions of HIFs, also seem to affect the behaviour of CSCs and the = maintenance=20 of the stem cell microenvironment. Experimental depletion of HIFs in = glioma CSCs=20 inhibits self-renewal and survival in vitro and = tumour=20 initiation potential in vivo= 164.=20 Furthermore, HIF2=CE=B1, the transcriptional targets of which = include POU5F1 (Ref. = 165),=20 induces stem-like behaviour and enhances tumorigenic potential when = transduced=20 into non-stem cells derived from human gliomas= 166.

The Notch pathway has repeatedly been linked to the = biology of=20 normal neural stem cells as well as glioma CSCs= 167.=20 Ligand binding to the Notch receptor results in its cleavage and the = release of=20 the Notch intracellular domain (NICD), the subsequent nuclear = translocation of=20 which activates various target genes. The Notch pathway is activated in = human=20 and mouse gliomas, and forced expression of NICD both induces the stem = cell=20 marker nestin and = cooperates=20 with KRAS to induce expansion of the SVZ in = vivo= 168.=20 Furthermore, increased Notch signalling enhances the efflux of cytotoxic = drugs=20 through ABC transporters such as ABCG2, a recognized = property of=20 stem-like tumour cells that contributes to their resistance to = conventional=20 therapies= 169,=20 = 170.=20 Using fluorescent Hoechst dye, which is also an ABCG2 substrate, stem = cells can=20 be effectively sorted by fluorescence-activated cell sorting (FACS) from = brain=20 tumours as a 'side population' (SP) that exhibits a lower level of = fluorescence=20 than their non-stem cell-like counterparts in the 'main population' = (MP)= 170,=20 = 171.=20 NICD overexpression increases SP cell number, with Notch pathway = inhibition=20 having the opposite effect= 170.=20 Extending these findings is a recent study demonstrating that nitric = oxide (NO),=20 which is secreted by the tumour vasculature, induces Notch signalling = and=20 augments the SP fraction in PDGF-driven gliomas, providing a mechanism = by which=20 specific molecular cues can maintain the stem-like character in the = perivascular=20 niche= 172.

The AKT pathway has also been identified as a major = effector of=20 stem-like behaviour in malignant brain tumours. Increasing AKT = signalling=20 through PTEN loss increases SP cell number in = mouse=20 glioblastomas, at least partially through the direct activation of ABCG2 = (Ref.=20 = 171).=20 Furthermore, in mouse medulloblastoma models, activation of the = PI3K=E2=80=93AKT=E2=80=93mTOR=20 pathway seems to contribute to the relative resistance of perivascular = CSCs to=20 therapeutic irradiation= 173.=20 Combining small molecule AKT pathway inhibitors with radiotherapy = significantly=20 decreases the survival of this resistant stem cell-like pool, indicating = a=20 promising avenue for future treatment strategies. Supporting these = findings,=20 another group has recently reported that PTEN = loss and=20 TP53 deletion are crucial for the maintenance of=20 self-renewal in neural stem cells and seem to mediate these effects at = least in=20 part through the induction of MYC4= 5.

The link between stem cell biology and brain cancer has=20 implications for nascent tumorigenesis and the cells responsible for the = initiation of the neoplastic process. More specifically, it is not clear = whether=20 malignant brain tumours primarily arise from pluripotent stem cells, = their more=20 differentiated progeny, or both. Once again, increasingly sophisticated = in vivo modelling systems have allowed researchers to = begin=20 addressing this question by carefully restricting oncogenic events to = small=20 subpopulations of cells within individual mouse brain tumours. Although=20 informative (if somewhat conflicting) observations have been made, the = data seem=20 to indicate a considerable degree of complexity underlying this issue = that=20 predictably echoes the cellular and molecular heterogeneity of the = tumour types=20 in question.

For medulloblastoma, two groups have recently = demonstrated that=20 dysregulated SHH signalling is sufficient to generate tumours from = multiple=20 distinct precursor cell populations. Indeed, driving oncogenesis in = either=20 neural stem cells or more differentiated granule neuron precursors = yields=20 medulloblastomas with roughly equal penetrance, although the precise = positioning=20 of each tumour does seem to depend on the anatomical distribution of its = pool of=20 initiating cells= 100,=20 = 101.=20 These data indicate that although various cell types of cerebellar = lineage are=20 competent to produce medulloblastomas given the appropriate oncogenic = stimulus,=20 a certain degree of heterogeneity in the resulting tumours can probably = be=20 attributed to differences in cell of origin.

Analogous experiments in glioma mouse models have used = viral=20 transduction methods for the precise localization of oncogenic stimuli = to=20 specific cellular subpopulations. In one study, cre = recombinase-expressing=20 adenovirus (adeno-cre) was used to functionally silence Nf1, Trp53 and/or Pten=20 in targeted foci in the brains of mice with floxed alleles for each = tumour=20 suppressor6= 3.=20 Stereotactic injection of adeno-cre into the SVZ invariably yielded = high-grade=20 astrocytomas, and application of the virus into either the cerebral = cortex or=20 striatum had minimal results, suggesting that tumour suppressor loss in=20 stem-like progenitor cells is both necessary and sufficient for = gliomagenesis.=20 Contrasting sharply with these findings are results from more recent=20 investigations using retrovirus-mediated PDGFB expression in either = adult mice=20 or newborn pups that were deficient in Cdkn2aINK4A, Cdkn2aARF=20 and/or Trp53 (Refs = 174,=20 = 175).=20 These studies demonstrated that driving PDGFB expression in = nestin+=20 progenitor cells, mature GFAP+ astrocytes or committed=20 oligodendroglial precursors is sufficient to generate gliomas. Moreover, = gliomas=20 were generated with equal penetrance regardless of whether retrovirus = was=20 delivered into the SVZ, cerebral cortex or cerebellum= 174.=20 Similarly, another group has effectively induced high-grade gliomas in = the mouse=20 striatum by driving EGFR vIII expression incombination with Cdkn2a and Pten loss5= 9,=20 providing another example of gliomagenesis derived from a non-stem-like = cellular=20 pool. The discrepancies in these studies indicate that several different = cell=20 types probably harbour tumorigenic potential and that their ability to = initiate=20 neoplasia may depend on the precise mechanisms governing the underlying=20 oncogenic stimulus (that is, RTK signalling compared with tumour = suppressor=20 loss) and/or the molecular subclass of the tumour in question.

To further complicate this issue, additional work has = suggested=20 that evolving brain cancers may incorporate large numbers of nominally=20 non-neoplastic cells that are not derived from their cell of origin, and = that=20 such recruited elements proliferate and substantially contribute to the=20 pathogenicity of the tumour mass as a whole= 176.=20 Such data argue that determining the precise cellular origins of brain = tumours,=20 although fascinating from an academic standpoint, may be less relevant = to the=20 development of effective treatment regimens than a fundamental = understanding of=20 the striking cellular and molecular complexity that evolves in these = neoplasms=20 over time.

Conclusions: = implications for therapy

As our understanding of the intricacies of glioma and=20 medulloblastoma biology has progressed, so too has the hope that such=20 breakthroughs will lead to more effective, less toxic, rationally = conceived=20 therapeutics. For both disease entities, the mainstays of nonsurgical = treatment=20 are notable in their uniformity, consisting of a combination of = radiation and=20 cytotoxic chemotherapy. However, as the functional determinants driving = brain=20 tumorigenesis continue to be elucidated, revealing among other things = the=20 remarkable cellular and molecular heterogeneity discussed above, the=20 opportunities for more targeted, individualizedintervention seem to be=20 increasing rapidly.

Indeed, initial efforts towards the stratification of = patients=20 with brain tumours into molecularly determined treatment groups have = already=20 begun. The discovery that promoter methylation and transcriptional = silencing of=20 O-6-methlylguanine-DNA methyltransferase (MGMT) results in improved chemosensitivity of = glioblastomas=20 has now been widely applied as a prognostic indicator for malignant = glioma. MGMT=20 repairs O-6-methylguanine DNA damage that is induced by alkylating = agents such=20 as temozolomide= =20 (currently the mainstay of anti-glioma chemotherapy), and strategies to = overcome=20 this resistance mechanism are the focus of numerous studies= 177,=20 = 178.=20 Also relevant to this discussion is the recent finding that = glioblastomas driven=20 by EGFR vIII may preferentially respond to the EGFR inhibitor erlotinib when PTEN=20 expression is retained= 179,=20 and so forming a molecular subgroup that is presumably more amenable to = targeted=20 therapeutics. These two examples foreshadow what will hopefully = constitute a=20 paradigm shift in the treatment of brain cancer to a model in which = patients=20 will be stratified by molecular characteristics into treatment groups = before the=20 initiation of more personalized, biologically grounded therapies. The = challenge=20 now becomes how to most efficiently and effectively segregate tumours = into=20 treatment-relevant subgroups, and the development of the necessary = biomarkers=20 for this purpose.

Innate and acquired resistance to therapeutic regimens = will=20 probably continue to frustrate efforts to combat brain cancer, as will = issues of=20 drug delivery (Bo= x 2).=20 In this regard, molecularly targeted therapies have been shown to suffer = from=20 the same deficiencies as their more conventional counterparts, as a = recent=20 report describing a case of widely metastatic medulloblastoma=20 demonstrates= 180.=20 In this instance, a tumour known to express a PTCH1-W844C mutant (that = leads to=20 the pathological activation of SHH signalling) was treated with a = specific SMO=20 inhibitor. Although this intervention initially resulted in dramatic = remission,=20 the tumour rapidly recurred in ~3 months having acquired a point = mutation in=20 SMO that rendered it refractory to the drug. = Striking=20 examples of acquired resistance mechanisms such as this abound in the=20 literature, are not unique to brain tumours and illustrate the need for=20 combinatorial regimens that are directed at multiple components of=20 disease-implicated pathways simultaneously. Furthermore, the presence of = stem-like cells in both glioma and medulloblastoma probably contributes = to=20 resistance phenotypes, and argues for the direct targeting of this = cellular=20 subpopulation, perhaps through the inhibition of Notch and/or = PI3K=E2=80=93AKT=E2=80=93mTOR=20 signalling, in conjunction with more conventional cytotoxic = therapies.

Bo= x 2 | Treatment challenges: the blood=E2=80=93brain = barrier
  • Fu= ll box=20

In conclusion, although numerous challenges remain, = notable=20 progress in the molecular characterization of malignant glioma and=20 medulloblastoma has paved the way for more rationally based treatment = strategies=20 that target specific genes and proteins. How best to implement these = promising=20 new therapies, particularly in what combinations and patient groups, = should be=20 the subject of intensive translational research in the years to = come.

T= op of page

Acknowledgements

The authors would like to thank M. Rosenblum for = providing=20 representative tumour micrographs.

Competing interests statement

The authors declare no competing financial=20 interests.

T= op of page

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                      This trial of EGFR kinase = inhibitors=20 suggests that patients with both the EGFR vIII mutation and intact = PTEN may be=20 a molecularly defined subgroup that is more likely to respond to = targeted=20 kinase inhibition.

                    • Yauch, R. L. et al. Smoothened=20 mutation confers resistance to a Hedgehog pathway inhibitor in=20 medulloblastoma. Science 326, 572=E2=80=93574 (2009).

                    • Huse, J. T. & Holland, E. C. Genetically=20 engineered mouse models of brain cancer and the promise of preclinical = testing. Brain Pathol. 19, 132=E2=80=93143 (2009).

                    • Charest, A. et al. ROS = fusion tyrosine=20 kinase activates a SH2 domain-containing = phospatase-2/phosphatidylinositol=20 3-kinase/mammalian target of rapamycin signaling axis to form = glioblastoma in=20 mice. Cancer Res. 66,=20 7473=E2=80=937481 (2006).

                    • Lassman, A. B. et al. Molecular study=20 of malignant gliomas treated with epidermal growth factor receptor = inhibitors:=20 tissue analysis from North American Brain Tumor Consortium Trials = 01=E2=80=9303 and=20 00=E2=80=9301. Clin. Cancer Res. 11, 7841=E2=80=937850 (2005).

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Author affiliations

  1. Departments of Pathology, 408 East 69th Street (Z1304), = New York, NY=20 10065, USA.
  2. Departments of Surgery, 408 East 69th Street (Z1304), New = York, NY=20 10065, USA.
  3. Departments of Neurosurgery, 408 East 69th Street (Z1304), = New York,=20 NY 10065, USA.
  4. Departments of Cancer Biology and Genetics, 408 East 69th = Street=20 (Z1304), New York, NY 10065, USA.
  5. Brain Tumor Center, Memorial Sloan-Kettering Cancer = Center, 408 East=20 69th Street (Z1304), New York, NY 10065, USA.

Correspondence to: Eric C. Holland2<= /A>,3<= /A>,4<= /A>,5<= /A>=20 Email: hollande@mskcc.org

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    • 14 May 2010 =E2=80=94 15 May 2010=20
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PADDING-LEFT: 37px; FONT-WEIGHT: bold; FONT-SIZE: 70%; PADDING-BOTTOM: = 4px; PADDING-TOP: 3px; BACKGROUND-REPEAT: no-repeat } #hdr .user-services .us-link A:visited { PADDING-RIGHT: 2px; BACKGROUND-POSITION: 10px 0.3ex; DISPLAY: block; = PADDING-LEFT: 37px; FONT-WEIGHT: bold; FONT-SIZE: 70%; PADDING-BOTTOM: = 4px; PADDING-TOP: 3px; BACKGROUND-REPEAT: no-repeat } #hdr .user-services .li1 A { BACKGROUND-IMAGE: = url(/common/includes/header/images/icons/01/icon_account_red_med.gif) } #hdr .user-services .li2 A { BACKGROUND-IMAGE: = url(/common/includes/header/images/icons/01/icon_ealert_red_med.gif) } #hdr .user-services .li3 A { BACKGROUND-IMAGE: = url(/common/includes/header/images/icons/01/icon_register_red_med.gif) } #hdr .user-services .li4 A { BACKGROUND-IMAGE: = url(/common/includes/header/images/icons/01/icon_subscribe_red_med.gif) } #hdr .user-services IMG.usi { BORDER-TOP-WIDTH: 0px; PADDING-LEFT: 5px; BORDER-LEFT-WIDTH: 0px; = BORDER-BOTTOM-WIDTH: 0px; BORDER-RIGHT-WIDTH: 0px } #hdr .user-services .ad203x90 { BORDER-TOP-WIDTH: 0px; PADDING-LEFT: 5px; BORDER-LEFT-WIDTH: 0px; = BORDER-BOTTOM-WIDTH: 0px; BORDER-RIGHT-WIDTH: 0px } #hdr #header-nav { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; LEFT: 10px; PADDING-BOTTOM: 0px; = MARGIN: 0px; BOTTOM: 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none; = POSITION: absolute } #hdr #header-nav LI { PADDING-RIGHT: 0px; PADDING-LEFT: 10px; BACKGROUND: = url(/common/includes/header/03/images/tab_l.gif) no-repeat left top; = FLOAT: left; PADDING-BOTTOM: 0px; PADDING-TOP: 0px } #hdr #header-nav LI.hilite { BACKGROUND-IMAGE: = url(/common/includes/header/03/images/tab_l_hilite.gif) } #hdr #header-nav A { PADDING-RIGHT: 10px; PADDING-LEFT: 0px; FONT-WEIGHT: bold; FONT-SIZE: = 90%; BACKGROUND: url(/common/includes/header/03/images/tab_r.gif) = no-repeat right top; FLOAT: left; PADDING-BOTTOM: 6px; PADDING-TOP: 6px; = TEXT-DECORATION: none } #hdr #header-nav .hilite A { BACKGROUND-IMAGE: = url(/common/includes/header/03/images/tab_r_hilite.gif) } #hdr #header-nav A:link { COLOR: #ce0808 } #hdr #header-nav A:visited { COLOR: #ce0808 } #hdr #header-nav .hilite A:link { COLOR: #fff } #hdr #header-nav .hilite A:visited { COLOR: #fff } #hdr .journal-header IMG { BORDER-TOP-WIDTH: 0px; DISPLAY: none! important; BORDER-LEFT-WIDTH: = 0px; BORDER-BOTTOM-WIDTH: 0px; BORDER-RIGHT-WIDTH: 0px } #hdr .journal-header-image { BORDER-TOP-WIDTH: 0px; DISPLAY: none! important; BORDER-LEFT-WIDTH: = 0px; BORDER-BOTTOM-WIDTH: 0px; BORDER-RIGHT-WIDTH: 0px } #hdr .journal-header { LEFT: 0px; WIDTH: 60%; POSITION: absolute; TOP: 15px; HEIGHT: 74px! = important } #hdr .login-nav { CLEAR: both; PADDING-RIGHT: 10px; BACKGROUND-POSITION: left top; = PADDING-LEFT: 10px; MIN-HEIGHT: 124px; PADDING-BOTTOM: 0px; PADDING-TOP: = 0px; BACKGROUND-REPEAT: no-repeat; POSITION: relative; BACKGROUND-COLOR: = #666 } #hdr .logon { RIGHT: 10px; POSITION: absolute; TOP: 0px; TEXT-ALIGN: right } #hdr .links-above.logon { TOP: 2.5ex } #hdr .logon A { PADDING-RIGHT: 0px; BACKGROUND-POSITION: left 0.3ex; PADDING-LEFT: = 18px; FONT-WEIGHT: bold; PADDING-BOTTOM: 1px; COLOR: #fff; LINE-HEIGHT: = 1.3; PADDING-TOP: 1px; BACKGROUND-REPEAT: no-repeat } #hdr .logon A.login { BACKGROUND-IMAGE: url(/common/includes/header/03/images/bg_logout.gif) } #hdr .logon A.login:hover { BACKGROUND-IMAGE: url(/common/includes/header/03/images/bg_login.gif) } #hdr .logon A.login:active { BACKGROUND-IMAGE: url(/common/includes/header/03/images/bg_login.gif) } #hdr .logon A.logoff { BACKGROUND-IMAGE: url(/common/includes/header/03/images/bg_login.gif) } #hdr .logon A.logoff:hover { BACKGROUND-IMAGE: url(/common/includes/header/03/images/bg_logout.gif) } #hdr .logon A.logoff:active { BACKGROUND-IMAGE: url(/common/includes/header/03/images/bg_logout.gif) } #hdr .logon P { FONT-SIZE: 80%; MARGIN: 0px; COLOR: #fff; PADDING-TOP: 8px } #hdr .logon .user { FONT-WEIGHT: bold } #hdr .logon .inst { FONT-WEIGHT: bold } #hdr .login-nav .list { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 70%; RIGHT: 0px; = PADDING-BOTTOM: 0px; MARGIN: 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: = none; POSITION: absolute } #hdr .login-nav .list LI { FLOAT: right } #hdr .login-nav .list A { PADDING-RIGHT: 10px; DISPLAY: block; PADDING-LEFT: 10px; FONT-WEIGHT: = bold; BACKGROUND: = url(/common/includes/header/03/images/bg_register_list.png) no-repeat = left bottom; PADDING-BOTTOM: 6px; COLOR: #fff; PADDING-TOP: 4px } #hdr .login-nav .list A:hover { BACKGROUND-IMAGE: = url(/common/includes/header/03/images/bg_register_list_hover.png) } ------=_NextPart_000_0000_01CAEC83.F1412610 Content-Type: text/css; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.nature.com/common/includes/footer/default/style/footer.css #ftr { BORDER-TOP-WIDTH: 0px; CLEAR: both; PADDING-RIGHT: 0px; PADDING-LEFT: = 0px; FONT-SIZE: 70%; PADDING-BOTTOM: 0px; MARGIN: 20px 0px 0px; = PADDING-TOP: 1px } #ftr .footer-inner { PADDING-RIGHT: 25px; PADDING-LEFT: 25px; BACKGROUND: = url(/common/images/footer_bg.png) #fff repeat-x 0px 0px; PADDING-BOTTOM: = 20px; MARGIN: 0px; PADDING-TOP: 1px } * HTML #ftr { FLOAT: left } #ftr A { TEXT-DECORATION: none } #ftr A:hover { TEXT-DECORATION: underline } #ftr ABBR { BORDER-TOP-WIDTH: 0px; BORDER-LEFT-WIDTH: 0px; BORDER-BOTTOM-WIDTH: = 0px; BORDER-RIGHT-WIDTH: 0px } #ftr UL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none } #ftr #footer-journal { PADDING-RIGHT: 25px; PADDING-LEFT: 25px; PADDING-BOTTOM: 0px; COLOR: = #66676b; PADDING-TOP: 0px } #ftr #footer-journal LI { PADDING-RIGHT: 2em; PADDING-LEFT: 0px; FLOAT: left; PADDING-BOTTOM: = 0.3em; MARGIN: 0px; PADDING-TOP: 0.3em } #ftr #footer-journal LI.journal-name { FONT-WEIGHT: bold; FONT-SIZE: 100%; FONT-STYLE: italic } #ftr #footer-journal LI.extra { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FLOAT: right; PADDING-BOTTOM: = 0.3em; PADDING-TOP: 0.3em } #ftr #footer-journal A { COLOR: #66676b } #ftr .footer-links { BORDER-RIGHT: #fff 1px dashed; PADDING-RIGHT: 2em; PADDING-LEFT: 2em; = FLOAT: left; PADDING-BOTTOM: 0px; MARGIN: 1em 0px 0px; PADDING-TOP: 0px } #ftr .first.footer-links { PADDING-LEFT: 0px } #ftr .last.footer-links { BORDER-RIGHT-WIDTH: 0px } #ftr .footer-links LI { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; = PADDING-TOP: 0.3em } #ftr .footer-links A { COLOR: #54606a } #ftr .search-form LABEL { COLOR: #54606a } #ftr .search-form { PADDING-RIGHT: 0px; PADDING-LEFT: 1em; FONT-SIZE: 100%; FLOAT: right; = PADDING-BOTTOM: 0px; MARGIN: 1em 0px; BORDER-LEFT: #fff 1px dashed; = PADDING-TOP: 0px } * HTML #ftr .search-form { WIDTH: 29em } #ftr .search-form LABEL { PADDING-RIGHT: 0.3em; DISPLAY: block; PADDING-LEFT: 0.3em; FONT-WEIGHT: = normal; FONT-SIZE: 100%; FLOAT: left; PADDING-BOTTOM: 0.3em; MARGIN: 0px = 0px 0px 0.3em; PADDING-TOP: 0.3em } #ftr .search-form INPUT.text { PADDING-RIGHT: 0.3em; DISPLAY: block; PADDING-LEFT: 0.3em; FONT-WEIGHT: = normal; FONT-SIZE: 100%; FLOAT: left; PADDING-BOTTOM: 0.3em; MARGIN: 0px = 0px 0px 0.3em; PADDING-TOP: 0.3em } #ftr .search-form INPUT.button { PADDING-RIGHT: 0.3em; DISPLAY: block; PADDING-LEFT: 0.3em; FONT-WEIGHT: = normal; FONT-SIZE: 100%; FLOAT: left; PADDING-BOTTOM: 0.3em; MARGIN: 0px = 0px 0px 0.3em; PADDING-TOP: 0.3em } #ftr .search-form INPUT.text { WIDTH: 15em } #ftr .search-form FIELDSET { BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; = BORDER-LEFT-WIDTH: 0px; BACKGROUND: none transparent scroll repeat 0% = 0%; BORDER-BOTTOM-WIDTH: 0px; PADDING-BOTTOM: 0px; MARGIN: 0px; = PADDING-TOP: 0px; BORDER-RIGHT-WIDTH: 0px } * HTML #ftr .search-form { POSITION: relative } * HTML #ftr .search-form FIELDSET { RIGHT: 0px; POSITION: absolute; TOP: 0px } #ftr .search-form INPUT { BORDER-RIGHT: #c7c8cd 1px solid; BORDER-TOP: #c7c8cd 1px solid; = BORDER-LEFT: #c7c8cd 1px solid; BORDER-BOTTOM: #c7c8cd 1px solid } #ftr .search-form INPUT.button { PADDING-RIGHT: 0.8em; PADDING-LEFT: 0.8em; BACKGROUND: = url(/common/images/footer_search_btn_bg.png) #fff repeat-x 0px 100%; = PADDING-BOTTOM: 0.2em; COLOR: #54606a; PADDING-TOP: 0.2em } * HTML #ftr .search-form INPUT.button { PADDING-RIGHT: 0.7em; PADDING-LEFT: 0.7em; PADDING-BOTTOM: 0.1em; = PADDING-TOP: 0.2em } #ftr .logo A { COLOR: #000 } #ftr .logo { PADDING-RIGHT: 7px; PADDING-LEFT: 236px; MIN-HEIGHT: 40px; BACKGROUND: = url(/common/images/npg_logo_full.png) no-repeat 0px 50%; PADDING-BOTTOM: = 7px; MARGIN: 5px 0px 0px; PADDING-TOP: 7px } * HTML #ftr .logo { HEIGHT: 40px } #ftr .logo LI { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0.3em; = PADDING-TOP: 0.3em } #ftr .logo LI.only { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0.3em; = PADDING-TOP: 1.3em } #ftr #footer-copyright { BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; = BORDER-LEFT-WIDTH: 0px; BORDER-BOTTOM-WIDTH: 0px; PADDING-BOTTOM: 0px; = MARGIN: 0px; PADDING-TOP: 0px; BORDER-RIGHT-WIDTH: 0px } ------=_NextPart_000_0000_01CAEC83.F1412610 Content-Type: text/css; charset="iso-8859-1" Content-Transfer-Encoding: 7bit Content-Location: http://www.nature.com/common/includes/footer/03/style/footer.css @import url( /common/includes/footer/default/style/footer.css ); ------=_NextPart_000_0000_01CAEC83.F1412610 Content-Type: text/css; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.nature.com/common/style/global.comments.css .comment-form DIV.field { PADDING-RIGHT: 0px! important; PADDING-LEFT: 0px! important; = PADDING-BOTTOM: 5px! important; PADDING-TOP: 0px! important } .comment-form DIV.indent { PADDING-RIGHT: 0px! important; PADDING-LEFT: 150px! important; = PADDING-BOTTOM: 5px! important; PADDING-TOP: 0px! important } .comment-form DIV.first { MARGIN-TOP: 10px } .comment-form DIV.last { MARGIN-BOTTOM: 10px } .comment-form DIV.wrap { PADDING-RIGHT: 10px! important; PADDING-LEFT: 10px! important; = PADDING-BOTTOM: 10px! important; PADDING-TOP: 10px! important } .comment-form FIELDSET { BORDER-TOP-WIDTH: 0px; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; = BORDER-LEFT-WIDTH: 0px; BORDER-BOTTOM-WIDTH: 0px; PADDING-BOTTOM: 0px; = MARGIN: 0px; PADDING-TOP: 0px; BORDER-RIGHT-WIDTH: 0px } .comment-form FIELDSET.contact-details { MARGIN-BOTTOM: 10px } .comment-form FIELDSET.contact-details LABEL { WIDTH: 8em } .comment-form FIELDSET.contact-details INPUT { MARGIN-BOTTOM: 5px } .comment-form LEGEND { FONT-WEIGHT: bold } .comment-form LABEL { DISPLAY: block; FONT-WEIGHT: bold; FONT-SIZE: 80%; FLOAT: left; WIDTH: = 150px } .comment-form .check { FLOAT: left } .comment-form .check LABEL { DISPLAY: inline; FONT-WEIGHT: normal; FLOAT: none } .comment-form TEXTAREA { BORDER-RIGHT: #e7e7e7 1px solid; BORDER-TOP: #e7e7e7 1px solid; = FONT-SIZE: 90%; MARGIN: 5px 0px; BORDER-LEFT: #e7e7e7 1px solid; WIDTH: = 100%; BORDER-BOTTOM: #e7e7e7 1px solid; FONT-FAMILY: = arial,helvetica,clean,sans-serif } .comment-form TEXTAREA:focus { BORDER-LEFT-COLOR: #999; BORDER-BOTTOM-COLOR: #999; BORDER-TOP-COLOR: = #999; BORDER-RIGHT-COLOR: #999 } .comment-form .text { BORDER-RIGHT: #aaaaaa 1px solid; PADDING-RIGHT: 3px; BORDER-TOP: = #aaaaaa 1px solid; PADDING-LEFT: 3px; PADDING-BOTTOM: 2px; MARGIN: 0px = 0px 5px; BORDER-LEFT: #aaaaaa 1px solid; WIDTH: 200px; PADDING-TOP: 2px; = BORDER-BOTTOM: #aaaaaa 1px solid } .comment-form P.norm { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 10px; MARGIN: = 0px; PADDING-TOP: 0px } .comment-form DIV P.norm { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; = PADDING-TOP: 0px } #comment-nav { BORDER-RIGHT: #aaaaaa 1px solid; PADDING-RIGHT: 10px; BORDER-TOP: = #aaaaaa 1px solid; PADDING-LEFT: 4px; FONT-SIZE: 80%; BACKGROUND: = url(/common/images/comment_button_bg.gif) #fff repeat-x 0px 100%; = PADDING-BOTTOM: 0px; MARGIN: 0px 0px 10px; BORDER-LEFT: #aaaaaa 1px = solid; PADDING-TOP: 10px; BORDER-BOTTOM: #aaaaaa 1px solid } #comment-nav UL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px; LIST-STYLE-TYPE: none } #comment-nav LI { PADDING-RIGHT: 0px; PADDING-LEFT: 21px; PADDING-BOTTOM: 10px; MARGIN: = 0px 0px 0px 4px; PADDING-TOP: 0px } #comment-nav LI.comments { BACKGROUND: url(/common/images/icons/comment_small.gif) no-repeat 0px = 0px } #comment-nav LI.feed { BACKGROUND: url(/common/images/icons/newsfeeds.gif) no-repeat 0px 0px } #comment-nav LI.what-is { BACKGROUND: url(/common/images/help.gif) no-repeat 0px 0px } #comment-help { PADDING-RIGHT: 0px! important; PADDING-LEFT: 0px! important; FONT-SIZE: = 80%; PADDING-BOTTOM: 0px! important; PADDING-TOP: 0px! important } #comment-help P.first { MARGIN-TOP: 0px; PADDING-TOP: 5px } #comment-help KBD { FONT-SIZE: 1.2em; FONT-FAMILY: monospace } .comment-form .submit { BORDER-RIGHT: #e7e7e7 1px solid; PADDING-RIGHT: 15px; BORDER-TOP: = #e7e7e7 1px solid; PADDING-LEFT: 15px; FONT-WEIGHT: bold; BACKGROUND: = url(/view/images/bg_button.gif) #ffffff repeat-x 0px 100%; FLOAT: right; = PADDING-BOTTOM: 2px; MARGIN: 0px; BORDER-LEFT: #e7e7e7 1px solid; = CURSOR: hand; COLOR: #58626b; PADDING-TOP: 2px; BORDER-BOTTOM: #e7e7e7 = 1px solid } .comments-notice A.submit-button { BORDER-RIGHT: #e7e7e7 1px solid; PADDING-RIGHT: 15px; BORDER-TOP: = #e7e7e7 1px solid; PADDING-LEFT: 15px; FONT-WEIGHT: bold; BACKGROUND: = url(/view/images/bg_button.gif) #ffffff repeat-x 0px 100%; FLOAT: right; = PADDING-BOTTOM: 2px; MARGIN: 0px; BORDER-LEFT: #e7e7e7 1px solid; = CURSOR: hand; COLOR: #58626b; PADDING-TOP: 2px; BORDER-BOTTOM: #e7e7e7 = 1px solid } .comment-form .submit:hover { BORDER-LEFT-COLOR: #e7e7e7; BORDER-BOTTOM-COLOR: #e7e7e7; COLOR: #000; = BORDER-TOP-COLOR: #e7e7e7; BORDER-RIGHT-COLOR: #e7e7e7 } .comments-notice A.submit-button:hover { BORDER-LEFT-COLOR: #e7e7e7; BORDER-BOTTOM-COLOR: #e7e7e7; COLOR: #000; = BORDER-TOP-COLOR: #e7e7e7; BORDER-RIGHT-COLOR: #e7e7e7 } .comments-notice 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DIV.comment { PADDING-LEFT: 30px; BACKGROUND: url(/view/images/icon_comment.gif) = no-repeat 0px 0px; MARGIN: 0px } OL.comments DIV.comment { PADDING-BOTTOM: 0px! important } OL.comments DIV.comment DIV.wrap { PADDING-BOTTOM: 0px! important } OL.comments .comment-id { FONT-SIZE: 90%; FLOAT: right; COLOR: #666! important; TEXT-DECORATION: = none } OL.comments DL.date { FLOAT: left; MARGIN-BOTTOM: 5px } OL.comments DL.date DT { DISPLAY: none } OL.comments DD { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } OL.comments DL.ugc { CLEAR: left } OL.comments DD P { MARGIN-TOP: 0px } OL.comments CITE.vcard { FONT-STYLE: normal } #content #comments DIV.comment DL.ugc { FONT-SIZE: 90% } #content #comments DIV.comment DL.date { FONT-SIZE: 90% } #content #comments DIV.comment DL.ugc * { FONT-SIZE: 100% } #content #comments DIV.comment DL.date * { FONT-SIZE: 100% } H3.comments { MARGIN-TOP: 20px! important } H3.divide { BORDER-TOP: 1px dotted; 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WT.bs=3Ddocument.body?document.body.offsetWidth+"x"+document.body.offsetH= eight:"unknown";=0A= }=0A= else{=0A= WT.bs=3Dwindow.innerWidth+"x"+window.innerHeight;=0A= }=0A= WT.fv=3D(function(){=0A= var i,flash;=0A= if (window.ActiveXObject){=0A= for(i=3D10;i>0;i--){=0A= try{=0A= flash=3Dnew ActiveXObject("ShockwaveFlash.ShockwaveFlash."+i);=0A= return i+".0";=0A= }=0A= catch(e){=0A= }=0A= }=0A= }=0A= else if (navigator.plugins&&navigator.plugins.length){=0A= for (i=3D0;i=3D0;j--){=0A= for(i=3D3;i>0;i--){=0A= v=3Di+"."+j;=0A= if (Silverlight.isInstalled(v)){=0A= slv=3Dv;=0A= break;=0A= }=0A= }=0A= if (slv=3D=3Dv){=0A= break;=0A= }=0A= }=0A= }=0A= }=0A= return slv;=0A= })();=0A= if (this.i18n){=0A= if (typeof(document.defaultCharset)=3D=3D"string"){=0A= WT.le=3Ddocument.defaultCharset;=0A= } =0A= else if (typeof(document.characterSet)=3D=3D"string"){=0A= WT.le=3Ddocument.characterSet;=0A= }=0A= else{=0A= WT.le=3D"unknown";=0A= }=0A= }=0A= WT.tv=3D"8.6.0";=0A= // WT.sp=3D"@@SPLITVALUE@@";=0A= WT.dl=3D"0";=0A= WT.ndl=3D"0";=0A= WT.ssl=3D(window.location.protocol.indexOf('https:')=3D=3D0)?"1":"0";=0A= DCS.dcsdat=3DdCurrent.getTime();=0A= DCS.dcssip=3Dthis.getHost();=0A= DCS.dcsuri=3Dwindow.location.pathname;=0A= WT.es=3DDCS.dcssip+DCS.dcsuri;=0A= if (window.location.search){=0A= DCS.dcsqry=3Dwindow.location.search;=0A= if (this.qp.length>0){=0A= for (var i=3D0;i');=0A= }=0A= }=0A= WebTrends.prototype.dcsMeta=3Dfunction(){=0A= var elems;=0A= if (document.all){=0A= elems=3Ddocument.all.tags("meta");=0A= }=0A= else if (document.documentElement){=0A= elems=3Ddocument.getElementsByTagName("meta");=0A= }=0A= if (typeof(elems)!=3D"undefined"){=0A= var length=3Delems.length;=0A= for (var i=3D0;i0){=0A= if (name.toUpperCase().indexOf("WT.")=3D=3D0){=0A= this.WT[name.substring(3)]=3Dcontent;=0A= }=0A= else if (name.toUpperCase().indexOf("DCSEXT.")=3D=3D0){=0A= this.DCSext[name.substring(7)]=3Dcontent;=0A= }=0A= else if (name.toUpperCase().indexOf("DCS.")=3D=3D0){=0A= this.DCS[name.substring(4)]=3Dcontent;=0A= }=0A= }=0A= }=0A= }=0A= }=0A= WebTrends.prototype.dcsTag=3Dfunction(){=0A= if (document.cookie.indexOf("WTLOPTOUT=3D")!=3D-1){=0A= return;=0A= }=0A= var WT=3Dthis.WT;=0A= var DCS=3Dthis.DCS;=0A= var DCSext=3Dthis.DCSext;=0A= var i18n=3Dthis.i18n;=0A= var = P=3D"http"+(window.location.protocol.indexOf('https:')=3D=3D0?'s':'')+":/= /"+this.domain+(this.dcsid=3D=3D""?'':'/'+this.dcsid)+"/dcs.gif?";=0A= if (i18n){=0A= WT.dep=3D"";=0A= }=0A= for (var N in DCS){=0A= if (DCS[N]&&(typeof DCS[N]!=3D"function")){=0A= P+=3Dthis.dcsA(N,DCS[N]);=0A= }=0A= }=0A= var keys=3D["co_f","vtid","vtvs","vt_f_tlv"];=0A= for (var i=3D0;i0)){=0A= P+=3Dthis.dcsA("WT.dep",WT.dep);=0A= }=0A= if (P.length>2048&&navigator.userAgent.indexOf('MSIE')>=3D0){=0A= P=3DP.substring(0,2040)+"&WT.tu=3D1";=0A= }=0A= this.dcsCreateImage(P);=0A= this.WT.ad=3D"";=0A= }=0A= WebTrends.prototype.dcsDebug=3Dfunction(){=0A= var t=3Dthis;=0A= var i=3Dt.images[0].src;=0A= var q=3Di.indexOf("?");=0A= var r=3Di.substring(0,q).split("/");=0A= var m=3D"Protocol
"+r[0]+"
";=0A= m+=3D"Domain
"+r[2]+"
";=0A= m+=3D"Path
/"+r[3]+"/"+r[4]+"
";=0A= m+=3D"Query = Params"+i.substring(q+1).replace(/\&/g,"
")+"";=0A= = m+=3D"
Cookies
"+document.cookie.replace(/\;/g,"
")= +"";=0A= if (t.w&&!t.w.closed){=0A= t.w.close();=0A= =0A= }=0A= = t.w=3Dwindow.open("","dcsDebug","width=3D500,height=3D650,scrollbars=3Dye= s,resizable=3Dyes");=0A= t.w.document.write(m);=0A= t.w.focus();=0A= }=0A= =0A= WebTrends.prototype.isonsiteHelper=3Dfunction(host)=0A= {=0A= var osda=3Dthis.onsitedoms.split(",");=0A= var len=3Dosda.length;=0A= for (x=3D0; x14)) {=0A= _tag.DCSext.gateway=3Dhost.substr(14,host.length);=0A= //return trimed version of host name=0A= return host.substr(0,14);=0A= } else {=0A= //else return full host=0A= return host;=0A= }=0A= }=0A= =0A= function dcsMultiTrack(){=0A= if (typeof(_tag)!=3D"undefined"){=0A= return(_tag.dcsMultiTrack());=0A= }=0A= }=0A= =0A= function dcsDebug(){=0A= if (typeof(_tag)!=3D"undefined"){=0A= return(_tag.dcsDebug());=0A= }=0A= }=0A= =0A= Function.prototype.wtbind =3D function(obj){=0A= var method=3Dthis;=0A= var temp=3Dfunction(){=0A= return method.apply(obj,arguments);=0A= };=0A= return temp;=0A= }=0A= =0A= String.prototype.trim =3D function () {=0A= return this.replace(/^\s*/, "").replace(/\s*$/, "");=0A= }=0A= =0A= =0A= ------=_NextPart_000_0000_01CAEC83.F1412610--