Remission of Invasive, Cancer Stem-Like Glioblastoma = Xenografts Using Lentiviral Vector-Mediated Suicide Gene Therapy

Results

Lentiviral pseudotyped vectors=20 efficiently transduce glioblastoma spheroids in = vitro

Human glioblastoma = spheroids derived=20 either directly from the patient (low generation) or from serial = in=20 vivo passages in the brains of nude rats (high generation), = were=20 infected with lentiviral LCMV-GP (5=C3=9710⁴ in 10 = =C2=B5l) or VSV-G=20 pseudotyped lentiviral vectors (both 5=C3=9710⁴ = particles in 10 =C2=B5l)=20 or with retroviral MLV-based vectors pseudotyped with LCMV-GP=20 (1=C3=9710⁵ particles in 10 =C2=B5l). The vectors were = prepared in the=20 same way for in vitro and in vivo experiments = (see materials and methods). Both lentiviral vectors = transduced=20 patient spheroids and high generation spheroids very efficiently = (Figure 1

).=20 In contrast, retroviral vectors transduced only a few single cells = in high=20 generation spheroids (Figure 1

)=20 and failed to transduce patient spheroids (data not shown). In = conclusion,=20 both lentiviral vectors are much more efficient in transducing = human=20 glioblastoma spheroids in vitro than retroviral = vectors.

Lentiviral pseudotyped vectors=20 efficiently and specifically transduce glioblastoma cells in=20 vivo

To compare the transduction = efficiency of=20 lentiviral and gammaretroviral vectors in vivo, we used a = xenograft model that reflects the angiogenic and invasive features = of=20 human glioblastoma in situ. The xenograft also expresses = the=20 neural progenitor marker nestin and closely recapitulates the = histology of=20 the patient tumor (Figure 2

).=20 The vectors were injected into the center of progressively growing = lesions=20 using microprocessor-controlled stereotactic infusion. The = injection=20 coordinates were estimated after analyzing MRI images for each = individual=20 lesion. The injection volume applied was 2=C3=9710 =C2=B5l and the = vector titre=20 1=C3=9710⁷/ml for all vectors. Transduction efficiency = was evaluated=20 7 days after vector injection. Both lentiviral pseudotyped vectors = showed=20 very efficient transduction of the tumors (Figure 3A,D

).=20 When analyzed at higher magnification, both LCMV-GP and VSV-G = pseudotyped=20 lentiviral vectors showed efficient transgene delivery to = nestin-positive=20 tumor cells in solid (Figure 3

B,E)=20 and invasive tumor areas (Figure 3C,F

).=20 In contrast, the retroviral vector only transduced a few scattered = tumor=20 cells near the injection site (Figure 3

=20 G,H). For a quantitative comparison of transduction efficiency = between the=20 two lentiviral pseudotyped vectors, the GFP-positive areas were = measured=20 on histological slides (see material and methods). The total volume of = transduced tumor=20 tissue was 7.05=C2=B13.51 mm³ for LCMV-GP pseudotyped = vectors and=20 4.05=C2=B12.04 mm³ for VSV-G pseudotyped vectors (Figure 3I

).=20 Although there was a difference in the mean, it was not = statistically=20 significant (p

=3D

0.269) due to high interindividual differences = (standard=20 deviations).

Figure=20 1

Transduction of=20 glioma spheroids by lenti- and retroviral = vectors.

Figure=20 2

Glioblastoma=20 patient biopsy and xenograft tumor show similar=20 histopathology.

To analyze transduction = specificity,=20 histological sections of invasive tumor areas were stained for rat = specific markers NeuN (for neurons) and nestin (for astrocytes and = progenitor cells). LCMV-GP pseudotyped lentiviral vectors = exclusively=20 transduced tumor cells in all invasive areas (Figure 4A

),=20 while normal brain cells were not transduced (Figure 4B,C

).=20 Also VSV-G pseudotyped vectors showed specific transduction of = tumor cells=20 in some invasive areas (Figure 4D,E

),=20 however, they also transduced a few host brain cells at other = sites (Figure 4G,H

Figure=20 3

Lentiviral vectors=20 efficiently transduce human glioma cells in=20 vivo.

Lentiviral pseudotyped vectors = transduce=20 cancer-stem-like glioma cells

To analyze the potential of = both=20 lentiviral vectors to infect cancer stem-like cells, transduced = tumors=20 were enzymatically dissociated and CD133 expression was measured = by flow=20 cytometry. Both vectors transduced CD133-positive and = CD133-negative cells=20 (Figure 5A

).=20 Although there were high interindividual differences in the = fraction of=20 total CD133-positive tumor cells in the different xenografts, both = vectors=20 showed similar efficiency in transducing CD133-positive cells, = which was=20 slightly higher than the overall fraction of CD133-positive cells = (table 1).

Figure=20 4

Specificity of=20 tumor cell transduction by lentiviral vectors.

Figure=20 5

Lentiviral vectors=20 transduce cancer stem-like cells.

The GFP-positive cells from = tumors=20 transduced with LCMV-GP or VSV-G pseudotyped lentiviral vectors = were=20 sorted and cultured in neural basal medium supplemented with EGF = and bFGF.=20 Transduced tumor cells from both vectors were able to form = spheroids (Figure 5B,E

).=20 Spheroids expressed the stem cell markers nestin and SOX2 (Figure 5C,D,F,G

).=20 Sorted cells were also plated under serum conditions. The cells = continued=20 to show significant expression of the stem cell markers nestin and = SOX2,=20 but also of the differentiation markers GFAP and =CE=B2-tubulinIII = (Figure 5H-O

Lentiviral pseudotyped vectors = expressing=20 the suicide gene HSV-1-tk mediate an efficient = therapeutic effect=20 in vivo

To evaluate the therapeutic = efficacy of=20 both lentiviral pseudotyoped vectors in the invasive xenograft = model,=20 vectors expressing the suicide gene HSV1-tk fused to eGFP = were=20 injected into established tumors when visible on MRI using the = same method=20 as described for the in vivo tropism study. The animals = were=20 treated daily with 50 mg/kg ganciclovir for 30 days starting 7 = days post=20 vector injection. Tumor growth was measured every 7=E2=80=9314 = days by MRI. After=20 4 weeks of treatment, 7 out of 8 animals in both the LCMV- and the = VSV-pseudotype treated groups had a complete remission on MRI (Figure 6

).=20 One animal in each group had a stable disease until the end of GC=20 treatment. All animals in the control groups developed large = tumors during=20 the treatment period of 30 days (Figure 6

).=20 Both, LCMV- and VSV-pseudotype treated animals had a highly = significant=20 survival advantage (p<0.001) compared to the control groups (Figure 7A

).=20 There was no statistically significant difference in survival = between the=20 two treatment groups.

Table=20 1

Transduction of=20 CD133+ cells by lentiviral vectors.

Figure=20 6

Tumors = treated with=20 lentiviral vectors and ganciclovir show complete remission = on=20 MRI.

Upon cessation of prodrug = administration,=20 all animals developed recurrent tumors, which could be classified = into=20 three different groups (Figure 7B-E

,=20 table 2). The = animals showed=20 either 1) local recurrences or 2) local and/or contralateral = recurrences=20 or 3) recurrences in other distant brain areas. There was no clear = difference in the recurrence pattern between the two vector types, = but=20 LCMV-pseudotyped vector-treated animals had more contralateral=20 recurrences, whereas VSV-G pseudotyped vector-treated animals had = more=20 local recurrences (Figure 7B-E

,=20 table 2). = Histopathological=20 and confocal microscopic analysis of the lesions revealed = GFP-positive=20 cells in all recurrent tumors demonstrating that not all = transduced glioma=20 cells were killed by ganciclovir treatment (Figure 7F-M

).=20 In VSV-G pseudotype-treated animals, the GFP-positive surviving = cells were=20 found in invasive areas (Figure 7F,G

),=20 the corpus callosum region (Figure 7H

)=20 and also in some regions of distant recurrences. One animal also = showed a=20 focus of transduced normal brain cells at the tumor border that = survived=20 GC treatment (Figure 7I

).=20 In the LCMV group, most GFP- positive cells were found in the = ipsilateral=20 hemisphere, in solid and invasive tumor areas (Figure 7J,K,L

),=20 with only a few cells seen in the contralateral hemisphere (Figure 7M

Figure=20 7

Therapeutic=20 efficiency of LCMV-GP and VSV-G pseudotyped lentiviral = vectors=20 in vivo.

	Table=20 2 Recurrences after=20 gene therapy with lentiviral vectors.
Top Abstract Introduction Materials=20 and Methods Results "=20 = src=3D"http://www.pubmedcentral.nih.gov/corehtml/pmc/pmcgifs/square.gif">= Discussion References	Discussion Future success of glioma gene = therapy will=20 depend on more potent vector systems that show higher transduction = efficiency than the systems that are available today. In addition, = the=20 application of representative animal models that recapitulate = both, the=20 invasive and angiogenic features of patient tumors, is vital in = order to=20 minimize the huge discrepancies between the experimental results = and=20 clinical outcomes previously observed for gene therapeutic = strategies for=20 brain cancer. To this end, we applied one of the most = clinically=20 relevant animal models for glioblastoma known. This model was = established=20 several years ago [20] and its growth pattern as = well as=20 geno- and phenotypic similarity to glioblastoma in patients has = been=20 extensively characterized [3]. A striking difference = of our=20 model compared to other cell-line based models is the highly = invasive=20 behaviour of the lesions, similar to glioblastoma in patients. Our = model=20 is based on spheroids derived from patient biopsies that are = passaged=20 serially in the brains of nude rats. First generation tumors are = highly=20 invasive and grow without signs of angiogenesis. Late generation = tumors=20 show an angiogenic phenotype, but are still invasive. Our in=20 vitro experiments revealed that both lentiviral vectors = transduced=20 spheroids derived from both low and high generation tumors very=20 efficiently. In contrast, retroviral vectors transduced only high=20 generation spheroids and displayed a much lower efficiency of gene = transfer than both lentiviral vectors. This difference can only be = attributed to the vector backbone, as the glycoprotein which is=20 responsible for virus entry into the cell was the same for the = retroviral=20 and one of the lentivral vectors applied (LCMV-GP). The most = important=20 feature that distinguishes lentiviral from retroviral vectors is = their=20 ability to infect non-dividing cells. It is known that glioma = spheroids,=20 especially primary biopsy spheroids, contain a significant = fraction of=20 non-dividing cells, which cannot be transduced by retroviral = vectors. It=20 has previously been shown that the cultured biopsy spheroids show = a=20 similar cell proliferation as seen in glioblastoma patients [20]. Previous studies have demonstrated that = retroviral=20 vectors can very efficiently transduce highly proliferative = monolayer=20 cultures of glioma cell lines [14]. However, monolayer cultures = change=20 their geno- and phenotypic characteristics under long term culture = and=20 thus are not a suitable model to answer clinically relevant = questions [26]. For in vivo experiments, we = selected a high=20 generation xenograft that showed both angiogenic and invasive = features and=20 recapitulated the histology of the patient lesion. Furthermore, = this=20 xenograft showed a high level of nestin expression similar to the = patient=20 material. In translational research it is crucial to assure that = the=20 experimental tumors truly reflect the corresponding patient's = tumor=20 properties to avoid using non-relevant animal models. However, = this=20 strategy is not common practice yet, based on the simplicity of = using=20 established cell lines for in vivo experiments. We showed a high transduction efficiency = of=20 lentiviral vectors for glioma cells in vivo, whereas = retroviral=20 vectors transduced a few scattered tumor cells near the injection = track.=20 This is in contrast to in vivo studies by others where = retroviral=20 vectors were very efficient, but as mentioned above, the models = applied=20 were non-invasive, based on cell lines cultured as monolayers [27]. Of note, the results of = clinical=20 studies using retroviral vectors showed the same low transduction=20 efficiency as observed in our model system [12]. This finding provides = further=20 evidence that the glioma model used here has a higher predictive = value for=20 the performance of a novel therapeutic approach in the clinic than = previous animal models. The tropism for glioma cells was more = specific with=20 LCMV-GP lentiviral pseudotyped vectors, as VSV-G pseudotyped = lentiviral=20 vectors also transduced few normal brain cells in invasive areas. = In=20 previous studies using a rat glioma model, we also showed a more = specific=20 transduction of glioma cells by LCMV-GP pseudotyped vectors = compared to=20 VSV-G pseudotyped vectors [18], [19]. In fact, in these studies, = the VSV-G=20 pseudotyped vectors transduced normal brain cells at a much higher = frequency than in this study. This can be explained by the mode of = vector=20 delivery, because in the previous studies, we injected the vectors = both=20 into the tumor core as well as into tumor border areas. In the = present=20 study, we injected the vectors into the tumor core only using = convection=20 enhanced delivery. We used this method because it results in a = high=20 distribution volume of drug and vector and is currently used as a = delivery=20 method in clinical studies [28]. In addition, the tumor = model we=20 apply here is highly invasive and lacks a sharply demarcated brain = tumor/normal brain interface, present in the rat glioma model. = Another=20 explanation could be the species difference as we used human = glioma cells=20 in this study in contrast to rat glioma cells in the previous = work. VSV-G=20 pseudotyped vectors might have a higher tropism for human glioma = cells=20 than for rat normal host cells. However, as the receptor for VSV-G = is=20 unknown [29], this remains a = hypothesis. The targeting of cancer stem cells or = cancer=20 stem-like cells in human tumors including glioblastoma has = recently=20 evolved as a major aim in cancer therapy. These stem cells are = suggested=20 to initiate cancer and might be resistant to therapy, thus being=20 responsible for tumor recurrence [30]=E2=80=93[32]. Yet, recent studies have = initiated a=20 controversial discussion whether cancer stem cells really exist [33], [34]. Therefore, we use the = term =E2=80=9Ccancer=20 stem-like cells=E2=80=9D in our study to designate cells which = have certain=20 stem-like properties described previously. We showed that both = lentiviral=20 vectors transduced CD133-positive and CD133-negative cells. = CD133-positive=20 cells have been identified as cancer initiating cells and cancer = stem=20 cells in many different cancers including glioblastoma [30], [35]. However, more recent reports = questioned these findings showing that CD133-negative = popopulations can=20 include cancer initiating cells as well [36], [37]. The efficient targeting of=20 CD133-positive and CD133-negative glioma cells has also been = described for=20 adenoviral vectors [38], [39]. We further demonstrated that sorted = cells from=20 tumors transduced either by lentiviral LCMV-GP or VSV-G = pseudotyped=20 lentiviral vectors had the ability to form spheroids upon = culturing in=20 neural basal medium supplemented with EGF and bFGF. Spheroids from = both=20 sorted cell populations expressed the neural stem cell markers = nestin and=20 SOX2 and showed the ability to express the differentiation markers = GFAP=20 and =CE=B2-tubulinIII under serum conditions. These properties = have been=20 described for neural progenitor cells [40] as well as for cancer = stem-like=20 cells in human glioblastoma [26]. Thus, the cell populations = transduced by=20 LCMV or VSV pseudotyped lentiviral vectors showed features of = cancer=20 stem-like cells which might be an important target for = therapy. In a therapeutic approach using the = suicide gene=20 HSV-1-tk fused to eGFP, we demonstrated a highly = significant=20 therapeutic effect for both lentiviral vectors compared to control = groups.=20 Using MRI to follow tumor growth, we detected complete remission = in 7 out=20 of 8 animals for LCMV-GP and VSV-G pseudotyped vectors after 30 = days of=20 ganciclovir treatment. HSV-1-tk has been reported to be = an=20 effective therapeutic gene in previous studies [19], [41]. The limited success in = clinical=20 studies has been a result of inefficient gene delivery systems = rather than=20 lack of efficacy of the suicide mechanism [11]. However, there is still = space for=20 improvement of the prodrug delivery such as application length, = treatment=20 intervals and route of delivery. Tai et al. demonstrated that = multiple=20 cycles of prodrug application are superior over one cycle of = prodrug [42]. In our study, we still = detected=20 GFP-positive tumor cells after one cycle (30 days) of ganciclovir=20 administration in treated animals indicating that application in = cycles=20 might also improve the therapeutic effect in this setting. = Further, these=20 results demonstrate that vector-transduced tumor cells retain the = ability=20 to invade brain tissue and migrate even to distant brain = regions. In conclusion, the present = study=20 demonstrates an efficient transduction and therapy of experimental = human=20 glioblastoma by lentiviral vectors. The inefficient gene transfer = by=20 gammaretroviral vectors is in line with the results obtained in = clinical=20 trials and thus confirms the high relevance of the spheroid-based = glioma=20 animal model for translational = research.
	Acknowledgments We thank Mariana Carstov, Narve Brekka, = Roswitha=20 Seyd, Hege Dale and Endy Spriet for expert technical=20 assistance.
	Footnotes Competing Interests: = The=20 authors have declared that no competing interests exist. Funding: This = work was=20 supported by the Research Council of Norway (grant 186492 to HM), = The=20 Norwegian Cancer Society, Helse Vest, Haukeland University = Hospital, the=20 Bergen Translational Research Programme, the European Commission = 6th=20 Framework Programme (Contract 504743) and by the Koeln Fortune = Program at=20 the University of Cologne (grant 28/2006 to HM). The funders had = no role=20 in study design, data collection and analysis, decision to = publish, or=20 preparation of the manuscript.
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(moveToY > 0 ? moveToY : moveToYDefault)=0A= }=0A= catch (e) {}=0A= =0A= var wLeftTopCornerOptions =3D ',left=3D' + moveToX + ',top=3D' + = moveToY + ',screenX=3D' + moveToX + ',screenY=3D' + moveToY=0A= =0A= allOptions =3D allOptions + wLeftTopCornerOptions=0A= =0A= w =3D window.open (link, windowname, allOptions)=0A= w.focus()=0A= =0A= link.target=3Dwindowname=0A= =0A= return false;=0A= }=0A= =0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function focuswin(windowname)=0A= {=0A= windowname =3D String(windowname).replace(/-/g, "_")=0A= w =3D = window.open("",windowname,"menubar=3Dyes,scrollbars=3Dyes,toolbar=3Dyes,l= ocation=3Dyes,status=3Dyes,directories=3Dyes,resizable=3Dyes");=0A= w.focus();=0A= =0A= return true;=0A= }=0A= =0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function reverseString (inStr)=0A= {=0A= var outStr =3D ''=0A= =0A= for (i =3D0; i <=3D inStr.length; i++)=0A= {=0A= outStr =3D inStr.charAt(i) + outStr=0A= }=0A= =0A= return outStr=0A= }=0A= =0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function reverseAndReplaceString (inStr, findStr, newStr)=0A= {=0A= return reverseString(inStr).replace(findStr, newStr)=0A= }=0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function initUnObscureEmail (className, innerHTML)=0A= {=0A= =0A= try{=0A= if (window.addEventListener)=0A= window.addEventListener('load', function() {unObscureEmail = (className, innerHTML)}, false)=0A= else if (window.attachEvent)=0A= window.attachEvent('onload', function() {unObscureEmail = (className, innerHTML)})=0A= }catch(e){=0A= }=0A= }=0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function unObscureEmail (className, innerHTML)=0A= {=0A= try {=0A= if (typeof(unObscuredEmails) =3D=3D 'undefined')=0A= unObscuredEmails =3D new Array()=0A= =0A= if (! unObscuredEmails[className])=0A= {=0A= =0A= var elmnts =3D document.getElementsByTagName("span")=0A= for (var i =3D 0, len =3D elmnts.length; i < len; i++)=0A= {=0A= if (elmnts.item(i).className.indexOf(className, " ") = !=3D -1)=0A= {=0A= elmnts.item(i).innerHTML =3D innerHTML;=0A= unObscuredEmails[className] =3D true=0A= =0A= }=0A= }=0A= }=0A= }=0A= catch(e){=0A= }=0A= }=0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function pubMedDbLinkSubmit(control) {=0A= try{=0A= if (control.pubmedOption)=0A= control =3D control.pubmedOption=0A= if (control.options)=0A= location.href =3D = control.options[control.options.selectedIndex].value;=0A= }=0A= catch(e){}=0A= return false;=0A= }=0A= =0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= // elements "a", "area" with "ref" attribute report to redirect utility = before dereferencing link=0A= //=0A= function initRedirectClicks(report_url) {=0A= =0A= if (report_url && typeof jQuery !=3D 'undefined')=0A= jQuery(document).click(function(e) {=0A= =0A= //=0A= if (!e) return true;=0A= //=0A= if (e.shiftKey || e.altKey || e.ctrlKey) return true;=0A= //=0A= var target =3D jQuery(e.target).closest("a[ref], area[ref]");=0A= if (!target || target.length =3D=3D 0) return true;=0A= //=0A= var ref =3D target.attr("ref");=0A= var href =3D target.attr("href")=0A= =0A= // special processing of href element for pubmed's authors=0A= if (typeof (href) !=3D 'undefined' && = href.indexOf('sites/entrez') && href.indexOf('%5Bauth%5D'))=0A= {=0A= var newHref =3D replacePubMedUnsupportedChars(href);=0A= if (newHref !=3D href)=0A= target.attr("href", newHref)=0A= }=0A= =0A= // append ref with value of href if 'redirect-to-url' is = missing in ref.=0A= if (typeof (ref) !=3D 'undefined' && = ref.indexOf('redirect-to-url') =3D=3D -1)=0A= {=0A= ref =3D ref + '&redirect-to-url=3D' + = encodeURIComponent(href)=0A= //=0A= jQuery.ajax({=0A= type: "HEAD",=0A= url: report_url + '?' + ref,=0A= timeout: 1000,=0A= async: false=0A= });=0A= }=0A= =0A= return true;=0A= });=0A= };=0A= =0A= // function to replace unsupported charachters in author names to be = searchable in PubMed database.=0A= function replacePubMedUnsupportedChars (str)=0A= {=0A= // replace low 128 chars automatically=0A= str =3D str.replace(/%26%23(x000[0-7][0-9a-f])%3b/ig,=0A= function($0, $1){=0A= return (String.fromCharCode('0' + $1))=0A= }=0A= )=0A= // replace others based on map and if it is not in the map replace = with empty string.=0A= str =3D = str.replace(/%26%23(x[0-9a-f][0-9a-f][0-9a-f][0-9a-f][0-9a-f])%3b/ig,=0A= function($0, $1){=0A= return (pubmedUnsupportedCharMap[$1] ? = pubmedUnsupportedCharMap[$1] : '')=0A= }=0A= )=0A= return str;=0A= }=0A= //=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= // Based on script written by Dean Edwards, 2005=0A= // http://dean.edwards.name/=0A= =0A= var pmc_script =3D {=0A= addEvent: function(element, type, handler) {=0A= // assign each event handler a unique ID=0A= if (!handler.$$guid) handler.$$guid =3D this.addEvent_guid++;=0A= // create a hash table of event types for the element=0A= if (!element.events) element.events =3D {};=0A= // create a hash table of event handlers for each element/event pair=0A= var handlers =3D element.events[type];=0A= if (!handlers) {=0A= handlers =3D element.events[type] =3D {};=0A= // store the existing event handler (if there is one)=0A= if (element["on" + type]) {=0A= handlers[0] =3D element["on" + type];=0A= }=0A= }=0A= // store the event handler in the hash table=0A= handlers[handler.$$guid] =3D handler;=0A= // assign a global event handler to do all the work=0A= element["on" + type] =3D handleEvent;=0A= =0A= =0A= function handleEvent(event) {=0A= var returnValue =3D true;=0A= // grab the event object (IE uses a global event object)=0A= event =3D event || fixEvent(window.event);=0A= // get a reference to the hash table of event handlers=0A= var handlers =3D this.events[event.type];=0A= // execute each event handler=0A= for (var i in handlers) {=0A= this.$$handleEvent =3D handlers[i];=0A= if (this.$$handleEvent(event) =3D=3D=3D false) {=0A= returnValue =3D false;=0A= }=0A= }=0A= return returnValue;=0A= };=0A= =0A= function fixEvent(event) {=0A= // add W3C standard event methods=0A= event.preventDefault =3D fixEvent.preventDefault;=0A= event.stopPropagation =3D fixEvent.stopPropagation;=0A= return event;=0A= };=0A= =0A= fixEvent.preventDefault =3D function() {=0A= this.returnValue =3D false;=0A= };=0A= =0A= fixEvent.stopPropagation =3D function() {=0A= this.cancelBubble =3D true;=0A= };=0A= },=0A= =0A= // a counter used to create unique IDs=0A= addEvent_guid: 1,=0A= =0A= removeEvent: function(element, type, handler) {=0A= // delete the event handler from the hash table=0A= if (element.events && element.events[type]) {=0A= delete element.events[type][handler.$$guid];=0A= }=0A= }=0A= }=0A= =0A= // = *************************************************************************= ***=0A= // implementation of figure's popup using jQuery and = jQuery.fn.hoverIntent lib=0A= // it set appropriate handlers for all "a" elements with "figpopup" = class name.=0A= // = *************************************************************************= ***=0A= if (typeof jQuery !=3D 'undefined' && typeof jQuery.fn.hoverIntent !=3D = 'undefined') {=0A= (function($j) {=0A= // = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D hoverHandlers = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=0A= var hoverHandlers =3D function (opts) {=0A= this.config =3D {}=0A= this.self =3D this;=0A= this.__init(opts)=0A= }=0A= =0A= $j.fn.extend(hoverHandlers.prototype, {=0A= //=0A= __init: function(opts) {=0A= $j.fn.extend(this.config, opts)=0A= },=0A= //=0A= over: function (el) {=0A= var canvas =3D $j('.large-thumb-canvas', el)=0A= var prnt =3D canvas.parent();=0A= var win =3D $j(window)=0A= =0A= //=0A= if (canvas && prnt && win)=0A= {=0A= =0A= // collect necessary coordinates from all = intresting objects=0A= canvas.coords =3D this._x_coords(canvas, = 'canvas')=0A= prnt.coords =3D this._x_coords(prnt, = 'parent')=0A= win.coords =3D this._x_coords(win, = 'window')=0A= =0A= // replace @src with value of @hires, because = href hold high resolution image and src low one.=0A= $j('img', canvas).attr('src',=0A= function(){=0A= var hires =3D $j(this).attr("hires");=0A= return (typeof (hires) !=3D = 'undefined' && hires !=3D this.src)=0A= ? hires : this.src=0A= }=0A= )=0A= =0A= // make arrangement of canvas in the view port = nearby parent element.=0A= var cnvsRltvToPrnt =3D = this._x_arrange_canvas(canvas.coords, prnt.coords, win.coords)=0A= =0A= // visualize the canvas with images.=0A= canvas.css('top', cnvsRltvToPrnt.top + 'px')=0A= canvas.css('left', cnvsRltvToPrnt.left + 'px')=0A= canvas.css('display', 'block')=0A= } // canvas=0A= }, // over=0A= //=0A= out: function (el) {=0A= var canvas =3D $j('.large-thumb-canvas', el)=0A= canvas.css('display', 'none')=0A= },=0A= //=0A= _x_offset: function(el, elname) {=0A= var c =3D {}=0A= if (el[0] =3D=3D window )=0A= c =3D this._x_scroll(el, elname)=0A= else=0A= c =3D el.offset()=0A= //console.info('%s.offset {top,left} =3D {%s, %s}', = elname, c.top, c.left)=0A= return c=0A= },=0A= _x_scroll: function(el, elname) {=0A= var c =3D {top: el.scrollTop(), left: = el.scrollLeft()}=0A= //console.info('%s.scroll {top,left} =3D {%s, %s}', = elname, c.top, c.left)=0A= return c=0A= },=0A= _x_width: function(el, elname) {=0A= var w =3D el.outerWidth() || el.width()=0A= //console.info('%s.width =3D %s; outerWidth =3D = %s; width =3D %s', elname, w, el.outerWidth(), el.width())=0A= //IE: alert(elname + '.width =3D ' + w + '; = outerWidth =3D ' + el.outerWidth() + 'width =3D ' + el.width())=0A= return w=0A= },=0A= _x_height: function(el, elname) {=0A= var h =3D el.outerHeight() || el.height()=0A= // console.info('%s.height =3D %s', elname, h)=0A= return h=0A= },=0A= _x_coords: function(el, elname) {=0A= var size =3D { width: this._x_width (el, elname), = height: this._x_height(el, elname)}=0A= var coords =3D {=0A= scroll: this._x_scroll(el, elname),=0A= width: size.width,=0A= height: size.height,=0A= offset: this._x_offset(el, elname),=0A= size: size=0A= }=0A= return coords=0A= },=0A= _x_get_rltv_coord: function(trgtObj, baseObj, = label) {=0A= var c =3D {top: trgtObj.top - baseObj.top, left: = trgtObj.left - baseObj.left}=0A= //console.info("%s {top: %s, left: %s}", label, = c.top, c.left)=0A= return c=0A= },=0A= //=0A= _x_get_empty_space: function(objCoords, = objSize, viewPortCoords, viewPortSize, label) {=0A= var objRelToViewPort =3D = this._x_get_rltv_coord(objCoords, viewPortCoords, '_x_get_empty_space: = for ' + label);=0A= var c =3D {above: objRelToViewPort.top,=0A= below: viewPortSize.height - = (objRelToViewPort.top + objSize.height),=0A= left: objRelToViewPort.left,=0A= right: viewPortSize.width - = (objRelToViewPort.left + objSize.width)}=0A= $j.each(c, function(k, v){c[k] =3D (v < 0 ? 0 : v)})=0A= //console.info("%s {above: %s, below: %s, left: %s, = right: %s}", label, c.above, c.below, c.left, c.right)=0A= return c=0A= },=0A= //=0A= _x_get_bigest_space_area_name: function(spaces, label) {=0A= var sArr =3D [];=0A= for (k in spaces){ sArr[sArr.length] =3D {k: k, v: = spaces[k]} }=0A= // sort in reverse order=0A= sArr.sort (function(a,b){return ( a.v < b.v ? 1 : ( = a.v > b.v ? - 1 : 0 ) )})=0A= // console.info('%s: %s', label, sArr[0].k)=0A= return sArr[0].k=0A= },=0A= //=0A= _x_get_space_ratios: function(spaces, = viewPortSize, label) {=0A= var ratios =3D {above: 0, left: 0}=0A= if (viewPortSize.height > 0)=0A= ratios.above =3D spaces.above / = viewPortSize.height=0A= if (viewPortSize.width > 0)=0A= ratios.left =3D spaces.left / viewPortSize.width=0A= // console.info('ratio: %s {above: %s, left: %s}', = label, ratios.above, ratios.left)=0A= return ratios=0A= },=0A= _x_arrange_canvas: function(c_c, prnt_c, = viewp_c) {=0A= // then calculate empty space areas around parent = element of the canvas, which is ususally an anchor ("a" element)=0A= var emptySpacesArndPrntInViewPort =3D = this._x_get_empty_space (prnt_c.offset, prnt_c.size, viewp_c.offset, = viewp_c.size, 'emptySpacesArndPrntInWinPort')=0A= =0A= // get the area name, where the most linear space = avaiable=0A= var areaName =3D = this._x_get_bigest_space_area_name(emptySpacesArndPrntInViewPort, = viewp_c.size, 'spacios areaName')=0A= =0A= // calculate the proportions of area to be taken by = canvas in empty space area=0A= // relativly to the parent element.=0A= var ratios =3D = this._x_get_space_ratios(emptySpacesArndPrntInViewPort, viewp_c.size, = 'ratios')=0A= =0A= // calculate parent's coordinates relative to view = port=0A= var prntRltvToViewPort =3D = this._x_get_rltv_coord(prnt_c.offset, viewp_c.offset, = 'prntRltvToViewPort')=0A= =0A= // declare canvas relative coordinates=0A= var cnvsRltvToPrnt =3D {top: 0, left: 0}=0A= =0A= // choose appropriate location for placing canvas.=0A= // and choose the 1st element of an array as the one = with the biggest area around parent of canvas.=0A= // console.info ('place it at the %s', = bigestEmptySpaceAreaName)=0A= // calculations are relative to the left corner of = the parent element of canvas. (it has to have the css property = position:relative)=0A= switch (areaName)=0A= {=0A= case 'above':=0A= cnvsRltvToPrnt.top =3D - c_c.height=0A= cnvsRltvToPrnt.left =3D prnt_c.width * 0.5 - = c_c.width * ratios.left=0A= break;=0A= case 'below':=0A= cnvsRltvToPrnt.top =3D prnt_c.height=0A= cnvsRltvToPrnt.left =3D prnt_c.width * 0.5 - = c_c.width * ratios.left=0A= break;=0A= case 'left':=0A= cnvsRltvToPrnt.left =3D - c_c.width=0A= cnvsRltvToPrnt.top =3D prnt_c.height * 0.5 = - c_c.height * ratios.above=0A= break;=0A= case 'right':=0A= cnvsRltvToPrnt.left =3D prnt_c.width=0A= cnvsRltvToPrnt.top =3D prnt_c.height * 0.5 = - c_c.height * ratios.above=0A= break;=0A= }=0A= =0A= // recalculate canvas' coordinates relative to = parent into coordinates relative to view port.=0A= var cnvsRltvToViewPort =3D {=0A= top: prntRltvToViewPort.top + = cnvsRltvToPrnt.top,=0A= left: prntRltvToViewPort.left + = cnvsRltvToPrnt.left=0A= }=0A= //console.info("cnvsRltvToPrnt {top:%s, left: %s}", = cnvsRltvToPrnt.top, cnvsRltvToPrnt.left)=0A= //console.info("cnvsRltvToViewPort {top:%s, left: = %s}", cnvsRltvToViewPort.top, cnvsRltvToViewPort.left)=0A= =0A= // adjust relative position of canvas to the window = if calculated values=0A= // are forcing canvas go out of view port=0A= // next order should be preserved to keep left top = corner visible always=0A= =0A= // adjust right side and move a bit to the left=0A= if (cnvsRltvToViewPort.left + c_c.width > = viewp_c.width)=0A= {=0A= var horAdj =3D c_c.width - (viewp_c.width - = cnvsRltvToViewPort.left)=0A= cnvsRltvToPrnt.left -=3D horAdj=0A= cnvsRltvToViewPort.left -=3D horAdj=0A= //console.log('adjust right side and move to = the left %spx', horizontalAdjustment)=0A= }=0A= =0A= // adjust below side and move to the top=0A= if (cnvsRltvToViewPort.top + c_c.height > = viewp_c.height)=0A= {=0A= var vertAdj =3D c_c.height - (viewp_c.height - = cnvsRltvToViewPort.top)=0A= cnvsRltvToPrnt.top -=3D vertAdj=0A= cnvsRltvToViewPort.top -=3D vertAdj=0A= // console.log('adjust below side and move to = the top %spx', verticalAdjustment)=0A= }=0A= =0A= // adjust left side and move to the right=0A= if (cnvsRltvToViewPort.left < 0)=0A= {=0A= // console.log('adjust left side and move to the = right %spx', -(cnvsLeftRelativeToWindowPort))=0A= cnvsRltvToPrnt.left -=3D = cnvsRltvToViewPort.left=0A= cnvsRltvToViewPort.left =3D 0=0A= }=0A= // adjust above side and move to the bottom=0A= if (cnvsRltvToViewPort.top < 0)=0A= {=0A= // console.log('adjust above side and move to = the bottom %spx', -(cnvsTopRelativeToWindowPort))=0A= cnvsRltvToPrnt.top -=3D = cnvsRltvToViewPort.top=0A= cnvsRltvToViewPort.top =3D 0=0A= }=0A= // console.info("cnvsRltvToPrnt adjusted {top: %s, = left: %s}", cnvsRltvToPrnt.top, cnvsRltvToPrnt.left)=0A= // console.info("cnvsRltvToViewPort adjusted {top: = %s, left: %s}", cnvsRltvToViewPort.top, cnvsRltvToViewPort.left)=0A= return cnvsRltvToPrnt=0A= }=0A= })=0A= // = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D end of hoverHandlers = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= =0A= // = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D $j.fn.figPopup = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function hoverOverHandler () {=0A= var h =3D new hoverHandlers();=0A= h.over(this)=0A= }=0A= =0A= function hoverOutHandler () {=0A= var h =3D new hoverHandlers();=0A= h.out(this)=0A= }=0A= =0A= $j.fn.figPopup =3D function(opts){=0A= var config =3D {=0A= interval: 500,=0A= timeout: 0,=0A= over: hoverOverHandler, // handler onMouseOver=0A= out: hoverOutHandler // handler onMouseOut=0A= }=0A= $j.extend(config, opts)=0A= return config=0A= }=0A= =0A= // = =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D end of $j.fn.figPopup = 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