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Publication history

Accepted article online:
14 Feb 2008=20
Published article online:
05 Mar 2008

Received December 14, 2007; revised manuscript = received=20 February 7, 2008; accepted February 8, 2008.

Abbreviations

AMPA: alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate
EAAT: excitatory amino acid transporter

Tables & Images

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Fig. 1 Gliomas destroy normal brain = as the=20 tumor expands. Examples of patient images from four = differe...

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Fig. 2 Gliomas release glutamate. = (a) Gliomas=20 in vivo do not express the GLT-1 glutamate transporter=20 (...

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Fig. 3 Cystine=E2=80=93glutamate = exchange in gliomas.=20 (a) Glioma cell lines and acute biopsies highly express = t...

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Fig. 4 Inhibition of system = X^c=20 causes GSH depletion and reduces tumor size in vivo. (a)=20 Sulfasalazine,...

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Fig. 5 Glioma cells respond to = glutamate as=20 they invade. (a) Ca²⁺ imaging shows oscillatory changes=20 in...

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Journal of Neurochemistry

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To cite this article: Harald Sontheimer (2008)
A = role=20 for glutamate in growth and invasion of primary brain tumors=20
doi:10.1111/j.1471-4159.2008.05301.x

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MINI-REVIEW

A role for glutamate in growth and invasion = of primary=20 brain tumors

Harald Sontheimer

Department of Neurobiology & Center for Glial Biology in=20 Medicine, The University of Alabama Birmingham, Birmingham, Alabama,=20 USA

Address correspondence and reprint = requests to=20 Harald Sontheimer PhD, Department of Neurobiology, The University of = Alabama at=20 Birmingham, 1719 6th Ave S., CIRC 410, Birmingham, AL 35294-0021, USA. = E-mail:=20 sontheimer@uab.edu

AMPA, = alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate; EAAT, excitatory = amino=20 acid transporter.

Abstract

The vast majority of primary brain tumors derive from = glial cells=20 and are collectively called gliomas. While, they share some genetic = mutations=20 with other cancers, they do present with a unique biology and have = developed=20 adaptations to meet specific biological needs. Notably, glioma growth is = physically restricted by the skull, and, unless normal brain cells are=20 destroyed, tumors cannot expand. To overcome this challenge, glioma = cells=20 release glutamate which causes excitotoxic death to surrounding neurons, = thereby=20 vacating room for tumor expansion. The released glutamate also explains=20 peritumoral seizures which are a common symptom early in the disease. = Glutamate=20 release occurs via system X^c, a cystine=E2=80=93glutamate = exchanger that=20 releases glutamate in exchange for cystine being imported for the = synthesis of=20 the cellular antioxidant GSH. It protects tumor cells from endogenously = produced=20 reactive oxygen and nitrogen species but also endows tumors with an = enhanced=20 resistance to radiation- and chemotherapy. Pre-clinical data = demonstrates that=20 pharmacological inhibition of system X^c causes GSH depletion = which=20 slows tumor growth and curtails tumor invasion in vivo. An Food = and Drug=20 Administration approved drug candidate is currently being introduced = into=20 clinical trials for the treatment of malignant glioma.

Gliomas

Malignant gliomas comprise a heterogeneous group of primary CNS = tumors that=20 are believed to originate from glial cells or their progenitor cells.=20 Approximately 18 000 new cases are reported annually and these = account for=20 over 12 000 deaths in the USA (Jemal=20 et al. 2006). Although the majority of gliomas present = in=20 patients over the age of 55, gliomas are the most common solid cancer in = children (Maher and Raffel = 2004).=20 Unfortunately, tumor incidence has increased steadily over the past=20 30 years (Jemal = et al.=20 2006) and the prognosis remains dismal (Azizi and Miyamoto 1998). Effective = therapies=20 are lacking thus limiting treatment to radiation therapy and, where = possible,=20 surgery (Butowski et al. = 2006). Average survival following diagnosis can be up to = 5 years but,=20 more commonly, patients diagnosed with high-grade glioma succumb to the = disease=20 within just 6=E2=80=9312 months (Huncharek and=20 Muscat 1998).

Tumors generally form only from growth competent cells, hence, in the = brain,=20 primary tumors arise typically from glial cells and cells associated = with the=20 vasculature and meninges. These tumors are collectively called gliomas = (Kleihues et al., = 1995) with=20 the majority believed to originate from astrocytes, or their progenitor = cells.=20 Astrocytes retain the ability to divide throughout life and respond to = acute=20 injury and neurological disease through proliferation and the formation = of scar=20 tissue (Little and = O=E2=80=99Callagha 2001).=20 These scar-associated astrocytes eventually divide and differentiate, = leaving a=20 tenacious tissue barrier. By contrast, glial-derived tumors fail to=20 differentiate thereby maintaining unrestrained growth. Events that = trigger=20 malignant transformation of glial cells into gliomas are poorly = understood.=20 Genetic alterations in oncogenes [v-src, murine-double-minute-2 (MDM-2), = cyclin-dependent kinase 4 (CDK-4), and epidermal growth factor receptor = (EGFR)]=20 and tumor suppressor genes (p53, p16, p15, and RB1) are common = characteristics=20 (Louis 1994; Von Deimling et al. = 1995; Maher et al. 2001; Shapiro 2001) of the = transformation of glial=20 progenitor cells into tumor-forming cells in mice (Holland et al. = 1998).

Gliomas share many fundamental biological alterations = with other=20 cancers. For example, they frequently show amplification of a = constitutively=20 active epidermal growth factor receptor that enhances tumor growth in = the=20 absence of exogenous growth factors (Tang=20 et al. 1997). Tumor suppressor genes such as p16 and p53 = are=20 frequently mutated (Von Deimling=20 et al. 1995). The induction of new blood vessels, or=20 neovascularization, is a typical feature of many tumors and also = characterizes=20 high-grade gliomas (Plate and Risau = 1995). Despite these commonalities with other tumors, gliomas = exhibit unique=20 biological traits and have developed adaptations to support their unique = biology. One of these physiological adaptations will be illustrated in = this=20 paper.

Physical constraints to tumor growth

Essentially all systemic tumors grow within soft tissue and are not=20 physically limited in their growth. By contrast, primary brain tumors = can only=20 expand within the bony cavity of the cranium which ultimately limits = tumor=20 growth. Eighty-five percent of cranial volume is occupied by brain = tissue with=20 the remaining 15% filled with CSF. Ultimately, this space becomes = insufficient=20 for tumor expansion, necessitating the destruction and removal of normal = brain=20 tissue. Early in the disease progression tumors can be seen to push into = the=20 fluid spaces and often displace brain tissue, leading for example to a = shift in=20 midline structures as illustrated in Fig. 1. It should be noted = that the=20 brain, like any body tissue, is incompressible given its cellular = constituents=20 are predominantly composed of water. However, text books and reviews = frequently=20 but incorrectly remark on the ability of growing tumors to compress the = brain.=20 One may refer more accurately to this phenomenon as a displacement of = tissue=20 into fluid-filled spaces, notably the ventricles. Figure 1 provides several = examples=20 illustrating how different sized tumors integrate into normal brain by=20 displacing the surrounding brain tissue. In each instance, however, the=20 characteristic gyrations of the cortical brain surface remains = essentially=20 unaltered and without evidence of compression. Hence, in each instance = tumors=20 have vacated the space into which they grew rather than simply pushing = it aside.=20 Surprisingly, little attention had been paid to the mechanism(s) whereby = gliomas=20 destroy normal brain tissue as they grow.

To fill this void, recent studies have examined this = question and=20 collectively suggest that glioma cells, at the growth margins of an = expanding=20 tumor, release the neurotransmitter glutamate into adjacent brain tissue = at=20 concentrations that are sufficient to cause neuronal cell death (Behrens et al. 2000; Chung et al. 2005). = Glutamate is=20 the major excitatory neurotransmitter in the brain and is normally = restricted to=20 the synaptic and perisynaptic space of glutamateric synapses. Here, the=20 transmitter binds to post-synaptic neuronal glutamate receptors and = mediates=20 fast signal transmission. In this restricted synaptic space glutamate = rises to=20 millimolar concentrations, yet its concentration in the extracellular = space is=20 typically very low, i.e. around 1 =CE=BCM, to prevent the erroneous = activation=20 of extrasynaptic glutamate receptors. Prolonged activation of neuronal = glutamate=20 receptors, particularly NMDA receptors, can trigger a sustained influx = of=20 Ca²⁺ which readily overwhelms intracellular Ca²⁺=20 regulatory processes ultimately leading to Ca²⁺-mediated cell = death=20 (Choi 1988). This process, = introduced=20 several decades ago (Olney = et al.=20 1971) and termed excitotoxicity, is now believed to be a final = common death=20 pathway in many neurological diseases including acute trauma, ischemic = stroke,=20 amyotrophic lateral scelerosis (ALS) and Alzheimer=E2=80=99s disease (Choi 1988; Lipton and Rosenberg 1994). = Because of the=20 vulnerability of the brain to excessive glutamate, protective mechanisms = evolved=20 in the form of Na⁺-dependent transport systems that maintain=20 extracellular glutamate at harmless micromolar concentrations (Danbolt 2001). These transporters = are=20 predominantly expressed on astrocytes (Danbolt 2001) and include the = excitatory=20 amino acid transporters 1 and 2 (EAAT1 and 2) formerly known as glial = amino acid=20 transporter and glutamate transporter-1 (Danbolt 2001). Their role in = neuroprotection=20 has been conclusively demonstrated through knockout studies in which a = loss of=20 glutamate uptake by glial cells resulted in widespread neurodegeneration = and=20 lethal epilepsy (Rothstein = et al.=20 1996; Tanaka et al. = 1997).

Glioma cells release glutamate and kill peritumoral neurons = by an=20 excitoxic mechanism

The first evidence that glial-derived tumor cells = release=20 glutamate rather than remove it from the extracellular space came from a = transport study that directly compared normal and malignant glial cells = (Ye et al. 1999). This = study used=20 glioma cell lines established from patients as well as acute patient = biopsy=20 tissues showing a lack of expression of the most prominent astrocytic = glutamate=20 transporter EAAT2 (glutamate transporter-1), a finding that was recently = corroborated by microarray analysis of glioma tissues (de Groot et al. 2005). = Staining=20 of tissue biopsies with EAAT2 antibodies clearly demarcates the tumor = boundaries=20 where non-malignant astrocytes prominently express EAAT2, yet gliomas = lack its=20 expression (Fig. 2a). = During=20 embryonic development, astrocytes also express EAAT1 (glial amino acid=20 transporter) and many cultured astrocytes maintain expression of this = related=20 member of the EAAT family of Na⁺-dependent transporters (Ullensvang et al. = 1997).=20 Interestingly, EAAT1 is found mislocalized to the nucleus of gliomas in = brain=20 biopsies from glioma patients (Ye=20 et al. 1999). This failure to express functional = glutamate=20 transporters results in significant reductions in glutamate uptake, = representing=20 at best 5% of that observed in normal astrocytes. More surprising was = the=20 converse finding that these tumor cells actually release glutamate. In = the=20 presence of extracellular cystine, a monolayer of cultured glioma cells = is able=20 to raise extracellular glutamate concentrations in a culture flask = 500-fold=20 within just a few hours (Fig. 2b).=20 When hippocampal or cortical neurons are placed in the vicinity of = gliomas,=20 neurons undergo NMDA-dependent excitotoxic cell death (Fig. 2c) (Ye and Sontheimer 1999). Further = molecular,=20 pharmacological, and ion-dependence studies ultimately led to the = identification=20 of system X^c, a cystine=E2=80=93glutamate exchanger (Ye et al. 1999), as = the=20 principal protein responsible for glutamate release from glioma cells = (Ye and Sontheimer 1999). Once = released into=20 the peritumoral space (Ye and = Sontheimer=20 1999; Takano et al. = 2001), glutamate causes widespread excitotoxic death of peritumoral = neurons=20 (Ye and Sontheimer 1999). We = and others=20 have proposed that this form of excitotoxic neuronal cell death allows = the tumor=20 to expand into the vacated space (Takano=20 et al. 2001). In a more recent study discussed below (Lyons et al. 2007), we = suggest=20 that the released glutamate may also serve as a trophic factor promoting = glioma=20 cell invasion and the formation of tumor metastasis. It is worth = mentioning that=20 glutamate has been shown to more broadly influence the biology of = malignant and=20 non-malignant glial cells. For example, activation of metabotropic, = G-protein=20 coupled glutamate receptors stimulates DNA synthesis and activates=20 mitogen-activated protein kinases in astrocytes (Schinkmann et al. = 2000). In=20 glioma cells, Ca²⁺ influx through=20 alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors = stimulates=20 cell proliferation through phosphorylation of AKT (Ishiuchi et al. 2007). = Moreover,=20 in areas of tissue inflammation, glutamate activates microglial cells = (Biber et al. 2007) = which would be=20 expected to contribute to the inflammatory milieu around a growing = tumor. These=20 additional effects of glutamate will undoubtedly contribute to the = evolution of=20 the disease and warrant further study.

Glutamate release is mediated by the = cystine=E2=80=93glutamate antiporter=20 system X^c

As indicated above, the Na⁺ independent release of = glutamate=20 occurs via the system X^c cystine glutamate antiporter. This=20 electroneutral, Na⁺ independent amino acid transporter (Sato et al. 1999) = exchanges=20 cystine for glutamate (GLU) (Ye=20 et al. 1999) and is up-regulated under conditions of = oxidative=20 stress (Kim et al. = 2001).=20 Molecular cloning identified this transporter as a dimeric protein = composed of a=20 catalytic (xCT) and a regulator subunit (4F2hc). The transporter is = found in=20 both normal and malignant human brain by western blot (Fig. 3a) but appears = universally=20 up-regulated in glioma tissues. Indeed, being responsible for the = cellular=20 synthesis of GSH and hence cellular redox regulation, it is not = surprising that=20 system X^c is regulated by oxidative stress and nitric oxide = (Dun et al. 2006) = presumably via=20 the activation of transcription factor NF-E2-related factor which = regulate xCT=20 transcription via binding to an antioxidant response element (Sun et al. 2005). In = normal glia=20 cells, system X^c does not account for a significant glutamate = release=20 as any glutamate release through the antiporter in conjunction with = cystine=20 uptake is quickly removed through reuptake by EAAT2 which has a much = higher=20 capacity for Glu transport and a high affinity of extracellular Glu. = This=20 concept is schematized in Fig. 3c. In=20 turn, the lack of reuptake mechanisms in gliomas explains a progressive=20 accumulation of glutamate in the vicinity of the tumor which inflicts=20 excitotoxic injury on adjacent neurons as schematized in Fig. 3d.

Although the initial studies investigating glutamate = release from=20 gliomas were based on cultured cells (Ye and=20 Sontheimer 1999) and animal models bearing experimental gliomas (Takano et al. 2001), = these=20 findings have now been corroborated in patients with malignant gliomas. = One of=20 these studies used microdialysis (Roslin=20 et al. 2003) to directly sample peritumoral fluids in = fully=20 ambulatory glioma patients; the other used spectroscopic magnetic = resonance=20 imaging to detect glutamate (Rijpkema=20 et al. 2003). Both studies confirm significant increases = in=20 peritumoral glutamate in all glioma patients examined. This finding = explains why=20 up to 80% of all glioma patients present with peritumoral seizures, many = of them=20 during early, often less malignant stages of the disease (Oberndorfer et al. = 2002). The=20 glutamate released from gliomas would be expected to activate neuronal = glutamate=20 receptors that underlie such seizures in the vicinity of the tumor and = likely=20 precede excitotoxic cell death.

Glutamate release is an obligatory byproduct of GSH=20 synthesis

While the excitotoxic elimination of peritumoral neurons = may be of=20 potential benefit to the growing tumor, it is unlikely that this pathway = evolved=20 with the primary purpose to kill neurons. Instead, it is more likely = that=20 glutamate release occurs as an obligatory byproduct of cystine uptake by = these=20 tumor cells (Fig. 3b and = e). Cystine=20 is an essential precursor for the biosynthesis of the cellular = antioxidant GSH,=20 a tripeptide of glutamate, cysteine (the reduced form of cystine) and = glycine.=20 The supply of cysteine is essential for GSH biosynthesis making cellular = uptake=20 of cystine rate limiting for overall GSH production. GSH levels are = increased in=20 gliomas and may make these tumors more resistant to oxidative stress and = exposure to certain chemotherapeutic drugs (Iida et al. 1997). = Importantly,=20 radiation damage which is mediated by hydroxyl radicals (Knuutila 1984) is also reduced by = GSH (Simone et al. 1983) = and hence=20 elevated GSH levels confer radiation resistance to tumors (Mitchell et al. = 1989).

Therapeutic targeting of system X^c-mediated = glutamate=20 release to contain tumor growth

If system X^c represent the major uptake pathway for = cystine and=20 release pathway for glutamate, one would expect that its inhibition = should=20 interfere with tumor growth in two ways. First, limiting cystine uptake = should=20 starve the cells of GSH making the cells more susceptible to oxidative=20 challenges such as radiation treatment. Second, the inhibition of = glutamate=20 release should curtail seizures and may contain tumor expansion. To = examine=20 these possibilities, two pharmacological inhibitors have been identified = as=20 suitable drug candidates. These are S-4CPG, a phenylgycin derivative and = agonist=20 for metabotrobic glutamate receptors (Ye and=20 Sontheimer 1999), and sulfasalazine (Chung=20 et al. 2005), a drug clinically used to treat chronic=20 inflammatory bowl disease. Both drugs inhibit cystine uptake and = glutamate=20 release at 100=E2=80=93250 =CE=BCM drug concentration (Chung et al. 2005). = Importantly,=20 a 24 h exposure to either drug causes the near complete depletion = of=20 intracellular GSH (Fig. 4a) = and in=20 turn leads to growth arrest of gliomas (Chung=20 et al. 2005). The growth retarding effect is entirely = because of=20 a depletion of GSH as cells can be rescued from growth arrest with a = membrane=20 permeant, GSH ester. As sulfasalazine is a Food and Drug Administration = approved=20 drug that can be readily given to patients, pre-clinical studies = examining its=20 growth retarding effect have mainly focused on this compound. = Specifically,=20 severe combined immunodeficient (scid) mice with implanted human = gliomas=20 were treated twice daily by i.p. injection of sulfasalazine for up to=20 10 weeks and tumor response was monitored by bioluminescence = imaging as=20 well as quantitative stereology on histopathological specimens (Chung et al. 2005). As=20 illustrated in Fig. 4, = sulfasalazine=20 reduced tumor volume by 60=E2=80=9380%. These studies were carried out = with=20 sulfasalazine doses comparable with those taken by patients suffering = from=20 Crohn=E2=80=99s disease for which an adequate safety profile is well = established. These=20 findings suggest a rapid path to clinical translation and the = author=E2=80=99s home=20 institution is in the process of initiating a clinical study to evaluate = oral=20 sulfasalazine in a phase I clinical study for patients with malignant=20 glioma.

As a second approach, clinical studies may seek to = inhibit the=20 glutamate receptors targeted on neurons and glioma cells, with neuronal = NMDA=20 receptor being the primary candidate. Although NMDA-receptor antagonists = have=20 had mixed results in the treatment of stroke (Lipton 2004), they may represent a = viable=20 treatment modality in advanced stages of brain cancer warranting further = study.=20 Use-dependent glutamate receptor antagonists such as Amantadine have = been=20 explored with promising indication toward reducing aberrant activation = of=20 neuronal NMDA receptors in clinical studies for stroke (Lipton 2004), Parkinson=E2=80=99s = disease (Verhagen et al. 1998) = and, based=20 on animal studies (Takano = et al.=20 2001), may indeed represent a viable treatment strategy for=20 gliomas.

Glutamate stimulates glioma metastasis

As discussed above, the unusual ability of glioma cells to invade the = normal=20 brain presents a huge clinical challenge. Consequently, a great deal of = research=20 has been devoted toward gaining a better understanding of the underlying = biology. This research has identified a multitude of factors and = adaptations=20 which include a preference for certain substrate for cell migration (Demuth and Berens 2004). Indeed, = invading=20 gliomas can synthesize their own unique extracellular matrix as they = invade (Zamecnik 2005). These cells = interact with=20 extracellular matrix through integrin receptors (Gladson 1999), also involved in = the dynamic=20 attachment/detachment of focal adhesion sites. Some of these dynamic = changes=20 appear to correlate with changes in intracellular Ca²⁺ (Manning et al. 2000) = and=20 intracellular Ca²⁺ oscillations frequently correlate with = cell=20 migration (Maghazachi 2000). = These have=20 also been observed in migratory glioma cells (Bordey et al. 2000).=20 Ca²⁺ oscillations can be triggered by a number of = extracellular=20 ligands including growth factors (Bryant=20 et al. 2004), lysophosphatidic acid (Manning et al. 2000) = and=20 neurotransmitters such as acetylcholine (Komuro and Rakic 1996) and = glutamate (Kim et al. 1994). = Glutamate is=20 of particular interest in this context as studies on cerebellar granule = cells=20 suggest an absolute requirement for glutamate-mediated Ca²⁺=20 oscillations in neuronal migration (Komuro=20 and Rakic 1996). Here, the activation of NMDA receptor causes the = transient=20 influx of Ca²⁺ which in turn regulates the rate and velocity = of=20 granule cell migration (Komuro and = Rakic=20 1998). Although glioma cells express receptors for glutamate, unlike = granule=20 cells, they do not express NMDA receptor. Instead, they express a = subclass of=20 AMPA receptors which is Ca²⁺ permeable (Lyons et al. 2007). = These=20 receptors lack the GluR2 subunit which is required to prevent = Ca²⁺=20 permeation (Hollmann = et al.=20 1991) resulting in Ca²⁺ permeable AMPA receptor. To = demonstrate a=20 role for these receptors in glioma migration, Ishiuchi et al. (2002) = transfected the GluR2 subunit into glioma cells using a viral = transfection=20 system. This rendered glioma cells unable to respond to glutamate with=20 Ca²⁺ oscillations and upon implantation into a host animal = brain=20 these glioma cells failed to invade. Hence glutamate acts to promote = cell=20 migration through activating Ca²⁺ entry. Although glioma = cells=20 utilize a different receptor system, they appear to recapitulate the = same=20 underlying biology that is observed in early development in neuronal = migration.=20 Interestingly, oligodendrocytes progenitor cells which may be a = non-malignant=20 precursor for gliomas (Dai = et al.=20 2001) have recently been shown to engage AMPA-receptor activation as = they=20 migrate. Here, glutamate binding to AMPA receptor causes the formation = of an=20 alphav integrin/proteolipid protein (PLP)/neurotransmitter receptor = protein=20 complex that reduces binding to the extracellular matrix thereby = enhancing=20 oligodendrocytes progenitor cells migration (Gudz et al. 2006).

In the case of neurons, the source for glutamate acting in a=20 migration-promoting way (i.e. as a =E2=80=98motogen=E2=80=99) is = unknown. In gliomas, glutamate=20 is release from the tumor cells themselves and may function in a dual = capacity.=20 It clears the way for the tumor growth, and it may activate AMPA = receptors on=20 the same or neighboring glioma cells to initiate the necessary = Ca²⁺=20 signal for promoting cell motility and invasion. Indeed, recent studies = support=20 this hypothesis (Lyons = et al.=20 2007), suggesting that glioma cells respond preferentially to = glutamate=20 released via system X^c. As illustrated in Fig. 5a, inhibition of = glutamate release=20 via system X^c using sulfasalazine inhibits Ca²⁺ = responses=20 and also reduces Transwell glioma migration (Fig. 5b). The fact that = migration could=20 be restored when glutamate was added back into the system in the = continued=20 presence of the system X^c inhibitor sulfasalazine (Fig. 5b) supports a motogenic = function=20 for glutamate. Moreover, the inhibition of AMPA receptors with Jolo-Tx, = a=20 specific inhibitor of Ca²⁺-permeable AMPA receptors, = prevented=20 migration stimulated by glutamate clearly implicating this receptor as = essential=20 in glioma invasion. Together this data supports the hypothesis that = glutamate=20 serves a dual purpose in glioma biology: (i) by acting as an = excitotoxin, it=20 clears space for tumor expansion thereby promoting tumor growth; and = (ii) by=20 acting as a motogen, it enhances the motility and consequently promotes = tumor=20 invasion.

Glioma cells often display chain migration whereby many = cells=20 follow a lone leader (Fig. 5c). It is=20 conceivable that the leading cell recruits its followers through the = targeted=20 (paracrine) release of glutamate as it migrates. These findings have = important=20 therapeutic implications as inhibition of either AMPA receptor on = gliomas or the=20 autocrine glutamate from glioma via system X^c should prevent = glioma=20 metastasis. As alluded to before, glutamate receptor antagonists may = represent a=20 viable approach to reduce glioma invasion and warrant further study. The = inhibition of glutamate release from gliomas using sulfasalazine has not = been=20 previously considered as a glioma therapeutic but now appears to be a = plausible=20 strategy to curtail glioma invasion.

Epilogue

As these examples illustrate, glioma cells utilize = transporters=20 and transmitter receptors in ways to enhance their unique biology. They = appear=20 to co-opt the function of these proteins which are normally involved in=20 cell=E2=80=93cell signaling or to maintain a homeostatic brain = environment. They use=20 them to enhance their own ability to grow and invade normal brain. = Unexpectedly,=20 amino acid transporters may be considered viable and much needed = therapeutic=20 targets for glioma and possibly many other cancers.

Acknowledgements

The author is grateful for the continued supported by = grants from=20 the National Institutes of Health RO1 NS-31234, RO1 NS-52634, RO1 = NS-36692, and=20 P50-CA97247.

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= url(/templates/jsp/_synergy.2/images/layout/btn_submit_icon.gif); = PADDING-BOTTOM: 0px! important; BORDER-LEFT: #999 1px outset; WIDTH: = 3.6em! important; PADDING-TOP: 0px! important; BORDER-BOTTOM: #999 1px = outset; BACKGROUND-REPEAT: no-repeat; BACKGROUND-COLOR: #fff } FORM INPUT.login { PADDING-RIGHT: 28px! important; PADDING-LEFT: 0px! important; = PADDING-BOTTOM: 0px! important; WIDTH: 3.8em! important; PADDING-TOP: = 2px! important } A.login { PADDING-RIGHT: 28px! important; PADDING-LEFT: 0px! important; = PADDING-BOTTOM: 0px! important; WIDTH: 3.8em! important; PADDING-TOP: = 2px! important } A.go_btn { PADDING-RIGHT: 1px! important; MARGIN-TOP: 4px; DISPLAY: block; = PADDING-LEFT: 1px! important; FLOAT: left; PADDING-BOTTOM: 1px! = important; MARGIN-RIGHT: 4em; PADDING-TOP: 1px! important } FORM INPUT.med { WIDTH: 6em! important } A.med { WIDTH: 6em! important } FORM INPUT.wide { WIDTH: 9.5em! important } A.wide { WIDTH: 9.5em! important } FORM INPUT.xwide { WIDTH: 15.3em! important; MARGIN-RIGHT: 8px } A.xwide { WIDTH: 15.3em! important; MARGIN-RIGHT: 8px } #header UL { CLEAR: right; PADDING-RIGHT: 7px; TEXT-ALIGN: right } #header UL#login_sublinks LI { PADDING-LEFT: 8px } #header UL#header_nav { PADDING-RIGHT: 2px; MARGIN-TOP: 8px } #header UL LI { DISPLAY: inline; LIST-STYLE-TYPE: none } DIV.btn_spacer { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 12px; = PADDING-TOP: 6px } #header UL#header_nav { FLOAT: right; WIDTH: auto; MARGIN-RIGHT: 2px } #header UL#header_nav LI { DISPLAY: block; Z-INDEX: 2; FLOAT: left; WIDTH: auto; POSITION: = relative } #header UL#header_nav LI UL.subnav_drop { BORDER-RIGHT: #999 1px solid; PADDING-RIGHT: 0px; BORDER-TOP: #999 1px = solid; PADDING-LEFT: 0px; Z-INDEX: 3; BACKGROUND: #ebebeb; LEFT: -999em; = VISIBILITY: hidden; PADDING-BOTTOM: 0px; BORDER-LEFT: #999 1px solid; = WIDTH: 14em; PADDING-TOP: 0px; BORDER-BOTTOM: #999 1px solid; POSITION: = absolute; TOP: 1.2em; TEXT-ALIGN: left } #header UL#header_nav LI UL.subnav_drop_show { BORDER-RIGHT: #999 1px solid; PADDING-RIGHT: 0px; BORDER-TOP: #999 1px = solid; PADDING-LEFT: 0px; Z-INDEX: 3; BACKGROUND: #ebebeb; LEFT: 0px; = PADDING-BOTTOM: 0px; BORDER-LEFT: #999 1px solid; WIDTH: 14em; = PADDING-TOP: 0px; BORDER-BOTTOM: #999 1px solid; POSITION: absolute; = TOP: 1.2em; TEXT-ALIGN: left } #header UL#header_nav LI:hover UL.subnav_drop { LEFT: 0px; VISIBILITY: visible } #header UL#header_nav LI.sfhover UL.subnav_drop { LEFT: 0px; VISIBILITY: visible } #header UL#header_nav LI:hover UL.rh_drop_1 { LEFT: -11.8em } #header UL#header_nav LI.sfhover UL.rh_drop_1 { LEFT: -11.8em } #header UL#header_nav LI:hover UL.rh_drop_2 { LEFT: -3.5em } #header UL#header_nav LI.sfhover UL.rh_drop_2 { LEFT: -3.5em } #header UL#header_nav LI UL LI A { PADDING-RIGHT: 3px; DISPLAY: block; PADDING-LEFT: 3px; PADDING-BOTTOM: = 2px; WIDTH: 14em; PADDING-TOP: 2px } #subheader { CLEAR: both; BORDER-BOTTOM: white 4px solid; BACKGROUND-COLOR: #d21c1b } #subheader SPAN { VISIBILITY: hidden } .homepage#subheader { CLEAR: both; BACKGROUND-POSITION: right top; OVERFLOW: hidden; = BORDER-BOTTOM: white 4px solid; BACKGROUND-REPEAT: repeat-x; HEIGHT: = 197px } #AdPlaceholder7 { BACKGROUND: #fff } .homepage #main_content H1 { PADDING-RIGHT: 6px; PADDING-LEFT: 6px; PADDING-BOTTOM: 2px; MARGIN: = 0px; PADDING-TOP: 2px; BACKGROUND-COLOR: #d62226 } OL { =09 } .tree_expander OL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 12px; = PADDING-TOP: 0px } .tree_expander OL LI { BACKGROUND-POSITION: 0px 2px; MARGIN-TOP: 6px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/expand_li.gif); = BACKGROUND-REPEAT: no-repeat; LIST-STYLE-TYPE: none } .tree_expander OL LI A { PADDING-LEFT: 15px } .tree_expander OL LI.expanded { BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/contract_li.gif) } .tree_expander OL OL { MARGIN-LEFT: 15px } .tree_expander OL.journal_titles LI { BACKGROUND-IMAGE: none; LIST-STYLE-TYPE: none } .tree_expander OL.journal_titles LI A { PADDING-LEFT: 0px } .tree_expander LI IMG { VERTICAL-ALIGN: top } .tree_expander .issues_list LI { BACKGROUND-IMAGE: none } OL.journals_expander OL.issues_list { MARGIN-LEFT: 0px } OL.journals_expander OL.issues_list LI { LIST-STYLE-TYPE: none } OL.journals_expander OL.journal_checklist { MARGIN-LEFT: 0px } OL.journals_expander OL.journal_checklist LI { LIST-STYLE-IMAGE: none; LIST-STYLE-TYPE: none } OL.journals_expander LI.subscribed_journal A { BACKGROUND-COLOR: #f8dddd } UL.user_access { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 4px; = PADDING-TOP: 4px } .homepage UL.user_access { WIDTH: auto; BORDER-BOTTOM: #ccc 1px solid } .top_border { BORDER-TOP: #ccc 1px solid; MARGIN-TOP: 8px } .bot_border { MARGIN-BOTTOM: 8px; BORDER-BOTTOM: #ccc 1px solid } UL.user_access LI { FLOAT: left; LINE-HEIGHT: 1.7em; MARGIN-RIGHT: 6px; LIST-STYLE-TYPE: = none } FORM#journal_display_control { PADDING-RIGHT: 0px; PADDING-LEFT: 6px; PADDING-BOTTOM: 4px; = 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BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/prev_article_link_arrow.gif);= PADDING-BOTTOM: 0px; PADDING-TOP: 0px } DIV#article_navigation SPAN.prev_article { BORDER-RIGHT: #ccc 1px solid; PADDING-RIGHT: 5px; PADDING-LEFT: 16px; = PADDING-BOTTOM: 0px; PADDING-TOP: 0px } DIV#article_navigation A.next_article { PADDING-RIGHT: 16px; BACKGROUND-POSITION: right center; PADDING-LEFT: = 5px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/next_article_link_arrow.gif);= PADDING-BOTTOM: 0px; PADDING-TOP: 0px } DIV#article_navigation SPAN.next_article { PADDING-RIGHT: 16px; PADDING-LEFT: 5px; PADDING-BOTTOM: 0px; = PADDING-TOP: 0px } DIV.full_text H2 { MARGIN: 7px 0px 0px } UL#article_authors { MARGIN: 7px 0px 0px } UL#article_authors LI { DISPLAY: inline } UL.author_affiliations { MARGIN-TOP: 6px } UL.author_affiliations LI { PADDING-RIGHT: 8px } UL.author_affiliations LI { DISPLAY: inline } UL.author_affiliations LI ADDRESS { DISPLAY: inline } ADDRESS.author_address { PADDING-RIGHT: 0px; BACKGROUND-POSITION: left top; BORDER-TOP: #ccc 1px = solid; DISPLAY: block; PADDING-LEFT: 25px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/icon_mail.gif); = PADDING-BOTTOM: 0px; MARGIN: 12px 0px 0px; PADDING-TOP: 5px; = BACKGROUND-REPEAT: no-repeat } DIV.full_text DIV.header_divide { MARGIN: 12px 0px 0px; HEIGHT: 18px; BACKGROUND-COLOR: #a3a3a3; = TEXT-ALIGN: right } DIV.full_text DIV.header_divide H3 { PADDING-RIGHT: 6px; PADDING-LEFT: 6px; BACKGROUND: #a3a3a3; = PADDING-BOTTOM: 2px; PADDING-TOP: 2px; TEXT-ALIGN: left } DIV.full_text DIV.header_divide H3.select_enabled { FLOAT: left } DIV.full_text DIV.IE7Hack H3.select_enabled { FLOAT: none! important } DIV.full_text DIV.IE7Hack SELECT { FLOAT: right } P { MARGIN: 12px 0px 0px } H1 { MARGIN: 12px 0px 0px } H4 { MARGIN: 12px 0px 0px } H5 { MARGIN: 12px 0px 0px } #back_to_top { MARGIN: 12px 0px 0px } DIV.article_begins { MARGIN: 12px 0px 0px } OL.references { MARGIN-TOP: 8px } OL.references LI { MARGIN-BOTTOM: 4px; MARGIN-LEFT: 24px } .premium_backfiles { BACKGROUND-POSITION: left center; PADDING-LEFT: 20px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/iconFullPlusAccess.gif); = BACKGROUND-REPEAT: no-repeat } .fullplus_access { BACKGROUND-POSITION: left center; PADDING-LEFT: 20px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/iconFullPlusAccess.gif); = BACKGROUND-REPEAT: no-repeat } .premium_access { BACKGROUND-POSITION: left center; PADDING-LEFT: 20px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/iconFullAccess.gif); = BACKGROUND-REPEAT: no-repeat } .full_access { BACKGROUND-POSITION: left center; PADDING-LEFT: 20px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/iconFullAccess.gif); = BACKGROUND-REPEAT: no-repeat } .partial_access { BACKGROUND-POSITION: left center; PADDING-LEFT: 20px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/iconPartAccess.gif); = BACKGROUND-REPEAT: no-repeat } 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BACKGROUND-REPEAT: = no-repeat } .online_open { BACKGROUND-POSITION: left center; PADDING-LEFT: 5px; MIN-HEIGHT: 14px; = BACKGROUND-REPEAT: no-repeat } UL.selection_menu { PADDING-RIGHT: 2px; BACKGROUND-POSITION: left center; BORDER-TOP: #fff = 2px solid; PADDING-LEFT: 22px; PADDING-BOTTOM: 3px; PADDING-TOP: 1px; = BACKGROUND-REPEAT: no-repeat; BACKGROUND-COLOR: #ededed } UL.selection_top { BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/icon_selection_menu_top.gif) } UL.selection_bottom { BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/icon_selection_menu_bot.gif) } UL.selection_menu LI { DISPLAY: inline } UL.selection_menu LI A { Z-INDEX: 4; POSITION: relative } UL#article_authors LI A { Z-INDEX: 4; POSITION: relative } UL.selection_menu LI A:hover { Z-INDEX: 5; BACKGROUND-COLOR: transparent } UL#article_authors LI A:hover { Z-INDEX: 5; BACKGROUND-COLOR: transparent } A.tooltiplink:hover { Z-INDEX: 5; BACKGROUND-COLOR: transparent } A.nameLink:hover { Z-INDEX: 5; BACKGROUND-COLOR: transparent } UL.selection_menu LI A SPAN { DISPLAY: none } UL#article_authors LI A SPAN.tooltip { DISPLAY: none } A.tooltiplink SPAN { DISPLAY: none } A.nameLink SPAN.tooltip { DISPLAY: none } UL.selection_menu LI A:hover SPAN { PADDING-RIGHT: 4px; BACKGROUND-POSITION: left top; DISPLAY: block; = PADDING-LEFT: 4px; LEFT: 0px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/toc_tooltip_bg.gif); = PADDING-BOTTOM: 4px; WIDTH: 189px; PADDING-TOP: 8px; BORDER-BOTTOM: #000 = 1px solid; BACKGROUND-REPEAT: no-repeat; POSITION: absolute; TOP: 18px; = TEXT-DECORATION: none } UL#article_authors LI A:hover SPAN.tooltip { PADDING-RIGHT: 4px; BACKGROUND-POSITION: left top; DISPLAY: block; = PADDING-LEFT: 4px; LEFT: 0px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/toc_tooltip_bg.gif); = PADDING-BOTTOM: 4px; WIDTH: 189px; PADDING-TOP: 8px; BORDER-BOTTOM: #000 = 1px solid; BACKGROUND-REPEAT: no-repeat; POSITION: absolute; TOP: 18px; = TEXT-DECORATION: none } A.nameLink:hover SPAN.tooltip { PADDING-RIGHT: 4px; BACKGROUND-POSITION: left top; DISPLAY: block; = PADDING-LEFT: 4px; LEFT: 0px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/toc_tooltip_bg.gif); = PADDING-BOTTOM: 4px; WIDTH: 189px; PADDING-TOP: 8px; BORDER-BOTTOM: #000 = 1px solid; BACKGROUND-REPEAT: no-repeat; POSITION: absolute; TOP: 18px; = TEXT-DECORATION: none } A:hover SPAN.tooltip .item { MARGIN-TOP: 1em; DISPLAY: block } A:hover SPAN.tooltip .first { MARGIN-TOP: 0px } A#toc_select_all { MARGIN-TOP: 8px; DISPLAY: block; FLOAT: left; WIDTH: 28px; TEXT-ALIGN: = center } DIV.toc_item { MARGIN-LEFT: 30px } DIV.toc_item H3 { PADDING-RIGHT: 6px; MARGIN-TOP: 15px; PADDING-LEFT: 3px; = PADDING-BOTTOM: 2px; PADDING-TOP: 2px; BACKGROUND-COLOR: #a3a3a3 } DIV.toc_item H4 { PADDING-RIGHT: 6px; MARGIN-TOP: 2px; PADDING-LEFT: 3px; PADDING-BOTTOM: = 2px; PADDING-TOP: 2px; BACKGROUND-COLOR: #ededed } DIV.toc_item H5 { MARGIN-TOP: 4px } DIV.toc_item .select_title { CLEAR: both; MARGIN-LEFT: -30px } DIV.toc_item .select_title SPAN.doi_checkbox { DISPLAY: block; FLOAT: left; WIDTH: 30px; TEXT-ALIGN: center } DIV.toc_item .select_title H5 { PADDING-LEFT: 30px } DIV.toc_item P { MARGIN-TOP: 6px } DIV.toc_item P.toc_author { MARGIN-TOP: 4px } DIV.toc_item UL.item_options { MARGIN-TOP: 6px; MARGIN-BOTTOM: 10px } DIV.toc_item UL.bordered { PADDING-BOTTOM: 14px; BORDER-BOTTOM: #ccc 1px solid } DIV.toc_item UL.item_options LI { DISPLAY: inline } #back_to_top { PADDING-RIGHT: 20px; BACKGROUND-POSITION: right center; DISPLAY: block; = PADDING-LEFT: 5px; BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/top_link_arrow.gif); = PADDING-BOTTOM: 2px; PADDING-TOP: 1px; BACKGROUND-REPEAT: no-repeat; = BACKGROUND-COLOR: #d21c1b; TEXT-ALIGN: right } .synergy_house H2 { PADDING-RIGHT: 6px; PADDING-LEFT: 6px; PADDING-BOTTOM: 2px; MARGIN: 7px = 0px 0px; PADDING-TOP: 2px; BACKGROUND-COLOR: #d21c1b } DIV.subscription_warning { PADDING-RIGHT: 6px; BORDER-TOP: #fff 1px solid; PADDING-LEFT: 3px; = PADDING-BOTTOM: 2px; PADDING-TOP: 2px; BACKGROUND-COLOR: #fae8e8 } .synergy_house TABLE { WIDTH: 100% } .synergy_house TABLE TH { PADDING-RIGHT: 2px; PADDING-LEFT: 2px; PADDING-BOTTOM: 7px; = PADDING-TOP: 7px; BORDER-BOTTOM: #ccc 1px solid; TEXT-ALIGN: left } .synergy_house TABLE TD { PADDING-RIGHT: 2px; PADDING-LEFT: 2px; PADDING-BOTTOM: 7px; = PADDING-TOP: 7px; BORDER-BOTTOM: #ccc 1px solid; TEXT-ALIGN: left } .synergy_house TABLE TH.rh { TEXT-ALIGN: right } .synergy_house TABLE TD.rh { TEXT-ALIGN: right } .synergy_house TABLE TH.remove { PADDING-RIGHT: 10px; BACKGROUND-POSITION: right center; = BACKGROUND-IMAGE: = url(/templates/jsp/_synergy.2/images/layout/icon_dn_arrow.gif); = BACKGROUND-REPEAT: no-repeat } .synergy_house UL.links_list { MARGIN: 4px 0px 8px; LIST-STYLE-TYPE: none } .synergy_house UL.links_list LI { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 3px; = PADDING-TOP: 2px } FORM#institution_select { PADDING-RIGHT: 3px; BORDER-TOP: #fff 5px solid; PADDING-LEFT: 3px; = PADDING-BOTTOM: 1px; PADDING-TOP: 1px; BACKGROUND-COLOR: #e1e1e1 } UL.advice { MARGIN-TOP: 8px; LIST-STYLE-TYPE: none } UL.advice LI { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 4px; = PADDING-TOP: 2px } OL.advice { MARGIN-TOP: 8px } OL.advice LI { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 4px; = MARGIN-LEFT: 25px; PADDING-TOP: 2px } UL.bulleted { MARGIN-LEFT: 17px; LIST-STYLE-TYPE: disc } DIV.display_controls { PADDING-RIGHT: 6px; BORDER-TOP: #fff 2px solid; PADDING-LEFT: 6px; = PADDING-BOTTOM: 4px; PADDING-TOP: 2px; BACKGROUND-COLOR: #fae8e8 } DIV.display_controls UL LI { DISPLAY: inline } DIV.display_controls A.rh { FLOAT: right } DIV.search_pagination { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 3px; = PADDING-TOP: 10px; TEXT-ALIGN: right } DIV.search_pagination H1 { FLOAT: left; MARGIN: 0px } DIV.search_pagination INPUT.go_btn { FLOAT: left; MARGIN-RIGHT: 3px } FORM.main_form H2 { MARGIN-BOTTOM: 10px } FORM.main_form H4 { MARGIN-BOTTOM: 4px } FORM.main_form P { MARGIN-TOP: 0px; MARGIN-BOTTOM: 4px } FORM.main_form DIV.row { CLEAR: both; PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: = 8px; PADDING-TOP: 0px } FORM.main_form LABEL { DISPLAY: block; FLOAT: left; WIDTH: 15em; PADDING-TOP: 2px; TEXT-ALIGN: = left } FORM.main_form DIV.form_title { DISPLAY: block; FLOAT: left; WIDTH: 15em; PADDING-TOP: 2px; TEXT-ALIGN: = left } FORM.main_form LABEL.inline { DISPLAY: inline; FLOAT: none; WIDTH: auto } FORM.main_form INPUT.text_field { WIDTH: 21.4em } FORM.main_form SELECT { WIDTH: 32.1em } FORM.main_form SELECT.exempt { WIDTH: auto } FORM.main_form SELECT.searchfield { FONT-WEIGHT: bold; WIDTH: 13em } FORM.main_form SELECT.searchop { WIDTH: 6em } FORM.main_form DIV.search_rh_box SELECT.exempt { WIDTH: 55px } FORM.main_form INPUT.go_btn { MARGIN-TOP: 12px } FORM.main_form DIV.inc_help_text { FLOAT: left; WIDTH: 29em } FORM.main_form DIV.inc_help_text P { 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Journal of Neurochemistry

MINI-REVIEW

A role for glutamate in growth and invasion = of primary=20 brain tumors

Abstract

Gliomas

Physical constraints to tumor growth

Glioma cells release glutamate and kill peritumoral neurons = by an=20 excitoxic mechanism

Glutamate release is mediated by the = cystine=E2=80=93glutamate antiporter=20 system Xc

Glutamate release is an obligatory byproduct of GSH=20 synthesis

Therapeutic targeting of system Xc-mediated = glutamate=20 release to contain tumor growth

Glutamate stimulates glioma metastasis

Epilogue

Acknowledgements

References

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Glutamate release is mediated by the = cystine=E2=80=93glutamate antiporter=20 system X^c

Therapeutic targeting of system X^c-mediated = glutamate=20 release to contain tumor growth