VEGF up-regulation by G93A superoxide dismutase and the role of malate-aspartate shuttle inhibition

Neurobiology of Disease

Volumn 37, Issue 3, 2010, Pages 673-681

  Mali, Yael ^a   Zisapel, Nava ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

ALS; Amyotrophic Lateral Sclerosis; HIF; Hypoxia; Malate aspartate shuttle; SOD1; VEGF

Indexed keywords

ASPARTIC ACID; DOXYCYCLINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MALIC ACID; SUPEROXIDE DISMUTASE; VASCULOTROPIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANAEROBIC METABOLISM; ANIMAL CELL; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; HYPOXIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

AMINOOXYACETIC ACID; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ASPARTIC ACID; CARBON DIOXIDE; CELL LINE, TRANSFORMED; ENZYME INHIBITORS; GREEN FLUORESCENT PROTEINS; HYBRIDOMAS; HYDROGEN PEROXIDE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALATES; METABOLIC NETWORKS AND PATHWAYS; MICE; RECOMBINANT FUSION PROTEINS; SUPEROXIDE DISMUTASE; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 75949112743     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.12.005     Document Type: Article

References (40)

1. Azzouz M., Ralph G.S., Storkebaum E., Walmsley L.E., Mitrophanous K.A., Kingsman S.M., Carmeliet P., and Mazarakis N.D. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429 (2004) 413-417
2. Beal M.F. Mitochondria and the pathogenesis of ALS. Brain 123 (2000) 1291-1292
3. Bendotti C., and Carri M.T. Lessons from models of SOD1-linked familial ALS. Trends Mol. Med. 10 (2004) 393-400
4. Berra E., Benizri E., Ginouvès A., Volmat V., Roux D., and Pouysségur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J. 22 (2003) 4082-4090
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt. Biochem. 72 (1976) 248-254
6. Brockington A., Wharton S.B., Fernando M., Gelsthorpe C.H., Baxter L., Ince P.G., Lewis C.E., and Shaw P.J. Expression of vascular endothelial growth factor and its receptors in the central nervous system in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 65 (2006) 26-36
7. 2+ concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Lett. 414 (1997) 365-368
8. Cashman N.R., Durham H.D., Blusztajn J.K., Oda K., Tabira T., Shaw I.T., Dahrouge S., and Antel J.P. Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 194 (1992) 209-221
9. Chen W., Saeed M., Mao H., Siddique N., Dellefave L., Hung W.Y., Deng H.X., Sufit R.L., Heller S.L., Haines J.L., Pericak-Vance M., and Siddique T. Lack of association of VEGF promoter polymorphisms with sporadic ALS. Neurology 67 (2006) 508-510
10. Denizot F., and Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89 (1986) 271-277
11. Garbuzova-Davis S., Saporta S., Haller E., Kolomey I., Bennett S.P., Potter H., and Sanberg P.R. Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS ONE 2 (2007) e1205
12. Greenway M.J., Andersen P.M., Russ C., Ennis S., Cashman S., Donaghy C., Patterson V., Swingler R., Kieran D., Prehn J., Morrison K.E., Green A., Acharya K.R., Brown Jr. R.H., and Hardiman O. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat. Genet. 38 (2006) 411-413
13. Ilzecka J. Cerebrospinal fluid vascular endothelial growth factor in patients with amyotrophic lateral sclerosis. Clin. Neurol. Neurosurg. 106 (2004) 289-293
14. Kruman I.I., Pedersen W.A., Springer J.E., and Mattson M.P. ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp. Neurol. 160 (1999) 28-39
15. Lambrechts D., Storkebaum E., Morimoto M., Del-Favero J., Desmet F., Marklund S.L., Wyns S., Thijs V., Andersson J., van Marion I., Al-Chalabi A., Bornes S., Musson R., Hansen V., Beckman L., Adolfsson R., Pall H.S., Prats H., Vermeire S., Rutgeerts P., Katayama S., Awata T., Leigh N., Lang-Lazdunski L., Dewerchin M., Shaw C., Moons L., Vlietinck R., Morrison K.E., Robberecht W., Van Broeckhoven C., Collen D., Andersen P.M., and Carmeliet P. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet. 34 (2003) 383-394
16. Lambrechts D., Poesen K., Fernández-Santiago R., Al-Chalabi A., Del Bo R., Van Vught P.W., Khan S., Marklund S., Brockington A., Van Marion I., Anneser J., Shaw C., Ludolph A., Leigh N., Comi G., Gasser T., Shaw P.J., Morrison K., Andersen P., Van den Berg L.H., Thijs V., Siddique T., Robberecht W., and Carmeliet P. Meta-analysis of VEGF variations in ALS: increased susceptibility in male carriers of the -2578AA genotype. J. Med. Genet. (2008) Jul 17. [Epub ahead of print]
17. Li B., Xu W., Luo C., Gozal D., and Liu R. VEGF-induced activation of the PI3-K/Akt pathway reduces mutant SOD1-mediated motor neuron cell death. Brain Res. Mol. Brain Res. 111 (2003) 155-164
18. Lu L., Zheng L., Viera L., Suswam E., Li Y., Li X., Estévez A.G., and King PH. Mutant Cu/Zn-superoxide dismutase associated with amyotrophic lateral sclerosis destabilizes vascular endothelial growth factor mRNA and down-regulates its expression. J. Neurosci. 27 30 (2007 Jul 25) 7929-7938
19. Mali Y., and Zisapel N. Gain of interaction of ALS-linked G93A superoxide dismutase with cytosolic malate dehydrogenase. Neurobiol. Dis. 32 (2008) 133-141
20. Mali Y., and Zisapel N. A novel decoy that interrupts G93A-superoxide dismutase gain of interaction with malate dehydrogenase improves survival in an amyotrophic lateral sclerosis cell model. J. Med. Chem. 52 (2009) 5442-5448
21. McCloskey D.P., Hintz T.M., and Scharfman H.E. Modulation of vascular endothelial growth factor (VEGF) expression in motor neurons and its electrophysiological effects. Brain Res. Bull. 76 (2008) 36-44
22. Menzies F.M., Cookson M.R., Taylor R.W., Turnbull D.M., Chrzanowska-Lightowlers Z.M., Dong L., Figlewicz D.A., and Shaw PJ. Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 125 (2002) 1522-1533
23. Mitchell M., Cashman K.S., et al. Disruption of mitochondrial malate-aspartate shuttle activity in mouse blastocysts impairs viability and fetal growth. Biol. Reprod. 80 2 (2009) 295-301
24. Murakami T., Ilieva H., Shiote M., Nagata T., Nagano I., Shoji M., and Abe K. Hypoxic induction of vascular endothelial growth factor is selectively impaired in mice carrying the mutant SOD1 gene. Brain Res. 989 (2003) 231-237
25. Novelli M., Fabregat M.E., et al. Metabolic and functional studies on isolated islets in a new rat model of type 2 diabetes. Mol. Cell. Endocrinol. 175 1-2 (2001) 57-66
26. Oosthuyse B., Moons L., Storkebaum E., Beck H., Nuyens D., Brusselmans K., Van Dorpe J., Hellings P., Gorselink M., Heymans S., Theilmeier G., Dewerchin M., Laudenbach V., Vermylen P., Raat H., Acker T., Vleminckx V., Van Den Bosch L., Cashman N., Fujisawa H., Drost M.R., Sciot R., Bruyninckx F., Hicklin D.J., Ince C., Gressens P., Lupu F., Plate K.H., Robberecht W., Herbert J.M., Collen D., and Carmeliet P. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 28 (2001) 131-138
27. Pan Y., Mansfield K.D., Bertozzi C.C., Rudenko V., Chan D.A., Giaccia A.J., and Simon M.C. Multiple factors affecting cellular redox status and energy metabolism modulate HIF prolyl hydroxylase activity in vivo and in vitro. Mol. Cell. Biol. 27 (2007) 912-925
28. Qutub A.A., and Popel A.S. Reactive oxygen species regulate hypoxia-inducible factor 1alpha differentially in cancer and ischemia. Mol. Cell. Biol. 28 (2008) 5106-5119
29. 2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res. Dev. Brain Res. 143 (2003) 33-46
30. Rizzardini M., Mangolini A., Lupi M., Ubezio P., Bendotti C., and Cantoni L. Low levels of ALS-linked Cu/Zn superoxide dismutase increase the production of reactive oxygen species and cause mitochondrial damage and death in motor neuron-like cells. J. Neurol. Sci. 232 (2005) 95-103
31. Salnikow K., Donald S.P., Bruick R.K., Zhitkovich A., Phang J.M., and Kasprzak K.S. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J. Biol. Chem. 279 (2004) 40337-40344
32. Shweiki D., Itin A., Soffer D., and Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359 (1992) 843-845
33. Storkebaum E., Lambrechts D., Dewerchin M., Moreno-Murciano M.P., Appelmans S., Oh H., Van Damme P., Rutten B., Man W.Y., De Mol M., Wyns S., Manka D., Vermeulen K., Van Den Bosch L., Mertens N., Schmitz C., Robberecht W., Conway E.M., Collen D., Moons L., and Carmeliet P. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat. Neurosci. 8 (2005) 85-92
34. Suzuki M., Watanabe T., Mikami H., Nomura M., Yamazaki T., Irie T., Yasui H.I., and Ono S. Immunohistochemical studies of vascular endothelial growth factor in skin of patients with amyotrophic lateral sclerosis. J. Neurol. Sci. (2009) Jul 8. [Epub ahead of print]
35. Tolosa L., Mir M., Asensio V.J., Olmos G., and Llado J. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J. Neurochem. 105 (2008) 1080-1090
36. Wang Y., Mao X.O., Xie L., Banwait S., Marti H.H., Greenberg D.A., and Jin K. Vascular endothelial growth factor overexpression delays neurodegeneration and prolongs survival in amyotrophic lateral sclerosis mice. J. Neurosci. 27 (2007) 304-307
37. Xie Y., Weydt P., Howland D.S., Kliot M., and Moller T. Inflammatory mediators and growth factors in the spinal cord of G93A SOD1 rats. Neuroreport 15 (2004) 2513-2516
38. Yoo M.H., Hyun H.J., Koh J.Y., and Yoon Y.H. Riluzole inhibits VEGF-induced endothelial cell proliferation in vitro and hyperoxia-induced abnormal vessel formation in vivo. Invest. Ophthalmol. Vis. Sci. 46 (2005) 4780-4787
39. Zheng C., Nennesmo I., Fadeel B., and Henter J.I. Vascular endothelial growth factor prolongs survival in a transgenic mouse model of ALS. Ann. Neurol. 56 (2004) 564-567
40. Zhong Z., Deane R., Ali Z., Parisi M., Shapovalov Y., O'Banion M.K., Stojanovic K., Sagare A., Boillee S., Cleveland D.W., and Zlokovic B.V. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat. Neurosci. 11 (2008) 420-422