Erratum: VEGF ligands and receptors: Implications in neurodevelopment and neurodegeneration (Cellular and Molecular Life Sciences DOI: 10.1007/s00018-013-1283-7);VEGF ligands and receptors: Implications in neurodevelopment and neurodegeneration

Cellular and Molecular Life Sciences

Volumn 70, Issue 10, 2013, Pages 1763-1778

  Carmeliet, Peter ^a,b   De Almodovar, Carmen Ruiz ^c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Neurodegeneration; Neurodevelopment; Vascular endothelial growth factor; VEGF; VEGF ligands; VEGF receptors

Indexed keywords

AMYLOID BETA PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVOVIRUS VECTOR; PLACENTAL GROWTH FACTOR; SUPEROXIDE DISMUTASE; VASCULOTROPIN; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANGIOGENESIS; BLOOD BRAIN BARRIER; CELL MIGRATION; DEGENERATIVE DISEASE; DENDRITE; GLIA CELL; GRANULE CELL; HUMAN; MOTONEURON; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PARKINSON DISEASE; PURKINJE CELL; RETINA GANGLION CELL; REVIEW; SIGNAL TRANSDUCTION; SPINAL GANGLION; SPINOCEREBELLAR DEGENERATION; SUBVENTRICULAR ZONE;

EID: 84876888723     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1332-2     Document Type: Erratum

References (96)

1. Koch S, Tugues S, Li X, Gualandi L, Claesson-Welsh L (2011) Signal transduction by vascular endothelial growth factor receptors. Biochem J 437(2):169-183. doi: 10.1042/BJ20110301
2. Holmes DI, Zachary I (2005) The vascular endothelial growth factor (VEGF) family: angiogenic factors in health and disease. Genome Biol 6(2):209. doi: 10.1186/gb-2005-6-2-209
3. Ruiz de Almodovar C, Lambrechts D, Mazzone M, Carmeliet P (2009) Role and therapeutic potential of VEGF in the nervous system. Physiol Rev 89(2):607-648
4. Mackenzie F, Ruhrberg C (2012) Diverse roles for VEGF-A in the nervous system. Development 139(8):1371-1380. doi: 10.1242/dev.072348
5. Rosenstein JM, Krum JM, Ruhrberg C (2010) VEGF in the nervous system. Organogenesis 6(2):107-114
6. Louissaint A Jr, Rao S, Leventhal C, Goldman SA (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34(6):945-960
7. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci U S A 99(18):11946-11950. doi: 10.1073/pnas.182296499
8. Sun Y, Jin K, Xie L, Childs J, Mao XO, Logvinova A, Greenberg DA (2003) VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Investig 111(12):1843-1851. doi: 10.1172/JCI17977
9. Wang Y, Jin K, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA (2007) VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J Neurosci Res 85(4):740-747. doi: 10.1002/jnr.21169
10. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36(8):827-835. doi: 10.1038/ng1395
11. Warner-Schmidt JL, Duman RS (2008) VEGF as a potential target for therapeutic intervention in depression. Curr Opin Pharmacol 8(1):14-19. doi: 10.1016/j.coph.2007.10.013
12. Jung KH, Chu K, Lee ST, Kim SJ, Sinn DI, Kim SU, Kim M, Roh JK (2006) Granulocyte colony-stimulating factor stimulates neurogenesis via vascular endothelial growth factor with STAT activation. Brain Res 1073-1074:190-201. doi: 10.1016/j.brainres.2005.12.037
13. Wada T, Haigh JJ, Ema M, Hitoshi S, Chaddah R, Rossant J, Nagy A, van der Kooy D (2006) Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival. J Neurosci 26(25):6803-6812. doi: 10.1523/JNEUROSCI.0526-06.2006
14. Xiao Z, Kong Y, Yang S, Li M, Wen J, Li L (2007) Upregulation of Flk-1 by bFGF via the ERK pathway is essential for VEGF-mediated promotion of neural stem cell proliferation. Cell Res 17(1):73-79. doi: 10.1038/sj.cr.7310126
15. Sun Y, Jin K, Childs JT, Xie L, Mao XO, Greenberg DA (2006) Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: evidence from knockout mice and growth factor administration. Dev Biol 289(2):329-335. doi: 10.1016/j.ydbio.2005.10.016
16. Calvo CF, Fontaine RH, Soueid J, Tammela T, Makinen T, Alfaro-Cervello C, Bonnaud F, Miguez A, Benhaim L, Xu Y, Barallobre MJ, Moutkine I, Lyytikka J, Tatlisumak T, Pytowski B, Zalc B, Richardson W, Kessaris N, Garcia-Verdugo JM, Alitalo K, Eichmann A, Thomas JL (2011) Vascular endothelial growth factor receptor 3 directly regulates murine neurogenesis. Genes Dev 25(8):831-844. doi: 10.1101/gad.615311
17. Le Bras B, Barallobre MJ, Homman-Ludiye J, Ny A, Wyns S, Tammela T, Haiko P, Karkkainen MJ, Yuan L, Muriel MP, Chatzopoulou E, Breant C, Zalc B, Carmeliet P, Alitalo K, Eichmann A, Thomas JL (2006) VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat Neurosci 9(3):340-348. doi: 10.1038/nn1646
18. Hayakawa K, Pham LD, Som AT, Lee BJ, Guo S, Lo EH, Arai K (2011) Vascular endothelial growth factor regulates the migration of oligodendrocyte precursor cells. J Neurosci 31(29):10666-10670. doi: 10.1523/JNEUROSCI.1944-11.2011
19. Van Den Bosch L, Storkebaum E, Vleminckx V, Moons L, Vanopdenbosch L, Scheveneels W, Carmeliet P, Robberecht W (2004) Effects of vascular endothelial growth factor (VEGF) on motor neuron degeneration. Neurobiol Dis 17(1):21-28. doi: 10.1016/j.nbd.2004.06.004
20. Tolosa L, Mir M, Asensio VJ, Olmos G, Llado J (2008) Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J Neurochem 105(4):1080-1090. doi: 10.1111/j.1471-4159.2007.05206.x
21. Qiu MH, Zhang R, Sun FY (2003) Enhancement of ischemia-induced tyrosine phosphorylation of Kv1.2 by vascular endothelial growth factor via activation of phosphatidylinositol 3-kinase. J Neurochem 87(6):1509-1517.
22. Ma YY, Li KY, Wang JJ, Huang YL, Huang Y, Sun FY (2009) Vascular endothelial growth factor acutely reduces calcium influx via inhibition of the Ca2+ channels in rat hippocampal neurons. J Neurosci Res 87(2):393-402. doi: 10.1002/jnr.21859
23. Cvetanovic M, Patel JM, Marti HH, Kini AR, Opal P (2011) Vascular endothelial growth factor ameliorates the ataxic phenotype in a mouse model of spinocerebellar ataxia type 1. Nat Med 17(11):1445-1447. doi: 10.1038/nm.2494
24. Kilic U, Kilic E, Jarve A, Guo Z, Spudich A, Bieber K, Barzena U, Bassetti CL, Marti HH, Hermann DM (2006) Human vascular endothelial growth factor protects axotomized retinal ganglion cells in vivo by activating ERK-1/2 and Akt pathways. J Neurosci 26(48):12439-12446. doi: 10.1523/JNEUROSCI.0434-06. 2006
25. Poesen K, Lambrechts D, Van Damme P, Dhondt J, Bender F, Frank N, Bogaert E, Claes B, Heylen L, Verheyen A, Raes K, Tjwa M, Eriksson U, Shibuya M, Nuydens R, Van Den Bosch L, Meert T, D'Hooge R, Sendtner M, Robberecht W, Carmeliet P (2008) Novel role for vascular endothelial growth factor (VEGF) receptor-1 and its ligand VEGF-B in motor neuron degeneration. J Neurosci 28(42):10451-10459. doi: 10.1523/JNEUROSCI.1092-08.2008
26. Li Y, Zhang F, Nagai N, Tang Z, Zhang S, Scotney P, Lennartsson J, Zhu C, Qu Y, Fang C, Hua J, Matsuo O, Fong GH, Ding H, Cao Y, Becker KG, Nash A, Heldin CH, Li X (2008) VEGF-B inhibits apoptosis via VEGFR-1-mediated suppression of the expression of BH3-only protein genes in mice and rats. J Clin Investig 118(3):913-923. doi: 10.1172/JCI33673
27. Schwarz Q, Gu C, Fujisawa H, Sabelko K, Gertsenstein M, Nagy A, Taniguchi M, Kolodkin AL, Ginty DD, Shima DT, Ruhrberg C (2004) Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes Dev 18(22):2822-2834
28. Schwarz Q, Waimey KE, Golding M, Takamatsu H, Kumanogoh A, Fujisawa H, Cheng HJ, Ruhrberg C (2008) Plexin A3 and plexin A4 convey semaphorin signals during facial nerve development. Dev Biol 324(1):1-9
29. Ruiz de Almodovar C, Coulon C, Salin PA, Knevels E, Chounlamountri N, Poesen K, Hermans K, Lambrechts D, Van Geyte K, Dhondt J, Dresselaers T, Renaud J, Aragones J, Zacchigna S, Geudens I, Gall D, Stroobants S, Mutin M, Dassonville K, Storkebaum E, Jordan BF, Eriksson U, Moons L, D'Hooge R, Haigh JJ, Belin MF, Schiffmann S, Van Hecke P, Gallez B, Vinckier S, Chedotal A, Honnorat J, Thomasset N, Carmeliet P, Meissirel C (2010) Matrix-binding vascular endothelial growth factor (VEGF) isoforms guide granule cell migration in the cerebellum via VEGF receptor Flk1. J Neurosci 30(45):15052-15066. doi: 10.1523/JNEUROSCI.0477-10.2010
30. Meissirel C, Ruiz de Almodovar C, Knevels E, Coulon C, Chounlamountri N, Segura I, de Rossi P, Vinckier S, Anthonis K, Deleglise B, de Mol M, Ali C, Dassonville K, Loyens E, Honnorat J, Michotte Y, Rogemond V, Smolders I, Voets T, Vivien D, Vanden Berghe P, Van Den Bosch L, Robberecht W, Chedotal A, Oliviero S, Dewerchin M, Schmucker D, Thomasset N, Salin P, Carmeliet P (2011) VEGF modulates NMDA receptors activity in cerebellar granule cells through Src-family kinases before synapse formation. Proc Natl Acad Sci USA 108(33):13782-13787. doi: 10.1073/pnas.1100341108
31. Komuro H, Rakic P (1993) Modulation of neuronal migration by NMDA receptors. Science 260(5104):95-97
32. Mancini JD, Atchison WD (2007) The NR2B subunit in NMDA receptors is functionally important during cerebellar granule cell migration. Neurosci Lett 429(2-3):87-90
33. Balenci L, Saoudi Y, Grunwald D, Deloulme JC, Bouron A, Bernards A, Baudier J (2007) IQGAP1 regulates adult neural progenitors in vivo and vascular endothelial growth factor-triggered neural progenitor migration in vitro. J Neurosci 27(17):4716-4724. doi: 10.1523/JNEUROSCI.0830-07.2007
34. Wittko IM, Schanzer A, Kuzmichev A, Schneider FT, Shibuya M, Raab S, Plate KH (2009) VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J Neurosci 29(27):8704-8714. doi: 10.1523/JNEUROSCI.5527-08.2009
35. Zhang H, Vutskits L, Pepper MS, Kiss JZ (2003) VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163(6):1375-1384. doi: 10.1083/jcb.200308040
36. Learte AR, Forero MG, Hidalgo A (2008) Gliatrophic and gliatropic roles of PVF/PVR signaling during axon guidance. Glia 56(2):164-176. doi: 10.1002/glia.20601
37. Hayakawa K, Seo JH, Pham LD, Miyamoto N, Som AT, Guo S, Kim KW, Lo EH, Arai K (2012) Cerebral endothelial derived vascular endothelial growth factor promotes the migration but not the proliferation of oligodendrocyte precursor cells in vitro. Neurosci Lett 513(1):42-46. doi: 10.1016/j.neulet.2012.02.004
38. Ryu JK, Cho T, Choi HB, Wang YT, McLarnon JG (2009) Microglial VEGF receptor response is an integral chemotactic component in Alzheimer's disease pathology. J Neurosci 29(1):3-13. doi: 10.1523/JNEUROSCI.2888-08.2009
39. Pitzer MR, Sortwell CE, Daley BF, McGuire SO, Marchionini D, Fleming M, Collier TJ (2003) Angiogenic and neurotrophic effects of vascular endothelial growth factor (VEGF165): studies of grafted and cultured embryonic ventral mesencephalic cells. Exp Neurol 182(2):435-445
40. Rosenstein JM, Mani N, Khaibullina A, Krum JM (2003) Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci 23(35):11036-11044 23/35/11036
41. Jin K, Mao XO, Greenberg DA (2006) Vascular endothelial growth factor stimulates neurite outgrowth from cerebral cortical neurons via Rho kinase signaling. J Neurobiol 66(3):236-242. doi: 10.1002/neu.20215
42. Bocker-Meffert S, Rosenstiel P, Rohl C, Warneke N, Held-Feindt J, Sievers J, Lucius R (2002) Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats. Invest Ophthalmol Vis Sci 43(6):2021-2026
43. Olbrich L, Foehring D, Happel P, Brand-Saberi B, Theiss C (2012) Fast rearrangement of the neuronal growth cone's actin cytoskeleton following VEGF stimulation. Histochem Cell Biol. doi: 10.1007/s00418-012-1036-y
44. Bellon A, Luchino J, Haigh K, Rougon G, Haigh J, Chauvet S, Mann F (2010) VEGFR2 (KDR/Flk1) signaling mediates axon growth in response to semaphorin 3E in the developing brain. Neuron 66(2):205-219. doi: 10.1016/j.neuron.2010.04.006
45. Nawabi H, Castellani V (2011) Axonal commissures in the central nervous system: how to cross the midline? Cell Mol Life Sci 68(15):2539-2553. doi: 10.1007/s00018-011-0691-9
46. Ruiz de Almodovar C, Fabre PJ, Knevels E, Coulon C, Segura I, Haddick PC, Aerts L, Delattin N, Strasser G, Oh WJ, Lange C, Vinckier S, Haigh J, Fouquet C, Gu C, Alitalo K, Castellani V, Tessier-Lavigne M, Chedotal A, Charron F, Carmeliet P (2011) VEGF mediates commissural axon chemoattraction through its receptor Flk1. Neuron 70(5):966-978. doi: 10.1016/j.neuron.2011.04.014
47. Erskine L, Reijntjes S, Pratt T, Denti L, Schwarz Q, Vieira JM, Alakakone B, Shewan D, Ruhrberg C (2011) VEGF signaling through neuropilin 1 guides commissural axon crossing at the optic chiasm. Neuron 70(5):951-965. doi: 10.1016/j.neuron.2011.02.052
48. Khaibullina AA, Rosenstein JM, Krum JM (2004) Vascular endothelial growth factor promotes neurite maturation in primary CNS neuronal cultures. Brain Res Dev Brain Res 148(1):59-68
49. Huang YF, Yang CH, Huang CC, Tai MH, Hsu KS (2010) Pharmacological and genetic accumulation of hypoxia-inducible factor-1alpha enhances excitatory synaptic transmission in hippocampal neurons through the production of vascular endothelial growth factor. J Neurosci 30(17):6080-6093. doi: 10.1523/JNEUROSCI.5493-09.2010
50. Kim BW, Choi M, Kim YS, Park H, Lee HR, Yun CO, Kim EJ, Choi JS, Kim S, Rhim H, Kaang BK, Son H (2008) Vascular endothelial growth factor (VEGF) signaling regulates hippocampal neurons by elevation of intracellular calcium and activation of calcium/calmodulin protein kinase II and mammalian target of rapamycin. Cell Signal 20(4):714-725
51. Huang YF, Yang CH, Huang CC, Hsu KS (2012) Vascular endothelial growth factor-dependent spinogenesis underlies antidepressant-like effects of enriched environment. J Biol Chem 287(49):40938-40955. doi: 10.1074/jbc.M112.392076
52. Licht T, Eavri R, Goshen I, Shlomai Y, Mizrahi A, Keshet E (2010) VEGF is required for dendritogenesis of newly born olfactory bulb interneurons. Development 137(2):261-271. doi: 10.1242/dev.039636
53. Licht T, Goshen I, Avital A, Kreisel T, Zubedat S, Eavri R, Segal M, Yirmiya R, Keshet E (2011) Reversible modulations of neuronal plasticity by VEGF. Proc Natl Acad Sci U S A 108(12):5081-5086. doi: 10.1073/pnas.1007640108
54. Mauceri D, Freitag HE, Oliveira AM, Bengtson CP, Bading H (2011) Nuclear calcium-VEGFD signaling controls maintenance of dendrite arborization necessary for memory formation. Neuron 71(1):117-130. doi: 10.1016/j.neuron.2011.04.022
55. Sondell M, Kanje M (2001) Postnatal expression of VEGF and its receptor flk-1 in peripheral ganglia. Neuroreport 12(1):105-108
56. Sondell M, Lundborg G, Kanje M (1999) Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci 19(14):5731-5740
57. Sondell M, Sundler F, Kanje M (2000) Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur J Neurosci 12(12):4243-4254
58. Kutcher ME, Klagsbrun M, Mamluk R (2004) VEGF is required for the maintenance of dorsal root ganglia blood vessels but not neurons during development. FASEB J 18(15):1952-1954. doi: 10.1096/fj.04-2320fje
59. Cheng L, Jia H, Lohr M, Bagherzadeh A, Holmes DI, Selwood D, Zachary I (2004) Anti-chemorepulsive effects of vascular endothelial growth factor and placental growth factor-2 in dorsal root ganglion neurons are mediated via neuropilin-1 and cyclooxygenase-derived prostanoid production. J Biol Chem 279(29):30654-30661. doi: 10.1074/jbc.M402488200
60. Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ (2002) Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109(6):693-705
61. Mukouyama YS, Gerber HP, Ferrara N, Gu C, Anderson DJ (2005) Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 132(5):941-952. doi: 10.1242/dev.01675
62. Verheyen A, Peeraer E, Nuydens R, Dhondt J, Poesen K, Pintelon I, Daniels A, Timmermans JP, Meert T, Carmeliet P, Lambrechts D (2012) Systemic anti-vascular endothelial growth factor therapies induce a painful sensory neuropathy. Brain 135(Pt 9):2629-2641. doi: 10.1093/brain/aws145
63. Dhondt J, Peeraer E, Verheyen A, Nuydens R, Buysschaert I, Poesen K, Van Geyte K, Beerens M, Shibuya M, Haigh JJ, Meert T, Carmeliet P, Lambrechts D (2011) Neuronal FLT1 receptor and its selective ligand VEGF-B protect against retrograde degeneration of sensory neurons. FASEB J 25(5):1461-1473. doi: 10.1096/fj.10-170944
64. Orr HT (2011) FTD and ALS: genetic ties that bind. Neuron 72(2):189-190. doi: 10.1016/j.neuron.2011.10.001
65. Storkebaum E, Ruiz de Almodovar C, Meens M, Zacchigna S, Mazzone M, Vanhoutte G, Vinckier S, Miskiewicz K, Poesen K, Lambrechts D, Janssen GM, Fazzi GE, Verstreken P, Haigh J, Schiffers PM, Rohrer H, Van der Linden A, De Mey JG, Carmeliet P (2010) Impaired autonomic regulation of resistance arteries in mice with low vascular endothelial growth factor or upon vascular endothelial growth factor trap delivery. Circulation 122(3):273-281
66. Marko SB, Damon DH (2008) VEGF promotes vascular sympathetic innervation. Am J Physiol Heart Circ Physiol 294(6):H2646-H2652. doi: 10.1152/ajpheart. 00291.2008
67. Long JB, Jay SM, Segal SS, Madri JA (2009) VEGF-A and Semaphorin3A: modulators of vascular sympathetic innervation. Dev Biol 334(1):119-132. doi: 10.1016/j.ydbio.2009.07.023
68. Saygili E, Pekassa M, Rackauskas G, Hommes D, Noor-Ebad F, Gemein C, Zink MD, Schwinger RH, Weis J, Marx N, Schauerte P, Rana OR (2011) Mechanical stretch of sympathetic neurons induces VEGF expression via a NGF and CNTF signaling pathway. Biochem Biophys Res Commun 410(1):62-67. doi: 10.1016/j.bbrc.2011.05.105
69. Calza L, Giardino L, Giuliani A, Aloe L, Levi-Montalcini R (2001) Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. Proc Natl Acad Sci U S A 98(7):4160-4165. doi: 10.1073/pnas.051626998
70. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, Kouri N, Wojtas A, Sengdy P, Hsiung GY, Karydas A, Seeley WW, Josephs KA, Coppola G, Geschwind DH, Wszolek ZK, Feldman H, Knopman DS, Petersen RC, Miller BL, Dickson DW, Boylan KB, Graff-Radford NR, Rademakers R (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72(2):245-256. doi: 10.1016/j.neuron.2011.09.011
71. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, Kalimo H, Paetau A, Abramzon Y, Remes AM, Kaganovich A, Scholz SW, Duckworth J, Ding J, Harmer DW, Hernandez DG, Johnson JO, Mok K, Ryten M, Trabzuni D, Guerreiro RJ, Orrell RW, Neal J, Murray A, Pearson J, Jansen IE, Sondervan D, Seelaar H, Blake D, Young K, Halliwell N, Callister JB, Toulson G, Richardson A, Gerhard A, Snowden J, Mann D, Neary D, Nalls MA, Peuralinna T, Jansson L, Isoviita VM, Kaivorinne AL, Holtta-Vuori M, Ikonen E, Sulkava R, Benatar M, Wuu J, Chio A, Restagno G, Borghero G, Sabatelli M, Heckerman D, Rogaeva E, Zinman L, Rothstein JD, Sendtner M, Drepper C, Eichler EE, Alkan C, Abdullaev Z, Pack SD, Dutra A, Pak E, Hardy J, Singleton A, Williams NM, Heutink P, Pickering-Brown S, Morris HR, Tienari PJ, Traynor BJ (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72(2):257-268. doi: 10.1016/j.neuron.2011.09.010
72. 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 MR, Sciot R, Bruyninckx F, Hicklin DJ, Ince C, Gressens P, Lupu F, Plate KH, Robberecht W, Herbert JM, Collen D, Carmeliet P (2001) Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet 28(2):131-138
73. Wang Y, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA, Jin K (2007) Vascular endothelial growth factor overexpression delays neurodegeneration and prolongs survival in amyotrophic lateral sclerosis mice. J Neurosci 27(2):304-307. doi: 10.1523/JNEUROSCI.4433-06.2007
74. Storkebaum E, Lambrechts D, Dewerchin M, Moreno-Murciano MP, Appelmans S, Oh H, Van Damme P, Rutten B, Man WY, De Mol M, Wyns S, Manka D, Vermeulen K, Van Den Bosch L, Mertens N, Schmitz C, Robberecht W, Conway EM, Collen D, Moons L, Carmeliet P (2005) Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 8(1):85-92. doi: 10.1038/nn1360
75. Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND (2004) VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429(6990):413-417. doi: 10.1038/nature02544
76. Lambrechts D, Poesen K, Fernandez-Santiago R, Al-Chalabi A, Del Bo R, Van Vught PW, Khan S, Marklund SL, Brockington A, van Marion I, Anneser J, Shaw C, Ludolph AC, Leigh NP, Comi GP, Gasser T, Shaw PJ, Morrison KE, Andersen PM, Van den Berg LH, Thijs V, Siddique T, Robberecht W, Carmeliet P (2009) Meta-analysis of vascular endothelial growth factor variations in amyotrophic lateral sclerosis: increased susceptibility in male carriers of the -2578AA genotype. J Med Genet 46(12):840-846. doi: 10.1136/jmg.2008.058222
77. Lu L, Zheng L, Viera L, Suswam E, Li Y, Li X, Estevez AG, King PH (2007) Mutant Cu/Zn-superoxide dismutase associated with amyotrophic lateral sclerosis destabilizes vascular endothelial growth factor mRNA and downregulates its expression. J Neurosci 27(30):7929-7938. doi: 10.1523/JNEUROSCI.1877-07.2007
78. Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, Sanberg PR (2007) Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modeling ALS. PLoS One 2(11):e1205. doi: 10.1371/journal.pone.0001205
79. Henkel JS, Beers DR, Wen S, Bowser R, Appel SH (2009) Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS. Neurology 72(18):1614-1616. doi: 10.1212/WNL.0b013e3181a41228
80. Argaw AT, Asp L, Zhang J, Navrazhina K, Pham T, Mariani JN, Mahase S, Dutta DJ, Seto J, Kramer EG, Ferrara N, Sofroniew MV, John GR (2012) Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J Clin Investig 122(7):2454-2468. doi: 10.1172/JCI60842
81. Bruck W, Bitsch A, Kolenda H, Bruck Y, Stiefel M, Lassmann H (1997) Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol 42(5):783-793. doi: 10.1002/ana.410420515
82. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR (2009) VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci U S A 106(6):1977-1982. doi: 10.1073/pnas.0808698106
83. Dobrogowska DH, Lossinsky AS, Tarnawski M, Vorbrodt AW (1998) Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J Neurocytol 27(3):163-173
84. Proescholdt MA, Jacobson S, Tresser N, Oldfield EH, Merrill MJ (2002) Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats. J Neuropathol Exp Neurol 61(10):914-925
85. Sun A, Binay KR, Xiang F, Zhao J, Wang Y, Xu L, Ma H, Wang K, Zou Y, Huang W, Ge J (2009) CTSS promoter -25G/A: not a risk factor for CHD in Chinese. Acta Cardiol 64(3):393-396
86. Storkebaum E, Quaegebeur A, Vikkula M, Carmeliet P (2011) Cerebrovascular disorders: molecular insights and therapeutic opportunities. Nat Neurosci 14(11):1390-1397. doi: 10.1038/nn.2947
87. Patel NS, Mathura VS, Bachmeier C, Beaulieu-Abdelahad D, Laporte V, Weeks O, Mullan M, Paris D (2010) Alzheimer's beta-amyloid peptide blocks vascular endothelial growth factor mediated signaling via direct interaction with VEGFR-2. J Neurochem 112(1):66-76. doi: 10.1111/j.1471-4159.2009.06426.x
88. Wang P, Xie ZH, Guo YJ, Zhao CP, Jiang H, Song Y, Zhu ZY, Lai C, Xu SL, Bi JZ (2011) VEGF-induced angiogenesis ameliorates the memory impairment in APP transgenic mouse model of Alzheimer's disease. Biochem Biophys Res Commun 411(3):620-626. doi: 10.1016/j.bbrc.2011.07.003
89. Faucheux BA, Bonnet AM, Agid Y, Hirsch EC (1999) Blood vessels change in the mesencephalon of patients with Parkinson's disease. Lancet 353(9157):981-982. doi: 10.1016/S0140-6736(99)00641-8
90. Mihci E, Ozkaynak SS, Sallakci N, Kizilay F, Yavuzer U (2011) VEGF polymorphisms and serum VEGF levels in Parkinson's disease. Neurosci Lett 494(1):1-5. doi: 10.1016/j.neulet.2011.02.027
91. Yasuhara T, Shingo T, Muraoka K, Kameda M, Agari T, Wen Ji Y, Hayase H, Hamada H, Borlongan CV, Date I (2005) Neurorescue effects of VEGF on a rat model of Parkinson's disease. Brain Res 1053(1-2):10-18. doi: 10.1016/j.brainres. 2005.05.027
92. Yasuhara T, Shingo T, Kobayashi K, Takeuchi A, Yano A, Muraoka K, Matsui T, Miyoshi Y, Hamada H, Date I (2004) Neuroprotective effects of vascular endothelial growth factor (VEGF) upon dopaminergic neurons in a rat model of Parkinson's disease. Eur J Neurosci 19(6):1494-1504. doi: 10.1111/j.1460-9568. 2004.03254.x
93. Tian YY, Tang CJ, Wang JN, Feng Y, Chen XW, Wang L, Qiao X, Sun SG (2007) Favorable effects of VEGF gene transfer on a rat model of Parkinson disease using adeno-associated viral vectors. Neurosci Lett 421(3):239-244. doi: 10.1016/j.neulet.2007.05.033
94. Falk T, Zhang S, Sherman SJ (2009) Vascular endothelial growth factor B (VEGF-B) is up-regulated and exogenous VEGF-B is neuroprotective in a culture model of Parkinson's disease. Mol Neurodegener 4:49. doi: 10.1186/1750-1326-4-49
95. Falk T, Yue X, Zhang S, McCourt AD, Yee BJ, Gonzalez RT, Sherman SJ (2011) Vascular endothelial growth factor-B is neuroprotective in an in vivo rat model of Parkinson's disease. Neurosci Lett 496(1):43-47. doi: 10.1016/j.neulet.2011.03.088
96. Orr HT (2012) Cell biology of spinocerebellar ataxia. J Cell Biol 197(2):167-177. doi: 10.1083/jcb.201105092