Characterization of neural stem/progenitor cells expressing VEGF and its receptors in the subventricular zone of newborn piglet brain

Neurochemical Research

Volumn 35, Issue 9, 2010, Pages 1455-1470

  Ara, Jahan ^a   Fekete, Saskia ^b   Zhu, Anli ^a   Frank, Melissa ^a  

^a ST CHRISTOPHER'S HOSPITAL FOR CHILDREN   (United States)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Neural stem progenitor cells; Newborn brain Piglet; Proliferation; Subventricular zone; VEGF

Indexed keywords

MESSENGER RNA; NESTIN; NEUROPILIN 1; NEUROPILIN 2; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VIMENTIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN LATERAL VENTRICLE; CELL CLONE; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL CULTURE; NEURAL STEM CELL; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PIGLET; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA SPLICING; SUBVENTRICULAR ZONE;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; BRAIN; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION PROFILING; INTERMEDIATE FILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MULTIPOTENT STEM CELLS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; PROTEIN ISOFORMS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SWINE; VASCULAR ENDOTHELIAL GROWTH FACTORS; VIMENTIN;

EID: 77957834353     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-010-0207-2     Document Type: Article

References (79)

1. Lindvall O, Kokaia Z (2006) Stem cells for the treatment of neurological disorders. Nature 441:1094-1096 (Pubitemid 43990722)
2. Palmer TD, Ray J, Gage FH (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6:474-186
3. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574
4. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740-744 (Pubitemid 38294593)
5. Emsley JG, Mitchell BD, Kempermann G, Macklis JD (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75:321-341 (Pubitemid 40733268)
6. Scheffler B, Edenhofer F, Brustle O (2006) Merging fields: stem cells in neurogenesis, transplantation, and disease modeling. Brain Pathol 16:155-168 (Pubitemid 43876476)
7. Li Y, Chopp M (1999) Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res 838:1-10 (Pubitemid 29389812)
8. Lindvall O, McKay R (2003) Brain repair by cell replacement and regeneration. Proc Natl Acad Sci USA 100:7430-7431 (Pubitemid 36759985)
9. Gu W, Brannstrom T, Wester P (2000) Cortical neurogenesis in adult rats after reversible photothrombotic stroke. J Cereb Blood Flow Metab 20:1166-1173 (Pubitemid 30636752)
10. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710-4715 (Pubitemid 32295041)
11. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neu-rogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-7778 (Pubitemid 28441018)
12. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738
13. Scharfman HE, Goodman JH, Sollas AL (2000) Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci 20:6144-6158
14. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970 (Pubitemid 35033700)
15. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA (2003) Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24:171-189 (Pubitemid 37194543)
16. Parent JM, Valentin VV, Lowenstein DH (2002) Prolonged seizures increase proliferating neuroblasts in the adult rat subven-tricular zone-olfactory bulb pathway. J Neurosci 22:3174-3188
17. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429-441 (Pubitemid 35232287)
18. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802-813 (Pubitemid 35403191)
19. Doetsch F (2003) A niche for adult neural stem cells. Curr Opin Genet Dev 13:543-550 (Pubitemid 37204933)
20. Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432 (Pubitemid 135711798)
21. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17:5820-5829 (Pubitemid 27310497)
22. Ogunshola OO, Antic A, Donoghue MJ, Fan SY, Kim H, Stewart WB, Madri JA, Ment LR (2002) Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J Biol Chem 277:11410-11415 (Pubitemid 34952908)
23. Schanzer A, Wachs FP, Wilhelm D, Acker T, Cooper-Kuhn C, Beck H, Winkler J, Aigner L, Plate KH, Kuhn HG (2004) Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol 14:237-248 (Pubitemid 39095985)
24. Ferrara N, Davis-Smyth T (1997) The biology of vascular endothelial growth factor. Endocr Rev 18:4-25 (Pubitemid 27076453)
25. Lei J, Jiang A, Pei D (1998) Identification and characterization of A new splicing variant of vascular endothelial growth factor: VEGF183. Biochim Biophys Acta 1443:400-406 (Pubitemid 29023374)
26. Poltorak Z, Cohen T, Sivan R, Kandelis Y, Spira G, Vlodavsky I, Keshet E, Neufeld G (1997) VEGF145, A secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J Biol Chem 272:7151-7158 (Pubitemid 27166421)
27. Ribeiro LA, Bacci ML, Seren E, Tamanini C, Forni M (2007) Characterization and differential expression of vascular endo-thelial growth factor isoforms and receptors in swine corpus luteum throughout estrous cycle. Mol Reprod Dev 74:163-171 (Pubitemid 46047986)
28. Robinson CJ, Stringer SE (2001) The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 114:853-865 (Pubitemid 32273121)
29. Whittle C, Gillespie K, Harrison R, Mathieson PW, Harper SJ (1999) Heterogeneous vascular endothelial growth factor (VEGF) isoform mRNA and receptor mRNA expression in human glomeruli, and the identification of VEGF148 mRNA, A novel truncated splice variant. Clin Sci (Lond) 97:303-312 (Pubitemid 29425324)
30. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9:669-676 (Pubitemid 36749215)
31. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z (1999) Vascular endothelial growth factor (VEGF) and its receptors. Faseb J 13:9-22 (Pubitemid 29038270)
32. Ferrara N (2000) VEGF: an update on biological and therapeutic aspects. Curr Opin Biotechnol 11:617-624
33. Flecknell PA, Wootton R, John M (1982) Accurate measurement of cerebral metabolism in the conscious, unrestrained neonatal piglet. II. Glucose and oxygen utilization. Biol Neonate 41: 221-226 (Pubitemid 12124003)
34. Haaland K, Loberg EM, Steen PA, Thoresen M (1997) Post-hypoxic hypothermia in newborn piglets. PediatrRes 41:505-512
35. Armstrong RJ, Tyers P, Jain M, Richards A, Dunnett SB, Rosser AE, Barker RA (2003) Transplantation of expanded neural precursor cells from the developing pig ventral mesencephalon in A rat model of Parkinson's disease. Exp Brain Res 151:204-217 (Pubitemid 36836528)
36. Isacson O, Deacon TW (1996) Specific axon guidance factors persist in the adult brain as demonstrated by pig neuroblasts transplanted to the rat. Neuroscience 75:827-837 (Pubitemid 26377052)
37. Zigova T, Song S, Willing AE, Hudson JE, Newman MB, Saporta S, Sanchez-Ramos JR, Sanberg PR (2002) Human umbilical cells express neural antigens after transplantation into the developing rat brain. Cell Transplant 11:265-274 (Pubitemid 34665827)
38. McGuckin C, Forraz N (2006) Mini-livers from umbilical cord blood stem cells. http://www.futurepundit.com/archives/003846.html
39. Sanberg PR, Willing AE, Cahill DW (2002) Novel cellular approaches to repair of neurodegenerative disease: from Sertoli cells to umbilical cord blood stem cells. Neurotox Res 4(2): 95-101
40. Ara J, Bannerman P, Shaheen F, Pleasure DE (2005) Schwann cell-autonomous role of neuropilin-2. J Neurosci Res 79:468-475 (Pubitemid 40283346)
41. Ara J, Bannerman P, Hahn A, Ramirez S, Pleasure D (2004) Modulation of sciatic nerve expression of class 3 semaphorins by nerve injury. Neurochem Res 29:1153-1159 (Pubitemid 39023489)
42. Rosser AE, Tyers P, ter Borg M, Dunnett SB, Svendsen CN (1997) Co-expression of MAP-2 and GFAP in cells developing from rat EGF responsive precursor cells. Brain Res Dev Brain Res 98:291-295 (Pubitemid 27075287)
43. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, Fraser RA, Couldwell WT, Kawaguchi A, Okano H, Nedergaard M, Goldman SA (2000) In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 6:271-277 (Pubitemid 30148618)
44. Carpenter MK, Cui X, Hu ZY, Jackson J, Sherman S, Seiger A, Wahlberg LU (1999) In vitro expansion of A multipotent population of human neural progenitor cells. Exp Neurol 158:265-278 (Pubitemid 29382819)
45. Gage FH (2000) Mammalian neural stem cells. Science (New York, NY) 287:1433-1438
46. Svendsen CN, Clarke DJ, Rosser AE, Dunnett SB (1996) Survival and differentiation of rat and human epidermal growth factor-responsive precursor cells following grafting into the lesioned adult central nervous system. Exp Neurol 137:376-388
47. Svendsen CN, ter Borg MG, Armstrong RJ, Rosser AE, Chandran S, Ostenfeld T, Caldwell MA (1998) A new method for the rapid and long term growth of human neural precursor cells. J Neurosci Methods 85:141-152 (Pubitemid 29003064)
48. Vescovi AL, Parati EA, Gritti A, Poulin P, Ferrario M, Wanke E, Frolichsthal-Schoeller P, Cova L, Arcellana-Panlilio M, Colombo A, Galli R (1999) Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp Neurol 156:71-83 (Pubitemid 29152984)
49. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 92:11879-11883 (Pubitemid 26014213)
50. Jin K, LaFevre-Bernt M, Sun Y, Chen S, Gafni J, Crippen D, Logvinova A, Ross CA, Greenberg DA, Ellerby LM (2005) FGF-2 promotes neurogenesis and neuroprotection and prolongs survival in A transgenic mouse model of Huntington's disease. Proc Natl Acad Sci USA 102:18189-18194 (Pubitemid 41798523)
51. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006) Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci USA 103:13198-13202 (Pubitemid 44338939)
52. Zhang RL, LeTourneau Y, Gregg SR et al (2007) Neuroblast division during migration toward the ischemic striatum: A study of dynamic migratory and proliferative characteristics of neuro-blasts from the subventricular zone. J Neurosci 27:3157-3162
53. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, Salani G, Martinello M, Cattalini A, Bergami A, Furlan R, Comi G, Constantin G, Martino G (2005) Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodula-tory mechanism. Nature 436:266-271 (Pubitemid 41021278)
54. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716 (Pubitemid 29278045)
55. Frederiksen K, McKay RD (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144-1151
56. Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328 (Pubitemid 16182611)
57. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express A new class of intermediate filament protein. Cell 60: 85-595 (Pubitemid 20083815)
58. Lothian C, Lendahl U (1997) An evolutionarily conserved region in the second intron of the human nestin gene directs gene expression to CNS progenitor cells and to early neural crest cells. Eur J Neurosci 9:452-462 (Pubitemid 27144014)
59. Bonfanti L, Theodosis DT (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the sube-pendymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neurosci 61:291-305 (Pubitemid 24287364)
60. Gates MA, Thomas LB, Howard EM, Laywell ED, Sajin B, Faissner A, Gotz B, Silver J, Steindler DA (1995) Cell and molecular analysis of the developing and adult mouse subven-tricular zone of the cerebral hemispheres. J Comp Neurol 361:249-266
61. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978-981 (Pubitemid 26066393)
62. Rousselot P, Alvarez-Buylla A, Lois C (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol 351:51-61
63. Zerlin M, Levison SW, Goldman JE (1995) Early patterns of migration, morphogenesis, and intermediate filament expression of subventricular zone cells in the postnatal rat forebrain. J Neurosci 15:7238-7249
64. Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127-1134 (Pubitemid 37346029)
65. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2006) Cellular composition and cytoarchitecture of the adult human subven-tricular zone: A niche of neural stem cells. J Comp Neurol 494:415-434 (Pubitemid 41794059)
66. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde YA, Gotz M (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5:308-315 (Pubitemid 34279810)
67. Lee JA, Cole GJ (2000) Localization of transition mRNA, A nestin-like intermediate filament family member, in chicken radial glia processes. J Comp Neurol 418:473-483
68. Parnavelas JG, Nadarajah B (2001) Radial glial cells are they really glia? Neuron 31:881-884 (Pubitemid 32925275)
69. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160 (Pubitemid 32846963)
70. Aharoni R, Arnon R, Eilam R (2005) Neurogenesis and neuroprotection induced by peripheral immunomodulatory treatment of experimental autoimmune encephalomyelitis. J Neurosci 25: 8217-8228 (Pubitemid 41292116)
71. Emery DL, Fulp CT, Saatman KE, Schutz C, Neugebauer E, Mcintosh TK (2005) Newly born granule cells in the dentate gyrus rapidly extend axons into the hippocampal CA3 region following experimental brain injury. J Neurotrauma 22:978-988 (Pubitemid 41362064)
72. Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44 (Pubitemid 34498810)
73. Bjorklund A, Lindvall O (2000) Self-repair in the brain. Nature 405:892-895 (Pubitemid 30435028)
74. Kuhn HG, Palmer TD, Fuchs E (2001) Adult neurogenesis: A compensatory mechanism for neuronal damage. Eur Arch Psychiatry Clin Neurosci 251:152-158 (Pubitemid 32963492)
75. 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 USA 99:11946-11950 (Pubitemid 34994504)
76. Maurer MH, Tripps WK, Feldmann RE Jr, Kuschinsky W (2003) Expression of vascular endothelial growth factor and its receptors in rat neural stem cells. Neurosci Lett 344:165-168 (Pubitemid 36694669)
77. Silverman WF, Krum JM, Mani N, Rosenstein JM (1999) Vascular, glial and neuronal effects of vascular endothelial growth factor in mesencephalic explant cultures. Neuroscience 90: 1529-1541 (Pubitemid 29170166)
78. Tonchev AB, Yamashima T, Sawamoto K, Okano H (2005) Enhanced proliferation of progenitor cells in the subventricular zone and limited neuronal production in the striatum and neocortex of adult macaque monkeys after global cerebral ischemia. J Neurosci Res 81:776-788 (Pubitemid 41532143)
79. Tonchev AB, Yamashima T, Zhao L, Okano HJ, Okano H (2003) Proliferation of neural and neuronal progenitors after global brain ischemia in young adult macaque monkeys. Mol Cell Neurosci 23:292-301 (Pubitemid 36703163)