Cell-cell signaling in the neurovascular unit

Neurochemical Research

Volumn 32, Issue 12, 2007, Pages 2032-2045

  Lok, Josephine ^a,b   Gupta, Punkaj ^a   Guo, Shuzhen ^a,b   Kim, Woo Jean ^a,b   Whalen, Michael J ^a   Van Leyen, Klaus ^a,b   Lo, Eng H ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Angiogenesis; Blood brain barrier; Neurodegeneration; Neurogenesis; Neuroprotection; Stroke

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; NEUROTROPHIN 3; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; CELL FUNCTION; CELL INTERACTION; CENTRAL NERVOUS SYSTEM DISEASE; GLIA CELL; HEMODYNAMICS; HOMEOSTASIS; NERVE CELL; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHORT SURVEY; SIGNAL TRANSDUCTION; STROKE;

ANIMALS; BLOOD-BRAIN BARRIER; CEREBROVASCULAR CIRCULATION; HUMANS; MUSCLE, SMOOTH, VASCULAR; NERVE GROWTH FACTORS; NEURONS; SIGNAL TRANSDUCTION;

EID: 35848949798     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-007-9342-9     Document Type: Short Survey

References (128)

1. Abbott NJ, Ronnback L, Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41-53
2. Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5:347-360
3. Park JA, Choi KS, Kim SY, Kim KW (2003) Coordinated interaction of the vascular and nervous systems: from molecule- to cell-based approaches. Biochem Biophys Res Commun 311:247-253
4. Allan S (2006) The neurovascular unit and the key role of astrocytes in the regulation of cerebral blood flow. Cerebrovasc Dis 21:137-138
5. Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173-185
6. Lo EH, Broderick JP, Moskowitz MA (2004) tPA and proteolysis in the neurovascular unit. Stroke 35:354-356
7. Drake CT, Iadecola C (2006) The role of neuronal signaling in controlling cerebral blood flow. Brain Lang, doi:10.1016/j.bandl.2006.08.002
8. Lassen NA, Larsen B (1980) Cortical activity in the left and right hemispheres during language-related brain functions. Phonetica 37:27-37
9. Foit A, Larsen B, Hattori S, Skinhoj E, Lassen NA (1980) Cortical activation during somatosensory stimulation and voluntary movement in man: a regional cerebral blood flow study. Electroencephalogr Clin Neurophysiol 50:426-436
10. Hougaard K, Oikawa T, Sveinsdottir E, Skinoj E, Ingvar DH, Lassen NA (1976) Regional cerebral blood flow in focal cortical epilepsy. Arch Neurol 33:527-535
11. Jones EG (1970) On the mode of entry of blood vessels into the cerebral cortex. J Anat 106:507-520
12. Edvinsson L, Hamel E (2002) Perivascular nerves in brain vessels. In: Edvinsson L, Krause DN (eds) Cerebral blood flow and metabolism. Lippincott, Williams and Wilkins, Philadelphia, pp 43-67
13. Iadecola C (1998) Cerebral circulatory dysregulation in ischemia. In: Ginsberg D, Bogousslavsky J (eds) Cerebrovascular diseases. Blackwell Science, Cambridge, MA, pp 319-322
14. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260-267
15. Cohen Z, Bonvento G, Lacombe P, Hamel E (1996) Serotonin in the regulation of brain microcirculation. Prog Neurobiol 50:335-362
16. Rennels ML, Nelson E (1975) Capillary innervation in the mammalian central nervous system: an electron microscopic demonstration. Am J Anat 144:233-241
17. Maynard EA, Schultz RL, Pease DC (1957) Electron microscopy of the vascular bed of rat cerebral cortex. Am J Anat 100:409-433
18. Hirase H (2005) A multi-photon window onto neuronal-glial-vascular communication. Trends Neurosci 28:217-219
19. Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195-199
20. Zonta M, Sebelin A, Gobbo S, Fellin T, Pozzan T, Carmignoto G (2003) Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J Physiol 553:407-414
21. Busija DW (1993) Cerebral autoregulation. In: Philis JW (ed) The regulation of cerebral blood flow. CRC Press, Boca Raton, pp 45-64
22. Fergus A, Lee KS (1997) GABAergic regulation of cerebral microvascular tone in the rat. J Cereb Blood Flow Metab 17:992-1003
23. Iadecola C (1998) Neurogenic control of the cerebral microcirculation: is dopamine minding the store? Nat Neurosci 1:263-265
24. Uddman R, Edvinsson L (1989) Neuropeptides in the cerebral circulation. Cerebrovasc Brain Metab Rev 1:230-252
25. Bhardwaj A, Northington FJ, Carhuapoma JR, Falck JR, Harder DR, Traystman RJ, Koehler RC (2000) P-450 epoxygenase and NO synthase inhibitors reduce cerebral blood flow response to N-methyl-d-aspartate. Am J Physiol Heart Circ Physiol 279: H1616-H1624
26. Buerk DG, Atochin DN, Riva CE (2003) Investigating the role of nitric oxide in regulating blood flow and oxygen delivery from in vivo electrochemical measurements in eye and brain. Adv Exp Med Biol 530:359-370
27. Faraci FM, Brian JE Jr (1995) 7-Nitroindazole inhibits brain nitric oxide synthase and cerebral vasodilatation in response to N-methyl-d-aspartate. Stroke 26:2172-2175; discussion 2176
28. Zhang F, Xu S, Iadecola C (1995) Role of nitric oxide and acetylcholine in neocortical hyperemia elicited by basal forebrain stimulation: evidence for an involvement of endothelial nitric oxide. Neuroscience 69:1195-1204
29. Wu DM, Kawamura H, Sakagami K, Kobayashi M, Puro DG (2003) Cholinergic regulation of pericyte-containing retinal microvessels. Am J Physiol Heart Circ Physiol 284:H2083-H2090
30. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT (2006) Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 9:1397-1403
31. Sokoya EM, Burns AR, Setiawan CT, Coleman HA, Parkington HC, Tare M (2006) Evidence for the involvement of myoendothelial gap junctions in EDHF-mediated relaxation in the rat middle cerebral artery. Am J Physiol Heart Circ Physiol 291: H385-H393
32. Cox SB, Woolsey TA, Rovainen CM (1993) Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J Cereb Blood Flow Metab 13:899-913
33. Erinjeri JP, Woolsey TA (2002) Spatial integration of vascular changes with neural activity in mouse cortex. J Cereb Blood Flow Metab 22:353-360
34. Ngai AC, Ko KR, Morii S, Winn HR (1988) Effect of sciatic nerve stimulation on pial arterioles in rats. Am J Physiol 254:H133-H139
35. Busse R, Fleming I (2003) Regulation of endothelium-derived vasoactive autacoid production by hemodynamic forces. Trends Pharmacol Sci 24:24-29
36. Peppiatt CM, Howarth C, Mobbs P, Attwell D (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443:700-704
37. Pelligrino DA (2006) Regulation of the cerebral circulation. J Appl Physiol 100:3-4
38. Mintun MA, Lundstrom BN, Snyder AZ, Vlassenko AG, Shulman GL, Raichle ME (2001) Blood flow and oxygen delivery to human brain during functional activity: theoretical modeling and experimental data. Proc Natl Acad Sci USA 98:6859-6864
39. Powers WJ, Hirsch IB, Cryer PE (1996) Effect of stepped hypoglycemia on regional cerebral blood flow response to physiological brain activation. Am J Physiol 270:H554-H559
40. Gotoh J, Kuang TY, Nakao Y, Cohen DM, Melzer P, Itoh Y, Pak H, Pettigrew K, Sokoloff L (2001) Regional differences in mechanisms of cerebral circulatory response to neuronal activation. Am J Physiol Heart Circ Physiol 280:H821-H829
41. Koehler RC, Gebremedhin D, Harder DR (2006) Role of astrocytes in cerebrovascular regulation. J Appl Physiol 100:307-317
42. White RP, Hindley C, Bloomfield PM, Cunningham VJ, Vallance P, Brooks DJ, Markus HS (1999) The effect of the nitric oxide synthase inhibitor L-NMMA on basal CBF and vasoneuronal coupling in man: a PET study. J Cereb Blood Flow Metab 19:673-678
43. Newman EA (2003) New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 26:536-542
44. Ngai AC, Coyne EF, Meno JR, West GA, Winn HR (2001) Receptor subtypes mediating adenosine-induced dilation of cerebral arterioles. Am J Physiol Heart Circ Physiol 280:H2329-H2335
45. Shin HK, Shin YW, Hong KW (2000) Role of adenosine A(2B) receptors in vasodilation of rat pial artery and cerebral blood flow autoregulation. Am J Physiol Heart Circ Physiol 278: H339-H344
46. Saez JC, Retamal MA, Basilio D, Bukauskas FF, Bennett MV (2005) Connexin-based gap junction hemichannels: gating mechanisms. Biochim Biophys Acta 1711:215-224
47. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488
48. Alloisio S, Cugnoli C, Ferroni S, Nobile M (2004) Differential modulation of ATP-induced calcium signalling by A1 and A2 adenosine receptors in cultured cortical astrocytes. Br J Pharmacol 141:935-942
49. Jimenez AI, Castro E, Mirabet M, Franco R, Delicado EG, Miras-Portugal MT (1999) Potentiation of ATP calcium responses by A2B receptor stimulation and other signals coupled to Gs proteins in type-1 cerebellar astrocytes. Glia. 26:119-128
50. Peakman MC, Hill SJ (1994) Adenosine A2B-receptor-mediated cyclic AMP accumulation in primary rat astrocytes. Br J Pharmacol 111:191-198
51. Allaman I, Lengacher S, Magistretti PJ, Pellerin L (2003) A2B receptor activation promotes glycogen synthesis in astrocytes through modulation of gene expression. Am J Physiol Cell Physiol 284:C696-C704
52. Pilitsis JG, Kimelberg HK (1998) Adenosine receptor mediated stimulation of intracellular calcium in acutely isolated astrocytes. Brain Res 798:294-303
53. Krimer LS, Muly EC 3rd, Williams GV, Goldman-Rakic PS (1998) Dopaminergic regulation of cerebral cortical microcirculation. Nat Neurosci 1:286-289
54. Niwa K, Araki E, Morham SG, Ross ME, Iadecola C (2000) Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J Neurosci 20:763-770
55. Niwa K, Haensel C, Ross ME, Iadecola C (2001) Cyclooxygenase-1 participates in selected vasodilator responses of the cerebral circulation. Circ Res 88:600-608
56. Verbeek MM, de Waal RM, Schipper JJ, Van Nostrand WE (1997) Rapid degeneration of cultured human brain pericytes by amyloid beta protein. J Neurochem 68:1135-1141
57. Hirase T, Staddon JM, Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, Fujimoto K, Tsukita S, Rubin LL (1997) Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 110 (Pt 14):1603-1613
58. Estrada C, Bready JV, Berliner JA, Pardridge WM, Cancilla PA (1990) Astrocyte growth stimulation by a soluble factor produced by cerebral endothelial cells in vitro. J Neuropathol Exp Neurol 49:539-549
59. Mi H, Haeberle H, Barres BA (2001) Induction of astrocyte differentiation by endothelial cells. J Neurosci 21:1538-1547
60. Mizuguchi H, Utoguchi N, Mayumi T (1997) Preparation of glial extracellular matrix: a novel method to analyze glial-endothelial cell interaction. Brain Res Brain Res Protoc 1:339-343
61. Schroeter ML, Mertsch K, Giese H, Muller S, Sporbert A, Hickel B, Blasig IE (1999) Astrocytes enhance radical defence in capillary endothelial cells constituting the blood-brain barrier. FEBS Lett 449:241-244
62. Regina A, Morchoisne S, Borson ND, McCall AL, Drewes LR, Roux F (2001) Factor(s) released by glucose-deprived astrocytes enhance glucose transporter expression and activity in rat brain endothelial cells. Biochim Biophys Acta 1540:233-242
63. Braet K, Cabooter L, Paemeleire K, Leybaert L (2004) Calcium signal communication in the central nervous system. Biol Cell 96:79-91
64. Leybaert L, Cabooter L, Braet K (2004) Calcium signal communication between glial and vascular brain cells. Acta Neurol Belg 104:51-56
65. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702-710
66. Hansson E, Ronnback L (2003) Glial neuronal signaling in the central nervous system. Faseb J 17:341-348
67. Huber JD, Egleton RD, Davis TP (2001) Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24:719-725
68. Pardrige WM (2003) Molecular biology of the blood brain barrier. In: The blood brain barrier. Humana Press, Totowa, NJ, pp 385-397
69. Lee G, Bendayan R (2004) Functional expression and localization of P-glycoprotein in the central nervous system: relevance to the pathogenesis and treatment of neurological disorders. Pharm Res 21:1313-1330
70. Berzin TM, Zipser BD, Rafii MS, Kuo-Leblanc V, Yancopoulos GD, Glass DJ, Fallon JR, Stopa EG (2000) Agrin and microvascular damage in Alzheimer's disease. Neurobiol Aging 21:349-355
71. Kalaria RN (1999) The blood-brain barrier and cerebrovascular pathology in Alzheimer's disease. Ann N Y Acad Sci 893:113-125
72. Kortekaas R, Leenders KL, van Oostrom JC, Vaalburg W, Bart J, Willemsen AT, Hendrikse NH (2005) Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann Neurol 57:176-179
73. Minagar A, Alexander JS (2003) Blood-brain barrier disruption in multiple sclerosis. Mult Scler 9:540-549
74. Wolburg H, Wolburg-Buchholz K, Kraus J, Rascher-Eggstein G, Liebner S, Hamm S, Duffner F, Grote EH, Risau W, Engelhardt B (2003) Localization of claudin-3 in tight junctions of the blood-brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol (Berl) 105:586-592
75. Abbott NJ (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200:629-638
76. Marroni M, Marchi N, Cucullo L, Abbott NJ, Signorelli K, Janigro D (2003) Vascular and parenchymal mechanisms in multiple drug resistance: a lesson from human epilepsy. Curr Drug Targets 4:297-304
77. Davies DC (2002) Blood-brain barrier breakdown in septic encephalopathy and brain tumours. J Anat 200:639-646
78. Liebner S, Fischmann A, Rascher G, Duffner F, Grote EH, Kalbacher H, Wolburg H (2000) Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol (Berl) 100:323-331
79. Warth A, Kroger S, Wolburg H (2004) Redistribution of aquaporin-4 in human glioblastoma correlates with loss of agrin immunoreactivity from brain capillary basal laminae. Acta Neuropathol (Berl) 107:311-318
80. Carmeliet P (2003) Blood vessels and nerves: common signals, pathways and diseases. Nat Rev Genet 4:710-720
81. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494
82. 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
83. Jin KL, Mao XO, Greenberg DA (2000) Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci USA 97:10242-10247
84. Matsuzaki H, Tamatani M, Yamaguchi A, Namikawa K, Kiyama H, Vitek MP, Mitsuda N, Tohyama M (2001) Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. Faseb J 15:1218-1220
85. 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
86. 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
87. Bagnard D, Vaillant C, Khuth ST, Dufay N, Lohrum M, Puschel AW, Belin MF, Bolz J, Thomasset N (2001) Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J Neurosci 21:3332-3341
88. Miao HQ, Soker S, Feiner L, Alonso JL, Raper JA, Klagsbrun M (1999) Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J Cell Biol 146:233-242
89. Ciccolini F, Svendsen CN (1998) Fibroblast growth factor 2 (FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: identification of neural precursors responding to both EGF and FGF-2. J Neurosci 18:7869-7880
90. 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
91. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16:1091-1100
92. Kilpatrick TJ, Bartlett PF (1995) Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J Neurosci 15:3653-3661
93. Palmer TD, Takahashi J, Gage FH (1997) The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8:389-404
94. Tao Y, Black IB, DiCicco-Bloom E (1996) Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF). J Comp Neurol 376:653-663
95. Wagner JP, Black IB, DiCicco-Bloom E (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 19:6006-6016
96. Barres BA, Schmid R, Sendnter M, Raff MC (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118:283-295
97. Cameron HA, Hazel TG, McKay RD (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36:287-306
98. Wolswijk G, Riddle PN, Noble M (1991) Platelet-derived growth factor is mitogenic for O-2Aadult progenitor cells. Glia 4:495-503
99. Ward NL, Lamanna JC (2004) The neurovascular unit and its growth factors: coordinated response in the vascular and nervous systems. Neurol Res 26:870-883
100. Coulthard MG, Duffy S, Down M, Evans B, Power M, Smith F, Stylianou C, Kleikamp S, Oates A, Lackmann M, Burns GF, Boyd AW (2002) The role of the Eph-ephrin signalling system in the regulation of developmental patterning. Int J Dev Biol 46:375-384
101. Knoll B, Drescher U (2002) Ephrin-As as receptors in topographic projections. Trends Neurosci 25:145-149
102. Gerety SS, Wang HU, Chen ZF, Anderson DJ (1999) Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 4:403-414
103. Wang HU, Chen ZF, Anderson DJ (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93:741-753
104. Wilson BD, Ii M, Park KW, Suli A, Sorensen LK, Larrieu-Lahargue F, Urness LD, Suh W, Asai J, Kock GA, Thorne T, Silver M, Thomas KR, Chien CB, Losordo DW, Li DY (2006) Netrins promote developmental and therapeutic angiogenesis. Science 313:640-644
105. Gassmann M, Lemke G (1997) Neuregulins and neuregulin receptors in neural development. Curr Opin Neurobiol 7:87-92
106. Russell KS, Stern DF, Polverini PJ, Bender JR (1999) Neuregulin activation of ErbB receptors in vascular endothelium leads to angiogenesis. Am J Physiol 277:H2205-H2211
107. Seghezzi G, Patel S, Ren CJ, Gualandris A, Pintucci G, Robbins ES, Shapiro RL, Galloway AC, Rifkin DB, Mignatti P (1998) Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 141:1659-1673
108. Pepper MS, Mandriota SJ (1998) Regulation of vascular endothelial growth factor receptor-2 (Flk-1) expression in vascular endothelial cells. Exp Cell Res 241:414-425
109. Cobbs CS, Chen J, Greenberg DA, Graham SH (1998) Vascular endothelial growth factor expression in transient focal cerebral ischemia in the rat. Neurosci Lett 249:79-82
110. Krum JM, Rosenstein JM (1998) VEGF mRNA and its receptor flt-1 are expressed in reactive astrocytes following neural grafting and tumor cell implantation in the adult CNS. Exp Neurol 154:57-65
111. Kuwaki T, Kurihara H, Cao WH, Kurihara Y, Unekawa M, Yazaki Y, Kumada M (1997) Physiological role of brain endothelin in the central autonomic control: from neuron to knockout mouse. Prog Neurobiol 51:545-579
112. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL (1999) Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534-537
113. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-7778
114. 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
115. 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
116. Lee SR, Kim HY, Rogowska J, Zhao BQ, Bhide P, Parent JM, Lo EH (2006) Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26:3491-3495
117. Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, Wang X, Lo EH (2006) Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med 12:441-445
118. Wang L, Zhang Z, Zhang R, Hafner MS, Wong HK, Jiao Z, Chopp M (2004) Erythropoietin up-regulates SOCS2 in neuronal progenitor cells derived from SVZ of adult rat. Neuroreport 15:1225-1229
119. Shyu WC, Lin SZ, Yang HI, Tzeng YS, Pang CY, Yen PS, Li H (2004) Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation 110:1847-1854
120. Chen J, Zacharek A, Zhang C, Jiang H, Li Y, Roberts C, Lu M, Kapke A, Chopp M (2005) Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 25:2366-2375
121. Weston GC, Haviv I, Rogers PA (2002) Microarray analysis of VEGF-responsive genes in myometrial endothelial cells. Mol Hum Reprod 8:855-863
122. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA (1999) Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 13:450-464
123. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340
124. Stankovic K, Rio C, Xia A, Sugawara M, Adams JC, Liberman MC, Corfas G (2004) Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear. J Neurosci 24:8651-8661
125. Esper RM, Loeb JA (2004) Rapid axoglial signaling mediated by neuregulin and neurotrophic factors. J Neurosci 24:6218-6227
126. Fekete DM, Wu DK (2002) Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12:35-42
127. Nakamura K, Martin KC, Jackson JK, Beppu K, Woo CW, Thiele CJ (2006) Brain-derived neurotrophic factor activation of TrkB induces vascular endothelial growth factor expression via hypoxia-inducible factor-1alpha in neuroblastoma cells. Cancer Res 66:4249-4255
128. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017-1021