VEGF-A angiogenesis induces a stable neovasculature in adult murine brain

Journal of Neuropathology and Experimental Neurology

Volumn 63, Issue 8, 2004, Pages 841-855

  Stiver, S I ^a,c   Tan, X ^a   Brown, L F ^a   Hedley Whyte, E T ^b   Dvorak, H F ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Adenovirus; Angiogenesis; Brain; Cerebrovascular disorders; Glioblastoma; Vascular endothelial growth factor (VEGF)

Indexed keywords

VASCULOTROPIN A;

ADENOVIRUS; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN INFARCTION; BRAIN TUMOR; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIOBLASTOMA; HEAD INJURY; IMMUNE RESPONSE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROKE; TUMOR GROWTH;

EID: 3843114299     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/63.8.841     Document Type: Article

References (70)

1. Wei L, Erinjeri JP, Rovainen CM, Woolsey TA. Collateral growth and angiogenesis around cortical stroke. Stroke 2001;32:2179-84
2. Rrupinski J, Kaluza J, Kumar P, Kumar S, Wang JM. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994; 25:1794-98
3. Issa R, Krupinski J, Bujny T, Kumar S, Kaluza J, Kumar P. Vascular endothelial growth factor and its receptor, KDR, in human brain tissue after ischemic stroke. Lab Invest 1999;79:417-25
4. Nag S, Takahashi JL, Kilty DW. Role of vascular endothelial growth factor in blood-brain barrier breakdown and angiogenesis in brain trauma. J Neuropathol Exp Neurol 1997;56:912-21
5. Papavassiliou E, Gogate N, Proescholdt M, et al. Vascular endothelial growth factor (vascular permeability factor) expression in injured rat brain. J Neurosci Res 1997;49:451-60
6. Marti HJ, Bernaudin M, Bellail A, et al. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 2000;156:965-76
7. Plate KH, Beck H, Danner S, Allegrini PR, Wiessner C. Cell type specific upregulation of vascular endothelial growth factor in an MCA-occlusion model of cerebral infarct. J Neuropathol Exp Neurol 1999;58:654-66
8. Conway EM, Zwerts F, Van Eygen V, et al. Survivin-dependent angiogenesis in ischemic brain: Molecular mechanisms of hypoxia-induced up-regulation. Am J Pathol 2003;163:935-46
9. Rojiani AM, Dorovini-Zis K. Glomeruloid vascular structures in glioblastoma multiforme: An immunohistochemical and ultrastructural study. J Neurosurg 1996;85:1078-84
10. Kleihues P, Louis DN, Scheithauer BW et al. The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol 2002;61:215-25
11. Koizumi T, Shiraishi T, Hagihara N, Tabuchi K, Hayashi T, Kawano T. Expression of vascular endothelial growth factors and their receptors in and around intracranial arteriovenous malformations. Neurosurgery 2002;50:117-24
12. Rothbart D, Awad IA, Lee J, Kim J, Harbaugh R, Criscuolo GR. Expression of angiogenic factors and structural proteins in central nervous system vascular malformations. Neurosurgery 1996;38:915-24
13. Breier G, Albrecht U, Sterrer S, Risau W. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 1992;114:521-32
14. Flamme I, Breier G, Risau W Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 1995;169:699-712
15. Flamme I, von Reutern M, Drexler HCA, Syed-Ali S, Risau W. Overexpression of vascular endothelial growth factor in the avian embryo induces hypervascularization and increased vascular permeability without alterations of embryonic pattern formation. Dev Biol 1995;171:399-414
16. Pettersson A, Nagy JA, Brown LF, et al. Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab Invest 2000;80:99-115
17. Proescholdt MA, Heiss JD, Walbridge S, et al. Vascular endothelial growth factor (VEGF) modulates vascular permeability and inflammation in rat brain. J Neuropathol Exp Neurol 1999;58:613-27
18. Krum JM, Mani N, Rosenstein JM. Angiogenic and astroglial responses to vascular endothelial growth factor administration in adult rat brain. Neuroscience 2002;110:589-604
19. Harrigan MR, Ennis SR, Masada T, Keep RF. Intraventricular infusion of vascular endothelial growth factor promotes cerebral angiogenesis with minimal brain edema. Neurosurgery 2002;50:589-98
20. Vogel J, Horner C, Haller C, Kuschinsky W. Heterologous expression of human VEGF165 in rat brain: Dose-dependent, heterogeneous effects on CBF in relation to vascular density and cross-sectional area. J Cereb Blood Flow Metab 2003;23:423-31
21. Yang GY, Xu B, Hashimoto T, et al. Induction of focal angiogenesis through adenoviral vector mediated vascular endothelial cell growth factor gene transfer in the mature mouse brain. Angiogenesis 2003; 6:151-58
22. Byrnes AP, Wood MJ, Charlton HM. Role of T cells in inflammation caused by adenovirus vectors in the brain. Gene Ther 1996;3:644-51
23. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chemistry 1992;267:26031-37
24. Dvorak HF, Nagy JA, Dvorak JT, Dvorak AM. Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules. Am J Pathol 1988;133:95-109
25. Ozerdem U, Monosov E, Stallcup WB. NG2 Proteoglycan expression by pericytes in pathological microvasculature. Microvasc Res 2002;63:129-34
26. Porter GA, Palade GE, Milici AJ. Differential binding of the lectins Griffonia simplicifolia I and Lycopersicon esculentum to microvascular endothelium: Organ-specific localization and partial glycoprotein characterization. Eur J Cell Biol 1990;51:85-95
27. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-β and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999;126:3047-55
28. Brown LF, Chester JF, Malt RA, Dvorak HF. Fibrin deposition in autochthonous Syrian hamster pancreatic adenocarcinomas induced by the chemical carcinogen N-nitroso-bis(2-oxopropyl)amine. J Natl Cancer Inst 1987;78:979-86
29. Hu BR, Liu CL, Ouyang Y, Blomgren K, Siesjo BK. Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J Cereb Blood Flow Metab 2000;20:1294-1300
30. Brown LF, Guidi AJ, Tognazzi K, Dvorak HF. Vascular permeability factor/vascular endothelial growth factor and vascular stroma formation in neoplasia. Insights from in situ hybridization studies. J Histochem Cytochem 1998;46:569-75
31. Brown LF, Berse B, Jackman RW, et al. Increased expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in kidney and bladder carcinomas. Am J Pathol 1993;143:1255-62
32. Brown LF, Dezube BJ, Tognazzi K, Dvorak HF, Yancopoulos GD. Expression of Tie1, Tie2, and Angiopoietins 1, 2, and 4 in Kaposi's Sarcoma and Cutaneous Angiosarcoma. Am J Pathol 2000;156:2179-83
33. Streit M, Stephen AE, Hawighorst T, et al. Systemic inhibition of tumor growth and angiogenesis by thrombospondin-2 using cell-based antiangiogenic gene therapy. Cancer Res 2002;62:2004-12
34. Hawighorst T, Oura H, Streit M, et al. Thrombospondin-1 selectively inhibits early-stage carcinogenesis and angiogenesis but not tumor lymphangiogenesis and lymphatic metastasis in transgenic mice. Oncogene 2002;21:7945-56
35. Sundberg C, Nagy JA, Brown LF, et al. Glomeruloid microvascular proliferation follows adenoviral vascular permeability factor/vascular endothelial growth factor-164 gene delivery. Am J Pathol 2001;158:1145-60
36. Davidson BL, Allen ED, Kozarsky KF, Wilson JM, Roessler BJ. A model system for in vivo gene transfer into the central nervous system using an adenoviral vector. Nat Genet 1993;3:219-23
37. Uchida T, Kajiwara K, Ideguchi M, Yoshikawa K, Morioka J, Suzuki M. Co-administration of adenovirus vector expressing CTLA4-Ig prolongs transgene expression in the brain of mice sensitized with adenovirus. Brain Res 2001;898:272-80
38. Byrnes AP, Rusby JE, Wood MJ, Charlton HM. Adenovirus gene transfer causes inflammation in the brain. Neuroscience 1995;66:1015-24
39. O'Connor WM, Davidson BL, Kaplitt MG, et al. Adenovirus vector-mediated gene transfer into human epileptogenic brain slices: Prospects for gene therapy in epilepsy. Exp Neurol 1997;148:167-78
40. Le Gal La Salle G, Robert JJ, Berrard S, et al. An adenovirus vector for gene transfer into neurons and glia in the brain. Science 1993; 259:988-90
41. Chodobski A, Chung I, Kozniewska E, et al. Early neutrophilic expression of vascular endothelial growth factor after traumatic brain injury. Neuroscience 2003;122:853-67
42. Nag S. Cold-injury of the cerebral cortex: Immunolocalization of cellular proteins and blood-brain barrier permeability studies. J Neuropathol Exp Neurol 1996;55:880-88
43. Dawson MR, Levine JM, Reynolds R. NG2-expressing cells in the central nervous system: Are they oligodendroglial progenitors? J Neurosci Res 2000;61:471-79
44. Maisonpierre PC, Suri C, Jones PF, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997;277:55-60
45. Lobov IB, Brooks PC, Lang RA. Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci U S A 2002;99:11205-10
46. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-β and VEGF Development 1998;125:1591-98
47. Weiss HR, Edelman NH. Effect of hypoxia on small vessel blood content of rabbit brain. Microvasc Res 1976;12:305-15
48. Kontos HA, Wei EP, Raper AJ, Rosenblum WI, Navari RM, Patterson JL Jr. Role of tissue hypoxia in local regulation of cerebral microcirculation. Am J Physiol 1978;234:H582-91
49. Bar T. The vascular system of the cerebral cortex. Adv Anat Embryol Cell Biol 1980;59:1-62
50. Papapetropoulos A, Fulton D, Mahboubi K, et al. Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J Biol Chem 2000;275:9102-5
51. Sundberg C, Kowanetz M, Brown LF, Detmar M, Dvorak HF. Stable expression of angiopoietin-1 and other markers by cultured pericytes: Phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab Invest 2002;82:387-401
52. Suri C, Jones PF, Patan S, et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996;87:1171-80
53. Papapetropoulos A, Garcia-Cardena G, Dengler TJ, Maisonpierre PC, Yancopoulos GD, Sessa WC. Direct actions of angiopoietin-1 on human endothelium: Evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors. Lab Invest 1999;79:213-23
54. Beck H, Acker T, Wiessner C, Allegrini PR, Plate KH. Expression of angiopoietin-1, angiopoietin-2, and tie receptors after middle cerebral artery occlusion in the rat. Am J Pathol 2000;157:1473-83
55. Wong AL, Haroon ZA, Werner S, Dewhirst MW, Greenberg CS, Peters KG. Tie2 expression and phosphorylation in angiogenic and quiescent adult tissues. Circ Res 1997;81:567-74
56. Nourhaghighi N, Teichert-Kuliszewska K, Davis J, Stewart DJ, Nag S. Altered expression of angiopoietins during blood-brain barrier breakdown and angiogenesis. Lab Invest 2003;83:1211-22
57. Lagord C, Berry M, Logan A. Expression of TGFbeta2 but not TGFbetal correlates with the deposition of scar tissue in the lesioned spinal cord. Mol Cell Neurosci 2002;20:69-92
58. Darland DC, D'Amore PA. TGF beta is required for the formation of capillary-like structures in three-dimensional cocultures of 10T1/ 2 and endothelial cells. Angiogenesis 2001;4:11-20
59. Bonanno E, Iurlaro M, Madri JA, Nicosia RF. Type IV collagen modulates angiogenesis and neovessel survival in the rat aorta model. In Vitro Cell Dev Biol Anim 2000;36:336-40
60. Nicosia RF, Bonanno E, Smith M, Yurchenco P. Modulation of angiogenesis in vitro by laminin-entactin complex. Dev Biol 1994; 164:197-206
61. Skalak TC, Price RJ, Zeller PJ. Where do new arterioles come from? Mechanical forces and microvessel adaptation. Microcirculation 1998;5:91-94
62. Price RJ, Skalak TC. Chronic alpha 1-adrenergic blockade stimulates terminal and arcade arteriolar development. Am J Physiol 1996;271:H752-59
63. Woo SH, Kim SE, Lee TH, Jeong JH, Seul JH. Effects of blood flow and venous network on the survival of the arterialized venous flap. Plast Reconstr Surg 1998;101:1280-89
64. Bruner JM, Tien RD, McLendon RE. Tumors of vascular origin. In: Bigner DD, McLendon RE, Bruner JM, eds. Russell & Rubinstein's pathology of tumors of the nervous system. 6th Ed. New York: Oxford University Press, 1998; Vol. 2:239-93
65. McCormick WF. The pathology of vascular ("ovenous" formations. J Neurosurg 1966;24:807-16
66. Rigamonti D, Johnson PC, Spetzler RF, Hadley MN, Drayer BP. Cavernous malformations and capillary telangiectasia: A spectrum within a single pathological entity. Neurosurgery 1991;28:60-64
67. Stehbens WE. Pathology of the cerebral blood vessels. St. Louis, MO: C.V. Mosby Co, 1972
68. Jellinger K. Vascular malformations of the central nervous system: A morphological overview. Neurosurg Rev 1986;9:177-216
69. Birner P, Piribauer M, Fischer I, et al. Vascular patterns in glioblastoma influence clinical outcome and associate with variable expression of angiogenic proteins: Evidence for distinct angiogenic subtypes. Brain Pathol 2003;13:133-43
70. Plate KH, Breier G, Weich HA, Risau W Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992;359:845-48.