Vascular endothelial growth factor (VEGF) modulates vascular permeability and inflammation in rat brain

Journal of Neuropathology and Experimental Neurology

Volumn 58, Issue 6, 1999, Pages 613-627

  Proescholdt, Martin A ^a   Heiss, John D ^a   Walbridge, Stuart ^a   Mühlhauser, Judith ^b,c   Capogrossi, Maurizio C ^b,c   Oldfield, Edward H ^a   Merrill, Marsha J ^a,d  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Adenovirus; Blood brain barrier; Brain edema; Inflammation; Major histocompatibility complex; Vascular permeability factor; VEGF

Indexed keywords

VASCULOTROPIN;

ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN EDEMA; IMMUNOMODULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0032991449     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199906000-00006     Document Type: Article

References (64)

1. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983;219:983-5
2. Keck PJ, Hauser SD, Krivi G, et al. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 1989;246: 1309-12
3. Leung DW, Cachianes G, Kuang W-J, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989;246:1306-9
4. Tischer E, Gospodarowicz D, Mitchell R, et al. Vascular endothelial growth factor: A new member of the platelet-derived growth factor gene family. Biochem Biophys Res Commun 1989;165:1198-206
5. 2-terminal amino acid sequence of guinea pig tumor-secreted vascular permeability factor. Cancer Res 1990;50: 1774-8
6. Klagsbrun M, D'Amore PA. Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev 1996;7:259-70
7. Thomas KA. Vascular endothelial growth factor, a potent and selective angiogenic agent. J Biol Chem 1996;271:603-6
8. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997;18:4-25
9. Brown LF, Detmar M, Claffey K, et al. Vascular permeability factor/vascular endothelial growth factor: A multifunctional angiogenic cytokine. Experientia, Suppl 1997;79:233-69
10. DeVries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992;255:989-91
11. Terman BI, Dougher-Vermazen M, Carrion ME, et al. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun 1992;187: 1579-86
12. Millauer B, Wizigmann-Voos S, Schnürch H, et al. High-affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 1993;72: 835-46
13. Quinn TP, Peters KG, DeVries C, Ferrara N, Williams LT. Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc Natl Acad Sci USA 1993;90:7533-7
14. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin C-H. Different signal transduction properties of kdr and flt-1, two receptors for vascular endothelial growth factor. J Biol Chem 1994;269:26988-95
15. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, Marmé D. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 1996;87:3336-43
16. Clauss M, Gerlach M, Gerlach H, et al. Vascular permeability factor: a tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration. J Exp Med 1990;172:1535-45
17. Collins PD, Connolly DT, Williams TJ. Characterization of the increase in vascular permeability induced by vascular permeability factor in vivo. Br J Pharmacol 1993;109:195-9
18. Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Science 1995;108:2369-79
19. Dvorak HF, Sioussat TM, Brown LF, et al. Distribution of vascular permeability factor (vascular endothelial growth factor) in tumors: concentration in tumor blood vessels. J Exp Med 1991;174:1275-78
20. Heiss JD, Papavassiliou E, Merrill MJ, et al. Mechanism of dexamethasone suppression of brain tumor-associated vascular permeability in rats: Involvement of the glucocorticoid receptor and vascular permeability factor. J Clin Invest 1996;98:1400-8
21. Yuan F, Chen Y, Dellian M, Safabakhsh N, Ferrara N, Jain RK. Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc Natl Acad Sci USA 1996;93:14765-70
22. Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res 1997;57:765-72
23. Long DM. Capillary ultrastructure and the blood-brain barrier in human malignant brain tumors. J Neurosurg 1970;32:127-44
24. 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;359:845-8
25. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843-5
26. Berkman RA, Merrill MJ, Reinhold WC, et al. Expression of the vascular permeability factor/vascular endothelial growth factor gene in central nervous system neoplasms. J Clin Invest 1993;91:153-9
27. Takano S, Yoshii Y, Kondo S, et al. Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients. Cancer Res 1996;56:2185-90
28. Dellian M, Witwer BP, Salehi HA, Yuan F, Jain RK. Quantitation and physiological characterization of angiogenic vessels in mice. Am J Pathol 1996;149:59-71
29. Criscuolo GR, Merrill MJ, Oldfield EH. Characterization of a protein product of human malignant glial tumors that induces microvascular permeability. Adv Neurol 1990;52:469-74
30. 189. Proc Natl Acad Sci USA 1997;94:12081-7
31. Kaya M, Chang L, Truong A, Brightman M. Effects of urokinase and vascular endothelial growth factor (VEGF) on brain vessels. Soc Neurosci Abstr 1996;22:53
32. 165 expressed by a replication-deficient recombinant adenovirus vector induces angiogenesis in vivo. Circ Res 1995;77:1077-86
33. Mühlhauser J, Pili R, Merrill MJ, et al. In vivo angiogenesis induced by recombinant adenovirus vectors coding either for secreted or non-secreted forms of acidic fibroblast growth factor. Human Gene Therapy 1995;6:1457-65
34. 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
35. Bondi A, Chieregatti G, Eusebi V, Fulcheri E, Bussolati G. The use of β-galactosidase as a tracer in immunocytochemistry. Histochemistry 1982;76:153-8
36. Akli S, Caillaud C, Vigne E, et al. Transfer of a foreign gene into the brain using adenovirus vectors. Nature Genet 1993;3:224-8
37. 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. Nature Genet 1993;3:219-23
38. 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
39. Blasberg RG, Gazendam J, Patlak CS, Fenstermacher JD. Quantitative autoradiographic studies of brain edema and a comparison of multi-isotope autoradiographic techniques. Adv Neurol 1980;28: 255-73
40. Cheng S-Y, Huang, H-J S, Nagane M, et al. Suppression of glioblastoma angiogenicity and tumorigenicity by inhibition of endogenous expression of vascular endothelial growth factor. Proc Natl Acad Sci USA 1996;93:8502-7
41. Bruce JN, Criscuolo GR, Merrill MJ, Moquin RR, Blacklock JB, Oldfield EH. Vascular permeability induced by protein product of malignant brain tumors: Inhibition by dexamethasone. J Neurosurg 1987;67:880-4
42. Plate KH, Breier G, Millauer B, Ullrich A, Risau W. Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res 1993;53: 5822-7
43. Plate KH, Breier G, Weich HA, Mennel HD, Risau W. Vascular endothelial growth factor and glioma angiogenesis: Coordinate induction of VEGF receptors, distribution of VEGF protein and possible in vivo regulatory mechanisms. Int J Cancer 1994;59:520-9
44. Kremer C, Breier G, Risau W, Plate KH. Up-regulation of flk-1/ vascular endothelial growth factor receptor 2 by its ligand in a cerebral slice culture system. Cancer Res 1997;57:3852-9
45. Barleon B, Siemeister G, Martiny-Baron G, Weindel K, Herzog C, Marmé D. Vascular endothelial growth factor up-regulates its receptor fms-like tyrosine kinase 1 (flt-1) and a soluble variant of flt-1 in human vascular endothelial cells. Cancer Res 1997;57:5421-5
46. Pollack IF, Lund RD. The blood-brain barrier protects foreign antigens in the brain from immune attack. Exp Neurol 1990;108: 114-21
47. Lindsberg PJ, Öhman J, Lehto T, et al. Complement activation in the central nervous system following blood-brain barrier damage in man. Ann Neurol 1996;40:587-96
48. Pedersen EB, McNulty JA, Castro AJ, Fox LM, Zimmer J, Finsen B. Enriched immune-environment of blood-brain barrier deficient areas of normal adult rats. J Neuroimm 1997;76:117-31
49. Wilson C, Kay MA. Immunomodulation to enhance gene therapy. Nat Med 1995;1:887-9
50. Bell MD, Taub DD, Kunkel SJ, et al. Recombinant human adenovirus with rat MIP-2 gene insertion causes prolonged PMN recruitment to the murine brain. Eur J Neurosci 1996;8:1803-11
51. Sobel RA, Mitchell ME, Fondren G. Intercellular adhesion molecule-1 (ICAM-1) in cellular immune reactions in the human central nervous system. Am J Pathol 1990;136:1309-16
52. Melder RJ, Koenig GC, Witwer BP, Safabakhsh N, Munn LL, Jain RK. During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat Med 1996;2:992-7
53. Hart MN, Fabry Z. CNS antigen presentation. Trends Neurosci. 1995;18:475-81
54. Folkman J, Brem H. Angiogenesis and inflammation. In: Gallin JI, Goldstein IM, Snyderman R, eds. Inflammation: Basic principles and clinical correlates. New York: Raven Press,1992:821-39
55. Johnson RT. The virology of demyelinating diseases. Ann Neurol 1994;36:S54-S60
56. Challoner PB, Smith KT, Parker JD, et al. Plaque-associated expression of human herpesvirus 6 in multiple sclerosis. Proc Natl Acad Sci USA 1995;92:7440-4
57. Gladson CL, Cheresh DA. Glioblastoma expression of vitronectin and the αvβ3 integrin adhesion mechanism for transformed glial cells. J Clin Invest 1991;88:1924-32
58. Rosenstein JM, Mani N, Silverman WF, Krum JM. Patterns of brain angiogenesis after vascular endothelial growth factor administration in vitro and in vivo. Proc Natl Acad Sci USA 1998;95:7086-91
59. Banai S, Jaklitsch MT, Shou M, et al. Angiogenic-induced enhancement of collateral blood flow to ischemic myocardium by vascular endothelial growth factor in dogs. Circulation 1994;89:2183-9
60. Pearlman JD, Hibberd MG, Chuang ML, et al. Magnetic resonance mapping demonstrates benefits of VEGF-induced myocardial angiogenesis. Nat Med 1995;1:1085-9
61. 165 in patient with ischaemic limb. Lancet 1996;348:370-4
62. Magovern CJ, Mack CA, Zhang J, Rosengart TK, Isom OW, Crystal RG. Regional angiogenesis induced in nonischemic tissue by an adenoviral vector expressing vascular endothelial growth factor. Hum Gene Ther 1997;8:215-27
63. Bobo RH, Laske DW, Akbasak A, Morrison PF, Dedrick RL, Oldfield EH. Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci USA 1994;91:2076-80
64. Caley DW, Maxwell DS. Development of the blood vessels and extracellular spaces during postnatal maturation of rat cerebral cortex. J Comp Neur 1970;138:31-48