Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats

Journal of Neuropathology and Experimental Neurology

Volumn 61, Issue 10, 2002, Pages 914-925

  Proescholdt, Martin A ^a   Jacobson, Steven ^a   Tresser, Nancy ^a   Oldfield, Edward H ^a   Merrill, Marsha J ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Astrocytes; Experimental allergic encephalomyelitis (EAE); Multiple sclerosis; Neuroinflammation; Vascular endothelial growth factor (VEGF); Vascular permeability factor

Indexed keywords

CELL ADHESION MOLECULE; MYELIN BASIC PROTEIN; VASCULOTROPIN;

ALLERGIC ENCEPHALITIS; ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; AUTOIMMUNE DISEASE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; CAPILLARY ENDOTHELIUM; CELL MIGRATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GROWTH REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFLAMMATION; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WHITE MATTER;

EID: 0036794017     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/61.10.914     Document Type: Article

References (77)

1. Compston A. Multiple sclerosis. In: Walton J, ed. Brain diseases of the nervous system. 10th Ed. Oxford, New York, Tokyo: Oxford University Press, 1993:366-82
2. Adams RD, Victor M, Ropper AH. Multiple sclerosis and allied demyelinative diseases. Principles of neurology. New York, St. Louis, San Francisco: McGraw Hill, 1997:902-27
3. Richardson EP, Jr. Pathology of multiple sclerosis: Some new developments, Clin Neurosci 1994;2:253-57
4. Prineas JW, McDonald J. Multiple sclerosis. In: Graham DI, Lantos PL, eds. Greenfield's neuropathology. 6th Ed. Vol. 1. London, Sydney, Auckland: Arnold, 1997:815-68
5. Ffrench-Constant C. Pathogenesis of multiple sclerosis. Lancet 1994;343:271-75
6. Poser CM. The role of trauma in the pathogenesis of multiple sclerosis: A review. Clin Neurol Neurosurg 1994;96:103-10
7. Gay D, Esiri M. Blood-brain barrier damage in acute multiple sclerosis plaques. An immunocytological study. Brain 1991;114:557-72
8. Rindfleisch E. Histologische Details zu der grauen Degeneration von Gehirn und Rückenmark. Virchow's Archiv für Pathologische Anatomie und Physiologie und für klinische Medizin 1863;26:474-83
9. Broman T. Supravital analysis of disorders in the cerebral vascular permeability II. Two cases of multiple sclerosis. Acta Psychiatr Neurol Scand (Suppl) 1947;46:58-71
10. Kermode AG, Thompson AJ, Tofts P, et al. Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Brain 1990;113:1477-89
11. Stone LA, Smith ME, Albert PS, et al. Blood-brain barrier disruption on contrast-enhanced MRI in patients with mild relapsing-remitting multiple sclerosis: Relationship to course, gender, and age. Neurology 1995;45:1122-26
12. Thorpe JW, Kidd D, Moseley IF, et al. Serial gadolinium-enhanced MRI of the brain and spinal cord in early relapsing-remitting multiple sclerosis. Neurology 1996;46:373-78
13. McLean BN, Zeman AZ, Barnes D, Thompson EJ. Patterns of blood-brain barrier impairment and clinical features in multiple sclerosis. J Neurol Neurosurg Psychiatry 1993;56:356-60
14. Kwon EE, Prineas JW. Blood-brain barrier abnormalities in longstanding multiple sclerosis lesions. An immunohistochemical study. J Neuropathol Exp Neurol 1994;53:625-36
15. Brown W. The capillaries in acute and subacute multiple sclerosis plaques: A morphometric analysis. Neurology 1978;28:84-92
16. Claudio L, Raine CS, Brosnan CF. Evidence of persistent blood-brain barrier abnormalities in chronic-progressive multiple sclerosis. Acta Neuropathol (Berl) 1995;90:228-38
17. Daniel PM, Lam DK, Pratt OE. Changes in the effectiveness of the blood-brain and blood-spinal cord barriers in experimental allergic encephalomyelitis. J Neurol Sci 1981;52:211-19
18. Juhler M, Barry DI, Offner H, Konat G, Klinken L, Paulson OB. Blood-brain and blood-spinal cord barrier permeability during the course of experimental allergic encephalomyelitis in the rat. Brain Res 1984;302:347-55
19. Zlokovic BV, Skundric DS, Segal MB, et al. Blood-brain barrier permeability changes during acute allergic encephalomyelitis induced in the guinea pig. Metab Brain Dis 1989;4:33-40
20. Hawkins CP, Mackenzie F, Tofts P, du Boulay EP, McDonald WI. Patterns of blood-brain barrier breakdown in inflammatory demyelination. Brain 1991;114:801-10
21. Claudio L, Kress Y, Norton WT, Brosnan CF. Increased vesicular transport and decreased mitochondrial content in blood-brain barrier endothelial cells during experimental autoimmune encephalomyelitis. Am J Pathol 1989;135:1157-68
22. Moor AC, de Vries HE, de Boer AG, Breimer DD. The blood-brain barrier and multiple sclerosis. Biochem Pharmacol 1994;47:1717-24
23. Abbott NJ. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol Neurobiol 2000;20:131-47
24. 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;219:983-85
25. 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
26. Clauss M. Molecular biology of the VEGF and the VEGF receptor family. Semin Thromb Hemost 2000;26:561-69
27. Ferrara N. Vascular endothelial growth factor: Molecular and biological aspects. Curr Top Microbiol Immunol 1999;237:1-30
28. Thomas KA. Vascular endothelial growth factor, a potent and selective angiogenic agent. J Biol Chem 1996;271:603-6
29. 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
30. Hatva E, Kaipainen A, Mentula P, et al. Expression of endothelial cell-specific receptor tyrosine kinases and growth factors in human brain tumors. Am J Pathol 1995;146:368-78
31. 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
32. Alvarez JA, Baird A, Tatum A, et al. Localization of basic fibroblast growth factor and vascular endothelial growth factor in human glial neoplasms. Mod Pathol 1992;5:303-7
33. Monacci WT, Merrill MJ, Oldfield EH. Expression of vascular permeability factor/vascular endothelial growth factor in normal rat tissues. Am J Physiol 1993;264:C995-C1002
34. Papavassiliou E, Gogate N, Proescholdt MA, et al. Vascular endothelial growth factor (vascular permeability factor) expression in injured rat brain. J Neurosci Res 1997;49:451-60
35. Kovacs Z, Ikezaki K, Samoto K, Inamura T, Fukui M. VEGF and flt: Expression time kinetics in rat brain infarct. Stroke 1996;27: 1865-73
36. Krum JM, Rosenstein JM. Transient coexpression of nestin, GFAP, and vascular endothelial growth factor in mature reactive astroglia following neural grafting or brain wounds. Exp Neurol 1999;160: 348-60
37. 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;91:153-59
38. 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
39. 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;59:520-29
40. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843-45
41. Machein MR, Plate KH, VEGF in brain tumors. J Neuro-Oncol 2000;50:109-20
42. 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
43. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, Marme 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
44. Koch AE, Harlow LA, Haines GK, et al. Vascular endothelial growth factor. A cytokine modulating endothelial function in rheumatoid arthritis. J Immunol 1994;152:4149-56
45. Brown LF, Yeo KT, Berse B, et al. Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J Exp Med 1992;176:1375-79
46. 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
47. Dvorak HF, Detmar M, Claffey KP, Nagy JA, van de Water L, Senger DR. Vascular permeability factor/vascular endothelial growth factor: An important mediator of angiogenesis in malignancy and inflammation. Int Arch Allergy Immunol 1995;107:233-35
48. 165 expressed by a replication-deficient recombinant adenovirus vector induces angiogenesis in vivo. Circ Res 1995;77:1077-86
49. Wilkinson DG. The theory and practice of in situ hybridization. In: Wilkinson D, ed. In situ hybridization: A practical approach, Vol. 1. Oxford, New York, Tokyo: Oxford University Press, 1992:1-13
50. Goverman J, Brabb T. Rodent models of experimental allergic encephalomyelitis applied to the study of multiple sclerosis. Lab Anim Sci 1996;46:482-92
51. Koh C-S, Gausas J, Paterson PY. Concordance and localization of maximal vascular permeability change, and fibrin deposition in the central neuraxis of Lewis rats with cell-transferred experimental allergic encephalomyelitis. J Neuroimmunol 1992;38:85-93
52. Swanborg RH. Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clin Immunol Immunopathol 1995;77:4-13
53. Morrison PF. Distributed models of drug kinetics. In: Atkinson AJ, ed. Principles of clinical pharmacology. San Diego: Academic Press, 2001:93-112
54. Redgate ES, Deutsch M, Boggs SS. Time of death of CNS tumorbearing rats can be reliably predicted by body weight-loss patterns. Lab Anim Sci 1991;41:269-73
55. Collins PD, Connolly DT, Williams TJ. Characterization of the increase in vascular permeability induced by vascular permeability factor in vivo. Br J Pharmacol 1993;109:195-99
56. Bates DO, Lodwick D, Williams B. Vascular endothelial growth factor and microvascular permeability. Microcirculation 1999;6:83-96
57. 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;98:1400-1408
58. Strugar JG, Rothbart D, Harrington W, Criscuolo GR. Vascular permeability factor in brain metastases: Correlation with vasogenic brain edema and tumor angiogenesis. J Neurosurg 1994;81:560-66
59. Poser CM. Notes on the pathogenesis of multiple sclerosis. Clin Neurosci 1994;2:258-65
60. Namer IJ, Steibel J, Poulet P, et al. Blood-brain barrier breakdown in MBP-specific T cell induced experimental allergic encephalomyelitis. A quantitative in vivo MRI study, Brain 1993;116: 147-59
61. Juhler M, Blasberg RG, Fenstermacher JD, Patlak CS, Paulson OB. A spatial analysis of the blood-brain barrier damage in experimental allergic encephalomyelitis. J Cereb Blood Flow Metab 1985;5: 545-53
62. Lindsberg PJ, Ohman 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
63. Graeber MB. Microglia, macrophages and the blood-brain barrier. Clin Neuropathol 1993;12:296-97
64. Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci 1995;108:2369-79
65. Feng D, Nagy JA, Hipp J, Dvorak HF, Dvorak AM. Vesiculo-vacuolar organelles and the regulation of venule permeability to macromolecules by vascular permeability factor, histamine, and serotonin. J Exp Med 1996;183:1981-86
66. Dobrogowska DH, Lossinsky AS, Tarnawski M, Vorbrodt AW. Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J Neurocytol 1998;27:163-73
67. Ferrara N. Natural killer cells, adhesion and tumor angiogenesis. Nat Med 1996;2:971-72
68. 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;2:992-97
69. 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
70. Wilcox CE, Ward AM, Evans A, Baker D, Rothlein R, Turk JL. Endothelial cell expression of the intercellular adhesion molecule1 (ICAM-1) in the central nervous system of guinea pigs during acute and chronic relapsing experimental allergic encephalomyelitis. J Neuroimmunol 1990;30:43-51
71. Archelos JJ, Previtali SC, Hartung HP. The role of integrins in immune-mediated diseases of the nervous system. Trends Neurosci 1999;22:30-38
72. Erälinna JP. Soilu-Hänninen M, Röyttä M, Hukkanen V, Salmi AA, Salonen R. Blood-brain barrier breakdown and increased intercellular adhesion molecule (ICAM-1/CD54) expression after Semliki Forest (A7) virus infection facilitates the development of experimental allergic encephalomyelitis. J Neuroimmunol 1996;66:103-14
73. Boyle EA, McGeer PL. Cellular immune response in multiple sclerosis plaques. Am J Pathol 1990;137:575-84
74. Williams KC, Ulvestad E, Hickey WF. Immunology of multiple sclerosis. Clin Neurosci 1994;2:229-45
75. Connolly DT, Heuvelman DM, Nelson R, et al. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest 1989;84:1470-78
76. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989;246:1306-9
77. Gospodarowicz D, Abraham JA, Schilling J. Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo stellate cells. Proc Natl Acad Sci U S A 1989;86:7311-15