Increased expression of fibronectin and the α5β1 integrin in angiogenic cerebral blood vessels of mice subject to hypobaric hypoxia

Molecular and Cellular Neuroscience

Volumn 38, Issue 1, 2008, Pages 43-52

  Milner, Richard ^a   Hung, Stephanie ^a   Erokwu, Bernadette ^b   Dore Duffy, Paula ^c   LaManna, Joseph C ^b   del Zoppo, Gregory J ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5 1 integrin; Angiogenesis; Capillary; CNS; Extracellular matrix (ECM); Fibronectin; Hypoxia; MECA 32

Indexed keywords

FIBRONECTIN; VERY LATE ACTIVATION ANTIGEN 5;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN HYPOXIA; CAPILLARY; CONTROLLED STUDY; ENDOTHELIUM CELL; HYPOBARISM; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANOXIA; BRAIN; CEREBROVASCULAR CIRCULATION; FIBRONECTINS; GENE EXPRESSION REGULATION; INTEGRIN ALPHA5BETA1; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC;

MUS;

EID: 43049153372     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.01.013     Document Type: Article

References (70)

1. Bader B., Rayburn H., Crowley D., and Hynes R. Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all alpha v integrins. Cell 95 (1998) 507-519
2. Bello L., Giussani C., Carrabba G., Pluderi M., Costa F., and Bikfalvi A. Angiogenesis and invasion in gliomas. Cancer Treat. Res. 117 (2004) 263-284
3. Campbell I., Abraham C., Masliah E., Kemper P., Inglis J., Oldstone M., and Mucke L. Neurologic disease induced in transgenic mice by the cerebral overexpression of interleukin 6. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 10061-10065
4. Castellani P., Viale G., Dorcaratto A., Nicolo G., Kaczmarek J., Querze G., and Zardi L. The fibronectin isoform containing the ED-B oncofetal domain: a marker of angiogenesis. Int. J. Cancer 59 (1994) 612-618
5. Chavez J.C., Agani F., Pichiule P., and LaManna J.C. Expression of hypoxic inducible factor 1a in the brain of rats during chronic hypoxia. J. Appl. Physiol. 89 (2000) 1937-1942
6. Chen H.H., Chien C.H., and Liu H.M. Correlation between angiogenesis and basic fibroblast growth factor expression in experimental brain infarct. Stroke 25 (1994) 1651-1657
7. Clark R.A.F., DellaPelle P., Manseau E., Lanigan J.M., Dvorak H.F., and Colvin R.B. Blood vessel fibronectin increases in conjunction with endothelial cell proliferation and capillary in growth during wound healing. J. Invest. Dermatol. 79 (1982) 269-276
8. Clark R.A.F., Quinn J.H., Winn H.J., Lanigan J.M., Dellepella P., and Colvin R.B. Fibronectin is produced by blood vessels in response to injury. J. Exp. Med. 156 (1982) 646-651
9. Däpp C., Gassmann M., Hoppeler H., and Flück M. Hypoxia-induced gene activity in disused oxidative muscle. Adv. Exp. Med. Biol. 588 (2006) 171-188
10. Dore-Duffy P., Balabanov R., Beaumont T., Hritz M.A., Harik S.I., and LaManna J.C. Endothelial activation following prolonged hypobaric hypoxia. Microvasc. Res. 57 (1999) 75-85
11. Eliceiri B.P., and Cheresh D. Adhesion events in angiogenesis. Curr. Opin. Cell Biol. 13 (2001) 563-568
12. Engelhardt B., Conley F.K., and Butcher E.C. Cell adhesion molecules on vessels during neuroinflammation in the mouse central nervous system. J. Neuroimmunol. 51 (1994) 199-208
13. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., and Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380 (1996) 439-442
14. Francis S.E., Goh K.L., Hodivala-Dilke K., Bader B.L., Stark M., Davidson D., and Hynes R.O. Central roles of alpha5 beta1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 927-933
15. Garcia J.H., Cox J., and Hudgins W. Ultrastructure of the microvasculature in experimental cerebral infarction. Acta Neuropath. 18 (1971) 273-285
16. George E.L., Georges-Labouesse E.N., Patel-King R.S., Rayburn H., and Hynes R.O. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119 (1993) 1079-1091
17. Hallman R., Mayer D.N., Berg E.L., Broermann R., and Butcher E.C. Novel mouse endothelial cell surface marker is suppressed during differentiation of the blood brain barrier. Dev. Dyn. 202 (1995) 325-332
18. Hayashi T., Noshita N., Sugawara T., and Chan P.H. Temporal profile of angiogenesis and expression of related genes in the brain after ischemia. J. Cereb. Blood Flow Metab. 23 (2003) 166-180
19. Hudlicka O., Milkiewicz M., Cotter M.A., and Brown M.D. Hypoxia and expression of VEGF-A protein in relation to capillary growth in electrically stimulated rat and rabbit skeletal muscles. Exp. Physiol. 87 (2002) 373-381
20. Iivanainen E., Kahari V.-M., Heino J., and Elenius K. Endothelial cell-matrix interactions. Microsc. Res. Tech. 60 (2003) 13-22
21. Ingber D. Extracellular matrix as a solid-state regulator in angiogenesis: identification of new targets for anti-cancer therapy. Semin. Cancer Biol. 3 (1992) 57-63
22. Ingber D., and Folkman J. Inhibition of angiogenesis through modulation of collagen metabolism. Lab. Invest. 59 (1988) 44-51
23. Jansen M., de Witt Hamer P.C., Witmer A.N., Troost D., and van Noorden C.J.F. Current perspectives on antiangiogenic strategies in the treatment of malignant gliomas. Brain Res. Rev. 45 (2004) 143-163
24. Jiang B., Liou G.I., Behzadian M.A., and Caldwell R.B. Astrocytes modulate retinal vasculogenesis: effects on fibronectin expression. J. Cell Sci. 107 (1994) 2499-2508
25. Kanaan A., Farahani R., Douglas R.M., LaManna J.C., and Haddad G.C. Effect of chronic continuous or intermittent hypoxia and reoxygenation on cerebral capillary density and myelination. Am. J. Physiol., Regul. Integr. Comp. Physiol. 290 (2006) R1105-R1114
26. Kim S., Bell K., Mousa S.A., and Varner J.A. Regulation of angiogenesis in vivo by ligation of integrin a5b1 with the central cell-binding domain of fibronectin. Am. J. Pathol. 156 (2000) 1345-1362
27. Kim S., Harris M., and Varner J.A. Regulation of avb3-mediated endothelial cell migration and angiogenesis by integrin a5b1 and protein kinase A. J. Biol. Chem. 275 (2000) 33920-33928
28. Kirkpatrick C.J., Kampe M., Rixen H., Fischer E.G., Ruchatz D., and Mittermayer C. In vitro studies on the expansion of endothelial cell monolayers on components of the basement membrane. Virchows Arch. B. Cell Pathol. Incl. Mol. Pathol. 58 (1990) 207-213
29. Klein S., Roghani M., and Rifkin D.B. Fibroblast growth factors as angiogenesis factors. EXS 79 (1997) 159-192
30. Krupinski J., Kaluza J., Kumar P., Kumar S., and Wang J.M. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 25 (1994) 1794-1798
31. Krupinski J., Kumar P., Kumar S., and Kaluza J. Increased expression of TGF-β1 in brain tissue after ischemic stroke in humans. Stroke 27 (1996) 852-857
32. Kuo N.-T., Benhayon D., Przybylski R.J., Martin R.J., and LaManna J.C. Prolonged hypoxia increases vascular endothelial growth factor mRNA and protein in adult mouse brain. J. Appl. Physiol. 86 (1999) 260-264
33. LaManna J.C., Vendel L.M., and Farrell R.M. Brain adaptation to chronic hypobaric hypoxia in rats. J. Appl. Physiol. 72 (1992) 2238-2243
34. LaManna J.C., Kuo N.T., and Lust W.D. Hypoxia-induced brain angiogenesis. Signals and consequences. Adv. Exp. Med. Biol. 454 (1998) 287-293
35. LaManna J.C., Chavez J.C., and Pichiule P. Structural and functional adaptation to hypoxia in the rat brain. J. Exp. Biol. 207 (2004) 3163-3169
36. Lehrman E., Kiefer R., Christensen T., Toyka K.V., Zimmer J., Diemer N.H., Hartung H.-P., and Finsen B. Microglia and macrophages are major sources of locally produced transforming growth factor-beta 1 after transient middle cerebral artery occlusion in rats. Glia 24 (1998) 437-448
37. Lin T.N., Sun S.W., Cheung W.M., and Chang C. Dynamic changes in cerebral blood flow and angiogenesis after transient focal cerebral ischemia in rats. Evaluation with serial magnetic resonance imaging. Stroke 33 (2002) 2985-2991
38. Madri J.A., Bell L., and Merwin J.R. Modulation of vascular cell behavior by transforming growth factors beta. Mol. Reprod. Dev. 32 (1992) 121-126
39. Maisonpierre P.C., Suri C., Jones P.F., Bartunkova S., Wiegand S.J., Radziejewski C., Compton D.L., McClain J., Aldrich T.H., Papadopoulos N., Daly T.J., Davis S., Sato T.N., and Yancopoulos G.D. Angiopoietin-2, a natural antagonist for Tie-2 that disrupts in vivo angiogenesis. Science 277 (1997) 55-60
40. Marin-Padilla M. Early vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies. J. Comp. Neurol. 241 (1985) 237-249
41. McIntosh L.C., Muckersie L., and Forrester J.V. Retinal capillary endothelial cells prefer different substrates for growth and migration. Tissue Cell 20 (1988) 193-209
42. Millauer B., Wizigmann-Voos S., Schnurch H., Martinez R., Moller N.P., Risau W., and Ulrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72 (1993) 835-846
43. Milner R., and Campbell I.L. Developmental regulation of b1 integrins during angiogenesis in the central nervous system. Mol. Cell. Neurosci. 20 (2002) 616-626
44. Milner R., and Campbell I.L. Increased expression of the beta 4 and alpha 5 integrin subunits in cerebral blood vessels of transgenic mice chronically producing the pro-inflammatory cytokines IL-6 or IFN-alpha in the central nervous system. Mol. Cell. Neurosci. 33 (2006) 429-440
45. Milner R., Crocker S.J., Hung S., Wang X., Frausto R.F., and Del Zoppo G.J. Fibronectin- and vitronectin-induced microglial activation and matrix metalloproteinase-9 expression is mediated by integrins α5β1 and αvβ5. J. Immunol. 178 (2007) 8158-8167
46. Milner R., Hung S., Wang X., Berg G., Spatz M., and del Zoppo G. Responses of endothelial cell and astrocyte matrix-integrin receptors to ischemia mimic those observed in the neurovascular unit. Stroke 39 (2007) 191-197
47. Neri D., Camemolla B., Nissim A., Leprini A., Querze G., Balza E., Pini A., Tarli L., Halin C., Neri P., Zardi L., and Winer G. Targeting by affinity-matured recombinant fragments of an angiogenesis associated fibronectin isoform. Nat. Biotechnol. 15 (1997) 1271-1275
48. Pichiule P., and LaManna J.C. Angiopoietin-2 and rat brain capillary remodeling during adaptation and de-adaptation to prolonged mild hypoxia. J. Appl. Physiol. 93 (2002) 1131-1139
49. Plate K.H. Mechanisms of angiogenesis in the brain. J. Neuropathol. Exp. Neurol. 58 (1999) 313-320
50. Plate K.H., Breier G., and Risau W. Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathol. 4 (1994) 207-218
51. Plate K.H., and Risau W. Angiogenesis in malignant gliomas. Glia 15 (1995) 339-347
52. Risau W., and Lemmon V. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev. Biol. 125 (1988) 441-450
53. Roberts A.B., Sporn M.B., Assoian R.K., Smith J.M., Roche N.S., Wakefield U., Heine I., Liotta A., Falanga J., Kehrl J.H., and Fauci A.S. Transforming growth factor type β: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 4167-4171
54. Rothbart D., Awad I.A., Lee J., Kim J., Harbaugh R., and Criscuolo G.R. Expression of angiogenic factors and structural proteins in central nervous system vascular malformations. Neurosurgery 38 (1996) 915-924
55. Ruocco A., Nicole O., Docagne F., Ali C., Chazaliel L., Komelski S., Yablonsky F., Roussel S., MacKenzie E.T., Vivien D., and Buisson A. A transforming growth factor-beta antagonist unmasks the neuroprotective role of this cytokine in excitotoxic and ischemic brain injury. J. Cereb. Blood Flow Metab. 19 (1999) 1345-1353
56. Sasaki H., Ray P.S., Zhu L., Otani H., Asahara T., and Maulik N. Hypoxia/reoxygenation promotes myocardial angiogenesis via an NF kappa B-dependent mechanism in a rat model of chronic myocardial infarction. J. Mol. Cell. Cardiol. 33 (2001) 283-294
57. Sasaki H., Fukuda S., Otani H., Zhu L., Yamaura G., Engelman R.M., Das D.K., and Maulik N. Hypoxic preconditioning triggers myocardial angiogenesis: a novel approach to enhance contractile functional reserve in rat with myocardial infarction. J. Mol. Cell. Cardiol. 34 (2002) 335-348
58. Sato T.N., Tozawa Y., Deutsch U., Wolburg-Buchholz K., Fujiwara Y., Gendron-Maguire M., Gridley T., Wolburg H., Risau W., and Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376 (1995) 70-74
59. Sparks D.L., Kuo Y.M., Roher A., Martin T., and Lukas R.J. Alterations of Alzheimer's disease in the cholesterol-fed rabbit, including vascular inflammation. Preliminary observations. Ann. N.Y. Acad. Sci. 903 (2000) 335-344
60. Stromblad S., and Cheresh D.A. Integrins, angiogenesis and vascular cell survival. Chem. Biol. 3 (1996) 881-885
61. Stupack D.G., and Cheresh D. Apoptotic cues from the extracellular matrix: regulators of angiogenesis. Oncogene 22 (2003) 9022-9029
62. Taverna D., and Hynes R.O. Reduced blood vessel formation and tumor growth in alpha5-integrin-negative teratocarcinomas and embryoid bodies. Cancer Res. 61 (2001) 5255-5261
63. Tonnesen M.G., Jenkins D., Siegal S.L., Lee L.A., Huff J.C., and Clark R.A. Expression of fibronectin, laminin, and factor VIII-related antigen during development of the human cutaneous microvasculature. J. Invest. Dermatol. 85 (1985) 564-568
64. Uranashi R., Baev N.I., Ng P.Y., Kim J.H., and Awad I.A. Expression of endothelial cell angiogenesis receptors in human cerebrovascular malformations. Neurosurgery 48 (2001) 359-367
65. Wang J., and Milner R. Fibronectin promotes brain capillary endothelial cell survival and proliferation through a5b1 and avb3 integrins via MAP kinase signaling. J. Neurochem. 96 (2006) 148-159
66. Wang L., Zhang Z., Wang Y., Zhang R., and Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35 (2004) 1732-1737
67. Wei L., Erinjeri J.P., Rovainen C.M., and Woolsey T.A. Collateral growth and angiogenesis around cortical stroke. Stroke 32 (2001) 2179-2184
68. Yang J.T., Rayburn H., and Hynes R.O. Embryonic mesodermal defects in a5 integrin-deficient mice. Development 119 (1993) 1093-1105
69. Yang J.T., Rayburn H., and Hynes R.O. Cell adhesion events mediated by α4 integrins are essential in placental and cardiac development. Development 121 (1995) 549-560
70. Zhu J., Motejlek K., Wang D., Zang K., Scmidt A., and Reichardt L.F. β8 integrins are required for vascular morphogenesis in mouse embryos. Development 129 (2002) 2891-2903