Hypoxia induces angiogenic factors in brain microvascular endothelial cells

Microvascular Research

Volumn 83, Issue 2, 2012, Pages 138-145

  Luo, J ^a   Martinez, J ^a   Yin, X ^a   Sanchez, A ^a   Tripathy, D ^a   Grammas, P ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; THROMBOSPONDIN 2; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BRAIN BLOOD VESSEL; CELL CULTURE; CELL HYPOXIA; CELL VIABILITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANGIOGENIC PROTEINS; ANIMALS; BLOTTING, WESTERN; BRAIN; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIN-1; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HEME OXYGENASE (DECYCLIZING); HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; OXYGEN; PHENOTYPE; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THROMBOSPONDINS; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

RATTUS;

EID: 84856802897     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2011.11.004     Document Type: Article

References (82)

1. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Aird W.C. Endothelial cell heterogeneity. Crit. Care Med. 2003, 31:5221-5230.
3. Bell R.D., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009, 118:103-113.
4. Blanchard K.L., Acquaviva A.M., Galson D.L., Bunn H.F. Hypoxic induction of the human erythropoietin gene: cooperation between the promoter and enhancer, each of which contains steroid receptor response elements. Mol. Cell. Biol. 1992, 12:5373-5385.
5. Boulanger C., Luscher T.F. Release of endothelin from the porcine aorta. Inhibition by endothelium-derived nitric oxide. J. Clin. Invest. 1990, 85:587-590.
6. Bourque S.L., Davidge S.T., Adams M.A. The interaction between endothelin-1 and nitric oxide in the vasculature: new perspectives. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R1288-R1295.
7. Brahimi-Horn M.C., Pouysségur J. HIF at a glance. J. Cell Sci. 2009, 122:1055-1057.
8. Brown W.R., Thore C.R. Review: cerebral microvascular pathology in ageing and neurodegeneration. Neuropathol. Appl. Neurobiol. 2011, 37:56-74.
9. Buee L., Hof P.R., Bouras C., Delacourte A., Perl D.P., Morrison J.H., Fillit H.M. Pathological alterations of the cerebral microvasculature in Alzheimer's disease and related dementing disorders. Acta Neuropathol. 1994, 87:469-480.
10. Buee L., Hof P.R., Delacourte A. Brain microvascular changes in Alzheimer's disease and other dementias. Ann. N. Y. Acad. Sci. 1997, 826:7-24.
11. Chi J.T., Chang H.Y., Haraldsen G., Jahnsen F.L., Troyanskaya O.G., Chang D.S., Wang Z., Rockson S.G., van de Rijn M., Botstein D., Brown P.O. Endothelial cell diversity revealed by global expression profiling. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10623-10628.
12. Closhen D., Bender B., Luhmann H.J., Kuhlmann C.R. CRP-induced levels of oxidative stress are higher in brain than aortic endothelial cells. Cytokine 2010, 50:117-120.
13. Craig L.E., Spelman J.P., Strandberg J.D., Zink M.C. Endothelial cells from diverse tissues exhibit differences in growth and morphology. Microvasc. Res. 1998, 55:65-76.
14. de la Torre J.C. Impaired cerebromicrovascular perfusion. Summary of evidence in support of its causality in Alzheimer's disease. Ann. N. Y. Acad. Sci. 2000, 924:136-152.
15. Desmond D.W., Moroney J.T., Sano M., Stern Y. Incidence of dementia after ischemic stroke: results of a longitudinal study. Stroke 2002, 33:2254-2260.
16. Diglio C.A., Liu W., Grammas P., Giacomelli F., Wiener J. Isolation and characterization of cerebral resistance vessel endothelium in culture. Tissue Cell 1993, 6:833-846.
17. Edelber J.M., Reed M.J. Aging and angiogenesis. Front. Biosci. 2003, 8:s1199-s1209.
18. Enholm B., Paavonen K., Ristimäki A., Kumar V., Gunji Y., Klefstrom J., Kivinen L., Laiho M., Olofsson B., Joukov V., Eriksson U., Alitalo K. Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum growth factors, oncoproteins and hypoxia. Oncogene 1997, 14:2475-2483.
19. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat. Med. 2003, 9:669-676.
20. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 1996, 16:4604-4613.
21. Grammas P. Neurovascular dysfunction, inflammation and endothelial activation: implications for the pathogenesis of Alzheimer's disease. J. Neuroinflammation 2011, 8:26.
22. Grammas P., Ovase R. Inflammatory factors are elevated in brain microvessels in Alzheimer's disease. Neurobiol. Aging 2001, 6:837-842.
23. Grammas P., Ovase R. Cerebrovascular transforming growth factor-beta contributes to inflammation in the Alzheimer's disease brain. Am. J. Pathol. 2002, 5:1583-1587.
24. Grammas P., Samany P.G., Thirumangalakudi L. Thrombin and inflammatory proteins are elevated in Alzheimer's disease microvessels: implications for disease pathogenesis. J. Alzheimers Dis. 2006, 9:51-58.
25. Grammas P., Martinez J., Miller B. Cerebral microvascular endothelium and the pathogenesis of neurodegenerative diseases. Expert Rev. Mol. Med. 2011, 10:e19.
26. Hackett P.H. High altitude cerebral edema and acute mountain sickness: a pathophysiology update. Adv. Exp. Med. Biol. 1999, 474:23-45.
27. Hu J., Discher D.J., Bishopric N.H., Webster K.A. Hypoxia regulates expression of the endothelin-1 gene through a proximal hypoxia-inducible factor-1 binding site on the antisense strand. Biochem. Biophys. Res. Commun. 1998, 245:894-899.
28. Isner J.M. Myocardial gene therapy. Nature 2002, 415:234-239.
29. Kalaria R.N. The role of cerebral ischemia in Alzheimer's disease. Neurobiol. Aging 2000, 21:321-330.
30. Kalaria R.N., Cohen D.L., Premkumar D.R., Nag S., LaManna J.C., Lust W.D. Vascular endothelial growth factor in Alzheimer's disease and experimental ischemia. Brain Res. Mol. Brain Res. 1998, 62:101-105.
31. Kaur C., Ling E.A. Blood brain barrier in hypoxic-ischemic conditions. Curr. Neurovasc. Res. 2008, 5:71-81.
32. Knowles J., Loizidou M., Taylor I. Endothelin-1 and angiogenesis in cancer. Curr. Vasc. Pharmacol. 2005, 3:309-314.
33. Kokmen E., Whisnant J.P., O'Fallon W.M., Chu C.P., Beard C.M. Dementia after ischemic stroke: a population-based study in Rochester, Minnesota (1960-1984). Neurology 1996, 46:154-159.
34. Kourembanas S., Marsden P.A., McQuillan L.P., Faller D.V. Hypoxia induces endothelin gene expression and secretion in cultured human endothelium. J. Clin. Invest. 1991, 88:1054-1057.
35. Laderoute K.R., Alarcon R.M., Brody M.D., Calaoagan J.M., Chen E.Y., Knapp A.M., Yun Z., Denko N.C., Giaccia A.J. Opposing effects of hypoxia on expression of the angiogenic inhibitor thrombospondin 1 and the angiogenic inducer vascular endothelial growth factor. Clin. Cancer Res. 2000, 6:2941-2950.
36. Landau E., Tirosh R., Pinson A., Banai S., Even-Ram S., Maoz M., Katzav S., Bar-Shavit R. Protection of thrombin receptor expression under hypoxia. J. Biol. Chem. 2000, 275:2281-2287.
37. Langenkamp E., Molema G. Microvascular endothelial cell heterogeneity: general concepts and pharmacological consequences for anti-angiogenic therapy of cancer. Cell Tissue Res. 2009, 335:205-222.
38. Lee J.S., Im D.S., An Y.S., Hong J.M., Gwag B.J., Joo I.S. Chronic cerebral hypoperfusion in a mouse model of Alzheimer's disease: an additional contributing factor of cognitive impairment. Neurosci. Lett. 2011, 489:84-88.
39. Liu Y., Cox S.R., Morita T., Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5' enhancer. Circ. Res. 1995, 77:638-643.
40. Loboda A., Jazwa A., Jozkowicz A., Dorosz J., Balla J., Molema G., Dulak J. Atorvastatin prevents hypoxia-induced inhibition of endothelial nitric oxide synthase expression but does not affect heme oxygenase-1 in human microvascular endothelial cells. Atherosclerosis 2006, 187:26-30.
41. Luo J., Grammas P. Endothelin-1 is elevated in Alzheimer's disease brain microvessels and is neuroprotective. J. Alzheimers Dis. 2010, 21:887-896.
42. Madri J.A. Modeling the neurovascular niche: implications for recovery from CNS injury. J. Physiol. Pharmacol. 2009, 60:95-104.
43. McQuillan L.P., Leung G.K., Marsden P.A., Kostyk S.K., Kourembanas S. Hypoxia inhibits expression of eNOS via transcriptional and posttranscriptional mechanisms. Am. J. Physiol. 1994, 267:H1921-H1927.
44. Miklossy J. Cerebral hypoperfusion induces cortical watershed microinfarcts which may further aggravate cognitive decline in Alzheimer's disease. Neurol. Res. 2003, 25:605-610.
45. Molema G. Heterogeneity in endothelial responsiveness to cytokines, molecular causes, and pharmacological consequences. Semin. Thromb. Hemost. 2010, 36:246-264.
46. Moroney J.T., Bagiella E., Desmond D.W., Paik M.C., Stern Y., Tatemichi T.K. Cerebral hypoxia and ischemia in the pathogenesis of dementia after stroke. Ann. N. Y. Acad. Sci. 1997, 826:433-436.
47. Motterlini R., Foresti R., Bassi R., Calabrese V., Clark J.E., Green C.J. Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric-oxide synthase and S-nitrosothiols. J. Biol. Chem. 2000, 275:13613-13620.
48. Nation D.A., Hong S., Jak A.J., Delano-Wood L., Mills P.J., Bondi M.W., Dimsdale J.E. Stress, exercise, and Alzheimer's disease: a neurovascular pathway. Med. Hypotheses 2011, 76:847-854.
49. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999, 13:9-22.
50. Oh H., Takagi H., Suzuma K., Otani A., Matsumura M., Honda Y. Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells. J. Biol. Chem. 1999, 274:15732-15739.
51. Oldendorf W.H., Cornford M.E., Brown W.J. The apparent work capability of the blood-brain barrier: a study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Ann. Neurol. 1977, 1:409-417.
52. Olszewska-Pazdrak B., Hein T.W., Olszewska P., Carney D.H. Chronic hypoxia attenuates VEGF signaling and angiogenic responses by downregulation of KDR in human endothelial cells. Am. J. Physiol. Cell Physiol. 2009, 296:C1162-C1170.
53. Paris D., Ganey N., Banasiak M., Laporte V., Patel N., Mullan M., Murphy S.F., Yee G.T., Bachmeier C., Ganey C., Beaulieu-Abdelahad D., Mathura V.S., Brem S., Mullan M. Impaired orthotopic glioma growth and vascularization in transgenic mouse models of Alzheimer's disease. J. Neurosci. 2010, 30:11251-11258.
54. Peers C., Pearson H.A., Boyle J.P. Hypoxia and Alzheimer's disease. Essays Biochem. 2007, 43:153-164.
55. Peers C., Dallas M.L., Boycott H.E., Scragg J.L., Pearson H.A., Boyle J.P. Hypoxia and neurodegeneration. Ann. N.Y. Acad. Sci. 2009, 1177:169-177.
56. Phelan M.W., Forman L.W., Perrine S.P., Faller D.V. Hypoxia increases thrombospondin-1 transcript and protein in cultured endothelial cells. J. Lab. Clin. Med. 1998, 132:519-529.
57. Pimenta de Castro I., Martins L.M., Tufi R. Mitochondrial quality control and neurological disease: an emerging connection. ERMM 2010, 12:e12.
58. Pogue A.I., Lukiw W.J. Angiogenic signaling in Alzheimer's disease. Neuroreport 2004, 15:1507-1510.
59. Pugh C.W., Ratcliffe P.J. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 2003, 9:677-684.
60. Quaegebeur A., Carmeliet P. Oxygen sensing: a common crossroad in cancer and neurodegeneration. Curr. Top. Microbiol. Immunol. 2010, 345:71-103.
61. Schipper H.M. Heme oxygenase-1: role in brain aging and neurodegeneration. Exp. Gerontol. 2000, 35:821-830.
62. Schipper H.M. Heme oxygenase-1 in Alzheimer's disease: a tribute to Moussa Youdim. J. Neural Transm. 2011, 118:381-387.
63. Schipper H.M., Song W., Zukor H., Hascalovici J.R., Zeligman D. Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement. J. Neurochem. 2009, 110:469-485.
64. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 1999, 15:551-578.
65. Shenberger J.S., Zhang L., Powell R.J., Barchowsky A. Hyperoxia enhances VEGF release from A549 cells via post-transcriptional processes. Free Radic. Biol. Med. 2007, 43:844-852.
66. Strijdom H., Jacobs S., Hattingh S., Page C., Lochner A. Nitric oxide production is higher in rat cardiac microvessel endothelial cells than ventricular cardiomyocytes in baseline and hypoxic conditions: a comparative study. FASEB J. 2006, 20:314-316.
67. Strijdom H., Chamane N., Lochner A. Nitric oxide in the cardiovascular system: a simple molecule with complex actions. Cardiovasc. J. Afr. 2009, 20:303-310.
68. Sun J., Hoshino H., Takaku K., Nakajima O., Muto A., Suzuki H., Tashiro S., Takahashi S., Shibahara S., Alam J., Taketo M.M., Yamamoto M., Igarashi K. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J. 2002, 21:5216-5224.
69. Suzuki M., Iso-o N., Takeshita S., Tsukamoto K., Mori I., Sato T., Ohno M., Nagai R., Ishizaka N. Facilitated angiogenesis induced by heme oxygenase-1 gene transfer in a rat model of hindlimb ischemia. Biochem. Biophys. Res. Commun. 2003, 302:138-143.
70. Tang N., Wang L., Esko J., Giordano F.J., Huang Y., Gerber H.P., Ferrara N., Johnson R.S. Loss of HIF-1 in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 2004, 6:485-495.
71. Tarkowski E., Issa R., Sjogren M., Wallin A., Blennow K., Tarkowski A., Kumar P. Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimer's disease and vascular dementia. Neurobiol. Aging 2002, 23:237-243.
72. Tenan M., Fulci G., Albertoni M., Diserens A.C., Hamou M.F., El Atifi-Borel M., Feige J.J., Pepper M.S., Van Meir E.G. Thrombospondin-1 is downregulated by anoxia and suppresses tumorigenicity of human glioblastoma cells. J. Exp. Med. 2000, 191:1789-1798.
73. Thirumangalakudi L., Samany P.G., Owoso A., Wiskar B., Grammas P. Angiogenic proteins are expressed by brain blood vessels in Alzheimer's disease. J. Alzheimers Dis. 2006, 10:111-118.
74. Tolosa L., Mir M., Asensio V.J., Olmos G., Lladó J. Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase. J. Neurochem. 2008, 105:1080-1090.
75. Tolosa L., Mir M., Olmos G., Lladó J. Vascular endothelial growth factor protects motoneurons from serum deprivation-induced cell death through phosphatidylinositol 3-kinase-mediated p38 mitogen-activated protein kinase inhibition. Neuroscience 2009, 158:1348-1355.
76. Vailhé B., Feige J.J. Thrombospondins as anti-angiogenic therapeutic agents. Curr. Pharm. Des. 2003, 9:583-588.
77. Wick A., Wick W., Waltenberger J., Weller M., Dichgans J., Schulz J.B. Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J. Neurosci. 2002, 22:6401-6407.
78. Wu Z., Guo H., Chow N., Sallstrom J., Bell R.D., Deane R., Brooks A.I., Kanagala S., Rubio M.A., Sagare A., Liu D., Li F., Armstrong D., Gasiewicz T., Zidovetzki R., Song X., Hofman F., Zlokovic B.V. Role of MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat. Med. 2005, 11:959-965.
79. Yamakawa M., Liu L.X., Date T., Belanger A.J., Vincent K.A., Akita G.Y., Kuriyama T., Cheng S.H., Gregory R.J., Jiang C. Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ. Res. 2003, 93:664-673.
80. Yamashita K., Discher D.J., Hu J., Bishopric N.H., Webster K.A. Molecular regulation of the endothelin-1 gene by hypoxia. Contributions of hypoxia-inducible factor-1, activator protein-1, GATA-2, and p300/CBP. J. Biol. Chem. 2001, 276:12645-12653.
81. Yin X., Wright J., Wall T., Grammas P. Brain endothelial cells synthesize neurotoxic thrombin in Alzheimer's disease. Am. J. Pathol. 2010, 176:1600-1606.
82. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.