Pathophysiological response to hypoxia - From the molecular mechanisms of malady to drug discovery: Inflammatory responses of hypoxia-inducible factor 1α (HIF-1α) in T cells observed in development of vascular remodeling

Journal of Pharmacological Sciences

Volumn 115, Issue 4, 2011, Pages 433-439

  Tomita, Shuhei ^a   Kihira, Yoshitaka ^a   Imanishi, Masaki ^a   Fukuhara, Yayoi ^a   Imamura, Yuko ^a   Ishizawa, Keisuke ^a   Ikeda, Yasumasa ^a   Tsuchiya, Koichiro ^a   Tamaki, Toshiaki ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Arteriosclerosis; Hypoxia; Hypoxia inducible factor 1 (HIF 1 ); T cell; Vascular remodeling

Indexed keywords

GAMMA INTERFERON; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; INTERLEUKIN 1; INTERLEUKIN 2; REACTIVE OXYGEN METABOLITE;

ADAPTIVE IMMUNITY; ANGIOGENESIS; ANTIBODY PRODUCTION; ARTERIOSCLEROSIS; B LYMPHOCYTE ACTIVATION; BLOOD VESSEL INJURY; CELL HYPOXIA; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE COURSE; EXTRACELLULAR MATRIX; GENE DISRUPTION; GENE EXPRESSION REGULATION; HUMAN; MICROENVIRONMENT; NONHUMAN; OXYGEN CONCENTRATION; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SHORT SURVEY; T LYMPHOCYTE ACTIVATION; VASCULITIS;

EID: 79955046642     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.10R22FM     Document Type: Short Survey

References (80)

1. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda). 2004;19:176-182. (Pubitemid 39481932)
2. Chen EY, Fujinaga M, Giaccia AJ. Hypoxic microenvironment within an embryo induces apoptosis and is essential for proper morphological development. Teratology. 1999;60:215-225. (Pubitemid 29478910)
3. Krishnan J, Ahuja P, Bodenmann S, Knapik D, Perriard E, Krek W, et al. Essential role of developmentally activated hypoxia-inducible factor 1alpha for cardiac morphogenesis and function. Circ Res. 2008;103:1139-1146.
4. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, Chan-Ling T, et al. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci. 1995;15:4738-4747.
5. Wikenheiser J, Doughman YQ, Fisher SA, Watanabe M. Differential levels of tissue hypoxia in the developing chicken heart. Dev Dyn. 2006;235:115-123. (Pubitemid 46939708)
6. Xu B, Doughman Y, Turakhia M, Jiang W, Landsettle CE, Agani FH, et al. Partial rescue of defects in Cited2-deficient embryos by HIF-1alpha heterozygosity. Dev Biol. 2007;301:130-140. (Pubitemid 46001381)
7. Semenza GL. Oxygen homeostasis. Wiley Interdisciplinary Reviews: Systems Biology and Medicine. 2009;2:336-361.
8. Poellinger L, Johnson RS. HIF-1 and hypoxic response: the plot thickens. Curr Opin Genet Dev. 2004;14:81-85. (Pubitemid 38167481)
9. Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A. 1993;90:4304-4308. (Pubitemid 23134215)
10. Semenza GL. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda). 2009;24:97-106.
11. Semenza GL. Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis. Blood. 2009;114:2015-2019.
12. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008; 30:393-402. (Pubitemid 351681994)
13. Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, Conaway JW. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci U S A. 2000;97:10430-10435.
14. Salceda S, Caro J. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem. 1997;272:22642-22647. (Pubitemid 27386079)
15. Mahon PC, Hirota K, Semenza GL. FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 2001;15:2675-2686. (Pubitemid 32988878)
16. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 2002;16:1466-1471. (Pubitemid 34686328)
17. Sandau KB, Zhou J, Kietzmann T, Brune B. Regulation of the hypoxia-inducible factor 1alpha by the inflammatory mediators nitric oxide and tumor necrosis factor-alpha in contrast to desferroxamine and phenylarsine oxide. J Biol Chem. 2001;276: 39805-39811.
18. Richard DE, Berra E, Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem. 2000;275:26765-26771.
19. Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Burgel T. Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett. 2002;512:157-162. (Pubitemid 34164471)
20. Treins C, Giorgetti-Peraldi S, Murdaca J, Semenza GL, Van Obberghen E. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem. 2002;277:27975-27981. (Pubitemid 34966746)
21. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 1998;12: 149-162. (Pubitemid 28060446)
22. Ryan HE, Lo J, Johnson RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. Embo J. 1998; 17:3005-3015. (Pubitemid 28254373)
23. Compernolle V, Brusselmans K, Franco D, Moorman A, Dewerchin M, Collen D, et al. Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1alpha. Cardiovasc Res. 2003; 60:569-579. (Pubitemid 37501114)
24. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 2000;60:4010-4015. (Pubitemid 30636574)
25. Tomita S, Ueno M, Sakamoto M, Kitahama Y, Ueki M, Maekawa N, et al. Defective brain development in mice lacking the Hif-1alpha gene in neural cells. Mol Cell Biol. 2003;23:6739-6749. (Pubitemid 37214645)
26. Pouyssegur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature. 2006; 441:437-443. (Pubitemid 44050138)
27. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. 2003;9:677-684. (Pubitemid 36749216)
28. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3:721-732. (Pubitemid 37328811)
29. Bjornheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol. 1999;19:870-876. (Pubitemid 29177331)
30. Jurrus ER, Weiss HS. In vitro tissue oxygen tensions in the rabbit aortic arch. Atherosclerosis. 1977;28:223-232.
31. Zemplenyi T, Crawford DW, Cole MA. Adaptation to arterial wall hypoxia demonstrated in vivo with oxygen microcathodes. Atherosclerosis. 1989;76:173-179. (Pubitemid 19101037)
32. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol. 2005;175: 6257-6263. (Pubitemid 41598863)
33. Torres Filho IP, Leunig M, Yuan F, Intaglietta M, Jain RK. Noninvasive measurement of microvascular and interstitial oxygen profiles in a human tumor in SCID mice. Proc Natl Acad Sci U S A. 1994;91:2081-2085. (Pubitemid 24092046)
34. Sluimer JC, Daemen MJ. Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. J Pathol. 2009;218: 7-29.
35. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645-657. (Pubitemid 36331777)
36. Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, et al. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol. 2003;163:1233-1243. (Pubitemid 37175073)
37. Negus RP, Turner L, Burke F, Balkwill FR. Hypoxia down-regulates MCP-1 expression: implications for macrophage distribution in tumors. J Leukoc Biol. 1998;63:758-765. (Pubitemid 28274839)
38. Lobanova EM, Tahanovich AD. Hydrogen peroxide metabolism in alveolar macrophages after exposure to hypoxia and heat. Physiol Res. 2006;55:569-575. (Pubitemid 44611202)
39. Bostrom P, Magnusson B, Svensson PA, Wiklund O, Boren J, Carlsson LM, et al. Hypoxia converts human macrophages into triglyceride-loaded foam cells. Arterioscler Thromb Vasc Biol. 2006;26:1871-1876. (Pubitemid 44305343)
40. Lattimore JD, Wilcox I, Nakhla S, Langenfeld M, Jessup W, Celermajer DS. Repetitive hypoxia increases lipid loading in human macrophages-a potentially atherogenic effect. Atherosclerosis. 2005;179:255-259. (Pubitemid 40364618)
41. Rydberg EK, Krettek A, Ullstrom C, Ekstrom K, Svensson PA, Carlsson LM, et al. Hypoxia increases LDL oxidation and expression of 15-lipoxygenase-2 in human macrophages. Arterioscler Thromb Vasc Biol. 2004;24:2040-2045. (Pubitemid 39482427)
42. Nozik-Grayck E, Stenmark KR. Role of reactive oxygen species in chronic hypoxia-induced pulmonary hypertension and vascular remodeling. Adv Exp Med Biol. 2007;618:101-112.
43. White CW. Commentary on "Hypoxia, hypoxic signaling, tissue damage, and detection of reactive oxygen species (ROS)". Free Radic Biol Med. 2006;40:923-927.
44. Kelley EE, Hock T, Khoo NK, Richardson GR, Johnson KK, Powell PC, et al. Moderate hypoxia induces xanthine oxidoreductase activity in arterial endothelial cells. Free Radic Biol Med. 2006;40:952-959. (Pubitemid 43376004)
45. Paddenberg R, Ishaq B, Goldenberg A, Faulhammer P, Rose F, Weissmann N, et al. Essential role of complex II of the respiratory chain in hypoxia-induced ROS generation in the pulmonary vasculature. Am J Physiol Lung Cell Mol Physiol. 2003;284: L710-L719. (Pubitemid 36459016)
46. Lau AK, Chaufour X, McLachlan C, Leichtweis SB, Celermajer DS, Sullivan C, et al. Intimal thickening after arterial balloon injury is increased by intermittent repetitive hypoxia, but intermittent repetitive hyperoxia is not protective. Atherosclerosis. 2006; 185:254-263.
47. Nakano D, Hayashi T, Tazawa N, Yamashita C, Inamoto S, Okuda N, et al. Chronic hypoxia accelerates the progression of atherosclerosis in apolipoprotein E-knockout mice. Hypertens Res. 2005;28:837-845. (Pubitemid 47400254)
48. Dimayuga P, Cercek B, Oguchi S, Fredrikson GN, Yano J, Shah PK, et al. Inhibitory effect on arterial injury-induced neointimal formation by adoptive B-cell transfer in Rag-1 knockout mice. Arterioscler Thromb Vasc Biol. 2002;22:644-649. (Pubitemid 34408747)
49. Dimayuga PC, Li H, Chyu KY, Fredrikson GN, Nilsson J, Fishbein MC, et al. T cell modulation of intimal thickening after vascular injury: the bimodal role of IFN-gamma in immune deficiency. Arterioscler Thromb Vasc Biol. 2005;25:2528-2534. (Pubitemid 43732274)
50. Hansson GK, Holm J, Holm S, Fotev Z, Hedrich HJ, Fingerle J. T lymphocytes inhibit the vascular response to injury. Proc Natl Acad Sci U S A. 1991;88:10530-10534. (Pubitemid 21915869)
51. Remskar M, Li H, Chyu KY, Shah PK, Cercek B. Absence of CD40 signaling is associated with an increase in intimal thickening after arterial injury. Circ Res. 2001;88:390-394. (Pubitemid 32200111)
52. Zhu B, Reardon CA, Getz GS, Hui DY. Both apolipoprotein E and immune deficiency exacerbate neointimal hyperplasia after vascular injury in mice. Arterioscler Thromb Vasc Biol. 2002; 22:450-455. (Pubitemid 34218753)
53. Shi Y, Zheng W, Rock KL. Cell injury releases endogenous adjuvants that stimulate cytotoxic T cell responses. Proc Natl Acad Sci U S A. 2000;97:14590-14595. (Pubitemid 32016620)
54. Wallin RP, Lundqvist A, More SH, von Bonin A, Kiessling R, Ljunggren HG. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 2002;23:130-135. (Pubitemid 34178294)
55. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007;81:1-5. (Pubitemid 46028489)
56. Dimayuga PC, Chyu KY, Cercek B. Immune responses regulating the response to vascular injury. Curr Opin Lipidol. 2010; 21:416-421.
57. Mitchell RN, Libby P. Vascular remodeling in transplant vasculopathy. Circ Res. 2007;100:967-978. (Pubitemid 46598921)
58. Schiffrin EL. T lymphocytes: a role in hypertension? Curr Opin Nephrol Hypertens. 2010;19:181-186.
59. Munder M, Mallo M, Eichmann K, Modolell M. Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: A novel pathway of autocrine macrophage activation. J Exp Med. 1998;187:2103-2108. (Pubitemid 28285581)
60. Gerdes N, Sukhova GK, Libby P, Reynolds RS, Young JL, Schonbeck U. Expression of interleukin (IL)-18 and functional IL-18 receptor on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for atherogenesis. J Exp Med. 2002;195:245-257. (Pubitemid 34461268)
61. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M, Ausoni S, et al. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res. 2001;89:1111-1121. (Pubitemid 34627868)
62. Savransky V, Nanayakkara A, Li J, Bevans S, Smith PL, Rodriguez A, et al. Chronic intermittent hypoxia induces atherosclerosis. Am J Respir Crit Care Med. 2007;175:1290-1297. (Pubitemid 46905755)
63. Sluimer JC, Gasc JM, van Wanroij JL, Kisters N, Groeneweg M, Sollewijn Gelpke MD, et al. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol. 2008;51:1258-1265. (Pubitemid 351400903)
64. Vink A, Schoneveld AH, Lamers D, Houben AJ, van der Groep P, van Diest PJ, et al. HIF-1 alpha expression is associated with an atheromatous inflammatory plaque phenotype and upregulated in activated macrophages. Atherosclerosis. 2007;195:e69-e75. (Pubitemid 350087978)
65. Sitkovsky M, Lukashev D. Regulation of immune cells by localtissue oxygen tension: HIF1 alpha and adenosine receptors. Nat Rev Immunol. 2005;5:712-721. (Pubitemid 43086172)
66. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6:508-519. (Pubitemid 43980523)
67. Jonasson L, Holm J, Hansson GK. Smooth muscle cells express Ia antigens during arterial response to injury. Lab Invest. 1988; 58:310-315.
68. Aihara K, Azuma H, Akaike M, Ikeda Y, Sata M, Takamori N, et al. Strain-dependent embryonic lethality and exaggerated vascular remodeling in heparin cofactor II-deficient mice. J Clin Invest. 2007;117:1514-1526. (Pubitemid 46871336)
69. Shindo T, Manabe I, Fukushima Y, Tobe K, Aizawa K, Miyamoto S, et al. Kruppel-like zinc-finger transcription factor KLF5/BTEB2 is a target for angiotensin II signaling and an essential regulator of cardiovascular remodeling. Nat Med. 2002;8:856-863.
70. Kurobe H, Urata M, Ueno M, Ueki M, Ono S, Izawa-Ishizawa Y, et al. Role of hypoxia-inducible factor 1alpha in T cells as a negative regulator in development of vascular remodeling. Arterioscler Thromb Vasc Biol. 2010;30:210-217.
71. Makino Y, Nakamura H, Ikeda E, Ohnuma K, Yamauchi K, Yabe Y, et al. Hypoxia-inducible factor regulates survival of antigen receptor-driven T cells. J Immunol. 2003;171:6534-6540. (Pubitemid 37532083)
72. Thiel M, Caldwell CC, Kreth S, Kuboki S, Chen P, Smith P, et al. Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS ONE. 2007;2:e853.
73. Karshovska E, Zernecke A, Sevilmis G, Millet A, Hristov M, Cohen CD, et al. Expression of HIF-1alpha in injured arteries controls SDF-1alpha mediated neointima formation in apolipoprotein E deficient mice. Arterioscler Thromb Vasc Biol. 2007; 27:2540-2547. (Pubitemid 350158903)
74. Whitman SC, Ravisankar P, Elam H, Daugherty A. Exogenous interferon-gamma enhances atherosclerosis in apolipoprotein E-/- mice. Am J Pathol. 2000;157:1819-1824.
75. Jeon MS, Esser C. The murine IL-2 promoter contains distal regulatory elements responsive to the Ah receptor, a member of the evolutionarily conserved bHLH-PAS transcription factor family. J Immunol. 2000;165:6975-6983. (Pubitemid 32001169)
76. Kojima H, Gu H, Nomura S, Caldwell CC, Kobata T, Carmeliet P, et al. Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1alpha-deficient chimeric mice. Proc Natl Acad Sci U S A. 2002;99:2170-2174. (Pubitemid 34169033)
77. Park JW, Chun YS, Kim MS. Hypoxia-inducible factor 1-related diseases and prospective therapeutic tools. J Pharmacol Sci. 2004;94:221-232.
78. Suzuki S, Oguro A, Osada-Oka M, Funae Y, Imaoka S. Epoxyeicosatrienoic acids and/or their metabolites promote hypoxic response of cells. J Pharmacol Sci. 2008;108:79-88.
79. Takeuchi Y, Takahashi M, Fuchikami J. Vulnerability of gastric mucosa to prednisolone in rats chronically exposed to cigarette smoke. J Pharmacol Sci. 2008;106:585-592. (Pubitemid 351556237)
80. Tanaka T, Nangaku M. Drug discovery for overcoming chronic kidney disease (CKD): prolyl-hydroxylase inhibitors to activate hypoxia-inducible factor (HIF) as a novel therapeutic approach in CKD. J Pharmacol Sci. 2009;109:24-31.