Hypoxia-induced signaling in the cardiovascular system

Annual Review of Physiology

Volumn 70, Issue , 2008, Pages 51-71

  Simon, M Celeste ^a,b   Liu, Liping ^a,b   Barnhart, Bryan C ^a   Young, Regina M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Oxygen; Stress responses; Transcription; Translation

Indexed keywords

ADENOVIRUS VECTOR; FIBROBLAST GROWTH FACTOR 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; INITIATION FACTOR 4F; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; VASCULOTROPIN; OXYGEN;

ACUTE DISEASE; CARDIOVASCULAR SYSTEM; CELL HYPOXIA; CELL PROLIFERATION; CELL TYPE; CHRONIC DISEASE; CLINICAL TRIAL; DISEASE SEVERITY; ENDOPLASMIC RETICULUM STRESS; HEART MUSCLE CELL; HEART MUSCLE OXYGEN CONSUMPTION; HOMEOSTASIS; HUMAN; HYPOXIA; ISCHEMIC HEART DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RNA TRANSPORT; SIGNAL TRANSDUCTION; STROKE; TUMOR CELL; VIRAL GENE DELIVERY SYSTEM; ANIMAL; ANOXIA; ISCHEMIA; METABOLISM; PHYSIOLOGY;

ANIMALS; ANOXIA; CARDIOVASCULAR SYSTEM; HOMEOSTASIS; HUMANS; ISCHEMIA; OXYGEN; SIGNAL TRANSDUCTION;

EID: 43549094707     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.70.113006.100526     Document Type: Review

References (94)

1. Ramirez-Bergeron DL, Simon MC. 2001. Hypoxia-inducible factor and the development of stem cells of the cardiovascular system. Stem Cells 19:279-86
2. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15:551-78
3. Giaccia AJ, Simon MC, Johnson R. 2004. The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev. 18:2183-94
4. Schofield CJ, Ratcliffe PJ. 2004. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mo. Cell Biol. 5:343-54
5. Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403-7
6. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12:149-62
7. Ryan HE, Lo J, Johnson RS. 1998. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J. 17:3005-15
8. Yu AY, Shimoda LA, Iyer NV, Huso DL, Sun X, et al. 1999. Impaired physiological responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1α. J. Clin. Invest. 103:691-96
9. Brusselmans K, Compernolle V, Tjwa M, Wiesener MS, Maxwell PH, et al. 2003. Heterozygous deficiency of hypoxia-inducible factor-2α protects mice against pulmonary hypertension and right ventricular dysfunction during prolonged hypoxia. J. Clin. Invest. 111:1519-27
10. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, et al. 2002. Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat. Med. 8:702-10
11. Tang N, Wang L, Esko J, Giordano FJ, Huang Y, et al. 2004. Loss of HIF-1α in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 6:485-95
12. Hochachka PW, Buck LT, Doll CJ, Land SC. 1996. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl. Acad. Sci. USA 93:9493-98
13. Liu L, Simon MC. 2004. Regulation of transcription and translation by hypoxia. Cancer Biol. Ther. 3:492-97
14. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, et al. 2002. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2α. Mol. Cell Biol. 22:7405-16
15. Wullschleger S, Loewith R, Hall MN. 2006. TOR signaling in growth and metabolism. Cell 124:471-84
16. Schroder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem. 74:739-89
17. Hellen CU, Sarnow P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15:1593-612
18. Koumenis C, Wouters BG. 2006. "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol. Cancer Res. 4:423-36
19. Averous J, Proud CG. 2006. When translation meets transformation: the mTOR story. Oncogene 25:6423-35
20. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC. 2006. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21:521-31
21. Winder WW, Hardie DG. 1999. AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am. J. Physiol. 277:E1-10
22. Arsham AM, Howell JJ, Simon MC. 2003. A novel HIF-independent hypoxic response regulating mTOR and its targets. J. Biol. Chem. 278:29655-60
23. Brugarolas J, Kaelin WG Jr. 2004. Dysregulation of HIF and VEGF is a unifying feature of the familial hamartoma syndromes. Cancer Cell 6:7-10
24. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, et al. 2004. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18:2893-904
25. Reiling JH, Hafen E. 2004. The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev. 18:2879-92
26. Bernardi R, Guernah I, Jin D, Grisendi S, Alimonti A, et al. 2006. PML inhibits HIF-1α translation and neoangiogenesis through repression of mTOR. Nature 442:779-85
27. Yoshida H. 2007. ER stress and diseases. FEBS J. 274:630-58
28. Marciniak SJ, Ron D. 2006. Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86:1133-49
29. Magagnin MG, Koritzinsky M, Wouters BG. 2006. Patterns of tumor oxygenation and their influence on the cellular hypoxic response and hypoxia-directed therapies. Drug Resist. Updat. 9:185-97
30. Koritzinsky M, Magagnin MG, van den Beucken T, Seigneuric R, Savelkouls K, et al. 2006. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J. 25:1114-25
31. Blais JD, Filipenko V, Bi M, Harding HP, Ron D, et al. 2004. Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol. Cell Biol. 24:7469-82
32. Wouters BG, van den Beucken T, Magagnin MG, Koritzinsky M, Fels D, Koumenis C. 2005. Control of the hypoxic response through regulation of mRNA translation. Semin. Cell Dev. Biol. 16:487-501
33. Connolly E, Braunstein S, Formend S, Schneider RJ. 2006. Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells. Mol. Cell Biol. 26:3955-65
34. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-63
35. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, et al. 2005. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24:3470-81
36. Romero-Ramirez L, Cao H, Nelson D, Hammond E, Lee AH, et al. 2004. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res. 64:5943-47
37. Sambandam N, Lopaschuk GD. 2003. AMP-activated protein kinase (AMPK) control of fatty acid and glucose metabolism in the ischemic heart. Prog. Lipid Res. 42:238-56
38. Hossmann KA. 1993. Disturbances of cerebral protein synthesis and ischemic cell death. Prog. Brain Res. 96:161-77
39. DeGracia DJ. 2004. Acute and persistent protein synthesis inhibition following cerebral reperfusion. J. Neurosci. Res. 77:771-76
40. Kirino T. 2002. Ischemic tolerance. J. Cereb. Blood Flow Metab. 22:1283-96
41. Arad M, Seidman CE, Seidman JG. 2007. AMP-activated protein kinase in the heart: role during health and disease. Circ. Res. 100:474-88
42. Hedhli N, Pelat M, Depre C. 2005. Protein turnover in cardiac cell growth and survival. Cardiovasc. Res. 68:186-96
43. Force T, Kuida K, Namchuk M, Parang K, Kyriakis JM. 2004. Inhibitors of protein kinase signaling pathways: emerging therapies for cardiovascular disease. Circulation 109:1196-205
44. Kapp LD, Lorsch JR. 2004. The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73:657-704
45. Brunn GJ, Hudson CC, Sekulic A, Williams JM, Hosoi H, et al. 1997. Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277:99-101
46. Mothe-Satney I, Yang D, Fadden P, Haystead TA, Lawrence JC Jr. 2000. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol. Cell Biol. 20:3558-67
47. Fingar DC, Blenis J. 2004. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23:3151-71
48. Holz MK, Ballif BA, Gygi SP, Blenis J. 2005. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123:569-80
49. De Benedetti A, Graff JR. 2004. eIF-4E expression and its role in malignancies and metastases. Oncogene 23:3189-99
50. Lee YM, Jeong CH, Koo SY, Son MJ, Song HS, et al. 2001. Determination of hypoxic region by hypoxia marker in developing mouse embryos in vivo: a possible signal for vessel development. Dev. Dyn. 220:175-86
51. Cipolleschi MG, Dello Sbarba P, Olivotto M. 1993. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 82:2031-37
52. Danet GH, Pan Y, Luongo JL, Bonnet DA, Simon MC. 2003. Expansion of human SCID-repopulating cells under hypoxic conditions. J. Clin. Invest. 112:126-35
53. Morrison SJ, Csete M, Groves AK, Melega W, Wold B, Anderson DJ. 2000. Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J. Neurosci. 20:7370-76
54. Studer L, Csete M, Lee SH, Kabbani N, Walikonis J, et al. 2000. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J. Neurosci. 20:7377-83
55. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. 1997. Regulation of human placental development by oxygen tension. Science 277:1669-72
56. Ramirez-Bergeron DL, Runge A, Adelman DM, Gohil M, Simon MC. 2006. HIF-dependent hematopoietic factors regulate the development of the embryonic vasculature. Dev. Cell 11:81-92
57. Brown JM, Wilson WR. 2004. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 4:437-47
58. Hockel M, Vaupel P. 2001. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst. 93:266-76
59. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, Huang LE. 2004. HIF-1α induces cell cycle arrest by functionally counteracting Myc. EMBO J. 23:1949-56
60. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, Johnson RS. 2003. Hypoxia-inducible factor 1α is essential for cell cycle arrest during hypoxia. Mol. Cell Biol. 23:359-69
61. Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC. 2007. HIF-2α promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 11:335-47
62. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. 2004. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol. Cell Biol. 24:200-16
63. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J. 2002. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev. 16:1472-87
64. Bjornsti MA, Houghton PJ. 2004. The TOR pathway: a target for cancer therapy. Nat. Rev. Cancer 4:335-48
65. Vivanco I, Sawyers CL. 2002. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2:489-501
66. Cogo A, Napolitano G, Michoud MC, Barbon DR, Ward M, Martin JG. 2003. Effects of hypoxia on rat airway smooth muscle cell proliferation. J. Appl. Physiol. 94:1403-9
67. Das M, Bouchey DM, Moore MJ, Hopkins DC, Nemenoff RA, Stenmark KR. 2001. Hypoxia-induced proliferative response of vascular adventitial fibroblasts is dependent on G protein-mediated activation of mitogen-activated protein kinases. J. Biol. Chem. 276:15631-40
68. Humar R, Kiefer FN, Berns H, Resink TJ, Battegay EJ. 2002. Hypoxia enhances vascular cell proliferation and angiogenesis in vitro via rapamycin (mTOR)-dependent signaling. FASEB J. 16:771-80
69. Gerasimovskaya EV, Tucker DA, Stenmark KR. 2005. Activation of phosphatidylinositol 3-kinase, Akt, and mammalian target of rapamycin is necessary for hypoxia-induced pulmonary artery adventitial fibroblast proliferation. J. Appl. Physiol. 98:722-31
70. Casey TM, Pakay JL, Guppy M, Arthur PG. 2002. Hypoxia causes downregulation of protein and RNA synthesis in noncontracting mammalian cardiomyocytes. Circ. Res. 90:777-83
71. Crozier SJ, Zhang X, Wang J, Cheung J, Kimball SR, Jefferson LS. 2006. Activation of signaling pathways and regulatory mechanisms of mRNA translation following myocardial ischemia-reperfusion. J. Appl. Physiol. 101:576-82
72. Fan C, Iacobas DA, Zhou D, Chen Q, Lai JK, et al. 2005. Gene expression and phenotypic characterization of mouse heart after chronic constant or intermittent hypoxia. Physiol. Genomics 22:292-307
73. Blais JD, Addison CL, Edge R, Falls T, Zhao H, et al. 2006. Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol. Cell Biol. 26:9517-32
74. Koritzinsky M, Seigneuric R, Magagnin MG, van den Beucken T, Lambin P, Wouters BG. 2005. The hypoxic proteome is influenced by gene-specific changes in mRNA translation. Radiother. Oncol. 76:177-86
75. Nordlie MA, Wold LE, Simkhovich BZ, Sesti C, Kloner RA. 2006. Molecular aspects of ischemic heart disease: ischemia/reperfusion-induced genetic changes and potential applications of gene and RNA interference therapy. J. Cardiovasc. Pharmacol. Ther. 11:17-30
76. Chen H, Shi S, Acosta L, Li W, Lu J, et al. 2004. BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131:2219-31
77. Nobori K, Ito H, Tamamori-Adachi M, Adachi S, Ono Y, et al. 2002. ATF3 inhibits doxorubicin-induced apoptosis in cardiac myocytes: a novel cardioprotective role of ATF3. J. Mol. Cell Cardiol. 34:1387-97
78. Rodriguez-Viciana P, Tetsu O, Tidyman WE, Estep AL, Conger BA, et al. 2006. Germline mutations in genes within the MAPK pathway cause cardio-facio-cutaneous syndrome. Science 311:1287-90
79. Park EH, Lee JM, Blais JD, Bell JC, Pelletier J. 2005. Internal translation initiation mediated by the angiogenic factor Tie2. J. Biol. Chem, 280:20945-53
80. Buermans HP, Redout EM, Schiel AE, Musters RJ, Zuidwijk M, et al. 2005. Microarray analysis reveals pivotal divergent mRNA expression profiles early in the development of either compensated ventricular hypertrophy or heart failure. Physiol. Genomics 21:314-23
81. Bull TM, Coldren CD, Geraci MW, Voelkel NF. 2007. Gene expression profiling in pulmonary hypertension. Proc. Am. Thorac. Soc. 4:117-20
82. Gebauer F, Hentze MW. 2004. Molecular mechanisms of translational control. Nat. Rev. Mol. Cell Biol. 5:827-35
83. van den Beucken T, Koritzinsky M, Wouters BG. 2006. Translational control of gene expression during hypoxia. Cancer Biol. Ther. 5:749-55
84. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, et al. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-108
85. Park EH, Lee JM, Pelletier J. 2006. The Tie2 5′ untranslated region is inhibitory to 5′ end-mediated translation initiation. FEBS Lett. 580:1309-19
86. Lang KJ, Kappel A, Goodall GJ. 2002. Hypoxia-inducible factor-1α mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol. Biol. Cell 13:1792-801
87. Huez I, Bornes S, Bresson D, Creancier L, Prats H. 2001. New vascular endothelial growth factor isoform generated by internal ribosome entry site-driven CUG translation initiation. Mol. Endocrinol. 15:2197-210
88. Bert AG, Grepin R, Vadas MA, Goodall GJ. 2006. Assessing IRES activity in the HIF-1α and other cellular 5′ UTRs. RNA 12:1074-83
89. Bornes S, Prado-Lourenco L, Bastide A, Zanibellato C, Iacovoni JS, et al. 2007. Translational induction of VEGF internal ribosome entry site elements during the early response to ischemic stress. Circ. Res. 100:305-8
90. Kozak M. 2005. A second look at cellular mRNA sequences said to function as internal ribosome entry sites. Nucleic Acids Res. 33:6593-602
91. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, et al. 2007. A microRNA signature of hypoxia. Mol. Cell Biol. 27:1859-67
92. Donker RB, Mouillet JF, Nelson DM, Sadovsky Y. 2007. The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol. Hum. Reprod. 13:273-79
93. Das DK, Maulik N, Moraru II. 1995. Gene expression in acute myocardial stress. Induction by hypoxia, ischemia, reperfusion, hyperthermia and oxidative stress. J. Mol. Cell Cardiol. 27:181-93
94. Hampton T. 2006. Search is on for cells that repair heart. JAMA 296:2541