Hypoxia-inducible factor-1alpha is a critical mediator of hypoxia induced apoptosis in cardiac H9c2 and kidney epithelial HK-2 cells

BMC Cardiovascular Disorders

Volumn 8, Issue , 2008, Pages

  Malhotra, Ricky ^a   Tyson, David W ^a   Rosevear, Henry M ^a   Brosius III, Frank C ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; CASPASE 3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; PROTEIN BAX; PROTEIN BCL 2; BAX PROTEIN, HUMAN; BAX PROTEIN, RAT; CASP3 PROTEIN, HUMAN; CASP3 PROTEIN, RAT; HIF1A PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL HYPOXIA; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; KIDNEY CELL; KIDNEY TUBULE EPITHELIUM; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE; UPREGULATION; WILD TYPE; ANIMAL; CELL LINE; ENZYMOLOGY; EPITHELIUM CELL; GENETICS; KIDNEY; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL HYPOXIA; CELL LINE; EPITHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IN SITU NICK-END LABELING; KIDNEY; MYOCYTES, CARDIAC; RATS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 44149095751     PISSN: None     EISSN: 14712261     Source Type: Journal    
DOI: 10.1186/1471-2261-8-9     Document Type: Article

References (50)

1. Wang GL Jiang B-H Rue EA Semenza GL Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension Proc Natl Acad Sci USA 1995, 92:5510-5514. 41725 7539918 10.1073/ pnas.92.12.5510
2. Semenza GL Hypoxia-inducible factor-1: Oxygen homeostasis and disease pathophysiology Trends Mol Med 2001, 8:345-350. 10.1016/ S1471-4914(01)02090-1
3. Metzen E Ratcliffe PJ HIF-hydroxylation and cellular oxygen sensing Biol Chem 2004, 3-4:223-230. 10.1515/BC.2004.016 15134335
4. Semenza GL Hypoxia-inducible factor1: Master regulator of O2 homeostasis Curr Opin Gen Dev 1998, 8:588-594. 10.1016/S0959-437X(98)80016-6
5. Brunelle JK Santore MT Budinger GR Tang Y Barret TA Zong WX Kandel E Keith B Simon C Thompson CB Hay N Chandel NS C-Myc sensitization to oxygen deprivation-induced cell death is dependent on Bax/Bak, but is independent of p53 and hypoxia inducible factor-1 J Biol Chem 2004, 279:4305-4312. 10.1074/jbc.M312241200 14627695
6. McClintock DS Santore MT Lee VY Brunelle J Budinger GR Zong WX Thompson CB Hay N Chandel NS Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death Mol Cell Biol 2002, 22:94-104. 134234 11739725 10.1128/MCB.22.1.94-104.2002
7. Yamamoto K Tomita N Yoshimura S Nakagami H Taniyama Y Yamasaki K Ogihara T Morishita R Hypoxia-induced renal epithelial cell death through caspase-dependent pathway: Role of Bcl-2, Bcl-xL and Bax in tubular injury Int J Mol Med 2004, 14:633-640. 15375594
8. Marin-Garcia J Goldenthal MJ Heart mitochondria signaling pathways: appraisal of an emerging field J Mol Med 2004, 82:565-578. 15221079
9. Carmeliet P Dor Y Herbert J-M Fukumara D Brusselmans K Dewerchin M Neeman M Bono F Abramovitch R Maxwell P Koch CJ Ratcliffe P Moons L Jain RK Collen D Keshet E Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis Nature 1998, 394:485-490. 10.1038/28867 9697772
10. Krick S Eul BG Hanze J Savai R Grimminger F Seeger W Rose F Role of hypoxia-inducible factor-1alpha in hypoxia-induced apoptosis of primary alveolar epithelial type II cells Am J Respir Cell Mol Biol 2005, 32:395-403. 10.1165/rcmb.2004-0314OC 15695738
11. Graham RM Frazier DP Thompson JW Haliko S Li H Wasserlauf BJ Spiga MG Bishopric NH Webster KA A unique pathway of cardiac myocyte death caused by hypoxia-acidosis J Exp Biol 2004, 207(Pt 18):3189-200. 10.1242/ jeb.01109 15299040
12. Piret JP Mottet D Raes M Michiels C Is HIF-1alpha a pro- or an anti-apoptotic protein? Biochem Pharmacol 2002, 64:889-92. 10.1016/ S0006-2952(02)01155-3 12213583
13. Greijer AE Wall van der E The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis J Clin Pathol 2004, 57:1009-14. 1770458 15452150 10.1136/jcp.2003.015032
14. Bruick RK Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia Proc Natl Acad Sci USA 2000, 97:9082-7. 16825 10922063 10.1073/pnas.97.16.9082
15. Akakura N Kobayashi M Horiuchi I Suzuki A Wang J Chen J Niizeki H Kawamura Ki Hosokawa M Asaka M Constitutive expression of hypoxia-inducible factor-1alpha renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation Cancer Res 2001, 61:6548-54. 11522653
16. Erler JT Cawthorne CJ Williams KJ Koritzinsky M Wouters BG Wilson C Miller C Demonacos C Stratford IJ Dive C Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance Mol Cell Biol 2004, 24:2875-89. 371100 15024076 10.1128/ MCB.24.7.2875-2889.2004
17. Chen J Zhao S Nakada K Kuge Y Tamaki N Okada F Wang J Shindo M Higashino F Takeda K Asaka M Katoh H Sugiyama T Hosokawa M Kobayashi M Dominant-negative hypoxia-inducible factor-1 alpha reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism Am J Pathol 2003, 162(4):1283-91. 1851236 12651620
18. Piret J-P Mottet D Raes M Michiels C CoCl2, a chemical inducer of hypoxia-inducible factor-1, and hypoxia reduce apoptotic cell death in hepatoma cell line HepG2 Ann NY Acad Sci 2002, 973:443-447. 12485908
19. Dai S Huang ML Hsu CYY Clifford Chao KS Inhibition of hypoxia inducible factor 1 alpha causes oxygen-independent cytotoxicity and induces p53 independent apoptosis in glioblastoma cells Int J Radiat Oncol Biol Phys 2003, 55:1027-1036. 12605983
20. Malhotra R Brosius FC III Glucose uptake and glycolysis reduce hypoxia-induced apoptosis in cultured cardiac myocytes J Biol Chem 1999, 274:12567-12575. 10.1074/jbc.274.18.12567 10212235
21. Lin Z Malhotra R Weinberg JM Merritt S Holzman LB Brosius FC III Increased GLUT1 expression prevents hypoxia-induced apoptosis and cJun-NH2-terminal kinase activation in vascular smooth muscle cells Am J Physiol 2000, 278:E958-E966.
22. Loberg RD Vesely E Brosius FC III Enhanced glycogen synthase kinase-3β activity mediates hypoxia-induced apoptosis of vascular smooth muscle cells and is prevented by glucose transport and metabolism J Biol Chem 2002, 277:41667-41673. 10.1074/jbc.M206405200 12200436
23. Malhotra R Tyson DGW Sone H Aoki K Kumagai AK Brosius FC III Glucose uptake and adenoviral mediated GLUT1 infection decrease hypoxia-induced HIF-1a levels in cardiac myocytes J Mol Cell Cardiol 2002, 34:1063-1073. 10.1006/jmcc.2002.2047 12234775
24. Gao W Ferguson G Connell P Walshe T Murphy R Birney YA O'brien C Cahill PA High glucose concentrations alter hypoxia-induced control of vascular smooth muscle cell growth via a HIF-1alpha-dependent pathway J Mol Cell Cardiol 2007, 42(3):609-619. 10.1016/j.yjmcc.2006.12.006 17321542
25. Jiang B-H Rue E Wang GL Roe R Semenza GL Dimerization, DNA binding, and transactivation properties of hypoxia inducible factor 1 J Biol Chem 1996, 271:17771-17778. 10.1074/jbc.271.30.17771 8663540
26. Reynolds A Leake D Boese Q Scaringe S Marshall WS Khvorova A Rational siRNA design for RNA interference Nature Biotechnology 2004, 22:326-330. 10.1038/nbt936 14758366
27. Hsu YT Wolter KG Youle RJ Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis Proc Natl Acad Sci USA 1997, 94:3668-72. 20498 9108035 10.1073/pnas.94.8.3668
28. Van Hoecke M Prigent-Tessier AS Garnier PE Bertrand NM Filomenko R Bettaieb A Marie C Beley AG Evidence of HIF-1 functional binding activity to caspase-3 promoter after photothrombotic cerebral ischemia Mol Cell Neurosci 2007, 34(1):40-7. 10.1016/j.mcn.2006.09.009 17101276
29. Sowter HM Ratcliffe PJ Watson P Greenberg AH Harris AL HIF-1- dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors Cancer Res 2001, 61:6669-6673. 11559532
30. Bruick RK Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia Proc Natl Acad Sci USA 2000, 97(16):9082-9087. 16825 10922063 10.1073/pnas.97.16.9082
31. An WG Kanekal M Simon MC Maltepe E Blagosklonny MV Stabilization of wild-type p53 by hypoxia-inducible factor 1α Nature 1998, 392:405-408. 10.1038/32925 9537326
32. Wright G Higgins JJ Raines RT Steenberger C Murphy E Activation of the prolyl hydroxylase oxygen-sensor results in induction of GLUT 1, heme oxygenase -1, and nitric-oxide synthase proteins and confers protection from metabolic inhibition to cardiomyocytes J Biol Chem 2003, 278:20235-20239. 10.1074/jbc.M301391200 12649278
33. Date T Mochizuki S Belanger AJ Yamakawa M Luo Z Vincent KA Cheng SH Gregory RJ Jiang C Expression of constitutively stable hybrid hypoxia-inducible factor-1 alpha protects cultured rat cardiomyoctes against simulated ischemia-reperfusion injury Am J Physiol Cell Physiol 2005, 288:C314-C320. 10.1152/ajpcell.00374.2004 15496478
34. Natarajan R Salloum FN Fisher BJ Kukreja RC Fowler AA 3rd Hypoxia inducible factor-1 activation by prolyl 4-hydroxylase-2 gene silencing attenuates myocardial ischemia reperfusion injury Circ Res 2006, 98:133-140. 10.1161/01.RES.0000197816.63513.27 16306444
35. Rathmell JC Fox CJ Plas DR Hammerman PS Cinalli RM Thompson CB Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival Mol Cell Biol 2003, 23:7315-7328. 230333 14517300 10.1128/MCB.23.20.7315-7328.2003
36. Lum JJ Bui T Gruber T Gordan JD Deberardinis RJ Covello KL Simon MC Thompson CB The transcription factor HIF-1alpha plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis Genes Dev 2007, 21:1037-1049. 1855230 17437992 10.1101/ gad.1529107
37. Morisette MR Howes AL Zhang T Heller Brown J Upregulation of GLUT1 expression is necessary for hypertrophy and survival of neonatal rat cardiomyocytes J Mol Cell Cardiol 2003, 35:1217-1227. 10.1016/ S0022-2828(03)00212-8 14519432
38. Stein AB Tang XL Guo Y Xuan YT Dawn B Bolli R Delayed adaptation of heart to stress: Late preconditioning Stroke 2004, 35:2676-2679. 10.1161/ 01.STR.0000143220.21382.fd 15459441
39. Vanden Hoek TL Shao Z Li C Zak R Schumacker PT Becker LB Reperfusion injury on cardiac myocytes after simulated ischemia Am J Physiol 1996, 270:H1334-H1341. 8967373
40. Thuerauf DJ Marcinko M Gude N Rubio M Sussman MA Glembotski CC Activation of the Unfolded Protein Response in Infracted Mouse Heart and Hypoxic cultured Cardiac Myocytes Cir Res 2006, 99:275-286. 10.1161/ 01.RES.0000233317.70421.03 16794188
41. Rutkowski DT Kaufman RJ A trip to the ER: Coping with stress Trends Cell Biol 2004, 14:20-28. 10.1016/j.tcb.2003.11.001 14729177
42. Harding HP Calfon M Urano F Novoa I Ron D Transcriptional and translational control in the mammalian unfolded protein response Ann Rev Cell Biol 2002, 18:575-599. 10.1146/annurev.cellbio.18.011402.160624 12142265
43. Ozawa T Hu JL Hu LJ Kong EL Bollen AW Lamborn KR Deen DF Functionality of hypoxia-induced BAX expression in a human glioblastoma xenograft model Cancer Gene Therapy 2005, 12:449-455. 15706354
44. Tanaka T Hanafusa N Ingelfinger JR Ohse T Fujita T Nangaku M Hypoxia induces apoptosis in SV40-immortalized rat proximal tubular cells through the mitochondrial pathways, devoid of HIF1-mediated upregulation of Bax Biochem Biophys Res Commun 2003, 309:222-31. 10.1016/ S0006-291X(03)01557-2 12943686
45. Chen D Li M Luo J Gu W Direct interactions between HIF-1 alpha and Mdm2 modulate p53 function J Biol Chem 2003, 278:13595-8. 10.1074/ jbc.C200694200 12606552
46. Ding WX Ni HM Chen X Yu J Zhang L Yin XM A coordinated action of Bax, PUMA, and p53 promotes MG-132-induced mitochondria activation and apoptosis in colon cancer cells Mol Cancer Ther 2007, 6:1062-1069. 10.1158/1535-7163.MCT-06-0541 17363499
47. Cheng J Cui R Chen CH Du J Oxidized Low-density lipoprotein stimulates p53-dependent activation of proapoptotic Bax leading to apoptosis of differentiated endothelial progenitor cells Endocrinology 2007, 148:2085-94. 10.1210/en.2006-1709 17289842
48. Mansfield KD Guzy RD Pan Y Young RM Cash TP Schumaker PT Simon MC Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-1α activation Cel Metab 2005, 1:393-399. 10.1016/j.cmet.2005.05.003 16054088
49. Chandel NS McClintock DS Feliciano CE Wood TM Melendez JA Rodriguez AM Schumaker PT Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor -1α during hypoxia: A mechanism of O2 sensing J Biol Chem 2000, 275:25130-25138. 10.1074/ jbc.M001914200 10833514
50. Zhang L Li L Liu H Prabhakaran K Zhang X Borowitz JL Isom GE HIF-1 alpha activation by a redox-senstive pathway mediates cyanide-induced BNIP3 upregulation and mitochondrial dependent cell death Free Radic Biol Med 2007, 43:117-127. 2048659 17561100 10.1016/j.freeradbiomed.2007.04.005