Hypoxia and mitochondrial oxidative metabolism

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 6-7, 2010, Pages 1171-1177

  Solaini, Giancarlo ^a   Baracca, Alessandra ^a   Lenaz, Giorgio ^a   Sgarbi, Gianluca ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Autophagy; F1F0 ATPase; Hypoxia; IF1; Mitochondrion; Oxidative phosphorylation; ROS

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; OXYGEN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; UBIQUINOL CYTOCHROME C REDUCTASE;

AUTOPHAGY; CELL DEATH; CELL STRUCTURE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; ENZYME KINETICS; GLYCOLYSIS; HUMAN; HYPOXIA; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN TENSION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RESPIRATORY CHAIN; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL HYPOXIA; ELECTRON TRANSPORT; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENERGY METABOLISM; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MODELS, BIOLOGICAL; OXYGEN; PROTEINS; REACTIVE OXYGEN SPECIES;

EID: 77953809481     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.02.011     Document Type: Review

References (90)

1. Sack M.N. Type 2 diabetes, mitochondrial biology and the heart. J. Mol. Cell. Cardiol. 2009, 46:842-849.
2. Catrina S.B., Okamoto K., Pereira T., Brismar K., Poellinger L. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 2004, 53:3226-3232.
3. Peers C., Pearson H.A., Boyle J.P. Hypoxia and Alzheimer's disease. Essays Biochem. 2007, 43:153-164.
4. 0-ATPase (ATP synthase) activities in platelets and brain from patients with Alzheimer's disease. Neurobiol. Aging 2002, 23:371-376.
5. Liu B., Tewari A.K., Zhang L., Green-Church K.B., Zweier J.L., Chen Y.R., He G. Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: mitochondria as the major target. Biochim. Biophys. Acta 2009, 1794:476-485.
6. Solaini G., Harris D.A. Biochemical dysfunction in heart mitochondria exposed to ischaemia and reperfusion. Biochem. J. 2005, 390:377-394.
7. Nizet V., Johnson R.S. Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 2009, 9:609-617.
8. 1 and glucose metabolism in the solid tumour. Nat. Rev. Cancer 2008, 8:705-713.
9. 2 availability on human cancer. Nat. Rev. Cancer 2008, 8:967-975.
10. Weinberg F., Chandel N.S. Mitochondrial metabolism and cancer. Ann. N.Y. Acad. Sci. 2009, 1177:66-73.
11. Baracca A., Chiaradonna F., Sgarbi G., Solaini G., Alberghina L., Lenaz G. Mitochondrial Complex I decrease is responsible for bioenergetic dysfunction in K-ras transformed cells. Biochim. Biophys. Acta 2010, 1797:314-323.
12. Bellance N., Lestienne P., Rossignol R. Mitochondria: from bioenergetics to the metabolic regulation of carcinogenesis. Front. Biosci. 2009, 14:4015-4034.
13. 2 solubility in aqueous media determined by a kinetic method. Anal. Biochem. 1985, 145:406-418.
14. Brahimi-Horn M.C., Pouysségur J. Oxygen, a source of life and stress. FEBS Lett. 2007, 581:3582-3589.
15. Santore M.T., McClintock D.S., Lee V.Y., Budinger G.R., Chandel N.S. Anoxia-induced apoptosis occurs through a mitochondria-dependent pathway in lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 282:L727-L734.
16. Viollet B., Athea Y., Mounier R., Guigas B., Zarrinpashneh E., Horman S., Lantier L., Hebrard S., Devin-Leclerc J., Beauloye C., Foretz M., Andreelli F., Ventura-Clapier R., Bertrand L. AMPK: lessons from transgenic and knockout animals. Front. Biosci. Review 2009, 14:19-44.
17. Semenza G.L., Wang G.L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 1992, 12:5447-5454.
18. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
19. Kaluz S., Kaluzová M., Stanbridge E.J. Rational design of minimal hypoxia-inducible enhancers. Biochem. Biophys. Res. Commun. 2008, 370:613-618.
20. Prabhakar N.R., Peng Y.J., Kumar G.K., Nanduri J., Di Giulio C., Lahiri S. Long-term regulation of carotid body function: acclimatization and adaptation. Adv. Exp. Med. Biol. 2009, 648:307-317.
21. Semenza G.L. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda) 2009, 24:97-106.
22. Coleman M.L., Ratcliffe P.J. Oxygen sensing and hypoxia-induced responses. Essays Biochem. 2007, 43:1-15.
23. Galkin A., Higgs A., Moncada S. Nitric oxide and hypoxia. Essays Biochem. 2007, 43:29-42.
24. Kenneth N.S., Rocha S. Regulation of gene expression by hypoxia. Biochem. J. 2008, 414:19-29.
25. Rocha S. Gene regulation under low oxygen: holding your breath for transcription. Trends Biochem. Sci. 2007, 32:389-397.
26. Taylor C.T. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem. J. 2008, 409:19-26.
27. Snyder C., Chandel N. Mitochondrial regulation of cell survival and death during low oxygen conditions. Antioxid. Redox Signal. 2009, 11:2673-2683.
28. Semenza G.L. Hypoxia-inducible factor 1 and cancer pathogenesis. IUBMB Life 2008, 60:591-597.
29. Semenza G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem. J. 2007, 405:1-9.
30. Pan Y., Mansfield K.D., Bertozzi C.C., Rudenko V., Chan D.A., Giaccia A.J., Simon M.C. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol. Cell. Biol. 2007, 27:912-925.
31. Lin X., David C.A., Donnelly J.B., Michaelides M., Chandel N.S., Huang X., Warrior U., Weinberg F., Tormos K.V., Fesik S.W., Shen Y. A chemical genomics screen highlights the essential role of mitochondria in HIF-1 regulation. Proc. Natl Acad. Sci. U. S. A. 2008, 105:174-179.
32. Eng C., Kiuru M., Fernandez M.J., Aaltonen L.A. A role for mitochondrial enzymes in inherited neoplasia and beyond. Nat. Rev. Cancer 2003, 3:193-202.
33. Koivunen P., Hirsilä M., Remes A.M., Hassinen I.E., Kivirikko K.I., Myllyharju J. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J. Biol. Chem. 2007, 282:4524-4532.
34. Kietzmann T., Görlach A. Reactive oxygen species in the control of hypoxia-inducible factor-mediated gene expression. Semin. Cell Dev. Biol. 2005, 16:474-486.
35. Gong Y., Agani F.H. Oligomycin inhibits HIF-1α expression in hypoxic tumor cells. Am. J. Physiol. Cell Physiol. 2005, 288:C1023-C1029.
36. Bell E.L., Klimova T., Chandel N.S. Targeting the mitochondria for cancer therapy: regulation of hypoxia-inducible factor by mitochondria. Antioxid. Redox Signal. 2008, 10:635-640.
37. Srinivas V., Leshchinsky I., Sang N., King M.P., Minchenko A., Caro J. Oxygen sensing and HIF-1 activation does not require an active mitochondrial respiratory chain electron-transfer pathway. J. Biol. Chem. 2001, 276:21995-21998.
38. Vaux E.C., Metzen E., Yeates K.M., Ratcliffe P.J. Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 2001, 198:296-302.
39. Guo S., Bragina O., Xu Y., Cao Z., Chen H., Zhou B., Morgan M., Lin Y., Jiang B.H., Liu K.J., Shi H. Glucose up-regulates HIF-1 alpha expression in primary cortical neurons in response to hypoxia through maintaining cellular redox status. J. Neurochem. 2008, 105:1849-1860.
40. Brunori M., Giuffrè A., Forte E., Mastronicola D., Barone M.C., Sarti P. Control of cytochrome c oxidase activity by nitric oxide. Biochim. Biophys. Acta 2004, 1655:365-371.
41. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
42. Chandel N.S., Budinger G.R., Schumacker P.T. Molecular oxygen modulates cytochrome c oxidase function. J. Biol. Chem. 1996, 271:18672-18677.
43. 2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 1998, 12:149-162.
44. Lum J.J., Bui T., Gruber M., Gordan J.D., DeBerardinis R.J., Covello K.L., Simon M.C., Thompson C.B. 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.
45. Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3:177-185.
46. Papandreou, Cairns R.A., Fontana L., Lim A.L., Denko N.C. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 2006, 3:187-197.
47. Fukuda R., Zhang H., Kim J.W., Shimoda L., Dang C.V., Semenza G.L. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007, 129:111-122.
48. Jezek P., Plecitá-Hlavatá L. Mitochondrial reticulum network dynamics in relation to oxidative stress, redox regulation, and hypoxia. Int. J. Biochem. Cell Biol. 2009, 41:1790-1804.
49. Chen H., Chomyn A., Chan D.C. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 2005, 280:26185-26192.
50. Parone P.A., Da Cruz S., Tondera D., Mattenberger Y., James D.I., Maechler P., Barja F., Martinou J.C. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS ONE 2008, 3:e3257.
51. Spinazzi M., Cazzola S., Bortolozzi M., Baracca A., Loro E., Casarin A., Solaini G., Sgarbi G., Casalena G., Cenacchi G., Malena A., Frezza C., Carrara F., Angelini C., Scorrano L., Salviati L., Vergani L. A novel deletion in the GTPase domain of OPA1 causes defects in mitochondrial morphology and distribution, but not in function. Hum. Mol. Genet. 2008, 17:3291-3302.
52. Zanelli S.A., Trimmer P.A., Solenski N.J. Nitric oxide impairs mitochondrial movement in cortical neurons during hypoxia. J. Neurochem. 2006, 97:724-736.
53. Mironov S.L. ADP regulates movements of mitochondria in neurons. Biophys. J. 2007, 92:2944-2952.
54. Soubannier V., McBride H.M. Positioning mitochondrial plasticity within cellular signaling cascades. Biochim. Biophys. Acta 2009, 1793:154-170.
55. Cheng Y., Gu X.Q., Bednarczyk P., Wiedemann F.R., Haddad G.G., Siemen D. Hypoxia increases activity of the BK-channel in the inner mitochondrial membrane and reduces activity of the permeability transition pore. Cell. Physiol. Biochem. 2008, 22:127-136.
56. Wilson D.F., Rumsey W.L., Green T.J., Vanderkooi J.M. The oxygen dependence of mitochondrial oxidative phosphorylation measured by a new optical method for measuring oxygen concentration. J. Biol. Chem. 1988, 263:2712-2718.
57. Palacios-Callender M., Quintero M., Hollis V.S., Springett R.J., Moncada S. Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7630-7635.
58. Wittenberg B.A., Wittenberg J.B. Transport of oxygen in muscle. Annu. Rev. Physiol. 1989, 51:857-878.
59. Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF 1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3:177-185.
60. Zhang H., Bosch-Marce M., Shimoda L.A., Tan Y.S., Baek J.H., Wesley J.B., Gonzalez F.J., Semenza G.L. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 2008, 283:10892-10903.
61. Cooper C.E., Giulivi C. Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. Am. J. Physiol. Cell Physiol. 2007, 292:C1993-C2003.
62. Galkin A., Abramov A.Y., Frakich N., Duchen M.R., Moncada S. Lack of oxygen deactivates mitochondrial Complex I: implications for ischemic injury?. J. Biol. Chem. 2009, 284:36055-36061.
63. Hagen T., Taylor C.T., Lam F., Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 2003, 302:1975-1978.
64. Poyton R.O., Ball K.A., Castello P.R. Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metab. 2009, 7:332-340.
65. Rosca M.G., Vazquez E.J., Kerner J., Parland W., Chandler M.P., Stanley W., Sabbah H.N., Hoppel C.L. Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc. Res. 2008, 80:30-39.
66. Genova M.L., Baracca A., Biondi A., Casalena G., Faccioli M., Falasca A.I., Formiggini G., Sgarbi G., Solaini G., Lenaz G. Is supercomplex organization of the respiratory chain required for optimal electron transfer activity?. Biochim. Biophys. Acta 2008, 1777:740-746.
67. Gnaiger E., Kuznetsov E.V. Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem. Soc. Trans. 2002, 30:252-258.
68. Turrens J.F. Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 1997, 17:3-8.
69. Lenaz G., Baracca A., Fato R., Genova M.L., Solaini G. New insights into structure and function of mitochondria and their role in aging and disease. Antioxid. Redox Signal. 2006, 8:417-437.
70. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl Acad. Sci. U. S. A. 1998, 95:11715-11720.
71. 2 sensing. J. Biol. Chem. 2000, 275:25130-25138.
72. Klimova T., Chandel N.S. Mitochondrial Complex III regulates hypoxic activation of HIF. Cell Death Differ. 2008, 15:660-666.
73. Tuttle S.W., Maity A., Oprysko P.R., Kachur A.V., Ayene I.S., Biaglow J.E., Koch C.J. Detection of reactive oxygen species via endogenous oxidative pentose phosphate cycle activity in response to oxygen concentration: implications for the mechanism of HIF-1alpha stabilization under moderate hypoxia. J. Biol. Chem. 2007, 282:36790-36796.
74. Mansfield K.D., Guzy R.D., Pan Y., Young R.M., Cash T.P., Schumacker P.T., Simon M.C. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab. 2005, 1:393-399.
75. Bell E.L., Klimova T.A., Eisembart J., Moraes C.T., Murphy M.P., Scott-Budinger G.R., Chandel N.S. The Qo site of the mitochondrial Complex III is required for the transduction of hypoxic signalling via reactive oxygen species production. J. Cell Biol. 2007, 177:1029-1036.
76. Stock D., Gibbons C., Arechaga I., Leslie A.G., Walker J.E. The rotary mechanism of ATP synthase. Curr. Opin. Struct. Biol. 2000, 10:672-679.
77. 0 during ATP synthesis. Biochim. Biophys. Acta 2003, 1606:137-146.
78. Rouslin W., Broge C.W. Mechanisms of ATP conservation during ischemia in slow and fast heart rate hearts. Am. J. Physiol. 1993, 264:C209-C216.
79. 1 and c subunit. Biochem. J. 2002, 362:165-171.
80. 0-ATPase activity. Mol. Cell. Biochem. 2000, 215:31-37.
81. 0-ATP synthase. Trends Biochem. Sci. 2009, 34:343-350.
82. Hamacher-Brady A., Brady N.R., Logue S.E., Sayen M.R., Jinno M., Kirshenbaum L.A., Gottlieb R.A., Gustafsson A.B. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 2007, 14:146-157.
83. Vellai T., Takács-Vellai K., Sass M., Klionsky D.J. The regulation of aging: does autophagy underlie longevity?. Trends Cell Biol. 2009, 19:487-494.
84. Salminen A., Kaarniranta K. Regulation of the aging process by autophagy. Trends Mol. Med. 2009, 15:217-224.
85. 0-ATPase inhibitor for degradation. Cell Death Differ. 2009, 16:603-612.
86. Solaini G., Sgarbi G., Lenaz G., Baracca A. Evaluating mitochondrial membrane potential in cells. Biosci. Rep. 2007, 27:11-21.
87. Brownrigg J.T., Kenny J.E. Fluorescence intensities and lifetimes of aromatic hydrocarbons in cyclohexane solution: evidence of contact charge-transfer interactions with oxygen. J. Phys. Chem. A 2009, 113:1049-1059.
88. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
89. Giraud M.F., Paumard P., Soubannier V., Vaillier J., Arselin G., Salin B., Schaeffer J., Brèthes D., di Rago J.P., Velours J. Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae?. Biochim. Biophys. Acta 2002, 1555:174-180.
90. Baracca A., Sgarbi G., Mattiazzi M., Casalena G., Pagnotta E., Valentino M.L., Moggio M., Lenaz G., Carelli V., Solaini G. Biochemical phenotypes associated with the mitochondrial ATP6 gene mutations at nt8993. Biochim. Biophys. Acta 2007, 1767:913-919.