Hypoxia-mediated degradation of Na,K-ATPase via mitochondrial reactive oxygen species and the ubiquitin-conjugating system

Circulation Research

Volumn 98, Issue 10, 2006, Pages 1314-1322

  Comellas, Alejandro P ^a   Dada, Laura A ^a   Lecuona, Emilia ^a   Pesce, Liuska M ^a   Chandel, Navdeep S ^a   Quesada, Nancy ^a   Budinger, G R Scott ^a   Strous, Ger J ^c   Ciechanover, Aaron ^a,b   Sznajder, Jacob I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Antioxidants; ATP; Cell adaptation; Oxygen; Proteasome

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CATALASE; CHLOROQUINE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE PEROXIDASE; IRON SULFUR PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; OXYGEN; PROTEASOME INHIBITOR; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SUPEROXIDE DISMUTASE; UBIQUITIN CONJUGATING ENZYME; PROTEASOME;

ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOPRECIPITATION; LYSOSOME; MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ANIMAL; ANOXIA; CELL CULTURE; CELL MEMBRANE; CRICETULUS; ENZYMOLOGY; HAMSTER; MALE; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; ANOXIA; CELL MEMBRANE; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; LYSOSOMES; MALE; MITOCHONDRIA; NA(+)-K(+)-EXCHANGING ATPASE; OXYGEN CONSUMPTION; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; UBIQUITIN-CONJUGATING ENZYMES;

EID: 33744994383     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000222418.99976.1d     Document Type: Article

References (61)

1. Kolar F, Ostadal B. Molecular mechanisms of cardiac protection by adaptation to chronic hypoxia. Physiol Res. 2004;53(suppl 1):S3-S13.
2. Hochachka PW, Buck LT, Doll CJ, Land SC. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci U S A. 1996;93:9493-9498.
3. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 2001;294:1337-1340.
4. 2-regulated prolyl hydroxylation. Science. 2001;292:468-472.
5. Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, Maxwell PH. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem. 2000;275:25733-25741.
6. Schroedl C, McClintock DS, Budinger GR, Chandel NS. Hypoxic but not anoxic stabilization of HIF-1alpha requires mitochondrial reactive oxygen species. Am J Physiol Lung Cell Mol Physiol. 2002;283:L922-L931.
7. Hochachka PW, Lutz PL. Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B Biochem Mol Biol. 2001;130:435-459.
8. Ewart HS, Klip A. Hormonal regulation of the Na(+)-K(+)-ATPase: mechanisms underlying rapid and sustained changes in pump activity. Am J Physiol. 1995;269:C295-C311.
9. Blanco G, Mercer RW. Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol. 1998;275:F633-F650.
10. McDonough AA, Geering K, Farley RA. The sodium pump needs its beta subunit. FASEB J. 1990;4:1598-1605.
11. Michiels C. Physiological and pathological responses to hypoxia. Am J Pathol. 2004;164:1875-1882.
12. Rajasekaran SA, Palmer LG, Quan K, Harper JF, Ball WJ Jr, Bander NH, Peralta Soler A, Rajasekaran AK. Na,K-ATPase beta-subunit is required for epithelial polarization, suppression of invasion, and cell motility. Mol Biol Cell. 2001;12:279-295.
13. Rajasekaran SA, Palmer LG, Moon SY, Peralta Soler A, Apodaca GL, Harper JF, Zheng Y, Rajasekaran AK. Na,K-ATPase activity is required for formation of tight junctions, desmosomes, and induction of polarity in epithelial cells. Mol Biol Cell. 2001;12:3717-3732.
14. Sznajder JI. Strategies to increase alveolar epithelial fluid removal in the injured lung. Am J Respir Crit Care Med. 1999;160:1441-1442.
15. Therien AG, Blostein R. Mechanisms of sodium pump regulation. Am J Physiol Cell Physiol. 2000;279:C541-C566.
16. Feraille E, Doucet A. Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev. 2001;81:345-418.
17. Dada LA, Chandel NS, Ridge KM, Pedemonte C, Bertorello AM, Sznajder JI. Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta. J Clin Invest. 2003;111:1057-1064.
18. Done SC, Leibiger IB, Efendiev R, Katz AI, Leibiger B, Berggren PO, Pedemonte CH, Bertorello AM. Tyrosine 537 within the Na+,K+-ATPase alpha-subunit is essential for AP-2 binding and clathrin-dependent endocytosis. J Biol Chem. 2002;277:17108-17111.
19. King MP, Attardi G. Isolation of human cell lines lacking mitochondrial DNA. Methods Enzymol. 1996;264:304-313.
20. Strous GJ, van Kerkhof P, Govers R, Ciechanover A, Schwartz AL. The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J. 1996;15:3806-3812.
21. Strous GJ, van Kerkhof P, Govers R, Rotwein P, Schwartz AL. Growth hormone-induced signal transduction depends on an intact ubiquitin system. J Biol Chem. 1997;272:40-43.
22. Ridge KM, Rutschman DH, Factor P, Katz AI, Bertorello AM, Sznajder JL. Differential expression of Na-K-ATPase isoforms in rat alveolar epithelial cells. Am J Physiol. 1997;273:L246-L255.
23. Dobbs LG, Gonzalez R, Williams MC. An improved method for isolating type II cells in high yield and purity. Am Rev Respir Dis. 1986;134:141-145.
24. Chandel NS, Budinger GR, Choe SH, Schumacker PT. Cellular respiration during hypoxia. Role of cytochrome oxidase as the oxygen sensor in hepatocytes. J Biol Chem. 1997;272:18808-18816.
25. Pesce L, Guerrero C, Comellas A, Ridge KM, Sznajder JI. Beta-agonists regulate Na,K-ATPase via novel MAPK/ERK and rapamycin-sensitive pathways. FEBS Lett. 2000;486:310-314.
26. Bertorello AM, Ridge KM, Chibalin AV, Katz AI, Sznajder JI. Isoproterenol increases Na+-K+-ATPase activity by membrane insertion of alpha-subunits in lung alveolar cells. Am J Physiol. 1999;276:L20-L27.
27. Ridge KM, Dada L, Lecuona E, Bertorello AM, Katz AI, Mochly-Rosen D, Sznajder JI. Dopamine-induced exocytosis of Na,K-ATPase is dependent on activation of protein kinase C-epsilon and -delta. Mol Biol Cell. 2002;13:1381-1389.
28. Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, Zeviani M, Scarpulla RC, Chandel NS. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 2005;1:409-414.
29. Clerici C, Matthay MA. Hypoxia regulates gene expression of alveolar epithelial transport proteins. J Appl Physiol. 2000;88:1890-1896.
30. Mairbaurl H, Wodopia R, Eckes S, Schulz S, Bartsch P. Impairment of cation transport in A549 cells and rat alveolar epithelial cells by hypoxia. Am J Physiol. 1997;273:L797-L806.
31. Vivona ML, Matthay M, Chabaud MB, Friedlander G, Clerici C. Hypoxia reduces alveolar epithelial sodium and fluid transport in rats: reversal by beta-adrenergic agonist treatment. Am J Respir Cell Mol Biol. 2001;25:554-561.
32. Planes C, Blot-Chabaud M, Matthay MA, Couette S, Uchida T, Clerici C. Hypoxia and beta 2-agonists regulate cell surface expression of the epithelial sodium channel in native alveolar epithelial cells. J Biol Chem. 2002;277:47318-47324.
33. Perkins GD, McAuley DF, Thickett DR, Gao F. The beta-agonist lung injury trial (BALTI): a randomized placebo-controlled clinical trial. Am J Respir Crit Care Med. 2006;173:281-287.
34. Sartori C, Allemann Y, Duplain H, Lepori M, Egli M, Lipp E, Hutter D, Turini P, Hugli O, Cook S, Nicod P, Scherrer U. Salmeterol for the prevention of high-altitude pulmonary edema. N Engl J Med. 2002;346:1631-1636.
35. Thevenod F, Friedmann JM. Cadmium-mediated oxidative stress in kidney proximal tubule cells induces degradation of Na+/K(+)-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASEB J. 1999;13:1751-1761.
36. Chambers SK, Gilmore-Hebert M, Kacinski BM, Benz EJ Jr. Changes in Na,K-ATPase gene expression during granulocytic differentiation of HL60 cells. Blood. 1992;80:1559-1564.
37. Chibalin AV, Katz AI, Berggren PO, Bertorello AM. Receptor-mediated inhibition of renal Na(+)-K(+)-ATPase is associated with endocytosis of its alpha- and beta-subunits. Am J Physiol. 1997;273:C1458-C1465.
38. Schumacker PT, Chandel N, Agusti AG. Oxygen conformance of cellular respiration in hepatocytes. Am J Physiol. 1993;265:L395-402.
39. Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol. 2003;19:141-172.
40. van Kerkhof P, Govers R, Alves dos Santos CM, Strous GJ. Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J Biol Chem. 2000;275:1575-1580.
41. Patrick GN, Bingol B, Weld HA, Schuman EM. Ubiquitin-mediated proteasome activity is required for agonist-induced endocytosis of GluRs. Curr Biol. 2003;13:2073-2081.
42. Dupre DJ, Chen Z, Le Gouill C, Theriault C, Parent JL, Rola-Pleszczynski M, Stankova J. Trafficking, ubiquitination, and down-regulation of the human platelet-activating factor receptor. J Biol Chem. 2003;278:48228-48235.
43. Hershko A, Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992;61:761-807.
44. van Kerkhof P, Strous GJ. The ubiquitin-proteasome pathway regulates lysosomal degradation of the growth hormone receptor and its ligand. Biochem Soc Trans. 2001;29:488-493.
45. Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 1998;17:7151-7160.
46. Klionsky DJ, Ohsumi Y. Vacuolar import of proteins and organelles from the cytoplasm. Annu Rev Cell Dev Biol. 1999;15:1-32.
47. Mayer RJ. The meteoric rise of regulated intracellular proteolysis. Nat Rev Mol Cell Biol. 2000;1:145-148.
48. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol. 2001;2:169-178.
49. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001;2:211-216.
50. Pickart CM. Ubiquitin enters the new millennium. Mol Cell. 2001;8:499-504.
51. Glickman MH. Getting in and out of the proteasome. Semin Cell Dev Biol. 2000;11:149-158.
52. Hicke L. Gettin' down with ubiquitin: turning off cell surface receptors, transporters and channels. Trends Cell Biol. 1999;9:107-112.
53. Kim W, Kaelin WG Jr. The von Hippel-Lindau tumor suppressor protein: new insights into oxygen sensing and cancer. Curr Opin Genet Dev. 2003;13:55-60.
54. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275:25130-25138.
55. Hensley K, Robinson KA, Gabbita SP, Salsman S, Floyd RA. Reactive oxygen species, cell signaling, and cell injury. Free Radic Biol Med. 2000;28:1456-1462.
56. Gabbita SP, Robinson KA, Stewart CA, Floyd RA, Hensley K. Redox regulatory mechanisms of cellular signal transduction. Arch Biochem Biophys. 2000;376:1-13.
57. Kulisz A, Chen N, Chandel NS, Shao Z, Schumacker PT. Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am J Physiol Lung Cell Mol Physiol. 2002;282:L1324-L1329.
58. Melov S, Ravenscroft J, Malik S, Gill MS, Walker DW, Clayton PE, Wallace DC, Malfroy B, Doctrow SR, Lithgow GJ. Extension of life-span with superoxide dismutase/catalase mimetics. Science. 2000;289:1567-1569.
59. Buccellato LJ, Tso M, Akinci OI, Chandel NS, Budinger GR. Reactive oxygen species are required for hyperoxia-induced Bax activation and cell death in alveolar epithelial cells. J Biol Chem. 2004;279:6753-6760.
60. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A. 1998;95:11715-11720.
61. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335-344.