Involvement of reactive oxygen species in a feed-forward mechanism of Na/K-ATPase-mediated signaling transduction

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 34249-34258

  Yan, Yanling ^a,c   Shapiro, Anna P ^b   Haller, Steven ^b   Katragadda, Vinai ^b   Liu, Lijun ^b   Tian, Jiang ^b   Basrur, Venkatesha ^d   Malhotra, Deepak ^b   Xie, Zi Jian ^b   Abraham, Nader G ^a   Shapiro, Joseph I ^a,b   Liu, Jiang ^a  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

^c YANSHAN UNIVERSITY   (China)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; CARDIOTONIC STEROIDS; N-ACETYL L-CYSTEINE; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; SIGNALING COMPLEX; SIGNALING TRANSDUCTION; SODIUM TRANSPORT;

ACETYLCYSTEINE; AMINO ACIDS; CARBONYLATION; OXYGEN; PROTEINS; SIGNAL TRANSDUCTION; SODIUM;

SIGNALING;

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); OUABAIN; PROTEASOME; PROTEIN KINASE P60; REACTIVE OXYGEN METABOLITE; SODIUM POTASSIUM ADENOSINE TRIPHOSPHATASE ALPHA 1 SUBUNIT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; LYSOSOME; NUCLEOTIDE BINDING SITE; OXIDATIVE STRESS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SODIUM ABSORPTION; SODIUM TRANSPORT;

HYPERTENSION; NA/K-ATPASE SIGNALING; NAK-ATPASE; REACTIVE OXYGEN SPECIES (ROS); SIGNAL TRANSDUCTION; SODIUM TRANSPORT;

ACETYLCYSTEINE; ANIMALS; CELL LINE; ENZYME INHIBITORS; FREE RADICAL SCAVENGERS; MULTIENZYME COMPLEXES; OUABAIN; PROTEIN CARBONYLATION; PROTEOLYSIS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-EXCHANGING ATPASE; SRC-FAMILY KINASES; SWINE;

EID: 84888366548     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.461020     Document Type: Article

References (50)

1. Tian, J., Cai, T., Yuan, Z., Wang, H., Liu, L., Haas, M., Maksimova, E., Huang, X. Y., and Xie, Z. J. (2006) Binding of Src to Na+/K+-ATPase forms afunctional signaling complex. Mol. Biol. Cell 17, 317-326
2. Li, Z., and Xie, Z. (2009) The Na/K-ATPase/Src complex and cardiotonic steroid-activated protein kinase cascades. Pflugers Arch. 457, 635-644
3. Xie, Z., Kometiani, P., Liu, J., Li, J., Shapiro, J. I., and Askari, A. (1999) Intracellular reactive oxygen species mediate the linkage of Na+/K+-ATPase to hypertrophy and its marker genes in cardiac myocytes. J. Biol. Chem. 274, 19323-19328
4. 2+ concentrations. J. Biol. Chem. 275, 27838-27844
5. Liu, L., Li, J., Liu, J., Yuan, Z., Pierre, S. V., Qu, W., Zhao, X., and Xie, Z. (2006) Involvement of Na+/K+-ATPase in hydrogen peroxide-induced hypertrophy in cardiac myocytes. Free Radic. Biol. Med. 41, 1548-1556
6. Huang, W. H, Wang, Y., and Askari, A. (1992) (Na+ + K+)-ATPase: inactivation and degradation induced by oxygen radicals. Int. J. Biochem. 24, 621-626
7. Thevenod, F., and Friedmann, J. M. (1999) Cadmium-mediated oxidative stress in kidney proximal tubule cells induces degradation of Na+/K+-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASEBJ. 13, 1751-1761
8. Figtree, G. A., Liu, C.-C, Bibert, S., Hamilton, E. J., Garcia, A., White, C. N., Chia, K. K., Cornelius, F., Geering, K., and Rasmussen, H. H. (2009) Reversible oxidative modification: A key mechanism of Na+-K+ pump regulation. Circ. Res. 105, 185-193
9. Petrushanko, I. Y., Yakushev, S., Mitkevich, V. A., Kamanina, Y. V., Ziganshin, R. H., Meng, X., Anashkina, A. A., Makhro, A., Lopina, O. D., Gassmann, M., Makarov, A. A., and Bogdanova, A. (2012) S-Glutathionylation of the Na, K-ATPase catalytic a subunit is a determinant of the enzyme redox sensitivity. J. Biol. Chem. 287, 32195-32205
10. Liu, J., Schuff-Werner, P., and Steiner, M. (2004) Double transfection improves small interfering RNA-induced thrombin receptor (PAR-1) gene silencing in DU 145 prostate cancer cells. FEBS Lett. 577, 175-180
11. Liu, J., Liang, M., Liu, L., Malhotra, D., Xie, Z., and Shapiro, J. I. (2005) Ouabain-induced endocytosis of the plasmalemmal Na/K-ATPase in LLC-PK1 cells requires caveolin-1. Kidney Int. 67, 1844-1854
12. Periyasamy, S. M., Liu, J., Tanta, F., Kabak, B., Wakefield, B., Malhotra, D., Kennedy, D. J., Nadoor, A., Fedorova, O. V., Gunning, W., Xie, Z., Bagrov, A. Y., and Shapiro, J. I. (2005) Salt loading induces redistribution of the plasmalemmal Na/K-ATPase in proximal tubule cells. Kidney Int. 67, 1868-1877
13. Cai, H., Wu, L., Qu, W., Malhotra, D., Xie, Z., Shapiro, J. I., and Liu, J. (2008) Regulation of apical NHE3 trafficking by ouabain-induced activation of the basolateral Na+-K+-ATPase receptor complex. Am. J. Physiol. Cell Physiol. 294, C555-C563
14. Fedorova, O. V., Shapiro, J. I., and Bagrov, A. Y. (2010) Endogenous cardiotonic steroids and salt-sensitive hypertension. Biochim. Biophys. Acta 1802, 1230-1236
15. Liu, J., and Xie, Z. J. (2010) The sodium pump and cardiotonic steroidsinduced signal transduction protein kinases and calcium-signaling microdomain in regulation of transporter trafficking. Biochim. Biophys. Acta 1802, 1237-1245
16. Qiang, W., Zuo, P., and Liu, J. (1999) Role of N-methyl-D-aspartate receptor-nitric oxide-cyclic guanosine monophosphate pathway in ischemic brain injury. Zhongguo YiXueKeXue Yuan Xue Bao 21, 175-179
17. Mokry, M., and Cuppen, E. (2008) The Atp1a1 gene from inbred Dahl salt sensitive rats does not contain the A1079Tmissensetransversion. Hypertension 51, 922-927
18. Nishi, A., Bertorello, A. M., and Aperia, A. (1993) Renal Na+, K+-ATPase in Dahl salt-sensitive rats: K+ dependence, effect of cell environment and protein kinases. Acta Physiol. Scand. 149, 377-384
19. Fedorova, O. V., Lakatta, E. G., and Bagrov, A. Y. (2000) Endogenous Na, K pump ligands are differentially regulated during acute NaCl loading of Dahl rats. Circulation 102, 3009-3014
20. Zanetti, M., D'Uscio, L. V., Peterson, T. E., Katusic, Z. S., and O'Brien, T. (2005) Analysis of superoxide anion production in tissue. Methods Mol. Med. 108, 65-72
21. Liu, J., Kesiry, R., Periyasamy, S. M., Malhotra, D., Xie, Z., and Shapiro, J. I. (2004) Ouabain induces endocytosis of plasmalemmal Na/K-ATPase in LLC-PK1 cells by a clathrin-dependent mechanism. Kidney Int. 66, 227-241
22. Liu, J., Yan, Y., Liu, L., Xie, Z., Malhotra, D., Joe, B., and Shapiro, J. I. (2011) Impairment of Na/K-ATPase signaling in renal proximal tubule contributes to Dahl salt-sensitive hypertension. J. Biol. Chem. 286, 22806-22813
23. Todi, S. V., Scaglione, K. M., Blount, J. R., Basrur, V., Conlon, K. P., Pastore, A., Elenitoba-Johnson, K., and Paulson, H. L. (2010) Activity and cellular functions of the deubiquitinating enzyme and polyglutamine disease protein Ataxin-3 are regulated by ubiquitination at lysine 117. J. Biol. Chem. 285, 39303-39313
24. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
25. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
26. Pedrioli, P. G. (2010) Trans-proteomic pipeline: a pipeline for proteomic analysis. Methods Mol. Biol. 604, 213-238
27. Panico, C, Luo, Z., Damiano, S., Artigiano, F., Gill, P., and Welch, W. J. (2009) Renal proximal tubular reabsorption is reduced in adult spontaneously hypertensive rats: roles of superoxide and Na+/H+ exchanger 3. Hypertension 54, 1291-1297
28. Schreck, C., and O'Connor, P. M. (2011) NAD (P) H oxidase and renal epithelial ion transport. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1023-R1029
29. Zhang, C, Imam, S. Z., Ali, S. F., and Mayeux, P. R. (2002) Peroxynitrite and the regulation of Na+, K+-ATPase activity by angiotensin II in the rat proximal tubule. Nitric Oxide 7, 30-35
30. Han, H. J., Lee, Y. J., Park, S. H., Lee, J. H., and Taub, M. (2005) High glucose-induced oxidative stress inhibits Na+/glucose cotransporter activity in renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 288, F988-F996
31. Liang, M., Cai, T., Tian, J., Qu, W., and Xie, Z. J. (2006) Functional characterization of Src-interacting Na/K-ATPase using RNA interference assay. J. Biol. Chem. 281, 19709-19719
32. Liang, M., Tian, J., Liu, L., Pierre, S., Liu, J., Shapiro, J., and Xie, Z. J. (2007) Identification of a pool of non-pumping Na/K-ATPase. J. Biol. Chem. 282, 10585-10593
33. Young, M. A., Gonfloni, S., Superti-Furga, G., Roux, B., and Kuriyan, J. (2001) Dynamic coupling between the SH2 and SH3 domains of c-Srcand Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105, 115-126
34. Bagrov, A. Y., and Shapiro, J. I. (2008) Endogenous digitalis: pathophysiologic roles and therapeutic applications. Nat. Clin. Pract. Nephrol. 4, 378-392
35. Blaustein, M. P., Zhang, J., Chen, L., Song, H, Raina, H, Kinsey, S. P., Izuka, M., Iwamoto, T., Kotlikoff, M. I., Lingrel, J. B., Philipson, K. D., Wier, W. G., and Hamlyn, J. M. (2009) The pump, the exchanger, and endogenous ouabain: signaling mechanisms that link salt retention to hypertension. Hypertension 53, 291-298
36. Schoner, W., and Scheiner-Bobis, G. (2008) Role of endogenous cardiotonic steroids in sodium homeostasis. Nephrol. Dial. Transplant. 23, 2723-2729
37. Dostanic-Larson, I., Van Huysse, J. W., Lorenz, J. N, and Lingrel, J. B. (2005) The highly conserved cardiac glycoside-binding site of Na, K-ATPase plays a role in blood pressure regulation. Proc. Natl. Acad. Sci. U. S. A. 102, 15845-15850
38. Loreaux, E. L., Kaul, B., Lorenz, J. N, and Lingrel, J. B. (2008) Ouabainsensitive a1 Na, K-ATPase enhances natriuretic response to saline load. J. Am. Soc. Nephrol. 19, 1947-1954
39. Nesher, M., Dvela, M., Igbokwe, V. U., Rosen, H, and Lichtstein, D. (2009) Physiological roles of endogenous ouabain in normal rats. Am. J. Physiol. Heart Circ. Physiol. 297, H2026-H2034
40. Kennedy, D. J., Vetteth, S., Periyasamy, S. M., Kanj, M., Fedorova, L., Khouri, S., Kahaleh, M. B., Xie, Z., Malhotra, D., Kolodkin, N. I., Lakatta, E. G., Fedorova, O. V., Bagrov, A. Y., and Shapiro, J. I. (2006) Central role for the cardiotonic steroid marinobufagenin in the pathogenesis of experimental uremic cardiomyopathy. Hypertension 47, 488-495
41. Kennedy, D. J., Vetteth, S., Xie, M., Periyasamy, S. M., Xie, Z., Han, C, Basrur, V., Mutgi, K., Fedorov, V., Malhotra, D., and Shapiro, J. I. (2006) Ouabain decreases sarco (endo) plasmic reticulum calcium ATPase activity in rat hearts by a process involving protein oxidation. Am. J. Physiol. Heart Circ. Physiol. 291, H3003-H3011
42. Giannoni, E., Buricchi, F., Raugei, G., Ramponi, G., and Chiarugi, P. (2005) Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol. Cell. Biol. 25, 6391-6403
43. Gross, C. L., Innace, J. K., Hovatter, R. C, Meier, H. L., and Smith, W. J. (1993) Biochemical manipulation of intracellular glutathione levels influences cytotoxicity to isolated human lymphocytes by sulfur mustard. Cell Biol. Toxicol. 9, 259-267
44. Bizzozero, O. A., Ziegler, J. L., De Jesus, G., and Bolognani, F. (2006) Acute depletion of reduced glutathione causes extensive carbonylation of rat brain proteins. J. Neurosci. Res. 83, 656-667
45. Dasgupta, A., Zheng, J., and Bizzozero, O. A. (2012) Protein carbonylation and aggregation precede neuronal apoptosis induced by partial glutathione depletion. ASNNeuro. 4, e00084
46. Zheng, J., and Bizzozero, O. A. (2010) Traditional reactive carbonyl scavengers do not prevent the carbonylation of brain proteins induced by acute glutathione depletion. Free Radic. Res. 44, 258-266
47. Yan, Y., Haller, S., Shapiro, A., Malhotra, N, Tian, J., Xie, Z., Malhotra, D., Shapiro, J. I., and Liu, J. (2012) Ouabain-stimulated trafficking regulation of the Na/K-ATPase and NHE3 in renal proximal tubule cells. Mol. Cell. Biochem. 367, 175-183
48. Liu, J., Periyasamy, S. M., Gunning, W., Fedorova, O. V., Bagrov, A. Y., Malhotra, D., Xie, Z., and Shapiro, J. I. (2002) Effects of cardiac glycosides on sodium pump expression and function in LLC-PK1 and MDCK cells. Kidney Int. 62, 2118-2125
49. Wong, C. M., Marcocci, L., Liu, L., and Suzuki, Y. J. (2010) Cell signaling by protein carbonylation and decarbonylation. Antioxid. Redox Signal. 12, 393-404
50. Yatime, L., Laursen, M., Morth, J. P., Esmann, M., Nissen, P., and Fedosova, N. U. (2011) Structural insights into the high affinity binding of cardiotonic steroids to the Na+, K+-ATPase. J. Struct. Biol. 174, 296-306