Hugh davson distinguished lectureship of the cell and molecular physiology section, 2015: Na+-k+-ATPase, a new class of plasma membrane receptors

American Journal of Physiology - Cell Physiology

Volumn 310, Issue 7, 2016, Pages C491-C495

  Aperia, Anita ^a   Akkuratov, Evgeny E ^a   Fontana, Jacopo Maria ^b   Brismar, Hjalmar ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Apoptosis; Na+ K+ ATPase; Ouabain; Receptor; Signaling

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM); CELL SURFACE RECEPTOR;

CELL MEMBRANE; CONFORMATIONAL TRANSITION; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; MITOCHONDRION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM; PHYSIOLOGY;

ANIMALS; HUMANS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84971329563     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00359.2015     Document Type: Review

References (74)

1. Abramowitz J, Dai C, Hirschi KK, Dmitrieva RI, Doris PA, Liu L, Allen JC. Ouabain- and marinobufagenin-induced proliferation of human umbilical vein smooth muscle cells and a rat vascular smooth muscle cell line, A7r5. Circulation 108: 3048–3053, 2003.
2. Aizman O, Uhlén P, Lal M, Brismar H, Aperia A. Ouabain, a steroid hormone that signals with slow calcium oscillations. Proc Natl Acad Sci U S A 98: 13420–13424, 2001.
3. Allen JC, Abramowitz J, Koksoy A. Low concentrations of ouabain activate vascular smooth muscle cell proliferation. Ann N Y Acad Sci 986: 504–508, 2003.
4. Aperia A. New roles for an old enzyme: Na, K-ATPase emerges as an interesting drug target. J Intern Med 261: 44–52, 2007.
5. Aydemir-Koksoy A, Abramowitz J, Allen JC. Ouabain-induced signaling and vascular smooth muscle cell proliferation. J Biol Chem 276: 46605–46611, 2001.
6. Bagrov AY, Shapiro JI, Fedorova OV. Endogenous cardiotonic steroids: physiology, pharmacology, and novel therapeutic targets. Pharmacol Rev 61: 9–38, 2009.
7. Blanco G. Na,K-ATPase subunit heterogeneity as a mechanism for tissue-specific ion regulation. Semin Nephrol 25: 292–303, 2005.
8. Blanco G, Wallace DP. Novel role of ouabain as a cystogenic factor in autosomal dominant polycystic kidney disease. Am J Physiol Renal Physiol 305: F797–F812, 2013.
9. Blaustein MP. Why isn’t endogenous ouabain more widely accepted? Am J Physiol Heart Circ Physiol 307: H635–H639, 2014.
10. Bublitz M, Poulsen H, Morth JP, Nissen P. In and out of the cation pumps: P-type ATPase structure revisited. Curr Opin Struct Biol 20: 431–439, 2010.
11. Burlaka I, Liu XL, Rebetz J, Arvidsson I, Yang L, Brismar H, Karpman D, Aperia A. Ouabain protects against Shiga toxin-triggered apoptosis by reversing the imbalance between Bax and Bcl-xL. J Am Soc Nephrol 24: 1413–1423, 2013.
12. Calderón-Montaño JM, Burgos-Morón E, Orta ML, Maldonado- Navas D, García-Domínguez I, López-Lázaro M. Evaluating the cancer therapeutic potential of cardiac glycosides. Biomed Res Int 2014: 794930, 2014.
13. Crank J. The Mathematics of Diffusion. Oxford, UK: Clarendon, 1979.
14. 2+ oscillations. Science 279: 227–230, 1998.
15. D’Urso G, Frascarelli S, Zucchi R, Biver T, Montali U. Cardioprotection by ouabain and digoxin in perfused rat hearts. J Cardiovasc Pharmacol 52: 333–337, 2008.
16. Dvela-Levitt M, Ami HCB, Rosen H, Shohami E, Lichtstein D. Ouabain improves functional recovery following traumatic brain injury. J Neurotrauma 31: 1942–1947, 2014.
17. Dvela-Levitt M, Cohen-Ben Ami H, Rosen H, Ornoy A, Hochner- Celnikier D, Granat M, Lichtstein D. Reduction in maternal circulating ouabain impairs offspring growth and kidney development. J Am Soc Nephrol 26: 1103–1114, 2015.
18. Dvela M, Rosen H, Ben-Ami HC, Lichtstein D. Endogenous ouabain regulates cell viability. Am J Physiol Cell Physiol 302: C442–C452, 2012.
19. 2+ oscillations. Cell Calcium 50: 424–432, 2011.
20. Fontana JM, Burlaka I, Khodus G, Brismar H, Aperia A. Calcium oscillations triggered by cardiotonic steroids. FEBS J 280: 5450–5455, 2013.
21. +-ATPase. Biochem Biophys Res Commun 446: 1151–1154, 2014.
22. +-ATPase in cardiac myocytes. Biophys J 105: 2695–2705, 2013.
23. Garlid KD, Costa ADT, Quinlan CL, Pierre SV, Dos Santos P. Cardioprotective signaling to mitochondria. J Mol Cell Cardiol 46: 858–866, 2009.
24. +- ATPase-mediated SFK-activated signalling pathway that regulates tight junction function in the mouse blastocyst. PloS One 6: e23704, 2011.
25. +-ATPase. J Biol Chem 275: 27832–27837, 2000.
26. Hamlyn JM, Blaustein MP, Bova S, DuCharme DW, Harris DW, Mandel F, Mathews WR, Ludens JH. Identification and characterization of a ouabain-like compound from human plasma. Proc Natl Acad Sci U S A 88: 6259–6263, 1991.
27. Jacobs BE, Liu Y, Pulina MV, Golovina VA, Hamlyn JM. Normal pregnancy: mechanisms underlying the paradox of a ouabain-resistant state with elevated endogenous ouabain, suppressed arterial sodium calcium exchange, and low blood pressure. Am J Physiol Heart Circ Physiol 302: H1317–H1329, 2012.
28. Jansson K, Nguyen ANT, Magenheimer BS, Reif GA, Aramadhaka LR, Bello-Reuss E, Wallace DP, Calvet JP, Blanco G. Endogenous concentrations of ouabain act as a cofactor to stimulate fluid secretion and cyst growth of in vitro ADPKD models via cAMP and EGFR-Src-MEK pathways. Am J Physiol Renal Physiol 303: F982–F990, 2012.
29. Kaplan JH. Biochemistry of Na, K-ATPase. Annu Rev Biochem 71: 511–535, 2002.
30. Karlish SJ, Stein WD. Cation activation of the pig kidney sodium pump: transmembrane allosteric effects of sodium. J Physiol 359: 119–149, 1985.
31. Kennedy DJ, Vetteth S, Periyasamy SM, Kanj M, Fedorova L, Khouri S, Kahaleh MB, Xie Z, Malhotra D, Kolodkin NI, Lakatta EG, Fedorova OV, Bagrov AY, Shapiro JI. Central role for the cardiotonic steroid marinobufagenin in the pathogenesis of experimental uremic cardiomyopathy. Hypertension 47: 488–495, 2006.
32. Khodus GR, Kruusmägi M, Li J, Liu XL, Aperia A. Calcium signaling triggered by ouabain protects the embryonic kidney from adverse developmental programming. Pediatr Nephrol 26: 1479–1482, 2011.
33. Khundmiri SJ, Metzler MA, Ameen M, Amin V, Rane MJ, Delamere NA. Ouabain induces cell proliferation through calcium-dependent phosphorylation of Akt (protein kinase B) in opossum kidney proximal tubule cells. Am J Physiol Cell Physiol 291: C1247–C1257, 2006.
34. Kolmakova EV, Haller ST, Kennedy DJ, Isachkina AN, Budny GV, Frolova EV, Piecha G, Nikitina ER, Malhotra D, Fedorova OV, Shapiro JI, Bagrov AY. Endogenous cardiotonic steroids in chronic renal failure. Nephrol Dial Transplant 26: 2912–2919, 2011.
35. +-ATPase to growth-related genes in cardiac myocytes. The roles of Ras and mitogen-activated protein kinases. J Biol Chem 273: 15249–15256, 1998.
36. Komiyama Y, Dong XH, Nishimura N, Masaki H, Yoshika M, Masuda M, Takahashi H. A novel endogenous digitalis, telocinobufagin, exhibits elevated plasma levels in patients with terminal renal failure. Clin Biochem 38: 36–45, 2005.
37. Lauf PK, Alqahtani T, Flues K, Meller J, Adragna NC. Interaction between Na-K-ATPase and Bcl-2 proteins BclXL and Bak. Am J Physiol Cell Physiol 308: C51–C60, 2015.
38. Lewis LK, Yandle TG, Hilton PJ, Jensen BP, Begg EJ, Nicholls MG. Endogenous ouabain is not ouabain. Hypertension 64: 680–683, 2014.
39. Li J, Khodus GR, Kruusmägi M, Kamali-Zare P, Liu XL, Eklöf AC, Zelenin S, Brismar H, Aperia A. Ouabain protects against adverse developmental programming of the kidney. Nat Commun 1: 42, 2010.
40. Li J, Zelenin S, Aperia A, Aizman O. Low doses of ouabain protect from serum deprivation-triggered apoptosis and stimulate kidney cell proliferation via activation of NF-kappaB. J Am Soc Nephrol 17: 1848–1857, 2006.
41. Li Z, Xie Z. The Na/K-ATPase/Src complex and cardiotonic steroidactivated protein kinase cascades. Pflügers Arch 457: 635–644, 2009.
42. Lingrel JB. The physiological significance of the cardiotonic steroid/ ouabain-binding site of the Na,K-ATPase. Annu Rev Physiol 72: 395–412, 2010.
43. Liu L, Zhao X, Pierre SV, Askari A. Association of PI3K-Akt signaling pathway with digitalis-induced hypertrophy of cardiac myocytes. Am J Physiol Cell Physiol 293: C1489–C1497, 2007.
44. Liu X, Spicarová Z, Rydholm S, Li J, Brismar H, Aperia A. Ankyrin B modulates the function of Na,K-ATPase/inositol 1,4,5-trisphosphate receptor signaling microdomain. J Biol Chem 283: 11461–11468, 2008.
45. +-ATPase subunit. Am J Physiol Heart Circ Physiol 295: H273–H280, 2008.
46. +-ATPase α1 isoform mediates ouabain-induced expression of cyclin D1 and proliferation of rat sertoli cells. Reproduction 144: 737–745, 2012.
47. Menger L, Vacchelli E, Kepp O, Eggermont A, Tartour E, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: cardiac glycosides and cancer therapy. Oncoimmunology 2: e23082, 2013.
48. Miyakawa-Naito A, Uhlén P, Lal M, Aizman O, Mikoshiba K, Brismar H, Zelenin S, Aperia A. Cell signaling microdomain with Na,KATPase and inositol 1,4,5-trisphosphate receptor generates calcium oscillations. J Biol Chem 278: 50355–50361, 2003.
49. Morgan EE, Li Z, Stebal C, Belliard A, Tennyson G, Salari B, Garlid KD, Pierre SV. Preconditioning by subinotropic doses of ouabain in the Langendorff perfused rabbit heart. J Cardiovasc Pharmacol 55: 234–239, 2010.
50. Nesher M, Shpolansky U, Viola N, Dvela M, Buzaglo N, Cohen Ben-Ami H., Rosen H., Lichtstein D. Ouabain attenuates cardiotoxicity induced by other cardiac steroids. Br J Pharmacol 160: 346–354, 2010.
51. Nguyen ANT, Wallace DP, Blanco G. Ouabain binds with high affinity to the Na,K-ATPase in human polycystic kidney cells and induces extracellular signal-regulated kinase activation and cell proliferation. J Am Soc Nephrol 18: 46–57, 2007.
52. +-bound state. Science 342: 123–127, 2013.
53. +-ATPase) with bound potassium and ouabain. Proc Natl Acad Sci U S A 106: 13742–13747, 2009.
54. Oshiro N, Dostanic-Larson I, Neumann JC, Lingrel JB. The ouabainbinding site of the α2 isoform of Na,K-ATPase plays a role in blood pressure regulation during pregnancy. Am J Hypertens 23: 1279–1285, 2010.
55. Pasdois P, Quinlan CL, Rissa A, Tariosse L, Vinassa B, Costa ADT, Pierre SV, Dos Santos P, Garlid KD. Ouabain protects rat hearts against ischemia-reperfusion injury via pathway involving src kinase, mitoKATP, and ROS. Am J Physiol Heart Circ Physiol 292: H1470–H1478, 2007.
56. Peng M, Huang L, Xie Z, Huang WH, Askari A. Partial inhibition of Na/K-ATPase by ouabain induces the Ca-dependent expressions of earlyresponse genes in cardiac myocytes. J Biol Chem 271: 10372–10378, 1996.
57. Pierre SV, Xie Z. The Na,K-ATPase receptor complex: its organization and membership. Cell Biochem Biophys 46: 303–316, 2006.
58. +-ATPase signaling cascade in rat hearts. Cardiovasc Res 73: 488–496, 2007.
59. Ponce A, Larre I, Castillo A, García-Villegas R, Romero A, Flores- Maldonado C, Martinez-Rendón J, Contreras RG, Cereijido M. Ouabain increases gap junctional communication in epithelial cells. Cell Physiol Biochem 34: 2081–2090, 2014.
60. Quinlan CL, Costa ADT, Costa CL, Pierre SV, Dos Santos P, Garlid KD. Conditioning the heart induces formation of signalosomes that interact with mitochondria to open mitoKATP channels. Am J Physiol Heart Circ Physiol 295: H953–H961, 2008.
61. +-ATPase. Cell Mol Life Sci 70: 205–222, 2013.
62. de Rezende Corrêa G, Araujo dos Santos A, Frederico Leite Fontes C, Giestal de Araujo E. Ouabain induces an increase of retinal ganglion cell survival in vitro: the involvement of protein kinase C. Brain Res 1049: 89–94, 2005.
63. Schneider R, Wray V, Nimtz M, Lehmann WD, Kirch U, Antolovic R, Schoner W. Bovine adrenals contain, in addition to ouabain, a second inhibitor of the sodium pump. J Biol Chem 273: 784–792, 1998.
64. Schrier RW. Renal volume, renin-angiotensin-aldosterone system, hypertension, and left ventricular hypertrophy in patients with autosomal dominant polycystic kidney disease. J Am Soc Nephrol 20: 1888–1893, 2009.
65. 2+ overload and neuronal apoptosis in excitotoxic stress. J Pharmacol Exp Ther 343: 596–607, 2012.
66. +-ATPase forms a functional signaling complex. Mol Biol Cell 17: 317–326, 2006.
67. Tian J, Liu J, Garlid KD, Shapiro JI, Xie Z. Involvement of mitogen-activated protein kinases and reactive oxygen species in the inotropic action of ouabain on cardiac myocytes. A potential role for mitochondrial K(ATP) channels. Mol Cell Biochem 242: 181–187, 2003.
68. Tian J, Li X, Liang M, Liu L, Xie JX, Ye Q, Kometiani P, Tillekeratne M, Jin R, Xie Z. Changes in sodium pump expression dictate the effects of ouabain on cell growth. J Biol Chem 284: 14921–14929, 2009.
69. Vella A, Gerber TC, Hayes DL, Reeder GS. Digoxin, hypercalcaemia, and cardiac conduction. Postgrad Med J 75: 554–556, 1999.
70. Weigand KM, Swarts HGP, Fedosova NU, Russel FGM, Koenderink JB. Na,K-ATPase activity modulates Src activation: a role for ATP/ADP ratio. Biochim Biophys Acta 1818: 1269–1273, 2012.
71. +-ATPase: activation of phosphatidylinositide 3-kinase IA/Akt by ouabain is independent of Src. Biochemistry (Mosc) 52: 9059–9067, 2013.
72. Wu J, Li D, Du L, Baldawi M, Gable ME, Askari A, Liu L. Ouabain prevents pathological cardiac hypertrophy and heart failure through activation of phosphoinositide 3-kinase α in mouse. Cell Biosci 5: 64, 2015.
73. Zhang S, Malmersjö S, Li J, Ando H, Aizman O, Uhlén P, Mikoshiba K, Aperia A. Distinct role of the N-terminal tail of the Na,K-ATPase catalytic subunit as a signal transducer. J Biol Chem 281: 21954–21962, 2006.
74. 2+ signaling in arterial smooth muscle cells. Am J Physiol Cell Physiol 304: C324–C333, 2013.