Inhibiting Na+/K+ ATPase can impair mitochondrial energetics and induce abnormal Ca2+ cycling and automaticity in guinea pig cardiomyocytes

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Li, Qince ^a,c   Pogwizd, Steven M ^a,b,c   Prabhu, Sumanth D ^a,c   Zhou, Lufang ^a,b,c  

^a University of Alabama at Birmingham   (United States)

^b and Radiation Oncology   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM ION; CARDIAC GLYCOSIDE; SODIUM CALCIUM EXCHANGE PROTEIN; ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CALCIUM; ION; REACTIVE OXYGEN METABOLITE;

ACTION POTENTIAL; ANIMAL CELL; ANTIARRHYTHMIC ACTIVITY; ARRHYTHMOGENESIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME METABOLISM; GUINEA PIG; HEART AUTOMATICITY; HEART MUSCLE CELL; MITOCHONDRIAL ENERGY TRANSFER; NONHUMAN; OXIDATIVE STRESS; WORKLOAD; ANIMAL; COMPUTER SIMULATION; CYTOLOGY; ENZYMOLOGY; HEART ARRHYTHMIA; HOMEOSTASIS; MEMBRANE POTENTIAL; METABOLISM; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIOXIDANTS; ARRHYTHMIAS, CARDIAC; CALCIUM; COMPUTER SIMULATION; GUINEA PIGS; HOMEOSTASIS; IONS; MEMBRANE POTENTIALS; MITOCHONDRIA; MYOCYTES, CARDIAC; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84899570545     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093928     Document Type: Article

References (56)

1. Liu T, Brown DA, O'Rourke B (2010) Role of mitochondrial dysfunction in cardiac glycoside toxicity. J Mol Cell Cardiol 49: 728-736.
2. Rahimtoola SH (2004) Digitalis therapy for patients in clinical heart failure. Circulation 109: 2942-2946.
3. Bers DM, Despa S (2009) Na+ transport in cardiac myocytes; Implications for excitation-contraction coupling. IUBMB Life 61: 215-221.
4. Hashim T, Elbaz S, Patel K, Morgan CJ, Fonarow GC, et al. (2013) Digoxin and 30-day All-cause Hospital Admission in Older Patients with Chronic Diastolic Heart Failure. The American journal of medicine.
5. Gonano LA, Sepulveda M, Rico Y, Kaetzel M, Valverde CA, et al. (2011) Calcium-calmodulin kinase II mediates digitalis-induced arrhythmias. Circ Arrhythm Electrophysiol 4: 947-957.
6. Rathore SS, Curtis JP, Wang Y, Bristow MR, Krumholz HM (2003) Association of serum digoxin concentration and outcomes in patients with heart failure. JAMA 289: 871-878.
7. Campia I, Sala V, Kopecka J, Leo C, Mitro N, et al. (2012) Digoxin and ouabain induce the efflux of cholesterol via liver X receptor signalling and the synthesis of ATP in cardiomyocytes. Biochem J 447: 301-311.
8. Ferrier GR (1977) Digitalis arrhythmias: role of oscillatory afterpotentials. Prog Cardiovasc Dis 19: 459-474.
9. Roberts BN, Christini DJ (2011) NHE Inhibition Does Not Improve Na+ or Ca2+ Overload During Reperfusion: Using Modeling to Illuminate the Mechanisms Underlying a Therapeutic Failure. Plos Computational Biology 7.
10. Maack C, Cortassa S, Aon MA, Ganesan AN, Liu T, et al. (2006) Elevated cytosolic Na+ decreases mitochondrial Ca2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ Res 99: 172-182.
11. Liu T, O'Rourke B (2008) Enhancing mitochondrial Ca2+ uptake in myocytes from failing hearts restores energy supply and demand matching. Circ Res 103: 279-288.
12. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476: 336-340.
13. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, et al. (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476: 341-345.
14. Dedkova EN, Blatter LA (2008) Mitochondrial Ca2+ and the heart. Cell Calcium 44: 77-91.
15. Liu T, O'Rourke B (2009) Regulation of mitochondrial Ca2+ and its effects on energetics and redox balance in normal and failing heart. J Bioenerg Biomembr 41: 127-132.
16. O'Rourke B, Blatter LA (2009) Mitochondrial Ca2+ uptake: tortoise or hare? J Mol Cell Cardiol 46: 767-774.
17. Denton RM, McCormack JG (1985) Ca2+ transport by mammalian mitochondria and its role in hormone action. Am J Physiol 249: E543-554.
18. Huser J, Blatter LA, Sheu SS (2000) Mitochondrial calcium in heart cells: beat-to-beat oscillations or slow integration of cytosolic transients? J Bioenerg Biomembr 32: 27-33.
19. Bassani JW, Bassani RA, Bers DM (1994) Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476: 279-293.
20. Bassani RA, Bassani JW, Bers DM (1992) Mitochondrial and sarcolemmal Ca2+ transport reduce [Ca2+]i during caffeine contractures in rabbit cardiac myocytes. J Physiol 453: 591-608.
21. Chen Y, Csordas G, Jowdy C, Schneider TG, Csordas N, et al. (2012) Mitofusin 2-containing mitochondrial-reticular microdomains direct rapid cardiomyocyte bioenergetic responses via interorganelle Ca2+ crosstalk. Circ Res 111: 863-875.
22. Csordas G, Hajnoczky G (2009) SR/ER-mitochondrial local communication: calcium and ROS. Biochim Biophys Acta 1787: 1352-1362.
23. Csordás G, Hajnóczky G (2009) SR/ER-mitochondrial local communication: Calcium and ROS. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1787: 1352-1362.
24. Sharma VK, Ramesh V, Franzini-Armstrong C, Sheu SS (2000) Transport of Ca2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. J Bioenerg Biomembr 32: 97-104.
25. Berridge MJ (2006) Calcium microdomains: organization and function. Cell Calcium 40: 405-412.
26. Franzini-Armstrong C (2007) ER-mitochondria communication. How privileged? Physiology (Bethesda) 22: 261-268.
27. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86: 369-408.
28. Ramesh V, Sharma VK, Sheu SS, Franzini-Armstrong C (1998) Structural proximity of mitochondria to calcium release units in rat ventricular myocardium may suggest a role in Ca2+ sequestration. Ann NY Acad Sci 853: 341-344.
29. Rizzuto R, Duchen MR, Pozzan T (2004) Flirting in little space: the ER/mitochondria Ca2+ liaison. Sci STKE 2004: re1.
30. Yan Y, Liu J, Wei C, Li K, Xie W, et al. (2008) Bidirectional regulation of Ca2+ sparks by mitochondria-derived reactive oxygen species in cardiac myocytes. Cardiovasc Res 77: 432-441.
31. Zhou L, Aon MA, Liu T, O'Rourke B (2011) Dynamic modulation of Ca(2+) sparks by mitochondrial oscillations in isolated guinea pig cardiomyocytes under oxidative stress. Journal of molecular and cellular cardiology 51: 632-639.
32. Florea SM, Blatter LA (2010) The role of mitochondria for the regulation of cardiac alternans. Front Physiol 1: 141.
33. Florea SM, Blatter LA (2012) Regulation of cardiac alternans by beta-adrenergic signaling pathways. Am J Physiol Heart Circ Physiol 303: H1047-1056.
34. Smith RM, Visweswaran R, Talkachova I, Wothe JK, Tolkacheva EG (2013) Uncoupling the mitochondria facilitates alternans formation in the isolated rabbit heart. Am J Physiol Heart Circ Physiol 305: H9-H18.
35. Zhou L, Cortassa S, Wei AC, Aon MA, Winslow RL, et al. (2009) Modeling cardiac action potential shortening driven by oxidative stress-induced mitochondrial oscillations in guinea pig cardiomyocytes. Biophys J 97: 1843-1852.
36. Wei AC, Aon MA, O'Rourke B, Winslow RL, Cortassa S (2011) Mitochondrial energetics, pH regulation, and ion dynamics: a computational-experimental approach. Biophys J 100: 2894-2903.
37. Kembro JM, Aon MA, Winslow RL, O'Rourke B, Cortassa S (2013) Integrating mitochondrial energetics, redox and ROS metabolic networks: a two-compartment model. Biophys J 104: 332-343.
38. Cortassa S, Aon MA, O'Rourke B, Jacques R, Tseng HJ, et al. (2006) A computational model integrating electrophysiology, contraction, and mitochondrial bioenergetics in the ventricular myocyte. Biophys J 91: 1564-1589.
39. Brandes R, Bers DM (1999) Analysis of the mechanisms of mitochondrial NADH regulation in cardiac trabeculae. Biophys J 77: 1666-1682.
40. Brandes R, Bers DM (1997) Intracellular Ca2+ increases the mitochondrial NADH concentration during elevated work in intact cardiac muscle. Circ Res 80: 82-87.
41. Brandes R, Bers DM (2002) Simultaneous measurements of mitochondrial NADH and Ca(2+) during increased work in intact rat heart trabeculae. Biophys J 83: 587-604.
42. Kajikawa M, Tsuura Y, Mukai E, Takeda T, Hamamoto Y, et al. (2002) Ouabain Suppresses Glucose-Induced Mitochondrial ATP Production and Insulin Release by Generating Reactive Oxygen Species in Pancreatic Islets. Diabetes 51: 2522-2529.
43. Ishida H, Kohmoto O, Bridge JH, Barry WH (1988) Alterations in cation homeostasis in cultured chick ventricular cells during and after recovery from adenosine triphosphate depletion. J Clin Invest 81: 1173-1181.
44. Fedida D, Noble D, Rankin AC, Spindler AJ (1987) The arrhythmogenic transient inward current iTI and related contraction in isolated guinea-pig ventricular myocytes. J Physiol 392: 523-542.
45. Li Q, O'Neill SC, Tao T, Li Y, Eisner D, et al. (2012) Mechanisms by which cytoplasmic calcium wave propagation and alternans are generated in cardiac atrial myocytes lacking T-tubules-insights from a simulation study. Biophys J 102: 1471-1482.
46. Mackenzie L, Roderick HL, Berridge MJ, Conway SJ, Bootman MD (2004) The spatial pattern of atrial cardiomyocyte calcium signalling modulates contraction. J Cell Sci 117: 6327-6337.
47. Bers DM (2001) Excitation-Contraction Coupling and Cardiac Contractile Force edn 2 Kluwer Academic, Dordrecht, Netherlands.
48. Magnus G, Keizer J (1998) Model of β-cell mitochondrial calcium handling and electrical activity. I.Cytoplasmic variables. Am J Physiol Cell Physiol 274: C1158-1173.
49. Matsuoka S, Sarai N, Jo H, Noma A (2004) Simulation of ATP metabolism in cardiac excitation-contraction coupling. Prog Biophys Mol Biol 85: 279-299.
50. Greenstein JL, Hinch R, Winslow RL (2006) Mechanisms of excitation-contraction coupling in an integrative model of the cardiac ventricular myocyte. Biophys J 90: 77-91.
51. Gauthier LD, Greenstein JL, Winslow RL (2012) Toward an integrative computational model of the Guinea pig cardiac myocyte. Front Physiol 3: 244.
52. Xie LH, Chen F, Karagueuzian HS, Weiss JN (2009) Oxidative-stress-induced afterdepolarizations and calmodulin kinase II signaling. Circ Res 104: 79-86.
53. Barrington PL, Meier CF Jr, Weglicki WB (1988) Abnormal electrical activity induced by free radical generating systems in isolated cardiocytes. J Mol Cell Cardiol 20: 1163-1178.
54. Horackova M, Ponka P, Byczko Z (2000) The antioxidant effects of a novel iron chelator salicylaldehyde isonicotinoyl hydrazone in the prevention of H(2)O(2) injury in adult cardiomyocytes. Cardiovasc Res 47: 529-536.
55. Gauthier LD, Greenstein JL, Cortassa S, O'Rourke B, Winslow RL (2013) A computational model of reactive oxygen species and redox balance in cardiac mitochondria. Biophys J 105: 1045-1056.
56. Akar FG, Aon MA, Tomaselli GF, O'Rourke B (2005) The mitochondrial origin of postischemic arrhythmias. J Clin Invest 115: 3527-3535.