PKCe{open} mediates serine phosphorylation of connexin43 induced by lysophosphatidylcholine in neonatal rat cardiomyocytes

Toxicology

Volumn 314, Issue 1, 2013, Pages 11-21

  Liao, Chih Kai ^a   Cheng, Hsiang Hsi ^a   Wang, Sheng De ^a   Yeih, Dong Feng ^a   Wang, Seu Mei ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Cardiomyocytes; Connexin43; Gap junction; Lysophosphatidylcholine; PKCe open ; Serine 368 phosphorylation

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CONNEXIN 43; LYSOPHOSPHATIDYLCHOLINE; PROTEIN KINASE C EPSILON; SERINE; UBIQUITIN; COLORING AGENT; INDOLE DERIVATIVE; SMALL INTERFERING RNA; TETRAZOLIUM; THIAZOLE DERIVATIVE; THIAZOLYL BLUE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL COMMUNICATION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GAP JUNCTION; HEART ARRHYTHMIA; HEART CONTRACTION; HEART MUSCLE CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LYSOSOME; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; UBIQUITINATION; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; HEART RATE; METABOLISM; PHOSPHORYLATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL SURVIVAL; COLORING AGENTS; CONNEXIN 43; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HEART RATE; IMMUNOPRECIPITATION; INDOLES; LYSOPHOSPHATIDYLCHOLINES; MALE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SERINE; TETRAZOLIUM SALTS; THIAZOLES;

EID: 84884708157     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.08.001     Document Type: Article

References (55)

1. Arnsdorf M.F., Sawicki G.J. The effects of lysophosphatidylcholine, a toxic metabolite of ischemia, on the components of cardiac excitability in sheep Purkinje fibers. Circ. Res. 1981, 49:16-30.
2. Bayer N., Schober D., Prchla E., Murphy R.F., Blaas D., Fuchs R. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J. Virol. 1998, 72:9645-9655.
3. Bowling N., Huang X., Sandusky G.E., Fouts R.L., Mintze K., Esterman M., Allen P.D., Maddi R., McCall E., Vlahos C.J. Protein kinase C-alpha and -epsilon modulate connexin-43 phosphorylation in human heart. J. Mol. Cell. Cardiol. 2001, 33:789-798.
4. Catarino S., Ramalho J.S., Marques C., Pereira P., Girao H. Ubiquitin-mediated internalization of connexin43 is independent of the canonical endocytic tyrosine-sorting signal. Biochem. J. 2011, 437:255-267.
5. Carter C.A. Protein kinase C as a drug target: implications for drug or dietprevention and treatment of cancer. Curr. Drug Targets 2000, 1:163-183.
6. Clarkson C.W., Ten Eick R.E. On the mechanism of lysophosphatidylcholine-induced depolarization of cat ventricular myocardium. Circ. Res. 1983, 52:543-556.
7. Corr P.B., Snyder D.W., Lee B.I., Gross R.W., Keim C.R., Sobel B.E. Pathophysiological concentrations of lysophosphatides and the slow response. Am. J. Physiol. 1982, 243:H187-H195.
8. Daleau P. Lysophosphatidylcholine, a metabolite which accumulates early in myocardium during ischemia, reduces gap junctional coupling in cardiac cells. J. Mol. Cell. Cardiol. 1999, 31:1391-1401.
9. Doble B.W., Ping P., Kardami E. The epsilon subtype of protein kinase C is required for cardiomyocyte connexin-43 phosphorylation. Circ. Res. 2000, 86:293-301.
10. Ek-Vitorin J.F., King T.J., Heyman N.S., Lampe P.D., Burt J.M. Selectivity of connexin 43 channels is regulated through protein kinase C-dependent phosphorylation. Circ. Res. 2006, 98:1498-1505.
11. El-Sherif N., Turitto G. Electrolyte disorders and arrhythmogenesis. Cardiol. J. 2011, 18:233-245.
12. Fykerud T.A., Kjenseth A., Schink K.O., Sirnes S., Bruun J., Omori Y., Brech A., Rivedal E., Leithe E. Smad ubiquitination regulatory factor-2 controls gap junction intercellular communication by modulating endocytosis and degradation of connexin43. J. Cell. Sci. 2012, 125:3966-3976.
13. Girao H., Pereira P. The proteasome regulates the interaction between Cx43 and ZO-1. J. Cell. Biochem. 2007, 102:719-728.
14. Gizurarson S., Shao Y., Miljanovic A., Ramunddal T., Boren J., Bergfeldt L., Omerovic E. Electrophysiological effects of lysophosphatidylcholine on HL-1 cardiomyocytes assessed with a microelectrode array system. Cell. Physiol. Biochem. 2012, 30:477-488.
15. Guerrero P.A., Schuessler R.B., Davis L.M., Beyer E.C., Johnson C.M., Yamada K.A., Saffitz J.E. Slow ventricular conduction in mice heterozygous for a connexin43 null mutation. J. Clin. Invest. 1997, 99:1991-1998.
16. Gumpert A.M., Varco J.S., Baker S.M., Piehl M., Falk M.M. Double-membrane gap junction internalization requires the clathrin-mediated endocytic machinery. FEBS. Lett. 2008, 582:2887-2892.
17. Hashizume H., Abiko Y. Cardiac cell injury induced by lysophosphatidylcholine. Nihon Yakurigaku Zasshi 1999, 114:287-293.
18. Hoque A.N., Hoque N., Hashizume H., Abiko Y. A study on dilazep: II. Dilazep attenuates lysophosphatidylcholine-induced mechanical and metabolic derangements in the isolated, working rat heart. Jpn. J. Pharmacol. 1995, 67:233-241.
19. Huang Y.S., Tseng Y.Z., Wu J.C., Wang S.M. Mechanism of oleic acid-induced gap junctional disassembly in rat cardiomyocytes. J. Mol. Cell. Cardiol. 2004, 37:755-766.
20. Hund T.J., Lerner D.L., Yamada K.A., Schuessler R.B., Saffitz J.E. Protein kinase Cepsilon mediates salutary effects on electrical coupling induced by ischemic preconditioning. Heart Rhythm. 2007, 4:1183-1193.
21. Jansen J.A., van Veen T.A., de Bakker J.M., van Rijen H.V. Cardiac connexins and impulse propagation. J. Mol. Cell. Cardiol. 2010, 48:76-82.
22. Jia S.J., Zhou Z., Zhang B.K., Hu Z.W., Deng H.W., Li Y.J. Asymmetric dimethylarginine damages connexin43-mediated endothelial gap junction intercellular communication. Biochem. Cell. Biol. 2009, 87:867-874.
23. Johnson J.A., Gray M.O., Chen C.H., Mochly-Rosen D. A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J. Biol. Chem. 1996, 271:24962-24966.
24. Jung S., Lee Y., Han S., Kim Y., Nam T., Ahn D. Lysophosphatidylcholine increases Ca current via activation of protein Kinase C in rabbit portal vein smooth muscle cells. Kor. J. Physiol. Pharmacol. 2008, 12:31-35.
25. Kieken F., Mutsaers N., Dolmatova E., Virgil K., Wit A.L., Kellezi A., Hirst-Jensen B.J., Duffy H.S., Sorgen P.L. Structural and molecular mechanisms of gap junction remodeling in epicardial border zone myocytes following myocardial infarction. Circ. Res. 2009, 104:1103-1112.
26. Kjenseth A., Fykerud T., Rivedal E., Leithe E. Regulation of gap junction intercellular communication by the ubiquitin system. Cell. Signal. 2010, 22:1267-1273.
27. Laing J.G., Tadros P.N., Westphale E.M., Beyer E.C. Degradation of connexin43 gap junctions involves both the proteasome and the lysosome. Exp. Cell Res. 1997, 236:482-492.
28. Lampe P.D., Lau A.F. Regulation of gap junctions by phosphorylation of connexins. Arch. Biochem. Biophys. 2000, 384:205-215.
29. Lampe P.D., Lau A.F. The effects of connexin phosphorylation on gap junctional communication. Int. J. Biochem. Cell. Biol. 2004, 36:1171-1186.
30. Lampe P.D., TenBroek E.M., Burt J.M., Kurata W.E., Johnson R.G., Lau A.F. Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J. Cell. Biol. 2000, 149:1503-1512.
31. Leithe E., Sirnes S., Fykerud T., Kjenseth A., Rivedal E. Endocytosis and post-endocytic sorting of connexins. Biochim. Biophys. Acta 2012, 1818:1870-1879.
32. Li C., Meng Q., Yu X., Jing X., Xu P., Luo D. Regulatory effect of connexin 43 on basal Ca2+ signaling in rat ventricular myocytes. PloS One 2012, 7:e36165.
33. Li Z., Vance D.E. Phosphatidylcholine and choline homeostasis. J. Lipid Res. 2008, 49:1187-1194.
34. Liang J.Y., Wang S.M., Chung T.H., Yang S.H., Wu J.C. Effects of 18-glycyrrhetinic acid on serine 368 phosphorylation of connexin43 in rat neonatal cardiomyocytes. Cell Biol. Int. 2008, 32:1371-1379.
35. Ma H., Hashizume H., Hara A., Yazawa K., Abiko Y. Protective effect of quinaprilat, an active metabolite of quinapril, on Ca2+-overload induced by lysophosphatidylcholine in isolated rat cardiomyocytes. Jpn. J. Pharmacol. 1999, 79:17-24.
36. Mackay K., Mochly-Rosen D. Arachidonic acid protects neonatal rat cardiac myocytes from ischaemic injury through epsilon protein kinase C. Cardiovasc. Res. 2001, 50:65-74.
37. Man R.Y., Wong T., Choy P.C. Effects of lysophosphoglycerides on cardiac arrhythmias. Life Sci. 1983, 32:1325-1330.
38. Matsumoto T., Kobayashi T., Kamata K. Role of lysophosphatidylcholine (LPC) in atherosclerosis. Curr. Med. Chem. 2007, 14:3209-3220.
39. Musil L.S., Goodenough D.A. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J. Cell. Biol. 1991, 115:1357-1374.
40. Opsahl H., Rivedal E. Quantitative determination of gap junction intercellular communication by scrape loading and image analysis. Cell Adhes. Commun. 2000, 7:367-375.
41. Parthasarathy S., Barnett J. Phospholipase A2 activity of low density lipoprotein: evidence for an intrinsic phospholipase A2 activity of apoprotein B-100. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:9741-9745.
42. Peng Y.S., Ding H.C., Lin Y.T., Syu J.P., Chen Y., Wang S.M. Uremic toxin p-cresol induces disassembly of gap junctions of cardiomyocytes. Toxicology 2012, 302:11-17.
43. Pogwizd S.M., Onufer J.R., Kramer J.B., Sobel B.E., Corr P.B. Induction of delayed afterdepolarizations and triggered activity in canine Purkinje fibers by lysophosphoglycerides. Circ. Res. 1986, 59:416-426.
44. Prokazova N.V., Zvezdina N.D., Korotaeva A.A. Effect of lysophosphatidylcholine on transmembrane signal transduction. Biochemistry (Mosc.) 1998, 63:31-37.
45. Saez J.C., Nairn A.C., Czernik A.J., Fishman G.I., Spray D.C., Hertzberg E.L. Phosphorylation of connexin43 and the regulation of neonatal rat cardiac myocyte gap junctions. J. Mol. Cell. Cardiol. 1997, 29:2131-2145.
46. Sedis S.P., Sequeira J.M., Altszuler H.M. Coronary sinus lysophosphatidylcholine accumulation during rapid atrial pacing. Am. J. Cardiol. 1990, 66:695-698.
47. Severs N.J., Bruce A.F., Dupont E., Rothery S. Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc. Res. 2008, 80:9-19.
48. Shah M.M., Martinez A.M., Fletcher W.H. The connexin43 gap junction protein is phosphorylated by protein kinase A and protein kinase C: in vivo and in vitro studies. Mol. Cell. Biochem. 2002, 238:57-68.
49. Sobel B.E., Corr P.B., Robison A.K., Goldstein R.A., Witkowski F.X., Klein M.S. Accumulation of lysophosphoglycerides with arrhythmogenic properties in ischemic myocardium. J. Clin. Invest. 1978, 62:546-553.
50. Solan J.L., Lampe P.D. Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biochim. Biophys. Acta 2005, 1711:154-163.
51. Solan J.L., Lampe P.D. Connexin43 phosphorylation: structural changes and biological effects. Biochem. J. 2009, 419:261-272.
52. Tomic-Carruthers N., Gorden P. Effects of proteasomal inhibitors on the maturation of the insulin proreceptor: an anatomical paradox. Biochem. Biophys. Res. Commun. 1998, 244:728-731.
53. Ver Donck L., Verellen G., Geerts H., Borgers M. Lysophosphatidylcholine-induced Ca(2+)-overload in isolated cardiomyocytes and effect of cytoprotective drugs. J. Mol. Cell. Cardiol. 1992, 24:977-988.
54. Woodley S.L., Ikenouchi H., Barry W.H. Lysophosphatidylcholine increases cytosolic calcium in ventricular myocytes by direct action on the sarcolemma. J. Mol. Cell. Cardiol. 1991, 23:671-680.
55. Zheng M., Wang Y., Kang L., Shimaoka T., Marni F., Ono K. Intracellular Ca(2+)- and PKC-dependent upregulation of T-type Ca(2+) channels in LPC-stimulated cardiomyocytes. J. Mol. Cell. Cardiol. 2010, 48:131-139.