Hypotonic swelling-induced activation of PKN1 mediates cell survival in cardiac myocytes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 1, 2011, Pages

  Kajimoto, Katsuya ^a   Shao, Dan ^a   Takagi, Hiromitsu ^a   Maceri, Gregorio ^a   Zablocki, Daniela ^a   Mukai, Hideyuki ^b   Ono, Yoshitaka ^b   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b KOBE UNIVERSITY   (Japan)

Author keywords

Heart; Mitogen activated protein kinase; Serine threonine protein kinase N1; Signal transduction

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN KINASE N1; PROTEIN KINASE PKC1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR ELK 1; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CELL SWELLING; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME BINDING; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HEART MUSCLE CELL; HYPOOSMOTIC STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SRC HOMOLOGY DOMAIN;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL ENLARGEMENT; CELL SURVIVAL; CELLS, CULTURED; DOWN-REGULATION; HYPOTONIC SOLUTIONS; IMMUNOPRECIPITATION; MITOGEN-ACTIVATED PROTEIN KINASES; MYOCARDIUM; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 78651336863     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00232.2010     Document Type: Article

References (59)

1. Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Zhu W, Kadowaki T, Yazaki Y. Rho family small G proteins play critical roles in mechanical stress- induced hypertrophic responses in cardiac myocytes. Circ Res 84: 458-466, 1999.
2. Amano M, Mukai H, Ono Y, Chihara K, Matsui T, Hamajima Y, Okawa K, Iwamatsu A, Kaibuchi K. Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science 271: 648-650, 1996. (Pubitemid 26052909)
3. Aoki H, Izumo S, Sadoshima J. Angiotensin II activates RhoA in cardiac myocytes:a critical role of RhoA in angiotensin II-induced premyofibril formation. Circ Res 81: 666-676, 1998.
4. Armstrong SC, Shivell LC, Ganote CE. Sarcolemmal blebs and osmotic fragility as correlates of irreversible ischemic injury in preconditioned isolated rabbit cardiomyocytes. J Mol Cell Cardiol 33: 149-160, 2001.
5. Atienza JM, Suh M, Xenarios I, Landgraf R, Colicelli J. Human ERK1 induces filamentous growth and cell wall remodeling pathways in Saccharomyces cerevisiae. J Biol Chem 275: 20638-20646, 2000.
6. Baumgarten CM, Clemo HF. Swelling-activated chloride channels in cardiac physiology and pathophysiology. Prog Biophys Mol Biol 82: 25-42, 2003.
7. + pump regulation in cardiac myocytes during hyposmolar swelling. Am J Physiol Cell Physiol 276: C1091-C1099, 1999.
8. Bickle M, Delley PA, Schmidt A, Hall MN. Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J 17: 2235-2245, 1998.
9. Blumer KJ, Johnson GL, Lange-Carter CA. Mammalian mitogen-activated protein kinase kinase kinase (MEKK) can function in a yeast mitogen-activated protein kinase pathway downstream of protein kinase C. Proc Natl Acad Sci USA 91: 4925-4929, 1994.
10. Bokoch GM, Bohl BP, Chuang TH. Guanine nucleotide exchange regulates membrane translocation of Rac/Rho GTP-binding proteins. J Biol Chem 269: 31674-31679, 1994.
11. Chiloeches A, Paterson HF, Marais R, Clerk A, Marshall CJ, Sugden PH. Regulation of Ras. GTP loading and Ras-Raf association in neonatal rat ventricular myocytes by G protein-coupled receptor agonists and phorbol ester. Activation of the extracellular signal-regulated kinase cascade by phorbol ester is mediated by Ras. J Biol Chem 274: 19762-19770, 1999.
12. Clark W, Rudnick S, LaPres J, Lesch M, Decker R. Hypertrophy of isolated adult feline heart cells following β-adrenergic-induced beating. Am J Physiol Cell Physiol 261: C530-C542, 1991.
13. Clemo HF, Baumgarten CM. Atrial natriuretic factor decreases cell volume of rabbit atrial and ventricular myocytes. Am J Physiol Cell Physiol 260: C681-C690, 1991.
14. Davenport KR, Sohaskey M, Kamada Y, Levin DE, Gustin MC. A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270: 30157-30161, 1995.
15. Dong LQ, Landa LR, Wick MJ, Zhu L, Mukai H, Ono Y, Liu F. Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton. Proc Natl Acad Sci USA 97: 5089-5094, 2000.
16. Drewnowska K, Baumgarten CM. Regulation of cellular volume in rabbit ventricular myocytes: bumetanide, chlorothiazide, and ouabain. Am J Physiol Cell Physiol 260: C122-C131, 1991.
17. Feranchak AP, Roman RM, Doctor RB, Salter KD, Toker A, Fitz JG. The lipid products of phosphoinositide 3-kinase contribute to regulation of cholangiocyte ATP and chloride transport. J Biol Chem 274: 30979-30986, 1999.
18. Flynn P, Mellor H, Casamassima A, Parker PJ. Rho GTPase control of protein kinase C-related protein kinase activation by 3-phosphoinositide- dependent protein kinase. J Biol Chem 275: 11064-11070, 2000.
19. Flynn P, Mellor H, Palmer R, Panayotou G, Parker PJ. Multiple interactions of PRK1 with RhoA. Functional assignment of the Hr1 repeat motif. J Biol Chem 273: 2698-2705, 1998.
20. Gray JV, Ogas JP, Kamada Y, Stone M, Levin DE, Herskowitz I. A role for the Pkc1 MAP kinase pathway of Saccharomyces cerevisiae in bud emergence and identification of a putative upstream regulator. EMBO J 16: 4924-4937, 1997.
21. Herskowitz I. MAP kinase pathways in yeast: for mating and more. Cell 80: 187-197, 1995.
22. Hirakawa M, Oike M, Watanabe M, Karashima Y, Ito Y. Pivotal role of integrin α5β1 in hypotonic stress-induced responses of human endothelium. FASEB J 20: 1992-1999, 2006.
23. Hoffmann EK, Simonsen LO. Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol Rev 69: 315-382, 1989.
24. Inagaki M, Schmelzle T, Yamaguchi K, Irie K, Hall MN, Matsumoto K. PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast. Mol Cell Biol 19: 8344-8352, 1999.
25. 1- mediated response. J Biol Chem 265: 13809-13817, 1990.
26. Janse MJ, Wit AL. Electrophysiological mechanisms of ventricular arrhythmias resulting from myocardial ischemia and infarction. Physiol Rev 69: 1049-1169, 1989.
27. Jennings RB, Reimer KA, Steenbergen C. Myocardial ischemia revisited. The osmolar load, membrane damage, and reperfusion. J Mol Cell Cardiol 18: 769-780, 1986.
28. Kamada Y, Jung US, Piotrowski J, Levin DE. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9: 1559-1571, 1995.
29. Kamada Y, Qadota H, Python CP, Anraku Y, Ohya Y, Levin DE. Activation of yeast protein kinase C by Rho1 GTPase. J Biol Chem 271: 9193-9196, 1996.
30. Kovacic B, Ilic D, Damsky CH, Gardner DG. c-Src activation plays a role in endothelin-dependent hypertrophy of the cardiac myocyte. J Biol Chem 273: 35185-35193, 1998.
31. Lee KS, Irie K, Gotoh Y, Watanabe Y, Araki H, Nishida E, Matsumoto K, Levin DE. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol Cell Biol 13: 3067-3075, 1993.
32. Levin DE, Bartlett-Heubusch E. Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J Cell Biol 116: 1221-1229, 1992.
33. Levin DE, Errede B. The proliferation of MAP kinase signaling pathways in yeast. Curr Opin Cell Biol 7: 197-202, 1995.
34. Low SY, Rennie MJ, Taylor PM. Signaling elements involved in amino acid transport responses to altered muscle cell volume. FASEB J 11: 1111-1117, 1997.
35. Marinissen MJ, Chiariello M, Gutkind JS. Regulation of gene expression by the small GTPase Rho through the ERK6 (p38γ) MAP kinase pathway. Genes Dev 15: 535-553, 2001.
36. Mellor H, Parker PJ. The extended protein kinase C superfamily. Biochem J 332: 281-292, 1998.
37. Morisco C, Zebrowski D, Condorelli G, Tsichlis P, Vatner SF, Sadoshima J. The Akt-glycogen synthase kinase 3β pathway regulates transcription of atrial natriuretic factor induced by β-adrenergic receptor stimulation in cardiac myocytes. J Biol Chem 275: 14466-14475, 2000.
38. Mukai H. The structure and function of PKN, a protein kinase having a catalytic domain homologous to that of PKC. J Biochem (Tokyo) 133: 17-27, 2003.
39. Mukai H, Kitagawa M, Shibata H, Takanaga H, Mori K, Shimakawa M, Miyahara M, Hirao K, Ono Y. Activation of PKN, a novel 120-kDa protein kinase with leucine zipper- like sequences, by unsaturated fatty acids and by limited proteolysis. Biochem Biophys Res Commun 204: 348-356, 1994.
40. Nagao M, Kaziro Y, Itoh H. The Src family tyrosine kinase is involved in Rho-dependent activation of c-Jun N-terminal kinase by Gα12. Oncogene 18: 4425-4434, 1999.
41. Nilius B, Voets T, Prenen J, Barth H, Aktories K, Kaibuchi K, Droogmans G, Eggermont J. Role of Rho and Rho kinase in the activation of volume-regulated anion channels in bovine endothelial cells. J Physiol 516: 67-74, 1999.
42. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 9: 484-496, 1995.
43. Nobes CD, Hawkins P, Stephens L, Hall A. Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J Cell Sci 108: 225-233, 1995.
44. Nonaka H, Tanaka K, Hirano H, Fujiwara T, Kohno H, Umikawa M, Mino A, Takai Y. A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. Embo J 14: 5931-5938, 1995.
45. Oishi K, Mukai H, Shibata H, Takahashi M, Ono Y. Identification and characterization of PKNβ, a novel isoform of protein kinase PKN: expression and arachidonic acid dependency are different from those of PKNα. Biochem Biophys Res Commun 261: 808-814, 1999.
46. Parker JC. In defense of cell volume? Am J Physiol Cell Physiol 265: C1191-C1200, 1993.
47. Qadota H, Anraku Y, Botstein D, Ohya Y. Conditional lethality of a yeast strain expressing human RHOA in place of RHO1. Proc Natl Acad Sci USA 91: 9317-9321, 1994.
48. Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18: 578-585, 1999.
49. Sadoshima J. Src mediates hypotonic stress-induced c-fos expression. Circulation 96, Suppl: I-555, 1997.
50. Sadoshima J, Qiu Z, Morgan JP, Izumo S. Tyrosine kinase activation is an immediate and essential step in hypotonic cell swelling-induced ERK activation and c-fos gene expression in cardiac myocytes. EMBO J 15: 5535-5546, 1996.
51. Shibata H, Mukai H, Inagaki Y, Homma Y, Kimura K, Kaibuchi K, Narumiya S, Ono Y. Characterization of the interaction between RhoA and the amino-terminal region of PKN. FEBS Lett 385: 221-224, 1996. (Pubitemid 26167461)
52. Takagi H, Hsu CP, Kajimoto K, Shao D, Yang Y, Maejima Y, Zhai P, Yehia G, Yamada C, Zablocki D, Sadoshima J. Activation of PKN mediates survival of cardiac myocytes in the heart during ischemia/ reperfusion. Circ Res 107: 642-649, 2010.
53. Takahashi M, Gotoh Y, Isagawa T, Nishimura T, Goyama E, Kim HS, Mukai H, Ono Y. Regulation of a mitogen-activated protein kinase kinase kinase, MLTK by PKN. J Biochem (Tokyo) 133: 181-187, 2003.
54. Takahashi M, Mukai H, Toshimori M, Miyamoto M, Ono Y. Proteolytic activation of PKN by caspase-3 or related protease during apoptosis. Proc Natl Acad Sci USA 95: 11566-11571, 1998.
55. Tilly BC, Edixhoven MJ, Tertoolen LG, Morii N, Saitoh Y, Narumiya S, de Jonge HR. Activation of the osmo-sensitive chloride conductance involves P21rho and is accompanied by a transient reorganization of the F-actin cytoskeleton. Mol Biol Cell 7: 1419-1427, 1996.
56. van der Wijk T, Dorrestijn J, Narumiya S, Maassen JA, de Jonge HR, Tilly BC. Osmotic swelling-induced activation of the extracellular-signal-regulated protein kinases Erk-1 and Erk-2 in intestine 407 cells involves the Ras/Raf-signalling pathway. Biochem J 331: 863-869, 1998.
57. Vandenberg JI, Rees SA, Wright AR, Powell T. Cell swelling and ion transport pathways in cardiac myocytes. Cardiovasc Res 32: 85-97, 1996.
58. Watanabe G, Saito Y, Madaule P, Ishizaki T, Fujisawa K, Morii N, Mukai H, Ono Y, Kakizuka A, Narumiya S. Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase Rho. Science 271: 645-648, 1996.
59. +/taurocholate cotransport polypeptide is mediated via the phosphoinositide 3-kinase signaling pathway. J Biol Chem 275: 29754-29760, 2000.