Inhibition of Rho-ROCK signaling induces apoptotic and non-apoptotic PS exposure in cardiomyocytes via inhibition of flippase

Journal of Molecular and Cellular Cardiology

Volumn 49, Issue 5, 2010, Pages 781-790

  Krijnen, Paul A J ^a,b   Sipkens, Jessica A ^a,b   Molling, Johan W ^a   Rauwerda, Jan A ^a,b   Stehouwer, Coen D A ^c   Muller, Alice ^a,b   Paulus, Walter J ^a,b   van Nieuw Amerongen, Geerten P ^a,b   Hack, C Erik ^a,b   Verhoeven, Arthur J ^d   van Hinsbergh, Victor W M ^a,b   Niessen, Hans W M ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d SANQUIN RESEARCH   (Netherlands)

Author keywords

Flippase; Phosphatidylserine exposure; Rho proteins; Rho associated kinase

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CASPASE 3; CLOSTRIDIUM DIFFICILE TOXIN B; EXOENZYME C3; FLIPPASE; H 1152; LIPOCORTIN 5; MEMBRANE PROTEIN; PHOSPHATIDYLSERINE; PROTEIN KINASE B; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; RHO KINASE INHIBITOR; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HEART MUSCLE CELL; HEART VENTRICLE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ADENOSINE TRIPHOSPHATE; ADP RIBOSE TRANSFERASES; AMIDES; ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BOTULINUM TOXINS; CASPASE 3; CELL LINE; CELL SEPARATION; ENZYME ACTIVATION; HUMANS; MYOCYTES, CARDIAC; PHOSPHATIDYLSERINES; PHOSPHOLIPID TRANSFER PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; RATS; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION;

CLOSTRIDIUM DIFFICILE; RATTUS;

EID: 77957239996     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.07.017     Document Type: Article

References (47)

1. Bretscher M.S. Asymmetrical lipid bilayer structure for biological membranes. Nat New Biol 1972, 236:11-12.
2. Op den Kamp J.A. Annu Rev Biochem 1979, 48:47-71.
3. Rothman J.E., Lenard J. Membrane asymmetry. Science 1977, 195:743-753.
4. Bevers E.M., Comfurius P., van Rijn J.L., Hemker H.C., Zwaal R.F. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 1982, 122:429-436.
5. Fadok V.A., Voelker D.R., Campbell P.A., Cohen J.J., Bratton D.L., Henson P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 1992, 148:2207-2216.
6. Zwaal R.F., Comfurius P., Bevers E.M. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005, 62:971-988.
7. Waring P., Lambert D., Sjaarda A., Hurne A., Beaver J. Increased cell surface exposure of phosphatidylserine on propidium iodide negative thymocytes undergoing death by necrosis. Cell Death Differ 1999, 6:624-637.
8. Fadok V.A., Bratton D.L., Henson P.M. Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J Clin Invest 2001, 108:957-962.
9. Krijnen P.A., Cillessen S.A., Manoe R., Muller A., Visser C.A., Meijer C.J., et al. Clusterin: a protective mediator for ischemic cardiomyocytes?. Am J Physiol Heart Circ Physiol 2005, 289:H2193-H2202.
10. Geske F.J., Lieberman R., Strange R., Gerschenson L.E. Early stages of p53-induced apoptosis are reversible. Cell Death Differ 2001, 8:182-191.
11. Hammill A.K., Uhr J.W., Scheuermann R.H. Annexin V staining due to loss of membrane asymmetry can be reversible and precede commitment to apoptotic death. Exp Cell Res 1999, 251:16-21.
12. Jaruga E., Salvioli S., Dobrucki J., Chrul S., Bandorowicz-Pikula J., Sikora E., et al. Apoptosis-like, reversible changes in plasma membrane asymmetry and permeability, and transient modifications in mitochondrial membrane potential induced by curcumin in rat thymocytes. FEBS Lett 1998, 433:287-293.
13. Martin S., Pombo I., Poncet P., David B., Arock M., Blank U. Immunologic stimulation of mast cells leads to the reversible exposure of phosphatidylserine in the absence of apoptosis. Int Arch Allergy Immunol 2000, 123:249-258.
14. Musters R.J., Probstl-Biegelmann E., van Veen T.A., Hoebe K.H., Op den Kamp J.A., Verkleij A.J., et al. Sarcolemmal phosphatidylethanolamine reorganization during simulated ischaemia and reperfusion: reversibility and ATP dependency. Mol Membr Biol 1996, 13:159-164.
15. Yang M.Y., Chuang H., Chen R.F., Yang K.D. Reversible phosphatidylserine expression on blood granulocytes related to membrane perturbation but not DNA strand breaks. J Leukoc Biol 2002, 71:231-237.
16. Post J.A., Verkleij A.J., Langer G.A. Organization and function of sarcolemmal phospholipids in control and ischemic/reperfused cardiomyocytes. J Mol Cell Cardiol 1995, 27:749-760.
17. Nijmeijer R., Lagrand W.K., Baidoshvili A., Lubbers Y.T., Hermens W.T., Meijer C.J., et al. Secretory type II phospholipase A(2) binds to ischemic myocardium during myocardial infarction in humans. Cardiovasc Res 2002, 53:138-146.
18. Nijmeijer R., Willemsen M., Meijer C.J., Visser C.A., Verheijen R.H., Gottlieb R.A., et al. Type II secretory phospholipase A2 binds to ischemic flip-flopped cardiomyocytes and subsequently induces cell death. Am J Physiol Heart Circ Physiol 2003, 285:H2218-H2224.
19. Daleke D.L. Regulation of transbilayer plasma membrane phospholipid asymmetry. J Lipid Res 2003, 44:233-242.
20. Daleke D.L., Huestis W.H. Incorporation and translocation of aminophospholipids in human erythrocytes. Biochemistry 1985, 24:5406-5416.
21. Manno S., Takakuwa Y., Mohandas N. Identification of a functional role for lipid asymmetry in biological membranes: phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc Natl Acad Sci USA 2002, 99:1943-1948.
22. Goossens E.L., Reutelingsperger C.P., Jongsma F.H., Kraayenhof R., Hermens W.T. Annexin V perturbs or stabilises phospholipid membranes in a calcium-dependent manner. FEBS Lett 1995, 359:155-158.
23. Saurel O., Cezanne L., Milon A., Tocanne J.F., Demange P. Influence of annexin V on the structure and dynamics of phosphatidylcholine/phosphatidylserine bilayers: a fluorescence and NMR study. Biochemistry 1998, 37:1403-1410.
24. Kunzelmann C., Freyssinet J.M., Martinez M.C. Rho A participates in the regulation of phosphatidylserine-dependent procoagulant activity at the surface of megakaryocytic cells. J Thromb Haemost 2004, 2:644-650.
25. Wheeler A.P., Ridley A.J. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp Cell Res 2004, 301:43-49.
26. Verhoeven A.J., Hilarius P.M., Dekkers D.W., Lagerberg J.W., de Korte D. Prolonged storage of red blood cells affects aminophospholipid translocase activity. Vox Sang 2006, 91:244-251.
27. Chong Z.Z., Kang J.Q., Maiese K. AKT1 drives endothelial cell membrane asymmetry and microglial activation through Bcl-xL and caspase 1, 3, and 9. Exp Cell Res 2004, 296:196-207.
28. Chong Z.Z., Kang J.Q., Maiese K. Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation 2002, 106:2973-2979.
29. Clerk A., Cullingford T.E., Fuller S.J., Giraldo A., Markou T., Pikkarainen S., et al. Signaling pathways mediating cardiac myocyte gene expression in physiological and stress responses. J Cell Physiol 2007, 212:311-322.
30. Krijnen P.A., Nijmeijer R., Meijer C.J., Visser C.A., Hack C.E., Niessen H.W. Apoptosis in myocardial ischaemia and infarction. J Clin Pathol 2002, 55:801-811.
31. Nijmeijer R., Lagrand W.K., Lubbers Y.T., Visser C.A., Meijer C.J., Niessen H.W., et al. C-reactive protein activates complement in infarcted human myocardium. Am J Pathol 2003, 163:269-275.
32. Djouder N., Schmidt G., Frings M., Cavalie A., Thelen M., Aktories K. Rac and phosphatidylinositol 3-kinase regulate the protein kinase B in Fc epsilon RI signaling in RBL 2H3 mast cells. J Immunol 2001, 166:1627-1634.
33. Herkert O., Diebold I., Brandes R.P., Hess J., Busse R., Gorlach A. NADPH oxidase mediates tissue factor-dependent surface procoagulant activity by thrombin in human vascular smooth muscle cells. Circulation 2002, 105:2030-2036.
34. Servant G., Weiner O.D., Herzmark P., Balla T., Sedat J.W., Bourne H.R. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 2000, 287:1037-1040.
35. Kam Y., Exton J.H. Role of phospholipase D1 in the regulation of mTOR activity by lysophosphatidic acid. FASEB J 2004, 18:311-319.
36. Hata Y., Miura M., Nakao S., Kawahara S., Kita T., Ishibashi T. Antiangiogenic properties of fasudil, a potent Rho-kinase inhibitor. Jpn J Ophthalmol 2008, 52:16-23.
37. Chang J., Xie M., Shah V.R., Schneider M.D., Entman M.L., Wei L., et al. Activation of Rho-associated coiled-coil protein kinase 1 (ROCK-1) by caspase-3 cleavage plays an essential role in cardiac myocyte apoptosis. Proc Natl Acad Sci USA 2006, 103:14495-14500.
38. Hippenstiel S., Schmeck B., N'Guessan P.D., Seybold J., Krull M., Preissner K., et al. Rho protein inactivation induced apoptosis of cultured human endothelial cells. Am J Physiol Lung Cell Mol Physiol 2002, 283:L830-L838.
39. Khwaja A., Sharpe C.C., Noor M., Hendry B.M. The role of geranylgeranylated proteins in human mesangial cell proliferation. Kidney Int 2006, 70:1296-1304.
40. Matarrese P., Falzano L., Fabbri A., Gambardella L., Frank C., Geny B., et al. Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels. J Biol Chem 2007, 282:9029-9041.
41. Reuveny M., Heller H., Bengal E. RhoA controls myoblast survival by inducing the phosphatidylinositol 3-kinase-Akt signaling pathway. FEBS Lett 2004, 569:129-134.
42. Sarrabayrouse G., Synaeve C., Leveque K., Favre G., Tilkin-Mariame A.F. Statins stimulate in vitro membrane FasL expression and lymphocyte apoptosis through RhoA/ROCK pathway in murine melanoma cells. Neoplasia 2007, 9:1078-1090.
43. Moore M., Marroquin B.A., Gugliotta W., Tse R., White S.R. Rho kinase inhibition initiates apoptosis in human airway epithelial cells. Am J Respir Cell Mol Biol 2004, 30:379-387.
44. Li X., Liu L., Tupper J.C., Bannerman D.D., Winn R.K., Sebti S.M., et al. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J Biol Chem 2002, 277:15309-15316.
45. He D., Hagen S.J., Pothoulakis C., Chen M., Medina N.D., Warny M., et al. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 2000, 119:139-150.
46. Liu T.S., Musch M.W., Sugi K., Walsh-Reitz M.M., Ropeleski M.J., Hendrickson B.A., et al. Protective role of HSP72 against Clostridium difficile toxin A-induced intestinal epithelial cell dysfunction. Am J Physiol Cell Physiol 2003, 284:C1073-C1082.
47. Colleau M., Herve P., Fellmann P., Devaux P.F. Transmembrane diffusion of fluorescent phospholipids in human erythrocytes. Chem Phys Lipids 1991, 57:29-37.