Lysophosphatidic acid stimulation of platelets rapidly induces Ca2+-dependent dephosphorylation of cofilin that is independent of dense granule secretion and aggregation

Blood Cells, Molecules, and Diseases

Volumn 38, Issue 3, 2007, Pages 269-279

  Pandey, Dharmendra ^a   Goyal, Pankaj ^a   Siess, Wolfgang ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Actin; Cofilin; LIM kinase; Lysophosphatidic; PAK; Phosphatase; Platelet; Rho kinase; Secretion; Shape change

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; COFILIN; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; F ACTIN; FIBRINOGEN; LIM PROTEIN; LYSOPHOSPHATIDIC ACID; P21 ACTIVATED KINASE; PROTEIN KINASE; PROTEIN LIMK 1; RHO KINASE; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CELL GRANULE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE SHAPE; THROMBOCYTE STRUCTURE;

ACTIN DEPOLYMERIZING FACTORS; AMIDES; BLOOD PLATELETS; CALCIUM; CALCIUM SIGNALING; CELL DEGRANULATION; CELL SHAPE; ENZYME INHIBITORS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOPHOSPHOLIPIDS; PHOSPHORYLATION; PLATELET AGGREGATION; PROTEIN-SERINE-THREONINE KINASES; PYRIDINES;

EID: 34047126537     PISSN: 10799796     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcmd.2007.01.002     Document Type: Article

References (60)

1. Siess W., and Tigyi G. Thrombogenic and atherogenic activities of lysophosphatidic acid. J. Cell. Biochem. 92 6 (2004) 1086-1094
2. Siess W., Zangl K.J., Essler M., Bauer M., Brandl R., Corrinth C., Bittman R., Tigyi G., and Aepfelbacher M. Lysophosphatidic acid mediates the rapid activation of platelets and endothelial cells by mildly oxidized low density lipoprotein and accumulates in human atherosclerotic lesions. Proc. Natl. Acad. Sci. U. S. A. 96 12 (1999) 6931-6936
3. Rother E., Brandl R., Baker D.L., Goyal P., Gebhard H., Tigyi G., and Siess W. Subtype-selective antagonists of lysophosphatidic Acid receptors inhibit platelet activation triggered by the lipid core of atherosclerotic plaques. Circulation 108 6 (2003) 741-747
4. Chen X., Yang X.Y., Wang N.D., Ding C., Yang Y.J., You Z.J., Su Q., and Chen J.H. Serum lysophosphatidic acid concentrations measured by dot immunogold filtration assay in patients with acute myocardial infarction. Scand. J. Clin. Lab. Invest. 63 7-8 (2003) 497-503
5. Retzer M., and Essler M. Lysophosphatidic acid-induced platelet shape change proceeds via Rho/Rho kinase-mediated myosin light-chain and moesin phosphorylation. Cell. Signal. 12 9-10 (2000) 645-648
6. Haseruck N., Erl W., Pandey D., Tigyi G., Ohlmann P., Ravanat C., Gachet C., and Siess W. The plaque lipid lysophosphatidic acid stimulates platelet activation and platelet-monocyte aggregate formation in whole blood: involvement of P2Y1 and P2Y12 receptors. Blood 103 7 (2004) 2585-2592
7. Fox J.E. Cytoskeletal proteins and platelet signaling. Thromb. Haemost. 86 1 (2001) 198-213
8. Hall A. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33 Pt 5 (2005) 891-895
9. Azim A.C., Barkalow K., Chou J., and Hartwig J.H. Activation of the small GTPases, rac and cdc42, after ligation of the platelet PAR-1 receptor. Blood 95 3 (2000) 959-964
10. Gratacap M.P., Payrastre B., Nieswandt B., and Offermanns S. Differential regulation of Rho and Rac through heterotrimeric G-proteins and cyclic nucleotides. J. Biol. Chem. 276 51 (2001) 47906-47913
11. Klages B., Brandt U., Simon M.I., Schultz G., and Offermanns S. Activation of G12/G13 results in shape change and Rho/Rho-kinase-mediated myosin light chain phosphorylation in mouse platelets. J. Cell Biol. 144 4 (1999) 745-754
12. Bauer M., Retzer M., Wilde J.I., Maschberger P., Essler M., Aepfelbacher M., Watson S.P., and Siess W. Dichotomous regulation of myosin phosphorylation and shape change by Rho-kinase and calcium in intact human platelets. Blood 94 5 (1999) 1665-1672
13. Moers A., Nieswandt B., Massberg S., Wettschureck N., Gruner S., Konrad I., Schulte V., Aktas B., Gratacap M.P., Simon M.I., Gawaz M., and Offermanns S. G13 is an essential mediator of platelet activation in hemostasis and thrombosis. Nat. Med. 9 11 (2003) 1418-1422
14. Soulet C., Hechler B., Gratacap M.P., Plantavid M., Offermanns S., Gachet C., and Payrastre B. A differential role of the platelet ADP receptors P2Y1 and P2Y12 in Rac activation. J. Thromb. Haemost. 3 10 (2005) 2296-2306
15. Suzuki-Inoue K., Yatomi Y., Asazuma N., Kainoh M., Tanaka T., Satoh K., and Ozaki Y. Rac, a small guanosine triphosphate-binding protein, and p21-activated kinase are activated during platelet spreading on collagen-coated surfaces: roles of integrin alpha(2)beta(1). Blood 98 13 (2001) 3708-3716
16. Soulet C., Gendreau S., Missy K., Benard V., Plantavid M., and Payrastre B. Characterisation of Rac activation in thrombin- and collagen-stimulated human blood platelets. FEBS Lett. 507 3 (2001) 253-258
17. Edwards D.C., Sanders L.C., Bokoch G.M., and Gill G.N. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1 5 (1999) 253-259
18. Maekawa M., Ishizaki T., Boku S., Watanabe N., Fujita A., Iwamatsu A., Obinata T., Ohashi K., Mizuno K., and Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285 5429 (1999) 895-898
19. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., and Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393 6687 (1998) 805-809
20. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., and Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393 6687 (1998) 809-812
21. McGough A., Pope B., Chiu W., and Weeds A. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138 4 (1997) 771-781
22. Galkin V.E., Orlova A., VanLoock M.S., Shvetsov A., Reisler E., and Egelman E.H. ADF/cofilin use an intrinsic mode of F-actin instability to disrupt actin filaments. J. Cell Biol. 163 5 (2003) 1057-1066
23. Ichetovkin I., Grant W., and Condeelis J. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr. Biol. 12 1 (2002) 79-84
24. Huang T.Y., DerMardirossian C., and Bokoch G.M. Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 18 1 (2006) 26-31
25. Matsui T., Amano M., Yamamoto T., Chihara K., Nakafuku M., Ito M., Nakano T., Okawa K., Iwamatsu A., and Kaibuchi K. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J. 15 9 (1996) 2208-2216
26. Amano M., Chihara K., Kimura K., Fukata Y., Nakamura N., Matsuura Y., and Kaibuchi K. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275 5304 (1997) 1308-1311
27. Schmitz U., Thommes K., Beier I., and Vetter H. Lysophosphatidic acid stimulates p21-activated kinase in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 291 3 (2002) 687-691
28. Jung I.D., Lee J., Lee K.B., Park C.G., Kim Y.K., Seo D.W., Park D., Lee H.W., Han J.W., and Lee H.Y. Activation of p21-activated kinase 1 is required for lysophosphatidic acid-induced focal adhesion kinase phosphorylation and cell motility in human melanoma A2058 cells. Eur. J. Biochem. 271 8 (2004) 1557-1565
29. Pandey D., Goyal P., Bamburg J.R., and Siess W. Regulation of LIM-kinase 1 and cofilin in thrombin-stimulated platelets. Blood 107 2 (2006) 575-583
30. Negrescu E.V., de Quintana K.L., and Siess W. Platelet shape change induced by thrombin receptor activation. Rapid stimulation of tyrosine phosphorylation of novel protein substrates through an integrin- and Ca(2+)-independent mechanism. J. Biol. Chem. 270 3 (1995) 1057-1061
31. Haserück N.R.E., Corrinth C., and Siess W. Comparison of platelet shape change and aggregation induced by lysophosphatidic acid and mildly oxidised LDL in platelet-rich plasma and in washed platelets. Platelets 11 6 (2000) 344-364
32. Cazenave J.P.M.J., Sutter-Bay A., Gachet C., Toti F., and Beretz A. A Centrifugation Techniques for the Preparation of Suspensions of Non Activated Washed Human Platelets (1993), Kluwer Academics Publishers
33. Ruf A., and Patscheke H. Flow cytometric detection of activated platelets: comparison of determining shape change, fibrinogen binding, and P-selectin expression. Semin. Thromb. Hemost. 21 2 (1995) 146-151
34. Maschberger P., Bauer M., Baumann-Siemons J., Zangl K.J., Negrescu E.V., Reininger A.J., and Siess W. Mildly oxidized low density lipoprotein rapidly stimulates via activation of the lysophosphatidic acid receptor Src family and Syk tyrosine kinases and Ca2+ influx in human platelets. J. Biol. Chem. 275 25 (2000) 19159-19166
35. Hartshorne D.J. Myosin phosphatase: subunits and interactions. Acta Physiol. Scand. 164 4 (1998) 483-493
36. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T., Tamakawa H., Yamagami K., Inui J., Maekawa M., and Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389 6654 (1997) 990-994
37. Sasaki Y., Suzuki M., and Hidaka H. The novel and specific Rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoquinoline)sulfonyl]-homopiperazine as a probing molecule for Rho-kinase-involved pathway. Pharmacol. Ther. 93 2-3 (2002) 225-232
38. Ohashi K., Nagata K., Maekawa M., Ishizaki T., Narumiya S., and Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J. Biol. Chem. 275 5 (2000) 3577-3582
39. Lee K.H., Meuer S.C., and Samstag Y. Cofilin: a missing link between T cell co-stimulation and rearrangement of the actin cytoskeleton. Eur. J. Immunol. 30 3 (2000) 892-899
40. Rhee S., and Grinnell F. P21-activated kinase 1: convergence point in PDGF- and LPA-stimulated collagen matrix contraction by human fibroblasts. J. Cell Biol. 172 3 (2006) 423-432
41. Vidal C., Geny B., Melle J., Jandrot-Perrus M., and Fontenay-Roupie M. Cdc42/Rac1-dependent activation of the p21-activated kinase (PAK) regulates human platelet lamellipodia spreading: implication of the cortical-actin binding protein cortactin. Blood 100 13 (2002) 4462-4469
42. Chang J.C., Chang H.H., Lin C.T., and Lo S.J. The integrin alpha6beta1 modulation of PI3K and Cdc42 activities induces dynamic filopodium formation in human platelets. J. Biomed. Sci. 12 6 (2005) 881-898
43. Menard R.E., and Mattingly R.R. Gbetagamma subunits stimulate p21-activated kinase 1 (PAK1) through activation of PI3-kinase and Akt but act independently of Rac1/Cdc42. FEBS Lett. 556 1-3 (2004) 187-192
44. Bokoch G.M. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72 (2003) 743-781
45. Zhang Z., Ottens A.K., Larner S.F., Kobeissy F.H., Williams M.L., Hayes R.L., and Wang K.K. Direct Rho-associated kinase inhibition induces cofilin dephosphorylation and neurite outgrowth in PC-12 cells. Cell. Mol. Biol. Lett. 11 1 (2006) 12-29
46. Meberg P.J., Ono S., Minamide L.S., Takahashi M., and Bamburg J.R. Actin depolymerizing factor and cofilin phosphorylation dynamics: response to signals that regulate neurite extension. Cell Motil. Cytoskelet. 39 2 (1998) 172-190
47. Yahara I., Aizawa H., Moriyama K., Iida K., Yonezawa N., Nishida E., Hatanaka H., and Inagaki F. A role of cofilin/destrin in reorganization of actin cytoskeleton in response to stresses and cell stimuli. Cell Struct. Funct. 21 5 (1996) 421-424
48. Minamide L.S., Striegl A.M., Boyle J.A., Meberg P.J., and Bamburg J.R. Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell Biol. 2 9 (2000) 628-636
49. Jang D.H., Han J.H., Lee S.H., Lee Y.S., Park H., Kim H., and Kaang B.K. Cofilin expression induces cofilin-actin rod formation and disrupts synaptic structure and function in Aplysia synapses. Proc. Natl. Acad. Sci. U. S. A. 102 44 (2005) 16072-16077
50. DesMarais V., Macaluso F., Condeelis J., and Bailly M. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J. Cell Sci. 117 Pt 16 (2004) 3499-3510
51. Carlsson A.E. Stimulation of actin polymerization by filament severing. Biophys. J. 90 2 (2006) 413-422
52. Pollard T.D., and Beltzner C.C. Structure and function of the Arp2/3 complex. Curr. Opin. Struct. Biol. 12 6 (2002) 768-774
53. Nagaoka R., Abe H., and Obinata T. Site-directed mutagenesis of the phosphorylation site of cofilin: its role in cofilin-actin interaction and cytoplasmic localization. Cell Motil. Cytoskelet. 35 3 (1996) 200-209
54. Ghosh M., Song X., Mouneimne G., Sidani M., Lawrence D.S., and Condeelis J.S. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304 5671 (2004) 743-746
55. Andrianantoandro E., and Pollard T.D. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell 24 1 (2006) 13-23
56. Pfannstiel J., Cyrklaff M., Habermann A., Stoeva S., Griffiths G., Shoeman R., and Faulstich H. Human cofilin forms oligomers exhibiting actin bundling activity. J. Biol. Chem. 276 52 (2001) 49476-49484
57. Davidson M.M., and Haslam R.J. Dephosphorylation of cofilin in stimulated platelets: roles for a GTP-binding protein and Ca2+. Biochem. J. 301 Pt 1 (1994) 41-47
58. Wang Y., Shibasaki F., and Mizuno K. Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J. Biol. Chem. 280 13 (2005) 12683-12689
59. Siess W. Molecular mechanisms of platelet activation. Physiol. Rev. 69 1 (1989) 58-178
60. Redondo P.C., Harper M.T., Rosado J.A., and Sage S.O. A role for cofilin in the activation of store-operated calcium entry by de novo conformational coupling in human platelets. Blood 107 3 (2006) 973-979