Gene targeting implicates Cdc42 GTPase in GPVI and non-GPVI mediated platelet filopodia formation, secretion and aggregation

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Akbar, Huzoor ^a   Shang, Xun ^b   Perveen, Rehana ^a,d   Berryman, Mark ^a   Funk, Kevin ^a   Johnson, James F ^b   Tandon, Narendra N ^c,e   Zheng, Yi ^b  

^a OHIO UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c OTSUKA PHARMACEUTICAL DEVELOPMENT AND COMMERCIALIZATION INC   (United States)

^d BAQAI MEDICAL UNIVERSITY   (Pakistan)

^e Cellphire Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COLLAGEN RELATED PEPTIDE; FIBRINOGEN; GUANOSINE TRIPHOSPHATASE; P21 ACTIVATED KINASE 1; P21 ACTIVATED KINASE 2; PADGEM PROTEIN; PEPTIDE; PROTEIN CDC42; PROTEIN KINASE B; THROMBIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; COLLAGEN-RELATED PEPTIDE; FIBRINOGEN RECEPTOR; P21 ACTIVATED KINASE; PLATELET MEMBRANE GLYCOPROTEIN VI;

ANIMAL CELL; ARTICLE; BLEEDING TIME; CELL DENSITY; CELL GRANULE; CELL ISOLATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ENZYME SYNTHESIS; FILOPODIUM; GENE TARGETING; HEMOSTASIS; MOUSE; NONHUMAN; PROTEIN FUNCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; THROMBOCYTE RELEASE REACTION; THROMBOCYTOPENIA; THROMBOCYTOPOIESIS; ANIMAL; BONE MARROW; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENE DELETION; METABOLISM; PATHOLOGY; PSEUDOPODIUM; SECRETION; SIGNAL TRANSDUCTION; THROMBOCYTE;

MUS;

ANIMALS; BLEEDING TIME; BLOOD PLATELETS; BONE MARROW; CARRIER PROTEINS; CDC42 GTP-BINDING PROTEIN; ENZYME ACTIVATION; FIBRINOGEN; GENE DELETION; GENE TARGETING; MICE; P21-ACTIVATED KINASES; PEPTIDES; PLATELET AGGREGATION; PLATELET MEMBRANE GLYCOPROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PSEUDOPODIA; SIGNAL TRANSDUCTION; THROMBIN; THROMBOCYTOPENIA;

EID: 79960567744     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022117     Document Type: Article

References (48)

1. Etienne-Manneville S, Hall A, (2002) Rho GTPases in cell biology. Nature 420: 629-635.
2. Vidali L, Chen F, Cicchetti G, Ohta Y, Kwiatkowski DJ, (2006) Rac1-null mouse embryonic fibroblasts are motile and respond to platelet-derived growth factor. Mol Biol Cell 17: 2377-2390.
3. Erickson JW, Cerione RA, (2001) Multiple roles for Cdc42 in cell regulation. Curr Opin Cell Biol 13: 153-157.
4. Ridley AJ, (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16: 522-529.
5. Jones NP, Katan M, (2007) Role of phospholipase Cgamma1 in cell spreading requires association with a beta-Pix/GIT1-containing complex, leading to activation of Cdc42 and Rac1. Mol Cell Biol 27: 5790-5805.
6. Mulloy JC, Cancelas JA, Filippi MD, Kalfa TA, Guo F, et al. (2010) Rho GTPases in hematopoiesis and hemopathies. Blood 115: 936-947.
7. Polakis PG, Snyderman R, Evans T, (1989) Characterization of G25K, a GTP-binding protein containing a novel putative nucleotide binding domain. Biochem Biophys Res Commun 160: 25-32.
8. Dash D, Aepfelbacher M, Siess W, (1995) Integrin alpha IIb beta 3-mediated translocation of CDC42Hs to the cytoskeleton in stimulated human platelets. J Biol Chem 270: 17321-17326.
9. Fox JE, (1993) Regulation of platelet function by the cytoskeleton. Adv Exp Med Biol 344: 175-185.
10. Azim AC, Barkalow K, Chou J, Hartwig JH, (2000) Activation of the small GTPases, rac and cdc42, after ligation of the platelet PAR-1 receptor. Blood 95: 959-964.
11. Vidal C, Geny B, Melle J, Jandrot-Perrus M, Fontenay-Roupie M, (2002) 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: 4462-4469.
12. Pula G, Poole AW, (2008) Critical roles for the actin cytoskeleton and cdc42 in regulating platelet integrin alpha2beta1. Platelets 19: 199-210.
13. Pleines I, Eckly A, Elvers M, Hagedorn I, Eliautou S, et al. (2010) Multiple alterations of platelet functions dominated by increased secretion in mice lacking Cdc42 in platelets. Blood 115: 3364-3373.
14. Yang L, Wang L, Geiger H, Cancelas JA, Mo J, et al. (2007) Rho GTPase Cdc42 coordinates hematopoietic stem cell quiescence and niche interaction in the bone marrow. Proc Natl Acad Sci U S A 104: 5091-5096.
15. Yang L, Wang L, Zheng Y, (2006) Gene targeting of Cdc42 and Cdc42GAP affirms the critical involvement of Cdc42 in filopodia induction, directed migration, and proliferation in primary mouse embryonic fibroblasts. Mol Biol Cell 17: 4675-4685.
16. Guo F, Hildeman D, Tripathi P, Velu CS, Grimes HL, et al. (2010) Coordination of IL-7 receptor and T-cell receptor signaling by cell-division cycle 42 in T-cell homeostasis. Proc Natl Acad Sci U S A 107: 18505-18510.
17. Lockyer S, Okuyama K, Begum S, Le S, Sun B, et al. (2006) GPVI-deficient mice lack collagen responses and are protected against experimentally induced pulmonary thromboembolism. Thromb Res 118: 371-380.
18. Szczur K, Zheng Y, Filippi MD, (2009) The small Rho GTPase Cdc42 regulates neutrophil polarity via CD11b integrin signaling. Blood 114: 4527-4537.
19. Akbar H, Kim J, Funk K, Cancelas JA, Shang X, et al. (2007) Genetic and pharmacologic evidence that Rac1 GTPase is involved in regulation of platelet secretion and aggregation. J Thromb Haemost 5: 1747-1755.
20. Huzoor A, Wang W, Kornhauser R, Volker C, Stock JB, (1993) Protein prenylcysteine analog inhibits agonist-receptor-mediated signal transduction in human platelets. Proc Natl Acad Sci U S A 90: 868-872.
21. Huzoor A, Winegar DA, Lapetina EG, (1991) Carboxyl methylation of platelet rap1 proteins is stimulated by guanosine 5′-(3-O-thio)triphosphate. J Biol Chem 266: 4387-4391.
22. Quinton TM, Murugappan S, Kim S, Jin J, Kunapuli SP, (2004) Different G protein-coupled signaling pathways are involved in alpha granule release from human platelets. J Thromb Haemost 2: 978-984.
23. Cambien B, Bergmeier W, Saffaripour S, Mitchell HA, Wagner DD, (2003) Antithrombotic activity of TNF-alpha. J Clin Invest 112: 1589-1596.
24. Jaffer ZM, Chernoff J, (2002) p21-activated kinases: three more join the Pak. Int J Biochem Cell Biol 34: 713-717.
25. Smith SD, Jaffer ZM, Chernoff J, Ridley AJ, (2008) PAK1-mediated activation of ERK1/2 regulates lamellipodial dynamics. J Cell Sci 121: 3729-3736.
26. Hall A, (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
27. Yang FC, Atkinson SJ, Gu Y, Borneo JB, Roberts AW, et al. (2001) Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc Natl Acad Sci U S A 98: 5614-5618.
28. Wang Z, Oh E, Thurmond DC, (2007) Glucose-stimulated Cdc42 signaling is essential for the second phase of insulin secretion. J Biol Chem 282: 9536-9546.
29. Wang Z, Thurmond DC, (2009) Mechanisms of biphasic insulin-granule exocytosis- roles of the cytoskeleton, small GTPases and SNARE proteins. J Cell Sci 122: 893-903.
30. Momboisse F, Lonchamp E, Calco V, Ceridono M, Vitale N, et al. (2009) betaPIX-activated Rac1 stimulates the activation of phospholipase D, which is associated with exocytosis in neuroendocrine cells. J Cell Sci 122: 798-806.
31. Li J, Luo R, Kowluru A, Li G, (2004) Novel regulation by Rac1 of glucose- and forskolin-induced insulin secretion in INS-1 beta-cells. Am J Physiol Endocrinol Metab 286: E818-827.
32. Hong-Geller E, Cerione RA, (2000) Cdc42 and Rac stimulate exocytosis of secretory granules by activating the IP(3)/calcium pathway in RBL-2H3 mast cells. J Cell Biol 148: 481-494.
33. Hong-Geller E, Holowka D, Siraganian RP, Baird B, Cerione RA, (2001) Activated Cdc42/Rac reconstitutes Fcepsilon RI-mediated Ca2+ mobilization and degranulation in mutant RBL mast cells. Proc Natl Acad Sci U S A 98: 1154-1159.
34. Thurmond DC, (2009) Insulin-regulated glucagon-like peptide-1 release from L cells: actin' out. Endocrinology 150: 5202-5204.
35. Dorsam RT, Kunapuli SP, (2004) Central role of the P2Y12 receptor in platelet activation. J Clin Invest 113: 340-345.
36. Cho MJ, Pestina TI, Steward SA, Lowell CA, Jackson CW, et al. (2002) Role of the Src family kinase Lyn in TxA2 production, adenosine diphosphate secretion, Akt phosphorylation, and irreversible aggregation in platelets stimulated with gamma-thrombin. Blood 99: 2442-2447.
37. Kroner C, Eybrechts K, Akkerman JW, (2000) Dual regulation of platelet protein kinase B. J Biol Chem 275: 27790-27798.
38. Woulfe D, Jiang H, Morgans A, Monks R, Birnbaum M, et al. (2004) Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J Clin Invest 113: 441-450.
39. Kim S, Jin J, Kunapuli SP, (2004) Akt activation in platelets depends on Gi signaling pathways. J Biol Chem 279: 4186-4195.
40. Weng Z, Li D, Zhang L, Chen J, Ruan C, et al. (2010) PTEN regulates collagen-induced platelet activation. Blood 116: 2579-2581.
41. Xiang B, Zhang G, Liu J, Morris AJ, Smyth SS, et al. (2010) A G(i)-independent mechanism mediating Akt phosphorylation in platelets. J Thromb Haemost 8: 2032-2041.
42. Li Z, Zhang G, Le Breton GC, Gao X, Malik AB, et al. (2003) Two waves of platelet secretion induced by thromboxane A2 receptor and a critical role for phosphoinositide 3-kinases. J Biol Chem 278: 30725-30731.
43. Kim S, Mangin P, Dangelmaier C, Lillian R, Jackson SP, et al. (2009) Role of phosphoinositide 3-kinase beta in glycoprotein VI-mediated Akt activation in platelets. J Biol Chem 284: 33763-33772.
44. Yang L, Wang L, Kalfa TA, Cancelas JA, Shang X, et al. (2007) Cdc42 critically regulates the balance between myelopoiesis and erythropoiesis. Blood 110: 3853-3861.
45. Shcherbina A, Cooley J, Lutskiy MI, Benarafa C, Gilbert GE, et al. (2010) WASP plays a novel role in regulating platelet responses dependent on alphaIIbbeta3 integrin outside-in signalling. Br J Haematol 148: 416-427.
46. Teo M, Manser E, Lim L, (1995) Identification and molecular cloning of a p21cdc42/rac1-activated serine/threonine kinase that is rapidly activated by thrombin in platelets. J Biol Chem 270: 26690-26697.
47. Chang JC, Chang HH, Lin CT, Lo SJ, (2005) The integrin alpha6beta1 modulation of PI3K and Cdc42 activities induces dynamic filopodium formation in human platelets. J Biomed Sci 12: 881-898.
48. Jirouskova M, Jaiswal JK, Coller BS, (2007) Ligand density dramatically affects integrin alpha IIb beta 3-mediated platelet signaling and spreading. Blood 109: 5260-5269.