S6K1 and mTOR regulate Rac1-driven platelet activation and aggregation

Blood

Volumn 118, Issue 11, 2011, Pages 3129-3136

  Aslan, Joseph E ^a,b   Tormoen, Garth W ^a   Loren, Cassandra P ^a   Pang, Jiaqing ^a   McCarty, Owen J T ^a,b  

^a Oregon Health and Science University Department of Biomedical Engineering   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN TYROSINE KINASE INHIBITOR; RAC1 PROTEIN; S6 KINASE; S6 KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; CYTOSKELETON; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SHEAR FLOW; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOGENESIS;

EID: 80052938277     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-02-331579     Document Type: Article

References (49)

1. Furie B, Furie BC. Thrombus formation in vivo. J Clin Invest. 2005;115(12):3355-3362. (Pubitemid 43121819)
2. Ruggeri ZM. Platelets in atherothrombosis. Nat Med. 2002;8(11):1227-1234. (Pubitemid 35373553)
3. Watson SP. Platelet activation by extracellular matrix proteins in haemostasis and thrombosis. Curr Pharm Des. 2009;15(12):1358-1372.
4. McCarty OJ, Larson MK, Auger JM, et al. Rac1 is essential for platelet lamellipodia formation and aggregate stability under flow. J Biol Chem. 2005; 280(47):39474-39484. (Pubitemid 41713905)
5. Watson SP, Auger JM, McCarty OJ, Pearce AC. GPVI and integrin alphaIIb beta3 signaling in platelets. J Thromb Haemost. 2005;3(8): 1752-1762. (Pubitemid 41716562)
6. Dann SG, Selvaraj A, Thomas G. mTOR Complex1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol Med. 2007;13(6):252-259. (Pubitemid 46836871)
7. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol. 2011;12(1):21-35.
8. Guertin DA, Sabatini DM. The pharmacology of mTOR inhibition. Sci Signal. 2009;2(67):pe24.
9. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol. 2009;27(13):2278-2287.
10. Berven LA, Crouch MF. Cellular function of p70S6K: a role in regulating cell motility. Immunol Cell Biol. 2000;78(4):447-451. (Pubitemid 30655572)
11. Zhou H, Huang S. mTOR signaling in cancer cell motility and tumor metastasis. Crit Rev Eukaryot Gene Expr. 2010;20(1):1-16.
12. Berven LA, Willard FS, Crouch MF. Role of the p70(S6K) pathway in regulating the actin cytoskeleton and cell migration. Exp Cell Res. 2004; 296(2):183-195. (Pubitemid 38624640)
13. Rhoads JM, Niu X, Odle J, Graves LM. Role of mTOR signaling in intestinal cell migration. Am J Physiol Gastrointest Liver Physiol. 2006;291(3): G510-517.
14. Sakakibara K, Liu B, Hollenbeck S, Kent KC. Rapamycin inhibits fibronectin-induced migration of the human arterial smooth muscle line (E47) through the mammalian target of rapamycin. Am J Physiol Heart Circ Physiol. 2005;288(6): H2861-2868.
15. Liu L, Li F, Cardelli JA, Martin KA, Blenis J, Huang S. Rapamycin inhibits cell motility by suppression of mTOR-mediated S6K1 and 4E-BP1 pathways. Oncogene. 2006;25(53):7029-7040. (Pubitemid 44722071)
16. Liu L, Chen L, Chung J, Huang S. Rapamycin inhibits F-actin reorganization and phosphorylation of focal adhesion proteins. Oncogene. 2008; 27(37):4998-5010.
17. Liu L, Chen L, Luo Y, et al. Rapamycin inhibits IGF-1 stimulated cell motility through PP2A pathway. PLoS One. 2010;5(5):e10578.
18. Crouch MF. Regulation of thrombin-induced stress fibre formation in Swiss 3T3 cells by the 70-kDa S6 kinase. Biochem Biophys Res Commun. 1997;233(1):193-199. (Pubitemid 27215934)
19. Chou MM, Blenis J. The 70 kDa S6 kinase complexes with and is activated by the Rho family G proteins Cdc42 and Rac1. Cell. 1996;85(4): 573-583. (Pubitemid 26157195)
20. Liu L, Luo Y, Chen L, et al. Rapamycin inhibits cytoskeleton reorganization and cell motility by suppressing RhoA expression and activity. J Biol Chem. 2010;285(49):38362-38373.
21. Ip CK, Cheung AN, Ngan HY, Wong AS. p70 S6 kinase in the control of actin cytoskeleton dynamics and directed migration of ovarian cancer cells. Oncogene. 2011;30(21):2420-32.
22. Gulhati P, Bowen KA, Liu J, et al. mTORC1 and mTORC2 Regulate EMT, Motility, and Metastasis of Colorectal Cancer via RhoA and Rac1 Signaling Pathways. Cancer Res. 2011;71(9):3246-3256.
23. Larson Y, Liu J, Stevens PD, et al. Tuberous sclerosis complex 2 (TSC2) regulates cell migration and polarity through activation of CDC42 and RAC1. J Biol Chem. 2010;285(32):24987-24998.
24. Chan S. Targeting the mammalian target of rapamycin (mTOR): a new approach to treating cancer. Br J Cancer. 2004;91(8):1420-1424. (Pubitemid 39486341)
25. Gabardi S, Baroletti SA. Everolimus: a proliferation signal inhibitor with clinical applications in organ transplantation, oncology, and cardiology. Pharmacotherapy. 2010;30(10):1044-1056.
26. Holmes DR, Jr., Kereiakes DJ, Garg S, et al. Stent thrombosis. J Am Coll Cardiol. 2010;56(17): 1357-1365.
27. Iakovou I, Schmidt T, Bonizzoni E, et al. Incidence, predictors, and outcome of thrombosis after successful implantation of drug-eluting stents. JAMA. 2005;293(17):2126-2130. (Pubitemid 40617065)
28. Baetta R, Granata A, Canavesi M, et al. Everolimus inhibits monocyte/macrophage migration in vitro and their accumulation in carotid lesions of cholesterol-fed rabbits. J Pharmacol Exp Ther. 2009;328(2):419-425.
29. Gee I, Trull AK, Charman SC, Alexander GJ. Sirolimus inhibits oxidative burst activity in transplant recipients. Transplantation. 2003;76(12): 1766-1768. (Pubitemid 38032428)
30. Semple JW, Freedman J. Platelets and innate immunity. Cell Mol Life Sci. 2010;67(4):499-511.
31. Itakura A, Aslan JE, Sinha S, et al. Characterization of human platelet binding of recombinant T cell receptor ligand. J Neuroinflammation. 2010;7:75.
32. Boylan B, Gao C, Rathore V, Gill JC, Newman DK, Newman PJ. Identification of FcgammaRIIa as the ITAM-bearing receptor mediating alphaIIbbeta3 outside-in integrin signaling in human platelets. Blood. 2008;112(7):2780-2786.
33. Robbe K, Otto-Bruc A, Chardin P, Antonny B. Dissociation of GDP dissociation inhibitor and membrane translocation are required for efficient activation of Rac by the Dbl homology-pleckstrin homology region of Tiam. J Biol Chem. 2003; 278(7):4756-4762. (Pubitemid 36800977)
34. Buchsbaum RJ, Connolly BA, Feig LA. Regulation of p70 S6 kinase by complex formation between the Rac guanine nucleotide exchange factor (Rac-GEF) Tiam1 and the scaffold spinophilin. J Biol Chem. 2003;278(21):18833-18841. (Pubitemid 36799265)
35. Yu K, Toral-Barza L, Shi C, et al. Biochemical, cellular, and in vivo activity of novel ATPcompetitive and selective inhibitors of the mammalian target of rapamycin. Cancer Res. 2009; 69(15):6232-6240.
36. Garcia-Martinez JM, Moran J, Clarke RG, et al. Ku-0063794 is a specific inhibitor of the mammalian target of rapamycin (mTOR). Biochem J. 2009;421(1):29-42.
37. Barry FA, Graham GJ, Fry MJ, Gibbins JM. Regulation of glycogen synthase kinase 3 in human platelets: a possible role in platelet function? FEBS Lett. 2003;553(1-2):173-178. (Pubitemid 37206346)
38. Haimovich B, Lipfert L, Brugge JS, Shattil SJ. Tyrosine phosphorylation and cytoskeletal reorganization in platelets are triggered by interaction of integrin receptors with their immobilized ligands. J Biol Chem. 1993;268(21):15868-15877. (Pubitemid 23222091)
39. Cosemans JM, Munnix IC, Wetzker R, Heller R, Jackson SP, Heemskerk JW. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood. 2006;108(9): 3045-3052.
40. Babinska A, Markell MS, Salifu MO, Akoad M, Ehrlich YH, Kornecki E. Enhancement of human platelet aggregation and secretion induced by rapamycin. Nephrol Dial Transplant. 1998;13(12): 3153-3159. (Pubitemid 28534723)
41. Pabla R, Weyrich AS, Dixon DA, et al. Integrindependent control of translation: engagement of integrin alphaIIbbeta3 regulates synthesis of proteins in activated human platelets. J Cell Biol. 1999;144(1):175-184. (Pubitemid 29047020)
42. Weyrich AS, Dixon DA, Pabla R, et al. Signaldependent translation of a regulatory protein, Bcl-3, in activated human platelets. Proc Natl Acad Sci U S A. 1998;95(10):5556-5561. (Pubitemid 28224133)
43. Weyrich AS, Denis MM, Schwertz H, et al. mTOR-dependent synthesis of Bcl-3 controls the retraction of fibrin clots by activated human platelets. Blood. 2007;109(5):1975-1983. (Pubitemid 46348195)
44. Luan FL, Ding R, Sharma VK, Chon WJ, Lagman M, Suthanthiran M. Rapamycin is an effective inhibitor of human renal cancer metastasis. Kidney Int. 2003; 63(3):917-926. (Pubitemid 36315569)
45. Huang S, Houghton PJ. Targeting mTOR signaling for cancer therapy. Curr Opin Pharmacol. 2003;3(4):371-377. (Pubitemid 36908940)
46. Sasaki AT, Firtel RA. Regulation of chemotaxis by the orchestrated activation of Ras, PI3K, and TOR. Eur J Cell Biol. 2006; 85(9-10):873-895. (Pubitemid 44334734)
47. Han S, Khuri FR, Roman J. Fibronectin stimulates nonsmall cell lung carcinoma cell growth through activation of Akt/mammalian target of rapamycin/S6 kinase and inactivation of LKB1/ AMP-activated protein kinase signal pathways. Cancer Res. 2006;66(1):315-323. (Pubitemid 43166038)
48. Kahan BD. Efficacy of sirolimus compared with azathioprine for reduction of acute renal allograft rejection: a randomised multicentre study. The Rapamune US Study Group. Lancet. 2000; 356(9225):194-202. (Pubitemid 30446974)
49. Pan CJ, Tang JJ, Weng YJ, Wang J, Huang N. Preparation and characterization of rapamycinloaded PLGA coating stent. J Mater Sci Mater Med. 2007;18(11):2193-2198. (Pubitemid 350167377)