View Item 

Show simple item record

TC21/RRas2 regulates glycoprotein VI–FcRγ‐mediated platelet activation and thrombus stability
dc.contributor.authorJanapati, S.
dc.contributor.authorWurtzel, J.
dc.contributor.authorDangelmaier, C.
dc.contributor.authorManne, B. K.
dc.contributor.authorBhavanasi, D.
dc.contributor.authorKostyak, J. C.
dc.contributor.authorKim, S.
dc.contributor.authorHolinstat, M.
dc.contributor.authorKunapuli, S. P.
dc.contributor.authorGoldfinger, L. E.
dc.date.accessioned2018-08-13T18:52:02Z
dc.date.available2019-10-01T16:02:11Zen
dc.date.issued2018-08
dc.identifier.citationJanapati, S.; Wurtzel, J.; Dangelmaier, C.; Manne, B. K.; Bhavanasi, D.; Kostyak, J. C.; Kim, S.; Holinstat, M.; Kunapuli, S. P.; Goldfinger, L. E. (2018). "TC21/RRas2 regulates glycoprotein VI–FcRγ‐mediated platelet activation and thrombus stability." Journal of Thrombosis and Haemostasis 16(8): 1632-1645.
dc.identifier.issn1538-7933
dc.identifier.issn1538-7836
dc.identifier.urihttps://hdl.handle.net/2027.42/145353
dc.publisherChurchill Livingstone Inc.
dc.publisherWiley Periodicals, Inc.
dc.subject.otherblood platelets
dc.subject.otherembolism and thrombosis
dc.subject.othermonomeric GTP‐binding proteins
dc.subject.otherRAS proteins
dc.subject.othercollagen receptors
dc.titleTC21/RRas2 regulates glycoprotein VI–FcRγ‐mediated platelet activation and thrombus stability
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelInternal Medicine and Specialties
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/145353/1/jth14197.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/145353/2/jth14197_am.pdf
dc.identifier.doi10.1111/jth.14197
dc.identifier.sourceJournal of Thrombosis and Haemostasis
dc.identifier.citedreferencePasvolsky R, Feigelson SW, Kilic SS, Simon AJ, Tal‐Lapidot G, Grabovsky V, Crittenden JR, Amariglio N, Safran M, Graybiel AM, Rechavi G, Ben‐Dor S, Etzioni A, Alon R. A LAD‐III syndrome is associated with defective expression of the Rap‐1 activator CalDAG‐GEFI in lymphocytes, neutrophils, and platelets. J Exp Med 2007; 204: 1571 – 82.
dc.identifier.citedreferenceFrench DL, Coller BS. Hematologically important mutations: Glanzmann thrombasthenia. Blood Cells Mol Dis 1997; 23: 39 – 51.
dc.identifier.citedreferenceNurden AT, Didry D, Rosa JP. Molecular defects of platelets in Bernard–Soulier syndrome. Blood Cells 1983; 9: 333 – 58.
dc.identifier.citedreferencePeyvandi F, Kunicki T, Lillicrap D. Genetic sequence analysis of inherited bleeding diseases. Blood 2013; 122: 3423 – 31.
dc.identifier.citedreferenceOertli B, Han J, Marte BM, Sethi T, Downward J, Ginsberg M, Hughes PE. The effector loop and prenylation site of R‐Ras are involved in the regulation of integrin function [In Process Citation]. Oncogene 2000; 19: 4961 – 9.
dc.identifier.citedreferenceEto K, Murphy R, Kerrigan SW, Bertoni A, Stuhlmann H, Nakano T, Leavitt AD, Shattil SJ. Megakaryocytes derived from embryonic stem cells implicate CalDAG‐GEFI in integrin signaling. Proc Natl Acad Sci USA 2002; 99: 12819 – 24.
dc.identifier.citedreferenceTao L, Zhang Y, Xi X, Kieffer N. Recent advances in the understanding of the molecular mechanisms regulating platelet integrin alphaIIbbeta3 activation. Protein Cell 2010; 1: 627 – 37.
dc.identifier.citedreferenceCanault M, Ghalloussi D, Grosdidier C, Guinier M, Perret C, Chelghoum N, Germain M, Raslova H, Peiretti F, Morange PE, Saut N, Pillois X, Nurden AT, Cambien F, Pierres A, van den Berg TK, Kuijpers TW, Alessi MC, Tregouet DA. Human CalDAG‐GEFI gene (RASGRP2) mutation affects platelet function and causes severe bleeding. J Exp Med 2014; 211: 1349 – 62.
dc.identifier.citedreferenceCifuni SM, Wagner DD, Bergmeier W. CalDAG‐GEFI and protein kinase C represent alternative pathways leading to activation of integrin alphaIIbbeta3 in platelets. Blood 2008; 112: 1696 – 703.
dc.identifier.citedreferenceSaci A, Liu WQ, Vidal M, Garbay C, Rendu F, Bachelot‐Loza C. Differential effect of the inhibition of Grb2–SH3 interactions in platelet activation induced by thrombin and by Fc receptor engagement. Biochem J 2002; 363: 717 – 25.
dc.identifier.citedreferenceMitin N, Rossman KL, Der CJ. Signaling interplay in Ras superfamily function. Curr Biol 2005; 15: R563 – 74.
dc.identifier.citedreferenceClark EA, Shattil SJ, Ginsberg MH, Bolen J, Brugge JS. Regulation of the protein tyrosine kinase pp72SYK by platelet agonists and the integrin αIIbβ3. J Biol Chem 1994; 269: 28859 – 64.
dc.identifier.citedreferenceYanaga F, Poole A, Asser U, Blake R, Schieven GL, Clark EA, Che‐Leung L, Watson SP. Syk interacts with tyrosine‐phosphorylated proteins in human platelets activated by collagen and cross‐linking of the Fcy‐IIA receptor. Biochem J 1995; 311: 471 – 8.
dc.identifier.citedreferencePoole A, Gibbins JM, Turner M, van Vugt M, van de Winkel J, Saito T, Tybulewicz VLJ, Watson SP. The Fc receptor gamma‐chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J 1997; 16: 2333 – 41.
dc.identifier.citedreferenceGeahlen RL. Syk and pTyr’d: signaling through the B cell antigen receptor. Biochim Biophys Acta 2009; 1793: 1115 – 27.
dc.identifier.citedreferencePalacios EH, Weiss A. Function of the Src‐family kinases, Lck and Fyn, in T‐cell development and activation. Oncogene 2004; 23: 7990 – 8000.
dc.identifier.citedreferenceEzumi Y, Kodama K, Uchiyama T, Takayama H. Constitutive and functional association of the platelet collagen receptor glycoprotein VI–Fc receptor gamma‐chain complex with membrane rafts. Blood 2002; 99: 3250 – 5.
dc.identifier.citedreferenceSchmitter T, Pils S, Sakk V, Frank R, Fischer KD, Hauck CR. The granulocyte receptor carcinoembryonic antigen‐related cell adhesion molecule 3 (CEACAM3) directly associates with Vav to promote phagocytosis of human pathogens. J Immunol 2007; 178: 3797 – 805.
dc.identifier.citedreferenceWatson SP, Herbert JM, Pollitt AY. GPVI and CLEC‐2 in hemostasis and vascular integrity. J Thromb Haemost 2010; 8: 1456 – 67.
dc.identifier.citedreferenceBergmeier W, Stefanini L. Platelet ITAM signaling. Curr Opin Hematol 2013; 20: 445 – 50.
dc.identifier.citedreferenceTadokoro S, Shattil S, Eto K, Tai V, Liddington R, de Pereda J, Ginsberg MH, Calderwood DA. Talin binding to integrin beta tails: a final common step in integrin activation. Science 2003; 302: 103 – 6.
dc.identifier.citedreferenceHynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002; 110: 673 – 87.
dc.identifier.citedreferenceHuang Y, Rangwala F, Fulkerson PC, Ling B, Reed E, Cox AD, Kamholz J, Ratner N. Role of TC21/R‐Ras2 in enhanced migration of neurofibromin‐deficient Schwann cells. Oncogene 2004; 23: 368 – 78.
dc.identifier.citedreferenceLuo H, Hao X, Ge C, Zhao F, Zhu M, Chen T, Yao M, He X, Li J. TC21 promotes cell motility and metastasis by regulating the expression of E‐cadherin and N‐cadherin in hepatocellular carcinoma. Int J Oncol 2010; 37: 853 – 9.
dc.identifier.citedreferenceJeong HW, Nam JO, Kim IS. The COOH‐terminal end of R‐Ras alters the motility and morphology of breast epithelial cells through Rho/Rho‐kinase. Cancer Res 2005; 65: 507 – 15.
dc.identifier.citedreferenceKeely PJ, Rusyn EV, Cox AD, Parise LV. R‐Ras signals through specific integrin alpha cytoplasmic domains to promote migration and invasion of breast epithelial cells. J Cell Biol 1999; 145: 1077 – 88.
dc.identifier.citedreferenceShen B, Zhao X, O’Brien KA, Stojanovic‐Terpo A, Delaney MK, Kim K, Cho J, Lam SC, Du X. A directional switch of integrin signalling and a new anti‐thrombotic strategy. Nature 2013; 503: 131 – 5.
dc.identifier.citedreferenceEstevez B, Shen B, Du X. Targeting integrin and integrin signaling in treating thrombosis. Arterioscler Thromb Vasc Biol 2014; 35: 24 – 9.
dc.identifier.citedreferenceLockyer S, Okuyama K, Begum S, Le S, Sun B, Watanabe T, Matsumoto Y, Yoshitake M, Kambayashi J, Tandon NN. GPVI‐deficient mice lack collagen responses and are protected against experimentally induced pulmonary thromboembolism. Thromb Res 2006; 118: 371 – 80.
dc.identifier.citedreferencePlow EF, Ginsberg MH, Furie B, Shattil SJ. The molecular basis of platelet function. In: Hoffman R, Benz EJ Jr, Shattil SJ, Furi B, Cohen HJ, Silberstein LE, eds. Hematology: Basic Principles and Practice. New York, NY: Churchill Livingstone Inc., 1995: 1524 – 35.
dc.identifier.citedreferenceKatagiri K, Hattori M, Minato N, Irie S, Takatsu K, Kinashi T. Rap1 is a potent activation signal for leukocyte function‐associated antigen 1 distinct from protein kinase C and phosphatidylinositol‐3‐OH kinase. Mol Cell Biol 2000; 20: 1956 – 69.
dc.identifier.citedreferenceReedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, van Kooyk Y, Salmon M, Buckley CD, Bos JL. The small GTPase, Rap1, mediates CD31‐induced integrin adhesion. J Cell Biol 2000; 148: 1151 – 8.
dc.identifier.citedreferenceArai A, Nosaka Y, Kanda E, Yamamoto K, Miyasaka N, Miura O. Rap1 is activated by erythropoietin or interleukin‐3 and is involved in regulation of beta1 integrin‐mediated hematopoietic cell adhesion. J Biol Chem 2001; 276: 10453 – 62.
dc.identifier.citedreferencede Bruyn KM, Rangarajan S, Reedquist KA, Figdor CG, Bos JL. The small GTPase Rap1 is required for Mn(2+)‐ and antibody‐induced LFA‐1‐ and VLA‐4‐mediated cell adhesion. J Biol Chem 2002; 277: 29468 – 76.
dc.identifier.citedreferenceSebzda E, Bracke M, Tugal T, Hogg N, Cantrell DA. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat Immunol 2002; 3: 251 – 8.
dc.identifier.citedreferenceHughes PE, Oertli B, Han J, Ginsberg MH. R‐Ras regulation of integrin function. Methods Enzymol 2001; 333: 163 – 71.
dc.identifier.citedreferenceHughes PE, Renshaw MW, Pfaff M, Forsyth J, Keivens VM, Schwartz MA, Ginsberg MH. Suppression of integrin activation: a novel function of a Ras/Raf‐initiated MAP kinase pathway. Cell 1997; 88: 521 – 30.
dc.identifier.citedreferenceHan J, Lim CJ, Watanabe N, Soriani A, Ratnikov B, Calderwood DA, Puzon‐McLaughlin W, Lafuente EM, Boussiotis VA, Shattil SJ, Ginsberg MH. Reconstructing and deconstructing agonist‐induced activation of integrin alphaIIbbeta3. Curr Biol 2006; 16: 1796 – 806.
dc.identifier.citedreferenceShock DD, He K, Wencel‐Drake JD, Parise LV. Ras activation in platelets after stimulation of the thrombin receptor, thromboxane A 2 receptor or protein kinase C. Biochem J 1997; 321: 525 – 30.
dc.identifier.citedreferenceTulasne D, Bori T, Watson SP. Regulation of RAS in human platelets. Evidence that activation of RAS is not sufficient to lead to ERK1‐2 phosphorylation. Eur J Biochem 2002; 269: 1511 – 17.
dc.identifier.citedreferenceKinbara K, Goldfinger LE, Hansen M, Chou FL, Ginsberg MH. Ras GTPases: integrins’ friends or foes? Nat Rev Mol Cell Biol 2003; 4: 767 – 76.
dc.identifier.citedreferenceSethi T, Ginsberg MH, Downward J, Hughes PE. The small GTP‐binding protein R‐Ras can influence integrin activation by antagonizing a Ras/Raf initiated integrin suppression pathway. Mol Biol Cell 1999; 10: 1799 – 809.
dc.identifier.citedreferenceDowal L, Yang W, Freeman MR, Steen H, Flaumenhaft R. Proteomic analysis of palmitoylated platelet proteins. Blood 2011; 118: e62 – 73.
dc.identifier.citedreferenceRosario M, Paterson HF, Marshall CJ. Activation of the Raf/MAP kinase cascade by the Ras‐related protein TC21 is required for the TC21‐mediated transformation of NIH 3T3 cells. EMBO J 1999; 18: 1270 – 9.
dc.identifier.citedreferenceRosario M, Paterson HF, Marshall CJ. Activation of the Ral and phosphatidylinositol 3′ kinase signaling pathways by the ras‐related protein TC21. Mol Cell Biol 2001; 21: 3750 – 62.
dc.identifier.citedreferenceSelf AJ, Caron E, Paterson HF, Hall A. Analysis of R‐Ras signalling pathways. J Cell Sci 2001; 114: 1357 – 66.
dc.identifier.citedreferenceMarte BM, Rodriguez‐Viciana P, Wennstrom S, Warne PH, Downward J. R‐Ras can activate the phosphoinositide 3‐kinase but not the MAP kinase arm of the Ras effector pathways. Curr Biol 1997; 7: 63 – 70.
dc.identifier.citedreferenceMovilla N, Crespo P, Bustelo XR. Signal transduction elements of TC21, an oncogenic member of the R‐Ras subfamily of GTP‐binding proteins. Oncogene 1999; 18: 5860 – 9.
dc.identifier.citedreferenceLarive RM, Abad A, Cardaba CM, Hernandez T, Canamero M, de Alava E, Santos E, Alarcon B, Bustelo XR. The Ras‐like protein R‐Ras2/TC21 is important for proper mammary gland development. Mol Biol Cell 2012; 23: 2373 – 87.
dc.identifier.citedreferenceDelgado P, Cubelos B, Calleja E, Martinez‐Martin N, Cipres A, Merida I, Bellas C, Bustelo XR, Alarcon B. Essential function for the GTPase TC21 in homeostatic antigen receptor signaling. Nat Immunol 2009; 10: 880 – 8.
dc.identifier.citedreferenceFrancischetti IM, Saliou B, Leduc M, Carlini CR, Hatmi M, Randon J, Faili A, Bon C. Convulxin, a potent platelet‐aggregating protein from Crotalus durissus terrificus venom, specifically binds to platelets. Toxicon 1997; 35: 1217 – 28.
dc.identifier.citedreferencede Rooij J, Bos JL. Minimal Ras‐binding domain of Raf1 can be used as an activation‐specific probe for Ras. Oncogene 1997; 14: 623 – 5.
dc.identifier.citedreferenceStefanini L, Boulaftali Y, Ouellette TD, Holinstat M, Desire L, Leblond B, Andre P, Conley PB, Bergmeier W. Rap1–Rac1 circuits potentiate platelet activation. Arterioscler Thromb Vasc Biol 2012; 32: 434 – 41.
dc.identifier.citedreferenceKim S, Dangelmaier C, Bhavanasi D, Meng S, Wang H, Goldfinger LE, Kunapuli SP. RhoG protein regulates glycoprotein VI–Fc receptor gamma‐chain complex‐mediated platelet activation and thrombus formation. J Biol Chem 2013; 288: 34230 – 8.
dc.identifier.citedreferenceDaniel JL, Dangelmaier CA, Mada S, Buitrago L, Jin J, Langdon WY, Tsygankov AY, Kunapuli SP, Sanjay A. Cbl‐b is a novel physiologic regulator of glycoprotein VI‐dependent platelet activation. J Biol Chem 2010; 285: 17282 – 91.
dc.identifier.citedreferenceKim S, Jin J, Kunapuli SP. Relative contribution of G‐protein‐coupled pathways to protease‐activated receptor‐mediated Akt phosphorylation in platelets. Blood 2006; 107: 947 – 54.
dc.identifier.citedreferenceMao G, Songdej N, Voora D, Goldfinger LE, Del Carpio‐Cano FE, Myers RA, Rao AK. Transcription factor RUNX1 regulates platelet PCTP (phosphatidylcholine transfer protein): implications for cardiovascular events: differential effects of RUNX1 variants. Circulation 2017; 136: 927 – 39.
dc.identifier.citedreferenceMao GF, Goldfinger LE, Fan DC, Lambert MP, Jalagadugula G, Freishtat R, Rao AK. Dysregulation of PLDN (pallidin) is a mechanism for platelet dense granule deficiency in RUNX1 haplodeficiency. J Thromb Haemost 2017; 15: 792 – 801.
dc.identifier.citedreferenceBynagari‐Settipalli YS, Lakhani P, Jin J, Bhavaraju K, Rico MC, Kim S, Woulfe D, Kunapuli SP. Protein kinase C isoform epsilon negatively regulates ADP‐induced calcium mobilization and thromboxane generation in platelets. Arterioscler Thromb Vasc Biol 2012; 32: 1211 – 19.
dc.identifier.citedreferenceShen MY, Hsiao G, Fong TH, Chen HM, Chou DS, Lin CH, Sheu JR, Hsu CY. Amyloid beta peptide‐activated signal pathways in human platelets. Eur J Pharmacol 2008; 588: 259 – 66.
dc.identifier.citedreferenceLewandrowski U, Wortelkamp S, Lohrig K, Zahedi RP, Wolters DA, Walter U, Sickmann A. Platelet membrane proteomics: a novel repository for functional research. Blood 2009; 114: e10 – 19.
dc.identifier.citedreferenceMartinez‐Martin N, Fernandez‐Arenas E, Cemerski S, Delgado P, Turner M, Heuser J, Irvine DJ, Huang B, Bustelo XR, Shaw A, Alarcon B. T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase‐dependent phagocytosis. Immunity 2011; 35: 208 – 22.
dc.identifier.citedreferenceAlarcon B, Martinez‐Martin N. RRas2. RhoG and T‐cell phagocytosis. Small GTPases 2012; 3: 97 – 101.
dc.identifier.citedreferenceBergmeier W, Schulte V, Brockhoff G, Bier U, Zirngibl H, Nieswandt B. Flow cytometric detection of activated mouse integrin alphaIIbbeta3 with a novel monoclonal antibody. Cytometry 2002; 48: 80 – 6.
dc.identifier.citedreferenceIsraels SJ, Gerrard JM, Jacques YV, McNicol A, Cham B, Nishibori M, Bainton DF. Platelet dense granule membranes contain both granulophysin and P‐selectin (GMP‐140). Blood 1992; 80: 143 – 52.
dc.identifier.citedreferenceWatson SP, Auger JM, McCarty OJ, Pearce AC. GPVI and integrin alphaIIb beta3 signaling in platelets. J Thromb Haemost 2005; 3: 1752 – 62.
dc.identifier.citedreferenceJung SM, Moroi M. Platelet glycoprotein VI. Adv Exp Med Biol 2008; 640: 53 – 63.
dc.identifier.citedreferenceZhi H, Rauova L, Hayes V, Gao C, Boylan B, Newman DK, McKenzie SE, Cooley BC, Poncz M, Newman PJ. Cooperative integrin/ITAM signaling in platelets enhances thrombus formation in vitro and in vivo. Blood 2013; 121: 1858 – 67.
dc.identifier.citedreferenceTomiyama Y, Kunicki TJ, Zipf TF, Ford SB, Aster RH. Response of human platelets to activating monoclonal antibodies: importance of Fc gamma RII (CD32) phenotype and level of expression. Blood 1992; 80: 2261 – 8.
dc.identifier.citedreferenceManne BK, Getz TM, Hughes CE, Alshehri O, Dangelmaier C, Naik UP, Watson SP, Kunapuli SP. Fucoidan is a novel platelet agonist for the C‐type lectin‐like receptor 2 (CLEC‐2). J Biol Chem 2013; 288: 7717 – 26.
dc.identifier.citedreferenceAlshehri OM, Montague S, Watson S, Carter P, Sarker N, Manne BK, Miller JL, Herr AB, Pollitt AY, O’Callaghan CA, Kunapuli S, Arman M, Hughes CE, Watson SP. Activation of glycoprotein VI (GPVI) and C‐type lectin‐like receptor‐2 (CLEC‐2) underlies platelet activation by diesel exhaust particles and other charged/hydrophobic ligands. Biochem J 2015; 468: 459 – 73.
dc.identifier.citedreferenceAlshehri OM, Hughes CE, Montague S, Watson SK, Frampton J, Bender M, Watson SP. Fibrin activates GPVI in human and mouse platelets. Blood 2015; 126: 1601 – 8.
dc.identifier.citedreferenceMammadova‐Bach E, Ollivier V, Loyau S, Schaff M, Dumont B, Favier R, Freyburger G, Latger‐Cannard V, Nieswandt B, Gachet C, Mangin PH, Jandrot‐Perrus M. Platelet glycoprotein VI binds to polymerized fibrin and promotes thrombin generation. Blood 2015; 126: 683 – 91.
dc.identifier.citedreferenceBaker EK, Tozer EC, Pfaff M, Shattil SJ, Loftus JC, Ginsberg MH. A genetic analysis of integrin function: Glanzmann thrombasthenia in vitro. Proc Natl Acad Sci USA 1997; 94: 1973 – 8.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
jth14197.pdf
Size:
981.3KB
Format:
PDF
View/Open
Name:
jth14197_am.pdf
Size:
928.0KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.