A newly identified complex of spinophilin and the tyrosine phosphatase, SHP-1, modulates platelet activation by regulating G protein-dependent signaling

Blood

Volumn 119, Issue 8, 2012, Pages 1935-1945

  Ma, Peisong ^a   Cierniewska, Aleksandra ^a   Signarvic, Rachel ^a   Cieslak, Marcin ^a   Kong, Hong ^a   Sinnamon, Andrew J ^a   Neubig, Richard R ^b   Newman, Debra K ^c   Stalker, Timothy J ^a   Brass, Lawrence F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c BLOOD RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GUANINE NUCLEOTIDE BINDING PROTEIN; PROSTACYCLIN; PROTEIN TYROSINE PHOSPHATASE SHP 1; SCAFFOLD PROTEIN; SPINOPHILIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INHIBITION KINETICS; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; THROMBOCYTE; THROMBOCYTE ACTIVATION;

EID: 84857520121     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-10-387910     Document Type: Article

References (45)

1. Offermanns S. Activation of platelet function through G protein-coupled receptors. Circ Res. 2006;99(12):1293-1304. (Pubitemid 44949665)
2. Mustard JF, Kinlough-Rathbone RL, Packham MA. Prostaglandins and platelets. Annu Rev Med. 1980;31:89-96.
3. Signarvic RS, Cierniewska A, Stalker TJ, et al. RGS/Gi2alpha interactions modulate platelet accumulation and thrombus formation at sites of vascular injury. Blood. 2010;116(26):6092-6100.
4. Xie GX, Palmer PP. How regulators of G protein signaling achieve selective regulation. J Mol Biol. 2007;366(2):349-365. (Pubitemid 46136207)
5. Bansal G, Druey KM, Xie Z. R4 RGS proteins: regulation of G-protein signaling and beyond. Pharmacol Ther. 2007;116(3):473-495. (Pubitemid 350116944)
6. Allen PB, Ouimet CC, Greengard P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci U S A. 1997;94(18):9956-9961. (Pubitemid 27408172)
7. Satoh A, Nakanishi H, Obaishi H, et al. Neurabin- II/spinophilin. An actin filament-binding protein with one PDZ domain localized at cadherin-based cell-cell adhesion sites. J Biol Chem. 1998;273(6):3470-3475. (Pubitemid 28109767)
8. Sarrouilhe D, di TommasoA, Metaye T, Ladeveze V. Spinophilin: from partners to functions. Biochimie. 2006;88(9):1099-1113.
9. Wang X, Zeng W, Soyombo AA, et al. Spinophilin regulates Ca2+ signalling by binding the N-terminal domain of RGS2 and the third intracellular loop of G-protein-coupled receptors. Nat Cell Biol. 2005;7(4):405-411. (Pubitemid 40533131)
10. Wang X, ZengW, Kim MS, Allen PB, Greengard P, Muallem S. Spinophilin/neurabin reciprocally regulate signaling intensity by G protein-coupled receptors. EMBO J. 2007;26(11):2768-2776. (Pubitemid 46884271)
11. Smith FD, Oxford GS, Milgram SL. Association of the D2 dopamine receptor third cytoplasmic loop with spinophilin, a protein phosphatase-1-interacting protein. J Biol Chem. 1999;274(28):19894-19900.
12. Richman JG, Brady AE, Wang Q, Hensel JL, Colbran RJ, Limbird LE. Agonist-regulated interaction between alpha2-adrenergic receptors and spinophilin. J Biol Chem. 2001;276(18):15003-15008.
13. Plutzky J, Neel BG, Rosenberg RD. Isolation of a src homology 2-containing tyrosine phosphatase. Proc Natl Acad Sci U S A. 1992;89(3):1123-1127.
14. Butkerait P, Zheng Y, Hallak H, et al. Expressionof the human 5-hydroxytryptamine1A receptor in Sf9 cells. Reconstitution of a coupled phenotype by co-expression of mammalian G protein subunits. J Biol Chem. 1995;270(31):18691-18699.
15. Feng J, Yan Z, Ferreira A, et al. Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad Sci U S A. 2000;97(16):9287-9292. (Pubitemid 30626711)
16. Zhu L, Bergmeier W, Wu J, et al. Regulated surface expression and shedding support a dual role for semaphorin 4D in platelet responses to vascular injury. Proc Natl Acad Sci U S A. 2007;104(5):1621-1626. (Pubitemid 46214640)
17. Yowe D, Weich N, Prabhudas M, et al. RGS18 is a myeloerythroid lineage-specific regulator of Gprotein-signalling molecule highly expressed in megakaryocytes. Biochem J. 2001;359(pt 1):109-118. (Pubitemid 32939212)
18. Nagata Y, Oda M, Nakata H, Shozaki Y, Kozasa T, Todokoro K. A novel regulator of G-protein signaling bearing GAP activity for Galphai and Galphaq in megakaryocytes. Blood. 2001;97(10):3051-3060.
19. Kim SD, Sung HJ, Park SK, et al. The expression patterns of RGS transcripts in platelets. Platelets. 2006;17(7):493-497. (Pubitemid 44665573)
20. Gagnon AW, Murray DL, Leadley RJ. Cloning and characterization of a novel regulator of G protein signalling in human platelets. Cell Signal. 2002;14(7):595-606. (Pubitemid 34304344)
21. Garcia A, Prabhakar S, Hughan S, et al. Differential proteome analysis of TRAP-activated platelets: involvement of DOK-2 and phosphorylation of RGS proteins. Blood. 2004;103(6):2088-2095. (Pubitemid 38326224)
22. Berthebaud M, Riviere C, Jarrier P, et al. RGS16 is a negative regulator of SDF-1-CXCR4 signaling in megakaryocytes. Blood. 2005;106(9):2962-2968. (Pubitemid 41565886)
23. Rowley JW, Oler A, Tolley ND, et al. Genomewide RNA-seq analysis of human and mouse platelet transcriptomes. Blood. 2011;118(14):e101-e111.
24. Hunt TW, Fields TA, Casey PJ, Peralta EG. RGS10 is a selective activator of Galphai GTPase activity. Nature. 1996;383(6596):175-177. (Pubitemid 26303981)
25. Barrow AD, Trowsdale J. You say ITAM and I say ITIM, let's call the whole thing off: the ambiguity of immunoreceptor signalling. Eur J Immunol. 2006;36(7):1646-1653. (Pubitemid 44089030)
26. Ravetch JV, Lanier LL. Immune inhibitory receptors. Science. 2000;290(5489):84-89.
27. Neel BG, Gu H, Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci. 2003;28(6):284-293. (Pubitemid 36776291)
28. Jones ML, Craik JD, Gibbins JM, Poole AW. Regulation of SHP-1 tyrosine phosphatase in human platelets by serine phosphorylation at its C terminus. J Biol Chem. 2004;279(39):40475-40483. (Pubitemid 39287638)
29. Lorenz U. SHP-1 and SHP-2 in T cells: two phosphatases functioning at many levels. Immunol Rev. 2009;228(1):342-359.
30. Chen L, Sung SS, Yip ML, et al. Discovery of a novel shp2 protein tyrosine phosphatase inhibitor. Mol Pharmacol. 2006;70(2):562-570. (Pubitemid 44092317)
31. Bjorbaek C, Buchholz RM, Davis SM, et al. Divergent roles of SHP-2 in ERK activation by leptin receptors. J Biol Chem. 2001;276(7):4747-4755.
32. Zhang Z, Shen K, Lu W, Cole PA. The role of Cterminal tyrosine phosphorylation in the regulation of SHP-1 explored via expressed protein ligation. J Biol Chem. 2003;278(7):4668-4674. (Pubitemid 36800966)
33. Pasquet JM, Quek L, Pasquet S, et al. Evidence of a role for SHP-1 in platelet activation by the collagen receptor glycoprotein VI. J Biol Chem. 2000;275(37):28526-28531.
34. Hanke JH, Gardner JP, Dow RL, et al. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynTdependent T cell activation. J Biol Chem. 1996; 271(2):695-701.
35. Allen PB, Zachariou V, Svenningsson P, et al. Distinct roles for spinophilin and neurabin in dopamine- mediated plasticity. Neuroscience. 2006;140(3):897-911. (Pubitemid 43767470)
36. Stafstrom-Davis CA, Ouimet CC, Feng J, Allen PB, Greengard P, Houpt TA. Impaired conditioned taste aversion learning in spinophilin knockout mice. Learn Mem. 2001;8(5):272-278. (Pubitemid 32959641)
37. Crittenden JR, Bergmeier W, Zhang Y, et al. CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat Med. 2004;10(9):982-986. (Pubitemid 39273740)
38. Sinnarajah S, Dessauer CW, Srikumar D, et al. RGS2 regulates signal transduction in olfactory neurons by attenuating activation of adenylyl cyclase III. Nature. 2001;409(6823):1051-1055. (Pubitemid 32204058)
39. Salim S, Sinnarajah S, Kehrl JH, Dessauer CW. Identification of RGS2 and type V adenylyl cyclase interaction sites. J Biol Chem. 2003;278(18):15842- 15849. (Pubitemid 36799699)
40. Murata T, Ushikubi F, Matsuoka T, et al. Altered pain perception and inflammatory response in mice lacking prostacyclin receptor. Nature. 1997;388(6643):678-682. (Pubitemid 27366439)
41. Li RY, Gaits F, Ragab-Thomas JM, et al. Protein tyrosine phosphatase SHP-1 fails to associate with cytoskeleton but is normally phosphorylated upon thrombin stimulation of thrombasthenic platelets. Thromb Haemost. 1997;77(1):150-154. (Pubitemid 27064985)
42. Hibbs ML, Harder KW, Armes J, et al. Sustained activation of Lyn tyrosine kinase in vivo leads to autoimmunity. J Exp Med. 2002;196(12):1593-1604. (Pubitemid 36026471)
43. Katsel PL, Tagliente TM, Schwarz TE, Craddock-Royal BD, Patel ND, Maayani S. Molecular and biochemical evidence for the presence of type III adenylyl cyclase in human platelets. Platelets. 2003;14(1):21-33. (Pubitemid 36237736)
44. Jones ML, Poole AW. Protein tyrosine phosphatases. Methods Mol Biol. 2004;273:169-178.
45. Abramow-Newerly M, Roy AA, Nunn C, Chidiac P. RGS proteins have a signalling complex: interactions between RGS proteins and GPCRs, effectors, and auxiliary proteins. Cell Signal. 2006;18(5):579-591. (Pubitemid 43113289)