A critical role for the transient receptor potential channel type 6 in human platelet activation

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Vemana, Hari Priya ^a   Karim, Zubair A ^a   Conlon, Christine ^a   Khasawneh, Fadi T ^a  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 [3 [(4 PHENYLSEMICARBAZIDO)METHYL] 7 OXABICYCLO[2.2.1]HEPT 2 YL] 5 HEPTENOIC ACID; ADENOSINE DIPHOSPHATE; CALCIUM; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FIBRINOGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; THROMBOXANE RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL AFFECTING AGENT; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BLOOD CLOTTING; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HEMOSTASIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; RECEPTOR UPREGULATION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION INHIBITION; THROMBOCYTE FUNCTION; THROMBOCYTE RELEASE REACTION; THROMBOSIS; ANIMAL; C57BL MOUSE; CELL CULTURE; METABOLISM; PHYSIOLOGY; THROMBOCYTE; THROMBOCYTE AGGREGATION;

ANIMALS; BLOOD PLATELETS; CELLS, CULTURED; HUMANS; MICE; MICE, INBRED C57BL; PLATELET ACTIVATION; PLATELET AGGREGATION; RECEPTORS, THROMBOXANE; TRPC CATION CHANNELS;

EID: 84939124316     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125764     Document Type: Article

References (53)

1. Behnke O (1970) Microtubules in disk-shaped blood cells. Int Rev Exp Pathol 9:1-92. PMID: 5499012
2. Parise LV, Venton DL, Le Breton GC (1984) Arachidonic acid-induced platelet aggregation is mediated by a thromboxane A2/prostaglandin H2 receptor interaction. J Pharmacol ExpTher 228:240-244. PMID: 6319669
3. Hamberg M, Svensson J, Samuelsson B (1975) Thromboxanes: a new group of biologically active compounds derived from prostaglandin endoperoxides. Proc Natl Acad Sci US A 72:2994-2998. PMID: 1059088
4. Ghali NI, Kattelman EJ, Hung SC, Schnorf KE, Le Breton GC, Venton DL. (1984) Synthesis of [17, 18-3H] trans-13-azaprostanoic acid. A labeled probe for the PGH2/TXA2 receptor. Prostaglandins 27:865-876. PMID: 6091182
5. Hung SC, Ghali NI, Venton DL, Le Breton GC (1983) Specific binding of the thromboxane A2 antagonist 13-azaprostanoic acid to human platelet membranes. BiochimBiophysActa 728:171-178. PMID: 6219702
6. Halushka PV, Mais DE, Mayeux PR, Morinelli TA (1989) Thromboxane, prostaglandin and leukotriene receptors. Annu Rev Pharmacol Toxicol 29:213-239. PMID: 2543270
7. Owen NE, Le Breton GC (1981) Ca2+mobilization in blood platelets as visualized by chlortetracycline fluorescence. Am J Physiol 241: H613-619. PMID: 6274207
8. Knezevic I, Borg C, Le Breton GC (1993) Identification of Gq as one of the G-proteins which copurify with human platelet thromboxane A2/prostaglandin H2 receptors. The Journal of biological chemistry 268:26011-26017. PMID: 8245033
9. Shenker A, Goldsmith P, Unson CG, Spiegel AM (1991) The G protein coupled to the thromboxane A2 receptor in human platelets is a member of the novel Gq family. The Journal of biological chemistry 266:9309-9313. PMID: 1851174
10. Kinsella BT, O'Mahony DJ, Fitzgerald GA (1997) The human thromboxane A2 receptor alpha isoform (TP alpha) functionally couples to the G proteins Gq and G11 in vivo and is activated by the isoprostane 8-epi prostaglandin F2 alpha. J Pharmacol Exp Ther 281:957-964. PMID: 9152406
11. Djellas Y, Manganello JM, Antonakis K, Le Breton GC (1999) Identification of Galpha13asoneof the G-proteins that couple to human platelet thromboxane A2 receptors. The Journal of biological chemistry 274:14325-14330. PMID: 10318854
12. Offermanns S, Hu YH, Simon MI (1996) Galpha12 and galpha13 are phosphorylated during platelet activation. The Journal of biological chemistry 271:26044-26048. PMID: 8824244
13. Offermanns S, Laugwitz KL, Spicher K, Schultz G (1994) G proteins of the G12 family are activated via thromboxane A2 and thrombin receptors in human platelets. Proc Natl Acad Sci U S A 91:504-508. PMID: 8290554
14. Ushikubi F, Nakamura K, Narumiya S (1994) Functional reconstitution of platelet thromboxane A2 receptors with Gqand Gi2 in phospholipid vesicles. Mol Pharmacol 46:808-816. PMID: 7969066
15. Gao Y, Tang S, Zhou S, Ware JA (2001) The thromboxane A2 receptor activates mitogen-activated protein kinase via protein kinase C-dependent Gi coupling and Src-dependent phosphorylation of the epidermal growth factor receptor. J Pharmacol Exp Ther 296:426-433. PMID: 11160627
16. Brass LF, Manning DR, Cichowski K, Abrams CS (1997) Signaling through G proteins in platelets: to the integrins and beyond. Thrombosis and haemostasis 78:581-589. PMID: 9198220
17. Yang J, Wu J, Kowalska MA, Dalvi A, Prevost N, O'Brien PJ, etal (2000) Loss of signaling through the G protein, Gz, results in abnormal platelet activation and altered responses to psychoactive drugs. Proc Natl Acad Sci U S A 97:9984-9989. PMID: 10954748
18. Klages B, Brandt U, Simon MI, Schultz G, Offermanns S (1999) Activation of G12/G13 results in shape change and Rho/Rho-kinase-mediated myosin light chain phosphorylation in mouse platelets. J Cell Biol 144:745-754. PMID: 10037795
19. Singh I, Knezevic N, Ahmmed GU, Kini V, Malik AB, Mehta D (2007) Galphaq-TRPC6-mediated Ca2+ entry induces RhoA activation and resultant endothelial cell shape change in response to thrombin. The Journal of biological chemistry 282:7833-7843. PMID: 17197445
20. Offermanns S, Toombs CF, Hu YH and Simon MI (1997) Defective platelet activation in G alpha (q)-deficientmice. Nature 389:183-186. PMID: 9296496
21. Bauer M, Retzer M, Wilde JI, Maschberger P, Essler M, Watson SP, etal. (1999) Dichotomous regulation of myosin phosphorylation and shape change by Rho-kinase and calcium in intact human platelets. Blood 94:1665-1672. PMID: 10477691
22. Authi KS (1993) Ca2+ homeostasis and intracellular pools in human platelets. Adv Exp Med Biol 344:83-104. PMID: 8209795
23. Quinton TM, Kim S, Dangelmaier C, Dorsam RT, Jin J, Daniel JL, etal. (2002) Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation. Biochem J 368:535-543. PMID: 12215172
24. Yang X, Sun L, Gabbeta J, Rao AK (1997) Platelet activation with combination of ionophore A23187 and a direct protein kinase C activator induces normal secretion in patients with impaired receptor mediated secretion and abnormal signal transduction. Thrombosis research 88:317-328. PMID: 9526952
25. Charo IF, Feinman RD, Detwiler TC (1977) Interrelations of platelet aggregation and secretion. The Journal of clinical investigation 60:866-873. PMID: 330568
26. Nesbitt WS, Giuliano S, Kulkarni S, Dopheide SM, Harper IS, Jackson SP (2003) Intercellular calcium communication regulates platelet aggregation and thrombus growth. J Cell Biol 160:1151-1161. PMID: 12668663
27. Liao Y, Plummer NW, George MD, Abramowitz J, Zhu MX, Birnbaumer L (2009) A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC: Orai complex may mediate store and receptor operated Ca2+ entry. Proc Natl Acad Sci U S A 106:3202-3206. doi: 10.1073/pnas.0813346106 PMID: 19221033
28. Authi KS (2007) TRP channels in platelet function. Handb Exp Pharmacol: 425-443.
29. Varga-Szabo D, Authi KS, Braun A, Bender M, Ambily A, Hassock SR, etal. (2008) Store-operated Ca (2+) entry in platelets occurs independently of transient receptor potential (TRP) C1. Pflugers Arch 457:377-387. doi: 10.1007/s00424-008-0531-4 PMID: 18546016
30. Carter RN, Tolhurst G, Walmsley G, Vizuete-Forster M, Miller N, Mahaut-Smith MP (2006) Molecular and electrophysiological characterization of transient receptor potential ion channels in the primary murine megakaryocyte. J Physiol 576:151-162. PMID: 16857711
31. Hassock SR, Zhu MX, Trost C, Flockerzi V, Authi KS (2002) Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-independent calcium entry channel. Blood 100:2801-2811. PMID: 12351388
32. Paez Espinosa EV, Murad JP, Ting HJ, Khasawneh FT (2012) Mouse transient receptor potential channel 6: role in hemostasis andthrombogenesis. Biochem Biophys Res Commun 417:853-856. doi: 10. 1016/j.bbrc.2011.12.058 PMID: 22206677
33. Karim ZA, Zhang J, Banerjee M, Chicka MC, Al Hawas R, Hamilton TR, etal. (2013) IkappaB kinase phosphorylation of SNAP-23 controls platelet secretion. Blood 121:4567-4574. doi: 10.1182/blood-2012-11-470468 PMID: 23613522
34. Lin OA, Karim ZA, Vemana HP, Espinosa EV, Khasawneh FT (2014) The antidepressant 5-HT2A receptor antagonists pizotifen and cyproheptadine inhibit serotonin-enhanced platelet function. PLoS One 9: e87026. doi: 10.1371/journal.pone.0087026 PMID: 24466319
35. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+indicators with greatly improved fluorescence properties. The Journal of biological chemistry 260:3440-3450. PMID: 3838314
36. Osdoit S, Rosa JP (2001) Fibrin clot retraction by human platelets correlates with alpha (IIb) beta (3) integrin-dependent protein tyrosine dephosphorylation. The Journal of biological chemistry 276:6703-6710. PMID: 11084040
37. Murad JP, Espinosa EV, Ting HJ, Khasawneh FT (2012) The C-terminal segment of the second extracellular loop of the thromboxane A2 receptor plays an important role in platelet aggregation. Biochemical pharmacology 83:88-96. doi: 10.1016/j.bcp. 2011.10.002 PMID: 22008592
38. Kattelman EJ, Venton DL, Le Breton GC (1986) Characterization of U46619 binding in unactivated, intact human platelets and determination of binding site affinities of fourTXA2/PGH2 receptor antagonists (13-APA, BM 13.177, ONO 3708 and SQ29, 548). Thrombosis research 41:471-481. PMID: 3008368
39. Murad JP, Espinosa EV, Ting HJ, McClure D, Khasawneh FT (2012) A novel antibody targeting the ligand binding domain of the thromboxane A (2) receptor exhibits antithrombotic properties in vivo. Biochem Biophys Res Commun 421:456-461. doi: 10.1016/j.bbrc.2012.04.011 PMID: 22503974
40. Du X, Ginsberg MH (1997) Integrin alpha IIb beta3 and platelet function. Thrombosis and haemostasis 78:96-100. PMID: 9198135
41. Shattil SJ, Brass LF (1987) Induction of the fibrinogen receptor on human platelets by intracellular mediators. The Journal of biological chemistry 262:992-1000. PMID: 3100533
42. Roedding AS, Li PP, Warsh JJ (2006) Characterization of the transient receptor potential channels mediating lysophosphatidic acid-stimulated calcium mobilization in B lymphoblasts. Life Sci 80:89-97. PMID: 16979191
43. Huang JS, Dong L, Kozasa T, Le Breton GC (2007) Signaling through G (alpha) 13 switch region I is essential for protease-activated receptor 1-mediated human platelet shape change, aggregation, and secretion. The Journal of biological chemistry 282:10210-10222. PMID: 17298951
44. Dorsam RT, Kim S, Jin J, Kunapuli SP (2002) Coordinated signaling through both G12/13 and G (i) pathways is sufficient to activate GPIIb/IIIa in human platelets. The Journal of biological chemistry 277:47588-47595. PMID: 12297512
45. Dorsam RT, Kunapuli SP (2004) Central role of the P2Y12 receptor in platelet activation. The Journal of clinical investigation 113:340-345. PMID: 14755328
46. Murugappa S, Kunapuli SP (2006) The role of ADP receptors in platelet function. Frontiers in bioscience: a journal and virtual library 11:1977-1986. PMID: 16368572
47. Krizaj D (2005) Compartmentalization of calcium entry pathways in mouse rods. Eur J Neurosci 22:3292-3296. PMID: 16367794
48. Parekh AB, Putney JW Jr. (2005) Store-operated calcium channels. Physiol Rev 85:757-810. PMID: 15788710
49. Bhattacharya B, Roberts RE (2003) Enhancement of alpha2-adrenoceptor-mediated vasoconstriction by the thromboxane-mimetic U46619 in the porcine isolated ear artery: role of the ERK-MAP kinase signal transduction cascade. British journal of pharmacology 139:156-162. PMID: 12746234
50. Huang Z, Liu P, Zhu L, Li N, Hu H (2014) P2X1-initiated p38 signalling enhances thromboxane A2-induced platelet secretion and aggregation. Thrombosis and haemostasis 112:142-150. doi: 10.1160/TH13-09-0726 PMID: 24633352
51. O'Brien KA, Stojanovic-Terpo A, Hay N, Du X (2011) An important role for Akt3 in platelet activation and thrombosis. Blood 118:4215-4223. doi: 10.1182/blood-2010-12-323204 PMID: 21821713
52. Ramanathan G, Gupta S, Thielmann I, Pleines I, Varga-Szabo D, May F, etal. (2012) Defective diacylglycerol-induced Ca2+ entry but normal agonist-induced activation responses in TRPC6-deficient mouse platelets. JThromb Haemost 10:419-429. doi: 10.1111/j.1538-7836.2011.04596.x PMID: 22176814
53. Almirza WH, Peters PH, van Zoelen EJ, Theuvenet AP (2012) Role of Trpc channels, Stim1 and Orai1 in PGF (2alpha)-induced calcium signaling in NRKfibroblasts. Cell Calcium 51:12-21. doi: 10.1016/j. ceca.2011.10.001 PMID: 22050845