Impact of the serum- and glucocorticoid-inducible kinase 1 on platelet dense granule biogenesis and secretion

Journal of Thrombosis and Haemostasis

Volumn 13, Issue 7, 2015, Pages 1325-1334

  Walker, B ^a   Schmid, E ^b   Russo, A ^a   Schmidt, E M ^a   Burk, O ^c   Munzer P ^a   Velic, A ^a   Macek, B ^a   Schaller, M ^b   Schwab, M ^b,c   Seabra, M C ^d   Gawaz, M ^a   Lang, F ^a   Borst, O ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c DR MARGARETE FISCHER BOSCH INSTITUTE OF CLINICAL PHARMACOLOGY   (Germany)

^d NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Biogenesis; Blood platelets; Rab27b protein, mouse; Secretory granules; Sgk1 protein, mouse

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD63 ANTIGEN; FERROUS CHLORIDE; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; PROTEIN RAB27B; PROTEOME; SEROTONIN; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG; VESICULAR TRANSPORT PROTEIN; CD63 PROTEIN, MOUSE; IMMEDIATE EARLY PROTEIN; PROTEIN SERINE THREONINE KINASE; RAB PROTEIN; RAB27B PROTEIN, MOUSE; SERUM-GLUCOCORTICOID REGULATED KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY INJURY; ARTICLE; BIOGENESIS; BLOOD CLOTTING; BLOOD VESSEL INJURY; CAROTID ARTERY LIGATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENETIC TRANSFECTION; IN VIVO STUDY; MALE; MEGAKARYOCYTE; MOUSE; NONHUMAN; PLATELET GRANULE BIOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; RAB27B GENE; RNA STABILITY; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE RELEASE REACTION; THROMBOCYTE STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; BLOOD; CAROTID ARTERY INJURY; CELL CULTURE; CELL GRANULE; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; GENETICS; GENOTYPE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; SECRETION (PROCESS); SECRETORY VESICLE; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOSIS; TIME FACTOR; ULTRASTRUCTURE; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIGENS, CD63; BLOOD PLATELETS; CAROTID ARTERY INJURIES; CELLS, CULTURED; CYTOPLASMIC GRANULES; DISEASE MODELS, ANIMAL; FEMALE; GENOTYPE; IMMEDIATE-EARLY PROTEINS; MALE; MEGAKARYOCYTES; MICE, KNOCKOUT; PHENOTYPE; PLATELET ACTIVATION; PLATELET AGGREGATION; PROTEIN-SERINE-THREONINE KINASES; RAB GTP-BINDING PROTEINS; RNA, MESSENGER; SECRETORY VESICLES; SEROTONIN; SIGNAL TRANSDUCTION; THROMBOSIS; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84935433391     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12998     Document Type: Article

References (39)

1. Borst O, Schmidt EM, Munzer P, Schonberger T, Towhid ST, Elvers M, Leibrock C, Schmid E, Eylenstein A, Kuhl D, May AE, Gawaz M, Lang F. The serum- and glucocorticoid-inducible kinase 1 (SGK1) influences platelet calcium signaling and function by regulation of Orai1 expression in megakaryocytes. Blood 2012; 119: 251-61.
2. Reed GL. Platelet secretory mechanisms. Semin Thromb Hemost 2004; 30: 441-50.
3. Borst O, Munzer P, Gatidis S, Schmidt EM, Schonberger T, Schmid E, Towhid ST, Stellos K, Seizer P, May AE, Lang F, Gawaz M. The inflammatory chemokine CXC motif ligand 16 triggers platelet activation and adhesion via CXC motif receptor 6-dependent phosphatidylinositide 3-kinase/Akt signaling. Circ Res 2012; 111: 1297-307.
4. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115: 3378-84.
5. Ren Q, Wimmer C, Chicka MC, Ye S, Ren Y, Hughson FM, Whiteheart SW. Munc13-4 is a limiting factor in the pathway required for platelet granule release and hemostasis. Blood 2010; 116: 869-77.
6. Gillitzer A, Peluso M, Bultmann A, Munch G, Gawaz M, Ungerer M. Effect of dominant negative SNAP-23 expression on platelet function. J Thromb Haemost 2008; 6: 1757-63.
7. King SM, McNamee RA, Houng AK, Patel R, Brands M, Reed GL. Platelet dense-granule secretion plays a critical role in thrombosis and subsequent vascular remodeling in atherosclerotic mice. Circulation 2009; 120: 785-91.
8. Lindemann S, Kramer B, Seizer P, Gawaz M. Platelets, inflammation and atherosclerosis. J Thromb Haemost 2007; 5(Suppl. 1): 203-11.
9. Lang PA, Contaldo C, Georgiev P, El-Badry AM, Recher M, Kurrer M, Cervantes-Barragan L, Ludewig B, Calzascia T, Bolinger B, Merkler D, Odermatt B, Bader M, Graf R, Clavien PA, Hegazy AN, Lohning M, Harris NL, Ohashi PS, Hengartner H, et al. Aggravation of viral hepatitis by platelet-derived serotonin. Nat Med 2008; 14: 756-61.
10. Flaumenhaft R. Molecular basis of platelet granule secretion. Arterioscler Thromb Vasc Biol 2003; 23: 1152-60.
11. Tolmachova T, Abrink M, Futter CE, Authi KS, Seabra MC. Rab27b regulates number and secretion of platelet dense granules. Proc Natl Acad Sci U S A 2007; 104: 5872-7.
12. Tiwari S, Italiano JE Jr, Barral DC, Mules EH, Novak EK, Swank RT, Seabra MC, Shivdasani RA. A role for Rab27b in NF-E2-dependent pathways of platelet formation. Blood 2003; 102: 3970-9.
13. Dahlberg J, Smith G, Norrving B, Nilsson P, Hedblad B, Engstrom G, Lovkvist H, Carlson J, Lindgren A, Melander O. Genetic variants in serum and glucocortocoid regulated kinase 1, a regulator of the epithelial sodium channel, are associated with ischaemic stroke. J Hypertens 2011; 29: 884-9.
14. Munzer P, Borst O, Walker B, Schmid E, Feijge MA, Cosemans JM, Chatterjee M, Schmidt EM, Schmidt S, Towhid ST, Leibrock C, Elvers M, Schaller M, Seizer P, Ferlinz K, May AE, Gulbins E, Heemskerk JW, Gawaz M, Lang F. Acid sphingomyelinase regulates platelet cell membrane scrambling, secretion, and thrombus formation. Arterioscler Thromb Vasc Biol 2014; 34: 61-71.
15. Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, Jackson CW, Hunt P, Saris CJ, Orkin SH. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell 1995; 81: 695-704.
16. Borst O, Munzer P, Schmid E, Schmidt EM, Russo A, Walker B, Yang W, Leibrock C, Szteyn K, Schmidt S, Elvers M, Faggio C, Shumilina E, Kuro-o M, Gawaz M, Lang F. 1, 25(OH)2 vitamin D3-dependent inhibition of platelet Ca2 + signaling and thrombus formation in klotho-deficient mice. FASEB J 2014; 28: 2108-19.
17. Eylenstein A, Gehring EM, Heise N, Shumilina E, Schmidt S, Szteyn K, Munzer P, Nurbaeva MK, Eichenmuller M, Tyan L, Regel I, Foller M, Kuhl D, Soboloff J, Penner R, Lang F. Stimulation of Ca2 + -channel Orai1/STIM1 by serum- and glucocorticoid-inducible kinase 1 (SGK1). FASEB J 2011; 25: 2012-21.
18. Ambrosio AL, Boyle JA, Di Pietro SM. Mechanism of platelet dense granule biogenesis: study of cargo transport and function of Rab32 and Rab38 in a model system. Blood 2012; 120: 4072-81.
19. Graham GJ, Ren Q, Dilks JR, Blair P, Whiteheart SW, Flaumenhaft R. Endobrevin/VAMP-8-dependent dense granule release mediates thrombus formation in vivo. Blood 2009; 114: 1083-90.
20. Lang F, Bohmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol Rev 2006; 86: 1151-78.
21. Ferreira IA, Mocking AI, Feijge MA, Gorter G, van Haeften TW, Heemskerk JW, Akkerman JW. Platelet inhibition by insulin is absent in type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol 2006; 26: 417-22.
22. Konopatskaya O, Gilio K, Harper MT, Zhao Y, Cosemans JM, Karim ZA, Whiteheart SW, Molkentin JD, Verkade P, Watson SP, Heemskerk JW, Poole AW. PKCalpha regulates platelet granule secretion and thrombus formation in mice. J Clin Invest 2009; 119: 399-407.
23. Harper MT, Poole AW. Diverse functions of protein kinase C isoforms in platelet activation and thrombus formation. J Thromb Haemost 2010; 8: 454-62.
24. Hampson A, O'Connor A, Smolenski A. Synaptotagmin-like protein 4 and Rab8 interact and increase dense granule release in platelets. J Thromb Haemost 2013; 11: 161-8.
25. Ninkovic I, White JG, Rangel-Filho A, Datta YH. The role of Rab38 in platelet dense granule defects. J Thromb Haemost 2008; 6: 2143-51.
26. Peters CG, Michelson AD, Flaumenhaft R. Granule exocytosis is required for platelet spreading: differential sorting of alpha-granules expressing VAMP-7. Blood 2012; 120: 199-206.
27. Chen D, Bernstein AM, Lemons PP, Whiteheart SW. Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 in dense core granule release. Blood 2000; 95: 921-9.
28. Golebiewska EM, Harper MT, Williams CM, Savage JS, Goggs R, Fischer von Mollard G, Poole AW. Syntaxin 8 Regulates Platelet Dense Granule Secretion, Aggregation and Thrombus Stability. J Biol Chem 2015; 290: 1536-45.
29. Ye S, Huang Y, Joshi S, Zhang J, Yang F, Zhang G, Smyth SS, Li Z, Takai Y, Whiteheart SW. Platelet secretion and hemostasis require syntaxin-binding protein STXBP5. J Clin Invest 2014; 124: 4517-28.
30. Meng R, Wu J, Harper DC, Wang Y, Kowalska MA, Abrams CS, Brass LF, Poncz M, Stalker TJ, Marks MS. Defective release of alpha-granule and lysosome contents from platelets in mouse Hermansky-Pudlak syndrome models. Blood 2015; 125: 1623-32.
31. Plutner H, Cox AD, Pind S, Khosravi-Far R, Bourne JR, Schwaninger R, Der CJ, Balch WE. Rab1b regulates vesicular transport between the endoplasmatic reticulum and successive Golgi compartments. J Cell Biol 1991; 115: 31-43.
32. Gerondopoulos A, Bastos RN, Yoshimura S, Anderson R, Carpanini S, Aligianis I, Handley MT, Barr FA. Rab18 and a Rab18 GEF complex are required for normal ERstructure. J Cell Biol 2014; 205: 707-20.
33. Polgár J, Reed GL. A critical role for N-ethylmaleimide-sensitive fusion protein (NSF) in platelet granule secretion. Blood 1999; 94: 1313-8.
34. Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 2012; 151: 1256-69.
35. Hay JC, Chao DS, Kuo CS, Scheller RH. Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell 1997; 89: 149-58.
36. Mota LJ, Ramsden AE, Liu M, Castle JD, Holden DW. SCAMP3 is a component of the Salmonella-induced tubular network and reveals an interaction between bacterial effectors and post-Golgi trafficking. Cell Microbiol 2009; 11: 1236-53.
37. Falguières T, Castle D, Gruenberg J. Regulation of the MVB pathway by SCAMP3. Traffic 2012; 13: 131-42.
38. Kuge O, Hara-Kuge S, Orci L, Ravazzola M, Amherdt M, Tanigawa G, Wieland FT, Rothman JE. zeta-COP, a subunit of coatomer, is required for COP-coated vesicle assembly. J Cell Biol 1993; 123: 1727-34.
39. Neubrand VE, Will RD, Möbius W, Poustka A, Wiemann S, Schu P, Dotti CG, Pepperkok R, Simpson JC. Gamma-BAR, a novel AP-1-interacting protein involved in post-Golgi trafficking. EMBO J 2005; 24: 1122-33.