The Actin Regulator Coronin-1A Modulates Platelet Shape Change and Consolidates Arterial Thrombosis

Abstract

Coronin-1A (Coro1A) belongs to a family of highly conserved actin-binding proteins that regulate cytoskeletal re-arrangement. In mammalians, Coro1A expression is most abundant in the haematopoietic lineage, where it regulates various cellular processes. The role of Coro1A in platelets has been previously unknown. Here, we identified Coro1A in human and mouse platelets. Genetic absence of Coro1A in mouse platelets inhibited agonist-induced actin polymerization and altered cofilin phosphoregulation, leading to a reduction in spreading and low-dose collagen induced aggregation. Furthermore, Coro1A-deficient mice displayed a defect in ferric chloride-induced arterial thrombosis with prolonged thrombus formation and reduced thrombus size. Immunofluorescence analysis revealed a less compact thrombus structure with reduced density of platelets and fibrinogen. In summary, Coro1A has a role in platelet biology with impact on spreading, aggregation and thrombosis.

Keywords

coronin-1A - coro1A - platelets - thrombosis - actin

• References

• 1 Jackson SP. Arterial thrombosis--insidious, unpredictable and deadly. Nat Med 2011; 17 (11) 1423-1436
• 2 Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013; 13 (01) 34-45
• 3 Stocker TJ, Ishikawa-Ankerhold H, Massberg S, Schulz C. Small but mighty: Platelets as central effectors of host defense. Thromb Haemost 2017; 117 (04) 651-661
• 4 Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2341-2349
• 5 Bearer EL, Prakash JM, Li Z. Actin dynamics in platelets. Int Rev Cytol 2002; 217: 137-182
• 6 Gandhi M, Goode BL. Coronin: the double-edged sword of actin dynamics. Subcell Biochem 2008; 48: 72-87
• 7 de Hostos EL, Bradtke B, Lottspeich F, Guggenheim R, Gerisch G. Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein beta subunits. EMBO J 1991; 10 (13) 4097-4104
• 8 de Hostos EL, Rehfuess C, Bradtke B. , et al. Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J Cell Biol 1993; 120 (01) 163-173
• 9 Liu SL, Needham KM, May JR, Nolen BJ. Mechanism of a concentration-dependent switch between activation and inhibition of Arp2/3 complex by coronin. J Biol Chem 2011; 286 (19) 17039-17046
• 10 Humphries CL, Balcer HI, D'Agostino JL. , et al. Direct regulation of Arp2/3 complex activity and function by the actin binding protein coronin. J Cell Biol 2002; 159 (06) 993-1004
• 11 Mikati MA, Breitsprecher D, Jansen S, Reisler E, Goode BL. Coronin enhances actin filament severing by recruiting cofilin to filament sides and altering F-actin conformation. J Mol Biol 2015; 427 (19) 3137-3147
• 12 Galkin VE, Orlova A, Brieher W, Kueh HY, Mitchison TJ, Egelman EH. Coronin-1A stabilizes F-actin by bridging adjacent actin protomers and stapling opposite strands of the actin filament. J Mol Biol 2008; 376 (03) 607-613
• 13 Chan KT, Creed SJ, Bear JE. Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Trends Cell Biol 2011; 21 (08) 481-488
• 14 Pick R, Begandt D, Stocker TJ. , et al. Coronin 1A, a novel player in integrin biology, controls neutrophil trafficking in innate immunity. Blood 2017; 130 (07) 847-858
• 15 Jayachandran R, Sundaramurthy V, Combaluzier B. , et al. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell 2007; 130 (01) 37-50
• 16 Yan M, Di Ciano-Oliveira C, Grinstein S, Trimble WS. Coronin function is required for chemotaxis and phagocytosis in human neutrophils. J Immunol 2007; 178 (09) 5769-5778
• 17 Moriceau S, Kantari C, Mocek J. , et al. Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: potential implication in neutrophils from cystic fibrosis patients. J Immunol 2009; 182 (11) 7254-7263
• 18 Thon JN, Montalvo A, Patel-Hett S. , et al. Cytoskeletal mechanics of proplatelet maturation and platelet release. J Cell Biol 2010; 191 (04) 861-874
• 19 Hla T, Galvani S, Rafii S, Nachman R. S1P and the birth of platelets. J Exp Med 2012; 209 (12) 2137-2140
• 20 Pircher J, Czermak T, Ehrlich A. , et al. Cathelicidins prime platelets to mediate arterial thrombosis and tissue inflammation. Nat Commun 2018; 9 (01) 1523
• 21 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
• 22 Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 2004; 304 (5671): 743-746
• 23 Falet H, Chang G, Brohard-Bohn B, Rendu F, Hartwig JH. Integrin alpha(IIb)beta3 signals lead cofilin to accelerate platelet actin dynamics. Am J Physiol Cell Physiol 2005; 289 (04) C819-C825
• 24 Bamburg JR, Bernstein BW. Roles of ADF/cofilin in actin polymerization and beyond. F1000 Biol Rep 2010; 2: 62
• 25 Novotny J, Chandraratne S, Weinberger T. , et al. Histological comparison of arterial thrombi in mice and men and the influence of Cl-amidine on thrombus formation. PLoS One 2018; 13 (01) e0190728
• 26 Fox JE. The platelet cytoskeleton. Thromb Haemost 1993; 70 (06) 884-893
• 27 Föger N, Jenckel A, Orinska Z, Lee KH, Chan AC, Bulfone-Paus S. Differential regulation of mast cell degranulation versus cytokine secretion by the actin regulatory proteins Coronin1a and Coronin1b. J Exp Med 2011; 208 (09) 1777-1787
• 28 Combaluzier B, Pieters J. Chemotaxis and phagocytosis in neutrophils is independent of coronin 1. J Immunol 2009; 182 (05) 2745-2752
• 29 Ge S, White JG, Haynes CL. Cytoskeletal F-actin, not the circumferential coil of microtubules, regulates platelet dense-body granule secretion. Platelets 2012; 23 (04) 259-263
• 30 Koseoglu S, Peters CG, Fitch-Tewfik JL. , et al. VAMP-7 links granule exocytosis to actin reorganization during platelet activation. Blood 2015; 126 (05) 651-660
• 31 Ojeda V, Castro-Castro A, Bustelo XR. Coronin1 proteins dictate rac1 intracellular dynamics and cytoskeletal output. Mol Cell Biol 2014; 34 (18) 3388-3406
• 32 Castro-Castro A, Ojeda V, Barreira M. , et al. Coronin 1A promotes a cytoskeletal-based feedback loop that facilitates Rac1 translocation and activation. EMBO J 2011; 30 (19) 3913-3927
• 33 Carlier MF, Ressad F, Pantaloni D. Control of actin dynamics in cell motility. Role of ADF/cofilin. J Biol Chem 1999; 274 (48) 33827-33830
• 34 Davidson MM, Haslam RJ. Dephosphorylation of cofilin in stimulated platelets: roles for a GTP-binding protein and Ca2+. Biochem J 1994; 301 (Pt 1): 41-47
• 35 Bender M, Eckly A, Hartwig JH. , et al. ADF/n-cofilin-dependent actin turnover determines platelet formation and sizing. Blood 2010; 116 (10) 1767-1775
• 36 Kile BT, Panopoulos AD, Stirzaker RA. , et al. Mutations in the cofilin partner Aip1/Wdr1 cause autoinflammatory disease and macrothrombocytopenia. Blood 2007; 110 (07) 2371-2380
• 37 Italiano Jr JE, Lecine P, Shivdasani RA, Hartwig JH. Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J Cell Biol 1999; 147 (06) 1299-1312
• 38 Föger N, Rangell L, Danilenko DM, Chan AC. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 2006; 313 (5788): 839-842
• 39 Thon JN, Italiano Jr JE. Does size matter in platelet production?. Blood 2012; 120 (08) 1552-1561
• 40 Paul DS, Casari C, Wu C. , et al. Deletion of the Arp2/3 complex in megakaryocytes leads to microthrombocytopenia in mice. Blood Adv 2017; 1 (18) 1398-1408