FlnA binding to PACSIN2 F-BAR domain regulates membrane tubulation in megakaryocytes and platelets

Blood

Volumn 126, Issue 1, 2015, Pages 80-88

  Begonja, Antonija Jurak ^a,b   Pluthero, Fred G ^c   Suphamungmee, Worawit ^d   Giannini, Silvia ^a,b   Christensen, Hilary ^c   Leung, Richard ^c   Lo, Richard W ^c,e   Nakamura, Fumihiko ^a,b   Lehman, William ^d   Plomann, Markus ^f   Hoffmeister, Karin M ^a,b   Kahr, Walter H A ^c,e   Hartwig, John H ^a,b   Falet, Hervé ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA1 INTEGRIN; F ACTIN; FILAMIN A; GLYCOPROTEIN IB ALPHA; PACSIN2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; FILAMIN; FLNA PROTEIN, HUMAN; PACSIN2 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL ACTIVATION; CELL MEMBRANE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENZYME REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MEGAKARYOCYTE MEMBRANE; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; THROMBOCYTE FUNCTION; THROMBOCYTE MEMBRANE; THROMBOCYTOPOIESIS; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; HEK293 CELL LINE; MEGAKARYOCYTE; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN; PSEUDOPODIUM; THROMBOCYTE; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOOD PLATELETS; CELL MEMBRANE; CELLS, CULTURED; FILAMINS; HEK293 CELLS; HUMANS; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PSEUDOPODIA;

EID: 84937810454     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-07-587600     Document Type: Article

References (60)

1. Mahaut-Smith MP, Thomas D, Higham AB, et al. Properties of the demarcation membrane system in living rat megakaryocytes. Biophys J. 2003; 84(4):2646-2654.
2. Schulze H, Korpal M, Hurov J, et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood. 2006;107(10):3868-3875.
3. Eckly A, Heijnen H, Pertuy F, et al. Biogenesis of the demarcation membrane system (DMS) in megakaryocytes. Blood. 2014;123(6):921-930.
4. van Nispen tot Pannerden H, de Haas F, Geerts W, Posthuma G, van Dijk S, Heijnen HF. The platelet interior revisited: electron tomography reveals tubular alpha-granule subtypes. Blood. 2010;116(7):1147-1156.
5. Peter BJ, Kent HM, Mills IG, et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 2004; 303(5657):495-499.
6. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell. 2005;9(6):791-804.
7. Itoh T, De Camilli P. BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim Biophys Acta. 2006;1761(8): 897-912.
8. Shimada A, Niwa H, Tsujita K, et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell. 2007;129(4):761-772.
9. Henne WM, Kent HM, Ford MG, et al. Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure. 2007; 15(7):839-852.
10. Frost A, Perera R, Roux A, et al. Structural basis of membrane invagination by F-BAR domains. Cell. 2008;132(5):807-817.
11. Qualmann B, Koch D, Kessels MM. Let's go bananas: revisiting the endocytic BAR code. EMBO J. 2011;30(17):3501-3515.
12. Rowley JW, Oler AJ, Tolley ND, et al. Genomewide RNA-seq analysis of human and mouse platelet transcriptomes. Blood. 2011;118(14): e101-e111.
13. Burkhart JM, Vaudel M, Gambaryan S, et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood. 2012;120(15): e73-e82.
14. Nikki M, Meriläinen J, Lehto VP. FAP52 regulates actin organization via binding to filamin. J Biol Chem. 2002;277(13):11432-11440.
15. Cousin H, Desimone DW, Alfandari D. PACSIN2 regulates cell adhesion during gastrulation in Xenopus laevis. Dev Biol. 2008;319(1):86-99.
16. Takkunen M, Hukkanen M, Liljeström M, Grenman R, Virtanen I. Podosome-like structures of non-invasive carcinoma cells are replaced in epithelial-mesenchymal transition by actin cometembedded invadopodia. J Cell Mol Med. 2010; 14(6B):1569-1593.
17. de Kreuk BJ, Nethe M, Fernandez-Borja M, et al. The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J Cell Sci. 2011;124(Pt 14):2375-2388.
18. Qualmann B, Kelly RB. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J Cell Biol. 2000;148(5): 1047-1062.
19. de Kreuk BJ, Anthony EC, Geerts D, Hordijk PL. The F-BAR protein PACSIN2 regulates epidermal growth factor receptor internalization. J Biol Chem. 2012;287(52):43438-43453.
20. Senju Y, Itoh Y, Takano K, Hamada S, Suetsugu S. Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. JCellSci.2011; 124(Pt 12):2032-2040.
21. Hansen CG, Howard G, Nichols BJ. Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci. 2011;124(Pt 16): 2777-2785.
22. Koch D, Westermann M, Kessels MM, Qualmann B. Ultrastructural freeze-fracture immunolabeling identifies plasma membrane-localized syndapin II as a crucial factor in shaping caveolae. Histochem Cell Biol. 2012;138(2):215-230.
23. Braun A, Pinyol R, Dahlhaus R, et al. EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell. 2005;16(8):3642-3658.
24. Kessels MM, Qualmann B. Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 2002;21(22):6083-6094.
25. Kessels MM, Dong J, Leibig W, Westermann P, Qualmann B. Complexes of syndapin II with dynamin II promote vesicle formation at the trans-Golgi network. J Cell Sci. 2006;119(Pt 8): 1504-1516.
26. Bender M, Giannini S, Grozovsky R, et al. Dynamin 2-dependent endocytosis is required for normal megakaryocyte development in mice. Blood. 2015;125(6):1014-1024.
27. Falet H. New insights into the versatile roles of platelet FlnA. Platelets. 2013;24(1):1-5.
28. Nurden P, Debili N, Coupry I, et al. Thrombocytopenia resulting from mutations in filamin A can be expressed as an isolated syndrome. Blood. 2011;118(22):5928-5937.
29. Berrou E, Adam F, Lebret M, et al. Heterogeneity of platelet functional alterations in patients with filamin A mutations. Arterioscler Thromb Vasc Biol. 2013;33(1):e11-e18.
30. Manchev VT, Hilpert M, Berrou E, et al. A new form of macrothrombocytopenia induced by a germ-line mutation in the PRKACG gene. Blood. 2014;124(16):2554-2563.
31. Falet H, Pollitt AY, Begonja AJ, et al. A novel interaction between FlnA and Syk regulates platelet ITAM-mediated receptor signaling and function. J Exp Med. 2010;207(9):1967-1979.
32. Jurak Begonja A, Hoffmeister KM, Hartwig JH, Falet H. FlnA-null megakaryocytes prematurely release large and fragile platelets that circulate poorly. Blood. 2011;118(8):2285-2295.
33. Falet H, Hoffmeister KM, Neujahr R, Hartwig JH. Normal Arp2/3 complex activation in platelets lacking WASp. Blood. 2002;100(6):2113-2122.
34. Falet H, Hoffmeister KM, Neujahr R, et al. Importance of free actin filament barbed ends for Arp2/3 complex function in platelets and fibroblasts. Proc Natl Acad Sci USA. 2002;99(26): 16782-16787.
35. Modregger J, Ritter B, Witter B, Paulsson M, Plomann M. All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci. 2000;113(Pt 24):4511-4521.
36. Nakamura F, Osborn TM, Hartemink CA, Hartwig JH, Stossel TP. Structural basis of filamin A functions. J Cell Biol. 2007;179(5):1011-1025.
37. Naviaux RK, Costanzi E, Haas M, Verma IM. The pCL vector system: rapid production of helperfree, high-titer, recombinant retroviruses. J Virol. 1996;70(8):5701-5705.
38. Kahr WH, Lo RW, Li L, et al. Abnormal megakaryocyte development and platelet function in Nbeal2(-/-) mice. Blood. 2013;122(19): 3349-3358.
39. Mazharian A, Thomas SG, Dhanjal TS, Buckley CD, Watson SP. Critical role of Src-Syk-PLCgamma2 signaling in megakaryocyte migration and thrombopoiesis. Blood. 2010; 116(5):793-800.
40. Ritter B, Modregger J, Paulsson M, Plomann M. PACSIN 2, a novel member of the PACSIN family of cytoplasmic adapter proteins. FEBS Lett. 1999; 454(3):356-362.
41. Nakamura F, Pudas R, Heikkinen O, et al. The structure of the GPIb-filamin A complex. Blood. 2006;107(5):1925-1932.
42. Kiema T, Lad Y, Jiang P, et al. The molecular basis of filamin binding to integrins and competition with talin. Mol Cell. 2006;21(3): 337-347.
43. Wang Q, Navarro MV, Peng G, et al. Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/ Syndapin. Proc Natl Acad Sci USA. 2009;106(31): 12700-12705.
44. Shimada A, Takano K, Shirouzu M, et al. Mapping of the basic amino-acid residues responsible for tubulation and cellular protrusion by the EFC/F-BAR domain of pacsin2/Syndapin II. FEBS Lett. 2010;584(6):1111-1118.
45. Plomann M, Wittmann JG, Rudolph MG. A hinge in the distal end of the PACSIN 2 F-BAR domain may contribute to membrane-curvature sensing. J Mol Biol. 2010;400(2):129-136.
46. Bai X, Meng G, Luo M, Zheng X. Rigidity of wedge loop in PACSIN 3 protein is a key factor in dictating diameters of tubules. J Biol Chem. 2012; 287(26):22387-22396.
47. Bai X, Zheng X. Tip-to-tip interaction in the crystal packing of PACSIN 2 is important in regulating tubulation activity. Protein Cell. 2013;4(9): 695-701.
48. Razinia Z, Mäkelä T,Ylänne J, Calderwood DA. Filamins in mechanosensing and signaling. Annu Rev Biophys. 2012;41:227-246.
49. Lad Y, Kiema T, Jiang P, et al. Structure of three tandem filamin domains reveals auto-inhibition of ligand binding. EMBO J. 2007;26(17):3993-4004.
50. Heikkinen OK, Ruskamo S, Konarev PV, et al. Atomic structures of two novel immunoglobulinlike domain pairs in the actin cross-linking protein filamin. J Biol Chem. 2009;284(37):25450-25458.
51. Senis YA, Sangrar W, Zirngibl RA, Craig AW, Lee DH, Greer PA. Fps/Fes and Fer non-receptor protein-tyrosine kinases regulate collagen- and ADP-induced platelet aggregation. J Thromb Haemost. 2003;1(5):1062-1070.
52. Elvers M, Beck S, Fotinos A, Ziegler M, Gawaz M. The GRAF family member oligophrenin1 is a RhoGAP with BAR domain and regulates Rho GTPases in platelets. Cardiovasc Res. 2012; 94(3):526-536.
53. Bleijerveld OB, van Holten TC, Preisinger C, et al. Targeted phosphotyrosine profiling of glycoprotein VI signaling implicates oligophrenin-1 in platelet filopodia formation. Arterioscler Thromb Vasc Biol. 2013;33(7):1538-1543.
54. Beck S, Fotinos A, Lang F, Gawaz M, Elvers M. Isoform-specific roles of the GTPase activating protein Nadrin in cytoskeletal reorganization of platelets. Cell Signal. 2013;25(1):236-246.
55. Beck S, Fotinos A, Gawaz M, Elvers M. Nadrin GAP activity is isoform- and target-specific regulated by tyrosine phosphorylation. Cell Signal. 2014;26(9):1975-1984.
56. Chen Y, Aardema J, Kale S, et al. Loss of the F-BAR protein CIP4 reduces platelet production by impairing membrane-cytoskeleton remodeling. Blood. 2013;122(10):1695-1706.
57. Sabri S, Foudi A, Boukour S, et al. Deficiency in the Wiskott-Aldrich protein induces premature proplatelet formation and platelet production in the bone marrow compartment. Blood. 2006;108(1): 134-140.
58. Falet H, Marchetti MP, Hoffmeister KM, Massaad MJ, Geha RS, Hartwig JH. Platelet-associated IgAs and impaired GPVI responses in platelets lacking WIP. Blood. 2009;114(21):4729-4737.
59. Quan A, Xue J, Wielens J, et al. Phosphorylation of syndapin I F-BAR domain at two helix-capping motifs regulates membrane tubulation. Proc Natl Acad Sci USA. 2012;109(10):3760-3765.
60. Rao Y, Ma Q, Vahedi-Faridi A, et al. Molecular basis for SH3 domain regulation of F-BARmediated membrane deformation. Proc Natl Acad Sci USA. 2010;107(18):8213-8218.