Mutations in the cofilin partner Aip1/Wdr1 cause autoinflammatory disease and macrothrombocytopenia

Blood

Volumn 110, Issue 7, 2007, Pages 2371-2380

  Kile, Benjamin T ^a,b,c   Panopoulos, Athanasia D ^d,e   Stirzaker, Roslynn A ^b,c   Hacking, Douglas F ^b   Tahtamouni, Lubna H ^f   Willson, Tracy A ^b   Mielke, Lisa A ^b,c   Henley, Katya J ^b   Zhang, Jian Guo ^b   Wicks, Ian P ^b   Stevenson, William S ^b   Nurden, Paquita ^g   Watowich, Stephanie S ^d   Justice, Monica J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e UNIVERSITY OF TEXAS   (United States)

^f HASHEMITE UNIVERSITY   (Jordan)

^g Ctr Geriatrie Ctr Hosp Univ B   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN INTERACTING PROTEIN 1; COFILIN; PROTEIN; UNCLASSIFIED DRUG; WD40 REPEAT PROTEIN 1;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOINFLAMMATORY DISEASE; CELL MATURATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSKELETON; EMBRYOTOXICITY; GENE LOCUS; GENE MUTATION; MEGAKARYOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THROMBOCYTE FUNCTION; THROMBOCYTOPENIA;

ACTIN DEPOLYMERIZING FACTORS; ALLELES; AMINO ACID SEQUENCE; ANIMALS; BLOOD PLATELETS; CELL DIFFERENTIATION; CELL MOVEMENT; CONSERVED SEQUENCE; HUMANS; INFLAMMATION; MEGAKARYOCYTES; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTATION; NEUTROPHILS; SEQUENCE ALIGNMENT; THROMBOCYTOPENIA;

EID: 34948884078     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-10-055087     Document Type: Article

References (63)

1. Ono S, Baillie DL, Benian GM. UNC-60B, an ADF/cofilin family protein, is required for proper assembly of actin into myofibrils in Caenorhabditis elegans body wall muscle. J Cell Biol. 1999;145:491-502.
2. Dawe HR, Minamide LS, Bamburg JR, Cramer LP. ADF/cofilin controls cell polarity during fibroblast migration. Curr Biol. 2003;13:252-257.
3. Chen J, Godt D, Gunsalus K, Kiss I, Goldberg M, Laski FA. Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nat Cell Biol. 2001;3:204-209.
4. 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;304:743-746.
5. Lappalainen P, Drubin DG. Cofilin promotes rapid actin filament turnover in vivo. Nature. 1997;388:78-82.
6. Gurniak CB, Perlas E, Witke W. The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Dev Biol. 2005;278:231-241.
7. Gunsalus KC, Bonaccorsi S, Williams E, Verni F, Gatti M, Goldberg ML. Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J Cell Biol. 1995;131:1243-1259.
8. Abe H, Obinata T, Minamide LS, Bamburg JR. Xenopus laevis actin-depolymerizing factor/cofilin: a phosphorylation-regulated protein essential for development. J Cell Biol. 1996;132:871-885.
9. Yonezawa N, Nishida E, Iida K, Yahara I, Sakai H. Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with actin by phosphoinositides. J Biol Chem. 1990;265:8382-8386.
10. Yonezawa N, Nishida E, Sakai H. pH control of actin polymerization by cofilin. J Biol Chem. 1985;260:14410-14412.
11. Morgan TE, Lockerbie RO, Minamide LS, Browning MD, Bamburg JR. Isolation and characterization of a regulated form of actin depolymerizing factor. J Cell Biol. 1993;122:623-633.
12. Niwa R, Nagata-Ohashi K, Takeichi M, Mizuno K, Uemura T. Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell. 2002;108:233-246.
13. Gohla A, Birkenfeld J, Bokoch GM. Chronophin, a novel HAD-type serine protein phosphatase, regulates cofilin-dependent actin dynamics. Nat Cell Biol. 2005;7:21-29.
14. Agnew BJ, Minamide LS, Bamburg JR. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J Biol Chem. 1995;270:17582-17587.
15. Arber S, Barbayannis FA, Hanser H, et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 1998;393:805-809.
16. Maekawa M, Ishizaki T, Boku S, et al. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science. 1999;285:895-898.
17. Moriyama K, Iida K, Yahara I. Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells. 1996;1:73-86.
18. Sumi T, Matsumoto K, Takai Y, Nakamura T. Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42-activated LIM-kinase 2. J Cell Biol. 1999;147:1519-1532.
19. Toshima J, Toshima JY, Takeuchi K, Mori R, Mizuno K. Cofilin phosphorylation and actin reorganization activities of testicular protein kinase 2 and its predominant expression in testicular Sertoli cells. J Biol Chem. 2001;276:31449-31458.
20. Gohla A, Bokoch GM. 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr Biol. 2002;12:1704-1710.
21. Rodal AA, Tetreault JW, Lappalainen P, Drubin DG, Amberg DC. Aip1p interacts with cofilin to disassemble actin filaments. J Cell Biol. 1999;145:1251-1264.
22. Okada K, Obinata T, Abe H. XAIP1: a Xenopus homologue of yeast actin interacting protein 1 (AIP1), which induces disassembly of actin filaments cooperatively with ADF/cofilin family proteins. J Cell Sci. 1999;112(Pt 10):1553-1565.
23. Okada K, Blanchoin L, Abe H, Chen H, Pollard TD, Bamburg JR. Xenopus actin-interacting protein 1 (XAip1) enhances cofilin fragmentation of filaments by capping filament ends. J Biol Chem. 2002;277:43011-43016.
24. Ono S, Mohri K, Ono K. Microscopic evidence that actin-interacting protein 1 actively disassembles actin-depolymerizing factor/Cofilin-bound actin filaments. J Biol Chem. 2004;279:14207-14212.
25. Rogers SL, Wiedemann U, Stuurman N, Vale RD. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J Cell Biol. 2003;162:1079-1088.
26. Ono S. The caenorhabditis elegans unc-78 gene encodes a homologue of actin-interacting protein 1 required for organised assembly of muscle actin filaments. Journal of Cell Biology. 2001;153:889-889.
27. Konzok A, Weber I, Simmeth E, Hacker U, Maniak M, Muller-Taubenberger A. DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J Cell Biol. 1999;146:453-464.
28. Ketelaar T, Allwood EG, Anthony R, Voigt B, Menzel D, Hussey PJ. The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr Biol. 2004;14:145-149.
29. Agrawal PB, Greenleaf RS, Tomczak KK, et al. Nemaline Myopathy with Minicores Caused by Mutation of the CFL2 Gene Encoding the Skeletal Muscle Actin-Binding Protein, Cofilin-2. Am J Hum Genet. 2007;80:162-167.
30. 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.
31. 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:C819-C825.
32. Pandey D, Goyal P, Bamburg JR, Siess W. Regulation of LIM-kinase 1 and cofilin in thrombin-stimulated platelets. Blood. 2006;107:575-583.
33. Eibert SM, Lee KH, Pipkorn R, et al. Cofilin peptide homologs interfere with immunological synapse formation and T cell activation. Proc Natl Acad Sci USA. 2004;101:1957-1962.
34. Samstag Y, Eckerskorn C, Wesselborg S, Henning S, Wallich R, Meuer SC. Costimulatory signals for human T-cell activation induce nuclear translocation of pp19/cofilin. Proc Natl Acad Sci USA. 1994;91:4494-4498.
35. Suzuki K, Yamaguchi T, Tanaka T, et al. Activation induces dephosphorylation of cofilin and its translocation to plasma membranes in neutrophil-like differentiated HL-60 cells. J Biol Chem. 1995;270:19551-19556.
36. Okada K, Takano-Ohmuro H, Obinata T, Abe H. Dephosphorylation of cofilin in polymorphonuclear leukocytes derived from peripheral blood. Exp Cell Res. 1996;227:116-122.
37. Heyworth PG, Robinson JM, Ding J, Ellis BA, Badwey JA. Cofilin undergoes rapid dephosphorylation in stimulated neutrophils and translocates to ruffled membranes enriched in products of the NADPH oxidase complex. Evidence for a novel cycle of phosphorylation and dephosphorylation. Histochem Cell Biol. 1997;108:221-233.
38. Kile BT, Hentges KE, Clark AT, et al. Functional genetic analysis of mouse chromosome 11. Nature. 2003;425:81-86.
39. Stryke D, Kawamoto M, Huang CC, et al. Bay-Genomics: a resource of insertional mutations in mouse embryonic stem cells. Nucleic Acids Res. 2003;31:278-281.
40. Alexander WS, Metcalf D, Dunn AR. Point mutations within a dimer interface homology domain of c-Mpl induce constitutive receptor activity and tumorigenicity. Embo J. 1995;14:5569-5578.
41. Panopoulos AD, Zhang L, Snow JW, et al. STAT3 governs distinct pathways in emergency granulopoiesis and mature neutrophils. Blood. 2006;108:3682-3690.
42. Boxio R, Bossenmeyer-Pourie C, Steinckwich N, Dournon C, Nusse O. Mouse bone marrow contains large numbers of functionally competent neutrophils. J Leukoc Biol. 2004;75:604-611.
43. Ault KA, Knowles C. In vivo biotinylation demonstrates that reticulated platelets are the youngest platelets in circulation. Exp Hematol. 1995;23:996-1001.
44. Kent PD, Michet CJ, Jr., Luthra HS. Relapsing polychondritis. Curr Opin Rheumatol. 2004;16:56-61.
45. Kuter DJ, Rosenberg RD. Appearance of a megakaryocyte growth-promoting activity, megapoietin, during acute thrombocytopenia in the rabbit. Blood. 1994;84:1464-1472.
46. Stoffel R, Wiestner A, Skoda RC. Thrombopoietin in thrombocytopenic mice: evidence against regulation at the mRNA level and for a direct regulatory role of platelets. Blood. 1996;87:567-573.
47. Yang C, Li YC, Kuter DJ. The physiological response of thrombopoietin (c-Mpl ligand) to thrombocytopenia in the rat. Br J Haematol. 1999;105:478-485.
48. Levin J, Levin FC, Metcalf D. The effects of acute thrombocytopenia on megakaryocyte-CFC and granulocyte-macrophage-CFC in mice: studies of bone marrow and spleen. Blood. 1980;56:274-283.
49. Shivdasani RA, Fujiwara Y, McDevitt MA, Orkin SH. A lineage-selective knockout establishes the critical role of transcription factor GATA-1 in megakaryocyte growth and platelet development. Embo J. 1997;16:3965-3973.
50. Corash L, Chen HY, Levin J, Baker G, Lu H, Mok Y. Regulation of thrombopoiesis: effects of the degree of thrombocytopenia on megakaryocyte ploidy and platelet volume. Blood. 1987;70:177-185.
51. Dibbert B, Weber M, Nikolaizik WH, et al. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc Natl Acad Sci USA. 1999;96:13330-13335.
52. Brannigan AE, O'Connell PR, Hurley H, et al. Neutrophil apoptosis is delayed in patients with inflammatory bowel disease. Shock. 2000;13:361-366.
53. Gourlay CW, Ayscough KR. The actin cytoskeleton: a key regulator of apoptosis and ageing? Nat Rev Mol Cell Biol. 2005;6:583-589.
54. Chua BT, Volbracht C, Tan KO, Li R, Yu VC, Li P. Mitochondrial translocation of cofilin is an early step in apoptosis induction. Nat Cell Biol. 2003;5:1083-1089.
55. Corash L, Levin J. The relationship between megakaryocyte ploidy and platelet volume in normal and thrombocytopenic C3H mice. Exp Hematol. 1990;18:985-989.
56. Corash L, Mok Y, Levin J, Baker G. Regulation of platelet heterogeneity: effects of thrombocytopenia on platelet volume and density. Exp Hematol. 1990;18:205-212.
57. Mason KD, Carpinelli MR, Fletcher JI, et al. Programmed anuclear cell death delimits platelet life span. Cell. 2007;128:1173-1186.
58. Hart A, Melet F, Grossfeld P, et al. Fli-1 is required for murine vascular and megakaryocytic development and is hemizygously deleted in patients with thrombocytopenia. Immunity. 2000;13:167-177.
59. Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, et al. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell. 1995;81:695-704.
60. Italiano JE, Jr., 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;147:1299-1312.
61. Patel SR, Richardson JL, Schulze H, et al. Differential roles of microtubule assembly and sliding in proplatelet formation by megakaryocytes. Blood. 2005;106:4076-4085.
62. Schulze H, Korpal M, Hurov J, et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood. 2006;107:3868-3875.
63. Redondo PC, Harper MT, Rosado JA, Sage SO. A role for cofilin in the activation of store-operated calcium entry by de novo conformational coupling in human platelets. Blood. 2006;107:973-979.