Cofilin regulator 14-3-3ζ is an evolutionarily conserved protein required for phagocytosis and microbial resistance

Journal of Leukocyte Biology

Volumn 89, Issue 5, 2011, Pages 649-659

  Ulvila, Johanna ^a,b   Vanha Aho, Leena Maija ^b   Kleino, Anni ^b,c   Vähä Mäkilä, Mari ^a   Vuoksio, Milka ^b   Eskelinen, Sinikka ^a   Hultmark, Dan ^b,c   Kocks, Christine ^d   Hallman, Mikko ^a   Parikka, Mataleena ^b   Rämet, Mika ^b  

^a UNIVERSITY OF OULU   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c UMEÅ UNIVERSITY   (Sweden)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Drosophila; Immunity; Macrophage; Plasmatocyte; Zebrafish

Indexed keywords

OUTER MEMBRANE PROTEIN REGULATOR; PROTEIN;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BLOOD CELL; COFILIN REGULATOR 14 3 3ZETA GENE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RNA INTERFERENCE; STAPHYLOCOCCUS AUREUS; ZEBRA FISH;

14-3-3 PROTEINS; ACTIN DEPOLYMERIZING FACTORS; ANIMALS; BIOLOGICAL EVOLUTION; CELLS, CULTURED; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE SILENCING; GENES, INSECT; HEMOCYTES; MALE; MICE; PHAGOCYTOSIS; RNA, SMALL INTERFERING; ZEBRAFISH;

BACTERIA (MICROORGANISMS); DANIO RERIO; DROSOPHILA MELANOGASTER; HEXAPODA; STAPHYLOCOCCUS AUREUS; VERTEBRATA;

EID: 79955817261     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0410195     Document Type: Article

References (54)

1. Stuart, L. M., Ezekowitz, R. A. (2005) Phagocytosis: elegant complexity. Immunity 22, 539-550.
2. Hoffmann, J. A., Kafatos, F. C., Janeway, C. A., Ezekowitz, R. A. (1999) Phylogenetic perspectives in innate immunity. Science 284, 1313-1318.
3. Cherry, S., Silverman, N. (2006) Host-pathogen interactions in Drosophila: new tricks from an old friend. Nat. Immunol. 7, 911-917.
4. Lemaitre, B., Hoffmann, J. (2007) The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743.
5. Kocks, C., Cho, J. H., Nehme, N., Ulvila, J., Pearson, A. M., Meister, M., Strom, C., Conto, S. L., Hetru, C., Stuart, L. M., Stehle, T., Hoffmann, J. A., Reichhart, J-M., Ferrandon, D., Rämet, M., Ezekowitz, R. A. B. (2005) Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123, 335-346.
6. Charroux, B., Royet, J. (2009) Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. Proc. Natl. Acad. Sci. USA 106, 9797-9802.
7. Defaye, A., Ewans, I., Crozatier, M., Wood, W., Lemaitre, B., Leulier, F. (2009) Genetic ablation of Drosophila phagocytes reveals their contribution to both development and resistance to bacterial infection. J. Innate Immun. 1, 322-334.
8. Franc, N. C., Heitzler, P., Ezekowitz, R. A., White, K. (1999) Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284, 1991-1994.
9. Rämet, M., Pearson, A., Manfruelli, P., Li, X., Koziel, H., Gobel, V., Chung, E., Krieger, M., Ezekowitz, R. A. (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15, 1027-1038.
10. Rämet, M., Manfruelli, P., Pearson, A., Mathey-Prevot, B., Ezekowitz, R. A. (2002) Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416, 644-648.
11. Philips, J. A., Rubin, E. J., Perrimon, N. (2005) Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309, 1251-1253.
12. Stuart, L. M., Deng, J., Silver, J. M., Takahashi, K., Tseng, A. A., Hennessy, E. J., Ezekowitz, R. A., Moore, K. J. (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOHterminal cytoplasmic domain. J. Cell Biol. 170, 477-485.
13. Watson, F. L., Puttmann-Holgado, R., Thomas, F., Lamar, D. L., Hughes, M., Kondo, M., Rebel, V. I., Schmucker, D. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309, 1874-1878.
14. Kurucz, É., Márkus, R., Zsámboki, J., Folkl-Medzihradsky, K., Darula, Z., Vilmos, P., Udvardy, A., Krausz, I., Lukacsovich, T., Gateff, E., Zettervall, C. J., Hultmark, D., Andó, I. (2007) Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 17, 649-654.
15. Cuttell, L., Vaughan, A., Silva, E., Escaron, C. J., Lavine, M., Van Goethem, E., Eid, J. P., Quirin, M., Franc, N. C. (2008) Undertaker, a Drosophila junctophilin, links Draper-mediated phagocytosis and calcium homeostasis. Cell 135, 524-534.
16. Agaisse, H., Burrack, L. S., Philips, J. A., Rubin, E. J., Perrimon, N., Higgins, D. E. (2005) Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309, 1248-1251.
17. Stroschein-Stevenson, S. L., Foley, E., O'Farrell, P. H., Johnson, A. D. (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. 4, e4.
18. Dietzl, G., Chen, D., Schnorrer, F., Su, K-C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., Dickson, B. J. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
19. Pearson, A., Lux, A., Krieger, M. (1995) Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 92, 4056-4060.
20. Ojaniemi, M., Glumoff, V., Harju, K., Liljeroos, M., Vuori, K., Hallman, M. (2003) Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur. J. Immunol. 33, 597-605.
21. Ulvila, J., Parikka, M., Kleino, A., Sormunen, R., Ezekowitz, R. A., Kocks, C., Rämet, M. (2006) Double-stranded RNA is internalized by scavenger receptormediated endocytosis in Drosophila S2 cells. J. Biol. Chem. 281, 14370-14375.
22. O'Brien, K. P., Remm, M., Sonnhammer, E. L. L. (2005) Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res. 33, D476-D480.
23. Cvejic, A., Hall, C., Bak-Maier, M., Flores, M. V., Crosier, P., Redd, M. J., Martin, P. (2008) Analysis of WASp function during the wound inflammatory response-live-imaging studies in zebrafish larvae. J. Cell Sci. 121, 3196-3206.
24. Kallio, J., Leinonen, A., Ulvila, J., Valanne, S., Ezekowitz, R. A. B., Rämet, M. (2005) Functional analysis of immune response genes in Drosophila identifies JNK pathway as a regulator of antimicrobial peptide gene expression in S2 cells. Microbes Infect. 7, 811-819.
25. Sinenko, S. A., Mathey-Prevot, B. (2004) Increased expression of Drosophila tetraspanin, Tsp68C, suppresses the abnormal proliferation of ytr-deficient and Ras/Raf-activated hemocytes. Oncogene 23, 9120-9128.
26. Pearson, A. M., Baksa, K., Rämet, M., Protas, M., McKee, M., Brown, D., Ezekowitz, R. A. (2003) Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect. 5, 815-824.
27. Clay, H., Davis, J. M., Beery, D., Huttenlocher, A., Lyons, S. E., Ramakrishnan, L. (2007) Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2, 29-39.
28. Valanne, S., Kleino, A., Myllymäki, H., Vuoristo, J., Rämet, R. (2007) Iap2 is required for a sustained response in the Drosophila Imd pathway. Dev. Comp. Immunol. 31, 991-1001.
29. Boutros, M., Kiger, A. A., Armknecht, S., Kerr, K., Hild, M., Koch, B., Haas, S. A., Consortium, H. F., Paro, R., Perrimon, N. (2004) Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303, 832-835.
30. Kleino, A., Valanne, S., Ulvila, J., Kallio, J., Myllymäki, H., Enwald, H., Stöven, S., Poidevin, M., Ueda, R., Hultmark, D., Lemaitre, B., Rämet, M. (2005) Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J. 24, 3423-3434.
31. Elrod-Erickson, M., Mishra, S., Schneider, D. (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10, 781-784.
32. Thrasher, A. J., Burns, S. O. (2010) WASP: a key immunological multitasker. Nat. Rev. Immunol. 10, 182-192.
33. Stradal, T., Courtney, K. D., Rottner, K., Hahne, P., Small, J. V., Pendergast, A. M. (2001) The Abl interactor proteins localize to sites of actin polymerization at the tips of lamellipodia and filopodia. Curr. Biol. 11, 891-895.
34. Kunda, P., Craig, G., Dominguez, V., Baum, B. (2003) Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 13, 1867-1875.
35. Ibarra, N., Pollitt, A., Insall, R. H. (2005) Cell architecture: from structure to function. Biochem. Soc. Trans. 33, 1243-1246.
36. Prajsnar, T. K., Cunliffe, V. T., Foster, S. J., Renshaw, S. A. (2008) A novel vertebrate model of Staphylococcus aureus infection reveals phagocyte-dependent resistance in zebrafish to non-host specialized pathogens. Cell. Microbiol. 10, 2312-2325.
37. Derré, I., Pypaert, M., Dautry-Varsat, A., Agaisse, H. (2007) RNAi screen in Drosophila cells reveals the involvement of the Tom complex in Chlamydia infection. PLoS Pathog. 3, 1446-1458.
38. Berti, C., Fontanella, B., Ferrentino, R., Meroni, G. (2004) Mig12, a novel Opitz syndrome gene product partner, is expressed in the embryonic ventral midline and co-operates with Mid1 to bundle and stabilize microtubules. BMC Cell Biol. 5, 9.
39. Guilherme, A., Soriano, N. A., Furcinitti, P. S., Czech, M. P. (2004) Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J. Biol. Chem. 279, 40062-40075.
40. Brannon, M. K., Davis, J. M., Mathias, J. R., Hall, C. J., Emerson, J. C., Crosier, P. S., Huttenlocher, A., Ramakrishnan, L., Moskowitz, S. M. (2009) Pseudomonas aeruginosa type III secretion system interacts with phagocytes to modulate systemic infection of zebrafish embryos. Cell. Microbiol. 11, 755-768.
41. Aitken, A. (1996) 14-3-3 and its possible role in co-ordinating multiple signaling pathways. Trends Cell Biol. 6, 341-347.
42. Skoulakis, E. M., Davis, R. L. (1998) 14-3-3 proteins in neuronal development and function. Mol. Neurobiol. 16, 269-284.
43. Peng, C. Y., Graves, P. R., Thomas, R. S., Wu, Z., Shaw, A. S., Piwnica-Worms, H. (1997) Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277, 1501-1505.
44. L. Cell 87, 619-628.
45. Morgan, A., Burgoyne, R. D. (1992) Exo1 and Exo2 proteins stimulate calcium-dependent exocytosis in permeabilized adrenal chromaffin cells. Nature 355, 833-836.
46. Broadie, K., Rushton, E., Skoulakis, E. M., Davis, R. L. (1997) Leonardo, a Drosophila 14-3-3 protein involved in learning, regulates presynaptic function. Neuron 19, 391-402.
47. Gaestel, M. (2006) MAPKAP kinases-MKs-two's company, three's a crowd. Nat. Rev. Mol. Cell Biol. 7, 120-130.
48. Fu, H., Subramanian, R. R., Masters, S. C. (2000) 14-3-3 proteins: structure, function and regulation. Annu. Rev. Pharmacol. Toxicol. 40, 617-647.
49. Huang, T. Y., DerMardirossian, C., Bokoch, G. M. (2006) Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 18, 26-31.
50. Birkenfeld, J., Betz, H., Roth, D. (2003) Identification of cofilin and LIMdomain-containing protein kinase 1 as novel interaction partners of 14- 3-3ζ. Biochem. J. 369, 45-54.
51. Soosairajah, J., Maiti, S., Wiggan, O., Sarmiere, P., Moussi, N., Sarcevic, B., Sampath, R., Bamburg, J. R., Bernard, O. (2005) Interplay between components of a novel LIM kinase-slingshot phosphatase complex regulates cofilin. EMBO J. 24, 473-486.
52. Stuart, L. M., Boulais, J., Charriere, G. M., Hennessy, E. J., Brunet, S., Jutras, I., Goyette, G., Rondeau, C., Letarte, S., Huang, H., Ye, P., Morales, F., Kocks, C., Bader, J. S., Desjardins, M., Ezekowitz, R. A. B. (2007) A systems biology analysis of the Drosophila phagosome. Nature 445, 95-101.
53. Delorme, V., Machacek, M., DerMardirossian, C., Anderson, K. L., Wittmann, T., Hanein, D., Waterman-Storer, C., Danuser, G., Bokoch, G. M. (2007) Cofilin activity downstream of Pak1 regulates cell protrusion efficiency by organizing lamellipodium and lamella actin networks. Dev. Cell 13, 646-662.
54. Gohla, A., Bokoch, G. M. (2002) 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr. Biol. 12, 1704-1710.