The Drosophila FHOD1-like formin Knittrig acts through Rok to promote stress fiber formation and directed macrophage migration during the cellular immune response

Development (Cambridge)

Volumn 141, Issue 6, 2014, Pages 1366-1380

  Lammel, Uwe ^a   Bechtold, Meike ^a   Risse, Benjamin ^a   Berh, Dimitri ^a   Fleige, Astrid ^a   Bunse, Ingrid ^a   Jiang, Xiaoyi ^a   Klämbt, Christian ^a   Bogdan, Sven ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Cellular immune response; Drosophila; F actin; Formin; Macrophages; Stress fiber; Tracheal development

Indexed keywords

ACTIN RELATED PROTEIN; FHOD1 PROTEIN; KNITTRIG PROTEIN; RHO KINASE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL SPREADING; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO DEVELOPMENT; EPITHELIUM; FORELIMB; GLIA; IN VIVO STUDY; MACROPHAGE; MACROPHAGE MIGRATION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRESS FIBER; SURVIVAL; TRACHEA; WOUND;

CELLULAR IMMUNE RESPONSE; DROSOPHILA; F-ACTIN; FORMIN; MACROPHAGES; STRESS FIBER; TRACHEAL DEVELOPMENT;

ANIMALS; CELL MOVEMENT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; IMMUNITY, CELLULAR; MACROPHAGES; MUTATION; RHO-ASSOCIATED KINASES; STRESS FIBERS;

EID: 84896871185     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.101352     Document Type: Article

References (65)

1. Anhezini, L., Saita, A. P., Costa, M. S., Ramos, R. G. and Simon, C. R. (2012). Fhos encodes a Drosophila Formin-like protein participating in autophagic programmed cell death. Genesis 50, 672-684.
2. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
3. Bogdan, S. and Klämbt, C. (2003). Kette regulates actin dynamics and genetically interacts with Wave and Wasp. Development 130, 4427-4437.
4. Burridge, K. and Wittchen, E. S. (2013). The tension mounts: stress fibers as forcegenerating mechanotransducers. J. Cell Biol. 200, 9-19.
5. Campellone, K. G. and Welch, M. D. (2010). A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251.
6. Carlier, M. F., Husson, C., Renault, L. and Didry, D. (2011). Control of actin assembly by the WH2 domains and their multifunctional tandem repeats in Spire and Cordon-Bleu. Int. Rev. Cell Mol. Biol. 290, 55-85.
7. Castrillon, D. H. and Wasserman, S. A. (1994). Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120, 3367-3377.
8. Chevrier, V., Piel, M., Collomb, N., Saoudi, Y., Frank, R., Paintrand, M., Narumiya, S., Bornens, M. and Job, D. (2002). The Rho-associated protein kinase p160ROCK is required for centrosome positioning. J. Cell Biol. 157, 807-817.
9. Emmons, S., Phan, H., Calley, J., Chen, W., James, B. and Manseau, L. (1995). Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus. Genes Dev. 9, 2482-2494.
10. Englund, C., Uv, A. E., Cantera, R., Mathies, L. D., Krasnow, M. A. and Samakovlis, C. (1999). adrift, a novel bnl-induced Drosophila gene, required for tracheal pathfinding into the CNS. Development 126, 1505-1514.
11. Farhadifar, R., Röper, J. C., Aigouy, B., Eaton, S. and Jülicher, F. (2007). The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 17, 2095-2104.
12. Firat-Karalar, E. N. and Welch, M. D. (2011). New mechanisms and functions of actin nucleation. Curr. Opin. Cell Biol. 23, 4-13.
13. Fricke, R., Gohl, C., Dharmalingam, E., Grevelhörster, A., Zahedi, B., Harden, N., Kessels, M., Qualmann, B. and Bogdan, S. (2009). Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr. Biol. 19, 1429-1437.
14. Gardberg, M., Kaipio, K., Lehtinen, L., Mikkonen, P., Heuser, V. D., Talvinen, K., Iljin, K., Kampf, C., Uhlen, M., Grénman, R. et al. (2013). FHOD1, a formin upregulated in epithelial-mesenchymal transition, participates in cancer cell migration and invasion. PLoS ONE 8, e74923.
15. Gasteier, J. E., Madrid, R., Krautkrämer, E., Schröder, S., Muranyi, W., Benichou, S. and Fackler, O. T. (2003). Activation of the Rac-binding partner FHOD1 induces actin stress fibers via a ROCK-dependent mechanism. J. Biol. Chem. 278, 38902-38912.
16. Gasteier, J. E., Schroeder, S., Muranyi, W., Madrid, R., Benichou, S. and Fackler, O. T. (2005). FHOD1 coordinates actin filament and microtubule alignment to mediate cell elongation. Exp. Cell Res. 306, 192-202.
17. Goode, B. L. and Eck, M. J. (2007). Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76, 593-627.
18. Gould, C. J., Maiti, S., Michelot, A., Graziano, B. R., Blanchoin, L. and Goode, B. L. (2011). The formin DAD domain plays dual roles in autoinhibition and actin nucleation. Curr. Biol. 21, 384-390.
19. Grosshans, J., Wenzl, C., Herz, H. M., Bartoszewski, S., Schnorrer, F., Vogt, N., Schwarz, H. and Müller, H. A. (2005). RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 132, 1009-1020.
20. Harris, E. S., Li, F. and Higgs, H. N. (2004). The mouse formin, FRLalpha, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments. J. Biol. Chem. 279, 20076-20087.
21. Harris, E. S., Rouiller, I., Hanein, D. and Higgs, H. N. (2006). Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J. Biol. Chem. 281, 14383-14392.
22. Hotulainen, P. and Lappalainen, P. (2006). Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173, 383-394.
23. Iskratsch, T., Lange, S., Dwyer, J., Kho, A. L., dos Remedios, C. and Ehler, E. (2010). Formin follows function: a muscle-specific isoform of FHOD3 is regulated by CK2 phosphorylation and promotes myofibril maintenance. J. Cell Biol. 191, 1159-1172.
24. Iskratsch, T., Yu, C. H., Mathur, A., Liu, S., Stévenin, V., Dwyer, J., Hone, J., Ehler, E. and Sheetz, M. (2013). FHOD1 Is Needed for Directed Forces and Adhesion Maturation during Cell Spreading and Migration. Dev. Cell 27, 545-559.
25. Jani, K. and Schöck, F. (2007). Zasp is required for the assembly of functional integrin adhesion sites. J. Cell Biol. 179, 1583-1597.
26. Johansson, K. C., Metzendorf, C. and Söderhäll, K. (2005). Microarray analysis of immune challenged Drosophila hemocytes. Exp. Cell Res. 305, 145-155.
27. Jurmeister, S., Baumann, M., Balwierz, A., Keklikoglou, I., Ward, A., Uhlmann, S., Zhang, J. D., Wiemann, S. and Sahin, Ö. (2012). MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol. Cell. Biol. 32, 633-651.
28. Kadandale, P., Stender, J. D., Glass, C. K. and Kiger, A. A. (2010). Conserved role for autophagy in Rho1-mediated cortical remodeling and blood cell recruitment. Proc. Natl. Acad. Sci. USA 107, 10502-10507.
29. Kan-O, M., Takeya, R., Abe, T., Kitajima, N., Nishida, M., Tominaga, R., Kurose, H. and Sumimoto, H. (2012a). Mammalian formin Fhod3 plays an essential role in cardiogenesis by organizing myofibrillogenesis. Biol. Open 1, 889-896.
30. Kan-O, M., Takeya, R., Taniguchi, K., Tanoue, Y., Tominaga, R. and Sumimoto, H. (2012b). Expression and subcellular localization of mammalian formin Fhod3 in the embryonic and adult heart. PLoS ONE 7, e34765.
31. Klämbt, C., Jacobs, J. R. and Goodman, C. S. (1991). The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64, 801-815.
32. Koka, S., Neudauer, C. L., Li, X., Lewis, R. E., McCarthy, J. B. and Westendorf, J. J. (2003). The formin-homology-domain-containing protein FHOD1 enhances cell migration. J. Cell Sci. 116, 1745-1755.
33. Kovar, D. R. (2006). Molecular details of formin-mediated actin assembly. Curr. Opin. Cell Biol. 18, 11-17.
34. Kunda, P., Craig, G., Dominguez, V. and 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. Leung, T., Chen, X. Q., Manser, E. and Lim, L. (1996). The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16, 5313-5327.
36. Liu, H., Mardahl-Dumesnil, M., Sweeney, S. T., O'Kane, C. J. and Bernstein, S. I. (2003). Drosophila paramyosin is important for myoblast fusion and essential for myofibril formation. J. Cell Biol. 160, 899-908.
37. Liu, R., Linardopoulou, E. V., Osborn, G. E. and Parkhurst, S. M. (2010). Formins in development: orchestrating body plan origami. Biochim. Biophys. Acta 1803, 207-225.
38. Manseau, L. J. and Schüpbach, T. (1989). cappuccino and spire: two unique maternal-effect loci required for both the anteroposterior and dorsoventral patterns of the Drosophila embryo. Genes Dev. 3, 1437-1452.
39. Matusek, T., Djiane, A., Jankovics, F., Brunner, D., Mlodzik, M. and Mihály, J. (2006). The Drosophila formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton. Development 133, 957-966.
40. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. and Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768.
41. Mi-Mi, L., Votra, S., Kemphues, K., Bretscher, A. and Pruyne, D. (2012). Z-line formins promote contractile lattice growth and maintenance in striated muscles of C. elegans. J. Cell Biol. 198, 87-102.
42. Moreira, C. G., Jacinto, A. and Prag, S. (2013). Drosophila integrin adhesion complexes are essential for hemocyte migration in vivo. Biol. Open 2, 795-801.
43. Otomo, T., Tomchick, D. R., Otomo, C., Panchal, S. C., Machius, M. and Rosen, M. K. (2005). Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature 433, 488-494.
44. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
45. Pollard, T. D. and Cooper, J. A. (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
46. Sánchez-Madrid, F. and Serrador, J. M. (2009). Bringing up the rear: defining the roles of the uropod. Nat. Rev. Mol. Cell Biol. 10, 353-359.
47. Sánchez-Soriano, N., Tear, G., Whitington, P. and Prokop, A. (2007). Drosophila as a genetic and cellular model for studies on axonal growth. Neural Dev. 2, 9.
48. Sander, M., Squarr, A. J., Risse, B., Jiang, X. and Bogdan, S. (2013). Drosophila pupal macrophages-a versatile tool for combined ex vivo and in vivo imaging of actin dynamics at high resolution. Eur. J. Cell Biol. 92, 349-354.
49. Schönichen, A. and Geyer, M. (2010). Fifteen formins for an actin filament: a molecular view on the regulation of human formins. Biochim. Biophys. Acta 1803, 152-163.
50. Schönichen, A., Mannherz, H. G., Behrmann, E., Mazur, A. J., Kühn, S., Silván, U., Schoenenberger, C. A., Fackler, O. T., Raunser, S., Dehmelt, L. et al. (2013). FHOD1 is a combined actin filament capping and bundling factor that selectively associates with actin arcs and stress fibers. J. Cell Sci. 126, 1891-1901.
51. Schulte, A., Stolp, B., Schönichen, A., Pylypenko, O., Rak, A., Fackler, O. T. and Geyer, M. (2008). The human formin FHOD1 contains a bipartite structure of FH3 and GTPase-binding domains required for activation. Structure 16, 1313-1323.
52. Simões, S. M., Blankenship, J. T., Weitz, O., Farrell, D. L., Tamada, M., Fernandez-Gonzalez, R. and Zallen, J. A. (2010). Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev. Cell 19, 377-388.
53. Sinenko, S. A. and 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.
54. Stephan, R., Gohl, C., Fleige, A., Klämbt, C. and Bogdan, S. (2011). Membranetargeted WAVE mediates photoreceptor axon targeting in the absence of the WAVE complex in Drosophila. Mol. Biol. Cell 22, 4079-4092.
55. Takeya, R. and Sumimoto, H. (2003). Fhos, a mammalian formin, directly binds to Factin via a region N-terminal to the FH1 domain and forms a homotypic complex via the FH2 domain to promote actin fiber formation. J. Cell Sci. 116, 4567-4575.
56. Takeya, R., Taniguchi, K., Narumiya, S. and Sumimoto, H. (2008). The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells. EMBO J. 27, 618-628.
57. Tanaka, H., Takasu, E., Aigaki, T., Kato, K., Hayashi, S. and Nose, A. (2004). Formin3 is required for assembly of the F-actin structure that mediates tracheal fusion in Drosophila. Dev. Biol. 274, 413-425.
58. Taniguchi, K., Takeya, R., Suetsugu, S., Kan-O, M., Narusawa, M., Shiose, A., Tominaga, R. and Sumimoto, H. (2009). Mammalian formin fhod3 regulates actin assembly and sarcomere organization in striated muscles. J. Biol. Chem. 284, 29873-29881.
59. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
60. Valanne, S., Kleino, A., Myllymäki, H., Vuoristo, J. and Rämet, M. (2007). Iap2 is required for a sustained response in the Drosophila Imd pathway. Dev. Comp. Immunol. 31, 991-1001.
61. Westendorf, J. J. (2001). The formin/diaphanous-related protein, FHOS, interacts with Rac1 and activates transcription from the serum response element. J. Biol. Chem. 276, 46453-46459.
62. Westendorf, J. J. and Koka, S. (2004). Identification of FHOD1-binding proteins and mechanisms of FHOD1-regulated actin dynamics. J. Cell. Biochem. 92, 29-41.
63. Wood, W. and Jacinto, A. (2007). Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat. Rev. Mol. Cell Biol. 8, 542-551.
64. Xu, N., Keung, B. and Myat, M. M. (2008). Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rhokinase. Dev. Biol. 321, 88-100.
65. Zobel, T. and Bogdan, S. (2013). A high resolution view of the fly actin cytoskeleton lacking a functional WAVE complex. J. Microsc. 251, 224-231.