The flare gene, which encodes the AIP1 protein of drosophila, functions to regulate F-actin disassembly in pupal epidermal cells

Genetics

Volumn 176, Issue 4, 2007, Pages 2223-2234

  Ren, Nan ^a   Charlton, Jeannette ^a   Adler, Paul N ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AIP1 PROTEIN; COFILIN; F ACTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL POLARITY; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EPIDERMIS CELL; GENE MUTATION; INSECT; INSECT DEVELOPMENT; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN STABILITY; YEAST;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL POLARITY; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; EPIDERMIS; FEMALE; GENES, INSECT; MALE; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PUPA; WING;

EID: 34548409590     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.072959     Document Type: Article

References (80)

1. ADLER, P. N., 2002 Planar signaling and morphogenesis in Drosophila. Dev. Cell 2: 525-535.
2. ADLER, P. N., J. LIU and J. CHARLTON, 2000 Cell size and the morphogenesis of wing hairs in Drosophila. Genesis 28: 82-91.
3. ADLER, P. N., C. ZHU and D. STONE, 2004 Inturned localizes to the proximal side of wing cells under the instruction of upstream planar polarity proteins. Curr. Biol. 14: 2046-2051.
4. AMONLIRDVIMAN, K., N. A. KHARE, D. R. TREE, W. S. CHEN, J. D. AXELROD et al., 2005 Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science 307: 423-426.
5. ARBER, S., F. A. BARBAYANNIS, H. HANSER, C. SCHNEIDER, C. A. STANYON et al., 1998 Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393: 805-809.
6. BALCER, H. I., A. L. GOODMAN, A. A. RODAL, E. SMITH, J. KUGLER et al., 2003 Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr. Biol. 13: 2159-2169.
7. BAUM, B., 2002 Winging it - actin on the fly. Dev. Cell 2: 125-126.
8. BAUM, B., and N. PERRIMON, 2001 Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat. Cell Biol. 3: 883-890.
9. BAUM, B., W. LI and N. PERRIMON, 2000 A cyclase-associated protein regulates actin and cell polarity during Drosophila oogenesis and in yeast. Curr. Biol. 10: 964-973.
10. BLAIR, A., A. TOMLINSON, H. PHAM, K. C. GUNSALUS, M. L. GOLDBERG et al., 2006 Twinstar, the Drosophila homolog of cofilin/ADF, is required for planar cell polarity patterning. Development 133: 1789-1797.
11. BRIEHER, W. M., H. Y. KUEH, B. A. BALLIF and T. J. MITCHISON, 2006 Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J. Cell Biol. 175: 315-324.
12. BRYAN, J., R. EDWARDS, P. MATSUDAIRA, J. OTTO and J. WULFKUHLE, 1993 Fascin, an echinoid actin-bundling protein, is a homolog of the Drosophila singed gene product. Proc. Natl. Acad. Sci. USA 90: 9115-9119.
13. CANT, K., B. A. KNOWLES, M. S. MOOSEKER and L. COOLEY, 1994 Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J. Cell Biol. 125: 369-380.
14. CHAE, J., M. J. KIM, J. H. GOO, S. COLLIER, D. GUBB et al., 1999 The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126: 5421-5429.
15. CHANUT-DELALANDE, H., I. FERNANDES, F. ROCH, F. PAYRE and S. PLAZA, 2006 Shavenbaby couples patterning to epidermal cell shape control. PLoS Biol. 4: e290.
16. CHEN, J., D. GODT, K. GUNSALUS, I. KISS, M. GOLDBERG et al., 2001 Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nat. Cell Biol. 3: 204-209.
17. CLARK, M. G., J. TEPLY, B. K. HAARER, S. C. VIGGIANO, D. SEPT et al., 2006 A genetic dissection of Aip1p's interactions leads to a model for Aip1p-cofilin cooperative activities. Mol Biol Cell 17: 1971-1984.
18. DICKINSON, W. J., and J. W. THATCHER, 1997 Morphogenesis of denticles and hairs in Drosophila embryos: involvement of actin-associated proteins that also affect adult structures. Cell Motil. Cytoskeleton 38: 9-21.
19. DORMANN, D., and C. J. WEIJER, 2006 Chemotactic cell movement during Dictyostelium development and gastrulation. Curr. Opin. Genet. Dev. 16: 367-373.
20. EGEA, G., F. LAZARO-DIEGUEZ and M. VILELLA, 2006 Actin dynamics at the Golgi complex in mammalian cells. Curr. Opin. Cell Biol. 18: 168-178.
21. ETIENNE-MANNEVILLE, S., 2004 Actin and microtubules in cell motility: Which one is in control? Traffic 5: 470-477.
22. FEDOROV, A. A., P. LAPPALAINEN, E. V. FEDOROV, D. G. DRUBIN and S. C. ALMO, 1997 Structure determination of yeast cofilin. Nat. Struct. Biol. 4: 366-369.
23. FRANK, D. J., R. HOPMANN, M. LENARTOWSKA and K. G. MILLER, 2006 Capping protein and the Arp2/3 complex regulate nonbundle actin filament assembly to indirectly control actin bundle positioning during Drosophila melanogaster bristle development. Mol. Biol. Cell 17: 3930-3939.
24. FUJIBUCHI, T., Y. ABE, T. TAKEUCHI, Y. IMAI, Y. KAMEI et al., 2005 AIP1/WDR1 supports mitotic cell rounding. Biochem. Biophys. Res. Commun. 327: 268-275.
25. GARCIA-BELLIDO, A., and J. DAPENA, 1974 Induction, detection and characterization of cell differentiation mutants in Drosophila. Molec. Gen. Genet. 128: 117-130.
26. GENG, W., B. HE, M. WANG and P. N. ADLER, 2000 The tricornered gene, which is required for the integrity of epidermal cell extensions, encodes the Drosophila nuclear DBF2-related kinase. Genetics 156: 1817-1828.
27. GERISCH, G., J. FAIX, J. KOHLER and A. MULLER-TAUBENBERGER, 2004 Actin-binding proteins required for reliable chromosome segregation in mitosis. Cell Motil. Cytoskeleton 57: 18-25.
28. GUILD, G. M., P. S. CONNELLY, K. A. VRANICH, M. K. SHAW and L. G. TILNEY, 2002 Actin filament turnover removes bundles from Drosophila bristle cells. J. Cell Sci. 115: 641-653.
29. GUILD, G. M., P. S. CONNELLY, L. RUGGIERO, K. A. VRANICH and L. G. TILNEY, 2005 Actin filament bundles in Drosophila wing hairs: hairs and bristles use different strategies for assembly. Mol. Biol. Cell 16: 3620-3631.
30. GUNSALUS, K. C., S. BONACCORSI, E. WILLIAMS, F. VERNI, M. GATTI et al., 1995 Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J. Cell Biol. 131: 1243-1259.
31. HE, B., and P. N. ADLER, 2002 The genetic control of arista lateral morphogenesis in Drosophila. Dev. Genes Evol. 212: 218-229.
32. HE, Y., X. FANG, K. EMOTO, Y. N. JAN and P. N. ADLER, 2005 The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development. Mol. Biol. Cell 16: 689-700.
33. HOPMANN, R., and K. G. MILLER, 2003 A balance of capping protein and profilin functions is required to regulate actin polymerization in Drosophila bristle. Mol. Biol. Cell 14: 118-128.
34. HOPMANN, R., J. A. COOPER and K. G. MILLER, 1996 Actin organization, bristle morphology, and viability are affected by actin capping protein mutations in Drosophila. J. Cell Biol. 133: 1293-1305.
35. HUDSON, A. M., and L. COOLEY, 2002 A subset of dynamic actin rearrangements in Drosophila requires the Arp2/3 complex. J. Cell Biol. 156: 677-687.
36. JANODY, F., and J. E. TREISMAN, 2006 Actin capping protein alpha maintains vestigial-expressing cells within the Drosophila wing disc epithelium. Development 133: 3349-3357.
37. KETELAAR, T., E. G. ALLWOOD, R. ANTHONY, B. VOIGT, D. MENZEL et al., 2004 The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr. Biol. 14: 145-149.
38. KIEHART, D. P., J. D. FRANKE, M. K. CHEE, R. A. MONTAGUE, T. L. CHEN et al., 2004 Drosophila crinkled, mutations of which disrupt morphogenesis and cause lethality, encodes fly myosin VIIA. Genetics 168: 1337-1352.
39. KODAMA, A., T. LECHLER and E. FUCHS, 2004 Coordinating cytoskeletal tracks to polarize cellular movements. J. Cell Biol. 167: 203-207.
40. KONZOK, A., I. WEBER, E. SIMMETH, U. HACKER, M. MANIAK et al., 1999 DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J. Cell Biol 146: 453-464.
41. LAPPALAINEN, P., E. V. FEDOROV, A. A. FEDOROV, S. C. ALMO and D. G. DRUBIN, 1997 Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J. 16: 5520-5530.
42. LEE, H., and P. N. ADLER, 2004 The grainy head transcription factor is essential for the function of the frizzled pathway in the Drosophila wing. Mech. Dev. 121: 37-49.
43. MARSTON, D. J., and B. GOLDSTEIN, 2006 Actin-based forces driving embryonic morphogenesis in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 16: 392-398.
44. MATHUR, J., 2006 Local interactions shape plant cells. Curr. Opin. Cell Biol. 18: 40-46.
45. MILLER, A. L., Y. WANG, M. S. MOOSEKER and A. J. KOLESKE, 2004 The Abl-related gene (Arg) requires its F-actin-microtubule cross-linking activity to regulate lamellipodial dynamics during fibroblast adhesion. J. Cell Biol. 165: 407-419.
46. MOHRI, K., and S. ONO, 2003 Actin filament disassembling activity of Caenorhabditis elegans actin-interacting protein 1 (UNC-78) is dependent on filament binding by a specific ADF/cofilin isoform. J. Cell Sci. 116: 4107-4118.
47. MOHRI, K., S. VOROBIEV, A. A. FEDOROV, S. C. ALMO and S. ONO, 2004 Identification of functional residues on Caenorhabditis elegans actin-interacting protein 1 (UNC-78) for disassembly of actin depolymerizing factor/cofilin-bound actin filaments. J. Biol. Chem. 279: 31697-31707.
48. MOHRI, K., K. ONO, R. YU, S. YAMASHIRO and S. ONO, 2006 Enhancement of actin-depolymerizing factor/cofilin-dependent actin disassembly by actin-interacting protein 1 is required for organized actin filament assembly in the Caenorhabditis elegans body wall muscle. Mol. Biol. Cell 17: 2190-2199.
49. NG, J., and L. LUO, 2004 Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44: 779-793.
50. NIWA, R., K. NAGATA-OHASHI, M. TAKEICHI, K. MIZUNO and T. UEMURA, 2002 Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108: 233-246.
51. OHASHI, K., T. HOSOYA, K. TAKAHASHI, H. HING and K. MIZUNO, 2000 A Drosophila homolog of LIM-kinase phosphorylates cofilin and induces actin cytoskeletal reorganization. Biochem. Biophys. Res. Commun. 276: 1178-1185.
52. OKADA, K., T. OBINATA and H. ABE, 1999 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. 112(Pt 10): 1553-1565.
53. OKADA, K., H. RAVI, E. M. SMITH and B. L. GOODE, 2006 Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: a coordinated mechanism for severing and capping filaments. Mol. Biol. Cell 17: 2855-2868.
54. ONO, S., 2001 The Caenorhabditis elegans unc-78 gene encodes a homologue of actin-interacting protein 1 required for organized assembly of muscle actin filaments. J. Cell Biol. 152: 1313-1319.
55. ONO, S., 2003 Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: new blades for twisted filaments. Biochemistry 42: 13363-13370.
56. ONO, S., K. MOHRI and K. ONO, 2004 Microscopic evidence that actininteracting protein 1 actively disassembles actin-depolymerizing factor/Cofilin-bound actin filaments. J. Biol. Chem. 279: 14207-14212.
57. PAAVILAINEN, V. O., E. BERTLING, S. FALCK and P. LAPPALAINEN, 2004 Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell Biol. 14: 386-394.
58. PARK, W. J., J. LIU, E. J. SHARP and P. N. ADLER, 1996 The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development 122: 961-969.
59. PETERSEN, N. S., D. H. LANKENAU, H. K. MITCHELL, P. YOUNG and V. G. CORCES, 1994 forked proteins are components of fiber bundles present in developing bristles of Drosophila melanogaster. Genetics 136: 173-182.
60. PILOT, F., and T. LECUIT, 2005 Compartmentalized morphogenesis in epithelia: from cell to tissue shape. Dev. Dyn. 232: 685-694.
61. PRUYNE, D., A. LEGESSE-MILLER, L. GAO, Y. DONG and A. BRETSCHER, 2004 Mechanisms of polarized growth and organelle segregation in yeast. Ann. Rev. Cell Dev. Biol. 20: 559-591.
62. REN, N., B. HE, D. STONE, S. KIRAKODU and P. N. ADLER, 2006 The shavenoid gene of Drosophila encodes a novel actin cytoskeleton interacting protein that promotes wing hair morphogenesis. Genetics 172: 1643-1653.
63. REVENU, C., R. ATHMAN, S. ROBINE and D. LOUVARD, 2004 The coworkers of actin filaments: from cell structures to signals. Nat. Rev. Mol. Cell Biol. 5: 635-646.
64. RODAL, A. A., J. W. TETREAULT, P. LAPPALAINEN, D. G. DRUBIN and D. C. AMBERG, 1999 Aip1p interacts with cofilin to disassemble actin filaments. J. Cell Biol. 145: 1251-1264.
65. RODRIGUEZ, O. C., A. W. SCHAEFER, C. A. MANDATO, P. FORSCHER, W. M. BEMENT et al., 2003 Conservedmicrotubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5: 599-609.
66. ROGERS, S. L., U. WIEDEMANN, N. STUURMAN and R. D. VALE, 2003 Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162: 1079-1088.
67. ROPER, K., S. L. GREGORY and N. H. BROWN, 2002 The 'spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J. Cell Sci. 115: 4215-4225.
68. SCHAFER, D. A., 2004 Regulating actin dynamics at membranes: a focus on dynamin. Traffic 5: 463-469.
69. SHIMADA, Y., S. YONEMURA, H. OHKURA, D. STRUTT and T. UEMURA, 2006 Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev. Cell 10: 209-222.
70. TILNEY, L. G., M. S. TILNEY and G. M. GUILD, 1995 F actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J. Cell Biol. 130: 629-638.
71. TILNEY, L. G., P. S. CONNELLY, K. A. VRANICH, M. K. SHAW and G. M. GUILD, 2000 Actin filaments and microtubules play different roles during bristle elongation in Drosophila. J. Cell Sci. 113(Pt 7): 1255-1265.
72. TREE, D. R. P., J. M. SHULMAN, R. ROUSSET, M. P. SCOTT, D. GUBB et al., 2002 Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109: 1-11.
73. TURNER, C. M., and P. N. ADLER, 1998 Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila. Mech. Dev. 70: 181-192.
74. USUI, T., Y. SHIMA, Y. SHIMADA, S. HIRANO, R. W. BURGESS et al., 1999 Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98: 585-595.
75. VERHEYEN, E. M., and L. COOLEY, 1994 Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120: 717-728.
76. VOEGTLI, W. C., A. Y. MADRONA and D. K. WILSON, 2003 The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J. Biol. Chem. 278: 34373-34379.
77. WAHLSTROM, G., M. VARTIAINEN, L. YAMAMOTO, P. K. MATTILA, P. LAPPALAINEN et al., 2001 Twinfilin is required for actin-dependent developmental processes in Drosophila. J. Cell Biol. 155: 787-796.
78. WELCH, M. D., and R. D. MULLINS, 2002 Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18: 247-288.
79. WONG, L. L., and P. N. ADLER, 1993 Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123: 209-221.
80. YANG, N., O. HIGUCHI, K. OHASHI, K. NAGATA, A. WADA et al., 1998 Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393: 809-812.