Crossveinless-c is a RhoGAP required for actin reorganization during morphogenesis

Development

Volumn 132, Issue 10, 2005, Pages 2389-2400

  Denholm, Barry ^a   Brown, Stephen ^a,b   Ray, Robert P ^c   Ruiz Gómez, Mar ^d   Skaer, Helen ^a   Hombría, James Castelli Gair ^a,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Actin cytoskeleton; Convergent extension; Crossveinless c; Drosophila; Morphogenesis; RhoGAP; RhoGTPase

Indexed keywords

ACTIN; CROSSVEINLESS C PROTEIN; RAC1 PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CYTOSKELETON; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE CONTROL; GENE INTERACTION; GENE ISOLATION; GENE MUTATION; GENE OVEREXPRESSION; MALPIGHIAN TUBULE; MOLECULAR DYNAMICS; MORPHOGENESIS; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

ACTINS; ALLELES; AMINO ACID SEQUENCE; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; GENE COMPONENTS; GTPASE-ACTIVATING PROTEINS; IMMUNOHISTOCHEMISTRY; MALPIGHIAN TUBULES; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTAGENESIS; POLYMORPHISM, SINGLE NUCLEOTIDE; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; SUBSTRATE SPECIFICITY; WING;

ANIMALIA;

EID: 21044459213     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01829     Document Type: Article

References (70)

1. Aviv, T., Lin, Z., Lau, S., Rendl, L. M., Sicheri, F. and Smibert, C. A. (2003). The RNA-binding SAM domain of Smaug defines a new family of post-transcriptional regulators. Nat. Struct. Biol. 10, 614-621.
2. Barrera, E. N., Poveda, J. A., Gonzalez-Ros, J. M. and Neira, J. L. (2003). Binding of the C-terminal sterile alpha motif (SAM) domain of human p73 to lipid membranes. J. Biol. Chem. 278, 46878-46885.
3. Barrett, T., Xiao, B., Dodson, E. J., Dodson, G., Ludbrook, S. B., Nurmahomed, K., Gamblin, S. J., Musacchio, A., Smerdon, S. J. and Eccleston, J. F. (1997). The structure of the GTPase-activating domain from p50rhoGAP. Nature 385, 458-461.
4. Bernards, A. (2003). GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim. Biophys. Acta. 1603, 47-82.
5. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
6. Bienz, M. (1994). Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet. 10, 22-26.
7. Billuart, P., Winter, C. G., Maresh, A., Zhao, X. and Luo, L. (2001). Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 107, 195-207.
8. Boettner, B. and van Aelst, L. (2002). The role of Rho GTPases in disease development. Gene 286, 155-174.
9. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
10. Bretscher, A., Edwards, K. and Fehon, R. G. (2002). ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599.
11. Ching, Y. P., Wong, C. M., Chan, S. F., Leung, T. H., Ng, D. C., Jin, D. Y. and Ng, I. O. (2003). Deleted in liver cancer (DLC) 2 encodes a RhoGAP protein with growth suppressor function and is underexpressed in hepatocellular carcinoma. J. Biol. Chem. 278, 10824-10830.
12. Chou, T. B. and Perrimon, N. (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
13. Clark, B. J., Wells, J., King, S. R. and Stocco, D. M. (1994). The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 269, 28314-28322.
14. Conley, C. A., Silburn, R., Singer, M. A., Ralston, A., Rohwer-Nutter, D., Olson, D. J., Gelbart, W. and Blair, S. S. (2000). Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127, 3947-3959.
15. Denholm, B. and Skaer, H. (2004). Development of Malpighian tubules in Insects. In Comprehensive Molecular Insect Science, Vol. 2 (ed. L. I. Gilbert, S. Gill and K. Iatrou), pp. 291-314. Oxford, UK: Elsevier.
16. Diaz-Benjumea, F. J. and Garcia-Bellido, A. (1990). Genetic analysis of the wing vein pattern of Drosophila. Roux's Arch. Develop. Biol. 198, 336-354.
17. Dutta, D., Bloor, J. W., Ruiz-Gomez, M., VijayRaghavan, K. and Kiehart, D. P. (2002). Real-time imaging of morphogenetic movements in Drosophila using Gal4-UAS-driven expression of GFP fused to the actin-binding domain of moesin. Genesis 34, 146-151.
18. Edmondson, M. (1952). New mutants report. Dros. Inf. Serv. 26, 60-62.
19. Etienne-Manneville, S. and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629-635.
20. Gautreau, A., Louvard, D. and Arpin, M. (2002). ERM proteins and NF2 tumor suppressor: the Yin and Yang of cortical actin organization and cell growth signaling. Curr. Opin. Cell Biol. 14, 104-109.
21. Green, J. B., Gardner, C. D., Wharton, R. P. and Aggarwal, A. K. (2003). RNA recognition via the SAM domain of Smaug. Mol. Cell 11, 1537-1548.
22. Guichard, A., Bergeret, E. and Griffin-Shea, R. (1997). Overexpression of RnRacGAP in Drosophila melanogaster deregulates cytoskeletal organisation in cellularising embryos and induces discrete imaginal phenotypes. Mech. Dev. 61, 49-62.
23. Hakeda-Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M., Nardine, T., Luo, L. and Dickson, B. J. (2002). Rac function and regulation during Drosophila development. Nature 416, 438-442.
24. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
25. Hanada, K., Kumagai, K., Yasuda, S., Miura, Y., Kawano, M., Fukasawa, M. and Nishijima, M. (2003). Molecular machinery for non-vesicular trafficking of ceramide. Nature 426, 803-809.
26. Hu, N. and Castelli-Gair, J. (1999). Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Dev. Biol. 214, 197-210.
27. Hummel, T., Leifker, K. and Klambt, C. (2000). The Drosophila HEM2/NAP1 homolog KETTE controls axonal pathfinding and cytoskeletal organization. Genes Dev. 14, 863-873.
28. Hussain, N. K., Jenna, S., Glogauer, M., Quinn, C. C., Wasiak, S., Guipponi, M., Antonarakis, S. E., Kay, B. K., Stossel, T. P., Lamarche-Vane, N. et al. (2001). Endocytic protein intersectin-1 regulates actin assembly via Cdc42 and N-WASP. Nat. Cell Biol. 3, 927-932.
29. Jaffe, A. B. and Hall, A. (2002). Rho GTPases in transformation and metastasis. Adv. Cancer Res. 84, 57-80.
30. Kaltschmidt, J. A., Lawrence, N., Morel, V., Balayo, T., Fernandez, B. G., Pelissier, A., Jacinto, A. and Martinez Arias, A. (2002). Planar polarity and actin dynamics in the epidermis of Drosophila. Nat. Cell Biol. 4, 937-944.
31. Kim, C. A. and Bowie, J. U. (2003). SAM domains: uniform structure, diversity of function. Trends Biochem. Sci. 28, 625-628.
32. Kitamura, T., Kitamura, Y., Yonezawa, K., Totty, N. E., Gout, I., Hara, K., Waterfield, M. D., Sakaue, M., Ogawa, W. and Kasuga, M. (1996). Molecular cloning of p125Nap1, a protein that associates with an SH3 domain of Nck. Biochem. Biophys. Res. Commun. 219, 509-514.
33. 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.
34. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
35. Leonard, D. A., Lin, R., Cerione, R. A. and Manor, D. (1998). Biochemical studies of the mechanism of action of the Cdc42-GTPase-activating protein. J. Biol. Chem. 273, 16210-16215.
36. Lundström, A., Gallio, M., Englund, C., Steneberg, P., Hemphala, J., Aspenstrom, P., Keleman, K., Falileeva, L., Dickson, B. J. and Samakovlis, C. (2004). Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev. 18, 2161-2171.
37. Martin, S. G., Dobi, K. C. and St Johnston, D. (2001). A rapid method to map mutations in Drosophila. Genome Biol. 2, RESEARCH0036.
38. Nagaraja, G. M. and Kandpal, R. P. (2004). Chromosome 13q12 encoded Rho GTPase activating protein suppresses growth of breast carcinoma cells, and yeast two-hybrid screen shows its interaction with several proteins. Biochem. Biophys. Res. Commun. 313, 654-665.
39. Nassar, N., Hoffman, G. R., Manor, D., Clardy, J. C. and Cerione, R. A. (1998). Structures of Cdc42 bound to the active and catalytically compromised forms of Cdc42GAP. Nat. Struct. Biol. 5, 1047-1052.
40. Nimnual, A. S., Taylor, L. J. and Bar-Sagi, D. (2003). Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5, 236-241.
41. Nobes, C. D. and Hall, A. (1995a). Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23, 456-459.
42. Nobes, C. D. and Hall, A. (1995b). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
43. Peck, J., Douglas, G. T., Wu, C. H. and Burbelo, P. D. (2002). Human RhoGAP domain-containing proteins: structure, function and evolutionary relationships. FEBS Lett. 528, 27-34.
44. Polesello, C. and Payre, F. (2004). Small is beautiful: what flies tell us about ERM protein function in development. Trends Cell Biol. 14, 294-302.
45. Raymond, K., Bergeret, E., Dagher, M. C., Breton, R., Griffin-Shea, R. and Fauvarque, M. O. (2001). The Rac GTPase-activating protein RotundRacGAP interferes with Drac1 and Dcdc42 signalling in Drosophila melanogaster. J. Biol. Chem. 276, 35909-35916.
46. Rittinger, K., Walker, P. A., Eccleston, J. F., Nurmahomed, K., Owen, D., Lane, E., Gamblin, S. J. and Smerdon, S. J. (1997a). Crystal structure of a small G protein in complex with the GTPase-activating protein rhoGAP. Nature 388, 693-697.
47. Rittinger, K., Walker, P. A., Eccleston, J. F., Smerdon, S. J. and Gamblin, S. J. (1997b). Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389, 758-762.
48. Romanowski, M. J., Soccio, R. E., Breslow, J. L. and Burley, S. K. (2002). Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StAR-related lipid transfer domain. Proc. Natl. Acad. Sci. USA 99, 6949-6954.
49. Sagnier, T., Grienenberger, A., Mariol, M., Berenger, H., Pradel, J. and Graba, Y. (2000). Dynamic expression of d-CdGAPr, a novel Drosophila melanogaster gene encoding a GTPase activating protein. Mech. Dev. 94, 267-270.
50. Sander, E. E., ten Klooster, J. P., van Delft, S., van der Kammen, R. A. and Collard, J. G. (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009-1022.
51. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F. and Wittinghofer, A. (1997). The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338.
52. Schenck, A., Bardoni, B., Langmann, C., Harden, N., Mandel, J. L. and Giangrande, A. (2003). CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38, 887-898.
53. Schultz, J., Ponting, C. P., Hofmann, K. and Bork, P. (1997). SAM as a protein interaction domain involved in developmental regulation. Protein Sci. 6, 249-253.
54. Scita, G., Nordstrom, J., Carbone, R., Tenca, P., Giardina, G., Gutkind, S., Bjarnegard, M., Betsholtz, C. and di Fiore, P. P. (1999). EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401, 290-293.
55. Sekimata, M., Kabuyama, Y., Emori, Y. and Homma, Y. (1999). Morphological changes and detachment of adherent cells induced by p122, a GTPase-activating protein for Rho. J. Biol. Chem. 274, 17757-17762.
56. Settleman, J. (2001). Rac 'n Rho: the music that shapes a developing embryo. Dev. Cell 1, 321-331.
57. Skaer, H. (1989). Cell division in Malpighian tubule development in D. melanogaster is regulated by a single tip cell. Nature 342, 566-569.
58. Soderling, S. H., Binns, K. L., Wayman, G. A., Davee, S. M., Ong, S. H., Pawson, T. and Scott, J. D. (2002). The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat. Cell Biol. 4, 970-975.
59. Sotillos, S. and Campuzano, S. (2000). DRacGAP, a novel Drosophila gene, inhibits EGFR/Ras signalling in the developing imaginal wing disc. Development 127, 5427-5438.
60. Soto, M. C., Qadota, H., Kasuya, K., Inoue, M., Tsuboi, D., Mello, C. C. and Kaibuchi, K. (2002). The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev. 16, 620-632.
61. Speck, O., Hughes, S. C., Noren, N. K., Kulikauskas, R. M. and Fehon, R. G. (2003). Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87.
62. Spradling, A. C., Stern, D., Beaton, A., Rhem, E. J., Laverty, T., Mozden, N., Misra, S. and Rubin, G. M. (1999). The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153, 135-177.
63. Stern, C. (1934). New mutants report. Dros. Inf. Serv. 1, 35-36.
64. Sudarsan, V., Pasalodos-Sanchez, S., Wan, S., Gampel, A. and Skaer, H. (2002). A genetic hierarchy establishes mitogenic signalling and mitotic competence in the renal tubules of Drosophila. Development 129, 935-944.
65. Sugawara, T., Holt, J. A., Driscoll, D., Strauss, J. F., 3rd, Lin, D., Miller, W. L., Patterson, D., Clancy, K. P., Hart, I. M., Clark, B. J. et al. (1995). Human steroidogenic acute regulatory protein: functional activity in COS-1 cells, tissue-specific expression, and mapping of the structural gene to 8p11.2 and a pseudogene to chromosome 13. Proc. Natl. Acad. Sci. USA 92, 4778-4782.
66. Tsuboi, D., Qadota, H., Kasuya, K., Amano, M. and Kaibuchi, K. (2002). Isolation of the interacting molecules with GEX-3 by a novel functional screening. Biochem. Biophys. Res. Commun. 292, 697-701.
67. Tsujishita, Y. and Hurley, J. H. (2000). Structure and lipid transport mechanism of a StAR-related domain. Nat. Struct. Biol. 7, 408-414.
68. Van Aelst, L. and Symons, M. (2002). Role of Rho family GTPases in epithelial morphogenesis. Genes Dev. 16, 1032-1054.
69. Welch, M. D. and Mullins, R. D. (2002). Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18, 247-288.
70. Zallen, J. A., Cohen, Y., Hudson, A. M., Cooley, L., Wieschaus, E. and Schejter, E. D. (2002). SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J. Cell Biol. 156, 689-701.