The Drosophila CD2AP/CIN85 orthologue Cindr regulates junctions and cytoskeleton dynamics during tissue patterning

Journal of Cell Biology

Volumn 180, Issue 6, 2008, Pages 1191-1204

  Johnson, Ruth I ^a   Seppa, Midori J ^b   Cagan, Ross L ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD2 ASSOCIATED PROTEIN; UVOMORULIN;

ARTICLE; CELL ADHESION; CELL MOTION; CELL SURFACE; CONTROLLED STUDY; CYTOSKELETON; DNA MODIFICATION; DROSOPHILA MELANOGASTER; EPITHELIUM; IMMUNOCYTOCHEMISTRY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA CELL;

ACTIN CAPPING PROTEINS; ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CADHERINS; CELL ADHESION; CELL ADHESION MOLECULES, NEURONAL; CYTOSKELETAL PROTEINS; CYTOSKELETON; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPITHELIUM; EYE; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERCELLULAR JUNCTIONS; MICROFILAMENT PROTEINS;

DROSOPHILA MELANOGASTER;

EID: 41549103330     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200706108     Document Type: Article

References (60)

1. Bao, S., and R. Cagan. 2005. Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev. Cell. 8:925-935.
2. Bao, S., and R. Cagan. 2006. Fast cloning inverted repeats for RNA interference. RNA. 12:2020-2024.
3. Bogler, O., F.B. Furnari, A. Kindler-Roehrborn, V.W. Sykes, R. Yung, H.J. Huang, and W.K. Cavenee. 2000. SETA: a novel SH3 domain-containing adapter molecule associated with malignancy in astrocytes. Neuro. Oncol. 2:6-15.
4. Brand, A.H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:401-415.
5. Brett, T.J., L.M. Traub, and D.H. Fremont. 2002. Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure. 10:797-809.
6. Bruck, S., T.B. Huber, R.J. Ingham, K. Kim, H. Niederstrasser, P.M. Allen, T. Pawson, J.A. Cooper, and A.S. Shaw. 2006. Identification of a novel inhibitory actin-capping protein binding motif in CD2-associated protein. J. Biol. Chem. 281:19196-19203.
7. Chen, B., S.C. Borinstein, J. Gillis, V.W. Sykes, and O. Bogler. 2000. The glioma-associated protein SETA interacts with AIP1/Alix and ALG-2 and modulates apoptosis in astrocytes. J. Biol. Chem. 275:19275-19281.
8. Cordero, J.B., D.E. Larson, C.R. Craig, R. Hays, and R. Cagan. 2007. Dynamic decapentaplegic signaling regulates patterning and adhesion in the Drosophila pupal retina. Development. 134:1861-1871.
9. Cormont, M., I. Meton, M. Mari, P. Monzo, F. Keslair, C. Gaskin, T.E. McGraw, and Y. Le Marchand-Brustel. 2 003. CD2AP/CMS regulates endosome morphology and traffic to the degradative pathway through its interaction with Rab4 and c-Cbl. Traffic. 4:97-112.
10. Delalle, I., C.M. Pfleger, E. Buff, P. Lueras, and I.K. Hariharan. 2005. Mutations in the Drosophila orthologs of the F-actin capping protein alpha- and beta-subunits cause actin accumulation and subsequent retinal degeneration. Genetics. 171:1757-1765.
11. Dikic, I. 2003. Mechanisms controlling EGF receptor endocytosis and degradation. Biochem. Soc. Trans. 31:1178-1181.
12. Dikic, I., and S. Giordano. 2003. Negative receptor signalling. Curr. Opin. Cell Biol. 15:128-135.
13. Dustin, M.L., M.W. Olszowy, A.D. Holdorf, J. Li, S. Bromley, N. Desai, P. Widder, F. Rosenberger, P.A. van der Merwe, P.M. Allen, and A.S. Shaw. 1998. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell. 94:667-677.
14. 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.
15. Gaidos, G., S. Soni, D.J. Oswald, P.A. Toselli, and K.H. Kirsch. 2007. Structure and function analysis of the CMS/CIN85 protein family identifies actin-bundling properties and heterotypic-complex formation. J. Cell Sci. 120:2366-2377.
16. Gauthier, N.C., P. Monzo, T. Gonzalez, A. Doye, A. Oldani, P. Gounon, V. Ricci, M. Cormont, and P. Boquet. 2007. Early endosomes associated with dynamic F-actin structures are required for late trafficking of H. pylori VacA toxin. J. Cell Biol. 177:343-354.
17. Gout, I., G. Middleton, J. Adu, N.N. Ninkina, L.B. Drobot, V. Filonenko, G. Matsuka, A.M. Davies, M. Waterfield, and V.L. Buchman. 2000. Negative regulation of PI 3-kinase by Ruk, a novel adaptor protein. EMBO J. 19:4015-4025.
18. Grzeschik, N.A., and E. Knust. 2005. IrreC/rst-mediated cell sorting during Drosophila pupal eye development depends on proper localisation of DE-cadherin. Development. 132:2035-2045.
19. Guild, G.M., P.S. Connelly, L. Ruggiero, K.A. Vranich, and L.G. Tilney. 2003. Long continuous actin bundles in Drosophila bristles are constructed by overlapping short filaments. J. Cell Biol. 162:1069-1077.
20. Hall, A. 2005. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33:891-895.
21. 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.
22. 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.
23. Huber, T.B., and T. Benzing. 2005. The slit diaphragm: a signaling platform to regulate podocyte function. Curr. Opin. Nephrol. Hypertens. 14: 211-216.
24. Hutchings, N.J., N. Clarkson, R. Chalkley, A.N. Barclay, and M.H. Brown. 2003. Linking the T cell surface protein CD2 to the actin-capping protein CAPZ via CMS and CIN85. J. Biol. Chem. 278:22396-22403.
25. Isenberg, G., U. Aebi, and T.D. Pollard. 1980. An actin-binding protein from Acanthamoeba regulates actin filament polymerization and interactions. Nature. 288:455-459.
26. Kirsch, K.H., M.M. Georgescu, T. Shishido, W.Y. Langdon, R.B. Birge, and H. Hanafusa. 2001. The adapter type protein CMS/CD2AP binds to the protooncogenic protein c-Cbl through a tyrosine phosphorylation-regulated Src homology 3 domain interaction. J. Biol. Chem. 276:4957-4963.
27. Kowanetz, K., J. Terzic, and I. Dikic. 2003. Dab2 links CIN85 with clathrin-mediated receptor internalization. FEBS Lett. 554:81-87.
28. Kurakin, A.V., S. Wu, and D.E. Bredesen. 2003. Atypical recognition consensus of CIN85/SETA/Ruk SH3 domains revealed by target-assisted iterative screening. J. Biol. Chem. 278:34102-34109.
29. Larson, D.E., Z. Liberman, and R.L. Cagan. 2008. Cellular behavior in the developing Drosophila pupal retina. Mech. Dev. 125:223-232.
30. Lehtonen, S., A. Ora, V.M. Olkkonen, L. Geng, M. Zerial, S. Somlo, and E. Lehtonen. 2000. In vivo interaction of the adapter protein CD2-associated protein with the type 2 polycystic kidney disease protein, polycystin-2. J. Biol. Chem. 275:32888-32893.
31. Lehtonen, S., F. Zhao, and E. Lehtonen. 2002. CD2-associated protein directly interacts with the actin cytoskeleton. Am. J. Physiol. Renal Physiol. 283:F734-F743.
32. Lehtonen, S., E. Lehtonen, K. Kudlicka, H. Holthofer, and M.G. Farquhar. 2004. Nephrin forms a complex with adherens junction proteins and CASK in podocytes and in Madin-Darby canine kidney cells expressing nephrin. Am. J. Pathol. 165:923-936.
33. Lynch, D.K., S.C. Winata, R.J. Lyons, W.E. Hughes, G.M. Lehrbach, V. Wasinger, G. Corthals, S. Cordwell, and R.J. Daly. 2003. A Cortactin-CD2- associated protein (CD2AP) complex provides a novel link between epidermal growth factor receptor endocytosis and the actin cytoskeleton. J. Biol. Chem. 278:21805-21813.
34. Mege, R.M., J. Gavard, and M. Lambert. 2006. Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 18:541-548.
35. Miller, D.T., and R.L. Cagan. 1998. Local induction of patterning and programmed cell death in the developing Drosophila retina. Development. 125:2327-2335.
36. Monzo, P., N.C. Gauthier, F. Keslair, A. Loubat, C.M. Field, Y. Le Marchand-Brustel, and M. Cormont. 2005. Clues to CD2-associated protein involvement in cytokinesis. Mol. Biol. Cell. 16:2891-2902.
37. Mustonen, H., A. Lepisto, S. Lehtonen, E. Lehtonen, P. Puolakkainen, and E. Kivilaakso. 2005. CD2AP contributes to cell migration and adhesion in cultured gastric epithelium. Biochem. Biophys. Res. Commun. 332:426-432.
38. Palmen, T., S. Lehtonen, A. Ora, D. Kerjaschki, C. Antignac, E. Lehtonen, and H. Holthofer. 2002. Interaction of endogenous nephrin and CD2-associated protein in mouse epithelial M-1 cell line. J. Am. Soc. Nephrol. 13: 1766-1772.
39. Parker, L., S. Gross, and L. Alphey. 2001. Vectors for the expression of tagged proteins in Drosophila. Biotechniques. 31:1280-1282, 1284, 1286.
40. Patari-Sampo, A., P. Ihalmo, and H. Holthofer. 2006. Molecular basis of the glomerular filtration: nephrin and the emerging protein complex at the podocyte slit diaphragm. Ann. Med. 38:483-492.
41. Peters, I., I. Tossidou, J. Achenbach, R. Woroniecki, M. Mengel, J.K. Park, M. Paschy, K. de Groot, H. Haller, and M. Schiffer. 2006. IGF-binding protein-3 modulates TGF-beta/BMP-signaling in glomerular podocytes. J. Am. Soc. Nephrol. 17:1644-1656.
42. Reiter, C., T. Schimansky, Z. Nie, and K.F. Fischbach. 1996. Reorganization of membrane contacts prior to apoptosis in the Drosophila retina: the role of the IrreC-rst protein. Development. 122:1931-1940.
43. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Seraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032.
44. Schiffer, M., P. Mundel, A.S. Shaw, and E.P. Bottinger. 2004. A novel role for the adaptor molecule CD2-associated protein in transforming growth factor-beta-induced apoptosis. J. Biol. Chem. 279:37004-37012.
45. Schiwek, D., N. Endlich, L. Holzman, H. Holthofer, W. Kriz, and K. Endlich. 2004. Stable expression of nephrin and localization to cell-cell contacts in novel murine podocyte cell lines. Kidney Int. 66:91-101.
46. Schmidt, M.H., B. Chen, L.M. Randazzo, and O. Bogler. 2003. SETA/CIN85/ Ruk and its binding partner AIP1 associate with diverse cytoskeletal elements, including FAKs, and modulate cell adhesion. J. Cell Sci. 116:2845-2855.
47. Schneider, T., C. Reiter, E. Eule, B. Bader, B. Lichte, Z. Nie, T. Schimansky, R.G. Ramos, and K.F. Fischbach. 1995. Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons. Neuron. 15:259-271.
48. Shih, N.Y., J. Li, V. Karpitskii, A. Nguyen, M.L. Dustin, O. Kanagawa, J.H. Miner, and A.S. Shaw. 1999. Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science. 286:312-315.
49. Shih, N.Y., J. Li, R. Cotran, P. Mundel, J.H. Miner, and A.S. Shaw. 2001. CD2AP localizes to the slit diaphragm and binds to nephrin via a novel C-terminal domain. Am. J. Pathol. 159:2303-2308.
50. Siripala, A.D., and M.D. Welch. 2007a. SnapShot: actin regulators I. Cell. 128:626.
51. Siripala, A.D., and M.D. Welch. 2007b. SnapShot: actin regulators II. Cell. 128:1014.
52. Take, H., S. Watanabe, K. Takeda, Z.X. Yu, N. Iwata, and S. Kajigaya. 2000. Cloning and characterization of a novel adaptor protein, CIN85, that interacts with c-Cbl. Biochem. Biophys. Res. Commun. 268:321-328.
53. Tepass, U., and K.P. Harris. 2007. Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol. 17:26-35.
54. Usami, Y., S. Popov, and H.G. Gottlinger. 2007. Potent rescue of human immunodefi ciency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J. Virol. 81:6614-6622.
55. Veraksa, A., A. Bauer, and S. Artavanis-Tsakonas. 2005. Analyzing protein complexes in Drosophila with tandem affinity purification-mass spectrometry. Dev. Dyn. 232:827-834.
56. Welsch, T., N. Endlich, W. Kriz, and K. Endlich. 2001. CD2AP and p130Cas localize to different F-actin structures in podocytes. Am. J. Physiol. Renal Physiol. 281:F769-F777.
57. Welsch, T., N. Endlich, G. Gokce, E. Doroshenko, J.C. Simpson, W. Kriz, A.S. Shaw, and K. Endlich. 2005. Association of CD2AP with dynamic actin on vesicles in podocytes. Am. J. Physiol. Renal Physiol. 289:F1134-F1143.
58. Woroniecki, R.P., M. Schiffer, A.S. Shaw, F.J. Kaskel, and E.P. Bottinger. 2006. Glomerular expression of transforming growth factor-beta (TGF-beta) isoforms in mice lacking CD2-associated protein. Pediatr. Nephrol. 21:333-338.
59. Wu, C., Y.P. Wairkar, C.A. Collins, and A. DiAntonio. 2005. Highwire function at the Drosophila neuromuscular junction: spatial, structural, and temporal requirements. J. Neurosci. 25:9557-9566.
60. Xu, T., and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 117:1223-1237.