The BNIP-2 and Cdc42GAP Homology (BCH) domain of p50RhoGAP/Cdc42GAP sequesters RhoA from inactivation by the adjacent GTPase-activating protein domain

Molecular Biology of the Cell

Volumn 21, Issue 18, 2010, Pages 3232-3246

  Zhou, Yi Ting ^a,b   Chew, Li Li ^a,b   Lin, Sheng Cai ^c   Low, Boon Chuan ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c XIAMEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GROWTH ASSOCIATED PROTEIN; PROTEIN BNIP2; PROTEIN CDC42; PROTEIN P50; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; ENZYME INACTIVATION; FEMALE; GENE DELETION; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REGULATORY MECHANISM; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BINDING SITES; GTPASE-ACTIVATING PROTEINS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HEK293 CELLS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RHOA GTP-BINDING PROTEIN; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

MAMMALIA; SCHIZOSACCHAROMYCES POMBE;

EID: 77956704550     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E09-05-0408     Document Type: Article

References (62)

1. Aghazadeh, B., Lowry, W. E., Huang, X. Y., and Rosen, M. K. (2000). Structural basis for relief of autoinhibition of the Dbl homology domain of protooncogene Vav by tyrosine phosphorylation. Cell 102, 625-633.
2. Barfod, E. T., Zheng, Y., Kuang, W. J., Hart, M. J., Evans, T., Cerione, R. A., and Ashkenazi, A. (1993). Cloning and expression of a human CDC42 GTPase-activating protein reveals a functional SH3-binding domain. J. Biol. Chem. 268, 26059-26062.
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., and Settleman, J. (2005). GAPs in growth factor signalling. Growth Factors 23, 143-149.
5. Bernards, A., and Settleman, J. (2007). GEFs in growth factor signaling. Growth Factors 25, 355-361.
6. Bi, F., Debreceni, B., Zhu, K., Salani, B., Eva, A., and Zheng, Y. (2001). Autoinhibition mechanism of proto-Dbl. Mol. Cell. Biol. 21, 1463-1474.
7. Bos, J. L., Rehmann, H., and Wittinghofer, A. (2007). GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865-877.
8. Brill, S., Li, S., Lyman, C. W., Church, D. M., Wasmuth, J. J., Weissbach, L., Bernards, A., and Snijders, A. J. (1996). The Ras GTPase-activating-protein-related human protein IQGAP2 harbors a potential actin binding domain and interacts with calmodulin and Rho family GTPases. Mol. Cell. Biol. 16, 4869-4878.
9. Buschdorf, J. P., Chew, L. L., Zhang, B., Cao, Q., Liang, F. Y., Liou, Y. C., Zhou, Y. T., and Low, B. C. (2006). Brain-specific BNIP-2-homology protein Caytaxin relocalises glutaminase to neurite terminals and reduces glutamate levels. J. Cell Sci. 119, 3337-3350.
10. Buschdorf, J. P., Chew, L. L., Soh, U. J., Liou, Y. C., and Low, B. C. (2008). Nerve growth factor stimulates interaction of Cayman ataxia protein BNIPH/Caytaxin with peptidyl-prolyl isomerase Pin1 in differentiating neurons. PLoS ONE 3, e2686.
11. Bustos, R. I., Forget, M. A., Settleman, J. E., and Hansen, S. H. (2008). Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr. Biol. 18, 1606-1611.
12. Dovas, A., and Couchman, J. R. (2005). RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390, 1-9.
13. Drugan, J. K., Rogers-Graham, K., Gilmer, T., Campbell, S., and Clark, G. J. (2000). The Ras/p120 GTPase-activating protein (GAP) interaction is regulated by the p120 GAP pleckstrin homology domain. J. Biol. Chem. 275, 35021-35027.
14. Etienne-Manneville, S., and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629-635.
15. Fauchereau, F., Herbrand, U., Chafey, P., Eberth, A., Koulakoff, A., Vinet, M. C., Ahmadian, M. R., Chelly, J., and Billuart, P. (2003). The RhoGAP activity of OPHN1, a new F-actin-binding protein, is negatively controlled by its amino-terminal domain. Mol. Cell Neurosci. 23, 574-586.
16. Gibson, R. M., Gandhi, P. N., Tong, X., Miyoshi, J., Takai, Y., Konieczkowski, M., Sedor, J. R., Wilson-Delfosse, A. L. (2004). An activating mutant of Rac1 that fails to interact with Rho GDP-dissociation inhibitor stimulates membrane ruffling in mammalian cells. Biochem. J. 378, 409-419. (Pubitemid 38367232)
17. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
18. Hancock, J. F., and Hall, A. (1993). A novel role for RhoGDI as an inhibitor of GAP proteins. EMBO J. 12, 1915-1921.
19. Hart, M. J., Jiang, X., Kozasa, T., Roscoe, W., Singer, W. D., Gilman, A. G., Sternweis, P. C., and Bollag, G. (1998). Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13. Science 280, 2112-2114.
20. Hatjiharissi, E. et al. (2007). Proteomic analysis of waldenstrom macroglobulinemia. Cancer Res. 67, 3777-3784.
21. Jaffe, A. B., and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269.
22. Jenna, S., Hussain, N. K., Danek, E. I., Triki, I., Wasiak, S., McPherson, P. S., and Lamarche-Vane, N. (2002). The activity of the GTPase-activating protein CdGAP is regulated by the endocytic protein intersectin. J. Biol. Chem. 277, 6366-6373.
23. Johnstone, C. N., Castellvi-Bel, S., Chang, L. M., Bessa, X., Nakagawa, H., Harada, H., Sung, R. K., Pique, J. M., Castells, A., and Rustgi, A. K. (2004). ARHGAP8 is a novel member of the RHOGAP family related to ARHGAP1/CDC42GAP/p50RHOGAP: mutation and expression analyses in colorectal and breast cancers. Gene 336, 59-71.
24. Kang, J. S., Bae, G. U., Yi, M. J., Yang, Y. J., Oh, J. E., Takaesu, G., Zhou, Y. T., Low, B. C., and Krauss, R. S. (2008). A Cdo-Bnip-2-Cdc42 signaling pathway regulates p38alpha/beta MAPK activity and myogenic differentiation. J. Cell Biol. 182, 497-507.
25. Kim, J. E., Billadeau, D. D., and Chen, J. (2005). The tandem BRCT domains of Ect2 are required for both negative and positive regulation of Ect2 in cytokinesis. J. Biol. Chem. 280, 5733-5739.
26. Lancaster, C. A., Taylor-Harris, P. M., Self, A. J., Brill, S., van Erp, H. E., and Hall, A. (1994). Characterization of rhoGAP. A GTPase-activating protein for rho-related small GTPases. J. Biol. Chem. 269, 1137-1142.
27. 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.
28. Ligeti, E., and Settleman, J. (2006). Regulation of RhoGAP specificity by phospholipids and prenylation. Methods Enzymol. 406, 104-117.
29. Ligeti, E., Dagher, M. C., Hernandez, S. E., Koleske, A. J., and Settleman, J. (2004). Phospholipids can switch the GTPase substrate preference of a GTPase-activating protein. J. Biol. Chem. 279, 5055-5508.
30. Low, B. C., Lim, Y. P., Lim, J., Wong, E. S., and Guy, G. R. (1999). Tyrosine phosphorylation of the Bcl-2-associated protein BNIP-2 by fibroblast growth factor receptor-1 prevents its binding to Cdc42GAP and Cdc42. J. Biol. Chem. 274, 33123-33130.
31. Low, B. C., Seow, K. T., and Guy, G. R. (2000). The BNIP-2 and Cdc42GAP homology domain of BNIP-2 mediates its homophilic association and heterophilic interaction with Cdc42GAP. J. Biol. Chem. 275, 37742-37751.
32. Lua, B. L., and Low, B. C. (2005). Activation of EGF receptor endocytosis and ERK1/2 signaling by BPGAP1 requires direct interaction with EEN/endophilin II and a functional RhoGAP domain. J. Cell Sci. 118, 2707-2721.
33. Moon, S. Y., Zang, H., and Zheng, Y. (2003). Characterization of a brain-specific Rho GTPase-activating protein, p200RhoGAP. J. Biol. Chem. 278, 4151-4159.
34. Moon, S. Y., and Zheng, Y. (2003). Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13-22.
35. Moskwa, P., Paclet, M. H., Dagher, M. C., and Ligeti, E. (2005). Autoinhibition of p50 Rho GTPase-activating protein (GAP) is released by prenylated small GTPases. J. Biol. Chem. 280, 6716-6720.
36. Mousley, C. J., Tyeryar, K. R., Vincent-Pope, P., Bankaitis, V. A. (2007) The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking. Biochim. Biophys. Acta 1771, 727-736.
37. Munter, S., Way, M. and Frischknecht, F. (2006). Signaling during pathogen infection. Sci. STKE 2006, re5.
38. 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.
39. Nomanbhoy, T. K., and Cerione, R. A. (1996). Characterization of the interaction between RhoGDI and Cdc42Hs using fluorescence spectroscopy. J. Biol. Chem. 271, 10004-10009.
40. Ridley, A. J., Self, A. J., Kasmi, F., Paterson, H. F., Hall, A., Marshall, C. J., and Ellis, C. (1993). rho family GTPase activating proteins p190, bcr and rhoGAP show distinct specificities in vitro and in vivo. EMBO J. 12, 5151-5160.
41. Rittinger, K., Walker, P. A., Eccleston, J. F., Smerdon, S. J., and Gamblin, S. J. (1997). Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389, 758-762.
42. Sahai, E., and Marshall, C. J. (2002). RHO-GTPases and cancer. Nat. Rev. Cancer 2, 133-142.
43. Schaaf, G. et al. (2008). Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol. Cell 29, 191-206.
44. Shang, X., Zhou, Y. T., and Low, B. C. (2003). Concerted regulation of cell dynamics by BNIP-2 and Cdc42GAP homology/Sec14p-like, proline-rich, and GTPase-activating protein domains of a novel Rho GTPase-activating protein, BPGAP1. J. Biol. Chem. 278, 45903-45914.
45. Shen, Y. et al. (2008). Nudel binds Cdc42GAP to modulate Cdc42 activity at the leading edge of migrating cells. Dev. Cell 14, 342-353.
46. Sirokmány, G., Szidonya, L., Kaldi, K., Gaborik, Z., Ligeti, E., and Geiszt, M. (2006). Sec14 homology domain targets p50RhoGAP to endosomes and provides a link between Rab and Rho GTPases. J. Biol. Chem. 281, 6096-6105.
47. Soh, U. J., and Low, B. C. (2008). BNIP2 extra long inhibits RhoA and cellular transformation by Lbc RhoGEF via its BCH domain. J. Cell Sci. 121, 1739-1749.
48. Song, J. Y., Lee, J. K., Lee, N. W., Jung, H. H., Kim, S. H., and Lee, K. W. (2008). Microarray analysis of normal cervix, carcinoma in situ, and invasive cervical cancer: identification of candidate genes in pathogenesis of invasion in cervical cancer. Int. J. Gynecol. Cancer 18, 1051-1059.
49. Szczur, K., Xu, H., Atkinson, S., Zheng, Y., Filippi, M. D. (2006). Rho GTPase CDC42 regulates directionality and random movement via distinct MAPK pathways in neutrophils. Blood 108, 4205-4213.
50. Tcherkezian, J., and Lamarche-Vane, N. (2007). Current knowledge of the large RhoGAP family of proteins. Biol. Cell 99, 67-86.
51. Tcherkezian, J., Triki, I., Stenne, R., Danek, E. I., and Lamarche-Vane, N. (2006). The human orthologue of CdGAP is a phosphoprotein and a GTPase-activating protein for Cdc42 and Rac1 but not RhoA. Biol. Cell 98, 445-456.
52. Vega, F. M., and Ridley, A. J. (2008). Rho GTPases in cancer cell biology. FEBS Lett. 582, 2093-2101.
53. Wang, L., Yang, L., Burns, K., Kuan, C. Y., and Zheng, Y. (2005). Cdc42GAP regulates c-Jun N-terminal kinase (JNK)-mediated apoptosis and cell number during mammalian perinatal growth. Proc. Natl. Acad. Sci. USA 102, 13484-13489.
54. Wang, L., Yang, L., Debidda, M., Witte, D., and Zheng, Y. (2007). Cdc42 GTPase-activating protein deficiency promotes genomic instability and premature aging-like phenotypes. Proc. Natl. Acad. Sci. USA 104, 1248-1253.
55. Wang, L., Yang, L., Filippi, M. D., Williams, D. A., and Zheng, Y. (2006). Genetic deletion of Cdc42GAP reveals a role of Cdc42 in erythropoiesis and hematopoietic stem/progenitor cell survival, adhesion, and engraftment. Blood 107, 98-105.
56. Xia, C., Ma, W., Stafford, L. J., Liu, C., Gong, L., Martin, J. F., and Liu, M. (2003). GGAPs, a new family of bifunctional GTP-binding and GTPase-activating proteins. Mol. Cell. Biol. 23, 2476-2488.
57. Xu, Y., Hortsman, H., Seet, L., Wong, S. H., and Hong, W. (2001). SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P. Nat. Cell Biol. 3, 658-666.
58. Yohe, M. E., Rossman, K. L., Gardner, O. S., Karnoub, A. E., Snyder, J. T., Gershburg, S., Graves, L. M., Der, C. J., and Sondek, J. (2007). Auto-inhibition of the Dbl family protein Tim by an N-terminal helical motif. J. Biol. Chem. 282, 13813-13823.
59. Zalcman, G., Closson, V., Camonis, J., Honore, N., Rousseau-Merck, M. F., Tavitian, A., and Olofsson, B. (1996). RhoGDI-3 is a new GDP dissociation inhibitor (GDI): identification of a non-cytosolic GDI protein interacting with the small GTP-binding proteins RhoB and RhoG. J. Biol. Chem. 271, 30366-30374.
60. Zhou, Y. T., Soh, U. J., Shang, X., Guy, G. R., and Low, B. C. (2002). The BNIP-2 and Cdc42GAP homology/Sec14p-like domain of BNIP-Sα is a novel apoptosis-inducing sequence. J. Biol. Chem. 277, 7483-7492.
61. Zhou, Y. T., Guy, G. R., and Low, B. C. (2005). BNIP-2 induces cell elongation and membrane protrusions by interacting with Cdc42 via a unique Cdc42-binding motif within its BNIP-2 and Cdc42GAP homology domain. Exp. Cell Res. 303, 263-274.
62. Zhou, Y. T., Guy, G. R., and Low, B. C. (2006). BNIP-Salpha induces cell rounding and apoptosis by displacing p50RhoGAP and facilitating RhoA activation via its unique motifs in the BNIP-2 and Cdc42GAP homology domain. Oncogene 25, 2393-2408.