The E3 ubiquitin ligase specificity subunit ASB2α targets filamins for proteasomal degradation by interacting with the filamin actin-binding domain

Journal of Cell Science

Volumn 124, Issue 15, 2011, Pages 2631-2641

  Razinia, Ziba ^a   Baldassarre, Massimiliano ^a   Bouaouina, Mohamed ^a   Lamsoul, Isabelle ^b,c   Lutz, Pierre G ^b,c   Calderwood, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

ASB2; Calponin homology domain; Filamin; Ubiquitylation

Indexed keywords

ASB2ALPHA PROTEIN; FILAMIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; UBIQUITINATION;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CHO CELLS; CONTRACTILE PROTEINS; CRICETINAE; CRICETULUS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IMMUNOBLOTTING; MICE; MICROFILAMENT PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; UBIQUITIN-PROTEIN LIGASES;

EID: 79961149492     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.084343     Document Type: Article

References (52)

1. Baldassarre, M., Razinia, Z., Burande, C. F., Lamsoul, I., Lutz, P. G. and Calderwood, D. A. (2009). Filamins regulate cell spreading and initiation of cell migration. PLoS ONE 4, e7830.
2. Bello, N. F., Lamsoul, I., Heuze, M. L., Metais, A., Moreaux, G., Calderwood, D. A., Duprez, D., Moog-Lutz, C. and Lutz, P. G. (2009). The E3 ubiquitin ligase specificity subunit ASB2beta is a novel regulator of muscle differentiation that targets filamin B to proteasomal degradation. Cell Death Differ. 16, 921-932.
3. Boengler, K., Pipp, F., Fernandez, B., Richter, A., Schaper, W. and Deindl, E. (2003). The ankyrin repeat containing SOCS box protein 5, a novel protein associated with arteriogenesis. Biochem. Biophys. Res. Commun. 302, 17-22.
4. Browne, K. A., Johnstone, R. W., Jans, D. A. and Trapani, J. A. (2000). Filamin (280-kDa actin-binding protein) is a caspase substrate and is also cleaved directly by the cytotoxic T lymphocyte protease granzyme B during apoptosis. J. Biol. Chem. 275, 39262-39266.
5. Burande, C. F., Heuze, M. L., Lamsoul, I., Monsarrat, B., Uttenweiler-Joseph, S. and Lutz, P. G. (2009). A label-free quantitative proteomics strategy to identify E3 ubiquitin ligase substrates targeted to proteasome degradation. Mol. Cell. Proteomics 8, 1719-1727.
6. Chen, H. S., Kolahi, K. S. and Mofrad, M. R. (2009). Phosphorylation facilitates the integrin binding of filamin under force. Biophys. J. 97, 3095-3104.
7. Chung, A. S., Guan, Y. J., Yuan, Z. L., Albina, J. E. and Chin, Y. E. (2005). Ankyrin repeat and SOCS box 3 (ASB3) mediates ubiquitination and degradation of tumor necrosis factor receptor II. Mol. Cell. Biol. 25, 4716-4726.
8. Debrincat, M. A., Zhang, J. G., Willson, T. A., Silke, J., Connolly, L. M., Simpson, R. J., Alexander, W. S., Nicola, N. A., Kile, B. T. and Hilton, D. J. (2007). Ankyrin repeat and suppressors of cytokine signaling box protein asb-9 targets creatine kinase B for degradation. J. Biol. Chem. 282, 4728-4737.
9. Diks, S. H., Bink, R. J., van de Water, S., Joore, J., van Rooijen, C., Verbeek, F. J., den Hertog, J., Peppelenbosch, M. P. and Zivkovic, D. (2006). The novel gene asb11: a regulator of the size of the neural progenitor compartment. J. Cell Biol. 174, 581-592.
10. Feng, Y. and Walsh, C. A. (2004). The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat. Cell Biol. 6, 1034-1038.
11. Gimona, M., Djinovic-Carugo, K., Kranewitter, W. J. and Winder, S. J. (2002). Functional plasticity of CH domains. FEBS Lett. 513, 98-106.
12. Glogauer, M., Arora, P., Chou, D., Janmey, P. A., Downey, G. P. and McCulloch, C. A. (1998). The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J. Biol. Chem. 273, 1689-1698.
13. Gorlin, J. B., Yamin, R., Egan, S., Stewart, M., Stossel, T. P., Kwiatkowski, D. J. and Hartwig, J. H. (1990). Human endothelial actin-binding protein (ABP-280, nonmuscle filamin): a molecular leaf spring. J. Cell Biol. 111, 1089-1105.
14. Guibal, F. C., Moog-Lutz, C., Smolewski, P., Di Gioia, Y., Darzynkiewicz, Z., Lutz, P. G. and Cayre, Y. E. (2002). ASB-2 inhibits growth and promotes commitment in myeloid leukemia cells. J. Biol. Chem. 277, 218-224.
15. Hart, A. W., Morgan, J. E., Schneider, J., West, K., McKie, L., Bhattacharya, S., Jackson, I. J. and Cross, S. H. (2006). Cardiac malformations and midline skeletal defects in mice lacking filamin A. Hum. Mol. Genet. 15, 2457-2467.
16. Hartwig, J. H., Tyler, J. and Stossel, T. P. (1980). Actin-binding protein promotes the bipolar and perpendicular branching of actin filaments. J. Cell Biol. 87, 841-848.
17. Heuze, M. L., Guibal, F. C., Banks, C. A., Conaway, J. W., Conaway, R. C., Cayre, Y. E., Benecke, A. and Lutz, P. G. (2005). ASB2 is an Elongin BC-interacting protein that can assemble with Cullin 5 and Rbx1 to reconstitute an E3 ubiquitin ligase complex. J. Biol. Chem. 280, 5468-5474.
18. Heuze, M. L., Lamsoul, I., Baldassarre, M., Lad, Y., Leveque, S., Razinia, Z., Moog-Lutz, C., Calderwood, D. A. and Lutz, P. G. (2008). ASB2 targets filamins A and B to proteasomal degradation. Blood 112, 5130-5140.
19. Ithychanda, S. S., Das, M., Ma, Y. Q., Ding, K., Wang, X., Gupta, S., Wu, C., Plow, E. F. and Qin, J. (2009). Migfilin, a molecular switch in regulation of integrin activation. J. Biol. Chem. 284, 4713-4722.
20. Jay, D., Garcia, E. J., Lara, J. E., Medina, M. A. and de la Luz Ibarra, M. (2000). Determination of a cAMP-dependent protein kinase phosphorylation site in the Cterminal region of human endothelial actin-binding protein. Arch. Biochem. Biophys. 377, 80-84.
21. Kiema, T., Lad, Y., Jiang, P., Oxley, C. L., Baldassarre, M., Wegener, K. L., Campbell, I. D., Ylanne, J. and Calderwood, D. A. (2006). The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell 21, 337-347.
22. Kile, B. T., Metcalf, D., Mifsud, S., DiRago, L., Nicola, N. A., Hilton, D. J. and Alexander, W. S. (2001). Functional analysis of Asb-1 using genetic modification in mice. Mol. Cell. Biol. 21, 6189-6197.
23. Kohroki, J., Fujita, S., Itoh, N., Yamada, Y., Imai, H., Yumoto, N., Nakanishi, T. and Tanaka, K. (2001). ATRA-regulated Asb-2 gene induced in differentiation of HL-60 leukemia cells. FEBS Lett. 505, 223-228.
24. Kohroki, J., Nishiyama, T., Nakamura, T. and Masuho, Y. (2005). ASB proteins interact with Cullin5 and Rbx2 to form E3 ubiquitin ligase complexes. FEBS Lett. 579, 6796-6802.
25. Krakow, D., Robertson, S. P., King, L. M., Morgan, T., Sebald, E. T., Bertolotto, C., Wachsmann-Hogiu, S., Acuna, D., Shapiro, S. S., Takafuta, T. et al. (2004). Mutations in the gene encoding filamin B disrupt vertebral segmentation, joint formation and skeletogenesis. Nat. Genet. 36, 405-410.
26. Lad, Y., Kiema, T., Jiang, P., Pentikainen, O. T., Coles, C. H., Campbell, I. D., Calderwood, D. A. and Ylanne, J. (2007). Structure of three tandem filamin domains reveals auto-inhibition of ligand binding. EMBO J. 26, 3993-4004.
27. Lad, Y., Jiang, P., Ruskamo, S., Harburger, D. S., Ylanne, J., Campbell, I. D. and Calderwood, D. A. (2008). Structural basis of the migfilin-filamin interaction and competition with integrin beta tails. J. Biol. Chem. 283, 35154-35163.
28. Lorenzi, M. and Gimona, M. (2008). Synthetic actin-binding domains reveal compositional constraints for function. Int. J. Biochem. Cell Biol. 40, 1806-1816.
29. Lu, J., Lian, G., Lenkinski, R., De Grand, A., Vaid, R. R., Bryce, T., Stasenko, M., Boskey, A., Walsh, C. and Sheen, V. (2007). Filamin B mutations cause chondrocyte defects in skeletal development. Hum. Mol. Genet. 16, 1661-1675.
30. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. and Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495.
31. McDaneld, T. G., Hancock, D. L. and Moody, D. E. (2004). Altered mRNA abundance of ASB15 and four other genes in skeletal muscle following administration of betaadrenergic receptor agonists. Physiol. Genomics 16, 275-283.
32. McDaneld, T. G., Hannon, K. and Moody, D. E. (2006). Ankyrin repeat and SOCS box protein 15 regulates protein synthesis in skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1672-R1682.
33. Nakamura, F., Osborn, T. M., Hartemink, C. A., Hartwig, J. H. and Stossel, T. P. (2007). Structural basis of filamin A functions. J. Cell Biol. 179, 1011-1025.
34. O'Connell, M. P., Fiori, J. L., Baugher, K. M., Indig, F. E., French, A. D., Camilli, T. C., Frank, B. P., Earley, R., Hoek, K. S., Hasskamp, J. H. et al. (2009). Wnt5A activates the calpain-mediated cleavage of filamin A. J. Invest. Dermatol. 129, 1782-1789.
35. Otey, C. A. and Carpen, O. (2004). Alpha-actinin revisited: a fresh look at an old player. Cell Motil. Cytoskeleton 58, 104-111.
36. Pentikainen, U. and Ylanne, J. (2009). The regulation mechanism for the auto-inhibition of binding of human filamin A to integrin. J. Mol. Biol. 393, 644-657.
37. Pudas, R., Kiema, T. R., Butler, P. J., Stewart, M. and Ylanne, J. (2005). Structural basis for vertebrate filamin dimerization. Structure 13, 111-119.
38. Robertson, S. P., Twigg, S. R., Sutherland-Smith, A. J., Biancalana, V., Gorlin, R. J., Horn, D., Kenwrick, S. J., Kim, C. A., Morava, E., Newbury-Ecob, R. et al. (2003). Localized mutations in the gene encoding the cytoskeletal protein filamin A cause diverse malformations in humans. Nat. Genet. 33, 487-491.
39. Ruskamo, S. and Ylanne, J. (2009). Structure of the human filamin A actin-binding domain. Acta Crystallogr. D Biol. Crystallogr. 65, 1217-1221.
40. Sheen, V. L., Dixon, P. H., Fox, J. W., Hong, S. E., Kinton, L., Sisodiya, S. M., Duncan, J. S., Dubeau, F., Scheffer, I. E., Schachter, S. C. et al. (2001). Mutations in the Xlinked filamin 1 gene cause periventricular nodular heterotopia in males as well as in females. Hum. Mol. Genet. 10, 1775-1783.
41. Stossel, T. P., Condeelis, J., Cooley, L., Hartwig, J. H., Noegel, A., Schleicher, M. and Shapiro, S. S. (2001). Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2, 138-145.
42. Thompson, T. G., Chan, Y. M., Hack, A. A., Brosius, M., Rajala, M., Lidov, H. G., McNally, E. M., Watkins, S. and Kunkel, L. M. (2000). Filamin 2 (FLN2): a musclespecific sarcoglycan interacting protein. J. Cell Biol. 148, 115-126.
43. Todaro, G. J. and Green, H. (1963). Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17, 299-313.
44. Umeda, T., Kouchi, Z., Kawahara, H., Tomioka, S., Sasagawa, N., Maeda, T., Sorimachi, H., Ishiura, S. and Suzuki, K. (2001). Limited proteolysis of filamin is catalyzed by caspase-3 in U937 and Jurkat cells. J. Biochem. 130, 535-542.
45. Vadlamudi, R. K., Li, F., Adam, L., Nguyen, D., Ohta, Y., Stossel, T. P. and Kumar, R. (2002). Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 4, 681-690.
46. van der Flier, A. and Sonnenberg, A. (2001). Structural and functional aspects of filamins. Biochim. Biophys. Acta 1538, 99-117.
47. van der Flier, A., Kuikman, I., Kramer, D., Geerts, D., Kreft, M., Takafuta, T., Shapiro, S. S. and Sonnenberg, A. (2002). Different splice variants of filamin-B affect myogenesis, subcellular distribution, and determine binding to integrin [beta] subunits. J. Cell Biol. 156, 361-376.
48. Wilcox, A., Katsanakis, K. D., Bheda, F. and Pillay, T. S. (2004). Asb6, an adipocytespecific ankyrin and SOCS box protein, interacts with APS to enable recruitment of elongins B and C to the insulin receptor signaling complex. J. Biol. Chem. 279, 38881-38888.
49. Woo, M. S., Ohta, Y., Rabinovitz, I., Stossel, T. P. and Blenis, J. (2004). Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol. Cell. Biol. 24, 3025-3035.
50. Zheng, L., Baek, H. J., Karsenty, G. and Justice, M. J. (2007). Filamin B represses chondrocyte hypertrophy in a Runx2/Smad3-dependent manner. J. Cell Biol. 178, 121-128.
51. Zhou, A. X., Hartwig, J. H. and Akyurek, L. M. (2010). Filamins in cell signaling, transcription and organ development. Trends Cell Biol. 20, 113-123.
52. Zhou, X., Boren, J. and Akyurek, L. M. (2007). Filamins in cardiovascular development. Trends Cardiovasc. Med. 17, 222-229.