The carboxyl tail of alpha-actinin-4 regulates its susceptibility to m-calpain and thus functions in cell migration and spreading

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 6, 2013, Pages 1051-1063

  Shao, Hanshuang ^a   Travers, Timothy ^a   Camacho, Carlos J ^a   Wells, Alan ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Adhesion; Calpain; Cytoskeleton; Migration; Phosphorylation

Indexed keywords

ALPHA ACTININ 4; CALPAIN 2; LYSINE; VALINE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; CYTOSKELETON; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ACTIN CYTOSKELETON; ACTININ; AMINO ACID MOTIFS; ANIMALS; CALPAIN; CELL ADHESION; CELL LINE; CELL MOVEMENT; FIBROBLASTS; HUMANS; MICE; PEPTIDE MAPPING; PHOSPHATIDYLINOSITOLS; PROTEIN STRUCTURE, TERTIARY; PSEUDOPODIA;

EID: 84875914364     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.02.015     Document Type: Article

References (37)

1. N. Agarwal, A.S. Adhikari, S.V. Iyer, K. Hekmatdoost, D.R. Welch, and T. Iwakuma MTBP suppresses cell migration and filopodia formation by inhibiting ACTN4 Oncogene 32 2013 462 470
2. M.C. Beckerle, K. Burridge, G.N. DeMartino, and D.E. Croall Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion Cell 51 1987 569 577
3. A. Blanchard, V. Ohanian, and D. Critchley The structure and function of alpha-actinin Journal of Muscle Research and Cell Motility 10 1989 280 289
4. E. Borrego-Diaz, F. Kerff, S.H. Lee, F. Ferron, Y. Li, and R. Dominguez Crystal structure of the actin-binding domain of alpha-actinin 1: evaluating two competing actin-binding models Journal of Structural Biology 155 2006 230 238
5. J. Chou, D.B. Stolz, N.A. Burke, S.C. Watkins, and A. Wells Distribution of gelsolin and phosphoinositol 4,5-bisphosphate in lamellipodia during EGF-induced motility International Journal of Biochemistry and Cell Biology 34 2002 776 790
6. M.D. Davison, and D.R. Critchley alpha-Actinins and the DMD protein contain spectrin-like repeats Cell 52 1988 159 160
7. N. Dourdin, A.K. Bhatt, P. Dutt, P.A. Greer, J.S. Arthur, and J.S. Elce Reduced cell migration and disruption of the actin cytoskeleton in calpain-deficient embryonic fibroblasts Journal of Biological Chemistry 276 2001 48382 48388
8. K. Fukami, K. Furuhashi, M. Inagaki, T. Endo, S. Hatano, and T. Takenawa Requirement of phosphatidylinositol 4,5-bisphosphate for alpha-actinin function Nature 359 1992 150 152
9. A. Glading, D.A. Lauffenburger, and A. Wells Cutting to the chase: calpain proteases in cell motility Trends in Cell Biology 12 2002 46 54
10. A. Glading, F. Uberall, S.M. Keyse, D.A. Lauffenburger, and A. Wells Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling Journal of Biological Chemistry 276 2001 23341 23348
11. K. Honda, T. Yamada, R. Endo, Y. Ino, M. Gotoh, and H. Tsuda Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion Journal of Cell Biology 140 1998 1383 1393
12. K. Honda, T. Yamada, Y. Hayashida, M. Idogawa, S. Sato, and F. Hasegawa Actinin-4 increases cell motility and promotes lymph node metastasis of colorectal cancer Gastroenterology 128 2005 51 62
13. G. Izaguirre, L. Aguirre, Y.P. Hu, H.Y. Lee, D.D. Schlaepfer, and B.J. Aneskievich The cytoskeletal/non-muscle isoform of alpha-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase Journal of Biological Chemistry 276 2001 28676 28685
14. S. Kikuchi, K. Honda, H. Tsuda, N. Hiraoka, I. Imoto, and T. Kosuge Expression and gene amplification of actinin-4 in invasive ductal carcinoma of the pancreas Clinical Cancer Research 14 2008 5348 5356
15. C.H. Kos, T.C. Le, S. Sinha, J.M. Henderson, S.H. Kim, and H. Sugimoto Mice deficient in alpha-actinin-4 have severe glomerular disease Journal of Clinical Investigation 111 2003 1683 1690
16. S.H. Lee, A. Weins, D.B. Hayes, M.R. Pollak, and R. Dominguez Crystal structure of the actin-binding domain of alpha-actinin-4 Lys255Glu mutant implicated in focal segmental glomerulosclerosis Journal of Molecular Biology 376 2008 317 324
17. L. Leloup, H. Shao, Y.H. Bae, B. Deasy, D. Stolz, and P. Roy m-Calpain activation is regulated by its membrane localization and by its binding to phosphatidylinositol 4,5-bisphosphate Journal of Biological Chemistry 285 2010 33549 33566
18. J.L. Michaud, M. Hosseini-Abardeh, K. Farah, and C.R. Kennedy Modulating alpha-actinin-4 dynamics in podocytes Cell Motility and the Cytoskeleton 66 2009 166 178
19. J.L. Michaud, L.I. Lemieux, M. Dube, B.C. Vanderhyden, S.J. Robertson, and C.R. Kennedy Focal and segmental glomerulosclerosis in mice with podocyte-specific expression of mutant alpha-actinin-4 Journal of the American Society of Nephrology 14 2003 1200 1211
20. Y. Ono, and H. Sorimachi Calpains: an elaborate proteolytic system Biochimica et Biophysica Acta 1824 2012 224 236
21. C.A. Otey, and O. Carpen Alpha-actinin revisited: a fresh look at an old player Cell Motility and the Cytoskeleton 58 2004 104 111
22. J.J. Otto Actin-bundling proteins Current Opinion in Cell Biology 6 1994 105 109
23. Q. Quick, and O. Skalli Alpha-actinin 1 and alpha-actinin 4: contrasting roles in the survival, motility, and RhoA signaling of astrocytoma cells Experimental Cell Research 316 2010 1137 1147
24. S.M. Schoenwaelder, S. Kulkarni, H.H. Salem, S. Imajoh-Ohmi, W. Yamao-Harigaya, and T.C. Saido Distinct substrate specificities and functional roles for the 78- and 76-kDa forms of mu-calpain in human platelets Journal of Biological Chemistry 272 1997 24876 24884
25. S. Sen, M. Dong, and S. Kumar Isoform-specific contributions of alpha-actinin to glioma cell mechanobiology PLoS ONE 4 2009 e8427
26. H. Shao, J. Chou, C.J. Baty, N.A. Burke, S.C. Watkins, and D.B. Stolz Spatial localization of m-calpain to the plasma membrane by phosphoinositide biphosphate binding during epidermal growth factor receptor-mediated activation Molecular and Cellular Biology 26 2006 5481 5496
27. H. Shao, J.H. Wang, M.R. Pollak, and A. Wells alpha-actinin-4 is essential for maintaining the spreading, motility and contractility of fibroblasts PLoS ONE 5 2010 e13921
28. H. Shao, C. Wu, and A. Wells Phosphorylation of alpha-actinin 4 upon epidermal growth factor exposure regulates its interaction with actin Journal of Biological Chemistry 285 2010 2591 2600
29. B. Sjoblom, A. Salmazo, and K. Djinovic-Carugo Alpha-actinin structure and regulation Cellular and Molecular Life Sciences 65 2008 2688 2701
30. C.R. Sprague, T.S. Fraley, H.S. Jang, S. Lal, and J.A. Greenwood Phosphoinositide binding to the substrate regulates susceptibility to proteolysis by calpain Journal of Biological Chemistry 283 2008 9217 9223
31. P. Tompa, P. Buzder-Lantos, A. Tantos, A. Farkas, A. Szilagyi, and Z. Banoczi On the sequential determinants of calpain cleavage Journal of Biological Chemistry 279 2004 20775 20785
32. T. Travers, H. Shao, A. Wells, and C. Camacho Towards a cogent quantitative model of the regulatory network of α-actinin-4 and actin interactions Biophysical Journal 104 2013 705 715
33. A. Weins, J.S. Schlondorff, F. Nakamura, B.M. Denker, J.H. Hartwig, and T.P. Stossel Disease-associated mutant alpha-actinin-4 reveals a mechanism for regulating its F-actin-binding affinity Proceedings of the National Academy of Sciences of the United States of America 104 2007 16080 16085
34. H. Xie, M.A. Pallero, K. Gupta, P. Chang, M.F. Ware, and W. Witke EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCgamma signaling pathway Journal of Cell Science 111 1998 615 624 Pt 5
35. S. Yamamoto, H. Tsuda, K. Honda, K. Onozato, M. Takano, and S. Tamai Actinin-4 gene amplification in ovarian cancer: a candidate oncogene associated with poor patient prognosis and tumor chemoresistance Modern Pathology 22 2009 499 507
36. J. Ylanne, K. Scheffzek, P. Young, and M. Saraste Crystal structure of the alpha-actinin rod reveals an extensive torsional twist Structure 9 2001 597 604
37. W.H. Ziegler, A.R. Gingras, D.R. Critchley, and J. Emsley Integrin connections to the cytoskeleton through talin and vinculin Biochemical Society Transactions 36 2008 235 239