Regulating cell migration: Calpains make the cut

Journal of Cell Science

Volumn 118, Issue 17, 2005, Pages 3829-3838

  Franco, Santos J ^a   Huttenlocher, Anna ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Calpain; Cell motility; Proteolysis

Indexed keywords

CALCIUM; CALPAIN; CALPASTATIN; GROWTH FACTOR; INTEGRIN; ISOENZYME; PHOSPHOLIPID; PROTEINASE;

APOPTOSIS; AUTOLYSIS; CALCIUM BINDING; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SPREADING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SUBSTRATE; INFLAMMATORY DISEASE; METASTASIS; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

CALPAIN; CELL MOVEMENT; GENE EXPRESSION REGULATION; HUMANS; MULTIGENE FAMILY; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION;

EID: 26244434596     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02562     Document Type: Review

References (145)

1. Arthur, J. S. and Crawford, C. (1996). Investigation of the interaction of mcalpain with phospholipids: calpain-phospholipid interactions. Biochim. Biophys. Acta 1293, 201-206.
2. Arthur, J. S., Elce, J. S., Hegadorn, C., Williams, K. and Greer, P. A. (2000). Disruption of the murine calpain small subunit gene, Capn4: calpain is essential for embryonic development but not for cell growth and division. Mol. Cell Biol. 20, 4474-4481.
3. Azam, M., Andrabi, S. S., Sahr, K. E., Kamath, L., Kuliopulos, A. and Chishti, A. H. (2001). Disruption of the mouse mu-calpain gene reveals an essential role in platelet function. Mol. Cell Biol. 21, 2213-2220.
4. Baki, A., Tompa, P., Alexa, A., Molnar, O. and Friedrich, P. (1996). Autolysis parallels activation of mu-calpain. Biochem. J. 318, 897-901.
5. Barnoy, S., Zipser, Y., Glaser, T., Grimberg, Y. and Kosower, N. S. (1999). Association of calpain (Ca(2+)-dependent thiol protease) with its endogenous inhibitor calpastatin in myoblasts. J. Cell Biochem. 74, 522-531.
6. Beckerle, M. C., Burridge, K., DeMartino, G. N. and Croall, D. E. (1987). Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion. Cell 51, 569-577.
7. Bhatt, A., Kaverina, I., Otey, C. and Huttenlocher, A. (2002). Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115, 3415-3425.
8. Bialkowska, K., Kulkarni, S., Du, X., Goll, D. E., Saido, T. C. and Fox, J. E. (2000). Evidence that beta3 integrin-induced Rac activation involves the calpain-dependent formation of integrin clusters that are distinct from the focal complexes and focal adhesions that form as Rac and RhoA become active. J. Cell Biol. 151, 685-696.
9. Bialkowska, K., Saido, T. C. and Fox, J. E. (2005). SH3 domain of spectrin participates in the activation of Rac in specialized calpain-induced integrin signaling complexes. J. Cell Sci. 118, 381-395.
10. Blanchard, H., Grochulski, P., Li, Y., Arthur, J. S., Davies, P. L., Elce, J. S. and Cygler, M. (1997). Structure of a calpain Ca(2+)-binding domain reveals a novel EF-hand and Ca(2+)-induced conformational changes. Nat. Struct. Biol. 4, 532-538.
11. Braun, C., Engel, M., Theisinger, B., Welter, C. and Seifert, M. (1999). CAPN 8, isolation of a new mouse calpain-isoenzyme. Biochem. Biophys. Res. Commun. 260, 671-675.
12. Calderwood, D. A. (2004). Integrin activation. J. Cell Sci. 117, 657-666.
13. Calderwood, D. A., Zent, R., Grant, R., Rees, D. J., Hynes, R. O. and Ginsberg, M. H. (1999). The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem. 274, 28071-28074.
14. Calderwood, D. A., Yan, B., de Pereda, J. M., Alvarez, B. G., Fujioka, Y., Liddington, R. C. and Ginsberg, M. H. (2002). The phosphotyrosine binding-like domain of talin activates integrins. J. Biol. Chem. 277, 21749-21758.
15. Carragher, N. O. and Frame, M. C. (2002). Calpain: a role in cell transformation and migration. Int. J. Biochem. Cell Biol. 34, 1539-1543.
16. Carragher, N. O., Levkau, B., Ross, R. and Raines, E. W. (1999). Degraded collagen fragments promote rapid disassembly of smooth muscle focal adhesions that correlates with cleavage of pp125(FAK), paxillin, and talin. J. Cell Biol. 147, 619-630.
17. Carragher, N. O., Fincham, V. J., Riley, D. and Frame, M. C. (2001). Cleavage of focal adhesion kinase by different proteases during SRC-regulated transformation and apoptosis. Distinct roles for calpain and caspases. J. Biol. Chem. 276, 4270-4275.
18. Carragher, N. O., Westhoff, M. A., Riley, D., Potter, D. A., Dutt, P., Elce, J. S., Greer, P. A. and Frame, M. C. (2002). v-Src-induced modulation of the calpain-calpastatin proteolytic system regulates transformation. Mol. Cell Biol. 22, 257-269.
19. Carragher, N. O., Westhoff, M. A., Fincham, V. J., Schaller, M. D. and Frame, M. C. (2003). A novel role for FAK as a protease-targeting adaptor protein: regulation by p42 ERK and Src. Curr. Biol. 13, 1442-1450.
20. Carragher, N. O., Fonseca, B. D. and Frame, M. C. (2004). Calpain activity is generally elevated during transformation but has oncogene-specific biological functions. Neoplasia 6, 53-73.
21. 2+-dependent proteinases (mu-calpain and m-calpain). J. Biol. Chem. 264, 10096-10103.
22. Cooray, P., Yuan, Y., Schoenwaelder, S. M., Mitchell, C. A., Salem, H. H. and Jackson, S. P. (1996). Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain. Biochem. J. 318, 41-47.
23. Covault, J., Liu, Q. Y. and el-Deeb, S. (1991). Calcium-activated proteolysis of intracellular domains in the cell adhesion molecules NCAM and N-cadherin. Brian Res. Mol. Brain Res. 11, 11-16.
24. Croall, D. E., Morrow, J. S. and DeMartino, G. N. (1986). Limited proteolysis of the erythrocyte membrane skeleton by calcium-dependent proteinases. Biochim. Biophys. Acta 882, 287-296.
25. Croce, K., Flaumenhaft, R., Rivers, M., Furie, B., Furie, B. C., Herman, I. M. and Potter, D. A. (1999). Inhibition of calpain blocks platelet secretion, aggregation, and spreading. J. Biol. Chem. 274, 36321-36327.
26. Cuevas, B. D., Abell, A. N., Witowsky, J. A., Yujiri, T., Johnson, N. L., Kesavan, K., Ware, M., Jones, P. L., Weed, S. A., DeBiasi, R. L. et al. (2003). MEKK1 regulates calpain-dependent proteolysis of focal adhesion proteins for rear-end detachment of migrating fibroblasts. EMBO J. 22, 3346-3355.
27. Cuzzocrea, S., McDonald, M. C., Mazzon, E., Siriwardena, D., Serraino, I., Dugo, L., Britti, D., Mazzullo, G., Caputi, A. P. and Thiemermann, C. (2000). Calpain inhibitor I reduces the development of acute and chronic inflammation. Am. J. Pathol. 157, 2065-2079.
28. Dear, T. N. and Boehm, T. (1999). Diverse mRNA expression patterns of the mouse calpain genes Capn5, Capn6 and Capn11 during development. Mech. Dev. 89, 201-209.
29. Dear, T. N. and Boehm, T. (2001). Identification and characterization of two novel calpain large subunit genes. Gene 274, 245-252.
30. Dear, N., Matena, K., Vingron, M. and Boehm, T. (1997). A new subfamily of vertebrate calpains lacking a calmodulin-like domain: implications for calpain regulation and evolution. Genomics 45, 175-184.
31. Dear, T. N., Moller, A. and Boehm, T. (1999). CAPN11: a calpain with high mRNA levels in testis and located on chromosome 6. Genomics 59, 243-247.
32. Dear, T. N., Meier, N. T., Hunn, M. and Boehm, T. (2000). Gene structure, chromosomal localization, and expression pattern of Capn12, a new member of the calpain large subunit gene family. Genomics 68, 152-160.
33. Dedieu, S., Mazeres, G., Poussard, S., Brustis, J. J. and Cottin, P. (2003). Myoblast migration is prevented by a calpain-dependent accumulation of MARCKS. Biol. Cell 95, 615-623.
34. Dourdin, N., Bhatt, A. K., Dutt, P., Greer, P. A., Arthur, J. S., Elce, J. S. and Huttenlocher, A. (2001). Reduced cell migration and disruption of the actin cytoskeleton in calpain-deficient embryonic fibroblasts. J. Biol. Chem. 276, 48382-48388.
35. Du, X., Saido, T. C., Tsubuki, S., Indig, F. E., Williams, M. J. and Ginsberg, M. H. (1995). Calpain cleavage of the cytoplasmic domain of the integrin beta 3 subunit. J. Biol. Chem. 270, 26146-26151.
36. Dulong, S., Goudenege, S., Vuillier-Devillers, K., Manenti, S., Poussard, S. and Cottin, P. (2004). Myristoylated alanine-rich C kinase substrate (MARCKS) is involved in myoblast fusion through its regulation by protein kinase Calpha and calpain proteolytic cleavage. Biochem. J. 382, 1015-1023.
37. 2+ requirement, and heterodimer stability in m-calpain. J. Biol. Chem. 272, 11268-11275.
38. Farkas, A., Tompa, P. and Friedrich, P. (2003). Revisiting ubiquity and tissue specificity of human calpains. Biol. Chem. 384, 945-949.
39. 2+-dependent protease during platelet activation. Blood 69, 537-545.
40. Franco, S., Perrin, B. and Huttenlocher, A. (2004a). Isoform specific function of calpain 2 in regulating membrane protrusion. Exp. Cell. Res. 299, 179-187.
41. Franco, S. J., Rodgers, M. A., Perrin, B. J., Han, J., Bennin, D. A., Critchley, D. R. and Huttenlocher, A. (2004b). Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell. Biol. 6, 977-983.
42. Frangioni, J. V., Oda, A., Smith, M., Salzman, E. W. and Neel, B. G. (1993). Calpain-catalyzed cleavage and subcellular relocation of protein phosphotyrosine phosphatase 1B (PTP-1B) in human platelets. EMBO J. 12, 4843-4856.
43. Franz, T., Vingron, M., Boehm, T. and Dear, T. N. (1999). Capn7: a highly divergent vertebrate calpain with a novel C-terminal domain. Mamm. Genome 10, 318-321.
44. 2+ requirement of calpain activation. Biochem. Biophys. Res. Commun. 323, 1131-1133.
45. Gafni, J., Hermel, E., Young, J. E., Wellington, C. L., Hayden, M. R. and Ellerby, L. M. (2004). Inhibition of calpain cleavage of huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J. Biol. Chem. 279, 20211-20220.
46. Gates, R. E. and King, L. E., Jr (1983). Proteolysis of the epidermal growth factor receptor by endogenous calcium-activated neutral protease from rat liver. Biochem. Biophys. Res. Commun. 113, 255-261.
47. Gil-Parrado, S., Popp, O., Knoch, T. A., Zahler, S., Bestvater, F., Felgentrager, M., Holloschi, A., Fernandez-Montalvan, A., Auerswald, E. A., Fritz, H. et al. (2003). Subcellular localization and in vivo subunit interactions of ubiquitous mu-calpain. J. Biol. Chem. 278, 16336-16346.
48. Glading, A., Chang, P., Lauffenburger, D. A. and Wells, A. (2000). Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. J. Biol. Chem. 275, 2390-2398.
49. Glading, A., Uberall, F., Keyse, S. M., Lauffenburger, D. A. and Wells, A. (2001). Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J. Biol. Chem. 276, 23341-23348.
50. Glading, A., Lauffenburger, D. A. and Wells, A. (2002). Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol. 12, 46-54.
51. Glading, A., Bodnar, R. J., Reynolds, I. J., Shiraha, H., Satish, L., Potter, D. A., Blair, H. C. and Wells, A. (2004). Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol. Cell Biol. 24, 2499-2512.
52. Goll, D. E., Dayton, W. R., Singh, I. and Robson, R. M. (1991). Studies of the alpha-actinin/actin interaction in the Z-disk by using calpain. J. Biol. Chem. 266, 8501-8510.
53. Goll, D. E., Thompson, V. F., Li, H., Wei, W. and Cong, J. (2003). The calpain system. Physiol. Rev. 83, 731-801.
54. Guroff, G. (1964). A neutral, calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239, 149-155.
55. Guttmann, R. P., Elce, J. S., Bell, P. D., Isbell, J. C. and Johnson, G. V. (1997). Oxidation inhibits substrate proteolysis by calpain I but not autolysis. J. Biol. Chem. 272, 2005-2012.
56. Hata, S., Sorimachi, H., Nakagawa, K., Maeda, T., Abe, K. and Suzuki, K. (2001). Domain II of m-calpain is a Ca(2+)-dependent cysteine protease. FEBS Lett. 501, 111-114.
57. Hood, J.-L., Logan, B. B., Sinai, A. P., Brooks, W. H. and Roszman, T. L. (2003). Association of the calpain/calpastatin network with subcellular organelles. Biochem. Biophys. Res. Commun. 310, 1200-1212.
58. Hood, J. L., Brooks, W. H. and Roszman, T. L. (2004). Differential compartmentalization of the calpain/calpastatin network with the endoplasmic reticulum and Golgi apparatus. J. Biol. Chem. 279, 43126-43135.
59. Horikawa, Y., Oda, N., Cox, N. J., Li, X., Orho-Melander, M., Hara, M., Hinokio, Y., Lindner, T. H., Mashima, H., Schwarz, P. E. et al. (2000). Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nat. Genet. 26, 163-175.
60. Hosfield, C. M., Elce, J. S., Davies, P. L. and Jia, Z. (1999). Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18, 6880-6889.
61. Huang, C., Tandon, N. N., Greco, N. J., Ni, Y., Wang, T. and Zhan, X. (1997). Proteolysis of platelet cortactin by calpain. J. Biol. Chem. 272, 19248-19252.
62. Huber, E., Vlasny, D., Jeckel, S., Stubenrauch, F. and Iftner, T. (2004). Gene profiling of cottontail rabbit papillomavirus-induced carcinomas identifies upregulated genes directly involved in stroma invasion as shown by small interfering RNA-mediated gene silencing. J. Virol. 78, 7478-7489.
63. Huff-Lonergan, E., Mitsuhashi, T., Beekman, D. D., Parrish, F. C., Jr, Olson, D. G. and Robson, R. M. (1996). Proteolysis of specific muscle structural proteins by mu-calpain at low pH and temperature is similar to degradation in postmortem bovine muscle. J. Anim. Sci. 74, 993-1008.
64. Huttenlocher, A., Palecek, S. P., Lu, Q., Zhang, W., Mellgren, R. L., Lauffenburger, D. A., Ginsberg, M. H. and Horwitz, A. F. (1997). Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272, 32719-32722.
65. 2+-requirement is due to the NH2-terminal processing of the large subunit. J. Biochem. (Tokyo) 100, 633-642.
66. Kambayashi, J., Kajiwara, Y., Sakon, M., Ohshiro, T. and Mori, T. (1986). Possible participation of calpain in myosin light chain phosphorylation of human platelets. Biochem. Int. 13, 571-578.
67. Kamei, M., Webb, G. C., Young, I. G. and Campbell, H. D. (1998). SOLH, a human homologue of the Drosophila melanogaster small optic lobes gene is a member of the calpain and zinc-finger gene families and maps to human chromosome 16p13.3 near CATM (cataract with microphthalmia). Genomics 51, 197-206.
68. Kifor, O., Kifor, I., Moore, F. D., Jr, Butters, R. R., Jr and Brown, E. M. (2003). m-Calpain colocalizes with the calcium-sensing receptor (CaR) in caveolae in parathyroid cells and participates in degradation of the CaR. J. Biol. Chem. 278, 31167-31176.
69. King, L. E., Jr and Gates, R. E. (1985). Calcium-activated neutral protease purified from beef lung: properties and use in defining structure of epidermal growth factor receptors. Arch. Biochem. Biophys. 242, 146-156.
70. 2+-activated neutral protease in human platelets. Biochem. Int. 6, 767-775.
71. Kulkarni, S., Saido, T. C., Suzuki, K. and Fox, J. E. (1999). Calpain mediates integrin-induced signaling at a point upstream of Rho family members. J. Biol. Chem. 274, 21265-21275.
72. Kulkarni, S., Goll, D. E. and Fox, J. E. (2002). Calpain cleaves RhoA generating a dominant-negative form that inhibits integrin-induced actin filament assembly and cell spreading. J. Biol. Chem. 277, 24435-24441.
73. Kwak, K. B., Chung, S. S., Kim, O. M., Kang, M. S., Ha, D. B. and Chung, C. H. (1993). Increase in the level of m-calpain correlates with the elevated cleavage of filamin during myogenic differentiation of embryonic muscle cells. Biochim. Biophys. Acta 1175, 243-249.
74. Lane, R. D., Allan, D. M. and Mellgren, R. L. (1992). A comparison of the intracellular distribution of mu-calpain, m-calpain, and calpastatin in proliferating human A431 cells. Exp. Cell Res. 203, 5-16.
75. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
76. Lin, G. D., Chattopadhyay, D., Maki, M., Wang, K. K., Carson, M., Jin, L., Yuen, P. W., Takano, E., Hatanaka, M., DeLucas, L. J. et al. (1997). Crystal structure of calcium bound domain VI of calpain at 1.9 Å resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nat. Struct. Biol. 4, 539-547.
77. Lokuta, M. A., Nuzzi, P. A. and Huttenlocher, A. (2003). Calpain regulates neutrophil chemotaxis. Proc. Natl. Acad. Sci. USA 100, 4006-4011.
78. Ma, H., Nakajima, E., Shih, M., Azuma, M. and Shearer, T. R. (2004). Expression of calpain small subunit 2 in mammalian tissues. Curr. Eye Res. 29, 337-347.
79. Mamoune, A., Luo, J. H., Lauffenburger, D. A. and Wells, A. (2003). Calpain-2 as a target for limiting prostate cancer invasion. Cancer Res. 63, 4632-4640.
80. Markmann, A., Schafer, S., Linz, W., Lohn, M., Busch, A. E. and Wohlfart, P. (2005). Down-regulation of calpain 9 is linked to hypertensive heart and kidney. Cell Physiol. Biochem. 15, 109-116.
81. Mellgren, R. L. and Lu, Q. (1994). Selective nuclear transport of mu-calpain. Biochem. Biophys. Res. Commun. 204, 544-550.
82. Melloni, E., Michetti, M., Salamino, F., Minafra, R. and Pontremoli, S. (1996). Modulation of the calpain autoproteolysis by calpastatin and phospholipids. Biochem. Biophys. Res. Commun. 229, 193-197.
83. Melloni, E., Michetti, M., Salamino, F. and Pontremoli, S. (1998). Molecular and functional properties of a calpain activator protein specific for mu-isoforms. J. Biol. Chem. 273, 12827-12831.
84. Melloni, E., Averna, M., Salamino, F., Sparatore, B., Minafra, R. and Pontremoli, S. (2000a). Acyl-CoA-binding protein is a potent m-calpain activator. J. Biol. Chem. 275, 82-86.
85. Melloni, E., Michetti, M., Salamino, F., Minafra, R., Sparatore, B. and Pontremoli, S. (2000b). Isolation and characterization of calpain activator protein from bovine brain. Methods Mol. Biol. 144, 99-105.
86. Melloni, E., Minafra, R., Salamino, F. and Pontremoli, S. (2000c). Properties and intracellular localization of calpain activator protein. Biochem. Biophys. Res. Commun. 272, 472-476.
87. Michetti, M., Viotti, P. L., Melloni, E. and Pontremoli, S. (1991). Mechanism of action of the calpain activator protein in rat skeletal muscle. Eur. J. Biochem. 202, 1177-1180.
88. Moldoveanu, T., Hosfield, C. M., Lim, D., Elce, J. S., Jia, Z. and Davies, P. L. (2002). A Ca(2+) switch aligns the active site of calpain. Cell 108, 649-660.
89. 2+ binding at two non-EF-hand sites. J. Biol. Chem. 279, 6106-6114.
90. Molinari, M., Anagli, J. and Carafoli, E. (1994). Ca(2+)-activated neutral protease is active in the erythrocyte membrane in its nonautolyzed 80-kDa form. J. Biol. Chem. 269, 27992-27995.
91. Morford, L. A., Forrest, K., Logan, B., Overstreet, L. K., Goebel, J., Brooks, W. H. and Roszman, T. L. (2002). Calpain II colocalizes with detergent-insoluble rafts on human and Jurkat T-cells. Biochem. Biophys. Res. Commun. 295, 540-546.
92. Newton, A. C. and Johnson, J. E. (1998). Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. Biochim. Biophys. Acta 1376, 155-172.
93. Nishihara, H., Nakagawa, Y., Ishikawa, H., Ohba, M., Shimizu, K. and Nakamura, T. (2001). Matrix vesicles and media vesicles as nonclassical pathways for the secretion of m-Calpain from MC3T3-E1 cells. Biochem. Biophys. Res. Commun. 285, 845-853.
94. Oda, A., Druker, B. J., Ariyoshi, H., Smith, M. and Salzman, E. W. (1993). pp60src is an endogenous substrate for calpain in human blood platelets. J. Biol. Chem. 268, 12603-12608.
95. Ono, Y., Shimada, H., Sorimachi, H., Richard, I., Saido, T. C., Beckmann, J. S., Ishiura, S. and Suzuki, K. (1998). Functional defects of a muscle-specific calpain, p94, caused by mutations associated with limb-girdle muscular dystrophy type 2A. J. Biol. Chem. 273, 17073-17078.
96. 2+ requirement. Structure (Camb.) 11, 1521-1526.
97. Palecek, S. P., Huttenlocher, A., Horwitz, A. F. and Lauffenburger, D. A. (1998). Physical and biochemical regulation of integrin release during rear detachment of migrating cells. J. Cell Sci. 111, 929-940.
98. Parnaud, G., Hammar, E., Rouiller, D. G. and Bosco, D. (2005). Inhibition of calpain blocks pancreatic beta-cell spreading and insulin secretion. Am. J. Physiol. Endocrinol. Metab. 289, E313-E321.
99. Paulhe, F., Bogyo, A., Chap, H., Perret, B. and Racaud-Sultan, C. (2001). Vascular smooth muscle cell spreading onto fibrinogen is regulated by calpains and phospholipase C. Biochem. Biophys. Res. Commun. 288, 875-881.
100. Perrin, B. J. and Huttenlocher, A. (2002). Calpain. Int. J. Biochem. Cell Biol. 34, 722-725.
101. Pfaff, M., Du, X. and Ginsberg, M. H. (1999). Calpain cleavage of integrin beta cytoplasmic domains. FEBS Lett. 460, 17-22.
102. Potter, D. A., Tirnauer, J. S., Janssen, R., Croall, D. E., Hughes, C. N., Fiacco, K. A., Mier, J. W., Maki, M. and Herman, I. M. (1998). Calpain regulates actin remodeling during cell spreading. J. Cell Biol. 141, 647-662.
103. Rafelski, S. M. and Theriot, J. A. (2004). Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73, 209-239.
104. Raynaud, F., Carnac, G., Marcilhac, A. and Benyamin, Y. (2004). m-Calpain implication in cell cycle during muscle precursor cell activation. Exp. Cell Res. 298, 48-57.
105. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
106. Rios-Doria, J., Day, K. C., Kuefer, R., Rashid, M. G., Chinnaiyan, A. M., Rubin, M. A. and Day, M. L. (2003). The role of calpain in the proteolytic cleavage of E-cadherin in prostate and mammary epithelial cells. J. Biol. Chem. 278, 1372-1379.
107. Rios-Doria, J., Kuefer, R., Ethier, S. P. and Day, M. L. (2004). Cleavage of beta-catenin by calpain in prostate and mammary tumor cells. Cancer Res. 64, 7237-7240.
108. 2+-binding domain. J. Biol. Chem. 273, 15879-15882.
109. Robles, E., Huttenlocher, A. and Gomez, T. M. (2003). Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain. Neuron 38, 597-609.
110. Rock, M. T., Dix, A. R., Brooks, W. H. and Roszman, T. L. (2000). Beta1 integrin-mediated T cell adhesion and cell spreading are regulated by calpain. Exp. Cell Res. 261, 260-270.
111. Rosenberger, G., Gal, A. and Kutsche, K. (2005). AlphaPIX associates with calpain 4, the small subunit of calpain, and has a dual role in integrin-mediated cell spreading. J. Biol. Chem. 280, 6879-6889.
112. Saido, T. C., Shibata, M., Takenawa, T., Murofushi, H. and Suzuki, K. (1992). Positive regulation of mu-calpain action by polyphosphoinositides. J. Biol. Chem. 267, 24585-24590.
113. Sakai, K., Hayashi, M., Kawashima, S. and Akanuma, H. (1989). Calcium-induced localization of calcium-activated neutral proteinase on plasma membranes. Biochim. Biophys. Acta 985, 51-54.
114. Salamino, F., De Tullio, R., Mengotti, P., Viotti, P. L., Melloni, E. and Pontremoli, S. (1993). Site-directed activation of calpain is promoted by a membrane-associated natural activator protein. Biochem. J. 290, 191-197.
115. Satish, L., Blair, H. C., Glading, A. and Wells, A. (2005). Interferon-inducible protein 9 (CXCL11)-induced cell motility in keratinocytes requires calcium flux-dependent activation of mu-calpain. Mol. Cell Biol. 25, 1922-1941.
116. Schoenwaelder, S. M., Kulkarni, S., Salem, H. H., Imajoh-Ohmi, S., Yamao-Harigaya, W., Saido, T. C. and Jackson, S. P. (1997). Distinct substrate specificities and functional roles for the 78- and 76-kDa forms of mu-calpain in human platelets. J. Biol. Chem. 272, 24876-24884.
117. Selliah, N., Brooks, W. H. and Roszman, T. L. (1996). Proteolytic cleavage of alpha-actinin by calpain in T cells stimulated with anti-CD3 monoclonal antibody. J. Immunol. 156, 3215-3221.
118. Serrano, K. and Devine, D. V. (2004). Vinculin is proteolyzed by calpain during platelet aggregation: 95 kDa cleavage fragment associates with the platelet cytoskeleton. Cell Motil. Cytoskeleton 58, 242-252.
119. Shields, D. C., Tyor, W. R., Deibler, G. E., Hogan, E. L. and Banik, N. L. (1998). Increased calpain expression in activated glial and inflammatory cells in experimental allergic encephalomyelitis. Proc. Natl. Acad. Sci. USA 95, 5768-5772.
120. Shields, D. C. and Banik, N. L. (1998). Upregulation of calpain activity and expression in experimental allergic encephalomyelitis: a putative role for calpain in demyelination. Brain Res. 794, 68-74.
121. Shiraha, H., Glading, A., Chou, J., Jia, Z. and Wells, A. (2002). Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain. Mol. Cell Biol. 22, 2716-2727.
122. Smith, S. D., Jia, Z., Huynh, K. K., Wells, A. and Elce, J. S. (2003). Glutamate substitutions at a PKA consensus site are consistent with inactivation of calpain by phosphorylation. FEBS Lett. 542, 115-118.
123. Sorimachi, H. and Suzuki, K. (2001). The structure of calpain. J. Biochem. (Tokyo) 129, 653-664.
124. Sorimachi, H., Ishiura, S. and Suzuki, K. (1993). A novel tissue-specific calpain species expressed predominantly in the stomach comprises two alternative splicing products with and without Ca(2+)-binding domain. J. Biol. Chem. 268, 19476-19482.
125. Sorimachi, H., Ono, Y. and Suzuki, K. (2000). Molecular analysis of p94 and its application to diagnosis of limb girdle muscular dystrophy type 2A. Methods Mol. Biol. 144, 75-84.
126. Stewart, M. P., McDowall, A. and Hogg, N. (1998). LFA-1-mediated adhesion is regulated by cytoskeletal restraint and by a Ca2+-dependent protease, calpain. J. Cell Biol. 140, 699-707.
127. Stoscheck, C. M., Gates, R. E. and King, L. E., Jr (1988). A search for EGF-elicited degradation products of the EGF receptor. J. Cell Biochem. 38, 51-63.
128. Strobl, S., Fernandez-Catalan, C., Braun, M., Huber, R., Masumoto, H., Nakagawa, K., Irie, A., Sorimachi, H., Bourenkow, G., Bartunik, H. et al. (2000). The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc. Natl. Acad. Sci. USA 97, 588-592.
129. Suzuki, K. and Sorimachi, H. (1998). A novel aspect of calpain activation. FEBS Lett. 433, 1-4.
130. Suzuki, K., Tsuji, S., Ishiura, S., Kimura, Y., Kubota, S. and Imahori, K. (1981a). Autolysis of calcium-activated neutral protease of chicken skeletal muscle. J. Biochem. (Tokyo) 90, 1787-1793.
131. 2+ ions. J. Biochem. (Tokyo) 90, 275-278.
132. Suzuki, K., Saido, T. C. and Hirai, S. (1992). Modulation of cellular signals by calpain. Ann. New York Acad. Sci. 674, 218-227.
133. Suzuki, K., Hata, S., Kawabata, Y. and Sorimachi, H. (2004). Structure, activation, and biology of calpain. Diabetes 53, S12-S18.
134. 2+-regulated phospholipid-binding domain. Biochem. Biophys. Res. Commun. 280, 1333-1339.
135. Tompa, P., Buzder-Lantos, P., Tantos, A., Farkas, A., Szilagyi, A., Banoczi, Z., Hudecz, F. and Friedrich, P. (2004). On the sequential determinants of calpain cleavage. J. Biol. Chem. 279, 20775-20785.
136. 2+/calmodulin-dependent protein kinase type IV in cultured neurons. J. Biol. Chem. 280, 2165-2175.
137. Tullio, R. D., Passalacqua, M., Averna, M., Salamino, F., Melloni, E. and Pontremoli, S. (1999). Changes in intracellular localization of calpastatin during calpain activation. Biochem. J. 343, 467-472.
138. Vanderklish, P. W. and Bahr, B. A. (2000). The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int. J. Exp. Pathol. 81, 323-339.
139. Verhallen, P. F., Bevers, E. M., Comfurius, P. and Zwaal, R. F. (1987). Correlation between calpain-mediated cytoskeletal degradation and expression of platelet procoagulant activity. A role for the platelet membrane-skeleton in the regulation of membrane lipid asymmetry? Biochim. Biophys. Acta 903, 206-217.
140. Wang, Y., Klijn, J. G., Zhang, Y., Sieuwerts, A. M., Look, M. P., Yang, F., Talantov, D., Timmermans, M., Meijer-van Gelder, M. E., Yu, J. et al. (2005). Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365, 671-679.
141. Webb, D. J., Parsons, J. T. and Horwitz, A. F. (2002). Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell. Biol. 4, E97-E100.
142. Wendt, A., Thompson, V. F. and Goll, D. E. (2004). Interaction of calpastatin with calpain: a review. Biol. Chem. 385, 465-472.
143. Xu, L. and Deng, X. (2004). Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induces phosphorylation of mu- and m-calpain in association with increased secretion, cell migration, and invasion. J. Biol. Chem. 279, 53683-53690.
144. Yan, B., Calderwood, D. A., Yaspan, B. and Ginsberg, M. H. (2001). Calpain cleavage promotes talin binding to the beta 3 integrin cytoplasmic domain. J. Biol. Chem. 276, 28164-28170.
145. Zatz, M. and Starling, A. (2005). Calpains and disease. New Engl. J. Med. 352, 2413-2423.