Epidermal Growth Factor Activates m-Calpain (Calpain II), at Least in Part, by Extracellular Signal-Regulated Kinase-Mediated Phosphorylation

Molecular and Cellular Biology

Volumn 24, Issue 6, 2004, Pages 2499-2512

  Glading, A ^a,d   Bodnar, R J ^a   Reynolds, I J ^a   Shiraha, H ^a   Satish, L ^a   Potter, D A ^c   Blair, H C ^a,b   Wells, A ^a,b  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHELATING AGENT; CALPAIN; CALPAIN II; EPIDERMAL GROWTH FACTOR; ESTROGEN RECEPTOR; GLUTAMIC ACID; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; TAMOXIFEN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL ADHESION; CELL DEADHESION; CELL MOTILITY; DRUG SENSITIVITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; BINDING SITES; CALCIUM; CALPAIN; CELL LINE; CELL MOVEMENT; DNA, COMPLEMENTARY; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; RECOMBINANT PROTEINS; SERINE;

ANIMALIA;

EID: 1542344328     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.6.2499-2512.2004     Document Type: Article

References (55)

1. 2+-dependent cysteine proteinase, calpains I and II are not phosphorylated in vivo. Biochem. Biophys. Res. Commun. 136:1090-1096.
2. Allen, F. D., C. F. Asnes, P. Chang, E. L. Elson, D. A. Lauffenburger, and A. Wells. 2002. EGF-induced matrix contraction is modulated by calpain. Wound Repair Regen. 10:67-76.
3. Bhatt, A., I. Kaverina, C. Otey, and A. Huttenlocher. 2002. Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115:3415-3425.
4. Bialkowska, K., S. Kulkarni, X. Du, D. E. Goll, T. C. Saido, and J. E. Fox. 2000. Evidence that β3 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. 151:685-695.
5. 2+ signals. J. Cell Sci. 114:2213-2222.
6. Branca, D., A. Gugliucci, D. Bano, M. Brini, and E. Carafoli. 1999. Expression, partial purification and functional properties of the muscle-specific calpain isoform p94. Eur. J. Biochem. 265:839-846.
7. Carragher, N. O., V. J. Fincham, D. Riley, and M. C. Frame. 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.
8. FAK, paxillin, and talin. J. Cell Biol. 147:619-629.
9. Chaudhuri, P., S. M. Colles, D. S. Damron, and L. M. Graham. 2003. Lysophosphatidylcholine inhibits endothelial cell migration by increasing intracellular calcium and activating calpain. Arterioscler. Thromb. Vasc. Biol. 23:218-223.
10. Chen, P., K. Gupta, and A. Wells. 1994. Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from mitogenesis. J. Cell Biol. 124:547-555.
11. Chen, P., H. Xie, and A. Wells. 1996. Mitogenic signaling from the EGF receptor is attenuated by a motility-associated phospholipase C-γ/protein kinase C feedback mechanism. Mol. Biol. Cell 7:871-881.
12. Chou, J., D. Beer-Stolz, N. Burke, S. C. Watkins, and A. Wells. 2002. Distribution of gelsolin and phosphoinositol 4,5-bisphosphate in lamellipodia during EGF-induced motility. Int. J. Biochem. Cell Biol. 34:776-790.
13. Chou, J., N. A. Burke, A. Iwabu, S. C. Watkins, and A. Wells. 2003. Directional motility induced by EGF requires cdc42. Exp. Cell Res. 287:47-56.
14. 2+-dependent proteinases (μ-calpain and m-calpain). J. Biol. Chem. 264:10096-10103.
15. Cooray, P., Y. Yuan, S. M. Schoenwaelder, C. A. Mitchell, H. H. Salem, and S. P. Jackson. 1996. Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain. Biochem. J. 318:41-47.
16. Croall, D. E., and G. N. DeMartino. 1991. Calcium activated neutral protease (calpain) system: structure, function, and regulation, Physiol. Rev. 71:813-847.
17. Fujitani, K., J. Kambayashi, M. Sakon, S. I. Ohmi, S. Kawashima, M. Yukawa, Y. Yano, H. Miyoshi, M. Ikeda, N. Shinoki, and M. Monden. 1997. Identification of μ-, m-calpains and calpastatin and capture of μ-calpain activation in endothelial cells. J. Cell. Biochem. 66:197-209.
18. Glading, A., P. Chang, D. A. Lauffenburger, and A. Wells. 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.
19. Glading, A., D. A. Lauffenburger, and A. Wells. 2002. Cutting to the chase: calpain proteases in cell migration. Trends Cell Biol. 12:46-54.
20. Glading, A., F. Uberall, S. M. Keyse, D. A. Lauffenburger, and A. Wells. 2001. Membrane proximal ERK signaling is required for M-calpain activation downstream of EGF receptor signaling. J. Biol. Chem. 276:23341-23348.
21. +2 indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-3445.
22. Guttmann, R. P., J. S. Elce, P. D. Bell, J. C. Isbell, and G. V. Johnson. 1997. Oxidation inhibits substrate proteolysis by calpain I, but not autolysis. J. Biol. Chem. 272:2005-2012.
23. Guttmann, R. P., and G. V. W. Johnson. 2000. Measurement of calpain activity in vitro and in situ using a fluorescent compound and tau as substrates. Methods Mol. Biol. 144:143-150.
24. 2+ mobilization patterns. Science 284:1527-1530.
25. 2+-dependent protease activity and a novel model of enzyme activation. EMBO J. 18:6880-6889.
26. Huttenlocher, A., S. P. Palecek, Q. Lu, W. Zhang, R. L. Mellgren, D. A. Lauffenburger, M. H. Ginsburg, and A. F. Horwitz. 1997. Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272: 32719-32722.
27. 2+-activated neutral protease. Biochemistry 27:8122-8128.
28. a. Inomata, M., M. Nakamura, S. Imajoh-Ohmi, and S. Kawashima. 1993. A variety of calpain/calpastatin systems in mammalian erythrocytes. Biochim. Biophys. Acta 1178:207-214.
29. Johnson, G. V. W., and R. P. Guttmann. 1997. Calpains: intact and active? Bioessays 19:1011-1018.
30. Kulkarni, S., D. E. Goll, and J. E. Fox. 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.
31. Lane, R. D., D. M. Allan, and R. L. Mellgren. 1992. A comparison of the intracellular distribution of μ-calpain, m-calpain, and calpastatin in proliferating human A431 cells. Exp. Cell Res. 203:5-16.
32. Littlewood, T. D., D. C. Hancock, P. S. Danielian, M. G. Parker, and G. I. Evans. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Research 23:1686-1690.
33. 1 arrest. Gene 182:123-128.
34. Melloni, E., M. Averna, F. Salamino, B. Sparatore, R. Minafra, and S. Pontermoli. 2000. Acyl-CoA-binding protein is a potent m-calpain activator. J. Biol. Chem. 275:82-86.
35. Melloni, E., M. Michetti, F. Salamino, and S. Pontermoli. 1998. Molecular and functional properties of a calpain activator protein specific for μ-isoforms. J. Biol. Chem. 273:12827-12831.
36. Michetti, M., P. L. Viotti, E. Melloni, and S. Pontremoli. 1991. Mechanism of action of the calpain activator protein in rat skeletal muscle. Eur. J. Biochem. 202:1177-1180.
37. 2+ influx in Swiss 3T3 fibroblasts in response to receptor stimulation. Biochem. J. 329:107-114.
38. 2+ switch aligns the active site of calpain. Cell 108:649-660.
39. Neuberger, T., A. K. Chakrabarti, T. Russell, G. H. DeVries, E. L. Hogan, and N. L. Banik. 1997. Immunolocalization of cytoplasmic and myelin m-calpain in transfected Schwann cells. I. Effect of treatment with growth factors. J. Neurosci. Res. 47:521-530.
40. Perrin, B. J., and A. Huttenlocher. 2002. Calpain. Int. J. Biochem. Cell Biol. 34:722-725.
41. Pfaff, M., X. Du, and M. H. Ginsberg. 1999. Calpain cleavage of integrin β cytoplasmic domains. FEBS Lett. 460:17-22.
42. Potter, D. A., J. S. Tirnauer, R. Janssen, D. E. Croall, C. N. Hughes, K. A. Fiacco, J. W. Mier, M. Maki, and I. M. Herman. 1998. Calpain regulates actin remodeling during cell spreading. J. Cell Biol. 141:647-662.
43. Salamino, F., R. DeTullio, P. Mengotti, P. L. Viotti, E. Melloni, and S. Pontremoli. 1993. Site-directed activation of calpain is promoted by a membrane-associated natural activator protein. Biochem. J. 290:191-197.
44. Shiraha, H., A. Glading, J. Chou, Z. Jia, and A. Wells. 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.
45. Shiraha, H., K. Gupta, A. Glading, and A. Wells. 1999. IP-10 inhibits epidermal growth factor-induced motility by decreasing epidermal growth factor receptor-mediated calpain activity. J. Cell Biol. 146:243-253.
46. Shuster, D. B., and I. M. Herman. 1995. Indirect association of ezrin with F-actin: isoform specificity and calcium sensitivity. J. Cell Biol. 128:837-848.
47. Smith, S. D., Z. Jia, K. K. Huynh, A. Wells, and J. S. Elce. 2003. Glutamate substitutions at a PKA consensus site are consistent with inactivation of calpain by phosphorylation. FEBS Lett. 542:115-118.
48. Sorimachi, H., S. Ishura, and K. Suzuki. 1997. Structure and physiological function of calpains. Biochem. J. 328:721-732.
49. Sorimachi, H., and K. Suzuki. 2001. The structure of calpain. J. Biochem. 129:653-664.
50. Strobl, S., C. Fernandez-Catalan, M. Braun, R. Huber, H. Masumoto, K. Nakagawa, A. Irie, H. Sorimachi, G. Bourenkow, H. Bartunik, K. Suzuki, and W. Bode. 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.
51. +2-regulated phospholipid-binding domain. Biochem. Biophys. Res. Commun. 280:1333-1339.
52. Tompa, P., Z. Mucsi, G. Orosz, and P. Friedrich. 2002. Calpastatin subdomains A and C are activators of calpain. J. Biol. Chem. 277:9022-9026.
53. Tranqui, L., and M. R. Block. 1995. Intracellular processing of talin occurs within focal adhesions. Exp. Cell Res. 217:149-156.
54. Upadhya, G. A., S. A. Topp, R. S. Hotchkiss, J. Anagli, and S. M. Strasberg. 2003. Effect of cold preservation on intracellular calcium concentration and calpain activity in rat sinusoidal endothelial cells. Hepatology 37:313-323.
55. Zhang, W., R. D. Lane, and R. L. Mellgren. 1996. The major calpain isozymes are long-lived proteins. Design of an antisense strategy for calpain depletion in cultured cells. J. Biol. Chem. 271:18825-18830.