Disruption of the murine calpain small subunit gene, Capn4: Calpain is essential for embryonic development but not for cell growth and division

Molecular and Cellular Biology

Volumn 20, Issue 12, 2000, Pages 4474-4481

  Arthur, J Simon C ^a,b   Elce, John S ^a   Hegadorn, Carol ^a   Williams, Karen ^a   Greer, Peter A ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CYCLIN D1; INTEGRIN; PROTEIN P53; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLEEDING; CARDIOVASCULAR SYSTEM; CELL CULTURE; CELL DIVISION; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ERYTHROID CELL; FIBROBLAST; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CALPAIN; CELL DIVISION; EMBRYONIC AND FETAL DEVELOPMENT; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE;

ANIMALIA; MAMMALIA; MURINAE;

EID: 0034116930     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.12.4474-4481.2000     Document Type: Article

References (71)

1. Arthur, J. S., P. A. Greer, and J. S. Elce. 1998. Structure of the mouse calpain small subunit gene. Biochim. Biophys. Acta 1388:247-252.
2. Arthur, J. S. C., and D. L. Mykles. 2000. Calpain zymography with casein or FITC-casein, p. 109-116. In J. C. Elce (ed.), Methods in molecular biology, vol. 144. Calpain protocols and methods. Humana Press Inc., Totowa, N.J.
3. Baghdiguian, S., M. Martin, I. Richard, F. Pons, C, Astier, N. Bourg, R. T. Hay, R. Chemaly, G. Halaby, J. Loiselet, L. V. Anderson, A. Lopez de Munain, M. Fardeau, P. Mangeat, J. S. Beckmann, and G. Lefranc. 1999. Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IκBα/NF-κB pathway in limb-girdle muscular dystrophy type 2A. Nat. Med. 5:503-511.
4. Balcerzak, D., S. Poussard, J. J. Brustis, N. Elamrani, M. Soriano, P. Cottin, and A. Ducastaing. 1995. An antisense oligodeoxyribonucleotide to m-calpain mRNA inhibits myoblast fusion. J. Cell Sci. 108:2077-2082.
5. Barnes, T. M., and J. Hodgkin. 1996. The tra-3 sex determination gene of Caenorhabditis elegans encodes a member of the calpain regulatory protease family. EMBO J. 15:4477-4484.
6. 2+-induced conformational changes. Nat. Struct. Biol. 4:532-538.
7. Carafoll, E., and M. Molinari. 1998. Calpain: a protease in search of a function? Biochem. Biophys. Res. Commun. 247:193-203.
8. Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, C. Declercq, J. Pawling, L. Moons, D. Collen, W. Risau, and A. Nagy. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
9. Dear, T. N., A. Moller, and T. Boehm. 1999. CAPN11: a calpain with high mRNA levels in testis and located on chromosome 6. Genomics 59:243-247.
10. Dear, T. N., and T. Boehm. 1999. Diverse mRNA expression patterns of the mouse calpain genes Capn5, Capn6 and Capn11 during development. Mech. Dev. 89:201-209.
11. Dourdin, N., D. Balcerzak, J. J. Brustis, S. Poussard, P. Cottin, and A. Ducastaing. 1999. Potential m-calpain substrates during myoblast fusion. Exp. Cell Res. 246:433-442.
12. Dutt, P., J. S. Arthur, D. E. Croall, and J. S. Elce. 1998. m-Calpain subunits remain associated in the presence of calcium. FEBS Lett. 436:367-371.
13. Elce, J. S., P. L. Davies, C. Hegadorn, D. H. Maurice, and J. S. C. Arthur. 1997. The effects of truncations of the small subunit on m-calpain activity and heterodimer formation. Biochem. J. 326:31-38.
14. Fadeel, B., B. Zhivotovsky, and S. Orrenius. 1999. All along the watchtower: on the regulation of apoptosis regulators. FASEB J. 13:1647-1657.
15. Feinberg, A. P., and B. Vogelstein. 1984. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Addendum. Anal. Biochem. 137:266-267.
16. Ferrara, N., K. Carver-Moore, H. Chen, M. Dowd, L. Lu, K. S. O'Shea, L. Powell-Braxton, K. J. Hillan, and M. W. Moore. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
17. Fong, G. H., J. Rossant, M. Gertsenstein, and M. L. Breitman. 1995. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70.
18. Fougerousse, F., M. Durand, L. Suel, O. Pourquie, A. L. Delezoide, N. B. Romero, M. Abitbol, and J. S. Beckmann. 1998. Expression of genes (CAPN3, SGCA, SGCB, and TTN) involved in progressive muscular dystrophies during early human development. Genomics 48:145-156.
19. Fox, J. E. B., and T. C. Saido. 1999. Calpain in signal transduction, p. 103-126. In K. K. W. Wang and P. W. Yuen (ed.), Calpain: pharmacology and toxicology of calcium-dependent protease. Taylor & Francis, Philadelphia, Pa.
20. Franz, T., M. Vingron, T. Boehm, and T. N. Dear. 1999. Capn7: a highly divergent vertebrate calpain with a novel C-terminal domain. Mamm. Genome 10:318-321.
21. Graham-Siegenthaler, K., S. Gauthier, P. L. Davies, and J. S. Elce. 1994. Active recombinant rat calpain II. Bacterially produced large and small subunits associate both in vivo and in vitro. J. Biol. Chem. 269:30457-30460.
22. Henkemeyer, M., D. J. Rossi, D. P. Holmyard, M. C. Puri, G. Mbamalu, K. Harpal, T. S. Shih, T. Jacks, and T. Pawson. 1995. Vascular system defects and neuronal apoptosis in mice lacking ras GTPase-activating protein. Nature 377:695-701.
23. Herasse, M., Y. Ono, F. Fougerousse, E. kimura, D. Stockholm, C. Beley, D. Montarras, C. Pinset, H. Sorimachi, K. Suzuki, J. S. Beckmann, and I. Richard. 1999. Expression and functional characteristics of calpain 3 isoforms generated through tissue-specific transcriptional and posttranscriptional events. Mol. Cell. Biol. 19:4047-4055.
24. Hill, D. P., and W. Wurst. 1993. Screening for novel pattern formation genes using gene trap approaches. Methods Enzymol. 225:664-681.
25. Hosfield, C. M., J. S. Elce, P. L. Davies, and Z. Jia. 1999. Crystal structure of calpain reveals the structural basis for Ca2+-dependent protease activity and a novel mode 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. Ginsberg, and A. F. Horwitz. 1997. Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272: 32719-32722.
27. Karlsson, J. O., S. Gustavsson, C. Hall, and E. Nilsson. 1985. A simple one-step procedure for the separation of calpain I, calpain II and calpastatin. Biochem. J. 231:201-204.
28. Kinbara, K., H. Sorimachi, S. Ishiura, and K. Suzuki. 1998. Skeletal muscle-specific calpain, p49: structure and physiological function. Biochem. Pharmacol. 56:415-420.
29. Kulkarni, S., T. C. Saido, K. Suzuki, and J. E. Fox. 1999. Calpain mediates integrin-induced signaling at a point upstream of Rho family members. J. Biol. Chem. 274:21265-21275.
30. Kwak, K. B., S. S. Chung, O. M. Kim, M. S. Kang, D. B. Ha, and C. H. Chung. 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.
31. Lin, G.-D., D. Chattopadhyay, M. Maki, K. K. W. Wang, M. Carson, L. Jin, P.-W. Yuen, E. Takano, M. Hatanaka, L. J. DeLucas, and S. V. L. Narayana. 1997. Crystal structure of calcium bound domain VI of calpain at 1.9Å resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nat. Struct. Biol. 4:539-547.
32. Lyons, I., L. M. Parsons, L. Hartley, R. Li, J. E. Andrews, L. Robb, and R. P. Harvey. 1995. Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9:1654-1666.
33. Matena, K., T. Boehm, and N. Dear. 1998. Genomic organization of mouse Capn5 and Capn6 genes confirms that they are a distinct calpain subfamily. Genomics 48:117-120.
34. McGinnis, K. M., M. E. Gnegy, Y. H. Park, N. Mukerjee, and K. K. Wang. 1999. Procaspase-3 and poly(ADP)ribose polymerase (PARP) are calpain substrates. Biochem. Biophys. Res. Commun. 263:94-99.
35. Mellgren, R. L. 1987. Calcium-dependent proteases: an enzyme system active at cellular membranes? FASEB J. 1:110-115.
36. Mellgren, R. L., W. Zhang, Q. Lu, and R. D. Lane. 1999. Involvement of calpains in cell cycle G1- to S-phase, p. 161-178. In K. K. W. Wang and P. W. Yuen (ed.), Calpain: pharmacology and toxicology of calcium-dependent protease. Taylor & Francis, Philadelphia, Pa.
37. Meyer, S. L., D. Bozyczko-Coyne, S. K. Mallya, C. M. Spais, R. Bihovsky, J. K. Kawooya, D. M. Lang, R. W. Scott, and R. Siman. 1996. Biologically active monomeric and heterodimeric recombinant human calpain I produced using the baculovirus expression system. Biochem. J. 314:511-519.
38. Meyers, E. N., M. Lewandoski, and G. R. Martin. 1998. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18:136-141.
39. Molinari, M., and E. Carafoli. 1997. Calpain: a cytosolic proteinase active at the membranes. J. Membr. Biol. 156:1-8.
40. Nagy, A., J. Rossant, R. Nagy, W. Abramow-Newerly, and J. C. Roder. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90:8424-8428.
41. Nakagawa, T., H. Zhu, N. Morishima, E. Li, J. Xu, B. A. Yankner, and J. Yuan. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98-103.
42. Ohno, S., Y. Emori, S. Imajoh, H. Kawasaki, M. Kisaragi, and K. Suzuki. 1984. Evolutionary origin of a calcium-dependent protease by fusion of genes for a thiol protease and a calcium-binding protein? Nature 312:566-570.
43. Ono, Y., H. Sorimachi, and K. Suzuki. 1998. Structure and physiology of calpain, an enigmatic protease. Biochem. Biophys. Res. Commun. 245:289-294.
44. Raser, K. J., A. Posner, and K. K. W. Wang. 1995. Casein zymography: a method to study mu-calpain, m-calpain, and their inhibitory agents. Arch. Biochem. Biophys. 319:211-216.
45. Richard, I., O. Broux, V. Allamand, F. Fougerousse, N. Chiannilkulchai, N. Bourg, L. Brenguier, C. Devaud, P. Pasturaud, C. Roudaut, et al. 1995. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2a. Cell 81:27-40.
46. Ruiz-Vela, A., G. Gonzalez de Buitrago, and C. Martinez-A. 1999. Implication of calpain in caspase activation during B cell clonal deletion. EMBO J. 18:4988-4998.
47. Samis, J. A., D. W. Back, E. J. Graham, C. I. DeLuca, and J. S. Elce. 1991. Constitutive expression of calpain II in the rat uterus during pregnancy and involution. Biochem. J. 276:293-299.
48. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
49. Schoenwaelder, S. M., and K. Burridge. 1999. Evidence for a calpeptin-sensitive protein-tyrosine phosphatase upstream of the small GTPase Rho. A novel role for the calpain inhibitor calpeptin in the inhibition of protein-tyrosine phosphatases. J. Biol. Chem. 274:14359-14367.
50. Schollmeyer, J. E. 1988. Calpain II involvement in mitosis. Science 240:911-913.
51. Shalaby, F., J. Rossant, T. P. Yamaguchi, M. Gertsenstein, X. F. Wu, M. L. Breitman, and A. C. Schuh. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66.
52. Sorimachi, H., S. Amano, S. Ishiura, and K. Suzuki. 1996. Primary sequences of rat mu-calpain large and small subunits are, respectively, moderately and highly similar to those of human. Biochim. Biophys. Acta 1309: 37-41.
53. Sorimachi, H., S. Ishiura, and K. Suzuki. 1997. Structure and physiological function of calpains. Biochem. J. 328:721-732.
54. Squier, M. K., and J. J. Cohen. 1997. Calpain, an upstream regulator of thymocyte apoptosis. J. Immunol. 158:3690-3697.
55. Squier, M. K., A. J. Sehnert, K. S. Sellins, A. M. Malkinson, E. Takano, and J. J. Cohen. 1999. Calpain and calpastatin regulate neutrophil apoptosis. J. Cell. Physiol. 178:311-319.
56. 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.
57. Suri, C., P. F. Jones, S. Patan, S. Bartunkova, P. C. Maisonpierre, S. Davis, T. N. Sato, and G. D. Yancopoulos. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171-1180.
58. Suzuki, K., and H. Sorimachi. 1998. A novel aspect of calpain activation. FEBS Lett. 433:1-4.
59. Thompson, V. F., and D. E. Goll. 2000. Purification of μ-calpain, m-calpain, and calpastatin from animal tissues, p. 3-16. In J. S. Eke (ed.), Methods in molecular biology, vol. 144. Calpain protocols and methods. Humana Press Inc., Totowa, N.J.
60. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
61. Tybulewicz, V. L., C. E. Crawford, P. K. Jackson, R. T. Bronson, and R. C. Mulligan. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65:1153-1163.
62. Vilei, E. M., S. Calderara, J. Anagli, S. Berardi, K. Hitomi, M. Maki, and E. Carafoli. 1997. Functional properties of recombinant calpain I and of mutants lacking domains III and IV of the catalytic subunit. J. Biol. Chem. 272:25802-25808.
63. Wang, K. K. W., and P. W. Yuen. 1999. Calpain substrates, assay methods, regulation, and its inhibitor agents, p. 77-101. In K. K. W. Wang and P. W. Yuen (ed.), Calpain: pharmacology and toxicology of calcium-dependent protease. Taylor & Francis, Philadelphia, Pa.
64. Waterhouse, N. J., D. M. Finucane, D. R. Green, J. S. Elce, S. Kumar, E. S. Alnemri, G. Litwack, K. Khanna, M. F. Lavin, and D. J. Watters. 1998. Calpain activation is upstream of caspases in radiation-induced apoptosis. Cell Death Differ. 5:1051-1061.
65. Wilson, G. M., E. A. Roberts, and R. G. Deeley. 1997. Modulation of LDL receptor mRNA stability by phorbol esters in human liver cell culture models. J. Lipid Res. 38:437-446.
66. Wolf, B. B., J. C. Goldstein, H. R. Stennicke, H. Beere, G. P. Amarante-Mendes, G. S. Salvesen, and D. R. Green. 1999. Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood 94:1683-1692.
67. Wood, D. E., and E. W. Newcomb. 1999. Caspase-dependent activation of calpain during drug-induced apoptosis. J. Biol. Chem. 274:8309-8315.
68. Yadav, S. S., D. Sindram, D. K. Perry, and P. A. Clavien. 1999. Ischemic preconditioning protects the mouse liver by inhibition of apoptosis through a caspase-dependent pathway. Hepatology 30:1223-1231.
69. Yoshizawa, T., H. Sorimachi, S. Tomioka, S. Ishiura, and K. Suzuki. 1995. A catalytic subunit of calpain possesses full proteolytic activity. FEBS Lett. 358:101-103.
70. Yoshizawa, T., H. Sorimachi, S. Tomioka, S. Ishiura, and K. Suzuki. 1995. Calpain dissociates into subunits in the presence of calcium ions. Biochem. Biophys. Res. Commun. 208:376-383.
71. Zhang, W., and R. L. Mellgren. 1996. Calpain subunits remain associated during catalysis. Biochem. Biophys. Res. Commun. 227:890-896.