Calpain chronicle-an enzyme family under multidisciplinary characterization

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 87, Issue 6, 2011, Pages 287-327

  Sorimachi, Hiroyuki ^a   Hata, Shoji ^a   Ono, Yasuko ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Calcium ion; Calpain; Calpainopathy; Gastropathy; Intracellular proteolysis; Muscular dystrophy

Indexed keywords

CALPAIN;

AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; CHEMISTRY; CLASSIFICATION; ENZYME ACTIVATION; GENERAL ASPECTS OF DISEASE; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CALPAIN; DISEASE; ENZYME ACTIVATION; HUMANS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PROTEIN STRUCTURE, TERTIARY;

ARCHAEA; EUKARYOTA;

EID: 79959301027     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.87.287     Document Type: Review

References (275)

1. Guroff, G. (1964) A neutral calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239, 149-155.
2. Lazarovici, P. (2000) Obituary: Dr. Gordon Guroff (1933-1999). J. Mol. Neurosci. 14, 1-2.
3. 2+. II. Identification of the kinase activating factor as a proteolytic enzyme. Biochemistry 7, 2116-2122.
4. 2+. Biochemistry 3, 1033-1039.
5. 2+-specific removal of Z lines from rabbit skeletal muscle. J. Cell Biol. 52, 367-381.
6. Takai, Y., Yamamoto, M., Inoue, M., Kishimoto, A. and Nishizuka, Y. (1977) A proenzyme of cyclic nucleotide-independent protein kinase and its activation by calcium-dependent neutral protease from rat liver. Biochem. Biophys. Res. Commun. 77, 542-550.
7. Ishiura, S., Murofushi, H., Suzuki, K. and Imahori, K. (1978) Studies of a calcium-activated neutral protease from chicken skeletal muscle. I. Purification and characterization. J. Biochem. 84, 225-230.
8. Suzuki, K., Tsuji, S., Ishiura, S., Kimura, Y., Kubota, S. and Imahori, K. (1981) Autolysis of calcium-activated neutral protease of chicken skeletal muscle. J. Biochem. 90, 1787-1793.
9. Suzuki, K. (1983) Reaction of calcium-activated neutral protease (CANP) with an epoxysuccinyl derivative (E64c) and iodoacetic acid. J. Biochem. 93, 1305-1312.
10. Suzuki, K. and Ishiura, S. (1983) Effect of metal ions on the structure and activity of calciumactivated neutral protease (CANP). J. Biochem. 93, 1463-1471.
11. 2+-dependent neutral protease in rat liver. J. Biochem. 84, 1657-1659.
12. 2+-dependent protease (calpain) and its high-molecularweight endogenous inhibitor (calpastatin). Adv. Enzyme Regul. 19, 407-424.
13. Ohno, S., Emori, Y., Imajoh, S., Kawasaki, H., Kisaragi, M. and Suzuki, K. (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.
14. Suzuki, K. (1991) Nomenclature of calcium dependent proteinase. Biomed. Biochim. Acta 50, 483-484.
15. Ohno, S., Minoshima, S., Kudoh, J., Fukuyama, R., Shimizu, Y., Ohmi-Imajoh, S., Shimizu, N. and Suzuki, K. (1990) Four genes for the calpain family locate on four distinct human chromosomes. Cytogenet. Cell Genet. 53, 225-229.
16. Croall, D.E. and DeMartino, G.N. (1991) Calciumactivated neutral protease (calpain) system: structure, function, and regulation. Physiol. Rev. 71, 813-847.
17. Goll, D.E., Thompson, V.F., Li, H., Wei, W. and Cong, J. (2003) The calpain system. Physiol. Rev. 83, 731-801.
18. Zatz, M. and Starling, A. (2005) Mechanisms of disease: Calpains and disease. N. Engl. J. Med. 352, 2413-2423.
19. 2+-dependent proteases in ischemic neuronal death: a conserved 'calpaincathepsin cascade' from nematodes to primates. Cell Calcium 36, 285-293.
20. Wendt, A., Thompson, V.F. and Goll, D.E. (2004) Interaction of calpastatin with calpain: a review. Biol. Chem. 385, 465-472.
21. Wells, A., Huttenlocher, A. and Lauffenburger, D.A. (2005) Calpain proteases in cell adhesion and motility. Int. Rev. Cytol. 245, 1-16.
22. Turner, M.D., Cassell, P.G. and Hitman, G.A. (2005) Calpain-10: from genome search to function. Diabetes Metab. Res. Rev. 21, 505-514.
23. 2+, calpain and 3-phosphorylated phosphatidyl inositides; decision-making signals in neutrophils as potential targets for therapeutics. J. Pharm. Pharmacol. 56, 565-571.
24. Sorimachi, H. and Kawabata, Y. (2003) Calpain and pathology in view of structure-function relationships. Nippon Yakurigaku Zasshi 122, 21-29 (in Japanese).
25. Ray, S.K., Hogan, E.L. and Banik, N.L. (2003) Calpain in the pathophysiology of spinal cord injury: neuroprotection with calpain inhibitors. Brain Res. Rev. 42, 169-185.
26. Ridderstrale, M., Parikh, H. and Groop, L. (2005) Calpain 10 and type 2 diabetes: are we getting closer to an explanation? Curr. Opin. Clin. Nutr. Metab. Care 8, 361-366.
27. Ray, S.K. and Banik, N.L. (2003) Calpain and its involvement in the pathophysiology of CNS injuries and diseases: therapeutic potential of calpain inhibitors for prevention of neurodegeneration. Curr. Drug Targets CNS Neurol. Disord. 2, 173-189.
28. Nixon, R.A. (2003) The calpains in aging and agingrelated diseases. Ageing Res. Rev. 2, 407-418.
29. Mehendale, H.M. and Limaye, P.B. (2005) Calpain: a death protein that mediates progression of liver injury. Trends Pharmacol. Sci. 26, 232-236.
30. Liu, X., Van Vleet, T. and Schnellmann, R.G. (2004) The role of calpain in oncotic cell death. Annu. Rev. Pharmacol. Toxicol. 44, 349-370.
31. Laval, S.H. and Bushby, K.M.D. (2004) Limb-girdle muscular dystrophies-From genetics to molecular pathology. Neuropathol. Appl. Neurobiol. 30, 91-105.
32. Horikawa, Y. (2005) Type 2 diabetes and genetic variations of calpain 10 gene. Nippon Rinsho 63, 155-159 (in Japanese).
33. Harwood, S.M., Yaqoob, M.M. and Allen, D.A. (2005) Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Ann. Clin. Biochem. 42, 415-431.
34. Friedrich, P., Tompa, P. and Farkas, A. (2004) The calpain-system of Drosophila melanogaster: coming of age. Bioessays 26, 1088-1096.
35. Franco, S.J. and Huttenlocher, A. (2005) Regulating cell migration: calpains make the cut. J. Cell Sci. 118, 3829-3838.
36. 2+dependent proteolysis in muscle wasting. Int. J. Biochem. Cell Biol. 37, 2134-2146.
37. Carragher, N.O. (2006) Calpain inhibition: a therapeutic strategy targeting multiple disease states. Curr. Pharm. Des. 12, 615-638.
38. Branca, D. (2004) Calpain-related diseases. Biochem. Biophys. Res. Commun. 322, 1098-1104.
39. Biswas, S., Harris, F., Dennison, S., Singh, J.P. and Phoenix, D. (2005) Calpains: enzymes of vision? Med. Sci. Monit. 11, RA301-RA310.
40. Biswas, S., Harris, F., Dennison, S., Singh, J. and Phoenix, D.A. (2004) Calpains: targets of cataract prevention? Trends Mol. Med. 10, 78-84.
41. Bartoli, M. and Richard, I. (2005) Calpains in muscle wasting. Int. J. Biochem. Cell Biol. 37, 2115-2133.
42. Baud, L., Fouqueray, B., Bellocq, A. and Peltier, J. (2003) Calpains participate in inflammatory reaction development. Med. Sci. (Paris) 19, 71-76 (in French).
43. Kuchay, S.M. and Chishti, A.H. (2007) Calpainmediated regulation of platelet signaling pathways. Curr. Opin. Hematol. 14, 249-254.
44. Liu, J., Liu, M.C. and Wang, K.K. (2008) Calpain in the CNS: from synaptic function to neurotoxicity. Sci. Signal. 1, re1.
45. Bertipaglia, I. and Carafoli, E. (2007) Calpains and human disease. Subcell. Biochem. 45, 29-53.
46. Croall, D.E. and Ersfeld, K. (2007) The calpains: modular designs and functional diversity. Genome Biol. 8, 218.
47. Suzuki, K., Hata, S., Kawabata, Y. and Sorimachi, H. (2004) Structure, activation, and biology of calpain. Diabetes 53, S12-S18.
48. Sorimachi, H., Ishiura, S. and Suzuki, K. (1997) Structure and physiological function of calpains. Biochem. J. 328, 721-732.
49. Murachi, T. (1983) Calpain and calpastatin. Trends Biochem. Sci. 8, 167-169.
50. Tanaka, K. (2009) The proteasome: overview of structure and functions. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 85, 12-36.
51. Mizushima, N. and Levine, B. (2010) Autophagy in mammalian development and differentiation. Nat. Cell Biol. 12, 823-830.
52. Tait, S.W. and Green, D.R. (2010) Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11, 621-632.
53. Ono, Y., Kakinuma, K., Torii, F., Irie, A., Nakagawa, K., Labeit, S., Abe, K., Suzuki, K. and Sorimachi, H. (2004) Possible regulation of the conventional calpain system by skeletal muscle-specific calpain, p94/calpain 3. J. Biol. Chem. 279, 2761-2771.
54. Ono, Y., Ojima, K., Torii, F., Takaya, E., Doi, N., Nakagawa, K., Hata, S., Abe, K. and Sorimachi, H. (2010) Skeletal muscle-specific calpain is an intracellular NaD-dependent protease. J. Biol. Chem. 285, 22986-22998.
55. Dutt, P., Croall, D.E., Arthur, S.C., De Veyra, T., Williams, K., Elce, J.S. and Greer, P.A. (2006) m-Calpain is required for preimplantation embryonic development in mice. BMC Dev. Biol. 6, 3.
56. Richard, I., Broux, O., Allamand, V., Fougerousse, F., Chiannilkulchai, N., Bourg, N., Brenguier, L., Devaud, C., Pasturaud, P., Roudaut, C., Hillaire, D., Passos-Bueno, M.-R., Zats, M., Tischfield, J.A., Fardeau, M., Jackson, C.E., Cohen, D. and Beckmann, J.S. (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81, 27-40.
57. Hata, S., Abe, M., Suzuki, H., Kitamura, F., Toyama-Sorimachi, N., Abe, K., Sakimura, K. and Sorimachi, H. (2010) Calpain 8/nCL-2 and Calpain 9/nCL-4 constitute an active protease complex, G-calpain, involved in gastric mucosal defense. PLoS Genet. 6, e1001040.
58. Yamada, M., Yoshida, Y., Mori, D., Takitoh, T., Kengaku, M., Umeshima, H., Takao, K., Miyakawa, T., Sato, M., Sorimachi, H., Wynshaw-Boris, A. and Hirotsune, S. (2009) Inhibition of calpain increases LIS1 expression and partially rescues in vivo phenotypes in a mouse model of lissencephaly. Nat. Med. 15, 1202-1207.
59. Kimura, Y., Koga, H., Araki, N., Mugita, N., Fujita, N., Takeshima, H., Nishi, T., Yamashima, T., Saido, T.C., Yamasaki, T., Moritake, K., Saya, H. and Nakao, M. (1998) The involvement of calpain-dependent proteolysis of the tumor suppressor NF2 (merlin) in schwannomas and meningiomas. Nat. Med. 4, 915-922.
60. Delaney, S.J., Hayward, D.C., Barleben, F., Fischbach, K.F. and Miklos, G.L. (1991) Molecular cloning and analysis of small optic lobes, a structural brain gene of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 88, 7214-7218.
61. Barnes, T.M. and Hodgkin, J. (1996) The tra-3 sex determination gene of Caenorhabditis elegans encodes a member of the calpain regulatory protease family. EMBO J. 15, 4477-4484.
62. Lid, S.E., Gruis, D., Jung, R., Lorentzen, J.A., Ananiev, E., Chamberlin, M., Niu, X., Meeley, R., Nichols, S. and Olsen, O.A. (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc. Natl. Acad. Sci. USA 99, 5460-5465.
63. Denison, S.H., Orejas, M. and Arst, H.N. Jr. (1995) Signaling of ambient pH in Aspergillus involves a cysteine protease. J. Biol. Chem. 270, 28519-28522.
64. Futai, E., Maeda, T., Sorimachi, H., Kitamoto, K., Ishiura, S. and Suzuki, K. (1999) The protease activity of a calpain-like cysteine protease in Saccharomyces cerevisiae is required for alkaline adaptation and sporulation. Mol. Gen. Genet. 260, 559-568.
65. Hayashi, M., Fukuzawa, T., Sorimachi, H. and Maeda, T. (2005) Constitutive activation of the pH-responsive Rim101 pathway in yeast mutants defective in late steps of the MVB/ESCRT pathway. Mol. Cell. Biol. 25, 9478-9490.
66. Suzuki, K. (1991) Historical background, current status, and future prospect of research on calcium dependent protease. Cell Technol. 10, 545-551 (in Japanese).
67. Suzuki, K. (1991) Determination of structure of calpain and East-West problem. Cell Technol. 10, 719-727 (in Japanese).
68. Suzuki, K. (1991) In search of physiological function of calpain. Cell Technol. 10, 878-885 (in Japanese).
69. Drummond, G.I. and Duncan, L. (1968) On the mechanism of activation of phosphorylase b kinase by calcium. J. Biol. Chem. 243, 5532-5538.
70. Fischer, E.H. and Krebs, E.G. (1955) Conversion of phosphorylase b to phosphorylase a in muscle extracts. J. Biol. Chem. 216, 121-132.
71. Krebs, E.G. and Fischer, E.H. (1955) Phosphorylase activity of skeletal muscle extracts. J. Biol. Chem. 216, 113-120.
72. 2+-dependent proteases (calpains) in post mortem proteolysis and meat tenderness. Biochimie 74, 239-245.
73. Kishimoto, A., Kajikawa, N., Tabuchi, H., Shiota, M. and Nishizuka, Y. (1981) Calcium-dependent neural proteases, widespread occurrence of a species of protease active at lower concentrations of calcium. J. Biochem. 90, 889-892.
74. Ogawa, Y., Takai, Y., Kawahara, Y., Kimura, S. and Nishizuka, Y. (1981) A new possible regulatory system for protein phosphorylation in human peripheral lymphocytes. I. Characterization of a calcium-activated, phospholipid-dependent protein kinase. J. Immunol. 127, 1369-1374.
75. Takai, Y., Kaibuchi, K., Sano, K. and Nishizuka, Y. (1982) Counteraction of calcium-activated, phospholipid-dependent protein kinase activation by adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate in platelets. J. Biochem. 91, 403-406.
76. Kishimoto, A., Kajikawa, N., Shiota, M. and Nishizuka, Y. (1983) Proteolytic activation of calcium-activated, phospholipid-dependent protein kinase by calcium-dependent neutral protease. J. Biol. Chem. 258, 1156-1164.
77. Ishiura, S., Sugita, H., Suzuki, K. and Imahori, K. (1979) Studies of a calcium-activated neutral protease from chicken skeletal muscle. II. Substrate specificity. J. Biochem. 86, 579-581.
78. Suzuki, K., Ishiura, S., Tsuji, S., Katamoto, T., Sugita, H. and Imahori, K. (1979) Calcium activated neutral protease from human skeletal muscle. FEBS Lett. 104, 355-358.
79. Sugita, H., Ishiura, S., Suzuki, K. and Imahori, K. (1980) Ca-activated neutral protease and its inhibitors: in vitro effect on intact myofibrils. Muscle Nerve 3, 335-339.
80. Sugita, H., Ishiura, S., Suzuki, K. and Imahori, K. (1980) Inhibition of epoxide derivatives on chicken calcium-activated neutral protease (CANP) in vitro and in vivo. J. Biochem. 87, 339-341.
81. 2+ ions. J. Biochem. 90, 275-278.
82. Suzuki, K. (1982) Activation mechanism of calciumactivated neutral protease. Seikagaku 54, 1264-1270 (in Japanese).
83. 2+. FEBS Lett. 140, 16-18.
84. 2+-activated protease possibly involved in myofibrillar protein turnover. Purification from porcine muscle. Biochemistry 15, 2150-2158.
85. Ohno, S., Akita, Y., Hata, A., Osada, S., Kubo, K., Konno, Y., Akimoto, K., Mizuno, K., Saido, T., Kuroki, T. and Suzuki, K. (1991) Structural and functional diversities of a family of signal transducing protein kinases, protein kinase C family; two distinct classes of PKC, conventional cPKC and novel nPKC. Adv. Enzyme Regul. 31, 287-303.
86. Sorimachi, H., Tsukahara, T., Okada-Ban, M., Sugita, H., Ishiura, S. and Suzuki, K. (1995) Identification of a third ubiquitous calpain species-chicken muscle expresses four distinct calpains. Biochim. Biophys. Acta 1261, 381-393.
87. Macqueen, D.J., Delbridge, M.L., Manthri, S. and Johnston, I.A. (2010) A newly classified vertebrate calpain protease, directly ancestral to CAPN1 and 2, episodically evolved a restricted physiological function in placental mammals. Mol. Biol. Evol. 27, 1886-1902.
88. Berti, P.J. and Storer, A.C. (1995) Alignment/phylogeny of the papain superfamily of cysteine proteases. J. Mol. Biol. 246, 273-283.
89. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., He, S., Hurwitz, D.I., Jackson, J.D., Ke, Z., Lanczycki, C.J., Liebert, C.A., Liu, C., Lu, F., Lu, S., Marchler, G.H., Mullokandov, M., Song, J.S., Tasneem, A., Thanki, N., Yamashita, R.A., Zhang, D., Zhang, N. and Bryant, S.H. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37, D205-D210.
90. Pontremoli, S. and Melloni, E. (1988) The role of calpain and protein kinase C in activation of human neutrophils. Prog. Clin. Biol. Res. 282, 195-208.
91. Noguchi, M., Sarin, A., Aman, M.J., Nakajima, H., Shores, E.W., Henkart, P.A. and Leonard, W.J. (1997) Functional cleavage of the common cytokine receptor. chain (.c) by calpain. Proc. Natl. Acad. Sci. USA 94, 11534-11539.
92. Leloup, L., Shao, H., Bae, Y.H., Deasy, B., Stolz, D., Roy, P. and Wells, A. (2010) m-Calpain activation is regulated by its membrane localization and by its binding to phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 285, 33549-33566.
93. Mellgren, R.L., Zhang, W., Miyake, K. and McNeil, P.L. (2007) Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J. Biol. Chem. 282, 2567-2575.
94. Mellgren, R.L. and Huang, X. (2007) Fetuin A stabilizes m-calpain and facilitates plasma membrane repair. J. Biol. Chem. 282, 35868-35877.
95. Danial, N.N. and Korsmeyer, S.J. (2004) Cell death: critical control points. Cell 116, 205-219.
96. Nakagawa, T. and Yuan, J. (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150, 887-894.
97. 2+-activated protease. J. Biol. Chem. 257, 9072-9077.
98. Inomata, M., Kasai, Y., Nakamura, M. and Kawashima, S. (1988) Activation mechanism of calcium-activated neutral protease. Evidence for the existence of intramolecular and intermolecular autolyses. J. Biol. Chem. 263, 19783-19787.
99. 2+-dependent proteinases (7-calpain and m-calpain). J. Biol. Chem. 264, 10096-10103.
100. Nakagawa, K., Masumoto, H., Sorimachi, H. and Suzuki, K. (2001) Dissociation of m-calpain subunits occurs after autolysis of the N-terminus of the catalytic subunit, and is not required for activation. J. Biochem. 130, 605-611.
101. Pal, G.P., Elce, J.S. and Jia, Z. (2001) Dissociation and aggregation of calpain in the presence of calcium. J. Biol. Chem. 276, 47233-47238.
102. 2+. Biochem. Biophys. Res. Commun. 257, 63-66.
103. Li, H., Thompson, V.F. and Goll, D.E. (2004) Effects of autolysis on properties of 7- and mcalpain. Biochim. Biophys. Acta 1691, 91-103.
104. Zhang, W. and Mellgren, R.L. (1996) Calpain subunits remain associated during catalysis. Biochem. Biophys. Res. Commun. 227, 890-896.
105. 2+. J. Biol. Chem. 277, 40296-40301.
106. Elce, J.S., Davies, P.L., Hegadorn, C., Maurice, D.H. and Arthur, J.S. (1997) The effects of truncations of the small subunit on m-calpain activity and heterodimer formation. Biochem. J. 326, 31-38.
107. 2+-dependent cysteine protease. FEBS Lett. 501, 111-114.
108. 2+-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18, 6880-6889.
109. Strobl, S., Fernandez-Catalan, C., Braun, M., Huber, R., Masumoto, H., Nakagawa, K., Irie, A., Sorimachi, H., Bourenkow, G., Bartunik, H., Suzuki, K. and Bode, W. (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.
110. Hanna, R.A., Campbell, R.L. and Davies, P.L. (2008) Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 456, 409-412.
111. Moldoveanu, T., Gehring, K. and Green, D.R. (2008) Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature 456, 404-408.
112. 2+ switch aligns the active site of calpain. Cell 108, 649-660.
113. Moldoveanu, T., Hosfield, C.M., Lim, D., Jia, Z. and Davies, P.L. (2003) Calpain silencing by a reversible intrinsic mechanism. Nat. Struct. Biol. 10, 371-378.
114. 2+-regulated phospholipid-binding domain. Biochem. Biophys. Res. Commun. 280, 1333-1339.
115. Minami, Y., Emori, Y., Imajoh-Ohmi, S., Kawasaki, H. and Suzuki, K. (1988) Carboxyl-terminal truncation and site-directed mutagenesis of the EF hand structure-domain of the small subunit of rabbit calcium-dependent protease. J. Biochem. 104, 927-933.
116. 2+ ions. J. Biochem. 101, 889-895.
117. Lin, G.D., Chattopadhyay, D., Maki, M., Wang, K.K., Carson, M., Jin, L., Yuen, P.W., Takano, E., Hatanaka, M., DeLucas, L.J. and Narayana, S.V. (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.
118. 2+-binding proteins with five EF-hand motifs. Biochem. J. 328, 718-720.
119. 2+-induced conformational changes. Nat. Struct. Biol. 4, 532-538.
120. Imajoh, S., Kawasaki, H. and Suzuki, K. (1987) The COOH-terminal E-F hand structure of calciumactivated neutral protease (CANP) is important for the association of subunits and resulting proteolytic activity. J. Biochem. 101, 447-452.
121. Schad, E., Farkas, A., Jekely, G., Tompa, P. and Friedrich, P. (2002) A novel human small subunit of calpains. Biochem. J. 362, 383-388.
122. 2+ ions in this enzyme. J. Biochem. 90, 1405-1411.
123. 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.
124. duVerle, D., Takigawa, I., Ono, Y., Sorimachi, H. and Mamitsuka, H. (2010) CaMPDB: a resource for calpain and modulatory proteolysis. Genome Inform. 22, 202-213.
125. Davis, T.L., Walker, J.R., Finerty, P.J. Jr., Mackenzie, F., Newman, E.M. and Dhe-Paganon, S. (2007) The crystal structures of human calpains 1 and 9 imply diverse mechanisms of action and auto-inhibition. J. Mol. Biol. 366, 216-229.
126. 2+-activation apparatus at 3.0Å resolution. Science 329, 182-186.
127. Moldoveanu, T., Campbell, R.L., Cuerrier, D. and Davies, P.L. (2004) Crystal structures of calpain-E64 and -leupeptin inhibitor complexes reveal mobile loops gating the active site. J. Mol. Biol. 343, 1313-1326.
128. 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.
129. Zimmerman, U.J., Boring, L., Pak, J.H., Mukerjee, N. and Wang, K.K. (2000) The calpain small subunit gene is essential: its inactivation results in embryonic lethality. IUBMB Life 50, 63-68.
130. Yoshizawa, T., Sorimachi, H., Tomioka, S., Ishiura, S. and Suzuki, K. (1995) A catalytic subunit of calpain possesses full proteolytic activity. FEBS Lett. 358, 101-103.
131. Azam, M., Andrabi, S.S., Sahr, K.E., Kamath, L., Kuliopulos, A. and Chishti, A.H. (2001) Disruption of the mouse 7-calpain gene reveals an essential role in platelet function. Mol. Cell. Biol. 21, 2213-2220.
132. 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.
133. Mellgren, R.L., Zhang, W., Miyake, K. and McNeil, P.L. (2006) Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J. Biol. Chem. 282, 2567-2575.
134. Demarchi, F., Bertoli, C., Copetti, T., Tanida, I., Brancolini, C., Eskelinen, E.L. and Schneider, C. (2006) Calpain is required for macroautophagy in mammalian cells. J. Cell Biol. 175, 595-605.
135. Farkas, A., Tompa, P. and Friedrich, P. (2003) Revisiting ubiquity and tissue specificity of human calpains. Biol. Chem. 384, 945-949.
136. Hata, A., Ohno, S., Akita, Y. and Suzuki, K. (1989) Tandemly reiterated negative enhancer-like elements regulate transcription of a human gene for the large subunit of calcium-dependent protease. J. Biol. Chem. 264, 6404-6411.
137. Valerio, D., Duyvesteyn, M.G., Dekker, B.M., Weeda, G., Berkvens, T.M., van der Voorn, L., van Ormondt, H. and van der Eb, A.J. (1985) Adenosine deaminase: characterization and expression of a gene with a remarkable promoter. EMBO J. 4, 437-443.
138. Melton, D.W., McEwan, C., McKie, A.B. and Reid, A.M. (1986) Expression of the mouse HPRT gene: deletional analysis of the promoter region of an Xchromosome linked housekeeping gene. Cell 44, 319-328.
139. Angel, P., Imagawa, M., Chiu, R., Stein, B., Imbra, R.J., Rahmsdorf, H.J., Jonat, C., Herrlich, P. and Karin, M. (1987) Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell 49, 729-739.
140. Lee, W., Mitchell, P. and Tjian, R. (1987) Purified transcription factor AP-1 interacts with TPAinducible enhancer elements. Cell 49, 741-752.
141. Nakamura, M., Mori, M., Morishita, Y., Mori, S. and Kawashima, S. (1992) Specific increase in calcium-activated neutral protease with low calcium sensitivity (m-calpain) in proerythroblastic K562 cell line cells induced to differentiation by phorbol 12-myristate 13-acetate. Exp. Cell Res. 200, 513-522.
142. Miyake, S., Emori, Y. and Suzuki, K. (1986) Gene organization of the small subunit of human calcium-activated neutral protease. Nucleic Acids Res. 14, 8805-8817.
143. Emori, Y., Kawasaki, H., Imajoh, S., Imahori, K. and Suzuki, K. (1987) Endogenous inhibitor for calcium-dependent cysteine protease contains four internal repeats that could be responsible for its multiple reactive sites. Proc. Natl. Acad. Sci. USA 84, 3590-3594.
144. Maki, M., Takano, E., Mori, H., Kannagi, R., Murachi, T. and Hatanaka, M. (1987) Repetitive region of calpastatin is a functional unit of the proteinase inhibitor. Biochem. Biophys. Res. Commun. 143, 300-308.
145. Maki, M., Takano, E., Mori, H., Sato, A., Murachi, T. and Hatanaka, M. (1987) All four internally repetitive domains of pig calpastatin possess inhibitory activities against calpains I and II. FEBS Lett. 223, 174-180.
146. Hata, S., Doi, N., Kitamura, F. and Sorimachi, H. (2007) Stomach-specific calpain, nCL-2/calpain 8, is active without calpain regulatory subunit and oligomerizes through C2-like domains. J. Biol. Chem. 282, 27847-27856.
147. Lee, H.J., Tomioka, S., Kinbara, K., Masumoto, H., Jeong, S.Y., Sorimachi, H., Ishiura, S. and Suzuki, K. (1999) Characterization of a human digestive tract-specific calpain, nCL-4, expressed in the baculovirus system. Arch. Biochem. Biophys. 362, 22-31.
148. Takano, J., Tomioka, M., Tsubuki, S., Higuchi, M., Iwata, N., Itohara, S., Maki, M. and Saido, T.C. (2005) Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. J. Biol. Chem. 280, 16175-16184.
149. Higuchi, M., Tomioka, M., Takano, J., Shirotani, K., Iwata, N., Masumoto, H., Maki, M., Itohara, S. and Saido, T.C. (2005) Distinct mechanistic roles of calpain and caspase activation in neurodegeneration as revealed in mice overexpressing their specific inhibitors. J. Biol. Chem. 280, 15229-15237.
150. Spencer, M.J. and Mellgren, R.L. (2002) Overexpression of a calpastatin transgene in mdx muscle reduces dystrophic pathology. Hum. Mol. Genet. 11, 2645-2655.
151. Tidball, J.G. and Spencer, M.J. (2002) Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J. Physiol. 545, 819-828.
152. Kent, M.P., Spencer, M.J. and Koohmaraie, M. (2004) Postmortem proteolysis is reduced in transgenic mice overexpressing calpastatin. J. Anim. Sci. 82, 794-801.
153. Geesink, G.H., Kuchay, S., Chishti, A.H. and Koohmaraie, M. (2006) Micro-calpain is essential for postmortem proteolysis of muscle proteins. J. Anim. Sci. 84, 2834-2840.
154. Dear, T.N. and Boehm, T. (2001) Identification and characterization of two novel calpain large subunit genes. Gene 274, 245-252.
155. Andresen, K., Tom, T.D. and Strand, M. (1991) Characterization of cDNA clones encoding a novel calcium-activated neutral proteinase from Schistosoma mansoni. J. Biol. Chem. 266, 15085-15090.
156. Ersfeld, K., Barraclough, H. and Gull, K. (2005) Evolutionary relationships and protein domain architecture in an expanded calpain superfamily in kinetoplastid parasites. J. Mol. Evol. 61, 742-757.
157. Hata, S., Nishi, K., Kawamoto, T., Lee, H.J., Kawahara, H., Maeda, T., Shintani, Y., Sorimachi, H. and Suzuki, K. (2001) Both the conserved and the unique gene structure of stomach-specific calpains reveal processes of calpain gene evolution. J. Mol. Evol. 53, 191-203.
158. Futai, E., Kubo, T., Sorimachi, H., Suzuki, K. and Maeda, T. (2001) Molecular cloning of PalBH, a mammalian homologue of the Aspergillus atypical calpain PalB. Biochim. Biophys. Acta 1517, 316-319.
159. Li, M., Martin, S.J., Bruno, V.M., Mitchell, A.P. and Davis, D.A. (2004) Candida albicans Rim13p, a protease required for Rim101p processing at acidic and alkaline pHs. Eukaryot. Cell 3, 741-751.
160. Futai, E., Sorimachi, H., Jeong, S.Y., Kitamoto, K., Ishiura, S. and Suzuki, K. (1999) Aspergillus oryzae palBory encodes a calpain-like protease: homology to Emericella nidulans PalB and conservation of functional regions. J. Biosci. Bioeng. 88, 438-440.
161. Villalobo, E., Moch, C., Fryd-Versavel, G., Fleury-Aubusson, A. and Morin, L. (2003) Cysteine proteases and cell differentiation: excystment of the ciliated protist Sterkiella histriomuscorum. Eukaryot. Cell 2, 1234-1245.
162. Horikawa, Y., Oda, N., Cox, N.J., Li, X., Orho-Melander, M., Hara, M., Hinokio, Y., Lindner, T.H., Mashima, H., Schwarz, P.E., del Bosque-Plata, L., Horikawa, Y., Oda, Y., Yoshiuchi, I., Colilla, S., Polonsky, K.S., Wei, S., Concannon, P., Iwasaki, N., Schulze, J., Baier, L.J., Bogardus, C., Groop, L., Boerwinkle, E., Hanis, C.L. and Bell, G.I. (2000) Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nat. Genet. 26, 163-175.
163. Margis, R. and Margis-Pinheiro, M. (2003) Phytocalpains: orthologous calcium-dependent cysteine proteinases. Trends Plant Sci. 8, 58-62.
164. Wang, C., Barry, J.K., Min, Z., Tordsen, G., Rao, A.G. and Olsen, O.A. (2003) The calpain domain of the maize DEK1 protein contains the conserved catalytic triad and functions as a cysteine proteinase. J. Biol. Chem. 278, 34467-34474.
165. Lid, S.E., Olsen, L., Nestestog, R., Aukerman, M., Brown, R.C., Lemmon, B., Mucha, M., Opsahl-Sorteberg, H.G. and Olsen, O.A. (2005) Mutation in the Arabidopisis thaliana DEK1 calpain gene perturbs endosperm and embryo development while over-expression affects organ development globally. Planta 221, 339-351.
166. Ahn, J.W., Kim, M., Lim, J.H., Kim, G.T. and Pai, H.S. (2004) Phytocalpain controls the proliferation and differentiation fates of cells in plant organ development. Plant J. 38, 969-981.
167. Bourgeau, G., Lapointe, H., Peloquin, P. and Mayrand, D. (1992) Cloning, expression, and sequencing of a protease gene (tpr) from Porphyromonas gingivalis W83 in Escherichia coli. Infect. Immun. 60, 3186-3192.
168. Wu, K.H. and Tai, P.C. (2004) Cys32 and His105 are the critical residues for the calcium-dependent cysteine proteolytic activity of CvaB, an ATPbinding cassette transporter. J. Biol. Chem. 279, 901-909.
169. Sorimachi, H., Saido, T.C. and Suzuki, K. (1994) New era of calpain research. Discovery of tissuespecific calpains. FEBS Lett. 343, 1-5.
170. Badalamente, M.A. and Stracher, A. (2000) Delay of muscle degeneration and necrosis in mdx mice by calpain inhibition. Muscle Nerve 23, 106-111.
171. Bartus, R.T., Hayward, N.J., Elliott, P.J., Sawyer, S.D., Baker, K.L., Dean, R.L., Akiyama, A., Straub, J.A., Harbeson, S.L., Li, Z. and Powers, J. (1994) Calpain inhibitor AK295 protects neurons from focal brain ischemia. Effects of postocclusion intra-arterial administration. Stroke 25, 2265-2270.
172. Sorimachi, H., Forsberg, N.E., Lee, H.J., Joeng, S.Y., Richard, I., Beckmann, J.S., Ishiura, S. and Suzuki, K. (1996) Highly conserved structure in the promoter region of the gene for muscle-specific calpain, p94. Biol. Chem. 377, 859-864.
173. Kawabata, Y., Hata, S., Ono, Y., Ito, Y., Suzuki, K., Abe, K. and Sorimachi, H. (2003) Newly identified exons encoding novel variants of p94/calpain 3 are expressed ubiquitously and overlap the,-glucosidase C gene. FEBS Lett. 555, 623-630.
174. De Tullio, R., Stifanese, R., Salamino, F., Pontremoli, S. and Melloni, E. (2003) Characterization of a new p94-like calpain form in human lymphocytes. Biochem. J. 375, 689-696.
175. König, N., Raynaud, F., Feane, H., Durand, M., Mestre-Francès, N., Rossel, M., Ouali, A. and Benyamin, Y. (2003) Calpain 3 is expressed in astrocytes of rat and Microcebus brain. J. Chem. Neuroanat. 25, 129-136.
176. Azuma, M., Fukiage, C., Higashine, M., Nakajima, T., Ma, H. and Shearer, T.R. (2000) Identification and characterization of a retina-specific calpain (Rt88) from rat. Curr. Eye Res. 21, 710-720.
177. Ma, H., Fukiage, C., Azuma, M. and Shearer, T.R. (1998) Cloning and expression of mRNA for calpain Lp82 from rat lens: splice variant of p94. Invest. Ophthalmol. Vis. Sci. 39, 454-461.
178. Fougerousse, F., Bullen, P., Herasse, M., Lindsay, S., Richard, I., Wilson, D., Suel, L., Durand, M., Robson, S., Abitbol, M., Beckmann, J.S. and Strachan, T. (2000) Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum. Mol. Genet. 9, 165-173.
179. 2+-binding domain. J. Biol. Chem. 268, 19476-19482.
180. Sorimachi, H., Imajoh-Ohmi, S., Emori, Y., Kawasaki, H., Ohno, S., Minami, Y. and Suzuki, K. (1989) Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and 7-types. Specific expression of the mRNA in skeletal muscle. J. Biol. Chem. 264, 20106-20111.
181. Sorimachi, H., Toyama-Sorimachi, N., Saido, T.C., Kawasaki, H., Sugita, H., Miyasaka, M., Arahata, K., Ishiura, S. and Suzuki, K. (1993) Musclespecific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268, 10593-10605.
182. Ono, Y., Hayashi, C., Doi, N., Kitamura, F., Shindo, M., Kudo, K., Tsubata, T., Yanagida, M. and Sorimachi, H. (2007) Comprehensive survey of p94/calpain 3 substrates by comparative proteomics-Possible regulation of protein synthesis by p94. Biotechnol. J. 2, 565-576.
183. Ono, Y., Torii, F., Ojima, K., Doi, N., Yoshioka, K., Kawabata, Y., Labeit, D., Labeit, S., Suzuki, K., Abe, K., Maeda, T. and Sorimachi, H. (2006) Suppressed disassembly of autolyzing p94/CAPN3 by N2A connectin/titin in a genetic reporter system. J. Biol. Chem. 281, 18519-18531.
184. Sorimachi, H., Kinbara, K., Kimura, S., Takahashi, M., Ishiura, S., Sasagawa, N., Sorimachi, N., Shimada, H., Tagawa, K., Maruyama, K. and Suzuki, K. (1995) Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence. J. Biol. Chem. 270, 31158-31162.
185. Chiannilkulchai, N., Pasturaud, P., Richard, I., Auffray, C. and Beckmann, J.S. (1995) A primary expression map of the chromosome 15q15 region containing the recessive form of limb-girdle muscular dystrophy (LGMD2A) gene. Hum. Mol. Genet. 4, 717-725.
186. Richard, I., Roudaut, C., Marchand, S., Baghdiguian, S., Herasse, M., Stockholm, D., Ono, Y., Suel, L., Bourg, N., Sorimachi, H., Lefranc, G., Fardeau, M., Sebille, A. and Beckmann, J.S. (2000) Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated I5B,/nuclear factor 5B pathway perturbation in mice. J. Cell Biol. 151, 1583-1590.
187. Kramerova, I., Kudryashova, E., Tidball, J.G. and Spencer, M.J. (2004) Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum. Mol. Genet. 13, 1373-1388.
188. 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.
189. Ojima, K., Kawabata, Y., Nakao, H., Nakao, K., Doi, N., Kitamura, F., Ono, Y., Hata, S., Suzuki, H., Kawahara, H., Bogomolovas, J., Witt, C., Ottenheijm, C., Labeit, S., Granzier, H., Toyama-Sorimachi, N., Sorimachi, M., Suzuki, K., Maeda, T., Abe, K., Aiba, A. and Sorimachi, H. (2010) Role of dynamic distribution of muscle-specific calpain in physical-stress adaptation and muscular dystrophy in mice. J. Clin. Invest. 120, 2672-2683.
190. Richard, I., Roudaut, C., Saenz, A., Pogue, R., Grimbergen, J.E., Anderson, L.V., Beley, C., Cobo, A.M., de Diego, C., Eymard, B., Gallano, P., Ginjaar, H.B., Lasa, A., Pollitt, C., Topaloglu, H., Urtizberea, J.A., de Visser, M., van der Kooi, A., Bushby, K., Bakker, E., Lopez de Munain, A., Fardeau, M. and Beckmann, J.S. (1999) Calpainopathy -a survey of mutations and polymorphisms. Am. J. Hum. Genet. 64, 1524-1540.
191. Sáenz, A., Leturcq, F., Cobo, A.M., Poza, J.J., Ferrer, X., Otaegui, D., Camaño, P., Urtasun, M., Vílchez, J., Gutiérrez-Rivas, E., Emparanza, J., Merlini, L., Paisán, C., Goicoechea, M., Blázquez, L., Eymard, B., Lochmuller, H., Walter, M., Bonnemann, C., Figarella-Branger, D., Kaplan, J.C., Urtizberea, J.A., Martí-Massó, J.F. and López de Munain, A. (2005) LGMD2A: genotype-phenotype correlations based on a large mutational survey on the calpain 3 gene. Brain 128, 732-742.
192. Hata, S., Koyama, S., Kawahara, H., Doi, N., Maeda, T., Toyama-Sorimachi, N., Abe, K., Suzuki, K. and Sorimachi, H. (2006) Stomachspecific calpain, nCL-2, localizes in mucus cells and proteolyzes the O-subunit of coatomer complex, O-COP. J. Biol. Chem. 281, 11214-11224.
193. Lee, H.J., Sorimachi, H., Jeong, S.Y., Ishiura, S. and Suzuki, K. (1998) Molecular cloning and characterization of a novel tissue-specific calpain predominantly expressed in the digestive tract. Biol. Chem. 379, 175-183.
194. Cao, Y., Zhao, H. and Grunz, H. (2001) xCL-2 is a novel m-type calpain and disrupts morphogenetic movements during embryogenesis in Xenopus laevis. Dev. Growth Differ. 43, 563-571.
195. Liu, K., Li, L. and Cohen, S.N. (2000) Antisense RNA-mediated deficiency of the calpain protease, nCL-4, in NIH3T3 cells is associated with neoplastic transformation and tumorigenesis. J. Biol. Chem. 275, 31093-31098.
196. Chen, C.J., Nguyen, T. and Shively, J.E. (2010) Role of calpain-9 and PKC-/ in the apoptotic mechanism of lumen formation in CEACAM1 transfected breast epithelial cells. Exp. Cell Res. 316, 638-648.
197. Caddick, M.X., Brownlee, A.G. and Arst, H.N. Jr. (1986) Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol. Gen. Genet. 203, 346-353.
198. Arst, H.N. Jr., Bailey, C.R. and Penfold, H.A. (1980) A possible rôle for acid phosphatase in .-amino-n-butyrate uptake in Aspergillus nidulans. Arch. Microbiol. 125, 153-158.
199. Arst, H.N. Jr., Bignell, E. and Tilburn, J. (1994) Two new genes involved in signalling ambient pH in Aspergillus nidulans. Mol. Gen. Genet. 245, 787-790.
200. Negrete-Urtasun, S., Denison, S.H. and Arst, H.N. Jr. (1997) Characterization of the pH signal transduction pathway gene palA of Aspergillus nidulans and identification of possible homologs. J. Bacteriol. 179, 1832-1835.
201. Maccheroni, W. Jr., May, G.S., Martinez-Rossi, N.M. and Rossi, A. (1997) The sequence of palF, an environmental pH response gene in Aspergillus nidulans. Gene 194, 163-167.
202. Denison, S.H., Negrete-Urtasun, S., Mingot, J.M., Tilburn, J., Mayer, W.A., Goel, A., Espeso, E.A., Peñalva, M.A. and Arst, H.N. Jr. (1998) Putative membrane components of signal transduction pathways for ambient pH regulation in Aspergillus and meiosis in Saccharomyces are homologous. Mol. Microbiol. 30, 259-264.
203. Negrete-Urtasun, S., Reiter, W., Diez, E., Denison, S.H., Tilburn, J., Espeso, E.A., Peñalva, M.A. and Arst, H.N. (1999) Ambient pH signal transduction in Aspergillus: completion of gene characterization. Mol. Microbiol. 33, 994-1003.
204. Herranz, S., Rodríguez, J.M., Bussink, H.J., Sanchez-Ferrero, J.C., Arst, H.N. Jr., Peñalva, M.A. and Vincent, O. (2005) Arrestin-related proteins mediate pH signaling in fungi. Proc. Natl. Acad. Sci. USA 102, 12141-12146.
205. Ridge, K.D., Abdulaev, N.G., Sousa, M. and Palczewski, K. (2003) Phototransduction: crystal clear. Trends Biochem. Sci. 28, 479-487.
206. Hervás-Aguilar, A., Rodríguez, J.M., Tilburn, J., Arst, H.N. Jr. and Peñalva, M.A. (2007) Evidence for the direct involvement of the proteasome in the proteolytic processing of the Aspergillus nidulans zinc finger transcription factor PacC. J. Biol. Chem. 282, 34735-34747.
207. Diez, E., Alvaro, J., Espeso, E.A., Rainbow, L., Suarez, T., Tilburn, J., Arst, H.N. Jr. and Peñalva, M.A. (2002) Activation of the Aspergillus PacC zinc finger transcription factor requires two proteolytic steps. EMBO J. 21, 1350-1359.
208. Mingot, J.M., Tilburn, J., Diez, E., Bignell, E., Orejas, M., Widdick, D.A., Sarkar, S., Brown, C.V., Caddick, M.X., Espeso, E.A., Arst, H.N. Jr. and Peñalva, M.A. (1999) Specificity determinants of proteolytic processing of Aspergillus PacC transcription factor are remote from the processing site, and processing occurs in yeast if pH signalling is bypassed. Mol. Cell. Biol. 19, 1390-1400.
209. Attaix, D., Ventadour, S., Codran, A., Bechet, D., Taillandier, D. and Combaret, L. (2005) The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem. 41, 173-186.
210. Murakami, Y., Matsufuji, S., Kameji, T., Hayashi, S., Igarashi, K., Tamura, T., Tanaka, K. and Ichihara, A. (1992) Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360, 597-599.
211. Orian, A., Whiteside, S., Israël, A., Stancovski, I., Schwartz, A.L. and Ciechanover, A. (1995) Ubiquitin-mediated processing of NF-5B transcriptional activator precursor p105. Reconstitution of a cell-free system and identification of the ubiquitin-carrier protein, E2, and a novel ubiquitin-protein ligase, E3, involved in conjugation. J. Biol. Chem. 270, 21707-21714.
212. Palombella, V.J., Rando, O.J., Goldberg, A.L. and Maniatis, T. (1994) The ubiquitin-proteasome pathway is required for processing the NF-5B1 precursor protein and the activation of NF-5B. Cell 78, 773-785.
213. Su, S.S. and Mitchell, A.P. (1993) Molecular characterization of the yeast meiotic regulatory gene RIM1. Nucleic Acids Res. 21, 3789-3797.
214. Su, S.S. and Mitchell, A.P. (1993) Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 133, 67-77.
215. Li, W. and Mitchell, A.P. (1997) Proteolytic activation of Rim1p, a positive regulator of yeast sporulation and invasive growth. Genetics 145, 63-73.
216. Mitchell, B.M., Wu, T.G., Jackson, B.E. and Wilhelmus, K.R. (2007) Candida albicans straindependent virulence and Rim13p-mediated filamentation in experimental keratomycosis. Invest. Ophthalmol. Vis. Sci. 48, 774-780.
217. Davis, D., Wilson, R.B. and Mitchell, A.P. (2000) RIM101-dependent and -independent pathways govern pH responses in Candida albicans. Mol. Cell. Biol. 20, 971-978.
218. Lambert, M., Blanchin-Roland, S., Le Louedec, F., Lépingle, A. and Gaillardin, C. (1997) Genetic analysis of regulatory mutants affecting synthesis of extracellular proteinases in the yeast Yarrowia lipolytica: identification of a RIM101/pacC homolog. Mol. Cell. Biol. 17, 3966-3976.
219. González-López, C.I., Ortiz-Castellanos, L. and Ruiz-Herrera, J. (2006) The ambient pH response Rim pathway in Yarrowia lipolytica: identification of YlRIM9 and characterization of its role in dimorphism. Curr. Microbiol. 53, 8-12.
220. Aréchiga-Carvajal, E.T. and Ruiz-Herrera, J. (2005) The RIM101/pacC homologue from the basidiomycete Ustilago maydis is functional in multiple pH-sensitive phenomena. Eukaryot. Cell 4, 999-1008.
221. Rodríguez-Galán, O., Galindo, A., Hervás-Aguilar, A., Arst, H.N. Jr. and Peñalva, M.A. (2009) Physiological involvement in pH signaling of Vps24-mediated recruitment of Aspergillus PalB cysteine protease to ESCRT-III. J. Biol. Chem. 284, 4404-4412.
222. Tilburn, J., Sánchez-Ferrero, J.C., Reoyo, E., Arst, H.N. Jr. and Peñalva, M.A. (2005) Mutational analysis of the pH signal transduction component PalC of Aspergillus nidulans supports distant similarity to BRO1 domain family members. Genetics 171, 393-401.
223. Xu, W., Smith, F.J. Jr., Subaran, R. and Mitchell, A.P. (2004) Multivesicular body-ESCRT components function in pH response regulation in Saccharomyces cerevisiae and Candida albicans. Mol. Biol. Cell 15, 5528-5537.
224. Cornet, M., Bidard, F., Schwarz, P., Da Costa, G., Blanchin-Roland, S., Dromer, F. and Gaillardin, C. (2005) Deletions of endocytic components VPS28 and VPS32 affect growth at alkaline pH and virulence through both RIM101-dependent and RIM101-independent pathways in Candida albicans. Infect. Immun. 73, 7977-7987.
225. Barwell, K.J., Boysen, J.H., Xu, W. and Mitchell, A.P. (2005) Relationship of DFG16 to the Rim101p pH response pathway in Saccharomyces cerevisiae and Candida albicans. Eukaryot. Cell 4, 890-899.
226. Blanchin-Roland, S., Da Costa, G. and Gaillardin, C. (2005) ESCRT-I components of the endocytic machinery are required for Rim101-dependent ambient pH regulation in the yeast Yarrowia lipolytica. Microbiology 151, 3627-3637.
227. Boysen, J.H. and Mitchell, A.P. (2006) Control of Bro1-domain protein Rim20 localization by external pH, ESCRT machinery, and the Saccharomyces cerevisiae Rim101 pathway. Mol. Biol. Cell 17, 1344-1353.
228. Kullas, A.L., Li, M. and Davis, D.A. (2004) Snf7p, a component of the ESCRT-III protein complex, is an upstream member of the RIM101 pathway in Candida albicans. Eukaryot. Cell 3, 1609-1618.
229. Rothfels, K., Tanny, J.C., Molnar, E., Friesen, H., Commisso, C. and Segall, J. (2005) Components of the ESCRT pathway, DFG16, and YGR122w are required for Rim101 to act as a corepressor with Nrg1 at the negative regulatory element of the DIT1 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 25, 6772-6788.
230. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M. and Sakaki, Y. (2001) A comprehensive twohybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98, 4569-4574.
231. 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.
232. Yorikawa, C., Takaya, E., Osako, Y., Tanaka, R., Terasawa, Y., Hamakubo, T., Mochizuki, Y., Iwanari, H., Kodama, T., Maeda, T., Hitomi, K., Shibata, H. and Maki, M. (2008) Human calpain 7/PalBH associates with a subset of ESCRT-III-related proteins in its N-terminal region and partly localizes to endocytic membrane compartments. J. Biochem. 143, 731-745.
233. Osako, Y., Maemoto, Y., Tanaka, R., Suzuki, H., Shibata, H. and Maki, M. (2010) Autolytic activity of human calpain 7 is enhanced by ESCRT-III-related protein IST1 through MITMIM interaction. FEBS J. 277, 4412-4426.
234. Katoh, K., Shibata, H., Suzuki, H., Nara, A., Ishidoh, K., Kominami, E., Yoshimori, T. and Maki, M. (2003) The ALG-2-interacting protein Alix associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting. J. Biol. Chem. 278, 39104-39113.
235. Missotten, M., Nichols, A., Rieger, K. and Sadoul, R. (1999) Alix, a novel mouse protein undergoing calcium-dependent interaction with the apoptosis-linked-gene 2 (ALG-2) protein. Cell Death Differ. 6, 124-129.
236. Sadoul, R. (2006) Do Alix and ALG-2 really control endosomes for better or for worse? Biol. Cell 98, 69-77.
237. 2+-dependent reaction. J. Biol. Chem. 274, 1533-1540.
238. Odorizzi, G. (2006) The multiple personalities of Alix. J. Cell Sci. 119, 3025-3032.
239. 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.
240. Sokol, S.B. and Kuwabara, P.E. (2000) Proteolysis in Caenorhabditis elegans sex determination: cleavage of TRA-2A by TRA-3. Genes Dev. 14, 901-906.
241. Syntichaki, P., Xu, K., Driscoll, M. and Tavernarakis, N. (2002) Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419, 939-944.
242. Kammenga, J.E., Doroszuk, A., Riksen, J.A., Hazendonk, E., Spiridon, L., Petrescu, A.J., Tijsterman, M., Plasterk, R.H. and Bakker, J. (2007) A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet. 3, e34.
243. 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.
244. Mugita, N., Kimura, Y., Ogawa, M., Saya, H. and Nakao, M. (1997) Identification of a novel, tissuespecific calpain htra-3; a human homologue of the Caenorhabditis elegans sex determination gene. Biochem. Biophys. Res. Commun. 239, 845-850.
245. Waghray, A., Wang, D.S., McKinsey, D., Hayes, R.L. and Wang, K.K. (2004) Molecular cloning and characterization of rat and human calpain-5. Biochem. Biophys. Res. Commun. 324, 46-51.
246. Franz, T., Winckler, L., Boehm, T. and Dear, T.N. (2004) Capn5 is expressed in a subset of T cells and is dispensable for development. Mol. Cell. Biol. 24, 1649-1654.
247. Gonzalez, A., Saez, M.E., Aragon, M.J., Galan, J.J., Vettori, P., Molina, L., Rubio, C., Real, L.M., Ruiz, A. and Ramirez-Lorca, R. (2006) Specific haplotypes of the CALPAIN-5 gene are associated with polycystic ovary syndrome. Hum. Reprod. 21, 943-951.
248. Sáez, M.E., Martinez-Larrad, M.T., Ramirez-Lorca, R., Gonzalez-Sánchez, J.L., Zabena, C., Martinez-Calatrava, M.J., González, A., Morón, F.J., Ruiz, A. and Serrano-Ríos, M. (2007) Calpain-5 gene variants are associated with diastolic blood pressure and cholesterol levels. BMC Med. Genet. 8, 1.
249. Fan, C., Iacobas, D.A., Zhou, D., Chen, Q., Lai, J.K., Gavrialov, O. and Haddad, G.G. (2005) Gene expression and phenotypic characterization of mouse heart after chronic constant or intermittent hypoxia. Physiol. Genomics 22, 292-307.
250. Tonami, K., Kurihara, Y., Aburatani, H., Uchijima, Y., Asano, T. and Kurihara, H. (2007) Calpain 6 is involved in microtubule stabilization and cytoskeletal organization. Mol. Cell. Biol. 27, 2548-2561.
251. Tonami, K., Kurihara, Y., Arima, S., Nishiyama, K., Uchijima, Y., Asano, T., Sorimachi, H. and Kurihara, H. (2011) Calpain 6, a microtubulestabilizing protein, regulates Rac1 activity and cell motility through interaction with GEF-H1. J. Cell Sci. 124, 1214-1223.
252. Baier, L.J., Permana, P.A., Yang, X., Pratley, R.E., Hanson, R.L., Shen, G.Q., Mott, D., Knowler, W.C., Cox, N.J., Horikawa, Y., Oda, N., Bell, G.I. and Bogardus, C. (2000) A calpain-10 gene polymorphism is associated with reduced muscle mRNA levels and insulin resistance. J. Clin. Invest. 106, R69-R73.
253. Stumvoll, M., Fritsche, A., Madaus, A., Stefan, N., Weisser, M., Machicao, F. and Häring, H. (2001) Functional significance of the UCSNP-43 polymorphism in the CAPN10 gene for proinsulin processing and insulin secretion in nondiabetic Germans. Diabetes 50, 2161-2163.
254. Muramatsu, Y., Taniguchi, Y., Kose, H., Matsumoto, K., Yamada, T. and Sasaki, Y. (2003) Capn10, a candidate gene responsible for type 2 diabetes mellitus in the OLETF rat. IUBMB Life 55, 533-537.
255. Cheverud, J.M., Fawcett, G.L., Jarvis, J.P., Norgard, E.A., Pavlicev, M., Pletscher, L.S., Polonsky, K.S., Ye, H., Bell, G.I. and Semenkovich, C.F. (2010) Calpain-10 is a component of the obesity-related quantitative trait locus Adip1. J. Lipid Res. 51, 907-913.
256. Johnson, J.D., Han, Z., Otani, K., Ye, H., Zhang, Y., Wu, H., Horikawa, Y., Misler, S., Bell, G.I. and Polonsky, K.S. (2004) RyR2 and calpain-10 delineate a novel apoptosis pathway in pancreatic islets. J. Biol. Chem. 279, 24794-24802.
257. Ma, H., Fukiage, C., Kim, Y.H., Duncan, M.K., Reed, N.A., Shih, M., Azuma, M. and Shearer, T.R. (2001) Characterization and expression of calpain 10. A novel ubiquitous calpain with nuclear localization. J. Biol. Chem. 276, 28525-28531.
258. Paul, D.S., Harmon, A.W., Winston, C.P. and Patel, Y.M. (2003) Calpain facilitates GLUT4 vesicle translocation during insulin-stimulated glucose uptake in adipocytes. Biochem. J. 376, 625-632.
259. Arrington, D.D., Van Vleet, T.R. and Schnellmann, R.G. (2006) Calpain 10: a mitochondrial calpain and its role in calcium-induced mitochondrial dysfunction. Am. J. Physiol. Cell Physiol. 291, C1159-C1171.
260. 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.
261. Kamei, M., Webb, G.C., Heydon, K., Hendry, I.A., Young, I.G. and Campbell, H.D. (2000) Solh, the mouse homologue of the Drosophila melanogaster small optic lobes gene: organization, chromosomal mapping, and localization of gene product to the olfactory bulb. Genomics 64, 82-89.
262. Correa, G.C., Margis-Pinheiro, M. and Margis, R. (2001) Identification, classification and expression pattern analysis of sugarcane cysteine proteinases. Genet. Mol. Biol. 24, 275-283.
263. Johnson, K.L., Degnan, K.A., Ross Walker, J. and Ingram, G.C. (2005) AtDEK1 is essential for specification of embryonic epidermal cell fate. Plant J. 44, 114-127.
264. Tian, Q., Olsen, L., Sun, B., Lid, S.E., Brown, R.C., Lemmon, B.E., Fosnes, K., Gruis, D.F., Opsahl-Sorteberg, H.G., Otegui, M.S. and Olsen, O.A. (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19, 3127-3145.
265. Hirokawa, T., Boon-Chieng, S. and Mitaku, S. (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378-379.
266. Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580.
267. Ersfeld, K., Barraclough, H. and Gull, K. (2005) Evolutionary relationships and protein domain architecture in an expanded calpain superfamily in kinetoplastid parasites. J. Mol. Evol. 61, 742-757.
268. Andrade, H.M., Murta, S.M., Chapeaurouge, A., Perales, J., Nirdé, P. and Romanha, A.J. (2008) Proteomic analysis of Trypanosoma cruzi resistance to Benznidazole. J. Proteome Res. 7, 2357-2367.
269. Giese, V., Dallagiovanna, B., Marchini, F.K., Pavoni, D.P., Krieger, M.A. and Goldenberg, S. (2008) Trypanosoma cruzi: a stage-specific calpain-like protein is induced after various kinds of stress. Mem. Inst. Oswaldo Cruz 103, 598-601.
270. Hertz-Fowler, C., Ersfeld, K. and Gull, K. (2001) CAP5.5, a life-cycle-regulated, cytoskeleton-associated protein is a member of a novel family of calpain-related proteins in Trypanosoma brucei. Mol. Biochem. Parasitol. 116, 25-34.
271. Olego-Fernandez, S., Vaughan, S., Shaw, M.K., Gull, K. and Ginger, M.L. (2009) Cell morphogenesis of Trypanosoma brucei requires the paralogous, differentially expressed calpain-related proteins CAP5.5 and CAP5.5V. Protist 160, 576-590.
272. Pereira, F.M., Elias, C.G., D'Avila-Levy, C.M., Branquinha, M.H. and Santos, A.L. (2009) Cysteine peptidases in Herpetomonas samuelpessoai are modulated by temperature and dimethylsulfoxide-triggered differentiation. Parasitology 136, 45-54.
273. Sangenito, L.S., Ennes-Vidal, V., Marinho, F.A., Da Mota, F.F., Santos, A.L., D'Avila-Levy, C.M. and Branquinha, M.H. (2009) Arrested growth of Trypanosoma cruzi by the calpain inhibitor MDL28170 and detection of calpain homologues in epimastigote forms. Parasitology 136, 433-441.
274. Saido, T.C., Sorimachi, H. and Suzuki, K. (1994) Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J. 8, 814-822.
275. Imahori, K. (1987) Calcium-dependent proteases. Tanpakushitsu Kakusan Koso 32, 93-95 (in Japanese).