The calpains in aging and aging-related diseases

Ageing Research Reviews

Volumn 2, Issue 4, 2003, Pages 407-418

  Nixon, Ralph A ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Calpains; Amyloid

Indexed keywords

AMYLOID BETA PROTEIN; CALPAIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ARTHRITIS; CATARACT; CELL MOTILITY; CYTOSKELETON; DEGENERATIVE DISEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYMOLOGY; GERIATRIC DISORDER; HUMAN; HYPERTENSION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION;

EID: 0141762744     PISSN: 15681637     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1568-1637(03)00029-1     Document Type: Review

References (113)

1. Adachi Y., Ishida-Takahashi A., Takahashi C., Takano E., Murachi T., Hatanaka M. Phosphorylation and subcellular distribution of calpastatin in human hematopoietic system cells. J. Biol. Chem. 266:1991;3968-3972.
2. Adamec E., Murrell J.R., Takao M., Hobbs W., Nixon R.A., Ghetti B., Vonsattel J.P. P301L tauopathy: confocal immunofluorescence study of perinuclear aggregation of the mutated protein. J. Neurol. Sci. 200:2002a;85-93.
3. Adamec E., Mohan P., Vonsattel J.P., Nixon R.A. Calpain activation in neurodegenerative diseases: confocal immunofluorescence study with antibodies specifically recognizing the active form of calpain 2. Acta Neuropathol. (Berl.). 104:2002;92-104.
4. Aizawa H., Saito Y., Nakamura T., Inoue M., Imanari T., Ohyama Y., Matsumura Y., Masuda H., Oba S., Mise N., Kimura K., Hasegawa A., Kurabayashi M., Kuro-o M., Nabeshima Y., Nagai R. Downregulation of the Klotho gene in the kidney under sustained circulatory stress in rats. Biochem. Biophys. Res. Commun. 249:1998;865-871.
5. Arthur J.S., Elce J.S., Hegadorn C., Williams K., Greer P.A. 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. 20:2000;4474-4481.
6. Aszodi A., Muller U., Friedrich P., Spatz H.C. Signal convergence on protein kinase A as a molecular correlate of learning. Proc. Natl. Acad. Sci. U.S.A. 88:1991;5832-5836.
7. Averna M., De Tullio R., Salamino F., Minafra R., Pontremoli S., Melloni E. Age-dependent degradation of calpastatin in kidney of hypertensive rats. J. Biol. Chem. 276:2001;38426-38432.
8. Azuma M., Shearer T.R. Involvement of calpain in diamide-induced cataract in cultured lenses. FEBS Lett. 307:1992;313-317.
9. Azuma M., Shearer T.R., Matsumoto T., David L.L., Murachi T. Calpain II in two in vivo models of sugar cataract. Exp. Eye Res. 51:1990;393-401.
10. 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., Bogardus C. A calpain-10 gene polymorphism is associated with reduced muscle mRNA levels and insulin resistance. J. Clin. Invest. 106:2000;R69-73.
11. Bartus R.T. The Calpain Hypothesis of Neurodegeneration: Evidence for a Common Cytotoxic Pathway. Neuroscientist. 3:1997;314-327.
12. Battaglia, F., Trinchese, F., Liu, S., Walter, S., Nixon, R.A., Arancio, O., 2003. Position Paper: calpain inhibitors, a treatment for Alzheimer's disease. J. Mol. Neurosci., in press.
13. Baudry M., DuBrin R., Beasley L., Leon M., Lynch G. Low levels of calpain activity in Chiroptera brain: implications for mechanisms of aging. Neurobiol. Aging. 7:1986;255-258.
14. Benuck M., Banay-Schwartz M., DeGuzman T., Lajtha A. Changes in brain protease activity in aging. J. Neurochem. 67:1996;2019-2029.
15. Besse S., Delcayre C., Chevalier B., Hardouin S., Heymes C., Bourgeois F., Moalic J.M., Swynghedauw B. Is the senescent heart overloaded and already failing. Cardiovasc. Drugs Ther. 8:1994;581-587. Review.
16. Blalock E.M., Porter N.M., Landfield P.W. Decreased G-protein-mediated regulation and shift in calcium channel types with age in hippocampal cultures. J. Neurosci. 19:1999;8674-8684.
17. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., Hof P.R. Tau protein isoforms. Brain Res. Brain Res. Rev. 33:2000;95-130. Review.
18. Carafoli E., Molinari M. Calpain: a protease in search of a function. Biochem. Biophys. Res. Commun. 247:1998;193-203. Review.
19. Chen M., He H., Zhan S., Krajewski S., Reed J.C., Gottlieb R.A. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J. Biol. Chem. 276:2001;30724-30728.
20. Chen M., Won D.J., Krajewski S., Gottlieb R.A. Calpain and mitochondria in ischemia/reperfusion injury. J. Biol. Chem. 277:2002;29181-29186.
21. Croall D.E., DeMartino G.N. Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol. Rev. 71:1991;813-847. Review.
22. Crocker S.J., Smith P.D., Jackson-Lewis V., Lamba W.R., Hayley S.P., Grimm E., Callaghan S.M., Slack R.S., Melloni E., Przedborski S., Robertson G.S., Anisman H., Merali Z., Park D.S. Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J. Neurosci. 23:2003;4081-4091.
23. Cuervo A.M., Dice J.F. Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275:2000a;31505-31513.
24. Cuervo A.M., Dice J.F. When lysosomes get old. Exp. Gerontol. 35:2000b;119-131. Review.
25. David L.L., Wright J.W., Shearer T.R. Calpain II induced insolubilization of lens beta-crystallin polypeptides may induce cataract. Biochim. Biophys. Acta. 1139:1992;210-216.
26. 2+ requirement, and heterodimer stability in m-calpain. J. Biol. Chem. 272:1997;11268-11275.
27. Friguet B., Bulteau A.L., Chondrogianni N., Conconi M., Petropoulos I. Protein degradation by the proteasome and its implications in aging. Ann. NY Acad. Sci. 908:2000;143-154. Review.
28. Gil-Parrado S., Fernandez-Montalvan A., Assfalg-Machleidt I., Popp O., Bestvater F., Holloschi A., Knoch T.A., Auerswald E.A., Welsh K., Reed J.C., Fritz H., Fuentes-Prior P., Spiess E., Salvesen G.S., Machleidt W. Ionomycin-activated calpain triggers apoptosis. A probable role for Bcl-2 family members. J. Biol. Chem. 277:2002;27217-27226.
29. Gil-Parrado S., Popp O., Knoch T.A., Zahler S., Bestvater F., Felgentrager M., Holloschi A., Fernandez-Montalvan A., Auerswald E.A., Fritz H., Fuentes-Prior P., Machleidt W., Spiess E. Subcellular localization and in vivo subunit interactions of ubiquitous μ-calpain. J. Biol. Chem. 278:2003;16336-16346.
30. Glading A., Chang P., Lauffenburger D.A., Wells A. Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. J. Biol. Chem. 275:2000;2390-2398.
31. Glading A., Lauffenburger D.A., Wells A. Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol. 12:2002;46-54. Review.
32. Goll D.E., Thompson V.F., Taylor R.G., Zalewska T. Is calpain activity regulated by membranes and autolysis or by calcium and calpastatin. Bioessays. 14:1992;549-556. Review.
33. Grabnitz F., Seiss M., Rucknagel K.P., Staudenbauer W.L. Structure of the beta-glucosidase gene bglA of Clostridium thermocellum. Sequence analysis reveals a superfamily of cellulases and beta-glycosidases including human lactase/phlorizin hydrolase. Eur. J. Biochem. 200:1991;301-309.
34. Grynspan F., Griffin W.B., Mohan P.S., Shea T.B., Nixon R.A. Calpains and calpastatin in SH-SY5Y neuroblastoma cells during retinoic acid-induced differentiation and neurite outgrowth: comparison with the human brain calpain system. J. Neurosci. Res. 48:1997a;181-191.
35. Grynspan F., Griffin W.R., Cataldo A., Katayama S., Nixon R.A. Active site-directed antibodies identify calpain II as an early-appearing and pervasive component of neurofibrillary pathology in Alzheimer's disease. Brain Res. 763:1997b;145-158.
36. Guroff G., Guroff G. A neutral calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239:1964;149.
37. 2+-activated protease. J. Biol. Chem. 257:1982;9072-9077.
38. 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., Bell G.I. Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nat. Genet. 26:2000;163-175.
39. Hosfield C.M., Elce J.S., Davies P.L., Jia Z. Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18:1999;6880-6889.
40. Huang Y., Wang K.K. The calpain family and human disease. Trends Mol. Med. 7:2001;355-3562. Review.
41. Ibrahim M., Upreti R.K., Kidwai A.M. Calpain from rat intestinal epithelial cells: age-dependent dynamics during cell differentiation. Mol. Cell Biochem. 131:1994;49-59.
42. Inomata M., Hayashi M., Ito Y., Matsubara Y., Takehana M., Kawashima S., Shumiya S. Comparison of Lp82- and m-calpain-mediated proteolysis during cataractogenesis in Shumiya cataract rat (SCR). Curr. Eye Res. 25:2002;207-213.
43. Jordan J., Galindo M.F., Miller R.J. Role of calpain- and interleukin-1 beta converting enzyme-like proteases in the beta-amyloid-induced death of rat hippocampal neurons in culture. J. Neurochem. 68:1997;1612-1621.
44. Karlsson J.O., Blennow K., Holmberg B., Janson I., Karlsson I., Nilsson E., Wallin A., Gottfries C.G. Dementia. 3:1992;200-204.
45. Keller J.N., Huang F.F., Markesbery W.R. Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience. 98:2000;149-156.
46. Kelley M.J., David L.L., Iwasaki N., Wright J., Shearer T.R. Alpha-crystallin chaperone activity is reduced by calpain II in vitro and in selenite cataract. J. Biol. Chem. 268:1993;18844-18849.
47. Kenessey A., Banay-Schwartz M., DeGuzman T., Lajtha A. Calpain II activity and calpastatin content in brain regions of 3- and 24-month-old rats. Neurochem. Res. 15:1990;243-249.
48. Kosik K.S., Qiu W.Q., Greenberg S. Cellular signaling pathways and cytoskeletal organization. Ann. NY Acad. Sci. 777:1996;114-120. Review.
49. Kuro-o M., Matsumura Y., Aizawa H., Kawaguchi H., Suga T., Utsugi T., Ohyama Y., Kurabayashi M., Kaname T., Kume E., Iwasaki H., Iida A., Shiraki-Iida T., Nishikawa S., Nagai R., Nabeshima Y.I. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature. 390:1997;45-51.
50. Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T., Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 275:2000;17166-17172.
51. Lankiewicz S., Marc Luetjens C., Truc Bui N., Krohn A.J., Poppe M., Cole G.M., Saido T.C., Prehn J.H. Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. J. Biol. Chem. 275:2000;17064-17071.
52. Lee W.J., Ma H., Takano E., Yang H.Q., Hatanaka M., Maki M. Molecular diversity in amino-terminal domains of human calpastatin by exon skipping. J. Biol. Chem. 267:1992;8437-8442.
53. Lu Q., Soria J.P., Wood J.G. p44mpk MAP kinase induces Alzheimer type alterations in tau function and in primary hippocampal neurons. J. Neurosci. Res. 35:1993;439-444.
54. Lynch, G., Larson, J., et al. (Eds.), 1986. Proteases, neuronal stability and brain aging: an hypothesis. Treatment Development Strategies for Alzheimer's Disease. Mark Powley Associates, Madison.
55. Ma H., Hata I., Shih M., Fukiage C., Nakamura Y., Azuma M., Shearer T.R. Lp82 is the dominant form of calpain in young mouse lens. Exp. Eye Res. 68:1999;447-456.
56. Maki M., Ma H., Takano E., Adachi Y., Lee W.J., Hatanaka M., Murachi T. Calpastatins: biochemical and molecular biological studies. Biomed. Biochim. Acta. 50:1991;509-516. Review.
57. Manya H., Inomata M., Fujimori T., Dohmae N., Sato Y., Takio K., Nabeshima Y., Endo T. Klotho protein deficiency leads to overactivation of mu-calpain. J. Biol. Chem. 277:2002;5503-5508.
58. Mathews P.M., Jiang Y., Schmidt S.D., Grbovic O.M., Mercken M., Nixon R.A. Calpain activity regulates the cell surface distribution of amyloid precursor protein. Inhibition of calpains enhances endosomal generation of beta-cleaved C-terminal APP fragments. J. Biol. Chem. 277:2002;36415-36424.
59. Mbebi C., See V., Mercken L., Pradier L., Muller U., Loeffler J.P. Amyloid precursor protein family-induced neuronal death is mediated by impairment of the neuroprotective calcium/calmodulin protein kinase IV-dependent signaling pathway. J. Biol. Chem. 277:2002;20979-20990.
60. Mellgren R.L. Interaction of human erythrocyte multicatalytic proteinase with polycations. Biochim. Biophys. Acta. 1040:1990;28-34.
61. Mellgren R.L., Lane R.D., Hegazy M.G., Reimann E.M. Adv. Prot. Phosphatases. 1:1985;259-275.
62. Melloni E., Michetti M., Salamino F., Minafra R., Pontremoli S. Modulation of the calpain autoproteolysis by calpastatin and phospholipids. Biochem. Biophys. Res. Commun. 229:1996;193-197.
63. Menard H.A., el-Amine M. The calpain-calpastatin system in rheumatoid arthritis. Immunol. Today. 17:1996;545-547. Review.
64. Moldoveanu T., Hosfield C.M., Lim D., Elce J.S., Jia Z., Davies P.L. A Ca(2+) switch aligns the active site of calpain. Cell. 108:2002;649-660.
65. Mouatt-Prigent A., Karlsson J.O., Agid Y., Hirsch E.C. Increased M-calpain expression in the mesencephalon of patients with Parkinson's disease but not in other neurodegenerative disorders involving the mesencephalon: a role in nerve cell death. Neuroscience. 73:1996;979-987.
66. 2+-requiring forms of calcium-activated neutral proteases. Biochemistry. 28:1989;449-455.
67. Nath R., Davis M., Probert A.W., Kupina N.C., Ren X., Schielke G.P., Wang K.K. Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem. Biophys. Res. Commun. 274:2000;16-21. Erratum in: Biochem. Biophys. Res. Commun. 276 (390).
68. Neumar R.W., Xu Y.A., Gada H., Guttmann R.P., Siman R. Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. J. Biol. Chem. 278:2003;14162-14167.
69. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 233:1986;305-312. Review.
70. Nixon R.A., Saito K.-I., Grynspan F., Griffin W.R., Katayama S., Honda T., Mohan P.S., Shea T.B., Beermann M.L. Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease. Ann. NY Acad. Sci. 747:1994;77-91.
71. Ouanounou A., Zhang L., Charlton M.P., Carlen P.L. Differential modulation of synaptic transmission by calcium chelators in young and aged hippocampal CA1 neurons: evidence for altered calcium homeostasis in aging. J. Neurosci. 19:1999;906-915.
72. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature. 402:1999;615-622.
73. Patzke H., Tsai L.H. Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29. J. Biol. Chem. 277:2002;8054-8060.
74. Peterson C., Goldman J.E. Alterations in calcium content and biochemical processes in cultured skin fibroblasts from aged and Alzheimer donors. Proc. Natl. Acad. Sci. U.S.A. 83:1986;2758-2762.
75. Pontremoli S., Melloni E., Michetti M., Sparatore B., Salamino F., Sacco O., Horecker B.L. Phosphorylation and proteolytic modification of specific cytoskeletal proteins in human neutrophils stimulated by phorbol 12-myristate 13-acetate. Proc. Natl. Acad. Sci. U.S.A. 84:1987;3604-3608.
76. Richard I., Broux O., Allamand V., Fougerousse F., Chiannilkulchai N., Bourg N., Brenguier L., Devaud C., Pasturaud P., Roudaut C.et al. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell. 81:1995;27-40.
77. Robles E., Huttenlocher A., Gomez T.M. Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain. Neuron. 38:2003;597-609.
78. Romero P.J., Salas V., Hernandez C. Calcium pump phosphoenzyme from young and old human red cells. Cell Biol. Int. 26:2002;945-949.
79. Saido T.C., Shibata M., Takenawa T., Murofushi H., Suzuki K. Positive regulation of mu-calpain action by polyphosphoinositides. J. Biol. Chem. 267:1992;24585-24590.
80. Saito K., Elce J.S., Hamos J.E., Nixon R.A. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. U.S.A. 90:1993;2628-2632.
81. Saito T., Onuki R., Fujita Y., Kusakawa G., Ishiguro K., Bibb J.A., Kishimoto T., Hisanaga S. Developmental regulation of the proteolysis of the p35 cyclin-dependent kinase 5 activator by phosphorylation. J. Neurosci. 23:2003;1189-1197.
82. Saitoh T., Masliah E., Jin L.W., Cole G.M., Wieloch T., Shapiro I.P. Protein kinases and phosphorylation in neurologic disorders and cell death. Lab. Invest. 64:1991;596-616. Review.
83. Salamino F., De Tullio R., Mengotti P., Viotti P.L., Melloni E., Pontremoli S. Site-directed activation of calpain is promoted by a membrane-associated natural activator protein. Biochem. J. 290(Pt1):1993; 191-197.
84. Sato K., Kawashima S. Calpain function in the modulation of signal transduction molecules. Biol. Chem. 382:2001;743-751. Review.
85. Schoenwaelder S.M., Yuan Y., Jackson S.P. Calpain regulation of integrin alpha IIb beta 3 signaling in human platelets. Platelets. 11:2000;189-198. Review.
86. Schwarz-Benmeir N., Glaser T., Kosower N.S. Band 3 protein degradation by calpain is enhanced in erythrocytes of old people. Biochem. J. 275(Pt1):1991;47-52.
87. Schwarz-Benmeir N., Glaser T., Barnoy S., Kosower N.S. Calpastatin in erythrocytes of young and old individuals. Biochem. J. 304:1994;365-370.
88. Sedarous, M., Keramaris, E., O'Hare, M., Melloni, E., Slack, R.S., Elce, J.S., Greer, P.A., Park, D.S., 2003. Calpains mediate p53 activation and neuronal death evoked by DNA damage. J. Biol. Chem. Apr 29 [epub ahead of print].
89. Shea T.B., Cressman C.M., Spencer M.J., Beermann M.L., Nixon R.A. Enhancement of neurite outgrowth following calpain inhibition is mediated by protein kinase C. J. Neurochem. 65:1995;517-527.
90. Shea T.B., Spencer M.J., Beermann M.L., Cressman C.M., Nixon R.A. Calcium influx into human neuroblastoma cells induces ALZ-50 immunoreactivity: involvement of calpain-mediated hydrolysis of protein kinase C. J. Neurochem. 66:1996;1539-1549.
91. Shearer T.R., Azuma M., David L.L., Murachi T. Amelioration of cataracts and proteolysis in cultured lenses by cysteine protease inhibitor E64. Invest. Ophthalmol. Vis. Sci. 32:1991;533-540.
92. Shiraha H., Glading A., Chou J., Jia Z., Wells A. Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain. Mol. Cell Biol. 22:2002;2716-2727.
93. Skaper S.D., Facci L., Strijbos P.J. Neuronal protein kinase signaling cascades and excitotoxic cell death. Ann. NY Acad. Sci. 939:2001;11-22. Review.
94. Sloane J.A., Hinman J.D., Lubonia M., Hollander W., Abraham C.R. Age-dependent myelin degeneration and proteolysis of oligodendrocyte proteins is associated with the activation of calpain-1 in the rhesus monkey. J. Neurochem. 84:2003;157-168.
95. Smith S.D., Jia Z., Huynh K.K., Wells A., Elce J.S. Glutamate substitutions at a PKA consensus site are consistent with inactivation of calpain by phosphorylation. FEBS Lett. 542:2003;115-118.
96. Song D.K., Malmstrom T., Kater S.B., Mykles D.L. Calpain inhibitors block Ca(2+)-induced suppression of neurite outgrowth in isolated hippocampal pyramidal neurons. J. Neurosci. Res. 39:1994;474-481.
97. Sorimachi H., Suzuki K. The structure of calpain. J. Biochem. (Tokyo). 129:2001;653-664. Review.
98. Stanciu M., DeFranco D.B. Prolonged nuclear retention of activated extracellular signal-regulated protein kinase promotes cell death generated by oxidative toxicity or proteasome inhibition in a neuronal cell line. J. Biol. Chem. 277:2002;4010-4017.
99. Suzuki K., Sorimachi H. A novel aspect of calpain activation. FEBS Lett. 433:1998;1-4. Review.
100. Suzuki K., Tsuji S., Ishiura S., Kimura Y., Kubota S., Imahori K. Autolysis of calcium-activated neutral protease of chicken skeletal muscle. J. Biochem. (Tokyo). 90:1981;1787-1793.
101. Syntichaki P., Xu K., Driscoll M., Tavernarakis N. Specific aspartyl and calpain proteases are required for neurodegeneration in C, elegans. Nature. 419:2002;939-944.
102. Szomor Z., Shimizu K., Yamamoto S., Yasuda T., Ishikawa H., Nakamura T. Externalization of calpain (calcium-dependent neutral cysteine proteinase) in human arthritic cartilage. Clin. Exp. Rheumatol. 17:1999;569-574.
103. 2+-dependent protease. Biochemistry. 27:1988;2205-2211.
104. Tremper-Wells B., Mathur A., Beaman-Hall C.M., Vallano M.L. Trophic agents that prevent neuronal apoptosis activate calpain and down-regulate CaMKIV. J. Neurochem. 81:2002;314-324.
105. Tullio R.D., Passalacqua M., Averna M., Salamino F., Melloni E., Pontremoli S. Changes in intracellular localization of calpastatin during calpain activation. Biochem. J. 343(Pt2):1999;467-472.
106. Varnum M.D., David L.L., Shearer T.R. Age-related changes in calpain II and calpastatin in rat lens. Exp. Eye Res. 49:1989;1053-1065.
107. Veeranna, K.T., Odrljin, T., Basavarajappa, B.S., Mohan, P.S., Peterhoff, C., Boland, B., Cataldo, A., Rudnicki, A., Li, B.S., Pant, H.C., Hungund, B.L., Arancio, O., Nixon, R.A., 2003. Calpain mediates calcium-induced activation of the Erk 1,2 MAPK pathway and cytoskeletal phosphorylation in neurons: relevance to Alzheimer's disease, unpublished results.
108. Vitto A., Nixon R.A. Calcium-activated neutral proteinase of human brain: subunit structure and enzymatic properties of multiple molecular forms. J. Neurochem. 47:1986;1039-1051.
109. Wang K.K. Calpain and caspase: can you tell the difference. Trends Neurosci. 23:2000;20-26. Review.
110. Wood D.E., Thomas A., Devi L.A., Berman Y., Beavis R.C., Reed J.C., Newcomb E.W. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene. 17:1998;1069-1078.
111. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 270:1995;1326-1331.
112. Yamamoto S., Shimizu K., Shimizu K., Suzuki K., Nakagawa Y., Yamamuro T. Calcium-dependent cysteine proteinase (calpain) in human arthritic synovial joints. Arthritis Rheum. 35:1992;1309-1317.
113. 2+-dependent cysteine proteinase, isolated from the same tissue. Biochim. Biophys. Acta. 798:1984;252-259.