Proteomic study of calpain interacting proteins during skeletal muscle aging

Biochimie

Volumn 92, Issue 12, 2010, Pages 1923-1933

  Brule C ^a   Dargelos, E ^a   Diallo, R ^a   Listrat, A ^b   Bechet D ^b   Cottin, P ^a   Poussard, S ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INRA and University of Auvergne   (France)

Author keywords

Alpha actinin; ATP synthase; Calpains; Ryanodine receptor; Sarcopenia

Indexed keywords

ALPHA ACTININ; ALPHA ACTININ 3; CALPAIN 1; CALPAIN 2; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RYANODINE RECEPTOR 1;

AGING; ALPHA CHAIN; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; IMMUNOPRECIPITATION; MALE; MASS SPECTROMETRY; MUSCLE ATROPHY; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; RAT; SKELETAL MUSCLE;

EID: 78650251479     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.09.003     Document Type: Article

References (71)

1. R.N. Baumgartner, K.M. Koehler, D. Gallagher, L. Romero, S.B. Heymsfield, R.R. Ross, P.J. Garry, and R.D. Lindeman Epidemiology of sarcopenia among the elderly in New Mexico Am. J. Epidemiol. 147 1998 755 763
2. P. Szulc, T.J. Beck, F. Marchand, and P.D. Delmas Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men-the MINOS study J. Bone Miner. Res. 20 2005 721 729
3. G.S. Lynch Emerging drugs for sarcopenia: age-related muscle wasting Expert Opin. Emerg. Drugs 9 2004 345 361
4. F. Dela, and M. Kjaer Resistance training, insulin sensitivity and muscle function in the elderly Essays Biochem. 42 2006 75 88
5. P.G. Giresi, E.J. Stevenson, J. Theilhaber, A. Koncarevic, J. Parkington, R.A. Fielding, and S.C. Kandarian Identification of a molecular signature of sarcopenia Physiol. Genomics 21 2005 253 263
6. S.V. Brooks, and J.A. Faulkner Skeletal muscle weakness in old age: underlying mechanisms Med. Sci. Sports Exerc. 26 1994 432 439
7. C.J. McNeil, T.J. Doherty, D.W. Stashuk, and C.L. Rice Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men Muscle Nerve 31 2005 461 467
8. M.S. Conley, R.A. Meyer, J.J. Bloomberg, D.L. Feeback, and G.A. Dudley Noninvasive analysis of human neck muscle function Spine 20 1995 2505 2512
9. M.G. Cree, B.R. Newcomer, C.S. Katsanos, M. Sheffield-Moore, D. Chinkes, A. Aarsland, R. Urban, and R.R. Wolfe Intramuscular and liver triglycerides are increased in the elderly J. Clin. Endocrinol. Metab. 89 2004 3864 3871
10. L. Edstrom, and L. Larsson Effects of age on contractile and enzyme-histochemical properties of fast- and slow-twitch single motor units in the rat J. Physiol. 392 1987 129 145
11. L. Larsson, G. Grimby, and J. Karlsson Muscle strength and speed of movement in relation to age and muscle morphology J. Appl. Physiol. 46 1979 451 456
12. A.J. Dirks, and C. Leeuwenburgh The role of apoptosis in age-related skeletal muscle atrophy Sports Med. 35 2005 473 483
13. A.J. Dirks, and C. Leeuwenburgh Aging and lifelong calorie restriction result in adaptations of skeletal muscle apoptosis repressor, apoptosis-inducing factor, X-linked inhibitor of apoptosis, caspase-3, and caspase-12 Free Radic. Biol. Med. 36 2004 27 39
14. D. Attaix, L. Mosoni, D. Dardevet, L. Combaret, P.P. Mirand, and J. Grizard Altered responses in skeletal muscle protein turnover during aging in anabolic and catabolic periods Int. J. Biochem. Cell Biol. 37 2005 1962 1973
15. K.E. Yarasheski Exercise, aging, and muscle protein metabolism J. Gerontol. A Biol. Sci. Med. Sci. 58 2003 M918 M922
16. D.E. Goll, V.F. Thompson, H. Li, W. Wei, and J. Cong The calpain system Physiol. Rev. 83 2003 731 801
17. E. Schad, A. Farkas, G. Jekely, P. Tompa, and P. Friedrich A novel human small subunit of calpains Biochem. J. 362 2002 383 388
18. J.M. Alderton, and R.A. Steinhardt How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes Trends Cardiovasc. Med. 10 2000 268 272
19. M. Averna, R. De Tullio, P. Capini, F. Salamino, S. Pontremoli, and E. Melloni Changes in calpastatin localization and expression during calpain activation: a new mechanism for the regulation of intracellular Ca(2+)-dependent proteolysis Cell Mol. Life Sci. 60 2003 2669 2678
20. S. Barnoy, M. Maki, and N.S. Kosower Overexpression of calpastatin inhibits L8 myoblast fusion Biochem. Biophys. Res. Commun. 332 2005 697 701
21. H. Li, V.F. Thompson, and D.E. Goll Effects of autolysis on properties of mu- and m-calpain Biochim. Biophys. Acta 1691 2004 91 103
22. K. Suzuki, T.C. Saido, and S. Hirai Modulation of cellular signals by calpain Ann. N. Y Acad. Sci. 674 1992 218 227
23. R.A. Nixon The calpains in aging and aging-related diseases Ageing Res. Rev. 2 2003 407 418
24. C. Perrin, C. Vergely, and L. Rochette Calpains and cardiac diseases Ann Cardiol Angeiol (Paris) 53 2004 259 266
25. I. Richard, C. Roudaut, S. Marchand, S. Baghdiguian, M. Herasse, D. Stockholm, Y. Ono, L. Suel, N. Bourg, H. Sorimachi, G. Lefranc, M. Fardeau, A. Sebille, and J.S. Beckmann Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IkappaBalpha/nuclear factor kappaB pathway perturbation in mice J. Cell Biol. 151 2000 1583 1590
26. S. Biswas, F. Harris, S. Dennison, J. Singh, and D.A. Phoenix Calpains: targets of cataract prevention? Trends Mol. Med. 10 2004 78 84
27. N.J. Cox, M.G. Hayes, C.A. Roe, T. Tsuchiya, and G.I. Bell Linkage of calpain 10 to type 2 diabetes: the biological rationale Diabetes 53 Suppl. 1 2004 S19 S25
28. Y. Matsushita, Y. Shimada, S. Kawara, K. Takehara, and S. Sato Autoantibodies directed against the protease inhibitor calpastatin in psoriasis Clin. Exp. Immunol. 139 2005 355 362
29. H.A. Menard, and M. el-Amine The calpain-calpastatin system in rheumatoid arthritis Immunol. Today 17 1996 545 547
30. I.A. Atencio, M. Ramachandra, P. Shabram, and G.W. Demers Calpain inhibitor 1 activates p53-dependent apoptosis in tumor cell lines Cell Growth Differ. 11 2000 247 253
31. S. Dedieu, S. Poussard, G. Mazeres, F. Grise, E. Dargelos, P. Cottin, and J.J. Brustis Myoblast migration is regulated by calpain through its involvement in cell attachment and cytoskeletal organization Exp. Cell Res. 292 2004 187 200
32. S.J. Franco, M.A. Rodgers, B.J. Perrin, J. Han, D.A. Bennin, D.R. Critchley, and A. Huttenlocher Calpain-mediated proteolysis of talin regulates adhesion dynamics Nat. Cell Biol. 6 2004 977 983
33. A. Glading, F. Uberall, S.M. Keyse, D.A. Lauffenburger, and A. Wells Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling J. Biol. Chem. 276 2001 23341 23348
34. A. Mamoune, J.H. Luo, D.A. Lauffenburger, and A. Wells Calpain-2 as a target for limiting prostate cancer invasion Cancer Res. 63 2003 4632 4640
35. G. Mazeres, L. Leloup, L. Daury, P. Cottin, and J.J. Brustis Myoblast attachment and spreading are regulated by different patterns by ubiquitous calpains Cell Motil. Cytoskeleton 63 2006 193 207
36. H. Manya, M. Inomata, T. Fujimori, N. Dohmae, Y. Sato, K. Takio, Y. Nabeshima, and T. Endo Klotho protein deficiency leads to overactivation of mu-calpain J. Biol. Chem. 277 2002 35503 35508
37. A. Ouanounou, L. Zhang, M.P. Charlton, and P.L. Carlen 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
38. P.J. Romero, V. Salas, and C. Hernandez Calcium pump phosphoenzyme from young and old human red cells Cell Biol. Int. 26 2002 945 949
39. O. Delbono Molecular mechanisms and therapeutics of the deficit in specific force in ageing skeletal muscle Biogerontology 3 2002 265 270
40. B. Fraysse, J.F. Desaphy, J.F. Rolland, S. Pierno, A. Liantonio, V. Giannuzzi, C. Camerino, M.P. Didonna, D. Cocchi, A. De Luca, and D. Conte Camerino Fiber type-related changes in rat skeletal muscle calcium homeostasis during aging and restoration by growth hormone Neurobiol. Dis. 21 2006 372 380
41. Y. Tan, N. Dourdin, C. Wu, T. De Veyra, J.S. Elce, and P.A. Greer Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis J. Biol. Chem. 281 2006 16016 16024
42. E. Dargelos, C. Brule, L. Combaret, A. Hadj-Sassi, S. Dulong, S. Poussard, and P. Cottin Involvement of the calcium-dependent proteolytic system in skeletal muscle aging Exp. Gerontol. 42 2007 1088 1098
43. P. Cottin, J.J. Brustis, S. Poussard, N. Elamrani, S. Broncard, and A. Ducastaing Ca(2+)-dependent proteinases (calpains) and muscle cell differentiation Biochim. Biophys. Acta 1223 1994 170 178
44. R.L. Levine, J.A. Williams, E.R. Stadtman, and E. Shacter Carbonyl assays for determination of oxidatively modified proteins Methods Enzymol. 233 1994 346 357
45. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
46. S. Goudenege, E. Dargelos, S. Claverol, M. Bonneu, P. Cottin, and S. Poussard Comparative proteomic analysis of myotube caveolae after milli-calpain deregulation Proteomics 7 2007 3289 3298
47. P.A. Figueiredo, S.K. Powers, R.M. Ferreira, F. Amado, H.J. Appell, and J.A. Duarte Impact of lifelong sedentary behavior on mitochondrial function of mice skeletal muscle J. Gerontol. A Biol. Sci. Med. Sci. 64 2009 927 939
48. J.H. Kim, H.B. Kwak, C. Leeuwenburgh, and J.M. Lawler Lifelong exercise and mild (8%) caloric restriction attenuate age-induced alterations in plantaris muscle morphology, oxidative stress and IGF-1 in the Fischer-344 rat Exp. Gerontol. 43 2008 317 329
49. N. Breusing, J. Arndt, P. Voss, N. Bresgen, I. Wiswedel, A. Gardemann, W. Siems, and T. Grune Inverse correlation of protein oxidation and proteasome activity in liver and lung Mech. Ageing Dev. 130 2009 748 753
50. M.M. Thomas, C. Vigna, A.C. Betik, A.R. Tupling, and R.T. Hepple Initiating treadmill training in late middle age offers modest adaptations in Ca2+ handling but enhances oxidative damage in senescent rat skeletal muscle Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010 10.1152/ajpregu.00663.2009
51. A.J. Dirks, T. Hofer, E. Marzetti, M. Pahor, and C. Leeuwenburgh Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle Ageing Res. Rev. 5 2006 179 195
52. N. Weisleder, and J. Ma Altered Ca2+ sparks in aging skeletal and cardiac muscle Ageing Res. Rev. 7 2008 177 188
53. K.A. Clark, A.S. McElhinny, M.C. Beckerle, and C.C. Gregorio Striated muscle cytoarchitecture: an intricate web of form and function Annu. Rev. Cell Dev. Biol. 18 2002 637 706
54. M. Fill, and J.A. Copello Ryanodine receptor calcium release channels Physiol. Rev. 82 2002 893 922
55. N. Ikemoto, M. Ronjat, L.G. Meszaros, and M. Koshita Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum Biochemistry 28 1989 6764 6771
56. M.W. Berchtold, H. Brinkmeier, and M. Muntener Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease Physiol. Rev. 80 2000 1215 1265
57. D. Bansal, K. Miyake, S.S. Vogel, S. Groh, C.C. Chen, R. Williamson, P.L. McNeil, and K.P. Campbell Defective membrane repair in dysferlin-deficient muscular dystrophy Nature 423 2003 168 172
58. Y. Huang, A. de Morree, A. van Remoortere, K. Bushby, R.R. Frants, J.T. Dunnen, and S.M. van der Maarel Calpain 3 is a modulator of the dysferlin protein complex in skeletal muscle Hum. Mol. Genet. 17 2008 1855 1866
59. M.R. Hara, M.B. Cascio, and A. Sawa GAPDH as a sensor of NO stress Biochim. Biophys. Acta 1762 2006 502 509
60. R. Badugu, M. Garcia, V. Bondada, A. Joshi, and J.W. Geddes N terminus of calpain 1 is a mitochondrial targeting sequence J. Biol. Chem. 283 2008 3409 3417
61. P. Kar, T. Chakraborti, K. Samanta, and S. Chakraborti Submitochondrial localization of associated mu-calpain and calpastatin Arch. Biochem. Biophys. 470 2008 176 186
62. F. Raynaud, E. Fernandez, G. Coulis, L. Aubry, X. Vignon, N. Bleimling, M. Gautel, Y. Benyamin, and A. Ouali Calpain 1-titin interactions concentrate calpain 1 in the Z-band edges and in the N2-line region within the skeletal myofibril Febs J. 272 2005 2578 2590
63. S. Goudenege, S. Poussard, S. Dulong, and P. Cottin Biologically active milli-calpain associated with caveolae is involved in a spatially compartmentalised signalling involving protein kinase C alpha and myristoylated alanine-rich C-kinase substrate (MARCKS) Int. J. Biochem. Cell Biol. 37 2005 1900 1910
64. A. Margreth, E. Damiani, and E. Bortoloso Sarcoplasmic reticulum in aged skeletal muscle Acta Physiol. Scand. 167 1999 331 338
65. S. Shevchenko, W. Feng, M. Varsanyi, and V. Shoshan-Barmatz Identification, characterization and partial purification of a thiol-protease which cleaves specifically the skeletal muscle ryanodine receptor/Ca2+ release channel J. Membr. Biol. 161 1998 33 43
66. A.M. Bellinger, S. Reiken, M. Dura, P.W. Murphy, S.X. Deng, D.W. Landry, D. Nieman, S.E. Lehnart, M. Samaru, A. LaCampagne, and A.R. Marks Remodeling of ryanodine receptor complex causes "leaky" channels: a molecular mechanism for decreased exercise capacity Proc. Natl. Acad. Sci. U S A 105 2008 2198 2202
67. B. Chabi, V. Ljubicic, K.J. Menzies, J.H. Huang, A. Saleem, and D.A. Hood Mitochondrial function and apoptotic susceptibility in aging skeletal muscle Aging Cell 7 2008 2 12
68. J.L. Hagen, D.J. Krause, D.J. Baker, M.H. Fu, M.A. Tarnopolsky, and R.T. Hepple Skeletal muscle aging in F344BN F1-hybrid rats: I. Mitochondrial dysfunction contributes to the age-associated reduction in VO2max J. Gerontol. A Biol. Sci. Med. Sci. 59 2004 1099 1110
69. B. Drew, S. Phaneuf, A. Dirks, C. Selman, R. Gredilla, A. Lezza, G. Barja, and C. Leeuwenburgh Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 2003 R474 R480
70. D. Capitanio, M. Vasso, C. Fania, M. Moriggi, A. Vigano, P. Procacci, V. Magnaghi, and C. Gelfi Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE Proteomics 9 2009 2004 2020
71. E. Dargelos, S. Poussard, C. Brule, L. Daury, and P. Cottin Calcium-dependent proteolytic system and muscle dysfunctions: a possible role of calpains in sarcopenia Biochimie 90 2008 359 368