Modern understanding of the role of calpains in muscles
- Авторлар: Muzhenya D.V.1, Lysenkov S.P.2, Tuguz A.R.1, Shumilov D.S.1
-
Мекемелер:
- Adyghe State University
- Maikop State Technological University
- Шығарылым: Том 29, № 1 (2025): PHYSIOLOGY. EXPERIMENTAL PHYSIOLOGY
- Беттер: 27-39
- Бөлім: PHYSIOLOGY. EXPERIMENTAL PHYSIOLOGY
- URL: https://journal-vniispk.ru/2313-0245/article/view/349496
- DOI: https://doi.org/10.22363/2313-0245-2025-29-1-27-39
- EDN: https://elibrary.ru/ETIJIQ
- ID: 349496
Дәйексөз келтіру
Толық мәтін
Аннотация
Relevance. The study and understanding of the physiological processes that occur in muscles during physical activity is a crucial area in modern sports physiology. As our theoretical and practical knowledge expands, we realize that the classical ideas about these physiological processes under stress conditions do not provide complete information. To fully comprehend these processes, we need to conduct further analysis and systematize the existing data. This will help us identify key elements that we can influence to regulate the direction and extent of certain physiological processes. One such candidate for this regulation is the calpain protein family (CAPN). Initially, they were associated with regulating signal transmission, but now they are considered proteases involved in the turnover of myofibrillar protein and the proteolytic cleavage of sarcomeric and cytoskeletal proteins. CAPNs are often seen as «harmful» degrading proteases in pathological conditions, such as cardiovascular diseases. However, in reality, they are processing proteases rather than degrading ones. They differ from other major intracellular proteolytic components because they act through proteolytic processing, causing changes in protein activity, localization, or structure. For example, CAPNs can regulate the activity of NOS by suppressing the production of nitric oxide during muscle contractions. This helps prevent the negative consequences caused by excess nitric oxide production. They also reduce the contractile activity of muscles by acting on structures called «triads». Calpains play a significant role in the reparative processes of muscles after physical activity. They regulate the processes of cell membrane repair and the restructuring of protein components in muscle fibers. Another notable difference from classical proteolysis systems, such as ubiquitin - proteasome and autophagic systems that require ATP, is that calpains are ATP-independent. However, uncontrolled activity of calpains can trigger a cascade of proapoptotic systems leading to apoptosis and the death of myocytes. Conclusion . Calpains play an important role in the physiological processes that occur in muscles both in a healthy state and in various pathologies. Thus, the functions of calpains are not limited only to proteolysis (protein breakdown) - they are much broader. Therefore, the study of these enzymes is an important area of research. It will help us identify informative targets for developing treatment methods and monitoring muscle health after intense exercise.
Негізгі сөздер
Авторлар туралы
Dmitriy Muzhenya
Adyghe State University
Хат алмасуға жауапты Автор.
Email: dmuzhenya@mail.ru
ORCID iD: 0000-0002-4379-0634
SPIN-код: 7910-6021
Maikop, Russian Federation
Sergey Lysenkov
Maikop State Technological University
Email: dmuzhenya@mail.ru
ORCID iD: 0000-0003-1179-8938
SPIN-код: 6665-0686
Maikop, Russian Federation
Aminat Tuguz
Adyghe State University
Email: dmuzhenya@mail.ru
ORCID iD: 0000-0002-7493-7192
SPIN-код: 5351-3387
Maikop, Russian Federation
Dmitriy Shumilov
Adyghe State University
Email: dmuzhenya@mail.ru
ORCID iD: 0000-0001-9636-6311
SPIN-код: 7173-2685
Maikop, Russian Federation
Әдебиет тізімі
- Lavin KM, Coen PM, Baptista LC, Bell MB, Drummer D, Harper SA, Lixandrão ME, McAdam JS, O’Bryan SM, Ramos S, Roberts LM, Vega RB, Goodpaster BH, Bamman MM, Buford TW. State of Knowledge on Molecular Adaptations to Exercise in Humans: Historical Perspectives and Future Directions. Comprehensive Physiology. 2022;12(2):3193—3279. doi: 10.1002/cphy.c200033
- Quadrilatero J, Alway SE, Dupont-Versteegden EE. Skeletal muscle apoptotic response to physical activity: potential mechanisms for protection. Applied Physiology, Nutrition, and Metabolism. 2011;36(5):608—617. doi: 10.1139/h11-064
- Sanford JA, Nogiec CD, Lindholm ME, Adkins JN, Amar D, Dasari S, Drugan JK, Fernández FM, Radom-Aizik S, Schenk S, Snyder MP, Tracy RP, Vanderboom P, Trappe S, Walsh MJ. Molecular Transducers of Physical Activity Consortium. Molecular Transducers of Physical Activity Consortium (MoTrPAC): Mapping the Dynamic Responses to Exercise. Cell. 2020;181(7):1464—1474. doi: 10.1016/j.cell.2020.06.004.
- Fonova EA, Zhalsanova IZ, Skryabin NA. Current aspects and approaches to molecular diagnostics of hereditary neuromuscular diseases. RUDN Journal of Medicine. 2024;28(2):282—292. doi: 10.22363/2313-0245-2024-28-1-282-292
- Solomon V, Goldberg AL. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. Journal of Biological Chemistry. 1996;271(43):26690—26697. doi: 10.1074/jbc.271.43.26690
- Sorimachi H, Ono Y. Regulation and physiological roles of the calpain system in muscular disorders. Cardiovascular Research. 2012;96(1):11—22. doi: 10.1093/cvr/cvs157
- Hyatt HW, Powers SK. The Role of Calpains in Skeletal Muscle Remodeling with Exercise and Inactivity-induced Atrophy. International Journal of Sports Medicine. 2020;41(14):994—1008. doi: 10.1055/a‑1199-7662
- Ono Y, Saido TC, Sorimachi H. Calpain research for drug discovery: Challenges and potential. Nature Reviews Drug Discovery. 2016;15:854—876. doi: 10.1038/nrd.2016.212
- Dókus LE, Yousef M, Bánóczi Z. Modulators of calpain activity: inhibitors and activators as potential drugs. Expert Opinion on Drug Discovery. 2020;15(4):471—486. doi: 10.1080/17460441.2020.1722638
- Murphy RM, Verburg E, Lamb GD. Ca2+ activation of diffusible and bound pools of mu-calpain in rat skeletal muscle. Journal of Physiology. 2006;576(Pt2):595—612. doi: 10.1113/jphysiol.2006.114090
- Mukund K, Subramaniam S. Skeletal muscle: A review of molecular structure and function, in health and disease. Wiley Interdisciplinary Reviews: Systems Biology and Medicine. 2020;12(1): e1462. doi: 10.1002/wsbm.1462
- Campbell RL, Davies PL. Structure-function relationships in calpains. Biochemical Journal. 2012;447(3):335—351. doi: 10.1042/BJ20120921
- Saez ME, Ramirez-Lorca R, Moron FJ, Ruiz A. The therapeutic potential of the calpain family: new aspects. Drug Discovery Today. 2006;11(19—20):917—923. doi: 10.1016/j.drudis.2006.08.009
- Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell. 2010;140(6):771—776. doi: 10.1016/j.cell.2010.03.006
- Edmunds T, Nagainis PA, Sathe SK, Thompson VF, Goll DE. Comparison of the autolyzed and unautolyzed forms of mu- and m-calpain from bovine skeletal muscle. Biochimica et Biophysica Acta. 1991;1077(2):197—208. doi: 10.1016/0167-4838 (91) 90059-9
- Beckmann JS, Spencer M. Calpain 3, the «gatekeeper» of proper sarcomere assembly, turnover and maintenance. Neuromuscular Disorders. 2008;18(12):913—921. doi: 10.1016/j.nmd.2008.08.005.
- Kramerova I, Kudryashova E, Ermolova N, Saenz A, Jaka O, López de Munain A, Spencer MJ. Impaired calcium calmodulin kinase signaling and muscle adaptation response in the absence of calpain 3. Human Molecular Genetics. 2012;21:3193—3204. doi: 10.1093/hmg/dds144
- Goll DE, Thompson VF, Li H, Wei W, Cong J The calpain system. Physiological Reviews. 2003;83:731—801. doi: 10.1152/physrev.00029.2002
- Baki A, Tompa P, Alexa A, Molnár O, Friedrich P. Autolysis parallels activation of mu-calpain. Biochemical Journal. 1996;318(Pt3):897—901. doi: 10.1042/bj3180897
- Nagainis PA, Wolfe FH, Sathe SK, Goll DE. Autolysis of the millimolar Ca2+-requiring form of the Ca2+-dependent proteinase from chicken skeletal muscle. Biochemistry and Cell Biology. 1988;66(10):1023—1031. doi: 10.1139/o88-118
- Murphy RM. Calpains, skeletal muscle function and exercise. Clinical and Experimental Pharmacology and Physiology. 2010;37(3):385—391. doi: 10.1111/j.1440-1681.2009.05310.x
- Kishimoto A, Mikawa K, Hashimoto K, Yasuda I, Tanaka S, Tominaga M, Kuroda T, Nishizuka Y. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). Journal of Biological Chemistry. 1989;264(7):4088—4092. PMID: 2537303
- Smuder AJ, Kavazis AN, Hudson MB, Nelson WB, Powers SK. Oxidation enhances myofibrillar protein degradation via calpain and caspase‑3. Free Radical Biology and Medicine. 2010;49(7):1152—1160. doi: 10.1016/j.freeradbiomed.2010.06.025
- Raastad T, Owe SG, Paulsen G, Enns D, Overgaard K, Crameri R, Kiil S, Belcastro A, Bergersen L, Hallén J. Changes in calpain activity, muscle structure, and function after eccentric exercise. Medicine & Science in Sports & Exercise. 2010;42(1):86—95. doi: 10.1249/MSS.0b013e3181ac7afa
- Purintrapiban J, Wang MC, Forsberg NE. Degradation of sarcomeric and cytoskeletal proteins in cultured skeletal muscle cells. Comparative Biochemistry and Physiology B. 2003;136(3):393—401. doi: 10.1016/s1096-4959(03)00201‑x
- Huang J, Forsberg NE. Role of calpain in skeletal-muscle protein degradation. Proceedings of the National Academy of Sciences USA. 1998;95(21):12100—12105. doi: 10.1073/pnas.95.21.12100
- Koohmaraie M. The role of Ca(2+)-dependent proteases (calpains) in post mortem proteolysis and meat tenderness. Biochimie. 1992;74(3):239—245. doi: 10.1016/0300-9084(92)90122‑u
- Bartoli M, Richard I. Calpains in muscle wasting. International Journal of Biochemistry & Cell Biology. 2005;37(10):2115—2133. doi: 10.1016/j.biocel.2004.12.012
- Goll DE, Neti G, Mares SW, Thompson VF. Myofibrillar protein turnover: the proteasome and the calpains. Journal of Animal Science. 2008;86(14): E19—35. doi: 10.2527/jas.2007-0395
- Kumar V, Atherton P, Smith K, Rennie MJ. Human muscle protein synthesis and breakdown during and after exercise. Journal of Applied Physiology (1985). 2009;106(6):2026—2039. doi: 10.1152/japplphysiol.91481.2008
- Lek A, Evesson FJ, Lemckert FA, Redpath GM, Lueders AK, Turnbull L, Whitchurch CB, North KN, Cooper ST. Calpains, cleaved mini-dysferlinC72, and L-type channels underpin calcium-dependent muscle membrane repair. Journal of Neuroscience. 2013;33(12):5085—5094. doi: 10.1523/JNEUROSCI.3560-12.2013
- Belcastro AN. Skeletal muscle calcium-activated neutral protease (calpain) with exercise. Journal of Applied Physiology (1985). 1993;74(3):1381—1386. doi: 10.1152/jappl.1993.74.3.1381
- Lametsch R, Roepstorff P, Møller HS, Bendixen E. Identification of myofibrillar substrates for μ-calpain. Meat Science. 2004;68(4):515—521. doi: 10.1016/j.meatsci.2004.03.018
- Roche JA, Lovering RM, Bloch RJ. Impaired recovery of dysferlin-null skeletal muscle after contraction-induced injury in vivo. Neuroreport. 2008;19(16):1579—1584. doi: 10.1097/WNR.0b013e328311ca35
- Indo HP, Yen HC, Nakanishi I, Matsumoto K, Tamura M, Nagano Y. A mitochondrial superoxide theory for oxidative stress diseases and aging. Journal of Clinical Biochemistry and Nutrition. 2015;56(1):1—7. doi: 10.3164/jcbn.14-42
- Lysenkov SP, Muzhenya DV, Tuguz AR, Urakova TU, Shumilov DS, Thakushinov IA, Thakushinov RA, Tatarkova EA, Urakova DM. Cholinergic deficiency in the cholinergic system as a pathogenetic link in the formation of various syndromes in COVID‑19. Chinese Journal of Physiology. 2023;66(1):1—13. doi: 10.4103/cjop.CJOP-D‑22-00072
- Averna M, Stifanese R, De Tullio R, Salamino F, Bertuccio M, Pontremoli S, Melloni E. Proteolytic degradation of nitric oxide synthase isoforms by calpain is modulated by the expression levels of HSP90. FEBS Journal. 2007;274(23):6116—6127. doi: 10.1111/j.1742-4658.2007.06133.x
- Bellocq A, Doublier S, Suberville S, Perez J, Escoubet B, Fouqueray B, Puyol DR, Baud L. Somatostatin increases glucocorticoid binding and signaling in macrophages by blocking the calpain-specific cleavage of Hsp 90. Journal of Biological Chemistry. 1999;274(52):36891—36896. doi: 10.1074/jbc.274.52.36891
- Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP. Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. American Journal of Physiology-Cell Physiology. 2010;298:365—376. doi: 10.1152/ajpcell.00365.2009
- Franzini-Armstrong C, Jorgensen AO. Structure and development of E-C coupling units in skeletal muscle. Annual Review of Physiology. 1994;56:509—534. doi: 10.1146/annurev.ph.56.030194.002453
- Kanzaki K, Watanabe D, Kuratani M, Yamada T, Matsunaga S, Wada M. Role of calpain in eccentric contraction-induced proteolysis of Ca2+-regulatory proteins and force depression in rat fast-twitch skeletal muscle. Journal of Applied Physiology (1985). 2017;122(2):396—405. doi: 10.1152/japplphysiol.00270.2016
- Setterberg IE, Le C, Frisk M, Li J, Louch WE. The Physiology and Pathophysiology of T-Tubules in the Heart. Frontiers in Physiology. 2021;12:718404. doi: 10.3389/fphys.2021.718404
- Hall DD, Takeshima H, Song LS. Structure, Function, and Regulation of the Junctophilin Family. Annual Review of Physiology. 2024;86:123—147. doi: 10.1146/annurev-physiol‑042022-014926
- Michel LY, Hoenderop JG, Bindels RJ. Calpain‑3‑mediated regulation of the Na+-Ca²+ exchanger isoform 3. Pflugers Archiv European Journal of Physiology. 2016;468(2):243—55. doi: 10.1007/s00424-015-1747-8
- Vermaelen M, Sirvent P, Raynaud F, Astier C, Mercier J, Lacampagne A, Cazorla O. Differential localization of autolyzed calpains 1 and 2 in slow and fast skeletal muscles in the early phase of atrophy. American Journal of Physiology-cell Physiology. 2007;292(5):1723—1731. doi: 10.1152/ajpcell.00398.2006
- Ojima K, Ono Y, Ottenheijm C, Hata S, Suzuki H, Granzier H, Sorimachi H. Non-proteolytic functions of calpain‑3 in sarcoplasmic reticulum in skeletal muscles. Journal of Molecular Biology. 2011;407(3):439—449. doi: 10.1016/j.jmb.2011.01.057
- Jude JA, Wylam ME, Walseth TF, Kannan MS. Calcium signaling in airway smooth muscle. Proceedings of the American Thoracic Society. 2008;5(1):15—22. doi: 10.1513/pats.200704-047VS
- Chen L, Tang F, Gao H, Zhang X, Li X, Xiao D. CAPN3: A musclespecific calpain with an important role in the pathogenesis of diseases (Review). International Journal of Molecular Medicine. 2021;48(5):203. doi: 10.3892/ijmm.2021.5036
- Aguti S, Gallus GN, Bianchi S, Salvatore S, Rubegni A, Berti G, Formichi P, De Stefano N, Malandrini A, Lopergolo D. Novel Biomarkers for Limb Girdle Muscular Dystrophy (LGMD). Cells. 2024;13(4):329. doi: 10.3390/cells13040329
- Fougerousse F, Bullen P, Herasse M, Lindsay S, Richard I, Wilson D, Suel L, Durand M, Robson S, Abitbol M, Beckmann JS, Strachan T. Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Human Molecular Genetics. 2000;9(2):165—173. doi: 10.1093/hmg/9.2.165
- Şahin İO, Karataş E, Demir M, Tan B, Per H, Özkul Y, Dündar M. A retrospective study on the clinical and molecular outcomes of calpainopathy in a Turkish patient cohort. Turkish Journal of Medical Sciences. 2023;54(1):86—98. doi: 10.55730/1300-0144.5769
- Kramerova I, Torres JA, Eskin A, Nelson SF, Spencer MJ. Calpain 3 and CaMKIIβ signaling are required to induce HSP70 necessary for adaptive muscle growth after atrophy. Human Molecular Genetics. 2018;27:1642—1653. doi: 10.1093/hmg/ddy071
- Lynch K, Fernandez G, Pappalardo A, Peluso JJ. Basic fibroblast growth factor inhibits apoptosis of spontaneously immortalized granulosa cells by regulating intracellular free calcium levels through a protein kinase Cdelta-dependent pathway. Endocrinology. 2000;141(11):4209—4217. doi: 10.1210/endo.141.11.7742
- Villani KR, Zhong R, Henley-Beasley CS, Rastelli G, Boncompagni S, Barton ER, Wei-LaPierre L. Loss of calpain 3 dysregulates store-operated calcium entry and its exercise response in mice. BioRxiv. 2024:2024.01.12.575391. doi: 10.1101/2024.01.12.575391
- Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nature Reviews Molecular Cell Biology. 2000;1(1):11—21. doi: 10.1038/35036035
- Lee HC, Walseth TF, Bratt GT, Hayes RN, Clapper DL. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. Journal of Biological Chemistry. 1989;264(3):1608—1615. PMID: 2912976
- Ernst IM, Fliegert R, Guse AH. Adenine Dinucleotide Second Messengers and T-lymphocyte Calcium Signaling. Frontiers in Immunology. 2013;4:259. doi: 10.3389/fimmu.2013.00259
- Baylor SM, Hollingworth S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. Journal of Physiology. 2003;551(Pt1):125—138. doi: 10.1113/jphysiol.2003.041608
- Galione A, Parrington J, Funnell T. Physiological roles of NAADP-mediated Ca2+ signaling. Science China Life Sciences. 2011;54(8):725—732. doi: 10.1007/s11427-011-4207-5
- Guse AH. Enzymology of Ca2+-Mobilizing Second Messengers Derived from NAD: From NAD Glycohydrolases to (Dual) NADPH Oxidases. Cells. 2023;12(4):675. doi: 10.3390/cells12040675.
- Lee HC, Aarhus R. A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. Journal of Biological Chemistry. 1995;270(5):2152—2157. doi: 10.1074/jbc.270.5.2152
- Churchill GC, Okada Y, Thomas JM, Genazzani AA, Patel S, Galione A. NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell. 2002;111(5):703—708. doi: 10.1016/s0092-8674 (02) 01082-6
- Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang KT, Lin P, Xiao R, Wang C, Zhu Y, Lin Y, Wyatt CN, Parrington J, Ma J, Evans AM, Galione A, Zhu MX. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature. 2009;459(7246):596—600. doi: 10.1038/nature08030
- Aley PK, Singh N, Brailoiu GC, Brailoiu E, Churchill GC. Nicotinic acid adenine dinucleotide phosphate (NAADP) is a second messenger in muscarinic receptor-induced contraction of guinea pig trachea. Journal of Biological Chemistry. 2013;288(16):10986—10993. doi: 10.1074/jbc.M113.458620
- Han Y, Weinman S, Boldogh I, Walker RK, Brasier AR. Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. Journal of Biological Chemistry. 1999;274:787—794. doi: 10.1074/jbc.274.2.787
- Iguchi-Hashimoto M, Usui T, Yoshifuji H, Shimizu M, Kobayashi S, Ito Y, Murakami K, Shiomi A, Yukawa N, Kawabata D, Nojima T, Ohmura K, Fujii T, Mimori T. Overexpression of a minimal domain of calpastatin suppresses IL‑6 production and Th17 development via reduced NF-κB and increased STAT5 signals. PLoS One. 2011;6: e27020. doi: 10.1371/journal.pone.0027020
- Kishimoto A, Mikawa K, Hashimoto K, Yasuda I, Tanaka S, Tominaga M, Kuroda T, Nishizuka Y. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). Journal of Biological Chemistry. 1989;264(7):4088—4092.
- Vasilev F, Limatola N, Chun JT, Santella L. Contributions of suboolemmal acidic vesicles and microvilli to the intracellular Ca2+ increase in the sea urchin eggs at fertilization. International Journal of Biological Sciences. 2019;15(4):757—775. doi: 10.7150/ijbs.28461
- Talbert EE, Smuder AJ, Min K, Kwon OS, Powers SK. Calpain and caspase‑3 play required roles in immobilization-induced limb muscle atrophy. Journal of Applied Physiology (1985). 2013;114(10):1482—1489. doi: 10.1152/japplphysiol.00925.2012
- Lovochkina ED. Diagnostic and prognostic role of cardiac pathology multicomplex autoimmune biological markers. RUDN Journal of Medicine. 2023;27(1):71—82. doi: 10.22363/2313-0245-2023-27-1-71-82
- Mandic A, Viktorsson K, Strandberg L, Heiden T, Hansson J, Linder S, Shoshan MC. Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Molecular and Cellular Biology. 2002;22(9):3003—3013. doi: 10.1128/MCB.22.9.3003-3013.2002
- Kobayashi S, Yamashita K, Takeoka T, Ohtsuki T, Suzuki Y, Takahashi R, Yamamoto K, Kaufmann SH, Uchiyama T, Sasada M, Takahashi A. Calpain-mediated X-linked inhibitor of apoptosis degradation in neutrophil apoptosis and its impairment in chronic neutrophilic leukemia. Journal of Biological Chemistry. 2002;277(37):33968—33977. doi: 10.1074/jbc.M203350200
- Bernardi P, Petronilli V, Di Lisa F, Forte M. A mitochondrial perspective on cell death. Trends in Biochemical Sciences. 2001;26(2):112—7. doi: 10.1016/s0968—0004(00)01745‑x
- Todt F, Cakir Z, Reichenbach F, Emschermann F, Lauterwasser J, Kaiser A, Ichim G, Tait SW, Frank S, Langer HF, Edlich F. Differential retrotranslocation of mitochondrial Bax and Bak. EMBO Journal. 2015;34(1):67—80. doi: 10.15252/embj.201488806
- Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differentiation. 2006;13(9):1423—1433. doi: 10.1038/sj.cdd.4401950
- Polster BM, Basañez G, Etxebarria A, Hardwick JM, Nicholls DG. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. Journal of Biological Chemistry. 2005;280(8):6447—54. doi: 10.1074/jbc.M413269200
- Cregan SP, Dawson VL, Slack RS. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene. 2004;23(16):2785—2796. doi: 10.1038/sj.onc.1207517
- Guo BS, Cheung KK, Yeung SS, Zhang BT, Yeung EW. Electrical stimulation influences satellite cell proliferation and apoptosis in unloading-induced muscle atrophy in mice. PLoS One. 2012;7(1): e30348. doi: 10.1371/journal.pone.0030348
Қосымша файлдар

