Skip to main content
Log in

Programmed Cell Death and its Implications for Skeletal Muscle Wasting

  • REVIEW ARTICLE
  • Published:
Indian Journal of Clinical Biochemistry Aims and scope Submit manuscript

Abstract

Skeletal muscle atrophy is an inevitable sequel of various factors such as cachexia, aging, fasting, denervation, and microgravity. It is characterized by reduced muscle protein through increased proteolysis and decreased protein synthesis. Recent research suggests that atrophy can significantly contribute to mortality among afflicted persons, and the hindrance of muscular deterioration is expected to extend lifespan. Programmed cell death or apoptosis is imperative for preserving the integrity of proliferative tissues. However, the exact role of apoptosis in post-mitotic tissues, such as skeletal muscle, remains less well-defined. Within the context of muscle atrophy, apoptosis occurs in both myonuclei as well as other types of muscle cells. The loss of muscle mass is likely attributed to the apoptotic demise of myonuclei, yet the mechanisms driving this process remain largely unknown. Both caspase-dependent and caspase-independent pathways have been implicated, with the specific mode of atrophy induction determining the apoptotic mechanisms utilized. Furthermore, it is still undetermined whether a reduction in apoptosis will ameliorate atrophy, necessitating distinct research strategies for various causes of skeletal muscle loss.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

All data obtained or analyzed during this study are included in this article.

References

  1. Yadav A, Yadav SS, Singh S, Dabur R. Natural products: Potential therapeutic agents to prevent skeletal muscle atrophy. Eur J Pharmacol. 2022. https://doi.org/10.1016/j.ejphar.2022.174995.

    Article  PubMed  Google Scholar 

  2. Joyce NC, Oskarsson B, Jin LW. Muscle biopsy evaluation in neuromuscular disorders. Phys Med Rehabil Clin N Am. 2012. https://doi.org/10.1016/j.pmr.2012.06.006.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Henderson CA, Gomez CG, Novak SM, Mi-Mi L, Gregorio CC. Overview of the muscle cytoskeleton. Compr Physiol. 2017. https://doi.org/10.1002/cphy.c160033.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gwin JA, Church DD, Wolfe RR, Ferrando AA, Pasiakos SM. Muscle protein synthesis and whole-body protein turnover responses to ingesting essential amino acids, intact protein, and protein-containing mixed meals with considerations for energy deficit. 2020. Nutrients. https://doi.org/10.3390/nu12082457.

  5. Roman W, Gomes ER. Nuclear positioning in skeletal muscle. Semin Cell Dev Biol. 2018. https://doi.org/10.1016/j.semcdb.2017.11.005.

    Article  PubMed  Google Scholar 

  6. Snijders T, Aussieker T, Holwerda A, Parise G, van Loon LJC, Verdijk LB. The concept of skeletal muscle memory: evidence from animal and human studies. Acta Physiol. 2020. https://doi.org/10.1111/apha.13465.

    Article  Google Scholar 

  7. Dupont-Versteegden EE. Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol. 2006. https://doi.org/10.3748/wjg.v12.i46.7463.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Dupont-Versteegden EE, Fluckey JD, Knox M, Gaddy D, Peterson CA. Effect of flywheel-based resistance exercise on processes contributing to muscle atrophy during unloading in adult rats. J Appl Physiol. 2006. https://doi.org/10.1152/japplphysiol.01540.2005.

    Article  PubMed  Google Scholar 

  9. Quadrilatero J, Bombardier E, Norris SM, Talanian JL, Palmer MS, Logan HM, et al. Prolonged moderate-intensity aerobic exercise does not alter apoptotic signaling and DNA fragmentation in human skeletal muscle. Am J Physiol Endocrinol Metab. 2010. https://doi.org/10.1152/ajpendo.00678.2009.

    Article  PubMed  Google Scholar 

  10. Yang Y, Jemiolo B, Trappe S. Proteolytic mRNA expression in response to acute resistance exercise in human single skeletal muscle fibers. J Appl Physiol. 2006. https://doi.org/10.1152/japplphysiol.00438.2006.

    Article  PubMed  Google Scholar 

  11. Powers SK, Deminice R, Ozdemir M, Yoshihara T, Bomkamp MP, Hyatt H. Exercise-induced oxidative stress: Friend or foe? J Sport Heal Sci. 2020;9:415–25. https://doi.org/10.1016/j.jshs.2020.04.001.

    Article  Google Scholar 

  12. Goldblatt ZE, Cirka HA, Billiar KL. Mechanical regulation of apoptosis in the cardiovascular system. Ann Biomed Eng. 2021. https://doi.org/10.1007/s10439-020-02659-x.

    Article  PubMed  Google Scholar 

  13. Schöneich C, Dremina E, Galeva N, Sharov V. Apoptosis in differentiating C2C12 muscle cells selectively targets Bcl-2-deficient myotubes. Apoptosis. 2014. https://doi.org/10.1007/s10495-013-0922-7.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bell RAV, Al-Khalaf MH, Brunette S, Alsowaida D, Chu A, Bandukwala H, et al. Chromatin reorganization during myoblast differentiation involves the caspase-dependent removal of SATB2. Cells. 2022. https://doi.org/10.3390/cells11060966.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Yang Y, Wang Z, Sun L, Shao L, Yang N, Yu D, et al. SATB1 mediates long-range chromatin interactions: a dual regulator of anti-apoptotic BCL2 and pro-apoptotic NOXA genes. PLoS ONE. 2015. https://doi.org/10.1371/journal.pone.0139170.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bai L, Liang R, Yang Y, Hou X, Wang Z, Zhu S, et al. MicroRNA-21 regulates PI3K/Akt/mTOR signaling by targeting TGFβI during skeletal muscle development in pigs. PLoS ONE. 2015. https://doi.org/10.1371/journal.pone.0119396.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Fu S, Yin L, Lin X, Lu J, Wang X. Effects of cyclic mechanical stretch on the proliferation of L6 myoblasts and its mechanisms: PI3K/Akt and MAPK signal pathways regulated by IGF-1 receptor. Int J Mol Sci. 2018. https://doi.org/10.3390/ijms19061649.

    Article  PubMed  PubMed Central  Google Scholar 

  18. He Y, Sun MM, Zhang GG, Yang J, Chen KS, Xu WW, et al. Targeting PI3K/Akt signal transduction for cancer therapy. Signal Transduct Target Ther. 2021. https://doi.org/10.1038/s41392-021-00828-5.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Beyfuss K, Hood DA. A systematic review of p53 regulation of oxidative stress in skeletal muscle. Redox Rep. 2018. https://doi.org/10.1080/13510002.2017.1416773.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Sladky VC, Villunger A. Uncovering the PIDDosome and caspase-2 as regulators of organogenesis and cellular differentiation. Cell Death Differ. 2020. https://doi.org/10.1038/s41418-020-0556-6.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lopez-Cruzan M, Sharma R, Tiwari M, Karbach S, Holstein D, Martin CR, et al. Caspase-2 resides in the mitochondria and mediates apoptosis directly from the mitochondrial compartment. Cell Death Discov. 2016. https://doi.org/10.1038/cddiscovery.2016.5.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Brown-Suedel AN, Bouchier-Hayes L. Caspase-2 Substrates: To Apoptosis, Cell Cycle Control, and Beyond. Front Cell Dev Biol. 2020. https://doi.org/10.3389/fcell.2020.610022.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Dehkordi HM, Tashakor A, Connell OE, Fearnhead HO. Apoptosomedependent myotube formation involves activation of caspase3 in differentiating myoblasts. Cell Death Dis. 2020. https://doi.org/10.1038/s41419-020-2502-4.

    Article  Google Scholar 

  24. Dick SA, Chang NC, Dumont NA, Bell RAV, Putinski C, Kawabe Y, et al. Caspase 3 cleavage of Pax7 inhibits self-renewal of satellite cells. Proc Natl Acad Sci U S A. 2015. https://doi.org/10.1073/pnas.1512869112.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Abraham AG, O’Neill E. PI3K/Akt-mediated regulation of p53 in cancer. Biochem Soc Trans. 2014. https://doi.org/10.1042/BST20140070.

    Article  PubMed  Google Scholar 

  26. Bratton SB, Salvesen GS. Regulation of the Apaf-1-caspase-9 apoptosome. J Cell Sci. 2010. https://doi.org/10.1242/jcs.073643.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Li P, Zhou L, Zhao T, Liu X, Zhang P, Liu Y, et al. Caspase-9: Structure mechanisms and clinical application. Oncotarget. 2017. https://doi.org/10.18632/oncotarget.15098.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Fernando P, Kelly JF, Balazsi K, Slack RS, Megeney LA. Caspase 3 activity is required for skeletal muscle differentiation. Proc Natl Acad Sci U S A. 2002;99:11025–30. https://doi.org/10.1073/pnas.162172899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jung YS, Qian Y, Chen X. Examination of the expanding pathways for the regulation of p21 expression and activity. Cell Signal. 2010. https://doi.org/10.1016/j.cellsig.2010.01.013.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Bloemberg D, Quadrilatero J. Mitochondrial pro-apoptotic indices do not precede the transient caspase activation associated with myogenesis. Biochim Biophys Acta - Mol Cell Res. 2014. https://doi.org/10.1016/j.bbamcr.2014.09.002.

    Article  Google Scholar 

  31. Rahman FA, Quadrilatero J. Mitochondrial apoptotic signaling involvement in remodeling during myogenesis and skeletal muscle atrophy. Semin Cell Dev Biol. 2023. https://doi.org/10.1016/j.semcdb.2022.01.011.

    Article  PubMed  Google Scholar 

  32. Kornasio R, Riederer I, Butler-Browne G, Mouly V, Uni Z, Halevy O. β-hydroxy-β-methylbutyrate (HMB) stimulates myogenic cell proliferation, differentiation and survival via the MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta - Mol Cell Res. 2009. https://doi.org/10.1016/j.bbamcr.2008.12.017.

    Article  Google Scholar 

  33. Marie Hardwick J, Soane L. Multiple functions of BCL-2 family proteins. Cold Spring Harb Perspect Biol. 2013. https://doi.org/10.1101/cshperspect.a008722.

    Article  PubMed  Google Scholar 

  34. Cook SA, Sugden PH, Clerk A. Regulation of Bcl-2 family proteins during development and in response to oxidative stress in cardiac myocytes association with changes in mitochondrial membrane potential. Circ Res. 1999. https://doi.org/10.1161/01.res.85.10.940.

    Article  PubMed  Google Scholar 

  35. Griffiths GS, Doe J, Jijiwa M, Van Ry P, Cruz V, de la Vega M, et al. Bit-1 is an essential regulator of myogenic differentiation. J Cell Sci. 2015. https://doi.org/10.1242/jcs.158964.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Seternes OM, Kidger AM, Keyse SM. Dual-specificity MAP kinase phosphatases in health and disease. Biochim Biophys Acta - Mol Cell Res. 2019. https://doi.org/10.1016/j.bbamcr.2018.09.002.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Singh GB, Cowan DB, Wang DZ. Tiny regulators of massive tissue: micrornas in skeletal muscle development, myopathies, and cancer cachexia. Front Oncol. 2020. https://doi.org/10.3389/fonc.2020.598964.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Cai B, Ma M, Chen B, Li Z, Abdalla BA, Nie Q, et al. MIR-16–5p targets SESN1 to regulate the p53 signaling pathway, affecting myoblast proliferation and apoptosis, and is involved in myoblast differentiation article. Cell Death Dis. 2018. https://doi.org/10.1038/s41419-018-0403-6.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Shen X, Tang J, Jiang R, Wang X, Yang Z, Huang Y, et al. CircRILPL1 promotes muscle proliferation and differentiation via binding miR-145 to activate IGF1R/PI3K/AKT pathway. Cell Death Dis. 2021. https://doi.org/10.1038/s41419-021-03419-y.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Peng S, Song C, Li H, Cao X, Ma Y, Wang X, et al. Circular RNA SNX29 Sponges miR-744 to regulate proliferation and differentiation of myoblasts by activating the Wnt5a/Ca2+ signaling pathway. Mol Ther Nucleic Acids. 2019. https://doi.org/10.1016/j.omtn.2019.03.009.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Kuang X, Wei C, Zhang T, Yang Z, Chi J, Wang L. MiR-378 inhibits cell growth and enhances apoptosis in human myelodysplastic syndromes. Int J Oncol. 2016. https://doi.org/10.3892/ijo.2016.3689.

    Article  PubMed  Google Scholar 

  42. Wei X, Li H, Zhang B, Li C, Dong D, Lan X, et al. miR-378a-3p promotes differentiation and inhibits proliferation of myoblasts by targeting HDAC4 in skeletal muscle development. RNA Biol. 2016. https://doi.org/10.1080/15476286.2016.1239008.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Li Y, Jiang J, Liu W, Wang H, Zhao L, Liu S, et al. MicroRNA-378 promotes autophagy and inhibits apoptosis in skeletal muscle. Proc Natl Acad Sci U S A. 2018. https://doi.org/10.1073/pnas.1803377115.

    Article  PubMed  PubMed Central  Google Scholar 

  44. McIlwain DR, Berger T, Mak TW. Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol. 2013. https://doi.org/10.1101/cshperspect.a008656.45.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Guicciardi ME, Gores GJ. Life and death by death receptors. FASEB J. 2009;23:1625–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Huang K, Zhang J, O’Neill KL, Gurumurthy CB, Quadros RM, Tu Y, et al. Cleavage by caspase 8 and mitochondrial membrane association activate the BH3-only protein bid during TRAIL-induced apoptosis. J Biol Chem. 2016. https://doi.org/10.1074/jbc.M115.711051.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Eskandari E, Eaves CJ. Paradoxical roles of caspase-3 in regulating cell survival, proliferation, and tumorigenesis. J Cell Biol. 2022. https://doi.org/10.1083/jcb.202201159.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Mishra P, Varuzhanyan G, Pham AH, Chan DC. Mitochondrial dynamics is a distinguishing feature of skeletal muscle fiber types and regulates organellar compartmentalization. Cell Metab. 2015. https://doi.org/10.1016/j.cmet.2015.09.027.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Shan ZX, Lin QX, Deng CY, Zhu JN, Mai LP, Liu JL, et al. MiR-1/miR-206 regulate Hsp60 expression contributing to glucose-mediated apoptosis in cardiomyocytes. FEBS Lett. 2010. https://doi.org/10.1016/j.febslet.2010.07.027.

    Article  PubMed  Google Scholar 

  50. Yu Y, Li X, Liu L, Chai J, Haijun Z, Chu W, et al. miR-628 promotes burn-induced skeletal muscle atrophy via targeting IRS1. Int J Biol Sci. 2016. https://doi.org/10.7150/ijbs.15496.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Plant PJ, Bain JR, Correa JE, Woo M, Batt J. Absence of caspase-3 protects against denervation-induced skeletal muscle atrophy. J Appl Physiol. 2009. https://doi.org/10.1152/japplphysiol.90932.2008.

    Article  PubMed  Google Scholar 

  52. Jan R, Chaudhry GS. Understanding apoptosis and apoptotic pathways targeted cancer therapeutics. Adv Pharm Bull. 2019. https://doi.org/10.15171/apb.2019.024.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Vitale I, Pietrocola F, Guilbaud E, Aaronson SA, Abrams JM, Adam D, et al. Apoptotic cell death in disease—current understanding of the NCCD 2023. Cell Death Differ. 2023. https://doi.org/10.1038/s41418-023-01153-w.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Barnes BT, Confides AL, Rich MM, Dupont-Versteegden EE. Distinct muscle apoptotic pathways are activated in muscles with different fiber types in a rat model of critical illness myopathy. J Muscle Res Cell Motil. 2015. https://doi.org/10.1007/s10974-015-9410-8.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Chen X, Chen L, Jiang S, Huang S. Maduramicin induces apoptosis and necrosis, and blocks autophagic flux in myocardial H9c2 cells. J Appl Toxicol. 2018. https://doi.org/10.1002/jat.3546.

    Article  PubMed  Google Scholar 

  56. Collins BC, Laakkonen EK, Lowe DA. Aging of the musculoskeletal system: How the loss of estrogen impacts muscle strength. Bone. 2019. https://doi.org/10.1016/j.bone.2019.03.033.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Karvinen S, Juppi HK, Le G, Cabelka CA, Mader TL, Lowe DA, et al. Estradiol deficiency and skeletal muscle apoptosis: Possible contribution of microRNAs. Exp Gerontol. 2021. https://doi.org/10.1016/j.exger.2021.111267.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Zhang X, Jing W. Upregulation of miR-122 is associated with cardiomyocyte apoptosis in atrial fibrillation. Mol Med Rep. 2018. https://doi.org/10.3892/mmr.2018.9124.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Kamiya M, Kimura N, Umezawa N, Hasegawa H, Yasuda S. Muscle fiber necroptosis in pathophysiology of idiopathic inflammatory myopathies and its potential as target of novel treatment strategy. Front Immunol. 2023. https://doi.org/10.3389/fimmu.2023.1191815.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Furtado GE, Narici MV, Dwolatzky T. Editorial: molecular and physiological aspects of sarcopenia in the older person: mechanisms, diagnostics and therapy. Front Med. 2023. https://doi.org/10.3389/fimmu.2023.1191815.

    Article  Google Scholar 

  61. Pistilli EE, Jackson JR, Alway SE. Death receptor-associated pro-apoptotic signaling in aged skeletal muscle. Apoptosis. 2006. https://doi.org/10.1007/s10495-006-0194-6.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ludwig-Galezowska AH, Flanagan L, Rehm M. Apoptosis repressor with caspase recruitment domain, a multifunctional modulator of cell death. J Cell Mol Med. 2011. https://doi.org/10.1111/j.1582-4934.2010.01221.x.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Belenichev IF, Aliyeva OG, Popazova OO, Bukhtiyarova NV. Involvement of heat shock proteins HSP70 in the mechanisms of endogenous neuroprotection: the prospect of using HSP70 modulators. Front Cell Neurosci. 2023. https://doi.org/10.3389/fncel.2023.1131683.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Lanneau D, Brunet M, Frisan E, Solary E, Fontenay M, Garrido C. Heat shock proteins: essential proteins for apoptosis regulation: apoptosis review series. J Cell Mol Med. 2008. https://doi.org/10.1111/j.1582-4934.2008.00273.x.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Marzetti E, Privitera G, Simili V, Wohlgemuth SE, Aulisa L, Pahor M, et al. Multiple pathways to the same end: Mechanisms of myonuclear apoptosis in sarcopenia of aging. ScientificWorldJournal. 2010. https://doi.org/10.1016/j.bbagen.2009.05.007.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Alm-Eldeen A, Khamis A, Elfiky N, Ahmad R. Quercetin modulates age-induced changes in the transcript levels of some apoptosis related genes in the skeletal muscles of male rats. Brazilian J Pharm Sci. 2020. https://doi.org/10.1590/S2175-979020200003180861.

    Article  Google Scholar 

  67. Marzetti E, Hwang JCY, Lees HA, Wohlgemuth SE, Dupont-Versteegden EE, Carter CS, et al. Mitochondrial death effectors: relevance to sarcopenia and disuse muscle atrophy. Biochim Biophys Acta Gen Subj. 2010. https://doi.org/10.1016/j.bbagen.2009.05.007.

    Article  Google Scholar 

  68. Yang X, Xue P, Chen H, Yuan M, Kang Y, Duscher D, et al. Denervation drives skeletal muscle atrophy and induces mitochondrial dysfunction, mitophagy and apoptosis via miR-142a-5p/MFN1 axis. Theranostics. 2020. https://doi.org/10.7150/thno.40857.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ikwegbue PC, Masamba P, Oyinloye BE, Kappo AP. Roles of heat shock proteins in apoptosis, oxidative stress, human inflammatory diseases, and cancer. Pharmaceuticals. 2018. https://doi.org/10.3390/ph11010002.

    Article  Google Scholar 

  70. Hrdinka M, Yabal M. Inhibitor of apoptosis proteins in human health and disease. Genes Immun. 2019. https://doi.org/10.1038/s41435-019-0078-8.

    Article  PubMed  Google Scholar 

  71. Haldar S, Basu A, Croce CM. Serine-70 is one of the critical sites for drug-induced Bcl2 phosphorylation in cancer cells. Cancer Res. 1998;58:1609–15.

    CAS  PubMed  Google Scholar 

  72. Dadsena S, Jenner A, García-Sáez AJ. Mitochondrial outer membrane permeabilization at the single molecule level. Cell Mol Life Sci. 2021. https://doi.org/10.1007/s00018-021-03771-4.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Gesing A, Masternak MM, Wang F, Lewinski A, Karbownik-Lewinska M, Bartke A. Decreased expression level of apoptosis-related genes and/or proteins in skeletal muscles, but not in hearts, of growth hormone receptor knockout mice. Exp Biol Med. 2011. https://doi.org/10.1258/ebm.2010.010202.

    Article  Google Scholar 

  74. Avrutsky MI, Troy CM. Caspase-9: A Multimodal Therapeutic Target With Diverse Cellular Expression in Human Disease. Front Pharmacol. 2021. https://doi.org/10.3389/fphar.2021.701301.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Parrish AB, Freel CD, Kornbluth S. Cellular mechanisms controlling caspase activation and function. Cold Spring Harb Perspect Biol. 2013. https://doi.org/10.1101/cshperspect.a008672.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Schwartz LM. Skeletal muscles do not undergo apoptosis during either atrophy or programmed cell death-revisiting the myonuclear domain hypothesis. Front Physiol. 2019. https://doi.org/10.3389/fphys.2018.01887.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Cavalcante GC, Schaan AP, Cabral GF, Santana-Da-Silva MN, Pinto P, Vidal AF, et al. A cell’s fate: An overview of the molecular biology and genetics of apoptosis. Int J Mol Sci. 2019. https://doi.org/10.3390/ijms20174133.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Bruusgaard JC, Johansen IB, Egner IM, Rana ZA, Gundersen K. Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining. Proc Natl Acad Sci U S A. 2010. https://doi.org/10.1073/pnas.0913935107.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Rajesh Dabur has suggested the idea and collected the content of this research article. Aarti Yadav edited the figures and manuscript.

Corresponding author

Correspondence to Rajesh Dabur.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical Approval

Not applicable.

Consent for Publication

Not Applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dabur, R., Yadav, A. Programmed Cell Death and its Implications for Skeletal Muscle Wasting. Ind J Clin Biochem (2024). https://doi.org/10.1007/s12291-024-01223-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12291-024-01223-x

Keywords

Navigation