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Mitochondrial network remodeling: an important feature of myogenesis and skeletal muscle regeneration

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Abstract

The remodeling of the mitochondrial network is a critical process in maintaining cellular homeostasis and is intimately related to mitochondrial function. The interplay between the formation of new mitochondria (biogenesis) and the removal of damaged mitochondria (mitophagy) provide a means for the repopulation of the mitochondrial network. Additionally, mitochondrial fission and fusion serve as a bridge between biogenesis and mitophagy. In recent years, the importance of these processes has been characterised in multiple tissue- and cell-types, and under various conditions. In skeletal muscle, the robust remodeling of the mitochondrial network is observed, particularly after injury where large portions of the tissue/cell structures are damaged. The significance of mitochondrial remodeling in regulating skeletal muscle regeneration has been widely studied, with alterations in mitochondrial remodeling processes leading to incomplete regeneration and impaired skeletal muscle function. Needless to say, important questions related to mitochondrial remodeling and skeletal muscle regeneration still remain unanswered and require further investigation. Therefore, this review will discuss the known molecular mechanisms of mitochondrial network remodeling, as well as integrate these mechanisms and discuss their relevance in myogenesis and regenerating skeletal muscle.

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References

  1. Baechler BL, Bloemberg D, Quadrilatero J (2019) Mitophagy regulates mitochondrial network signaling, oxidative stress, and apoptosis during myoblast differentiation. Autophagy 15:1606–1619. https://doi.org/10.1080/15548627.2019.1591672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bernardini JP, Lazarou M, Dewson G (2017) Parkin and mitophagy in cancer. Oncogene 36:1315–1327. https://doi.org/10.1038/onc.2016.302

    Article  CAS  PubMed  Google Scholar 

  3. Bloemberg D, Quadrilatero J (2019) Autophagy, apoptosis, and mitochondria: molecular integration and physiological relevance in skeletal muscle. Am J Physiol Cell Physiol 317:C111–C130. https://doi.org/10.1152/ajpcell.00261.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. LeBleu VS, O’Connell JT, Gonzalez Herrera KN et al (2014) PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol 16:992–1003. https://doi.org/10.1038/ncb3039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rimbaud S, Garnier A, Ventura-Clapier R (2009) Mitochondrial biogenesis in cardiac pathophysiology. Pharmacol Rep 61:131–138. https://doi.org/10.1016/S1734-1140(09)70015-5

    Article  CAS  PubMed  Google Scholar 

  6. Salem AF, Whitaker-Menezes D, Howell A et al (2012) Mitochondrial biogenesis in epithelial cancer cells promotes breast cancer tumor growth and confers autophagy resistance. Cell Cycle 11:4174–4180. https://doi.org/10.4161/cc.22376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Schumacker PT, Gillespie MN, Nakahira K et al (2014) Mitochondria in lung biology and pathology: more than just a powerhouse. Am J Physiol Lung Cell Mol Physiol 306:L962–L974. https://doi.org/10.1152/ajplung.00073.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Zhou J, Li G, Zheng Y et al (2015) A novel autophagy/mitophagy inhibitor liensinine sensitizes breast cancer cells to chemotherapy through DNM1L-mediated mitochondrial fission. Autophagy 11:1259–1279. https://doi.org/10.1080/15548627.2015.1056970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Fu W, Liu Y, Yin H (2019) Mitochondrial dynamics: biogenesis, fission, fusion, and mitophagy in the regulation of stem cell behaviors. In: Stem cells international. https://www.hindawi.com/journals/sci/2019/9757201/. Accessed 5 June 2020

  10. Wagatsuma A, Kotake N, Yamada S (2011) Muscle regeneration occurs to coincide with mitochondrial biogenesis. Mol Cell Biochem 349:139–147. https://doi.org/10.1007/s11010-010-0668-2

    Article  CAS  PubMed  Google Scholar 

  11. Nichenko AS, Southern WM, Tehrani KF et al (2020) Mitochondrial-specific autophagy linked to mitochondrial dysfunction following traumatic freeze injury in mice. Am J Physiol Cell Physiol 318:C242–C252. https://doi.org/10.1152/ajpcell.00123.2019

    Article  CAS  PubMed  Google Scholar 

  12. Finck BN, Kelly DP (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Investig 116:615–622. https://doi.org/10.1172/JCI27794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lin J, Handschin C, Spiegelman BM (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1:361–370. https://doi.org/10.1016/j.cmet.2005.05.004

    Article  CAS  PubMed  Google Scholar 

  14. Gleyzer N, Scarpulla RC (2011) PGC-1-related coactivator (PRC), a sensor of metabolic stress, orchestrates a redox-sensitive program of inflammatory gene expression. J Biol Chem 286:39715–39725. https://doi.org/10.1074/jbc.M111.291575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Liang H, Ward WF (2006) PGC-1α: a key regulator of energy metabolism. Adv Physiol Educ 30:145–151. https://doi.org/10.1152/advan.00052.2006

    Article  PubMed  Google Scholar 

  16. Sonoda J, Mehl IR, Chong L-W et al (2007) PGC-1beta controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc Natl Acad Sci USA 104:5223–5228. https://doi.org/10.1073/pnas.0611623104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Fernandez-Marcos PJ, Auwerx J (2011) Regulation of PGC-1α, a nodal regulator of mitochondrial biogenesis1234. Am J Clin Nutr 93:884S-890S. https://doi.org/10.3945/ajcn.110.001917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Arany Z, Lebrasseur N, Morris C et al (2007) The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab 5:35–46. https://doi.org/10.1016/j.cmet.2006.12.003

    Article  CAS  PubMed  Google Scholar 

  19. Islam H, Hood DA, Gurd BJ (2020) Looking beyond PGC-1α: emerging regulators of exercise-induced skeletal muscle mitochondrial biogenesis and their activation by dietary compounds. Appl Physiol Nutr Metab 45:11–23. https://doi.org/10.1139/apnm-2019-0069

    Article  PubMed  Google Scholar 

  20. Kamei Y, Ohizumi H, Fujitani Y et al (2003) PPARgamma coactivator 1beta/ERR ligand 1 is an ERR protein ligand, whose expression induces a high-energy expenditure and antagonizes obesity. Proc Natl Acad Sci USA 100:12378–12383. https://doi.org/10.1073/pnas.2135217100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Philp A, Perez-Schindler J, Green C et al (2010) Pyruvate suppresses PGC1alpha expression and substrate utilization despite increased respiratory chain content in C2C12 myotubes. Am J Physiol Cell Physiol 299:C240-250. https://doi.org/10.1152/ajpcell.00438.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Shao D, Liu Y, Liu X et al (2010) PGC-1 beta-regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERR alpha. Mitochondrion 10:516–527. https://doi.org/10.1016/j.mito.2010.05.012

    Article  CAS  PubMed  Google Scholar 

  23. Wilson L, Yang Q, Szustakowski JD et al (2007) Pyruvate induces mitochondrial biogenesis by a PGC-1 alpha-independent mechanism. Am J Physiol, Cell Physiol 292:C1599-1605. https://doi.org/10.1152/ajpcell.00428.2006

    Article  CAS  Google Scholar 

  24. Popov DV, Lysenko EA, Kuzmin IV et al (2015) Regulation of PGC-1α isoform expression in skeletal muscles. Acta Naturae 7:48–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rowe GC, Jiang A, Arany Z (2010) PGC-1 coactivators in cardiac development and disease. Circ Res 107:825–838. https://doi.org/10.1161/CIRCRESAHA.110.223818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chan JY, Kwong M, Lu R et al (1998) Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. EMBO J 17:1779–1787. https://doi.org/10.1093/emboj/17.6.1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ristevski S, O’Leary DA, Thornell AP et al (2004) The ETS transcription factor GABPalpha is essential for early embryogenesis. Mol Cell Biol 24:5844–5849. https://doi.org/10.1128/MCB.24.13.5844-5849.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ploumi C, Daskalaki I, Tavernarakis N (2017) Mitochondrial biogenesis and clearance: a balancing act. FEBS J 284:183–195. https://doi.org/10.1111/febs.13820

    Article  CAS  PubMed  Google Scholar 

  29. Bruni F, Polosa PL, Gadaleta MN et al (2010) Nuclear respiratory factor 2 induces the expression of many but not all human proteins acting in mitochondrial DNA transcription and replication. J Biol Chem 285:3939–3948. https://doi.org/10.1074/jbc.M109.044305

    Article  CAS  PubMed  Google Scholar 

  30. Domcke S, Bardet AF, Adrian Ginno P et al (2015) Competition between DNA methylation and transcription factors determines binding of NRF1. Nature 528:575–579. https://doi.org/10.1038/nature16462

    Article  CAS  PubMed  Google Scholar 

  31. Ryu D, Jo YS, Lo Sasso G et al (2014) A SIRT7-dependent acetylation switch of GABPβ1 controls mitochondrial function. Cell Metab 20:856–869. https://doi.org/10.1016/j.cmet.2014.08.001

    Article  CAS  PubMed  Google Scholar 

  32. Schreiber SN, Knutti D, Brogli K et al (2003) The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor alpha (ERRalpha). J Biol Chem 278:9013–9018. https://doi.org/10.1074/jbc.M212923200

    Article  CAS  PubMed  Google Scholar 

  33. Schreiber SN, Emter R, Hock MB et al (2004) The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci USA 101:6472–6477. https://doi.org/10.1073/pnas.0308686101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Cho Y, Hazen BC, Russell AP, Kralli A (2013) Peroxisome proliferator-activated receptor γ coactivator 1 (PGC-1)- and estrogen-related receptor (ERR)-induced regulator in muscle 1 (Perm1) is a tissue-specific regulator of oxidative capacity in skeletal muscle cells. J Biol Chem 288:25207–25218. https://doi.org/10.1074/jbc.M113.489674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cho Y, Hazen BC, Gandra PG et al (2016) Perm1 enhances mitochondrial biogenesis, oxidative capacity, and fatigue resistance in adult skeletal muscle. FASEB J 30:674–687. https://doi.org/10.1096/fj.15-276360

    Article  CAS  PubMed  Google Scholar 

  36. Cho Y, Tachibana S, Hazen BC et al (2019) Perm1 regulates CaMKII activation and shapes skeletal muscle responses to endurance exercise training. Mol Metab 23:88–97. https://doi.org/10.1016/j.molmet.2019.02.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lin J, Wu H, Tarr PT et al (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418:797–801. https://doi.org/10.1038/nature00904

    Article  CAS  PubMed  Google Scholar 

  38. Rowe GC, El-Khoury R, Patten IS et al (2012) PGC-1α is dispensable for exercise-induced mitochondrial biogenesis in skeletal muscle. PLoS ONE. https://doi.org/10.1371/journal.pone.0041817

    Article  PubMed  PubMed Central  Google Scholar 

  39. Zechner C, Lai L, Zechner JF et al (2010) Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity. Cell Metab 12:633–642. https://doi.org/10.1016/j.cmet.2010.11.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lelliott CJ, Medina-Gomez G, Petrovic N et al (2006) Ablation of PGC-1beta results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol 4:e369. https://doi.org/10.1371/journal.pbio.0040369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Yamano K, Youle RJ (2011) Coupling mitochondrial and cell division. Nat Cell Biol 13:1026–1027. https://doi.org/10.1038/ncb2334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Twig G, Shirihai OS (2011) The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal 14:1939–1951. https://doi.org/10.1089/ars.2010.3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Youle RJ, Karbowski M (2005) Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6:657–663. https://doi.org/10.1038/nrm1697

    Article  CAS  PubMed  Google Scholar 

  44. Chen H, Vermulst M, Wang YE et al (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141:280–289. https://doi.org/10.1016/j.cell.2010.02.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ramos ES, Motori E, Brüser C et al (2019) Mitochondrial fusion is required for regulation of mitochondrial DNA replication. PLoS Genet 15:e1008085. https://doi.org/10.1371/journal.pgen.1008085

    Article  CAS  Google Scholar 

  46. Kraus F, Ryan MT (2017) The constriction and scission machineries involved in mitochondrial fission. J Cell Sci 130:2953–2960. https://doi.org/10.1242/jcs.199562

    Article  CAS  PubMed  Google Scholar 

  47. Ramachandran R (2018) Mitochondrial dynamics: the dynamin superfamily and execution by collusion. Semin Cell Dev Biol 76:201–212. https://doi.org/10.1016/j.semcdb.2017.07.039

    Article  CAS  PubMed  Google Scholar 

  48. Osellame LD, Singh AP, Stroud DA et al (2016) Cooperative and independent roles of the Drp1 adaptors Mff, MiD49 and MiD51 in mitochondrial fission. J Cell Sci 129:2170–2181. https://doi.org/10.1242/jcs.185165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Fröhlich C, Grabiger S, Schwefel D et al (2013) Structural insights into oligomerization and mitochondrial remodelling of dynamin 1-like protein. EMBO J 32:1280–1292. https://doi.org/10.1038/emboj.2013.74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mears JA, Lackner LL, Fang S et al (2011) Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat Struct Mol Biol 18:20–26. https://doi.org/10.1038/nsmb.1949

    Article  CAS  PubMed  Google Scholar 

  51. Morita M, Prudent J, Basu K et al (2017) mTOR controls mitochondrial dynamics and cell survival via MTFP1. Mol Cell 67:922-935.e5. https://doi.org/10.1016/j.molcel.2017.08.013

    Article  CAS  PubMed  Google Scholar 

  52. Tondera D, Czauderna F, Paulick K et al (2005) The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J Cell Sci 118:3049–3059. https://doi.org/10.1242/jcs.02415

    Article  CAS  PubMed  Google Scholar 

  53. Cho B, Cho HM, Jo Y et al (2017) Constriction of the mitochondrial inner compartment is a priming event for mitochondrial division. Nat Commun 8:15754. https://doi.org/10.1038/ncomms15754

    Article  PubMed  PubMed Central  Google Scholar 

  54. Chen H, Detmer SA, Ewald AJ et al (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160:189–200. https://doi.org/10.1083/jcb.200211046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ishihara N, Eura Y, Mihara K (2004) Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J Cell Sci 117:6535–6546. https://doi.org/10.1242/jcs.01565

    Article  CAS  PubMed  Google Scholar 

  56. Ban T, Ishihara T, Kohno H et al (2017) Molecular basis of selective mitochondrial fusion by heterotypic action between OPA1 and cardiolipin. Nat Cell Biol 19:856–863. https://doi.org/10.1038/ncb3560

    Article  CAS  PubMed  Google Scholar 

  57. Anand R, Wai T, Baker MJ et al (2014) The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission. J Cell Biol 204:919–929. https://doi.org/10.1083/jcb.201308006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Lee H, Smith SB, Yoon Y (2017) The short variant of the mitochondrial dynamin OPA1 maintains mitochondrial energetics and cristae structure. J Biol Chem 292:7115–7130. https://doi.org/10.1074/jbc.M116.762567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Friedman JR, Lackner LL, West M et al (2011) ER tubules mark sites of mitochondrial division. Science 334:358–362. https://doi.org/10.1126/science.1207385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Moltedo O, Remondelli P, Amodio G (2019) The mitochondria-endoplasmic reticulum contacts and their critical role in aging and age-associated diseases. Front Cell Dev Biol. https://doi.org/10.3389/fcell.2019.00172

    Article  PubMed  PubMed Central  Google Scholar 

  61. Sugiura A, Nagashima S, Tokuyama T et al (2013) MITOL regulates endoplasmic reticulum-mitochondria contacts via Mitofusin2. Mol Cell 51:20–34. https://doi.org/10.1016/j.molcel.2013.04.023

    Article  CAS  PubMed  Google Scholar 

  62. Ji W-K, Chakrabarti R, Fan X et al (2017) Receptor-mediated Drp1 oligomerization on endoplasmic reticulum. J Cell Biol 216:4123–4139. https://doi.org/10.1083/jcb.201610057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Korobova F, Ramabhadran V, Higgs HN (2013) An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339:464–467. https://doi.org/10.1126/science.1228360

    Article  CAS  PubMed  Google Scholar 

  64. Korobova F, Gauvin TJ, Higgs HN (2014) A role for myosin II in mammalian mitochondrial fission. Curr Biol 24:409–414. https://doi.org/10.1016/j.cub.2013.12.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Abrisch RG, Gumbin SC, Wisniewski BT et al (2020) Fission and fusion machineries converge at ER contact sites to regulate mitochondrial morphology. J Cell Biol. https://doi.org/10.1083/jcb.201911122

    Article  PubMed  PubMed Central  Google Scholar 

  66. Frohman MA (2015) Role of mitochondrial lipids in guiding fission and fusion. J Mol Med (Berl) 93:263–269. https://doi.org/10.1007/s00109-014-1237-z

    Article  CAS  Google Scholar 

  67. Parra V, Eisner V, Chiong M et al (2008) Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc Res 77:387–397. https://doi.org/10.1093/cvr/cvm029

    Article  CAS  PubMed  Google Scholar 

  68. Kuzmicic J, Parra V, Verdejo HE et al (2014) Trimetazidine prevents palmitate-induced mitochondrial fission and dysfunction in cultured cardiomyocytes. Biochem Pharmacol 91:323–336. https://doi.org/10.1016/j.bcp.2014.07.022

    Article  CAS  PubMed  Google Scholar 

  69. Bustillo-Zabalbeitia I, Montessuit S, Raemy E et al (2014) Specific interaction with cardiolipin triggers functional activation of dynamin-related protein 1. PLoS ONE 9:e102738. https://doi.org/10.1371/journal.pone.0102738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Francy CA, Alvarez FJD, Zhou L et al (2015) The mechanoenzymatic core of dynamin-related protein 1 comprises the minimal machinery required for membrane constriction. J Biol Chem 290:11692–11703. https://doi.org/10.1074/jbc.M114.610881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Francy CA, Clinton RW, Fröhlich C et al (2017) Cryo-EM studies of Drp1 reveal cardiolipin interactions that activate the helical oligomer. Sci Rep 7:10744. https://doi.org/10.1038/s41598-017-11008-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Macdonald PJ, Stepanyants N, Mehrotra N et al (2014) A dimeric equilibrium intermediate nucleates Drp1 reassembly on mitochondrial membranes for fission. Mol Biol Cell 25:1905–1915. https://doi.org/10.1091/mbc.E14-02-0728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Stepanyants N, Macdonald PJ, Francy CA et al (2015) Cardiolipin’s propensity for phase transition and its reorganization by dynamin-related protein 1 form a basis for mitochondrial membrane fission. Mol Biol Cell 26:3104–3116. https://doi.org/10.1091/mbc.E15-06-0330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Ugarte-Uribe B, Mueller H-M, Otsuki M et al (2014) Dynamin-related protein 1 (Drp1) promotes structural intermediates of membrane division. J Biol Chem jbc.M114.575779. https://doi.org/10.1074/jbc.M114.575779

  75. Baba T, Kashiwagi Y, Arimitsu N et al (2014) Phosphatidic acid (PA)-preferring phospholipase A1 regulates mitochondrial dynamics. J Biol Chem 289:11497–11511. https://doi.org/10.1074/jbc.M113.531921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Choi S-Y, Huang P, Jenkins GM et al (2006) A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat Cell Biol 8:1255–1262. https://doi.org/10.1038/ncb1487

    Article  CAS  PubMed  Google Scholar 

  77. Adachi Y, Itoh K, Yamada T et al (2016) Coincident phosphatidic acid interaction restrains Drp1 in mitochondrial division. Mol Cell 63:1034–1043. https://doi.org/10.1016/j.molcel.2016.08.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Adachi Y, Iijima M, Sesaki H (2018) An unstructured loop that is critical for interactions of the stalk domain of Drp1 with saturated phosphatidic acid. Small GTPases 9:472–479. https://doi.org/10.1080/21541248.2017.1321614

    Article  CAS  PubMed  Google Scholar 

  79. Kubli DA, Gustafsson ÅB (2012) Mitochondria and mitophagy: the Yin and Yang of cell death control. Circ Res 111:1208–1221. https://doi.org/10.1161/CIRCRESAHA.112.265819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Leonhard K, Herrmann JM, Stuart RA et al (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J 15:4218–4229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Leonhard K, Guiard B, Pellecchia G et al (2000) Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol Cell 5:629–638. https://doi.org/10.1016/s1097-2765(00)80242-7

    Article  CAS  PubMed  Google Scholar 

  82. Karunadharma PP, Basisty N, Chiao YA et al (2015) Respiratory chain protein turnover rates in mice are highly heterogeneous but strikingly conserved across tissues, ages, and treatments. FASEB J 29:3582–3592. https://doi.org/10.1096/fj.15-272666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Soubannier V, McLelland G-L, Zunino R et al (2012) A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr Biol 22:135–141. https://doi.org/10.1016/j.cub.2011.11.057

    Article  CAS  PubMed  Google Scholar 

  84. Soubannier V, Rippstein P, Kaufman BA et al (2012) Reconstitution of mitochondria derived vesicle formation demonstrates selective enrichment of oxidized cargo. PLoS ONE 7:e52830. https://doi.org/10.1371/journal.pone.0052830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Bravo-San Pedro JM, Kroemer G, Galluzzi L (2017) Autophagy and mitophagy in cardiovascular disease. Circ Res 120:1812–1824. https://doi.org/10.1161/CIRCRESAHA.117.311082

    Article  CAS  PubMed  Google Scholar 

  86. Kerr JS, Adriaanse BA, Greig NH et al (2017) Mitophagy and Alzheimer’s disease: cellular and molecular mechanisms. Trends Neurosci 40:151–166. https://doi.org/10.1016/j.tins.2017.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Liu J, Liu W, Li R, Yang H (2019) Mitophagy in Parkinson’s disease: from pathogenesis to treatment. Cells. https://doi.org/10.3390/cells8070712

    Article  PubMed  PubMed Central  Google Scholar 

  88. VanderVeen BN, Fix DK, Carson JA (2017) Disrupted skeletal muscle mitochondrial dynamics, mitophagy, and biogenesis during cancer cachexia: a role for inflammation. In: Oxidative medicine and cellular longevity. https://www.hindawi.com/journals/omcl/2017/3292087/. Accessed 7 June 2020

  89. Matsuda N, Sato S, Shiba K et al (2010) PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 189:211–221. https://doi.org/10.1083/jcb.200910140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Narendra DP, Jin SM, Tanaka A et al (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8:e1000298. https://doi.org/10.1371/journal.pbio.1000298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Greene AW, Grenier K, Aguileta MA et al (2012) Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep 13:378–385. https://doi.org/10.1038/embor.2012.14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Deas E, Plun-Favreau H, Gandhi S et al (2011) PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum Mol Genet 20:867–879. https://doi.org/10.1093/hmg/ddq526

    Article  CAS  PubMed  Google Scholar 

  93. Jin SM, Lazarou M, Wang C et al (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol 191:933–942. https://doi.org/10.1083/jcb.201008084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Meissner C, Lorenz H, Weihofen A et al (2011) The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J Neurochem 117:856–867. https://doi.org/10.1111/j.1471-4159.2011.07253.x

    Article  CAS  PubMed  Google Scholar 

  95. Shi G, Lee JR, Grimes DA et al (2011) Functional alteration of PARL contributes to mitochondrial dysregulation in Parkinson’s disease. Hum Mol Genet 20:1966–1974. https://doi.org/10.1093/hmg/ddr077

    Article  CAS  PubMed  Google Scholar 

  96. Yamano K, Youle RJ (2013) PINK1 is degraded through the N-end rule pathway. Autophagy 9:1758–1769. https://doi.org/10.4161/auto.24633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Lazarou M, Jin SM, Kane LA, Youle RJ (2012) Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev Cell 22:320–333. https://doi.org/10.1016/j.devcel.2011.12.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Okatsu K, Uno M, Koyano F et al (2013) A dimeric PINK1-containing complex on depolarized mitochondria stimulates Parkin recruitment. J Biol Chem 288:36372–36384. https://doi.org/10.1074/jbc.M113.509653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Aerts L, Craessaerts K, De Strooper B, Morais VA (2015) PINK1 kinase catalytic activity is regulated by phosphorylation on serines 228 and 402. J Biol Chem 290:2798–2811. https://doi.org/10.1074/jbc.M114.620906

    Article  CAS  PubMed  Google Scholar 

  100. Okatsu K, Oka T, Iguchi M et al (2012) PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun 3:1016. https://doi.org/10.1038/ncomms2016

    Article  CAS  PubMed  Google Scholar 

  101. Chaugule VK, Burchell L, Barber KR et al (2011) Autoregulation of Parkin activity through its ubiquitin-like domain. EMBO J 30:2853–2867. https://doi.org/10.1038/emboj.2011.204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Iguchi M, Kujuro Y, Okatsu K et al (2013) Parkin-catalyzed ubiquitin-ester transfer is triggered by PINK1-dependent phosphorylation. J Biol Chem 288:22019–22032. https://doi.org/10.1074/jbc.M113.467530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Kondapalli C, Kazlauskaite A, Zhang N et al (2012) PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol 2:120080. https://doi.org/10.1098/rsob.120080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Shiba-Fukushima K, Imai Y, Yoshida S et al (2012) PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep 2:1002. https://doi.org/10.1038/srep01002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kane LA, Lazarou M, Fogel AI et al (2014) PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol 205:143–153. https://doi.org/10.1083/jcb.201402104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Kazlauskaite A, Kondapalli C, Gourlay R et al (2014) Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J 460:127–139. https://doi.org/10.1042/BJ20140334

    Article  CAS  PubMed  Google Scholar 

  107. Koyano F, Okatsu K, Kosako H et al (2014) Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510:162–166. https://doi.org/10.1038/nature13392

    Article  CAS  PubMed  Google Scholar 

  108. Sarraf SA, Raman M, Guarani-Pereira V et al (2013) Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496:372–376. https://doi.org/10.1038/nature12043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Youle RJ, van der Bliek AM (2012) Mitochondrial fission, fusion, and stress. Science 337:1062–1065. https://doi.org/10.1126/science.1219855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Ordureau A, Sarraf SA, Duda DM et al (2014) Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol Cell 56:360–375. https://doi.org/10.1016/j.molcel.2014.09.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Zheng X, Hunter T (2013) Parkin mitochondrial translocation is achieved through a novel catalytic activity coupled mechanism. Cell Res 23:886–897. https://doi.org/10.1038/cr.2013.66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Heo J-M, Ordureau A, Paulo JA et al (2015) The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol Cell 60:7–20. https://doi.org/10.1016/j.molcel.2015.08.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Lazarou M, Sliter DA, Kane LA et al (2015) The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature 524:309–314. https://doi.org/10.1038/nature14893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Yamano K, Matsuda N, Tanaka K (2016) The ubiquitin signal and autophagy: an orchestrated dance leading to mitochondrial degradation. EMBO Rep 17:300–316. https://doi.org/10.15252/embr.201541486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Zhang J, Ney PA (2009) Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ 16:939–946. https://doi.org/10.1038/cdd.2009.16

    Article  CAS  PubMed  Google Scholar 

  116. Bellot G, Garcia-Medina R, Gounon P et al (2009) Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 29:2570–2581. https://doi.org/10.1128/MCB.00166-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Hanna RA, Quinsay MN, Orogo AM et al (2012) Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem 287:19094–19104. https://doi.org/10.1074/jbc.M111.322933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Novak I, Kirkin V, McEwan DG et al (2010) Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11:45–51. https://doi.org/10.1038/embor.2009.256

    Article  CAS  PubMed  Google Scholar 

  119. Rikka S, Quinsay MN, Thomas RL et al (2011) Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover. Cell Death Differ 18:721–731. https://doi.org/10.1038/cdd.2010.146

    Article  CAS  PubMed  Google Scholar 

  120. Schwarten M, Mohrlüder J, Ma P et al (2009) Nix directly binds to GABARAP: a possible crosstalk between apoptosis and autophagy. Autophagy 5:690–698. https://doi.org/10.4161/auto.5.5.8494

    Article  CAS  PubMed  Google Scholar 

  121. Zhu Y, Massen S, Terenzio M et al (2013) Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J Biol Chem 288:1099–1113. https://doi.org/10.1074/jbc.M112.399345

    Article  CAS  PubMed  Google Scholar 

  122. Rogov VV, Stolz A, Ravichandran AC et al (2017) Structural and functional analysis of the GABARAP interaction motif (GIM). EMBO Rep 18:1382–1396. https://doi.org/10.15252/embr.201643587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Zhang T, Xue L, Li L et al (2016) BNIP3 protein suppresses PINK1 kinase proteolytic cleavage to promote mitophagy. J Biol Chem 291:21616–21629. https://doi.org/10.1074/jbc.M116.733410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Koentjoro B, Park J-S, Sue CM (2017) Nix restores mitophagy and mitochondrial function to protect against PINK1/Parkin-related Parkinson’s disease. Sci Rep 7:44373. https://doi.org/10.1038/srep44373

    Article  PubMed  PubMed Central  Google Scholar 

  125. Chen G, Han Z, Feng D et al (2014) A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol Cell 54:362–377. https://doi.org/10.1016/j.molcel.2014.02.034

    Article  CAS  PubMed  Google Scholar 

  126. Liu L, Feng D, Chen G et al (2012) Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol 14:177–185. https://doi.org/10.1038/ncb2422

    Article  CAS  PubMed  Google Scholar 

  127. Wu W, Tian W, Hu Z et al (2014) ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep 15:566–575. https://doi.org/10.1002/embr.201438501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Chen Z, Liu L, Cheng Q et al (2017) Mitochondrial E3 ligase MARCH5 regulates FUNDC1 to fine-tune hypoxic mitophagy. EMBO Rep 18:495–509. https://doi.org/10.15252/embr.201643309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Wu W, Lin C, Wu K et al (2016) FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions. EMBO J 35:1368–1384. https://doi.org/10.15252/embj.201593102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Edlich F, Lücke C (2011) From cell death to viral replication: the diverse functions of the membrane-associated FKBP38. Curr Opin Pharmacol 11:348–353. https://doi.org/10.1016/j.coph.2011.03.011

    Article  CAS  PubMed  Google Scholar 

  131. Bhujabal Z, Birgisdottir ÅB, Sjøttem E et al (2017) FKBP8 recruits LC3A to mediate Parkin-independent mitophagy. EMBO Rep 18:947–961. https://doi.org/10.15252/embr.201643147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Saita S, Shirane M, Nakayama KI (2013) Selective escape of proteins from the mitochondria during mitophagy. Nat Commun 4:1410. https://doi.org/10.1038/ncomms2400

    Article  CAS  PubMed  Google Scholar 

  133. Yoo S-M, Yamashita S, Kim H et al (2020) FKBP8 LIRL-dependent mitochondrial fragmentation facilitates mitophagy under stress conditions. FASEB J 34:2944–2957. https://doi.org/10.1096/fj.201901735R

    Article  CAS  PubMed  Google Scholar 

  134. Strappazzon F, Nazio F, Corrado M et al (2015) AMBRA1 is able to induce mitophagy via LC3 binding, regardless of PARKIN and p62/SQSTM1. Cell Death Differ 22:419–432. https://doi.org/10.1038/cdd.2014.139

    Article  CAS  PubMed  Google Scholar 

  135. Van Humbeeck C, Cornelissen T, Hofkens H et al (2011) Parkin interacts with Ambra1 to induce mitophagy. J Neurosci 31:10249–10261. https://doi.org/10.1523/JNEUROSCI.1917-11.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Wei Y, Chiang W-C, Sumpter R et al (2017) Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor. Cell 168:224-238.e10. https://doi.org/10.1016/j.cell.2016.11.042

    Article  CAS  PubMed  Google Scholar 

  137. Yan C, Gong L, Chen L et al (2020) PHB2 (prohibitin 2) promotes PINK1-PRKN/Parkin-dependent mitophagy by the PARL-PGAM5-PINK1 axis. Autophagy 16:419–434. https://doi.org/10.1080/15548627.2019.1628520

    Article  CAS  PubMed  Google Scholar 

  138. Chu CT, Ji J, Dagda RK et al (2013) Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat Cell Biol 15:1197–1205. https://doi.org/10.1038/ncb2837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Kagan VE, Jiang J, Huang Z et al (2016) NDPK-D (NM23-H4)-mediated externalization of cardiolipin enables elimination of depolarized mitochondria by mitophagy. Cell Death Differ 23:1140–1151. https://doi.org/10.1038/cdd.2015.160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Sentelle RD, Senkal CE, Jiang W et al (2012) Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy. Nat Chem Biol 8:831–838. https://doi.org/10.1038/nchembio.1059

    Article  PubMed  PubMed Central  Google Scholar 

  141. Carling D, Mayer FV, Sanders MJ, Gamblin SJ (2011) AMP-activated protein kinase: nature’s energy sensor. Nat Chem Biol 7:512–518. https://doi.org/10.1038/nchembio.610

    Article  CAS  PubMed  Google Scholar 

  142. Hardie DG (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25:1895–1908. https://doi.org/10.1101/gad.17420111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Cantó C, Jiang LQ, Deshmukh AS et al (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11:213–219. https://doi.org/10.1016/j.cmet.2010.02.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Jäger S, Handschin C, St-Pierre J, Spiegelman BM (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 104:12017–12022. https://doi.org/10.1073/pnas.0705070104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Mihaylova MM, Shaw RJ (2011) The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13:1016–1023. https://doi.org/10.1038/ncb2329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Marin TL, Gongol B, Zhang F et al (2017) AMPK promotes mitochondrial biogenesis and function by phosphorylating the epigenetic factors DNMT1, RBBP7, and HAT1. Sci Signal. https://doi.org/10.1126/scisignal.aaf7478

    Article  PubMed  PubMed Central  Google Scholar 

  147. Ducommun S, Deak M, Sumpton D et al (2015) Motif affinity and mass spectrometry proteomic approach for the discovery of cellular AMPK targets: identification of mitochondrial fission factor as a new AMPK substrate. Cell Signal 27:978–988. https://doi.org/10.1016/j.cellsig.2015.02.008

    Article  CAS  PubMed  Google Scholar 

  148. Toyama EQ, Herzig S, Courchet J et al (2016) Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress. Science 351:275–281. https://doi.org/10.1126/science.aab4138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Gwinn DM, Shackelford DB, Egan DF et al (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214–226. https://doi.org/10.1016/j.molcel.2008.03.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Inoki K, Zhu T, Guan K-L (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–590. https://doi.org/10.1016/s0092-8674(03)00929-2

    Article  CAS  PubMed  Google Scholar 

  151. Greer EL, Oskoui PR, Banko MR et al (2007) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282:30107–30119. https://doi.org/10.1074/jbc.M705325200

    Article  CAS  PubMed  Google Scholar 

  152. Mammucari C, Milan G, Romanello V et al (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–471. https://doi.org/10.1016/j.cmet.2007.11.001

    Article  CAS  PubMed  Google Scholar 

  153. Zhao J, Brault JJ, Schild A et al (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–483. https://doi.org/10.1016/j.cmet.2007.11.004

    Article  CAS  PubMed  Google Scholar 

  154. Tian W, Li W, Chen Y et al (2015) Phosphorylation of ULK1 by AMPK regulates translocation of ULK1 to mitochondria and mitophagy. FEBS Lett 589:1847–1854. https://doi.org/10.1016/j.febslet.2015.05.020

    Article  CAS  PubMed  Google Scholar 

  155. Wang B, Nie J, Wu L et al (2018) AMPKα2 protects against the development of heart failure by enhancing mitophagy via PINK1 phosphorylation. Circ Res 122:712–729. https://doi.org/10.1161/CIRCRESAHA.117.312317

    Article  CAS  PubMed  Google Scholar 

  156. Seabright AP, Fine NHF, Barlow JP et al (2020) AMPK activation induces mitophagy and promotes mitochondrial fission while activating TBK1 in a PINK1-Parkin independent manner. FASEB J 34:6284–6301. https://doi.org/10.1096/fj.201903051R

    Article  CAS  PubMed  Google Scholar 

  157. Richter B, Sliter DA, Herhaus L et al (2016) Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc Natl Acad Sci USA 113:4039–4044. https://doi.org/10.1073/pnas.1523926113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Vargas-Ortiz K, Pérez-Vázquez V, Macías-Cervantes MH (2019) Exercise and sirtuins: a way to mitochondrial health in skeletal muscle. Int J Mol Sci. https://doi.org/10.3390/ijms20112717

    Article  PubMed  PubMed Central  Google Scholar 

  159. Gerhart-Hines Z, Rodgers JT, Bare O et al (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 26:1913–1923. https://doi.org/10.1038/sj.emboj.7601633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Gerhart-Hines Z, Dominy JE, Blättler SM et al (2011) The cAMP/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+). Mol Cell 44:851–863. https://doi.org/10.1016/j.molcel.2011.12.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Jing E, Emanuelli B, Hirschey MD et al (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci USA 108:14608–14613. https://doi.org/10.1073/pnas.1111308108

    Article  PubMed  PubMed Central  Google Scholar 

  162. Amat R, Planavila A, Chen SL et al (2009) SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-gamma Co-activator-1alpha (PGC-1alpha) gene in skeletal muscle through the PGC-1alpha autoregulatory loop and interaction with MyoD. J Biol Chem 284:21872–21880. https://doi.org/10.1074/jbc.M109.022749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Kong X, Wang R, Xue Y et al (2010) Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS ONE 5:e11707. https://doi.org/10.1371/journal.pone.0011707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Pfluger PT, Herranz D, Velasco-Miguel S et al (2008) Sirt1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci USA 105:9793–9798. https://doi.org/10.1073/pnas.0802917105

    Article  PubMed  PubMed Central  Google Scholar 

  165. Ding M, Feng N, Tang D et al (2018) Melatonin prevents Drp1-mediated mitochondrial fission in diabetic hearts through SIRT1-PGC1α pathway. J Pineal Res 65:e12491. https://doi.org/10.1111/jpi.12491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Li M-Y, Ding J-Q, Tang Q et al (2019) SIRT1 activation by SRT1720 attenuates bone cancer pain via preventing Drp1-mediated mitochondrial fission. Biochim Biophys Acta Mol Basis Dis 1865:587–598. https://doi.org/10.1016/j.bbadis.2018.12.017

    Article  CAS  PubMed  Google Scholar 

  167. Qin R, Zhang L, Lin D et al (2019) Sirt1 inhibits HG-induced endothelial injury: role of Mff-based mitochondrial fission and F-actin homeostasis-mediated cellular migration. Int J Mol Med 44:89–102. https://doi.org/10.3892/ijmm.2019.4185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Lovy A, Ahumada-Castro U, Bustos G et al (2020) Concerted action of AMPK and sirtuin-1 induces mitochondrial fragmentation upon inhibition of Ca2+ transfer to mitochondria. Front Cell Dev Biol. https://doi.org/10.3389/fcell.2020.00378

    Article  PubMed  PubMed Central  Google Scholar 

  169. Liu J, Yan W, Zhao X et al (2019) Sirt3 attenuates post-infarction cardiac injury via inhibiting mitochondrial fission and normalization of AMPK-Drp1 pathways. Cell Signal 53:1–13. https://doi.org/10.1016/j.cellsig.2018.09.009

    Article  CAS  PubMed  Google Scholar 

  170. Zhou D, Jiang Y (2019) Sirtuin 3 attenuates neuroinflammation-induced apoptosis in BV-2 microglia. Aging (Albany NY) 11:9075–9089. https://doi.org/10.18632/aging.102375

    Article  CAS  Google Scholar 

  171. Zhou J, Shi M, Li M et al (2019) Sirtuin 3 inhibition induces mitochondrial stress in tongue cancer by targeting mitochondrial fission and the JNK-Fis1 biological axis. Cell Stress Chaperones 24:369–383. https://doi.org/10.1007/s12192-019-00970-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Wang Q, Xu J, Li X et al (2019) Sirt3 modulate renal ischemia-reperfusion injury through enhancing mitochondrial fusion and activating the ERK-OPA1 signaling pathway. J Cell Physiol 234:23495–23506. https://doi.org/10.1002/jcp.28918

    Article  CAS  PubMed  Google Scholar 

  173. Tseng AHH, Shieh S-S, Wang DL (2013) SIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage. Free Radic Biol Med 63:222–234. https://doi.org/10.1016/j.freeradbiomed.2013.05.002

    Article  CAS  PubMed  Google Scholar 

  174. Tyagi A, Nguyen CU, Chong T et al (2018) SIRT3 deficiency-induced mitochondrial dysfunction and inflammasome formation in the brain. Sci Rep 8:17547. https://doi.org/10.1038/s41598-018-35890-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Guedouari H, Daigle T, Scorrano L, Hebert-Chatelain E (2017) Sirtuin 5 protects mitochondria from fragmentation and degradation during starvation. Biochim Biophys Acta Mol Cell Res 1864:169–176. https://doi.org/10.1016/j.bbamcr.2016.10.015

    Article  CAS  PubMed  Google Scholar 

  176. Jang S, Kang HT, Hwang ES (2012) Nicotinamide-induced mitophagy: event mediated by high NAD+/NADH ratio and SIRT1 protein activation. J Biol Chem 287:19304–19314. https://doi.org/10.1074/jbc.M112.363747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Kobayashi Y, Furukawa-Hibi Y, Chen C et al (2005) SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress. Int J Mol Med 16:237–243

    CAS  PubMed  Google Scholar 

  178. Li R, Xin T, Li D et al (2018) Therapeutic effect of Sirtuin 3 on ameliorating nonalcoholic fatty liver disease: the role of the ERK-CREB pathway and Bnip3-mediated mitophagy. Redox Biol 18:229–243. https://doi.org/10.1016/j.redox.2018.07.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Yu W, Gao B, Li N et al (2017) Sirt3 deficiency exacerbates diabetic cardiac dysfunction: role of Foxo3A-Parkin-mediated mitophagy. Biochim Biophys Acta Mol Basis Dis 1863:1973–1983. https://doi.org/10.1016/j.bbadis.2016.10.021

    Article  CAS  PubMed  Google Scholar 

  180. Das S, Mitrovsky G, Vasanthi HR, Das DK (2014) Antiaging properties of a grape-derived antioxidant are regulated by mitochondrial balance of fusion and fission leading to mitophagy triggered by a signaling network of Sirt1-Sirt3-Foxo3-PINK1-PARKIN. Oxid Med Cell Longev. https://doi.org/10.1155/2014/345105

    Article  PubMed  PubMed Central  Google Scholar 

  181. Kang HT, Hwang ES (2009) Nicotinamide enhances mitochondria quality through autophagy activation in human cells. Aging Cell 8:426–438. https://doi.org/10.1111/j.1474-9726.2009.00487.x

    Article  CAS  PubMed  Google Scholar 

  182. Di Sante G, Pestell TG, Casimiro MC et al (2015) Loss of Sirt1 promotes prostatic intraepithelial neoplasia, reduces mitophagy, and delays PARK2 translocation to mitochondria. Am J Pathol 185:266–279. https://doi.org/10.1016/j.ajpath.2014.09.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Akimoto T, Pohnert SC, Li P et al (2005) Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280:19587–19593. https://doi.org/10.1074/jbc.M408862200

    Article  CAS  PubMed  Google Scholar 

  184. Wright DC, Geiger PC, Han D-H et al (2007) Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 282:18793–18799. https://doi.org/10.1074/jbc.M611252200

    Article  CAS  PubMed  Google Scholar 

  185. Zhang Y, Uguccioni G, Ljubicic V et al (2014) Multiple signaling pathways regulate contractile activity-mediated PGC-1α gene expression and activity in skeletal muscle cells. Physiol Rep. https://doi.org/10.14814/phy2.12008

    Article  PubMed  PubMed Central  Google Scholar 

  186. McGee SL, Hargreaves M (2004) Exercise and myocyte enhancer factor 2 regulation in human skeletal muscle. Diabetes 53:1208–1214. https://doi.org/10.2337/diabetes.53.5.1208

    Article  CAS  PubMed  Google Scholar 

  187. Zhao M, New L, Kravchenko VV et al (1999) Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol 19:21–30. https://doi.org/10.1128/mcb.19.1.21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Kashatus JA, Nascimento A, Myers LJ et al (2015) Erk2 phosphorylation of Drp1 promotes mitochondrial fission and MAPK-driven tumor growth. Mol Cell 57:537–551. https://doi.org/10.1016/j.molcel.2015.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Yu T, Jhun BS, Yoon Y (2011) High-glucose stimulation increases reactive oxygen species production through the calcium and mitogen-activated protein kinase-mediated activation of mitochondrial fission. Antioxid Redox Signal 14:425–437. https://doi.org/10.1089/ars.2010.3284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Pyakurel A, Savoia C, Hess D, Scorrano L (2015) Extracellular regulated kinase phosphorylates mitofusin 1 to control mitochondrial morphology and apoptosis. Mol Cell 58:244–254. https://doi.org/10.1016/j.molcel.2015.02.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Dagda RK, Zhu J, Kulich SM, Chu CT (2008) Mitochondrially localized ERK2 regulates mitophagy and autophagic cell stress: implications for Parkinson’s disease. Autophagy 4:770–782. https://doi.org/10.4161/auto.6458

    Article  CAS  PubMed  Google Scholar 

  192. Hirota Y, Yamashita S, Kurihara Y et al (2015) Mitophagy is primarily due to alternative autophagy and requires the MAPK1 and MAPK14 signaling pathways. Autophagy 11:332–343. https://doi.org/10.1080/15548627.2015.1023047

    Article  PubMed  PubMed Central  Google Scholar 

  193. Park JH, Ko J, Park YS et al (2017) Clearance of damaged mitochondria through PINK1 stabilization by JNK and ERK MAPK signaling in chlorpyrifos-treated neuroblastoma cells. Mol Neurobiol 54:1844–1857. https://doi.org/10.1007/s12035-016-9753-1

    Article  CAS  PubMed  Google Scholar 

  194. Yu W, Xu M, Zhang T et al (2019) Mst1 promotes cardiac ischemia-reperfusion injury by inhibiting the ERK-CREB pathway and repressing FUNDC1-mediated mitophagy. J Physiol Sci 69:113–127. https://doi.org/10.1007/s12576-018-0627-3

    Article  CAS  PubMed  Google Scholar 

  195. Handschin C, Rhee J, Lin J et al (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc Natl Acad Sci USA 100:7111–7116. https://doi.org/10.1073/pnas.1232352100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Ryder JW, Bassel-Duby R, Olson EN, Zierath JR (2003) Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J Biol Chem 278:44298–44304. https://doi.org/10.1074/jbc.M304510200

    Article  CAS  PubMed  Google Scholar 

  197. Wu H, Kanatous SB, Thurmond FA et al (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296:349–352. https://doi.org/10.1126/science.1071163

    Article  CAS  PubMed  Google Scholar 

  198. Akimoto T, Ribar TJ, Williams RS, Yan Z (2004) Skeletal muscle adaptation in response to voluntary running in Ca2+/calmodulin-dependent protein kinase IV-deficient mice. Am J Physiol Cell Physiol 287:C1311-1319. https://doi.org/10.1152/ajpcell.00248.2004

    Article  CAS  PubMed  Google Scholar 

  199. Cereghetti GM, Stangherlin A, Martins de Brito O et al (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci USA 105:15803–15808. https://doi.org/10.1073/pnas.0808249105

    Article  PubMed  PubMed Central  Google Scholar 

  200. Cribbs JT, Strack S (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8:939–944. https://doi.org/10.1038/sj.embor.7401062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Yu R, Jin S-B, Lendahl U et al (2019) Human Fis1 regulates mitochondrial dynamics through inhibition of the fusion machinery. EMBO J. https://doi.org/10.15252/embj.201899748

    Article  PubMed  PubMed Central  Google Scholar 

  202. Bo T, Yamamori T, Suzuki M et al (2018) Calmodulin-dependent protein kinase II (CaMKII) mediates radiation-induced mitochondrial fission by regulating the phosphorylation of dynamin-related protein 1 (Drp1) at serine 616. Biochem Biophys Res Commun 495:1601–1607. https://doi.org/10.1016/j.bbrc.2017.12.012

    Article  CAS  PubMed  Google Scholar 

  203. Xu S, Wang P, Zhang H et al (2016) CaMKII induces permeability transition through Drp1 phosphorylation during chronic β-AR stimulation. Nat Commun. https://doi.org/10.1038/ncomms13189

    Article  PubMed  PubMed Central  Google Scholar 

  204. Gómez-Sánchez R, Gegg ME, Bravo-San Pedro JM et al (2014) Mitochondrial impairment increases FL-PINK1 levels by calcium-dependent gene expression. Neurobiol Dis 62:426–440. https://doi.org/10.1016/j.nbd.2013.10.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Safiulina D, Kuum M, Choubey V et al (2019) Miro proteins prime mitochondria for Parkin translocation and mitophagy. EMBO J. https://doi.org/10.15252/embj.201899384

    Article  PubMed  Google Scholar 

  206. Zhang X, Yuan D, Sun Q et al (2017) Calcium/calmodulin-dependent protein kinase regulates the PINK1/Parkin and DJ-1 pathways of mitophagy during sepsis. FASEB J 31:4382–4395. https://doi.org/10.1096/fj.201601096RRR

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Boss O, Bachman E, Vidal-Puig A et al (1999) Role of the beta(3)-adrenergic receptor and/or a putative beta(4)-adrenergic receptor on the expression of uncoupling proteins and peroxisome proliferator-activated receptor-gamma coactivator-1. Biochem Biophys Res Commun 261:870–876. https://doi.org/10.1006/bbrc.1999.1145

    Article  CAS  PubMed  Google Scholar 

  208. Gómez-Ambrosi J, Frühbeck G, Martínez JA (2001) Rapid in vivo PGC-1 mRNA upregulation in brown adipose tissue of Wistar rats by a beta(3)-adrenergic agonist and lack of effect of leptin. Mol Cell Endocrinol 176:85–90. https://doi.org/10.1016/s0303-7207(01)00451-8

    Article  PubMed  Google Scholar 

  209. Jerums G, Hardy KJ, Eisman JA (1977) The cyclic AMP response to glucagon. Comparison of tissue and plasma cyclic AMP levels in the rabbit. Diabetes 26:81–88. https://doi.org/10.2337/diab.26.2.81

    Article  CAS  PubMed  Google Scholar 

  210. Miura S, Kai Y, Kamei Y, Ezaki O (2008) Isoform-specific increases in murine skeletal muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) mRNA in response to beta2-adrenergic receptor activation and exercise. Endocrinology 149:4527–4533. https://doi.org/10.1210/en.2008-0466

    Article  CAS  PubMed  Google Scholar 

  211. Pfeifle B, Pfeifle R, Faulhaber JD, Ditschuneit H (1980) Thyroid hormone stimulation of lipolysis and cyclic adenosine 3′,5′-monophosphate accumulation in human adipose tissue. Horm Metab Res 12:711–713. https://doi.org/10.1055/s-2007-999242

    Article  CAS  PubMed  Google Scholar 

  212. Puigserver P, Wu Z, Park CW et al (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829–839. https://doi.org/10.1016/s0092-8674(00)81410-5

    Article  CAS  PubMed  Google Scholar 

  213. Chang C-R, Blackstone C (2007) Drp1 phosphorylation and mitochondrial regulation. EMBO Rep 8:1088–1089. https://doi.org/10.1038/sj.embor.7401118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Merrill RA, Dagda RK, Dickey AS et al (2011) Mechanism of neuroprotective mitochondrial remodeling by PKA/AKAP1. PLoS Biol 9:e1000612. https://doi.org/10.1371/journal.pbio.1000612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Pryde KR, Smith HL, Chau K-Y, Schapira AHV (2016) PINK1 disables the anti-fission machinery to segregate damaged mitochondria for mitophagy. J Cell Biol 213:163–171. https://doi.org/10.1083/jcb.201509003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. da Rosa SC, Martens MD, Field JT et al (2019) Nix induced mitochondrial fission, mitophagy, and myocyte insulin resistance are abrogated by PKA phosphorylation. bioRxiv. https://doi.org/10.1101/825828

    Article  Google Scholar 

  217. Dumont NA, Bentzinger CF, Sincennes M-C, Rudnicki MA (2015) Satellite cells and skeletal muscle regeneration. Compr Physiol 5:1027–1059. https://doi.org/10.1002/cphy.c140068

    Article  PubMed  Google Scholar 

  218. Grounds MD (1991) Towards understanding skeletal muscle regeneration. Pathol Res Pract 187:1–22. https://doi.org/10.1016/S0344-0338(11)81039-3

    Article  CAS  PubMed  Google Scholar 

  219. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551

    Article  CAS  PubMed  Google Scholar 

  220. Tidball JG (2011) Mechanisms of muscle injury, repair, and regeneration. Compr Physiol 1:2029–2062. https://doi.org/10.1002/cphy.c100092

    Article  PubMed  Google Scholar 

  221. Rahman FA, Krause MP (2020) PAI-1, the plasminogen system, and skeletal muscle. Int J Mol Sci 21:7066. https://doi.org/10.3390/ijms21197066

    Article  CAS  PubMed Central  Google Scholar 

  222. Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:R345–R353. https://doi.org/10.1152/ajpregu.00454.2004

    Article  CAS  PubMed  Google Scholar 

  223. Rahman FA, Angus SA, Stokes K et al (2020) Impaired ECM remodeling and macrophage activity define necrosis and regeneration following damage in aged skeletal muscle. Int J Mol Sci. https://doi.org/10.3390/ijms21134575

    Article  PubMed  PubMed Central  Google Scholar 

  224. Hardy D, Besnard A, Latil M et al (2016) Comparative study of injury models for studying muscle regeneration in mice. PLoS ONE 11:e0147198. https://doi.org/10.1371/journal.pone.0147198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  225. Le Moal E, Pialoux V, Juban G et al (2016) Redox control of skeletal muscle regeneration. Antioxid Redox Signal 27:276–310. https://doi.org/10.1089/ars.2016.6782

    Article  CAS  Google Scholar 

  226. Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139:2845–2856. https://doi.org/10.1242/dev.069088

    Article  CAS  PubMed  Google Scholar 

  227. Bloemberg D, Quadrilatero J (2016) Effect of mitochondrial fission inhibition on C2C12 differentiation. Data Brief 7:634–640. https://doi.org/10.1016/j.dib.2016.02.070

    Article  PubMed  PubMed Central  Google Scholar 

  228. Kim B, Kim J-S, Yoon Y et al (2013) Inhibition of Drp1-dependent mitochondrial division impairs myogenic differentiation. Am J Physiol Regul Integr Comp Physiol 305:R927-938. https://doi.org/10.1152/ajpregu.00502.2012

    Article  CAS  PubMed  Google Scholar 

  229. Kraft CS, LeMoine CMR, Lyons CN et al (2006) Control of mitochondrial biogenesis during myogenesis. Am J Physiol Cell Physiol 290:C1119-1127. https://doi.org/10.1152/ajpcell.00463.2005

    Article  CAS  PubMed  Google Scholar 

  230. Moyes CD, Mathieu-Costello OA, Tsuchiya N et al (1997) Mitochondrial biogenesis during cellular differentiation. Am J Physiol 272:C1345-1351. https://doi.org/10.1152/ajpcell.1997.272.4.C1345

    Article  CAS  PubMed  Google Scholar 

  231. Redpath CJ, Khalil MB, Drozdzal G et al (2013) Mitochondrial hyperfusion during oxidative stress is coupled to a dysregulation in calcium handling within a C2C12 cell model. PLoS ONE 8:e69165. https://doi.org/10.1371/journal.pone.0069165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Sin J, Andres AM, Taylor DJR et al (2016) Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts. Autophagy 12:369–380. https://doi.org/10.1080/15548627.2015.1115172

    Article  CAS  PubMed  Google Scholar 

  233. LaBarge S, McDonald M, Smith-Powell L et al (2014) Estrogen-related receptor-α (ERRα) deficiency in skeletal muscle impairs regeneration in response to injury. FASEB J 28:1082–1097. https://doi.org/10.1096/fj.13-229211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Nichenko AS, Southern WM, Atuan M et al (2016) Mitochondrial maintenance via autophagy contributes to functional skeletal muscle regeneration and remodeling. Am J Physiol Cell Physiol 311:C190-200. https://doi.org/10.1152/ajpcell.00066.2016

    Article  PubMed  Google Scholar 

  235. Ainbinder A, Boncompagni S, Protasi F, Dirksen RT (2015) Role of mitofusin-2 in mitochondrial localization and calcium uptake in skeletal muscle. Cell Calcium 57:14–24. https://doi.org/10.1016/j.ceca.2014.11.002

    Article  CAS  PubMed  Google Scholar 

  236. Koves TR, Noland RC, Bates AL et al (2005) Subsarcolemmal and intermyofibrillar mitochondria play distinct roles in regulating skeletal muscle fatty acid metabolism. Am J Physiol Cell Physiol 288:C1074-1082. https://doi.org/10.1152/ajpcell.00391.2004

    Article  CAS  PubMed  Google Scholar 

  237. Cogswell AM, Stevens RJ, Hood DA (1993) Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol 264:C383-389. https://doi.org/10.1152/ajpcell.1993.264.2.C383

    Article  CAS  PubMed  Google Scholar 

  238. Kirkwood SP, Munn EA, Brooks GA (1986) Mitochondrial reticulum in limb skeletal muscle. Am J Physiol Cell Physiol 251:C395–C402. https://doi.org/10.1152/ajpcell.1986.251.3.C395

    Article  CAS  Google Scholar 

  239. Picard M, White K (1985) Turnbull DM (2013) Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study. J Appl Physiol 114:161–171. https://doi.org/10.1152/japplphysiol.01096.2012

    Article  Google Scholar 

  240. Glancy B, Hartnell LM, Malide D et al (2015) Mitochondrial reticulum for cellular energy distribution in muscle. Nature 523:617–620. https://doi.org/10.1038/nature14614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Bleck CKE, Kim Y, Willingham TB, Glancy B (2018) Subcellular connectomic analyses of energy networks in striated muscle. Nat Commun 9:5111. https://doi.org/10.1038/s41467-018-07676-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Eisner V, Lenaers G, Hajnóczky G (2014) Mitochondrial fusion is frequent in skeletal muscle and supports excitation–contraction coupling. J Cell Biol 205:179–195. https://doi.org/10.1083/jcb.201312066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Schiaffino S (2017) Losing pieces without disintegrating: contractile protein loss during muscle atrophy. Proc Natl Acad Sci USA 114:1753–1755. https://doi.org/10.1073/pnas.1700190114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Vertel BM, Fischman DA (1977) Mitochondrial development during myogenesis. Dev Biol 58:356–371. https://doi.org/10.1016/0012-1606(77)90097-5

    Article  CAS  PubMed  Google Scholar 

  245. Barbieri E, Battistelli M, Casadei L et al (2011) Morphofunctional and biochemical approaches for studying mitochondrial changes during myoblasts differentiation. J Aging Res. https://doi.org/10.4061/2011/845379

    Article  PubMed  PubMed Central  Google Scholar 

  246. Robinson MM, Sather BK, Burney ER et al (2019) Robust intrinsic differences in mitochondrial respiration and H2O2 emission between L6 and C2C12 cells. Am J Physiol Cell Physiol 317:C339–C347. https://doi.org/10.1152/ajpcell.00343.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Touvier T, De Palma C, Rigamonti E et al (2015) Muscle-specific Drp1 overexpression impairs skeletal muscle growth via translational attenuation. Cell Death Dis 6:e1663. https://doi.org/10.1038/cddis.2014.595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Favaro G, Romanello V, Varanita T et al (2019) DRP1-mediated mitochondrial shape controls calcium homeostasis and muscle mass. Nat Commun 10:2576. https://doi.org/10.1038/s41467-019-10226-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  249. Romanello V, Sandri M (2010) Mitochondrial biogenesis and fragmentation as regulators of muscle protein degradation. Curr Hypertens Rep 12:433–439. https://doi.org/10.1007/s11906-010-0157-8

    Article  CAS  PubMed  Google Scholar 

  250. Romanello V, Guadagnin E, Gomes L et al (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29:1774–1785. https://doi.org/10.1038/emboj.2010.60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Romanello V, Sandri M (2020) The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass. Cell Mol Life Sci. https://doi.org/10.1007/s00018-020-03662-0

    Article  PubMed  PubMed Central  Google Scholar 

  252. Baldelli S, Aquilano K, Ciriolo MR (2014) PGC-1α buffers ROS-mediated removal of mitochondria during myogenesis. Cell Death Dis 5:e1515. https://doi.org/10.1038/cddis.2014.458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Remels AHV, Langen RCJ, Schrauwen P et al (2010) Regulation of mitochondrial biogenesis during myogenesis. Mol Cell Endocrinol 315:113–120. https://doi.org/10.1016/j.mce.2009.09.029

    Article  CAS  PubMed  Google Scholar 

  254. Shintaku J, Peterson JM, Talbert EE et al (2016) MyoD regulates skeletal muscle oxidative metabolism cooperatively with alternative NF-κB. Cell Rep 17:514–526. https://doi.org/10.1016/j.celrep.2016.09.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  255. Tezze C, Romanello V, Desbats MA et al (2017) Age-associated loss of OPA1 in muscle impacts muscle mass, metabolic homeostasis, systemic inflammation, and epithelial senescence. Cell Metab 25:1374-1389.e6. https://doi.org/10.1016/j.cmet.2017.04.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Rodríguez-Nuevo A, Díaz-Ramos A, Noguera E et al (2018) Mitochondrial DNA and TLR9 drive muscle inflammation upon Opa1 deficiency. EMBO J. https://doi.org/10.15252/embj.201796553

    Article  PubMed  PubMed Central  Google Scholar 

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J.Q. is supported by a Natural Sciences and Engineering Research Council (NSERC) of Canada grant. F.A.R. is a recipient of an Ontario Graduate Scholarship (OGS).

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    Fasih Ahmad Rahman & Joe Quadrilatero

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Rahman, F.A., Quadrilatero, J. Mitochondrial network remodeling: an important feature of myogenesis and skeletal muscle regeneration. Cell. Mol. Life Sci. 78, 4653–4675 (2021). https://doi.org/10.1007/s00018-021-03807-9

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