5,074
Views
5
CrossRef citations to date
0
Altmetric
Research Paper

CREG1 improves the capacity of the skeletal muscle response to exercise endurance via modulation of mitophagy

, , , , , , , & show all
Pages 4102-4118 | Received 07 May 2020, Accepted 12 Mar 2021, Published online: 18 Apr 2021

References

  • Kim TN, Choi KM. Sarcopenia: definition, epidemiology, and pathophysiology. J Bone Metab. 2013 May;20(1):1–10. PMID: 24524049, PMCID: PMC3780834.
  • Balan E, Schwalm C, Naslain D, et al. Regular endurance exercise promotes fission, mitophagy, and oxidative phosphorylation in human skeletal muscle independently of age. Front Physiol. 2019 Aug 22;10:1088. PMID: 31507451, PMCID: PMC6713923;10:1088.
  • Baracos VE, Martin L, Korc M, et al. Cancer-associated cachexia. Nat Rev Dis Primers. 2018 Jan 18;4:17105. PMID: 29345251.
  • Toth MJ, Callahana DM, Miller MS et al., Skeletal muscle fiber size and fiber type distribution in human cancer: effects of weight loss and relationship to physical function. Clin Nutr. 2016 Dec;35(6):1359–1365. PMID: 27010836 PMCID: PMC6411286. 2016
  • Baracos VE, Mazurak VC, Bhullar AS. Cancer cachexia is defined by an ongoing loss of skeletal muscle mass. Ann Palliat Med. 2019;8(1):3–12. PMID: 30685982.
  • Zieff GH, Wagoner CW, Paterson C, et al. Cardiovascular consequences of skeletal muscle impairments in breast cancer. Sports (Basel). 2020 May 31;8(6):80. PMID: 32486406 PMCID: PMC7353641.
  • Ono T, Takada S, Kinugawa S, et al. Curcumin ameliorates skeletal muscle atrophy in type 1 diabetic mice by inhibiting protein ubiquitination. Exp Physiol. 2015 Sep;100(9):1052–1063. PMID: 25998196.
  • Bilodeau PA, Coyne ES, Wing SS. The ubiquitin proteasome system in atrophying skeletal muscle: roles and regulation. Am J Physiol Cell Physiol. 2016 Sep 1;311(3):C392–403. PMID: 27510905.
  • Borgia D, Malena A, Spinazzi M, et al. Increased mitophagy in the skeletal muscle of spinal and bulbar muscular atrophy patients. Hum Mol Genet. 2017 Mar 15;26(6):1087–1103. PMID: 28087734 PMCID: PMC5409076.
  • Sato Y, Ohtsubo H, Nihei N, et al. Apobec2 deficiency causes mitochondrial defects and mitophagy in skeletal muscle. Faseb J. 2018 Mar;32(3):1428–1439. PMID: 29127187 PMCID: PMC5892721.
  • Castagnaro S, Chrisam M, Cescon M, et al. Extracellular collagen vi has prosurvival and autophagy instructive properties in mouse fibroblasts. Front Physiol. 2018 Aug 17 PMID: 30174616 PMCID: PMC6107713;9:1129.
  • Sin J, Andres AM, Taylor DJR, et al. Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts. Autophagy. 2016;12(2):369–380. PMID: 26566717 PMCID: PMC4836019.
  • Sarparanta J, García-Macia M, Singh R. Autophagy and mitochondria in obesity and type 2 diabetes. Curr Diabetes Rev. 2017;13(4):352–369. PMID: 26900135.
  • Baechler BL, Bloemberg D, Quadrilatero J. Mitophagy regulates mitochondrial network signaling, oxidative stress, and apoptosis during myoblast differentiation. Autophagy. 2019 Sep;15(9):1606–1619. PMID: 30859901 PMCID: PMC6693454.
  • Ji LL, Yeo D. Mitochondrial dysregulation and muscle disuse atrophy. F1000Res. 2019 Sep;8 (F1000Faculty Rev):1621. PMID: 31559011 PMCID: PMC6743252.
  • Veal E, Eisenstein M, Tseng ZH, et al. A cellular repressor of e1a-stimulated genes that inhibits activation by E2F. Mol Cell Biol. 1998 Sep;18(9):5032–5041. PMID: 9710587 PMCID: PMC109088.
  • Veal E, Groisman R, Eisenstein M, et al. The secreted glycoprotein CREG enhances differentiation of NTERA-2 human embryonal carcinoma cells. Oncogene. 2000 Apr 20;19(17):2120–2128. PMID: 10815803.
  • Veal E, Groisman R, Eisenstein M, et al. The crystal structure of CREG, a secreted glycoprotein involved in cellular growth and differentiation. Proc Natl Acad Sci USA. 2005 Dec 20;102(51):18326–18331. PMID: 16344469 PMCID: PMC1317909.
  • Ya-Ling H, Peng G, Ming-Yu S, et al. Secreted CREG inhibits cell proliferation mediated by mannose 6-phosphate/insulin-like growth factor II receptor in NIH3T3 fibroblasts. Genes Cells. 2008 Sep;13(9):977–986. PMID: 18691225.
  • Liu Y, Tian X, Liu S et al. DNA hypermethylation: a novel mechanism of creg gene suppression and atherosclerogenic endothelial dysfunction Redox Biol 2020May; 32: 101444. PMID: 32067910.
  • Sacher M, Bacco AD, Lunin VV, et al. Cellular repressor of e1a-stimulated genes is a bona fide lysosomal protein which undergoes proteolytic maturation during its biosynthesis. Exp Cell Res. 2008 Oct 1;314(16):3036–3047. PMID: 18621046.
  • Yan C-H, Yang L, Tian X-X, et al. CREG1 ameliorates myocardial fibrosis associated with autophagy activation and Rab7 expression. Biochim Biophys Acta. 2015 Feb;1852(2):353–364. PMID: 25774384.
  • Song H, Yan C, Tian X, et al. CREG protects from myocardial ischemia/reperfusion injury by regulating myocardial autophagy and apoptosis. Biochim Biophys Acta Mol Basis Dis. 2017 Aug;1863(8):1893–1903. PMID: 27840305.
  • Fujita R, Yoshioka K, Seko D, et al. Zmynd17 controls muscle mitochondrial quality and whole-body metabolism. Faseb J. 2018 Sep;32(9):5012–5025. PMID: 29913553.
  • Sánchez BJ, Anne-Marie K, Jean-Philippe Leduc-Gaudet T, et al. Depletion of HuR in murine skeletal muscle enhances exercise endurance and prevents cancer-induced muscle atrophy. Nat Commun. 2019 Sep 13;10(1):4171. PMID: 31519904 PMCID: PMC6744452.
  • Yang L, Liu Y, Tian X, et al. Cellular repressor of E1A-stimulated genes is a critical determinant of vascular remodeling in response to angiotensinII. Arterioscler Thromb Vasc Biol. 2017 Mar;37(3):485–494. PMID: 28062494.
  • Russell AP, Foletta VC, Snow RJ, et al. Skeletal muscle mitochondria: a major player in exercise, health and disease. Biochim Biophys Acta. 2014 Apr;1840(4):1276–1284. PMID: 24291686.
  • Lundby C, Jacobs RA. Adaptations of skeletal muscle mitochondria to exercise training. Exp Physiol. 2016 Jan;101(1):17–22. PMID: 26440213.
  • Meinild Lundby A-K, Jacobs RA, Gehrig S, et al. Exercise training increases skeletal muscle mitochondrial volume density by enlargement of existing mitochondria and not de novo biogenesis. Acta Physiol (Oxf). 2018 Jan;222(1). PMID: 28580772 https://doi.org/10.1111/apha.12905
  • Yin Y, Guoliang L, Yang J, et al. PTENα regulates mitophagy and maintains mitochondrial quality control. Autophagy. 2018;14(10):1742–1760. PMID: 29969932 PMCID: PMC6135630.
  • Okamoto T, Ishida R, Yamamoto H, et al. Functional structure and physiological functions of mammalian wild-type HSP60. Arch Biochem Biophys. 2015 Nov 15 PMID: 26427351;586:10–19.
  • Lian W-S, Jih-Yang K, Chen Y-S, et al. Chaperonin 60 sustains osteoblast autophagy and counteracts glucocorticoid aggravation of osteoporosis by chaperoning RPTOR. Cell Death Dis. 2018 Sep 17;9(10):938. PMID: 30224697 PMCID: PMC6141469.
  • Marino Gammazza A, Macaluso F, Di Felice V, et al. Hsp60 in skeletal muscle fiber biogenesis and homeostasis: from physical exercise to skeletal muscle pathology. Cells. 2018 Nov 22;7(12):224. PMID: 30469470 PMCID: PMC6315887.
  • Lian WS, Ko JY, Chen YS, et al. Chaperonin 60 sustains osteoblast autophagy and counteracts glucocorticoid aggravation of osteoporosis by chaperoning RPTOR. Cell Death Dis. 2018 Sep 17;9(10). 938.PMID: 30224697.
  • Gomes MJ, Martinez PF, Pagan LU, et al. Skeletal muscle aging: influence of oxidative stress and physical exercise. Oncotarget. 2017 Mar 21;8(12):20428–20440. PMID: 28099900 PMCID: PMC5386774.
  • Tieland M, Trouwborst I, Clark BC et al. Skeletal muscle performance and ageing J Cachexia Sarcopenia Muscle 2018Feb;9(1)3–19. PMID: 29151281 PMCID: PMC5803609.
  • Landers-Ramos RQ, Prior SJ. The microvasculature and skeletal muscle health in aging. Exerc Sport Sci Rev. 2018 Jul;46(3):172–179. PMID: 29652695 PMCID: PMC6005745.
  • Leduc-Gaudet J-P, Reynaud O, Hussain SN, et al. Parkin overexpression protects from ageing-related loss of muscle mass and strength. J Physiol. 2019 Apr;597(7):1975–1991. PMID: 30614532 PMCID: PMC6441909.
  • Favaro G, Romanello V, Varanita T, et al. DRP1-mediated mitochondrial shape controls calcium homeostasis and muscle mass. Nat Commun. 2019 Jun 12;10(1):2576. PMID: 31189900 PMCID: PMC6561930.
  • Mansueto G, Armani A, Viscomi C, et al. Transcription factor EB controls metabolic flexibility during exercise. Cell Metab. 2017 Jan 10;25(1):182–196. PMID: 28011087 PMCID: PMC5241227.
  • Gouspillou G, Godin R, Piquereau J, et al. Protective role of Parkin in skeletal muscle contractile and mitochondrial function. J Physiol. 2018 Jul;596(13):2565–2579. PMID: 29682760 PMCID: PMC6023825.
  • Gan Z, Tingting F, Kelly DP, et al. Skeletal muscle mitochondrial remodeling in exercise and diseases. Cell Res. 2018 Oct;28(10):969–980. PMID: 30108290 PMCID: PMC6170448.
  • Carter HN, Kim Y, Erlich AT, et al. Autophagy and mitophagy flux in young and aged skeletal muscle following chronic contractile activity. J Physiol. 2018 Aug;596(16):3567–3584. PMID: 29781176 PMCID: PMC6092298.
  • Leermakers PA, Kneppers AEM, Schols AMWJ, et al. Skeletal muscle unloading results in increased mitophagy and decreased mitochondrial biogenesis regulation. Muscle Nerve. 2019 Dec;60(6):769–778. PMID: 31495926 PMCID: PMC6900132.
  • Triolo M, Hood DA. Mitochondrial breakdown in skeletal muscle and the emerging role of the lysosomes. Arch Biochem Biophys. 2019 Jan;661:66–73. PMID: 30439362.
  • Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 2013 Jan;20(1):31–42. PMID: 22743996 PMCID: PMC3524633.
  • Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys. 2007 Jun 15;462(2):245–253. PMID: 17475204 PMCID: PMC2756107.
  • Vigié P, Camougrand N. Role of mitophagy in the mitochondrial quality control. Med Sci (Paris). 2017 Mar;33(3):231–237. PMID: 28367808.
  • Pickles S, Vigié P, Youle RJ. Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr Biol. 2018 Feb 19;28(4):R170–R185. PMID: 29462587.
  • Hood DA, Memme JM, Oliveira AN, et al. Maintenance of skeletal muscle mitochondria in health, exercise, and aging. Annu Rev Physiol. 2019 Feb 10; 81:19–41. PMID: 30216742.
  • Ghobrial G, Araujo L. The structure and biological function of CREG. Front Cell Dev Biol. 2018 Oct 26; 6: 136. PMID: 30416997 PMCID: PMC6212480;
  • Tian K, Song Y, Zhou K, et al. Chaperonin of group I: upregulation of HSP60 expression in the postnatal rat cochlea and rats with drug-induced hearing loss. Cell Stress Chaperones. 2018 Nov;23(6):1311–1317. PMID: 30196524 PMCID: PMC6237686.
  • Cappello F, De Macario EC, Rappa F, et al. Immunohistochemistry of human hsp60 in health and disease: from autoimmunity to cancer. Methods Mol Biol. 2018;1709:293–305. PMID: 29177667
  • Guo J, Xiao L, Zhang W, et al. HSP60-regulated mitochondrial proteostasis and protein translation promote tumor growth of ovarian cancer. Sci Rep. 2019 Sep 2;9(1):12628. PMID: 31477750 PMCID: PMC6718431.
  • Vilasi S, Bulone D, Bavisotto CC, et al. Chaperonin of group I: oligomeric spectrum and biochemical and biological implications. Front Mol Biosci. 2018 Jan 25;4:99. PMID: 29423396 PMCID: PMC5788889.
  • Tan Y, Zhang Y, Huo Z-J, et al. Molecular Cloning of Heat Shock Protein 10 (Hsp10) and 60 (Hsp60) cDNAs from Galeruca Daurica (Coleoptera: chrysomelidae) and their expression analysis. Bull Entomol Res. 2018 Aug;108(4):510–522. PMID: 29081303.
  • Ishida R, Okamoto T, Motojima F, et al. Physicochemical properties of the mammalian molecular chaperone HSP60. Int J Mol Sci. 2018 Feb 6;19(2):489. PMID: 29415503 PMCID: PMC5855711.
  • Livingston MJ, Wang J, Zhou J, et al. Clearance of damaged mitochondria via mitophagy is important to the protective effect of ischemic preconditioning in kidneys. Autophagy. 2019 Dec;15(12):2142–2162. PMID: 31066324 PMCID: PMC6844514.
  • Meng Q, Li BX, Xiao X. Toward developing chemical modulators of Hsp60 as potential therapeutics. Front Mol Biosci. 2018 Apr 20;5:35. PMID: 29732373 PMCID: PMC5920047.
  • Xianming D, Jiang X, Tian R, et al. RAB2 regulates the formation of autophagosome and autolysosome in mammalian cells. Autophagy. 2019 Oct;15(10):1774–1786. PMID: 30957628 PMCID: PMC6735470.
  • Frezza C, Cipolat S, Scorrano L, et al. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc. 2007;2(2):287–295. PMID: 17406588.
  • Cardenes N, Corey C, Geary L, et al. Platelet bioenergetic screen in sickle cell patients reveals mitochondrial complex V inhibition, which contributes to platelet activation. Blood. 2014 May 1;123(18):2864–2872. PMID: 24677541 PMCID: PMC4007612.
  • Nayak MK, Dhanesha N, Doddapattar P, et al. Dichloroacetate, an inhibitor of pyruvate dehydrogenase kinases, inhibits platelet aggregation and arterial Thrombosis. Blood Adv. 2018 Aug 14;2(15):2029–2038. PMID: 30108111 PMCID: PMC6093723.
  • Hariharan N, Zhai P, Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal. 2011 Jun;14(11):2179–2190. PMID: 20812860 PMCID: PMC3085947.
  • Dimauro I, Antonioni A, Mercatelli N et al. The early response of αB-crystallin to a single bout of aerobic exercise in mouse skeletal muscles depends upon fiber oxidative features Redox Biol. 2019Jun;24:101183. PMID: 30974319 PMCID: PMC6454247.
  • Guang X, Ting L, Chen J, et al. Autosomal dominant retinitis pigmentosa-associated gene PRPF8 is essential for hypoxia-induced mitophagy through regulating ULK1 mRNA splicing. Autophagy. 2018;14(10):1818–1830. PMID: 30103670 PMCID: PMC6135625.
  • Guoliang L, Yang J, Yang C, et al. PTEN regulates mitophagy and maintains mitochondrial quality control. Autophagy. 2018;14(10):1742–1760. PMID: 29969932 PMCID: PMC6135630.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.