Skeletal muscle type-specific mitochondrial adaptation to high-fat diet relies on differential autophagy modulation.
Atg7
fatty acids
obesity
skeletal muscle fiber
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
01
09
2021
received:
23
06
2020
accepted:
03
09
2021
entrez:
23
9
2021
pubmed:
24
9
2021
medline:
28
10
2021
Statut:
ppublish
Résumé
In obesity, skeletal muscle mitochondrial activity changes to cope with increased nutrient availability. Autophagy has been proposed as an essential mechanism involved in the regulation of mitochondrial metabolism. Still, the contribution of autophagy to mitochondrial adaptations in skeletal muscle during obesity is unknown. Here, we show that in response to high-fat diet (HFD) feeding, distinct skeletal muscles in mice exhibit differentially regulated autophagy that may modulate mitochondrial activity. We observed that after 4 and 40 weeks of high-fat diet feeding, OXPHOS subunits and mitochondrial DNA content increased in the oxidative soleus muscle. However, in gastrocnemius muscle, which has a mixed fiber-type composition, the mitochondrial mass increased only after 40 weeks of HFD feeding. Interestingly, fatty acid-supported mitochondrial respiration was enhanced in gastrocnemius, but not in soleus muscle after a 4-week HFD feeding. This increased metabolic profile in gastrocnemius was paralleled by preserving autophagy flux, while autophagy flux in soleus was reduced. To determine the role of autophagy in this differential response, we used an autophagy-deficient mouse model with partial deletion of Atg7 specifically in skeletal muscle (SkM-Atg7
Identifiants
pubmed: 34555201
doi: 10.1096/fj.202001593RR
doi:
Substances chimiques
Atg7 protein, mouse
0
Fatty Acids
0
Autophagy-Related Protein 7
EC 6.2.1.45
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e21933Subventions
Organisme : NIA NIH HHS
ID : R56 AG063820
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL108379
Pays : United States
Informations de copyright
© 2021 Federation of American Societies for Experimental Biology.
Références
(NCD-RisC) NRFC. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19·2 million participants. Lancet. 2016;387(10026):1377-1396.
Wells GD, Noseworthy MD, Hamilton J, Tarnopolski M, Tein I. Skeletal muscle metabolic dysfunction in obesity and metabolic syndrome. Can J Neurol Sci. 2008;35(1):31-40.
Barclay CJ. Energy demand and supply in human skeletal muscle. J Muscle Res Cell Motil. 2017;38(2):143-155.
Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev. 2011;91(4):1447-1531.
Bloemberg D, Quadrilatero J. Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis. PLoS One. 2012;7(4):e35273.
Augusto V, Padovani CR, Eduardo G, Campos R. Skeletal muscle fiber types in C57Bl6J mice. Braz J Morphol Sci. 2004;21:89-94.
Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Arch. 1985;403(4):369-376.
Oberbach A, Bossenz Y, Lehmann S, et al. Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care. 2006;29(4):895-900.
DeNies MS, Johnson J, Maliphol AB, et al. Diet-induced obesity alters skeletal muscle fiber types of male but not female mice. Physiol Rep. 2014;2(1):e00204.
Stuart CA, McCurry MP, Marino A, et al. Slow-twitch fiber proportion in skeletal muscle correlates with insulin responsiveness. J Clin Endocrinol Metab. 2013;98(5):2027-2036.
Albers PH, Pedersen AJT, Birk JB, et al. Human muscle fiber type-specific insulin signaling: impact of obesity and type 2 diabetes. Diabetes. 2015;64(2):485-497.
Twig G, Hyde B, Shirihai OS. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta. 2008;1777(9):1092-1097.
Lin J, Wu H, Tarr PT, et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature. 2002;418(6899):797-801.
Choi CS, Befroy DE, Codella R, et al. Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci U S A. 2008;105(50):19926-19931.
Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8(11):931-937.
Parzych KR, Klionsky DJ. An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal. 2014;20(3):460-473.
Ichimura Y, Kirisako T, Takao T, et al. A ubiquitin-like system mediates protein lipidation. Nature. 2000;408(6811):488-492.
Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1-222.
Rogov V, Dötsch V, Johansen T, Kirkin V. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53(2):167-178.
Yamano K, Matsuda N, Tanaka K. The ubiquitin signal and autophagy: an orchestrated dance leading to mitochondrial degradation. EMBO Rep. 2016;17(3):300-316.
Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183(5):795-803.
Pickles S, Vigié P, Youle RJ. Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr Biol. 2018;28(4):R170-R185.
Fortini P, Ferretti C, Iorio E, et al. The fine tuning of metabolism, autophagy and differentiation during in vitro myogenesis. Cell Death Dis. 2016;7(3):e2168.
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.
Baldelli S, Aquilano K, Ciriolo MR. PGC-1α buffers ROS-mediated removal of mitochondria during myogenesis. Cell Death Dis. 2014;5(11):e1515.
Ma X, Liu H, Murphy JT, et al. Regulation of the transcription factor EB-PGC1α axis by beclin-1 controls mitochondrial quality and cardiomyocyte death under stress. Mol Cell Biol. 2015;35(6):956-976.
Nezich CL, Wang C, Fogel AI, Youle RJ. MiT/TFE transcription factors are activated during mitophagy downstream of Parkin and Atg5. J Cell Biol. 2015;210(3):435-450.
Lira VA, Okutsu M, Zhang M, et al. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J. 2013;27(10):4184-4193.
Ju J-S, Jeon S-I, Park J-Y, et al. Autophagy plays a role in skeletal muscle mitochondrial biogenesis in an endurance exercise-trained condition. J Physiol Sci. 2016;66(5):417-430.
Vainshtein A, Tryon LD, Pauly M, Hood DA. Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle. Am J Physiol Cell Physiol. 2015;308(9):C710-C719.
Garcia-Roves P, Huss JM, Han D-H, et al. Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci U S A. 2007;104(25):10709-10713.
Turner N, Bruce CR, Beale SM, et al. Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes. 2007;56(8):2085-2092.
Hancock CR, Han D-H, Chen M, et al. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci U S A. 2008;105(22):7815-7820.
Li J, Kanasaki M, Xu L, et al. A ketogenic amino acid rich diet benefits mitochondrial homeostasis by altering the AKT/4EBP1 and autophagy signaling pathways in the gastrocnemius and soleus. Biochim Biophys Acta Gen Subj. 2018;1862(7):1547-1555.
Qi Z, Xia J, Xue X, He Q, Ji L, Ding S. Long-term treatment with nicotinamide induces glucose intolerance and skeletal muscle lipotoxicity in normal chow-fed mice: compared to diet-induced obesity. J Nutr Biochem. 2016;36:31-41.
Zhou B, Li H, Liu J, et al. Autophagic dysfunction is improved by intermittent administration of osteocalcin in obese mice. Int J Obes (Lond). 2016;40(5):833-843.
Liu Y, Palanivel R, Rai E, et al. Adiponectin stimulates autophagy and reduces oxidative stress to enhance insulin sensitivity during high-fat diet feeding in mice. Diabetes. 2015;64(1):36-48.
Jørgensen MS, Tornqvist KS, Hvid H. Calculation of glucose dose for intraperitoneal glucose tolerance tests in lean and obese mice. J Am Assoc Lab Anim Sci. 2017;56(1):95-97.
Benedé-Ubieto R, Estévez-Vázquez O, Ramadori P, Cubero FJ, Nevzorova YA. Guidelines and considerations for metabolic tolerance tests in mice. Diabetes Metab Syndr Obes. 2020;13:439-450.
Terry RL, Wells DJ. Histopathological evaluation of skeletal muscle with specific reference to mouse models of muscular dystrophy. Curr Protoc Mouse Biol. 2016;6(4):343-363.
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45.
Anderson EJ, Lustig ME, Boyle KE, et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest. 2009;119(3):573-581.
Lark DS, Torres MJ, Lin CT, Ryan TE, Anderson EJ, Neufer PD. Direct real-time quantification of mitochondrial oxidative phosphorylation efficiency in permeabilized skeletal muscle myofibers. Am J Physiol Cell Physiol. 2016;311(2):C239-C245.
Kim KH, Jeong YT, Oh H, et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med. 2013;19(1):83-92.
Tong M, Saito T, Zhai P, et al. Mitophagy is essential for maintaining cardiac function during high fat diet-induced diabetic cardiomyopathy. Circ Res. 2019;124(9):1360-1371.
Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140(3):313-326.
Jain SS, Paglialunga S, Vigna C, et al. High-fat diet-induced mitochondrial biogenesis is regulated by mitochondrial-derived reactive oxygen species activation of CaMKII. Diabetes. 2014;63(6):1907-1913.
Yuzefovych LV, Musiyenko SI, Wilson GL, Rachek LI. Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced insulin resistance mice. PLoS One. 2013;8(1):e54059.
Bonnard C, Durand A, Peyrol S, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest. 2008;118(2):789-800.
Ghaben AL, Scherer PE. Adipogenesis and metabolic health. Nat Rev Mol Cell Biol. 2019;20(4):242-258.
Müller MJ, Lagerpusch M, Enderle J, Schautz B, Heller M, Bosy-Westphal A. Beyond the body mass index: tracking body composition in the pathogenesis of obesity and the metabolic syndrome. Obes Rev. 2012;13(Suppl 2):6-13.
Shortreed KE, Krause MP, Huang JH, et al. Muscle-specific adaptations, impaired oxidative capacity and maintenance of contractile function characterize diet-induced obese mouse skeletal muscle. PLoS One. 2009;4(10):e7293.
Sparks LM, Xie H, Koza RA, et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes. 2005;54(7):1926-1933.
Koves TR, Ussher JR, Noland RC, et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 2008;7(1):45-56.
Pietrangelo L, D’Incecco A, Ainbinder A, et al. Age-dependent uncoupling of mitochondria from Ca2+ release units in skeletal muscle. Oncotarget. 2015;6(34):35358-35371.
Del Campo A, Contreras-Hernández I, Castro-Sepúlveda M, et al. Muscle function decline and mitochondria changes in middle age precede sarcopenia in mice. Aging (Albany NY). 2018;10(1):34-55.
Kwong JQ, Huo J, Bround MJ, et al. The mitochondrial calcium uniporter underlies metabolic fuel preference in skeletal muscle. JCI Insight. 2018;3(22):e121689.
Pan X, Liu J, Nguyen T, et al. The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat Cell Biol. 2013;15(12):1464-1472.
Stephenson EJ, Camera DM, Jenkins TA, et al. Skeletal muscle respiratory capacity is enhanced in rats consuming an obesogenic Western diet. Am J Physiol Endocrinol Metab. 2012;302(12):E1541-E1549.
Schrauwen P, Hoppeler H, Billeter R, Bakker AH, Pendergast DR. Fiber type dependent upregulation of human skeletal muscle UCP2 and UCP3 mRNA expression by high-fat diet. Int J Obes Relat Metab Disord. 2001;25(4):449-456.
Masiero E, Agatea L, Mammucari C, et al. Autophagy is required to maintain muscle mass. Cell Metab. 2009;10(6):507-515.
Wu JJ, Quijano C, Chen E, et al. Mitochondrial dysfunction and oxidative stress mediate the physiological impairment induced by the disruption of autophagy. Aging (Albany NY). 2009;1(4):425-437.
Lim Y-M, Lim H, Hur KY, et al. Systemic autophagy insufficiency compromises adaptation to metabolic stress and facilitates progression from obesity to diabetes. Nat Commun. 2014;5:4934.
Pereira RO, Tadinada SM, Zasadny FM, et al. OPA1 deficiency promotes secretion of FGF21 from muscle that prevents obesity and insulin resistance. Embo J. 2017;36(14):2126-2145.
Yan Z, Kronemberger A, Blomme J, et al. Exercise leads to unfavourable cardiac remodelling and enhanced metabolic homeostasis in obese mice with cardiac and skeletal muscle autophagy deficiency. Sci Rep. 2017;7(1):7894.
Singh R, Kaushik S, Wang Y, et al. Autophagy regulates lipid metabolism. Nature. 2009;458(7242):1131-1135.
Nishida Y, Arakawa S, Fujitani K, et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature. 2009;461(7264):654-658.
Hirota Y, Yamashita S-I, Kurihara Y, et al. Mitophagy is primarily due to alternative autophagy and requires the MAPK1 and MAPK14 signaling pathways. Autophagy. 2015;11(2):332-343.