Mitochondrial dynamics, quality control and miRNA regulation in skeletal muscle: Implications for obesity and related metabolic disease

Clinical Science

Volumn 130, Issue 11, 2016, Pages 843-852

  Dahlmans, Dennis ^a   Houzelle, Alexandre ^a   Schrauwen, Patrick ^a   Hoeks, Joris ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Metabolic disease; MicroRNAs; Mitochondria; Obesity; Skeletal muscle

Indexed keywords

LIPID; MICRORNA; MITOCHONDRIAL PROTEIN;

HUMAN; METABOLIC DISORDER; METABOLIC REGULATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; QUALITY CONTROL; REGULATORY MECHANISM; REVIEW; SKELETAL MUSCLE; UNFOLDED PROTEIN RESPONSE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; METABOLIC DISEASES; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DYNAMICS; MUSCLE, SKELETAL; OBESITY;

EID: 85014082042     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150780     Document Type: Review

References (54)

1. Ng, M., Fleming, T., Robinson, M., Thomson, B., Graetz, N., Margono, C., Mullany, E.C., Biryukov, S., Abbafati, C., Abera, S.F. et al. (2014) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384, 766-781
2. Goodpaster, B.H., Theriault, R., Watkins, S.C. and Kelley, D.E. (2000) Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49, 467-472
3. DeFronzo, R.A. and Tripathy, D. (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32 Suppl 2, S157-S163
4. Coen, P.M., Hames, K.C., Leachman, E.M., DeLany, J.P., Ritov, V.B., Menshikova, E.V., Dube, J.J., Stefanovic-Racic, M., Toledo, F.G. and Goodpaster, B.H. (2013) Reduced skeletal muscle oxidative capacity and elevated ceramide but not diacylglycerol content in severe obesity. Obesity (Silver Spring) 21, 2362-2371
5. Kelley, D.E., He, J., Menshikova, E.V. and Ritov, V.B. (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944-2950
6. Kim, J.Y., Hickner, R.C., Cortright, R.L., Dohm, G.L. and Houmard, J.A. (2000) Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279, E1039-E1044
7. Lefort, N., Glancy, B., Bowen, B., Willis, W.T., Bailowitz, Z., De Filippis, E.A., Brophy, C., Meyer, C., Hojlund, K., Yi, Z. and Mandarino, L.J. (2010) Increased reactive oxygen species production and lower abundance of complex I subunits and carnitine palmitoyltransferase 1B protein despite normal mitochondrial respiration in insulin-resistant human skeletal muscle. Diabetes 59, 2444-2452
8. Smirnova, E., Shurland, D.L., Ryazantsev, S.N. and van der Bliek, A.M. (1998) A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143, 351-358
9. Jovaisaite, V. and Auwerx, J. (2015) The mitochondrial unfolded protein response-synchronizing genomes. Curr. Opin. Cell Biol. 33, 74-81
10. Roy, M., Reddy, P.H., Iijima, M. and Sesaki, H. (2015) Mitochondrial division and fusion in metabolism. Curr. Opin. Cell Biol. 33, 111-118
11. Iqbal, S. and Hood, D.A. (2015) The role of mitochondrial fusion and fission in skeletal muscle function and dysfunction. Front. Biosci. (Landmark Ed) 20, 157-172
12. Loson, O.C., Song, Z., Chen, H. and Chan, D.C. (2013) Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24, 659-667
13. Kobayashi, S. and Liang, Q. (2015) Autophagy and mitophagy in diabetic cardiomyopathy. Biochim. Biophys. Acta 1852, 252-261
14. Jheng, H.F., Tsai, P.J., Guo, S.M., Kuo, L.H., Chang, C.S., Su, I.J., Chang, C.R. and Tsai, Y.S. (2012) Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol. Cell. Biol. 32, 309-19
15. Nie, Q., Wang, C., Song, G., Ma, H., Kong, D., Zhang, X., Gan, K. and Tang, Y. (2014) Mitofusin 2 deficiency leads to oxidative stress that contributes to insulin resistance in rat skeletal muscle cells. Mol. Biol. Rep. 41, 6975-6983
16. Liu, R., Jin, P., Yu, L., Wang, Y., Han, L., Shi, T. and Li, X. (2014) Impaired mitochondrial dynamics and bioenergetics in diabetic skeletal muscle. PLoS One 9, e92810
17. Lionetti, L., Mollica, M.P., Donizzetti, I., Gifuni, G., Sica, R., Pignalosa, A., Cavaliere, G., Gaita, M., De Filippo, C., Zorzano, A. and Putti, R. (2014) High-lard and high-fish-oil diets differ in their effects on function and dynamic behaviour of rat hepatic mitochondria. PLoS One 9, e92753
18. Sebastian, D., Hernandez-Alvarez, M.I., Segales, J., Sorianello, E., Munoz, J.P., Sala, D., Waget, A., Liesa, M., Paz, J.C., Gopalacharyulu, P. et al. (2012) Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. Proc. Natl. Acad. Sci. U.S.A. 109, 5523-5528
19. Kong, D., Song, G., Wang, C., Ma, H., Ren, L., Nie, Q., Zhang, X. and Gan, K. (2013) Overexpression of mitofusin 2 improves translocation of glucose transporter 4 in skeletal muscle of highfat dietfed rats through AMPactivated protein kinase signaling. Mol. Med. Rep. 8, 205-210
20. Lally, J.S., Herbst, E.A., Matravadia, S., Maher, A.C., Perry, C.G., Ventura-Clapier, R. and Holloway, G.P. (2013) Over-expressing mitofusin-2 in healthy mature mammalian skeletal muscle does not alter mitochondrial bioenergetics. PLoS One 8, e55660
21. Wang, L., Ishihara, T., Ibayashi, Y., Tatsushima, K., Setoyama, D., Hanada, Y., Takeichi, Y., Sakamoto, S., Yokota, S., Mihara, K. et al. (2015) Disruption of mitochondrial fission in the liver protects mice from diet-induced obesity and metabolic deterioration. Diabetologia 58, 2371-2380
22. Bach, D., Pich, S., Soriano, F.X., Vega, N., Baumgartner, B., Oriola, J., Daugaard, J.R., Lloberas, J., Camps, M., Zierath, J.R. et al. (2003) Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278, 17190-17197
23. Fealy, C.E., Mulya, A., Lai, N. and Kirwan, J.P. (2014) Exercise training decreases activation of the mitochondrial fission protein dynamin-related protein-1 in insulin-resistant human skeletal muscle. J. Appl. Physiol. (1985) 117, 239-245
24. Houtkooper, R.H., Mouchiroud, L., Ryu, D., Moullan, N., Katsyuba, E., Knott, G., Williams, R.W. and Auwerx, J. (2013) Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497, 451-457
25. Chacinska, A., Koehler, C.M., Milenkovic, D., Lithgow, T. and Pfanner, N. (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644
26. Al-Furoukh, N., Ianni, A., Nolte, H., Holper, S., Kruger, M., Wanrooij, S. and Braun, T. (2015) ClpX stimulates the mitochondrial unfolded protein response (UPR) in mammalian cells. Biochim. Biophys. Acta 1853, 2580-2591
27. Jovaisaite, V., Mouchiroud, L. and Auwerx, J. (2014) The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J. Exp. Biol. 217 (Pt 1), 137-143
28. Andreux, P.A., Williams, E.G., Koutnikova, H., Houtkooper, R.H., Champy, M.F., Henry, H., Schoonjans, K., Williams, R.W. and Auwerx, J. (2012) Systems genetics of metabolism: the use of the BXD murine reference panel for multiscalar integration of traits. Cell 150, 1287-1299
29. Disatnik, M.H., Hwang, S., Ferreira, J.C. and Mochly-Rosen, D. (2015) New therapeutics to modulate mitochondrial dynamics and mitophagy in cardiac diseases. J. Mol. Med. (Berl) 93, 279-287
30. Jin, S.M. and Youle, R.J. (2013) The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 9, 1750-1757
31. Glick, D., Barth, S. and Macleod, K.F. (2010) Autophagy: cellular and molecular mechanisms. J. Pathol. 221, 3-12
32. Rong, J.X., Qiu, Y., Hansen, M.K., Zhu, L., Zhang, V., Xie, M., Okamoto, Y., Mattie, M.D., Higashiyama, H., Asano, S. et al. (2007) Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone. Diabetes 56, 1751-1760
33. Drew, B.G., Ribas, V., Le, J.A., Henstridge, D.C., Phun, J., Zhou, Z., Soleymani, T., Daraei, P., Sitz, D., Vergnes, L. et al. (2014) HSP72 is a mitochondrial stress sensor critical for Parkin action, oxidative metabolism, and insulin sensitivity in skeletal muscle. Diabetes 63, 1488-1505
34. Henstridge, D.C., Bruce, C.R., Drew, B.G., Tory, K., Kolonics, A., Estevez, E., Chung, J., Watson, N., Gardner, T., Lee-Young, R.S. et al. (2014) Activating HSP72 in rodent skeletal muscle increases mitochondrial number and oxidative capacity and decreases insulin resistance. Diabetes 63, 1881-1894
35. Bruce, C.R., Carey, A.L., Hawley, J.A. and Febbraio, M.A. (2003) Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52, 2338-2345
36. Chung, J., Nguyen, A.K., Henstridge, D.C., Holmes, A.G., Chan, M.H., Mesa, J.L., Lancaster, G.I., Southgate, R.J., Bruce, C.R., Duffy, S.J. et al. (2008) HSP72 protects against obesity-induced insulin resistance. Proc. Natl. Acad. Sci. U.S.A. 105, 1739-1744
37. Imatoh, T., Sugie, T., Miyazaki, M., Tanihara, S., Baba, M., Momose, Y., Uryu, Y. and Une, H. (2009) Is heat shock protein 60 associated with type 2 diabetes mellitus? Diabetes Res. Clin. Pract. 85, 208-212.
38. Venojarvi, M., Aunola, S., Puhke, R., Marniemi, J., Hamalainen, H., Halonen, J.P., Lindstrom, J., Rastas, M., Hallsten, K., Nuutila, P. et al. (2008) Exercise training with dietary counselling increases mitochondrial chaperone expression in middle-aged subjects with impaired glucose tolerance. BMC Endocr. Disord. 8, 3
39. Abubaker, J., Tiss, A., Abu-Farha, M., Al-Ghimlas, F., Al-Khairi, I., Baturcam, E., Cherian, P., Elkum, N., Hammad, M., John, J. et al. (2013) DNAJB3/HSP-40 cochaperone is downregulated in obese humans and is restored by physical exercise. PLoS One 8, e69217
40. Tiss, A., Khadir, A., Abubaker, J., Abu-Farha, M., Al-Khairi, I., Cherian, P., John, J., Kavalakatt, S., Warsame, S., Al-Ghimlas, F. et al. (2014) Immunohistochemical profiling of the heat shock response in obese non-diabetic subjects revealed impaired expression of heat shock proteins in the adipose tissue. Lipids Health Dis. 13, 106
41. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
42. Gallagher, I.J., Scheele, C., Keller, P., Nielsen, A.R., Remenyi, J., Fischer, C.P., Roder, K., Babraj, J., Wahlestedt, C., Hutvagner, G. et al. (2010) Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome. Med. 2, 9
43. Bork-Jensen, J., Scheele, C., Christophersen, D.V., Nilsson, E., Friedrichsen, M., Fernandez-Twinn, D.S., Grunnet, L.G., Litman, T., Holmstrom, K. et al. (2015) Glucose tolerance is associated with differential expression of microRNAs in skeletal muscle: results from studies of twins with and without type 2 diabetes. Diabetologia 58, 363-373
44. Agarwal, P., Srivastava, R., Srivastava, A.K., Ali, S. and Datta, M. (2013) miR-135a targets IRS2 and regulates insulin signaling and glucose uptake in the diabetic gastrocnemius skeletal muscle. Biochim. Biophys. Acta 1832, 1294-1303
45. Gao, Y., Wu, F., Zhou, J., Yan, L., Jurczak, M.J., Lee, H.Y., Yang, L., Mueller, M., Zhou, X.B., Dandolo, L. et al. (2014) The H19/let-7 double-negative feedback loop contributes to glucose metabolism in muscle cells. Nucleic Acids Res. 42, 13799-13811
46. Sripada, L., Tomar, D., Prajapati, P., Singh, R., Singh, A.K. and Singh, R. (2012) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7, e44873
47. Barrey, E., Saint-Auret, G., Bonnamy, B., Damas, D., Boyer, O. and Gidrol, X. (2011) Pre-microRNA and mature microRNA in human mitochondria. PloS one 6, e20220
48. Li, J., Li, Y., Jiao, J., Wang, J., Li, Y., Qin, D. and Li, P. (2014) Mitofusin 1 is negatively regulated by microRNA 140 in cardiomyocyte apoptosis. Mol. Cell Biol. 34, 1788-1799
49. el Azzouzi, H., Leptidis, S., Dirkx, E., Hoeks, J., van Bree, B., Brand, K., McClellan, E.A., Poels, E., Sluimer, J.C., van den Hoogenhof, M.M. et al. (2013) The hypoxia-inducible microRNA cluster miR-199a approximately 214 targets myocardial PPARdelta and impairs mitochondrial fatty acid oxidation. Cell Metab. 18, 341-354
50. Yamamoto, H., Morino, K., Nishio, Y., Ugi, S., Yoshizaki, T., Kashiwagi, A. and Maegawa, H. (2012) MicroRNA-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcription factor A and Forkhead box j3. Am. J. Physiol. Endocrinol. Metab. 303, E1419-E1427
51. Aoi, W., Naito, Y., Mizushima, K., Takanami, Y., Kawai, Y., Ichikawa, H. and Yoshikawa, T. (2010) The microRNA miR-696 regulates PGC-1[alpha] in mouse skeletal muscle in response to physical activity. Am. J. Physiol. Endocrinol. Metab. 298, E799-E806
52. Hoeks, J. and Schrauwen, P. (2012) Muscle mitochondria and insulin resistance: a human perspective. Trends Endocrinol. Metab. 23, 444-450
53. Zhang, Y., Yang, L., Gao, Y.F., Fan, Z.M., Cai, X.Y., Liu, M.Y., Guo, X.R., Gao, C.L. and Xia, Z.K. (2013) MicroRNA-106b induces mitochondrial dysfunction and insulin resistance in C2C12 myotubes by targeting mitofusin-2. Mol. Cell. Endocrinol. 381, 230-240
54. Mohamed, J.S., Hajira, A., Pardo, P.S. and Boriek, A.M. (2014) MicroRNA-149 inhibits PARP-2 and promotes mitochondrial biogenesis via SIRT-1/PGC-1alpha network in skeletal muscle. Diabetes 63, 1546-1559