MicroRNA-208b progressively declines after spinal cord injury in humans and is inversely related to myostatin expression

Physiological Reports

Volumn 3, Issue 11, 2015, Pages

  Boon, Hanneke ^a   Sjögren, Rasmus J O ^a   Massart, Julie ^a   Egan, Brendan ^a   Kostovski, Emil ^b,c   Iversen, Per O ^c,d   Hjeltnes, Nils ^b   Chibalin, Alexander V ^a   Widegren, Ulrika ^a   Zierath, Juleen R ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SUNNAAS REHABILITATION HOSPITAL   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

MicroRNA; skeletal muscle; spinal cord injury

Indexed keywords

EID: 84977662794     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12622     Document Type: Article

References (56)

1. Adams, C. M., M. Suneja, S. Dudley-Javoroski, and R. K. Shields. 2011. Altered mRNA expression after long-term soleus electrical stimulation training in humans with paralysis. Muscle Nerve 43:65–75.
2. Aksnes, A. K., N. Hjeltnes, E. O. Wahlstrom, A. Katz, J. R. Zierath, and H. Wallberg-Henriksson. 1996. Intact glucose transport in morphologically altered denervated skeletal muscle from quadriplegic patients. Am. J. Physiol. 271:E593–E600.
3. Ambros, V. 2004. The functions of animal microRNAs. Nature 431:350–355.
4. Andersen, C. L., J. L. Jensen, and T. F. Orntoft. 2004. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64:5245–5250.
5. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297.
6. Bartel, D. P., and C. Z. Chen. 2004. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5:396–400.
7. Bauman, W. A., and A. M. Spungen. 1994. Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism 43:749–756.
8. Bell, M. L., M. Buvoli, and L. A. Leinwand. 2010. Uncoupling of expression of an intronic microRNA and its myosin host gene by exon skipping. Mol. Cell. Biol. 30:1937–1945.
9. Bodine, S. C. 2013. Disuse-induced muscle wasting. Int. J. Biochem. Cell Biol. 45:2200–2208.
10. Callis, T. E., K. Pandya, H. Y. Seok, R. H. Tang, M. Tatsuguchi, Z. P. Huang, et al. 2009. MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J. Clin. Invest. 119:2772–2786.
11. Duckworth, W. C., S. S. Solomon, P. Jallepalli, C. Heckemeyer, J. Finnern, and A. Powers. 1980. Glucose intolerance due to insulin resistance in patients with spinal cord injuries. Diabetes 29:906–910.
12. Durieux, A. C., A. Amirouche, S. Banzet, N. Koulmann, R. Bonnefoy, M. Pasdeloup, et al. 2007. Ectopic expression of myostatin induces atrophy of adult skeletal muscle by decreasing muscle gene expression. Endocrinology 148:3140–3147.
13. Egan, B., and J. R. Zierath. 2013. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17:162–184.
14. Elia, L., R. Contu, M. Quintavalle, F. Varrone, C. Chimenti, M. A. Russo, et al. 2009. Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation 120:2377–2385.
15. Gan, Z., J. Rumsey, B. C. Hazen, L. Lai, T. C. Leone, R. B. Vega, et al. 2013. Nuclear receptor/microRNA circuitry links muscle fiber type to energy metabolism. J. Clin. Invest. 123:2564–2575.
16. Ge, Y., Y. Sun, and J. Chen. 2011. IGF-II is regulated by microRNA-125b in skeletal myogenesis. J. Cell Biol. 192:69–81.
17. Gonzalez-Cadavid, N. F., W. E. Taylor, K. Yarasheski, I. Sinha-Hikim, K. Ma, S. Ezzat, et al. 1998. Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc. Natl Acad. Sci. USA 95:14938–14943.
18. Hjeltnes, N., A. K. Aksnes, K. I. Birkeland, J. Johansen, A. Lannem, and H. Wallberg-Henriksson. 1997. Improved body composition after 8 week of electrically stimulated leg cycling in tetraplegic patients. Am. J. Physiol. 273:R1072–R1079.
19. Hjeltnes, N., D. Galuska, M. Bjornholm, A. K. Aksnes, A. Lannem, J. R. Zierath, et al. 1998. Exercise-induced overexpression of key regulatory proteins involved in glucose uptake and metabolism in tetraplegic persons: molecular mechanism for improved glucose homeostasis. FASEB J. 12:1701–1712.
20. Hua, Y., Y. Zhang, and J. Ren. 2012. IGF-1 deficiency resists cardiac hypertrophy and myocardial contractile dysfunction: role of microRNA-1 and microRNA-133a. J. Cell Mol. Med. 16:83–95.
21. Ju, C. R., and R. C. Chen. 2012. Serum myostatin levels and skeletal muscle wasting in chronic obstructive pulmonary disease. Respir. Med. 106:102–108.
22. Kirshblum, S. C., S. P. Burns, F. Biering-Sorensen, W. Donovan, D. E. Graves, A. Jha, et al. 2011. International standards for neurological classification of spinal cord injury (revised 2011). J. Spinal Cord Med. 34:535–546.
23. Kostovski, E., H. Boon, N. Hjeltnes, L. S. Lundell, M. Ahlsen, A. V. Chibalin, et al. 2013. Altered content of AMP-activated protein kinase isoforms in skeletal muscle from spinal cord injured subjects. Am. J. Physiol. Endocrinol. Metab. 305:E1071–E1080.
24. Kramer, D. K., M. Ahlsen, J. Norrbom, E. Jansson, N. Hjeltnes, T. Gustafsson, et al. 2006. Human skeletal muscle fibre type variations correlate with PPAR alpha, PPAR delta and PGC-1 alpha mRNA. Acta. Physiol. (Oxf) 188:207–216.
25. Kulkarni, S. S., H. K. Karlsson, F. Szekeres, A. V. Chibalin, A. Krook, and J. R. Zierath. 2011. Suppression of 5'-nucleotidase enzymes promotes AMP-activated protein kinase (AMPK) phosphorylation and metabolism in human and mouse skeletal muscle. J. Biol. Chem. 286:34567-34574.
26. Lanceta, J., R. A. Prough, R. Liang, and E. Wang. 2010. MicroRNA group disorganization in aging. Exp. Gerontol. 45:269–278.
27. Lee, S. J. 2004. Regulation of muscle mass by myostatin. Annu. Rev. Cell Dev. Biol. 20:61–86.
28. Lee, R. C., R. L. Feinbaum, and V. Ambros. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854.
29. Leger, B., R. Senese, A. W. Al-Khodairy, O. Deriaz, C. Gobelet, J. P. Giacobino, et al. 2009. Atrogin-1, MuRF1, and FoXO, as well as phosphorylated GSK-3beta and 4E-BP1 are reduced in skeletal muscle of chronic spinal cord-injured patients. Muscle Nerve 40:69–78.
30. Leung, A. K., and P. A. Sharp. 2010. MicroRNA functions in stress responses. Mol. Cell 40:205–215.
31. Liu, M., D. Zhang, C. Shao, J. Liu, F. Ding, and X. Gu. 2007. Expression pattern of myostatin in gastrocnemius muscle of rats after sciatic nerve crush injury. Muscle Nerve 35:649–656.
32. Long, Y. C., E. Kostovski, H. Boon, N. Hjeltnes, A. Krook, and U. Widegren. 2011. Differential expression of metabolic genes essential for glucose and lipid metabolism in skeletal muscle from spinal cord injured subjects. J. Appl. Physiol. 110:1204–1210.
33. McCarthy, J. J. 2011. The MyomiR network in skeletal muscle plasticity. Exerc. Sport Sci. Rev. 39:150–154.
34. McCarthy, J. J., K. A. Esser, C. A. Peterson, and E. E. Dupont-Versteegden. 2009. Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy. Physiol. Genomics 39:219–226.
35. McFarlane, C., A. Vajjala, H. Arigela, S. Lokireddy, X. Ge, S. Bonala, et al. 2014. Negative auto-regulation of myostatin expression is mediated by Smad3 and microRNA-27. PLoS ONE 9:e87687.
36. McPherron, A. C., A. M. Lawler, and S. J. Lee. 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83–90.
37. Mendell, J. T., and E. N. Olson. 2012. MicroRNAs in stress signaling and human disease. Cell 148:1172–1187.
38. Monteys, A. M., R. M. Spengler, J. Wan, L. Tecedor, K. A. Lennox, Y. Xing, et al. 2010. Structure and activity of putative intronic miRNA promoters. RNA 16:495–505.
39. Petrie, M. A., M. Suneja, E. Faidley, and R. K. Shields. 2014. A minimal dose of electrically induced muscle activity regulates distinct gene signaling pathways in humans with spinal cord injury. PLoS ONE 9:e115791.
40. van Rooij, E., L. B. Sutherland, X. Qi, J. A. Richardson, J. Hill, and E. N. Olson. 2007. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316:575–579.
41. van Rooij, E., D. Quiat, B. A. Johnson, L. B. Sutherland, X. Qi, J. A. Richardson, et al. 2009. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell 17:662–673.
42. Russell, A. P., S. Lamon, H. Boon, S. Wada, I. Guller, E. L. Brown, et al. 2013. Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J. Physiol. 591:4637–4653.
43. Schuelke, M., K. R. Wagner, L. E. Stolz, C. Hubner, T. Riebel, W. Komen, et al. 2004. Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med. 350:2682–2688.
44. Shields, R. K., and S. Dudley-Javoroski. 2006. Musculoskeletal plasticity after acute spinal cord injury: effects of long-term neuromuscular electrical stimulation training. J. Neurophysiol. 95:2380–2390.
45. Small, E. M., J. R. O'Rourke, V. Moresi, L. B. Sutherland, J. McAnally, R. D. Gerard, et al. 2010. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc. Natl Acad. Sci. USA 107:4218–4223.
46. Snijders, T., B. T. Wall, M. L. Dirks, J. M. Senden, F. Hartgens, J. Dolmans, et al. 2014. Muscle disuse atrophy is not accompanied by changes in skeletal muscle satellite cell content. Clin. Sci. (Lond.) 126:557–566.
47. Spungen, A. M., R. H. Adkins, C. A. Stewart, J. Wang, R. N. Jr Pierson, R. L. Waters, et al. 2003. Factors influencing body composition in persons with spinal cord injury: a cross-sectional study. J. Appl. Physiol. 95:2398–2407.
48. Talmadge, R. J. 2000. Myosin heavy chain isoform expression following reduced neuromuscular activity: potential regulatory mechanisms. Muscle Nerve 23:661–679.
49. Verdijk, L. B., M. L. Dirks, T. Snijders, J. J. Prompers, M. Beelen, R. A. Jonkers, et al. 2012. Reduced satellite cell numbers with spinal cord injury and aging in humans. Med. Sci. Sports Exerc. 44:2322–2330.
50. Wada, S., Y. Kato, M. Okutsu, S. Miyaki, K. Suzuki, Z. Yan, et al. 2011. Translational suppression of atrophic regulators by microRNA-23a integrates resistance to skeletal muscle atrophy. J. Biol. Chem. 286:38456–38465.
51. Wahman, K., M. S. Nash, J. E. Lewis, A. Seiger, and R. Levi. 2010. Increased cardiovascular disease risk in Swedish persons with paraplegia: The Stockholm spinal cord injury study. J. Rehabil. Med. 42:489–492.
52. Wang, X. H. 2013. MicroRNA in myogenesis and muscle atrophy. Curr. Opin. Clin. Nutr. Metab. Care 16:258–266.
53. Wightman, B., I. Ha, and G. Ruvkun. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855–862.
54. Yan, B., C. D. Zhu, J. T. Guo, L. H. Zhao, and J. L. Zhao. 2013. miR-206 regulates the growth of the teleost tilapia (Oreochromis niloticus) through the modulation of IGF-1 gene expression. J. Exp. Biol. 216:1265–1269.
55. Zachwieja, J. J., S. R. Smith, I. Sinha-Hikim, N. Gonzalez-Cadavid, and S. Bhasin. 1999. Plasma myostatin-immunoreactive protein is increased after prolonged bed rest with low-dose T3 administration. J. Gravit. Physiol. 6:11–15.
56. Zierath, J. R., and J. A. Hawley. 2004. Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol. 2:e348.