miR-23a is decreased during muscle atrophy by a mechanism that includes calcineurin signaling and exosome-mediated export

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 6, 2014, Pages

  Hudson, Matthew B ^a   Woodworth Hobbs, Myra E ^b   Zheng, Bin ^a   Rahnert, Jill A ^a   Blount, Mitsi A ^a   Gooch, Jennifer L ^a,c   Searles, Charles D ^a,c   Russ Price, S ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Atrophy; Calcineurin; Gene expression; Glucocorticoids; microRNA; Skeletal muscle

Indexed keywords

ATROGIN 1; CALCINEURIN; DEXAMETHASONE; MESSENGER RNA; MICRORNA; MICRORNA 23A; MUSCLE RING FINGER 1 PROTEIN; UNCLASSIFIED DRUG; DSCR1 PROTEIN, MOUSE; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GLUCOCORTICOID; MIRN23B MICRORNA, MOUSE; MUSCLE PROTEIN; SIGNAL PEPTIDE; STREPTOZOCIN; TRANSCRIPTION FACTOR NF AT C3; TRANSCRIPTION FACTOR NF-AT C3; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVE SITE; EXOSOME; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; INTRACELLULAR TRANSPORT; MALE; MOUSE; MUSCLE ATROPHY; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TRANSCRIPTION REGULATION; WILD TYPE; ANIMAL; ATROPHY; BIOSYNTHESIS; CELL CULTURE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

ATROPHY; CALCINEURIN; GENE EXPRESSION; GLUCOCORTICOIDS; MICRORNA; SKELETAL MUSCLE;

ANIMALS; BIOLOGICAL TRANSPORT; CALCINEURIN; CELLS, CULTURED; DEXAMETHASONE; DIABETES MELLITUS, EXPERIMENTAL; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR ATROPHY; NFATC TRANSCRIPTION FACTORS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; STREPTOZOCIN;

EID: 84899998574     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00266.2013     Document Type: Article

References (50)

1. Allen DL, Loh AS. Posttranscriptional mechanisms involving microRNA-27a and b contribute to fast-specific and glucocorticoid-mediated myostatin expression in skeletal muscle. Am J Physiol Cell Physiol 300: C124-C137, 2011.
2. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, function. Cell 116: 281-297, 2004.
3. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
4. Bueno OF, Wilkins BJ, Tymitz KM, Glascock BJ, Kimball TF, Lorenz JN, Molkentin JD. Impaired cardiac hypertrophic response in calcineurin Aβ-deficient mice. Proc Natl Acad Sci USA 99: 4586-4591, 2002.
5. Chen GQ, Lu KR, Yang YQ, Wang S, Bie MJ. [Effects of oxidative stress on MuRF1 expression in skeletal muscle of diabetic rats]. Sichuan Da Xue Xue Bao Yi Xue Ban 42: 349-352, 2011.
6. Crist CG, Buckingham M. Megarole for microRNA in muscle disease. Cell Metab 12: 425-426, 2010.
7. Davies KJ, Ermak G, Rothermel BA, Pritchard M, Heitman J, Ahnn J, Henrique-Silva F, Crawford D, Canaider S, Strippoli P, Carinci P, Min KT, Fox DS, Cunningham KW, Bassel-Duby R, Olson EN, Zhang Z, Williams RS, Gerber HP, Perez-Riba M, Seo H, Cao X, Klee CB, Redondo JM, Maltais LJ, Bruford EA, Povey S, Molkentin JD, McKeon FD, Duh EJ, Crabtree GR, Cyert MS, de la Luna S, Estivill X. Renaming the DSCR1/Adapt78 gene family as RCAN: regulators of calcineurin. FASEB J 21: 3023-3028, 2007.
8. Dehoux M, Van Beneden R, Pasko N, Lause P, Verniers J, Underwood L, Ketelslegers JM, Thissen JP. Role of the insulin-like growth factor I decline in the induction of atrogin-1/MAFbx during fasting and diabetes. Endocrinology 145: 4806-4812, 2004.
9. Friday BB, Pavlath GK. A calcineurin-and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cells. J Cell Sci 114: 303-310, 2001.
10. Fry CS. Tiny transporters: how exosomes and calcineurin signaling regulate miR-23a levels during muscle atrophy. Focus on "miR-23a is decreased during muscle atrophy by a mechanism that includes calcineurin signaling and exosome-mediated export. " Am J Physiol Cell Physiol (22 January 2014). doi:10.1152/ajpcell.00022.2014.
11. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98: 14440-14445, 2001.
12. Guescini M, Guidolin D, Vallorani L, Casadei L, Gioacchini AM, Tibollo P, Battistelli M, Falcieri E, Battistin L, Agnati LF, Stocchi V. C2C12 myoblasts release micro-vesicles containing mtDNA and proteins involved in signal transduction. Exp Cell Res 316: 1977-1984, 2010.
13. Hudson MB, Price SR. Calcineurin: a poorly understood regulator of muscle mass. Int J Biochem Cell Biol 45: 2173-2178, 2013.
14. Hudson MB, Smuder AJ, Nelson WB, Bruells CS, Levine S, Powers SK. Both high level pressure support ventilation and controlled mechanical ventilation induce diaphragm dysfunction and atrophy. Crit Care Med 40: 1254-1260, 2012.
15. Jabr RI, Wilson AJ, Riddervold MH, Jenkins AH, Perrino BA, Clapp LH. Nuclear translocation of calcineurin Aβ but not calcineurin Aα by platelet-derived growth factor in rat aortic smooth muscle. Am J Physiol Cell Physiol 292: C2213-C2225, 2007.
16. Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287: C834-C843, 2004.
17. Jansen F, Yang X, Hoyer FF, Paul K, Heiermann N, Becher MU, Abu Hussein N, Kebschull M, Bedorf J, Franklin BS, Latz E, Nickenig G, Werner N. Endothelial microparticle uptake in target cells is annexin I/phosphatidylserine receptor dependent and prevents apoptosis. Arterioscler Thromb Vasc Biol 32: 1925-1935, 2012.
18. Jansen KM, Pavlath GK. Mannose receptor regulates myoblast motility and muscle growth. J Cell Biol 174: 403-413, 2006.
19. Kukreti H, Amuthavalli K, Harikumar A, Sathiyamoorthy S, Feng PZ, Anantharaj R, Tan SL, Lokireddy S, Bonala S, Sriram S, Mc-Farlane C, Kambadur R, Sharma M. Muscle-specific microRNA1 (miR1) targets heat shock protein 70 (HSP70) during dexamethasone mediated atrophy. J Biol Chem 288: 6663-6678, 2013.
20. Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17: 1807-1819, 2006.
21. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18: 39-51, 2004.
22. Lee S, Vasudevan S. Post-transcriptional stimulation of gene expression by microRNAs. Adv Exp Med Biol 768: 97-126, 2013.
23. Li HH, Kedar V, Zhang C, McDonough H, Arya R, Wang DZ, Patterson C. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J Clin Invest 114: 1058-1071, 2004.
24. Li HH, Willis MS, Lockyer P, Miller N, McDonough H, Glass DJ, Patterson C. Atrogin-1 inhibits Akt-dependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of forkhead proteins. J Clin Invest 117: 3211-3223, 2007.
25. Lin Z, Murtaza I, Wang K, Jiao J, Gao J, Li PF. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci USA 106: 12103-12108, 2009.
26. McClung JM, Judge AR, Powers SK, Yan Z. p38 MAPK links oxidative stress to autophagy-related gene expression in cachectic muscle wasting. Am J Physiol Cell Physiol 298: C542-C549, 2010.
27. Mitch WE, Bailey JL, Wang X, Jurkovitz C, Newby D, Price SR. Evaluation of signals activating ubiquitin-proteasome proteolysis in a model of muscle wasting. Am J Physiol Cell Physiol 276: C1132-C1138, 1999.
28. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105: 10513-10518, 2008.
29. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, Milosevic J, Tkacheva OA, Divito SJ, Jordan R, Lyons-Weiler J, Watkins SC, Morelli AE. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119: 756-766, 2012.
30. Powers SK, Smuder AJ, Judge AR. Oxidative stress and disuse muscle atrophy: cause or consequence? Curr Opin Clin Nutr Metab Care 15: 240-245, 2012.
31. Price SR, Bailey JL, Wang X, Jurkovitz C, England BK, Ding X, Phillips LS, Mitch WE. Muscle wasting in insulinopenic rats results from activation of the ATP-dependent, ubiquitin-proteasome proteolytic pathway by a mechanism including gene transcription. J Clin Invest 98: 1703-1708, 1996.
32. Price SR, Gooch JL, Donaldson SK, Roberts-Wilson TK. Muscle atrophy in chronic kidney disease results from abnormalities in insulin signaling. J Ren Nutr 20: S24-S28, 2010.
33. Qiu S, Huang D, Yin D, Li F, Li X, Kung HF, Peng Y. Suppression of tumorigenicity by microRNA-138 through inhibition of EZH2-CDK4/6-pRb-E2F1 signal loop in glioblastoma multiforme. Biochim Biophys Acta 1832: 1697-1707, 2013.
34. Reddy RN, Knotts TL, Roberts BR, Molkentin JD, Price SR, Gooch JL. Calcineurin Aβ is required for hypertrophy but not matrix expansion in the diabetic kidney. J Cell Mol Med 15: 414-422, 2011.
35. Roberts-Wilson TK, Reddy RN, Bailey JL, Zheng B, Ordas R, Gooch JL, Price SR. Calcineurin signaling and PGC-1α expression are suppressed during muscle atrophy due to diabetes. Biochim Biophys Acta 1803: 960-967, 2010.
36. Russell AP, Lamon S, Boon H, Wada S, Guller I, Brown EL, Chibalin AV, Zierath JR, Snow RJ, Stepto N, Wadley GD, Akimoto T. Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J Physiol 591: 4637-4653, 2013.
37. Russell AP, Wada S, Vergani L, Hock MB, Lamon S, Leger B, Ushida T, Cartoni R, Wadley GD, Hespel P, Kralli A, Soraru G, Angelini C, Akimoto T. Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis. Neurobiol Dis 49C: 107-117, 2012.
38. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140-155, 2007.
39. Shao R, Shi Z, Gotwals PJ, Koteliansky VE, George J, Rockey DC. Cell and molecular regulation of endothelin-1 production during hepatic wound healing. Mol Biol Cell 14: 2327-2341, 2003.
40. Sharkey JW, Antoine DJ, Park BK. Validation of the isolation and quantification of kidney enriched miRNAs for use as biomarkers. Biomarkers 17: 231-239, 2012.
41. Shen H, Liu T, Fu L, Zhao S, Fan B, Cao J, Li X. Identification of microRNAs involved in dexamethasone-induced muscle atrophy. Mol Cell Biochem 381: 105-113, 2013.
42. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593, 2009.
43. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659, 2007.
44. Wada S, Kato Y, Okutsu M, Miyaki S, Suzuki K, Yan Z, Schiaffino S, Asahara H, Ushida T, Akimoto T. Translational suppression of atrophic regulators by microRNA-23a integrates resistance to skeletal muscle atrophy. J Biol Chem 286: 38456-38465, 2011.
45. Wang XH, Hu Z, Klein JD, Zhang L, Fang F, Mitch WE. Decreased miR-29 suppresses myogenesis in CKD. J Am Soc Nephrol 22: 2068-2076, 2011.
46. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94: 110-118, 2004.
47. Yates LA, Norbury CJ, Gilbert RJ. The long and short of microRNA. Cell 153: 516-519, 2013.
48. Ying SY, Chang DC, Lin SL. The microRNA. Methods Mol Biol 936: 1-19, 2013.
49. Zhang BW, Zimmer G, Chen J, Ladd D, Li E, Alt FW, Wiederrecht G, Cryan J, O'Neill EA, Seidman CE, Abbas AK, Seidman JG. T cell responses in calcineurin Aα-deficient mice. J Exp Med 183: 413-420, 1996.
50. Zheng B, Ohkawa S, Li H, Roberts-Wilson TK, Price SR. FOXO3a mediates signaling crosstalk that coordinates ubiquitin and atrogin-1/ MAFbx expression during glucocorticoid-induced skeletal muscle atrophy. FASEB J 24: 2660-2669, 2010.