Rotator cuff tear reduces muscle fiber specific force production and induces macrophage accumulation and autophagy
dc.contributor.author | Gumucio, Jonathan P. | en_US |
dc.contributor.author | Davis, Max E. | en_US |
dc.contributor.author | Bradley, Joshua R. | en_US |
dc.contributor.author | Stafford, Patrick L. | en_US |
dc.contributor.author | Schiffman, Corey J. | en_US |
dc.contributor.author | Lynch, Evan B. | en_US |
dc.contributor.author | Claflin, Dennis R. | en_US |
dc.contributor.author | Bedi, Asheesh | en_US |
dc.contributor.author | Mendias, Christopher L. | en_US |
dc.date.accessioned | 2012-11-07T17:04:34Z | |
dc.date.available | 2014-02-03T16:21:43Z | en_US |
dc.date.issued | 2012-12 | en_US |
dc.identifier.citation | Gumucio, Jonathan P.; Davis, Max E.; Bradley, Joshua R.; Stafford, Patrick L.; Schiffman, Corey J.; Lynch, Evan B.; Claflin, Dennis R.; Bedi, Asheesh; Mendias, Christopher L. (2012). "Rotator cuff tear reduces muscle fiber specific force production and induces macrophage accumulation and autophagy." Journal of Orthopaedic Research 30(12): 1963-1970. <http://hdl.handle.net/2027.42/94259> | en_US |
dc.identifier.issn | 0736-0266 | en_US |
dc.identifier.issn | 1554-527X | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/94259 | |
dc.description.abstract | Full‐thickness tears to the rotator cuff can cause severe pain and disability. Untreated tears progress in size and are associated with muscle atrophy and an infiltration of fat to the area, a condition known as “fatty degeneration.” To improve the treatment of rotator cuff tears, a greater understanding of the changes in the contractile properties of muscle fibers and the molecular regulation of fatty degeneration is essential. Using a rat model of rotator cuff injury, we measured the force generating capacity of individual muscle fibers and determined changes in muscle fiber type distribution that develop after a full thickness rotator cuff tear. We also measured the expression of mRNA and miRNA transcripts involved in muscle atrophy, lipid accumulation, and matrix synthesis. We hypothesized that a decrease in specific force of rotator cuff muscle fibers, an accumulation of type IIb fibers, and an upregulation in fibrogenic, adipogenic, and inflammatory gene expression occur in torn rotator cuff muscles. Thirty days following rotator cuff tear, we observed a reduction in muscle fiber force production, an induction of fibrogenic, adipogenic, and autophagocytic mRNA and miRNA molecules, and a dramatic accumulation of macrophages in areas of fat accumulation. © 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 30:1963–1970, 2012 | en_US |
dc.publisher | Wiley Subscription Services, Inc., A Wiley Company | en_US |
dc.subject.other | Rotator Cuff | en_US |
dc.subject.other | Autophagy | en_US |
dc.subject.other | Fatty Degeneration | en_US |
dc.subject.other | Muscle Fiber Contractility | en_US |
dc.title | Rotator cuff tear reduces muscle fiber specific force production and induces macrophage accumulation and autophagy | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Department of Orthopaedic Surgery, University of Michigan Medical School, 109 Zina Pitcher Place, BSRB 2017, Ann Arbor, Michigan 48109‐2200 | en_US |
dc.contributor.affiliationum | Department of Orthopaedic Surgery, University of Michigan Medical School, 109 Zina Pitcher Place, BSRB 2017, Ann Arbor, Michigan 48109‐2200. T: 734‐764‐3250; F: 734‐647‐0003 | en_US |
dc.contributor.affiliationum | Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan | en_US |
dc.contributor.affiliationum | Department of Surgery, Section of Plastic Surgery, University of Michigan, Ann Arbor, Michigan | en_US |
dc.contributor.affiliationum | Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, Michigan | en_US |
dc.identifier.pmid | 22696414 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/94259/1/22168_ftp.pdf | |
dc.identifier.doi | 10.1002/jor.22168 | en_US |
dc.identifier.source | Journal of Orthopaedic Research | en_US |
dc.identifier.citedreference | van Rooij E, Sutherland LB, Thatcher JE, et al. 2008. Dysregulation of microRNAs after myocardial infarction reveals a role of miR‐29 in cardiac fibrosis. Proc Natl Acad Sci USA 105: 13027 – 13032. | en_US |
dc.identifier.citedreference | Docheva D, Hunziker EB, Fässler R, et al. 2005. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol 25: 699 – 705. | en_US |
dc.identifier.citedreference | Maeda T, Sakabe T, Sunaga A, et al. 2011. Conversion of mechanical force into TGF‐β‐mediated biochemical signals. Curr Biol 21: 933 – 941. | en_US |
dc.identifier.citedreference | Mendias CL, Bakhurin KI, Faulkner JA. 2008. Tendons of myostatin‐deficient mice are small, brittle, and hypocellular. Proc Natl Acad Sci USA 105: 388 – 393. | en_US |
dc.identifier.citedreference | Murchison ND, Price BA, Conner DA, et al. 2007. Regulation of tendon differentiation by scleraxis distinguishes force‐transmitting tendons from muscle‐anchoring tendons. Development 134: 2697 – 2708. | en_US |
dc.identifier.citedreference | Gulotta LV, Kovacevic D, Packer JD, et al. 2011. Bone marrow‐derived mesenchymal stem cells transduced with scleraxis improve rotator cuff healing in a rat model. Am J Sports Med 39: 1282 – 1289. | en_US |
dc.identifier.citedreference | Joe AWB, Yi L, Natarajan A, et al. 2010. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12: 153 – 163. | en_US |
dc.identifier.citedreference | Kwiecinski M, Noetel A, Elfimova N, et al. 2011. Hepatocyte growth factor (HGF) inhibits collagen I and IV synthesis in hepatic stellate cells by miRNA‐29 induction. PLoS ONE 6: e24568. | en_US |
dc.identifier.citedreference | Thum T, Catalucci D, Bauersachs J. 2008. MicroRNAs: novel regulators in cardiac development and disease. Cardiovasc Res 79: 562 – 570. | en_US |
dc.identifier.citedreference | Itoigawa Y, Kishimoto KN, Sano H, et al. 2011. Molecular mechanism of fatty degeneration in rotator cuff muscle with tendon rupture. J Orthop Res 29: 861 – 866. | en_US |
dc.identifier.citedreference | Wang Y‐X. 2010. PPARs: diverse regulators in energy metabolism and metabolic diseases. Cell Res 20: 124 – 137. | en_US |
dc.identifier.citedreference | Buers I, Hofnagel O, Ruebel A, et al. 2011. Lipid droplet associated proteins: an emerging role in atherogenesis. Histol Histopathol 26: 631 – 642. | en_US |
dc.identifier.citedreference | Friedman AD, Keefer JR, Kummalue T, et al. 2003. Regulation of granulocyte and monocyte differentiation by CCAAT/enhancer binding protein alpha. Blood Cells Mol Dis 31: 338 – 341. | en_US |
dc.identifier.citedreference | Olefsky JM, Glass CK. 2010. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72: 219 – 246. | en_US |
dc.identifier.citedreference | Phillips SA, Choe CC, Ciaraldi TP, et al. 2005. Adipocyte differentiation‐related protein in human skeletal muscle: relationship to insulin sensitivity. Obes Res 13: 1321 – 1329. | en_US |
dc.identifier.citedreference | Trajkovski M, Hausser J, Soutschek J, et al. 2011. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474: 649 – 653. | en_US |
dc.identifier.citedreference | Lee EK, Lee MJ, Abdelmohsen K, et al. 2011. miR‐130 suppresses adipogenesis by inhibiting peroxisome proliferator‐activated receptor gamma expression. Mol Cell Biol 31: 626 – 638. | en_US |
dc.identifier.citedreference | Yang Z, Bian C, Zhou H, et al. 2011. MicroRNA hsa‐miR‐138 inhibits adipogenic differentiation of human adipose tissue‐derived mesenchymal stem cells through adenovirus EID‐1. Stem cell Dev 20: 259 – 267. | en_US |
dc.identifier.citedreference | Xie H, Lim B, Lodish HF. 2009. MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 58: 1050 – 1057. | en_US |
dc.identifier.citedreference | Li H, Zhang Z, Zhou X, et al. 2010. Effects of MicroRNA‐143 in the differentiation and proliferation of bovine intramuscular preadipocytes. Mol Biol Rep 38: 4273 – 4280. | en_US |
dc.identifier.citedreference | Kim SY, Kim AY, Lee HW, et al. 2010. miR‐27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun 392: 323 – 328. | en_US |
dc.identifier.citedreference | Inoue T, Plieth D, Venkov CD, et al. 2005. Antibodies against macrophages that overlap in specificity with fibroblasts. Kidney Int 67: 2488 – 2493. | en_US |
dc.identifier.citedreference | Li H, Song Y, Li F, et al. 2010. Identification of lipid droplet‐associated proteins in the formation of macrophage‐derived foam cells using microarrays. Int J Mol Med 26: 231 – 239. | en_US |
dc.identifier.citedreference | Yonezawa T, Kurata R, Kimura M, et al. 2011. Which CIDE are you on? Apoptosis and energy metabolism. Mol Biosyst 7: 91 – 100. | en_US |
dc.identifier.citedreference | Tontonoz P, Nagy L, Alvarez JG, et al. 1998. PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93: 241 – 252. | en_US |
dc.identifier.citedreference | Funderburk SF, Wang QJ, Yue Z. 2010. The Beclin 1–VPS34 complex – at the crossroads of autophagy and beyond. Trends Cell Biol 20: 355 – 362. | en_US |
dc.identifier.citedreference | Martinet W, De Meyer GRY. 2009. Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res 104: 304 – 317. | en_US |
dc.identifier.citedreference | Bottinelli R, Canepari M, Pellegrino MA, et al. 1996. Force‐velocity properties of human skeletal muscle fibres: myosin heavy chain isoform and temperature dependence. J Physiol 495: 573 – 586. | en_US |
dc.identifier.citedreference | Gerber C, Fuchs B, Hodler J. 2000. The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am 82: 505 – 515. | en_US |
dc.identifier.citedreference | Nishimura T. 2010. The role of intramuscular connective tissue in meat texture. Anim Sci J 81: 21 – 27. | en_US |
dc.identifier.citedreference | Bedi A, Dines J, Warren RF, et al. 2010. Massive tears of the rotator cuff. J Bone Joint Surg Am 92: 1894 – 1908. | en_US |
dc.identifier.citedreference | Walsworth MK, Doukas WC, Murphy KP, et al. 2009. Descriptive analysis of patients undergoing shoulder surgery at a tertiary care military medical center. Mil Med 174: 642 – 644. | en_US |
dc.identifier.citedreference | Goutallier D, Postel JM, Bernageau J, et al. 1994. Fatty muscle degeneration in cuff ruptures. Pre‐ and postoperative evaluation by CT scan. Clin Orthop Relat Res 304: 78 – 83. | en_US |
dc.identifier.citedreference | Gladstone JN, Bishop JY, Lo IKY, et al. 2007. Fatty infiltration and atrophy of the rotator cuff do not improve after rotator cuff repair and correlate with poor functional outcome. Am J Sports Med 35: 719 – 728. | en_US |
dc.identifier.citedreference | Rokito AS, Zuckerman JD, Gallagher MA, et al. 1996. Strength after surgical repair of the rotator cuff. J Shoulder Elbow Surg 5: 12 – 17. | en_US |
dc.identifier.citedreference | Hawke TJ, Garry DJ. 2001. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534 – 551. | en_US |
dc.identifier.citedreference | Das R, Rich J, Kim HM, et al. 2010. Effects of botulinum toxin‐induced paralysis on postnatal development of the supraspinatus muscle. J Orthop Res 29: 281 – 288. | en_US |
dc.identifier.citedreference | Frey E, Regenfelder F, Sussmann P, et al. 2009. Adipogenic and myogenic gene expression in rotator cuff muscle of the sheep after tendon tear. J Orthop Res 27: 504 – 509. | en_US |
dc.identifier.citedreference | Kim HM, Galatz LM, Lim C, et al. 2011. The effect of tear size and nerve injury on rotator cuff muscle fatty degeneration in a rodent animal model. J Shoulder Elbow Surg (in press). | en_US |
dc.identifier.citedreference | Meyer DC, Hoppeler H, von Rechenberg B, et al. 2004. A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthop Res 22: 1004 – 1007. | en_US |
dc.identifier.citedreference | Smith C, Kruger MJ, Smith RM, et al. 2008. The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med 38: 947 – 969. | en_US |
dc.identifier.citedreference | Terman A, Gustafsson B, Brunk UT. 2007. Autophagy, organelles and ageing. J Pathol 211: 134 – 143. | en_US |
dc.identifier.citedreference | Sandri M. 2011. New findings of lysosomal proteolysis in skeletal muscle. Curr Opin Clin Nutr Metab Care 14: 223 – 229. | en_US |
dc.identifier.citedreference | Brennecke J, Stark A, Russell RB, et al. 2005. Principles of microRNA‐target recognition. PLoS Biol 3: e85. | en_US |
dc.identifier.citedreference | McCarthy JJ. 2011. The MyomiR network in skeletal muscle plasticity. Exerc Sport Sci Rev 39: 150 – 154. | en_US |
dc.identifier.citedreference | McGregor RA, Choi MS. 2011. MicroRNAs in the regulation of adipogenesis and obesity. Curr Mol Med 11: 304 – 316. | en_US |
dc.identifier.citedreference | Bauersachs J. 2010. Regulation of myocardial fibrosis by MicroRNAs. J Cardiovasc Pharmacol 56: 454 – 459. | en_US |
dc.identifier.citedreference | Soslowsky LJ, Carpenter JE, DeBano CM, et al. 1996. Development and use of an animal model for investigations on rotator cuff disease. J Shoulder Elbow Surg 5: 383 – 392. | en_US |
dc.identifier.citedreference | Liu X, Manzano G, Kim HT, et al. 2011. A rat model of massive rotator cuff tears. J Orthop Res 29: 588 – 595. | en_US |
dc.identifier.citedreference | Bedi A, Fox AJS, Harris PE, et al. 2010. Diabetes mellitus impairs tendon‐bone healing after rotator cuff repair. J Shoulder Elbow Surg 19: 978 – 988. | en_US |
dc.identifier.citedreference | Mendias CL, Kayupov E, Bradley JR, et al. 2011. Decreased specific force and power production of muscle fibers from myostatin‐deficient mice are associated with a suppression of protein degradation. J Appl Physiol 111: 185 – 191. | en_US |
dc.identifier.citedreference | Panchangam A, Claflin DR, Palmer ML, et al. 2008. Magnitude of sarcomere extension correlates with initial sarcomere length during lengthening of activated single fibers from soleus muscle of rats. Biophys J 95: 1890 – 1901. | en_US |
dc.identifier.citedreference | Claflin DR, Larkin LM, Cederna PS, et al. 2011. Effects of high‐ and low‐velocity resistance training on the contractile properties of skeletal muscle fibers from young and older humans. J Appl Physiol 111: 1021 – 1030. | en_US |
dc.identifier.citedreference | Schmittgen TD, Livak KJ. 2008. Analyzing real‐time PCR data by the comparative C(T) method. Nat Protoc 3: 1101 – 1108. | en_US |
dc.identifier.citedreference | Mannava S, Plate JF, Whitlock PW, et al. 2011. Evaluation of in vivo rotator cuff muscle function after acute and chronic detachment of the supraspinatus tendon: an experimental study in an animal model. J Bone Joint Surg Am 93: 1702 – 1711. | en_US |
dc.identifier.citedreference | Meyer DC, Gerber C, von Rechenberg B, et al. 2011. Amplitude and strength of muscle contraction are reduced in experimental tears of the rotator cuff. Am J Sports Med 39: 1456 – 1461. | en_US |
dc.identifier.citedreference | Ward SR, Sarver JJ, Eng CM, et al. 2010. Plasticity of muscle architecture after supraspinatus tears. J Orthop Sports Phys Ther 40: 729 – 735. | en_US |
dc.identifier.citedreference | Schiaffino S, Reggiani C. 1996. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76: 371 – 423. | en_US |
dc.identifier.citedreference | Eisenberg I, Alexander MS, Kunkel LM. 2009. miRNAS in normal and diseased skeletal muscle. J Cell Mol Med 13: 2 – 11. | en_US |
dc.identifier.citedreference | Sandri M. 2008. Signaling in muscle atrophy and hypertrophy. Physiology 23: 160 – 170. | en_US |
dc.identifier.citedreference | Lang CH, Huber D, Frost RA. 2007. Burn‐induced increase in atrogin‐1 and MuRF‐1 in skeletal muscle is glucocorticoid independent but downregulated by IGF‐I. Am J Physiol Regul Integr Comp Physiol 292: R328 – R336. | en_US |
dc.identifier.citedreference | Schmutz S, Fuchs T, Regenfelder F, et al. 2009. Expression of atrophy mRNA relates to tendon tear size in supraspinatus muscle. Clin Orthop Relat Res 467: 457 – 464. | en_US |
dc.identifier.citedreference | Wada S, Kato Y, Okutsu M, et al. 2011. Translational suppression of atrophic regulators by miR‐23a integrates resistance to skeletal muscle atrophy. J Biol Chem 44: 38456 – 38465. | en_US |
dc.identifier.citedreference | Villalta SA, Rinaldi C, Deng B, et al. 2011. Interleukin‐10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype. Hum Mol Genet 20: 790 – 805. | en_US |
dc.identifier.citedreference | Barton ER, Gimbel JA, Williams GR, et al. 2005. Rat supraspinatus muscle atrophy after tendon detachment. J Orthop Res 23: 259 – 265. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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