MMP inhibition as a potential method to augment the healing of skeletal muscle and tendon extracellular matrix

Journal of Applied Physiology

Volumn 115, Issue 6, 2013, Pages 884-891

  Davis, Max E ^a   Gumucio, Jonathan P ^a   Sugg, Kristoffer B ^a   Bedi, Asheesh ^a   Mendias, Christopher L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Collagen; Extracellular matrix; MMP; Muscle injury; Tendinopathy; TIMP

Indexed keywords

COLLAGEN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; TISSUE INHIBITOR OF METALLOPROTEINASE;

ANIMAL; DRUG EFFECT; ENZYMOLOGY; EXTRACELLULAR MATRIX; HUMAN; INJURY; METABOLISM; MMP; MUSCLE INJURY; PHYSIOLOGY; REGENERATION; REVIEW; SKELETAL MUSCLE; TENDINITIS; TENDON; TENDON INJURY; WOUND HEALING;

COLLAGEN; EXTRACELLULAR MATRIX; MMP; MUSCLE INJURY; TENDINOPATHY; TIMP;

ANIMALS; COLLAGEN; EXTRACELLULAR MATRIX; HUMANS; MATRIX METALLOPROTEINASE INHIBITORS; MATRIX METALLOPROTEINASES; MUSCLE, SKELETAL; REGENERATION; TENDON INJURIES; TENDONS; TISSUE INHIBITOR OF METALLOPROTEINASES; WOUND HEALING;

EID: 84884248376     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00137.2013     Document Type: Review

References (89)

1. Alameddine HS. Matrix metalloproteinases in skeletal muscles: friends or foes? Neurobiol Dis 48: 508-518, 2012.
2. Almarza AJ, Augustine SM, Woo SL. Changes in gene expression of matrix constituents with respect to passage of ligament and tendon fibroblasts. Ann Biomed Eng 36: 1927-1933, 2008.
3. Andres BM, Murrell GAC. Treatment of tendinopathy: what works, what does not, and what is on the horizon. Clin Orthop Relat Res 466: 1539-1554, 2008.
4. Archambault J, Tsuzaki M, Herzog W, Banes AJ. Stretch and interleukin-1beta induce matrix metalloproteinases in rabbit tendon cells in vitro. J Orthop Res 20: 36-39, 2002.
5. Archambault JM, Jelinsky SA, Lake SP, Hill AA, Glaser DL, Soslowsky LJ. Rat supraspinatus tendon expresses cartilage markers with overuse. J Orthop Res 25: 617-624, 2007.
6. Bedi A, Fox AJS, Kovacevic D, Deng XH, Warren RF, Rodeo SA. Doxycycline-mediated inhibition of matrix metalloproteinases improves healing after rotator cuff repair. Am J Sports Med 38: 308-317, 2010.
7. Bedi A, Kovacevic D, Hettrich C, Gulotta LV, Ehteshami JR, Warren RF, Rodeo SA. The effect of matrix metalloproteinase inhibition on tendon-to-bone healing in a rotator cuff repair model. J Shoulder Elbow Surg 19: 384-391, 2010.
8. Benjamin M, Kumai T, Milz S, Boszczyk BM, Boszczyk AA, Ralphs JR. The skeletal attachment of tendons-tendon "entheses". Comp Biochem Physiol A Mol Integr Physiol 133: 931-945, 2002.
9. Bi Y, Ehirchiou D, Kilts TM, Inkson CA, Embree MC, Sonoyama W, Li L, Leet AI, Seo BM, Zhang L, Shi S, Young MF. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13: 1219-1227, 2007.
10. Bramono DS, Richmond JC, Weitzel PP, Kaplan DL, Altman GH. Matrix metalloproteinases and their clinical applications in orthopaedics. Clin Orthop Relat Res 428: 272-285, 2004.
11. Brinckmann J. Collagen-primer in structure, processing and assembly. Top Curr Chem 247: 1-229, 2005.
12. Calve S, Isaac J, Gumucio JP, Mendias CL. Hyaluronic acid, HAS1, and HAS2 are significantly upregulated during muscle hypertrophy. Am J Physiol Cell Physiol 303: C577-C588, 2012.
13. Canty EG, Lu Y, Meadows RS, Shaw MK, Holmes DF, Kadler KE. Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J Cell Biol 165: 553-563, 2004.
14. Cawston TE. Metalloproteinase inhibitors and the prevention of connective tissue breakdown. Pharmacol Ther 70: 163-182, 1996.
15. Chiquet M, Gelman L, Lutz R, Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim Biophys Acta 1793: 911-920, 2009.
16. Del Buono A, Oliva F, Longo UG, Rodeo SA, Orchard J, Denaro V, Maffulli N. Metalloproteases and rotator cuff disease. J Shoulder Elbow Surg 21: 200-208, 2012.
17. Deyl Z, Miksík I. Advanced separation methods for collagen parent alpha-chains, their polymers and fragments. J Chromatogr B Biomed Sci Appl 739: 3-31, 2000.
18. Drummond AH, Beckett P, Brown PD, Bone EA, Davidson AH, Galloway WA, Gearing AJ, Huxley P, Laber D, McCourt M, Whittaker M, Wood LM, Wright A. Preclinical and clinical studies of MMP inhibitors in cancer. Ann N Y Acad Sci 878: 228-235, 1999.
19. Eppley BL, Woodell JE, Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plast Reconstr Surg 114: 1502-1508, 2004.
20. Gladstone JN, Bishop JY, Lo IKY, Flatow EL. 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, 2007.
21. Gustafsson T. Vascular remodelling in human skeletal muscle. Biochem Soc Trans 39: 1628-1632, 2011.
22. Hatta T, Sano H, Sakamoto N, Kishimoto KN, Sato M, Itoi E. Nicotine reduced MMP-9 expression in the primary porcine tenocytes exposed to cyclic stretch. J Orthop Res 31: 645-650, 2013.
23. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551, 2001.
24. Heinemeier KM, Olesen JL, Haddad F, Langberg H, Kjaer M, Baldwin KM, Schjerling P. Expression of collagen and related growth factors in rat tendon and skeletal muscle in response to specific contraction types. J Physiol 582: 1303-1316, 2007.
25. Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M. Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb 14C. FASEB J 27: 2074-2079, 2013.
26. Izu Y, Ezura Y, Mizoguchi F, Kawamata A, Nakamoto T, Nakashima K, Hayata T, Hemmi H, Bonaldo P, Noda M. Type VI collagen deficiency induces osteopenia with distortion of osteoblastic cell morphology. Tissue Cell 44: 1-6, 2012.
27. Järvinen TAH, Järvinen TLN, Kääriäinen M, Kalimo H, Järvinen M. Muscle injuries: biology and treatment. Am J Sports Med 33: 745-764, 2005.
28. Józa LG, Kannus P. Human Tendons: Anatomy, Physiology, and Pathology. Champaign, IL: Human Kinetics, 1997, p. ix, 574.
29. Kalvegren H, Jonsson S, Jonasson L. Release of matrix metalloproteinases-1 and-2, but not-9, from activated platelets measured by enzymelinked immunosorbent assay. Platelets 22: 572-578, 2011.
30. Kardon G. Muscle and tendon morphogenesis in the avian hind limb. Development 125: 4019-4032, 1998.
31. Karousou E, Ronga M, Vigetti D, Passi A, Maffulli N. Collagens, proteoglycans, MMP-2, MMP-9 and TIMPs in human achilles tendon rupture. Clin Orthop Relat Res 466: 1577-1582, 2008.
32. Kherif S, Lafuma C, Dehaupas M, Lachkar S, Fournier JG, Verdière-Sahuqué M, Fardeau M, Alameddine HS. Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles. Dev Biol 205: 158-170, 1999.
33. Khoshnoodi J, Pedchenko V, Hudson BG. Mammalian collagen IV. Microsc Res Tech 71: 357-370, 2008.
34. Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84: 649-698, 2004.
35. Koskinen SO, Heinemeier KM, Olesen JL, Langberg H, Kjaer M. Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon-related connective tissue. J Appl Physiol 96: 861-864, 2004.
36. Lakemeier S, Schwuchow SA, Peterlein CD, Foelsch C, Fuchs-Winkelmann S, Archontidou-Aprin E, Paletta JR, Schofer MD. Expression of matrix metalloproteinases 1, 3, and 9 in degenerated long head biceps tendon in the presence of rotator cuff tears: an immunohistological study. BMC Musculoskelet Disord 11: 271, 2010.
37. LaStayo PC, Woolf JM, Lewek MD, Snyder-Mackler L, Reich T, Lindstedt SL. Eccentric muscle contractions: their contribution to injury, prevention, rehabilitation, and sport. J Orthop Sports Phys Ther 33: 557-571, 2003.
38. Listrat A, Picard B, Geay Y. Age-related changes and location of type I, III, IV, V and VI collagens during development of four foetal skeletal muscles of double-muscled and normal bovine animals. Tissue Cell 31: 17-27, 1999.
39. Lo IKY, Marchuk LL, Hollinshead R, Hart DA, Frank CB. Matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase mRNA levels are specifically altered in torn rotator cuff tendons. Am J Sports Med 32: 1223-1229, 2004.
40. MacIntosh BR, Gardiner PF, McComas AJ. Skeletal Muscle: Form and Function. Champaign, IL: Human Kinetics, 2006, p. viii, 423.
41. Mackey AL, Donnelly AE, Turpeenniemi-Hujanen T, Roper HP. Skeletal muscle collagen content in humans after high-force eccentric contractions. J Appl Physiol 97: 197-203, 2004.
42. Maeda T, Sakabe T, Sunaga A, Sakai K, Rivera AL, Keene DR, Sasaki T, Stavnezer E, Iannotti J, Schweitzer R, Ilic D, Baskaran H, Sakai T. Conversion of mechanical force into TGF-mediated biochemical signals. Curr Biol 21: 933-941, 2011.
43. Maffulli N, Almekinders L. (Editors) The Achilles Tendon. London: Springer, 2007.
44. Maffulli N, Renström P, Leadbetter WB. (Editors) Tendon Injuries: Basic Science and Clinical Medicine. London: Springer, 2005.
45. Marqueti RC, Marqueti RdC, Heinemeier KM, Durigan JLQ, de Andrade Perez SE, Schjerling P, Kjaer M, Carvalho HF, Selistre-de-Araujo HS. Gene expression in distinct regions of rat tendons in response to jump training combined with anabolic androgenic steroid administration. Eur J Appl Physiol 112: 1505-1515, 2012.
46. McCarrel TM, Minas T, Fortier LA. Optimization of leukocyte concentration in platelet-rich plasma for the treatment of tendinopathy. J Bone Joint Surg Am 94: e143(141-148), 2012.
47. Mendias CL, Bakhurin KI, Faulkner JA. Tendons of myostatin-deficient mice are small, brittle, and hypocellular. Proc Natl Acad Sci U S A 105: 388-393, 2008.
48. Mendias CL, Gumucio JP, Bakhurin KI, Lynch EB, Brooks SV. Physiological loading of tendons induces scleraxis expression in epitenon fibroblasts. J Orthop Res 30: 606-612, 2012.
49. Mendias CL, Gumucio JP, Davis ME, Bromley CW, Davis CS, Brooks SV. Transforming growth factor-beta induces skeletal muscle atrophy and fibrosis through the induction of atrogin-1 and scleraxis. Muscle Nerve 45: 55-59, 2012.
50. Mienaltowski MJ, Adams SM, Birk DE. Regional differences in stem cell/progenitor cell populations from the mouse achilles tendon. Tissue Eng Part A 19: 199-210, 2013.
51. Mishra A, Woodall J Jr, Vieira A. Treatment of tendon and muscle using platelet-rich plasma. Clin Sports Med 28: 113-125, 2009.
52. Molloy T, Wang Y, Murrell G. The roles of growth factors in tendon and ligament healing. Sports Med 33: 381-394, 2003.
53. Moore CS, Crocker SJ. An alternate perspective on the roles of TIMPs and MMPs in pathology. Am J Pathol 180: 12-16, 2012.
54. Mu X, Urso ML, Murray K, Fu F, Li Y. Relaxin regulates MMP expression and promotes satellite cell mobilization during muscle healing in both young and aged mice. Am J Pathol 177: 2399-2410, 2010.
55. Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, Schweitzer R. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 134: 2697-2708, 2007.
56. Murphy G. Tissue inhibitors of metalloproteinases. Genome Biol 12: 233, 2011.
57. Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138: 3625-3637, 2011.
58. Nadarajah VD, van Putten M, Chaouch A, Garrood P, Straub V, Lochmuller H, Ginjaar HB, Aartsma-Rus AM, van Ommen GJ, den Dunnen JT, and t'Hoen PA. Serum matrix metalloproteinase-9 (MMP-9) as a biomarker for monitoring disease progression in Duchenne muscular dystrophy (DMD). Neuromuscul Disord NMD 21: 569-578, 2011.
59. Nagase H, Woessner JF Jr. Matrix metalloproteinases. J Biol Chem 274: 21491-21494, 1999.
60. Neth P, Ries C, Karow M, Egea V, Ilmer M, Jochum M. The Wnt signal transduction pathway in stem cells and cancer cells: influence on cellular invasion. Stem Cell Rev 3: 18-29, 2007.
61. Nishimura T, Nakamura K, Kishioka Y, Kato-Mori Y, Wakamatsu J, Hattori A. Inhibition of matrix metalloproteinases suppresses the migration of skeletal muscle cells. J Muscle Res Cell Motil 29: 37-44, 2008.
62. Orchard J, Massey A, Brown R, Cardon-Dunbar A, Hofmann J. Successful management of tendinopathy with injections of the MMPinhibitor aprotinin. Clin Orthop Relat Res 466: 1625-1632, 2008.
63. Paoloni J, De Vos RJ, Hamilton B, Murrell GA, Orchard J. Plateletrich plasma treatment for ligament and tendon injuries. Clin J Sport Med 21: 37-45, 2011.
64. Park HB, Yang JH, Chung KH. Characterization of the cytokine profile of platelet rich plasma (PRP) and PRP-induced cell proliferation and migration: Upregulation of matrix metalloproteinase-1 and-9 in HaCaT cells. Korean J Hematol 46: 265-273, 2011.
65. Pasternak B, Aspenberg P. Metalloproteinases and their inhibitorsdiagnostic and therapeutic opportunities in orthopedics. Acta Orthop 80: 693-703, 2009.
66. Pryce BA, Brent AE, Murchison ND, Tabin CJ, Schweitzer R. Generation of transgenic tendon reporters, ScxGFP and ScxAP, using regulatory elements of the scleraxis gene. Dev Dyn 236: 1677-1682, 2007.
67. Purslow PP, Trotter JA. The morphology and mechanical properties of endomysium in series-fibred muscles: variations with muscle length. J Muscle Res Cell Motil 15: 299-308, 1994.
68. Ramaswamy KS, Palmer ML, van der Meulen JH, Renoux A, Kostrominova TY, Michele DE, Faulkner JA. Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats. J Physiol 589: 1195-1208, 2011.
69. Riley G. Tendinopathy-from basic science to treatment. Nat Clin Pract Rheumatol 4: 82-89, 2008.
70. Roach DM, Fitridge RA, Laws PE, Millard SH, Varelias A, Cowled PA. Up-regulation of MMP-2 and MMP-9 leads to degradation of type IV collagen during skeletal muscle reperfusion injury; protection by the MMP inhibitor, doxycycline. Eur J Vasc Endovasc Surg 23: 260-269, 2002.
71. Rowe RG, Keena D, Sabeh F, Willis AL, Weiss SJ. Pulmonary fibroblasts mobilize the membrane-tethered matrix metalloprotease, MT1-MMP, to destructively remodel and invade interstitial type I collagen barriers. Am J Physiol Lung Cell Mol Physiol 301: L683-L692, 2011.
72. Rullman E, Norrbom J, Stromberg A, Wagsater D, Rundqvist H, Haas T, Gustafsson T. Endurance exercise activates matrix metalloproteinases in human skeletal muscle. J Appl Physiol 106: 804-812, 2009.
73. Sabatelli P, Gualandi F, Gara SK, Grumati P, Zamparelli A, Martoni E, Pellegrini C, Merlini L, Ferlini A, Bonaldo P, Maraldi NM, Paulsson M, Squarzoni S, Wagener R. Expression of collagen VI 5 and 6 chains in human muscle and in Duchenne muscular dystrophy-related muscle fibrosis. Matrix Biol 31: 187-196, 2012.
74. Scott A, Sampaio A, Abraham T, Duronio C, Underhill TM. Scleraxis expression is coordinately regulated in a murine model of patellar tendon injury. J Orthop Res 29: 289-296, 2011.
75. Senga K, Kobayashi M, Hattori H, Yasue K, Mizutani H, Ueda M, Hoshino T. Type VI collagen in mouse masseter tendon, from osseous attachment to myotendinous junction. Anat Rec 243: 294-302, 1995.
76. Sheth U, Simunovic N, Klein G, Fu F, Einhorn TA, Schemitsch E, Ayeni OR, Bhandari M. Efficacy of autologous platelet-rich plasma use for orthopaedic indications: a meta-analysis. J Bone Joint Surg Am 94: 298-307, 2012.
77. Shin HS, Oh HY. The effect of platelet-rich plasma on wounds of OLETF rats using expression of matrix metalloproteinase-2 and-9 mRNA. Arch Plast Surg 39: 106-112, 2012.
78. Snoek-van Beurden PAM, Von den Hoff JW. Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors. Biotechniques 38: 73-83, 2005.
79. Sundman EA, Cole BJ, Fortier LA. Growth factor and catabolic cytokine concentrations are influenced by the cellular composition of plateletrich plasma. Am J Sports Med 39: 2135-2140, 2011.
80. Taylor DW, Petrera M, Hendry M, Theodoropoulos JS. A systematic review of the use of platelet-rich plasma in sports medicine as a new treatment for tendon and ligament injuries. Clin J Sport Med 21: 344-352, 2011.
81. Thampatty BP, Li H, Im HJ, Wang JH. EP4 receptor regulates collagen type-I, MMP-1, and MMP-3 gene expression in human tendon fibroblasts in response to IL-1 beta treatment. Gene 386: 154-161, 2007.
82. Tsukada S, Westwick JK, Ikejima K, Sato N, Rippe RA. SMAD and p38 MAPK signaling pathways independently regulate alpha1(I) collagen gene expression in unstimulated and transforming growth factor-betastimulated hepatic stellate cells. J Biol Chem 280: 10055-10064, 2005.
83. Wang B, Komers R, Carew R, Winbanks CE, Xu B, Herman-Edelstein M, Koh P, Thomas M, Jandeleit-Dahm K, Gregorevic P, Cooper ME, Kantharidis P. Suppression of microRNA-29 expression by TGFbeta1 promotes collagen expression and renal fibrosis. J Am Soc Nephrol 23: 252-265, 2012.
84. Wang JHC. Mechanobiology of tendon. J Biomech 39: 1563-1582, 2006.
85. Woessner JF. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93: 440-447, 1961.
86. Xu Y, Murrell GAC. The basic science of tendinopathy. Clin Orthop Relat Res 466: 1528-1538, 2008.
87. Yang G, Im HJ, Wang JH. Repetitive mechanical stretching modulates IL-1beta induced COX-2, MMP-1 expression, and PGE2 production in human patellar tendon fibroblasts. Gene 363: 166-172, 2005.
88. Zimowska M, Brzoska E, Swierczynska M, Streminska W, Moraczewski J. Distinct patterns of MMP-9 and MMP-2 activity in slow and fast twitch skeletal muscle regeneration in vivo. Int J Dev Biol 52: 307-314, 2008.
89. Zimowska M, Olszynski KH, Swierczynska M, Streminska W, Ciemerych MA. Decrease of MMP-9 activity improves soleus muscle regeneration. Tissue Eng 18: 1183-1192, 2012.