Use of an antifibrotic agent improves the effect of platelet-rich plasma on muscle healing after injury

Journal of Bone and Joint Surgery

Volumn 95, Issue 11, 2013, Pages 980-988

  Terada, Satoshi ^a   Ota, Shusuke ^a   Kobayashi, Makoto ^a   Kobayashi, Tetsuo ^a   Mifune, Yutaka ^a   Takayama, Koji ^a   Witt, Michelle ^a   Vadalà, Gianluca ^b   Oyster, Nick ^a   Otsuka, Takanobu ^c   Fu, Freddie H ^d   Huard, Johnny ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^c NAGOYA CITY UNIVERSITY   (Japan)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; LOSARTAN; LOSARTAN POTASSIUM; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN; ANGIOTENSIN 1 RECEPTOR ANTAGONIST;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CONVALESCENCE; FEMALE; HEALING; MOUSE; MUSCLE CONTUSION; MUSCLE FUNCTION; MUSCLE GROWTH; MUSCLE HEALING; MUSCLE INJURY; MUSCLE REGENERATION; MUSCLE STRENGTH; MYOFIBROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTE COUNT; THROMBOCYTE RICH PLASMA; TIBIALIS ANTERIOR MUSCLE; ANIMAL; C57BL MOUSE; CONTUSION; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; INJURY; METABOLISM; PATHOLOGY; REGENERATION; SKELETAL MUSCLE; WOUND HEALING;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; CONTUSIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; LOSARTAN; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; PLATELET-RICH PLASMA; REGENERATION; TRANSFORMING GROWTH FACTOR BETA1; WOUND HEALING;

EID: 84883185489     PISSN: 00219355     EISSN: 15351386     Source Type: Journal    
DOI: 10.2106/JBJS.L.00266     Document Type: Article

References (53)

1. Andia I, Sánchez M, Maffulli N. Platelet rich plasma therapies for sports muscle injuries: any evidence behind clinical practice? Expert Opin Biol Ther. 2011 Apr;11(4):509-18.
2. Foster TE, Puskas BL, Mandelbaum BR, Gerhardt MB, Rodeo SA. Platelet-rich plasma: from basic science to clinical applications. Am J Sports Med. 2009 Nov; 37(11):2259-72.
3. Hammond JW, Hinton RY, Curl LA, Muriel JM, Lovering RM. Use of autologous platelet-rich plasma to treat muscle strain injuries. Am J Sports Med. 2009 Jun;37(6):1135-42.
4. Ranzato E, Balbo V, Boccafoschi F, Mazzucco L, Burlando B. Scratch wound closure of C2C12 mouse myoblasts is enhanced by human platelet lysate. Cell Biol Int. 2009 Sep;33(9):911-7.
5. Anitua E, Sanchez M, Merayo-Lloves J, De la Fuente M, Muruzabal F, Orive G. Plasma rich in growth factors (PRGF-Endoret) stimulates proliferation and migration of primary keratocytes and conjunctival fibroblasts and inhibits and reverts TGF-beta1-induced myodifferentiation. Invest Ophthalmol Vis Sci. 2011 Aug;52(9): 6066-73.
6. Bir SC, Esaki J, Marui A, Yamahara K, Tsubota H, Ikeda T, Sakata R. Angiogenic properties of sustained release platelet-rich plasma: characterization in-vitro and in the ischemic hind limb of the mouse. J Vasc Surg. 2009 Oct;50(4):870-9: e2.
7. Kim ES, Kim JJ, Park EJ. Angiogenic factor-enriched platelet-rich plasma enhances in vivo bone formation around alloplastic graft material. J Adv Prosthodont. 2010 Mar;2(1):7-13.
8. Milano G, Sanna Passino E, Deriu L, Careddu G, Manunta L, Manunta A, Saccomanno MF, Fabbriciani C. The effect of platelet rich plasma combined with microfractures on the treatment of chondral defects: an experimental study in a sheep model. Osteoarthritis Cartilage. 2010 Jul;18(7):971-80.
9. Nagata M, Messora M, Okamoto R, Campos N, Pola N, Esper L, Sbrana M, Fucini S, Garcia V, Bosco A. Influence of the proportion of particulate autogenous bone graft/platelet-rich plasma on bone healing in critical-size defects: an immunohistochemical analysis in rat calvaria. Bone. 2009 Aug;45(2):339-45.
10. Nishimori M, Matsumoto T, Ota S, Kopf S, Mifune Y, Harner C, Ochi M, Fu FH, Huard J. Role of angiogenesis after muscle derived stem cell transplantation in injured medial collateral ligament. J Orthop Res. 2012 Apr;30(4):627-33.
11. Beye JA, Hart DA, Bray RC, McDougall JJ, Salo PT. Injury-induced changes in mRNA levels differ widely between anterior cruciate ligament and medial collateral ligament. Am J Sports Med. 2008 Jul;36(7):1337-46.
12. Hildebrand KA, Frank CB. Scar formation and ligament healing. Can J Surg. 1998 Dec;41(6):425-9.
13. Silder A, Heiderscheit BC, Thelen DG, Enright T, Tuite MJ. MR observations of long-term musculotendon remodeling following a hamstring strain injury. Skeletal Radiol. 2008 Dec;37(12):1101-9.
14. Fukushima K, Badlani N, Usas A, Riano F, Fu F, Huard J. The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med. 2001 Jul-Aug;29(4):394-402.
15. Negishi S, Li Y, Usas A, Fu FH, Huard J. The effect of relaxin treatment on skeletal muscle injuries. Am J Sports Med. 2005 Dec;33(12):1816-24.
16. Foster W, Li Y, Usas A, Somogyi G, Huard J. Gamma interferon as an antifibrosis agent in skeletal muscle. J Orthop Res. 2003 Sep;21(5):798-804.
17. Nozaki M, Li Y, Zhu J, Ambrosio F, Uehara K, Fu FH, Huard J. Improved muscle healing after contusion injury by the inhibitory effect of suramin on myostatin, a negative regulator of muscle growth. Am J Sports Med. 2008 Dec;36(12):2354-62.
18. Arimura T, Helbling-Leclerc A, Massart C, Varnous S, Niel F, Lacène E, Fromes Y, Toussaint M, Mura AM, Keller DI, Amthor H, Isnard R, Malissen M, Schwartz K, Bonne G. Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet. 2005 Jan 1;14(1):155-69.
19. Rahimi RA, Leof EB. TGF-beta signaling: a tale of two responses. J Cell Biochem. 2007 Oct 15;102(3):593-608.
20. el-Agroudy AE, Hassan NA, Foda MA, Ismail AM, el-Sawy EA, Mousa O, Ghoneim MA. Effect of angiotensin II receptor blocker on plasma levels of TGF-beta 1 and interstitial fibrosis in hypertensive kidney transplant patients. Am J Nephrol. 2003 Sep-Oct;23(5):300-6.
21. Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K. Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev Biol. 2004 Jun 1;270(1):19-30.
22. Lim DS, Lutucuta S, Bachireddy P, Youker K, Evans A, Entman M, Roberts R, Marian AJ. Angiotensin II blockade reverses myocardial fibrosis in a transgenic mouse model of human hypertrophic cardiomyopathy. Circulation. 2001 Feb 13; 103(6):789-91.
23. Uhal BD, Wang R, Laukka J, Zhuang J, Soledad-Conrad V, Filippatos G. Inhibition of amiodarone-induced lung fibrosis but not alveolitis by angiotensin system antagonists. Pharmacol Toxicol. 2003 Feb;92(2):81-7.
24. Huard J, Li Y, Fu FH. Muscle injuries and repair: current trends in research. J Bone Joint Surg Am. 2002 May;84(5):822-32.
25. Fakhfakh R, Lamarre Y, Skuk D, Tremblay JP. Losartan enhances the success of myoblast transplantation. Cell Transplant. 2012;21(1): 139-52.
26. Cohn RD, van Erp C, Habashi JP, Soleimani AA, Klein EC, Lisi MT, Gamradt M, ap Rhys CM, Holm TM, Loeys BL, Ramirez F, Judge DP, Ward CW, Dietz HC. Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat Med. 2007 Feb;13(2): 204-10.
27. Bedair HS, Karthikeyan T, Quintero A, Li Y, Huard J. Angiotensin II receptor blockade administered after injury improves muscle regeneration and decreases fibrosis in normal skeletal muscle. Am J Sports Med. 2008 Aug;36(8): 1548-54.
28. Lee SJ, Lee YS, Zimmers TA, Soleimani A, Matzuk MM, Tsuchida K, Cohn RD, Barton ER. Regulation of muscle mass by follistatin and activins. Mol Endocrinol. 2010 Oct;24(10):1998-2008.
29. Zhu J, Li Y, Lu A, Gharaibeh B, Ma J, Kobayashi T, Quintero AJ, Huard J. Follistatin improves skeletal muscle healing after injury and disease through an interaction with muscle regeneration, angiogenesis, and fibrosis. Am J Pathol. 2011 Aug;179(2):915-30.
30. Kobayashi T, Uehara K, Ota S, Tobita K, Ambrosio F, Cummins JH, Terada S, Fu FH, Huard J. The timing of administration of a clinically relevant dose of losartan influences the healing process after contusion induced muscle injury. J Appl Physiol. 2013 Jan;114(2):262-73.
31. Plachokova AS, van den Dolder J, van den Beucken JJ, Jansen JA. Bone regenerative properties of rat, goat and human platelet-rich plasma. Int J Oral Maxillofac Surg. 2009 Aug;38(8):861-9.
32. Brecher G, Cronkite EP. Morphology and enumeration of human blood platelets. J Appl Physiol. 1950 Dec;3(6):365-77.
33. Crisco JJ, Jokl P, Heinen GT, Connell MD, Panjabi MM. A muscle contusion injury model. Biomechanics, physiology, and histology. Am J Sports Med. 1994 Sep-Oct; 22(5):702-10.
34. Kasemkijwattana C, Menetrey J, Somogyl G, Moreland MS, Fu FH, Buranapanitkit B, Watkins SC, Huard J. Development of approaches to improve the healing following muscle contusion. Cell Transplant. 1998 Nov-Dec;7(6): 585-98.
35. Diaz JA, Fischer DA, Rettig AC, Davis TJ, Shelbourne KD. Severe quadriceps muscle contusions in athletes. A report of three cases. Am J Sports Med. 2003 Mar-Apr;31(2):289-93.
36. Ogawa M, Hirose N, Ogimoto M, Matsuki H, Miki K, Kinoshita M, Koga A, Saku K. Chronic beneficial effects of type 1 angiotensin II receptor antagonist in patients with chronic hypoxemic pulmonary diseases. Cardiology. 2002;97(2): 111-2.
37. Ota S, Uehara K, Nozaki M, Kobayashi T, Terada S, Tobita K, Fu FH, Huard J. Intramuscular transplantation of muscle-derived stem cells accelerates skeletal muscle healing after contusion injury via enhancement of angiogenesis. Am J Sports Med. 2011 Sep;39(9):1912-22.
38. Qu Z, Huard J. Matching host muscle and donor myoblasts for myosin heavy chain improves myoblast transfer therapy. Gene Ther. 2000 Mar;7(5): 428-37.
39. Hurme T, Kalimo H. Activation of myogenic precursor cells after muscle injury. Med Sci Sports Exerc. 1992 Feb;24(2):197-205.
40. Menetrey J, Kasemkijwattana C, Fu FH, Moreland MS, Huard J. Suturing versus immobilization of a muscle laceration. A morphological and functional study in a mouse model. Am J Sports Med. 1999 Mar-Apr;27(2):222-9.
41. Lee JY, Peng H, Usas A, Musgrave D, Cummins J, Pelinkovic D, Jankowski R, Ziran B, Robbins P, Huard J. Enhancement of bone healing based on ex vivo gene therapy using human muscle-derived cells expressing bone morphogenetic protein 2. Hum Gene Ther. 2002 Jul 1;13(10):1201-11.
42. Wright-Carpenter T, Opolon P, Appell HJ, Meijer H, Wehling P, Mir LM. Treatment of muscle injuries by local administration of autologous conditioned serum: animal experiments using a muscle contusion model. Int J Sports Med. 2004 Nov;25(8): 582-7.
43. Deasy BM, Feduska JM, Payne TR, Li Y, Ambrosio F, Huard J. Effect of VEGF on the regenerative capacity of muscle stem cells in dystrophic skeletal muscle. Mol Ther. 2009 Oct;17(10):1788-98.
44. Ochoa O, Sun D, Reyes-Reyna SM, Waite LL, Michalek JE, McManus LM, Shireman PK. Delayed angiogenesis and VEGF production in CCR2-/- mice during impaired skeletal muscle regeneration. Am J Physiol Regul Integr Comp Physiol. 2007 Aug;293(2):R651-61.
45. Li Y, Foster W, Deasy BM, Chan Y, Prisk V, Tang Y, Cummins J, Huard J. Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am J Pathol. 2004 Mar;164(3):1007-19.
46. Pohlers D, Brenmoehl J, Löffler I, Müller CK, Leipner C, Schultze-Mosgau S, Stallmach A, Kinne RW, Wolf G. TGF-beta and fibrosis in different organs - molecular pathway imprints. Biochim Biophys Acta. 2009 Aug;1792(8):746-56.
47. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest. 2007 Mar;117(3):524-9.
48. Giovanini AF, Gonzaga CC, Zielak JC, Deliberador TM, Kuczera J, Göringher I, de Oliveira Filho MA, Baratto-Filho F, Urban CA. Platelet-rich plasma (PRP) impairs the craniofacial bone repair associated with its elevated TGF-β levels and modulates the co-expression between collagen III and a-smooth muscle actin. J Orthop Res. 2011 Mar;29(3):457-63.
49. Krneta J, Kroll J, Alves F, Prahst C, Sananbenesi F, Dullin C, Kimmina S, Phillips DJ, Augustin HG. Dissociation of angiogenesis and tumorigenesis in follistatin- and activin-expressing tumors. Cancer Res. 2006 Jun 1;66(11): 5686-95.
50. Nguyen F, Guigand L, Goubault-Leroux I, Wyers M, Cherel Y. Microvessel density in muscles of dogs with golden retriever muscular dystrophy. Neuromuscul Disord. 2005 Feb;15(2):154-63.
51. Brooks JH, Fuller CW, Kemp SP, Reddin DB. Incidence, risk, and prevention of hamstring muscle injuries in professional rugby union. Am J Sports Med. 2006 Aug; 34(8):1297-306.
52. Castillo TN, Pouliot MA, Kim HJ, Dragoo JL. Comparison of growth factor and platelet concentration from commercial platelet-rich plasma separation systems. Am J Sports Med. 2011 Feb;39(2):266-71.
53. Soomekh DJ. Current concepts for the use of platelet-rich plasma in the foot and ankle. Clin Podiatr Med Surg. 2011 Jan;28(1):155-70.