Mesenchymal stem cell therapy in horses: Useful beyond orthopedic injuries?

Veterinary Quarterly

Volumn 33, Issue 4, 2013, Pages 234-241

  De Schauwer, Catharina ^a   Van de Walle, Gerlinde R ^b   Van Soom, Ann ^a   Meyer, Evelyne ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Cornell University ^*  (United States)

Author keywords

equine; horse; mesenchymal stem cells; non orthopedic applications; orthopedic applications; stem cell therapy

Indexed keywords

ANIMALS; CELL DIFFERENTIATION; HORSE DISEASES; HORSES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MUSCULOSKELETAL DISEASES;

EID: 84893741408     PISSN: 01652176     EISSN: 18755941     Source Type: Journal    
DOI: 10.1080/01652176.2013.800250     Document Type: Review

References (84)

1. Agung M, Ochi M, Yanada S, Adachi N, Izuta Y, Yamasaki T, Toda K. 2006. Mobilization of bone marrow-derived mesenchymal stem cells into the injured tissues after intraarticular injection and their contribution to tissue regeneration. Knee Surg Sport Tr A. 14:1307-1314.
2. Alfaqeh H, Norhamdan MY, Chua KH, Chen HC, Aminuddin BS, Ruszymah BH. 2008. Cell based therapy for osteoarthritis in a sheep model: gross and histological assessment. Med J Malaysia.63:37-38.
3. Alves AG, Stewart AA, Dudhia J, Kasashima Y, Goodship AE, Smith RK. 2011. Cell-based therapies for tendon and ligament injuries. Vet Clin N Am: Equine.27:315-333.
4. Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, Pennesi G. 2005. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol. 35:1482-1490.
5. Badiavas EV, Falanga V. 2003. Treatment of chronic wounds with bone marrow-derived cells. Arch Dermatol. 139:510-516.
6. Borjesson DL, Peroni JF. 2011. The regenerative medicine laboratory: facilitating stem cell therapy for equine disease. J Lab Clin Med. 31:109-123.
7. Brehm W, Burk J, Delling U, Gittel C, Ribitsch I. 2012. Stem cell-based tissue engineering in veterinary orthopaedics. Cell Tissue Res. 347:677-688.
8. Caniglia CJ, Schramme MC, Smith RK. 2012. The effect of intralesional injection of bone marrow derived mesenchymal stem cells and bone marrow supernatant on collagen fibril size in a surgical model of equine superficial digital flexor tendonitis. Equine Vet J. 44:587-593.
9. Carstanjen B, Desbois C, Hekmati M, Behr L. 2006. Succesful engraftment of cultured autologous mesenchymal stem cells in a surgically repaired soft palate defect in an adult horse. Can J Vet Res. 70:143-147.
10. Chen CP, Lee YJ, Chiu ST, Shyu WC, Lee MY, Huang SP, Li H. 2006. The application of stem cells in the treatment of ischemic diseaeses. Histol Histopathol. 21:1209-1216.
11. Clegg P, Pinchbeck GL. 2011. Evidence-based medicine and stem cell therapy: how do we know such technologies are safe and efficacious? Vet Clin N Am: Equine27:373-382
12. Crovace A, Lacitignola L, Rossi G, Francioso E. 2010. Histological and immunohistochemical evaluation of autologous cultured bone marrow mesenchymal stem cells and bone marrow mononucleated cells in collagenase-induced tendinitis of equine superficial digital flexor tendon. Vet Med Int. 2010: Article ID 250978. doi:10.4061/2010/250978.
13. Deeg CA, Ehrenhofer M, Thurau SR, Reese S, Wildner G, Kaspers B. 2002. Immunopathology of recurrent uveitis in spontaneously diseased horses. Exp Eye Res. 75:127-133.
14. Deeg CA, Hauck SM, Amann B, Pompetzki D, Altmann F, Raith A, Schmalzl T, Stangassinger M, Ueffing M. 2008. Equine recurrent uveïtis - a spontaneous horse model of uveitis. Opthalmic Res. 40:151-153.
15. Del Bue M, Ricco S, Ramoni R, Conti V, Gnudi G, Grolli S. 2008. Equine adipose-tissue derived mesenchymal stem cells and platelet concentrates: their association in vitro and in vivo. Vet Res Commun. 32:S51-S55.
16. de Mattos Carvalho A, Alves ALG, Gomes de Oliveira PG, Alvarez LEC, Amorim RL, Hussni CA, Deffune E. 2011. Use of adipose tissue -derived mesenchymal stem cells for experimental tendinitis therapy in equines. J Equine Vet Sci. 31:26-34.
17. De Schauwer C, Meyer E, Cornillie P, De Vliegher S, Van de Walle GR, Hoogewijs MK, Declercq H, Govaere J, Demeyere K, Cornelissen M, Van Soom A. 2011. Optimization of the isolation, culture and characterization of equine umbilical cord blood mesenchymal stromal cells. Tissue Eng Part C. 17:1061-1070.
18. Engiles JB. 2010. Pathology of the distal phalanx in equine laminitis: more than just a skin deep. Vet Clin N Am: Equine26:155-165.
19. Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, Grigoriadis N, Lavon I, Baniyash M, Lassman H, Ben-Hur T. 2007. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol. 61:209-218.
20. Ferris DJ, Frisbie DD, Kisiday JD, McIlwraith CW, Hague BA, Major MD, Schneider RK, Zubrod CJ, Watkins JJ, Kawcak CE, Goodrich LR. 2009a. Clinical follow-up of horses treated with bone marrow-derived mesenchymal stem cells for musculoskeletal lesions. Am Assoc Equine Pract Proc. 55:59-60.
21. Ferris D, Frisbie D, Kisiday J, McIlwraith CW, Hague B, Major M, Schneider R, Zubrod C, Watkins J, Kawcak C, Goodrich L. 2009b. Clinical evaluation of bone marrow-derived mesenchymal stem cells in naturally occurring joint disease. Regenerative Med. 4:S16.
22. Fortier LA, Travis AJ. 2011. Stem cells in veterinary medicine. Stem Cell Res Ther. 2:9.
23. Franco Lambert AP, Fraga Zandonai A, Bonatto D, Cantarelli Machado D, Pêgas Henriques A. 2009. Differentiation of human adipose-derived adult stem cells into neuronal tissue: does it work? Differentiation.77:221-228.
24. Frisbie DD, Kisiday JD, Kawcak CE, Werpy NM, McIlwraith CW. 2009. Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthopaed Res. 27:1675-1680.
25. Frisbie DD, Stewart MC. 2011. Cell-based therapies for equine joint disease. Vet Clin N Am: Equine27:335-349.
26. Galvin N, Collins D. 2004. Perinatal asphyxia syndrome in the foal: review and a case report. Irish Vet J. 57:707-714.
27. Gershwin LJ. 2007. Veterinary autoimmunity - autoimmune diseases in domestic animals. Ann NY Acad Sci. 1109:109-116.
28. Gilger BC, Deeg CA. 2011. Equine recurrent uveitis. In: Equine ophthalmology. 2nd ed. St. Louis, MO:Saunders Elsevier; p.317-349.
29. Godwin EE, Young NJ, Dudhia J, Beamish IC, Smith RK. 2012. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon. Equine Vet J. 44:25-32.
30. Gonzalez MA, Gonzalez-Rey E, Rico L, Büscher D, Delgado M. 2009. Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum. 60:1006-1019.
31. Grigolo B, Lisignoli G, Desando G, Cavallo C, Marconi E, Tschon M, Giavaresi G, Fini M, Giardino R, Facchini A. 2009. Osteoarthritis treated with mesenchymal stem cells on hyaluronan-based scaffold in rabbit. Tissue Eng Part C Method. 15:647-658.
32. Gu Z, Akiyama K, Ma X, Zhang H, Feng X, Yao G, Hou Y, Lu L, Gilkeson GS, Silver RM, et al. 2010. Transplantation of umbilical cord mesenchymal stem cells alleviates lupus nephritis in MRL/lpr mice. Lupus. 19:1502-1514.
33. Guest DJ, Smith, MR, Allen WR. 2008. Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: preliminary study. Equine Vet J. 40:178-181.
34. Gupta PK, Das AK, Chullikana A, Majumdar AS. 2012. Mesenchymal stem cells for cartilage repair in osteoarthritis. Stem Cell Res Ther. 3:25.
35. Jamnig A, Lepperdinger G. 2012. From tendon to nerve: an MSC for all seasons. Can J Physiol Pharm. 90:295-306.
36. Koch TG, Berg LC, Betts DH. 2009. Current and future regenerative medicine - principles, concepts, and therapeutic use of stem cell therapy and tissue engineering in equine medicine. Can Vet J. 50:155-165.
37. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA. 2009. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy. 11:377-391.
38. Kon E, Muraglia A, Corsi A, Bianco P, Marcacci M, Martin I, Boyde A, Ruspantini I, Chistolini P, Rocca M, et al. 2000. Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J Biomed Mater Res. 49:328-337.
39. Kraus KH, Kirker-Head C. 2006. Mesenchymal stem cells and bone regeneration. Vet Surg. 35:232-242.
40. Lange C, Tögel F, Ittrich H, Clayton F, Nolte-Ernsting C, Zander AR, Westenfelder C. 2005. Administered mesenchymal stem cells enhance recovery from ischemia/reperfusion-induced acute renal failure in rats. Kidney Int. 68:1613-1617.
41. Leppänen M, Tulamo R-M, Heikkilä P, Katiskalahti T. 2009. Follow-up of equine tendon and ligament injuries 18-24 months after treatment with enriched autologous adipose-derived mesenchymal stem cells - a clinical study. Regenerative Med. 4:S21-S22.
42. Li Y, Chen J, Chen XG, Wang L, Gautam SC, Xu YX, Katakowski M, Zhang LJ, Lu M, Janakiraman N, Chopp M. 2002. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology59:514-523.
43. Li N, Li XR, Yuan JQ. 2009. Effects of bone-marrow mesenchymal stem cells transplanted into vitreous cavity of rat injured by ischemia/reperfusion. Graefes Arch Clin Exp Ophthalmol. 247:503-514.
44. Liang J, Zhang H, Hua B, Wang H, Lu L, Shi S, Hou Y, Zeng X, Gilkeson GS, Sun L. 2010. Allogenic mesenchymal stem cells transplantation in refractory systemic lupus eryhtematosus: a pilot clinical study. Ann Rheum Dis. 69:1423-1429.
45. Liu G, Zhao L, Zhang W, Cui L, Liu W, Cao Y. 2008. Repair of goat tibial defects with bone marrow stromal cells and beta-tricalcium phosphate. J Mater Sci Mater Med. 19:2367-2376.
46. Lu P, Tuszynski MH. 2005. Can bone marrow-derived stem cells differentiate into functional neurons? Exp Neurol.193:273-278.
47. Ma Y, Xu Y, Xiao Z, Yang W, Zhang C, Song E, Du Y, Li L. 2006. Reconstruction of chemically burned rat corneal surface by bone marrow-derived human mesenchymal stem cells. Stem Cells24:315-321.
48. Ma K, Fox L, Shi G, Shen J, Liu Q, Pappas JD, Cheng J, Qu T. 2011. Generation of neural stem cell-like cells from bone marrow-derived human mesenchymal stem cells. Neurol Res. 33:1083-1093.
49. Marcacci M, Kon E, Moukhachev V, Lavroukov A, Kutepov S, Quarto R, Mastrogiacomo M, Cancedda R. 2007. Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study. Tissue Eng. 13:947-955.
50. Marfe G, Massaro-Giordano M, Ranalli M, Cozzoli E, Di Stefano C, Malafoglia V, Polettini M, Gambacurta A. 2012a. Blood derived stem cells: an ameliorative therapy in veterinary ophthalmology. J Cell Physiol. 227:1250-1256.
51. Marfe G, Rotta G, De Martino L, Tafani M, Fiorito F, Di Stefano C, Polettini M, Ranalii M, Russo MA, Gambacurta A. 2012b. A new clinical approach: use of blood-derived stem cells (BDSCs) for superficial digital flexor tendon injuries in horses. Life Sci. 90:825-830.
52. Matsumoto T, Cooper GM, Gharaibeh B, Meszaros LB, Li G, Usas A, Fu FH, Huard J. 2009. Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of muscle-derived stem cells expressing bone morphogenetic protein 4 and soluble Flt-1. Arthritis Rheum. 60:1390-1405.
53. McIlwraith CW, Frisbie DD, Rodkey WG, Kisiday JD, Werpy NM, Kawcak CE, Steadman JR. 2011. Evaluation of intra-articular mesenchymal stem cells to augment healing of microfractured chondral defects. Arthroscopy27:1552-1561.
54. Murphy JM, Fink DJ, Hunziker EB, Barry FP. 2003. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 48:3464-3474.
55. Nery AA, Nascimento IC, Glaser T, Bassaneze V, Krieger JE, Ulrich H. 2013. Human mesenchymal stem cells: from immunophenotyping by flow cytometry to clinical applications. Cytometry Part A.83:48-61.
56. Nixon AJ, Dahlgren LA, Haupt JL, Yeager AE, Ward DL. 2008. Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis. Am J Vet Res. 69:928-937.
57. Ohnishi S, Yanagawa B, Tanaka K, Miyahara Y, Obata H, Kataoka M, Kodama M, Ishibashi-Ueda H, Kangawa K, Kitamura S, Nagaya N. 2007. Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis. J Mol Cell Cardiol. 42:88-97.
58. Pacini S, Spinabella S, Trombi L, Fazzi R, Galimberti S, Dini F, Carlucci F, Petrini M. 2007. Suspension of bone marrow-derived undifferentiated mesenchymal stromal cells for repair of superficial digital flexor tendon in race horses. Tissue Eng. 13:2949-2955.
59. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M. 2001. Repair of large bone defects with the use of autologous bonemarrow stromal cells. N Engl J Med. 344:385-386.
60. Quintavalla J, Uziel-Fusi S, Yin J, Boehnlein E, Pastor G, Blancuzzi V, Singh HN, Kraus KH, O'Byrne E, Pellas TC. 2002. Fluorescently labeled mesenchymal stem cells (MSCs) maintain multilineage potential and can be detected following implantation into articular cartilage defects. Biomaterials23:109-119.
61. Ra JC, Shin IS, Kim SH, Kang SK, Kang BC, Lee HY, Kim YJ, Jo JY, Yoon EJ, Choi HJ, Kwon E. 2011. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem Cells Dev. 8:1297-1308.
62. Richardson LE, Dudhia J, Clegg PD, Smith R. 2007. Stem cells in veterinary medicine - attempts at regenerating equine tendon after injury. Trends Biotechnol. 25:409-416.
63. Sadan O, Melamed E, Offen D. 2009. Bone marrow-derived mesenchymal stem cell therapy for neurodegenerative diseases. Expert Opin Biol Ther. 9:1487-1497.
64. Saito T, Kuang J, Bittira B, Al-Khaldi A, Chiu RCJ. 2002. Xenotransplant cardiac chimera: immune tolerance of adult stem cells. Ann Thorac Surg. 74:19-24.
65. Sasaki M, Abe R, Fujita Y, Ando S, Inokuma D, Shimizu H. 2008. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell types. J Immunol. 180:2581-2587.
66. Schnabel LV, Lynch ME, van der Meulen MC, Yeager AE, Kornatowski MA, Nixon AJ. 2009. Mesenchymal stem cells and insulin-like growth factor-I gene-enhanced mesenchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons. J Orthopaed Res. 27:1392-1398.
67. Sensebe L, Krampera M, Schrezenmeier H, Bourin P, Giordano R. 2010. Mesenchymal stem cells for clinical application. Vox Sanguinis. 98:93-107.
68. Shi D, Wang D, Li X, Zhang H, Che N, Lu Z, Sun L. 2012. Allogeneic transplantation of umbilical cord-derived mesenchymal stem cells for diffuse alveolar hemorrhage in systemic lupus erythematosus. Clin Rheumatol. 31:841-846.
69. Smith RKW, Korda M, Blunn GW, Goodship AE. 2003. Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment. Equine Vet J. 35:99-102.
70. Smith RKW. 2008. Mesenchymal stem cell therapy for equine tendinopathy. Disabil Rehabil. 30:1752-1758.
71. Sordi V, Piemonti L. 2011. Therapeutic plasticity of stem cells and allograft tolerance. Cytotherapy13:647-660.
72. Stewart MC. 2011. Cell-based therapies: current issues and future directions. Vet Clin N Am: Equine27:393-399.
73. Stewart MC, Stewart AA. 2011. Mesenchymal stem cells: characteristics, sources, mechanisms of action. Vet Clin N Am: Equine27:243-261.
74. Sun L, Akiyama K, Zhang H, Yamaza T, Hou Y, Zhao S, Xu T, Le A, Shi S. 2009. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells27:1421-1432.
75. Tang YL, Zhao Q, Qin X, Shen L, Cheng L, Ge J, Phillips ME. 2005. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg. 80:229-237.
76. Taylor SE, Smith RKW, Clegg PD. 2007. Mesenchymal stem cell therapy in equine musculoskeletal disease: scientific fact or clinical fiction? Equine Vet J.39:172-180.
77. Terai S, Sakaida I, Yamamoto N, Omori K, Watanabe T, Ohata S, Katada T, Miyamoto K, Shinoda K, Nishina H, Okita K. 2003. An in vivo model for monitoring trans-differentiation of bone marrow cells into functional hepatocytes. J Biochem. 134:551-558.
78. Theoret C. 2009. Tissue engineering in wound repair: the three "R"s - repair, replace, regenerate. Vet Surg. 38:905-913.
79. Tögel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. 2005. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol. 289:F31-F42.
80. van Buul GM, Villafuertes E, Bos PK, Waarsing JH, Kops N, Narcisi R, Weinans H, Verhaar JAN, Bernsen MR, van Osch GJVM. 2012. Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture. Osteoarthr Cartilage20:1186-1196.
81. Wenisch S, Trinkaus K, Hild A, Hose D, Heiss C, Alt V, Klisch C, Meissl H, Schnettler R. 2006. Immunochemical, ultrastructural and electrophysiological investigations of bone-derived stem cells in the course of neuronal differentiation. Bone38:911-921.
82. Wilke MM, Nydam DV, Nixon AJ. 2007. Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model. J Orthopaed Res. 25:913-925.
83. Wilmink JM, van Herten J, van Weeren PR, Barneveld A. 2002. Retrospective study of primary intention healing and sequestrum formation in horses compared to ponies under clinical circumstances. Equine Vet J. 34:270-273.
84. Zhu CJ, Dong JX, Li J, Zhang MJ, Wang LP, Luo L. 2011. Preliminary study on the mechanism of acupoint injection of bone marrow mesenchymal stem cells in improving blood flow in the rat of hind limb ischemia. J Tradit Chin Med. 31:241-245.