Synovial mesenchymal stem cells promote meniscus regeneration augmented by an autologous achilles tendon graft in a rat partial meniscus defect model

Stem Cells

Volumn 33, Issue 6, 2015, Pages 1927-1938

  Ozeki, Nobutake ^a   Muneta, Takeshi ^a   Matsuta, Seiya ^a   Koga, Hideyuki ^a   Nakagawa, Yusuke ^a   Mizuno, Mitsuru ^b   Tsuji, Kunikazu ^c   Mabuchi, Yo ^b   Akazawa, Chihiro ^b   Kobayashi, Eiji ^d   Saito, Tomoyuki ^a   Sekiya, Ichiro ^b  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Arthritis; Cellular therapy; Mesenchymal stem cells; Stem cell transplantation

Indexed keywords

LUCIFERASE;

ACHILLES TENDON; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; AUTOTRANSPLANTATION; CARTILAGE DEGENERATION; CELL MATURATION; CELL MIGRATION; CELL SURVIVAL; CELL TRACKING; CHONDROPROTECTION; CONTROLLED STUDY; FLOW CYTOMETRY; HISTOLOGY; HISTOPATHOLOGY; KNEE DISEASE; MALE; MENISCECTOMY; MENISCUS DEFECT; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; RAT; SYNOVIUM; TENDON GRAFT; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DISEASE MODEL; MESENCHYMAL STROMA CELL; PHYSIOLOGY; PROCEDURES; REGENERATION; REGENERATIVE MEDICINE;

ANIMALIA; RATTUS;

ACHILLES TENDON; ANIMALS; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RATS; REGENERATION; REGENERATIVE MEDICINE; SYNOVIAL MEMBRANE;

EID: 84929832736     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2030     Document Type: Article

References (50)

1. Burks RT, Metcalf MH, Metcalf RW,. Fifteen-year follow-up of arthroscopic partial meniscectomy. Arthroscopy 1997; 13: 673-679.
2. Englund M, Roos EM, Roos HP, et al., Patient-relevant outcomes fourteen years after meniscectomy: Influence of type of meniscal tear and size of resection. Rheumatology 2001; 40: 631-639.
3. Englund M, Roemer FW, Hayashi D, et al., Meniscus pathology, osteoarthritis and the treatment controversy. Nat Rev Rheumatol 2012; 8: 412-419.
4. Garrett WE, Swiontkowski MF, Weinstein JN, et al., American Board of Orthopaedic Surgery Practice of the Orthopaedic Surgeon: Part-II, certification examination case mix. J Bone Joint Surg Am 2006; 88: 660-667.
5. Andersson-Molina H, Karlsson H, Rockborn P,. Arthroscopic partial and total meniscectomy: A long-term follow-up study with matched controls. Arthroscopy 2002; 18: 183-189.
6. Rodeo SA,. Meniscal allografts - where do we stand? Am J Sports Med 2001; 29: 246-261.
7. Hommen JP, Applegate GR, Del Pizzo W,. Meniscus allograft transplantation: Ten-year results of cryopreserved allografts. Arthroscopy 2007; 23: 388-393.
8. McDermott I,. Meniscal tears, repairs and replacement: Their relevance to osteoarthritis of the knee. Br J Sports Med 2011; 45: 292-297.
9. Zaffagnini S, Marcheggiani Muccioli GM, Lopomo N, et al., Prospective long-term outcomes of the medial collagen meniscus implant versus partial medial meniscectomy: A minimum 10-year follow-up study. Am J Sports Med 2011; 39: 977-985.
10. Kohn D, Wirth CJ, Reiss G, et al., Medial meniscus replacement by a tendon autograft. Experiments in sheep. J Bone Joint Surg Br 1992; 74: 910-917.
11. Johnson LL, Feagin JA,. Autogenous tendon graft substitution for absent knee joint meniscus: A pilot study. Arthroscopy 2000; 16: 191-196.
12. Fithian DC, Kelly MA, Mow VC,. Material properties and structure-function relationships in the menisci. Clin Orthop Relat Res 1990: 19-31.
13. Friedenstein AJ, Deriglasova UF, Kulagina NN, et al., Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 1974; 2: 83-92.
14. Prockop DJ,. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997; 276: 71-74.
15. Murphy JM, Fink DJ, Hunziker EB, et al., Stem cell therapy in a caprine model of osteoarthritis. Arthrit Rheumat 2003; 48: 3464-3474.
16. Moriguchi Y, Tateishi K, Ando W, et al., Repair of meniscal lesions using a scaffold-free tissue-engineered construct derived from allogenic synovial MSCs in a miniature swine model. Biomaterials 2013; 34: 2185-2193.
17. Shen W, Chen J, Zhu T, et al., Intra-articular injection of human meniscus stem/progenitor cells promotes meniscus regeneration and ameliorates osteoarthritis through stromal cell-derived factor-1/CXCR4-mediated homing. Stem Cells Transl Med 2014; 3: 387-394.
18. Vangsness CT, Jr., Farr J, 2nd, Boyd J, et al., Adult human mesenchymal stem cells delivered via intra-articular injection to the knee following partial medial meniscectomy: A randomized, double-blind, controlled study. J Bone Joint Surg Am 2014; 96: 90-98.
19. De Bari C, Dell'Accio F, Tylzanowski P, et al., Multipotent mesenchymal stem cells from adult human synovial membrane. Arthrit Rheumat 2001; 44: 1928-1942.
20. Sakaguchi Y, Sekiya I, Yagishita K, et al., Comparison of human stem cells derived from various mesenchymal tissues: Superiority of synovium as a cell source. Arthrit Rheumat 2005; 52: 2521-2529.
21. Yoshimura H, Muneta T, Nimura A, et al., Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 2007; 327: 449-462.
22. Matsukura Y, Muneta T, Tsuji K, et al., Mesenchymal stem cells in synovial fluid increase after meniscus injury. Clinical Orthop Relat Res 2014; 472: 1357-1364.
23. Horie M, Sekiya I, Muneta T, et al., Intra-articular Injected synovial stem cells differentiate into meniscal cells directly and promote meniscal regeneration without mobilization to distant organs in rat massive meniscal defect. Stem Cells 2009; 27: 878-887.
24. Horie M, Driscoll MD, Sampson HW, et al., Implantation of allogenic synovial stem cells promotes meniscal regeneration in a rabbit meniscal defect model. J Bone Joint Surg Am 2012; 94: 701-712.
25. Hakamata Y, Murakami T, Kobayashi E,. "Firefly rats" as an organ/cellular source for long-term in vivo bioluminescent imaging. Transplantation 2006; 81: 1179-1184.
26. Inoue H, Ohsawa I, Murakami T, et al., Development of new inbred transgenic strains of rats with LacZ or GFP. Biochem Biophys Res Comm 2005; 329: 288-295.
27. Koga H, Muneta T, Ju YJ, et al., Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells 2007; 25: 689-696.
28. Miyamoto T, Muneta T, Tabuchi T, et al., Intradiscal transplantation of synovial mesenchymal stem cells prevents intervertebral disc degeneration through suppression of matrix metalloproteinase-related genes in nucleus pulposus cells in rabbits. Arthrit Res Ther 2010; 12: R206.
29. Suzuki S, Muneta T, Tsuji K, et al., Properties and usefulness of aggregates of synovial mesenchymal stem cells as a source for cartilage regeneration. Arthrit Res Ther 2012; 14: R136.
30. Ozeki N, Muneta T, Koga H, et al., Transplantation of Achilles tendon treated with bone morphogenetic protein 7 promotes meniscus regeneration in a rat model of massive meniscal defect. Arthrit Rheumat 2013; 65: 2876-2886.
31. Inoue A, Takahashi KA, Arai Y, et al., The therapeutic effects of basic fibroblast growth factor contained in gelatin hydrogel microspheres on experimental osteoarthritis in the rabbit knee. Arthrit Rheumat 2006; 54: 264-270.
32. Pauli C, Grogan SP, Patil S, et al., Macroscopic and histopathologic analysis of human knee menisci in aging and osteoarthritis. Osteoarthrit Cartil 2011; 19: 1132-1141.
33. Mankin HJ, Dorfman H, Lippiello L, et al., Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 1971; 53: 523-537.
34. Zaffagnini S, Marcheggiani Muccioli GM, Bulgheroni P, et al., Arthroscopic collagen meniscus implantation for partial lateral meniscal defects: A 2-year minimum follow-up study. Am J Sports Med 2012; 40: 2281-2288.
35. Verdonk P, Beaufils P, Bellemans J, et al., Successful treatment of painful irreparable partial meniscal defects with a polyurethane scaffold: Two-year safety and clinical outcomes. Am J Sports Med 2012; 40: 844-853.
36. Muneta T, Sekiya I, Yagishita K, et al., Two-bundle reconstruction of the anterior cruciate ligament using semitendinosus tendon with endobuttons: Operative technique and preliminary results. Arthroscopy 1999; 15: 618-624.
37. Nakamura T, Sekiya I, Muneta T, et al., Arthroscopic, histological and MRI analyses of cartilage repair after a minimally invasive method of transplantation of allogeneic synovial mesenchymal stromal cells into cartilage defects in pigs. Cytotherapy 2012; 14: 327-338.
38. Nakagawa Y, Muneta T, Kondo S, et al., Synovial mesenchymal stem cells promote healing after meniscal repair in microminipigs. Osteoarthrit Cartil 2015, in press.
39. Koga H, Shimaya M, Muneta T, et al., Local adherent technique for transplanting mesenchymal stem cells as a potential treatment of cartilage defect. Arthrit Res Ther 2008; 10: R84.
40. Horie M, Choi H, Lee RH, et al., Intra-articular injection of human mesenchymal stem cells (MSCs) promote rat meniscal regeneration by being activated to express Indian hedgehog that enhances expression of type II collagen. Osteoarthrit Cartil 2012; 20: 1197-1207.
41. Shimaya M, Muneta T, Ichinose S, et al., Magnesium enhances adherence and cartilage formation of synovial mesenchymal stem cells through integrins. Osteoarthrit Cartil 2010; 18: 1300-1309.
42. Dominici M, Le Blanc K, Mueller I, et al., Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317.
43. Okuno M, Muneta T, Koga H, et al., Meniscus regeneration by syngeneic, minor mismatched, and major mismatched transplantation of synovial mesenchymal stem cells in a rat model. J Orthop Res 2014; 32: 928-936.
44. Tamai K, Yamazaki T, Chino T, et al., PDGFRalpha-positive cells in bone marrow are mobilized by high mobility group box 1 (HMGB1) to regenerate injured epithelia. Proc Natl Acad Sci USA 2011; 108: 6609-6614.
45. Caplan AI, Dennis JE,. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98: 1076-1084.
46. Sekiya I, Larson BL, Vuoristo JT, et al., Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 2005; 320: 269-276.
47. Mizumoto Y, Moseley T, Drews M, et al., Acceleration of regenerate ossification during distraction osteogenesis with recombinant human bone morphogenetic protein-7. J Bone Joint Surg Am 2003; 85-A Suppl 3: 124-130.
48. Kessler MW, Barr J, Greenwald R, et al., Enhancement of Achilles tendon repair mediated by matrix metalloproteinase inhibition via systemic administration of doxycycline. J Orthopaed Res 2014; 32: 500-506.
49. Gerwin N, Bendele AM, Glasson S, et al., The OARSI histopathology initiative-Recommendations for histological assessments of osteoarthritis in the rat. Osteoarthrit Cartil 2010; 18: S24-S34.
50. Katagiri H, Muneta T, Tsuji K, et al., Transplantation of aggregates of synovial mesenchymal stem cells regenerates meniscus more effectively in a rat massive meniscal defect. Biochem Biophys Res Comm 2013; 435: 603-609.