Repair of large animal partial-thickness cartilage defects through intraarticular injection of matrix-rejuvenated synovium-derived stem cells

Tissue Engineering - Part A

Volumn 19, Issue 9-10, 2013, Pages 1144-1154

  Pei, Ming ^a,b   He, Fan ^a   Li, Jingting ^a   Tidwell, John E ^a   Jones, Alvin C ^a   McDonough, E Barry ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b West Virginia University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; DEFECTS; REPAIR; STEM CELLS; THREE DIMENSIONAL; TISSUE; TISSUE REGENERATION;

CARTILAGE REGENERATION; CHONDROGENIC MARKERS; CHONDROGENIC POTENTIAL; GLYCOSAMINOGLYCANS; IMMUNOHISTOCHEMISTRY; INTRA-ARTICULAR INJECTION; REPLICATIVE SENESCENCE; TRANSFORMING GROWTH FACTORS;

CARTILAGE;

ANIMALIA; PRUNELLA (ANGIOSPERM); SUIDAE;

TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL; ARTICLE; CARTILAGE; CELL CULTURE; CHONDROGENESIS; CYTOLOGY; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; PHYSIOLOGY; STEM CELL; SWINE; SYNOVIUM;

ANIMALS; CARTILAGE; CELLS, CULTURED; CHONDROGENESIS; IMMUNOHISTOCHEMISTRY; STEM CELLS; SWINE; SYNOVIAL MEMBRANE; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3;

EID: 84875614440     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0351     Document Type: Article

References (46)

1. Curl, W.W., Krome, J., Gordon, E.S., Rushing, J., Smith, B.P., and Poehling, G.G. Cartilage injuries: a review of 31,516 knee arthroscopies. Arthroscopy 13, 456, 1997.
2. Buckwalter, J.A. Articular cartilage: injuries and potential for healing. J Orthop Sports Phys Ther 28, 192, 1998.
3. Jackson, D.W., Simon, T.M., & Aberman, H.M. Symptomatic articular cartilage degeneration: the impact in the new millennium. Clin Orthop Relat Res 391 Suppl, S14, 2001.
4. Lubowitz, J.H. Partial-thickness articular cartilage defects: evaluation and treatment. Oper Tech Orthop 16, 227, 2006.
5. Reiter, S. Evidence-based evaluation of study results of symptomatic glucosamine therapy. Z Rheumatol 64, 456, 2005.
6. Godwin, M., & Dawes, M. Intra-articular steroid injections for painful knees. Systematic review with meta-analysis. Can Fam Physician 50, 241, 2004.
7. Arrich, J., Piribauer, F., Mad, P., Schmid, D., Klaushofer, K., and Mullner, M. Intra-articular hyaluronic acid for the treatment of osteoarthritis of the knee: systematic review and meta-analysis. CMAJ 172, 1039, 2005.
8. Owens, B.D., Stickles, B.J., Balikian, P., & Busconi, B.D. Prospective analysis of radiofrequency versus mechanical debridement of isolated patellar chondral lesions. Arthroscopy 18, 151, 2002.
9. Hunziker, E.B., & Rosenberg, L.C. Repair of partialthickness defects in articular cartilage: cell recruitment from the synovial membrane. J Bone Joint Surg Am 78, 721, 1996.
10. Bianco, P., & Robey, P.G. Stem cells in tissue engineering. Nature 414, 118, 2001.
11. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswai, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., & Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
12. Prockop, D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276, 71, 1997.
13. Le Blanc, K., & Ringde'n, O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 262, 509, 2007.
14. Pei, M., He, F., Kish, V., & Vunjak-Novakovic, G. Engineering of functional cartilage tissue using stem cells from synovial lining: a preliminary study. Clin Orthop Relat Res 466, 1880, 2008.
15. Pei, M., He, F., Boyce, B.M., & Kish, V.L. Repair of fullthickness femoral condyle cartilage defects using allogeneic synovial cell-engineered tissue constructs. Osteoarthritis Cartilage 17, 714, 2009.
16. Agung, M., Ochi, M., Yanada, S., Adachi, N., Izuta, Y., Yamasaki, T., & Toda, K. Mobilization of bone marrowderived mesenchymal stem cells into the injured tissues after intraarticular injection and their contribution to tissue regeneration. Knee Surg Sports Traumatol Arthrosc 14, 1307, 2006.
17. Lee, K.B., Hui, J.H., Song, I.C., Ardany, L., & Lee, E.H. Injectable mesenchymal stem cell therapy for large cartilage defects-a porcine model. Stem Cells 25, 2964, 2007.
18. Murphy, J.M., Fink, D.J., Hunziker, E.B., & Barry, F.P. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48, 3464, 2003.
19. He, F., Chen, X., & Pei, M. Reconstruction of an in vitro tissue-specific microenvironment to rejuvenate synoviumderived stem cells for cartilage tissue engineering. Tissue Eng Part A 15, 3809, 2009.
20. Li, J., & Pei, M. Cell senescence: a challenge in cartilage engineering and regeneration. Tissue Eng Part B Rev 18, 270, 2012.
21. Bruder, S.P., Jaiswal, N., & Haynesworth, S.E. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64, 278, 1997.
22. Javazon, E.H., Beggs, K.J., & Flake, A.W. Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 32, 414, 2004.
23. Vacanti, V., Kong, E., Suzuki, G., Sato, K., Canty, J.M., and Lee, T. Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture. J Cell Physiol 205, 194, 2005.
24. He, F., & Pei, M. Extracellular matrix enhances differentiation of adipose stem cells from infrapatellar fat pad toward chondrogenesis. J Tissue Eng Regen Med [Epub ahead of print]; DOI: 10.1002/term.505, 2011.
25. Li, J., & Pei, M. Optimization of an in vitro three-dimensional microenvironment to reprogram synovium-derived stem cells for cartilage tissue engineering. Tissue Eng Part A 17, 703, 2011.
26. Pei, M., He, F., & Wei, L. Three dimensional cell expansion substrate for cartilage tissue engineering and regeneration: a comparision in decellularized matrix deposited by synovium-derived stem cells and chondrocytes. J Tissue Sci Eng 2, 104, 2011.
27. Pei, M., Li, J.T., Shoukry, M., & Zhang, Y. A review of decellularized stem cell matrix: a novel cell expansion system for cartilage tissue engineering. Eur Cell Mater 22, 333, 2011.
28. Pei, M., He, F., & Kish, V.L. Expansion on extracellular matrix deposited by human bone marrow stromal cells facilitates stem cell proliferation and tissue-specific lineage potential. Tissue Eng Part A 17, 3067, 2011.
29. Jones, B., & Pei, M. Synovium-derived stem cells: a tissuespecific stem cell for cartilage tissue engineering and regeneration. Tissue Eng Part B Rev 18, 301, 2012.
30. Barry, F., Boynton, R.E., Liu, B., & Murphy, J.M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components. Exp Cell Res 268, 189, 2001.
31. James, A.W., Xu, Y., Lee, J.K., Wang, R., & Longaker, M.T. Differential effects of TGF-beta1 and TGF-beta3 on chondrogenesis in posterofrontal cranial suture-derived mesenchymal cells in vitro. Plast Reconstr Surg 123, 31, 2009.
32. Kolambkar, Y.M., Peister, A., Soker, S., Atala, A., and Guldberg, R.E. Chondrogenic differentiation of amniotic fluid-derived stem cells. J Mol Histol 38, 405, 2007.
33. Mueller, M.B., Fischer, M., Zellner, J., Berner, A., Dienstknecht, T., Prantl, L., Kujat, R., Nerlich, M., Tuan, R.S., and Angele, P. Hypertrophy in mesenchymal stem cell chondrogenesis: effect of TGF-beta isoforms and chondrogenic conditioning. Cells Tissues Organs 192, 158, 2010.
34. Li, J.T., He, F., & Pei, M. Creation of an in vitro microenvironment to enhance human fetal synovium-derived stem cell chondrogenesis. Cell Tissue Res 345, 357, 2011.
35. Pei, M., He, F., & Vunjak-Novakovic, G. Synoviumderived stem cell-based chondrogenesis. Differentiation 76, 1044, 2008.
36. Koga, H., Shimaya, M., Muneta, T., Nimura, A., Morito, T., Hayashi, M., Suzuki, S., Ju, Y.J., Mochizuki, T., & Sekiya, I. Local adherent technique for transplanting mesenchymal stem cells as a potential treatment of cartilage defect. Arthritis Res Ther 10, R84, 2008.
37. Arufe, M.C., De la Fuente, A., Mateos, J., Fuentes, I., De Toro, F.J., & Blanco, F.J. Analysis of the chondrogenic potential and secretome of mesenchymal stem cells derived from human umbilical cord stroma. Stem Cells Dev 20, 1199, 2011.
38. Reilly, G.C., Golden, E.B., Grasso-Knight, G., & Leboy, P.S. Differential effects of ERK and p38 signaling in BMP-2 stimulated hypertrophy of cultured chick sternal chondrocytes. Cell Commun Signal 3, 3, 2005.
39. Caputi, M., Groeger, A.M., Esposito, V., Dean, C., De Luca, A., Pacilio, C., Muller, M.R., Giordano, G.G., Baldi, F., Wolner, E., & Giordano, A. Prognostic role of cyclin D1 in lung cancer. Relationship to proliferating cell nuclear antigen. Am J Respir Cell Mol Biol 20, 746, 1999.
40. Grimaud, E., Heymann, D., & Re'dini, F. Recent advances in TGF-beta effects on chondrocyte metabolism. Potential therapeutic roles of TGF-beta in cartilage disorders. Cytokine Growth Factor Rev 13, 241, 2002.
41. Vinatier, C., Mrugala, D., Jorgensen, C., Guicheux, J., and Noel, D. Cartilage engineering: a crucial combination of cells, biomaterials and biofactors. Trends Biotechnol 27, 307, 2009.
42. Gelse, K., Muhle, C., Franke, O., Park, J., Jehle, M., Durst, K., Goken, M., Hennig, F., von der Mark, K., & Schneider, H. Cell-based resurfacing of large cartilage defects: long-term evaluation of grafts from autologous transgene-activated periosteal cells in a porcine model of osteoarthritis. Arthritis Rheum 58, 475, 2008.
43. Bentley, G., Kreutner, A., & Ferguson, A.B. Synovial regeneration and articular cartilage changes after synovectomy in normal and steroid-treated rabbits. J Bone Joint Surg Br 57, 454, 1975.
44. Campbell, W.G., Jr., & Callahan, B.C. Regeneration of synovium of rabbit knees after total chemical synovectomy by ingrowth of connective tissue-forming elements from adjacent bone. A light and electron microscopic study. Lab Invest 24, 404, 1971.
45. Mochizuki, T., Muneta, T., Sakaguchi, Y., Nimura, A., Yokoyama, A., Koga, H., & Sekiya, I. Higher chondrogenic potential of fibrous synovium-and adipose synoviumderived cells compared with subcutaneous fat-derived cells. Arthritis Rheum 54, 843, 2006.
46. Loeuille, D., Chary-Valckenaere, I., Champigneulle, J., Rat, A.C., Toussaint, F., Pinzano-Watrin, A., Goebel, J.C., Mainard, D., Blum, A., Pourel, J., Netter, P., & Gillet, P. Macroscopic and microscopic features of synovial membrane inflammation in the osteoarthritic knee: correlating magnetic resonance imaging findings with disease severity. Arthritis Rheum 52, 3492, 2005.