Ovine synovial membrane-derived mesenchymal progenitor cells retain the phenotype of the original tissue that was exposed to in-vivo inflammation: Evidence for a suppressed chondrogenic differentiation potential of the cells

Inflammation Research

Volumn 61, Issue 6, 2012, Pages 599-608

  Ando, Wataru ^a   Heard, Bryan J ^a   Chung, May ^a   Nakamura, Norimasa ^b   Frank, Cyril B ^a   Hart, David A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Chondrogenesis; Inflammation; Interleukin (IL); Matrix metalloproteinases (MMP); Mesenchymal progenitor cells (MPCs)

Indexed keywords

COLLAGENASE 3; GAG PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; STROMELYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL POPULATION; CELL SIZE; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POSTOPERATIVE INFLAMMATION; POSTOPERATIVE PERIOD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNOVIAL FLUID; SYNOVIUM; UPREGULATION;

ANIMALS; ARTHRITIS; CELL DIFFERENTIATION; FEMALE; INTERLEUKIN-1BETA; JOINTS; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 3; MESENCHYMAL STEM CELLS; PHENOTYPE; RNA, MESSENGER; SHEEP; SYNOVIAL FLUID; SYNOVIAL MEMBRANE;

EID: 84865119761     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-012-0450-x     Document Type: Article

References (40)

1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multi-lineage potential of adult human mesenchymal stem cells. Science. 1999;284:143-7. (Pubitemid 29282067)
2. Jankowski RJ, Deasy BM, Huard J. Muscle-derived stem cells. Gene Ther. 2002;9:642-7. (Pubitemid 34575318)
3. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001;44:1928-42. (Pubitemid 32758241)
4. Wickham MQ, Erickson GR, Gimble JM, Vail TP, Guilak F. Multipotent stromal cells derived from the infrapatellar fat pad of the knee. Clin Orthop. 2003;412:196-212. (Pubitemid 36793127)
5. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood. 2003;103:1669-75.
6. Miao Z, Jin J, Chen L, Zhu J, Huang W, Zhao J, et al. Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int. 2006;30:681-7. (Pubitemid 44331625)
7. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum. 2005;52:2521-9. (Pubitemid 41117441)
8. Ando W, Tateishi K, Hart DA, Katakai D, Tanaka Y, Nakata K, et al. Cartilage repair using in vitro generated scaffold-free tissue engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials. 2007;28:5462-70. (Pubitemid 47599635)
9. Mor A, Abramson SB, Pillinger MH. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clin Immunol. 2005;115(2):118-28. (Pubitemid 40693079)
10. Jones EA, English A, Henshaw K, Kinsey SE, Markham AF. Enumeration and phenotypic characterization of synovial fluid multipotential mesenchymal progenitor cells in inflammatory and degenerative arthritis. Arthritis Rheum. 2004;50:817-27. (Pubitemid 38326182)
11. Harvanová D, Tóthová T, Sarišský M, Amrichová J, Rosocha J. Isolation and characterization of synovial mesenchymal stem cells. Folia Biol (Praha). 2011;57(3):119-24.
12. Fernandes JC, Martel-Pelletier J, Pelletier JP. The role of cytokines in osteoarthritis pathophysiology. Biorheology. 2002;39:237-46. (Pubitemid 34626067)
13. Cameron M, Buchgraber A, Passler H, Vogt M, Thonar E, Fu F, et al. The natural history of the anterior cruciate ligament-deficient knee. Changes in synovial fluid cytokine and keratan sulfate concentrations. Am J Sports Med. 1997;25:751-4. (Pubitemid 27508409)
14. Irie K, Uchiyama E, Iwaso H. Intraarticular inflammatory cytokines in acute anterior cruciate ligament injured knee. Knee. 2003;10:93-6. (Pubitemid 36324521)
15. Higuchi H, Shirakura K, Kimura M, Terauchi M, Shinozaki T, Watanabe H, et al. Changes in biochemical parameters after anterior cruciate ligament injury. Int Orthop. 2006;30:43-7.
16. Marks PH, Donaldson ML. Inflammatory cytokine profiles associated with chondral damage in the anterior cruciate ligament- deficient knee. Arthroscopy. 2005;21:1342-7. (Pubitemid 41735200)
17. Tung JT, Fenton JI, Arnold C, Alexander L, Yuzbasiyan-Gurkan V, Venta PJ, et al. Recombinant equine interleukin-1beta induces putative mediators of articular cartilage degradation in equine chondrocytes. Can J Vet Res. 2002;66:19-25. (Pubitemid 34173145)
18. Jasser MZ, Mitchell PG, Cheung HS. Induction of stromelysin-1 and collagenase synthesis in fibrochondrocytes by tumor necrosis factor-alpha. Matrix Biol. 1994;14:241-9. (Pubitemid 24136384)
19. Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum. 2002;46:704-13. (Pubitemid 34218142)
20. Alsalameh S, Amin R, Gemba T, Lotz M. Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis Rheum. 2004;50:1522-32. (Pubitemid 38608074)
21. Dudics V, Kunstár A, Kovács J, Lakatos T, Géher P, Gömör B, et al. Chondrogenic potential of mesenchymal stem cells from patients with rheumatoid arthritis and osteoarthritis: measurements in a microculture system. Cells Tissues Organs. 2009;89: 307-16.
22. Scharstuhl A, Mutsaers HA, Pennings SW, Szarek WA, Russel FG, Wagener FA. Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology. Stem Cells. 2007;25:3244-51. (Pubitemid 350294450)
23. Frank CB, Jackson DW. The science of reconstruction of the anterior cruciate ligament. J Bone Joint Surg Am. 1997;79: 1556-76. (Pubitemid 27459303)
24. Fleming BC, Hulstyn MJ, Oksendahl HL, Fadale PD. Ligament injury reconstruction and osteoarthritis. Curr Opin Orthop. 2005;16:354-62.
25. Heard BJ, Achari Y, Chung M, Shrive NG, Frank CB. Early joint tissue changes are highly correlated with a set of inflammatory and degradative synovial biomarkers after ACL autograft and its sham surgery in an ovine model. J Orthop Res. 2011;29(8): 1185-92.
26. Kuh SU, Zhu Y, Li J, Tsai KJ, Fei Q, Hutton WC, et al. Can TGFbeta1 and rhBMP-2 act in synergy to transform bone marrow stem cells to discogenic-type cells? Acta Neurochir (Wien). 2008;150:1073-9.
27. Tateishi K, Higuchi C, Ando W, Nakata K, Hashimoto J, Hart DA, et al. The immunosuppressant FK506 promotes development of the chondrogenic phenotype in human synovial stromal cells via modulation of the Smad signaling pathway. Osteoarthr Cartil. 2007;15:709-18. (Pubitemid 46760622)
28. Magari K, Nishigaki F, Sasakawa T, Ogawa T, Miyata S, Ohkubo Y, et al. Anti-arthritic properties of FK506 on collagen-induced arthritis in rats. Inflamm Res. 2003;52:524-9. (Pubitemid 38063118)
29. Reno C, Marchuk L, Sciore P, Frank CB, Hart DA. Rapid isolation of total RNA from small samples of hypocellular, dense connective tissues. Biotechniques. 1997;22:1082-6. (Pubitemid 27248981)
30. Nakajima I, Muroya S, Chikuni K. Growth arrest by octanoate is required for porcine preadipocyte differentiation. Biochem Biophys Res Commun. 2003;309:702-8. (Pubitemid 37083309)
31. Hong L, Colpan A, Peptan IA. Modulations of 17-beta estradiol on osteogenic and adipogenic differentiations of human mesenchymal stem cells. Tissue Eng. 2006;12:2747-53. (Pubitemid 46141243)
32. Hellio Le Graverand MP, Reno C, Hart DA. Heterogenous response of knee cartilage to pregnancy in the rabbit: assessment of specific mRNA levels. Osteoarthr Cartil. 2000;8:53-62. (Pubitemid 30032727)
33. Lu T, Achari Y, Rattner JB, Hart DA. Evidence that estrogen receptor beta enhances MMP-13 promoter activity in HIG-82 cells and that this enhancement can be influenced by ligands and involves specific promoter sites. Biochem Cell Biol. 2007;85: 326-36. (Pubitemid 47025912)
34. Zou L, Zou X, Chen L, Li H, Mygind T, Kassem M, et al. Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern. J Orthop Res. 2008;26:56-64.
35. Majumdar MK, Wang E, Morris EA. BMP-2 and BMP-9 promotes chondrogenic differentiation of human multipotential mesenchymal cells and overcomes the inhibitory effect of IL-1. J Cell Physiol. 2001;189:275-84. (Pubitemid 33063295)
36. Okuma-Yoshioka C, Seto H, Kadono Y, Hikita A, Oshima Y, Kurosawa H, et al. Tumor necrosis factor-alpha inhibits chondrogenic differentiation of synovial fibroblasts through p38 mitogen activating protein kinase pathways. Mod Rheumatol. 2008;18:366-78.
37. Wehling N, Palmer GD, Pilapil C, Liu F, Wells JW, Müller PE, et al. Interleukin-1beta and tumor necrosis factor alpha inhibit chondrogenesis by human mesenchymal stem cells through NFkappaB- dependent pathways. Arthritis Rheum. 2009;60:801-12.
38. Lacey DC, Simmons PJ, Graves SE, Hamilton JA. Proinflammatory cytokines inhibit osteogenic differentiation from stem cells: implications for bone repair during inflammation. Osteoarthr Cartil. 2009;17:735-42.
39. Murphy G, Nagase H. Reappraising metalloproteinases in rheumatoid arthritis and osteoarthritis: destruction or repair? Nat Clin Pract Rheumatol. 2008;4:128-35. (Pubitemid 351338627)
40. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69:562-73. (Pubitemid 43139720)