Monocyte chemotactic protein-1 inhibits chondrogenesis of synovial mesenchymal progenitor cells: An in vitro study

Stem Cells

Volumn 31, Issue 10, 2013, Pages 2253-2265

  Harris, Quinn ^a   Seto, Jonathan ^a   O'Brien, Kate ^a   Lee, Poh S ^a   Kondo, Colleen ^a   Heard, Bryan J ^a,b   Hart, David A ^a,b   Krawetz, Roman J ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Adult stem cells; Arthritis; Chemokine; Chondrogenesis

Indexed keywords

MONOCYTE CHEMOTACTIC PROTEIN 1; TELOMERASE; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTOME;

ADULT; ARTICLE; CELL ACTIVATION; CHONDROGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KNEE; MESENCHYMAL STEM CELL; OSTEOARTHRITIS; PROTEIN EXPRESSION; PROTEIN MICROARRAY; SYNOVIAL FLUID; SYNOVIOCYTE; SYNOVIUM; UPREGULATION; WESTERN BLOTTING;

ADULT STEM CELLS; ARTHRITIS; CHEMOKINE; CHONDROGENESIS;

CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOKINE CCL2; CHONDROGENESIS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; MESENCHYMAL STROMAL CELLS; OSTEOARTHRITIS, KNEE; SYNOVIAL FLUID; SYNOVIAL MEMBRANE; TELOMERASE; TRANSCRIPTOME;

EID: 84887920943     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1477     Document Type: Article

References (74)

1. Reginster JY. The prevalence and burden of arthritis. Rheumatology (Oxford) 2002;41:3-6.
2. Woolf AD, Pfleger B. Burden of major musculoskeletal conditions. Bull World Health Organ 2003;81:646-656.
3. Goldring MB, Marcu KB Cartilage homeostasis in health and rheumatic diseases. Arthritis Res Ther 2009;11:224.
4. Vinardell T, Sheehy EJ, Buckley CT et al. A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources. Tissue Eng Part A 2012;18: 1161-1170.
5. Kurth TB, Dell'accio F, Crouch V et al. Functional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo. Arthritis Rheum 2011;63:1289-1300.
6. Lee CH, Cook JL, Mendelson A et al. Regeneration of the articular surface of the rabbit synovial joint by cell homing: A proof of concept study. Lancet 2010;376:440-448.
7. Maurice H, Crone M, Watt I. Synovial chondromatosis. J Bone Joint Surg Br 1988;70:807-811.
8. Allard SA, Maini RN, Muirden KD Cells and matrix expressing cartilage components in fibroblastic tissue in rheumatoid pannus. Scand J Rheumatol Suppl 1988;76:125-129.
9. Archer CW, Dowthwaite GP, Francis-West P. Development of synovial joints. Birth Defects Res C Embryo Today 2003;69:144-155.
10. Chen FM, Wu LA, Zhang M et al. Homing of endogenous stem/progenitor cells for in situ tissue regeneration: Promises, strategies, and translational perspectives. Biomaterials 2011;32:3189-3209.
11. Jones E, McGonagle D. Human bone marrow mesenchymal stem cells in vivo. Rheumatology (Oxford) 2008;47:126-131.
12. Bielby R, Jones E, McGonagle D. The role of mesenchymal stem cells in maintenance and repair of bone. Injury 2007;38:S26-S32.
13. Herrera MB, Bussolati B, Bruno S et al. Mesenchymal stem cells contribute to the renal repair of acute tubular epithelial injury. Int J Mol Med 2004;14:1035-1041.
14. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. Int Soc Cell Ther Posit Statem Cytother 2006;8:315-317.
15. McGonagle D, Jones E. A potential role for synovial fluid mesenchymal stem cells in ligament regeneration. Rheumatology (Oxford) 2008; 47:1114-1116.
16. Jones EA, Crawford A, English A et al. Synovial fluid mesenchymal stem cells in health and early osteoarthritis: Detection and functional evaluation at the single-cell level. Arthritis Rheum 2008;58: 1731-1740.
17. Horie M, Sekiya I, Muneta T et al. Intra-articular Injected synovial stem cells differentiate into meniscal cells directly and promote menis-cal regeneration without mobilization to distant organs in rat massive meniscal defect. Stem Cells 2009;27:878-887.
18. Morito T, Muneta T, Hara K et al. Synovial fluid-derived mesenchymal stem cells increase after intra-articular ligament injury in humans. Rheumatology (Oxford) 2008;47:1137-1143.
19. 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.
20. Ando W, Tateishi K, Hart DA et al. Cartilage repair using an in vitro generated scaffold-free tissue-engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials 2007;28: 5462-5470.
21. Ando W, Tateishi K, Katakai D et al. In vitro generation of a scaffold-free tissue-engineered construct (TEC) derived from human synovial mesenchymal stem cells: Biological and mechanical properties and further chondrogenic potential. Tissue Eng Part A 2008;14: 2041-2049.
22. Kanamoto T, Nakamura N, Nakata K et al. Articular cartilage regeneration using stem cells. Clin Calcium 2008;18:1744-1749.
23. Hunziker EB, Rosenberg LC Repair of partial-thickness defects in articular cartilage: Cell recruitment from the synovial membrane. J Bone Joint Surg Am 1996;78:721-733.
24. Hunziker EB. Growth-factor-induced healing of partial-thickness defects in adult articular cartilage. Osteoarthritis Cartilage 2001;9:22-32.
25. Hermida-Gomez T., Fuentes-Boquete I, Gimeno-Longas MJ et al. Bone marrow cells immunomagnetically selected for CD271 + antigen promote in vitro the repair of articular cartilage defects. Tissue Eng Part A 2011;17:1169-1179.
26. Koga H, Shimaya M, Muneta T et al. Local adherent technique for transplanting mesenchymal stem cells as a potential treatment of cartilage defect. Arthritis Res Ther 2008;10:R84.
27. Koga H, Muneta T, Nagase T et al. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: Suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res 2008;333:207-215.
28. Sakaguchi Y, Sekiya I, Yagishita K et al. Comparison of human stem cells derived from various mesenchymal tissues: Superiority of syno-vium as a cell source. Arthritis Rheum 2005;52:2521-2529.
29. Lee SY, Nakagawa T, Reddi AH Mesenchymal progenitor cells derived from synovium and infrapatellar fat pad as a source for superficial zone cartilage tissue engineering: Analysis of superficial zone protein/lubricin expression. Tissue Eng Part A 2010;16:317-3125.
30. Fan J, Varshney RR, Ren L et al. Synovium-derived mesenchymal stem cells: A new cell source for musculoskeletal regeneration. Tissue Eng Part B Rev 2009;15:75-86.
31. Belema-Bedada F., Uchida S, Martire A et al. Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2008;2:566-575.
32. Dwyer RM, Potter-Beirne SM, Harrington KA et al. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 2007;13:5020-5027.
33. Honczarenko M, Le Y, Swierkowski M et al. Human bone marrow stromal cells express a distinct set of biologically functional chemo-kine receptors. Stem Cells 2006;24:1030-1041.
34. Low QE, Drugea IA, Duffner LA et al. Wound healing in MIP-1alpha(-/-) and MCP-1(-/-) mice. Am J Pathol 2001;159:457-463.
35. Endres M, Andreas K, Kalwitz G et al. Chemokine profile of synovial fluid from normal, osteoarthritis and rheumatoid arthritis patients: CCL25, CXCL10 and XCL1 recruit human subchondral mesenchymal progenitor cells. Osteoarthr Cartil 2010;18:1458-1466.
36. Fong EL, Chan CK, Goodman SB Stem cell homing in musculoskel-etal injury. Biomaterials 2011;32:395-409.
37. Shinohara K, Greenfield S, Pan H et al. Stromal cell-derived factor-1 and monocyte chemotactic protein-3 improve recruitment of osteo-genic cells into sites of musculoskeletal repair. J Orthop Res 2011;29: 1064-1069.
38. Smith MD, Triantafillou S, Parker A et al. Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J Rheumatol 1997;24:365-371.
39. Fernandes JC, Martel-Pelletier J, Pelletier JP The role of cytokines in osteoarthritis pathophysiology. Biorheology 2002;39:237-246.
40. Malemud CJ, Islam N, Haqqi TM Pathophysiological mechanisms in osteoarthritis lead to novel therapeutic strategies. Cells Tissues Organs 2003;174:34-48.
41. Malemud CJ. Cytokines as therapeutic targets for osteoarthritis. Bio-drugs 2004;18:23-35.
42. Goldring SR, Goldring MB The role of cytokines in cartilage matrix degeneration in osteoarthritis. Clin Orthop Relat Res. 2004; (427):S27-S36.
43. Benito MJ, Veale DJ, FitzGerald O et al. Synovial tissue inflammation in early and late osteoarthritis. Ann Rheum Dis 2005;64:1263-1267.
44. Nishimura M, Segami N, Kaneyama K et al. Proinflammatory cyto-kines and arthroscopic findings of patients with internal derangement and osteoarthritis of the temporomandibular joint. Br J Oral Maxillofac Surg 2002;40:68-71.
45. Pujol JP, Chadjichristos C, Legendre F et al. Interleukin-1 and transforming growth factor-beta 1 as crucial factors in osteoarthritic cartilage metabolism. Connect Tissue Res 2008;49:293-297.
46. Ainola MM, Mandelin JA, Liljeström MP et al. Pannus invasion and cartilage degradation in rheumatoid arthritis: Involvement of MMP-3 and interleukin-1beta. Clin Exp Rheumatol 2005;23:644-650.
47. Ando W, Heard BJ, Chung M et al. 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. Inflamm Res 2012;61:599-608.
48. Wehling N, Palmer GD, Pilapil C et al. Interleukin-1beta and tumor necrosis factor alpha inhibit chondrogenesis by human mesenchymal stem cells through NF-kappaB-dependent pathways. Arthritis Rheum 2009;60:801-812.
49. Wilson CG, Palmer AW, Zuo F et al. Selective and non-selective met-alloproteinase inhibitors reduce IL-1-induced cartilage degradation and loss of mechanical properties. Matrix Biol 2007;26:259-268.
50. Nakajima S, Naruto T, Miyamae T et al. Interleukin-6 inhibits early differentiation of ATDC5 chondrogenic progenitor cells. Cytokine 2009;47:91-97.
51. Krawetz RJ, Wu YE, Martin L et al. Synovial fluid progenitors expressing CD90+ from normal but not osteoarthritic joints undergo chondrogenic differentiation without micro-mass culture. Plos One 2012;7:e43616.
52. Krawetz R, Wu YE, Rancourt DE et al. Osteoblasts suppress high bone turnover caused by osteolytic breast cancer in-vitro. Exp Cell Res 2009;315:2333-2342.
53. Yang C, Przyborski S, Cooke MJ et al. A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 2008;26:850-863.
54. Pelletier AJ, van der Laan LJ, Hildbrand P et al. Presentation of che-mokine SDF-1 alpha by fibronectin mediates directed migration of T cells. Blood 2000;96:2682-2690.
55. Borzì RM, Mazzetti I, Cattini L et al. Human chondrocytes express functional chemokine receptors and release matrix-degrading enzymes in response to C-X-C and C-C chemokines. Arthritis Rheum 2000;43: 1734-1741.
56. Takagi T, Naito Y, Inoue M et al. Inhalation of carbon monoxide ameliorates collagen-induced arthritis in mice and regulates the articular expression of IL-1beta and MCP-1. Inflammation 2009;32:83-88.
57. Pulsatelli L, Dolzani P, Piacentini A et al. Chemokine production by human chondrocytes. J Rheumatol 1999;26:1992-2001.
58. Gong JH, Ratkay LG, Waterfield JD et al. An antagonist of monocyte chemoattractant protein 1 (MCP-1) inhibits arthritis in the MRL-lpr mouse model. J Exp Med 1997;186:131-137.
59. Han Y, Lefebvre V. L-Sox5 and Sox6 drive expression of the aggre-can gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol Cell Biol 2008;28:4999-5013.
60. Yeh LC, Lee JC Identification of an osteogenic protein-1 responsive element in the aggrecan promoter. Biochem Biophys Res Commun 2004;323:223-228.
61. Cho JH, Kim SH, Park KD et al. Chondrogenic differentiation of human mesenchymal stem cells using a thermosensitive poly(N-isopro-pylacrylamide) and watersoluble chitosan copolymer. Biomaterials 2004;25:5743-5751.
62. Nishioka K, Dennis JE, Gao J et al. Sustained Wnt protein expression in chondral constructs from mesenchymal stem cells. J Cell Physiol 2005;203:6-14.
63. Mwale F, Stachura D, Roughley P et al. Limitations of using aggrecan and type X collagen as markers of chondrogenesis in mesenchymal stem cell differentiation. J Orthop Res 2006 24:1791-1798.
64. Legendre F, Dudhia J, Pujol JP et al. JAK/STAT but not ERK1/ERK2 pathway mediates interleukin (IL)-6/soluble IL-6R down-regulation of type II collagen, aggrecan core, and link protein transcription in articular chondrocytes. Association with a down-regulation of SOX9 expression. J Biol Chem 2003;278:2903-2912.
65. Namba A, Aida Y, Suzuki N et al. Effects of IL-6 and soluble IL-6 receptor on the expression of cartilage matrix proteins in human chon-drocytes. Connect Tissue Res 2007;48:263-270.
66. Arendt BK, Velazquez-Dones A, Tschumper RC et al. Interleukin 6 induces monocyte chemoattractant protein-1 expression in myeloma cells. Leukemia 2002;16:2142-2147.
67. Viedt C, Vogel J, Athanasiou T et al. Monocyte chemoattractant protein-1 induces proliferation and interleukin-6 production in human smooth muscle cells by differential activation of nuclear factor-kappaB and activator protein-1. Arterioscler Thromb Vasc Biol 2002;22:914-920.
68. Garapaty S, Mahajan MA, Samuels HH Components of the CCR4-NOT complex function as nuclear hormone receptor coactivators via association with the NRC-interacting Factor NIF-1. J Biol Chem 2008;283:6806-6816.
69. Johnstone B, Hering TM, Caplan AI et al. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998;238:265-272.
70. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
71. Mackay AM, Beck SC, Murphy JM et al. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 1998;4:415-428.
72. Rollins BJ. Monocyte chemoattractant protein 1: A potential regulator of monocyte recruitment in inflammatory disease. Mol Med Today 1996;2:198-204.
73. Shi C, Jia T, Mendez-Ferrer S et al. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity 2011;34:590-601.
74. Sekiya I, Ojima M, Suzuki S et al. Human mesenchymal stem cells in synovial fluid increase in the knee with degenerated cartilage and osteoarthritis. J Orthop Res 2012;30:943-949.