Thrombospondin-2 secreted by human umbilical cord blood-derived mesenchymal stem cells promotes chondrogenic differentiation

Stem Cells

Volumn 31, Issue 10, 2013, Pages 2136-2148

  Jeong, Sang Young ^a,b   Kim, Dong Hyun ^a   Ha, Jueun ^a   Jin, Hye Jin ^a   Kwon, Soon Jae ^a   Chang, Jong Wook ^a   Choi, Soo Jin ^a   Oh, Wonil ^a   Yang, Yoon Sun ^a   Kim, Gonhyung ^c   Kim, Jae Sung ^d   Yoon, Jung Ro ^e   Cho, Dong Hyung ^b   Jeon, Hong Bae ^a  

^a MEDIPOST Co Ltd   (South Korea)

^b Kyung Hee University   (South Korea)

^c Chungbuk National University   (South Korea)

^d Korea Institute of Radiation and Medical Science   (South Korea)

^e Seoul Veterans Hospital   (South Korea)

Author keywords

Human umbilical cord blood derived mesenchymal stem cells; Osteoarthritis; Paracrine action; Secretome; Synovial fluid; Thrombospondin 2

Indexed keywords

AGGRECAN; COLLAGEN TYPE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROTROPHIC FACTOR; NOTCH RECEPTOR; PROTEIN KINASE C ALPHA; SMALL INTERFERING RNA; THROMBOSPONDIN 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA2;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOARTHRITIS; PARACRINE SIGNALING; PROTEIN EXPRESSION; SYNOVIAL FLUID; UMBILICAL CORD BLOOD; UPREGULATION;

HUMAN UMBILICAL CORD BLOOD-DERIVED MESENCHYMAL STEM CELLS; OSTEOARTHRITIS; PARACRINE ACTION; SECRETOME; SYNOVIAL FLUID; THROMBOSPONDIN-2;

ADULT; AGED; ANIMALS; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MESENCHYMAL STROMAL CELLS; MICE; MIDDLE AGED; OSTEOARTHRITIS, KNEE; RABBITS; REGENERATION; REGENERATIVE MEDICINE; SYNOVIAL FLUID; THROMBOSPONDINS;

EID: 84887979199     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1471     Document Type: Article

References (58)

1. Caplan AI. The mesengenic process. Clin Plast Surg 1994;21:429-435.
2. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
3. Wang M, Yang Y, Yang D et al. The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology 2009;126:220-232.
4. Kim DS, Kim JH, Lee JK et al. Overexpression of CXC chemokine receptors is required for the superior glioma-tracking property of umbilical cord blood-derived mesenchymal stem cells. Stem Cells Dev 2009;18:511-519.
5. Bieback K, Kern S, Kluter H et al. Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 2004;22:625-634.
6. Granero-Molto F., Myers TJ, Weis JA et al. Mesenchymal stem cells expressing insulin-like growth factor-I (MSCIGF) promote fracture healing and restore new bone formation in Irs1 knockout mice: Analyses of MSCIGF autocrine and paracrine regenerative effects. Stem Cells 2011;29:1537-1548.
7. Chen L, Tredget EE, Wu PY et al. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008;3:e1886.
8. Tang YL, Zhao Q, Qin X et al. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 2005;80:229-236, discussion 236-227
9. Kim JY, Kim DH, Kim DS et al. Galectin-3 secreted by human umbilical cord blood-derived mesenchymal stem cells reduces amyloid-beta42 neurotoxicity in vitro. FEBS Lett 2010;584:3601-3608.
10. Kim JY, Kim DH, Kim JH et al. Soluble intracellular adhesion molecule-1 secreted by human umbilical cord blood-derived mesen-chymal stem cell reduces amyloid-beta plaques. Cell Death Differ 2012;19:680-691.
11. Granero-Molto F., Weis JA, Longobardi L et al. Role of mesenchymal stem cells in regenerative medicine: Application to bone and cartilage repair. Expert Opin Biol Ther 2008;8:255-268.
12. van Buul G.M., Villafuertes E, Bos PK et al. Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteo-arthritic synovium and cartilage explant culture. Osteoarthritis Cartilage 2012;20:1186-1196.
13. Wu L, Prins HJ, Helder MN et al. Trophic effects of mesenchymal stem cells in chondrocyte co-cultures are independent of culture conditions and cell sources. Tissue Eng Part A 2012;18:1542-1551.
14. 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. Osteoarthritis Cartilage 2012;20:1197-1207.
15. Qi Y, Feng G, Yan W. Mesenchymal stem cell-based treatment for cartilage defects in osteoarthritis. Mol Biol Rep 2012;39:5683-5689.
16. Schurgers E, Kelchtermans H, Mitera T et al. Discrepancy between the in vitro and in vivo effects of murine mesenchymal stem cells on T-cell proliferation and collagen-induced arthritis. Arthritis Res Ther 2010;12:R31.
17. Hill CL, Hunter DJ, Niu J et al. Synovitis detected on magnetic resonance imaging and its relation to pain and cartilage loss in knee osteo-arthritis. Ann Rheum Dis 2007;66:1599-1603.
18. Ayral X, Pickering EH, Woodworth TG et al. Synovitis: A potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis - Results of a 1 year longitudinal arthroscopic study in 422 patients. Osteoarthritis Cartilage 2005;13:361-367.
19. Kruger JP, Endres M, Neumann K et al. Chondrogenic differentiation of human subchondral progenitor cells is affected by synovial fluid from donors with osteoarthritis or rheumatoid arthritis. J Orthop Surg Res 2012;7:10.
20. Oh CD, Chun JS Signaling mechanisms leading to the regulation of differentiation and apoptosis of articular chondrocytes by insulin-like growth factor-1. J Biol Chem 2003;278:36563-36571.
21. Frenkel SR, Bradica G, Brekke JH et al. Regeneration of articular cartilage - Evaluation of osteochondral defect repair in the rabbit using multiphasic implants. Osteoarthritis Cartilage 2005;13:798-807.
22. DeLise AM, Stringa E, Woodward WA et al. Embryonic limb mesen-chyme micromass culture as an in vitro model for chondrogenesis and cartilage maturation. Methods Mol Biol 2000;137:359-375.
23. Tare RS, Howard D, Pound JC et al. Tissue engineering strategies for cartilage generation - Micromass and three dimensional cultures using human chondrocytes and a continuous cell line. Biochem Biophys Res Commun 2005;333:609-621.
24. Haab BB. Antibody arrays in cancer research. Mol Cell Proteomics 2005;4:377-383.
25. Oh CD, Chang SH, Yoon YM et al. Opposing role of mitogen-activated protein kinase subtypes, erk-1/2 and p38, in the regulation of chondrogenesis of mesenchymes. J Biol Chem 2000;275:5613-5619.
26. Chang SH, Oh CD, Yang MS et al. Protein kinase C regulates chon-drogenesis of mesenchymes via mitogen-activated protein kinase signaling. J Biol Chem 1998;273:19213-19219.
27. Oldershaw RA, Tew SR, Russell AM et al. Notch signaling through Jagged-1 is necessary to initiate chondrogenesis in human bone marrow stromal cells but must be switched off to complete chondrogene-sis. Stem Cells 2008;26:666-674.
28. Shapiro F, Koide S, Glimcher MJ Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 1993;75:532-553.
29. Lee MJ, Kim J, Kim MY et al. Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mes-enchymal stem cells. J Proteome Res 2010;9:1754-1762.
30. Streit M, Riccardi L, Velasco P et al. Thrombospondin-2: A potent endogenous inhibitor of tumor growth and angiogenesis. Proc Natl Acad Sci USA 1999;96:14888-14893.
31. Bornstein P, Armstrong LC, Hankenson KD et al. Thrombospondin 2, a matricellular protein with diverse functions. Matrix Biol 2000;19: 557-568.
32. Hankenson KD, Bain SD, Kyriakides TR et al. Increased marrow-derived osteoprogenitor cells and endosteal bone formation in mice lacking thrombospondin 2. J Bone Miner Res 2000;15:851-862.
33. Hankenson KD, Bornstein P. The secreted protein thrombospondin 2 is an autocrine inhibitor of marrow stromal cell proliferation. J Bone Miner Res 2002;17:415-425.
34. Taylor DK, Meganck JA, Terkhorn S et al. Thrombospondin-2 influences the proportion of cartilage and bone during fracture healing. J Bone Miner Res 2009;24:1043-1054.
35. Hankenson KD, James IE, Apone S et al. Increased osteoblastogenesis and decreased bone resorption protect against ovariectomy-induced bone loss in thrombospondin-2-null mice. Matrix Biol 2005;24:362-370.
36. Hankenson KD, Ausk BJ, Bain SD et al. Mice lacking thrombospon-din 2 show an atypical pattern of endocortical and periosteal bone formation in response to mechanical loading. Bone 2006;38:310-316.
37. Carron JA, Bowler WB, Wagstaff SC et al. Expression of members of the thrombospondin family by human skeletal tissues and cultured cells. Biochem Biophys Res Commun 1999;263:389-391.
38. Kyriakides TR, Zhu YH, Smith LT et al. Mice that lack thrombospon-din 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol 1998;140:419-430.
39. Alford AI, Reddy AB, Goldstein SA et al. Two molecular weight species of thrombospondin-2 are present in bone and differentially modulated in fractured and nonfractured tibiae in a murine model of bone healing. Calcif Tissue Int 2012;90:420-428.
40. Meng H, Zhang X, Hankenson KD et al. Thrombospondin 2 potentiates notch3/jagged1 signaling. J Biol Chem 2009;284:7866-7874.
41. Noth U, Steinert AF, Tuan RS Technology insight: Adult mesenchy-mal stem cells for osteoarthritis therapy. Nat Clin Pract Rheumatol 2008;4:371-380.
42. Sato M, Uchida K, Nakajima H et al. Direct transplantation of mesen-chymal stem cells into the knee joints of Hartley strain guinea pigs with spontaneous osteoarthritis. Arthritis Res Ther 2012;14:R31.
43. Mokbel AN, El Tookhy OS, Shamaa AA et al. Homing and reparative effect of intra-articular injection of autologus mesenchymal stem cells in osteoarthritic animal model. Bmc Musculoskelet Disord 2011;12: 259.
44. Lee KB, Hui JH, Song IC et al. Injectable mesenchymal stem cell therapy for large cartilage defects-a porcine model. Stem Cells 2007; 25:2964-2971.
45. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991;9:641-650.
46. Tang QO, Carasco CF, Gamie Z et al. Preclinical and clinical data for the use of mesenchymal stem cells in articular cartilage tissue engineering. Expert Opin Biol Ther 2012;12:1361-1382.
47. Caplan AI, Dennis JE Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084.
48. Chen FH, Tuan RS Mesenchymal stem cells in arthritic diseases. Arthritis Res Ther 2008;10:223.
49. Park MJ, Park HS, Cho ML et al. Transforming growth factor beta-transduced mesenchymal stem cells ameliorate experimental autoimmune arthritis through reciprocal regulation of Treg/Th17 cells and osteoclastogenesis. Arthritis Rheum 2011;63:1668-1680.
50. Leijs MJ, van Buul GM, Lubberts E et al. Effect of arthritic synovial fluids on the expression of immunomodulatory factors by mesenchy-mal stem cells: An explorative in vitro study. Front Immunol 2012;3: 231.
51. Koelling S, Kruegel J, Irmer M et al. Migratory chondrogenic progenitor cells from repair tissue during the later stages of human osteoar-thritis. Cell Stem Cell 2009;4:324-335.
52. Seol D, McCabe DJ, Choe H et al. Chondrogenic progenitor cells respond to cartilage injury. Arthritis Rheum 2012;64:3626-3637.
53. Pagnotto MR, Wang Z, Karpie JC et al. Adeno-associated viral gene transfer of transforming growth factor-beta1 to human mesenchymal stem cells improves cartilage repair. Gene Ther 2007;14:804-813.
54. 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.
55. Zhang ZY, Teoh SH, Chong MS et al. Neo-vascularization and bone formation mediated by fetal mesenchymal stem cell tissue-engineered bone grafts in critical-size femoral defects. Biomaterials 2010;31:608-620.
56. Yan H, Yu C. Repair of full-thickness cartilage defects with cells of different origin in a rabbit model. Arthroscopy 2007;23:178-187.
57. E X, Cao Y, Meng H et al. Dendritic cells of synovium in experimental model of osteoarthritis of rabbits. Cell Physiol Biochem 2012;30: 23-32.
58. Caplan AI, Correa D. The MSC: An injury drugstore. Cell Stem Cell 2011;9:11-15.