Mesenchymal stem cells markedly suppress inflammatory bone destruction in rats with adjuvant-induced arthritis

Laboratory Investigation

Volumn 94, Issue 3, 2014, Pages 286-296

  Takano, Toshio ^a   Li, Yin Ji ^a   Kukita, Akiko ^b   Yamaza, Takayoshi ^a   Ayukawa, Yasunori ^a   Moriyama, Kanako ^a   Uehara, Norihisa ^a   Nomiyama, Hisayuki ^c   Koyano, Kiyoshi ^a   Kukita, Toshio ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b SAGA UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

bone destruction; chemokine receptors; chemotaxis; inflammation; MIP 1 ; MSC; osteoclastogenesis; SDF 1

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; INTERLEUKIN 10; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; OSTEOPROTEGERIN; STROMAL CELL DERIVED FACTOR 1ALPHA;

ADJUVANT ARTHRITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DESTRUCTION; BONE MARROW CULTURE; BONE RADIOGRAPHY; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IN VITRO STUDY; JOINT SWELLING; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THICKNESS;

ANIMALS; ARTHRITIS, EXPERIMENTAL; BONE RESORPTION; CELL DIFFERENTIATION; CHEMOKINE CCL3; CHEMOKINE CXCL12; CHEMOKINES; CHEMOTAXIS; CYTOKINES; FEMALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; OSTEOCLASTS; RATS; RATS, INBRED LEW; RECEPTORS, CHEMOKINE;

EID: 84896873337     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.152     Document Type: Article

References (53)

1. Huey DJ, Hu JC, Athanasiou KA. Unlike bone, cartilage regeneration remains elusive. Science 2012;338:917-921.
2. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
3. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008;8:726-736.
4. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970;3:393-403.
5. Lee K, Kim H, Kim JM, Kim JR, Kim KJ, Kim YJ, et al. Systemic transplantation of human adipose-derived stem cells stimulates bone repair by promoting osteoblast and osteoclast function. J Cell Mol Med 2011;15:2082-2094.
6. Oh W, Kim DS, Yang YS, Lee JK. Immunological properties of umbilical cord blood-derived mesenchymal stromal cells. Cell Immunol 2008;251:116-123.
7. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499-3506.
8. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 2008;371:1579-1586.
9. Djouad F, Fritz V, Apparailly F, Louis-Plence P, Bony C, Sany J, et al. Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis Rheum 2005;52:1595-1603.
10. Zhou K, Zhang H, Jin O, Feng X, Yao G, Hou Y, et al. Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr mice. Cell Mol Immunol 2008; 5:417-424.
11. Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM, et al. Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 2008;26:1065-1073.
12. Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, et al. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci USA 2006;103:17438-17443.
13. Feldmann M, Brennan FM, Maini RN. Rheumatoid arthritis. Cell 1996; 85:307-310.
14. Gough A, Sambrook P, Devlin J, Huissoon A, Njeh C, Robbins S, et al. Osteoclastic activation is the principal mechanism leading to secondary osteoporosis in rheumatoid arthritis. J Rheumatol 1998;25:1282-1289.
15. Gravallese EM, Harada Y, Wang JT, Gorn AH, Thornhill TS, Goldring SR. Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis. Am J Pathol 1998;152:943-951.
16. Colpaert FC. Evidence that adjuvant arthritis in the rat is associated with chronic pain. Pain 1987;28:201-222.
17. Broxmeyer HE, Kim CH, Cooper SH, Hangoc G, Hromas R, Pelus LM. Effects of CC, CXC, C, and CX3C chemokines on proliferation of myeloid progenitor cells, and insights into SDF-1-induced chemotaxis of progenitors. Ann N Y Acad Sci 1999;872:142-162, discussion 163.
18. Han ZC, Lu M, Li J, Defard M, Boval B, Schlegel N, et al. Platelet factor 4 and other CXC chemokines support the survival of normal hematopoietic cells and reduce the chemosensitivity of cells to cytotoxic agents. Blood 1997;89:2328-2335.
19. Lataillade JJ, Clay D, Dupuy C, Rigal S, Jasmin C, Bourin P, et al. Chemokine SDF-1 enhances circulating CD34() cell proliferation in synergy with cytokines: Possible role in progenitor survival. Blood 2000;95:756-768.
20. Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol 2004;36:1882-1886.
21. Fuller K, Owens JM, Chambers TJ. Macrophage inflammatory protein-1 alpha and IL-8 stimulate the motility but suppress the resorption of isolated rat osteoclasts. J Immunol 1995;154:6065-6072.
22. Votta BJ, White JR, Dodds RA, James IE, Connor JR, Lee-Rykaczewski E, et al. CKbeta-8 [CCL23], a novel CC chemokine, is chemotactic for human osteoclast precursors and is expressed in bone tissues. J Cell Physiol 2000;183:196-207.
23. Kukita T, Nakao J, Hamada F, Kukita A, Inai T, Kurisu K, et al. Recombinant LD78 protein, a member of the small cytokine family, enhances osteoclast differentiation in rat bone marrow culture system. Bone Miner 1992;19:215-223.
24. Kukita T, Nomiyama H, Ohmoto Y, Kukita A, Shuto T, Hotokebuchi T, et al. Macrophage inflammatory protein-1 alpha (LD78) expressed in human bone marrow: Its role in regulation of hematopoiesis and osteoclast recruitment. Lab Invest 1997;76:399-406.
25. Watanabe T, Kukita T, Kukita A, Wada N, Toh K, Nagata K, et al. Direct stimulation of osteoclastogenesis by MIP-1alpha: Evidence obtained from studies using RAW264 cell clone highly responsive to RANKL. J Endocrinol 2004;180:193-201.
26. Toh K, Kukita T, Wu Z, Kukita A, Sandra F, Tang QY, et al. Possible involvement of MIP-1alpha in the recruitment of osteoclast progenitors to the distal tibia in rats with adjuvant-induced arthritis. Lab Invest 2004;84:1092-1102.
27. Han JH, Choi SJ, Kurihara N, Koide M, Oba Y, Roodman GD. Macrophage inflammatory protein-1alpha is an osteoclastogenic factor in myeloma that is independent of receptor activator of nuclear factor kappaB ligand. Blood 2001;97:3349-3353.
28. Abe M, Hiura K, Wilde J, Moriyama K, Hashimoto T, Ozaki S, et al. Role for macrophage inflammatory protein (MIP)-1alpha and MIP-1beta in the development of osteolytic lesions in multiple myeloma. Blood 2002;100:2195-2202.
29. Nagasawa T. Microenvironmental niches in the bone marrow required for B-cell development. Nat Rev Immunol 2006;6:107-116.
30. D'Apuzzo M, Rolink A, Loetscher M, Hoxie JA, Clark-Lewis I, Melchers F, et al. The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4. Eur J Immunol 1997;27:1788-1793.
31. Delgado E, Finkel V, Baggiolini M, Mackay CR, Steinman RM, Granelli-Piperno A. Mature dendritic cells respond to SDF-1, but not to several beta-chemokines. Immunobiology 1998;198:490-500.
32. Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T. Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci USA 2003;100:5319-5323.
33. Zheng H, Fu G, Dai T, Huang H. Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway. J Cardiovasc Pharmacol 2007;50:274-280.
34. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-56.
35. Kukita A, Kukita T, Ouchida M, Maeda H, Yatsuki H, Kohashi O. Osteoclast-derived zinc finger (OCZF) protein with POZ domain, a possible transcriptional repressor, is involved in osteoclastogenesis. Blood 1999;94:1987-1997.
36. Kukita A, Kukita T, Hata K, Kurisu K, Kohashi O. Heat-Treated osteoblastic cell (ROS17/2.8)-conditioned medium induces the formation of osteoclast-like cells. Bone Miner 1993;23:113-127.
37. Li Y-J, Kukita A, Watanabe T, Takano T, Qu P, Sanematsu K, Ninomiya Y, Kukita T. Nordihydroguaiaretic acid inhibition of NFATct suppresses osteoclastogenesis and arthritis bone destruction in rats. Lab Invest 2012;92:1777-1787.
38. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009;15:42-49.
39. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: Role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008;111:1327-1333.
40. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 2007;109:228-234.
41. Bartholomew A, Patil S, Mackay A, Nelson M, Buyaner D, Hardy W, et al. Baboon mesenchymal stem cells can be genetically modified to secrete human erythropoietin in vivo. Hum Gene Ther 2001;12:1527-1541.
42. Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 2005;35:1482-1490.
43. Fuller K, Lean JM, Bayley KE, Wani MR, Chambers TJ. A role for TGFbeta(1) in osteoclast differentiation and survival. J Cell Sci 2000;113:2445-2453.
44. Chenu C, Pfeilschifter J, Mundy GR, Roodman GD. Transforming growth factor beta inhibits formation of osteoclast-like cells in longterm human marrow cultures. Proc Natl Acad Sci USA 1988;85: 5683-5687.
45. Xu LX, Kukita T, Kukita A, Otsuka T, Niho Y, Iijima T. Interleukin-10 selectively inhibits osteoclastogenesis by inhibiting differentiation of osteoclast progenitors into preosteoclast-like cells in rat bone marrow culture system. J Cell Physiol 1995;165:624-629.
46. Hong MH, Williams H, Jin CH, Pike JW. The inhibitory effect of interleukin-10 on mouse osteoclast formation involves novel tyrosinephosphorylated proteins. J Bone Miner Res 2000;15:911-918.
47. Garaulet G, Altranca A, Torrente M, Escolano A, Lopez-Fontal R, Hortelano S, Redondo JM, Rodriguez A. IL10 released by a new inflammation-regulated Lentiviral system efficiently attenuates zymosan-induced arthritis. Mol Ther 2013;21:119-130.
48. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, et al. Osteoprotegerin: A novel secreted protein involved in the regulation of bone density. Cell 1997;89:309-319.
49. Oshita K, Yamaoka K, Udagawa N, Fukuyo S, Sonomoto K, Maeshima K, et al. Human mesenchymal stem cells inhibit osteoclastogenesis through osteoprotegerin production. Arthritis Rheum 2011;63: 1658-1667.
50. Chamberlain G, Fox J, Ashton B, Middleton J. Concise Review: Mesenchymakl stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007;25:2739-2749.
51. Ringe J, Strassburg S, Neumann K, Endres M, Notter M, Burmester GR, et al. Towards in situ tissue repair: Human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J Cell Biochem 2007;101:135-146.
52. Park MJ, Park HS, Cho ML, Oh HJ, Cho YG, Min SY, 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.
53. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998;393:595-599.