Comparative immunomodulatory properties of adipose-derived mesenchymal stem cells conditioned media from BALB/c, C57BL/6, and DBA mouse strains

Journal of Cellular Biochemistry

Volumn 114, Issue 4, 2013, Pages 955-965

  Hashemi, Seyed Mahmoud ^a   Hassan, Zuhair Mohammad ^a   Pourfathollah, Ali Akbar ^a   Soudi, Sara ^a   Shafiee, Abbas ^b   Soleimani, Masoud ^a  

^a TARBIAT MODARES UNIVERSITY   (Iran)

^b STEM CELL TECHNOLOGY RESEARCH CENTER   (Iran)

Author keywords

ADIPOSE DERIVED MESENCHYMAL STEM CELLS; CONDITIONED MEDIA; IMMUNOMODULATORY PROPERTIES; MOUSE STRAINS

Indexed keywords

5' NUCLEOTIDASE; ATAXIN 1; BETA1 INTEGRIN; ENDOGLIN; HERMES ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; NITRIC OXIDE; THY 1 ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN RECEPTOR;

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; COLONY FORMING UNIT; COMPARATIVE STUDY; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; DBA MOUSE; ENZYME SYNTHESIS; IMMUNOASSAY; IMMUNOMODULATION; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; STEM CELL TRANSPLANTATION;

ADIPOSE TISSUE; ANIMALS; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; IMMUNOLOGIC FACTORS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERLEUKIN-10; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED DBA; NITRIC OXIDE; SPECIES SPECIFICITY; SPLEEN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84874283661     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24437     Document Type: Article

References (50)

1. Barzilay R, Sadan O, Melamed E, Offen D,. 2009. Comparative characterization of bone marrow-derived mesenchymal stromal cells from four different rat strains. Cytotherapy 11: 435-442.
2. Batten P, Sarathchandra P, Antoniw JW, Tay SS, Lowdell MW, Taylor PM, Yacoub MH,. 2006. Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: Relevance to tissue engineering human heart valves. Tissue Eng 12: 2263-2273.
3. Bouffi C, Bony C, Courties G, Jorgensen C, Noel D,. 2010. IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS ONE 5: e14247.
4. Che N, Li X, Zhou S, Liu R, Shi D, Lu L, Sun L,. 2012. Umbilical cord mesenchymal stem cells suppress B-cell proliferation and differentiation. Cell Immunol 274: 46-53.
5. Choi EW, Shin IS, Lee HW, Park SY, Park JH, Nam MH, Kim JS, Woo SK, Yoon EJ, Kang SK, Ra JC, Youn HY, Hong SH,. 2011. Transplantation of CTLA4Ig gene-transduced adipose tissue-derived mesenchymal stem cells reduces inflammatory immune response and improves Th1/Th2 balance in experimental autoimmune thyroiditis. J Gene Med 13: 3-16.
6. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E, Gini B, Bach SD, Martinello M, Bifari F, Galie M, Turano E, Budui S, Sbarbati A, Krampera M, Bonetti B,. 2009. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 27: 2624-2635.
7. Cutler AJ, Limbani V, Girdlestone J, Navarrete CV,. 2010. Umbilical cord-derived mesenchymal stromal cells modulate monocyte function to suppress T cell proliferation. J Immunol 185: 6617-6623.
8. Darlington PJ, Boivin MN, Renoux C, Francois M, Galipeau J, Freedman MS, Atkins HL, Cohen JA, Solchaga L, Bar-Or A,. 2010. Reciprocal Th1 and Th17 regulation by mesenchymal stem cells: Implication for multiple sclerosis. Ann Neurol 68: 540-545.
9. De Vooght V, Vanoirbeek JAJ, Luyts K, Haenen S, Nemery B, Hoet PHM,. 2010. Choice of mouse strain influences the outcome in a mouse model of chemical-induced asthma. PLoS ONE 5: e12581.
10. DelaRosa O, Lombardo E, Beraza A, Mancheno-Corvo P, Ramirez C, Menta R, Rico L, Camarillo E, Garcia L, Abad JL, Trigueros C, Delgado M, Buscher D,. 2009. Requirement of IFN-gamma-mediated indoleamine 2,3-dioxygenase expression in the modulation of lymphocyte proliferation by human adipose-derived stem cells. Tissue Eng Part A 15: 2795-2806.
11. Duffy MM, Pindjakova J, Hanley SA, McCarthy C, Weidhofer GA, Sweeney EM, English K, Shaw G, Murphy JM, Barry FP, Mahon BP, Belton O, Ceredig R, Griffin MD,. 2011. Mesenchymal stem cell inhibition of T-helper 17 cell-differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor. Eur J Immunol 41: 2840.
12. English K, French A, Wood KJ,. 2010. Mesenchymal stromal cells: Facilitators of successful transplantation ? Cell Stem Cell 7: 431-442.
13. Ge W, Jiang J, Arp J, Liu W, Garcia B, Wang H,. 2010. Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression. Transplantation 90: 1312-1320.
14. Gimble JM, Bunnell BA, Chiu ES, Guilak F,. 2011. Concise review: Adipose-derived stromal vascular fraction cells and stem cells: Let's not get lost in translation. Stem Cells 29: 749-754.
15. Ivanova-Todorova E, Bochev I, Mourdjeva M, Dimitrov R, Bukarev D, Kyurkchiev S, Tivchev P, Altunkova I, Kyurkchiev DS,. 2009. Adipose tissue-derived mesenchymal stem cells are more potent suppressors of dendritic cells differentiation compared to bone marrow-derived mesenchymal stem cells. Immunol Lett 126: 37-42.
16. Jarvinen L, Badri L, Wettlaufer S, Ohtsuka T, Standiford TJ, Toews GB, Pinsky DJ, Peters-Golden M, Lama VN,. 2008. Lung resident mesenchymal stem cells isolated from human lung allografts inhibit T cell proliferation via a soluble mediator. J Immunol 181: 4389-4396.
17. Kang JW, Kang KS, Koo HC, Park JR, Choi EW, Park YH,. 2008. Soluble factors-mediated immunomodulatory effects of canine adipose tissue-derived mesenchymal stem cells. Stem Cells Dev 17: 681-693.
18. Keyser KA, Beagles KE, Kiem HP,. 2007. Comparison of mesenchymal stem cells from different tissues to suppress T-cell activation. Cell Transplant 16: 555-562.
19. Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, Heifetz A, Ludlow JW, Stricker DM, Potiny S, Green P, Halvorsen YD, Cheatham B, Storms RW, Gimble JM,. 2007. Cytokine profile of human adipose-derived stem cells: Expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol 212: 702-709.
20. Lee JM, Jung J, Lee HJ, Cho KJ, Hwang SG, Kim GJ,. 2012. Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells. Int Immunopharmacol 13: 219-224.
21. Li Y, Zhang C, Xiong F, Yu MJ, Peng FL, Shang YC, Zhao CP, Xu YF, Liu ZS, Zhou C, Wu JL,. 2008. Comparative study of mesenchymal stem cells from C57BL/10 and mdx mice. BMC Cell Biol 9: 24.
22. Li FR, Wang XG, Deng CY, Qi H, Ren LL, Zhou HX,. 2010. Immune modulation of co-transplantation mesenchymal stem cells with islet on T and dendritic cells. Clin Exp Immunol 161: 357-363.
23. Lu X, Liu T, Gu L, Huang C, Zhu H, Meng W, Xi Y, Li S, Liu Y,. 2009. Immunomodulatory effects of mesenchymal stem cells involved in favoring type 2 T cell subsets. Transpl Immunol 22: 55-61.
24. Mahanonda R, Sa-Ard-Iam N, Montreekachon P, Pimkhaokham A, Yongvanichit K, Fukuda MM, Pichyangkul S,. 2007. IL-8 and IDO expression by human gingival fibroblasts via TLRs. J Immunol 178: 1151-1157.
25. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D,. 2004. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 103: 4619-4621.
26. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM,. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164: 6166-6173.
27. Mohseny AB, Hogendoorn PC,. 2011. Concise review: Mesenchymal tumors: When stem cells go mad. Stem Cells 29: 397-403.
28. Nasef A, Mazurier C, Bouchet S, Francois S, Chapel A, Thierry D, Gorin NC, Fouillard L,. 2008. Leukemia inhibitory factor: Role in human mesenchymal stem cells mediated immunosuppression. Cell Immunol 253: 16-22.
29. Nauta AJ, Fibbe WE,. 2007. Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506.
30. Nemeth K, Keane-Myers A, Brown JM, Metcalfe DD, Gorham JD, Bundoc VG, Hodges MG, Jelinek I, Madala S, Karpati S, Mezey E,. 2010. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci U S A 107: 5652-5657.
31. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ,. 2004. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103: 1662-1668.
32. Phinney DG, Kopen G, Isaacson RL, Prockop DJ,. 1999. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: Variations in yield, growth, and differentiation. J Cell Biochem 72: 570-585.
33. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, Taureau C, Cousin B, Abbal M, Laharrague P, Penicaud L, Casteilla L, Blancher A,. 2005. Immunomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br J Haematol 129: 118-129.
34. Rafei M, Campeau PM, Aguilar-Mahecha A, Buchanan M, Williams P, Birman E, Yuan S, Young YK, Boivin M-N, Forner K, Basik M, Galipeau J,. 2009. Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. J Immunol 182: 5994-6002.
35. Rasmusson I, Ringden O, Sundberg B, Le Blanc K,. 2005. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res 305: 33-41.
36. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K,. 2007. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109: 228-234.
37. Selmani Z, Naji A, Gaiffe E, Obert L, Tiberghien P, Rouas-Freiss N, Carosella ED, Deschaseaux F,. 2009. HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation 87: S62-S66.
38. Sheng H, Wang Y, Jin Y, Zhang Q, Zhang Y, Wang L, Shen B, Yin S, Liu W, Cui L, Li N,. 2008. A critical role of IFNgamma in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Res 18: 846-857.
39. Shi M, Liu ZW, Wang FS,. 2011. Immunomodulatory properties and therapeutic application of mesenchymal stem cells. Clin Exp Immunol 164: 1-8.
40. Sioud M, Mobergslien A, Boudabous A, Floisand Y,. 2011. Mesenchymal stem cell-mediated T cell suppression occurs through secreted galectins. Int J Oncol 38: 385-390.
41. Steinman L,. 2007. A brief history of TH17, the first major revision in the TH1/TH2 hypothesis of T cell-mediated tissue damage. Nat Med 13: 139-145.
42. Sudres M, Norol F, Trenado A, Gregoire S, Charlotte F, Levacher B, Lataillade JJ, Bourin P, Holy X, Vernant JP, Klatzmann D, Cohen JL,. 2006. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol 176: 7761-7767.
43. Sung JH, Yang HM, Park JB, Choi GS, Joh JW, Kwon CH, Chun JM, Lee SK, Kim SJ,. 2008. Isolation and characterization of mouse mesenchymal stem cells. Transplant Proc 40: 2649-2654.
44. Svobodova E, Krulova M, Zajicova A, Pokorna K, Prochazkova J, Trosan P, Holan V,. 2011. The role of mouse mesenchymal stem cells in differentiation of naive T-cells into anti-inflammatory regulatory T-cell or proinflammatory helper T-cell 17 population. Stem Cells Dev 21: 901-910.
45. Tatara R, Ozaki K, Kikuchi Y, Hatanaka K, Oh I, Meguro A, Matsu H, Sato K, Ozawa K,. 2011. Mesenchymal stromal cells inhibit Th17 but not regulatory T-cell differentiation. Cytotherapy 13: 686.
46. Uccelli A, Moretta L, Pistoia V,. 2008. Mesenchymal stem cells in health and disease. Nat Rev Immunol 8: 726-736.
47. Yamamoto N, Akamatsu H, Hasegawa S, Yamada T, Nakata S, Ohkuma M, Miyachi E-I, Marunouchi T, Matsunaga K,. 2007. Isolation of multipotent stem cells from mouse adipose tissue. J Dermatol Sci 48: 43-52.
48. Yanez R, Oviedo A, Aldea M, Bueren JA, Lamana ML,. 2010. Prostaglandin E2 plays a key role in the immunosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res 316: 3109-3123.
49. Yang SH, Park MJ, Yoon IH, Kim SY, Hong SH, Shin JY, Nam HY, Kim YH, Kim B, Park CG,. 2009. Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10. Exp Mol Med 41: 315-324.
50. Yoo KH, Jang IK, Lee MW, Kim HE, Yang MS, Eom Y, Lee JE, Kim YJ, Yang SK, Jung HL, Sung KW, Kim CW, Koo HH,. 2009. Comparison of immunomodulatory properties of mesenchymal stem cells derived from adult human tissues. Cell Immunol 259: 150-156.