The murine Pbx1-d lupus susceptibility allele accelerates mesenchymal stem cell differentiation and impairs their immunosuppressive function

Journal of Immunology

Volumn 194, Issue 1, 2015, Pages 43-55

  Lu, Shun ^a   Zeumer, Leilani ^a   Sorensen, Heather ^b   Yang, Hong ^a   Ng, Yunfai ^a   Yu, Fahong ^b   Riva, Alberto ^b   Croker, Byron ^a   Wallet, Shannon ^b   Morel, Laurence ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN; INTERLEUKIN 2; PRE B CELL LEUKEMIA HOMEOBOX 1 D PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; ISOPROTEIN; PBX1 PROTEIN, MOUSE; TOLL LIKE RECEPTOR;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC SUSCEPTIBILITY; IMMUNE DEFICIENCY; IMMUNOGLOBULIN PRODUCTION; IMMUNOPHENOTYPING; INFLAMMATION; INNATE IMMUNITY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOBLAST; PATHOGENESIS; PBX1 D GENE; SLE1A1 GENE; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; AUTOIMMUNITY; BIOSYNTHESIS; C57BL MOUSE; CYTOLOGY; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MESENCHYMAL STROMA CELL; PATHOLOGY; SECRETION (PROCESS);

ANIMALS; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; GENE EXPRESSION; HOMEODOMAIN PROTEINS; IMMUNE TOLERANCE; IMMUNOGLOBULINS; IMMUNOLOGIC MEMORY; INFLAMMATION; INTERLEUKIN-2; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; OSTEOBLASTS; PROTEIN ISOFORMS; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTORS;

EID: 84919625457     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401851     Document Type: Article

References (50)

1. Morel, L. 2010. Genetics of SLE: Evidence from mouse models. Nat. Rev. Rheumatol. 6: 348-357.
2. Morel, L. 2012. Mapping lupus susceptibility genes in the NZM2410 mouse model. Adv. Immunol. 115: 113-139.
3. Morel, L., B. P. Croker, K. R. Blenman, C. Mohan, G. Huang, G. Gilkeson, and E. K. Wakeland. 2000. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc. Natl. Acad. Sci. USA 97: 6670-6675.
4. Cuda, C. M., S. Li, S. Liang, Y. Yin, H. H. Potula, Z. Xu, M. Sengupta, Y. Chen, E. Butfiloski, H. Baker, et al. 2012. Pre-B cell leukemia homeobox 1 is associated with lupus susceptibility in mice and humans. J. Immunol. 188: 604-614.
5. Mohan, C., E. Alas, L. Morel, P. Yang, and E. K. Wakeland. 1998. Genetic dissection of SLE pathogenesis. Sle1 on murine chromosome 1 leads to a selective loss of tolerance to H2A/H2B/DNA subnucleosomes. J. Clin. Invest. 101: 1362-1372.
6. Chen, Y., C. Cuda, and L. Morel. 2005. Genetic determination of T cell help in loss of tolerance to nuclear antigens. J. Immunol. 174: 7692-7702.
7. Cuda, C. M., L. Zeumer, E. S. Sobel, B. P. Croker, and L. Morel. 2010. Murine lupus susceptibility locus Sle1a requires the expression of two sub-loci to induce inflammatory T cells. Genes Immun. 11: 542-553.
8. Morel, L., X. H. Tian, B. P. Croker, and E. K. Wakeland. 1999. Epistatic modifiers of autoimmunity in a murine model of lupus nephritis. Immunity 11: 131-139.
9. Morel, L., K. R. Blenman, B. P. Croker, and E. K. Wakeland. 2001. The major murine systemic lupus erythematosus susceptibility locus, Sle1, is a cluster of functionally related genes. Proc. Natl. Acad. Sci. USA 98: 1787-1792.
10. Mann, R. S., and S. K. Chan. 1996. Extra specificity from extradenticle: The partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet. 12: 258-262.
11. Sengupta, M., S. Liang, H. H. S. Potula, L. J. Chang, and L. Morel. 2012. The SLE-Associated Pbx1-d isoform acts as a dominant-negative transcriptional regulator. Genes Immun. 13: 653-657.
12. Ficara, F., M. J. Murphy, M. Lin, and M. L. Cleary. 2008. Pbx1 regulates selfrenewal of long-term hematopoietic stem cells by maintaining their quiescence. Cell Stem Cell 2: 484-496.
13. Gordon, J. A., M. Q. Hassan, S. Saini, M. Montecino, A. J. van Wijnen, G. S. Stein, J. L. Stein, and J. B. Lian. 2010. Pbx1 represses osteoblastogenesis by blocking Hoxa10-mediated recruitment of chromatin remodeling factors. Mol. Cell. Biol. 30: 3531-3541.
14. Djouad, F., C. Bouffi, S. Ghannam, D. Noël, and C. Jorgensen. 2009. Mesenchymal stem cells: Innovative therapeutic tools for rheumatic diseases. Nat. Rev. Rheumatol. 5: 392-399.
15. Ghannam, S., C. Bouffi, F. Djouad, C. Jorgensen, and D. Noël. 2010. Immunosuppression by mesenchymal stem cells: Mechanisms and clinical applications. Stem Cell Res Ther 1: 2.
16. Collins, E., and G. Gilkeson. 2013. Hematopoetic and mesenchymal stem cell transplantation in the treatment of refractory systemic lupus erythematosus- where are we now? Clin. Immunol. 148: 328-334.
17. MacDonald, G. I. A., A. Augello, and C. De Bari. 2011. Role of mesenchymal stem cells in reestablishing immunologic tolerance in autoimmune rheumatic diseases. Arthritis Rheum. 63: 2547-2557.
18. Sun, L., D. Wang, J. Liang, H. Zhang, X. Feng, H. Wang, B. Hua, B. Liu, S. Ye, X. Hu, et al. 2010. Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum. 62: 2467-2475.
19. Nie, Y., C. Lau, A. Lie, G. Chan, and M. Mok. 2010. Defective phenotype of mesenchymal stem cells in patients with systemic lupus erythematosus. Lupus 19: 850-859.
20. Li, X., L. Liu, D. Meng, D. Wang, J. Zhang, D. Shi, H. Liu, H. Xu, L. Lu, and L. Sun. 2012. Enhanced apoptosis and senescence of bone-marrow-derived mesenchymal stem cells in patients with systemic lupus erythematosus. Stem Cells Dev. 21: 2387-2394.
21. Bocelli-Tyndall, C., L. Bracci, G. Spagnoli, A. Braccini, M. Bouchenaki, R. Ceredig, V. Pistoia, I. Martin, and A. Tyndall. 2007. Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and autoimmune disease patients reduce the proliferation of autologous- and allogeneic- stimulated lymphocytes in vitro. Rheumatology (Oxford) 46: 403-408.
22. Sun, L., K. Akiyama, H. Zhang, T. Yamaza, Y. Hou, S. Zhao, T. Xu, A. Le, and S. Shi. 2009. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 27: 1421-1432.
23. Zhou, K., H. Zhang, O. Jin, X. Fen, G. Yao, Y. Hou, and L. Sun. 2008. Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr mice. Cell. Mol. Immunol., 5: 417-424.
24. Gu, F., I. Molano, P. Ruiz, L. Sun, and G. S. Gilkeson. 2012. Differential effect of allogeneic versus syngeneic mesenchymal stem cell transplantation in MRL/ lpr and (NZB/NZW)F1 mice. Clin. Immunol. 145: 142-152.
25. Akiyama, K., Y.-O. You, T. Yamaza, C. Chen, L. Tang, Y. Jin, X.-D. Chen, S. Gronthos, and S. Shi. 2012. Characterization of bone marrow derived mesenchymal stem cells in suspension. Stem Cell Res. Ther. 3: 40.
26. Youd, M., C. Blickarz, L. Woodworth, T. Touzjian, A. Edling, J. Tedstone, M. Ruzek, R. Tubo, J. Kaplan, and T. Lodie. 2010. Allogeneic mesenchymal stem cells do not protect NZB3NZW F1 mice from developing lupus disease. Clin. Exp. Immunol. 161: 176-186.
27. Schena, F., C. Gambini, A. Gregorio, M. Mosconi, D. Reverberi, M. Gattorno, S. Casazza, A. Uccelli, L. Moretta, A. Martini, and E. Traggiai. 2010. Interferong- dependent inhibition of B cell activation by bone marrow-derived mesenchymal stem cells in a murine model of systemic lupus erythematosus. Arthritis Rheum. 62: 2776-2786.
28. Choi, E. W., I. S. Shin, S. Y. Park, J. H. Park, J. S. Kim, E. J. Yoon, S. K. Kang, J. C. Ra, and S. H. Hong. 2012. Reversal of serologic, immunologic, and histologic dysfunction in mice with systemic lupus erythematosus by long-term serial adipose tissue-derived mesenchymal stem cell transplantation. Arthritis Rheum. 64: 243-253.
29. Abumaree, M., M. Al Jumah, R. A. Pace, and B. Kalionis. 2012. Immunosuppressive properties of mesenchymal stem cells. Stem Cell Rev. 8: 375-392.
30. Yao, J. Q. Y., and F. Yu. 2011. DEB: A web interface for RNA-seq digital gene expression analysis. Bioinformation 7: 44-45.
31. Xu, Z., C. M. Cuda, B. P. Croker, and L. Morel. 2011. The NZM2410-derived lupus susceptibility locus Sle2c1 increases Th17 polarization and induces nephritis in fas-deficient mice. Arthritis Rheum. 63: 764-774.
32. Nakajima, H., M. Ito, Y. Morikawa, T. Komori, Y. Fukuchi, F. Shibata, S. Okamoto, and T. Kitamura. 2009. Wnt modulators, SFRP-1, and SFRP-2 are expressed in osteoblasts and differentially regulate hematopoietic stem cells. Biochem. Biophys. Res. Commun. 390: 65-70.
33. Tian, G., J.-L. Li, D.-G. Wang, and D. Zhou. 2014. Targeting IL-10 in autoimmune diseases. Cell Biochem. Biophys. 70: 37-49.
34. Wang, S., L. Ding, S. S. Liu, C. Wang, R. X. Leng, G. M. Chen, Y. G. Fan, H. F. Pan, and D. Q. Ye. 2012. IL-33: A potential therapeutic target in autoimmune diseases. J. Investig. Med. 60: 1151-1156.
35. Koga, T., C. M. Hedrich, M. Mizui, N. Yoshida, K. Otomo, L. A. Lieberman, T. Rauen, J. C. Crispín, and G. C. Tsokos. 2014. CaMK4-dependent activation of AKT/mTOR and CREM-A underlies autoimmunity-Associated Th17 imbalance. J. Clin. Invest. 124: 2234-2245.
36. Villarreal, D. O., and D. B. Weiner. 2014. Interleukin 33: A switch-hitting cytokine. Curr. Opin. Immunol. 28: 102-106.
37. Wakeland, E. K., K. Liu, R. R. Graham, and T. W. Behrens. 2001. Delineating the genetic basis of systemic lupus erythematosus. Immunity 15: 397-408.
38. Wang, H., M. Wu, and Y. Liu. 2012. Are mesenchymal stem cells major sources of safe signals in immune system? Cell. Immunol. 272: 112-116.
39. Marigo, I., and F. Dazzi. 2011. The immunomodulatory properties of mesenchymal stem cells. Semin. Immunopathol. 33: 593-602.
40. Hayashi, T. 2010. Therapeutic strategies for SLE involving cytokines: Mechanism-oriented therapies especially IFN-g targeting gene therapy. J. Biomed. Biotechnol. 2010: 461641.
41. Krampera, M. 2011. Mesenchymal stromal cell "licensing": A multistep process. Leukemia 25: 1408-1414.
42. Sang, A., Y. Yin, Y.-Y. Zheng, and L. Morel. 2012. Animal models of molecular pathology: Systemic lupus erythematosus. Prog. Mol. Biol. Transl. Sci. 105: 321-370.
43. Carrion, F., E. Nova, C. Ruiz, F. Diaz, C. Inostroza, D. Rojo, G. Mönckeberg, and F. E. Figueroa. 2010. Autologous mesenchymal stem cell treatment increased T regulatory cells with no effect on disease activity in two systemic lupus erythematosus patients. Lupus 19: 317-322.
44. Brinster, C., and E. M. Shevach. 2008. Costimulatory effects of IL-1 on the expansion/differentiation of CD4+CD25+Foxp3+ and CD4+CD25+Foxp32 T cells. J. Leukoc. Biol. 84: 480-487.
45. Triplett, T. A., B. D. Curti, P. R. Bonafede, W. L. Miller, E. B. Walker, and A. D. Weinberg. 2012. Defining a functionally distinct subset of human memory CD4+ T cells that are CD25POS and FOXP3NEG. Eur. J. Immunol. 42: 1893-1905.
46. Ma, X., N. Che, Z. Gu, J. Huang, D. Wang, J. Liang, Y. Hou, G. Gilkeson, L. Lu, and L. Sun. 2013. Allogenic mesenchymal stem cell transplantation ameliorates nephritis in lupus mice via inhibition of B-cell activation. Cell Transplant. 22: 2279-2290.
47. Cigni, A., P. V. Pileri, R. Faedda, P. Gallo, A. Sini, A. E. Satta, R. Marras, E. Carta, D. Argiolas, I. Rum, and A. Masala. 2014. Interleukin 1, interleukin 6, interleukin 10, and tumor necrosis factor a in active and quiescent systemic lupus erythematosus. J. Investig. Med. 62: 825-829.
48. Song, G. G., J.-H. Kim, Y. H. Seo, S. J. Choi, J. D. Ji, and Y. H. Lee. 2014. Associations between interleukin 1 polymorphisms and susceptibility to systemic lupus erythematosus: A meta-Analysis. Hum. Immunol. 75: 105-112.
49. Li, P., S.-H. Li, J. Wu, W.-F. Zang, S. Dhingra, L. Sun, R. D. Weisel, and R.-K. Li. 2013. Interleukin-6 downregulation with mesenchymal stem cell differentiation results in loss of immunoprivilege. J. Cell. Mol. Med. 17: 1136-1145.
50. Deng, Y., S. Yi, G. Wang, J. Cheng, Y. Zhang, W. Chen, Y. Tai, S. Chen, G. Chen, W. Liu, et al. 2014. Umbilical cord-derived mesenchymal stem cells instruct dendritic cells to acquire tolerogenic phenotypes through the IL-6- mediated upregulation of SOCS1. Stem Cells Dev. 23: 2080-2092.