Pre-B cell leukemia homeobox 1 is associated with lupus susceptibility in mice and humans

Journal of Immunology

Volumn 188, Issue 2, 2012, Pages 604-614

  Cuda, Carla M ^a,d   Li, Shiwu ^a   Liang, Shujuan ^a   Yin, Yiming ^a   Potula, Hari Hara S K ^a   Xu, Zhiwei ^a   Sengupta, Mayami ^a   Chen, Yifang ^a,e   Butfiloski, Edward ^a   Baker, Henry ^b   Chang, Lung Ji ^b   Dozmorov, Igor ^c   Sobel, Eric S ^a   Morel, Laurence ^a  

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

^b UNIVERSITY OF FLORIDA   (United States)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA;

ADULT; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE FUNCTION; GENE LOCATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HUMAN; LEUKEMIA CELL LINE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PHENOTYPE; PRE B CELL LEUKEMIA HOMEOBOX 1 GENE; PRIORITY JOURNAL; REGULATOR GENE; REGULATORY T LYMPHOCYTE; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC LUPUS ERYTHEMATOSUS 1A 1 GENE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; UPREGULATION;

ADULT; ANIMALS; DNA-BINDING PROTEINS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNE TOLERANCE; IMMUNOLOGIC MEMORY; JURKAT CELLS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; RNA SPLICING; T-LYMPHOCYTE SUBSETS; TRANSCRIPTION FACTORS;

EID: 84862908808     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002362     Document Type: Article

References (56)

1. Mohan, C., S. Adams, V. Stanik, and S. K. Datta. 1993. Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus. J. Exp. Med. 177: 1367-1381. (Pubitemid 23117127)
2. Datta, S. K. 2003. Major peptide autoepitopes for nucleosome-centered T and B cell interaction in human and murine lupus. Ann. N. Y. Acad. Sci. 987: 79-90. (Pubitemid 36584009)
3. Kong, P. L., J. M. Odegard, F. Bouzahzah, J. Y. Choi, L. D. Eardley, C. E. Zielinski, and J. E. Craft. 2003. Intrinsic T cell defects in systemic autoimmunity. Ann. N. Y. Acad. Sci. 987: 60-67. (Pubitemid 36584007)
4. Crispín, J. C., V. C. Kyttaris, Y. T. Juang, and G. C. Tsokos. 2008. How signaling and gene transcription aberrations dictate the systemic lupus erythematosus T cell phenotype. Trends Immunol. 29: 110-115.
5. La Cava, A. 2008. T-regulatory cells in systemic lupus erythematosus. Lupus 17: 421-425. (Pubitemid 351798720)
6. Humrich, J. Y., H. Morbach, R. Undeutsch, P. Enghard, S. Rosenberger, O.Weigert, L. Kloke, J. Heimann, T. Gaber, S. Brandenburg, et al. 2010. Homeostatic imbalance of regulatory and effector T cells due to IL-2 deprivation amplifies murine lupus. Proc. Natl. Acad. Sci. USA 107: 204-209.
7. Nalbandian, A., J. C. Crispín, and G. C. Tsokos. 2009. Interleukin-17 and systemic lupus erythematosus: current concepts. Clin. Exp. Immunol. 157: 209-215.
8. Morel, L. 2010. Genetics of SLE: evidence from mouse models. Nat. Rev. Rheumatol. 6: 348-357.
9. Haraldsson, M. K., C. A. Louis-Dit-Sully, B. R. Lawson, G. Sternik, M. L. Santiago-Raber, N. R. Gascoigne, A. N. Theofilopoulos, and D. H. Kono. 2008. The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity 28: 40-51.
10. 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. (Pubitemid 40806274)
11. Cuda, C. M., S. Wan, E. S. Sobel, B. P. Croker, and L. Morel. 2007. Murine lupus susceptibility locus Sle1a controls regulatory T cell number and function through multiple mechanisms. J. Immunol. 179: 7439-7447.
12. 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.
13. 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. (Pubitemid 30412772)
14. 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. (Pubitemid 32165576)
15. H17 and regulatory T cells. Nature 441: 235-238.
16. Axtell, R. C., M. S. Webb, S. R. Barnum, and C. Raman. 2004. Cutting edge: critical role for CD5 in experimental autoimmune encephalomyelitis: inhibition of engagement reverses disease in mice. J. Immunol. 173: 2928-2932. (Pubitemid 39141996)
17. Rocke, D. M., and B. Durbin. 2001. A model for measurement error for gene expression arrays. J. Comput. Biol. 8: 557-569. (Pubitemid 34053496)
18. Dozmorov, I. M., and I. Lefkovits. 2009. Internal standard-based analysis of microarray data. 1. Analysis of differential gene expressions. Nucleic Acids Res. 37: 6323-6339.
19. Chung, E. Y., J. Liu, Y. Homma, Y. Zhang, A. Brendolan, M. Saggese, J. Han, R. Silverstein, L. Selleri, and X. Ma. 2007. Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity 27: 952-964. (Pubitemid 350251222)
20. Morel, L., U. H. Rudofsky, J. A. Longmate, J. Schiffenbauer, and E. K. Wakeland. 1994. Polygenic control of susceptibility to murine systemic lupus erythematosus. Immunity 1: 219-229.
21. Srivastava, B., R. C. Lindsley, N. Nikbakht, and D. Allman. 2005. Models for peripheral B cell development and homeostasis. Semin. Immunol. 17: 175-182. (Pubitemid 40488976)
22. Xu, Z., B. Duan, B. P. Croker, and L. Morel. 2006. STAT4 deficiency reduces autoantibody production and glomerulonephritis in a mouse model of lupus. Clin. Immunol. 120: 189-198. (Pubitemid 44080678)
23. Lee, Y. K., R. Mukasa, R. D. Hatton, and C. T. Weaver. 2009. Developmental plasticity of Th17 and Treg cells. Curr. Opin. Immunol. 21: 274-280.
24. + regulatory T cells and inhibits development of Th17 cells by enhancing TGF-β-driven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J. Immunol. 181: 2277-2284.
25. Blenman, K. R., B. Duan, Z. Xu, S. Wan, M. A. Atkinson, T. R. Flotte, B. P. Croker, and L. Morel. 2006. IL-10 regulation of lupus in the NZM2410 murine model. Lab. Invest. 86: 1136-1148. (Pubitemid 44624150)
26. Lu, Q., and M. P. Kamps. 1996. Selective repression of transcriptional activators by Pbx1 does not require the homeodomain. Proc. Natl. Acad. Sci. USA 93: 470-474. (Pubitemid 26038179)
27. Sun, H. B., Y. X. Zhu, T. Yin, G. Sledge, and Y. C. Yang. 1998. MRG1, the product of a melanocyte-specific gene related gene, is a cytokine-inducible transcription factor with transformation activity. Proc. Natl. Acad. Sci. USA 95: 13555-13560. (Pubitemid 28523010)
28. Esser, C., A. Rannug, and B. Stockinger. 2009. The aryl hydrocarbon receptor in immunity. Trends Immunol. 30: 447-454.
29. Wang, K. C., A. L. Cheng, S. E. Chuang, H. C. Hsu, and I. J. Su. 2000. Retinoic acid-induced apoptotic pathway in T-cell lymphoma: identification of four groups of genes with differential biological functions. Exp. Hematol. 28: 1441-1450.
30. Nagy, G., A. Koncz, and A. Perl. 2005. T- and B-cell abnormalities in systemic lupus erythematosus. Crit. Rev. Immunol. 25: 123-140. (Pubitemid 40910585)
31. 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. (Pubitemid 29428806)
32. Benson, M. J., K. Pino-Lagos, M. Rosemblatt, and R. J. Noelle. 2007. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204: 1765-1774. (Pubitemid 47236315)
33. + regulatory T cells via a TGF-b and retinoic acid-dependent mechanism. J. Exp. Med. 204: 1757-1764.
34. H17 and regulatory T cell differentiation mediated by retinoic acid. Science 317: 256-260.
35. Sun, C. M., J. A. Hall, R. B. Blank, N. Bouladoux, M. Oukka, J. R. Mora, and Y. Belkaid. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204: 1775-1785. (Pubitemid 47236316)
36. + regulatory T cells by retinoic acid. J. Immunol. 183: 4119-4126.
37. + regulatory T cells. J. Immunol. 179: 3724-3733.
38. + Treg cell conversion of naive T cells. Immunity 30: 471-472, author reply 472-473.
39. hi cells. Immunity 29: 758-770.
40. Kinoshita, K., B. S. Yoo, Y. Nozaki, M. Sugiyama, S. Ikoma, M. Ohno, M. Funauchi, and A. Kanamaru. 2003. Retinoic acid reduces autoimmune renal injury and increases survival in NZB/W F1 mice. J. Immunol. 170: 5793-5798. (Pubitemid 36617874)
41. Pérez de Lema, G., F. J. Lucio-Cazaña, A. Molina, B. Luckow, H. Schmid, C. de Wit, V. Moreno-Manzano, B. Banas, F. Mampaso, and D. Schlöndorff. 2004. Retinoic acid treatment protects MRL/lpr lupus mice from the development of glomerular disease. Kidney Int. 66: 1018-1028. (Pubitemid 39121006)
42. Kinoshita, K., K. Kishimoto, H. Shimazu, Y. Nozaki, M. Sugiyama, S. Ikoma, and M. Funauchi. 2010. Successful treatment with retinoids in patients with lupus nephritis. Am. J. Kidney Dis. 55: 344-347.
43. 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.
44. Berkes, C. A., D. A. Bergstrom, B. H. Penn, K. J. Seaver, P. S. Knoepfler, and S. J. Tapscott. 2004. Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol. Cell 14: 465-477. (Pubitemid 38648800)
45. Knoepfler, P. S., and M. P. Kamps. 1997. The Pbx family of proteins is strongly upregulated by a post-transcriptional mechanism during retinoic acid-induced differentiation of P19 embryonal carcinoma cells. Mech. Dev. 63: 5-14. (Pubitemid 27214498)
46. Qin, P., J. M. Haberbusch, K. J. Soprano, and D. R. Soprano. 2004. Retinoic acid regulates the expression of PBX1, PBX2, and PBX3 in P19 cells both transcriptionally and post-translationally. J. Cell. Biochem. 92: 147-163.
47. Mojsin, M., and M. Stevanovic. 2010. PBX1 and MEIS1 up-regulate SOX3 gene expression by direct interaction with a consensus binding site within the basal promoter region. Biochem. J. 425: 107-116.
48. Qin, P., R. Cimildoro, D. M. Kochhar, K. J. Soprano, and D. R. Soprano. 2002. PBX, MEIS, and IGF-I are potential mediators of retinoic acid-induced proximodistal limb reduction defects. Teratology 66: 224-234. (Pubitemid 35266238)
49. Qin, P., J. M. Haberbusch, Z. Zhang, K. J. Soprano, and D. R. Soprano. 2004. Pre-B cell leukemia transcription factor (PBX) proteins are important mediators for retinoic acid-dependent endodermal and neuronal differentiation of mouse embryonal carcinoma P19 cells. J. Biol. Chem. 279: 16263-16271. (Pubitemid 38509320)
50. 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. (Pubitemid 351598079)
51. Penkov, D., M. Palazzolo, A. Mondino, and F. Blasi. 2008. Cytosolic sequestration of Prep1 influences early stages of T cell development. PLoS ONE 3: e2424.
52. Jensen, C. J., B. J. Oldfield, and J. P. Rubio. 2009. Splicing, cis genetic variation and disease. Biochem. Soc. Trans. 37: 1311-1315.
53. Araki, M., D. Chung, S. Liu, D. B. Rainbow, G. Chamberlain, V. Garner, K. M. D. Hunter, L. Vijayakrishnan, L. B. Peterson, M. Oukka, et al. 2009. Genetic evidence that the differential expression of the ligand-independent isoform of CTLA-4 is the molecular basis of the Idd5.1 type 1 diabetes region in nonobese diabetic mice. J. Immunol. 183: 5146-5157.
54. Kumar, K. R., L. Li, M. Yan, M. Bhaskarabhatla, A. B. Mobley, C. Nguyen, J. M. Mooney, J. D. Schatzle, E. K. Wakeland, and C. Mohan. 2006. Regulation of B cell tolerance by the lupus susceptibility gene Ly108. Science 312: 1665-1669. (Pubitemid 43902668)
55. Keszei, M., C. Detre, S. T. Rietdijk, P. Muñoz, X. Romero, S. B. Berger, S. Calpe, G. Liao,W. Castro, A. Julien, et al. 2011. A novel isoform of the Ly108 gene ameliorates murine lupus. J. Exp. Med. 208: 811-822.
56. Tsao, B. P. 2003. The genetics of human systemic lupus erythematosus. Trends Immunol. 24: 595-602. (Pubitemid 37338528)