Cyclin-dependent kinase inhibitor Cdkn2c deficiency promotes B1a cell expansion and autoimmunity in a mouse model of lupus

Journal of Immunology

Volumn 189, Issue 6, 2012, Pages 2931-2940

  Potula, Hari Hara S K ^a   Xu, Zhiwei ^a   Zeumer, Leilani ^a   Sang, Allison ^a   Croker, Byron P ^a,b   Morel, Laurence ^a  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINUCLEAR ANTIBODY; CYCLIN D2; CYCLIN DEPENDENT KINASE INHIBITOR 2C; DOUBLE STRANDED DNA ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 17;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; B1A CELL; CDKN2C GENE; CELL EXPANSION; CELL SIZE; CONTROLLED STUDY; CYCLIN DEPENDENT KINASE INHIBITOR 2C DEFICIENCY; CYTOKINE PRODUCTION; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC SUSCEPTIBILITY; HUMORAL IMMUNITY; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPHADENOPATHY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; SLE2C1 GENE;

ANIMALS; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; CYCLIN-DEPENDENT KINASE INHIBITOR P18; CYCLIN-DEPENDENT KINASES; DISEASE MODELS, ANIMAL; IMMUNOPHENOTYPING; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, INBRED NZB; MICE, KNOCKOUT; MICE, TRANSGENIC;

EID: 84866150900     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200556     Document Type: Article

References (42)

1. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300. (Pubitemid 34293426)
2. Piatelli, M. J., D. Tanguay, T. L. Rothstein, and T. C. Chiles. 2003. Cell cycle control mechanisms in B-1 and B-2 lymphoid subsets. Immunol. Res. 27: 31-52.
3. Solvason, N., W. W. Wu, D. Parry, D. Mahony, E. W. Lam, J. Glassford, G. G. Klaus, P. Sicinski, R. Weinberg, Y. J. Liu, et al. 2000. Cyclin D2 is essential for BCR-mediated proliferation and CD5 B cell development. Int. Immunol. 12: 631-638. (Pubitemid 30248896)
4. Mataraza, J. M., J. R. Tumang, M. R. Gumina, S. M. Gurdak, T. L. Rothstein, and T. C. Chiles. 2006. Disruption of cyclin D3 blocks proliferation of normal B-1a cells, but loss of cyclin D3 is compensated by cyclin D2 in cyclin D3-deficient mice. J. Immunol. 177: 787-795. (Pubitemid 44036578)
5. Tanguay, D. A., T. P. Colarusso, S. Pavlovic, M. Irigoyen, R. G. Howard, J. Bartek, T. C. Chiles, and T. L. Rothstein. 1999. Early induction of cyclin D2 expression in phorbol ester-responsive B-1 lymphocytes. J. Exp. Med. 189: 1685-1690. (Pubitemid 29272684)
6. Duan, B., and L. Morel. 2006. Role of B-1a cells in autoimmunity. Autoimmun. Rev. 5: 403-408. (Pubitemid 44143033)
7. Enghard, P., J. Y. Humrich, V. T. Chu, E. Grussie, F. Hiepe, G. R. Burmester, A. Radbruch, C. Berek, and G. Riemekasten. 2010. Class switching and consecutive loss of dsDNA-reactive B1a B cells from the peritoneal cavity during murine lupus development. Eur. J. Immunol. 40: 1809-1818.
8. Moreth, K., R. Brodbeck, A. Babelova, N. Gretz, T. Spieker, J. Zeng-Brouwers, J. Pfeilschifter, M. F. Young, R. M. Schaefer, and L. Schaefer. 2010. The proteoglycan biglycan regulates expression of the B cell chemoattractant CXCL13 and aggravates murine lupus nephritis. J. Clin. Invest. 120: 4251-4272.
9. Mohan, C., L. Morel, P. Yang, and E. K. Wakeland. 1998. Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupusprone mice. Arthritis Rheum. 41: 1652-1662. (Pubitemid 28459925)
10. Zhong, X., W. Gao, N. Degauque, C. Bai, Y. Lu, J. Kenny, M. Oukka, T. B. Strom, and T. L. Rothstein. 2007. Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur. J. Immunol. 37: 2400-2404. (Pubitemid 47423610)
11. Griffin, D. O., N. E. Holodick, and T. L. Rothstein. 2011. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70-. J. Exp. Med. 208: 67-80.
12. Griffin, D. O., and T. L. Rothstein. 2011. A small CD11b(+) human B1 cell subpopulation stimulates T cells and is expanded in lupus. J. Exp. Med. 208: 2591-2598.
13. Xu, Z., E. J. Butfiloski, E. S. Sobel, and L. Morel. 2004. Mechanisms of peritoneal B-1a cells accumulation induced by murine lupus susceptibility locus Sle2. J. Immunol. 173: 6050-6058. (Pubitemid 39487760)
14. Xu, Z., B. Duan, B. P. Croker, E. K. Wakeland, and L. Morel. 2005. Genetic dissection of the murine lupus susceptibility locus Sle2: contributions to increased peritoneal B-1a cells and lupus nephritis map to different loci. J. Immunol. 175: 936-943. (Pubitemid 41094977)
15. Xu, Z., H. H. Potula, A. Vallurupalli, D. Perry, H. Baker, B. P. Croker, I. Dozmorov, and L. Morel. 2011. Cyclin-dependent kinase inhibitor Cdkn2c regulates B cell homeostasis and function in the NZM2410-derived murine lupus susceptibility locus Sle2c1. J. Immunol. 186: 6673-6682.
16. 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.
17. Sherr, C. J., and J. M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13: 1501-1512. (Pubitemid 29297917)
18. Wang, Y. Y., Z. Li, D. Jiao, Z. Zhang, X. Shao, J. Yuan, and P. Yu. 2010. RNA interference reveals a requirement for both p18INK4c and p27Kip1 in B lymphopoiesis. J Mol Cell Biol 2: 209-216.
19. Morse, L., D. Chen, D. Franklin, Y. Xiong, and S. Chen-Kiang. 1997. Induction of cell cycle arrest and B cell terminal differentiation by CDK inhibitor p18 (INK4c) and IL-6. Immunity 6: 47-56. (Pubitemid 27130214)
20. Tourigny, M. R., J. Ursini-Siegel, H. Lee, K. M. Toellner, A. F. Cunningham, D. S. Franklin, S. Ely, M. H. Chen, X. F. Qin, Y. Xiong, et al. 2002. CDK inhibitor p18(INK4c) is required for the generation of functional plasma cells. Immunity 17: 179-189. (Pubitemid 35245960)
21. Potula, H. H., and L. Morel. 2012. Genetic variation at a Yin-Yang 1 response site regulates the transcription of cyclin-dependent kinase inhibitor p18(INK4C) transcript in lupus-prone mice. J. Immunol. 188: 4992-5002.
22. Sicinski, P., J. L. Donaher, Y. Geng, S. B. Parker, H. Gardner, M. Y. Park, R. L. Robker, J. S. Richards, L. K. McGinnis, J. D. Biggers, et al. 1996. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature 384: 470-474. (Pubitemid 26414665)
23. 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)
24. Niu, H., E. S. Sobel, and L. Morel. 2008. Defective B-cell response to T-dependent immunization in lupus-prone mice. Eur. J. Immunol. 38: 3028-3040.
25. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962. (Pubitemid 44894955)
26. 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)
27. Nashi, E., Y. Wang, and B. Diamond. 2010. The role of B cells in lupus pathogenesis. Int. J. Biochem. Cell Biol. 42: 543-550.
28. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18. (Pubitemid 41019653)
29. Mohan, C., L. Morel, P. Yang, and E. K. Wakeland. 1997. Genetic dissection of systemic lupus erythematosus pathogenesis: Sle2 on murine chromosome 4 leads to B cell hyperactivity. J. Immunol. 159: 454-465. (Pubitemid 127493732)
30. Heidari, Y., A. E. Bygrave, R. J. Rigby, K. L. Rose, M. J. Walport, H. T. Cook, T. J. Vyse, and M. Botto. 2006. Identification of chromosome intervals from 129 and C57BL/6 mouse strains linked to the development of systemic lupus erythematosus. Genes Immun. 7: 592-599. (Pubitemid 44614874)
31. Carlucci, F., L. Fossati-Jimack, I. E. Dumitriu, Y. Heidari, M. J. Walport, M. Szajna, P. Baruah, O. A. Garden, H. T. Cook, and M. Botto. 2010. Identification and characterization of a lupus suppressor 129 locus on chromosome 3. J. Immunol. 184: 6256-6265.
32. Cohen, P. L., and R. A. Eisenberg. 1992. The lpr and gld genes in systemic autoimmunity: life and death in the Fas lane. Immunol. Today 13: 427-428.
33. Crispín, J. C., and G. C. Tsokos. 2010. Interleukin-17-producing T cells in lupus. Curr. Opin. Rheumatol. 22: 499-503.
34. Malumbres, M., R. Sotillo, D. Santamaría, J. Galán, A. Cerezo, S. Ortega, P. Dubus, and M. Barbacid. 2004. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 118: 493-504. (Pubitemid 39485668)
35. Berthet, C., and P. Kaldis. 2006. Cdk2 and Cdk4 cooperatively control the expression of Cdc2. Cell Div. 1: 10.
36. Doreau, A., A. Belot, J. Bastid, B. Riche, M. C. Trescol-Biemont, B. Ranchin, N. Fabien, P. Cochat, C. Pouteil-Noble, P. Trolliet, et al. 2009. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat. Immunol. 10: 778-785.
37. Strasser, A., P. J. Jost, and S. Nagata. 2009. The many roles of FAS receptor signaling in the immune system. Immunity 30: 180-192.
38. Kobayashi, S., T. Hirano, M. Kakinuma, and T. Uede. 1993. Transcriptional repression and differential splicing of Fas mRNA by early transposon (ETn) insertion in autoimmune lpr mice. Biochem. Biophys. Res. Commun. 191: 617-624. (Pubitemid 23222680)
39. Kovalev, G. I., D. S. Franklin, V. M. Coffield, Y. Xiong, and L. Su. 2001. An important role of CDK inhibitor p18(INK4c) in modulating antigen receptor-mediated T cell proliferation. J. Immunol. 167: 3285-3292. (Pubitemid 32852569)
40. Kim, K., Y. K. Sung, C. P. Kang, C. B. Choi, C. Kang, and S. C. Bae. 2009. A regulatory SNP at position -899 in CDKN1A is associated with systemic lupus erythematosus and lupus nephritis. Genes Immun. 10: 482-486.
41. Arias, C. F., A. Ballesteros-Tato, M. I. García, J. Martín-Caballero, J. M. Flores, C. Martínez-A, and D. Balomenos. 2007. p21CIP1/WAF1 controls proliferation of activated/memory T cells and affects homeostasis and memory T cell responses. J. Immunol. 178: 2296-2306. (Pubitemid 46233428)
42. Katagiri, K., Y. Ueda, T. Tomiyama, K. Yasuda, Y. Toda, S. Ikehara, K. I. Nakayama, and T. Kinashi. 2011. Deficiency of Rap1-binding protein RAPL causes lymphoproliferative disorders through mislocalization of p27kip1. Immunity 34: 24-38.