NF-κB factors control the induction of NFATc1 in B lymphocytes

European Journal of Immunology

Volumn 44, Issue 11, 2014, Pages 3392-3402

  Muhammad, Khalid ^a   Alrefai, Hani ^a   Marienfeld, Ralf ^b   Pham, Duong Anh Thuy ^a   Murti, Krisna ^a   Patra, Amiya K ^a   Avots, Andris ^a   Bukur, Valesca ^c   Sahin, Ugur ^c   Kondo, Eisaku ^d   Klein Hessling, Stefan ^a   Serfling, Edgar ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF ULM   (Germany)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^d AICHI CANCER CENTER HOSPITAL   (Japan)

Author keywords

Chromatin; Induction; Lymphocytes; NF B; Nfatc1 gene; Transcription

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ISOPROTEIN; NFATC1 PROTEIN, MOUSE; PROTEIN BINDING; RELA PROTEIN, MOUSE; RELB PROTEIN, MOUSE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

ANIMAL; B LYMPHOCYTE; BINDING SITE; BIOSYNTHESIS; C57BL MOUSE; CHICKEN; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MOUSE; PROMOTER REGION;

ANIMALS; B-LYMPHOCYTES; BINDING SITES; CHICKENS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B P50 SUBUNIT; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

EID: 84916888146     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444756     Document Type: Article

References (48)

1. Serfling, E., Avots, A. and Neumann, M., The architecture of the interleukin-2 promoter: a reflection of T lymphocyte activation. Biochim. Biophys. Acta 1995. 1263: 181-200.
2. Durand, D. B., Shaw, J. P., Bush, M. R., Replogle, R. E., Belagaje, R. and Crabtree, G. R., Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol. Cell. Biol. 1988. 8: 1715-1724.
3. Serfling, E., Barthelmas, R., Pfeuffer, I., Schenk, B., Zarius, S., Swoboda, R., Mercurio, F. et al., Ubiquitous and lymphocyte-specific factors are involved in the induction of the mouse interleukin 2 gene in T lymphocytes. EMBO J. 1989. 8: 465-473.
4. Kel, A., Kel-Margoulis, O., Babenko, V. and Wingender, E., Recognition of NFATp/AP-1 composite elements within genes induced upon the activation of immune cells. J. Mol. Biol. 1999. 288: 353-376.
5. Fraser, J. D., Irving, B. A., Crabtree, G. R. and Weiss, A., Regulation of interleukin-2 gene enhancer activity by the T cell accessory molecule CD28. Science 1991. 251: 313-316.
6. Verweij, C. L., Geerts, M. and Aarden, L. A., Activation of interleukin-2 gene transcription via the T-cell surface molecule CD28 is mediated through an NF-kB-like response element. J. Biol. Chem. 1991. 266: 14179-14182.
7. Huang, D. B., Chen, Y. Q., Ruetsche, M., Phelps, C. B. and Ghosh, G., X-ray crystal structure of proto-oncogene product c-Rel bound to the CD28 response element of IL-2. Structure 2001. 9: 669-678.
8. Kunsch, C., Ruben, S. M. and Rosen, C. A., Selection of optimal kappa B/Rel DNA-binding motifs: interaction of both subunits of NF-kappa B with DNA is required for transcriptional activation. Mol. Cell. Biol. 1992. 12: 4412-4421.
9. Jin, L., Sliz, P., Chen, L., Macian, F., Rao, A., Hogan, P. G. and Harrison, S. C., An asymmetric NFAT1 dimer on a pseudo-palindromic kappa B-like DNA site. Nat. Struct. Biol. 2003. 10: 807-811.
10. Giffin, M. J., Stroud, J. C., Bates, D. L., von Koenig, K. D., Hardin, J. and Chen, L., Structure of NFAT1 bound as a dimer to the HIV-1 LTR kappa B element. Nat. Struct. Biol. 2003. 10: 800-806.
11. Chen, L., Glover, J. N., Hogan, P. G., Rao, A. and Harrison, S. C., Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature 1998. 392: 42-48.
12. Zhou, P., Sun, L. J., Dotsch, V., Wagner, G. and Verdine, G. L., Solution structure of the core NFATC1/DNA complex. Cell 1998. 92: 687-696.
13. Wolfe, S. A., Zhou, P., Dotsch, V., Chen, L., You, A., Ho, S. N., Crabtree, G. R. et al., Unusual Rel-like architecture in the DNA-binding domain of the transcription factor NFATc. Nature 1997. 385: 172-176.
14. Serfling, E., Berberich-Siebelt, F., Chuvpilo, S., Jankevics, E., Klein-Hessling, S., Twardzik, T. and Avots, A., The role of NF-AT transcription factors in T cell activation and differentiation. Biochim. Biophys. Acta 2000. 1498: 1-18.
15. Hogan, P. G., Chen, L., Nardone, J. and Rao, A., Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003. 17: 2205-2232.
16. Crabtree, G. R. and Olson, E. N., NFAT signaling: choreographing the social lives of cells. Cell 2002. 109(Suppl): S67-S79.
17. Serfling, E., Avots, A., Klein-Hessling, S., Rudolf, R., Vaeth, M. and Berberich-Siebelt, F., NFATc1/alphaA: the other face of NFAT factors in lymphocytes. Cell Commun. Signal. 2012. 10: 16-25.
18. Bhattacharyya, S., Deb, J., Patra, A. K., Thuy Pham, D. A., Chen, W., Vaeth, M., Berberich-Siebelt, F. et al., NFATc1 affects mouse splenic B cell function by controlling the calcineurin-NFAT signaling network. J. Exp. Med. 2011. 208: 823-839.
19. Schulze-Luehrmann, J. and Ghosh, S., Antigen-receptor signaling to nuclear factor kappa B. Immunity 2006. 25: 701-715.
20. Beg, A. A., Sha, W. C., Bronson, R. T., Ghosh, S. and Baltimore, D., Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 1995. 376: 167-170.
21. Sha, W. C., Liou, H. C., Tuomanen, E. I. and Baltimore, D., Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 1995. 80: 321-330.
22. Snapper, C. M., Zelazowski, P., Rosas, F. R., Kehry, M. R., Tian, M., Baltimore, D. and Sha, W. C., B cells from p50/NF-kappa B knockout mice have selective defects in proliferation, differentiation, germ-line CH transcription, and Ig class switching. J. Immunol. 1996. 156: 183-191.
23. Kontgen, F., Grumont, R. J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D. and Gerondakis, S., Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 1995. 9: 1965-1977.
24. Gilmore, T. D. and Gerondakis, S., The c-Rel transcription factor in development and disease. Genes Cancer 2011. 2: 695-711.
25. Nojima, T., Haniuda, K., Moutai, T., Matsudaira, M., Mizokawa, S., Shiratori, I., Azuma, T. et al., In-vitro derived germinal centre B cells differentially generate memory B or plasma cells in vivo. Nat. Commun. 2011. 2: 465-476.
26. Chuvpilo, S., Jankevics, E., Tyrsin, D., Akimzhanov, A., Moroz, D., Jha, M. K., Schulze-Luehrmann, J. et al., Autoregulation of NFATc1/A expression facilitates effector T cells to escape from rapid apoptosis. Immunity 2002. 16: 881-895.
27. Fruman, D. A., Pai, S. Y., Burakoff, S. J. and Bierer, B. E., Characterization of a mutant calcineurin A alpha gene expressed by EL4 lymphoma cells. Mol. Cell. Biol. 1995. 15: 3857-3863.
28. Pohl, T., Gugasyan, R., Grumont, R. J., Strasser, A., Metcalf, D., Tarlinton, D., Sha, W. et al., The combined absence of NF-kappa B1 and c-Rel reveals that overlapping roles for these transcription factors in the B cell lineage are restricted to the activation and function of mature cells. Proc. Natl. Acad. Sci. USA 2002. 99: 4514-4519.
29. Gerondakis, S. and Siebenlist, U., Roles of the NF-kappaB pathway in lymphocyte development and function. Cold Spring Harb. Perspect. Biol. 2010. 2: a000182.
30. Hayden, M. S. and Ghosh, S., NF-kappaB in immunobiology. Cell Res. 2011. 21: 223-244.
31. Banerjee, A., Grumont, R., Gugasyan, R., White, C., Strasser, A. and Gerondakis, S., NF-kappaB1 and c-Rel cooperate to promote the survival of TLR4-activated B cells by neutralizing Bim via distinct mechanisms. Blood 2008. 112: 5063-5073.
32. Grumont, R. J., Rourke, I. J., O'Reilly, L. A., Strasser, A., Miyake, K., Sha, W. and Gerondakis, S., B lymphocytes differentially use the Rel and nuclear factor kappaB1 (NF-kappaB1) transcription factors to regulate cell cycle progression and apoptosis in quiescent and mitogen-activated cells. J. Exp. Med. 1998. 187: 663-674.
33. Macian, F., Lopez-Rodriguez, C. and Rao, A., Partners in transcription: NFAT and AP-1. Oncogene 2001. 20: 2476-2489.
34. Pham, L. V., Tamayo, A. T., Yoshimura, L. C., Lin-Lee, Y. C. and Ford, R. J., Constitutive NF-kappaB and NFAT activation in aggressive B-cell lymphomas synergistically activates the CD154 gene and maintains lymphoma cell survival. Blood 2005. 106: 3940-3947.
35. Liu, Q., Chen, Y., Auger-Messier, M. and Molkentin, J. D., Interaction between NFkappaB and NFAT coordinates cardiac hypertrophy and pathological remodeling. Circ. Res. 2012. 110: 1077-1086.
36. Hobeika, E., Thiemann, S., Storch, B., Jumaa, H., Nielsen, P. J., Pelanda, R. and Reth, M., Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 2006. 103: 13789-13794.
37. Kwon, K., Hutter, C., Sun, Q., Bilic, I., Cobaleda, C., Malin, S. and Busslinger, M., Instructive role of the transcription factor E2 A in early B lymphopoiesis and germinal center B cell development. Immunity 2008. 28: 751-762.
38. Vaeth, M., Schliesser, U., Muller, G., Reissig, S., Satoh, K., Tuettenberg, A., Jonuleit, H. et al., Dependence on nuclear factor of activated T-cells (NFAT) levels discriminates conventional T cells from Foxp3+ regulatory T cells. Proc. Natl. Acad. Sci. USA 2012. 109: 16258-16263.
39. Oh-Hora, M., Komatsu, N., Pishyareh, M., Feske, S., Hori, S., Taniguchi, M., Rao, A. et al., Agonist-selected T cell development requires strong T cell receptor signaling and store-operated calcium entry. Immunity 2013. 38: 881-895.
40. Aliprantis, A. O., Ueki, Y., Sulyanto, R., Park, A., Sigrist, K. S., Sharma, S. M., Ostrowski, M. C. et al., NFATc1 in mice represses osteoprotegerin during osteoclastogenesis and dissociates systemic osteopenia from inflammation in cherubism. J. Clin. Invest. 2008. 118: 3775-3789.
41. Hock, M., Vaeth, M., Rudolf, R., Patra, A. K., Pham, D. A., Muhammad, K., Pusch, T. et al., NFATc1 induction in peripheral T and B lymphocytes. J. Immunol. 2013. 190: 2345-2353.
42. Yamamoto, K., Hirano, S., Ishiai, M., Morishima, K., Kitao, H., Namikoshi, K., Kimura, M. et al., Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination. Mol. Cell. Biol. 2005. 25: 34-43.
43. Suhasini, M., Reddy, C. D., Reddy, E. P., DiDonato, J. A. and Pilz, R. B., cAMP-induced NF-kappaB (p50/relB) binding to a c-myb intronic enhancer correlates with c-myb up-regulation and inhibition of erythroleukemia cell differentiation. Oncogene 1997. 15: 1859-1870.
44. Pierce, J. W., Lenardo, M. and Baltimore, D., Oligonucleotide that binds nuclear factor NF-kappa B acts as a lymphoid-specific and inducible enhancer element. Proc. Natl. Acad. Sci. USA 1988. 85: 1482-1486.
45. Toth, C. R., Hostutler, R. F., Baldwin, A. S., Jr. and Bender, T. P., Members of the nuclear factor kappa B family transactivate the murine c-myb gene. J. Biol. Chem. 1995. 270: 7661-7671.
46. Ueda, T., Akiyama, N., Sai, H., Oya, N., Noda, M., Hiraoka, M. and Kizaka-Kondoh, S., c-IAP2 is induced by ionizing radiation through NF-kappaB binding sites. FEBS Lett. 2001. 491: 40-44.
47. Zhang, B., Wang, Z., Li, T., Tsitsikov, E. N. and Ding, H. F., NF-kappaB2 mutation targets TRAF1 to induce lymphomagenesis. Blood 2007. 110: 743-751.
48. Lee, H. H., Dadgostar, H., Cheng, Q., Shu, J. and Cheng, G., NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. USA 1999. 96: 9136-9141.