Differential role for cyclic AMP response element binding protein-1 in multiple stages of B cell development, differentiation, and survival

Journal of Immunology

Volumn 176, Issue 4, 2006, Pages 2208-2218

  Chen, Hui Chen ^a   Byrd, John C ^a,b   Muthusamy, Natarajan ^a,b  

^a College of Pharmacy ^*  (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DINITROPHENOL; CD24 ANTIGEN; CD45 ANTIGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMEDIATE EARLY PROTEIN; KEYHOLE LIMPET HEMOCYANIN; LEUKOSIALIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR JUNB; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; BONE MARROW; CELL CYCLE S PHASE; CELL MATURATION; CELL SURVIVAL; FLOW CYTOMETRY; GENE EXPRESSION; MOUSE; NONHUMAN; PERITONEUM; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SPLEEN; TRANSGENE; TRANSGENIC MOUSE;

EID: 32044462046     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.4.2208     Document Type: Article

References (66)

1. Montminy, M. R., K. A. Sevarino, J. A. Wagner, G. Mandel, and R. H. Goodman. 1986. Identification of a cyclic-AMP responsive element within the rat somatostatin gene. Proc. Natl. Acad. Sci. USA 83: 6682-6686.
2. Comb, M., N. C. Burnberg, A. Seascholtz, E. Herbert, and H. M. Goodman. 1986. A cyclic-AMP- and phorbol ester-inducible DNA element. Nature 323: 353-356.
3. Masquilier, D., and P. Sassone-Corsi. 1992. Transcriptional cross-talk: nuclear factors CREM and CREB bind to AP-1 sites and inhibit activation by Jun. J. Biol. Chem. 267: 22460-22466.
4. Benbrook, D. M., and N. C. Jones. 1990. Heterodimer formation between CREB and JUN proteins. Oncogene 5: 295-302.
5. Hai, T., and T. Curran. 1991. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl. Acad. Sci. USA 88: 3720-3724.
6. Yamamoto, K. K., G. A. Gonzalez, W. H. Biggs, 3rd, and M. R. Montminy. 1988. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature 334: 494-498.
7. Gonzalez, G. A., and M. R. Montminy. 1989. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59: 675-679.
8. Nichols, M., F. Weih, W. Schmid, C. DeVack, E. Kowenz-Leutz, B. Luckow, M. Boshart, and G. Schutz. 1992. Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EMBO J. 11: 3337-3346.
9. Chrivia, J. C., R. P. Kwok, N. Lamb, M. Hagiwara, M. R. Montminy, and R. H. Goodman. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365: 855-859.
10. Arias, J., A. S. Alberts, P. Brindle, F. X. Claret, T. Smeal, M. Karin, J. Feramisco, and M. Montminy. 1994. Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370: 226-228.
11. Kwok, R. P., J. R. Lundblad, J. C. Chrivia, J. P. Richards, H. P. Bachinger, R. G. Brennan, S. G. Roberts, M. R. Green, and R. H. Goodman. 1994. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370: 223-226.
12. Sun, P., and R. A. Maurer. 1995. An inactivating point mutation demonstrates that interaction of cAMP response element binding protein (CREB) with the CREB binding protein is not sufficient for transcriptional activation. J. Biol. Chem. 270: 7041-7044.
13. Parker, D., K. Ferreri, T. Nakajima, V. J. LaMorte, R. Evans, S. C. Koerber, C. Hoeger, and M. R. Montminy. 1996. Phosphorylation of CREB at Ser-133 induces complex formation with CREB-binding protein via a direct mechanism. Mol. Cell. Biol. 16: 694-703.
14. Hagiwara, M., P. Brindle, A. Harootunian, R. Armstrong, J. Rivier, W. Vale, R. Tsien, and M. R. Montminy. 1993. Coupling of hormonal stimulation and transcription via cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol. Cell. Biol. 13: 4852-4859.
15. Xie, H., and T. L. Rothstein. 1995. Protein kinase C mediates activation of nuclear cAMP response element-binding protein (CREB) in B lymphocytes stimulated through surface Ig. J. Immunol. 154: 1717-1723.
16. Matthews, R. P., C. R. Guthrie, L. M. Wailes, X. Zhao, A. R. Means, and G. S. McKnight. 1994. Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell. Biol. 14: 6107-6116.
17. 2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252: 1427-1430.
18. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8: 2527-2539.
19. Ginty, D. D., A. Bonni, and M. E. Greenberg. 1994. Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77: 713-725.
20. 133 kinase in human melanocytes. Cell Growth Differ. 6: 291-302.
21. Xing, J., D. D. Ginty, and M. E. Greenberg. 1996. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273: 959-963.
22. Muthusamy, N., and J. M. Leiden. 1998. A protein kinase C-, Ras-, and RSK2-dependent signal transduction pathway activates the cAMP-responsive element-binding protein transcription factor following T cell receptor engagement. J. Biol. Chem. 273: 22841-22847.
23. Xie, H., T. C. Chiles, and T. L. Rothstein. 1993. Induction of CREB activity via the surface Ig receptor of B cells. J. Immunol. 151: 880-889.
24. Xie, H., Z. Wang, and T. L. Rothstein. 1996. Signaling pathways for antigen receptor-mediated induction of transcription factor CREB in B lymphocytes. Cell. Immunol. 169: 264-270.
25. Frissora, F., H. C. Chen, J. Durbin, S. Bondada, and N. Muthusamy. 2003. IFN-γ-mediated inhibition of antigen receptor-induced B cell proliferation and CREB-1 binding activity requires STAT-1 transcription factor. Eur. J. Immunol. 33: 907-912.
26. Dey, A., D. W. Nebert, and K. Ozato. 1991. The AP-1 site and the cAMP- and serum response elements of the c-fos gene are constitutively occupied in vivo. DNA Cell Biol 10: 537-544.
27. Amato, S. F., K. Nakajima, T. Hirano, and T. C. Chiles. 1996. Transcriptional regulation of the junB promoter in mature B lymphocytes: activation through a cyclic adenosine 3′,5′-monophosphate-like binding site. J. Immunol. 157: 146-155.
28. Amato, S. F., K. Nakajima, T. Hirano, and T. C. Chiles. 1997. Transcriptional regulation of the junB gene in B lymphocytes: role of protein kinase A and a membrane Ig-regulated protein phosphatase. J. Immunol. 159: 4676-4685.
29. Huang, D., P. M. Shipman-Appasamy, D. J. Orten, S. H. Hinrichs, and M. B. Prystowsky. 1994. Promoter activity of the proliferating-cell nuclear antigen gene is associated with inducible CRE-binding proteins in interleukin 2-stimulated T lymphocytes. Mol. Cell. Biol. 14: 4233-4243.
30. Barton, K., N. Muthusamy, M. Chanyangam, C. Fischer, C. Clendenin, and J. M. Leiden. 1996. Defective thymocyte proliferation and IL-2 production in transgenic mice expressing a dominant-negative form of CREB. Nature 379: 81-85.
31. Powell, J. D., C. G. Lerner, G. R. Ewoldt, and R. H. Schwartz. 1999. The -180 site of the IL-2 promoter is the target of CREB/CREM binding in T cell anergy. J. Immunol. 163: 6631-6639.
32. Wilson, B. E., E. Mochon, and L. M. Boxer. 1996. Induction of bcl-2 expression by phosphorylated CREB proteins during B-cell activation and rescue from apoptosis. Mol. Cell. Biol. 16: 5546-5556.
33. Zhang, C. Y., Y. L. Wu, and L. M. Boxer. 2002. Impaired proliferation and survival of activated B cells in transgenic mice that express a dominant-negative cAMP-response element-binding protein transcription factor in B cells. J. Biol. Chem. 277: 48359-48365.
34. Rudolph, D., A. Tafuri, P. Gass, G. J. Hammerling, B. Arnold, and G. Schutz. 1998. Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response element binding protein. Proc. Natl. Acad. Sci. USA 95: 4481-4486.
35. Hummler, E., T. J. Cole, J. A. Blendy, R. Ganss, A. Aguzzi, W. Schmid, F. Beermann, and G. Schutz. 1994. Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proc. Natl. Acad. Sci. USA 91: 5647-5651.
36. Su, G. H., H. M. Chen, N. Muthusamy, L. A. Garrett-Sinha, D. Baunoch, D. G. Tenen, and M. C. Simon. 1997. Defective B cell receptor-mediated responses in mice lacking the Ets protein, Spi-B. EMBO J. 16: 7118-7129.
37. Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.
38. Rolink, A. G., J. Andersson, and F. Melchers. 2004. Molecular mechanisms guiding late stages of B-cell development. Immunol. Rev. 197: 41-50.
39. Hardy, R. R., C. E. Carmack, S. A. Shinton, J. D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse hone marrow. J. Exp. Med. 173: 1213-1225.
40. Bakiri, L., D. Lallemand, E. Bossy-Wetzel, and M. Yaniv. 2000. Cell cycle-dependent variations in c-Jun and JunB phosphorylation: a role in the control of cyclin D1 expression. EMBO J. 19: 2056-2068.
41. Mechta-Grigoriou, F., D. Gerald, and M. Yaniv. 2001. The mammalian Jun proteins: redundancy and specificity. Oncogene 20: 2378-2389.
42. Shaulian, E., and M. Karin. 2001. AP-1 in cell proliferation and survival. Oncogene 20: 2390-2400.
43. Shaulian, E., and M. Karin. 2002. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4: E131-E136.
44. Bhushan, A., and L. R. Covey. 2001. CREB/ATF proteins enhance the basal and CD154- and IL-4-induced transcriptional activity of the human Ig γ1 proximal promoter. Eur. J. Immunol. 31: 653-664.
45. Strasser, A., A. W. Harris, L. M. Corcoran, and S. Cory. 1994. Bcl-2 expression promotes B- but not T-lymphoid development in scid mice. Nature 368: 457-460.
46. L transgene. Immunity 4: 291-299.
47. Wang, J. M., J. R. Chao, W. Chen, M. L. Kuo, J. J. Yen, and H. F. Yang-Yen. 1999. The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/Akt signaling pathway through a transcription factor complex containing CREB. Mol. Cell. Biol. 19: 6195-6206.
48. de Groot, R. P., and P. Sassone-Corsi. 1992. Activation of Jun/AP-1 by protein kinase A. Oncogene 7: 2281-2286.
49. Fujita, K., S. Imoto, J. Phuchareon, and T. Tokuhisa. 1994. c-fos and jun gene expression in murine precursor B lymphocytes developed in the interleukin-7-dependent bone marrow cell culture. Immunobiology 190: 13-22.
50. Imoto, S., L. Hu, Y. Tomita, J. Phuchareon, U. Ruther, and T. Tokuhisa. 1996. A regulatory role of c-Fos in the development of precursor B lymphocytes mediated by interleukin-7. Cell. Immunol. 169: 67-74.
51. von Freeden-Jeffry, U., P. Vieira, L. A. Lucian, T. McNeil, S. E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181: 1519-1526.
52. Peschon, J. J., P. J. Morrissey, K. H. Grabstein, F. J. Ramsdell, E. Maraskovsky, B. C. Gliniak, L. S. Park, S. F. Ziegler, D. E. Williams, C. B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180: 1955-1960.
53. Schütte, J., J. Viallet, M. Nau, S. Segal, J. Fedorko, and J. Minna. 1989. jun-B inhibits and c-fos stimulates the transforming and trans-activating activities of c-jun. Cell 59: 987-997.
54. Deng, T., and M. Karin. 1993. JunB differs from c-Jun in its DNA-binding and dimerization domains, and represses c-Jun by formation of inactive heterodimers. Genes Dev. 7: 479-490.
55. Mauviel, A., K. Y. Chung, A. Agarwal, K. Tamai, and J. Uitto. 1996. Cell-specific induction of distinct oncogenes of the Jun family is responsible for differential regulation of collagenase gene expression by transforming growth factor β in fibroblasts and keratinocytes. J. Biol. Chem. 271: 10917-109223.
56. Kong, Y. Y., H. Yoshida, I. Sarosi, H. L. Tan, E. Timms, C. Capparelli, S. Morony, A. J. Oliveira-dos-Santos, G. Van, A. Itie, et al. 1999. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397: 315-323.
57. Manabe, N., H. Kawaguchi, H. Chikuda, C. Miyaura, M. Inada, R. Nagai, Y. Nabeshima, K. Nakamura, A. M. Sinclair, R. H. Scheuermann, and M. Kuro-o. 2001. Connection between B lymphocyte and osteoclast differentiation pathways. J. Immunol. 167: 2625-2631.
58. Cariappa, A., and S. Pillai. 2002. Antigen-dependent B-cell development. Curr. Opin. Immunol. 14: 241-249.
59. Mao, C. S., and J. Stavnezer. 2001. Differential regulation of mouse germline Ig γI and ε promoters by IL-4 and CD40. J. Immunol. 167: 1522-1534.
60. Shi, M. J., S. R. Park, P. H. Kim, and J. Stavnezer. 2001. Roles of Ets proteins, NF-κB and nocodazole in regulating induction of transcription of mouse germline Igα RNA by transforming growth factor βI. Int. Immunol. 13: 733-746.
61. + B cells and natural IgM-secreting cells: reconstitution potential of adult bone marrow, spleen and peritoneal cells. Eur. J. Immunol. 22: 1243-1251.
62. Hardy, R. R., and K. Hayakawa. 1991. A developmental switch in B lymphopoiesis. Proc. Natl. Acad. Sci. USA 88: 11550-11554.
63. Karras, J. G., Z. Wang, L. Huo, R. G. Howard, D. A. Frank, and T. L. Rothstein. 1997. Signal transducer and activator of transcription-3 (STAT3) is constitutively activated in normal, self-renewing B-1 cells but only inducibly expressed in conventional B lymphocytes. J. Exp. Med. 185: 1035-1042.
64. + B-1 cells have signaling properties similar to tolerant B cells. J. Biol. Chem. 277: 30707-30715.
65. Gubina, E., X. Luo, E. Kwon, K. Sakamoto, Y. F. Shi, and R. A. Mufson. 2001. β Cytokine receptor-induced stimulation of cAMP response element binding protein phosphorylation requires protein kinase C in myeloid cells: a novel cytokine signal transduction cascade. J. Immunol. 167: 4303-4310.
66. Shankar, D. B., J. C. Cheng, K. Kinjo, N. Federman, T. B. Moore, A. Gill, N. P. Rao, E. M. Landaw, and K. M. Sakamoto. 2005. The role of CREB as a proto-oncogene in hematopoiesis and in acute myeloid leukemia. Cancer Cell 7: 351-354.