Myc stimulates B lymphocyte differentiation and amplifies calcium signaling

Journal of Cell Biology

Volumn 179, Issue 4, 2007, Pages 717-731

  Habib, Tania ^a   Park, Heon ^a   Tsang, Mark ^a   De Alborán, Ignacio Moreno ^b   Nicks, Andrea ^a   Wilson, Leslie ^a   Knoepfler, Paul S ^d   Andrews, Sarah ^c   Rawlings, David J ^c   Eisenman, Robert N ^d   Iritani, Brian M ^a,d  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); BRUTON TYROSINE KINASE; CALCIUM; MYC PROTEIN; PROTEIN KINASE; PROTEIN TEC; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARCINOGENESIS; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; KNOCKOUT MOUSE; LYMPHOCYTE PROLIFERATION; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY;

ANIMALS; B-LYMPHOCYTES; CALCIUM; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; FIBROBLASTS; GENES, MYC; GENES, REPORTER; LUCIFERASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NFATC TRANSCRIPTION FACTORS; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; PROTO-ONCOGENE PROTEINS C-MYC;

MUS; MUS MUSCULUS;

EID: 36349002340     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200704173     Document Type: Article

References (47)

1. Aifantis, I., F. Gounari, L. Scorrano, C. Borowski, and H. von Boehmer. 2001. Constitutive pre-TCR signaling promotes differentiation through Ca2+ mobilization and activation of NF-kappaB and NFAT. Nat. Immunol. 2:403-409.
2. Asagiri M., K. Sato, T. Usami, S. Ochi, H. Nishina, H. Yoshida, I. Morita, E.F. Wagner, Mak, T.W., E. Serfling, and H. Takayanagi. 2005. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J. Exp. Med. 202:1261-1269.
3. Charron, J., B.A. Malynn, P. Fisher, V. Stewart, L. Jeannotte, S.P. Goff, E.J. Robertson, and F.W. Alt. 1992. Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes Dev. 6:2248-2257.
4. Chen, J., P.A. McLean, B.G. Neel, G. Okunade, G.E. Shull, and H.H. Wortis. 2004. CD22 attenuates calcium signaling by potentiating plasma membrane calcium-ATPase activity. Nat. Immunol. 5:651-657.
5. Chuvpilo, S., E. Jankevics, D. Tyrsin, A. Akimzhanov, D. Moroz, M.K. Jha, J. Schulze-Luehrmann, B. Santner-Nanan, E. Feoktistova, T. Konig, et al. 2002. Autoregulation of NFATc1/A expression facilitates effector T cells to escape from rapid apoptosis. Immunity. 16:881-895.
6. Crabtree, G.R. 2001. Calcium, calcineurin, and the control of transcription. J. Biol. Chem. 276:2313-2316.
7. Davis, A.C., M. Wims, G.D. Spotts, S.R. Hann, and A. Bradley. 1993. A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev. 7:671-682.
8. de Alboran, I.M., R.C. O'Hagan, F. Gartner, B. Malynn, L. Davidson, R. Rickert, K. Rajewsky, R.A. DePinho, and F.W. Alt. 2001. Analysis of C-MYC function in normal cells via conditional gene-targeted mutation. Immunity. 14:45-55.
9. Dillon, S.R., and M.S. Schlissel. 2002. Partial restoration of B cell development in Jak-3(-/-) mice achieved by co-expression of IgH and Eμ-myc transgenes. Int. Immunol. 14:893-904.
10. Dolmetsch, R.E., R.S. Lewis, C.C. Goodnow, and J.I. Healy. 1997. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature. 386:855-858.
11. Eisenman, R.N. 2001. Deconstructing myc. Genes Dev. 15:2023-2030.
12. Ellmeier, W., S. Jung, M.J. Sunshine, F. Hatam, Y. Xu, D. Baltimore, H. Mano, and D.R. Littman. 2000. Severe B cell deficiency in mice lacking the tec kinase family members Tec and Btk. J. Exp. Med. 192:1611-1624.
13. Fleming, H.E., and C.J. Paige. 2002. Cooperation between IL-7 and the pre-B cell receptor: a key to B cell selection. Semin. Immunol. 14:423-430.
14. Fluckiger, A.C., Z. Li, R.M. Kato, M.I. Wahl, H.D. Ochs, R. Longnecker, J.P. Kinet, O.N. Witte, A.M. Scharenberg, and D.J. Rawlings. 1998. Btk/Tec kinases regulate sustained increases in intracellular Ca2+ following B-cell receptor activation. EMBO J. 17:1973-1985.
15. Fruman, D.A., S.B. Snapper, C.M. Yballe, F.W. Alt, and L.C. Cantley. 1999. Phosphoinositide 3-kinase knockout mice: role of p85alpha in B cell development and proliferation. Biochem. Soc. Trans. 27:624-629.
16. Gandarillas, A., and F.M. Watt. 1997. c-Myc promotes differentiation of human epidermal stem cells. Genes Dev. 11:2869-2882.
17. Glynne, R., S. Akkaraju, J.I. Healy, J. Rayner, C.C. Goodnow, and D.H. Mack. 2000. How self-tolerance and the immunosuppressive drug FK506 prevent B-cell mitogenesis. Nature. 403:672-676.
18. Grumont, R.J., A. Strasser, and S. Gerondakis. 2002. B cell growth is controlled by phosphatidylinositol 3-kinase-dependent induction of Rel/NF-kappaB regulated c-myc transcription. Mol. Cell. 10:1283-1294.
19. Hardy, R.R., and K. Hayakawa. 2001. B cell development pathways. Annu. Rev. Immunol. 19:595-621.
20. Harris, A.W., C.A. Pinkert, M. Crawford, W.Y. Langdon, R.L. Brinster, and J.M. Adams. 1988. The Eμ-myc transgenic mouse. A model for high-incidence spontaneous lymphoma and leukemia of early B cells. J. Exp. Med. 167:353-371.
21. Hayashi, K., M. Yamamoto, T. Nojima, R. Goitsuka, and D. Kitamura. 2003. Distinct signaling requirements for Dmu selection, IgH allelic exclusion, pre-B cell transition, and tumor suppression in B cell progenitors. Immunity. 18:825-836.
22. Heim, R., T. Iwata, E. Zvaritch, H.P. Adamo, B. Rutishauser, E.E. Strehler, D. Guerini, and E. Carafoli. 1992. Expression, purification, and properties of the plasma membrane Ca2+ pump and of its N-terminally truncated 105-kDa fragment. J. Biol. Chem. 267:24476-24484.
23. Hendriks, R.W., and R. Kersseboom. 2005. Involvement of SLP-65 and Btk in tumor suppression and malignant transformation of pre-B cells. Semin. Immunol. 18:67-76.
24. Hendriks, R.W., and S. Middendorp. 2004. The pre-BCR checkpoint as a cellautonomous proliferation switch. Trends Immunol. 25:249-256.
25. Im, S.H., and A. Rao. 2004. Activation and deactivation of gene expression by Ca2+/calcineurin-NFAT-mediated signaling. Mol. Cells. 18:1-9.
26. Iritani, B.M., K.A. Forbush, M.A. Farrar, and R.M. Perlmutter. 1997. Control of B cell development by Ras-mediated activation of Raf. EMBO J. 16:7019-7031.
27. Iritani, B.M., J. Alberola-Ila, K.A. Forbush, and R.M. Perimutter. 1999. Distinct signals mediate maturation and allelic exclusion in lymphocyte progenitors. Immunity. 10:713-722.
28. June, C.H., and P.S. Rabinovitch. 1990. Flow cytometric measurement of intracellular ionized calcium in single cells with indo-1 and fluo-3. Methods Cell Biol. 33:37-58.
29. Knoepfler, P.S., P.F. Cheng, and R.N. Eisenman. 2002. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev. 16:2699-2712.
30. Langdon, W.Y., A.W. Harris, S. Cory, and J.M. Adams. 1986. The c-myc oncogene perturbs B lymphocyte development in E-mu-myc transgenic mice. Cell. 47:11-18.
31. Li, L.H., C. Nerlov, G. Prendergast, D. MacGregor, and E.B. Ziff. 1994. c-Myc represses transcription in vivo by a novel mechanism dependent on the initiator element and Myc box II. EMBO J. 13:4070-4079.
32. Morrow, M.A., G. Lee, S. Gillis, G.D. Yancopoulos, and F.W. Alt. 1992. Interleukin-7 induces N-myc and c-myc expression in normal precursor B lymphocytes. Genes Dev. 6:61-70.
33. Murphy, M.J., A. Wilson, and A. Trumpp. 2005. More than just proliferation: Myc function in stem cells. Trends Cell Biol. 15:128-137.
34. Pelengaris, S., M. Khan, and G. Evan. 2002. c-MYC: more than just a matter of life and death. Nat. Rev. Cancer. 2:764-776.
35. Rawlings, D.J. 1999. Bruton's tyrosine kinase controls a sustained calcium signal essential for B lineage development and function. Clin. Immunol. 91:243-253.
36. Rickert, R.C., J. Roes, and K. Rajewsky. 1997. B lymphocyte-specific, Cremediated mutagenesis in mice. Nucleic Acids Res. 25:1317-1318.
37. Sauer, B. 2002. Cre/lox: one more step in the taming of the genome. Endocrine. 19:221-228.
38. Shiio, Y., S. Donohoe, E.C. Yi, D.R. Goodlett, R. Aebersold, and R.N. Eisenman. 2002. Quantitative proteomic analysis of Myc oncoprotein function. EMBO J. 21:5088-5096.
39. 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.
40. Staller, P., K. Peukert, A. Kiermaier, J. Seoane, J. Lukas, H. Karsunky, T. Moroy, J. Bartek, J. Massague, F. Hanel, and M. Eilers. 2001. Repression of p15INK4b expression by Myc through association with Miz-1. Nat. Cell Biol. 3:392-399.
41. Thompson, C.B., E.H. Humphries, L.M. Carlson, C.L. Chen, and P.E. Neiman. 1987. The effect of alterations in myc gene expression on B cell development in the bursa of Fabricius. Cell. 51:371-381.
42. Webb, S.E., and A.L. Miller. 2003. Calcium signalling during embryonic development. Nat. Rev. Mol. Cell Biol. 4:539-551.
43. Wen, R., Y. Chen, J. Schuman, G. Fu, S. Yang, W. Zhang, D.K. Newman, and D. Wang. 2004. An important role of phospholipase Cgamma1 in pre-B-cell development and allelic exclusion. EMBO J. 23:4007-4017.
44. Whitfield, J.F. 1992. Calcium signals and cancer. Crit. Rev. Oncog. 3:55-90.
45. Winslow, M.M., E.M. Gallo, J.R. Neilson, and G.R. Crabtree. 2006. The calcineurin phosphatase complex modulates immunogenic B cell responses. Immunity. 24:141-152.
46. Zeller, K.I., X. Zhao, C.W. Lee, K.P. Chiu, F. Yao, J.T. Yustein, H.S. Ooi, Y.L. Orlov, A. Shahab, H.C. Yong, et al. 2006. Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc. Natl. Acad. Sci. USA. 103:17834-17839.
47. Zimmerman, K., and F.W. Alt. 1990. Expression and function of myc family genes. Crit. Rev. Oncog. 2:75-95.