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

Journal of Immunology

Volumn 177, Issue 2, 2006, Pages 787-795

  Mataraza, Jennifer M ^a   Tumang, Joseph R ^b   Gumina, Maria R ^a   Gurdak, Sean M ^b   Rothstein, Thomas L ^b,c   Chiles, Thomas C ^a  

^a BOSTON COLLEGE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CYCLIN D2; CYCLIN D3; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; LIPOPOLYSACCHARIDE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN P16INK4A; RETINOBLASTOMA PROTEIN;

ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DNA SYNTHESIS; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION;

EID: 33745822076     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.2.787     Document Type: Article

References (51)

1. 1 phase of the cell cycle. Cell. 65: 701-713.
2. Kozar, K., and P. Sicinski. 2005. Cell cycle progression without cyclin D-CDK4 and cyclin D-CDK6 complexes. Cell Cycle 4: 388-391.
3. Bates, S., L. Bonetta, D. Macallan, D. Parry, A. Holder, C. Dickson, and G. Peters. 1994. CDK6 (PLSTIRE) and CDK4 (PSK-J3) are a distinct subset of the cyclin-dependent kinases that associate with cyclin D1. Oncogene 9: 71-79.
4. Kato, J. Y., M. Matsuoka, D. K. Strom, and C. J. Sherr. 1994. Regulation of cyclin D-dependent kinase 4 (cdk4) by cdk4-activating kinase. Mol. Cell. Biol. 14: 2713-2721.
5. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14: 2077-2086.
6. 1 cyclins. Cell 71: 323-334.
7. Lundberg, A. S., and R. A. Weinberg. 1998. Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol. Cell. Biol. 18: 753-761.
8. 1. Cell 98: 859-869.
9. 1-phase progression. Genes Dev. 13: 1501-1512.
10. Ortega, S., M. Malumbres, and M. Barbacid. 2002. Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim. Biophys. Acta 1602: 73-87.
11. Serrano, M., G. J. Hannon, and D. Beach. 1993. A new regulatory motif in cell cycle control causing specific inhibition of cyclin D/CDK4. Nature 366: 704-707.
12. Bruce, J. L., R. K. Hurford, Jr., M. Classon, J. Koh, and N. Dyson. 2000. Requirements for cell cycle arrest by p16INK4a. Mol. Cell 6: 737-742.
13. Sherr, C. J., and J. M. Roberts. 2004. Living with or without cyclins and cyclin-dependent kinases. Genes Dev. 18: 2699-2711.
14. Malumbres, M., R. Sotillo, D. Santamaria, J. Galan, 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.
15. Kozar, K., M. A. Ciemerych, V. I. Rebel, H. Shigematsu, A. Zagozdzon, E. Sicinska, Y. Geng, Q. Yu, S. Bhattacharya, R. T. Bronson, et al. 2004. Mouse development and cell proliferation in the absence of D-cyclins. Cell 118: 477-491.
16. Inaba, T., H. Matsushime, M. Valentine, M. F. Roussel, C. J. Sherr, and A. T. Look. 1992. Genomic organization, chromosomal localization, and independent expression of human cyclin D genes. Genomics 13: 565-574.
17. Xiong, Y., J. Menninger, D. Beach, and D. C. Ward. 1992. Molecular cloning and chromosomal mapping of CCND genes encoding human D-type cyclins. Genomics 13: 575-584.
18. 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: 470-474.24.
19. Solvason, N., W. W. Wu, N. Kabra, X. Wu, E. Lees, and M. C. Howard. 1996. Induction of cell cycle regulatory proteins in anti-immunoglobulin-stimulated mature B lymphocytes. J. Exp. Med. 184: 407-417.
20. 1 cell cycle stage following delivery of complete versus partial activation stimuli. Mol. Immunol. 33: 1139-1151.
21. Mohamedali, A., I. Soeiro, N. C. Lea, J. Glassford, L. Banerji, G. J. Mufti, E. W.-F. Lam, and S. B. Thomas. 2003. Cyclin D2 controls B cell progenitor numbers. J. Leukocyte Biol. 74: 1141-1145.
22. 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.
23. Lam, E. W., J. Glassford, L. Banerji, N. S. Thomas, P. Sicinski, and G. G. Klaus. 2000. Cyclin D3 compensates for loss of cyclin D2 in mouse B-lymphocytes activated via the antigen receptor and CD40. J. Biol. Chem. 275: 3479-3484.
24. Hsia, C. Y., S. Cheng, A. M. Owyang, S. F. Dowdy, and H. C. Liou. 2002. C-Rel regulation of the cell cycle in primary mouse B lymphocytes. Int. Immunol. 14: 905-916.
25. Wang, Z., P. Sicinski, R. A. Weinberg, Y. Zhang, and K. Ravid. 1996. Characterization of the mouse cyclin D3 gene: exon/intron organization and promoter activity. Genomics 35: 156-163.
26. 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.
27. Herzenberg, L. A. 2000. B-1 cells: the lineage question revisited. Immunol. Rev. 175: 9-22.
28. Rothstein, T. L. 2002. Cutting edge commentary: two B-1 or not to be one. J. Immunol. 168: 4257-4261.
29. Hardy R. R., and K. Hayakawa. 2001. B cell development pathways. Annu. Rev. Immunol. 19: 595-621.
30. Herzenberg, L. A., A. M. Stall, P. A. Lalor, C. Sidman, W. A. Moore, D. R. Parks, and L. A. Herzenberg. 1986. The Ly-1 B cell lineage. Immunol. Rev. 93: 81-102.
31. Caligaris-Cappio, F., M. Gobbi, M. Bofill, and G. Janossy. 1982. Infrequent normal B lymphocytes express features of B-chronic lymphocytic leukemia. J. Exp. Med. 155: 623-628.
32. Stall, A. M., M. C. Farinas, D. M. Tarlinton, P. A. Lalor, L. A. Herzenberg, and S. Strober. 1988. Ly-1 B-cell clones similar to human chronic lymphocytic leukemias routinely develop in older normal mice and young autoimmune (New Zealand Black-related) animals. Proc. Natl. Acad. Sci. USA 85: 7312-7316.
33. Marti, G. E., R. A. Metcalf, and E. Raveche. 1995. The natural history of a lymphoproliferative disorder in aged NZB mice. Curr. Top. Microbiol. Immunol. 194: 117-126.
34. Hayakawa, K., R. R. Hardy, A. M. Stall, and L. A. Herzenberg. 1986. Immunoglobulin bearing B cells reconstitute and maintain the marine Ly- 1 B cell lineage. Eur. J. Immunol. 16: 1313-1316.
35. Rothstein, T. L., and D. L. Kolber. 1988. Anti-Ig antibody inhibits the phorbol ester-induced stimulation of peritoneal B cells. J. Immunol. 141: 4089-4093.
36. Morris, D. L., and T. L. Rothstein. 1993. Abnormal transcription factor induction through the surface immunoglobulin M receptor of B-1 lymphocytes. J. Exp. Med. 177: 857-861.
37. Rothstein T. L., and D. L. Kolber. 1988. Peritoneal B cells respond to phorbol esters in the absence of a co-mitogen. J. Immunol. 140: 2880-2885.
38. 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-1a lymphocytes. J. Exp. Med. 189: 1685-1690.
39. Tanguay, D. A., T. P. Colarusso, C. Doughty, S. Pavlovic, T. L. Rothstein, and T. C. Chiles. 2001. Differences in the signaling requirements for activation of assembled cyclin D3-cdk4 complexes in B-1a and B-2 lymphocytes. J. Immunol. 166: 4273-4277.
40. Tanguay, D. A., and T. C. Chiles. 1996. Regulation of the catalytic subunit (p34PSK-J3/cdk4) for the major D- type cyclin in mature B lymphocytes. J. Immunol. 156: 539-548.
41. Sicinska, E., I. Aifantis, L. Le Cam, W. Swat, C. Borowski, Q. Yu, A. A. Ferrando, S. D. Levin, Y. Geng, H. von Boehmer, and P. Sicinki. 2003. Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 4: 451-461.
42. Tumang, J. R., W. D. Hastings, C. Bai, and T. L. Rothstein. 2004. Peritoneal and splenic B-1a cells are separable by phenotypic, functional, and transcriptomic characteristics. Eur. J. Immunol. 34: 2158-2167.
43. Fahraeus, R., J. M. Paramio, K. L. Ball, S. Lain, and D. P. Lane. 1996. Inhibition of pRb phosphorylation and cell cycle progression by a 20-resdiue peptide derived from p16CDKN2/INK4A. Curr. Biol. 6: 84-91.
44. 1. Cancer Res. 59: 2577-2580.
45. Tumang, J. R., R. Frances, S. G. Yeo, and T. L. Rothstein. 2005. Cutting edge: spontaneously Ig-secreting B-1 cells violate the accepted paradigm for expression of differentiation-associated transcription factors. J. Immunol. 174: 3173-3177.
46. Lane, P., T. Brocker, S. Hubele, E. Padovan, A. Lanzavecchia, and F. McConnell. 1993. Soluble CD40 ligand can replace the normal T cell-derived CD40 ligand signal to B cells in T cell-dependent activation. J. Exp. Med. 177: 1209-1213.
47. Francis, D. A., J. G. Karras, X. Y. Ke, R. Sen, and T. L. Rothstein. 1995. Induction of the transcription factors NF-κB, AP-1 and NF-AT during B cell stimulation through the CD40 receptor. Int. Immunol. 7: 151-161.
48. Kushnuer, J. A., M. A. Ciemerych, E. Sicinska, L. M. Wartschow, M. Teta, S. Y. Long, P. Sicinski, and M. F. White. 2005. Cyclins D2 and D1 are essential for postnatal pancreatic β-cell growth. Mol. Cell. Biol. 25: 3752-3762.
49. Peterson, L. F., A. Boyapati, V. Ranganathan, A. Iwama, D. G. Tenen, S. Tsai, and D.-E. Zhang. 2005. The hematopoietic transcription factor AML1 (RUNX1) is negatively regulated by the cell cycle protein cyclin D3. Mol. Cell. Biol. 25: 10205-10219.
50. Sun, M., Y. Wei, L. Yao, J. Xie, X. Chen, H. Wang, J. Jang, and J. Gu. 2006. Identification of extracellular signal-regulated kinase 3 as a new interaction partner of cyclin D3. Biochem. Biophys. Res. Commun. 340: 209-214.
51. Shen, X., Y. Yang, W. Liu, M. Sun, J. Jaing, H. Zong, and J. Gu. 2004. Identification of the p28 subunit of eukaryotic initiation factor 3(eIF3k) as a new interaction partner of cyclin D3. FEBS Lett. 573: 139-146.