Identification of cyclin D3 as a direct target of E2A using DamID

Molecular and Cellular Biology

Volumn 24, Issue 19, 2004, Pages 8790-8802

  Song, Siyuan ^a   Cooperman, Jonathan ^a   Letting, Danielle L ^a   Blobel, Gerd A ^a   Choi, John Kim ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D3; DNA; HYBRID PROTEIN; LENTIVIRUS VECTOR; METHYLTRANSFERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2A; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; CELL MATURATION; CHROMATIN; CONTROLLED STUDY; E BOX ELEMENT; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR CLONING; MOLECULAR DYNAMICS; MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN TARGETING;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CYCLINS; DNA; DNA-BINDING PROTEINS; GENETIC VECTORS; LENTIVIRUS; MICE; PROMOTER REGIONS (GENETICS); SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC); TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

ESCHERICHIA COLI; LENTIVIRUS;

EID: 4544221502     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.19.8790-8802.2004     Document Type: Article

References (68)

1. Ando, K., F. Ajchenbaum-Cymbalista, and J. D. Griffin. 1993. Regulation of G1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc. Natl. Acad. Sci. USA 90:9571-9575.
2. Bain, G., E. C. Maandag, D. J. Izon, D. Arnsen, A. M. Kruisbeek, B. C. Weintraub, I. Krop, M. S. Schlissel, A. J. Feeney, and M. van Roon. 1994. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79:885-892.
3. Bartkova, J., J. Lukas, M. Strauss, and J. Bartek. 1998. Cyclin D3: requirement for G1/S transition and high abundance in quiescent tissues suggest a dual role in proliferation and differentiation. Oncogene 17:1027-1037.
4. Bergsagel, P. L., and W. M. Kuehl. 2001. Chromosome translocations in multiple myeloma. Oncogene 20:5611-5622.
5. Boonen, G. J., B. A. van Oirschot, A. van Diepen, W. J. Mackus, L. F. Verdonck, G. Rijksen, and R. H. Medema. 1999. Cyclin D3 regulates proliferation and apoptosis of leukemic T cell lines. J. Biol. Chem. 274:34676-34682.
6. Brooks, A. R., D. Shiffman, C. S. Chan, E. E. Brooks, and P. G. Milner. 1996. Functional analysis of the human cyclin D2 and cyclin D3 promoters. J. Biol. Chem. 271:9090-9099.
7. Carter, R. S., P. Ordentlich, and T. Kadesch. 1997. Selective utilization of basic helix-loop-helix-leucine zipper proteins at the immunoglobulin heavy-chain enhancer. Mol. Cell. Biol. 17:18-23.
8. Chang, M. W., E. Barr, M. M. Lu, K. Barton, and J. M. Leiden. 1995. Adenovirus-mediated over-expression of the cyclin/cyclin-dependent kinase inhibitor, p21 inhibits vascular smooth muscle cell proliferation and neointima formation in the rat carotid artery model of balloon angioplasty. J. Clin. Investig. 96:2260-2268.
9. Choi, J. K., N. Hoang, A. M. Vilardi, P. Conrad, S. G. Emerson, and A. M. Gewirtz. 2001. Hybrid HIV/MSCV LTR enhances transgene expression of lentiviral vectors in human CD34(+) hematopoietic cells. Stem Cells 19:236-246.
10. Choi, J. K., C. P. Shen, H. S. Radomska, L. A. Eckhardt, and T. Kadesch. 1996. E47 activates the Ig-heavy chain and TdT loci in non-B cells. EMBO J. 15:5014-5021.
11. Decker, T., F. Schneller, S. Hipp, C. Miething, T. Jahn, J. Duyster, and C. Peschel. 2002. Cell cycle progression of chronic lymphocytic leukemia cells is controlled by cyclin D2, cyclin D3, cyclin-dependent kinase (cdk) 4 and the cdk inhibitor p27. Leukemia 16:327-334.
12. Engel, I., and C. Murre. 1999. Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proc. Natl. Acad. Sci. USA 96:996-1001.
13. Fernandez, P. C., S. R. Frank, L. Wang, M. Schroeder, S. Liu, J. Greene, A. Cocito, and B. Amati. 2003. Genomic targets of the human c-Myc protein. Genes Dev. 17:1115-1129.
14. Filipits, M., U. Jaeger, G. Pohl, T. Stranzl, I. Simonitsch, A. Kaider, C. Skrabs, and R. Pirker. 2002. Cyclin D3 is a predictive and prognostic factor in diffuse large B-cell lymphoma. Clin. Cancer Res. 8:729-733.
15. Forsberg, E. C., K. M. Downs, H. M. Christensen, H. Im, P. A. Nuzzi, and E. H. Bresnick. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. USA 97:14494-14499.
16. Gisler, R., and M. Sigvardsson. 2002. The human V-preB promoter is a target for coordinated activation by early B cell factor and E47. J. Immunol. 168:5130-5138.
17. Greenbaum, S., and Y. Zhuang. 2002. Identification of E2A target genes in B lymphocyte development by using a gene tagging-based chromatin immunoprecipitation system. Proc. Natl. Acad. Sci. USA 99:15030-15035.
18. Hagman, J., A. Travis, and R. Grosschedl. 1991. A novel lineage-specific nuclear factor regulates mb-1 gene transcription at the early stages of B cell differentiation. EMBO J. 10:3409-3417.
19. Herblot, S., P. D. Aplan, and T. Hoang. 2002. Gradient of E2A activity in B-cell development. Mol. Cell. Biol. 22:886-900.
20. Hsu, L. Y., J. Lauring, H. E. Liang, S. Greenbaum, D. Cado, Y. Zhuang, and M. S. Schlissel. 2003. A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity 19:105-117.
21. Jacobs, Y., C. Vierra, and C. Nelson. 1993. E2A expression, nuclear localization, and in vivo formation of DNA- and non-DNA-binding species during B-cell development. Mol. Cell. Biol. 13:7321-7333.
22. Johnson, K. D., J. A. Grass, M. E. Boyer, C. M. Kiekhaefer, G. A. Blobel, M. J. Weiss, and E. H. Bresnick. 2002. Cooperative activities of hematopoietic regulators recruit RNA polymerase II to a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. USA 99:11760-11765.
23. Kato, J. Y., and C. J. Sherr. 1993. Inhibition of granulocyte differentiation by G1 cyclins D2 and D3 but not D1. Proc. Natl. Acad. Sci. USA 90:11513-11517.
24. Kee, B. L., R. R. Rivera, and C. Murre. 2001. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-beta. Nat. Immunol. 2:242-247.
25. Kladde, M. P., and R. T. Simpson. 1994. Positioned nucleosomes inhibit Dam methylation in vivo. Proc. Natl. Acad. Sci. USA 91:1361-1365.
26. Knudsen, K. E., A. F. Fribourg, M. W. Strobeck, J. M. Blanchard, and E. S. Knudsen. 1999. Cyclin A is a functional target of retinoblastoma tumor suppressor protein-mediated cell cycle arrest. J. Biol. Chem. 274:27632-27641.
27. Lee, J. S., C. H. Lee, and J. H. Chung. 1998. Studying the recruitment of Sp1 to the beta-globin promoter with an in vivo method: protein position identification with nuclease tail (PIN*POINT). Proc. Natl. Acad. Sci. USA 95: 969-974.
28. Lisitsyn, N., and M. Wigler. 1993. Cloning the differences between two complex genomes. Science 259:946-951.
29. Look, A. T. 1997. Oncogenic transcription factors in the human acute leukemias. Science 278:1059-1064.
30. Ma, Y., J. Yuan, M. Huang, R. Jove, and W. D. Cress. 2003. Regulation of the cyclin D3 promoter by E2F1. J. Biol. Chem. 278:16770-16776.
31. Mahmoud, M. S., N. Huang, M. Nobuyoshi, I. A. Lisukov, H. Tanaka, and M. M. Kawano. 1996. Altered expression of Pax-5 gene in human myeloma cells. Blood 87:4311-4315.
32. Maloney, K. W., L. McGavran, L. F. Odom, and S. P. Hunger. 1998. Different patterns of homozygous p16INK4A and p15INK4B deletions in childhood acute lymphoblastic leukemias containing distinct E2A translocations. Leukemia 12:1417-1421.
33. Molkentin, J. D., B. L. Black, J. F. Martin, and E. N. Olson. 1995. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125-1136.
34. Naldini, L., U. Blomer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
35. Okamoto, A., D. J. Demetrick, E. A. Spillare, K. Hagiwara, S. P. Hussain, W. P. Bennett, K. Forrester, B. Gerwin, M. Serrano, D. H. Beach, et al. 1994. Mutations and altered expression of p16INK4 in human cancer. Proc. Natl. Acad. Sci. USA 91:11045-11049.
36. Orian, A., B. Van Steensel, J. Delrow, H. J. Bussemaker, L. Li, T. Sawado, E. Williams, L. W. Loo, S. M. Cowley, C. Yost, S. Pierce, B. A. Edgar, S. M. Parkhurst, and R. N. Eisenman. 2003. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 17:1101-1114.
37. O'Riordan, M., and R. Grosschedl. 1999. Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity 11:21-31.
38. Pagano, M., R. Pepperkok, F. Verde, W. Ansorge, and G. Draetta. 1992. Cyclin A is required at two points in the human cell cycle. EMBO J. 11:961-971.
39. Pagliuca, A., P. Gallo, P. De Luca, and L. Lania. 2000. Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors' promoter activity and negatively affect cell growth. Cancer Res. 60:1376-1382.
40. Park, S. T., G. P. Nolan, and X. H. Sun. 1999. Growth inhibition and apoptosis due to restoration of E2A activity in T cell acute lymphoblastic leukemia cells. J. Exp. Med. 189:501-508.
41. Peverali, F. A., T. Ramqvist, R. Saffrich, R. Pepperkok, M. V. Barone, and L. Philipson. 1994. Regulation of G1 progression by E2A and Id helix-loop-helix proteins. EMBO J. 13:4291-4301.
42. Prabhu, S., A. Ignatova, S. T. Park, and X. H. Sun. 1997. Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol. Cell. Biol. 17:5888-5896.
43. Quelle, D. E., R. A. Ashmun, S. A. Shurtleff, J. Y. Kato, D. Bar-Sagi, M. F. Roussel, and C. J. Sherr. 1993. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7:1559-1571.
44. Reynisdottir, I., K. Polyak, A. Iavarone, and J. Massague. 1995. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev. 9:1831-1845.
45. Roman-Gomez, J., J. A. Castillejo, A. Jimenez, M. G. Gonzalez, F. Moreno, C. Rodriguez Mdel, M. Barrios, J. Maldonado, and A. Torres. 2002. 5′ CpG island hypermethylation is associated with transcriptional silencing of the p21(CIP1/WAF1/SDI1) gene and confers poor prognosis in acute lymphoblastic leukemia. Blood 99:2291-2296.
46. Romanow, W. J., A. W. Langerak, P. Goebel, I. L. Wolvers-Tettero, J. J. van Dongen, A. J. Feeney, and C. Murre. 2000. E2A and EBF act in synergy with the V(D)J recombinase to generate a diverse immunoglobulin repertoire in nonlymphoid cells. Mol. Cell 5:343-353.
47. Ruezinsky, D., H. Beckmann, and T. Kadesch. 1991. Modulation of the IgH enhancer's cell type specificity through a genetic switch. Genes Dev. 5:29-37.
48. Rutherford, M. N., and D. P. LeBrun. 1998. Restricted expression of E2A protein in primary human tissues correlates with proliferation and differentiation. Am. J. Pathol. 153:165-173.
49. Shaughnessy, J., Jr., A. Gabrea, Y. Qi, L. Brents, F. Zhan, E. Tian, J. Sawyer, B. Barlogie, P. L. Bergsagel, and M. Kuehl. 2001. Cyclin D3 at 6p21 is dysregulated by recurrent chromosomal translocations to immunoglobulin loci in multiple myeloma. Blood 98:217-223.
50. Shen, C. P., and T. Kadesch. 1995. B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Biol. 15:4518-4524.
51. Sigvardsson, M., M. O'Riordan, and R. Grosschedl. 1997. EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity 7:25-36.
52. Sonoki, T., L. Harder, D. E. Horsman, L. Karran, 1. Taniguchi, T. G. Willis, S. Gesk, D. Steinemann, E. Zucca, B. Schlegelberger, F. Sole, A. J. Mungall, R. D. Gascoyne, R. Siebert, and M. J. Dyer. 2001. Cyclin D3 is a target gene of t(6,14)(p21.1;q32.3) of mature B-cell malignancies. Blood 98:2837-2844.
53. Suzuki, R., H. Kuroda, H. Komatsu, Y. Hosokawa, Y. Kagami, M. Ogura, S. Nakamura, Y. Kodera, Y. Morishima, R. Ueda, and M. Seto. 1999. Selective usage of D-type cyclins in lymphoid malignancies. Leukemia 13:1335-1342.
54. Tamayo, P., D. Slonim, J. Mesirov, Q. Zhu, S. Kitareewan, E. Dmitrovsky, E. S. Lander, and T. R. Golub. 1999. Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. Proc. Natl. Acad. Sci. USA 96:2907-2912.
55. Teramoto, N., K. Pokrovskaja, L. Szekely, A. Polack, T. Yoshino, T. Akagi, and G. Klein. 1999. Expression of cyclin D2 and D3 in lymphoid lesions. Int. J. Cancer 81:543-550.
56. Tremblay, M., S. Herblot, E. Lecuyer, and T. Hoang. 2003. Regulation of pTα gene expression by a dosage of E2A, HEB, and SCL. J. Biol. Chem. 278:12680-12687.
57. van Steensel, B., and S. Henikoff. 2000. Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat. Biotechnol. 18:424-428.
58. Voronova, A., and D. Baltimore. 1990. Mutations that disrupt DNA binding and dimer formation in the E47 helix-loop-helix protein map to distinct domains. Proc. Natl. Acad. Sci. USA 87:4722-4726.
59. Waldman, T., K. W. Kinzler, and B. Vogelstein. 1995. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 55:5187-5190.
60. Wang, Z., Y. Zhang, J. Lu, S. Sun, and K. Ravid. 1999. Mp1 ligand enhances the transcription of the cyclin D3 gene: a potential role for Sp1 transcription factor. Blood 93:4208-4221.
61. Weintraub, H., T. Genetta, and T. Kadesch. 1994. Tissue-specific gene activation by MyoD: determination of specificity by cis-acting repression elements. Genes Dev. 8:2203-2211.
62. Wines, D. R., P. B. Talbert, D. V. Clark, and S. Henikoff. 1996. Introduction of a DNA methyltransferase into Drosophila to probe chromatin structure in vivo. Chromosoma 104:332-340.
63. Yang, M., H. Nomura, Y. Hu, S. Kaneko, H. Kaneko, M. Tanaka, and K. Nakashima. 1998. Prolactin-induced expression of TATA-less cyclin D3 gene is mediated by Sp1 and AP2. Biochem. Mol. Biol. Int. 44:51-58.
64. Yeoh, E. J., M. E. Ross, S. A. Shurtleff, W. K. Williams, D. Patel, R. Mahfouz, F. G. Behm, S. C. Raimondi, M. V. Relling, A. Patel, C. Cheng, D. Campana, D. Wilkins, X. Zhou, J. Li, H. Liu, C. H. Pui, W. E. Evans, C. Naeve, L. Wong, and J. R. Downing. 2002. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 1:133-143.
65. Young, J. L., and R. W. Miller. 1975. Incidence of malignant tumors in U.S. children. J. Pediatr. 86:254-258.
66. Zhao, F., A. Vilardi, R. J. Neely, and J. K. Choi. 2001. Promotion of cell cycle progression by basic helix-loop-helix E2A. Mol. Cell. Biol. 21:6346-6357.
67. Zhuang, Y., P. Cheng, and H. Weintraub. 1996. B-lymphocyte development is regulated by the combined dosage of three basic helix-loop-helix genes, E2A, E2-2, and HEB. Mol. Cell. Biol. 16:2898-2905.
68. Zhuang, Y., P. Soriano, and H. Weintraub. 1994. The helix-loop-helix gene E2A is required for B cell formation. Cell 79:875-884.