Mutations of N-terminal regions render the retinoblastoma protein insufficient for functions in development and tumor suppression

Molecular and Cellular Biology

Volumn 17, Issue 12, 1997, Pages 7342-7352

  Riley, Daniel J ^a   Liu, Chia Yang ^a   Lee, Wen Hwa ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOBLASTOMA PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; EMBRYO; EMBRYOPATHY; GENE DELETION; GROWTH RETARDATION; HYPOPHYSIS TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

EID: 0030712246     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.12.7342     Document Type: Article

References (59)

1. Baker, J., J.-P. Lui, E. J. Robertson, and A. Efstratiadis. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73-82.
2. Bernards, R., G. M. Shackleford, M. R. Gerber, J. M. Horowitz, S. H. Friend, M. Shartl, E. Bogenmann, J. M. Rapaport, T. McGee, T. P. Dryja, and R. A. Weinberg. 1989. Structure and expression of the murine retinoblastoma gene and characterization of its encoded protein. Proc. Natl. Acad. Sci. USA 86:6474-6478.
3. 706 to Phe substitution in the retinoblastoma protein causes loss of binding to the SV40 T antigen. Cell Growth Differ. 1:647-651.
4. Bignon, Y.-J., Y. Chen, C.-Y. Chang, D. J. Riley, J. J. Windle, P. L. Mellon, and W.-H. Lee. 1993. Expression of a retinoblastoma transgene results in dwarf mice. Genes Dev. 7:1654-1662.
5. Bookstein, R., and W.-H. Lee. 1991. Molecular genetics of the retinoblastoma tumor suppressor gene. Crit. Rev. Oncog. 2:211-227.
6. Buchkovich, K., L. A. Duffy, and E. Harlow. 1989. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58:1097-1105.
7. Chang, C.-Y., D. J. Riley, E. Y.-H. P. Lee, and W.-H. Lee. 1993. Quantitative effects of the retinoblastoma gene on mouse development and tissue-specific tumorigenesis. Cell Growth Differ. 4:1057-1064.
8. Chen, P.-L., P. Scully, J.-Y. Shew, J. Y.-J. Wang, and W.-H. Lee. 1989. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell 58:1193-1198.
9. Chen, P.-L., D. J. Riley, and W.-H. Lee. 1995. The retinoblastoma protein as a fundamental mediator of growth and differentiation signals. Crit. Rev. Eukaryotic Gene Expr. 2:79-95.
10. Chen, P.-L., D. J. Riley, S. Chen-Kiang, and W.-H. Lee. 1996. Retinoblastoma protein directly interacts with and activates the transcription factor NF-IL6. Proc. Natl. Acad. Sci. USA 93:465-469.
11. Chen, P.-L., D. J. Riley, Y. Chen, and W.-H. Lee. 1996. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes Dev. 10:2794-2804.
12. Clarke, A. R., E. R. Maandag, M. van Roon, N. M. T. van der Lugt, M. van der Valk, M. L. Hooper, A. Berns, and H. te Riele. 1992. Requirement for a functional Rb-1 gene in murine development. Nature 359:328-330.
13. DeChiara, T. M., A. Efstratiadis, and E. Robertson. 1990. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345:78-80.
14. Dryja, T. J., J. Rapaport, T. L. McGee, T. M. Nork, and T. L. Schwartz. 1993. Molecular etiology of low-penetrance retinoblastoma in two pedigrees. Am. J. Hum. Genet. 52:1122-1128.
15. Durfee, T., M. A. Mancini, D. Jones, S. J. Elledge, and W.-H. Lee. 1994. The amino terminal region of the retinoblastoma gene product binds a novel nuclear matrix protein that localizes to RNA processing centers. J. Cell Biol. 127:609-622.
16. Enesco, M., and C. P. Leblond. 1962. Increase in cell number as a factor in the growth of organs and tissues of the young male rat. J. Embryol. Exp. Morphol. 10:530-563.
17. Ewen, M. E., Y. Xing, J. B. Lawrence, and D. M. Livingston. 1991. Molecular cloning, chromosomal mapping, and expression of the cDNA for p107, a retinoblastoma gene product-related protein. Cell 66:1155-1164.
18. Fung, Y.-K. T., A. T'Ang, A. L. Murphee, F.-H. Zhang, W.-R. Qui, S.-W. Wang, X. H. Shi, L. Lee, B. Driscol, and K.-J. Wu. 1993. The RB gene product suppresses growth of normal cells. Oncogene 8:2659-2672.
19. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
20. Goodrich, D. W., N. P. Wang, Y. Qian, E. Y.-H. P. Lee, and W.-H. Lee. 1991. The retinoblastoma gene product regulates progression through G1 phase of the cell cycle. Cell 67:293-302.
21. Gu, W., J. W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadal Ginard. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
22. Hannon, G. J., D. Demetrick, and D. Beach. 1993. Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev. 7:2378-2391.
23. Harlow, E., and D. P. Lane. 1988. Antibodies. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
24. Δ19neo allele in the mouse. Oncogene 10:1615-1620.
25. Hensey, C. E., F. Hong, T. Durfee, Y.-W. Qian, E. Y.-H. P. Lee, and W.-H. Lee. 1994. Identification of discrete structural domains in the retinoblastoma protein: amino-terminal domain is required for its oligomerization. J. Biol. Chem. 269:1380-1387.
26. Hinds, P. W., S. Mittnacht, V. Dulic, A. Arnold, S. I. Reed, and R. A. Weinberg. 1992. Regulation of retinoblastoma function by ectopic expression of human cyclins. Cell 70:993-1006.
27. Hogan, B., F. Constantini, and E. Lacy. 1986. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. N.Y.
28. Hogg, A., B. Bia, Z. Onadim, and J. K. Cowelett. 1993. Molecular mechanisms of oncogenic mutations in tumors from patients with bilateral and unilateral retinoblastoma. Proc. Natl. Acad. Sci. USA 90:7351-7355.
29. Hong, F. D., H.-J. S. Huang, H. To, L.-J. S. Young, A. Oro, R. Bookstein, E. Lee, and W.-H. Lee. 1989. Structure of the human retinoblastoma gene. Proc. Natl. Acad. Sci. USA 86:5502-5506.
30. Δ20/+ mice are predisposed to tumors of the pituitary gland with nearly complete penetrance. Oncogene 9:1021-1027.
31. Hu, Q., N. Dyson, and E. Harlow. 1990. The regions of the retinoblastoma protein needed for binding to adenovirus E1A or SV40 large T antigen are common sites for mutation. EMBO J. 9:1147-1155.
32. Huang, S., N. P. Wang, B. Y. Tseng, W.-H. Lee, and E. Y.-H. P. Lee. 1990. Two distinct and frequently mutated regions of the retinoblastoma protein are required for binding to SV40 T antigen. EMBO J. 9:1815-1822.
33. Inoue, A., T. Torigoe, K. Sogahata, K. Kamiguchi, S. Takahashi, Y. Sawada, M. Saijo, Y. Taja, S. Ishii, N. Sato, and N. Kikuchi. 1996. 70-kDa heat shock cognate protein interacts directly with the N-terminal region of the retinoblastoma protein. J. Biol. Chem. 270:22571-22576.
34. Jacks, T., A. Fazeli, E. M. Schmitt, R. T. Bronson, M. A. Goodell, and R. A. Weinberg. 1992. Effects of an Rb mutation in the mouse. Nature 359:295-300.
35. Kaye, F. J., R. A. Kratzke, J. L. Gerster, and J. M. Horowitz. 1990. A single amino acid substitution results in a retinoblastoma protein defective in phosphorylation and oncoprotein binding. Proc. Natl. Acad. Sci. USA 87: 6922-6926.
36. Lee, E. Y.-H. P., C.-Y. Chang, N. Hu, C.-C. Lai, K. Herrup, W.-H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288-294.
37. Lee, E. Y.-H. P., N. Hu, S.-S. F. Yuan, L. A. Cox, A. Bradley, W.-H. Lee, and K. Herrup. 1994. Dual roles for the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev. 8:2008-2021.
38. Lee, W.-H., R. Bookstein, F. Hong, L.-J. Young, J.-Y. Shew, and E. Y.-H. P. Lee. 1987. Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science 235:1394-1399.
39. Lee, W.-H., Y. Zhu, F. Hong, M. A. Mancini, Y.-C. Ueng, P.-L. Chen, and D. J. Riley. 1994. The corral hypothesis: a novel regulatory mode for retinoblastoma protein function. Cold Spring Harbor Symp. Quant. Biol. 59:97-107.
40. Lees, J. A., K. J. Buchkovitch, D. R. Marshak, C. W. Anderson, and E. Harlow. 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 10:4279-4290.
41. Li, Y., C. Graham, S. Lacy, A. M. V. Duncan, and P. Whyte. 1993. The adenovirus E1A-associated 130-kD protein is encoded by a member of the retinoblastoma gene family and physically interacts with cyclins A and E. Genes Dev. 7:2366-2377.
42. Liu, C.-Y., A. Flesken-Nikitin, S. Li, Y. Zeng, and W.-H. Lee. 1996. Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes Dev. 10:1835-1843.
43. Lohmann, D. R., B. Brandt, W. Hopping, E. Passage, and B. Horsthemke. 1994. Distinct RB1 gene mutations with low penetrance in hereditary retinoblastoma. Hum. Genet. 94:349-354.
44. Mayol, X., X. Grana, A. Baldi, N. Sang, Q. Hu, and A. Giordano. 1993. Cloning of a new member of the retinoblastoma gene family (pRB2) which binds to the E1A transforming domain. Oncogene 8:2561-2566.
45. Molkentin, J. D., and E. N. Olson. 1996. Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc. Natl. Acad. Sci. USA 93:9366-9373.
46. Nevins, J. R. 1992. E2F: a link between the retinoblastoma tumor suppressor protein and viral oncoproteins. Science 258:424-429.
47. +/- mice. Genes Dev. 10:1870-1879.
48. Novitch, B. G., G. J. Mulligan, T. Jacks, and A. B. Lassar. 1996. Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. J. Cell Biol. 135:441-456.
49. Qian, Y., C. Luckey, L. Horton, M. Esser, and D. J. Templeton. 1992. Biological function of the retinoblastoma protein requires domains for hyperphosphorylation and transcription factor binding. Mol. Cell. Biol. 12: 5363-5372.
50. Qin, X. Q., T. Chittenden, D. M. Livingston, and W. G. Kaelin. 1992. Identification of a growth suppression domain within the retinoblastoma gene product. Genes Dev. 6:953-964.
51. Riley, D. J., E. Y.-H. P. Lee, and W.-H. Lee. 1994. The retinoblastoma protein: more than a tumor suppressor. Annu. Rev. Cell Biol. 10:1-29.
52. +/- mice. Nat. Med. 2:1316-1321.
53. -/- muscle cells. Science 264:1467-1471.
54. Sterner, J. M., Y. Tao, S. B. Kennett, H. G. Kim, and J. M. Horowitz. 1996. The amino terminus of the retinoblastoma (Rb) protein associates with a cyclin-dependent kinase-like kinase via Rb amino acids required for growth suppression. Cell Growth Differ. 7:53-64.
55. Wang, N. P., P.-L. Chen, S.-H. Huang, L. A. Donoso, W.-H. Lee, and E. Y.-H. P. Lee. 1990. DNA binding activity of retinoblastoma protein is intrinsic to its carboxyl terminal region. Cell Growth Differ. 1:233-239.
56. Williams, B. O., L. Remington, D. M. Albert, S. Makai, R. T. Bronson, and T. Jacks. 1994. Cooperative tumorigeneic effects of germline mutations of Rb and p53. Nat. Genet. 7:480-484.
57. Xu, H. J., K. Xu, Y. Zhou, J. Li, W. F. Benedict, and S. X. Hu. 1994. Enhanced tumor cell growth suppression by an N-terminal truncated retinoblastoma protein. Proc. Natl. Acad. Sci. USA 91:9837-9841.
58. Xu, H. J., Y. Zhou, J. Seigne, G. S. Perng, M. Mixon, C. Zhang, J. Li, W. F. Benedict, and S. X. Hu. 1996. Enhanced tumor suppressor gene therapy via replication deficient adenovirus vectors expressing an N-terminal truncated retinoblastoma protein. Cancer Res. 56:2245-2249.
59. Zacksenhaus, E., Z. Jiang, D. Chung, J. D. Marth, R. A. Phillips, and B. L. Gallie. 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:3051-3064.