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Science 13 March 1987:
Vol. 235. no. 4794, pp. 1394 - 1399
DOI: 10.1126/science.3823889
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Articles

Science, Vol 235, Issue 4794, 1394-1399
Copyright © 1987 by American Association for the Advancement of Science

articles

Human retinoblastoma susceptibility gene: cloning, identification, and sequence

WH Lee, R Bookstein, F Hong, LJ Young, JY Shew, and EY Lee

Recent evidence indicates the existence of a genetic locus in chromosome region 13q14 that confers susceptibility to retinoblastoma, a cancer of the eye in children. A gene encoding a messenger RNA (mRNA) of 4.6 kilobases (kb), located in the proximity of esterase D, was identified as the retinoblastoma susceptibility (RB) gene on the basis of chromosomal location, homozygous deletion, and tumor-specific alterations in expression. Transcription of this gene was abnormal in six of six retinoblastomas examined: in two tumors, RB mRNA was not detectable, while four others expressed variable quantities of RB mRNA with decreased molecular size of about 4.0 kb. In contrast, full-length RB mRNA was present in human fetal retina and placenta, and in other tumors such as neuroblastoma and medulloblastoma. DNA from retinoblastoma cells had a homozygous gene deletion in one case and hemizygous deletion in another case, while the remainder were not grossly different from normal human control DNA. The gene contains at least 12 exons distributed in a region of over 100 kb. Sequence analysis of complementary DNA clones yielded a single long open reading frame that could encode a hypothetical protein of 816 amino acids. A computer-assisted search of a protein sequence database revealed no closely related proteins. Features of the predicted amino acid sequence include potential metal-binding domains similar to those found in nucleic acid-binding proteins. These results provide a framework for further study of recessive genetic mechanisms in human cancers.


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Subconjunctival Topotecan in Fibrin Sealant in the Treatment of Transgenic Murine Retinoblastoma.
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Invest. Ophthalmol. Vis. Sci. 49, 490-496
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Dicot and monocot plants differ in retinoblastoma-related protein subfamilies.
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J. Exp. Bot. 58, 1663-1675
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A new human retrovirus associated with prostate cancer.
H. Fan (2007)
PNAS 104, 1449-1450
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Retinoblastoma tumor suppressor: where cancer meets the cell cycle..
E. S. Knudsen and K. E. Knudsen (2006)
Experimental Biology and Medicine 231, 1271-1281
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The Retinoblastoma Protein Is Required for Ras-Induced Oncogenic Transformation.
J. P. Williams, T. Stewart, B. Li, R. Mulloy, D. Dimova, and M. Classon (2006)
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Effects of celecoxib in human retinoblastoma cell lines and in a transgenic murine model of retinoblastoma.
C T Tong, S A Howard, H R Shah, K R Van Quill, E T Lin, H E Grossniklaus, and J M O'Brien (2005)
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Cyclosporin A Inhibits Calcineurin/Nuclear Factor of Activated T-Cells Signaling and Induces Apoptosis in Retinoblastoma Cells.
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Epigenetic Changes in Prostate Cancer: Implication for Diagnosis and Treatment.
L.-C. Li, P. R. Carroll, and R. Dahiya (2005)
J Natl Cancer Inst 97, 103-115
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From ORFeome to Biology: A Functional Genomics Pipeline.
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Genome Res. 14, 2136-2144
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Cell type-specific effects of Rb deletion in the murine retina.
D. MacPherson, J. Sage, T. Kim, D. Ho, M. E. McLaughlin, and T. Jacks (2004)
Genes & Dev. 18, 1681-1694
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Oncogenes and Tumor Suppressor Genes in Breast Cancer: Potential Diagnostic and Therapeutic Applications.
C. Osborne, P. Wilson, and D. Tripathy (2004)
Oncologist 9, 361-377
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Mouse models of childhood cancer of the nervous system.
M A Dyer (2004)
J. Clin. Pathol. 57, 561-576
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Retinoblastoma Protein Is Frequently Absent or Phosphorylated in Anaplastic Large-Cell Lymphoma.
G. Z. Rassidakis, R. Lai, M. Herling, C. Cromwell, A. Schmitt-Graeff, and L. J. Medeiros (2004)
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IGF-I stimulates human intestinal smooth muscle cell growth by regulation of G1 phase cell cycle proteins.
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Rapid Identification of Germline Mutations in Retinoblastoma by Protein Truncation Testing.
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Arch Ophthalmol 122, 239-248
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Retinoblastoma Protein and CCAAT/Enhancer-Binding Protein {beta} Are Required for 1,25-Dihydroxyvitamin D3-Induced Monocytic Differentiation of HL60 Cells.
Y. Ji and G. P. Studzinski (2004)
Cancer Res. 64, 370-377
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E2F3 Loss Has Opposing Effects on Different pRB-Deficient Tumors, Resulting in Suppression of Pituitary Tumors but Metastasis of Medullary Thyroid Carcinomas.
U. Ziebold, E. Y. Lee, R. T. Bronson, and J. A. Lees (2003)
Mol. Cell. Biol. 23, 6542-6552
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Loss of PTEN Promotes Tumor Development in Malignant Melanoma.
J. M. Stahl, M. Cheung, A. Sharma, N. R. Trivedi, S. Shanmugam, and G. P. Robertson (2003)
Cancer Res. 63, 2881-2890
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Gene Expression Networks Underlying Retinoic Acid-Induced Differentiation of Human Retinoblastoma Cells.
A. Li, X. Zhu, B. Brown, and C. M. Craft (2003)
Invest. Ophthalmol. Vis. Sci. 44, 996-1007
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Loss of pRb2/p130 Expression Is Associated with Unfavorable Clinical Outcome in Lung Cancer.
M. Caputi, A. M. Groeger, V. Esposito, A. De Luca, V. Masciullo, A. Mancini, F. Baldi, E. Wolner, and A. Giordano (2002)
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Identification of Frequent G2 Checkpoint Impairment and a Homozygous Deletion of 14-3-3{epsilon} at 17p13.3 in Small Cell Lung Cancers.
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Expression of a human polyomavirus oncoprotein and tumour suppressor proteins in medulloblastomas.
L Del Valle, J Baehring, C Lorenzana, A Giordano, K Khalili, and S Croul (2001)
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Chromosomal Abnormalities Subdivide Ependymal Tumors into Clinically Relevant Groups.
Y. Hirose, K. Aldape, A. Bollen, C. D. James, D. Brat, K. Lamborn, M. Berger, and B. G. Feuerstein (2001)
Am. J. Pathol. 158, 1137-1143
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RB2/p130 Gene-enhanced Expression Down-Regulates Vascular Endothelial Growth Factor Expression and Inhibits Angiogenesis in Vivo.
P. P. Claudio, P. Stiegler, C. M. Howard, C. Bellan, C. Minimo, G. M. Tosi, J. Rak, A. Kovatich, Paola De Fazio, P. Micheli, et al. (2001)
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Differential Genetic Alterations in von Hippel-Lindau Syndrome-Associated and Sporadic Pheochromocytomas.
B. U. Bender, M. Gutsche, S. Gläsker, B. Müller, G. Kirste, C. Eng, and H. P. H. Neumann (2000)
J. Clin. Endocrinol. Metab. 85, 4568-4574
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Deregulation of the Rb and p53 Pathways in Uveal Melanoma.
M. A. Brantley Jr. and J. W. Harbour (2000)
Am. J. Pathol. 157, 1795-1801
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The Rb/E2F pathway: expanding roles and emerging paradigms.
J. W. Harbour and D. C. Dean (2000)
Genes & Dev. 14, 2393-2409
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Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum.
S. Marino, M. Vooijs, H. van der Gulden, J. Jonkers, and A. Berns (2000)
Genes & Dev. 14, 994-1004
   Abstract »    Full Text »
Loss of pRb Expression in Pituitary Adenomas Is Associated with Methylation of the RB1 CpG Island.
D. J. Simpson, N. A. Hibberts, A. M. McNicol, R. N. Clayton, and W. E. Farrell (2000)
Cancer Res. 60, 1211-1216
   Abstract »    Full Text »
Aromatic Hydrocarbon Receptor Interaction with the Retinoblastoma Protein Potentiates Repression of E2F-dependent Transcription and Cell Cycle Arrest.
A. Puga, S. J. Barnes, T. P. Dalton, C.-y. Chang, E. S. Knudsen, and M. A. Maier (2000)
J. Biol. Chem. 275, 2943-2950
   Abstract »    Full Text »    PDF »
Mutations in the Retinoblastoma-related Gene RB2/p130 in Lung Tumors and Suppression of Tumor Growth in Vivo by Retrovirus-mediated Gene Transfer.
P. P. Claudio, C. M. Howard, C. Pacilio, C. Cinti, G. Romano, C. Minimo, N. M. Maraldi, J. D. Minna, L. Gelbert, L. Leoncini, et al. (2000)
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Allelic Loss in Esophageal Squamous Cell Carcinoma Patients with and without Family History of Upper Gastrointestinal Tract Cancer.
N. Hu, M. J. Roth, M. R. Emmert-Buck, Z.-Z. Tang, M. Polymeropolous, Q.-H. Wang, A. M. Goldstein, X.-Y. Han, S. M. Dawsey, T. Ding, et al. (1999)
Clin. Cancer Res. 5, 3476-3482
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The Chromosome 10 Monosomy Common in Human Melanomas Results from the Loss of Two Separate Tumor Suppressor Loci.
G. P. Robertson, R. A. Herbst, M. Nagane, H-J. S. Huang, and W. K. Cavenee (1999)
Cancer Res. 59, 3596-3601
   Abstract »    Full Text »    PDF »
Paradoxical Increase in Retinoblastoma Protein in Colorectal Carcinomas May Protect Cells from Apoptosis.
H. Yamamoto, J.-W. Soh, T. Monden, M. G. Klein, L. M. Zhang, H. Shirin, N. Arber, N. Tomita, I. Schieren, C. A. Stein, et al. (1999)
Clin. Cancer Res. 5, 1805-1815
   Abstract »    Full Text »    PDF »
The Molecular Pathogenesis of Corticotroph Tumors.
P. L. M. Dahia and A. B. Grossman (1999)
Endocr. Rev. 20, 136-155
   Abstract »    Full Text »
Urinary Bladder Transitional Cell Carcinogenesis Is Associated with Down-Regulation of NF1 Tumor Suppressor Gene in Vivo and in Vitro.
V. Aaltonen, P. J. Bostrom, K.-O. Soderstrom, O. Hirvonen, J. Tuukkanen, M. Nurmi, M. Laato, and J. Peltonen (1999)
Am. J. Pathol. 154, 755-765
   Abstract »    Full Text »    PDF »
Novel Mechanisms of E2F Induction by BK Virus Large-T Antigen: Requirement of Both the pRb-Binding and the J Domains.
K. F. Harris, J. B. Christensen, E. H. Radany, and M. J. Imperiale (1998)
Mol. Cell. Biol. 18, 1746-1756
   Abstract »    Full Text »
A thyroid hormone receptor coactivator negatively regulated by the retinoblastoma protein.
K.-H. Chang, Y. Chen, T.-T. Chen, W.-H. Chou, P.-L. Chen, Y.-Y. Ma, T. L. Yang-Feng, X. Leng, M.-J. Tsai, B. W. O'Malley, et al. (1997)
PNAS 94, 9040-9045
   Abstract »    Full Text »    PDF »
Retinoblastoma in a Dog.
N. A. Syed, T. M. Nork, G. L. Poulsen, R. C. Riis, C. George, and D. M. Albert (1997)
Arch Ophthalmol 115, 758-763
   Abstract »    PDF »
High Molecular Weight Protein Phosphatase Type 1Dephosphorylates the Retinoblastoma Protein.
D. A. Nelson, N. A. Krucher, and J. W. Ludlow (1997)
J. Biol. Chem. 272, 4528-4535
   Abstract »    Full Text »    PDF »
p202, an Interferon-inducible Modulator of Transcription, Inhibits Transcriptional Activation by the p53 Tumor Suppressor Protein, and a Segment from the p53-binding Protein 1That Binds to p202 Overcomes This Inhibition.
B. Datta, B. Li, D. Choubey, G. Nallur, and P. Lengyel (1996)
J. Biol. Chem. 271, 27544-27555
   Abstract »    Full Text »    PDF »
Targeted disruption of p107: functional overlap between p107 and Rb..
M H Lee, B O Williams, G Mulligan, S Mukai, R T Bronson, N Dyson, E Harlow, and T Jacks (1996)
Genes & Dev. 10, 1621-1632
   Abstract »    PDF »
Molecular Cloning and Developmental Expression of Mouse p130, a Member of the Retinoblastoma Gene Family.
G. Chen, C. T. Guy, H.-W. Chen, N. Hu, E. Y.-H. P. Lee, and W.-H. Lee (1996)
J. Biol. Chem. 271, 9567-9572
   Abstract »    Full Text »    PDF »
Binding of an Interferon-inducible Protein (p202) to the Retinoblastoma Protein.
D. Choubey and P. Lengyel (1995)
J. Biol. Chem. 270, 6134-6140
   Abstract »    Full Text »    PDF »
The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein..
A Iavarone, P Garg, A Lasorella, J Hsu, and M A Israel (1994)
Genes & Dev. 8, 1270-1284
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Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53..
K A Howes, N Ransom, D S Papermaster, J G Lasudry, D M Albert, and J J Windle (1994)
Genes & Dev. 8, 1300-1310
   Abstract »    PDF »
The Corral Hypothesis: A Novel Regulatory Mode for Retinoblastoma Protein Function.
W.-H. Lee, Y. Xu, F. Hong, T. Durfee, M.A. Mancini, Y.-C. Ueng, P.-L. Chen, and D. Riley (1994)
Cold Spring Harb Symp Quant Biol 59, 97-107
   Abstract »    PDF »
Pseudo Low Penetrance in Retinoblastoma: Fortuitous Familial Aggregation of Sporadic Cases Caused by Independently Derived Mutations in Two Large Pedigrees.
F. L. Munier, M. X. Wang, M. A. Spence, F. Thonney, A. Balmer, G. Pescia, L. A. Donoso, and A. L. Murphree (1993)
Arch Ophthalmol 111, 1507-1511
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Cloning of Tumor Suppressor Genes Involved in Solid Tumor Development.
D. I. Smith and M. del Mar Alonso (1993)
Arch Otolaryngol Head Neck Surg 119, 1210-1216
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Expression of a retinoblastoma transgene results in dwarf mice..
Y J Bignon, Y Chen, C Y Chang, D J Riley, J J Windle, P L Mellon, and W H Lee (1993)
Genes & Dev. 7, 1654-1662
   Abstract »    PDF »
Regulation of the Ets-related transcription factor Elf-1 by binding to the retinoblastoma protein.
C. Wang, B Petryniak, C. Thompson, W. Kaelin, and J. Leiden (1993)
Science 260, 1330-1335
   Abstract »    PDF »
The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit..
T Durfee, K Becherer, P L Chen, S H Yeh, Y Yang, A E Kilburn, W H Lee, and S J Elledge (1993)
Genes & Dev. 7, 555-569
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Identification of a growth suppression domain within the retinoblastoma gene product..
X Q Qin, T Chittenden, D M Livingston, and W G Kaelin (1992)
Genes & Dev. 6, 953-964
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An Ocular Melanoma-Associated Antigen: Molecular Characterization.
M. X. Wang, J. J. Earley Jr, J. A. Shields, and L. A. Donoso (1992)
Arch Ophthalmol 110, 399-404
   Abstract »    PDF »
Tumor suppressor genes.
R. Weinberg (1991)
Science 254, 1138-1146
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Growth factors and cancer.
S. Aaronson (1991)
Science 254, 1146-1153
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Molecular basis of mouse developmental mutants..
A D Reith and A Bernstein (1991)
Genes & Dev. 5, 1115-1123
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A mouse model of the aniridia-Wilms tumor deletion syndrome.
T Glaser, J Lane, and D Housman (1990)
Science 250, 823-827
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A Transgenic Mouse Model for Trilateral Retinoblastoma.
J. M. O'Brien, D. M. Marcus, R. Bernards, J. L. Carpenter, J. J. Windle, P. Mellon, and D. M. Albert (1990)
Arch Ophthalmol 108, 1145-1151
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Suppression of tumorigenicity of human prostate carcinoma cells by replacing a mutated RB gene.
R Bookstein, J. Shew, P. Chen, P Scully, and W. Lee (1990)
Science 247, 712-715
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Tumorigenicity in human melanoma cell lines controlled by introduction of human chromosome 6.
J. Trent, E. Stanbridge, H. McBride, E. Meese, G Casey, D. Araujo, C. Witkowski, and R. Nagle (1990)
Science 247, 568-571
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Identifying tumor suppressor genes in human colorectal cancer.
E. Stanbridge (1990)
Science 247, 12-13
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Identification of a chromosome 18q gene that is altered in colorectal cancers.
E. Fearon, K. Cho, J. Nigro, S. Kern, J. Simons, J. Ruppert, Hamilton SR, A. Preisinger, G Thomas, K. Kinzler, et al. (1990)
Science 247, 49-56
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Tumor suppressor genes: the puzzle and the promise.
R Sager (1989)
Science 246, 1406-1412
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Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product.
K Mihara, X. Cao, A Yen, S Chandler, B Driscoll, A. Murphree, A T'Ang, and Y. Fung (1989)
Science 246, 1300-1303
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p53: a frequent target for genetic abnormalities in lung cancer.
T Takahashi, M. Nau, I Chiba, M. Birrer, R. Rosenberg, M Vinocour, M Levitt, H Pass, A. Gazdar, and J. Minna (1989)
Science 246, 491-494
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Cloning of breakpoints of a chromosome translocation identifies the AN2 locus.
M Gessler, K. Simola, and G. Bruns (1989)
Science 244, 1575-1578
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The Molecular Biology of Medullary Thyroid Carcinoma: A Model for Cancer Development and Progression.
B. D. Nelkin, A. C. de Bustros, M. Mabry, and S. B. Baylin (1989)
JAMA 261, 3130-3135
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Allelotype of colorectal carcinomas.
B Vogelstein, E. Fearon, S. Kern, Hamilton SR, A. Preisinger, Y Nakamura, and R White (1989)
Science 244, 207-211
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Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas.
S. Baker, E. Fearon, J. Nigro, Hamilton SR, A. Preisinger, J. Jessup, P vanTuinen, D. Ledbetter, D. Barker, Y Nakamura, et al. (1989)
Science 244, 217-221
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The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product.
N Dyson, P. Howley, K Munger, and E Harlow (1989)
Science 243, 934-937
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Point mutational inactivation of the retinoblastoma antioncogene.
J. Horowitz, D. Yandell, S. Park, S Canning, P Whyte, K Buchkovich, E Harlow, R. Weinberg, and T. Dryja (1989)
Science 243, 937-940
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Suppression of the neoplastic phenotype by replacement of the RB gene in human cancer cells.
H. Huang, J. Yee, J. Shew, P. Chen, R Bookstein, T Friedmann, E. Lee, and W. Lee (1988)
Science 242, 1563-1566
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Structural rearrangement of the retinoblastoma gene in human breast carcinoma.
A T'Ang, J. Varley, S Chakraborty, A. Murphree, and Y. Fung (1988)
Science 242, 263-266
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Identification of germline and somatic mutations affecting the retinoblastoma gene.
J. Dunn, R. Phillips, A. Becker, and B. Gallie (1988)
Science 241, 1797-1800
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Concerted nonsyntenic allelic loss in human colorectal carcinoma.
D. Law, S Olschwang, J. Monpezat, D Lefrancois, D Jagelman, N. Petrelli, G Thomas, and A. Feinberg (1988)
Science 241, 961-965
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Cutaneous Malignant Melanoma in Survivors of Heritable Retinoblastoma.
E. I. Traboulsi, L. E. Zimmerman, and H. J. Manz (1988)
Arch Ophthalmol 106, 1059-1061
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Abnormalities in structure and expression of the human retinoblastoma gene in SCLC.
J. Harbour, S. Lai, J Whang-Peng, A. Gazdar, J. Minna, and F. Kaye (1988)
Science 241, 353-357
   Abstract »    PDF »
Inactivation of the retinoblastoma susceptibility gene in human breast cancers.
E. Lee, H To, J. Shew, R Bookstein, P Scully, and W. Lee (1988)
Science 241, 218-221
   Abstract »    PDF »
Absence of TGF-beta receptors and growth inhibitory responses in retinoblastoma cells.
A Kimchi, X. Wang, R. Weinberg, S Cheifetz, and J Massague (1988)
Science 240, 196-199
   Abstract »    PDF »
Cone cell-specific genes expressed in retinoblastoma.
E Bogenmann, M. Lochrie, and M. Simon (1988)
Science 240, 76-78
   Abstract »    PDF »
Recent Studies of the Retinoblastoma Gene: What It Means to the Ophthalmologist.
D. M. Albert and T. P. Dryja (1988)
Arch Ophthalmol 106, 181-182
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The CD14 monocyte differentiation antigen maps to a region encoding growth factors and receptors.
S. Goyert, E Ferrero, W. Rettig, A. Yenamandra, F Obata, and M. Le Beau (1988)
Science 239, 497-500
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Anti-oncogenes and the Negative Regulation of Cell Growth.
J.M. Horowitz, S.H. Friend, R.A. Weinberg, P. Whyte, K. Buchkovich, and E. Harlow (1988)
Cold Spring Harb Symp Quant Biol 53, 843-847
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The approaching era of the tumor suppressor genes.
G Klein (1987)
Science 238, 1539-1545
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Molecular genetics: applications to the clinical neurosciences.
J. Martin (1987)
Science 238, 765-772
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Pancreatic neoplasia induced by SV40 T-antigen expression in acinar cells of transgenic mice.
D. Ornitz, R. Hammer, A Messing, R. Palmiter, and R. Brinster (1987)
Science 238, 188-193
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Clonal analysis of human colorectal tumors.
E. Fearon, Hamilton SR, and B Vogelstein (1987)
Science 238, 193-197
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Genetics and Cancer Prevention: What the Future May Hold.
C. Carter and M. Reichman (1987)
Eval Health Prof 10, 359-364
   Abstract »    PDF »
Structural evidence for the authenticity of the human retinoblastoma gene.
Y. Fung, A. Murphree, A T'Ang, J Qian, S. Hinrichs, and W. Benedict (1987)
Science 236, 1657-1661
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Disease diagnosis by recombinant DNA methods.
C. Caskey (1987)
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Science. ISSN 0036-8075 (print), 1095-9203 (online)