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Originally published in Science Express on 11 October 2007
Science 16 November 2007:
Vol. 318. no. 5853, pp. 1108 - 1113
DOI: 10.1126/science.1145720
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Research Articles

The Genomic Landscapes of Human Breast and Colorectal Cancers

Laura D. Wood,1* D. Williams Parsons,1* Siân Jones,1* Jimmy Lin,1* Tobias Sjöblom,1*{dagger} Rebecca J. Leary,1 Dong Shen,1 Simina M. Boca,1,2 Thomas Barber,1{ddagger} Janine Ptak,1 Natalie Silliman,1 Steve Szabo,1 Zoltan Dezso,3 Vadim Ustyanksky,3 Tatiana Nikolskaya,3,4 Yuri Nikolsky,3 Rachel Karchin,5 Paul A. Wilson,5 Joshua S. Kaminker,6 Zemin Zhang,6 Randal Croshaw,7 Joseph Willis,8 Dawn Dawson,8 Michail Shipitsin,9 James K. V. Willson,10 Saraswati Sukumar,11 Kornelia Polyak,9 Ben Ho Park,11 Charit L. Pethiyagoda,12 P. V. Krishna Pant,12 Dennis G. Ballinger,12 Andrew B. Sparks,12§ James Hartigan,13 Douglas R. Smith,13 Erick Suh,13 Nickolas Papadopoulos,1 Phillip Buckhaults,7 Sanford D. Markowitz,14 Giovanni Parmigiani,1|| Kenneth W. Kinzler,1|| Victor E. Velculescu,1|| Bert Vogelstein1||

Human cancer is caused by the accumulation of mutations in oncogenes and tumor suppressor genes. To catalog the genetic changes that occur during tumorigenesis, we isolated DNA from 11 breast and 11 colorectal tumors and determined the sequences of the genes in the Reference Sequence database in these samples. Based on analysis of exons representing 20,857 transcripts from 18,191 genes, we conclude that the genomic landscapes of breast and colorectal cancers are composed of a handful of commonly mutated gene "mountains" and a much larger number of gene "hills" that are mutated at low frequency. We describe statistical and bioinformatic tools that may help identify mutations with a role in tumorigenesis. These results have implications for understanding the nature and heterogeneity of human cancers and for using personal genomics for tumor diagnosis and therapy.

1 The Ludwig Center for Cancer Genetics and Therapeutics and The Howard Hughes Medical Institute at The Johns Hopkins Kimmel Cancer Center, Baltimore, MD 21231, USA.
2 Department of Biostatistics, Johns Hopkins Medical Institutions, Baltimore, MD 21231, USA.
3 GeneGo, St. Joseph, MI 49085, USA.
4 Vavilov Institute of General Genetics, Moscow, Russia.
5 Department of Biomedical Engineering, Institute of Computational Medicine, Johns Hopkins University, Baltimore, MD 21218, USA.
6 Department of Bioinformatics, Genentech, San Francisco, CA 94080, USA.
7 Department of Pathology and Microbiology, The Center for Colon Cancer Research, and The South Carolina Cancer Center, Division of Basic Research, The University of South Carolina, School of Medicine, Columbia, SC 29229, USA.
8 Department of Pathology and Ireland Cancer Center, Case Western Reserve University and University Hospitals of Cleveland, Cleveland, OH 44106, USA.
9 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA.
10 Harold C. Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA.
11 The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.
12 Perlegen Sciences, Mountain View, CA 94043, USA.
13 Agencourt Bioscience Corporation, Beverly, MA 01915, USA.
14 Department of Medicine and Ireland Cancer Center, Case Western Reserve University and University Hospitals of Cleveland, and Howard Hughes Medical Institute, Cleveland, OH 44106, USA.

* These authors contributed equally to this work.

{dagger} Present address: Department of Genetics and Pathology, Uppsala University, SE-751 85 Uppsala, Sweden.

{ddagger} Present address: Lilly Research Labs, Eli Lilly and Company, Indianapolis, IN 42685, USA.

§ Present address: Complete Genomics, Sunnyvale, CA 94085, USA.

|| To whom correspondence should be addressed. E-mail: gp{at}jhu.edu (G.P.); kinzlke{at}jhmi.edu (K.W.K.); velculescu{at}jhmi.edu (V.E.V.); vogelbe{at}welch.jhu.edu (B.V.)

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A Bicistronic CYCLIN D1-TROP2 mRNA Chimera Demonstrates a Novel Oncogenic Mechanism in Human Cancer.
E. Guerra, M. Trerotola, R. Dell' Arciprete, V. Bonasera, B. Palombo, T. El-Sewedy, T. Ciccimarra, C. Crescenzi, F. Lorenzini, C. Rossi, et al. (2008)
Cancer Res. 68, 8113-8121
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Prioritization of candidate cancer genes--an aid to oncogenomic studies.
S. J. Furney, B. Calvo, P. Larranaga, J. A. Lozano, and N. Lopez-Bigas (2008)
Nucleic Acids Res. 36, e115
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Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses.
S. Jones, X. Zhang, D. W. Parsons, J. C.-H. Lin, R. J. Leary, P. Angenendt, P. Mankoo, H. Carter, H. Kamiyama, A. Jimeno, et al. (2008)
Science 321, 1801-1806
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An Integrated Genomic Analysis of Human Glioblastoma Multiforme.
D. W. Parsons, S. Jones, X. Zhang, J. C.-H. Lin, R. J. Leary, P. Angenendt, P. Mankoo, H. Carter, I-M. Siu, G. L. Gallia, et al. (2008)
Science 321, 1807-1812
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Cell type-specific DNA methylation patterns in the human breast.
N. Bloushtain-Qimron, J. Yao, E. L. Snyder, M. Shipitsin, L. L. Campbell, S. A. Mani, M. Hu, H. Chen, V. Ustyansky, J. E. Antosiewicz, et al. (2008)
PNAS 105, 14076-14081
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Profiling SLCO and SLC22 genes in the NCI-60 cancer cell lines to identify drug uptake transporters.
M. Okabe, G. Szakacs, M. A. Reimers, T. Suzuki, M. D. Hall, T. Abe, J. N. Weinstein, and M. M. Gottesman (2008)
Mol. Cancer Ther. 7, 3081-3091
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A Novel Acetylenic Tricyclic bis-(Cyano Enone) Potently Induces Phase 2 Cytoprotective Pathways and Blocks Liver Carcinogenesis Induced by Aflatoxin.
K. Liby, M. M. Yore, B. D. Roebuck, K. J. Baumgartner, T. Honda, C. Sundararajan, H. Yoshizawa, G. W. Gribble, C. R. Williams, R. Risingsong, et al. (2008)
Cancer Res. 68, 6727-6733
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Tumorigenic activity and therapeutic inhibition of Rheb GTPase.
K. J. Mavrakis, H. Zhu, R. L.A. Silva, J. R. Mills, J. Teruya-Feldstein, S. W. Lowe, W. Tam, J. Pelletier, and H.-G. Wendel (2008)
Genes & Dev. 22, 2178-2188
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A genome-wide RNAi screen for Wnt/{beta}-catenin pathway components identifies unexpected roles for TCF transcription factors in cancer.
W. Tang, M. Dodge, D. Gundapaneni, C. Michnoff, M. Roth, and L. Lum (2008)
PNAS 105, 9697-9702
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A comprehensive assay for targeted multiplex amplification of human DNA sequences.
S. Krishnakumar, J. Zheng, J. Wilhelmy, M. Faham, M. Mindrinos, and R. Davis (2008)
PNAS 105, 9296-9301
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The new paradigm of flow cell sequencing.
R. A. Holt and S. J.M. Jones (2008)
Genome Res. 18, 839-846
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The Previously Undescribed ZKSCAN3 (ZNF306) Is a Novel "Driver" of Colorectal Cancer Progression.
L. Yang, S. R. Hamilton, A. Sood, T. Kuwai, L. Ellis, A. Sanguino, G. Lopez-Berestein, and D. D. Boyd (2008)
Cancer Res. 68, 4321-4330
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BRAFV600E Mutation Is Associated with Preferential Sensitivity to Mitogen-Activated Protein Kinase Kinase Inhibition in Thyroid Cancer Cell Lines.
R. Leboeuf, J. E. Baumgartner, M. Benezra, R. Malaguarnera, D. Solit, C. A. Pratilas, N. Rosen, J. A. Knauf, and J. A. Fagin (2008)
J. Clin. Endocrinol. Metab. 93, 2194-2201
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Mechanisms of malignant progression.
R. A. Weinberg (2008)
Carcinogenesis 29, 1092-1095
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Defining the blueprint of the cancer genome.
V. E. Velculescu (2008)
Carcinogenesis 29, 1087-1091
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Genome-Wide Promoter Analysis Uncovers Portions of the Cancer Methylome.
M. O. Hoque, M. S. Kim, K. L. Ostrow, J. Liu, G. B. A. Wisman, H. L. Park, M. L. Poeta, C. Jeronimo, R. Henrique, A. Lendvai, et al. (2008)
Cancer Res. 68, 2661-2670
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Comparative lesion sequencing provides insights into tumor evolution.
S. Jones, W.-d. Chen, G. Parmigiani, F. Diehl, N. Beerenwinkel, T. Antal, A. Traulsen, M. A. Nowak, C. Siegel, V. E. Velculescu, et al. (2008)
PNAS 105, 4283-4288
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Newer Cytotoxic Agents: Attacking Cancer Broadly.
B. A. Teicher (2008)
Clin. Cancer Res. 14, 1610-1617
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An Oncogene-Induced DNA Damage Model for Cancer Development.
T. D. Halazonetis, V. G. Gorgoulis, and J. Bartek (2008)
Science 319, 1352-1355
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Chromatid cohesion defects may underlie chromosome instability in human colorectal cancers.
T. D. Barber, K. McManus, K. W. Y. Yuen, M. Reis, G. Parmigiani, D. Shen, I. Barrett, Y. Nouhi, F. Spencer, S. Markowitz, et al. (2008)
PNAS 105, 3443-3448
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Clonal Selection in Malignant Transformation of Human Fibroblasts Transduced with Defined Cellular Oncogenes.
A. M. Mahale, Z. A.T. Khan, M. Igarashi, G. J. Nanjangud, R. F. Qiao, S. Yao, S. W. Lee, and S. A. Aaronson (2008)
Cancer Res. 68, 1417-1426
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