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Published Online October 11, 2007
Science DOI: 10.1126/science.1145720

Research Articles

Submitted on May 29, 2007
Accepted on October 1, 2007

The Genomic Landscapes of Human Breast and Colorectal Cancers

Laura D. Wood 1{dagger}, D. Williams Parsons 1{dagger}, Siân Jones 1{dagger}, Jimmy Lin 1{dagger}, Tobias Sjöblom 2{dagger}, Rebecca J. Leary 1, Dong Shen 1, Simina M. Boca 3, Thomas Barber 4, Janine Ptak 1, Natalie Silliman 1, Steve Szabo 1, Zoltan Dezso 5, Vadim Ustyanksky 5, Tatiana Nikolskaya 6, Yuri Nikolsky 5, Rachel Karchin 7, Paul A. Wilson 7, Joshua S. Kaminker 8, Zemin Zhang 8, Randal Croshaw 9, Joseph Willis 10, Dawn Dawson 10, Michail Shipitsin 11, James K. V. Willson 12, Saraswati Sukumar 13, Kornelia Polyak 11, Ben Ho Park 13, Charit L. Pethiyagoda 14, P. V. Krishna Pant 14, Dennis G. Ballinger 14, Andrew B. Sparks 15, James Hartigan 16, Douglas R. Smith 16, Erick Suh 16, Nickolas Papadopoulos 1, Phillip Buckhaults 9, Sanford D. Markowitz 17, Giovanni Parmigiani 3*, Kenneth W. Kinzler 1*, Victor E. Velculescu 1*, Bert Vogelstein 1*

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 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.; Present address: Department of Genetics and Pathology, Uppsala University, SE-571 85 Uppsala, Sweden.
3 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.; Departments of Bioinformatics and Pathology, Johns Hopkins Medical Institutions, Baltimore, MD 21231, USA.
4 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.; Present address: Lilly Research Labs, Eli Lilly and Company, Indianapolis, IN 42685, USA.
5 GeneGo, Inc., St. Joseph, MI 49085, USA.
6 GeneGo, Inc., St. Joseph, MI 49085, USA.; Vavilov Institute of General Genetics, Moscow, Russia.
7 Department of Biomedical Engineering, Institute of Computational Medicine, Johns Hopkins University, Baltimore, MD 21218, USA.
8 Department of Bioinformatics, Genentech Inc., San Francisco, CA 94080, USA.
9 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.
10 Department of Pathology and Ireland Cancer Center, Case Western Reserve University and University Hospitals of Cleveland, Cleveland, OH 44106, USA.
11 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA.
12 Harold C. Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA.
13 The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, MD 21231, USA.
14 Perlegen Sciences, Mountain View, CA 94043, USA.
15 Perlegen Sciences, Mountain View, CA 94043, USA.; Present address: Complete Genomics, Inc., Sunnyvale, CA 94085, USA.
16 Agencourt Bioscience Corporation, Beverly, MA 01915, USA.
17 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.

* To whom correspondence should be addressed.
Giovanni Parmigiani , E-mail: gp{at}jhu.edu
Kenneth W. Kinzler , E-mail: kinzlke{at}jhmi.edu
Victor E. Velculescu , E-mail: velculescu{at}jhmi.edu
Bert Vogelstein , E-mail: vogelbe{at}welch.jhu.edu

{dagger}These authors contributed equally to this work.

Human cancer is caused by the accumulation of mutations in oncogenes and tumor suppressor genes. To catalogue 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.


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C. S. Fuchs, R. M. Goldberg, D. J. Sargent, J. A. Meyerhardt, B. M. Wolpin, E. M. Green, H. C. Pitot, and M. Pollak (2008)
Clin. Cancer Res. 14, 8263-8269
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Unbiased Screening for Transcriptional Targets of ZKSCAN3 Identifies Integrin {beta}4 and Vascular Endothelial Growth Factor as Downstream Targets.
L. Yang, L. Zhang, Q. Wu, and D. D. Boyd (2008)
J. Biol. Chem. 283, 35295-35304
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A genomic approach to colon cancer risk stratification yields biologic insights into therapeutic opportunities.
K. S. Garman, C. R. Acharya, E. Edelman, M. Grade, J. Gaedcke, S. Sud, W. Barry, A. M. Diehl, D. Provenzale, G. S. Ginsburg, et al. (2008)
PNAS 105, 19432-19437
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Mining the Epigenome for Methylated Genes in Lung Cancer.
M. Tessema and S. A. Belinsky (2008)
Proceedings of the ATS 5, 806-810
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Genome-Wide Functional Synergy between Amplified and Mutated Genes in Human Breast Cancer.
Y. Nikolsky, E. Sviridov, J. Yao, D. Dosymbekov, V. Ustyansky, V. Kaznacheev, Z. Dezso, L. Mulvey, L. E. Macconaill, W. Winckler, et al. (2008)
Cancer Res. 68, 9532-9540
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Identification of Pbx1, a Potential Oncogene, as a Notch3 Target Gene in Ovarian Cancer.
J. T. Park, I.-M. Shih, and T.-L. Wang (2008)
Cancer Res. 68, 8852-8860
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Nested Patch PCR enables highly multiplexed mutation discovery in candidate genes.
K. E. Varley and R. D. Mitra (2008)
Genome Res. 18, 1844-1850
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Integrated analysis of homozygous deletions, focal amplifications, and sequence alterations in breast and colorectal cancers.
R. J. Leary, J. C. Lin, J. Cummins, S. Boca, L. D. Wood, D. W. Parsons, S. Jones, T. Sjoblom, B.-H. Park, R. Parsons, et al. (2008)
PNAS 105, 16224-16229
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Loss of the Epigenetic Tumor Suppressor SNF5 Leads to Cancer without Genomic Instability.
E. S. McKenna, C. G. Sansam, Y.-J. Cho, H. Greulich, J. A. Evans, C. S. Thom, L. A. Moreau, J. A. Biegel, S. L. Pomeroy, and C. W. M. Roberts (2008)
Mol. Cell. Biol. 28, 6223-6233
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The Conflict Between Complex Systems and Reductionism.
H. H. Q. Heng (2008)
JAMA 300, 1580-1581
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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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