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A taxonomy of epithelial human cancer and their metastases

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Gevaert, Olivier Daemen, Anneleen De Moor, Bart Libbrecht, Louis [UCL]

BACKGROUND: Microarray technology has allowed to molecularly characterize many different cancer sites. This technology has the potential to individualize therapy and to discover new drug targets. However, due to technological differences and issues in standardized sample collection no study has evaluated the molecular profile of epithelial human cancer in a large number of samples and tissues. Additionally, it has not yet been extensively investigated whether metastases resemble their tissue of origin or tissue of destination. METHODS: We studied the expression profiles of a series of 1566 primary and 178 metastases by unsupervised hierarchical clustering. The clustering profile was subsequently investigated and correlated with clinico-pathological data. Statistical enrichment of clinico-pathological annotations of groups of samples was investigated using Fisher exact test. Gene set enrichment analysis (GSEA) and DAVID functional enrichment analysis were used to investigate the molecular pathways. Kaplan-Meier survival analysis and log-rank tests were used to investigate prognostic significance of gene signatures. RESULTS: Large clusters corresponding to breast, gastrointestinal, ovarian and kidney primary tissues emerged from the data. Chromophobe renal cell carcinoma clustered together with follicular differentiated thyroid carcinoma, which supports recent morphological descriptions of thyroid follicular carcinoma-like tumors in the kidney and suggests that they represent a subtype of chromophobe carcinoma. We also found an expression signature identifying primary tumors of squamous cell histology in multiple tissues. Next, a subset of ovarian tumors enriched with endometrioid histology clustered together with endometrium tumors, confirming that they share their etiopathogenesis, which strongly differs from serous ovarian tumors. In addition, the clustering of colon and breast tumors correlated with clinico-pathological characteristics. Moreover, a signature was developed based on our unsupervised clustering of breast tumors and this was predictive for disease-specific survival in three independent studies. Next, the metastases from ovarian, breast, lung and vulva cluster with their tissue of origin while metastases from colon showed a bimodal distribution. A significant part clusters with tissue of origin while the remaining tumors cluster with the tissue of destination. CONCLUSION: Our molecular taxonomy of epithelial human cancer indicates surprising correlations over tissues. This may have a significant impact on the classification of many cancer sites and may guide pathologists, both in research and daily practice. Moreover, these results based on unsupervised analysis yielded a signature predictive of clinical outcome in breast cancer. Additionally, we hypothesize that metastases from gastrointestinal origin either remember their tissue of origin or adapt to the tissue of destination. More specifically, colon metastases in the liver show strong evidence for such a bimodal tissue specific profile.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2009
Language Anglais
Journal information "BMC Medical Genomics" - Vol. 2, no.1, p. 69 [1-16] (2009)
Peer reviewed yes
Publisher BioMed Central Ltd. ((United Kingdom) London)
issn 1755-8794
e-issn 1755-8794
Publication status Publié
Affiliation [KUL]
MESH Subject Cluster Analysis ; Systems Biology ; Gene Expression Profiling ; Genomics ; Humans ; Internationality ; Neoplasm Metastasis ; Neoplasms, Glandular and Epithelial ; Neoplasms, Unknown Primary ; Oligonucleotide Array Sequence Analysis
Links
  1. Chung Christine H., Bernard Philip S., Perou Charles M., Molecular portraits and the family tree of cancer, 10.1038/ng1038
  2. Golub T. R., Molecular Classification of Cancer: Class Discovery and Class Prediction by Gene Expression Monitoring, 10.1126/science.286.5439.531
  3. Weigelt Britta, Hu Zhiyuan, He Xiaping, Livasy Chad, Carey Lisa A., Ewend Matthew G., Glas Annuska M., Perou Charles M., van't Veer Laura J., Molecular Portraits and 70-Gene Prognosis Signature Are Preserved throughout the Metastatic Process of Breast Cancer, 10.1158/0008-5472.can-05-2553
  4. Sorlie T., Tibshirani R., Parker J., Hastie T., Marron J. S., Nobel A., Deng S., Johnsen H., Pesich R., Geisler S., Demeter J., Perou C. M., Lonning P. E., Brown P. O., Borresen-Dale A.-L., Botstein D., Repeated observation of breast tumor subtypes in independent gene expression data sets, 10.1073/pnas.0932692100
  5. Hayes D. Neil, Monti Stefano, Parmigiani Giovanni, Gilks C. Blake, Naoki Katsuhiko, Bhattacharjee Arindam, Socinski Mark A., Perou Charles, Meyerson Matthew, Gene Expression Profiling Reveals Reproducible Human Lung Adenocarcinoma Subtypes in Multiple Independent Patient Cohorts, 10.1200/jco.2005.05.1748
  6. Perou Charles M., Sørlie Therese, Eisen Michael B., van de Rijn Matt, Jeffrey Stefanie S., Rees Christian A., Pollack Jonathan R., Ross Douglas T., Johnsen Hilde, Akslen Lars A., Fluge Øystein, Pergamenschikov Alexander, Williams Cheryl, Zhu Shirley X., Lønning Per E., Børresen-Dale Anne-Lise, Brown Patrick O., Botstein David, 10.1038/35021093
  7. Bhattacharjee A., Richards W. G., Staunton J., Li C., Monti S., Vasa P., Ladd C., Beheshti J., Bueno R., Gillette M., Loda M., Weber G., Mark E. J., Lander E. S., Wong W., Johnson B. E., Golub T. R., Sugarbaker D. J., Meyerson M., Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses, 10.1073/pnas.191502998
  8. Alizadeh Ash A., Eisen Michael B., Davis R. Eric, Ma Chi, Lossos Izidore S., Rosenwald Andreas, Boldrick Jennifer C., Sabet Hajeer, Tran Truc, Yu Xin, Powell John I., Yang Liming, Marti Gerald E., Moore Troy, Hudson James, Lu Lisheng, Lewis David B., Tibshirani Robert, Sherlock Gavin, Chan Wing C., Greiner Timothy C., Weisenburger Dennis D., Armitage James O., Warnke Roger, Levy Ronald, Wilson Wyndham, Grever Michael R., Byrd John C., Botstein David, Brown Patrick O., Staudt Louis M., Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling, 10.1038/35000501
  9. Sorlie T., Perou C. M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M. B., van de Rijn M., Jeffrey S. S., Thorsen T., Quist H., Matese J. C., Brown P. O., Botstein D., Lonning P. E., Borresen-Dale A.-L., Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications, 10.1073/pnas.191367098
  10. Ramaswamy S., Tamayo P., Rifkin R., Mukherjee S., Yeang C.-H., Angelo M., Ladd C., Reich M., Latulippe E., Mesirov J. P., Poggio T., Gerald W., Loda M., Lander E. S., Golub T. R., Multiclass cancer diagnosis using tumor gene expression signatures, 10.1073/pnas.211566398
  11. Giordano Thomas J., Shedden Kerby A., Schwartz Donald R., Kuick Rork, Taylor Jeremy M.G., Lee Nana, Misek David E., Greenson Joel K., Kardia Sharon L.R., Beer David G., Rennert Gad, Cho Kathleen R., Gruber Stephen B., Fearon Eric R., Hanash Samir, Organ-Specific Molecular Classification of Primary Lung, Colon, and Ovarian Adenocarcinomas Using Gene Expression Profiles, 10.1016/s0002-9440(10)62509-6
  12. Rhodes D. R., Yu J., Shanker K., Deshpande N., Varambally R., Ghosh D., Barrette T., Pandey A., Chinnaiyan A. M., Large-scale meta-analysis of cancer microarray data identifies common transcriptional profiles of neoplastic transformation and progression, 10.1073/pnas.0401994101
  13. Ramaswamy Sridhar, Ross Ken N., Lander Eric S., Golub Todd R., A molecular signature of metastasis in primary solid tumors, 10.1038/ng1060
  14. Glinsky Gennadi V., Berezovska Olga, Glinskii Anna B., Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer, 10.1172/jci23412
  15. Pavlidis Nicholas, Fizazi Karim, Cancer of unknown primary (CUP), 10.1016/j.critrevonc.2004.10.002
  16. Tothill Richard W., Kowalczyk Adam, Rischin Danny, Bousioutas Alex, Haviv Izhak, van Laar Ryan K., Waring Paul M., Zalcberg John, Ward Robyn, Biankin Andrew V., Sutherland Robert L., Henshall Susan M., Fong Kwun, Pollack Jonathan R., Bowtell David D.L., Holloway Andrew J., An Expression-Based Site of Origin Diagnostic Method Designed for Clinical Application to Cancer of Unknown Origin, 10.1158/0008-5472.can-04-3617
  17. Bender Richard A., Erlander Mark G., Molecular Classification of Unknown Primary Cancer, 10.1053/j.seminoncol.2008.10.002
  18. Bloom Greg, Yang Ivana V., Boulware David, Kwong Ka Yin, Coppola Domenico, Eschrich Steven, Quackenbush John, Yeatman Timothy J., Multi-Platform, Multi-Site, Microarray-Based Human Tumor Classification, 10.1016/s0002-9440(10)63090-8
  19. Ma XJ, Patel R, Wang XQ, Salunga R, Murage J, Desai R, et al: Molecular classification of human cancers using a 92-gene real-time quantitative polymerase chain reaction assay. Archives of Pathology & Laboratory Medicine. 2006, 130: 465-473.
  20. Talantov Dimitri, Baden Jonathan, Jatkoe Tim, Hahn Kristina, Yu Jack, Rajpurohit Yashoda, Jiang Yiqiu, Choi Chang, Ross Jeffrey S., Atkins David, Wang Yixin, Mazumder Abhijit, A Quantitative Reverse Transcriptase-Polymerase Chain Reaction Assay to Identify Metastatic Carcinoma Tissue of Origin, 10.2353/jmoldx.2006.050136
  21. Barrett T, Suzek TO, Troup DB, Wilhite SE, Ngau WC, Ledoux P, et al: NCBI GEO: mining millions of expression profiles--database and tools. Nucleic Acids Res. 2005, D562-6. 33 Database
  22. Wilson C. L., Miller C. J., Simpleaffy: a BioConductor package for Affymetrix Quality Control and data analysis, 10.1093/bioinformatics/bti605
  23. Dai M., Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data, 10.1093/nar/gni179
  24. Subramanian A., Tamayo P., Mootha V. K., Mukherjee S., Ebert B. L., Gillette M. A., Paulovich A., Pomeroy S. L., Golub T. R., Lander E. S., Mesirov J. P., Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles, 10.1073/pnas.0506580102
  25. Dennis Glynn, Sherman Brad T, Hosack Douglas A, Yang Jun, Gao Wei, Lane H Clifford, Lempicki Richard A, 10.1186/gb-2003-4-5-p3
  26. Huang Da, Sherman Brad T, Tan Qina, Collins Jack R, Alvord W Gregory, Roayaei Jean, Stephens Robert, Baseler Michael W, Lane H Clifford, Lempicki Richard A, The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists, 10.1186/gb-2007-8-9-r183
  27. Nelson P. S., Clegg N., Arnold H., Ferguson C., Bonham M., White J., Hood L., Lin B., The program of androgen-responsive genes in neoplastic prostate epithelium, 10.1073/pnas.182376299
  28. Cuatrecasas Miriam, Catasus Luis, Palacios José, Prat Jaime, Transitional Cell Tumors of the Ovary : A Comparative Clinicopathologic, Immunohistochemical, and Molecular Genetic Analysis of Brenner Tumors and Transitional Cell Carcinomas, 10.1097/pas.0b013e318188b84c
  29. Eichhorn John H, Young Robert H, Transitional Cell Carcinoma of the Ovary : A Morphologic Study of 100 Cases With Emphasis on Differential Diagnosis, 10.1097/00000478-200404000-00004
  30. Tickoo Satish K., Gopalan Anuradha, Pathologic Features of Renal Cortical Tumors, 10.1016/j.ucl.2008.07.001
  31. Ayala G, Tuxhorn JA, Wheeler TM, Frolov A, Scardino PT, Ohori M, et al: Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clin Cancer Res. 2003, 9: 4792-4801.
  32. Brugarolas James, Renal-Cell Carcinoma — Molecular Pathways and Therapies, 10.1056/nejme068263
  33. Staller Peter, Sulitkova Jitka, Lisztwan Joanna, Moch Holger, Oakeley Edward J., Krek Wilhelm, Chemokine receptor CXCR4 downregulated by von Hippel–Lindau tumour suppressor pVHL, 10.1038/nature01874
  34. Liu Xiong, Yu Xueping, Zack Donald J, Zhu Heng, Qian Jiang, TiGER: a database for tissue-specific gene expression and regulation, 10.1186/1471-2105-9-271
  35. Yoder Brian J., Wilkinson Edward J., Massoll Nicole A., Molecular and Morphologic Distinctions between Infiltrating Ductal and Lobular Carcinoma of the Breast, 10.1111/j.1524-4741.2007.00393.x
  36. Lacroix M, Stable 'portrait' of breast tumors during progression: data from biology, pathology and genetics, 10.1677/erc.1.00758
  37. Weigelt B, Horlings HM, Kreike B, Hayes MM, Hauptmann M, Wessels LFA, de Jong D, Van de Vijver MJ, Veer LJ Van't, Peterse JL, Refinement of breast cancer classification by molecular characterization of histological special types, 10.1002/path.2407
  38. Sotiriou Christos, Pusztai Lajos, Gene-Expression Signatures in Breast Cancer, 10.1056/nejmra0801289
  39. Rakha E. A., Elsheikh S. E., Aleskandarany M. A., Habashi H. O., Green A. R., Powe D. G., El-Sayed M. E., Benhasouna A., Brunet J.-S., Akslen L. A., Evans A. J., Blamey R., Reis-Filho J. S., Foulkes W. D., Ellis I. O., Triple-Negative Breast Cancer: Distinguishing between Basal and Nonbasal Subtypes, 10.1158/1078-0432.ccr-08-2132
  40. Sotiriou Christos, Wirapati Pratyaksha, Loi Sherene, Harris Adrian, Fox Steve, Smeds Johanna, Nordgren Hans, Farmer Pierre, Praz Viviane, Haibe-Kains Benjamin, Desmedt Christine, Larsimont Denis, Cardoso Fatima, Peterse Hans, Nuyten Dimitry, Buyse Marc, Van de Vijver Marc J., Bergh Jonas, Piccart Martine, Delorenzi Mauro, Gene Expression Profiling in Breast Cancer: Understanding the Molecular Basis of Histologic Grade To Improve Prognosis, 10.1093/jnci/djj052
  41. Ivshina A. V., George J., Senko O., Mow B., Putti T. C., Smeds J., Lindahl T., Pawitan Y., Hall P., Nordgren H., Wong J. E.L., Liu E. T., Bergh J., Kuznetsov V. A., Miller L. D., Genetic Reclassification of Histologic Grade Delineates New Clinical Subtypes of Breast Cancer, 10.1158/0008-5472.can-05-4414
  42. Ignatiadis M., Sotiriou C., Understanding the Molecular Basis of Histologic Grade, 10.1159/000123848
  43. Yu Jack X, Sieuwerts Anieta M, Zhang Yi, Martens John WM, Smid Marcel, Klijn Jan GM, Wang Yixin, Foekens John A, Pathway analysis of gene signatures predicting metastasis of node-negative primary breast cancer, 10.1186/1471-2407-7-182
  44. Hu Zhiyuan, Fan Cheng, Oh Daniel S, Marron JS, He Xiaping, Qaqish Bahjat F, Livasy Chad, Carey Lisa A, Reynolds Evangeline, Dressler Lynn, Nobel Andrew, Parker Joel, Ewend Matthew G, Sawyer Lynda R, Wu Junyuan, Liu Yudong, Nanda Rita, Tretiakova Maria, Orrico Alejandra, Dreher Donna, Palazzo Juan P, Perreard Laurent, Nelson Edward, Mone Mary, Hansen Heidi, Mullins Michael, Quackenbush John F, Ellis Matthew J, Olopade Olufunmilayo I, Bernard Philip S, Perou Charles M, 10.1186/1471-2164-7-96
  45. Sloan Erica K., Ciocca Daniel R., Pouliot Normand, Natoli Anthony, Restall Christina, Henderson Michael A., Fanelli Mariel A., Cuello-Carrión Fernando D., Gago Francisco E., Anderson Robin L., Stromal Cell Expression of Caveolin-1 Predicts Outcome in Breast Cancer, 10.2353/ajpath.2009.080924
  46. Witkiewicz Agnieszka K., Dasgupta Abhijit, Sotgia Federica, Mercier Isabelle, Pestell Richard G., Sabel Michael, Kleer Celina G., Brody Jonathan R., Lisanti Michael P., An Absence of Stromal Caveolin-1 Expression Predicts Early Tumor Recurrence and Poor Clinical Outcome in Human Breast Cancers, 10.2353/ajpath.2009.080873
  47. Lukes L., Crawford N. P.S., Walker R., Hunter K. W., The Origins of Breast Cancer Prognostic Gene Expression Profiles, 10.1158/0008-5472.can-08-3520
  48. Witkiewicz Agnieszka K., Dasgupta Abhijit, Nguyen Katherine, Liu Chengbao, Kovatich Albert J., Schwartz Gordon F., Pestell Richard G., Sotgia Federica, Rui Hallgeir, Lisanti Michael P., Stromal caveolin-1 levels predict early DCIS progression to invasive breast cancer, 10.4161/cbt.8.11.8874
  49. Ma Xiao-Jun, Dahiya Sonika, Richardson Elizabeth, Erlander Mark, Sgroi Dennis C, Gene expression profiling of the tumor microenvironment during breast cancer progression, 10.1186/bcr2222
  50. Pavlakis Kitty, Messini Irene, Vrekoussis Thomas, Yiannou Petros, Keramopoullos Dimitrios, Louvrou Niki, Liakakos Theodoros, Stathopoulos Efstathios N, The assessment of angiogenesis and fibroblastic stromagenesis in hyperplastic and pre-invasive breast lesions, 10.1186/1471-2407-8-88
  51. Troup S, Njue C, Kliewer EV, Parisien M, Roskelley C, Chakravarti S, et al: Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer. Clin Cancer Res. 2003, 9: 207-214.
  52. Wennmalm Kristian, Östman Arne, Bergh Jonas, Stromal signature identifies basal breast cancers, 10.1038/nm0309-237
  53. Schedin Pepper, Borges Virginia, Breaking down barriers: the importance of the stromal microenvironment in acquiring invasiveness in young women's breast cancer, 10.1186/bcr2235
  54. Finak Greg, Bertos Nicholas, Pepin Francois, Sadekova Svetlana, Souleimanova Margarita, Zhao Hong, Chen Haiying, Omeroglu Gulbeyaz, Meterissian Sarkis, Omeroglu Atilla, Hallett Michael, Park Morag, Stromal gene expression predicts clinical outcome in breast cancer, 10.1038/nm1764
  55. Oien Karin A., Pathologic Evaluation of Unknown Primary Cancer, 10.1053/j.seminoncol.2008.10.009
  56. Laberke H.-G., Klingebiel Th., Quack G., A Contribution to the Morphology and Pathogenesis of Thyroid-Like Lesions in the Kidney, 10.1016/s0344-0338(83)80018-1
  57. Amin Mahul B., Gupta Ruta, Ondrej Hes, McKenney Jesse K., Michal Michal, Young Andrew N., Paner Gladell P., Junker Kerstin, Epstein Jonathan I., Primary Thyroid-like Follicular Carcinoma of the Kidney : Report of 6 Cases of a Histologically Distinctive Adult Renal Epithelial Neoplasm, 10.1097/pas.0b013e31818cb8f5
  58. Jung Soo Jin, Chung Jae Il, Park Sun Hwa, Ayala Alberto G., Ro Jae Y., Thyroid Follicular Carcinoma-like Tumor of Kidney : A Case Report With Morphologic, Immunohistochemical, and Genetic Analysis, 10.1097/01.pas.0000194745.10670.dd
  59. Bast Robert C., Hennessy Bryan, Mills Gordon B., The biology of ovarian cancer: new opportunities for translation, 10.1038/nrc2644
  60. Seidman JD, Russell P, Kurman RJ: Surface epithelial tumors of the ovary. Blaustein's pathology of the female genital tract. Edited by: Ancell Blaustein, Robert J Kurman. 2002, New York: Springer-Verlag, 791-904.
  61. Kang Hakjung, O'Connell Jessica B., Maggard Melinda A., Sack Jonathan, Ko Clifford Y., A 10-Year Outcomes Evaluation of Mucinous and Signet-Ring Cell Carcinoma of the Colon and Rectum : , 10.1007/s10350-004-0932-1
  62. Naora Honami, Montell Denise J., Ovarian Cancer Metastasis: Integrating insights from disparate model organisms, 10.1038/nrc1611
  63. SMORENBURG S, $alpha;2-Macroglobulin is mainly produced by cancer cells and not by hepatocytes in rats with colon carcinoma metastases in liver, 10.1053/jhep.1996.v23.pm0008617438
  64. Sukata Tokuo, Uwagawa Satoshi, Ozaki Keisuke, Sumida Kayo, Kikuchi Kaoru, Kushida Masahiko, Saito Koichi, Morimura Keiichirou, Oeda Kenji, Okuno Yasuyoshi, Mikami Nobuyoshi, Fukushima Shoji, α2-Macroglobulin: A Novel Cytochemical Marker Characterizing Preneoplastic and Neoplastic Rat Liver Lesions Negative for Hitherto Established Cytochemical Markers, 10.1016/s0002-9440(10)63406-2
  65. Matouk Imad J., Abbasi Ibrahim, Hochberg Abraham, Galun Eithan, Dweik Hassan, Akkawi Mutaz, Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis : , 10.1097/meg.0b013e328306a3a2
  66. Khambata-Ford Shirin, Garrett Christopher R., Meropol Neal J., Basik Mark, Harbison Christopher T., Wu Shujian, Wong Tai W., Huang Xin, Takimoto Chris H., Godwin Andrew K., Tan Benjamin R., Krishnamurthi Smitha S., Burris Howard A., Poplin Elizabeth A., Hidalgo Manuel, Baselga Jose, Clark Edwin A., Mauro David J., Expression of Epiregulin and Amphiregulin and K-ras Mutation Status Predict Disease Control in Metastatic Colorectal Cancer Patients Treated With Cetuximab, 10.1200/jco.2006.10.5437
  67. Pantaleo M A, Astolfi A, Nannini M, Paterini P, Piazzi G, Ercolani G, Brandi G, Martinelli G, Pession A, Pinna A D, Biasco G, Gene expression profiling of liver metastases from colorectal cancer as potential basis for treatment choice, 10.1038/sj.bjc.6604681
  68. Ki Dong Hyuk, Jeung Hei-Cheul, Park Chan Hee, Kang Seung Hee, Lee Gui Youn, Lee Won Suk, Kim Nam Kyu, Chung Hyun Chul, Rha Sun Young, Whole genome analysis for liver metastasis gene signatures in colorectal cancer, 10.1002/ijc.22975
  69. Ramasamy Adaikalavan, Mondry Adrian, Holmes Chris C, Altman Douglas G, Key Issues in Conducting a Meta-Analysis of Gene Expression Microarray Datasets, 10.1371/journal.pmed.0050184
  70. Snyder Michael, Weissman Sherman, Gerstein Mark, Personal phenotypes to go with personal genomes, 10.1038/msb.2009.32
  71. Belmont John, McGuire Amy L, The futility of genomic counseling: essential role of electronic health records, 10.1186/gm48
  72. Chin Koei, DeVries Sandy, Fridlyand Jane, Spellman Paul T., Roydasgupta Ritu, Kuo Wen-Lin, Lapuk Anna, Neve Richard M., Qian Zuwei, Ryder Tom, Chen Fanqing, Feiler Heidi, Tokuyasu Taku, Kingsley Chris, Dairkee Shanaz, Meng Zhenhang, Chew Karen, Pinkel Daniel, Jain Ajay, Ljung Britt Marie, Esserman Laura, Albertson Donna G., Waldman Frederic M., Gray Joe W., Genomic and transcriptional aberrations linked to breast cancer pathophysiologies, 10.1016/j.ccr.2006.10.009
  73. Miller L. D., Smeds J., George J., Vega V. B., Vergara L., Ploner A., Pawitan Y., Hall P., Klaar S., Liu E. T., Bergh J., From The Cover: An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival, 10.1073/pnas.0506230102
  74. Pittman J., Huang E., Dressman H., Horng C.-F., Cheng S. H., Tsou M.-H., Chen C.-M., Bild A., Iversen E. S., Huang A. T., Nevins J. R., West M., Integrated modeling of clinical and gene expression information for personalized prediction of disease outcomes, 10.1073/pnas.0401736101
Bibliographic reference Gevaert, Olivier ; Daemen, Anneleen ; De Moor, Bart ; Libbrecht, Louis. A taxonomy of epithelial human cancer and their metastases. In: BMC Medical Genomics, Vol. 2, no.1, p. 69 [1-16] (2009)
Permanent URL http://hdl.handle.net/2078/187446