Gene expression profiling to dissect the complexity of cancer biology: Pitfalls and promise

Seminars in Cancer Biology

Volumn 22, Issue 3, 2012, Pages 250-260

  Raspe, Eric ^a,b   Decraene, Charles ^c,d   Berx, Geert ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c INSTITUT CURIE   (France)

^d CNRS   (France)

Author keywords

Cancer stem cells; Gene expression profiles; Metastasis; Microarray

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER B5; CD133 ANTIGEN; CD24 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; HERMES ANTIGEN; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

CANCER RECURRENCE; CANCER RELAPSE; CANCER STEM CELL; CIRCULATING TUMOR CELL; DATA ANALYSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENOMICS; HIGH THROUGHPUT SCREENING; HUMAN; ONCOLOGY; OUTCOME ASSESSMENT; PREDICTIVE VALUE; REVIEW;

GENE EXPRESSION PROFILING; HUMANS; INDIVIDUALIZED MEDICINE; NEOPLASMS; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 84861182680     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.02.011     Document Type: Review

References (184)

1. Ferlay J., Shin H.R., Bray F., Forman D., Mathers C., Parkin D.M. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010, 127:2893-2917.
2. Jemal A., Siegel R., Xu J., Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010, 60:277300.
3. Monzon F.A., Lyons-Weiler M., Buturovic L.J., Rigl C.T., Henner W.D., Sciulli C., et al. Multicenter validation of a 1,550-gene expression profile for identification of tumor tissue of origin. J Clin Oncol 2009, 27:2503-2508.
4. Ramaswamy S., Tamayo P., Rifkin R., Mukherjee S., Yeang C.H., Angelo M., et al. Multiclass cancer diagnosis using tumor gene expression signatures. Proc Natl Acad Sci U S A 2001, 98:15149-15154.
5. Su A.I., Welsh J.B., Sapinoso L.M., Kern S.G., Dimitrov P., Lapp H., et al. Molecular classification of human carcinomas by use of gene expression signatures. Cancer Res 2001, 61:7388-7393.
6. van Laar R.K., Ma X.J., de Jong D., Wehkamp D., Floore A.N., Warmoes M.O., et al. Implementation of a novel microarray-based diagnostic test for cancer of unknown primary. Int J Cancer 2009, 125:1390-1397.
7. Fidler I.J., Hart I.R. Biological diversity in metastatic neoplasms: origins and implications. Science 1982, 217:998-1003.
8. Heppner G.H. Tumor heterogeneity. Cancer Res 1984, 44:2259-2265.
9. Marusyk A., Polyak K. Tumor heterogeneity: causes and consequences. Biochim Biophys Acta 2011, 1805:105-117.
10. Perou C.M., Sorlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
11. Sorlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001, 98:10869-10874.
12. Sorlie T., Wang Y., Xiao C., Johnsen H., Naume B., Samaha R.R., et al. Distinct molecular mechanisms underlying clinically relevant subtypes of breast cancer: gene expression analyses across three different platforms. BMC Genomics 2006, 7:127.
13. Slamon D.J., Clark G.M., Wong S.G., Levin W.J., Ullrich A., McGuire W.L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235:177-182.
14. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
15. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
16. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100:3983-3988.
17. Dalerba P., Cho R.W., Clarke M.F. Cancer stem cells: models and concepts. Annu Rev Med 2007, 58:267-284.
18. Maenhaut C., Dumont J.E., Roger P.P., van Staveren W.C. Cancer stem cells: a reality, a myth, a fuzzy concept or a misnomer? An analysis. Carcinogenesis 2010, 31:149-158.
19. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8:755-768.
20. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5:275-284.
21. Frank N.Y., Schatton T., Frank M.H. The therapeutic promise of the cancer stem cell concept. J Clin Invest 2010, 120:41-50.
22. Li X., Lewis M.T., Huang J., Gutierrez C., Osborne C.K., Wu M.F., et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679.
23. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
24. Baumann M., Krause M., Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 2008, 8:545-554.
25. Diehn M., Cho R.W., Clarke M.F. Therapeutic implications of the cancer stem cell hypothesis. Semin Radiat Oncol 2009, 19:78-86.
26. Phillips T.M., McBride W.H., Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 98:1777-1785.
27. Woodward W.A., Chen M.S., Behbod F., Alfaro M.P., Buchholz T.A., Rosen J.M. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci U S A 2007, 104:618-623.
28. Barry W.T., Kernagis D.N., Dressman H.K., Griffis R.J., Hunter J.D., Olson J.A., et al. Intratumor heterogeneity and precision of microarray-based predictors of breast cancer biology and clinical outcome. J Clin Oncol 2010, 28:2198-2206.
29. Brabletz T., Jung A., Spaderna S., Hlubek F., Kirchner T. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 2005, 5:744-749.
30. Roesch A., Vogt T., Stolz W., Dugas M., Landthaler M., Becker B. Discrimination between gene expression patterns in the invasive margin and the tumour core of malignant melanomas. Melanoma Res 2003, 13:503-509.
31. Schuetz C.S., Bonin M., Clare S.E., Nieselt K., Sotlar K., Walter M., et al. Progression-specific genes identified by expression profiling of matched ductal carcinomas in situ and invasive breast tumors, combining laser capture microdissection and oligonucleotide microarray analysis. Cancer Res 2006, 66:5278-5286.
32. Chi J.T., Wang Z., Nuyten D.S., Rodriguez E.H., Schaner M.E., Salim A., et al. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med 2006, 3:e47.
33. Elvidge G.P., Glenny L., Appelhoff R.J., Ratcliffe P.J., Ragoussis J., Gleadle J.M. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 2006, 281:15215-15226.
34. Greijer A.E., van der Groep P., Kemming D., Shvarts A., Semenza G.L., Meijer G.A., et al. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol 2005, 206:291-304.
35. Hu C.J., Wang L.Y., Chodosh L.A., Keith B., Simon M.C. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 2003, 23:9361-9374.
36. Scandurro A.B., Weldon C.W., Figueroa Y.G., Alam J., Beckman B.S. Gene microarray analysis reveals a novel hypoxia signal transduction pathway in human hepatocellular carcinoma cells. Int J Oncol 2001, 19:129-135.
37. Sowter H.M., Raval R.R., Moore J.W., Ratcliffe P.J., Harris A.L. Predominant role of hypoxia-inducible transcription factor (Hif)-1alpha versus Hif-2alpha in regulation of the transcriptional response to hypoxia. Cancer Res 2003, 63:6130-6134.
38. Wang V., Davis D.A., Haque M., Huang L.E., Yarchoan R. Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res 2005, 65:3299-3306.
39. Jungermann K., Kietzmann T. Zonation of parenchymal and nonparenchymal metabolism in liver. Annu Rev Nutr 1996, 16:179-203.
40. Wilson W.R., Hay M.P. Targeting hypoxia in cancer therapy. Nat Rev Cancer 2011, 11:393-410.
41. Simon M.C., Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 2008, 9:285-296.
42. Schena M., Shalon D., Davis R.W., Brown P.O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 1995, 270:467-470.
43. Schena M., Shalon D., Heller R., Chai A., Brown P.O., Davis R.W. Parallel human genome analysis: microarray-based expression monitoring of 1000 genes. Proc Natl Acad Sci U S A 1996, 93:10614-10619.
44. DeRisi J., Penland L., Brown P.O., Bittner M.L., Meltzer P.S., Ray M., et al. Use of a cDNA microarray to analyse gene expression patterns in human cancer. Nat Genet 1996, 14:457-460.
45. Lee J.C., Stiles D., Lu J., Cam M.C. A detailed transcript-level probe annotation reveals alternative splicing based microarray platform differences. BMC Genomics 2007, 8:284.
46. Meyniel J.P., Cottu P.H., Decraene C., Stern M.H., Couturier J., Lebigot I., et al. A genomic and transcriptomic approach for a differential diagnosis between primary and secondary ovarian carcinomas in patients with a previous history of breast cancer. BMC Cancer 2010, 10:222.
47. Creighton C.J., Li X., Landis M., Dixon J.M., Neumeister V.M., Sjolund A., et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci U S A 2009, 106:13820-13825.
48. Hennessy B.T., Gonzalez-Angulo A.M., Stemke-Hale K., Gilcrease M.Z., Krishnamurthy S., Lee J.S., et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res 2009, 69:4116-4124.
49. Prat A., Parker J.S., Karginova O., Fan C., Livasy C., Herschkowitz J.I., et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010, 12:R68.
50. Charafe-Jauffret E., Ginestier C., Monville F., Finetti P., Adelaide J., Cervera N., et al. Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 2006, 25:2273-2284.
51. Hollestelle A., Nagel J.H., Smid M., Lam S., Elstrodt F., Wasielewski M., et al. Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res Treat 2010, 121:53-64.
52. Neve R.M., Chin K., Fridlyand J., Yeh J., Baehner F.L., Fevr T., et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515-527.
53. Stratford J.K., Bentrem D.J., Anderson J.M., Fan C., Volmar K.A., Marron J.S., et al. A six-gene signature predicts survival of patients with localized pancreatic ductal adenocarcinoma. Plos Med 2010, 7:e1000307.
54. Aldred M.A., Huang Y., Liyanarachchi S., Pellegata N.S., Gimm O., Jhiang S., et al. Papillary and follicular thyroid carcinomas show distinctly different microarray expression profiles and can be distinguished by a minimum of five genes. J Clin Oncol 2004, 22:3531-3539.
55. Giordano T.J., Kuick R., Thomas D.G., Misek D.E., Vinco M., Sanders D., et al. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene 2005, 24:6646-6656.
56. Dhanasekaran S.M., Barrette T.R., Ghosh D., Shah R., Varambally S., Kurachi K., et al. Delineation of prognostic biomarkers in prostate cancer. Nature 2001, 412:822-826.
57. Lapointe J., Li C., Higgins J.P., van de Rijn M., Bair E., Montgomery K., et al. Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci U S A 2004, 101:811-816.
58. Singh D., Febbo P.G., Ross K., Jackson D.G., Manola J., Ladd C., et al. Gene expression correlates of clinical prostate cancer behavior. Cancer Cell 2002, 1:203-209.
59. Beer D.G., Kardia S.L., Huang C.C., Giordano T.J., Levin A.M., Misek D.E., et al. Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med 2002, 8:816-824.
60. Bhattacharjee A., Richards W.G., Staunton J., Li C., Monti S., Vasa P., et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 2001, 98:13790-13795.
61. Wang T., Hopkins D., Schmidt C., Silva S., Houghton R., Takita H., et al. Identification of genes differentially over-expressed in lung squamous cell carcinoma using combination of cDNA subtraction and microarray analysis. Oncogene 2000, 19:1519-1528.
62. Chen X., Cheung S.T., So S., Fan S.T., Barry C., Higgins J., et al. Gene expression patterns in human liver cancers. Mol Biol Cell 2002, 13:1929-1939.
63. Chen X., Leung S.Y., Yuen S.T., Chu K.M., Ji J., Li R., et al. Variation in gene expression patterns in human gastric cancers. Mol Biol Cell 2003, 14:3208-3215.
64. Takahashi M., Rhodes D.R., Furge K.A., Kanayama H., Kagawa S., Haab B.B., et al. Gene expression profiling of clear cell renal cell carcinoma: gene identification and prognostic classification. Proc Natl Acad Sci U S A 2001, 98:9754-9759.
65. Gibson P., Tong Y., Robinson G., Thompson M.C., Currle D.S., Eden C., et al. Subtypes of medulloblastoma have distinct developmental origins. Nature 2010, 468:1095-1099.
66. Rickman D.S., Bobek M.P., Misek D.E., Kuick R., Blaivas M., Kurnit D.M., et al. Distinctive molecular profiles of high-grade and low-grade gliomas based on oligonucleotide microarray analysis. Cancer Res 2001, 61:6885-6891.
67. Bittner M., Meltzer P., Chen Y., Jiang Y., Seftor E., Hendrix M., et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000, 406:536-540.
68. Network T.C.G.A.R. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615.
69. Welsh J.B., Zarrinkar P.P., Sapinoso L.M., Kern S.G., Behling C.A., Monk B.J., et al. Analysis of gene expression profiles in normal and neoplastic ovarian tissue samples identifies candidate molecular markers of epithelial ovarian cancer. Proc Natl Acad Sci U S A 2001, 98:1176-1181.
70. Belbin T.J., Singh B., Barber I., Socci N., Wenig B., Smith R., et al. Molecular classification of head and neck squamous cell carcinoma using cDNA microarrays. Cancer Res 2002, 62:1184-1190.
71. Kuriakose M.A., Chen W.T., He Z.M., Sikora A.G., Zhang P., Zhang Z.Y., et al. Selection and validation of differentially expressed genes in head and neck cancer. Cell Mol Life Sci 2004, 61:1372-1383.
72. Alon U., Barkai N., Notterman D.A., Gish K., Ybarra S., Mack D., et al. Broad patterns of gene expression revealed by clustering analysis of tumor and normal colon tissues probed by oligonucleotide arrays. Proc Natl Acad Sci U S A 1999, 96:6745-6750.
73. Alizadeh A.A., Eisen M.B., Davis R.E., Ma C., Lossos I.S., Rosenwald A., et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000, 403:503-511.
74. Golub T.R., Slonim D.K., Tamayo P., Huard C., Gaasenbeek M., Mesirov J.P., et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 1999, 286:531-537.
75. van't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536.
76. Sotiriou C., Pusztai L. Gene-expression signatures in breast cancer. N Engl J Med 2009, 360:790-800.
77. Hannemann J., Oosterkamp H.M., Bosch C.A., Velds A., Wessels L.F., Loo C., et al. Changes in gene expression associated with response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2005, 23:3331-3342.
78. Holleman A., Cheok M.H., den Boer M.L., Yang W., Veerman A.J., Kazemier K.M., et al. Gene-expression patterns in drug-resistant acute lymphoblastic leukemia cells and response to treatment. N Engl J Med 2004, 351:533-542.
79. Lugthart S., Cheok M.H., den Boer M.L., Yang W., Holleman A., Cheng C., et al. Identification of genes associated with chemotherapy crossresistance and treatment response in childhood acute lymphoblastic leukemia. Cancer Cell 2005, 7:375-386.
80. Jansen M.P., Foekens J.A., van Staveren I.L., Dirkzwager-Kiel M.M., Ritstier K., Look M.P., et al. Molecular classification of tamoxifen-resistant breast carcinomas by gene expression profiling. J Clin Oncol 2005, 23:732-740.
81. Ayers M., Symmans W.F., Stec J., Damokosh A.I., Clark E., Hess K., et al. Gene expression profiles predict complete pathologic response to neoadjuvant paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide chemotherapy in breast cancer. J Clin Oncol 2004, 22:2284-2293.
82. Chang J.C., Wooten E.C., Tsimelzon A., Hilsenbeck S.G., Gutierrez M.C., Elledge R., et al. Gene expression profiling for the prediction of therapeutic response to docetaxel in patients with breast cancer. Lancet 2003, 362:362-369.
83. Dressman H.K., Hans C., Bild A., Olson J.A., Rosen E., Marcom P.K., et al. Gene expression profiles of multiple breast cancer phenotypes and response to neoadjuvant chemotherapy. Clin Cancer Res 2006, 12:819-826.
84. Hatzis C., Pusztai L., Valero V., Booser D.J., Esserman L., Lluch A., et al. A genomic predictor of response and survival following taxane-anthracycline chemotherapy for invasive breast cancer. J Am Med Assoc 2011, 305:1873-1881.
85. Hess K.R., Anderson K., Symmans W.F., Valero V., Ibrahim N., Mejia J.A., et al. Pharmacogenomic predictor of sensitivity to preoperative chemotherapy with paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide in breast cancer. J Clin Oncol 2006, 24:4236-4244.
86. Specht K., Harbeck N., Smida J., Annecke K., Reich U., Naehrig J., et al. Expression profiling identifies genes that predict recurrence of breast cancer after adjuvant CMF-based chemotherapy. Breast Cancer Res Treat 2009, 118:45-56.
87. Tabchy A., Valero V., Vidaurre T., Lluch A., Gomez H., Martin M., et al. Evaluation of a 30-gene paclitaxel, fluorouracil, doxorubicin, and cyclophosphamide chemotherapy response predictor in a multicenter randomized trial in breast cancer. Clin Cancer Res 2010, 16:5351-5361.
88. Chanrion M., Negre V., Fontaine H., Salvetat N., Bibeau F., Mac Grogan G., et al. A gene expression signature that can predict the recurrence of tamoxifen-treated primary breast cancer. Clin Cancer Res 2008, 14:1744-1752.
89. Loi S., Haibe-Kains B., Desmedt C., Wirapati P., Lallemand F., Tutt A.M., et al. Predicting prognosis using molecular profiling in estrogen receptor-positive breast cancer treated with tamoxifen. BMC Genomics 2008, 9:239.
90. Loi S., Haibe-Kains B., Majjaj S., Lallemand F., Durbecq V., Larsimont D., et al. PIK3CA mutations associated with gene signature of low mTORC1 signaling and better outcomes in estrogen receptor-positive breast cancer. Proc Natl Acad Sci U S A 2010, 107:10208-10213.
91. Vendrell J.A., Robertson K.E., Ravel P., Bray S.E., Bajard A., Purdie C.A., et al. A candidate molecular signature associated with tamoxifen failure in primary breast cancer. Breast Cancer Res 2008, 10:R88.
92. Huang L., Zhao S., Frasor J.M., Dai Y. An integrated bioinformatics approach identifies elevated cyclin E2 expression and E2F activity as distinct features of tamoxifen resistant breast tumors. PLoS One 2011, 6:e22274.
93. Shoemaker R.H. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer 2006, 6:813-823.
94. Liu H., D'Andrade P., Fulmer-Smentek S., Lorenzi P., Kohn K.W., Weinstein J.N., et al. mRNA and microRNA expression profiles of the NCI-60 integrated with drug activities. Mol Cancer Ther 2010, 9:1080-1091.
95. Ross D.T., Scherf U., Eisen M.B., Perou C.M., Rees C., Spellman P., et al. Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 2000, 24:227-235.
96. Scherf U., Ross D.T., Waltham M., Smith L.H., Lee J.K., Tanabe L., et al. A gene expression database for the molecular pharmacology of cancer. Nat Genet 2000, 24:236-244.
97. Shankavaram U.T., Reinhold W.C., Nishizuka S., Major S., Morita D., Chary K.K., et al. Transcript and protein expression profiles of the NCI-60 cancer cell panel: an integromic microarray study. Mol Cancer Ther 2007, 6:820-832.
98. Staunton J.E., Slonim D.K., Coller H.A., Tamayo P., Angelo M.J., Park J., et al. Chemosensitivity prediction by transcriptional profiling. Proc Natl Acad Sci U S A 2001, 98:10787-10792.
99. Coser K.R., Wittner B.S., Rosenthal N.F., Collins S.C., Melas A., Smith S.L., et al. Antiestrogen-resistant subclones of MCF-7 human breast cancer cells are derived from a common monoclonal drug-resistant progenitor. Proc Natl Acad Sci U S A 2009, 106:14536-14541.
100. Fan M., Yan P.S., Hartman-Frey C., Chen L., Paik H., Oyer S.L., et al. Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant. Cancer Res 2006, 66:11954-11966.
101. Gomez B.P., Riggins R.B., Shajahan A.N., Klimach U., Wang A., Crawford A.C., et al. Human X-box binding protein-1 confers both estrogen independence and antiestrogen resistance in breast cancer cell lines. FASEB J 2007, 21:4013-4027.
102. Watts G.S., Futscher B.W., Isett R., Gleason-Guzman M., Kunkel M.W., Salmon S.E. cDNA microarray analysis of multidrug resistance: doxorubicin selection produces multiple defects in apoptosis signaling pathways. J Pharmacol Exp Ther 2001, 299:434-441.
103. Lee J.K., Havaleshko D.M., Cho H., Weinstein J.N., Kaldjian E.P., Karpovich J., et al. A strategy for predicting the chemosensitivity of human cancers and its application to drug discovery. Proc Natl Acad Sci U S A 2007, 104:13086-13091.
104. Potti A., Dressman H.K., Bild A., Riedel R.F., Chan G., Sayer R., et al. Genomic signatures to guide the use of chemotherapeutics. Nat Med 2006, 12:1294-1300.
105. Borst P., Wessels L. Do predictive signatures really predict response to cancer chemotherapy. Cell Cycle 2010, 9:4836-4840.
106. Coombes K.R., Wang J., Baggerly K.A. Microarrays: retracing steps. Nat Med 2007, 13:1276-1277. author reply 7-8.
107. Liedtke C., Wang J., Tordai A., Symmans W.F., Hortobagyi G.N., Kiesel L., et al. Clinical evaluation of chemotherapy response predictors developed from breast cancer cell lines. Breast Cancer Res Treat 2010, 121:301-309.
108. Weigelt B., Pusztai L., Ashworth A., Reis-Filho J.S. Challenges translating breast cancer gene signatures into the clinic. Nat Rev Clin Oncol 2011.
109. Liu R., Wang X., Chen G.Y., Dalerba P., Gurney A., Hoey T., et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med 2007, 356:217-226.
110. Imbeaud S., Auffray C. 'The 39 steps' in gene expression profiling: critical issues and proposed best practices for microarray experiments. Drug Discov Today 2005, 10:1175-1182.
111. Clement-Ziza M., Gentien D., Lyonnet S., Thiery J.P., Besmond C., Decraene C. Evaluation of methods for amplification of picogram amounts of total RNA for whole genome expression profiling. BMC Genomics 2009, 10:246.
112. Bertucci F., Nasser V., Granjeaud S., Eisinger F., Adelaide J., Tagett R., et al. Gene expression profiles of poor-prognosis primary breast cancer correlate with survival. Hum Mol Genet 2002, 11:863-872.
113. Huang E., Cheng S.H., Dressman H., Pittman J., Tsou M.H., Horng C.F., et al. Gene expression predictors of breast cancer outcomes. Lancet 2003, 361:1590-1596.
114. Korkola J.E., Blaveri E., DeVries S., Moore D.H., 2nd Hwang E.S., Chen Y.Y., et al. Identification of a robust gene signature that predicts breast cancer outcome in independent data sets. BMC Cancer 2007, 7:61.
115. Sotiriou C., Neo S.Y., McShane L.M., Korn E.L., Long P.M., Jazaeri A., et al. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A 2003, 100:10393-10398.
116. Wang Y., Klijn J.G., Zhang Y., Sieuwerts A.M., Look M.P., Yang F., et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005, 365:671-679.
117. Abba M.C., Lacunza E., Butti M., Aldaz C.M. Breast cancer biomarker discovery in the functional genomic age: a systematic review of 42 gene expression signatures. Biomark Insights 2010, 5:103-118.
118. Ein-Dor L., Zuk O., Domany E. Thousands of samples are needed to generate a robust gene list for predicting outcome in cancer. Proc Natl Acad Sci U S A 2006, 103:5923-5928.
119. Venet D., Dumont J.E., Detours V. Most random gene expression signatures are significantly associated with breast cancer outcome. PloS Comput Biol 2011, 2011.
120. Mosley J.D., Keri R.A. Cell cycle correlated genes dictate the prognostic power of breast cancer gene lists. BMC Med Genomics 2008, 1:11.
121. Desmedt C., Sotiriou C. Proliferation: the most prominent predictor of clinical outcome in breast cancer. Cell Cycle 2006, 5:2198-2202.
122. Haibe-Kains B., Desmedt C., Sotiriou C., Bontempi G. A comparative study of survival models for breast cancer prognostication based on microarray data: does a single gene beat them all. Bioinformatics 2008, 24:2200-2208.
123. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 2011, 17:320-329.
124. Bissell M.J., Radisky D. Putting tumours in context. Nat Rev Cancer 2001, 1:46-54.
125. Finak G., Bertos N., Pepin F., Sadekova S., Souleimanova M., Zhao H., et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008, 14:518-527.
126. Tebbit C.L., Zhai J., Untch B.R., Ellis M.J., Dressman H.K., Bentley R.C., et al. Novel tumor sampling strategies to enable microarray gene expression signatures in breast cancer: a study to determine feasibility and reproducibility in the context of clinical care. Breast Cancer Res Treat 2009, 118:635-643.
127. Verde P., Casalino L., Talotta F., Yaniv M., Weitzman J.B. Deciphering AP-1 function in tumorigenesis: fra-ternizing on target promoters. Cell Cycle 2007, 6:2633-2639.
128. Carrot Huang L.E., stick. HIF-alpha engages c-Myc in hypoxic adaptation. Cell Death Differ 2008, 15:672-677.
129. Lee H.K., Hsu A.K., Sajdak J., Qin J., Pavlidis P. Coexpression analysis of human genes across many microarray data sets. Genome Res 2004, 14:1085-1094.
130. Zhang W., Morris Q.D., Chang R., Shai O., Bakowski M.A., Mitsakakis N., et al. The functional landscape of mouse gene expression. J Biol 2004, 3:21.
131. Clarke R., Ressom H.W., Wang A., Xuan J., Liu M.C., Gehan E.A., et al. The properties of high-dimensional data spaces: implications for exploring gene and protein expression data. Nat Rev Cancer 2008, 8:37-49.
132. Rowland B.D., Bernards R., Peeper D.S. The KLF4 tumour suppressor is a transcriptional repressor of p53 that acts as a context-dependent oncogene. Nat Cell Biol 2005, 7:1074-1082.
133. Smith C.L., O'Malley B.W. Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr Rev 2004, 25:45-71.
134. Li C., Wong W.H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 2001, 98:31-36.
135. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
136. Hubbell E., Liu W.M., Mei R. Robust estimators for expression analysis. Bioinformatics 2002, 18:1585-1592.
137. Hekstra D., Taussig A.R., Magnasco M., Naef F. Absolute mRNA concentrations from sequence-specific calibration of oligonucleotide arrays. Nucleic Acids Res 2003, 31:1962-1968.
138. Carter S.L., Eklund A.C., Mecham B.H., Kohane I.S., Szallasi Z. Redefinition of Affymetrix probe sets by sequence overlap with cDNA microarray probes reduces cross-platform inconsistencies in cancer-associated gene expression measurements. BMC Bioinformatics 2005, 6:107.
139. Dai M., Wang P., Boyd A.D., Kostov G., Athey B., Jones E.G., et al. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 2005, 33:e175.
140. Harbig J., Sprinkle R., Enkemann S.A. A sequence-based identification of the genes detected by probesets on the Affymetrix U133 plus 2.0 array. Nucleic Acids Res 2005, 33:e31.
141. Liu H., Zeeberg B.R., Qu G., Koru A.G., Ferrucci A., Kahn A., et al. AffyProbeMiner: a web resource for computing or retrieving accurately redefined Affymetrix probe sets. Bioinformatics 2007, 23:2385-2390.
142. Sandberg R., Larsson O. Improved precision and accuracy for microarrays using updated probe set definitions. BMC Bioinformatics 2007, 8:48.
143. Nurtdinov R.N., Vasiliev M.O., Ershova A.S., Lossev I.S., Karyagina A.S. PLANdbAffy: probe-level annotation database for affymetrix expression microarrays. Nucleic Acids Res 2010, 38:D726-D730.
144. Ferrari F., Bortoluzzi S., Coppe A., Sirota A., Safran M., Shmoish M., et al. Novel definition files for human genechips based on GeneAnnot. BMC Bioinformatics 2007, 8:446.
145. McCall M.N., Bolstad B.M., Irizarry R.A. Frozen robust multiarray analysis (fRMA). Biostatistics 2010, 11:242-253.
146. Kellen E., Vansant G., Christiaens M.R., Neven P., Van Limbergen E. Lifestyle changes and breast cancer prognosis: a review. Breast Cancer Res Treat 2009, 114:13-22.
147. Glinsky G.V., Berezovska O., Glinskii A.B. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest 2005, 115:1503-1521.
148. Ben-Porath I., Thomson M.W., Carey V.J., Ge R., Bell G.W., Regev A., et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008, 40:499-507.
149. Hassan K.A., Chen G., Kalemkerian G.P., Wicha M.S., Beer D.G. An embryonic stem cell-like signature identifies poorly differentiated lung adenocarcinoma but not squamous cell carcinoma. Clin Cancer Res 2009, 15:6386-6390.
150. Fortunel N.O., Otu H.H., Ng H.H., Chen J., Mu X., Chevassut T., et al. Comment on 'Stemness': transcriptional profiling of embryonic and adult stem cells and a stem cell molecular signature. Science 2003, 302:393. author reply.
151. Wong D.J., Liu H., Ridky T.W., Cassarino D., Segal E., Chang H.Y. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2008, 2:333-344.
152. Kim J., Woo A.J., Chu J., Snow J.W., Fujiwara Y., Kim C.G., et al. A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 2010, 143:313-324.
153. Koeva M., Forsberg E.C., Stuart J.M. Computational integration of homolog and pathway gene module expression reveals general stemness signatures. PLoS One 2011, 6:e18968.
154. Shats I., Gatza M.L., Chang J.T., Mori S., Wang J., Rich J., et al. Using a stem cell-based signature to guide therapeutic selection in cancer. Cancer Res 2011, 71:1772-1780.
155. Mizuno H., Spike B.T., Wahl G.M., Levine A.J. Inactivation of p53 in breast cancers correlates with stem cell transcriptional signatures. Proc Natl Acad Sci U S A 2010, 107:22745-22750.
156. Zhao T., Xu Y. p53 and stem cells: new developments and new concerns. Trends Cell Biol 2010, 20:170-175.
157. Cicalese A., Bonizzi G., Pasi C.E., Faretta M., Ronzoni S., Giulini B., et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009, 2009.
158. Merlos-Suarez A., Barriga F.M., Jung P., Iglesias M., Cespedes M.V., Rossell D., et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011, 8:511-524.
159. Pece S., Tosoni D., Confalonieri S., Mazzarol G., Vecchi M., Ronzoni S., et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010, 140:62-73.
160. Eisterer W., Jiang X., Christ O., Glimm H., Lee K.H., Pang E., et al. Different subsets of primary chronic myeloid leukemia stem cells engraft immunodeficient mice and produce a model of the human disease. Leukemia 2005, 19:435-441.
161. Neering S.J., Bushnell T., Sozer S., Ashton J., Rossi R.M., Wang P.Y., et al. Leukemia stem cells in a genetically defined murine model of blast-crisis CML. Blood 2007, 110:2578-2585.
162. Read T.A., Fogarty M.P., Markant S.L., McLendon R.E., Wei Z., Ellison D.W., et al. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 2009, 15:135-147.
163. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., et al. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
164. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
165. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
166. Bhat-Nakshatri P., Appaiah H., Ballas C., Pick-Franke P., Goulet R., Badve S., et al. SLUG/SNAI2 and tumor necrosis factor generate breast cells with CD44+/CD24- phenotype. BMC Cancer 2010, 10:411.
167. Shipitsin M., Campbell L.L., Argani P., Weremowicz S., Bloushtain-Qimron N., Yao J., et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007, 11:259-273.
168. Marcato P., Dean C.A., Pan D., Araslanova R., Gillis M., Joshi M., et al. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cells 2011, 2011.
169. Baumann P., Cremers N., Kroese F., Orend G., Chiquet-Ehrismann R., Uede T., et al. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 2005, 65:10783-10793.
170. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011, 17:313-319.
171. Zhou J., Wang H., Cannon V., Wolcott K.M., Song H., Yates C. Side population rather than CD133(+) cells distinguishes enriched tumorigenicity in hTERT-immortalized primary prostate cancer cells. Mol Cancer 2011, 10:112.
172. Eppert K., Takenaka K., Lechman E.R., Waldron L., Nilsson B., van Galen P., et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 2011, 17:1086-1093.
173. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
174. Pinner S., Jordan P., Sharrock K., Bazley L., Collinson L., Marais R., et al. Intravital imaging reveals transient changes in pigment production and Brn2 expression during metastatic melanoma dissemination. Cancer Res 2009, 69:7969-7977.
175. Quintana E., Shackleton M., Foster H.R., Fullen D.R., Sabel M.S., Johnson T.M., et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 2010, 18:510-523.
176. Takeda N., Jain R., Leboeuf M.R., Wang Q., Lu M.M., Epstein J.A. Interconversion Between Intestinal Stem Cell Populations in Distinct Niches. Science 2011.
177. Tian H., Biehs B., Warming S., Leong K.G., Rangell L., Klein O.D., et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 2011, 478:255-259.
178. Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644.
179. Pantel K., Alix-Panabieres C., Riethdorf S. Cancer micrometastases. Nat Rev Clin Oncol 2009, 6:339-351.
180. Lianidou E.S., Markou A. Circulating tumor cells in breast cancer: detection systems, molecular characterization, and future challenges. Clin Chem 2011, 57:1242-1255.
181. Sieuwerts A.M., Kraan J., Bolt J., van der Spoel P., Elstrodt F., Schutte M., et al. Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumor cells. J Natl Cancer Inst 2009, 101:61-66.
182. Mostert B., Kraan J., Bolt-de Vries J., van der Spoel P., Sieuwerts A.M., Schutte M., et al. Detection of circulating tumor cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Res Treat 2011, 127:33-41.
183. Fehm T., Becker S., Duerr-Stoerzer S., Sotlar K., Mueller V., Wallwiener D., et al. Determination of HER2 status using both serum HER2 levels and circulating tumor cells in patients with recurrent breast cancer whose primary tumor was HER2 negative or of unknown HER2 status. Breast Cancer Res 2007, 9:R74.
184. Aktas B., Muller V., Tewes M., Zeitz J., Kasimir-Bauer S., Loehberg C.R., et al. Comparison of estrogen and progesterone receptor status of circulating tumor cells and the primary tumor in metastatic breast cancer patients. Gynecol Oncol 2011, 122:356-360.