Progression of ductal carcinoma in situ to invasive breast cancer is associated with gene expression programs of EMT and myoepithelia

Breast Cancer Research and Treatment

Volumn 133, Issue 3, 2012, Pages 1009-1024

  Knudsen, Erik S ^a,b   Ertel, Adam ^a,b,c   Davicioni, Elai ^d   Kline, Jessica ^b   Schwartz, Gordon F ^a,b   Witkiewicz, Agnieszka K ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d GenomeDx Biosciences Inc   (Canada)

Author keywords

Disease progression; Ductal carcinoma in situ; EMT; Invasive breast cancer

Indexed keywords

ESTROGEN RECEPTOR;

ACCURACY; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER SURGERY; CLASSIFIER; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; INTRADUCTAL CARCINOMA; INVASIVE BREAST CANCER; MYOEPITHELIUM; PRIORITY JOURNAL; STROMA;

BREAST NEOPLASMS; CARCINOMA, DUCTAL; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CLUSTER ANALYSIS; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; RECEPTORS, ESTROGEN; REPRODUCIBILITY OF RESULTS; STROMAL CELLS; SURVIVAL ANALYSIS;

EID: 84863725803     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-011-1894-3     Document Type: Article

References (40)

1. Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906-920
2. Collins LC, Tamimi RM, Baer HJ, Connolly JL, Colditz GA, Schnitt SJ (2005) Outcome of patients with ductal carcinoma in situ untreated after diagnostic biopsy: results from the Nurses' Health Study. Cancer 103(9):1778-1784
3. Wang SY, Shamliyan T, Virnig BA, Kane R (2011) Tumor characteristics as predictors of local recurrence after treatment of ductal carcinoma in situ: a meta-analysis. Breast Cancer Res Treat 127(1):1-14
4. Schnitt SJ (2010) Local outcomes in ductal carcinoma in situ based on patient and tumor characteristics. J Natl Cancer Inst Monogr 2010(41):158-161
5. Tsikitis VL, Chung MA (2006) Biology of ductal carcinoma in situ classification based on biologic potential. Am J Clin Oncol 29(3):305-310
6. Sakorafas GH, Farley DR, Peros G (2008) Recent advances and current controversies in the management of DCIS of the breast. Cancer Treat Rev 34(6):483-497
7. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borre-sen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406(6797):747-752
8. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lonning P, Bor-resen-Dale AL (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98(19):10869-10874
9. Buyse M, Loi S, van't Veer L, Viale G, Delorenzi M, Glas AM, d'Assignies MS, Bergh J, Lidereau R, Ellis P, Harris A, Bogaerts J, Therasse P, Floore A, Amakrane M, Piette F, Rutgers E, Sotiriou C, Cardoso F, Piccart MJ (2006) Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. J Natl Cancer Inst 98(17):1183-1192
10. Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, Hiller W, Fisher ER, Wickerham DL, Bryant J, Wolmark N (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351(27):2817-2826
11. Ma XJ, Hilsenbeck SG, Wang W, Ding L, Sgroi DC, Bender RA, Osborne CK, Allred DC, Erlander MG (2006) The HOX-B13:IL17BR expression index is a prognostic factor in early-stage breast cancer. J Clin Oncol 24(28):4611-4619
12. Ma XJ, Salunga R, Tuggle JT, Gaudet J, Enright E, McQuary P, Payette T, Pistone M, Stecker K, Zhang BM, Zhou YX, Varnholt H, Smith B, Gadd M, Chatfield E, Kessler J, Baer TM, Erlander MG, Sgroi DC (2003) Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA 100(10):5974-5979. doi:10.1073/pnas.0931261100
13. Ma XJ, Dahiya S, Richardson E, Erlander M, Sgroi DC (2009) Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res 11(1):R7
14. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, Schnitt S, Sellers WR, Polyak K (2004) Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6(1): 17-32
15. Holland R, Peterse JL, Millis RR, Eusebi V, Faverly D, van de Vijver MJ, Zafrani B (1994) Ductal carcinoma in situ: a proposal for a new classification. Semin Diagn Pathol 11(3): 167-180
16. Elston EW, Ellis IO (1993) Method for grading breast cancer. J Clin Pathol 46(2):189-190
17. Moeder CB, Giltnane JM, Harigopal M, Molinaro A, Robinson A, Gelmon K, Huntsman D, Camp RL, Rimm DL (2007) Quantitative justification of the change from 10% to 30% for human epidermal growth factor receptor 2 scoring in the American Society of Clinical Oncology/College of American Pathol-ogists guidelines: tumor heterogeneity in breast cancer and its implications for tissue microarray based assessment of outcome. J Clin Oncol 25(34):5418-5425
18. Fuller AP, Palmer-Toy D, Erlander MG, Sgroi DC (2003) Laser capture microdissection and advanced molecular analysis of human breast cancer. J Mammary Gland Biol Neoplasia 8(3):335-345
19. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Ser B 64(3):479-498. doi:10.1111/1467-9868.00346
20. Gruvberger-Saal SK, Bendahl PO, Saal LH, Laakso M, Hegardt C, Eden P, Peterson C, Malmstrom P, Isola J, Borg A, Ferno M (2007) Estrogen receptor beta expression is associated with tamoxifen response in ERalpha-negative breast carcinoma. Clin Cancer Res 13(7):1987-1994. doi:10.1158/1078-0432.CCR-06-1823
21. Zaravinos A, Lambrou GI, Boulalas I, Delakas D, Spandidos DA (2010) Identification of common differentially expressed genes in urinary bladder cancer. PLoS One 6(4):e18135. doi:10.1371/journal.pone.0018135
22. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460(7254):473-478. doi:10.1038/nature08162
23. Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19(3):368-375
24. Hackstadt AJ, Hess AM (2009) Filtering for increased power for microarray data analysis. BMC Bioinform 10:11. doi:10.1186/1471-2105-10-11
25. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 98(9):5116-5121. doi:10.1073/pnas.091062498
26. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA, Mani SA (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci USA 107(35):15449-15454. doi:10.1073/pnas.1004900107
27. Grigoriadis A, Mackay A, Reis-Filho JS, Steele D, Iseli C, Stevenson BJ, Jongeneel CV, Valgeirsson H, Fenwick K, Iravani M, Leao M, Simpson AJ, Strausberg RL, Jat PS, Ashworth A, Neville AM, O'Hare MJ (2006) Establishment of the epithelial-specific transcriptome of normal and malignant human breast cells based on MPSS and array expression data. Breast Cancer Res 8(5):R56. doi:10.1186/bcr1604
28. Kim H, Watkinson J, Varadan V, Anastassiou D (2010) Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1. BMC Med Genomics 3:51. doi:10.1186/1755-8794-3-51
29. Schuetz CS, Bonin M, Clare SE, Nieselt K, Sotlar K, Walter M, Fehm T, Solomayer E, Riess O, Wallwiener D, Kurek R, Neubauer HJ (2006) 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 66(10): 5278-5286
30. Hannemann J, Velds A, Halfwerk JB, Kreike B, Peterse JL, van de Vijver MJ (2006) Classification of ductal carcinoma in situ by gene expression profiling. Breast Cancer Res 8(5):R61. doi: 10.1186/bcr1613
31. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102(43):15545-15550. doi:10.1073/pnas.0506580102
32. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinfor-matics resources. Nat Protoc 4(1):44-57. doi:10.1038/nprot. 2008.211
33. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evan-gelista C, Kim IF, Soboleva A, Tomashevsky M, Edgar R (2007) NCBI GEO: mining tens of millions of expression profiles-database and tools update. Nucleic Acids Res 35(suppl-1):D760-D765. doi:10.1093/nar/gkl887
34. Brazma A, Parkinson H, Sarkans U, Shojatalab M, Vilo J, Abeygunawardena N, Holloway E, Kapushesky M, Kemmeren P, Lara GG, Oezcimen A, Rocca-Serra P, Sansone SA (2003) Ar-rayExpress-a public repository for microarray gene expression data at the EBI. Nucleic Acids Res 31(1):68-71
35. Ertel A, Dean JL, Rui H, Liu C, Witkiewicz AK, Knudsen KE, Knudsen ES (2010) RB-pathway disruption in breast cancer: differential association with disease subtypes, disease-specific prognosis and therapeutic response. Cell Cycle 9(20):4153-4163
36. Muggerud AA, Hallett M, Johnsen H, Kleivi K, Zhou W, Tahmasebpoor S, Amini RM, Botling J, Borresen-Dale AL, Sorlie T, Warnberg F (2010) Molecular diversity in ductal carcinoma in situ (DCIS) and early invasive breast cancer. Mol Oncol 4(4):357-368
37. Liotta LA, Stetler-Stevenson WG (1991) Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res 51(18 Suppl):5054s-5059s
38. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57-70
39. Guarino M (2007) Epithelial-mesenchymal transition and tumour invasion. Int J Biochem Cell Biol 39(12):2153-2160
40. Jones C, Mackay A, Grigoriadis A, Cossu A, Reis-Filho JS, Fulford L, Dexter T, Davies S, Bulmer K, Ford E, Parry S, Budroni M, Palmieri G, Neville AM, O'Hare MJ, Lakhani SR (2004) Expression profiling of purified normal human luminal and myoepithelial breast cells: identification of novel prognostic markers for breast cancer. Cancer Res 64(9): 3037-3045