The basal-like breast carcinoma phenotype is regulated by SLUG gene expression

Journal of Pathology

Volumn 214, Issue 1, 2008, Pages 25-37

  Storci, G ^a,b   Sansone, P ^a,b   Trere, D ^b   Tavolari, S ^b   Taffurelli, M ^a   Ceccarelli, C ^a   Guarnieri, T ^b   Paterini, P ^a,b   Pariali, M ^a   Montanaro, L ^b   Santini, D ^a   Chieco, P ^a   Bonafe M ^a,b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Basal like breast carcinoma; Hypoxia; SLUG; Stem cells

Indexed keywords

BMI1 PROTEIN; CD133 ANTIGEN; TRANSCRIPTION FACTOR SLUG;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOMA; CELL STRAIN MCF 7; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; UPREGULATION;

EID: 38049043823     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2254     Document Type: Article

References (51)

1. Landis SH, Murray T, Bolden S, Wingo PA. Cancer statistics. 1999. CA Cancer J Clin 1999;49:8-31.
2. Andre F, Pusztai L. Molecular classification of breast cancer: implications for selection of adjuvant chemotherapy. Nature Clin Pract Oncol 2006;3:621-632.
3. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000;406:747-752.
4. Pusztai L, Mazouni C, Anderson K, Wu Y, Symmans WF. Molecular classification of breast cancer: limitations and potential. Oncologist 2006;11:868-877.
5. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004;10:5367-5374.
6. Carey LA, Dees EC, Sawyer L, Gatti L, Moore DT, Collichio F, et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 2007;13:2329-2334.
7. Cleator S, Heller W, Coombes RC. Triple-negative breast cancer: therapeutic options. Lancet Oncol 2007;8:235-244.
8. Boecker W, Buerger H. Evidence of progenitor cells of glandular and myoepithelial cell lineages: cells in the human adult breast epithelium: a new progenitor (adult stem) concept. Cell Prolif 2003;36:73-84.
9. Bertucci F, Cervera N, Birnbaum D. A gene signature in breast cancer. N Engl J Med 2007;356:1887-1888.
10. Liu R, Wang X, Chen GY, 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.
11. Thiery J. Epithelial-mesenchymal transitions in tumour progression. Nature Rev 2002;2:442-454.
12. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100:3983-3988.
13. Dontu G, El-Ashry D, Wicha MS. Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol Metab 2004;15:193-197.
14. Tripathi MK, Misra S, Chaudhuri G. Negative regulation of the expression of cytokeratins 8 and 19 by SLUG repressor protein in human breast cells. Biochem Biophys Res Commun 2005;329:508-515.
15. Martinez-Estrada OM, Culleres A, Soriano FX, Peinado H, Bolos V, Martinez FO, et al. The transcription factors Slug and Snail act as repressors of claudin-1 expression in epithelial cells. Biochem J 2006;394:449- 457.
16. Barrallo-Gimeno A, Nieto MA. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005;132:3151-3161.
17. Conacci-Sorrell M, Simcha I, Ben-Yedidia T, Blechman J, Savagner P, Ben-Ze'ev A. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of β-catenin signaling, Slug, and MAPK. J Cell Biol 2003;163:847-857.
18. Shih JY, Tsai MF, Chang TH, Chang YL, Yuan A, Yu CJ, et al. Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin Cancer Res 2005;11:8070- 8078.
19. Gupta PB, Kuperwasser C, Brunet JP, Ramaswamy S, Kuo WL, Gray JW, et al. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nature Genet 2005;37:1047-1054.
20. Shioiri M, Shida T, Koda K, Oda K, Seike K, Nishimura M, et al. Slug expression is an independent prognostic parameter for poor survival in colorectal carcinoma patients. Br J Cancer 2006;94:1816-1822.
21. Elloul S, Elstrand MB, Nesland JM, Trope CG, Kvalheim G, Goldberg I, et al. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005;103:1631-1643.
22. Come C, Magnino F, Bibeau F, De Santa Barbara P, Becker KF, Theillet C, et al. Snail and Slug play distinct roles during breast carcinoma progression. Clin Cancer Res 2006;12:5395-5402.
23. Martin TA, Goyal A, Watkins G, Jiang WG. Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol 2005;12:488-496.
24. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253-1270.
25. Sansone P, Storci G, Giovannini C, Pandolfi S, Pianetti S, Taffurelli M, et al. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells 2007;25:807-815.
26. WHO. The World Health Organization histologic typing of breast tumours (2nd edition). Am J Clin Pathol 1982;78:806-816.
27. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991;19:403-410.
28. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, Wicha MS. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res 2004;6:R605-R615.
29. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005;65:5506-5511.
30. Chieco P, Jonker A, Van Noorden CJF (eds). Image Cytometry. BIOS: Oxford, 2001.
31. Reiner A, Neumeister B, Spona J, Reiner G, Schemper M, Jakesz R. Immunocytochemical localization of estrogen and progesterone receptor and prognosis in human primary breast cancer. Cancer Res 1990;50:7057- 7061.
32. Abd El-Rehim DM, Pinder SE, Paish CE, Bell J, Blamey RW, Robertson JF, et al. Expression of luminal and basal cytokeratins in human breast carcinoma. J Pathol 2004;203:661-671.
33. Livasy CA, Karaca G, Nanda R, Tretiakova MS, Olopade OI, Moore DT, et al. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod Pathol 2006;19:264-271.
34. 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.
35. Rodriguez-Pinilla SM, Sarrio D, Honrado E, Moreno-Bueno G, Hardisson D, Calero F, et al. Vimentin and laminin expression is associated with basal-like phenotype in both sporadic and BRCA1-associated breast carcinomas. J Clin Pathol 2007;60:1006-1012.
36. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 2007;104:973-978.
37. Bertheau P, Turpin E, Rickman DS, Espie M, de Reynies A, Feugeas JP, et al. Exquisite sensitivity of TP53 mutant and basal breast cancers to a dose-dense epirubicin-cyclophosphamide regimen. PLoS Med 2007;20:e90.
38. Garcia S, Dales JP, Charafe-Jauffret E, Carpentier-Meunier S, Andrac-Meyer L, Jacquemier J, et al. Poor prognosis in breast carcinomas correlates with increased expression of targetable CD146 and c-Met and with proteomic basal-like phenotype. Hum Pathol 2007;38:830-841.
39. Makretsov NA, Huntsman DG, Nielsen TO, Yorida E, Peacock M, Cheang MC, et al. Hierarchical clustering analysis of tissue microarray immunostaining data identifies prognostically significant groups of breast carcinoma. Clin Cancer Res 2004;10:6143-6151.
40. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 2006;66:6063-6071.
41. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106-110.
42. Brennan DJ, Jirstrom K, Kronblad A, Millikan RC, Landberg G, Duffy MJ, et al. CA IX is an independent prognostic marker in premenopausal breast cancer patients with one to three positive lymph nodes and a putative marker of radiation resistance. Clin Cancer Res 2006;12:6421-6431.
43. Boecker W, Moll R, Poremba C, Holland R, Van Diest PJ, Dervan P, et al. Common adult stem cells in the human breast give rise to glandular and myoepithelial cell lineages: a new cell biological concept. Lab Invest 2002;82:737-746.
44. Suda T, Arai F, Hirao A. Hematopoietic stem cells and their niche. Trends Immunol 2005;26:426-433.
45. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007;104:5431-5436.
46. Fulford LG, Reis-Filho JS, Ryder K, Jones C, Gillett CE, Hanby A, et al. Basal-like grade III invasive ductal carcinoma of the breast: patterns of metastasis and long-term survival. Breast Cancer Res 2007;9:R4.
47. Sotiriou C, Neo SY, McShane LM, Korn EL, Long PM, 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.
48. Sorlie T, Perou CM, 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.
49. Banerjee S, Reis-Filho JS, Ashley S, Steele D, Ashworth A, Lakhani SR, et al. Basal-like breast carcinomas: clinical outcome and response to chemotherapy. J Clin Pathol 2006;59:729-735.
50. Rouzier R, Perou CM, Symmans WF, Ibrahim N, Cristofanilli M, Anderson K, et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res 2005;11:5678-5685.
51. James CR, Quinn JE, Mullan PB, Johnston PG, Harkin DP. BRCA1, a potential predictive biomarker in the treatment of breast cancer. Oncologist 2007;12:142-150.