Independent prognostic value of the basal-like phenotype of breast cancer and associations with EGFR and candidate stem cell marker BMI-1

Histopathology

Volumn 52, Issue 3, 2008, Pages 370-380

  Arnes, J B ^a   Collett, K ^a   Akslen, L A ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Basal like phenotype; Biomarkers; BMI1; Breast carcinoma; EGFR; EZH2; Immunohistochemistry; Oct 4; Prognosis; Stem cell; Tissue microarrays

Indexed keywords

BMI1 PROTEIN; CADHERIN; CELL MARKER; CYTOKERATIN 5; EPIDERMAL GROWTH FACTOR RECEPTOR; EZH2 PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; LYMPH NODE; MAJOR CLINICAL STUDY; MULTIVARIATE ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TUMOR DIFFERENTIATION;

AGED; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; DNA-BINDING PROTEINS; FEMALE; HUMANS; MASTECTOMY; MIDDLE AGED; NEOPLASMS, BASAL CELL; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; PHENOTYPE; PROGNOSIS; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; REPRESSOR PROTEINS; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 38849208351     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/j.1365-2559.2007.02957.x     Document Type: Article

References (71)

1. Perou CM, Sorlie T, Eisen MB et al. Molecular portraits of human breast tumours. Nature 2000 406 747 752.
2. Sorlie T, Perou CM, Tibshirani R et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 2001 98 10869 10874.
3. van 't Veer LJ, Dai H, van de Vijver MJ et al. Expression profiling predicts outcome in breast cancer. Breast Cancer Res. 2003 5 57 58.
4. Sotiriou C, Neo SY, McShane LM et al. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc. Natl. Acad. Sci. USA 2003 100 10393 10398.
5. Sorlie T, Tibshirani R, Parker J et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. USA 2003 100 8418 8423.
6. Arnes JB, Brunet JS, Stefansson I et al. Placental cadherin and the basal epithelial phenotype of BRCA1-related breast cancer. Clin. Cancer Res. 2005 11 4003 4011.
7. Foulkes WD, Brunet JS, Stefansson IM et al. The prognostic implication of the basal-like (cyclin E high/p27 low/p53+/glomeruloid-microvascular- proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res. 2004 64 830 835.
8. Goffin JR, Straume O, Chappuis PO et al. Glomeruloid microvascular proliferation is associated with p53 expression, germline BRCA1 mutations and an adverse outcome following breast cancer. Br. J. Cancer 2003 89 1031 1034.
9. Chappuis PO, Kapusta L, Begin LR et al. Germline BRCA1/2 mutations and p27(Kip1) protein levels independently predict outcome after breast cancer. J. Clin. Oncol. 2000 18 4045 4052.
10. Straume O, Chappuis PO, Salvesen HB et al. Prognostic importance of glomeruloid microvascular proliferation indicates an aggressive angiogenic phenotype in human cancers. Cancer Res. 2002 62 6808 6811.
11. Nielsen TO, Hsu FD, Jensen K et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin. Cancer Res. 2004 10 5367 5374.
12. Livasy CA, Karaca G, Nanda R et al. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod. Pathol. 2006 19 264 271.
13. Abd El-Rehim DM, Pinder SE, Paish CE et al. Expression and co-expression of the members of the epidermal growth factor receptor (EGFR) family in invasive breast carcinoma. Br. J. Cancer 2004 91 1532 1542.
14. Klijn JG, Berns PM, Schmitz PI, Foekens JA. The clinical significance of epidermal growth factor receptor (EGF-R) in human breast cancer: a review on 5232 patients. Endocr. Rev. 1992 13 3 17.
15. Baselga J, Arteaga CL. Critical update and emerging trends in epidermal growth factor receptor targeting in cancer. J. Clin. Oncol. 2005 23 2445 2459.
16. Siegel-Lakhai WS, Beijnen JH, Schellens JH. Current knowledge and future directions of the selective epidermal growth factor receptor inhibitors erlotinib (Tarceva) and gefitinib (Iressa). Oncologist 2005 10 579 589.
17. Foulkes WD. BRCA1 functions as a breast stem cell regulator. J. Med. Genet. 2004 41 1 5.
18. Bocker W, Moll R, Poremba C 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.
19. Alkema MJ, Wiegant J, Raap AK, Berns A, van Lohuizen M. Characterization and chromosomal localization of the human proto-oncogene BMI-1. Hum. Mol. Genet. 1993 2 1597 1603.
20. Jacobs JJ, van Lohuizen M. Polycomb repression: from cellular memory to cellular proliferation and cancer. Biochim. Biophys. Acta 2002 1602 151 161.
21. Haupt Y, Bath ML, Harris AW, Adams JM. bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. Oncogene 1993 8 3161 3164.
22. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev. 1999 13 2678 2690.
23. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999 397 164 168.
24. Raaphorst FM, Meijer CJ, Fieret E et al. Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. Neoplasia 2003 5 481 488.
25. Vonlanthen S, Heighway J, Altermatt HJ et al. The bmi-1 oncoprotein is differentially expressed in non-small cell lung cancer and correlates with INK4A-ARF locus expression. Br. J. Cancer 2001 84 1372 1376.
26. Breuer RH, Snijders PJ, Smit EF et al. Increased expression of the EZH2 polycomb group gene in BMI-1-positive neoplastic cells during bronchial carcinogenesis. Neoplasia 2004 6 736 743.
27. Dukers DF, van Galen JC, Giroth C et al. Unique polycomb gene expression pattern in Hodgkin's lymphoma and Hodgkin's lymphoma-derived cell lines. Am. J. Pathol. 2004 164 873 881.
28. van Kemenade FJ, Raaphorst FM, Blokzijl T et al. Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood 2001 97 3896 3901.
29. Raaphorst FM, van Kemenade FJ, Fieret E et al. Cutting edge: polycomb gene expression patterns reflect distinct B cell differentiation stages in human germinal centers. J. Immunol. 2000 164 1 4.
30. Liu S, Dontu G, Mantle ID et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006 66 6063 6071.
31. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 2003 22 5323 5335.
32. Kleer CG, Cao Q, Varambally S et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc. Natl. Acad. Sci. USA 2003 100 11606 11611.
33. Collett K, Eide GE, Arnes J et al. Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Clin. Cancer Res. 2006 12 1168 1174.
34. Bachmann IM, Halvorsen OJ, Collett K et al. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J. Clin. Oncol. 2006 24 268 273.
35. Visser HP, Gunster MJ, Kluin-Nelemans HC et al. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br. J. Haematol. 2001 112 950 958.
36. Rosner MH, Vigano MA, Ozato K et al. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 1990 345 686 692.
37. Okamoto K, Okazawa H, Okuda A, Sakai M, Muramatsu M, Hamada H. A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 1990 60 461 472.
38. Pan GJ, Chang ZY, Scholer HR, Pei D. Stem cell pluripotency and transcription factor Oct4. Cell Res. 2002 12 321 329.
39. Pesce M, Scholer HR. Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 2001 19 271 278.
40. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 2000 24 372 376.
41. Nichols J, Zevnik B, Anastassiadis K et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998 95 379 391.
42. Looijenga LH, Stoop H, de Leeuw HP et al. POU5F1 (OCT3/4) identifies cells with pluripotent potential in human germ cell tumors. Cancer Res. 2003 63 2244 2250.
43. Gidekel S, Pizov G, Bergman Y, Pikarsky E. Oct-3/4 is a dose-dependent oncogenic fate determinant. Cancer Cell 2003 4 361 370.
44. Ezeh UI, Turek PJ, Reijo RA, Clark AT. Human embryonic stem cell genes OCT4, NANOG, STELLAR, and GDF3 are expressed in both seminoma and breast carcinoma. Cancer 2005 104 2255 2265.
45. Ponti D, Costa A, Zaffaroni N et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005 65 5506 5511.
46. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005 65 10946 10951.
47. Collett K, Stefansson IM, Eide J et al. A basal epithelial phenotype is more frequent in interval breast cancers compared with screen detected tumors. Cancer Epidemiol. Biomarkers Prev. 2005 14 1108 1112.
48. Nocito A, Kononen J, Kallioniemi OP, Sauter G. Tissue microarrays (TMAs) for high-throughput molecular pathology research. Int. J. Cancer 2001 94 1 5.
49. Bhargava R, Chen B, Klimstra DS et al. Comparison of two antibodies for immunohistochemical evaluation of epidermal growth factor receptor expression in colorectal carcinomas, adenomas, and normal mucosa. Cancer 2006 106 1857 1862.
50. Kersting C, Packeisen J, Leidinger B et al. Pitfalls in immunohistochemical assessment of EGFR expression in soft tissue sarcomas. J. Clin. Pathol. 2006 59 585 590.
51. DAKO. Dako website http://www.dako.com [last accessed on 25 January 2008].
52. Aas T, Borresen AL, Geisler S et al. Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nat. Med. 1996 2 811 814.
53. Straume O, Akslen LA. Alterations and prognostic significance of p16 and p53 protein expression in subgroups of cutaneous melanoma. Int. J. Cancer 1997 74 535 539.
54. Rakha E, Putti T, Abd El-Rehim D et al. Morphological and immunophenotypic analysis of breast carcinomas with basal and myoepithelial differentiation. J. Pathol. 2006 208 495 506.
55. Gamallo C, Moreno-Bueno G, Sarrio D, Calero F, Hardisson D, Palacios J. The prognostic significance of P-cadherin in infiltrating ductal breast carcinoma. Mod. Pathol. 2001 14 650 654.
56. Chung GG, Zerkowski MP, Ocal IT et al. beta-Catenin and p53 analyses of a breast carcinoma tissue microarray. Cancer 2004 100 2084 2092.
57. Reis-Filho JS, Pinheiro C, Lambros MB et al. EGFR amplification and lack of activating mutations in metaplastic breast carcinomas. J. Pathol. 2006 209 445 453.
58. Witton CJ, Reeves JR, Going JJ, Cooke TG, Bartlett JM. Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer. J. Pathol. 2003 200 290 297.
59. DiGiovanna MP, Stern DF, Edgerton SM, Whalen SG, Moore D 2nd., Thor AD. Relationship of epidermal growth factor receptor expression to ErbB-2 signaling activity and prognosis in breast cancer patients. J. Clin. Oncol. 2005 23 1152 1160.
60. Bhargava R, Gerald WL, Li AR et al. EGFR gene amplification in breast cancer: correlation with epidermal growth factor receptor mRNA and protein expression and HER-2 status and absence of EGFR-activating mutations. Mod. Pathol. 2005 18 1027 1033.
61. Ferrero JM, Ramaioli A, Largillier R et al. Epidermal growth factor receptor expression in 780 breast cancer patients: a reappraisal of the prognostic value based on an eight-year median follow-up. Ann. Oncol. 2001 12 841 846.
62. Quintela I, Corte MD, Allende MT et al. Expression and prognostic value of EGFR in invasive breast cancer. Oncol. Rep. 2005 14 1655 1663.
63. Bianchi S, Palli D, Falchetti M et al. ErbB-receptors expression and survival in breast carcinoma: a 15-year follow-up study. J. Cell. Physiol. 2006 206 702 708.
64. Al-Hajj M, Clarke MF. Self-renewal and solid tumor stem cells. Oncogene 2004 23 7274 7282.
65. Lahad JP, Mills GB, Coombes KR. Stem cell-ness: a "magic marker" for cancer. J. Clin. Invest. 2005 115 1463 1467.
66. Glinsky GV, Berezovska O, Glinskii AB. 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.
67. Bocker W. Keratin 5-positive cells in the breast are progenitor cells of glandular and myoepithelial differentiation. A cell biological model as a basis of breast pathology. Verh. Dtsch. Ges. Pathol. 2001 85 206 207.
68. de Jong J, Stoop H, Dohle GR et al. Diagnostic value of OCT3/4 for pre-invasive and invasive testicular germ cell tumours. J. Pathol. 2005 206 242 249.
69. Cheng L, Thomas A, Roth LM, Zheng W, Michael H, Karim FW. OCT4: a novel biomarker for dysgerminoma of the ovary. Am. J. Surg. Pathol. 2004 28 1341 1346.
70. Cheng L. Establishing a germ cell origin for metastatic tumors using OCT4 immunohistochemistry. Cancer 2004 101 2006 2010.
71. Suo G, Han J, Wang X, Zhang J, Zhao Y, Dai J. Oct4 pseudogenes are transcribed in cancers. Biochem. Biophys. Res. Commun. 2005 337 1047 1051.