Bmi-1, c-myc, and Snail expression in primary breast cancers and their metastases-elevated Bmi-1 expression in late breast cancer relapses

Virchows Archiv

Volumn 459, Issue 1, 2011, Pages 31-39

  Joensuu, Kristiina ^a   Hagström, Jaana ^a,b   Leidenius, Marjut ^c   Haglund, Caj ^a,c   Andersson, Leif C ^a   Sariola, Hannu ^c   Heikkilä, Päivi ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Breast cancer; Immunohistochemistry; Tumor dormancy

Indexed keywords

BMI1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; KI 67 ANTIGEN; PROGESTERONE RECEPTOR; TRANSCRIPTION FACTOR SNAIL;

ADULT; ARTICLE; AXILLARY LYMPH NODE; BREAST CANCER; CANCER RELAPSE; CANCER STEM CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; METASTASIS; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BREAST NEOPLASMS; DNA-BINDING PROTEINS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHATIC METASTASIS; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 79959961046     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-011-1096-8     Document Type: Article

References (50)

1. M van Lohuizen S Verbeek B Scheijen E Wientjens H van der Gulden A Berns 1991 Identification of cooperating oncogenes in Eμ-myc transgenic mice by provirus tagging Cell 65 5 737 752 1904008 10.1016/0092-8674(91)90382-9 (Pubitemid 121001306)
2. Y Haupt WS Alexander G Barri SP Klinken JM Adams 1991 Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in Eμ-myc transgenic mice Cell 65 5 753 763 1904009 10.1016/0092-8674(91) 90383-A 1:CAS:528:DyaK38XnslGnsQ%3D%3D (Pubitemid 121001307)
3. DP Satijn KM Hamer J den Blaauwen AP Otte 2001 The polycomb group protein EED interacts with YY1 and both proteins induce neural tissue in Xenopus embryos Mol Cell Biol 21 4 1360 1369 11158321 10.1128/MCB.21.4.1360-1369.2001 1:CAS:528:DC%2BD3MXovVCmtA%3D%3D (Pubitemid 32114983)
4. JJ Jacobs B Scheijen JW Voncken K Kieboom A Berns M van Lohuizen 1999 Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF Genes Dev 13 20 2678 2690 10541554 10.1101/gad.13.20. 2678 1:CAS:528:DyaK1MXnt1Wqs7w%3D (Pubitemid 29508555)
5. JH Kim SY Yoon SH Jeong SY Kim SK Moon JH Joo Y Lee IS Choe JW Kim 2004 Overexpression of Bmi-1 oncoprotein correlates with axillary lymph node metastases in invasive ductal breast cancer Breast 13 5 383 388 15454193 10.1016/j.breast.2004.02.010 (Pubitemid 39549787)
6. M Al-Hajj MS Wicha A Benito-Hernandez SJ Morrison MF Clarke 2006 Prospective identification of tumorigenic breast cancer cells Proc Natl Acad Sci U S A 100 7 3983 3988 10.1073/pnas.0530291100
7. S Liu G Dontu ID Mantle S Patel NS Ahn KW Jackson P Suri MS Wicha 2006 Hedgehog signalling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells Cancer Res 66 12 6063 6071 16778178 10.1158/0008-5472.CAN-06-0054 1:CAS:528:DC%2BD28XlvVSksrY%3D
8. LB Song MS Zeng WT Liao L Zhang HY Mo WL Liu JY Shao QL Wu MZ Li YF Xia LW Fu WL Huang GP Dimri V Band YX Zeng 2006 Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells Cancer Res 66 12 6225 6232 16778197 10.1158/0008-5472.CAN-06-0094 1:CAS:528:DC%2BD28XlvVSkt70%3D
9. H Wang K Pan HK Zhang DS Weng J Zhou JJ Li W Huang HF Song MS Chen J Xia 2008 Increased polycomb-group oncogene Bmi-1 expression correlates with poor prognosis in hepatocellular carcinoma J Cancer Res Clin Oncol 134 5 535 541 17917742 10.1007/s00432-007-0316-8 1:CAS:528:DC%2BD1cXjsF2ju7k%3D (Pubitemid 351422607)
10. V Häyry O Tynninen HK Haapasalo J Wölfer W Paulus M Hasselblatt H Sariola A Paetau S Sarna M Niemelä K Wartiovaara NN Nupponen 2008 Stem cell protein Bmi-1 is an independent marker for poor prognosis in oligodendroglial tumors Neuropathol Appl Neurobiol 34 5 555 563 18346113 10.1111/j.1365-2990.2008.00949.x
11. C Leung M Lingbeek O Shakhova J Liu E Tanger P Saremaslani M van Lohuizen S Marino 2004 Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas Nature 428 6980 337 341 15029199 10.1038/nature02385 1:CAS:528:DC%2BD2cXitFCnur8%3D (Pubitemid 38418806)
12. K Vrzalikova J Skarda J Ehrmann PG Murray E Fridman J Kopolovic P Knizetova M Hajduch J Klein V Kolek L Radova Z Kolar 2008 Prognostic value of Bmi-1 oncoprotein in NSCLC patients: a tissue microarray study J Cancer Res Clin Oncol 134 9 1037 1042 18264721 10.1007/s00432-008-0361-y 1:CAS:528: DC%2BD1cXps12msrg%3D
13. V Häyry LK Mäkinen T Atula H Sariola A Mäkitie I Leivo H Keski-Säntti J Lundin C Haglund J Hagström 2010 Bmi-1 expression predicts prognosis in squamous cell carcinoma of the tongue Br J Cancer 102 5 892 897 20145620 10.1038/sj.bjc.6605544
14. JM Bishop 1982 Retroviruses and cancer genes Adv Cancer Res 37 1 32 6763842 10.1016/S0065-230X(08)60880-5 1:CAS:528:DyaL3sXms1aitA%3D%3D
15. B Vennstrom D Sheiness J Zabielski JM Bishop 1982 Isolation and characterization of c-myc, a cellular homolog of the oncogene (v-myc) of avian myelocytomatosis virus strain 29 J Virol 42 3 773 779 6284994 1:CAS:528:DyaL38XktVWmtr0%3D (Pubitemid 12125621)
16. PH Rabbits JV Watson A Lamond A Forster MA Stinson G Evan W Fischer E Atherton R Sheppard TH Rabbitts 1985 Metabolism of c-myc gene products: c-myc mRNA and protein expression in the cell cycle EMBO J 4 8 2009 2015
17. EA Harrington MR Bennett A Fanidi GI Evan 1994 c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines EMBO J 13 14 3286 3295 8045259 1:CAS:528:DyaK2cXlt1Kjtbk%3D (Pubitemid 24226943)
18. LT Amundadottir MD Johnson G Merlino GH Smith RB Dickson 1995 Synergistic interaction of transforming growth factor alfa and c-myc in mouse mammary and salivary gland tumorigenesis Cell Growth Differ 6 6 737 748 7669729 1:CAS:528:DyaK2MXmt1amsrc%3D
19. S Pelengaris M Khan G Evan 2002 c-MYC: more than just a matter of life and death Nat Rev Cancer 2 10 764 776 12360279 10.1038/nrc904 1:CAS:528:DC%2BD38XnsVGrtbw%3D (Pubitemid 37328911)
20. SM Rodriguez-Pinilla RL Jones MB Lambros E Arriola K Savage M James SE Pinder JS Reis-Filho 2007 MYC amplification in breast cancer: a chromogenic in situ hybridisation study J Clin Pathol 60 9 1017 1023 17158641 10.1136/jcp.2006.043869 (Pubitemid 47441935)
21. DJ Liao RB Dickson 2000 c-Myc in breast cancer Endocr Relat Cancer 7 3 143 164 11021963 10.1677/erc.0.0070143 1:CAS:528:DC%2BD3cXot1Wrs7Y%3D
22. SL Deming SJ Nass RB Dickson BJ Trock 2000 C-myc amplification in breast cancer: a meta-analysis of its occurrence and prognostic relevance Br J Cancer 83 12 1688 1695 11104567 10.1054/bjoc.2000.1522 1:CAS:528:DC%2BD3MXktFCksQ%3D%3D (Pubitemid 32001715)
23. M van Lohuizen M Frasch E Wientjens A Berns 1991 Sequence similarity between the mammalian bmi-1 proto-oncogene and Drosophila regulatory genes Psc and Su(z)2 Nature 353 6342 353 355 1922340 10.1038/353353a0 (Pubitemid 21912509)
24. Y Haupt ML Bath AW Harris JM Adams 1993 Bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis Oncogene 8 11 3161 3164 8414519 1:CAS:528:DyaK2cXivVCnsw%3D%3D (Pubitemid 23312924)
25. LS Levy PA Lobelle-Rich J Overbaugh 1993 Flvi-2, a target of retroviral insertional mutagenesis in feline thymic lymphosarcomas, encodes bmi-1 Oncogene 8 7 1833 1838 8390036 1:CAS:528:DyaK3sXmtVSktrg%3D (Pubitemid 23212416)
26. E Batlle E Sancho C Francí D Domínguez M Monfar J Baulida A García De Herreros 2000 The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumor cells Nat Cell Biol 2 2 84 89 10655587 10.1038/35000034 1:CAS:528:DC%2BD3cXhtVyltLo%3D
27. A Cano MA Pérez-Moreno I Rodrigo A Locascio MJ Blanco MG del Barrio F Portillo MA Nieto 2000 The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat Cell Biol 2 2 76 83 10655586 10.1038/35000025 1:CAS:528:DC%2BD3cXhtVyltLw%3D
28. H Peinado D Olmeda A Cano 2007 Snail, Zeb and bHLH factors in tumor progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7 6 415 428 17508028 10.1038/nrc2131 1:CAS:528:DC%2BD2sXls1Kjs70%3D (Pubitemid 46809165)
29. CW Cheng PE Wu JC Yu CS Huang CT Yue CW Wu CY Shen 2001 Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene Oncogene 20 29 3814 3823 11439345 10.1038/sj.onc.1204505 1:CAS:528:DC%2BD3MXlt1KrsL8%3D (Pubitemid 32646192)
30. I Poser D Domínguez AG de Herreros A Varnai R Buettner AK Bosserhoff 2001 Loss of E-cadherin expression in melanoma cells involves up-regulation of the transcriptional repressor Snail J Biol Chem 276 27 24661 24666 11323412 10.1074/jbc.M011224200 1:CAS:528:DC%2BD3MXlt1agsb8%3D
31. MJ Blanco G Moreno-Bueno D Sarrio A Locascio A Cano J Palacios MA Nieto 2002 Correlation of Snail expression with histological grade and lymph node status in breast carcinomas Oncogene 21 20 3241 3246 12082640 10.1038/sj.onc.1205416 1:CAS:528:DC%2BD38XktFGjsrY%3D (Pubitemid 34548095)
32. K Sugimachi S Tanaka T Kameyama K Taguchi S Aishima M Shimada K Sugimachi M Tsuneyoshi 2003 Transcriptional repressor Snail and progression of human hepatocellular carcinoma Clin Cancer Res 9 7 2657 2664 12855644 1:CAS:528:DC%2BD3sXlt1yrs7w%3D (Pubitemid 36842110)
33. D Olmeda G Moreno-Bueno JM Flores A Fabra F Portillo A Cano 2007 SNAI1 is required for tumor growth and lymph node metastasis of human breast carcinoma MDA-MB-231 cells Cancer Res 67 24 11721 11731 18089802 10.1158/0008-5472.CAN-07- 2318 1:CAS:528:DC%2BD2sXhsVCjs7vK
34. K Joensuu P Heikkilä LC Andersson 2008 Tumor dormancy: elevated expression of stanniocalcins in late relapsing breast cancer Cancer Lett 265 1 76 83 18355956 10.1016/j.canlet.2008.02.022 1:CAS:528:DC%2BD1cXlvFyhsLc%3D
35. CW Elston IO Ellis 1991 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 19 5 403 410 1757079 10.1111/j.1365-2559.1991.tb00229.x 1:STN:280:DyaK38%2FpvVSltw%3D%3D
36. AC Wolff ME Hammond JN Schwarts KL Hagerty DC Allred RJ Cote M Dowsett PL Fitzgibbons WM Hanna A Langer LM McShane S Paik MD Pegram EA Perez MF Press A Rhodes C Sturgeon SE Taube R Tubbs GH Vance M van de Vijver TM Wheeler DF Hayes 2007 American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal grwth factor receptor 2 testing in breast cancer Arch Pathol Lab Med 131 1 18 43 19548375 1:CAS:528: DC%2BD2sXhsVOmu74%3D (Pubitemid 46174133)
37. ZP Pavelic K Pavelic CP Carter L Pavelic 1992 Heterogeneity of c-myc expression in histologically similar infiltrating ductal carcinomas of the breast J Cancer Res Clin Oncol 118 1 16 22 1309531 10.1007/BF01192306 1:STN:280:DyaK387gsFWksw%3D%3D
38. LP Pertschuk EH Tobin P Tanapat, et al. 1980 Histochemical analyses of steroid hormone receptors in breast and prostatic carcinoma J Histochem Cytochem 28 8 799 810 7440959 10.1177/28.8.7440959 1:STN:280:DyaL3M%2FntVKhug%3D%3D (Pubitemid 11253570)
39. MC Cheang SK Chia D Voduc D Gao S Leung J Snider M Watson S Davies PS Bernard JS Parker CM Perou MJ Ellis TO Nielsen 2009 Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer J Natl Cancer Inst 101 10 736 750 19436038 10.1093/jnci/djp082 1:CAS:528:DC%2BD1MXmtlyit74%3D
40. FM Raaphorst CJ Meijer E Fieret T Blokzijl E Mommers H Buerger J Packeisen RA Sewalt AP Otte PJ van Diest 2003 Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene Neoplasia 5 6 481 488 14965441 1:CAS:528:DC%2BD2cXht1Wgtr0%3D (Pubitemid 38045085)
41. D Mihic-Probst A Kuster S Kilgus B Bode-Lesniewska B Ingold-Heppner C Leung M Storz B Seifert S Marino P Schraml R Dummer H Moch 2007 Consistent expression of the stem cell renewal factor BMI-1 in primary and metastatic melanoma Int J Cancer 121 8 1764 1770 17597110 10.1002/ijc.22891 1:CAS:528:DC%2BD2sXhtVyktb7N (Pubitemid 47417295)
42. JA Aguirre-Ghiso 2007 Models, mechanisms and clinical evidence for cancer dormancy Nat Rev Cancer 7 11 834 846 17957189 10.1038/nrc2256 1:CAS:528:DC%2BD2sXht1Wgsb%2FO (Pubitemid 350006258)
43. Y Feng LB Song BH Guo WT Liao MZ Li WL Liu MS Zeng L Zhang 2007 Expression and significance of Bmi-1 in breast cancer Chin J of Cancer 26 2 154 157 1:CAS:528:DC%2BD1cXkt1Klurs%3D
44. YJ Choi YL Choi EY Cho YK Shin KW Sung YK Hwang SJ Lee G Kong JE Lee JS Kim JH Kim JH Yang SJ Nam 2009 Expression of Bmi-1 protein in tumor tissues is associated with favourable prognosis in breast cancer patients Breast Cancer Res Treat 113 1 83 93 18228133 10.1007/s10549-008-9909-4 1:CAS:528: DC%2BD1cXhsFWrs7nJ
45. ER Andrechek RD Cardiff JT Chang ML Gatza CR Acharya A Potti JR Nevins 2009 Genetic heterogeneity of Myc-induced mammary tumors reflecting diverse phenotypes including metastatic potential Proc Natl Acad Sci U S A 106 38 6387 16392 10.1073/pnas.0901250106
46. DA Spandidos M Yiagnisis K Papadimitriou JK Field 1989 Ras, c-myc and c-erB-2 oncoproteins in human breast cancer Anticancer Res 9 5 1385 1393 2574023 1:STN:280:DyaK3c%2Fnt12gtQ%3D%3D
47. ZP Pavelic L Pavelic EE Lower M Gapany S Gapany EA Barker HD Preisler 1992 c-myc, c-erB-2, and Ki-67 expression in normal breast tissue and in invasive and non-invasive breast carcinoma Cancer Res 52 9 2597 2602 1348967 1:CAS:528:DyaK38XktVGhsb8%3D
48. AP Locker CS Dowle IO Ellis CW Elston RW Blamey K Sikora G Evan RA Robins 1989 c-myc oncogene product expression and prognosis in operable breast cancer Br J Cancer 60 5 669 672 2679850 10.1038/bjc.1989.337 1:STN:280: DyaK3c%2FivVSmsQ%3D%3D (Pubitemid 19275728)
49. C Côme F Magnino F Bibeau BP De Santa KF Becker C Theillet P Savagner 2006 Snail and slug play distinct roles during breast carcinoma progression Clin Cancer Res 12 18 5395 5402 17000672 10.1158/1078-0432.CCR-06- 0478 (Pubitemid 44497253)
50. LB Song J Li WT Liao Y Feng CP Yu LJ Hu QL Kong LH Xu X Zhang WL Liu MZ Li L Zhang TB Kang LW Fu WL Huang YF Xia SW Tsao M Li V Band H Band QH Shi YX Zeng MS Zeng 2009 The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells J Clin Invest 119 12 3626 3636 19884659 10.1172/JCI39374 1:CAS:528:DC%2BD1MXhsFCit7jL