Epstein-Barr virus as a marker of biological aggressiveness in breast cancer

British Journal of Cancer

Volumn 104, Issue 2, 2011, Pages 332-337

  Mazouni, C ^a,b   Fina, F ^a   Romain, S ^a   Ouafik, L ^c   Bonnier, P ^d   Brandone, J M ^e   Martin, P M ^a  

^a ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c University of the Mediterranean Aix Marseille II   (France)

^d Clinique Beauregard   (France)

^e Clinique Bouchard   (France)

Author keywords

breast cancer; Epstein Barr virus; HER2; real time quantitative PCR; thymidine kinase

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; THYMIDINE KINASE; VIRUS DNA;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER GRADING; CLINICAL FEATURE; CONTROLLED STUDY; ENZYME ACTIVITY; EPSTEIN BARR VIRUS INFECTION; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS GENOME;

BASE SEQUENCE; BREAST NEOPLASMS; DNA PRIMERS; DNA, VIRAL; FEMALE; GENES, ERBB-2; GENOME, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; MIDDLE AGED; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR MARKERS, BIOLOGICAL;

EID: 78751480740     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6606048     Document Type: Article

References (61)

1. Amarante MK, Watanabe MA (2009) The possible involvement of virus in breast cancer. J Cancer Res Clin Oncol 135: 329-337
2. Arbach H, Viglasky V, Lefeu F, Guinebretière JM, Ramirez V, Bride N, Boualaga N, Bauchet T, Peyrat JP, Mathieu MC, Mourah S, Podgorniak MP, Seignerin JM, Takada K, Joab I (2006) Epstein-Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol). J Virol 80: 845-853
3. Berebbi M, Martin PM, Berthois Y, Bernard AM, Blangy D (1990) Estradiol dependence of the specific mammary tissue targeting of polyoma virus oncogenicity in nude mice. Oncogene 5: 505-509
4. Bloom HJ, Richardson WW (1957) Histological grading and prognosis in breast cancer; a study of 1409 cases of which 359 have been followed for 15 years. Br J Cancer 11: 359-377
5. Bonnet M, Guinebretiere JM, Kremmer E, Grunewald V, Benhamou E, Contesso G, Joab I (1999) Detection of Epstein-Barr virus in invasive breast cancers. J Natl Cancer Inst 91: 1376-1381
6. Bouchet C, Hacène K, Martin PM, Becette V, Tubiana-Hulin M, Lasry S, Oglobine J, Spyratos F (1999) Dissemination risk index based on plasminogen activator system components in primary breast cancer. J Clin Oncol 17: 3048-3057
7. Brink AA, Van Den Brule AJ, Van Diest P, Meijer CJ (2000) Re: detection of Epstein Barr virus in invasive breast cancers. J Natl Cancer Inst 92: 655-656
8. Chang KL, Chen YY, Shibata D, Weiss LM (1992) Description of an in situ hybridization methodology for detection of Epstein-Barr virus RNA in paraffin-embedded tissues, with a survey of normal and neoplastic tissues. Diagn Mol Pathol 1: 246-255
9. Chu JS, Chen CC, Chang KJ (1998) In situ detection of Epstein-Barr virus in breast cancer. Cancer Lett 124: 53-57
10. Chu PG, Chang KL, Chen YY, Chen WG, Weiss LM (2001) No significant association of Epstein-Barr virus infection with invasive breast carcinoma. Am J Pathol 159: 571-578
11. Cox B, Richardson A, Graham P, Gislefoss RE, Jellum E, Rollag H (2010) Breast cancer, cytomegalovirus and Epstein-Barr virus: a nested case-control study. Br J Cancer 102: 1665-1669
12. Dadmanesh F, Peterse JL, Sapino A, Fonelli A, Eusebi V (2001) Lymphoepithelioma-like carcinoma of the breast: lack of evidence of Epstein-Barr virus infection. Histopathology 38: 54-61
13. De Villiers EM, Sandstrom RE, zur Hausen H, Buck CE (2005) Presence of papillomavirus sequences in condylomatous lesions of the mamillae and in invasive carcinoma of the breast. Breast Cancer Res 7: R1-11
14. Deshpande CG, Badve S, Kidwai N, Longnecker R (2002) Lack of expression of the Epstein-Barr Virus (EBV) gene products, EBERs, EBNA1, LMP1, and LMP2A, in breast cancer cells. Lab Invest 82: 1193-1199
15. Fawzy S, Sallam M, Awad NM (2008) Detection of Epstein-Barr virus in breast carcinoma in Egyptian women. Clin Biochem 41: 486-492
16. Fina F, Romain S, Ouafik L, Palmari J, Ben Ayed F, Benharkat S, Bonnier P, Spyratos F, Foekens JA, Rose C, Buisson M, Gérard H, Reymond MO, Seigneurin JM, Martin PM (2001) Frequency and genome load of Epstein-Barr virus in 509 breast cancers from different geographical areas. Br J Cancer 84: 783-790
17. Gaffey MJ, Frierson Jr HF, Mills SE, Boyd JC, Zarbo RJ, Simpson JF, Gross LK, Weiss LM (1993) Medullary carcinoma of the breast. Identification of lymphocyte subpopulations and their significance. Mod Pathol 6: 721-728
18. Geurts-Moespot J, Leake R, Benraad TJ, Sweep CG (2000) Twenty years of experience with the steroid receptor external quality assessment program - the paradigm for tumour biomarker EQA studies. On behalf of the EORTC Receptor and Biomarker Study Group. Int J Oncol 17: 13-22
19. Gill MB, Kutok JL, Fingeroth JD (2007) Epstein-Barr virus thymidine kinase is a centrosomal resident precisely localized to the periphery of centrioles. J Virol 81: 6523-6535
20. Gilles SI, Romain S, Casellas P, Ouafik L, Fina F, Combes T, Vuaroquaux V, Seitz JF, Bonnier P, Galiègue S, Carayon P, Martin PM (2003) Mutation analysis in the coding sequence of thymidine kinase 1 in breast and colorectal cancer. Int J Biol Markers 18: 1-6
21. Glaser SL, Ambinder RF, DiGiuseppe JA, Horn-Ross PL, Hsu JL (1998) Absence of Epstein-Barr virus EBER-1 transcripts in an epidemio-logically diverse group of breast cancers. Int J Cancer 75: 555-558
22. Glaser SL, Hsu JL, Gulley ML (2004) Epstein-Barr virus and breast cancer: state of the evidence for viral carcinogenesis. Cancer Epidemiol Biomarkers Prev 13: 688-697
23. Hengstschläger M, Knöfler M, Müllner EW, Ogris E, Wintersberger E, Wawra E (1994) Different regulation of thymidine kinase during the cell cycle of normal versus DNA tumor virus-transformed cells. J Biol Chem 269: 13836-13842
24. Herrmann K, Niedobitek G (2003) Lack of evidence for an association of Epstein-Barr virus infection with breast carcinoma. Breast Cancer Res 5: R13-R17
25. Horiuchi K, Mishima K, Ohsawa M, Aozasa K (1994) Carcinoma of stomach and breast with lymphoid stroma: localisation of Epstein-Barr virus. J Clin Pathol 47: 538-540
26. Hu LF, Chen F, Zhen QF, Zhang YW, Luo Y, Zheng X, Winberg G, Ernberg I, Klein G (1995) Differences in the growth pattern and clinical course of EBV-LMP1 expressing and non-expressing nasopharyngeal carcinomas. Eur J Cancer 31A: 658-660
27. Huang J, Chen H, Hutt-Fletcher L, Ambinder RF, Hayward SD (2003) Lytic viralreplication as a contributor to the detection of Epstein-Barr virus in breast cancer. J Virol 77: 13267-13274
28. Isaacs C, Stearns V, Hayes DF (2001) New prognostic factors for breast cancer recurrence. Semin Oncol 28: 53-67
29. Joshi D, Quadri M, Gangane N, Joshi R, Gangane N (2009) Association of Epstein Barr virus infection (EBV) with breast cancer in rural Indian women. PLoS One 4: e8180
30. Kalkan A, Ozdarendeli A, Bulut Y, Yekeler H, Cobanoglu B, Doymaz MZ (2005) Investigation of Epstein-Barr virus DNA in formalin-fixed and paraffin- embedded breast cancer tissues. Med Princ Pract 14: 268-271
31. Kulka J, Kovalszky I, Svastics E, Berta M, Füle T (2008) Lymphoepithe-lioma-like carcinoma of the breast: not Epstein-Barr virus-, but human papilloma virus-positive. Hum Pathol 39: 298-301
32. Kösel S, Grasbon-Frodl EM, Arima K, Chimelli L, Hahn M, Hashizume Y, Hulette C, Ikeda K, Jacobsen PF, Jones M, Kobayashi M, Love S, Mizutani T, Rosemberg S, Sasaki A, Smith TW, Takahashi H, Vortmeyer AO, Graeber MB (2001) Inter-laboratory comparison of DNA preservation in archival paraffin-embedded human brain tissue from participating centres on four continents. Neurogenetics 3: 163-170
33. Labrecque LG, Barnes DM, Fentiman IS, Griffin BE (1995) Epstein-Barr virus in epithelial cell tumors: a breast cancer study. Cancer Res 55: 39-45
34. Lamy PJ, Nanni I, Fina F, Bibeau F, Romain S, Dussert C, Penault Llorca F, Grenier J, Ouafik LH, Martin PM (2006) Reliability and discriminant validity of HER2 gene quantification and chromosome 17 aneusomy analysis by real-time PCR in primary breast cancer. Int J Biol Markers 21: 20-29
35. Lespagnard L, Cochaux P, Larsimont D, Degeyter M, Velu T, Heimann R (1995) Absence of Epstein-Barr virus in medullary carcinoma of the breast as demonstrated by immunophenotyping, in situ hybridization and polymerase chain reaction. Am J Clin Pathol 103: 449-452
36. Luqmani Y, Shousha S (1995) Presence of Epstein-Barr virus in breast carcinoma. Int J Oncol 6: 899-903
37. McCall SA, Lichy JH, Bijwaard KE, Aguilera NS, Chu WS, Taubenberger JK (2001) Epstein-Barr virus detection in ductal carcinoma of the breast. J Natl Cancer Inst 93: 148-150
38. McGuire WL, Clark GM, Dressler LG, Owens MA (1986) Role of steroid hormone receptors as prognostic factors in primary breast cancer. NCI Monogr 1: 19-23
39. Murray PG, Lissauer D, Junying J, Davies G, Moore S, Bell A, Timms J, Rowlands D, McConkey C, Reynolds GM, Ghataura S, England D, Caroll R, Young LS (2003) Reactivity with a monoclonal antibody to Epstein-Barr virus (EBV) nuclear antigen 1 defines a subset of aggressive breast cancers in the absence of the EBV genome. Cancer Res 63: 2338-2343
40. Nandi S, Guzman RC, Yang J (1995) Hormones and mammary carcinogenesis in mice, rats, and humans: a unifying hypothesis. Proc Natl Acad Sci USA 92: 3650-3657
41. Perkins RS, Sahm K, Marando C, Dickson-Witmer D, Pahnke GR, Mitchell M, Petrelli NJ, Berkowitz IM, Soteropoulos P, Aris VM, Dunn SP, Krueger LJ (2006) Analysis of Epstein-Barr virus reservoirs in paired blood and breast cancer primary biopsy specimens by real time PCR. Breast Cancer Res 8: R70
42. Perrigoue JG, den Boon JA, Friedl A, Newton MA, Ahlquist P, Sugden B (2005) Lack of association between EBV and breast carcinoma. Cancer Epidemiol Biomarkers Prev 14: 809-814
43. Preciado MV, Chabay PA, De Matteo EN, Gonzalez P, Grinstein S, Actis A, Gass HD (2005) Epstein-Barr virus in breast carcinoma in Argentina. Arch Pathol Lab Med 129: 377-381
44. Révillion F, Bonneterre J, Peyrat JP (1998) ERBB2 oncogene in human breast cancer and its clinical significance. Eur J Cancer 34: 791-808
45. Richardson AK, Cox B, McCredie MR, Dite GS, Chang JH, Gertig DM, Southey MC, Giles GG, Hopper JL (2004) Cytomegalovirus, Epstein-Barr virus and risk of breast cancer before age 40 years: a case-control study. Br J Cancer 90: 2149-2152
46. Romain S, Bendahl PO, Guirou O, Malmström P, Martin PM, Fernö M (2001) DNA-synthesizing enzymes in breast cancer (thymidine kinase, thymidylate synthaseand thymidylate kinase): association with flow cytometric S-phase fraction and relative prognostic importance in node-negative premenopausal patients. Int J Cancer 95: 56-61
47. Romain S, Christensen IJ, Chinot O, Balslev I, Rose C, Martin PM, Thorpe SM (1995) Prognostic value of cytosolic thymidine kinase activity as a marker of proliferation in breast cancer. Int J Cancer 61: 7-12
48. Romain S, Spyratos F, Descotes F, Daver A, Rostaing-Puissant B, Bougnoux P, Colonna M, Bolla M, Martin PM (2000) Prognostic of DNA-synthesizing enzyme activities (thymidine kinase and thymidylate synthase) in 908 T1-T2, N0-N1, M0 breast cancers: a retrospective multicenter study. Int J Cancer 87: 860-868
49. Romain S, Spyratos F, Guirou O, Deytieux S, Chinot O, Martin PM (1994) Technical evaluation of thymidine kinase assay in cytosols from breast cancers. EORTC Receptor Study Group Report. Eur J Cancer 30A: 2163-2165
50. Rose C, Thorpe SM, Andersen KW, Pedersen BV, Mouridsen HT, Blichert-Toft M, Rasmussen BB (1985) Beneficial effect of adjuvant tamoxifen therapy in primary breast cancer patients with high oestrogen receptor values. Lancet 1: 16-19
51. Sambrook J, Fritsch EF, Maniatis T (1982) Molecular cloning: a laboratory manual. Harbor Laboratory: Cold Spring
52. Satoh Y, Takasaka N, Hoshikawa Y, Osaki M, Ohfuji S, Ito H, Kaibara N, Kurata T, Sairenji T (1998) Pretreatment with restriction enzyme or bovine serum albumin for effective PCR amplification of Epstein-Barr virus DNA in DNA extracted from paraffin-embedded gastric carcinoma tissue. J Clin Microbiol 36: 3423-3425
53. Thorne LB, Ryan JL, Elmore SH, Glaser SL, Gulley ML (2005) Real-time PCR measures Epstein-Barr virus DNA in archival breast adenocarcino-mas. Diagn Mol Pathol 14: 29-33
54. Trabelsi A, Rammeh S, Stita W, Mokni M, Mourou A, Korbi S (2008) Detection of Epstein-Barr virus in breast cancers with lymphoid stroma. Ann Biol Clin 66: 59-62
55. Tsai JH, Hsu CS, Tsai CH, Su JM, Liu YT, Cheng MH, Wei JC, Chen FL, Yang CC (2007) Relationship between viral factors, axillary lymph node status and survival in breast cancer. J Cancer Res Clin Oncol 133: 13-21
56. Williams C, Pontén F, Moberg C, Söderkvist P, Uhlén M, Pontén J, Sitbon G, Lundeberg J (1999) A high frequency of sequence alterations is due to formalin fixation of archival specimens. Am J Pathol 155: 1467-1471
57. Yamauchi H, Stearns V, Hayes DF (2001) When is a tumor marker ready for prime time? A case study of c-erbB-2 as a predictive factor in breast cancer. J Clin Oncol 19: 2334-2356
58. Yasui Y, Potter JD, Stanford JL, Rossing MA, Winget MD, Bronner M, Daling J (2001) Breast cancer risk and 'delayed' primary Epstein-Barr virus infection. Cancer Epidemiol Biomarkers Prev 10: 9-16 (Pubitemid 32106039)
59. Yuan J, Cahir-McFarland E, Zhao B, Kieff E (2006) Virus and cell RNAs expressed during Epstein-Barr virus replication. J Virol 80: 2548-2565
60. Zur Hausen H (1991) Viruses in human cancers. Science 254: 1167-1173
61. Zur Hausen H (2009) The search for infectious causes of human cancers: where and why. Virology 392: 1-10