The oncogenic potential of human cytomegalovirus and breast cancer

Frontiers in Oncology

Volumn 4 AUG, Issue , 2014, Pages

  Herbein, Georges ^a   Kumar, Amit ^a  

^a Department of Virology and Department of Pathogens and Inflammation UPRES EA4266 SFR FED 4234 CHRU Besançon University of Franche Comte ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPECITABINE; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; SORAFENIB; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; BREAST MILK; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNOCOMPROMISED PATIENT; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MONOCYTE; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PREVALENCE; REAL TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; VIRAL TROPISM;

EID: 84906226880     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00230     Document Type: Article

References (89)

1. Sørlie 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) 98:10869-74.
2. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature (2012) 490:61-70. doi: 10.1038/nature11412.
3. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol (2009) 27:1160-7. doi: 10.1200/JCO.2008.18.1370.
4. Ban KA, Godellas CV. Epidemiology of Breast Cancer. Surg Oncol Clin N Am (2014) 23:409-422. doi: 10.1016/j.soc.2014.03.011.
5. Zur Hausen H. The search for infectious causes of human cancers: where and why. Virology (2009) 392:1-10. doi: 10.1016/j.virol.2009.06.001.
6. Alibek K, Kakpenova A, Mussabekova A, Sypabekova M, Karatayeva N. Role of viruses in the development of breast cancer. Infect Agent Cancer (2013) 8:32.
7. Coaquette A, Bourgeois A, Dirand C, Varin A, Chen W, Herbein G. Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients. Clin Infect Dis (2004) 39:155-61.
8. Britt W. Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol (2008) 325:417-70.
9. Michaelis M, Doerr HW, Cinatl J. The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia (2009) 11:1-9.
10. Soroceanu L, Cobbs CS. Is HCMV a tumor promoter? Virus Res. (2011) 157:193-203. doi: 10.1016/j.virusres.2010.10.026.
11. Geder KM, Lausch R, O'Neill F, Rapp F. Oncogenic transformation of human embryo lung cells by human cytomegalovirus. Science (1976) 192:1134-7.
12. Clanton DJ, Jariwalla RJ, Kress C, Rosenthal LJ. Neoplastic transformation by a cloned human cytomegalovirus DNA fragment uniquely homologous to one of the transforming regions of herpes simplex virus type 2. Proc Natl Acad Sci U S A (1983) 80:3826-30.
13. Lepiller Q, Abbas W, Kumar A, Tripathy MK, Herbein G. HCMV activates the IL-6-JAK-STAT3 axis in HepG2 cells and primary human hepatocytes. PLoS One (2013) 8:e59591. doi: 10.1371/journal.pone.0059591.
14. Moore DH, Charney J, Kramarsky B, Lasfargues EY, Sarkar NH, Brennan MJ, et al. Search for a human breast cancer virus. Nature (1971) 229:611-4.
15. Gumus M, Yumuk PF, Salepci T, Aliustaoglu M, Dane F, Ekenel M, et al. HPV DNA frequency and subset analysis in human breast cancer patients' normal and tumoral tissue samples. J Exp Clin Cancer Res (2006) 25:515-21.
16. Wang T, Zeng X, Li W, Zhu H, Wang G, Liu X, et al. Detection and analysis of human papillomavirus (HPV) DNA in breast cancer patients by an effective method of HPV capture. PLoS One (2014) 9:e90343. doi: 10.1371/journal.pone.0090343.
17. Grinstein S, Preciado MV, Gattuso P, Chabay PA, Warren WH, De Matteo E, et al. Demonstration of Epstein-Barr virus in carcinomas of various sites. Cancer Res (2002) 62:4876-8.
18. Wang-Johanning F, Frost AR, Johanning GL, Khazaeli MB, LoBuglio AF, Shaw DR, et al. Expression of human endogenous retrovirus k envelope transcripts in human breast cancer. Clin Cancer Res (2001) 7:1553-60.
19. Hachana M, Amara K, Ziadi S, Gacem RB, Korbi S, Trimeche M. Investigation of human JC and BK polyomaviruses in breast carcinomas. Breast Cancer Res Treat (2012) 133:969-77. doi: 10.1007/s10549-011-1876-5.
20. Richardson A. Is breast cancer caused by late exposure to a common virus? Med Hypotheses (1997) 48:491-7.
21. Cox B, Richardson A, Graham P, Gislefoss RE, Jellum E, Rollag H. Breast cancer, cytomegalovirus and Epstein-Barr virus: a nested case-control study. Br J Cancer (2010) 102:1665-9. doi: 10.1038/sj.bjc.6605675.
22. Asanuma H, Numazaki K, Nagata N, Hotsubo T, Horino K, Chiba S. Role of milk whey in the transmission of human cytomegalovirus infection by breast milk. Microbiol Immunol (1996) 40:201-4.
23. Hamprecht K, Maschmann J, Vochem M, Dietz K, Speer CP, Jahn G. Epidemiology of transmission of cytomegalovirus from mother to preterm infant by breastfeeding. Lancet (2001) 357:513-8.
24. Tsai JH, Tsai CH, Cheng MH, Lin SJ, Xu FL, Yang CC. Association of viral factors with non-familial breast cancer in Taiwan by comparison with non-cancerous, fibroadenoma, and thyroid tumor tissues. J Med Virol (2005) 75:276-81.
25. Harkins LE, Matlaf LA, Soroceanu L, Klemm K, Britt WJ, Wang W, et al. Detection of human cytomegalovirus in normal and neoplastic breast epithelium. Herpesviridae (2010) 1:8. doi: 10.1186/2042-4280-1-8.
26. Taher C, de Boniface J, Mohammad AA, Religa P, Hartman J, Yaiw KC, et al. High prevalence of human cytomegalovirus proteins and nucleic acids in primary breast cancer and metastatic sentinel lymph nodes. PLoS One (2013) 8:e56795. doi: 10.1371/journal.pone.0056795.
27. Antonsson A, Bialasiewicz S, Rockett RJ, Jacob K, Bennett IC, Sloots TP. Exploring the prevalence of ten polyomaviruses and two herpes viruses in breast cancer. PLoS One (2012) 7:e39842. doi: 10.1371/journal.pone.0039842.
28. Utrera-Barillas D, Valdez-Salazar HA, Gómez-Rangel D, Alvarado-Cabrero I, Aguilera P, Gómez-Delgado A, Ruiz-Tachiquin ME. Is human cytomegalovirus associated with breast cancer progression? Infect Agent Cancer (2013) 8:12. doi: 10.1186/1750-9378-8-12.
29. Lazzeroni M, Serrano D. Potential use of vaccines in the primary prevention of breast cancer in high-risk patients. Breast Care (Basel) (2012) 7:281-7. doi: 10.1159/000342167.
30. Khan KA, Coaquette A, Davrinche C, Herbein G. Bcl-3-regulated transcription from major immediate-early promoter of human cytomegalovirus in monocyte-derived macrophages. J Immunol (2009) 182:7784-94. doi: 10.4049/jimmunol.0803800.
31. Wang D, Shenk T. Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci USA (2005) 102(50):18153-8.
32. Belzile JP, Stark TJ, Yeo GW, Spector DH. Human cytomegalovirus infection of human embryonic stem cell-derived primitive neural stem cells is restricted at several steps but leads to the persistence of viral DNA. J Virol (2014) 88:4021-39. doi: 10.1128/JVI.03492-13.
33. Chan G, Nogalski MT, Yurochko AD. Activation of EGFR on monocytes is required for human cytomegalovirus entry and mediates cellular motility. Proc Natl Acad Sci USA (2009) 106:22369-74. doi: 10.1073/pnas.0908787106.
34. Hargett, Shenk TE. Experimental human cytomegalovirus latency in CD14+ monocytes. Proc Natl Acad Sci USA (2010) 107(46):20039-44. doi: 10.1073/pnas.1014509107.
35. Chan G, Bivins-Smith ER, Smith MS, Yurochko AD. NF-kappaB and phosphatidylinositol 3-kinase activity mediates the HCMV-induced atypical M1/M2 polarization of monocytes. Virus Res (2009) 144:329-33. doi: 10.1016/j.virusres.2009.04.026.
36. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell (2010) 140:883-99. doi: 10.1016/j.cell.2010.01.025.
37. Lepiller Q, Tripathy MK, Di Martino V, Kantelip B, Herbein G. Increased HCMV seroprevalence in patients with hepatocellular carcinoma. Virol J (2011) 8:485. doi: 10.1186/1743-422X-8-485.
38. El-Shinawi M, Mohamed HT, El-Ghonaimy EA, Tantawy M, Younis A, Schneider RJ, Mohamed MM. Human cytomegalovirus infection enhances NF-?B/p65 signaling in inflammatory breast cancer patients. PLoS One (2013) 8:e55755. doi: 10.1371/journal.pone.0055755.
39. Tang X. Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett (2013) 332:3-10. doi: 10.1016/j.canlet.2013.01.024.
40. Luo Y, Zhou H, Krueger J, Kaplan C, Lee SH, Dolman C, et al. Targeting tumorassociated macrophages as a novel strategy against breast cancer. J Clin Invest (2006) 116:2132-2141.
41. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, et al. Decoding human cytomegalovirus. Science (2012) 338:1088-93. doi: 10.1126/science.1227919.
42. Murphy E, Rigoutsos I, Shibuya T, Shenk TE. Reevaluation of human cytomegalovirus coding potential. Proc Natl Acad Sci U S A (2003) 100:13585-90.
43. Davison AJ, Dolan A, Akter P, Addison C, Dargan DJ, Alcendor DJ, et al. The human cytomegalovirus genome revisited: comparison with the chimpanzee cytomegalovirus genome. J Gen Virol (2003) 84:17-28.
44. Kalejta RF, Shenk T. Manipulation of the cell cycle by human cytomegalovirus. Front Biosci (2002) 7:d295-306.
45. Zhu H, Shen Y, Shenk T. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol (1995) 69:7960-70.
46. Speir E, Modali R, Huang ES, Leon MB, Shawl F, Finkel T, et al. Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science (1994) 265:391-4.
47. Bego MG, St Jeor S. Human cytomegalovirus infection of cells of hematopoietic origin: HCMV-induced immunosuppression, immune evasion, and latency. Exp Hematol (2006) 34:555-70.
48. Maussang D, Verzijl D, van Walsum M, Leurs R, Holl J, PleskoffO, et al. Human cytomegalovirus-encoded chemokine receptor US28 promotes tumorigenesis. Proc Natl Acad Sci U S A (2006) 103:13068-73.
49. Slinger E, Maussang D, Schreiber A, Siderius M, Rahbar A, Fraile-Ramos A, et al. HCMV-encoded chemokine receptor US28 mediates proliferative signaling through the IL-6-STAT3 axis. Sci Signal (2010) 3:ra58. doi: 10.1126/scisignal.2001180.
50. Shen Y, Zhu H, Shenk T. Human cytomagalovirus IE1 and IE2 proteins are mutagenic and mediate "hit-and-run" oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc Natl Acad Sci USA (1997) 94:3341-5.
51. Strååt K, Liu C, Rahbar A, Zhu Q, Liu L, Wolmer-Solberg N, et al. Activation of telomerase by human cytomegalovirus. J Natl Cancer Inst (2009) 101:488-97. doi: 10.1093/jnci/djp031.
52. Fortunato EA, Dell'Aquila ML, Spector DH. Specific chromosome 1 breaks induced by human cytomegalovirus. Proc Natl Acad Sci USA (2000) 97:853-8.
53. Siew VK, Duh CY, Wang SK. Human cytomegalovirus UL76 induces chromosome aberrations. J Biomed Sci (2009) 16:107. doi: 10.1186/1423-0127-16-107.
54. Michaelis M, Paulus C, Löschmann N, Dauth S, Stange E, Doerr HW, et al. The multi-targeted kinase inhibitor sorafenib inhibits human cytomegalovirus replication. Cell Mol Life Sci (2011) 68:1079-90. doi: 10.1007/s00018-010-0510-8.
55. Fumarola C, Caffarra C, La Monica S, Galetti M, Alfieri RR, Cavazzoni A, et al. Effects of sorafenib on energy metabolism in breast cancer cells: role of AMPKmTORC1 signaling. Breast Cancer Res Treat (2013) 141:67-78. doi: 10.1007/s10549-013-2668-x.
56. Baselga J, Segalla JG, Roché H, Del Giglio A, Pinczowski H, Ciruelos EM, et al. Sorafenib in combination with capecitabine: an oral regimen for patients with HER2-negative locally advanced or metastatic breast cancer. J Clin Oncol (2012) 30:1484-91. doi: 10.1200/JCO.2011.36.7771.
57. Baselga J, Costa F, Gomez H, Hudis CA, Rapoport B, Roche H, et al. A phase 3 trial comparing capecitabine in combination with sorafenib or placebo for treatment of locally advanced or metastatic HER2-negative breast cancer (the RESILIENCE study): study protocol for a randomized controlled trial. Trials (2013) 14:228. doi: 10.1186/1745-6215-14-228.
58. Diaz N, Minton S, Cox C, Bowman T, Gritsko T, Garcia R, et al. Activation of stat3 in primary tumors from high-risk breast cancer patients is associated with elevated levels of activated SRC and survivin expression. Clin Cancer Res (2006) 12:20-8.
59. Reitsma JM, Sato H, Nevels M, Terhune SS, Paulus C. Human cytomegalovirus IE1 protein disrupts interleukin-6 signaling by sequestering STAT3 in the nucleus. J Virol (2013) 87:10763-76. doi: 10.1128/JVI.01197-13.
60. Valle Oseguera CA, Spencer JV. cmvIL-10 stimulates the invasive potential of MDAMB- 231 breast cancer cells. PLoS One (2014) 9:e88708. doi: 10.1371/journal.pone.0088708.
61. Kotenko SV, Saccani S, Izotova LS, Mirochnitchenko OV, Pestka S. Human cytomegalovirus harbors its own unique IL-10 homolog (cmvIL-10). Proc Natl Acad Sci USA (2000) 97:1695-700.
62. Lin L, Hutzen B, Zuo M, Ball S, Deangelis S, Foust E, et al. Novel STAT3 phosphorylation inhibitors exhibit potent growth-suppressive activity in pancreatic and breast cancer cells. Cancer Res (2010) 70:2445-54. doi: 10.1158/0008-5472.CAN-09-2468.
63. Zhang X, Yue P, Page BD, Li T, Zhao W, Namanja AT, et al. Orally bioavailable smallmolecule inhibitor of transcription factor Stat3 regresses human breast and lung cancer xenografts. Proc Natl Acad Sci USA (2012) 109:9623-8. doi: 10.1073/pnas.1121606109.
64. Lauring J, Park BH, WolffAC. The phosphoinositide-3-kinase-Akt-mTOR pathway as a therapeutic target in breast cancer. J Natl Compr Canc Netw (2013) 11:670-8.
65. Yu Y, Alwine JC. Human cytomegalovirus major immediate-early proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylinositide 3'-OH kinase pathway and the cellular kinase Akt. J Virol (2002) 76:3731-8.
66. Kapoor A, He R, Venkatadri R, Forman M, Arav-Boger R. Wnt modulating agents inhibit human cytomegalovirus replication Antimicrob Agents Chemother (2013) 57:2761-7. doi: 10.1128/AAC.00029-13.
67. Angelova M, Zwezdaryk K, Ferris M, Shan B, Morris CA, Sullivan DE. Human cytomegalovirus infection dysregulates the canonical Wnt/ß-catenin signaling pathway. PLoS Pathog (2012) 8:e1002959. doi: 10.1371/journal.ppat.1002959.
68. Lamb R, Ablett MP, Spence K, Landberg G, Sims AH, Clarke RB. Wnt pathway activity in breast cancer sub-types and stem-like cells. PLoS One (2013) 8:e67811. doi: 10.1371/journal.pone.0067811.
69. Bao R, Christova T, Song S, Angers S, Yan X, Attisano L. Inhibition of tankyrases induces Axin stabilization and blocks Wnt signalling in breast cancer cells. PLoS One (2012) 7:e48670. doi: 10.1371/journal.pone.0048670.
70. Mazouni C, Fina F, Romain S, Ouafik L, Bonnier P, Brandone JM, et al. Epstein-Barr virus as a marker of biological aggressiveness in breast cancer. Br J Cancer (2011) 104:332-7. doi: 10.1038/sj.bjc.6606048.
71. Heng B, Glenn WK, Ye Y, Tran B, Delprado W, Lutze-Mann L, et al. Human papilloma virus is associated with breast cancer. Br J Cancer (2009) 101:1345-50. doi: 10.1038/sj.bjc.6605282.
72. Frega A, Lorenzon L, Bononi M, De Cesare A, Ciardi A, Lombardi D, et al. Evaluation of E6 and E7 mRNA expression in HPV DNA positive breast cancer. Eur J Gynaecol Oncol (2012) 33:164-7.
73. Ohba K, Ichiyama K, Yajima M, Gemma N, Nikaido M, Wu Q, et al. In vivo and in vitro studies suggest a possible involvement of HPV infection in the early stage of breast carcinogenesis via APOBEC3B induction. PLoS One (2014) 9:e97787. doi: 10.1371/journal.pone.0097787.
74. Hachana M, Trimeche M, Ziadi S, Amara K, Korbi S. Evidence for a role of the Simian Virus 40 in human breast carcinomas. Breast Cancer Res Treat (2009) 113:43-58. doi: 10.1007/s10549-008-9901-z.
75. Wang Y, Melana SM, Baker B, Bleiweiss I, Fernandez-Cobo M, Mandeli JF, et al. High prevalence of MMTV-like env gene sequences in gestational breast cancer. Med Oncol (2003) 20:233-6.
76. Melana SM, Nepomnaschy I, Hasa J, Djougarian A, Djougarian A, Holland JF, et al. Detection of human mammary tumor virus proteins in human breast cancer cells. J Virol Methods (2010) 163:157-61. doi: 10.1016/j.jviromet.2009.09.015.
77. Wang-Johanning F, Frost AR, Johanning GL, Khazaeli MB, LoBuglio AF, Shaw DR, et al. Expression of human endogenous retrovirus k envelope transcripts in human breast cancer. Clin Cancer Res (2001) 7:1553-60.
78. Golan M, Hizi A, Resau JH, Yaal-Hahoshen N, Reichman H, Keydar I, Tsarfaty I. Human endogenous retrovirus (HERV-K) reverse transcriptase as a breast cancer prognostic marker. Neoplasia (2008) 10:521-33.
79. Liu CY, Tseng LM, Su JC, Chang KC, Chu PY, Tai WT, et al. Novel sorafenib analogues induce apoptosis through SHP-1 dependent STAT3 inactivation in human breast cancer cells. Breast Cancer Res (2013) 15:R63.
80. Saura C, Bendell J, Jerusalem G, Su S, Ru Q, De Buck S, et al. Phase Ib study of Buparlisib plus Trastuzumab in patients with HER2-positive advanced or metastatic breast cancer that has progressed on Trastuzumab-based therapy. Clin Cancer Res (2014) 20:1935-45. doi: 10.1158/1078-0432.CCR-13-1070.
81. Smith MS, Bentz GL, Smith PM, Bivins ER, Yurochko AD. HCMV activates PI(3)K in monocytes and promotes monocyte motility and transendothelial migration in a PI(3)K-dependent manner. J Leukoc Biol. (2004) 76:65-76.
82. Serra V, Markman B, Scaltriti M, Eichhorn PJ, Valero V, Guzman M, et al. NVPBEZ235, a dual PI3K/mTOR inhibitor, prevents PI3K signaling and inhibits the growth of cancer cells with activating PI3K mutations. Cancer Res (2008) 68:8022-30. doi: 10.1158/0008-5472.
83. Sangai T, Akcakanat A, Chen H, Tarco E, Wu Y, Do KA, et al. Biomarkers of response to Akt inhibitor MK-2206 in breast cancer. Clin Cancer Res (2012) 18:5816-28. doi: 10.1158/1078-0432.CCR-12-1141.
84. Boyle KA, Pietropaolo RL, Compton T. Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol Cell Biol. 1999 May;19(5):3607-13. PMID:10207084.
85. Johnson RA, Huong SM, Huang ES. Activation of the mitogen-activated protein kinase p38 by human cytomegalovirus infection through two distinct pathways: a novel mechanism for activation of p38. J Virol (2000) 74:1158-67.
86. Rodems SM, Spector DH. Extracellular signal-regulated kinase activity is sustained early during human cytomegalovirus infection. J Virol (1998) 72:9173-80.
87. Reeves MB, Breidenstein A, Compton T. Human cytomegalovirus activation of ERK and myeloid cell leukemia-1 protein correlates with survival of latently infected cells. Proc Natl Acad Sci USA (2012) 109:588-93. doi: 10.1073/pnas.1114966108.
88. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res (2004) 64:7099-109.
89. Rinehart J, Adjei AA, Lorusso PM, Waterhouse D, Hecht JR, Natale RB, et al. Multicenter phase II study of the oral MEK inhibitor, CI-1040, in patients with advanced non-small-cell lung, breast, colon, and pancreatic cancer. J Clin Oncol (2004) 22:4456-62.