An epidemiological and molecular study of the relationship between smoking, risk of nasopharyngeal carcinoma, and epsteinbarr virus activation

Journal of the National Cancer Institute

Volumn 104, Issue 18, 2012, Pages 1396-1410

  Xu, Feng Hua ^a,b   Xiong, Dan ^a   Xu, Ya Fei ^a   Cao, Su Mei ^a   Xue, Wen Qiong ^a   Qin, Hai De ^a   Liu, Wen Sheng ^a   Cao, Jing Yan ^a   Zhang, Ying ^a   Feng, Qi Sheng ^a   Chen, Li Zhen ^b   Li, Man Zhi ^a   Liu, Zhi Wei ^a   Liu, Qing ^a   Hong, Ming Huang ^a   Shugart, Yin Yao ^c   Zeng, Yi Xin ^a   Zeng, Mu Sheng ^a   Jia, Wei Hua ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BFRF3 GENE; CANCER RISK; CANCER STAGING; CHINA; CIGARETTE SMOKING; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE; GENE EXPRESSION; GP350 GENE; HUMAN; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; NASOPHARYNX CARCINOMA; PRIORITY JOURNAL; RTA GENE; SMOKING; VIRUS ACTIVATION; ZTA GENE;

ADULT; AGED; ANTIBODIES, VIRAL; ASIAN CONTINENTAL ANCESTRY GROUP; CASE-CONTROL STUDIES; CELL LINE, TUMOR; CHINA; DOSE-RESPONSE RELATIONSHIP, DRUG; EPSTEIN-BARR VIRUS INFECTIONS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; FOOD HABITS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNOGLOBULIN A; INCIDENCE; LOGISTIC MODELS; LUCIFERASES; MALE; MIDDLE AGED; NASOPHARYNGEAL NEOPLASMS; ODDS RATIO; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; SMOKING; TRANS-ACTIVATORS; TRANSFECTION; VIRUS ACTIVATION;

EID: 84866644742     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djs320     Document Type: Article

References (83)

1. Yu MC, Yuan JM. Epidemiology of nasopharyngeal carcinoma. Semin Cancer Biol. 2002;12(6):421-429.
2. Ou SH, Zell JA, Ziogas A, Anton-Culver H. Epidemiology of nasopharyngeal carcinoma in the United States: improved survival of Chinese patients within the keratinizing squamous cell carcinoma histology. Ann Oncol. 2007;18(1):29-35.
3. Busson P, Ooka T, Corbex M. Nasopharyngeal carcinomas and Epstein-Barr virus: from epidemiology and detection to therapy. Med Sci (Paris). 2004;20(4):453-457.
4. Ng WT, Choi CW, Lee MC, Chan SH, Yau TK, Lee AW. Familial nasopharyngeal carcinoma in Hong Kong: epidemiology and implication in screening. Fam Cancer. 2009;8(2):103-108.
5. Takeshita H, Furukawa M, Fujieda S, et al. Epidemiological research into nasopharyngeal carcinoma in the Chubu region of Japan. Auris Nasus Larynx. 1999;26(3):277-286.
6. Pattle SB, Farrell PJ. The role of Epstein-Barr virus in cancer. Expert Opin Biol Ther. 2006;6(11):1193-1205.
7. Raab-Traub N. Epstein-Barr virus in the pathogenesis of NPC. Semin Cancer Biol. 2002;12(6):431-441.
8. Hsu WL, Chen JY, Chien YC, et al. Independent effect of EBV and cigarette smoking on nasopharyngeal carcinoma: a 20-year follow-up study on 9,622 males without family history in Taiwan. Cancer Epidemiol Biomarkers Prev. 2009;18(4):1218-1226.
9. Chien YC, Chen JY, Liu MY, et al. Serologic markers of Epstein-Barr virus infection and nasopharyngeal carcinoma in Taiwanese men. N Engl J Med. 2001;345(26):1877-1882.
10. Zeng Y, Zhong JM, Li LY, et al. Follow-up studies on Epstein-Barr virus IgA/VCA antibody-positive persons in Zangwu County, China. Intervirology. 1983;20(4):190-194.
11. Zeng Y, Zhang LG, Wu YC, et al. Prospective studies on nasopharyngeal carcinoma in Epstein-Barr virus IgA/VCA antibody-positive persons in Wuzhou City, China. Int J Cancer. 1985;36(5):545-547.
12. Zong YS, Sham JS, Ng MH, et al. Immunoglobulin A against viral capsid antigen of Epstein-Barr virus and indirect mirror examination of the nasopharynx in the detection of asymptomatic nasopharyngeal carcinoma. Cancer. 1992;69(1):3-7.
13. Joab I, Triki H, de Saint Martin J, Perricaudet M, Nicolas JC. Detection of anti-Epstein-Barr virus trans-activator (ZEBRA) antibodies in sera from patients with human immunodeficiency virus. J Infect Dis. 1991;163(1):53-56.
14. Tedeschi R, Pin E, Martorelli D, et al. Serum antibody response to lytic and latent Epstein-Barr virus antigens in undifferentiated nasopharyngeal carcinoma patients from an area of nonendemicity. Clin Vaccine Immunol. 2007;14(4):435-441.
15. Rickinson AB, Kieff E. Epstein-Barr virus. In: Knipe DM, Howley PM, eds. Field's Virology. 4th ed. Philadelphia, PA: Lippincott, Williams and Wilkins; 2001:2575-2627.
16. Feng P, Ren EC, Liu D, Chan SH, Hu H. Expression of Epstein-Barr virus lytic gene BRLF1 in nasopharyngeal carcinoma: potential use in diagnosis. J Gen Virol. 2000;81(pt 10):2417-2423.
17. Pepperl S, Benninger-D?ing G, Modrow S, Wolf H, Jilg W. Immediate-early transactivator Rta of Epstein-Barr virus (EBV) shows multiple epitopes recognized by EBV-specific cytotoxic T lymphocytes. J Virol. 1998;72(11):8644-8649.
18. zur Hausen H, O'Neill FJ, Freese UK, Hecker E. Persisting oncogenic herpesvirus induced by the tumour promotor TPA. Nature. 1978; 272(5651):373-375.
19. Fang CY, Lee CH, Wu CC, et al. Recurrent chemical reactivations of EBV promotes genome instability and enhances tumor progression of nasopharyngeal carcinoma cells. Int J Cancer. 2009;124(9):2016-2025.
20. Jiang JH, Wang N, Li A, et al. Hypoxia can contribute to the induction of the Epstein-Barr virus (EBV) lytic cycle. J Clin Virol. 2006;37(2):98-103.
21. Luka J, Kallin B, Klein G. Induction of the Epstein-Barr virus (EBV) cycle in latently infected cells by n-butyrate. Virology. 1979;94(1):228-231.
22. Yoshida M, Kijima M, Akita M, Beppu T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem. 1990;265(28):17174-17179.
23. Shao YM, Poirier S, Ohshima H, et al. Epstein-Barr virus activation in Raji cells by extracts of preserved food from high risk areas for nasopharyngeal carcinoma. Carcinogenesis. 1988;9(8):1455-1457.
24. Zeng Y, Zhong JM, Ye SQ, et al. Screening of Epstein-Barr virus early antigen expression inducers from Chinese medicinal herbs and plants. Biomed Environ Sci. 1994;7(1):50-55.
25. Liu MY, Chang YL, Ma J, et al. Evaluation of multiple antibodies to Epstein-Barr virus as markers for detecting patients with nasopharyngeal carcinoma. J Med Virol. 1997;52(3):262-269.
26. Lo YM, Chan LY, Lo KW, et al. Quantitative analysis of cell-free Epstein-Barr virus DNA in plasma of patients with nasopharyngeal carcinoma. Cancer Res. 1999;59(6):1188-1191.
27. Tong JH, Lo KW, Au FW, Huang DP, To KF. Re: discrete alterations in the BZLF1 promoter in tumor and non-tumor-associated Epstein-Barr virus. J Natl Cancer Inst. 2003;95(13):1008-1009; author reply 1009.
28. Chang ET, Adami HO. The enigmatic epidemiology of nasopharyngeal carcinoma. Cancer Epidemiol Biomarkers Prev. 2006;15(10):1765-1777.
29. Ren ZF, Liu WS, Qin HD, et al. Effect of family history of cancers and environmental factors on risk of nasopharyngeal carcinoma in Guangdong, China. Cancer Epidemiol. 2010;34(4):419-424.
30. Jia WH, Luo XY, Feng BJ, et al. Traditional Cantonese diet and nasopharyngeal carcinoma risk: a large-scale case-control study in Guangdong, China. BMC Cancer. 2010;10:446. http://www.biomedcentral. com/1471-2407/10/446. Accessed May 26, 2012.
31. Ruan HL, Xu FH, Liu WS, et al. Alcohol and tea consumption in relation to the risk of nasopharyngeal carcinoma in Guangdong, China. Front Med China. 2010;4(4):448-456.
32. Arizona Cancer Center. Questionnaires. http://www.azcc.arizona.edu/ research/shared-services/bmss/questionnaires. Accessed May 26, 2012.
33. European Monitoring Centre for Drugs and Drug Addiction. Lifetime drinking history. http://www.emcdda.europa.eu/html.cfm/index4163EN. html. Accessed May 26, 2012.
34. Centers for Disease Control and Prevention. Alcohol. http://www.cdc.gov/ alcohol/faqs.htm. Accessed May 26, 2012.
35. Qin HD, Jia WH, Zhang LL, et al. Elevated Epstein-Barr virus seroreactivity among unaffected members of families with nasopharyngeal carcinoma. J Med Virol. 2011;83(10):1792-1798.
36. Shen GP, Pan QH, Hong MH, et al. Human genetic variants of homologous recombination repair genes first found to be associated with Epstein-Barr virus antibody titers in healthy Cantonese. Int J Cancer. 2011;129(6):1459-1466.
37. Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt's lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J Virol. 1994;68(9):6069-6073.
38. Shimizu N, Yoshiyama H, Takada K. Clonal propagation of Epstein-Barr virus (EBV) recombinants in EBV-negative Akata cells. J Virol. 1996;70(10):7260-7263.
39. Lan K, Verma SC, Murakami M, Bajaj B, Robertson ES. Epstein-Barr virus (EBV): infection, propagation, quantitation, and storage. Curr Protoc Microbiol. 2007;Chapter 14:Unit 14E.2.
40. Song LB, Zeng MS, Liao WT, et al. Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells. Cancer Res. 2006;66(12):6225-6232.
41. Song LB, Li J, Liao WT, et al. The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest. 2009;119(12):3626-3636.
42. Chang LK, Liu ST. Activation of the BRLF1 promoter and lytic cycle of Epstein-Barr virus by histone acetylation. Nucleic Acids Res. 2000;28(20):3918-3925.
43. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989:142-152.
44. Rothman KJ. The estimation of synergy or antagonism. Am J Epidemiol. 1976;103(5):506-511.
45. Liu Y, Huang Q, Liu W, et al. Establishment of VCA and EBNA1 IgA-based combination by enzyme-linked immunosorbent assay as preferred screening method for nasopharyngeal carcinoma: a two-stage design with a preliminary performance study and a mass screening in southern China. Int J Cancer. 2012;131(2):406-416.
46. Skol AD, Scott LJ, Abecasis GR, Boehnke M. Joint analysis is more efficient than replication-based analysis for two-stage genome-wide association studies. Nat Genet. 2006;38(2):209-213.
47. Gu D, Kelly TN, Wu X, et al. Mortality attributable to smoking in China. N Engl J Med. 2009;360(2):150-159.
48. Tyczynski JE, Bray F, Parkin DM. Lung cancer in Europe in 2000: epidemiology, prevention, and early detection. Lancet Oncol. 2003;4(1):45-55.
49. Yuan J, Ma J, Zheng H, et al. Overexpression of OLC1, cigarette smoke, and human lung tumorigenesis. J Natl Cancer Inst. 2008;100(22):1592-1605.
50. Haiman CA, Stram DO, Wilkens LR, et al. Ethnic and racial differences in the smoking-related risk of lung cancer. N Engl J Med. 2006;354(4):333-342.
51. Jee SH, Ohrr H, Sull JW, Samet JM. Cigarette smoking, alcohol drinking, hepatitis B, and risk for hepatocellular carcinoma in Korea. J Natl Cancer Inst. 2004;96(24):1851-1856.
52. Giovannucci E, Rimm EB, Stampfer MJ, et al. A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. men. J Natl Cancer Inst. 1994;86(3):183-191.
53. Brennan JA, Boyle JO, Koch WM, et al. Association between cigarette smoking and mutation of the p53 gene in squamous-cell carcinoma of the head and neck. N Engl J Med. 1995;332(11):712-717.
54. Liu X, Togo S, Al-Mugotir M, et al. NF-kappaB mediates the survival of human bronchial epithelial cells exposed to cigarette smoke extract. Respir Res. 2008;9:66. http://respiratory-research.com/content/9/1/66. Accessed May 26, 2012.
55. Vaughan TL, Shapiro JA, Burt RD, et al. Nasopharyngeal cancer in a low-risk population: defining risk factors by histological type. Cancer Epidemiol Biomarkers Prev. 1996;5(8):587-593.
56. Friborg JT, Yuan JM, Wang R, Koh WP, Lee HP, Yu MC. A prospective study of tobacco and alcohol use as risk factors for pharyngeal carcinomas in Singapore Chinese. Cancer. 2007;109(6):1183-1191.
57. West S, Hildesheim A, Dosemeci M. Non-viral risk factors for nasopharyngeal carcinoma in the Philippines: results from a case-control study. Int J Cancer. 1993;55(5):722-727.
58. Cheng YJ, Hildesheim A, Hsu MM, et al. Cigarette smoking, alcohol consumption and risk of nasopharyngeal carcinoma in Taiwan. Cancer Causes Control. 1999;10(3):201-207.
59. Chow WH, McLaughlin JK, Hrubec Z, Nam JM, Blot WJ. Tobacco use and nasopharyngeal carcinoma in a cohort of US veterans. Int J Cancer. 1993;55(4):538-540.
60. Yuan JM, Wang XL, Xiang YB, Gao YT, Ross RK, Yu MC. Non-dietary risk factors for nasopharyngeal carcinoma in Shanghai, China. Int J Cancer. 2000;85(3):364-369.
61. Zhu K, Levine RS, Brann EA, Hall HI, Caplan LS, Gnepp DR. Case-control study evaluating the homogeneity and heterogeneity of risk factors between sinonasal and nasopharyngeal cancers. Int J Cancer. 2002;99(1):119-123.
62. Shao JY, Li YH, Gao HY, et al. Comparison of plasma Epstein-Barr virus (EBV) DNA levels and serum EBV immunoglobulin A/virus capsid antigen antibody titers in patients with nasopharyngeal carcinoma. Cancer. 2004;100(6):1162-1170.
63. Chen CJ, Liang KY, Chang YS, et al. Multiple risk factors of nasopharyngeal carcinoma: Epstein-Barr virus, malarial infection, cigarette smoking and familial tendency. Anticancer Res. 1990;10(2B):547-553.
64. Nam JM, McLaughlin JK, Blot WJ. Cigarette smoking, alcohol, and nasopharyngeal carcinoma: a case-control study among U.S. whites. J Natl Cancer Inst. 1992;84(8):619-622.
65. Yu MC, Garabrant DH, Huang TB, Henderson BE. Occupational and other non-dietary risk factors for nasopharyngeal carcinoma in Guangzhou, China. Int J Cancer. 1990;45(6):1033-1039.
66. Lin TM, Chen KP, Lin CC, et al. Retrospective study on nasopharyngeal carcinoma. J Natl Cancer Inst. 1973;51(5):1403-1408.
67. Hecht SS. Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention. Lancet Oncol. 2002;3(8):461-469.
68. Takahashi H, Ogata H, Nishigaki R, Broide DH, Karin M. Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta-and JNK1-dependent inflammation. Cancer Cell. 2010;17(1):89-97.
69. Gulsvik A, Fagerhoi MK. Smoking and immunoglobulin levels. Lancet. 1979;1(8113):449.
70. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun. 2010;34(3):J258-J265.
71. Abdulamir AS, Hafidh RR, Abdulmuhaimen N, et al. The distinctive profile of risk factors of nasopharyngeal carcinoma in comparison with other head and neck cancer types. BMC Public Health. 2008;8:400. http://www. biomedcentral.com/1471-2458/8/400. Accessed May 26, 2012.
72. Chang ET, Zheng T, Lennette ET, et al. Heterogeneity of risk factors and antibody profiles in Epstein-Barr virus genome-positive and-negative Hodgkin lymphoma. J Infect Dis. 2004;189(12):2271-2281.
73. Halprin J, Scott AL, Jacobson L, et al. Enzyme-linked immunosorbent assay of antibodies to Epstein-Barr virus nuclear and early antigens in patients with infectious mononucleosis and nasopharyngeal carcinoma. Ann Intern Med. 1986;104(3):331-337.
74. Kudoh A, Fujita M, Kiyono T, et al. Reactivation of lytic replication from B cells latently infected with Epstein-Barr virus occurs with high S-phase cyclin-dependent kinase activity while inhibiting cellular DNA replication. J Virol. 2003;77(2):851-861.
75. Lu CC, Jeng YY, Tsai CH, et al. Genome-wide transcription program and expression of the Rta responsive gene of Epstein-Barr virus. Virology. 2006;345(2):358-372.
76. Chang Y, Tung CH, Huang YT, Lu J, Chen JY, Tsai CH. Requirement for cell-to-cell contact in Epstein-Barr virus infection of nasopharyngeal carcinoma cells and keratinocytes. J Virol. 1999;73(10):8857-8866.
77. Imai S, Nishikawa J, Takada K. Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells. J Virol. 1998;72(5):4371-4378.
78. Tsang CM, Zhang G, Seto E, et al. Epstein-Barr virus infection in immortalized nasopharyngeal epithelial cells: regulation of infection and phenotypic characterization. Int J Cancer. 2010;127(7):1570-1583.
79. Mochanko K, Fejes M, Breazavscek DM, Suarez A, Bachmann AE. The relation between Epstein-Barr virus antibodies and clinical symptomatology and immunodeficiency in patients with Hodgkin's disease. Cancer. 1979;44(6):2065-2070.
80. Fan H, Nicholls J, Chua D, et al. Laboratory markers of tumor burden in nasopharyngeal carcinoma: a comparison of viral load and serologic tests for Epstein-Barr virus. Int J Cancer. 2004;112(6):1036-1041.
81. Tan EL, Selvaratnam G, Kananathan R, et al. Quantification of Epstein-Barr virus DNA load, interleukin-6, interleukin-10, transforming growth factor-beta1 and stem cell factor in plasma of patients with nasopharyngeal carcinoma. BMC Cancer. 2006;6:227. http://www.biomedcentral. com/1471-2407/6/227. Accessed May 26, 2012.
82. Xu J, Menezes J, Prasad U, Ahmad A. Elevated serum levels of transforming growth factor beta1 in Epstein-Barr virus-associated nasopharyngeal carcinoma patients. Int J Cancer. 1999;84(4):396-399.
83. Hong GK, Gulley ML, Feng WH, Delecluse HJ, Holley-Guthrie E, Kenney SC. Epstein-Barr virus lytic infection contributes to lymphoproliferative disease in a SCID mouse model. J Virol. 2005;79(22):13993-14003.