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Published in: BMC Infectious Diseases 1/2013

Open Access 01-12-2013 | Research article

Analysis of mutations in the E6 oncogene of human papillomavirus 16 in cervical cancer isolates from Moroccan women

Authors: Zineb Qmichou, Meriem Khyatti, Mohamed Berraho, My Mustapha Ennaji, Laila Benbacer, Chakib Nejjari, Noureddine Benjaafar, Abdellatif Benider, Mohammed Attaleb, Mohammed El Mzibri

Published in: BMC Infectious Diseases | Issue 1/2013

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Abstract

Background

Worldwide, cervical cancer is the second most common cancer in women. High-risk human papillomavirus (HPV) play a crucial role in the etiology of cervical cancer and the most prevalent genotype is HPV16. HPV 16 intratypic variants have been reported to differ in their prevalence, biological and biochemical properties. The present study was designed to analyze and identify HPV type 16 E6 variants among patients with cervical cancer in Morocco.

Methods

A total of 103 HPV16 positive samples were isolated from 129 cervical cancer cases, and variant status was subsequently determined by DNA sequencing of the E6 gene.

Results

Isolates from patients were grouped into the European (E), African (Af) and North-American (NA1) phylogenetic clusters with a high prevalence of E lineage (58.3%). The Af and NA1 variants were detected in 31.1% and 11.6% of the HPV16 positive specimens, respectively, whereas, only 3% of cases were prototype E350T. No European-Asian (EA), Asian (As) or Asian-American (AA) variants were observed in our HPV16-positive specimens. At the amino acid level, the most prevalent non-synonymous variants were L83V (T350G), H78Y (C335T), E113D (A442C), Q14D (C143G/G145T) and R10I (G132T), and were observed respectively in 65%, 41.8%, 38.8%, 30.1% and 23.3% of total samples.
Moreover, HPV16 European variants were mostly identified in younger women at early clinical diagnosis stages. Whereas, HPV16 Af variants were most likely associated with cervical cancer development in older women with pronounced aggressiveness.

Conclusion

This study suggests a predominance of E lineage strains among Moroccan HPV 16 isolates and raises the possibility that HPV16 variants have a preferential role in progression to malignancy and could be associated with the more aggressive nature of cervical cancer.
Literature
1.
go back to reference Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010, 127: 2893-2917. 10.1002/ijc.25516.CrossRefPubMed Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010, 127: 2893-2917. 10.1002/ijc.25516.CrossRefPubMed
2.
go back to reference Benider A, Bennani Othmani M, Harif M, Karkouri M, Quessar A, Sahraoui S, Sqali S: Registre des cancers de la région du grand Casablanca, année 2004. Edition. 2007, 73- Benider A, Bennani Othmani M, Harif M, Karkouri M, Quessar A, Sahraoui S, Sqali S: Registre des cancers de la région du grand Casablanca, année 2004. Edition. 2007, 73-
3.
go back to reference Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM: Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer. 2007, 121: 621-632. 10.1002/ijc.22527.CrossRefPubMed Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM: Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer. 2007, 121: 621-632. 10.1002/ijc.22527.CrossRefPubMed
4.
go back to reference Lalaoui K, El Mzibri M, Amrani M, Belabbas MA, Lazo PA: Human papillomavirus DNA in cervical lesions from Morocco and its implications for cancer control. Clin Microbiol Infect. 2003, 9: 144-148. 10.1046/j.1469-0691.2003.00494.x.CrossRefPubMed Lalaoui K, El Mzibri M, Amrani M, Belabbas MA, Lazo PA: Human papillomavirus DNA in cervical lesions from Morocco and its implications for cancer control. Clin Microbiol Infect. 2003, 9: 144-148. 10.1046/j.1469-0691.2003.00494.x.CrossRefPubMed
5.
go back to reference El Mzibri M, Amrani M, Khair MM, Attaleb M, Jaddi H, Ennaji MM, Khan B, Belabbas MA: Prevalence of human papilloma virus infection in malignant lesions of the uterine cervix in Morocco. World J Nucl Med. 2009, 8: 192-196. El Mzibri M, Amrani M, Khair MM, Attaleb M, Jaddi H, Ennaji MM, Khan B, Belabbas MA: Prevalence of human papilloma virus infection in malignant lesions of the uterine cervix in Morocco. World J Nucl Med. 2009, 8: 192-196.
6.
go back to reference Meftah El khair M, Ennaji MM, El kebbaj R, Ait Mhand R, Attaleb M, El Mzibri M: p53 Codon 72 polymorphism and risk of cervical carcinoma in Moroccan women. Med Oncol. 2010, 27: 861-866. 10.1007/s12032-009-9297-6.CrossRefPubMed Meftah El khair M, Ennaji MM, El kebbaj R, Ait Mhand R, Attaleb M, El Mzibri M: p53 Codon 72 polymorphism and risk of cervical carcinoma in Moroccan women. Med Oncol. 2010, 27: 861-866. 10.1007/s12032-009-9297-6.CrossRefPubMed
7.
go back to reference de Villiers E, Fauquet C, Broker TR, Bernard HU, zur Hausen H: Classification of papillomaviruses. Virology. 2004, 324: 17-27. 10.1016/j.virol.2004.03.033.CrossRefPubMed de Villiers E, Fauquet C, Broker TR, Bernard HU, zur Hausen H: Classification of papillomaviruses. Virology. 2004, 324: 17-27. 10.1016/j.virol.2004.03.033.CrossRefPubMed
8.
go back to reference Yamada T, Wheeler CM, Halpern AL, Stewart AC, Hildesheim A, Jenison SA: Human papillomavirus type 16 variant lineages in United States populations characterized by nucleotide sequence analysis of the E6, L2, and L1 coding segments. J Virol. 1995, 69: 7743-7753.PubMedPubMedCentral Yamada T, Wheeler CM, Halpern AL, Stewart AC, Hildesheim A, Jenison SA: Human papillomavirus type 16 variant lineages in United States populations characterized by nucleotide sequence analysis of the E6, L2, and L1 coding segments. J Virol. 1995, 69: 7743-7753.PubMedPubMedCentral
9.
go back to reference Zur Hausen H: Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer. 2002, 2: 342-350. 10.1038/nrc798.CrossRefPubMed Zur Hausen H: Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer. 2002, 2: 342-350. 10.1038/nrc798.CrossRefPubMed
10.
go back to reference Lizano M, Berumen J, Garcia-Carranca A: HPV-related carcinogenesis: basic concepts, viral types and variants. Arch Med Res. 2009, 40: 428-434. 10.1016/j.arcmed.2009.06.001.CrossRefPubMed Lizano M, Berumen J, Garcia-Carranca A: HPV-related carcinogenesis: basic concepts, viral types and variants. Arch Med Res. 2009, 40: 428-434. 10.1016/j.arcmed.2009.06.001.CrossRefPubMed
11.
go back to reference Kim MK, Kim HS, Kim SH, Oh JM, Han JY, Lim JM, Juhnn YS, Song YS: Human papillomavirus type 16 E5 oncoprotein as a new target for cervical cancer treatment. Biochem Pharmacol. 2010, 80: 1930-1935. 10.1016/j.bcp.2010.07.013.CrossRefPubMed Kim MK, Kim HS, Kim SH, Oh JM, Han JY, Lim JM, Juhnn YS, Song YS: Human papillomavirus type 16 E5 oncoprotein as a new target for cervical cancer treatment. Biochem Pharmacol. 2010, 80: 1930-1935. 10.1016/j.bcp.2010.07.013.CrossRefPubMed
12.
go back to reference Yamada T, Manos MM, Peto J, Greer CE, Munoz N, Bosch FX, Wheeler CM: Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. J Virol Methods. 1997, 71: 2463-2472. Yamada T, Manos MM, Peto J, Greer CE, Munoz N, Bosch FX, Wheeler CM: Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. J Virol Methods. 1997, 71: 2463-2472.
13.
go back to reference Huertas-Salgado A, Martin-Gamez DC, Moreno P, Murillo R, Bravo MM, Villa L, Molano M: E6 Molecular variants of human papillomavirus (HPV) type 16: an updated and unified criterion for clustering and nomenclature. Virology. 2011, 410: 201-215. 10.1016/j.virol.2010.10.039.CrossRefPubMed Huertas-Salgado A, Martin-Gamez DC, Moreno P, Murillo R, Bravo MM, Villa L, Molano M: E6 Molecular variants of human papillomavirus (HPV) type 16: an updated and unified criterion for clustering and nomenclature. Virology. 2011, 410: 201-215. 10.1016/j.virol.2010.10.039.CrossRefPubMed
14.
go back to reference Hildesheim A, Schiffman M, Bromley C, Wacholder S, Herrero R, Rodriguez A, Bratti MC, Sherman ME, Scarpidis U, Lin QQ, et al: Human papillomavirus type 16 variants and risk of cervical cancer. J Natl Cancer Inst. 2001, 93: 315-318. 10.1093/jnci/93.4.315.CrossRefPubMed Hildesheim A, Schiffman M, Bromley C, Wacholder S, Herrero R, Rodriguez A, Bratti MC, Sherman ME, Scarpidis U, Lin QQ, et al: Human papillomavirus type 16 variants and risk of cervical cancer. J Natl Cancer Inst. 2001, 93: 315-318. 10.1093/jnci/93.4.315.CrossRefPubMed
15.
go back to reference Xi LF, Koutsky LA, Hildesheim A, Galloway DA, Wheeler CM, Winer RL, Ho J, Kiviat NB: Risk for high-grade cervical intraepithelial neoplasia associated with variants of human papillomavirus types 16 and 18. Cancer Epidemiol Biomarkers Prev. 2007, 16: 4-10. 10.1158/1055-9965.EPI-06-0670.CrossRefPubMed Xi LF, Koutsky LA, Hildesheim A, Galloway DA, Wheeler CM, Winer RL, Ho J, Kiviat NB: Risk for high-grade cervical intraepithelial neoplasia associated with variants of human papillomavirus types 16 and 18. Cancer Epidemiol Biomarkers Prev. 2007, 16: 4-10. 10.1158/1055-9965.EPI-06-0670.CrossRefPubMed
16.
go back to reference Villa LL, Sichero L, Rahal P, Caballero O, Ferenczy A, Rohan T, Franco EL: Molecular variants of human papillomavirus types 16 and 18 preferentially associated with cervical neoplasia. J Gen Virol. 2000, 81: 2959-2968.CrossRefPubMed Villa LL, Sichero L, Rahal P, Caballero O, Ferenczy A, Rohan T, Franco EL: Molecular variants of human papillomavirus types 16 and 18 preferentially associated with cervical neoplasia. J Gen Virol. 2000, 81: 2959-2968.CrossRefPubMed
17.
go back to reference Berumen J, Ordonez RM, Lazcano E, Salmeron J, Galvan SC, Estrada RA, Yunes E, Garcia-Carranca A, Gonzalez-Lira G, Madrigal-de la Campa A: Asian-American variants of human papillomavirus 16 and risk for cervical cancer: a case–control study. J Natl Cancer Inst. 2001, 93: 1325-1330. 10.1093/jnci/93.17.1325.CrossRefPubMed Berumen J, Ordonez RM, Lazcano E, Salmeron J, Galvan SC, Estrada RA, Yunes E, Garcia-Carranca A, Gonzalez-Lira G, Madrigal-de la Campa A: Asian-American variants of human papillomavirus 16 and risk for cervical cancer: a case–control study. J Natl Cancer Inst. 2001, 93: 1325-1330. 10.1093/jnci/93.17.1325.CrossRefPubMed
18.
go back to reference Li N, Franceschi S, Howell-Jones R, Snijders PJ, Clifford GM: Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. Int J Cancer. 2010, 128: 927-935.CrossRef Li N, Franceschi S, Howell-Jones R, Snijders PJ, Clifford GM: Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. Int J Cancer. 2010, 128: 927-935.CrossRef
19.
go back to reference Kammer C, Tommasino M, Syrjanen S, Delius H, Hebling U, Warthorst U, Pfister H, Zehbe I: Variants of the long control region and the E6 oncogene in European human papillomavirus type 16 isolates: implications for cervical disease. Br J Cancer. 2002, 86: 269-273. 10.1038/sj.bjc.6600024.CrossRefPubMedPubMedCentral Kammer C, Tommasino M, Syrjanen S, Delius H, Hebling U, Warthorst U, Pfister H, Zehbe I: Variants of the long control region and the E6 oncogene in European human papillomavirus type 16 isolates: implications for cervical disease. Br J Cancer. 2002, 86: 269-273. 10.1038/sj.bjc.6600024.CrossRefPubMedPubMedCentral
20.
go back to reference Grodzki M, Besson G, Clavel C, Arslan A, Franceschi S, Birembaut P, Tommasino M, Zehbe I: Increased risk for cervical disease progression of French women infected with the human papillomavirus type 16 E6-350G variant. Cancer Epidemiol Biomarkers Prev. 2006, 15: 820-822. 10.1158/1055-9965.EPI-05-0864.CrossRefPubMed Grodzki M, Besson G, Clavel C, Arslan A, Franceschi S, Birembaut P, Tommasino M, Zehbe I: Increased risk for cervical disease progression of French women infected with the human papillomavirus type 16 E6-350G variant. Cancer Epidemiol Biomarkers Prev. 2006, 15: 820-822. 10.1158/1055-9965.EPI-05-0864.CrossRefPubMed
21.
go back to reference Xi LF, Kiviat NB, Hildesheim A, Galloway DA, Wheeler CM, Ho J, Koutsky LA: Human papillomavirus type 16 and 18 variants: racerelated distribution and persistence. J Natl Cancer Inst. 2006, 98: 1045-1052. 10.1093/jnci/djj297.CrossRefPubMed Xi LF, Kiviat NB, Hildesheim A, Galloway DA, Wheeler CM, Ho J, Koutsky LA: Human papillomavirus type 16 and 18 variants: racerelated distribution and persistence. J Natl Cancer Inst. 2006, 98: 1045-1052. 10.1093/jnci/djj297.CrossRefPubMed
22.
go back to reference Lee K, Magalhaes I, Clavel C, Briolat J, Birembaut P, Tommasino M, Zehbe I: Human papillomavirus 16 E6, L1, L2 and E2 gene variants in cervical lesion progression. Virus Res. 2008, 131: 106-110. 10.1016/j.virusres.2007.08.003.CrossRefPubMed Lee K, Magalhaes I, Clavel C, Briolat J, Birembaut P, Tommasino M, Zehbe I: Human papillomavirus 16 E6, L1, L2 and E2 gene variants in cervical lesion progression. Virus Res. 2008, 131: 106-110. 10.1016/j.virusres.2007.08.003.CrossRefPubMed
23.
go back to reference Burk RD, Terai M, Gravitt PE, Brinton LA, Kurman RJ, Barnes WA, Greenberg MD, Hadjimichael OC, Fu L, McGowan L, et al: Distribution of human papillomavirus types 16 and 18 variants in squamous cell carcinomas and adenocarcinomas of the cervix. Cancer Res. 2003, 63: 7215-7220.PubMed Burk RD, Terai M, Gravitt PE, Brinton LA, Kurman RJ, Barnes WA, Greenberg MD, Hadjimichael OC, Fu L, McGowan L, et al: Distribution of human papillomavirus types 16 and 18 variants in squamous cell carcinomas and adenocarcinomas of the cervix. Cancer Res. 2003, 63: 7215-7220.PubMed
24.
go back to reference Zuna RE, Moore WE, Shanesmith RP, Dunn ST, Wang SS, Schiffman M, Blakey GL, Teel T: Association of HPV16 E6 variants with diagnostic severity in cervical cytology samples of 354 women in a US population. Int J Cancer. 2009, 125: 2609-2613. 10.1002/ijc.24706.CrossRefPubMedPubMedCentral Zuna RE, Moore WE, Shanesmith RP, Dunn ST, Wang SS, Schiffman M, Blakey GL, Teel T: Association of HPV16 E6 variants with diagnostic severity in cervical cytology samples of 354 women in a US population. Int J Cancer. 2009, 125: 2609-2613. 10.1002/ijc.24706.CrossRefPubMedPubMedCentral
25.
go back to reference Quint KD, de Koning MN, van Doorn LJ, Quint WG, Pirog EC: HPV genotyping and HPV16 variant analysis in glandular and squamous neoplastic lesions of the uterine cervix. Gynecol Oncol. 2010, 117: 297-301. 10.1016/j.ygyno.2010.02.003.CrossRefPubMed Quint KD, de Koning MN, van Doorn LJ, Quint WG, Pirog EC: HPV genotyping and HPV16 variant analysis in glandular and squamous neoplastic lesions of the uterine cervix. Gynecol Oncol. 2010, 117: 297-301. 10.1016/j.ygyno.2010.02.003.CrossRefPubMed
26.
go back to reference Schiffman M, Rodriguez AC, Chen Z, Wacholder S, Herrero R, Hildesheim A, Desalle R, Befano B, Yu K, Safaeian M, et al: A population-based prospective study of carcinogenic human papillomavirus variant lineages, viral persistence, and cervical neoplasia. Cancer Res. 2010, 70: 3159-3169. 10.1158/0008-5472.CAN-09-4179.CrossRefPubMedPubMedCentral Schiffman M, Rodriguez AC, Chen Z, Wacholder S, Herrero R, Hildesheim A, Desalle R, Befano B, Yu K, Safaeian M, et al: A population-based prospective study of carcinogenic human papillomavirus variant lineages, viral persistence, and cervical neoplasia. Cancer Res. 2010, 70: 3159-3169. 10.1158/0008-5472.CAN-09-4179.CrossRefPubMedPubMedCentral
27.
go back to reference de Araujo Souza PS, Sichero L, Macia PC: HPV variants and HLA polymorphisms: the role of variability on the risk of cervical cancer. Future Oncol. 2009, 5: 359-370. 10.2217/fon.09.8.CrossRefPubMed de Araujo Souza PS, Sichero L, Macia PC: HPV variants and HLA polymorphisms: the role of variability on the risk of cervical cancer. Future Oncol. 2009, 5: 359-370. 10.2217/fon.09.8.CrossRefPubMed
28.
go back to reference KrennHrubec K, Mrad K, Sriha B, Ben Ayed F, Bottalico DM, Ostolaza J, Smith B, Tchaikovska T, Soliman AS, Burk RD: HPV types and variants among cervical cancer tumors in three regions of Tunisia. J Med Virol. 2011, 83: 651-657. 10.1002/jmv.22011.CrossRefPubMedPubMedCentral KrennHrubec K, Mrad K, Sriha B, Ben Ayed F, Bottalico DM, Ostolaza J, Smith B, Tchaikovska T, Soliman AS, Burk RD: HPV types and variants among cervical cancer tumors in three regions of Tunisia. J Med Virol. 2011, 83: 651-657. 10.1002/jmv.22011.CrossRefPubMedPubMedCentral
29.
go back to reference Sambrook J, Fritsch EF, Maniatis T: Molecular cloning: a laboratory manual 2nd ed. NY’ Cold Spring Harbor Laboratory. 1989, 1659-Press Sambrook J, Fritsch EF, Maniatis T: Molecular cloning: a laboratory manual 2nd ed. NY’ Cold Spring Harbor Laboratory. 1989, 1659-Press
30.
go back to reference Lee SH, Vigliotti VS, Vigliotti JS, Pappu S: Routine human papillomavirus genotyping by DNA sequencing in community hospital laboratories. Infect Agent Cancer. 2007, 2: 11-10.1186/1750-9378-2-11.CrossRefPubMedPubMedCentral Lee SH, Vigliotti VS, Vigliotti JS, Pappu S: Routine human papillomavirus genotyping by DNA sequencing in community hospital laboratories. Infect Agent Cancer. 2007, 2: 11-10.1186/1750-9378-2-11.CrossRefPubMedPubMedCentral
31.
go back to reference Meftah El khair M, El Mzibri M, Mhand RA, Benider A, Benchekroun N, Fahime EM, Benchekroun MN, Ennaji MM: Molecular detection and genotyping of human papillomavirus in cervical carcinoma biopsies in an area of high incidence of cancer from Moroccan women. J Med Virol. 2009, 81: 678-684. 10.1002/jmv.21279.CrossRefPubMed Meftah El khair M, El Mzibri M, Mhand RA, Benider A, Benchekroun N, Fahime EM, Benchekroun MN, Ennaji MM: Molecular detection and genotyping of human papillomavirus in cervical carcinoma biopsies in an area of high incidence of cancer from Moroccan women. J Med Virol. 2009, 81: 678-684. 10.1002/jmv.21279.CrossRefPubMed
32.
go back to reference Tornesello ML, Losito S, Benincasa G, Fulciniti F, Botti G, Greggi S, Buonaguro L, Buonaguro FM: Human papillomavirus (HPV) genotypes and HPV16 variants and risk of adenocarcinoma and squamous cell carcinoma of the cervix. Gynecol Oncol. 2011, 121: 32-42. 10.1016/j.ygyno.2010.12.005.CrossRefPubMed Tornesello ML, Losito S, Benincasa G, Fulciniti F, Botti G, Greggi S, Buonaguro L, Buonaguro FM: Human papillomavirus (HPV) genotypes and HPV16 variants and risk of adenocarcinoma and squamous cell carcinoma of the cervix. Gynecol Oncol. 2011, 121: 32-42. 10.1016/j.ygyno.2010.12.005.CrossRefPubMed
33.
go back to reference Lee SH, Vigliotti VS, Vigliotti JS, Pappu S: Validation of human papillomavirus genotyping by signature DNA sequence analysis. BMC Clin Pathol. 2009, 9: 3-10.1186/1472-6890-9-3.CrossRefPubMedPubMedCentral Lee SH, Vigliotti VS, Vigliotti JS, Pappu S: Validation of human papillomavirus genotyping by signature DNA sequence analysis. BMC Clin Pathol. 2009, 9: 3-10.1186/1472-6890-9-3.CrossRefPubMedPubMedCentral
34.
go back to reference Lizano M, De la Cruz-Hernandez E, Carrillo-Garcia A, Garcia-Carranca A, Ponce de Leon-Rosales S, Duenas-Gonzalez A, Hernandez-Hernandez DM, Mohar A: Distribution of HPV16 and 18 intratypic variants in normal cytology, intraepithelial lesions, and cervical cancer in a Mexican population. Gynecol Oncol. 2006, 102: 230-235. 10.1016/j.ygyno.2005.12.002.CrossRefPubMed Lizano M, De la Cruz-Hernandez E, Carrillo-Garcia A, Garcia-Carranca A, Ponce de Leon-Rosales S, Duenas-Gonzalez A, Hernandez-Hernandez DM, Mohar A: Distribution of HPV16 and 18 intratypic variants in normal cytology, intraepithelial lesions, and cervical cancer in a Mexican population. Gynecol Oncol. 2006, 102: 230-235. 10.1016/j.ygyno.2005.12.002.CrossRefPubMed
35.
go back to reference Seedorf K, Krammer G, Durst M, Suhai S, Rowekamp WG: Human papillomavirus type 16 DNA sequence. Virology. 1985, 145: 181-185. 10.1016/0042-6822(85)90214-4.CrossRefPubMed Seedorf K, Krammer G, Durst M, Suhai S, Rowekamp WG: Human papillomavirus type 16 DNA sequence. Virology. 1985, 145: 181-185. 10.1016/0042-6822(85)90214-4.CrossRefPubMed
36.
go back to reference Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003, 348: 518-527. 10.1056/NEJMoa021641.CrossRefPubMed Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003, 348: 518-527. 10.1056/NEJMoa021641.CrossRefPubMed
37.
go back to reference Clifford GM, Smith JS, Aguado T, Franceschi S: Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br J Cancer. 2003, 89: 101-105. 10.1038/sj.bjc.6601024.CrossRefPubMedPubMedCentral Clifford GM, Smith JS, Aguado T, Franceschi S: Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br J Cancer. 2003, 89: 101-105. 10.1038/sj.bjc.6601024.CrossRefPubMedPubMedCentral
38.
go back to reference de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, et al: Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 2010, 11: 1048-1056. 10.1016/S1470-2045(10)70230-8.CrossRefPubMed de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, et al: Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 2010, 11: 1048-1056. 10.1016/S1470-2045(10)70230-8.CrossRefPubMed
39.
go back to reference Zehbe I, Voglino G, Delius H, Wilander E, Tommasino M: Risk of cervical cancer and geographical variations of human papillomavirus 16 E6 polymorphisms. Lancet. 1998, 352: 1441-1442. 10.1016/S0140-6736(05)61263-9.CrossRefPubMed Zehbe I, Voglino G, Delius H, Wilander E, Tommasino M: Risk of cervical cancer and geographical variations of human papillomavirus 16 E6 polymorphisms. Lancet. 1998, 352: 1441-1442. 10.1016/S0140-6736(05)61263-9.CrossRefPubMed
40.
go back to reference Pande S, Jain N, Prusty BK, Bhambhani S, Gupta S, Sharma R, Batra S, Das BC: Human papillomavirus type 16 variant analysis of E6, E7, and L1 genes and long control region in biopsy samples from cervical cancer patients in north India. J Clin Microbiol. 2008, 46: 1060-1066. 10.1128/JCM.02202-07.CrossRefPubMedPubMedCentral Pande S, Jain N, Prusty BK, Bhambhani S, Gupta S, Sharma R, Batra S, Das BC: Human papillomavirus type 16 variant analysis of E6, E7, and L1 genes and long control region in biopsy samples from cervical cancer patients in north India. J Clin Microbiol. 2008, 46: 1060-1066. 10.1128/JCM.02202-07.CrossRefPubMedPubMedCentral
41.
go back to reference Chan SY, Ho L, Ong CK, Chow V, Drescher B, Durst M, ter Meulen J, Villa L, Luande J, Mgaya HN, Bernard HU: Molecular variants of human papillomavirus type16 from four continents suggest ancient pandemic spread of the virus and its coevolution with humankind. J Virol. 1992, 66: 2057-2066.PubMedPubMedCentral Chan SY, Ho L, Ong CK, Chow V, Drescher B, Durst M, ter Meulen J, Villa L, Luande J, Mgaya HN, Bernard HU: Molecular variants of human papillomavirus type16 from four continents suggest ancient pandemic spread of the virus and its coevolution with humankind. J Virol. 1992, 66: 2057-2066.PubMedPubMedCentral
42.
go back to reference Cornet I, Gheit T, Franceschi S, Vignat J, Burk RD, Sylla BS, Tommasino M, Clifford GM, the IARC HPV Variant Study Group: Human papillomavirus type 16 genetic variants: phylogeny and classification based on E6 and LCR. J Virol. 2013, 86: 6855-6861.CrossRef Cornet I, Gheit T, Franceschi S, Vignat J, Burk RD, Sylla BS, Tommasino M, Clifford GM, the IARC HPV Variant Study Group: Human papillomavirus type 16 genetic variants: phylogeny and classification based on E6 and LCR. J Virol. 2013, 86: 6855-6861.CrossRef
43.
go back to reference Pista A, Oliviera A, Barateiro A, Costa H, Verdasca N, Paixão : Molecular variants of human papillomavirus type 16 and 18 and risk for cervical neoplasia in Portugal. J Med Virol. 2007, 79: 1889-1897. 10.1002/jmv.21002.CrossRefPubMed Pista A, Oliviera A, Barateiro A, Costa H, Verdasca N, Paixão : Molecular variants of human papillomavirus type 16 and 18 and risk for cervical neoplasia in Portugal. J Med Virol. 2007, 79: 1889-1897. 10.1002/jmv.21002.CrossRefPubMed
44.
go back to reference Tornesello ML, Duraturo ML, Salatiello I, Buonaguro L, Losito S, Botti G, Stellato G, Greggi S, Piccoli R, Pilotti S, et al: Analysis of human papillomavirus type-16 variants in Italian women with cervical intraepithelial neoplasia and cervical cancer. J Med Virol. 2004, 74: 117-126. 10.1002/jmv.20154.CrossRefPubMed Tornesello ML, Duraturo ML, Salatiello I, Buonaguro L, Losito S, Botti G, Stellato G, Greggi S, Piccoli R, Pilotti S, et al: Analysis of human papillomavirus type-16 variants in Italian women with cervical intraepithelial neoplasia and cervical cancer. J Med Virol. 2004, 74: 117-126. 10.1002/jmv.20154.CrossRefPubMed
45.
go back to reference Tu JJ, Kuhn L, Denny L, Beattie KJ, Lorincz A, Wright TC: Molecular variants of human papillomavirus type 16 and risk for cervical neoplasia in south Africa. Int J Gynecol Cancer. 2006, 16: 736-742. 10.1111/j.1525-1438.2006.00401.x.CrossRefPubMed Tu JJ, Kuhn L, Denny L, Beattie KJ, Lorincz A, Wright TC: Molecular variants of human papillomavirus type 16 and risk for cervical neoplasia in south Africa. Int J Gynecol Cancer. 2006, 16: 736-742. 10.1111/j.1525-1438.2006.00401.x.CrossRefPubMed
46.
go back to reference Chopjitt P, Ekalaksananan T, Pientong C, Kongyingyoes B, Kleebkaow P, Charoensri N: Prevalence of human papillomavirus type 16 and its variants in abnormal squamous cervical cells in northeast Thailand. Int J Infect Dis. 2009, 13: 212-219. 10.1016/j.ijid.2008.06.017.CrossRefPubMed Chopjitt P, Ekalaksananan T, Pientong C, Kongyingyoes B, Kleebkaow P, Charoensri N: Prevalence of human papillomavirus type 16 and its variants in abnormal squamous cervical cells in northeast Thailand. Int J Infect Dis. 2009, 13: 212-219. 10.1016/j.ijid.2008.06.017.CrossRefPubMed
47.
go back to reference Hu X, Guo Z, Tianyun P, Pont en F, Wilander E, Andersson S, Pont en J: HPV typing and HPV16 E6-sequence variations in synchronous lesions of cervical squamous-cell carcinoma from Swedish patients. Int J Cancer. 1999, 83: 34-37. 10.1002/(SICI)1097-0215(19990924)83:1<34::AID-IJC7>3.0.CO;2-Q.CrossRefPubMed Hu X, Guo Z, Tianyun P, Pont en F, Wilander E, Andersson S, Pont en J: HPV typing and HPV16 E6-sequence variations in synchronous lesions of cervical squamous-cell carcinoma from Swedish patients. Int J Cancer. 1999, 83: 34-37. 10.1002/(SICI)1097-0215(19990924)83:1<34::AID-IJC7>3.0.CO;2-Q.CrossRefPubMed
48.
go back to reference Sun M, Gao L, Liu Y, Zhao Y, Wang X, Pan Y, Ning T, Cai H, Yang H, Zhai W, Ke Y: Whole genome sequencing and evolutionary analysis of human papillomavirus type 16 in central China. PloS one. 2012, 7: e36577-10.1371/journal.pone.0036577.CrossRefPubMedPubMedCentral Sun M, Gao L, Liu Y, Zhao Y, Wang X, Pan Y, Ning T, Cai H, Yang H, Zhai W, Ke Y: Whole genome sequencing and evolutionary analysis of human papillomavirus type 16 in central China. PloS one. 2012, 7: e36577-10.1371/journal.pone.0036577.CrossRefPubMedPubMedCentral
49.
go back to reference Chakrabarti O, Veeraraghavalu K, Tergaonkar V, Liu Y, Androphy EJ, Stanley MA, Krishna S: Human papillomavirus type 16 E6 amino acid 83 variants enhance E6-mediated MAPK signaling and differentially regulate tumorigenesis by notch signaling and oncogenic Ras. J Virol. 2004, 78: 5934-5945. 10.1128/JVI.78.11.5934-5945.2004.CrossRefPubMedPubMedCentral Chakrabarti O, Veeraraghavalu K, Tergaonkar V, Liu Y, Androphy EJ, Stanley MA, Krishna S: Human papillomavirus type 16 E6 amino acid 83 variants enhance E6-mediated MAPK signaling and differentially regulate tumorigenesis by notch signaling and oncogenic Ras. J Virol. 2004, 78: 5934-5945. 10.1128/JVI.78.11.5934-5945.2004.CrossRefPubMedPubMedCentral
50.
go back to reference van Duin M, Snijders PJ, Vossen MT, Klaassen E, Voorhorst F, Verheijen RH, Helmerhorst TJ, Meijer CJ, Walboomers JM: Analysis of human papillomavirus type 16 E6 variants in relation to p53 codon 72 polymorphism genotypes in cervical carcinogenesis. J Gen Virol. 2000, 81: 317-325.CrossRefPubMed van Duin M, Snijders PJ, Vossen MT, Klaassen E, Voorhorst F, Verheijen RH, Helmerhorst TJ, Meijer CJ, Walboomers JM: Analysis of human papillomavirus type 16 E6 variants in relation to p53 codon 72 polymorphism genotypes in cervical carcinogenesis. J Gen Virol. 2000, 81: 317-325.CrossRefPubMed
51.
go back to reference Zehbe I, Richard C, DeCarlo CA, Shai A, Lambert PF, Lichtig H, Tommasino M, Sherman L: Human papillomavirus 16 E6 variants differ in their dysregulation of human keratinocyte differentiation and apoptosis. Virology. 2009, 383: 69-77. 10.1016/j.virol.2008.09.036.CrossRefPubMed Zehbe I, Richard C, DeCarlo CA, Shai A, Lambert PF, Lichtig H, Tommasino M, Sherman L: Human papillomavirus 16 E6 variants differ in their dysregulation of human keratinocyte differentiation and apoptosis. Virology. 2009, 383: 69-77. 10.1016/j.virol.2008.09.036.CrossRefPubMed
52.
go back to reference Stöppler H, Koval D, Schlegel R: The serine protease inhibitors TLCK and TPCK inhibit the in vitro immortalization of primary human keratinocytes by HPV-18 DNA. Oncogene. 1996, 13: 1545-1548.PubMed Stöppler H, Koval D, Schlegel R: The serine protease inhibitors TLCK and TPCK inhibit the in vitro immortalization of primary human keratinocytes by HPV-18 DNA. Oncogene. 1996, 13: 1545-1548.PubMed
53.
go back to reference Wu Y, Chen Y, Li L, Yu G, He Y, Zhang Y: Analysis of mutations in the E6/E7 oncogenes and L1 gene of human papillomavirus 16 cervical cancer isolates from China. J Gen Virol. 2006, 87: 1181-1188. 10.1099/vir.0.81649-0.CrossRefPubMed Wu Y, Chen Y, Li L, Yu G, He Y, Zhang Y: Analysis of mutations in the E6/E7 oncogenes and L1 gene of human papillomavirus 16 cervical cancer isolates from China. J Gen Virol. 2006, 87: 1181-1188. 10.1099/vir.0.81649-0.CrossRefPubMed
54.
go back to reference Tonon SA, Basiletti J, Badano I, Alonio LV, Villa LL, Teyssie AR, Picconi MA: Human papillomavirus type 16 molecular variants in Guarani Indian women from Misiones, Argentina. Int J Infect Dis. 2007, 11: 76-81. 10.1016/j.ijid.2006.01.002.CrossRefPubMed Tonon SA, Basiletti J, Badano I, Alonio LV, Villa LL, Teyssie AR, Picconi MA: Human papillomavirus type 16 molecular variants in Guarani Indian women from Misiones, Argentina. Int J Infect Dis. 2007, 11: 76-81. 10.1016/j.ijid.2006.01.002.CrossRefPubMed
55.
go back to reference Picconi MA, Alonio LV, Sichero L, Mbayed V, Villa LL, Gronda J, Campos R, Teyssié A: Human papillomavirus type-16 variants in Quechua aboriginals from Argentina. J Med Virol. 2003, 69: 546-555. 10.1002/jmv.10343.CrossRefPubMed Picconi MA, Alonio LV, Sichero L, Mbayed V, Villa LL, Gronda J, Campos R, Teyssié A: Human papillomavirus type-16 variants in Quechua aboriginals from Argentina. J Med Virol. 2003, 69: 546-555. 10.1002/jmv.10343.CrossRefPubMed
56.
go back to reference DeFilippis RA, Goodwin EC, Wu L, DiMaio D: Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation, senescence, and apoptosis in HeLa cervical carcinoma cells. J Virol. 2003, 77: 1551-1563. 10.1128/JVI.77.2.1551-1563.2003.CrossRefPubMedPubMedCentral DeFilippis RA, Goodwin EC, Wu L, DiMaio D: Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation, senescence, and apoptosis in HeLa cervical carcinoma cells. J Virol. 2003, 77: 1551-1563. 10.1128/JVI.77.2.1551-1563.2003.CrossRefPubMedPubMedCentral
57.
go back to reference Chen Z, Terai M, Fu L, Herrero R, DeSalle R, Burk RD: Diversifying selection in human papillomavirus type 16 lineages based on complete genome analyses. J Virol. 2005, 79: 7014-7023. 10.1128/JVI.79.11.7014-7023.2005.CrossRefPubMedPubMedCentral Chen Z, Terai M, Fu L, Herrero R, DeSalle R, Burk RD: Diversifying selection in human papillomavirus type 16 lineages based on complete genome analyses. J Virol. 2005, 79: 7014-7023. 10.1128/JVI.79.11.7014-7023.2005.CrossRefPubMedPubMedCentral
58.
go back to reference Zehbe I, Mytilineos J, Wikström I, Henriksen R, Edler L, Tommasino M: Association between human papillomavirus 16 E6 variants and human leukocyte antigen class I polymorphism in cervical cancer of Swedish women. Hum Immunol. 2003, 64: 538-542. 10.1016/S0198-8859(03)00033-8.CrossRefPubMed Zehbe I, Mytilineos J, Wikström I, Henriksen R, Edler L, Tommasino M: Association between human papillomavirus 16 E6 variants and human leukocyte antigen class I polymorphism in cervical cancer of Swedish women. Hum Immunol. 2003, 64: 538-542. 10.1016/S0198-8859(03)00033-8.CrossRefPubMed
59.
go back to reference Ellis JR JKP, Baird J, Hounsell EF VRD, Rowe M, Hopkins D, Duggan-Keen MF, Bartholomew JS, Young LS: The association of an HPV16 oncogene variant with HLA-B7 has implications for vaccine design in cervical cancer. Nat Med. 1995, 1: 464-470. 10.1038/nm0595-464.CrossRefPubMed Ellis JR JKP, Baird J, Hounsell EF VRD, Rowe M, Hopkins D, Duggan-Keen MF, Bartholomew JS, Young LS: The association of an HPV16 oncogene variant with HLA-B7 has implications for vaccine design in cervical cancer. Nat Med. 1995, 1: 464-470. 10.1038/nm0595-464.CrossRefPubMed
60.
go back to reference Bartholomew JS, Stacey SN, Coles B, Burt DJ, Arrand JR, Stern PL: Identification of a naturally processed HLA A0201-restricted viral peptide from cells expressing human papillomavirus type 16 E6 oncoprotein. Eur J Immunol. 1994, 24: 3175-3179. 10.1002/eji.1830241239.CrossRefPubMed Bartholomew JS, Stacey SN, Coles B, Burt DJ, Arrand JR, Stern PL: Identification of a naturally processed HLA A0201-restricted viral peptide from cells expressing human papillomavirus type 16 E6 oncoprotein. Eur J Immunol. 1994, 24: 3175-3179. 10.1002/eji.1830241239.CrossRefPubMed
Metadata
Title
Analysis of mutations in the E6 oncogene of human papillomavirus 16 in cervical cancer isolates from Moroccan women
Authors
Zineb Qmichou
Meriem Khyatti
Mohamed Berraho
My Mustapha Ennaji
Laila Benbacer
Chakib Nejjari
Noureddine Benjaafar
Abdellatif Benider
Mohammed Attaleb
Mohammed El Mzibri
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2013
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-13-378

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