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Abstract

Human papillomavirus 52 (HPV52) infection is prevalent in the Chinese population, and variations in HPV52 show correlations with oncogenicity. However, no specific variation in HPV52 was reported to show relevancy to infection characteristics. In this study, we retrieved 222 isolates of E6 and L1 full-length genes from 197 Chinese women with HPV52 infection. After sequence alignment and phylogenetic tree construction, we found that 98.39 % of the collected variants belonged to the sublineage B2 and two variants displayed incongruence between the phylogenetic tree of E6 and L1. The analysis of the infection pattern showed that the presence of C6480A/T mutation in the L1 gene was associated with single infection (=0.01) and persistent infection (=0.047) of HPV52, while the A6516G nucleotide change was relevant to transient infection (=0.018). Our data also indicated that variations T309C in the E6 gene and C6480T, C6600A in L1 were more commonly presented in patients with high-grade cytology (<0.05). One HPV52 breakthrough infection after vaccination was identified, which hinted at the immune escape post-vaccination. Young coitarche age and non-condom usage were correlated to multiple infections. This study provided insight into the polymorphism of HPV52 and revealed the impact of variations in HPV52 on its infection characteristics.

Funding
This study was supported by the:
  • Science and Technology Commission of Shanghai Municipality (Award 21Y11906500)
    • Principle Award Recipient: LiYanyun
  • National Natural Science Foundation of China (Award 82272970)
    • Principle Award Recipient: LiYanyun
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-04-27
2024-05-04
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References

  1. Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX et al. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 2010; 202:1789–1799 [View Article] [PubMed]
    [Google Scholar]
  2. Bruni L AG, Serrano B, Mena M, Collado JJ, Gómez D et al. Human papillomavirus and related diseases in the world. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre); 2022Feb
  3. Zhang J, Cheng K, Wang Z. Prevalence and distribution of human papillomavirus genotypes in cervical intraepithelial neoplasia in China: a meta-analysis. Arch Gynecol Obstet 2020; 302:1329–1337 [View Article] [PubMed]
    [Google Scholar]
  4. Chen L, Dong Y, Li J, Zhao J, Wang D et al. The genomic distribution map of human papillomavirus in Western China. Epidemiol Infect 2021; 149:e135 [View Article] [PubMed]
    [Google Scholar]
  5. Zhang C, Park J-S, Grce M, Hibbitts S, Palefsky JM et al. Geographical distribution and risk association of human papillomavirus genotype 52-variant lineages. J Infect Dis 2014; 210:1600–1604 [View Article] [PubMed]
    [Google Scholar]
  6. Ding T, Wang X, Ye F, Cheng X, Ma D et al. Distribution of human papillomavirus 58 and 52 E6/E7 variants in cervical neoplasia in Chinese women. Gynecol Oncol 2010; 119:436–443 [View Article] [PubMed]
    [Google Scholar]
  7. Choi YJ, Ki EY, Zhang C, Ho WCS, Lee S-J et al. Analysis of sequence variation and risk association of human papillomavirus 52 variants circulating in Korea. PLoS One 2016; 11:e0168178 [View Article] [PubMed]
    [Google Scholar]
  8. Shanmugasundaram S, You J. Targeting persistent human papillomavirus infection. Viruses 2017; 9:229 [View Article] [PubMed]
    [Google Scholar]
  9. Rositch AF, Koshiol J, Hudgens MG, Razzaghi H, Backes DM et al. Patterns of persistent genital human papillomavirus infection among women worldwide: a literature review and meta-analysis. Int J Cancer 2013; 133:1271–1285 [View Article] [PubMed]
    [Google Scholar]
  10. Hoffman SR, Le T, Lockhart A, Sanusi A, Dal Santo L et al. Patterns of persistent HPV infection after treatment for cervical intraepithelial neoplasia (CIN): a systematic review. Int J Cancer 2017; 141:8–23 [View Article] [PubMed]
    [Google Scholar]
  11. Gusho E, Laimins L. Human papillomaviruses target the DNA damage repair and innate immune response pathways to allow for persistent infection. Viruses 2021; 13:1390 [View Article] [PubMed]
    [Google Scholar]
  12. Sanchez GI, Kleter B, Gheit T, van Doorn L-J, de Koning MNC et al. Clinical evaluation of polymerase chain reaction reverse hybridization assay for detection and identification of human papillomavirus type 16 variants. J Clin Virol 2011; 51:165–169 [View Article] [PubMed]
    [Google Scholar]
  13. Tornesello ML, Losito S, Benincasa G, Fulciniti F, Botti G et al. Human papillomavirus (HPV) genotypes and HPV16 variants and risk of adenocarcinoma and squamous cell carcinoma of the cervix. Gynecol Oncol 2011; 121:32–42 [View Article] [PubMed]
    [Google Scholar]
  14. Lee K, Magalhaes I, Clavel C, Briolat J, Birembaut P et al. Human papillomavirus 16 E6, L1, L2 and E2 gene variants in cervical lesion progression. Virus Res 2008; 131:106–110 [View Article] [PubMed]
    [Google Scholar]
  15. Zhang L, Yang B, Zhang A, Zhou A, Yuan J et al. Association between human papillomavirus type 16 E6 and E7 variants with subsequent persistent infection and recurrence of cervical high-grade squamous intraepithelial lesion after conization. J Med Virol 2016; 88:1982–1988 [View Article] [PubMed]
    [Google Scholar]
  16. Escobar-Escamilla N, González-Martínez BE, Araiza-Rodríguez A, Fragoso-Fonseca DE, Pedroza-Torres A et al. Mutational landscape and intra-host diversity of human papillomavirus type 16 long control region and E6 variants in cervical samples. Arch Virol 2019; 164:2953–2961 [View Article] [PubMed]
    [Google Scholar]
  17. Cornet I, Gheit T, Clifford GM, Combes J-D, Dalstein V et al. Human papillomavirus type 16 E6 variants in France and risk of viral persistence. Infect Agent Cancer 2013; 8:4 [View Article] [PubMed]
    [Google Scholar]
  18. Gauthier B, Cerigo H, Coutlée F, Franco EL, Brassard P. Persistence of human papillomavirus 16, 18 and 52 variants in Inuit women from Northern Quebec, Canada. Int J Circumpolar Health 2018; 77:1556556 [View Article] [PubMed]
    [Google Scholar]
  19. Aho J, Hankins C, Tremblay C, Forest P, Pourreaux K et al. Genomic polymorphism of human papillomavirus type 52 predisposes toward persistent infection in sexually active women. J Infect Dis 2004; 190:46–52 [View Article] [PubMed]
    [Google Scholar]
  20. Sun Z, Lu Z, Liu J, Wang G, Zhou W et al. Genomic polymorphism of human papillomavirus type 52 in women from Northeast China. Int J Mol Sci 2012; 13:14962–14972 [View Article] [PubMed]
    [Google Scholar]
  21. Ishizaki A, Matsushita K, Hoang HTT, Agdamag DM, Nguyen CH et al. E6 and E7 variants of human papillomavirus-16 and -52 in Japan, the Philippines, and Vietnam. J Med Virol 2013; 85:1069–1076 [View Article] [PubMed]
    [Google Scholar]
  22. Schlecht NF, Diaz A, Nucci-Sack A, Shyhalla K, Shankar V et al. Incidence and types of human papillomavirus infections in adolescent girls and young women immunized with the human papillomavirus accine. JAMA Netw Open 2021; 4:e2121893 [View Article] [PubMed]
    [Google Scholar]
  23. Guo F, Hirth JM, Berenson AB. Comparison of HPV prevalence between HPV-vaccinated and non-vaccinated young adult women (20-26 years). Hum Vaccin Immunother 2015; 11:2337–2344 [View Article] [PubMed]
    [Google Scholar]
  24. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  25. Burk RD, Harari A, Chen Z. Human papillomavirus genome variants. Virology 2013; 445:232–243 [View Article] [PubMed]
    [Google Scholar]
  26. Zhang Y, Cao M, Wang M, Ding X, Jing Y et al. Genetic variability in E6, E7, and L1 genes of human papillomavirus genotype 52 from Southwest China. Gene 2016; 585:110–118 [View Article] [PubMed]
    [Google Scholar]
  27. Bravo IG, Alonso A. Mucosal human papillomaviruses encode four different E5 proteins whose chemistry and phylogeny correlate with malignant or benign growth. J Virol 2004; 78:13613–13626 [View Article] [PubMed]
    [Google Scholar]
  28. Narechania A, Chen Z, DeSalle R, Burk RD. Phylogenetic incongruence among oncogenic genital alpha human papillomaviruses. J Virol 2005; 79:15503–15510 [View Article] [PubMed]
    [Google Scholar]
  29. Shah SD, Doorbar J, Goldstein RA. Analysis of host-parasite incongruence in papillomavirus evolution using importance sampling. Mol Biol Evol 2010; 27:1301–1314 [View Article] [PubMed]
    [Google Scholar]
  30. Gong Y, Sui L, Li Y. Recombination in papillomavirus: controversy and possibility. Virus Res 2022; 314:198756 [View Article] [PubMed]
    [Google Scholar]
  31. Chen Z, Schiffman M, Herrero R, Desalle R, Anastos K et al. Evolution and taxonomic classification of human papillomavirus 16 (HPV16)-related variant genomes: HPV31, HPV33, HPV35, HPV52, HPV58 and HPV67. PLoS One 2011; 6:e20183 [View Article] [PubMed]
    [Google Scholar]
  32. Gagnon S, Hankins C, Money D, Pourreaux K et al. Polymorphism of the L1 capsid gene and persistence of human papillomavirus type 52 infection in women at high risk or infected by HIV. J Acquir Immune Defic Syndr 2007; 44:61–65 [View Article] [PubMed]
    [Google Scholar]
  33. Chen Z, Terai M, Fu L, Herrero R, DeSalle R et al. Diversifying selection in human papillomavirus type 16 lineages based on complete genome analyses. J Virol 2005; 79:7014–7023 [View Article] [PubMed]
    [Google Scholar]
  34. Chen Z, Schiffman M, Herrero R, DeSalle R, Anastos K et al. Evolution and taxonomic classification of alphapapillomavirus 7 complete genomes: HPV18, HPV39, HPV45, HPV59, HPV68 and HPV70. PLoS One 2013; 8:e72565 [View Article] [PubMed]
    [Google Scholar]
  35. Martínez MA, Jordan-Paiz A, Franco S, Nevot M. Synonymous genome recoding: a tool to explore microbial biology and new therapeutic strategies. Nucleic Acids Res 2019; 47:10506–10519 [View Article] [PubMed]
    [Google Scholar]
  36. Oyervides-Muñoz MA, Pérez-Maya AA, Sánchez-Domínguez CN, Berlanga-Garza A, Antonio-Macedo M et al. Multiple HPV infections and viral load association in persistent cervical lesions in Mexican women. Viruses 2020; 12:380 [View Article] [PubMed]
    [Google Scholar]
  37. De Brot L, Pellegrini B, Moretti ST, Carraro DM, Soares FA et al. Infections with multiple high-risk HPV types are associated with high-grade and persistent low-grade intraepithelial lesions of the cervix. Cancer Cytopathol 2017; 125:138–143 [View Article] [PubMed]
    [Google Scholar]
  38. Wang X, Wu S, Li Y. Risks for cervical abnormalities in women with non-16/18 high-risk human papillomavirus infections in south Shanghai, China. J Med Virol 2021; 93:6355–6361 [View Article] [PubMed]
    [Google Scholar]
  39. Hajia M, Sohrabi A. Possible synergistic interactions among multiple HPV genotypes in women suffering from genital neoplasia. Asian Pac J Cancer Prev 2018; 19:785–789 [View Article] [PubMed]
    [Google Scholar]
  40. Brant AC, Menezes AN, Felix SP, Almeida LM, Moreira MAM. Preferential expression of a HPV genotype in invasive cervical carcinomas infected by multiple genotypes. Genomics 2020; 112:2942–2948 [View Article] [PubMed]
    [Google Scholar]
  41. Zhou D, Dejnirattisai W, Supasa P, Liu C, Mentzer AJ et al. Evidence of escape of SARS-CoV-2 variant B.1.351 from natural and vaccine-induced sera. Cell 2021; 184:2348–2361 [View Article] [PubMed]
    [Google Scholar]
  42. Garcia-Beltran WF, Lam EC, St Denis K, Nitido AD, Garcia ZH et al. Multiple SARS-CoV-2 variants escape neutralization by vaccine-induced humoral immunity. Cell 2021; 184:2372–2383 [View Article] [PubMed]
    [Google Scholar]
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