Treffer: Codon Usage Pattern of Papillomavirus E6, E7, and L1 Genes Across Hosts.
Title:
Codon Usage Pattern of Papillomavirus E6, E7, and L1 Genes Across Hosts.
Authors:
Liu X; National Infrastructures for Translational Medicine, the State Key Laboratory for Complex, Severe, and Rare Diseases, Institute of Clinical Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Shuaifuyuan No. 1, Dongcheng District, Beijing, 100730, China., Li K; School of Engineering Medicine, Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Interdisciplinary Innovation Institute of Medicine and Engineering, Beihang University, Beijing, 100730, China.; Microbiome Dynamics, Leibniz Institute for Natural Product Research and Infection Biology - Hans Knöll Institute, 07745, Jena, Germany., Chen X; National Infrastructures for Translational Medicine, the State Key Laboratory for Complex, Severe, and Rare Diseases, Institute of Clinical Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Shuaifuyuan No. 1, Dongcheng District, Beijing, 100730, China.; Department of Obstetrics and Gynecology, Peking Union Medical College Hospital, Beijing, 100730, China.; National Clinical Research Center for Obstetric and Gynecologic Diseases, Beijing, 100730, China., Li Y; National Infrastructures for Translational Medicine, the State Key Laboratory for Complex, Severe, and Rare Diseases, Institute of Clinical Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Shuaifuyuan No. 1, Dongcheng District, Beijing, 100730, China., Sun T; National Infrastructures for Translational Medicine, the State Key Laboratory for Complex, Severe, and Rare Diseases, Institute of Clinical Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Shuaifuyuan No. 1, Dongcheng District, Beijing, 100730, China., Huang R; Department of Obstetrics and Gynecology, Peking Union Medical College Hospital, Beijing, 100730, China., Shi Y; Biomedical Engineering Facility of National Infrastructures for Translational Medicine, Peking Union Medical College Hospital, Beijing, 100730, China., He Z; School of Engineering Medicine, Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Interdisciplinary Innovation Institute of Medicine and Engineering, Beihang University, Beijing, 100730, China. hezilong@buaa.edu.cn.; School of Engineering Medicine, Beihang University, No. 37 Xueyuan Road, Haidian District, Beijing, 100191, China. hezilong@buaa.edu.cn., Li L; National Infrastructures for Translational Medicine, the State Key Laboratory for Complex, Severe, and Rare Diseases, Institute of Clinical Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Shuaifuyuan No. 1, Dongcheng District, Beijing, 100730, China. lileigh@163.com.; Department of Obstetrics and Gynecology, Peking Union Medical College Hospital, Beijing, 100730, China. lileigh@163.com.; National Clinical Research Center for Obstetric and Gynecologic Diseases, Beijing, 100730, China. lileigh@163.com.
Source:
Current microbiology [Curr Microbiol] 2025 Aug 29; Vol. 82 (10), pp. 481. Date of Electronic Publication: 2025 Aug 29.
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: Springer International Country of Publication: United States NLM ID: 7808448 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-0991 (Electronic) Linking ISSN: 03438651 NLM ISO Abbreviation: Curr Microbiol Subsets: MEDLINE
Imprint Name(s):
Original Publication: New York, Springer International.
MeSH Terms:
Codon Usage* , Oncogene Proteins, Viral*/genetics , Papillomaviridae*/genetics , Papillomaviridae*/classification , Capsid Proteins*/genetics , Papillomavirus E7 Proteins*/genetics, Phylogeny ; Evolution, Molecular ; Genome, Viral ; Humans ; Papillomavirus Infections/virology ; Selection, Genetic ; Codon
References:
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Stanley MA, Sterling JC (2014) Host responses to infection with human papillomavirus. Curr Probl Dermatol 45:58–74. https://doi.org/10.1159/000355964. (PMID: 10.1159/00035596424643178)
Chen Z, Schiffman M, Herrero R, Desalle R, Burk RD (2007) Human papillomavirus (HPV) types 101 and 103 isolated from cervicovaginal cells lack an E6 open reading frame (ORF) and are related to gamma-papillomaviruses. Virology 360(2):447–453. https://doi.org/10.1016/j.virol.2006.10.022. (PMID: 10.1016/j.virol.2006.10.02217125811)
Ye M, Li S, Luo P, Tang X, Gong Q, Mei B (2022) Genetic variation of E6, E7, and L1 genes of human papillomavirus 51 from central China. J Med Virol 94(6):2811–2823. https://doi.org/10.1002/jmv.27603. (PMID: 10.1002/jmv.2760335048388)
Parvathy ST, Udayasuriyan V, Bhadana V (2022) Codon usage bias. Mol Biol Rep 49(1):539–565. https://doi.org/10.1007/s11033-021-06749-4. (PMID: 10.1007/s11033-021-06749-434822069)
Bahir I, Fromer M, Prat Y, Linial M (2009) Viral adaptation to host: a proteome-based analysis of codon usage and amino acid preferences. Mol Syst Biol 5:311. https://doi.org/10.1038/msb.2009.71. (PMID: 10.1038/msb.2009.71198882062779085)
King KM, Rajadhyaksha EV, Tobey IG, Van Doorslaer K (2022) Synonymous nucleotide changes drive papillomavirus evolution. Tumour Virus Res 14:200248. https://doi.org/10.1016/j.tvr.2022.200248. (PMID: 10.1016/j.tvr.2022.200248362658369589209)
Shin YC, Bischof GF, Lauer WA, Desrosiers RC (2015) Importance of codon usage for the temporal regulation of viral gene expression. Proc Natl Acad Sci U S A 112(45):14030–14035. https://doi.org/10.1073/pnas.1515387112. (PMID: 10.1073/pnas.1515387112265042414653223)
Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I (1999) Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J Virol 73(6):4972–4982. https://doi.org/10.1128/JVI.73.6.4972-4982.1999. (PMID: 10.1128/JVI.73.6.4972-4982.199910233959112541)
Zhao KN, Chen J (2011) Codon usage roles in human papillomavirus. Rev Med Virol 21(6):397–411. https://doi.org/10.1002/rmv.707. (PMID: 10.1002/rmv.70722025363)
Zhao KN, Liu WJ, Frazer IH (2003) Codon usage bias and A+T content variation in human papillomavirus genomes. Virus Res 98(2):95–104. https://doi.org/10.1016/j.virusres.2003.08.019. (PMID: 10.1016/j.virusres.2003.08.01914659556)
Liu W, Li J, Du H, Ou Z (2021) Mutation profiles, glycosylation site distribution and codon usage bias of human papillomavirus type 16. Viruses. https://doi.org/10.3390/v13071281. (PMID: 10.3390/v13071281350622628780094)
Kocjan BJ, Seme K, Cimerman M, Kovanda A, Potocnik M, Poljak M (2009) Genomic diversity of human papillomavirus (HPV) genotype 38. J Med Virol 81(2):288–295. https://doi.org/10.1002/jmv.21392. (PMID: 10.1002/jmv.2139219107968)
Tan X, Bao S, Lu X, Lu B, Shen W, Jiang C (2024) Comprehensive analysis of codon usage bias in Human Papillomavirus type 51. Pol J Microbiol 73(4):455–465. https://doi.org/10.33073/pjm-2024-036. (PMID: 10.33073/pjm-2024-0363946591011639286)
Tan X, Xie Y, Jiang C, Li H, Lu Y, Shen W, Chen J (2024) Codon usage bias of human papillomavirus type 33 and 58: a comprehensive analysis. J Basic Microbiol 64(5):e2300636. https://doi.org/10.1002/jobm.202300636. (PMID: 10.1002/jobm.20230063638346260)
Tan X, Zhou W, Jing S, Shen W, Lu B (2025) Decoding codon usage in human papillomavirus type 59. Virus Genes. https://doi.org/10.1007/s11262-025-02148-0. (PMID: 10.1007/s11262-025-02148-04003821412052745)
da Silva-Junior AHP, de Oliveira Silva RC, Gurgel A, Barros-Junior MR, Nascimento KCG, Santos DL et al (2024) Identification and functional implications of the E5 oncogene polymorphisms of human papillomavirus type 16. Trop Med Infect Dis. https://doi.org/10.3390/tropicalmed9070140. (PMID: 10.3390/tropicalmed90701403905818211281449)
Ren J, Li Q, Shen W, Tan X (2025) Decoding codon usage patterns in high-risk human papillomavirus genomes: a comprehensive analysis. Curr Microbiol 82(4):148. https://doi.org/10.1007/s00284-025-04131-2. (PMID: 10.1007/s00284-025-04131-239987223)
Van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D, Liou D et al (2017) The papillomavirus episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res 45(D1):D499–D506. https://doi.org/10.1093/nar/gkw879. (PMID: 10.1093/nar/gkw87928053164)
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. https://doi.org/10.1093/bioinformatics/btu153. (PMID: 10.1093/bioinformatics/btu15324642063)
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066. https://doi.org/10.1093/nar/gkf436. (PMID: 10.1093/nar/gkf43612136088135756)
Price MN, Dehal PS, Arkin AP (2009) Fasttree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26(7):1641–1650. https://doi.org/10.1093/molbev/msp077. (PMID: 10.1093/molbev/msp077193770592693737)
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296. https://doi.org/10.1093/nar/gkab301. (PMID: 10.1093/nar/gkab301338857858265157)
Zhang Z, Li J, Cui P, Ding F, Li A, Townsend JP, Yu J (2012) Codon deviation coefficient: a novel measure for estimating codon usage bias and its statistical significance. BMC Bioinform 13:43. https://doi.org/10.1186/1471-2105-13-43. (PMID: 10.1186/1471-2105-13-43)
Stanley MA, Sterling JC (2014) Host responses to infection with human papillomavirus. Curr Probl Dermatol 45:58–74. https://doi.org/10.1159/000355964. (PMID: 10.1159/00035596424643178)
Chen Z, Schiffman M, Herrero R, Desalle R, Burk RD (2007) Human papillomavirus (HPV) types 101 and 103 isolated from cervicovaginal cells lack an E6 open reading frame (ORF) and are related to gamma-papillomaviruses. Virology 360(2):447–453. https://doi.org/10.1016/j.virol.2006.10.022. (PMID: 10.1016/j.virol.2006.10.02217125811)
Ye M, Li S, Luo P, Tang X, Gong Q, Mei B (2022) Genetic variation of E6, E7, and L1 genes of human papillomavirus 51 from central China. J Med Virol 94(6):2811–2823. https://doi.org/10.1002/jmv.27603. (PMID: 10.1002/jmv.2760335048388)
Parvathy ST, Udayasuriyan V, Bhadana V (2022) Codon usage bias. Mol Biol Rep 49(1):539–565. https://doi.org/10.1007/s11033-021-06749-4. (PMID: 10.1007/s11033-021-06749-434822069)
Bahir I, Fromer M, Prat Y, Linial M (2009) Viral adaptation to host: a proteome-based analysis of codon usage and amino acid preferences. Mol Syst Biol 5:311. https://doi.org/10.1038/msb.2009.71. (PMID: 10.1038/msb.2009.71198882062779085)
King KM, Rajadhyaksha EV, Tobey IG, Van Doorslaer K (2022) Synonymous nucleotide changes drive papillomavirus evolution. Tumour Virus Res 14:200248. https://doi.org/10.1016/j.tvr.2022.200248. (PMID: 10.1016/j.tvr.2022.200248362658369589209)
Shin YC, Bischof GF, Lauer WA, Desrosiers RC (2015) Importance of codon usage for the temporal regulation of viral gene expression. Proc Natl Acad Sci U S A 112(45):14030–14035. https://doi.org/10.1073/pnas.1515387112. (PMID: 10.1073/pnas.1515387112265042414653223)
Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I (1999) Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J Virol 73(6):4972–4982. https://doi.org/10.1128/JVI.73.6.4972-4982.1999. (PMID: 10.1128/JVI.73.6.4972-4982.199910233959112541)
Zhao KN, Chen J (2011) Codon usage roles in human papillomavirus. Rev Med Virol 21(6):397–411. https://doi.org/10.1002/rmv.707. (PMID: 10.1002/rmv.70722025363)
Zhao KN, Liu WJ, Frazer IH (2003) Codon usage bias and A+T content variation in human papillomavirus genomes. Virus Res 98(2):95–104. https://doi.org/10.1016/j.virusres.2003.08.019. (PMID: 10.1016/j.virusres.2003.08.01914659556)
Liu W, Li J, Du H, Ou Z (2021) Mutation profiles, glycosylation site distribution and codon usage bias of human papillomavirus type 16. Viruses. https://doi.org/10.3390/v13071281. (PMID: 10.3390/v13071281350622628780094)
Kocjan BJ, Seme K, Cimerman M, Kovanda A, Potocnik M, Poljak M (2009) Genomic diversity of human papillomavirus (HPV) genotype 38. J Med Virol 81(2):288–295. https://doi.org/10.1002/jmv.21392. (PMID: 10.1002/jmv.2139219107968)
Tan X, Bao S, Lu X, Lu B, Shen W, Jiang C (2024) Comprehensive analysis of codon usage bias in Human Papillomavirus type 51. Pol J Microbiol 73(4):455–465. https://doi.org/10.33073/pjm-2024-036. (PMID: 10.33073/pjm-2024-0363946591011639286)
Tan X, Xie Y, Jiang C, Li H, Lu Y, Shen W, Chen J (2024) Codon usage bias of human papillomavirus type 33 and 58: a comprehensive analysis. J Basic Microbiol 64(5):e2300636. https://doi.org/10.1002/jobm.202300636. (PMID: 10.1002/jobm.20230063638346260)
Tan X, Zhou W, Jing S, Shen W, Lu B (2025) Decoding codon usage in human papillomavirus type 59. Virus Genes. https://doi.org/10.1007/s11262-025-02148-0. (PMID: 10.1007/s11262-025-02148-04003821412052745)
da Silva-Junior AHP, de Oliveira Silva RC, Gurgel A, Barros-Junior MR, Nascimento KCG, Santos DL et al (2024) Identification and functional implications of the E5 oncogene polymorphisms of human papillomavirus type 16. Trop Med Infect Dis. https://doi.org/10.3390/tropicalmed9070140. (PMID: 10.3390/tropicalmed90701403905818211281449)
Ren J, Li Q, Shen W, Tan X (2025) Decoding codon usage patterns in high-risk human papillomavirus genomes: a comprehensive analysis. Curr Microbiol 82(4):148. https://doi.org/10.1007/s00284-025-04131-2. (PMID: 10.1007/s00284-025-04131-239987223)
Van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D, Liou D et al (2017) The papillomavirus episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res 45(D1):D499–D506. https://doi.org/10.1093/nar/gkw879. (PMID: 10.1093/nar/gkw87928053164)
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. https://doi.org/10.1093/bioinformatics/btu153. (PMID: 10.1093/bioinformatics/btu15324642063)
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066. https://doi.org/10.1093/nar/gkf436. (PMID: 10.1093/nar/gkf43612136088135756)
Price MN, Dehal PS, Arkin AP (2009) Fasttree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26(7):1641–1650. https://doi.org/10.1093/molbev/msp077. (PMID: 10.1093/molbev/msp077193770592693737)
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296. https://doi.org/10.1093/nar/gkab301. (PMID: 10.1093/nar/gkab301338857858265157)
Zhang Z, Li J, Cui P, Ding F, Li A, Townsend JP, Yu J (2012) Codon deviation coefficient: a novel measure for estimating codon usage bias and its statistical significance. BMC Bioinform 13:43. https://doi.org/10.1186/1471-2105-13-43. (PMID: 10.1186/1471-2105-13-43)
Grant Information:
Z220013 the State Key Laboratory for Complex, Severe and Rare Diseases in Peking Union Medical College Hospital, by the Key Research Project of Beijing Natural Science Foundation; 2024-I2M-C&T-B-029 the CAMS Innovation Fund for Medical Sciences (CIFMS); 2022-PUMCH-B-083 the National High Level Hospital Clinical Research Funding; 2022-PUMCH-C-010 the National High Level Hospital Clinical Research Funding; 2022-PUMCH-C-022 the National High Level Hospital Clinical Research Funding; 2022-PUMCH-D-003 the National High Level Hospital Clinical Research Funding; UHB12577 Peking Union Medical College Hospital Young Reserve Talent Development Program
Substance Nomenclature:
0 (Oncogene Proteins, Viral)
0 (Capsid Proteins)
0 (Papillomavirus E7 Proteins)
0 (Codon)
0 (Capsid Proteins)
0 (Papillomavirus E7 Proteins)
0 (Codon)
Entry Date(s):
Date Created: 20250829 Date Completed: 20250829 Latest Revision: 20250919
Update Code:
20250919
DOI:
10.1007/s00284-025-04468-8
PMID:
40879819
Database:
MEDLINE
Weitere Informationen
This study investigates the codon usage preferences of papillomaviruses across different hosts and examines the evolutionary relationships of key genes (L1, E6, and E7). Complete genome sequences of 86 papillomavirus strains were retrieved from the PaVE database. Phylogenetic trees were constructed using MAFFT and ITOL, and codon usage indices, including RSCU, ENC, CAI, and GC3, were calculated using CodonW. ENC-GC3, Neutrality, and PR2-bias analyses were conducted to explore the factors shaping codon usage patterns. The analyzed genomes were categorized into five groups (Clade1, Clade2, Clade3, Clade4, and Others), exhibiting variations in CAI and ENC values. Phylogenetic analysis revealed three distinct gene clusters. ENC-GC3, Neutrality, and PR2-bias analyses demonstrated that both natural selection and mutation pressure influence codon usage. These findings suggest that codon usage preferences and the evolutionary dynamics of L1, E6, and E7 genes differ across hosts, driven by a combination of selection and mutational forces.
(© 2025. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)
Declarations. Competing interests: All authors declare that they have no conflicts of interest to disclose. Ethical Approval: Not applicable. Informed Consent: Not applicable.