• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jvirolPermissionsJournals.ASM.orgJournalJV ArticleJournal InfoAuthorsReviewers
J Virol. May 1996; 70(5): 3127–3136.
PMCID: PMC190175

Intratype variation in 12 human papillomavirus types: a worldwide perspective.

Abstract

In this study, we have examined intratype human papillomavirus (HPV) sequence variation in a worldwide collection of cervical specimens. Twelve different HPV types including HPV-18, HPV-33, HPV-35, HPV-39, HPV-45, HPV-51, HPV-52, HPV-58, HPV-59, HPV-68 (ME180), MM9/PAP238A (recently designated HPV-73), and a novel partial genomic HPV sequence designated MM4/Wl3B were analyzed in this study. Cervical specimens were collected as part of epidemiological investigations conducted in New Mexico and an international study of invasive cervical cancer (IBSCC). Specimens from several countries including Argentina, Brazil, Bolivia, Benin, Cuba, Colombia, Chile, Germany, Mali, Panama, Paraguay, Spain, Algeria, Uganda, Guinea, Tanzania, Indonesia, Philippines, Thailand, and the United States were evaluated. Specimen DNAs were subjected to amplification with the MY09/11 L1 consensus PCR system. The PCR products were cloned, and an approximately 410-bp region in the L1 open reading frame was sequenced from 146 specimens (approximately 60,000 bp). Within a single HPV type, nucleotide diversity varied between 0.2 and 2.9% (i.e., between any pair of variants) and the majority of nucleotide changes were synonymous (amino acid conserving). These data provide information pertinent to HPV diagnostic probe development and are potentially relevant to future rational vaccine strategies. Similarly, amino acid diversity varied between 0 and 5.1%. Some of these amino acid changes may represent markers of intertype evolutionary relationships. Presuming that HPVs have evolved under the same constraints as their corresponding hosts, the limited genetic diversity observed for all HPVs studied to date may reflect an evolutionary bottleneck occurring in both virus and host populations.

Full Text

The Full Text of this article is available as a PDF (279K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bauer HM, Ting Y, Greer CE, Chambers JC, Tashiro CJ, Chimera J, Reingold A, Manos MM. Genital human papillomavirus infection in female university students as determined by a PCR-based method. JAMA. 1991 Jan 23;265(4):472–477. [PubMed]
  • Becker TM, Wheeler CM, McGough NS, Parmenter CA, Jordan SW, Stidley CA, McPherson RS, Dorin MH. Sexually transmitted diseases and other risk factors for cervical dysplasia among southwestern Hispanic and non-Hispanic white women. JAMA. 1994 Apr 20;271(15):1181–1188. [PubMed]
  • Berkhout RJ, Tieben LM, Smits HL, Bavinck JN, Vermeer BJ, ter Schegget J. Nested PCR approach for detection and typing of epidermodysplasia verruciformis-associated human papillomavirus types in cutaneous cancers from renal transplant recipients. J Clin Microbiol. 1995 Mar;33(3):690–695. [PMC free article] [PubMed]
  • Bernard HU, Chan SY, Manos MM, Ong CK, Villa LL, Delius H, Peyton CL, Bauer HM, Wheeler CM. Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J Infect Dis. 1994 Nov;170(5):1077–1085. [PubMed]
  • Bosch FX, Manos MM, Muñoz N, Sherman M, Jansen AM, Peto J, Schiffman MH, Moreno V, Kurman R, Shah KV. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J Natl Cancer Inst. 1995 Jun 7;87(11):796–802. [PubMed]
  • Brown WM, George M, Jr, Wilson AC. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. [PMC free article] [PubMed]
  • Cann RL, Stoneking M, Wilson AC. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. [PubMed]
  • Chan SY, Delius H, Halpern AL, Bernard HU. Analysis of genomic sequences of 95 papillomavirus types: uniting typing, phylogeny, and taxonomy. J Virol. 1995 May;69(5):3074–3083. [PMC free article] [PubMed]
  • Chan SY, Ho L, Ong CK, Chow V, Drescher B, Dürst M, ter Meulen J, Villa L, Luande J, Mgaya HN, et al. Molecular variants of human papillomavirus type 16 from four continents suggest ancient pandemic spread of the virus and its coevolution with humankind. J Virol. 1992 Apr;66(4):2057–2066. [PMC free article] [PubMed]
  • Cole ST, Danos O. Nucleotide sequence and comparative analysis of the human papillomavirus type 18 genome. Phylogeny of papillomaviruses and repeated structure of the E6 and E7 gene products. J Mol Biol. 1987 Feb 20;193(4):599–608. [PubMed]
  • Deau MC, Favre M, Jablonska S, Rueda LA, Orth G. Genetic heterogeneity of oncogenic human papillomavirus type 5 (HPV5) and phylogeny of HPV5 variants associated with epidermodysplasia verruciformis. J Clin Microbiol. 1993 Nov;31(11):2918–2926. [PMC free article] [PubMed]
  • Deau MC, Favre M, Orth G. Genetic heterogeneity among human papillomaviruses (HPV) associated with epidermodysplasia verruciformis: evidence for multiple allelic forms of HPV5 and HPV8 E6 genes. Virology. 1991 Oct;184(2):492–503. [PubMed]
  • Delius H, Hofmann B. Primer-directed sequencing of human papillomavirus types. Curr Top Microbiol Immunol. 1994;186:13–31. [PubMed]
  • de Villiers EM. Heterogeneity of the human papillomavirus group. J Virol. 1989 Nov;63(11):4898–4903. [PMC free article] [PubMed]
  • de Villiers EM. Human pathogenic papillomavirus types: an update. Curr Top Microbiol Immunol. 1994;186:1–12. [PubMed]
  • Dürst M, Gissmann L, Ikenberg H, zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812–3815. [PMC free article] [PubMed]
  • Eckert KA, Kunkel TA. DNA polymerase fidelity and the polymerase chain reaction. PCR Methods Appl. 1991 Aug;1(1):17–24. [PubMed]
  • Ellis JR, Keating PJ, Baird J, Hounsell EF, Renouf DV, Rowe M, Hopkins D, Duggan-Keen MF, Bartholomew JS, Young LS, et al. The association of an HPV16 oncogene variant with HLA-B7 has implications for vaccine design in cervical cancer. Nat Med. 1995 May;1(5):464–470. [PubMed]
  • Eluf-Neto J, Booth M, Muñoz N, Bosch FX, Meijer CJ, Walboomers JM. Human papillomavirus and invasive cervical cancer in Brazil. Br J Cancer. 1994 Jan;69(1):114–119. [PMC free article] [PubMed]
  • Eschle D, Dürst M, ter Meulen J, Luande J, Eberhardt HC, Pawlita M, Gissmann L. Geographical dependence of sequence variation in the E7 gene of human papillomavirus type 16. J Gen Virol. 1992 Jul;73(Pt 7):1829–1832. [PubMed]
  • Gibbons A. Mitochondrial Eve: wounded, but not dead yet. Science. 1992 Aug 14;257(5072):873–875. [PubMed]
  • Giles RE, Blanc H, Cann HM, Wallace DC. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6715–6719. [PMC free article] [PubMed]
  • Hecht JL, Kadish AS, Jiang G, Burk RD. Genetic characterization of the human papillomavirus (HPV) 18 E2 gene in clinical specimens suggests the presence of a subtype with decreased oncogenic potential. Int J Cancer. 1995 Jan 27;60(3):369–376. [PubMed]
  • Hedges SB, Kumar S, Tamura K, Stoneking M. Human origins and analysis of mitochondrial DNA sequences. Science. 1992 Feb 7;255(5045):737–739. [PubMed]
  • Heinzel PA, Chan SY, Ho L, O'Connor M, Balaram P, Campo MS, Fujinaga K, Kiviat N, Kuypers J, Pfister H, et al. Variation of human papillomavirus type 6 (HPV-6) and HPV-11 genomes sampled throughout the world. J Clin Microbiol. 1995 Jul;33(7):1746–1754. [PMC free article] [PubMed]
  • Hildesheim A, Schiffman MH, Gravitt PE, Glass AG, Greer CE, Zhang T, Scott DR, Rush BB, Lawler P, Sherman ME, et al. Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis. 1994 Feb;169(2):235–240. [PubMed]
  • Ho L, Chan SY, Burk RD, Das BC, Fujinaga K, Icenogle JP, Kahn T, Kiviat N, Lancaster W, Mavromara-Nazos P, et al. The genetic drift of human papillomavirus type 16 is a means of reconstructing prehistoric viral spread and the movement of ancient human populations. J Virol. 1993 Nov;67(11):6413–6423. [PMC free article] [PubMed]
  • Ho L, Chan SY, Chow V, Chong T, Tay SK, Villa LL, Bernard HU. Sequence variants of human papillomavirus type 16 in clinical samples permit verification and extension of epidemiological studies and construction of a phylogenetic tree. J Clin Microbiol. 1991 Sep;29(9):1765–1772. [PMC free article] [PubMed]
  • Icenogle JP, Sathya P, Miller DL, Tucker RA, Rawls WE. Nucleotide and amino acid sequence variation in the L1 and E7 open reading frames of human papillomavirus type 6 and type 16. Virology. 1991 Sep;184(1):101–107. [PubMed]
  • Jacobs MV, de Roda Husman AM, van den Brule AJ, Snijders PJ, Meijer CJ, Walboomers JM. Group-specific differentiation between high- and low-risk human papillomavirus genotypes by general primer-mediated PCR and two cocktails of oligonucleotide probes. J Clin Microbiol. 1995 Apr;33(4):901–905. [PMC free article] [PubMed]
  • Kitasato H, Delius H, zur Hausen H, Sorger K, Rösl F, de Villiers EM. Sequence rearrangements in the upstream regulatory region of human papillomavirus type 6: are these involved in malignant transition? J Gen Virol. 1994 May;75(Pt 5):1157–1162. [PubMed]
  • Lowy DR, Kirnbauer R, Schiller JT. Genital human papillomavirus infection. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2436–2440. [PMC free article] [PubMed]
  • Manos MM, Waldman J, Zhang TY, Greer CE, Eichinger G, Schiffman MH, Wheeler CM. Epidemiology and partial nucleotide sequence of four novel genital human papillomaviruses. J Infect Dis. 1994 Nov;170(5):1096–1099. [PubMed]
  • Muñoz N, Bosch FX, de Sanjosé S, Tafur L, Izarzugaza I, Gili M, Viladiu P, Navarro C, Martos C, Ascunce N, et al. The causal link between human papillomavirus and invasive cervical cancer: a population-based case-control study in Colombia and Spain. Int J Cancer. 1992 Nov 11;52(5):743–749. [PubMed]
  • Ong CK, Chan SY, Campo MS, Fujinaga K, Mavromara-Nazos P, Labropoulou V, Pfister H, Tay SK, ter Meulen J, Villa LL, et al. Evolution of human papillomavirus type 18: an ancient phylogenetic root in Africa and intratype diversity reflect coevolution with human ethnic groups. J Virol. 1993 Nov;67(11):6424–6431. [PMC free article] [PubMed]
  • Peyton CL, Jansen AM, Wheeler CM, Stewart AC, Peto J, Bosch FX, Muñoz N, Teyssie AR, Torroella M, Wabinga HR. A novel human papillomavirus sequence from an international cervical cancer study. J Infect Dis. 1994 Nov;170(5):1093–1095. [PubMed]
  • Peyton CL, Wheeler CM. Identification of five novel human papillomavirus sequences in the New Mexico triethnic population. J Infect Dis. 1994 Nov;170(5):1089–1092. [PubMed]
  • Pushko P, Sasagawa T, Cuzick J, Crawford L. Sequence variation in the capsid protein genes of human papillomavirus type 16. J Gen Virol. 1994 Apr;75(Pt 4):911–916. [PubMed]
  • Reuter S, Delius H, Kahn T, Hofmann B, zur Hausen H, Schwarz E. Characterization of a novel human papillomavirus DNA in the cervical carcinoma cell line ME180. J Virol. 1991 Oct;65(10):5564–5568. [PMC free article] [PubMed]
  • de Roda Husman AM, Walboomers JM, Meijer CJ, Risse EK, Schipper ME, Helmerhorst TM, Bleker OP, Delius H, van den Brule AJ, Snijders PJ. Analysis of cytomorphologically abnormal cervical scrapes for the presence of 27 mucosotropic human papillomavirus genotypes, using polymerase chain reaction. Int J Cancer. 1994 Mar 15;56(6):802–806. [PubMed]
  • Rogers AR, Harpending H. Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol. 1992 May;9(3):552–569. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Schiffman MH, Bauer HM, Hoover RN, Glass AG, Cadell DM, Rush BB, Scott DR, Sherman ME, Kurman RJ, Wacholder S, et al. Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst. 1993 Jun 16;85(12):958–964. [PubMed]
  • Schiffman MH, Bauer HM, Lorincz AT, Manos MM, Byrne JC, Glass AG, Cadell DM, Howley PM. Comparison of Southern blot hybridization and polymerase chain reaction methods for the detection of human papillomavirus DNA. J Clin Microbiol. 1991 Mar;29(3):573–577. [PMC free article] [PubMed]
  • Schiffman MH, Kiviat NB, Burk RD, Shah KV, Daniel RW, Lewis R, Kuypers J, Manos MM, Scott DR, Sherman ME, et al. Accuracy and interlaboratory reliability of human papillomavirus DNA testing by hybrid capture. J Clin Microbiol. 1995 Mar;33(3):545–550. [PMC free article] [PubMed]
  • Shadan FF, Villarreal LP. Coevolution of persistently infecting small DNA viruses and their hosts linked to host-interactive regulatory domains. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4117–4121. [PMC free article] [PubMed]
  • Shamanin V, Glover M, Rausch C, Proby C, Leigh IM, zur Hausen H, de Villiers EM. Specific types of human papillomavirus found in benign proliferations and carcinomas of the skin in immunosuppressed patients. Cancer Res. 1994 Sep 1;54(17):4610–4613. [PubMed]
  • Smits HL, Traanberg KF, Krul MR, Prussia PR, Kuiken CL, Jebbink MF, Kleyne JA, van den Berg RH, Capone B, de Bruyn A, et al. Identification of a unique group of human papillomavirus type 16 sequence variants among clinical isolates from Barbados. J Gen Virol. 1994 Sep;75(Pt 9):2457–2462. [PubMed]
  • Snijders PJ, van den Brule AJ, Schrijnemakers HF, Snow G, Meijer CJ, Walboomers JM. The use of general primers in the polymerase chain reaction permits the detection of a broad spectrum of human papillomavirus genotypes. J Gen Virol. 1990 Jan;71(Pt 1):173–181. [PubMed]
  • Stewart AC, Gravitt PE, Cheng S, Wheeler CM. Generation of entire human papillomavirus genomes by long PCR: frequency of errors produced during amplification. Genome Res. 1995 Aug;5(1):79–88. [PubMed]
  • Templeton AR. Human origins and analysis of mitochondrial DNA sequences. Science. 1992 Feb 7;255(5045):737–737. [PubMed]
  • van den Brule AJ, Meijer CJ, Bakels V, Kenemans P, Walboomers JM. Rapid detection of human papillomavirus in cervical scrapes by combined general primer-mediated and type-specific polymerase chain reaction. J Clin Microbiol. 1990 Dec;28(12):2739–2743. [PMC free article] [PubMed]
  • van den Brule AJ, Snijders PJ, Raaphorst PM, Schrijnemakers HF, Delius H, Gissmann L, Meijer CJ, Walboomers JM. General primer polymerase chain reaction in combination with sequence analysis for identification of potentially novel human papillomavirus genotypes in cervical lesions. J Clin Microbiol. 1992 Jul;30(7):1716–1721. [PMC free article] [PubMed]
  • Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC. African populations and the evolution of human mitochondrial DNA. Science. 1991 Sep 27;253(5027):1503–1507. [PubMed]
  • Wheeler CM, Parmenter CA, Hunt WC, Becker TM, Greer CE, Hildesheim A, Manos MM. Determinants of genital human papillomavirus infection among cytologically normal women attending the University of New Mexico student health center. Sex Transm Dis. 1993 Sep-Oct;20(5):286–289. [PubMed]
  • Xi LF, Demers W, Kiviat NB, Kuypers J, Beckmann AM, Galloway DA. Sequence variation in the noncoding region of human papillomavirus type 16 detected by single-strand conformation polymorphism analysis. J Infect Dis. 1993 Sep;168(3):610–617. [PubMed]
  • 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 Dec;69(12):7743–7753. [PMC free article] [PubMed]
  • zur Hausen H. Viruses in human cancers. Science. 1991 Nov 22;254(5035):1167–1173. [PubMed]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...