Genetic diversity of JC virus in the Saami and the Finns: Implications for their population history
Corresponding Author
Hiroshi Ikegaya
Department of Forensic Medicine, University of Turku, Turku, Finland 20520
Department of Forensic Medicine, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanSearch for more papers by this authorHuai-Ying Zheng
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorPekka J. Saukko
Department of Forensic Medicine, University of Turku, Turku, Finland 20520
Search for more papers by this authorLeena Varesmaa-Korhonen
Ivalo Health Center, Ivalo, Finland 99800
Search for more papers by this authorTapani Hovi
Department of Microbiology, National Public Health Institute, Mannerheimintie, Helsinki, Finland 00300
Search for more papers by this authorTimo Vesikari
Department of Virology and Vaccine Research, University of Tampere Medical School, Tampere, Finland 33014
Search for more papers by this authorHideki Suganami
Graduate Course of Biomedical Statistics, Tokyo University of Science, Tokyo, Japan162-8602
Search for more papers by this authorTomokazu Takasaka
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorChie Sugimoto
Tsukuba Primate Center for Medical Science, National Institute of Infectious Diseases, Tsukuba, Japan 305-0843
Search for more papers by this authorYasuo Ohasi
Department of Biostatistics/Epidemiology and Preventive Health Science, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorTadaichi Kitamura
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorYoshiaki Yogo
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorCorresponding Author
Hiroshi Ikegaya
Department of Forensic Medicine, University of Turku, Turku, Finland 20520
Department of Forensic Medicine, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanSearch for more papers by this authorHuai-Ying Zheng
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorPekka J. Saukko
Department of Forensic Medicine, University of Turku, Turku, Finland 20520
Search for more papers by this authorLeena Varesmaa-Korhonen
Ivalo Health Center, Ivalo, Finland 99800
Search for more papers by this authorTapani Hovi
Department of Microbiology, National Public Health Institute, Mannerheimintie, Helsinki, Finland 00300
Search for more papers by this authorTimo Vesikari
Department of Virology and Vaccine Research, University of Tampere Medical School, Tampere, Finland 33014
Search for more papers by this authorHideki Suganami
Graduate Course of Biomedical Statistics, Tokyo University of Science, Tokyo, Japan162-8602
Search for more papers by this authorTomokazu Takasaka
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorChie Sugimoto
Tsukuba Primate Center for Medical Science, National Institute of Infectious Diseases, Tsukuba, Japan 305-0843
Search for more papers by this authorYasuo Ohasi
Department of Biostatistics/Epidemiology and Preventive Health Science, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorTadaichi Kitamura
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorYoshiaki Yogo
Department of Urology, Faculty of Medicine, University of Tokyo, Tokyo, Japan 113-0033
Search for more papers by this authorAbstract
The JC virus (JCV) genotyping method was used to gain insights into the population history of the Saami and the Finns, both speaking Finno-Ugric languages and living in close geographic proximity. Urine samples from Saami and Finns, collected in northern and southern Finland, respectively, were used to amplify a 610-bp JCV-DNA region containing abundant type-specific mutations. Based on restriction site polymorphisms in the amplified fragments, we classified JCV isolates into one of the three superclusters of JCV, type A, B, or C. All 15 Saami isolates analyzed and 41 of 43 Finnish isolates analyzed were classified as type A, the European type, and two samples from Finns were classified as type B, the African/Asian type. We then amplified and sequenced a 583-bp JCV-DNA region from the type A isolates of Saami and Finns. According to type-determining nucleotides within the region, we classified type A isolates into EU-a1, -a2, or -b. Most type A isolates from Saami were classified as EU-a1, while type A isolates from Finns were distributed among EU-a1, EU-a2, and EU-b. This trend in the JCV-genotype distribution was statistically significant. On a phylogenetic tree based on complete sequences, most of the type A isolates from Saami were clustered in a single clade within EU-a1, while those from Finns were distributed throughout EU-a1, EU-a2, and EU-b. These findings are discussed in the context of the population history of the Saami and the Finns. This study provides new complete JCV DNA sequences derived from populations of anthropological interest. Am J Phys Anthropol 128:185-193, 2005. © 2005 Wiley-Liss, Inc.
LITERATURE CITED
- Agostini HT, Ryschkewitsch CF, Stoner GL. 1996. Genotype profile of human polyomavirus JC excreted in urine of immunocompetent individuals. J Clin Microbiol 34: 159–164.
- Agostini HT, Yanagihara R, Davis V, Ryschkewitsch CF, Stoner GL. 1997. Asian genotypes of JC virus in Native Americans and in a Pacific Island population: markers of viral evolution and human migration. Proc Natl Acad Sci USA 94: 14542–14546.
- Agostini HT, Ryschkewitsch CF, Stoner GL. 1998. JC virus type 1 has multiple subtypes: three new complete genomes. J Gen Virol 79: 801–805.
-
Agostini HT,
Jobes DV,
Stoner GL.
2001a.
Molecular evolution and epidemiology of JC virus. In:
K Khalili,
GL Stoner, editors.
Human polyomaviruses: molecular and clinical perspectives.
New York:
John Wiley & Sons. p
491–526.
10.1002/0471221945.ch18 Google Scholar
- Agostini HT, Deckhut A, Jobes DV, Girones R, Schlunck G, Prost MG, Frias C, Perez-Trallero E, Ryschkewitsch CF, Stoner GL. 2001b. Genotypes of JC virus in East, Central and Southwest Europe. J Gen Virol 82: 1221–1231.
-
Agresti A.
2002.
Categorical data analysis,
2nd ed.
New York:
Wiley-Interscience. p
82–83.
10.1002/0471249688 Google Scholar
- Ault GS, Stoner GL. 1992. Two major types of JC virus defined in progressive multifocal leukoencephalopathy brain by early and late coding region DNA sequences. J Gen Virol 73: 2669–2678.
- Chesters PM, Heritage J, McCance DJ. 1983. Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. J Infect Dis 147: 676–684.
- Chima SC, Ryschkewitsch CF, Stoner GL. 1998. Molecular epidemiology of human polyomavirus JC in Biaka Pygmies and Bantu of Central Africa. Mem Inst Oswaldo Cruz 93: 615–623.
- Cole CN, Conzen SD. 2001. Polyomaviridae: the viruses and their replication. In: DM Knipe, PM Howley, DE Griffin, MA Martin, RA Lamb, B Roizman, SE Straus, editors. Fields virology, 4th ed. Philadelphia: Lippincott Williams & Wilkins. p 2141–2173.
- Disotell TR. 2003. Discovering human history from stomach bacteria. Genome Biol 4: 213.
- Dubois V, Moret H, Lafon ME, Brodard V, Icart J, Ruffault A, Guist'hau O, Buffet-Janvresse C, Abbed K, Dussaix E, Ingrand D. 2001. JC virus genotypes in France: molecular epidemiology and potential significance for progressive multifocal leukoencephalopathy. J Infect Dis 183: 213–217.
- Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
- Fernandez-Cobo M, Agostini HT, Britez G, Ryschkewitsch CF, Stoner GL. 2002. Strains of JC virus in Amerind-speakers of North America (Salish) and South America (Guarani), Na-Dene-speakers of New Mexico (Navajo), and modern Japanese suggest links through an ancestral Asian population. Am J Phys Anthropol 118: 154–168.
- Finnilä S, Hassinen IE, Ala-Kokko L, Majamaa K. 2000. Phylogenetic network of the mtDNA haplogroup U in northern Finland based on sequence analysis of the complete coding region by conformation-sensitive gel electrophoresis. Am J Hum Genet 66: 1017–1026.
- Frisque RJ, Bream GL, Cannella MT. 1984. Human polyomavirus JC virus genome. J Virol 51: 458–469.
- Guo J, Sugimoto C, Kitamura T, Ebihara H, Kato A, Guo Z, Liu J, Zheng SP, Wang YL, Na YQ, Suzuki M, Taguchi F, Yogo Y. 1998. Four geographically distinct genotypes of JC virus are prevalent in China and Mongolia: implications for the racial composition of modern China. J Gen Virol 79: 2499–2505.
- Hatwell JN, Sharp PM. 2000. Evolution of human polyomavirus JC. J Gen Virol 81: 1191—1200.
-
Hills DM,
Bull JJ.
1993.
An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis.
Syst Biol
42:
182–192.
10.1093/sysbio/42.2.182 Google Scholar
- Jobes DV, Friedlaender JS, Mgone CS, Agostini HT, Koki G, Yanagihara R, Ng TCN, Chima SC, Ryschkewitsch CF, Stoner GL. 2001. New JC virus (JCV) genotypes from Papua New Guinea and Micronesia (type 8 and type 2E) and evolutionary analysis of 32 complete JCV genomes. Arch Virol 146: 2097–2113.
- Kato A, Kitamura T, Sugimoto C, Ogawa Y, Nakazato K, Nagashima K, Hall WW, Kawabe K, Yogo Y. 1997. Lack of evidence for the transmission of JC polyomavirus between human populations. Arch Virol 142: 875–882.
- Kato A, Sugimoto C, Zheng H-Y, Kitamura T, Yogo Y. 2000. Lack of disease-specific amino acid changes in the viral proteins of JC virus isolates from the brain with progressive multifocal leukoencephalopathy. Arch Virol 145: 2173–2182.
- Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111–120.
- Kitamura T, Aso Y, Kuniyoshi N, Hara K, Yogo Y. 1990. High incidence of urinary JC virus excretion in nonimmunosuppressed older patients. J Infect Dis 161: 1128–1133.
- Kitamura T, Kunitake T, Guo J, Tominaga T, Kawabe K, Yogo Y. 1994. Transmission of the human polyomavirus JC virus occurs both within the family and outside the family. J Clin Microbiol 32: 2359–2363.
- Kitamura T, Sugimoto C, Kato A, Ebihara H, Suzuki M, Taguchi F, Kawabe K, Yogo Y. 1997. Persistent JC virus (JCV) infection is demonstrated by continuous shedding of the same JCV strains. J Clin Microbiol 35: 1255–1257.
- Kitamura T, Sugimoto C, Ebihara H, Kato A, Guo J, Taguchi F, Tominaga T, Ogawa Y, Ohta N, Kizu N, Imamura K, Funaki H, Kurosawa T, Ichikawa S, Suzuki T, Chiba K, Nagashima K, Yasumoto S, Yogo Y. 1998. Peopling of Japan as revealed by genotyping of urinary JC virus DNA. Anthropol Sci 106: 311–325.
-
Kittles RA,
Bergen AW,
Urbanek M,
Virkkunen M,
Linnoila M,
Goldman D,
Long JC.
1999.
Autosomal, mitochondrial, and Y chromosome DNA variation in Finland: evidence for a male-specific bottleneck.
Am J Phys Anthropol
108:
381–399.
10.1002/(SICI)1096-8644(199904)108:4<381::AID-AJPA1>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- Kunitake T, Kitamura T, Guo J, Taguchi F, Kawabe K, Yogo Y. 1995. Parent-to-child transmission is relatively common in the spread of the human polyomavirus JC virus. J Clin Microbiol 33: 1448–1451.
- Lahermo P, Sajantila A, Sistonen P, Lukka M, Aula P, Peltonen L, Savontaus ML. 1996. The genetic relationship between the Finns and the Finnish Saami (Lapps): analysis of nuclear DNA and mtDNA. Am J Hum Genet 58: 1309–1322.
- Lahermo P, Savontaus ML, Sistonen P, Beres J, de Knijff P, Aula P, Sajantila A. 1999. Y chromosomal polymorphisms reveal founding lineages in the Finns and the Saami. Eur J Hum Genet 7: 447–458.
- Meinilä M, Finnilä S, Majamaa K. 2001. Evidence for mtDNA admixture between the Finns and the Saami. Hum Hered 52: 160–170.
- Miranda JJ, Sugimoto C, Paraguison R, Takasaka T, Zheng H-Y, Yogo Y. 2003. Genetic diversity of JC virus in the modern Filipino population: implications for the peopling of the Philippines. Am J Phys Anthropol 120: 125–132.
- Padgett BL, Walker DL. 1973. Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. J Infect Dis 127: 467–470.
- Pagani E, Delbue S, Mancuso R, Borghi E, Tarantini L, Ferrante P. 2003. Molecular analysis of JC virus genotypes circulating among the Italian healthy population. J Neurovirol 9: 559–566.
- Page RD. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358.
- Pavesi A. 2003. African origin of polyomavirus JC and implications for prehistoric human migrations. J Mol Evol 56: 564–572.
- Rosser ZH, Zerjal T, Hurles ME, Adojaan M, Alavantic D, Amorim A, Amos W, Armenteros M, Arroyo E, Barbujani G, Beckman G, Beckman L, Bertranpetit J, Bosch E, Bradley DG, Brede G, Cooper G, Corte-Real HB, de Knijff P, Decorte R, Dubrova YE, Evgrafov O, Gilissen A, Glisic S, Golge M, Hill EW, Jeziorowska A, Kalaydjieva L, Kayser M, Kivisild T, Kravchenko SA, Krumina A, Kucinskas V, Lavinha J, Livshits LA, Malaspina P, Maria S, McElreavey K, Meitinger TA, Mikelsaar AV, Mitchell RJ, Nafa K, Nicholson J, Norby S, Pandya A, Parik J, Patsalis PC, Pereira L, Peterlin B, Pielberg G, Prata MJ, Previdere C, Roewer L, Rootsi S, Rubinsztein DC, Saillard J, Santos FR, Stefanescu G, Sykes BC, Tolun A, Villems R, Tyler-Smith C, Jobling MA. 2000. Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language. Am J Hum Genet 67: 1526–1543.
- Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
- Sajantila A, Lahermo P, Anttinen T, Lukka M, Sistonen P, Savontaus ML, Aula P, Beckman L, Tranebjaerg L, Gedde-Dahl T, Issel-Tarver L, DiRienzo A, Pääbo S. 1995. Genes and languages in Europe: an analysis of mitochondrial lineages. Genome Res 5: 42–52.
- Saruwatari L, Zheng H-Y, Takasaka T, Sugimoto C, Sakai E, Bo Bo, Nwe Nwe Aung, Kitamura T, Yogo Y, Ohno N. 2002. Peopling of Myanmar as demonstrated by genotyping of urinary JC virus DNA. Anthropol Sci 110: 235–249.
- Simoni L, Calafell F, Pettener D, Bertranpetit J, Barbujani G. 2000. Geographic patterns of mtDNA diversity in Europe. Am J Hum Genet 66: 262–278.
- Sugimoto C, Kitamura T, Guo J, Al-Ahdal MN, Shchelkunov SN, Otova B, Ondrejka P, Chollet J-Y, El-Safi S, Ettayebi M, Grésenguet G, Kocagöz T, Chaiyarasamee S, Thant KZ, Thein S, Moe K, Kobayashi N, Taguchi F, Yogo Y. 1997. Typing of urinary JC virus DNA offers a novel means of tracing human migrations. Proc Natl Acad Sci USA 94: 9191–9196.
- Sugimoto C, Hasegawa M, Kato A, Zheng H-Y, Ebihara H, Taguchi F, Kitamura T, Yogo Y. 2002a. Evolution of human polyomavirus JC: implications for the population history of humans. J Mol Evol 54: 285–297.
- Sugimoto C, Hasegawa M, Zheng H-Y, Demenev V, Sekino Y, Kojima K, Honjo T, Kida H, Hovi T, Vesikari T, Schalken JA, Tomita K, Mitsunobu Y, Ikegaya H, Kobayashi N, Kitamura T, Yogo Y. 2002b. JC virus strains indigenous to northeastern Siberians and Canadian Inuits are unique but evolutionally related to those distributed throughout Europe and Mediterranean areas. J Mol Evol 55: 322–335.
- Suzuki M, Zheng H-Y, Takasaka T, Sugimoto C, Kitamura T, Beutler E, Yogo Y. 2002. Asian genotypes of JC virus in Japanese-Americans suggests familial transmission. J Virol 76: 10074–10078.
- Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
- Tominaga T, Yogo Y, Kitamura T, Aso Y. 1992. Persistence of archetypal JC virus DNA in normal renal tissue derived from tumor-bearing patients. Virology 186: 736–741.
- Torroni A, Huoponen K, Francalacci P, Petrozzi M, Morelli L, Scozzari R, Obinu D, Savontaus ML, Wallace DC. 1996. Classification of European mtDNAs from an analysis of three European populations. Genetics 144: 1835–1850.
- Torroni A, Bandelt HJ, D'Urbano L, Lahermo P, Moral P, Sellitto D, Rengo C, Forster P, Savontaus ML, Bonne-Tamir B, Scozzari R. 1998. mtDNA analysis reveals a major late Paleolithic population expansion from southwestern to northeastern Europe. Am J Hum Genet 62: 1137–1152.
- Torroni A, Bandelt HJ, Macaulay V, Richards M, Cruciani F, Rengo C, Martinez-Cabrera V, Villems R, Kivisild T, Metspalu E, Parik J, Tolk HV, Tambets K, Forster P, Karger B, Francalacci P, Rudan P, Janicijevic B, Rickards O, Savontaus ML, Huoponen K, Laitinen V, Koivumaki S, Sykes B, Hickey E, Novelletto A, Moral P, Sellitto D, Coppa A, Al-Zaheri N, Santachiara-Benerecetti AS, Semino O, Scozzari R. 2001. A signal, from human mtDNA, of postglacial recolonization in Europe. Am J Hum Genet 69: 844–852.
- Walker DL, Padgett BL. 1983. The epidemiology of human polyomaviruses. Prog Clin Biolo Res 105: 99–106.
- Yanagihara R, Nerurkar VR, Scheirich I, Agostini HT, Mgone CS, Cui X, Jobes DV, Cubitt CL, Ryschkewitsch CF, Hrdy DB, Friedlaender JS, Stoner GL. 2002. JC virus genotypes in the western Pacific suggest Asian mainland relationships and virus association with early population movements. Hum Biol 74: 473–488.
-
Yogo Y,
Sugimoto C.
2001.
The archetype concept and regulatory region rearrangement. In:
K Khalili,
GL Stoner, editors.
Human polyomaviruses: molecular and clinical perspectives.
New York:
John Wiley & Sons. p
127–148.
10.1002/0471221945.ch7 Google Scholar
- Yogo Y, Iida T, Taguchi F, Kitamura T, Aso Y. 1991. Typing of human polyomavirus JC virus on the basis of restriction fragment length polymorphisms. J Clin Microbiol 29: 2130–2138.
- Yogo Y, Zheng H-Y, Hasegawa M, Sugimoto C, Tanaka S, Honjo T, Kobayashi N, Ohta N, Kitamura T. 2003. Phylogenetic analysis of JC virus DNAs detected in Ainus: an attempt to elucidate the origin and diversity of the Ainu. Anthropol Sci (Jpn Ser) 111: 19–34.
- Zerjal T, Dashnyam B, Pandya A, Kayser M, Roewer L, Santos FR, Schiefenhovel W, Fretwell N, Jobling MA, Harihara S, Shimizu K, Semjidmaa D, Sajantila A, Salo P, Crawford MH, Ginter EK, Evgrafov OV, Tyler-Smith C. 1997. Genetic relationships of Asians and Northern Europeans, revealed by Y-chromosomal DNA analysis. Am J Hum Genet 60: 1174–1183.
- Zheng H-Y, Sugimoto C, Hasegawa M, Kobayashi N, Kanayama A, Rodas A, Mejia M, Nakamichi J, Guo J, Kitamura T, Yogo Y. 2003. Phylogenetic relationships among JC virus strains in Japanese/Koreans and Native Americans speaking Amerind or Na-Dene. J Mol Evol 56: 18–27.
- Zheng H-Y, Kitamura T, Takasaka T, Chen Q, Yogo Y. 2004. Unambiguous identification of JC polyomavirus strains transmitted from parents to children. Arch Virol 149: 261–273.
