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Heterogeneity of class I and class II MHC sequences in Schistosoma japonicum from different endemic regions in mainland China

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Abstract

The present study examined sequence variation in class I and class II major histocompatibility complex (MHC) genes among Schistosoma japonicum isolates from different endemic regions in mainland China and assessed the level of horizontal gene transfer and sequence similarity between parasites and their hosts. S. japonicum cercariae were used to infect male adult rabbits to obtain adult S. japonicum samples. A portion of the class I MHC gene (pMHC I) and class II MHC genes (pMHC II) were amplified separately from individual adult trematodes by polymerase chain reaction and sequenced. Among all the examined isolates of S. japonicum, sequence differences between male and female parasites were 0.0–26.6% for pMHC I and 0.0–7.0% for pMHC II. Sequence variations between male and female parasites among different geographical locations from the mountainous areas were 1.1–26.6% for pMHC I and 1.5–3.0% for pMHC II. Sequence variations between samples from Yunnan and those from Sichuan were 2.7–23.5% for pMHC I and 1.1–3.7% for pMHC II. In the lake/marshland areas, sequence variations between male and female parasites among different geographical locations were 0.0–25.0% for pMHC I and 0.0–7.0% for pMHC II. Sequence variations between S. japonicum isolates from mountainous areas, and those from lake/marshland areas were 0.0–26.1% for pMHC I and 0.4–6.1% for pMHC II. BLASTN analysis indicated that all the pMHC II sequences showed high homology to a portion of exon 3 in rabbit MHC class II DP beta gene with more than 89% similarity, and all the pMHC I sequences except isolates in Yunnan (Eryuan) revealed high homology to the portion of exon 2 in rabbit MHC I gene with more than 81% similarity. Phylogenetic analysis showed no specific clustering comprising parasites from single geographical or endemic regions, and the paired parasites were even found in different clusters. These results demonstrated that pMHC I and II of S. japonicum isolates in mainland China existed heterogeneity, but the pMHC I, II, or combined sequences were not suitable markers for examining genetic relationship among different isolates from endemic regions in mainland China.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI–BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Chilton NB, Gasser RB, Beveridge I (1995) Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). Int J Parasitol 25:647–651

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP: phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Hernandez HJ, Wang Y, Tzellas N, Stadecker MJ (1997) Expression of class II, but not class I, major histocompatibility complex molecules is required for granuloma formation in infection with Schistosoma mansoni. Eur J Immunol 27:1170–1176

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Imase A, Kobayashi K, Ohmae H, Matsuda H, Iwamura Y (2001) Horizontal and vertical transmission of mouse class I MHC sequence in Schistosoma mansoni. Parasitology 123:163–168

    Article  CAS  PubMed  Google Scholar 

  • Imase A, Matsuda H, Irie Y, Iwamura Y (2003) Existence of host DNA sequences in schistosomes––horizontal and vertical transmission. Parasitol Int 52:369–373

    Article  CAS  PubMed  Google Scholar 

  • Imase A, Ohmae H, Iwamura Y, Kirinoki M, Matsuda H (2004) A comparative study on mouse MHC class I sequences detected in Schistosoma japonicum recovered from BALB/c (H–2d) and C57BL/6 (H–2b) mice. Southeast Asian J Trop Med Public Health 35:10–18

    CAS  PubMed  Google Scholar 

  • Iwamura Y, Yonekawa H, Irie Y (1995) Detection of host DNA sequences including the H–2 locus of the major histocompatibility complex in schistosomes. Parasitology 110:163–170

    Article  CAS  PubMed  Google Scholar 

  • Marche PN, Tykocinski ML, Max EE, Kindt TJ (1985) Structure of a functional rabbit class I MHC gene: similarity to human class I genes. Immunogenetics 21:71–82

    Article  CAS  PubMed  Google Scholar 

  • McGarvey ST, Zhou XN, Willingham AL 3rd, Feng Z, Olveda R (1999) The epidemiology and host–parasite relationships of Schistosoma japonicum in definitive hosts. Parasitol Today 15:214–215

    Article  CAS  PubMed  Google Scholar 

  • McManus DP, Ross AG, Williams GM, Sleigh AC, Wiest P, Erlich H, Trachtenberg E, Guanling W, McGarvey ST, Li YS, Waine GJ (2001) HLA class II antigens positively and negatively associated with hepatosplenic schistosomiasis in a Chinese population. Int J Parasitol 31:674–680

    Article  CAS  PubMed  Google Scholar 

  • Nelson GS (1975) Schistosomiasis. Charles C. Thomas, Springfield, Illinois, USA

    Google Scholar 

  • Okada A, Imase A, Matsuda H, Ohmae H, Hata H, Iwamura Y (2006) Heterogeneity of class I and class II MHC sequences in Schistosoma mansoni. Parasitol Res 99:21–27

    Article  PubMed  Google Scholar 

  • Page RD (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Ross AG, Sleigh AC, Li Y, Davis GM, Williams GM, Jiang Z, Feng Z, McManus DP (2001) Schistosomiasis in the People’s Republic of China: prospects and challenges for the 21st century. Clin Microbiol Rev 14:270–295

    Article  CAS  PubMed  Google Scholar 

  • Shrivastava J, Qian BZ, Mcvean G, Webster JP (2005) An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Mol Ecol 14:839–849

    Article  CAS  PubMed  Google Scholar 

  • Sittisombut N, Mordacq J, Knight KL (1988) Rabbit MHC. II. Sequence analysis of the R–DP alpha– and beta–genes. J Immunol 140:3237–3243

    CAS  PubMed  Google Scholar 

  • Strimmer K, Von Haeseler A (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969

    CAS  Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and other methods). Sinauer Associates, Sunderland, MA

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Tykocinski ML, Marche PN, Max EE, Kindt TJ (1984) Rabbit class I MHC genes: cDNA clones define full–length transcripts of an expressed gene and a putative pseudogene. J Immunol 133:2261–2269

    CAS  PubMed  Google Scholar 

  • Waine GJ, Ross AG, Williams GM, Sleigh AC, McManus DP (1998) HLA class II antigens are associated with resistance or susceptibility to hepatosplenic disease in a Chinese population infected with Schistosoma japonicum. Int J Parasitol 28:537–542

    Article  CAS  PubMed  Google Scholar 

  • Zhao GH, Mo XH, Zou FC, Li J, Weng YB, Lin RQ, Xia CM, Zhu XQ (2009a) Genetic variability among Schistosoma japonicum isolates from different endemic regions in China revealed by sequences of three mitochondrial DNA genes. Vet Parasitol 162:67–74

    Article  CAS  PubMed  Google Scholar 

  • Zhao GH, Li J, Zou FC, Mo XH, Yuan ZG, Lin RQ, Weng YB, Zhu XQ (2009b) ISSR, an effective molecular approach for studying genetic variability among Schistosoma japonicum isolates from different epidemic provinces in mainland China. Infect Genet Evol 9:903–907

    Article  CAS  PubMed  Google Scholar 

  • Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, Chen XY, Zheng J, Utzinger J (2005) The public health significance and control of schistosomiasis in China–then and now. Acta Trop 96:97–105

    Article  PubMed  Google Scholar 

  • Zhou P, Chen N, Zhang RL, Lin RQ, Zhu XQ (2008) Food–borne parasitic zoonoses in China: perspective for control. Trends Parasitol 24:190–196

    Article  PubMed  Google Scholar 

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Acknowledgments

This work is supported in part by the National Basic Research Program (973 program) of China (grant number 2007CB513104) and the Program for Changjiang Scholars and Innovative Research Team in University (grant number IRT0723). Professor Baozhen Qian of Bioengineering Institute, Zhejiang Academy of Medical Sciences, China was thanked for providing some S. japonicum samples used in the present study. The experiments comply with the current laws of the country in which the experiments were performed.

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Correspondence to X. Q. Zhu.

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Zhao, G.H., Li, J., Zou, F.C. et al. Heterogeneity of class I and class II MHC sequences in Schistosoma japonicum from different endemic regions in mainland China. Parasitol Res 106, 201–206 (2009). https://doi.org/10.1007/s00436-009-1652-1

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  • DOI: https://doi.org/10.1007/s00436-009-1652-1

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