Skip to main content
SpringerLink
Log in

Association of ABCB9 and COL22A1 Gene Polymorphism with Human Predisposition to Severe Forms of Tick-Borne Encephalitis

  • HUMAN GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Tick-borne encephalitis (TBE) is caused by a neurotropic RNA virus from the Flavivirus genus. TBE is characterized by a significant variability of clinical manifestations from nonparalytic forms (fever, meningitis) to severe paralytic (focal) forms (meningoencephalitis, poliomyelitis, polioencephalomyelitis). The result of interaction between a virus and a host (and, consequently, the viral disease course and outcome) largely depends on genetically determined ability of the host (particularly, human) organism immune system to suppress the development of viral infection. However, hereditary predisposition to TBE has been rather poorly studied in human populations. In this study, the results of whole exome sequencing of DNA samples from 22 Russian non-immunized TBE patients with severe TBE forms and 17 control individuals from the same populations are presented. Sixteen single nucleotide polymorphisms (SNPs) associated with predisposition to severe forms of TBE were identified. The genotype and allele frequencies for three of these SNPs localized in the ABCB9 (rs4148866, G/A, intron), COL22A1 (rs4909444, G/T, Ala938Asp), and ITGAL (rs1557672, G/A, intron) genes were then studied in larger samples of patients with different forms of TBE (n = 177) and in the control population (n = 215). As a result, the association of the ABCB9 and COL22A1 gene SNPs with the development of severe forms of TBE was for the first time demonstrated in the Russian population. The hypothesis regarding a possible mechanism of the effect of the ABCB9 gene intronic SNP on the process of human infection with TBE virus is considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Gritsun, T.S., Lashkevich, V.A., and Gould, E.A., Tick-borne encephalitis, Antiviral Res., 2003, vol. 57, pp. 129—146. https://doi.org/10.1016/S0166-3542(02)00206-1

    Article  CAS  PubMed  Google Scholar 

  2. Ruzek, D., Dobler, G., and Donoso Mantke, O., Tick-borne encephalitis: pathogenesis and clinical implications, Travel Med. Infect. Dis., 2010, vol. 8, pp. 223—232. https://doi.org/10.1016/j.tmaid.2010.06.004

    Article  PubMed  Google Scholar 

  3. Suss, J., Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia—an overview, Ticks Tick-Borne Dis., 2011, vol. 2, pp. 2—15. https://doi.org/10.1016/j.ttbdis.2010.10.007

    Article  PubMed  Google Scholar 

  4. Bogovic, P. and Strle, F., Tick-borne encephalitis: a review of epidemiology, clinical characteristics, and management, World J. Clin. Cases, 2015, vol. 3, pp. 430—441. https://doi.org/10.12998/wjcc.v3.i5.430

    Article  PubMed  PubMed Central  Google Scholar 

  5. Chapman, S.J. and Hill, A.V., Human genetic susceptibility to infectious disease, Nat. Rev. Genet., 2012, vol. 13, pp. 175—188. https://doi.org/10.1038/nrg3114

    Article  CAS  PubMed  Google Scholar 

  6. Khor, C.C. and Hibberd, M.L., Host—pathogen interactions revealed by human genome-wide surveys, Trends Genet., 2012, vol. 28, pp. 233—243. https://doi.org/10.1016/j.tig.2012.02.001

    Article  CAS  PubMed  Google Scholar 

  7. Yudin, N.S., Barkhash, A.V., Maksimov, V.N., et al., Human genetic predisposition to diseases caused by viruses from Flaviviridae family, Mol. Biol. (Moscow), 2018, vol. 52, no. 2, pp. 165—181. https://doi.org/10.1134/S0026893317050223.

    Article  CAS  Google Scholar 

  8. Barkhash, A.V., Perelygin, A.A., Babenko, V.N., et al., Variability in the 2'-5'-oligoadenylate synthetase gene cluster is associated with human predisposition to tick-borne encephalitis virus-induced disease, J. Infect. Dis., 2010, vol. 202, no. 12, p. 9.

    Article  CAS  Google Scholar 

  9. Barkhash, A.V., Perelygin, A.A., Babenko, V.N., et al., Single nucleotide polymorphism in the promoter region of the CD209 gene is associated with human predisposition to severe forms of tick-borne encephalitis, Antiviral Res., 2012, vol. 93, no. 1, pp. 64—68. https://doi.org/10.1016/j.antiviral.2011.10.017

    Article  CAS  PubMed  Google Scholar 

  10. Barkhash, A.V., Voevoda, M.I., and Romaschenko, A.G., Association of single nucleotide polymorphism rs3775291 in the coding region of the TLR3 gene with predisposition to tick-borne encephalitis in a Russian population, Antiviral Res., 2013, vol. 99, no. 2, pp. 136—138. https://doi.org/10.1016/j.antiviral.2013.05.008

    Article  CAS  PubMed  Google Scholar 

  11. Barkhash, A.V., Babenko, V.N., Voevoda, M.I., and Romaschenko, A.G., Association of IL28B and IL10 gene polymorphism with predisposition to tick-borne encephalitis in a Russian population, Ticks Tick-Borne Dis., 2016, vol. 7, no. 5, pp. 808—812. https://doi.org/10.1016/j.ttbdis.2016.03.019

    Article  PubMed  Google Scholar 

  12. Barkhash, A.V., Yurchenko, A.A., Yudin, N.S., et al., A matrix metalloproteinase 9 (MMP9) gene single nucleotide polymorphism is associated with predisposition to tick-borne encephalitis virus-induced severe central nervous system disease, Ticks Tick-Borne Dis., 2018, vol. 9, no. 4, pp. 763—767. https://doi.org/10.1016/j.ttbdis.2018.02.010

    Article  PubMed  Google Scholar 

  13. Ovsyannikova, A.K., Rymar, O.D., Shakhtshneider, E.V., et al., ABCC8-related maturity-onset diabetes of the young (MODY12): clinical features and treatment perspective, Diabetes Ther., 2016, vol. 7, no. 3, pp. 591—600. https://doi.org/10.1007/s13300-016-0192-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Andrews, S., FastQC: A Quality Control Tool for High Throughput Sequence Data: Version 0.11.2, Cambridge, UK: Babraham Institute, 2014. http://www.bioinformatics.babraham.ac.uk/projects/fastqc.

  15. Bolger, A.M., Lohse, M., and Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 2014, vol. 30, no. 15, pp. 2114—2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Li, H. and Durbin, R., Fast and accurate short read alignment with Burrows—Wheeler transform, Bioinformatics, 2009, vol. 25, no. 14, pp. 1754—1760. https://doi.org/10.1093/bioinformatics/btp324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li, H., Handsaker, B., Wysoker, A., et al., The sequence alignment/map format and SAMtools, Bioinformatics, 2009, vol. 25, no. 16, pp. 2078—2079. https://doi.org/10.1093/bioinformatics/btp352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. McKenna, A., Hanna, M., Banks, E., et al., The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res., 2010, vol. 20, no. 9, pp. 1297—1303. https://doi.org/10.1101/gr.107524.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sherry, S.T., Ward, M.H., Kholodov, M., et al., dbSNP: the NCBI database of genetic variation, Nucleic Acids Res., 2001, vol. 29, no. 1, pp. 308—311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. International HapMap Consortium et al., A second generation human haplotype map of over 3.1 million SNPs, Nature, 2007, vol. 449, no. 7164, pp. 851—861.

  21. 1000 Genomes Project Consortium et al., An integrated map of genetic variation from 1092 human genomes, Nature, 2012, vol. 491, no. 7422, pp. 56—65. https://doi.org/10.1038/nature11632

  22. Mills, R.E., Pittard, W.S., Mullaney, J.M., et al., Natural genetic variation caused by small insertions and deletions in the human genome, Genome Res., 2011, vol. 21, no. 6, pp. 830—839. https://doi.org/10.1101/gr.115907.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wang, K., Li, M., and Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data, Nucleic Acids Res., 2010, vol. 38, no. 16. e164. https://doi.org/10.1093/nar/gkq603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Purcell, S., Neale, B., Todd-Brown, K., et al., PLINK: a tool set for whole-genome association and population-based linkage analyses, Am. J. Hum. Gen., 2007, vol. 81, no. 3, pp. 559—575.

    Article  CAS  Google Scholar 

  25. Neff, M.M., Turk, E., and Kalishman, M., Web-based primer design for single nucleotide polymorphism analysis, Trends Genet., 2002, vol. 18, no. 12, pp. 613—615. https://doi.org/10.1016/S0168-9525(02)02820-2

    Article  CAS  PubMed  Google Scholar 

  26. Zaykin, D.V. and Pudovkin, A.I., Two programs to estimate significance of χ2 values using pseudo-probability tests, J. Hered., 1993, vol. 84, p. 152.

    Article  Google Scholar 

  27. Guo, Y., Long, J., He, J., et al., Exome sequencing generates high quality data in non-target regions, BMC Genomics, 2012, vol. 13, p. 194. https://doi.org/10.1186/1471-2164-13-194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wang, Y., Shu, Y., Xiao, Y., et al., Hypomethylation and overexpression of ITGAL (CD11a) in CD4(+) T cells in systemic sclerosis, Clin. Epigenet., 2014, vol. 6, p. 25. https://doi.org/10.1186/1868-7083-6-25

    Article  CAS  Google Scholar 

  29. Gizaw, M. and Anandakumar, P., A review on ATP binding cassette (ABC) transporters, Int. J. Pharma Res. Health Sci., 2017, vol. 5, no. 2, pp. 1607—1615. https://doi.org/10.21276/ijprhs.2017.02.01

    Article  CAS  Google Scholar 

  30. Holland, I.B. and Blight, M.A., ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans, J. Mol. Biol., 1999, vol. 293, no. 2, pp. 381—399. https://doi.org/10.1006/jmbi.1999.2993

    Article  CAS  PubMed  Google Scholar 

  31. Jones, P.M. and George, A.M., The ABC transporter structure and mechanism: perspectives on recent research, Cell. Mol. Life Sci., 2004, vol. 61, no. 6, pp. 682—699. https://doi.org/10.1007/s00018-003-3336-9

    Article  CAS  PubMed  Google Scholar 

  32. Ohara, T., Ohashi-Kobayashi, A., and Maeda, M., Biochemical characterization of transporter associated with antigen processing (TAP)-like (ABCB9) expressed in insect cells, Biol. Pharm. Bull., 2008, vol. 31, no. 1, pp. 1—5. https://doi.org/10.1248/bpb.31.1

    Article  PubMed  Google Scholar 

  33. Bangert, I., Tumulka, F., and Abele, R., The lysosomal polypeptide transporter TAPL: more than a housekeeping factor? Biol. Chem., 2011, vol. 392, nos. 1—2. https://doi.org/10.1515/BC.2011.007

  34. Zollmann, T., Bock, C., Graab, P., and Abele, R., Team work at its best—TAPL and its two domains, Biol. Chem., 2015, vol. 396, nos. 9—10. https://doi.org/10.1515/hsz-2014-0319

  35. Kobayashi, A., Hori, S., Suita, N., and Maeda, M., Gene organization of human transporter associated with antigen processing-like (TAPL, ABCB9): analysis of alternative splicing variants and promoter activity, Biochem. Biophys. Res. Commun., 2003, vol. 309, no. 4, pp. 815—822. https://doi.org/10.1016/j.bbrc.2003.08.081

    Article  CAS  PubMed  Google Scholar 

  36. Zhao, C., Tampé, R., and Abele, R., TAP and TAP-like – brothers in arms?, Naunyn Schmiedebergs Arch. Pharmacol., 2006, vol. 372, no. 6, pp. 444—450. https://doi.org/10.1007/s00210-005-0028-z

    Article  CAS  PubMed  Google Scholar 

  37. Zhang, F., Zhang, W., Liu, L., et al., Characterization of ABCB9, an ATP binding cassette protein associated with lysosomes, J. Biol. Chem., 2000, vol. 275, no. 30, pp. 23287—23294. https://doi.org/10.1074/jbc.M001819200

    Article  CAS  PubMed  Google Scholar 

  38. Burset, M., Seledtsov, I.A., and Solovyev, V.V., SpliceDB: database of canonical and non-canonical mammalian splice sites, Nucleic Acids Res., 2001, vol. 29, no. 1, pp. 255—259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Förch, P., Merendino, L., Martínez, C., and Valcárcel, J., U2 small nuclear ribonucleoprotein particle (snRNP) auxiliary factor of 65 kDa, U2AF65, can promote U1 snRNP recruitment to 5' splice sites, Biochem J., 2003, vol. 372, pp. 235—240. https://doi.org/10.1042/BJ20021202

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lindenbach, B.D., Thiel, H.-J., and Rice, C.M., Flaviviridae: the viruses and their replication, in Fields Virology, Philadelphia: Lippincott-Raven, 2007, 5th ed., pp. 1101—1152.

    Google Scholar 

  41. Koch, M., Schulze, J., Hansen, U., et al., A novel marker of tissue junctions, collagen XXII, J. Biol. Chem., 2004, vol. 279, no. 21, pp. 22514—22521. https://doi.org/10.1074/jbc.M400536200

    Article  CAS  PubMed  Google Scholar 

  42. Charvet, B., Guiraud, A., Malbouyres, M., et al., Knockdown of col22a1 gene in zebrafish induces a muscular dystrophy by disruption of the myotendinous junction, Development, 2013, vol. 140, no. 22, pp. 4602—4613. https://doi.org/10.1242/dev.096024

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

This work was supported by the Russian Science Foundation (project no. 16-15-00127).

Author information

Authors and Affiliations

  1. Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, 630090 , Novosibirsk, Russia

    A. V. Barkhash, A. A. Yurchenko, N. S. Yudin, M. I. Voevoda & A. G. Romaschenko

  2. Novosibirsk State University, 630090, Novosibirsk, Russia

    N. S. Yudin & M. I. Voevoda

  3. Scientific Centre for Family Health and Human Reproduction Problems, 664003, Irkutsk, Russia

    I. V. Kozlova

  4. Irkutsk Regional Infectious Clinical Hospital, 664043, Irkutsk, Russia

    I. A. Borishchuk

  5. Scientific Research Institute of Medical Problems of the North, Federal Research Center Krasnoyarsk Science Center, Siberian Branch, Russian Academy of Sciences, 660022, Krasnoyarsk, Russia

    M. V. Smolnikova & O. I. Zaitseva

  6. City Infectious Clinical Hospital No. 1, 630099, Novosibirsk, Russia

    L. L. Pozdnyakova

Authors
  1. A. V. Barkhash
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Yurchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. S. Yudin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. V. Kozlova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. A. Borishchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. V. Smolnikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. O. I. Zaitseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. L. L. Pozdnyakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. I. Voevoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. A. G. Romaschenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. V. Barkhash.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement of compliance with standards of research involving humans as subjects. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This study was approved by the Bioethics Committee of the Institute of Cytology and Genetics (Siberian Branch, Russian Academy of Sciences). All patients gave written informed consent for participation in the study.

Additional information

Translated by A. Barkhash

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barkhash, A.V., Yurchenko, A.A., Yudin, N.S. et al. Association of ABCB9 and COL22A1 Gene Polymorphism with Human Predisposition to Severe Forms of Tick-Borne Encephalitis. Russ J Genet 55, 368–377 (2019). https://doi.org/10.1134/S1022795419030025

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795419030025

Keywords:

Search

Navigation