Killer cell immunoglobulin-like receptor alleles influence susceptibility to occult hepatitis B infection in the West African population

Momeiyi Michee Bazie; Florencia Wendkuuni Djigma; Mahamoudou  Sanou; Pegdwendé Abel Sorgho; Abdoul Karim Ouattara; Dorcas Obiri-Yeboah; Nadège Kapieko; Herman Karim Sombie; Prosper Bado; Edwige Tampoubila Yelemkoure; Isabelle Touwendpoulimdé Kiendrebeogo; Marius Bolni Nagalo; Albert Théophane Yonli; Jacques Simpore

doi:10.4081/jphia.2023.2586

Authors

Momeiyi Michee Bazie Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou, Burkina Faso.
Florencia Wendkuuni Djigma
florencia.djigma@gmail.com
Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso. https://orcid.org/0000-0002-6895-6725
Mahamoudou Sanou Department of Pharmacy, Joseph Ki-Zerbo University, Ouagadougou, Burkina Faso.
Pegdwendé Abel Sorgho Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso.
Abdoul Karim Ouattara Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso.
Dorcas Obiri-Yeboah Department of Microbiology and Immunology, School of Medical Sciences, University of Cape Coast, Ghana.
Nadège Kapieko Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso.
Herman Karim Sombie Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso. https://orcid.org/0000-0001-6996-8990
Prosper Bado Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso. https://orcid.org/0000-0002-4317-5930
Edwige Tampoubila Yelemkoure Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry- Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso.
Isabelle Touwendpoulimdé Kiendrebeogo Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso. https://orcid.org/0000-0002-4684-4650
Marius Bolni Nagalo Division of Hematology and Oncology, Mayo Clinic, Scottsdale, Arizona, United States. https://orcid.org/0000-0002-2173-7912
Albert Théophane Yonli Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso.
Jacques Simpore Molecular Biology and Genetics Laboratory (LABIOGENE), Department of Biochemistry-Microbiology, Joseph Ki-Zerbo University, Ouagadougou; Pietro Annigoni Biomolecular Research Center (CERBA), Ouagadougou, Burkina Faso. https://orcid.org/0000-0002-0415-9161

Background. Occult hepatitis B infection (OBI) is a public health problem in Burkina Faso. OBI represents a risk factor for the development of cirrhosis and hepatocellular carcinoma (HCC). OBI could be due to mutant viruses undetectable by HBsAg assays or a strong suppression of viral replication and gene expression under the pression of the host immune system.

Objective. To investigate the role of killer cell immunoglobulin-like receptor (KIR) gene polymorphisms in patients with OBI in Burkina Faso compared to healthy and chronic hepatitis B subjects.

Methods. A total of 286 participants was recruited, including 42 cases of OBI, 110 cases of chronic hepatitis B and 134 HBV negative subjects. SSP-PCR was performed to search for the presence of KIR genes. The HBV viral load was determined by qPCR.

Results. The frequencies of the activator gene KIR2DS5 (p=0.045) and the pseudogene KIR2DP1 (p<0.001) in patients with OBI were higher than those in patients with chronic hepatitis. These genes are associated with susceptibility of occult hepatitis B infection. The frequencies of the inhibitory KIR gene KIR2DL3 (p=0.01) of patients with occult hepatitis B were lower than those in chronic hepatitis B patients. This gene KIR2DL3 is associated with protection against occult hepatitis B infection. Also, the frequencies of the inhibitory KIR genes KIR2DL2 (p<0.001), KIR2DL3 (p<0.001) and activators KIR2DS2 (p<0.001) in chronic hepatitis B patients were higher compared to the frequencies of the KIR genes in healthy subjects. These genes KIR2DL3, KIR2DL5 (A, B), KIR3DL3, KIR3DS1, KIR2DL2 and KIR2DS2 are thought to be genes associated with the susceptibility to OBI.

Conclusion. The KIR2DS5 and KIR2DP1 genes could be associated with susceptibility to OBI. As for the KIR gene KIR2DL3 could be associated with protection against occult hepatitis B infection.

Raimondo G, Pollicino T, Cacciola I, Squadrito G. Occult hepatitis B virus infection. J Hepatol. 2007;46:160–70. DOI: https://doi.org/10.1016/j.jhep.2006.10.007

Allain J, Candotti D. Diagnostic algorithm for HBV safe transfusion. Blood Transfus. 2009;7:174–82.

Feld J, Janssen HLA, Abbas Z, Elewaut A, Ferenci P, Isakov V, et al. World Gastroenterology Organisation Global Guideline Hepatitis B. J Clin Gastroenterol [Internet]. 2016;50(9):691–703. Available from: https://journals.lww.com/jcge/fulltext/2016/10000/World%7B%5C_%7DGastroenterology%7B%5C_%7DOrganisation%7B%5C_%7DGlobal.4.aspx DOI: https://doi.org/10.1097/MCG.0000000000000647

Pollicino T, Saitta C. Occult hepatitis B virus and hepatocellular carcinoma. World J Gastroenterol. 2014;20(20):5951–61. DOI: https://doi.org/10.3748/wjg.v20.i20.5951

OMS. Hepatitis B [Internet]. 2020. p. 1–9. Available from: https://www.who.int/news-room/fact-sheets/detail/hepatitis-b

Somda KS, Sermé AK, Coulibaly A, Cissé K, Sawadogo A, Sombié AR, et al. Hepatitis B Surface Antigen Should Not Be the Only Sought Marker to Distinguish Blood Donors towards Hepatitis B Virus Infection in High Prevalence Area. Open J Gastroenterol [Internet]. 2016;06(11):362–72. Available from: http://www.scirp.org/journal/doi.aspx?DOI=10.4236/ojgas.2016.611039 DOI: https://doi.org/10.4236/ojgas.2016.611039

Diarra B, Yonli AT, Sorgho PA, Compaore TR. Occult Hepatitis B Virus Infection and Associated Genotypes among HBsAg-negative Subjects in Burkina Faso. Mediterr J Hematol Infect Dis. 2018;10:1–9. DOI: https://doi.org/10.4084/mjhid.2018.007

Vallet-Pichard A, Pol S. L ’ hépatite B occulte. Virologie. 2008;12(2):87–94.

Xu R, Zhang X, Zhang W, Fang Y, Zheng S, Yu X. Association of Human APOBEC3 Cytidine Deaminases With the Generation of Hepatitis Virus B x Antigen Mutants and Hepatocellular Carcinoma. Hepatology. 2007;46(6):1810–20. DOI: https://doi.org/10.1002/hep.21893

Vivekanandan P, Daniel HD, Kannangai R, Martinez-murillo F, Torbenson M. Hepatitis B Virus Replication Induces Methylation of both Host and Viral DNA. J Virol. 2010;84(9):4321–9. DOI: https://doi.org/10.1128/JVI.02280-09

Yindom LM, Mendy M, Bodimeade C, Chambion C, Aka P, Whittle HC, et al. KIR content genotypes associate with carriage of hepatitis B surface antigen, e antigen and HBV viral load in Gambians. PLoS One. 2017;12(11):1–14. DOI: https://doi.org/10.1371/journal.pone.0188307

Trowsdale J. Genetic and Functional Relationships between MHC and NK Receptor Genes HLA class I and NK receptors are encoded within. Immunity. 2001;15:363–74. DOI: https://doi.org/10.1016/S1074-7613(01)00197-2

Kulkarni S, Martin MP, Carrington M. The Ying and Yang of HLA and KIR in Human Disease. Semin Immunol. 2008;20(6):343–52. DOI: https://doi.org/10.1016/j.smim.2008.06.003

Marsh SGE, Parham P, Dupont B, Geraghty DE, Trowsdale J, Middleton D, et al. Killer-cell immunoglobulin-like receptor (KIR) nomenclature report, 2002. Immunogenetics. 2003;55:220–6. DOI: https://doi.org/10.1007/s00251-003-0571-z

Vilches C, Parham P. KIR: Diverse, Rapidly Evolving Receptors of Innate and Adaptive Immunity. Annu Rev Immunol [Internet]. 2002;20(1):217–51. Available from: http://www.annualreviews.org/doi/10.1146/annurev.immunol.20.092501.134942 DOI: https://doi.org/10.1146/annurev.immunol.20.092501.134942

Robinson J, Halliwell JA, McWilliam H, Lopez R, Marsh SGE. IPD - The Immuno Polymorphism Database. Nucleic Acids Res. 2013;41(D1):1234–40. DOI: https://doi.org/10.1093/nar/gks1140

González-Galarza FF, Takeshita LYC, Santos EJM, Kempson F, Maia MHT, Da Silva ALS, et al. Allele frequency net 2015 update: New features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations. Nucleic Acids Res. 2015;43(D1):D784–8. DOI: https://doi.org/10.1093/nar/gku1166

Faure M, Long EO. KIR2DL4 (CD158d), an NK Cell-Activating Receptor with Inhibitory Potential. J Immunol. 2002;4:6208–14. DOI: https://doi.org/10.4049/jimmunol.168.12.6208

Uhrberg M, Parham P, Wernet P. Definition of gene content for nine common group B haplotypes of the Caucasoid population: KIR haplotypes contain between seven and eleven KIR genes. Immunogenetics. 2002;54(4):221–9. DOI: https://doi.org/10.1007/s00251-002-0463-7

Mcqueen KL, Dorighi KM, Guethlein LA, Wong R, Parham P. Donor-Recipient Combinations of Group A and B KIR Haplotypes and HLA Class I Ligand Affect the Outcome of HLA-Matched, Sibling Donor Hematopoietic Cell Transplantation. Hum Immunol. 2007;68(5):309–23. DOI: https://doi.org/10.1016/j.humimm.2007.01.019

Ashouri E, Farjadian S, Reed EF, Ghaderi A, Rajalingam R. KIR gene content diversity in four Iranian populations. Immunogenetics. 2009;61:483–92. DOI: https://doi.org/10.1007/s00251-009-0378-7

Sorgho PA, Martinson JJ, Djigma FW, Yonli AT, Nagalo BM, Compaore TR, et al. Insights into the interplay between KIR gene frequencies and chronic HBV infection in Burkina Faso. Mediterr J Hematol Infect Dis. 2018;10:11. DOI: https://doi.org/10.4084/mjhid.2018.060

Zhi-ming L, Yu-lian J, Zhao-lei F, Chun-xiao W, Zhen-fang D, Bing-chang Z, et al. Polymorphisms of Killer Cell Immunoglobulin-like Receptor Gene: Possible Association with Susceptibility to or Clearance of Hepatitis B Virus Infection in Chinese Han Population. Croat Med J [Internet]. 2007;48(6):800–7. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2213808/ DOI: https://doi.org/10.3325/cmj.2007.6.800

Kibar F, Ozturk OG, Ulu A, Erken E, Inal S, Dinkci S, et al. Role of KIR genes and genotypes in susceptibility to or protection against hepatitis B virus infection in a Turkish cohort. Med Sci Monit [Internet]. 2014;20:28–34. Available from: http://www.medscimonit.com/abstract/index/idArt/889893 DOI: https://doi.org/10.12659/MSM.889893

Hu K. A Practical Approach to Management of Chronic Hepatitis B. Int J Med Sci. 2005;2(1):17–23. DOI: https://doi.org/10.7150/ijms.2.17

Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1. DOI: https://doi.org/10.1093/nar/16.3.1215

Kulkarni S, Martin MP, Carrington M. KIR Genotyping by Multiplex PCR-SSP. Methods Mol Biol. 2010;612:365–75. DOI: https://doi.org/10.1007/978-1-60761-362-6_25

WHO. Lignes directrices pour la prévention, les soins et le traitement en faveur des personnes atteintes d’une infection à hépatite B chronique [Internet]. 2015. 176 p. Available from: http://apps.who.int/iris

Simpore J, Savadogo A, Ilboudo D, Nadambega MC, Esposito M, Yara J, et al. Toxoplasma gondii, HCV, and HBV seroprevalence and co-infection among HIV-positive and -negative pregnant women in Burkina Faso. J Med Virol [Internet]. 2006 Jun [cited 2018 May 20];78(6):730–3. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16628587 DOI: https://doi.org/10.1002/jmv.20615

Tao I, Compaoré TR, Diarra B, Djigma F, Zohoncon TM, Assih M, et al. Seroepidemiology of Hepatitis B and C Viruses in the General Population of Burkina Faso. Hepat Res Treat. 2014;5. DOI: https://doi.org/10.1155/2014/781843

Sanou AM, Benkirane K, Tinto B, Cissé A, Sagna T, Ilboudo AK, et al. Prevalence of Hepatitis B virus and Hepatitis D virus Coinfection in Western Burkina Faso and molecular characterization of the detected virus strains. Int J Infect Dis [Internet]. 2018;70:15–9. Available from: http://dx.doi.org/10.1016/j.ijid.2018.02.004 DOI: https://doi.org/10.1016/j.ijid.2018.02.004

INSD. Emploi et chômage: Enquête multisectorielle continue (EMC) [Internet]. 2014. Available from: www.insd.bf

Carrington M, Norman P. The KIR Gene Cluster [Internet]. National Center for Biotechnology Information (US). 2003. 227 p. Available from: https://www.ncbi.nlm.nih.gov/books/NBK10135/

Delves, Peter J., Roitt IM. The immune system First of Two Parts. N Engl J Med. 2000;343(1):37–49. DOI: https://doi.org/10.1056/NEJM200007063430107

Norman P, Carrington CVF, Byng M, Maxwell LD, Curran MD, Stephens HAF, et al. Natural killer cell immunoglobulin-like receptor (KIR) locus profiles in African and South Asian populations. Genes Immun. 2002;3:86–95. DOI: https://doi.org/10.1038/sj.gene.6363836

Parham P. Immunogenetics of killer-cell immunoglobulin-like receptors. Tissue Antigens. 2003;62:194–200. DOI: https://doi.org/10.1034/j.1399-0039.2003.00126.x

Single RM, Martin MP, Gao X, Meyer D, Yeager M, Kidd JR, et al. Global diversity and evidence for coevolution of KIR and HLA. Nat Genet. 2007;39:1114–9. DOI: https://doi.org/10.1038/ng2077

Lu Z, Zhang B, Chen S, Gai Z, Feng Z, Liu X, et al. Association of KIR Genotypes and Haplotypes with Susceptibility to Chronic Hepatitis B Virus Infection in Chinese Han Population. Cell Mol Immunol [Internet]. 2008;5(6):457–63. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3842051&tool=pmcentrez&rendertype=abstract DOI: https://doi.org/10.1038/cmi.2008.57

Bazie, M. M., Djigma, F. W., Sanou, M., Sorgho, P. A., Ouattara, A. K., Obiri-Yeboah, D., Kapieko, N., Sombie, H. K., Bado, P., Yelemkoure, E. T., Kiendrebeogo, I. T., Nagalo, M. B., Yonli, A. T., & Simpore, J. (2023). Killer cell immunoglobulin-like receptor alleles influence susceptibility to occult hepatitis B infection in the West African population. Journal of Public Health in Africa, 14(9). https://doi.org/10.4081/jphia.2023.2586