DOI QR코드

DOI QR Code

Major histocompatibility complex genes exhibit a potential immunological role in mixed Eimeria-infected broiler cecum analyzed using RNA sequencing

  • Minjun Kim (Division of Animal and Dairy Science, Chungnam National University) ;
  • Thisarani Kalhari Ediriweera (Department of Bio-AI Convergence, Chungnam National University) ;
  • Eunjin Cho (Department of Bio-AI Convergence, Chungnam National University) ;
  • Yoonji Chung (Division of Animal and Dairy Science, Chungnam National University) ;
  • Prabuddha Manjula (Department of Animal Science, Uva Wellassa University) ;
  • Myunghwan Yu (Division of Animal and Dairy Science, Chungnam National University) ;
  • John Kariuki Macharia (Division of Animal and Dairy Science, Chungnam National University) ;
  • Seonju Nam (Division of Animal and Dairy Science, Chungnam National University) ;
  • Jun Heon Lee (Division of Animal and Dairy Science, Chungnam National University)
  • Received : 2023.10.11
  • Accepted : 2023.11.28
  • Published : 2024.06.01

Abstract

Objective: This study was conducted to investigate the differential expression of the major histocompatibility complex (MHC) gene region in Eimeria-infected broiler. Methods: We profiled gene expression of Eimeria-infected and uninfected ceca of broilers sampled at 4, 7, and 21 days post-infection (dpi) using RNA sequencing. Differentially expressed genes (DEGs) between two sample groups were identified at each time point. DEGs located on chicken chromosome 16 were used for further analysis. Kyoto encyclopedia of genes and genomes (KEGG) pathway analysis was conducted for the functional annotation of DEGs. Results: Fourteen significant (false discovery rate <0.1) DEGs were identified at 4 and 7 dpi and categorized into three groups: MHC-Y class I genes, MHC-B region genes, and non-MHC genes. In Eimeria-infected broilers, MHC-Y class I genes were upregulated at 4 dpi but downregulated at 7 dpi. This result implies that MHC-Y class I genes initially activated an immune response, which was then suppressed by Eimeria. Of the MHC-B region genes, the DMB1 gene was upregulated, and TAP-related genes significantly implemented antigen processing for MHC class I at 4 dpi, which was supported by KEGG pathway analysis. Conclusion: This study is the first to investigate MHC gene responses to coccidia infection in chickens using RNA sequencing. MHC-B and MHC-Y genes showed their immune responses in reaction to Eimeria infection. These findings are valuable for understanding chicken MHC gene function.

Keywords

Acknowledgement

This research was funded by a grant from the National Research Foundation, Republic of Korea (grant number 2022R1F1A1064025).

References

  1. Madlala T, Okpeku M, Adeleke MA. Understanding the interactions between Eimeria infection and gut microbiota, towards the control of chicken coccidiosis: a review. Parasite 2021;28:48. https://doi.org/10.1051/parasite/2021047 
  2. Laurent F, Mancassola R, Lacroix S, Menezes R, Naciri M. Analysis of chicken mucosal immune response to Eimeria tenella and Eimeria maxima infection by quantitative reverse transcription-PCR. Infect Immun 2001;69:2527-34. https://doi.org/10.1128/iai.69.4.2527-2534.2001 
  3. Jang SI, Lillehoj HS, Lee SH, et al. Eimeria maxima recombinant Gam82 gametocyte antigen vaccine protects against coccidiosis and augments humoral and cell-mediated immunity. Vaccine 2010;28:2980-5. https://doi.org/10.1016/j.vaccine.2010.02.011 
  4. Lillehoj HS, Min W, Dalloul RA. Recent progress on the cytokine regulation of intestinal immune responses to Eimeria. Poult Sci 2004;83:611-23. https://doi.org/10.1093/ps/83.4.611 
  5. Zhou H, Lamont SJ. Chicken MHC class I and II gene effects on antibody response kinetics in adult chickens. Immunogenetics 2003;55:133-40. https://doi.org/10.1007/s00251-003-0566-9 
  6. Eizaguirre C, Lenz TL, Kalbe M, Milinski M. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 2012;3:621. https://doi.org/10.1038/ncomms1632 
  7. Montero BK, Wasimuddin, Schwensow N, et al. Evidence of MHC class I and II influencing viral and helminth infection via the microbiome in a non-human primate. PLoS Pathog 2021;17:e1009675. https://doi.org/10.1371/journal.ppat.1009675 
  8. Miller MM, Taylor RL Jr. Brief review of the chicken major histocompatibility complex: the genes, their distribution on chromosome 16, and their contributions to disease resistance. Poult Sci 2016;95:375-92. https://doi.org/10.3382/ps/pev379 
  9. Manjula P, Kim M, Cho S, Seo D, Lee JH. High levels of genetic variation in MHC-linked microsatellite markers from native chicken breeds. Genes 2021;12:240. https://doi.org/10.3390/genes12020240 
  10. Zhang J, Goto RM, Miller MM. A simple means for MHC-Y genotyping in chickens using short tandem repeat sequences. Immunogenetics 2020;72:325-32. https://doi.org/10.1007/s00251-020-01166-6 
  11. Kim M, Chung Y, Manjula P, et al. Time-series transcriptome analysis identified differentially expressed genes in broiler chicken infected with mixed Eimeria species. Front Genet 2022;13:886781. https://doi.org/10.3389/fgene.2022.886781 
  12. Xu ZY, Yu Y, Liu Y, et al. Differential expression of pro-inflammatory and anti-inflammatory genes of layer chicken bursa after experimental infection with infectious bursal disease virus. Poult Sci 2019;98:5307-14. https://doi.org/10.3382/ps/pez312 
  13. Williams J, Soutter F, Burrell C, et al. Differential expression of microRNAs in the caecal content and faeces of broiler chickens experimentally infected with Eimeria. Avian Pathol 2022;51:395-405. https://doi.org/10.1080/03079457.2022.2076581 
  14. Yu M, Jeon JO, Cho HM, et al. Broiler responses to dietary 3,4,5-trihydroxybenzoic acid and oregano extracts under Eimeria challenge conditions. J Anim Sci Technol 2021;63:1362-75. https://doi.org/10.5187/jast.2021.e121 
  15. Wickramasuriya SS, Park I, Lee Y, et al. Oral delivery of Bacillus subtilis expressing chicken NK-2 peptide protects against Eimeria acervulina infection in broiler chickens. Front Vet Sci 2021;8:684818. https://doi.org/10.3389/fvets.2021.684818 
  16. Ahmed MM, Akram MW, Tahir MHN, et al. Avian coccidiosis: recent advances in alternative control strategies and vaccine development. Agrobiol Rec 2020;1:26-30. https://doi.org/10.47278/journal.abr/2020.004 
  17. Venkatas J, Adeleke MA. A review of Eimeria antigen identification for the development of novel anticoccidial vaccines. Parasitol Res 2019;118:1701-10. https://doi.org/10.1007/s00436-019-06338-2 
  18. Boulton K, Nolan MJ, Wu Z, et al. Phenotypic and genetic variation in the response of chickens to Eimeria tenella induced coccidiosis. Genet Sel Evol 2018;50:63. https://doi.org/10.1186/s12711-018-0433-7 
  19. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139-40. https://doi.org/10.1093/bioinformatics/btp616 
  20. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995;57:289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x 
  21. Wickham H. ggplot2: elegant graphics for data analysis. 2nd ed. Cham, Switzerland: Springer; 2016. https://doi.org/10.1007/978-3-319-24277-4 
  22. Morris GM, Woods WG, Richards DG, Gasser RB. Investigating a persistent coccidiosis problem on a commercial broiler-breeder farm utilising PCR-coupled capillary electrophoresis. Parasitol Res 2007;101:583-9. https://doi.org/10.1007/s00436-007-0516-9 
  23. Long PL, Johnson J, Wyatt RD. Pathological and clinical effects of Eimeria tenella in partially immune chickens. J Comp Pathol 1981;91:581-7. https://doi.org/10.1016/0021-9975(81)90087-6 
  24. Ritz U, Seliger B. The transporter associated with antigen processing (TAP): structural integrity, expression, function, and its clinical relevance. Mol Med 2001;7:149-58. https://doi.org/10.1007/BF03401948 
  25. Goldszmid RS, Sher A. Processing and presentation of antigens derived from intracellular protozoan parasites. Curr Opin Immunol 2010;22:118-23. https://doi.org/10.1016/j.coi.2010.01.017 
  26. Chazara O, Tixier-Boichard M, Morin V, Zoorob R, Bed'Hom B. Organisation and diversity of the class II DM region of the chicken MHC. Mol Immunol 2011;48:1263-71. https://doi.org/10.1016/j.molimm.2011.03.009 
  27. Parker A, Stains K, Butter C, Kaufman J. The non-classical class II genes of the chicken, DMA and DMB, are similar to those of mammals, but a second DMB gene (DMB1) is differentially expressed with unusual regulatory and structural features. 15th International Congress of Immunology (ICI); 2013 Aug 22-27; Milan, Italy. https://doi.org/10.3389/conf.fimmu.2013.02.01174 
  28. Parker A, Kaufman J. What chickens might tell us about the MHC class II system. Curr Opin Immunol 2017;46:23-9. https://doi.org/10.1016/j.coi.2017.03.013 
  29. Connell S, Meade KG, Allan B, et al. Avian resistance to Campylobacter jejuni colonization is associated with an intestinal immunogene expression signature identified by mRNA sequencing. PLoS One. 2012;7:e40409. https://doi.org/10.1371/journal.pone.0040409 
  30. Geng T, Guan X, Smith EJ. Screening for genes involved in antibody response to sheep red blood cells in the chicken, Gallus gallus. Poult Sci 2015;94:2099-107. https://doi.org/10.3382/ps/pev224 
  31. Wu G, Liu L, Qi Y, et al. Splenic gene expression profiling in White Leghorn layer inoculated with the Salmonella enterica serovar E nteritidis. Anim Genet 2015;46:617-26. https://doi.org/10.1111/age.12341 
  32. Casterlow S, Li H, Gilbert ER, et al. An antimicrobial peptide is downregulated in the small intestine of Eimeria maxima-infected chickens. Poult Sci 2011;90:1212-9. https://doi.org/10.3382/ps.2010-01110 
  33. Kim T, Hunt HD, Parcells MS, van Santen V, Ewald SJ. Two class I genes of the chicken MHC have different functions: BF1 is recognized by NK cells while BF2 is recognized by CTLs. Immunogenetics 2018;70:599-611. https://doi.org/10.1007/s00251-018-1066-2 
  34. Kaufman J. Innate immune genes of the chicken MHC and related regions. Immunogenetics 2022;74:167-77. https://doi.org/10.1007/s00251-021-01229-2 
  35. Wang W, Huang Y, Yu Y, et al. Fish TRIM39 regulates cell cycle progression and exerts its antiviral function against iridovirus and nodavirus. Fish Shellfish Immunol 2016;50:1-10. https://doi.org/10.1016/j.fsi.2016.01.016 
  36. Goto RM, Warden CD, Shiina T, et al. The Gallus gallus RJF reference genome reveals an MHCY haplotype organized in gene blocks that contain 107 loci including 45 specialized, polymorphic MHC class I loci, 41 C-type lectin-like loci, and other loci amid hundreds of transposable elements. G3 (Bethesda) 2022;12:jkac218. https://doi.org/10.1093/g3journal/jkac218