Natural Killer Cell Receptor Genes in Camels: Another Mammalian Model
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
Grantová podpora
P 24706
Austrian Science Fund FWF - Austria
P 29623
Austrian Science Fund FWF - Austria
PubMed
31312212
PubMed Central
PMC6614441
DOI
10.3389/fgene.2019.00620
Knihovny.cz E-zdroje
- Klíčová slova
- SNP, camelid, leukocyte receptor complex, microsatellites, natural killer complex,
- Publikační typ
- časopisecké články MeSH
Due to production of special homodimeric heavy chain antibodies, somatic hypermutation of their T-cell receptor genes and unusually low diversity of their major histocompatibility complex genes, camels represent an important model for immunogenetic studies. Here, we analyzed genes encoding selected natural killer cell receptors with a special focus on genes encoding receptors for major histocompatibility complex (MHC) class I ligands in the two domestic camel species, Camelus dromedarius and Camelus bactrianus. Based on the dromedary genome assembly CamDro2, we characterized the genetic contents, organization, and variability of two complex genomic regions, the leukocyte receptor complex and the natural killer complex, along with the natural cytotoxicity receptor genes NCR1, NCR2, and NCR3. The genomic organization of the natural killer complex region of camels differs from cattle, the phylogenetically most closely related species. With its minimal set of KLR genes, it resembles this complex in the domestic pig. Similarly, the leukocyte receptor complex of camels is strikingly different from its cattle counterpart. With KIR pseudogenes and few LILR genes, it seems to be simpler than in the pig. The syntenies and protein sequences of the NCR1, NCR2, and NCR3 genes in the dromedary suggest that they could be human orthologues. However, only NCR1 and NCR2 have a structure of functional genes, while NCR3 appears to be a pseudogene. High sequence similarities between the two camel species as well as with the alpaca Vicugna pacos were observed. The polymorphism in all genes analyzed seems to be generally low, similar to the rest of the camel genomes. This first report on natural killer cell receptor genes in camelids adds new data to our understanding of specificities of the camel immune system and its functions, extends our genetic knowledge of the innate immune variation in dromedaries and Bactrian camels, and contributes to studies of natural killer cell receptors evolution in mammals.
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Abdallah H. R., Faye B. (2013). Typology of camel farming system in Saudi Arabia. Emir. J. Food Agric. 25, 250–260. 10.9755/ejfa.v25i4.15491 DOI
Allan A. J., Sanderson N. D., Gubbins S., Ellis S. A., Hammond J. A. (2015). Cattle NK cell heterogeneity and the influence of MHC class I. J. Immunol. 195, 2199–2206. 10.4049/jimmunol.1500227 PubMed DOI PMC
Antonacci R., Mineccia M., Lefranc M., Ashmaoui H. M. E., Lanave C., Piccinni B., et al. (2011). Expression and genomic analyses of Camelus dromedarius T cell receptor delta (TRD) genes reveal a variable domain repertoire enlargement due to CDR3 diversification and somatic mutation. Mol. Immunol. 48, 1384–1396. 10.1016/j.molimm.2011.03.011 PubMed DOI
Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC
Braud V. M., Allan D. S., O’Callaghan C. A., Söderström K., D’Andrea A., Ogg G. S., et al. (1998). HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391, 795–799. 10.1038/35869 PubMed DOI
Breese M. R., Liu Y. (2013). NGSUtils: a software suite for analyzing and manipulating next-generation sequencing datasets. Bioinformatics 29, 494–496. 10.1093/bioinformatics/bts731 PubMed DOI PMC
Carrillo-Bustamante P., Kesmir C., de Boer R. J. (2016). The evolution of natural killer cell receptors. Immunogenetics 68, 3–18. 10.1007/s00251-015-0869-7 PubMed DOI PMC
Ciccarese S., Vaccarelli G., Lefranc M., Tasco G., Consiglio A., Casadio R., et al. (2014). Characteristics of the somatic hypermutation in the Camelus dromedarius T cell receptor gamma (TRG) and delta (TRD) variable domains. Dev. Comp. Immunol. 46, 300–313. 10.1016/j.dci.2014.05.001 PubMed DOI
Davis M. P., van Dongen S., Abreu-Goodger C., Bartonicek N., Enright A. J. (2013). Kraken: a set of tools for quality control and analysis of high-throughput sequence data. Methods 63, 41–49. 10.1016/j.ymeth.2013.06.027 PubMed DOI PMC
Daws M. R., Ke-Zheng D., Zinöcker S., Naper Ch., Kveberg L., Hedrich H. J., et al. (2012). Identification of an MHC class I ligand for the single member of a killer cell lectin-like receptor family, KLRH1. J. Immunol. 189, 5178–5184. 10.4049/jimmunol.1201983 PubMed DOI
De Meyer T., Muyldermans S., Depicker A. (2014). Nanobody-based products as research and diagnostic tools. Trends Biotechnol. 32, 263–270. 10.1016/j.tibtech.2014.03.001 PubMed DOI
DePristo M. A., Banks E., Poplin R., Garimella K. V., Maguire J. R., Hartl C., et al. (2011). A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498. 10.1038/ng.806 PubMed DOI PMC
Dimasi N., Biassoni R. (2005). Structural and functional aspects of the Ly49 natural killer cell receptors. Immunol. Cell. Biol. 83, 1–8. 10.1111/j.1440-1711.2005.01301.x PubMed DOI
Elbers J. P., Rogers M. F., Perelman P. L., Proskuryakova A. A., Serdyukova N. A., Johnson W. E., et al. (2019). Improving Illumina assemblies with Hi-C and long reads: an example with the North African dromedary. Mol. Ecol. Resour. 00, 1–12. 10.1111/1755-0998.13020 PubMed DOI PMC
Fitak R. R., Mohandesan E., Corander J., Burger P. A. (2016). The de novo genome assembly and annotation of a female domestic dromedary of North African origin. Mol. Ecol. Resour. 16, 314–324. 10.1111/1755-0998.12443 PubMed DOI PMC
Gossner C., Danielson N., Gervelmeyer A., Berthe F., Faye B., Aaslav K. K., et al. (2014). Human-dromedary camel interactions and the risk of acquiring zoonotic Middle East respiratory syndrome coronavirus infection. Zoonoses Public Health. 63, 1–9. 10.1111/zph.12171 PubMed DOI PMC
Guethlein L. A., Norman P. J., Hilton H. G., Parham P. (2015). Co-evolution of MHC class I and variable NK cell receptors in placental mammals. Immunol. Rev. 267, 259–282. 10.1111/imr.12326 PubMed DOI PMC
Hall T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41, 95–98.
Hamerman J. A., Ogasawara K., Lanier L. L. (2005). NK cells in innate immunity. Curr. Opin. Immunol. 17, 29–35. 10.1016/j.col.2004.11.001 PubMed DOI
Hamers-Casterman C., Atarhouch T., Muyldermans S., Robinson G., Hammers E., Songa E. B., et al. (1993). Naturally occurring antibodies devoid of light chains. Nature 363, 446–448. 10.1038/363446a0 PubMed DOI
Hao L., Klein J., Nei M. (2006). Heterogenous but conserved natural killer receptor gene complexes in four major orders of mammals. Proc. Natl. Acad. Sci. U. S. A. 103, 3192–3197. 10.1073/pnas.0511280103 PubMed DOI PMC
Hemida M. G., Elmoslemany A., Al-Hizab F., Alnaeem A., Almathen F., Faye B., et al. (2017). Dromedary camels and the transmission of Middle East respiratory syndrome coronavirus (MERS-CoV). Transbound. Emerg. Dis. 64, 344–353. 10.1111/tbed.12401 PubMed DOI PMC
Hogan L., Bhuju S., Jones D. C., Laing K., Trowsdale J., Butcher P., et al. (2012). Characterisation of bovine leukocyte Ig-like receptors. PLoS One 7, e34291. 10.1371/journal.pone.0034291 PubMed DOI PMC
Hussen J., Shawaf T., Al-herz A. I., Alturaifi H. R., Alluwaimi A. M. (2017). Reactivity of commercially available monoclonal antibodies to human CD antigens with peripheral blood leucocytes of dromedary camels (Camelus dromedarius). Open Vet. J. 7, 150–156. 10.4314/ovj.v7i2.12 PubMed DOI PMC
Ito M., Maruyama T., Saito N., Koganei S., Yamamoto K., Matsumoto N. (2006). Killer cell lectin-like receptor G1 binds three members of the classical cadherin family to inhibit NK cell cytotoxicity. J. Exp. Med. 203, 289–295. 10.1084/jem20051986 PubMed DOI PMC
Jirimutu, Wang Z., Ding G., Chen G., Sun Y., Sun Z., et al. (2012). Genome sequences of wild and domestic Bactrian camels. Nat. Commun. 3, 1202. 10.1038/ncomms2192 PubMed DOI PMC
Kelley J., Walter L., Trowsdale J. (2005). Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet. 2, e27. 10.1371/journal.pgen.0010027 PubMed DOI PMC
Koch J., Steinle A., Watzl C., Mandelboim O. (2013). Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol. 34, 182–191. 10.1016/j.it.2013.01.003 PubMed DOI
Lanier L. L. (1998). NK cell receptors. Annu. Rev. Immunol. 16, 359–393. 10.1146/annurev.immunol.16.1.359 PubMed DOI
Lanier L. L. (2005). NK cell recognition. Annu. Rev. Immunol. 23, 225–274. 10.1146/annurev.immunol.23.021704.115526 PubMed DOI
Lanier L. L. (2015). NKG2D receptor and its ligands in host defense. Cancer Immunol. Res. 3, 575–582. 10.1158/2326-6066.CIR-15-0098 PubMed DOI PMC
Lanier L. L., Corliss B., Wu J., Phillips J. H. (1998). Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 8, 693–701. 10.1016/S1074-7613(00)80574-9 PubMed DOI
Li H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv®. Accessed January 21, 2019
Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. (2009). The sequence alignment/map format and SAM tools. Bioinformatics 25, 2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC
Librado P., Rozas J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452. 10.1093/bioinformatics/btp187 PubMed DOI
Marsch S. G. E., Parham P., Dupont B., Geraghty D. E., Trowsdale J., Middleton D., et al. (2003). Killer-cell immunoglobulin-like receptor (KIR) nomenclature report, 2002. Immunogenetics 55, 220–226. 10.1007/s00251-003-0571-z PubMed DOI
Martin A. M., Kulski J. K., Witt C., Pontarotti P., Christiansen F. T. (2002). Leukocyte Ig-like receptor complex (LRC) in mice and men. Trends Immunol. 23, 81–88. 10.1016/S1471-4906(01)02155-X PubMed DOI
Martin M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12. 10.14806/ej.17.1.200 DOI
Megersa B., Markemann A., Angassa A., Ogutu J. O., Piepho H., Zarate A. V. (2014). Livestock diversification: an adaptive strategy to climate change and rangeland ecosystem changes in southern Ethiopia. Hum. Ecol. 42, 509–520. 10.1007/s10745-014-9668-2 DOI
Mossad A. A., Elbagoury A. R., Khalid A. M., Waters W. R., Tibary A., Hamilton M. J., et al. (2006). Identification of monoclonal antibody reagents for use in the study of immune response in camel and water buffalo. Proc. Int. Sci. Conf. Camels 13, 2391–2411.
Muyldermans S., Baral T. N., Retamozzo V. C., De Baetselier P., De Genst E., Kinne J., et al. (2009). Camelid immunoglobulins and nanobody technology. Vet. Immunol. Immunopathol. 128, 178–183. 10.1016/j.vetimm.2008.10.299 PubMed DOI
Parham P., Moffett A. (2013). Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 13, 133–144. 10.1038/nri3370 PubMed DOI PMC
Plasil M., Mohandesan E., Fitak R. R., Musilova P., Kubickova S., Burger P. A., et al. (2016). The major histocompatibility complex in Old World camelids and low polymorphism of its class II genes. BMC Genomics 17, 167. 10.1186/s12864-016-2500-1 PubMed DOI PMC
Plasil M., Wijkmark S., Elbers J. P., Oppelt J., Burger P. A., Horin P. (2019). The major histocompatibility complex of Old World camelids: class I and class I-related genes. HLA 93, 203–215. 10.1111/tan.13510 PubMed DOI
Saether P. C., Westgaard I. H., Hoelsbrekken S. E., Benjamin J., Lanier L. L., Fossum S., et al. (2008). KLRE/I1 and KLRE/I2: a novel pair of heterodimeric receptors that inversely regulate NK cell cytotoxicity. J. Immunol. 181, 3177–3182. 10.4049/jimmunol.181.5.3177 PubMed DOI PMC
Sanderson N. D., Norman P. J., Guethlein L. A., Ellis S. A., Williams C., Breen M., et al. (2014). Definition of the cattle killer cell Ig-like receptor gene family: comparison with aurochs and human counterparts. J. Immunol. 193, 6016–6030. 10.4049/jimmunol.1401980 PubMed DOI PMC
Schenkel A. R., Kingry L. C., Slayden R. A. (2013). The Ly49 gene family. Front. Immunol. 4, 90. 10.3389/fimmu.2013.00090 PubMed DOI PMC
Schwartz J. C., Gibson M. S., Heimeier D., Koren S., Phillippy A. M., Bickhart D. M., et al. (2017). The evolution of the natural killer complex; a comparison between mammals using new high-quality genome assemblies and targeted annotation. Immunogenetics 69, 255–269. 10.1007/s00251-017-0973-y PubMed DOI PMC
Schwartz J. C., Hammond J. A. (2018). The unique evolution of the pig LRC, a single KIR but expansion of LILR and a novel Ig receptor family. Immunogenetics 70, 661–669. 10.1007/s00251-018-1067-1 PubMed DOI PMC
Steeland S., Vandenbroucke R. E., Libert C. (2016). Nanobodies as therapeutics: big opportunities for small antibodies. Drug Discov. Today 21, 1076–1113. 10.1016/j.drudis.2016.04.003 PubMed DOI
Stephens M., Donnelly P. (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73, 1162–1169. 10.1086/379378 PubMed DOI PMC
Storset A. K., Slettedal I., Williams J. L., Law A., Dissen E. (2003). Natural killer cell receptors in cattle: a bovine killer cell immunoglobulin-like receptor multigene family contains members with divergent signaling motifs. Eur. J. Immunol. 33, 980–990. 10.1002/eji.200323710 PubMed DOI
Tamura K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol. Biol. Evol. 9, 678–687. 10.1093/oxfordjournals.molbev.a040752 PubMed DOI
Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Evolution 28, 2731–2739. 10.1093/molbev/msr121 PubMed DOI PMC
Trowsdale J., Barten R., Haude A., Stewart C. A., Beck S., Wilson M. J. (2001). The genomic context of natural killer receptor extended gene families. Immunol. Rev. 181, 20–38. 10.1034/j.1600-065X.2001.1810102.x PubMed DOI
Vaccarelli G., Antonacci R., Tasco G., Yang F., Giordano L., El Ashmaoui H. M., et al. (2012). Generation of diversity by somatic mutation in the Camelus dromedarius T-cell receptor gamma variable domains. Eur. J. Immunol. 42, 3416–3428. 10.1002/eji.201142176 PubMed DOI
Vance R. E., Kraft J. R., Altman J. D., Jensen P. E., Raulet D. H. (1998). Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class I molecule Qa-1(b). J. Exp. Med. 188, 1841–1848. 10.1084/jem.188.10.1841 PubMed DOI PMC
Vivier E., Raulet D. H., Moretta A., Caligiuri M. A., Zitvogel L., Lanier L. L., et al. (2011). Innate or adaptive immunity? The example of natural killer cells. Science 331, 44–49. 10.1126/science.1198687 PubMed DOI PMC
Watson E. E., Kochore H. H., Dabasso B. H. (2016). Camels and climate resilience: adaptation in northern Kenya. Hum. Ecol. 44, 701–713. 10.1007/s10745-016-9858-1 PubMed DOI PMC
Wernery U., Kinne J. (2012). Foot and mouth disease and similar virus infections in camelids: a review. Rev. Sci. Tech. Off. Int. Epiz. 31, 907–918. 10.20506/rst.31.3.2160 PubMed DOI
Wu H., Guang X., Al-Fageeh M. B., Cao J., Pan S., Zhou H., et al. (2014). Camelid genomes reveal evolution and adaptation to desert environments. Nat. Commun. 5, 5188. 10.1038/ncomms6188 PubMed DOI
Zidan M., Pabst R. (2008). Unique microanatomy of ileal Peyer’s patches of the one humped camel (Camelus dromedarius) is not age-dependent. Anat. Rec. 291, 1023–1028. 10.1002/ar.20697 PubMed DOI
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