Abstract
The northern pig-tailed macaque (Macaca leonina) has been considered as an independent species from the pig-tailed macaque group. We have previously reported that this species macaque has the potential to be a useful animal model in HIV/AIDS pathogenesis and vaccine studies due to its susceptibility to HIV-1. To develop this animal into a potential HIV/AIDS model, we have studied the classical MHC genes of this animal. In this study, the non-classical MHC genes Malo-DM and Malo-DO alleles were first characterized by sequencing and cloning in 12 unrelated northern pig-tailed macaques. A total of 20 full-length sequences identified include 4 Malo-DMA, 5 Malo-DMB, 7 Malo-DOA, and 4 Malo-DOB alleles. Most of these allele sequences were shared between northern pig-tailed macaque and other macaque species in exon 2. The full-length MHC-DM and MHC-DO sequences provide more comprehensive analysis of immunogenetics of northern pig-tailed macaques and increase the value of the macaques in further biomedical studies.
This is a preview of subscription content, log in via an institution to check access.
References
De Groot NG, Otting N, Robinson J et al (2012) Nomenclature report on the major histocompatibility complex genes and alleles of Great Ape, Old and New World monkey species. Immunogenetics 64:615–631. https://doi.org/10.1007/s00251-012-0617-1
Feng ML, Liu RZ, Shen T et al (2012) Analysis of HLA-DM polymorphisms in the Chinese Han population. Tissue Antigens 79:157–164. https://doi.org/10.1111/j.1399-0039.2012.01838.x
Guce AI, Mortimer SE, Yoon T et al (2013) HLA-DO acts as a substrate mimic to inhibit HLA-DM by a competitive mechanism. Nat Struct Mol Biol 20:90–98. https://doi.org/10.1038/nsmb.2460
Hatziioannou T, Ambrose Z, Chung NPY et al (2009) A macaque model of HIV-1 infection. Proc Natl Acad Sci U S A 106:4425–4429. https://doi.org/10.1073/pnas.0812587106
Hatziioannou T, Del Prete GQ, Keele BF, et al (2014) HIV-1-induced AIDS in monkeys. Science (80-) 344:1401–1405. https://doi.org/10.1126/science.1250761
Jegaskanda S, Amarasena TH, Laurie KL et al (2013) Standard trivalent influenza virus protein vaccination does not prime antibody-dependent cellular cytotoxicity in macaques. J Virol 87:13706–13718. https://doi.org/10.1128/JVI.01666-13
Karl JA, Heimbruch KE, Vriezen CE et al (2014) Survey of major histocompatibility complex class II diversity in pig-tailed macaques. Immunogenetics 66:613–623. https://doi.org/10.1007/s00251-014-0797-y
Kimata JT (2014) Stepping toward a macaque model of HIV-1 induced AIDS. Viruses 6:3643–3651. https://doi.org/10.3390/v6093643
Kuang YQ, Tang X, Liu FL et al (2009) Genotyping of TRIM5 locus in northern pig-tailed macaques (Macaca leonina), a primate species susceptible to human immunodeficiency virus type 1 infection. Retrovirology 6:58. https://doi.org/10.1186/1742-4690-6-58
Lei AH, Zhang GH, Tian RR et al (2014) Replication potentials of HIV-1/HSIV in PBMCs from northern pig-tailed macaque (Macaca leonina). Zool Res 35:186–195. https://doi.org/10.11813/j.issn.0254-5853.2014.3.186
Lian XD, Zhang XH, Dai ZX, Zheng YT (2016) Cloning, sequencing, and polymorphism analysis of novel classical MHC class I alleles in northern pig-tailed macaques (Macaca leonina). Immunogenetics 68:261–274. https://doi.org/10.1007/s00251-015-0897-3
Liao CH, Kuang YQ, Liu HL et al (2007) A novel fusion gene, TRIM5-cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. AIDS 21(Suppl 8):S19–S26. https://doi.org/10.1097/01.aids.0000304692.09143.1b
Liu B, Jin Y, Lu Y et al (2015) Comprehensive identification of high-frequency and combination MHC-DMA and -DMB alleles in a cohort of Chinese rhesus macaques and cynomolgus macaques of Vietnamese origin. Hum Immunol 76:109–112. https://doi.org/10.1016/j.humimm.2015.01.019
Malaivijitnond S, Arsaithamkul V, Tanaka H et al (2012) Boundary zone between northern and southern pig-tailed macaques and their morphological differences. Primates 53:377–389. https://doi.org/10.1007/s10329-012-0316-4
Moon SM, Gu H, Ryu HJ et al (2005) Identification of four novel HLA-DOA alleles, DOA*010106, DOA*0102, DOA*0103, and DOA*0104N, by sequence-based typing. Tissue Antigens 66:242–245. https://doi.org/10.1111/j.1399-0039.2005.00446.x
Morris P, Shaman J, Attaya M et al (1994) An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368:551–554. https://doi.org/10.1038/368551a0
Pang W, Lü LB, Wang Y et al (2013) Measurement and analysis of hematology and blood chemistry parameters in northern pig-tailed macaques (Macaca leonina). Zool Res 34:89–96. https://doi.org/10.3724/SP.J.1141.2013.02089
Pang W, Zhang GH, Jiang J, et al (2017) HIV-1 can infect northern pig-tailed macaques (Macaca leonina) and form viral reservoirs in vivo. Sci Bull (in press). https://doi.org/10.1016/j.scib.2017.09.020
Pezeshki AM, Azar GA, Mourad W et al (2013) HLA-DO increases bacterial superantigen binding to human MHC molecules by inhibiting dissociation of class II-associated invariant chain peptides. Hum Immunol 74:1280–1287. https://doi.org/10.1016/j.humimm.2013.05.010
Robinson J, Halliwell JA, McWilliam H et al (2013) IPD—the immuno polymorphism database. Nucleic Acids Res 41:1234–1240. https://doi.org/10.1093/nar/gks1140
Vallender EJ, Miller GM (2013) Nonhuman primate models in the genomic era: a paradigm shift. ILAR J 54:154–165. https://doi.org/10.1093/ilar/ilt044
Van Lith M, Van Ham M, Neefjes J (2002) Novel polymorphisms in HLA-DOA and HLA-DOB in B-cell malignancies. Immunogenetics 54:591–595. https://doi.org/10.1007/s00251-002-0500-6
Yi W, Seth NP, Martillotti T et al (2010) Targeted regulation of self-peptide presentation prevents type I diabetes in mice without disrupting general immunocompetence. J Clin Invest 120:1324–1336. https://doi.org/10.1172/JCI40220
Zhang XL, Pang W, Deng DY et al (2014) Analysis of immunoglobulin, complements and CRP levels in serum of captive northern pig-tailed macaques (Macaca leonina). Zool Res 35:196–203. 10.11813/j.issn.0254-5853.2014.3.196
Zhang MX, Zheng HY, Jiang J et al (2017) Predict disease progression from T cell phenotypes in northern pig-tailed macaques ( Macaca leonina ) during SIVmac239 infection. Immunology. https://doi.org/10.1111/imm.12794
Zheng HY, Zhang MX, Zhang LT et al (2014) Flow cytometric characterizations of leukocyte subpopulations in the peripheral blood of northern pig-tailed macaques (Macaca leonina). Zool Res 35:465–473
Acknowledgements
The authors thank Natasja de Groot, NelOtting, and IMGT Non-Human Primate Nomenclature Committee for naming the Malo-DM and Malo-DO alleles.
Funding
This work was supported by the Key Scientific and Technological Program of China (2017ZX10304402-002), the National Basic Research Program of China (2012CBA01305), the National Natural Science Foundation of China (81373124, 81671627, 81172876, 81471620, 81571606), the Knowledge Innovation Program of CAS (ZDRW-ZS-2016-4-2), and the Natural Science Foundation of Yunnan Province (2014FB181, P0120150150).
Author information
Authors and Affiliations
Contributions
Xiao-Dong Lian performed the experiments and wrote the paper; Xiao-Dong Lian, Xi-He Zhang, and Zheng-Xi Dai analyzed the data; and Yong-Tang Zheng conceived and designed the experiments.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Lian, XD., Zhang, XH., Dai, ZX. et al. Identification of the major histocompatibility complex class-II DM and DO alleles in a cohort of northern pig-tailed macaques (Macaca leonina). Immunogenetics 70, 271–277 (2018). https://doi.org/10.1007/s00251-017-1036-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00251-017-1036-0