Skip to main content
SpringerLink
Log in

Molecular characterization of major histocompatibility complex class I genes from the giant panda (Ailuropoda melanoleuca)

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The major histocompatibility complex class I genes play crucial roles in the adaptive immune system of vertebrates against intracellular pathogens. To date, no class I genes from the giant panda (Ailuropoda melanoleuca) has been reported, even none from species of Ursidae. In this study, we successfully identified three class I genes from a giant panda bacterial artificial chromosome library and designated them as Aime-128, 152, and 1906, respectively. Pairwise sequence alignments revealed that (1) the Aime-1906 always possessed the lowest identities (52–86%) in different regions compared with the Aime-128 and 152 and (2) the Aime-128 also varied from the Aime-152 in the regions of 5′ untranslated region (UTR), 3′ UTR, and exon1, whose similarities were 83%, 87%, and 91%, respectively. Comparison of structure characteristics indicated that the Aime-128 possessed all conserved amino acids important to the function of antigen presentation while the Aime-152 and 1906 presented two and five mutated residues. Analysis of phylogenetic trees demonstrated that the Aime-128, 152, and 1906 were clustered into three different branches with 99% or 100% bootstrap values. As a result, these three kinds of evidence supported that the Aime-1906, 152, and 128 should be derived from different loci. Furthermore, in view of a prestop codon in the exon 7 and patterns of amino acid replacement within alleles, the Aime-1906 gene is predicted to be a nonclassical locus, which is most closely related to dog leukocyte antigen 79 in the phylogenetic tree constructed with various mammalian class I loci.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aldridge BM, Bowen L, Smith BR, Antonelis GA, Gulland F, Stott JL (2006) Paucity of class I MHC gene heterogeneity between individuals in the endangered Hawaiian monk seal population. Immunogenetics 58:203–215

    Article  PubMed  CAS  Google Scholar 

  • Bernatchez L, Landry C (2003) MHC studies in nonmode vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377

    Article  PubMed  CAS  Google Scholar 

  • Bjorkman P, Parham P (1990) Structure, function and diversity of class I major histocompatibility molecules. Ann Rev Biochem 59:253–288

    Article  PubMed  CAS  Google Scholar 

  • Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512–518

    Article  PubMed  CAS  Google Scholar 

  • Braud VM, Allan DS, McMichael AJ (1999) Functions of nonclassical MHC and non-MHC -encoded class I molecules. Curr Opin Immunol 11:100–108

    Article  PubMed  CAS  Google Scholar 

  • Burnett RC, Geraghty DE (1995) Structure and expression of a divergent canine class I gene. J Immunol 155:4278–4285

    PubMed  CAS  Google Scholar 

  • Cadavid LF, Shufflebotham C, Ruiz FJ, Yeager M, Hughes AL, Watkins DI (1997) Evolutionary instability of the major histocompatibility complex class I loci in New World primates. Proc Natl Acad Sci U S A 94:14536–14541

    Article  PubMed  CAS  Google Scholar 

  • Dutra AS, Mignot E, Puck JM (1996) Gene localization and syntenic mapping by FISH in the dog. Cytogenet Cell Genet 74:113–117

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich R, Lifshitz R, Pescovitz MD, Rudikoff S, Singer DS (1987) Tissue-specific expression and structure of a divergent member of a class I MHC gene family. Immunol 139:593–602

    CAS  Google Scholar 

  • Ellis SA, Bontrop RE, Antczak DF, Ballingall K, Davies CJ, Kaufman J, Kennedy LJ, Robinson J, Smith DM, Stear MJ, Stet RJ, Waller MJ, Walter L, Marsh SG, ISAG/IUIS-VIC Comparative MHC Nomenclature Committee (2006) ISAG/IUIS-VIC Comparative MHC Nomenclature Committee report, 2005. Immunogenetics 57:953–958

    Article  PubMed  Google Scholar 

  • Gouin N, Wright AM, Miska KB, Parra ZE, Samollow PB, Baker ML, Miller RD (2006) Modo-UG, a marsupial nonclassical MHC class I locus. Immunogenetics 58:396–406

    Article  CAS  Google Scholar 

  • Holmes EC, Roberts AF, Staines KA, Ellis SA (2003) Evolution of major histocompatibility complex class I genes in Cetartiodactyls. Immunogenetics 55:193–202

    Article  PubMed  CAS  Google Scholar 

  • Houlden BA, Greville WD, Sherwin WB (1996) Evolution of MHC class I loci in marsupials: characterization of sequences from koala (Phascolarctos cinereus). Mol Biol Evol 13:1119–1127

    PubMed  CAS  Google Scholar 

  • Howcroft TK, Raval A, Weissman JD, Gegonne A, Singer DS (2003) Distinct transcriptional pathways regulate basal and activated major histocompatibility complex class I expression. Mol Cell Biol 23:3377–3391

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170

    Article  PubMed  CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, NY, USA, pp 21–132

    Google Scholar 

  • Kelly J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695

    Article  CAS  Google Scholar 

  • Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219

    PubMed  CAS  Google Scholar 

  • Koller BH, Orr HT (1985) Cloning and complete sequence of an HLA-A2 gene: analysis of two HLA-A alleles at the nucleotide level. J Immunol 134:2727–2733

    PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lam MK-P, Belov K, Harrison G, Cooper D (2001) An MHC class I gene in the Australian brushtail possum (Trichosurus vulpecula). Immunogenetics 53:430–433

    Article  PubMed  CAS  Google Scholar 

  • Lanier LL (1997) Natural killer cell receptors and MHC class I interactions. Curr Opin Immunol 9:126–131

    Article  PubMed  CAS  Google Scholar 

  • LeMaoult J, Le Discorde M, Rouas-Freiss N, Moreau P, Menier C, McCluskey J, Carosella ED (2003) Biology and functions of human leukocyte antigen-G in health and sickness. Tissue Antigens 62:273–284

    Article  PubMed  CAS  Google Scholar 

  • Mayer W, Williams N, O'hUigin C, Vincek V, Zaleska-Rutczynska Z, Klein J (1993) Class I major histocompatibility complex genes of the red-necked wallaby, Macropus rufogriseus. Mol Phylogenet Evol 2:23–30

    Article  PubMed  CAS  Google Scholar 

  • Miller HC, Belov K, Daugherty CH (2006) MHC Class I genes in the Tuatara (Sphenodon spp.): evolution of the MHC in an ancient reptilian order. Mol Biol Evol 23:949–956

    Article  PubMed  CAS  Google Scholar 

  • Miska K, Harrison G, Hellman L, Millar R (2002) The major histocompatibility complex in monotremes: an analysis of the evolution of the MHC class I genes across all three mammalian subclasses. Immunogenetics 54:381–393

    Article  PubMed  CAS  Google Scholar 

  • Miska K, Wright AM, Lundgren R, Sasaki-McClees R, Osterman A, Gale J, Miller R (2004) Analysis of a marsupial MHC region containing two recently duplicated class I loci. Mamm Genome 15:851–864

    Article  PubMed  CAS  Google Scholar 

  • MOF, WWF (1989) A comprehensive survey report on China's giant panda and its habitat. China Alliance Press, Hong Kong

    Google Scholar 

  • Pascalis H, Heraud JM, Fendel R, Lavergne A, Kazanji M (2003) Molecular characterization of major histocompatibility complex class 1 (MHC-I) from squirrel monkeys (Saimiri sciureus). Immunogenetics 55:633–639

    Article  PubMed  CAS  Google Scholar 

  • Piontkivska H, Nei M (2003) Birth-and-death evolution in primate MHC class I genes: divergence time estimates. Mol Biol Evol 20:601–609

    Article  PubMed  CAS  Google Scholar 

  • Rebecca L, Tallmadge RL, Lear TL, Antczak DF (2005) Genomic characterization of MHC class I genes of the horse. Immunogenetics 57:763–774

    Article  CAS  Google Scholar 

  • Rodgers JR, Cook RG (2005) MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol 5:459–471

    Article  PubMed  CAS  Google Scholar 

  • Sachdev M, Sankaranarayanan R, Reddanna P, Thangaraj K, Singh L (2005) Major histocompatibility complex class I polymorphism in Asiatic lions. Tissue Antigens 66:9–18

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Sammut B, Laurens V, Tournefier A (1997) Isolation of Mhc class I cDNAs from the axolotl Ambystoma mexicanum. Immunogenetics 45:285–294

    Article  PubMed  CAS  Google Scholar 

  • State Forestry Administration (2006) The 3rd national survey report on giant panda in China. Science Press, Beijing

    Google Scholar 

  • Sun J, Leahy DJ, Kavathas PB (1995) Interaction between CD8 and major histocompatibility complex (MHC) class I mediated by multiple contact surfaces that include the alpha 2 and alpha 3 domains of MHC class I. J Exp Med 182:1275–1280

    Article  PubMed  CAS  Google Scholar 

  • Takahashi K, Rooney AP, Nei M (2000) Origins and divergence times of mammalian class II MHC gene clusters. J Hered 91:198–204

    Article  PubMed  CAS  Google Scholar 

  • van den Elsen PJ, Peijnenburg A, van Eggermond MC, Gobin SJ (1998) Shared regulatory elements in the promoters of MHC class I and class II genes. Immunol Today 19:308–312

    Article  PubMed  Google Scholar 

  • van den Elsen PJ, Holling TM, Kuipers HF, van der Stoep N (2004) Transcriptional regulation of antigen presentation. Curr Opin Immunol 16:67–75

    Article  PubMed  CAS  Google Scholar 

  • Villadangos JA, Galocha B, Lopez D, Calvo V, Castro JLD (1992) Role of binding pockets for amino-terminal peptide residues in HLA-B27 allorecognition. J Immunol 149:505–510

    PubMed  CAS  Google Scholar 

  • Wagner JL, Creer SA, Storb R (2000) Dog class I gene DLA-88 histocompatibility typing by PCR-SSCP and sequencing. Tissue Antigens 55:564–567

    Article  PubMed  CAS  Google Scholar 

  • Wagner JL, Palti Y, DiDario D, Faraco J (2005) Sequence of the canine major histocompatibility complex region containing non-classical class I genes. Tissue Antigens 65:549–555

    Article  PubMed  CAS  Google Scholar 

  • Wan QH, Zhu L, Wu H, Fang SG (2006) Major histocompatibility complex class II variation in the giant panda (Ailuropoda melanoleuca). Mol Ecol 15:2441–2450

    Article  PubMed  CAS  Google Scholar 

  • Yuhki N, O'Brien SJ (1990) DNA recombination and natural selection pressure sustain genetic sequence diversity of the feline MHC class I genes. J Exp Med 172:621–630

    Article  PubMed  CAS  Google Scholar 

  • Zeng CJ, Yu JQ, Pan HJ, Wan QH, Fang SG (2005) Assignment of giant panda MHC class II gene cluster to chromosome 9q by fluorescence in situ hybridization. Cytogenet Genome Res 109:533

    Article  PubMed  Google Scholar 

  • Zeng CJ, Pan HJ, Gong SB, Yu JQ, Wan QH, Fang SG (2007) Giant panda BAC library construction and assembly of a 650-kb contig spanning major histocompatibility complex class II region. BMC genomics 8:315

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Long Z (1983) The vicissitudes of the giant panda. Acta Zoologica Sinica 29:93–10

    Google Scholar 

  • Zhu L, Ruan XD, Ge YF, Wan QH, Fang SG (2007) Low major histocompatibility complex class II DQA diversity in the Giant Panda (Ailuropoda melanoleuca). BMC Genet 8:29

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Basic Research Program of China (973 program; No.2007CB411600) and from the National Science Fund for Distinguished Young Scholars (No. 30325009). We thank Mr. Chris Wood for his help in English language.

Author information

Authors and Affiliations

  1. College of Life Sciences, Zhejiang University, Zijingang Campus, No.388 Yu Hang Tang Road, Hangzhou, 310058, Zhejiang, People’s Republic of China

    Hui-Juan Pan, Qiu-Hong Wan & Sheng-Guo Fang

  2. State Conservation Center for Gene Resources of Endangered Wildlife and the Key Laboratory of Conservation Genetics and Reproductive Biology for Endangered Wild Animals of the Ministry of Education, Hangzhou, 310058, People’s Republic of China

    Hui-Juan Pan, Qiu-Hong Wan & Sheng-Guo Fang

Authors
  1. Hui-Juan Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiu-Hong Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sheng-Guo Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sheng-Guo Fang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

Primer sets used in PCR reactions for cDNA and gDNA are listed in the table below. The E23-S and E23-AS were used to screen the cDNA and genomic BAC library. The 3′-CDS and 5′ PCR primer were from SMART cDNA Library Construction Kit (Clontech). UP-TSP and DOWN-TSP primers were designed to obtain upstream and downstream sequences of the Aime-1906 gene. DW-ACP, DW-ACPN, and universal primer were from DNA walking SpeedUp™ Premix kit (Seegene). RD1 was designed to isolate the promoter sequence of Aime-152. The 128whole, 152whole, and 1906whole aimed to obtain the whole sequences of the three genes and 128-E23, 152-E123, and 1906-E23 were used for allelic diversity detection. Ta represents annealing temperature and E(min) is extension time (DOC 40 kb).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pan, HJ., Wan, QH. & Fang, SG. Molecular characterization of major histocompatibility complex class I genes from the giant panda (Ailuropoda melanoleuca). Immunogenetics 60, 185–193 (2008). https://doi.org/10.1007/s00251-008-0281-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-008-0281-7

Keywords

Search

Navigation