Immunogenetics

, Volume 62, Issue 6, pp 383–395

Comprehensive analysis and characterization of the TCR α chain sequences in the common marmoset

  • Yoshiki Fujii
  • Takaji Matsutani
  • Kazutaka Kitaura
  • Satsuki Suzuki
  • Tsunetoshi Itoh
  • Tomohiko Takasaki
  • Ryuji Suzuki
  • Ichiro Kurane
Original Paper

Abstract

The common marmoset (Callithrix jacchus) is useful as a nonhuman primate model of human diseases. Although the marmoset model has great potential for studying autoimmune diseases and immune responses against pathogens, little information is available regarding the genes involved in adaptive immunity. Here, we identified one TCR α constant (TRAC), 46 TRAJ (joining), and 35 TRAV (variable) segments from marmoset cDNA. Marmoset TRAC, TRAJ, and TRAV shared 80%, 68–100%, and 79–98% identity with their human counterparts at the amino acid level, respectively. The amino acid sequences were less conserved in TRAC than in TCRβ chain constant (TRBC). Comparative analysis of TRAV between marmosets and humans showed that the rates of synonymous substitutions per site (dS) were not significantly different between the framework regions (FRs) and complementarity determining regions (CDRs), whereas the rates of nonsynonymous substitutions per site (dN) were significantly lower in the FRs than in CDRs. Interestingly, the dN values of the CDRs were greater for TRBV than TRAV. These results suggested that after the divergence of Catarrhini from Platyrrhini, amino acid substitutions were decreased in the FRs by purifying selection and occurred more frequently in CDRβ than in CDRα by positive selection, probably depending on structural and functional constraints. This study provides not only useful information facilitating the investigation of adaptive immunity using the marmoset model but also new insight into the molecular evolution of the TCR heterodimer in primate species.

Keywords

Common marmoset T cell receptors Evolution Comparative immunology 

Supplementary material

251_2010_445_MOESM1_ESM.doc (76 kb)
Supplemental Table 1Comparison of rates of synonymous (dS) or nonsynonymous substitutions per site (dN) in FRs and CDRs of TRBV between humans and the Rhesus monkeys (Macaca mulatta). (DOC 76 kb)
251_2010_445_MOESM2_ESM.doc (1 mb)
Supplemental Figure 1Total RNA was separately extracted from seven individual common marmosets (nos. 1–7). PCR amplification was performed with either TRAV8-6s1 (s1) or TRAV8-6s2 (s2) and CjCA3 primer. The cDNA clones encoding TRAV8-6s1 or TRAV8-6s2 segment were used as positive control. (DOC 1056 kb)

References

  1. Abbott DH, Barnett DK, Colman RJ, Yamamoto ME, Schultz-Darken NJ (2003) Aspects of common marmoset basic biology and life history important for biomedical research. Comp Med 53:339–350PubMedGoogle Scholar
  2. Adams AP, Aronson JF, Tardif SD, Patterson JL, Brasky KM, Geiger R, de la Garza M, Carrion R Jr, Weaver SC (2008) Common marmosets (Callithrix jacchus) as a nonhuman primate model to assess the virulence of eastern equine encephalitis virus strains. J Virol 82:9035–9042CrossRefPubMedGoogle Scholar
  3. Ando K, Maeda J, Inaji M, Okauchi T, Obayashi S, Higuchi M, Suhara T, Tanioka Y (2008) Neurobehavioral protection by single dose l-deprenyl against MPTP-induced parkinsonism in common marmosets. Psychopharmacology (Berl) 195:509–516CrossRefGoogle Scholar
  4. Antunes SG, de Groot NG, Brok H, Doxiadis G, Menezes AA, Otting N, Bontrop RE (1998) The common marmoset: a new world primate species with limited Mhc class II variability. Proc Natl Acad Sci U S A 95:11745–11750CrossRefPubMedGoogle Scholar
  5. Arden B, Clark SP, Kabelitz D, Mak TW (1995) Human T-cell receptor variable gene segment families. Immunogenetics 42:455–500PubMedGoogle Scholar
  6. Arnaiz-Villena A, Martinez-Laso J, Serrano-Vela JI, Reguera R, Moscoso J (2007) HLA-G polymorphism and evolution. Tissue Antigens 69(Suppl 1):156–159CrossRefPubMedGoogle Scholar
  7. Boyson JE, McAdam SN, Gallimore A, Golos TG, Liu X, Gotch FM, Hughes AL, Watkins DI (1995) The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41:59–68CrossRefPubMedGoogle Scholar
  8. Bright H, Carroll AR, Watts PA, Fenton RJ (2004) Development of a GB virus B marmoset model and its validation with a novel series of hepatitis C virus NS3 protease inhibitors. J Virol 78:2062–2071CrossRefPubMedGoogle Scholar
  9. 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 94:14536–14541CrossRefPubMedGoogle Scholar
  10. Davis MM, Bjorkman PJ (1988) T-cell antigen receptor genes and T-cell recognition. Nature 334:395–402CrossRefPubMedGoogle Scholar
  11. Ding YH, Smith KJ, Garboczi DN, Utz U, Biddison WE, Wiley DC (1998) Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 8:403–411CrossRefPubMedGoogle Scholar
  12. Efron B, Halloran E, Holmes S (1996) Bootstrap confidence levels for phylogenetic trees. Proc Natl Acad Sci U S A 93:13429–13434CrossRefPubMedGoogle Scholar
  13. Favre N, Daubenberger C, Marfurt J, Moreno A, Patarroyo M, Pluschke G (1998) Sequence and diversity of T-cell receptor alpha V, J, and C genes of the owl monkey Aotus nancymaae. Immunogenetics 48:253–259CrossRefPubMedGoogle Scholar
  14. Fujii Y, Kitaura K, Nakamichi K, Takasaki T, Suzuki R, Kurane I (2008) Accumulation of T-cells with selected T-cell receptors in the brains of Japanese encephalitis virus-infected mice. Jpn J Infect Dis 61:40–48PubMedGoogle Scholar
  15. Garcia KC, Degano M, Pease LR, Huang M, Peterson PA, Teyton L, Wilson IA (1998) Structural basis of plasticity in T cell receptor recognition of a self peptide–MHC antigen. Science 279:1166–1172CrossRefPubMedGoogle Scholar
  16. Genain CP, Hauser SL (1997) Creation of a model for multiple sclerosis in Callithrix jacchus marmosets. J Mol Med 75:187–197CrossRefPubMedGoogle Scholar
  17. Genain CP, Lee-Parritz D, Nguyen MH, Massacesi L, Joshi N, Ferrante R, Hoffman K, Moseley M, Letvin NL, Hauser SL (1994) In healthy primates, circulating autoreactive T cells mediate autoimmune disease. J Clin Invest 94:1339–1345CrossRefPubMedGoogle Scholar
  18. Hennecke J, Wiley DC (2001) T cell receptor–MHC interactions up close. Cell 104:1–4CrossRefPubMedGoogle Scholar
  19. Hennecke J, Carfi A, Wiley DC (2000) Structure of a covalently stabilized complex of a human alphabeta T-cell receptor, influenza HA peptide and MHC class II molecule, HLA-DR1. Embo J 19:5611–5624CrossRefPubMedGoogle Scholar
  20. Hughes AL, Nei M (1989) Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6:559–579PubMedGoogle Scholar
  21. Igarashi T, Sakuma T, Isogai M, Nagata R, Kamataki T (1997) Marmoset liver cytochrome P450s: study for expression and molecular cloning of their cDNAs. Arch Biochem Biophys 339:85–91CrossRefPubMedGoogle Scholar
  22. Jaeger EE, Bontrop RE, Lanchbury JS (1994) Structure, diversity, and evolution of the T-cell receptor VB gene repertoire in primates. Immunogenetics 40:184–191CrossRefPubMedGoogle Scholar
  23. Jorgensen JL, Esser U, Fazekas de St Groth B, Reay PA, Davis MM (1992) Mapping T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature 355:224–30CrossRefPubMedGoogle Scholar
  24. Klug S, Neubert R, Stahlmann R, Thiel R, Ryffel B, Car BD, Neubert D (1994) Effects of recombinant human interleukin 6 (rhIL-6) in marmosets (Callithrix jacchus). 1. General toxicity and hematological changes. Arch Toxicol 68:619–631CrossRefPubMedGoogle Scholar
  25. Lefranc MP (2007) WHO-IUIS Nomenclature Subcommittee for immunoglobulins and T cell receptors report. Immunogenetics 59:899–902CrossRefPubMedGoogle Scholar
  26. Lefranc MP, Lefranc G (2001) The T cell receptor FactsBook. Academic, San DiegoGoogle Scholar
  27. Lefranc MP, Duprat E, Kaas Q, Tranne M, Thiriot A, Lefranc G (2005) IMGT unique numbering for MHC groove G-DOMAIN and MHC superfamily (MhcSF) G-LIKE-DOMAIN. Dev Comp Immunol 29:917–938CrossRefPubMedGoogle Scholar
  28. Mansfield K (2003) Marmoset models commonly used in biomedical research. Comp Med 53:383–392PubMedGoogle Scholar
  29. Matsutani T, Yoshioka T, Tsuruta Y, Iwagami S, Suzuki R (1997) Analysis of TCRAV and TCRBV repertoires in healthy individuals by microplate hybridization assay. Hum Immunol 56:57–69CrossRefPubMedGoogle Scholar
  30. Matsutani T, Yoshioka T, Tsuruta Y, Iwagami S, Toyosaki-Maeda T, Horiuchi T, Miura AB, Watanabe A, Takada G, Suzuki R, Hirokawa M (2000) Restricted usage of T-cell receptor alpha-chain variable region (TCRAV) and T-cell receptor beta-chain variable region (TCRBV) repertoires after human allogeneic haematopoietic transplantation. Br J Haematol 109:759–769CrossRefPubMedGoogle Scholar
  31. Matsutani T, Ohashi Y, Yoshioka T, Tsuruta Y, Doi H, Satomi S, Suzuki R (2003a) Skew in T-cell receptor usage and clonal T-cell expansion in patients with chronic rejection of transplanted kidneys. Transplantation 75:398–407CrossRefPubMedGoogle Scholar
  32. Matsutani T, Sakurai Y, Yoshioka T, Tsuruta Y, Suzuki R, Shima M, Yoshioka A (2003b) Replacement therapy with plasma-derived factor VIII concentrates induces skew in T-cell receptor usage and clonal expansion of CD8+ T-cell in HIV-seronegative hemophilia patients. Thromb Haemost 90:279–292PubMedGoogle Scholar
  33. Maynard J, Petersson K, Wilson DH, Adams EJ, Blondelle SE, Boulanger MJ, Wilson DB, Garcia KC (2005) Structure of an autoimmune T cell receptor complexed with class II peptide–MHC: insights into MHC bias and antigen specificity. Immunity 22:81–92PubMedGoogle Scholar
  34. Meyer-Olson D, Brady KW, Blackard JT, Allen TM, Islam S, Shoukry NH, Hartman K, Walker CM, Kalams SA (2003) Analysis of the TCR beta variable gene repertoire in chimpanzees: identification of functional homologs to human pseudogenes. J Immunol 170:4161–4169PubMedGoogle Scholar
  35. Naeher D, Luescher IF, Palmer E (2002) A role for the alpha-chain connecting peptide motif in mediating TCR–CD8 cooperation. J Immunol 169:2964–2970PubMedGoogle Scholar
  36. Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A 94:7799–7806CrossRefPubMedGoogle Scholar
  37. Quint DJ, Buckham SP, Bolton EJ, Solari R, Champion BR, Zanders ED (1990) Immunoregulation in the common marmoset, Calithrix jaccus: functional properties of T and B lymphocytes and their response to human interleukins 2 and 4. Immunology 69:616–621PubMedGoogle Scholar
  38. Reinherz EL, Tan K, Tang L, Kern P, Liu J, Xiong Y, Hussey RE, Smolyar A, Hare B, Zhang R, Joachimiak A, Chang HC, Wagner G, Wang J (1999) The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286:1913–1921CrossRefPubMedGoogle Scholar
  39. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  40. Sawai H, Kawamoto Y, Takahata N, Satta Y (2004) Evolutionary relationships of major histocompatibility complex class I genes in simian primates. Genetics 166:1897–1907CrossRefPubMedGoogle Scholar
  41. Shiobara N, Suzuki Y, Aoki H, Gotoh A, Fujii Y, Hamada Y, Suzuki S, Fukui N, Kurane I, Itoh T, Suzuki R (2007) Bacterial superantigens and T cell receptor beta-chain-bearing T cells in the immunopathogenesis of ulcerative colitis. Clin Exp Immunol 150:13–21PubMedCrossRefGoogle Scholar
  42. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  43. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedGoogle Scholar
  44. Tsuruta Y, Iwagami S, Furue S, Teraoka H, Yoshida T, Sakata T, Suzuki R (1993) Detection of human T cell receptor cDNAs (alpha, beta, gamma and delta) by ligation of a universal adaptor to variable region. J Immunol Methods 161:7–21CrossRefPubMedGoogle Scholar
  45. Tynan FE, Burrows SR, Buckle AM, Clements CS, Borg NA, Miles JJ, Beddoe T, Whisstock JC, Wilce MC, Silins SL, Burrows JM, Kjer-Nielsen L, Kostenko L, Purcell AW, McCluskey J, Rossjohn J (2005) T cell receptor recognition of a ‘super-bulged’ major histocompatibility complex class I-bound peptide. Nat Immunol 6:1114–1122CrossRefPubMedGoogle Scholar
  46. Uccelli A, Oksenberg JR, Jeong MC, Genain CP, Rombos T, Jaeger EE, Giunti D, Lanchbury JS, Hauser SL (1997) Characterization of the TCRB chain repertoire in the New World monkey Callithrix jacchus. J Immunol 158:1201–1207PubMedGoogle Scholar
  47. Yaguchi M, Tabuse M, Ohta S, Ohkusu-Tsukada K, Takeuchi T, Yamane J, Katoh H, Nakamura M, Matsuzaki Y, Yamada M, Itoh T, Nomura T, Toyama Y, Okano H, Toda M (2009) Transplantation of dendritic cells promotes functional recovery from spinal cord injury in common marmoset. Neurosci Res 65:384–392CrossRefPubMedGoogle Scholar
  48. Yoshida R, Yoshioka T, Yamane S, Matsutani T, Toyosaki-Maeda T, Tsuruta Y, Suzuki R (2000) A new method for quantitative analysis of the mouse T-cell receptor V region repertoires: comparison of repertoires among strains. Immunogenetics 52:35–45CrossRefPubMedGoogle Scholar
  49. Yoshioka T, Matsutani T, Iwagami S, Tsuruta Y, Kaneshige T, Toyosaki T, Suzuki R (1997) Quantitative analysis of the usage of human T cell receptor alpha and beta chain variable regions by reverse dot blot hybridization. J Immunol Methods 201:145–155CrossRefPubMedGoogle Scholar
  50. Yoshioka T, Matsutani T, Iwagami S, Toyosaki-Maeda T, Yutsudo T, Tsuruta Y, Suzuki H, Uemura S, Takeuchi T, Koike M, Suzuki R (1999) Polyclonal expansion of TCRBV2- and TCRBV6-bearing T cells in patients with Kawasaki disease. Immunology 96:465–472CrossRefPubMedGoogle Scholar
  51. Yoshioka T, Matsutani T, Toyosaki-Maeda T, Suzuki H, Uemura S, Suzuki R, Koike M, Hinuma Y (2003) Relation of streptococcal pyrogenic exotoxin C as a causative superantigen for Kawasaki disease. Pediatr Res 53:403–410CrossRefPubMedGoogle Scholar
  52. Zuhlke U, Weinbauer G (2003) The common marmoset (Callithrix jacchus) as a model in toxicology. Toxicol Pathol 31:123–127CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Yoshiki Fujii
    • 1
    • 2
  • Takaji Matsutani
    • 3
  • Kazutaka Kitaura
    • 1
    • 2
  • Satsuki Suzuki
    • 4
  • Tsunetoshi Itoh
    • 3
  • Tomohiko Takasaki
    • 2
  • Ryuji Suzuki
    • 1
  • Ichiro Kurane
    • 2
  1. 1.Department of Rheumatology and Clinical Immunology, Clinical Research Center for Allergy and RheumatologySagamihara National Hospital, National Hospital OrganizationSagamiharaJapan
  2. 2.Department of Virology INational Institute of Infectious DiseasesTokyoJapan
  3. 3.Division of Immunology and Embryology, Department of Cell BiologyTohoku University School of MedicineSendaiJapan
  4. 4.Section of Biological Science, Research Center for OdontologyNippon Dental University School of Life DentistryTokyoJapan

Personalised recommendations