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Identifying and structurally characterizing CD1b in Aotus nancymaae owl monkeys

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Abstract

This study reports the molecular characterization and tissue expression of the non-human Aotus nancymaae primate CD1b isoform in the search for an experimental animal model to be used in evaluating the role of non-peptide antigen-presentation molecules in the immune response to infectious agents. CD1b expression on the surface of A. nancymaae peripheral blood monocyte-derived dendritic cells, shown by flow cytometry, was made possible by using human CD1b isoform antibodies. Studying the expression of CD1b-encoded transcripts revealed this molecule’s broad distribution in several tissues. The A. nancymaae CD1b transcript-encoded amino-acid sequence showed 95.5% identity with the human sequence. Such high sequence homology was reflected in the identical structural conservation of how pockets A′, C′ and F′ and tunnel T′ conforming the antigen’s binding site are organized, the similar arrangement of those amino-acids interacting with the T-cell receptor (TCR) during antigen presentation, and the conservation of YQNI-motif sequence in the cytoplasmatic tail (responsible for the molecule’s intracellular trafficking in humans). Comparing the structure of human CD1a and CD1b and mouse CD1d proteins with CD1b structure in A. nancymaae obtained by minimization revealed that changes in the latter molecule’s α1 and α2 domains imposed a narrowing of the antigen-binding groove in A. nancymaae CD1b. The high structural similarity between A. nancymaae CD1b and that from humans presented in this study leads to A. nancymaae being proposed as a suitable experimental animal model for analyzing CD1b in vivo, mainly in bacterial and parasite infections such as tuberculosis and malaria, respectively.

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References

  • Akari H, Terao K, Murayama Y, Nam KH, Yoshikawa Y (1997) Peripheral blood CD4+CD8+ lymphocytes in cynomolgus monkeys are of resting memory T lineage. Int Immunol 9:591–597

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Angénieux C, Salamero J, Fricker D, Wurtz J-M, Maitre B, Cazenave J-P, Hanau D, de la Salle H (2003) Common characteristics of the human and rhesus macaque CD1e molecules: conservation of biochemicals and biological properties during primate evolution. Immunogenetics. 54:842–849

    PubMed  Google Scholar 

  • Balk SP, Bleicher PA, Terhorst C (1991) Isolation and expression of cDNA encoding the murine homologues of CD1. J Immunol 146:768–774

    CAS  PubMed  Google Scholar 

  • Batuwangala T, Shepherd D Gadola SD, Gibson KJC, Zaccai NR, Fersht AR, Besra GS, Cerendulo V, Jones EY (2004) The crystal structure of human CD1b with a bound bacterial glycolipid. J Immunol 172:2382–2388

    CAS  PubMed  Google Scholar 

  • Beckman EM, Porcelli SA, Morita CT, Behar SM, Furlong ST, Brenner MB (1994) Recognition of a lipid antigen by CD1-restricted αβ+ T-cells. Nature 372:691–694

    Article  CAS  PubMed  Google Scholar 

  • Blumberg RS, Terhorst C, Bleicher P, McDermott FV, Allan CH, Landau SB, Trier JS, Balk SP (1991) Expression of a non-polymorphic MHC class-I-like molecule, CD1D, by human intestinal epithelial cells. J Immunol 147:2518–2524

    CAS  PubMed  Google Scholar 

  • Briken V, Jackman RM, Dasgupta S, Hoening S, Porcelli SA (2002) Intracellular trafficking of newly synthesised CD1b molecules. EMBO J 21:825–832

    Article  CAS  PubMed  Google Scholar 

  • Calabi F, Belt KT, Yu CY, Bradbury A, Mandy WJ, Milstein C (1989a) The rabbit CD1 and evolutionary conservation of the CD1 gene family. Immunogenetics 30:370–377

    CAS  PubMed  Google Scholar 

  • Calabi F, Bilsland CAG, Yu CY, Bradbury A, Belt KT, Martin LH, Milstein C (1989b) Recent progress in the molecular study of CD1. In: Knapp W et al (eds) Leukocyte Typing IV. Oxford University Press, Oxford, pp 254–258

    Google Scholar 

  • Calabi F, Jarvis JM, Martin L, Milstein C (1989c) Two cases of CD1 genes. Eur J Immunol 19:285–292

    CAS  PubMed  Google Scholar 

  • Chun T, Wang K, Zuckermann FA, Gaskins HR (1999) Molecular cloning and characterization of a novel CD1 gene from the pig. J Immunol 162:6562–6571

    CAS  PubMed  Google Scholar 

  • Dascher CC, Hiromatsu K, Naylor JW, Brauer PP, Brown KA, Storey JR, Behar SM, Kawasaki ES, Porcelli SA, Brenner MB, LeClair KP (1999) Conservation of CD1 multigene family in the guinea pig. J Immunol 163:5478–5488

    CAS  PubMed  Google Scholar 

  • Dascher CC, Hiromatsu K, Xiong X, Sugita M, Buhlmann JE, Dodge IL, Lee SY, Roura-Mir C, Watts GF, Roy CJ, Behar SM, Clemens DL, Porcelli SA, Brenner MB (2002) Conservation of CD1 intracellular trafficking patterns between mammalian species. J Immunol 169:6951–6958

    CAS  PubMed  Google Scholar 

  • Delgado G, Parra-Lopez CA, Vargas LE, Hoya R, Estupinan M, Guzman F, Torres A, Alonso C, Velez ID, Spinel C, Patarroyo ME (2003) Characterizing cellular immune response to kinetoplastid membrane protein-11 (KMP-11) during Leishmania (Viannia) panamensis infection using dendritic cells (DCs) as antigen presenting cells (APCs). Parasite Immunol 25:199–209

    Article  CAS  PubMed  Google Scholar 

  • Diaz D, Naegeli M, Rodríguez R, Niño-Vasquez J, Moreno A, Patarroyo ME, Pluschke G, Daubenberger C (2000a) Sequence and diversity of MHC DQA and DQB genes of the owl monkey Aotus nancymaae. Immunogenetics 51:528–537

    Article  CAS  PubMed  Google Scholar 

  • Diaz OL, Daubenberger CA, Rodriguez R, Naegeli M, Moreno A, Patarroyo M, Pluschke G (2000b) Immunoglobulin kappa light-chain V, J, and C gene sequences of the owl monkey Aotus nancymaae. Immunogenetics 51:212–218

    Article  CAS  PubMed  Google Scholar 

  • Diaz D, Daubenberger CA, Zalac T, Rodriguez R, Patarroyo ME (2002) Sequence and expression of MHC-DPB1 molecules of the New World monkey Aotus nancymaae, a primate model for Plasmodium falciparum. Immunogenetics 54:251–259

    Article  CAS  PubMed  Google Scholar 

  • Dutia BM, Hopkins J (1991) Analysis of the CD1 cluster in sheep. Vet Immunol Immunolpathol 27:189–194

    Article  CAS  Google Scholar 

  • Ernst WA, Maher J, Cho S, Niazi KR, Chatterjee D, Moody DB, Besra GS, Watanabe Y, Jensen PE, Porcelli SA, Kronenberg M, Modlin RL (1998) Molecular interaction of CD1b with lipoglycan antigens. Immunity 8:331–340

    Article  CAS  PubMed  Google Scholar 

  • 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 Aotus nancymaae owl monkey. Immunogenetics 48:253–259

    Article  CAS  PubMed  Google Scholar 

  • Gadola SD, Zaccai NR, Harlos K, Shepherd D, Castro-Palomino JC, Ritter G, Schmidt RR, Jones EY, Cerendulo V (2002) Structure of human CD1b with bound ligands at 2.3 Å, a maze for alkyl chains. Nat Immunol 3:721–726

    CAS  PubMed  Google Scholar 

  • Guerrero JE, Pacheco DP, Suarez CF, Martinez P, Aristizabal F, Moncada CA, Patarroyo ME, Patarroyo MA (2003) Characterizing T-cell receptor γ-variable gene in Aotus nancymaae owl monkey peripheral blood. Tissue Antigens 61:1–11

    Article  PubMed  Google Scholar 

  • Hayes SH, Knight KL (2001) Group 1 CD1 genes in rabbit. J Immunol 166:403–410

    CAS  PubMed  Google Scholar 

  • Hernandez E, Suarez CF, Mendez JA, Echeverry SJ, Murillo LA, Patarroyo ME (2002) Identification, cloning, and sequencing of different cytokine genes in four species of owl monkey. Immunogenetics 54:645–653

    Article  CAS  PubMed  Google Scholar 

  • Kasai K, Matsuura A, Kikuchi K, Hashimoto Y, Ichimiya S (1997) Localization of rat CD1 transcripts and protein in rats tissues. An analysis of rat CD1 expression by in situ hybridization and immunohistochemistry. Clin Exp Immunol 109:317–322

    Article  CAS  Google Scholar 

  • Kashiwase K, Kikuchi A, Ando Y, Nicol A, Porcelli SA, Tokunaga K, Omine M, Satake M, Juji T, Nieda M, Koezuka Y (2003) The CD1d natural killer T-cell antigen presentation pathway is highly conserved between humans and rhesus macaques. Immunogenetics 54:776–781

    CAS  PubMed  Google Scholar 

  • Kawashima T, Norose Y, Watanabe Y, Enomoto Y, Narazaki H, Watari E, Tanaka S, Takahashi H, Yano I, Brenner MB, Sugita M (2003) Cutting edge: major CD8 T cell response to live bacillus Calmette-Guérin is mediated by Cd1 molecules. J Immunol 170:5345–5348

    CAS  PubMed  Google Scholar 

  • Kayvan RN, Chiu MW, Mendoza RM, Degano M, Moody DB, Melian A, Wilson IA, Kronenberg M, Porcelli SA, Modlin RL (2001) The A′ and F′ pockets of human CD1b are both required for optimal presentation of lipid antigens to T cells. J Immunol 166:2562–2570

    PubMed  Google Scholar 

  • Machugh ND, Bensaid A, Davis WC, Howard CJ, Parsons KR, Jones B, Kaushal A (1988) Characterization of a bovine thymic differentiation antigen analogous to CD1 in the human. Scand J Immunol 27:541–547

    CAS  PubMed  Google Scholar 

  • Martin LH, Calabi F, Lefebvre F-A, Bilsland CAG, Milstein C (1987) Structure and expression of the human thymocyte antigens CD1a, CD1b, and CD1c. Proc Natl Acad Sci USA 84:9189–9193

    CAS  PubMed  Google Scholar 

  • Mansura A, Hashimoto Y, Kinebuchi M, Kasai K, Ichimiya S, Katabami S, Chen H, Shimisu T, Kikuchi K (1997) Rat CD1 antigen: structure, expression and function. Transplant Proc 29:1705–1706

    Article  PubMed  Google Scholar 

  • Moody DB, Reinhold BB, Guy MR, Beckman EM, Frederique DE, Furlong ST, Ye S, Reinhold VN, Sieling PA, Modlin RL, Besra GS, Porcelli SA (1997) Structural requirements for glycolipid antigen recognition by CD1b-restricted T-cells. Science 278:283–286

    Article  CAS  PubMed  Google Scholar 

  • Moody DB, Briken V, Cheng TY, Roura-Mir C, Guy MR, Geho DH, Tykocinski ML, Besra GS, Porcelli SA (2002) Lipid length controls antigen entry into endosomal and non-endosomal pathways for CD1b presentation. Nat Immunol 3:435–442

    CAS  PubMed  Google Scholar 

  • Moreno CA, Rodriguez R, Oliveira GA, Ferreira V, Nussenzweig RS, Moya Castro ZR, Calvo-Calle JM, Nardin E (1999) Preclinical evaluation of a synthetic Plasmodium falciparum MAP malaria vaccine in Aotus monkeys and mice. Vaccine 18:89–99

    Article  CAS  PubMed  Google Scholar 

  • Niño-Vasquez J, Vogel D, Rodriguez R, Moreno A, Patarroyo M, Pluschke G, Daubenberger C (2000) Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites. Immunogenetics 51:219–230

    Article  PubMed  Google Scholar 

  • Parsons KR, Machugh ND (1991) Individual antigens of cattle. Bovine CD1 (boCD1). Vet Immunol Immunolpathol 27:37–41

    Article  CAS  Google Scholar 

  • Patarroyo ME, Romero P, Torres ML, Clavijo P, Moreno A, Martinez A, Rodriguez R, Guzman F, Cabezas E (1987) Induction of protective immunity against experimental infection with malaria using synthetic peptides. Nature 328:629–632

    Article  CAS  PubMed  Google Scholar 

  • Porcelli SA (1995) The CD1 family: a third lineage of antigen-presenting molecules. Adv Immunol 59:1

    CAS  PubMed  Google Scholar 

  • Rhin SM, Dutia BM, Howard CJ, Hopkins J (1996) Discrimination of two subsets of CD1 molecules in the sheep. Vet Immunol Immunolpathol 52:265–270

    Article  Google Scholar 

  • Rivera Z, Granados G, Pinto M, Varon D, Carvajal C, Chaves F, Calvo J, Rodriguez R, Guzman F, Patarroyo ME (2002) Double dimer peptide constructs are immunogenic and protective against Plasmodium falciparum in the experimental Aotus monkey model. J Pept Res 59:62–70

    CAS  PubMed  Google Scholar 

  • Rosas JE, Pedraz JL, Hernandez RM, Gascon AR, Igartua M, Guzman F, Rodriguez R, Cortes J, Patarroyo ME (2002) Remarkably high antibody levels and protection against P. falciparum malaria in Aotus monkeys after a single immunisation of SPf66 encapsulated in PLGA microspheres. Vaccine 20:1707–1710

    Article  CAS  PubMed  Google Scholar 

  • Satin AD, Hermonat PL, Ravaggi A, Chiriva-Internati M, Cannon MJ, Hiserodt JC, Pecorelli S, Parham GP (1999) Expression of surface antigens during the differentiation of human dendritic cells vs macrophages from blood monocytes in vitro. Immunobiology 200:187–204

    PubMed  Google Scholar 

  • Sieling PA, Chatterjee D, Porcelli SA, Prigozy TI, Mazzaccaro RJ, Soriano T, Bloom BR, Brenner MB, Kronenberg M, Brennan PJ, Modlin RL (1995) CD1-restricted T-cell recognition of microbial lipoglycan antigens. Science 269:227–230

    CAS  PubMed  Google Scholar 

  • Sieling PA, Jullien D, Dahlem M, Tedder TF, Rea TH, Modlin RL, Porcelli SA (1999) CD1 expression by dendritic cells in human leprosy lesions: correlation with effective host immunity. J Immunol 162:1851–1858

    CAS  PubMed  Google Scholar 

  • Stenger S, Mazzaccaro RJ, Uyemura K, Cho S, Barnes PF, Rosat JP, Sette A, Brenner MB, Porcelli SA, Bloom BR, Modlin RL (1997) Differential effects of cytolytic T-cell subsets on intracellular infection. Science 276:1684–1687

    Article  CAS  PubMed  Google Scholar 

  • Stenger S, Niazi KR, Modlin RL (1998) Down-regulation of CD1 on antigen-presenting cells by infection with Mycobacterium tuberculosis. J Immunol 161:3582–3588

    CAS  PubMed  Google Scholar 

  • Suárez CF, Cardenas PP, Llanos-Ballestas EJ, Martinez P, Obregón M, Patarroyo ME, Patarroyo MA (2003) α1 and α2 domains of Aotus MHC class-I and Catarrhini MHC class-Ia share similar characteristics. Tissue Antigens 61:362–373

    PubMed  Google Scholar 

  • Sugita M, grant EP, van Donselaar E, Hsu VW, Rogers RA, Peters PJ, Brenner MB (1999) Separate pathways for antigen presentation by CD1 molecules. Immunity 11:743

    Article  CAS  PubMed  Google Scholar 

  • Sugita M, Vander Wel N, Rogers RA, Peters PJ, Brenner MB (2000) CD1c molecules broadly survey the endocytic system. Proc Natl Acad Sci USA 97:8445–8450

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Honeyman MC, Harrison LC (1997) Dendritic cells generated from human blood in granulocyte macrophage-colony stimulating factor and interleukin-7. Hum Immunol 55:103–116

    Article  CAS  PubMed  Google Scholar 

  • Vecino W, Daubenberger C, Rodriguez R, Moreno A, Patarroyo M, Pluschke G (1999) Sequence and diversity of T-cell receptor β-chain V and J genes of the Aotus nancymaae owl monkey. Immunogenetics 49:792–799

    Article  CAS  PubMed  Google Scholar 

  • Zajonc DM, Elsliger MA, Teyton L, Wilson IA (2003) Crystal structure of CD1a in complex with a sulfatide self at a resolution of 2.15 Å. Nat Immunol 4:808–815

    Article  CAS  PubMed  Google Scholar 

  • Zeng Z, Castaño AR, Segelke BW, Stura EA, Peterson PA, Wilson IA (1997) Crystal structure of mouse CD1: an MHC-like fold with a large hydrophobic binding groove. Science 277:339–345

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research has been supported by the Colombian President’s Office and the Colombian Ministry of Health. The experiments reported here comply with the current Ministry of Health laws and other Colombian institutions’ regulations. We would like to thank Jason Garry for patiently reading this manuscript.

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Correspondence to Carlos Parra-López.

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Castillo, F., Guerrero, C., Trujillo, E. et al. Identifying and structurally characterizing CD1b in Aotus nancymaae owl monkeys. Immunogenetics 56, 480–489 (2004). https://doi.org/10.1007/s00251-004-0716-8

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  • DOI: https://doi.org/10.1007/s00251-004-0716-8

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