Characterizing the CD3 epsilon chain from the New World primate Aotus nancymaae
Keywords:
immune system, receptors, antigen, T-cell, CD3 antigens, adaptor proteins, signal transducing
Abstract
Introduction. The T-cell receptor (TCR)-associated complex, CD3 (d, g, e) and z-chains are essential transmembrane proteins for signal transduction during T cell activation and immune response, as well as during thymocyte development.Objective. This work established the CD3ε-chain primary structure for the New World owl monkey Aotus nancymaae.
Materials and methods. Total RNA was isolated from peripheral blood mononuclear cells; CD3ε molecule was amplified, cloned and sequenced.
Results. The CD3ε amino acid sequence was deduced for the owl monkey Aotus nancymaae.
It has an identity for nucleotide and amino acid sequences with the human counterpart of 84% and 76%, respectively. As described in other species, the Aotus CD3-e molecule is very variable in the extracellular region and greatly conserved in the intracellular domain. Even though high variability occurs in the CD3ε-extracellular domain, the subregions involved in ectodomain folding are conserved.
Conclusions. The primary structure suggested that the Aotus protein has a functional role similar to that of humans, and that the initial T-cell activation steps are also similar. However, the great variation observed in CD3ε-extracellular region in humans in contrast to the Aotus (especially in areas that are surface-exposed) indicated that some monoclonal antibodies against the human CD3 complex will not recognize these Aotus determinants.
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References
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24. Vernot JP, Pérez-Quintero LA, Perdomo-Arciniegas AM, Quijano S, Patarroyo ME. Herpesvirus saimiri immortalization of Aotus T lymphocytes specific for an immunogenically modified peptide of Plasmodium falciparum merozoite surface antigen 2. Immunol Cell Biol. 2005;83:67-74.
25. Niño-Vásquez JJ, Vogel D, Rodríguez R, Moreno A, Patarroyo ME, Pluschke G, et al. Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites. Immunogenetics. 2000;51:219-30.
26. Díaz D, Naegeli M, Rodríguez R, Niño-Vásquez JJ, Moreno A, Patarroyo ME, et al. Sequence and diversity of MHC DQA and DQB genes of the owl monkey Aotus nancymaae. Immunogenetics. 2000;51:528-37.
27. Montoya GE, Vernot JP, Patarroyo ME. Partial characterization of the CD45 phosphatase cDNA in the owl monkey ( A. vociferans). Am J Primatol. 2002;57:1-11.
28. Rost B, Sander C. Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 1993;232:584-99.
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30. Sun ZYJ, Kim KS, Wagner G, Reinherz EL. Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 eg heterodimer. Cell. 2001;105:913-23.
31. Arnett KL, Harrison SC, Wiley DC. Crystal structure of a human CD3-ed dimer in complex with a UCHT1 single-chain antibody fragment. Proc Natl Acad Sci USA. 2004;101:16268-73.
32. Kjer-Nielsen L, Dunstone MA, Kostenko L, Ely LK, Beddoe T, Mifsud N, et al. Crystal structure of the human T cell receptor CD3ε g heterodimer complexed to the therapeutic mAb OKT3. Proc Natl Acad Sci USA. 2004;101:7675-80.
33. Salmerón A, Sánchez-Madrid F, Ursa MA, Fresno M, Alarcón B. A conformational epitope expressed upon association of CD3-e with either CD3-d or CD3-g is the main target for recognition by anti-CD3 monoclonal antibodies. J Immunol. 1991;147:3047-52
34. Liu YY, Wang Z, Thomas J, Goodwin KJ, Stavrou S, Neville DM Jr. Polymorphisms of CD3ε in cynomolgus and rhesus monkeys and their relevance to anti-CD3 antibodies and immunotoxins. Immunol Cell Biol. 2007;85:357-62.
35. Call ME, Pyrdol J, Wiedmann M, Wucherpfennig KW. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell. 2002;111:967-79.
36. Call ME, Wucherpfennig KW. Molecular mechanisms for the assembly of the T cell receptor–CD3 complex. Mol Immunol. 2004;40:1295-305.
37. Pitcher LA, Mathis MA, Young JA, DeFord LM, Purtic B, Wulfing C, et al. The CD3 ge/de signaling module provides normal T cell functions in the absence of the TCR z immunoreceptor tyrosine-based activation motifs. Eur J Immunol. 2005;35:3643-54.
38. Lysechko TL, Ostergaard HL. Differential src family kinase activity requirements for CD3z phosphorylation/ ZAP70 recruitment and CD3ε phosphorylation. J Immunol. 2005;174:7807-14.
39. Davis MM. A new trigger for T cells. Cell. 2002;110: 285-7
40. Szymczak AL, Workman CJ, Gil D, Dilioglou S, Vignali KM, Palmer E, et al. The CD3 proline-rich sequence, and its interaction with Nck, is not required for T cell development and function. J Immunol. 2005;175:270-5.
2. Gynsin J. Animal models: primates. En: Sherman IW, editor. Malaria: parasite biology, pathogenesis and pro-tection. Washington, DC: ASM Press; 1998. p. 419-39.
3. Stowers AW, Miller L H. Are trials in new world monkeys on the critical path for blood-stage malaria vaccine development? Trends Parasitol. 2001;17:415-9.
4. Vogel TU, Evans DT, Urvater JA, OConnor DH, Hughes AL, Watkins DI. Major histocompatibility complex class I genes in primates: co-evolution with pathogens. Immunol Rev. 1999;167:327-37.
5. Bontrop RE, Otting N, de Groot NG, Doxiadis GG. Major histocompatibility complex class II polymorphisms in primates. Immunol Rev. 1999;167:339-50.
6. Heppner DG, Cummings JF, Ockenhouse C, Kester KE, Lyon JA, Gordon DM. New world monkey efficacy trials for malaria vaccine development: critical path or detour? Trends Parasitol. 2001;17:419-25.
7. Cantrell D. T cell antigen receptor signal transduction pathways. Annu Rev Immunol. 1996;14:259-74.
8. Germain RN, Štefanová I. The dynamics of T cell receptor signaling: complex orchestration and key roles of tempo and cooperation. Annu Rev Immunol. 1999;17:467-522.
9. Zamoyska R, Basson A, Filby A, Legname G, Lovatt M, Seddon B. The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol Rev. 2003;191:107-18.
10. Pitcher LA, van Oers NS. T-cell receptor signal transmission: who gives an ITAM? Trends Immunol. 2003;24:554-60.
11. Werlen G, Palmer E. The TCR signalosome: a dynamic structure with expanding complexity. Curr Opin Immunol. 2002;14:299-305.
12. Pan Q, Brodeur JF, Drbal K, Dave VP. Different role for mouse and human CD3ä/å heterodimer in preT cell receptor (preTCR) function: Human CD3d/e heterodimer restores the defective preTCR function in CD3g- and CD3 gd-deficient mice. Mol Immunol. 2006;43:1741-50.
13. Gil D, Schamel WW, Montoya M, Sánchez-Madrid F, Alarcón B. Recruitment of Nck by CD3 reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell. 2002;109:901-12.
14. Alarcón B, Gil D, Delgado P, Schamel WW. Initiation of TCR signaling: regulation within CD3 dimers. Immunol Rev. 2003;191:38-46.
15. Gil D, Schrum AG, Alarcón B, Palmer E. T cell receptor engagement by peptide-MHC ligands induces a conformational change in the CD3 complex of thymocytes. J Exp Med. 2005;201:517-22.
16. Gold DP, Puck JM, Pettey CL, Cho M, Coligan J, Woody JN, et al. Isolation of cDNA clones encoding the 20K non-glycosylated polypeptide chain of the human T-cell receptor/T3 complex. Nature. 1986;321: 431-4.
17. Gold DP, Clevers H, Alarcon B, Dunlap S, Novotny J, Williams AF, et al. Evolutionary relationship between the T3 chains of the T-cell receptor complex and the immunoglobulin supergene family. Proc Natl Acad Sci USA. 1987;84:7649-53.
18. Uda A, Tanabayashi K, Mukai R, Yachi M, Nam KH, Yamada A. CD3 polymorphism in cynomolgus monkeys (Macaca fascicularis). J Med Primatol. 2001;30:141-7.
19. Clevers H, Dunlap S, Saito H, Georgopoulos K, Wileman T, Terhorst C. Characterization and expression of the murine CD3-e gene. Proc Natl Acad Sci USA. 1988;85:8623-7.
20. Clevers HC, Dunlap S, Wileman TE, Terhorst C. Human CD3-e gene contains three miniexons and is transcribed from a non-TATA promoter. Proc Natl Acad Sci USA. 1988;85:8156-60.
21. Tunnacliffe A, Olsson C, Buluwela L, Rabbitts TH. Organization of the human CD3 locus on chromosome 11. Eur J Immunol. 1988;18:1639-42.
22. Pinzón-Charry A, Vernot JP, Rodríguez R, Patarroyo ME. Proliferative response of peripheral blood lymphocytes to mitogens in the owl monkey Aotus nancymae. J Med Primatol. 2003;32:31-8.
23. Montoya GE, Vernot JP, Patarroyo ME. Comparative analysis of CD45 proteins in primate context: owl monkeys vs humans. Tissue Antigens. 2004;64:165-72.
24. Vernot JP, Pérez-Quintero LA, Perdomo-Arciniegas AM, Quijano S, Patarroyo ME. Herpesvirus saimiri immortalization of Aotus T lymphocytes specific for an immunogenically modified peptide of Plasmodium falciparum merozoite surface antigen 2. Immunol Cell Biol. 2005;83:67-74.
25. Niño-Vásquez JJ, Vogel D, Rodríguez R, Moreno A, Patarroyo ME, Pluschke G, et al. Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites. Immunogenetics. 2000;51:219-30.
26. Díaz D, Naegeli M, Rodríguez R, Niño-Vásquez JJ, Moreno A, Patarroyo ME, et al. Sequence and diversity of MHC DQA and DQB genes of the owl monkey Aotus nancymaae. Immunogenetics. 2000;51:528-37.
27. Montoya GE, Vernot JP, Patarroyo ME. Partial characterization of the CD45 phosphatase cDNA in the owl monkey ( A. vociferans). Am J Primatol. 2002;57:1-11.
28. Rost B, Sander C. Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 1993;232:584-99.
29. Rost B, Fariselli P, Casadio R. Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci. 1996;5:1704-18.
30. Sun ZYJ, Kim KS, Wagner G, Reinherz EL. Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 eg heterodimer. Cell. 2001;105:913-23.
31. Arnett KL, Harrison SC, Wiley DC. Crystal structure of a human CD3-ed dimer in complex with a UCHT1 single-chain antibody fragment. Proc Natl Acad Sci USA. 2004;101:16268-73.
32. Kjer-Nielsen L, Dunstone MA, Kostenko L, Ely LK, Beddoe T, Mifsud N, et al. Crystal structure of the human T cell receptor CD3ε g heterodimer complexed to the therapeutic mAb OKT3. Proc Natl Acad Sci USA. 2004;101:7675-80.
33. Salmerón A, Sánchez-Madrid F, Ursa MA, Fresno M, Alarcón B. A conformational epitope expressed upon association of CD3-e with either CD3-d or CD3-g is the main target for recognition by anti-CD3 monoclonal antibodies. J Immunol. 1991;147:3047-52
34. Liu YY, Wang Z, Thomas J, Goodwin KJ, Stavrou S, Neville DM Jr. Polymorphisms of CD3ε in cynomolgus and rhesus monkeys and their relevance to anti-CD3 antibodies and immunotoxins. Immunol Cell Biol. 2007;85:357-62.
35. Call ME, Pyrdol J, Wiedmann M, Wucherpfennig KW. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell. 2002;111:967-79.
36. Call ME, Wucherpfennig KW. Molecular mechanisms for the assembly of the T cell receptor–CD3 complex. Mol Immunol. 2004;40:1295-305.
37. Pitcher LA, Mathis MA, Young JA, DeFord LM, Purtic B, Wulfing C, et al. The CD3 ge/de signaling module provides normal T cell functions in the absence of the TCR z immunoreceptor tyrosine-based activation motifs. Eur J Immunol. 2005;35:3643-54.
38. Lysechko TL, Ostergaard HL. Differential src family kinase activity requirements for CD3z phosphorylation/ ZAP70 recruitment and CD3ε phosphorylation. J Immunol. 2005;174:7807-14.
39. Davis MM. A new trigger for T cells. Cell. 2002;110: 285-7
40. Szymczak AL, Workman CJ, Gil D, Dilioglou S, Vignali KM, Palmer E, et al. The CD3 proline-rich sequence, and its interaction with Nck, is not required for T cell development and function. J Immunol. 2005;175:270-5.
How to Cite
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Vernot JP, del Castillo H. Characterizing the CD3 epsilon chain from the New World primate Aotus nancymaae. biomedica [Internet]. 2008 Jun. 1 [cited 2024 May 16];28(2):262-70. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/97
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