αβ and γδ T cell receptors: Similar but different.

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Abstrakt

Tytuł:: αβ and γδ T cell receptors: Similar but different.
Autorzy:: Morath A; Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Freiburg, Germany.; Institute of Biology III, Faculty of Biology, University of Freiburg, Freiburg, Germany.; Spemann Graduate School of Biology and Medicine (SGBM), University of Freiburg, Freiburg, Germany.
Schamel WW; Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Freiburg, Germany.; Institute of Biology III, Faculty of Biology, University of Freiburg, Freiburg, Germany.; Center for Chronic Immunodeficiency (CCI), Medical Center Freiburg and Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Źródło:: Journal of leukocyte biology [J Leukoc Biol] 2020 Jun; Vol. 107 (6), pp. 1045-1055. Date of Electronic Publication: 2020 Jan 29.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't; Review
Język:: English
Imprint Name(s):: Publication: 2023- : Oxford : Oxford University Press
Original Publication: New York : Alan R. Liss, c1984-
MeSH Terms:: CD3 Complex/*immunology
Cell Lineage/*immunology
Receptors, Antigen, T-Cell, alpha-beta/*immunology
Receptors, Antigen, T-Cell, gamma-delta/*immunology
T-Lymphocytes/*immunology
Amino Acid Sequence ; Animals ; Antibodies/pharmacology ; CD3 Complex/antagonists & inhibitors ; CD3 Complex/chemistry ; CD3 Complex/genetics ; Cell Differentiation ; Cell Lineage/genetics ; Gene Expression ; Glycosylation ; Humans ; Ligands ; Mice ; Protein Binding/drug effects ; Receptors, Antigen, T-Cell, alpha-beta/chemistry ; Receptors, Antigen, T-Cell, alpha-beta/genetics ; Receptors, Antigen, T-Cell, gamma-delta/chemistry ; Receptors, Antigen, T-Cell, gamma-delta/genetics ; Signal Transduction ; T-Lymphocytes/classification ; T-Lymphocytes/cytology ; T-Lymphocytes/drug effects ; Thymus Gland/cytology ; Thymus Gland/immunology
References:: Rast JP, Anderson MK, Strong SJ, Luer C, Litman RT, Litman GW. α, β, γ, and δ T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity. 1997;6(1):1-11.
Allison TJ, Winter CC, Fournié JJ, Bonneville M, Garboczi DN. Structure of a human gammadelta T-cell antigen receptor. Nature. 2001;411(6839):820-824.
Touma M, Chang H-C, Sasada T, Handley M, Clayton LK, Reinherz EL. The TCR C beta FG loop regulates alpha beta T cell development. J Immunol. 2006;176(11):6812-6823.
Sasada T, Touma M, Chang H-C, Clayton LK, Wang J-h, Reinherz EL. Involvement of the TCR C beta FG loop in thymic selection and T cell function. J Exp Med. 2002;195(11):1419-1431.
Swamy M, Minguet S, Siegers GM, Alarcón B, Schamel WWA. A native antibody-based mobility-shift technique (NAMOS-assay) to determine the stoichiometry of multiprotein complexes. J Immunol Methods. 2007;324(1-2):74-83.
Siegers GM, Swamy M, Fernández-Malavé E, et al. Different composition of the human and the mouse γδ T cell receptor explains different phenotypes of CD3γ and CD3δ immunodeficiencies. J Exp Med. 2007;204(11):2537-2544.
Punt JA, Roberts JL, Kearse KP, Singer A. Stoichiometry of the T cell antigen receptor (TCR) complex: each TCR/CD3 complex contains one TCR alpha, one TCR beta, and two CD3 epsilon chains. J Exp Med. 1994;180(2):587-593.
Hayes SM, Love PE. Distinct structure and signaling potential of the gamma delta TCR complex. Immunity. 2002;16(6):827-838.
Dadi HK, Simon AJ, Roifman CM. Effect of CD3delta deficiency on maturation of alpha/beta and gamma/delta T-cell lineages in severe combined immunodeficiency. N Engl J Med. 2003;349(19):1821-1828.
Basile GdS, Geissmann F, Flori E, et al. Severe combined immunodeficiency caused by deficiency in either the δ or the ε subunit of CD3. J Clin Invest. 2004;114(10):1512-1517.
Dave VP, Cao Z, Browne C, et al. CD3 delta deficiency arrests development of the alpha beta but not the gamma delta T cell lineage. EMBO J. 1997;16(6):1360-1370.
Muñoz-Ruiz M, Ribot JC, Grosso AR, et al. TCR signal strength controls thymic differentiation of discrete proinflammatory γδ T cell subsets. Nat Immunol. 2016;17(6):721-727.
Koyasu S. CD3+CD16+NK1.1+B220+ large granular lymphocytes arise from both alpha-beta TCR+CD4−CD8− and gamma-delta TCR+CD4−CD8− cells. J Exp Med. 1994;179(6):1957-1972.
Park SY, Arase H, Wakizaka K, et al. Differential contribution of the FcR gamma chain to the surface expression of the T cell receptor among T cells localized in epithelia: analysis of FcR gamma-deficient mice. Eur J Immunol. 1995;25(7):2107-2110.
Orloff DG, Ra CS, Frank SJ, Klausner RD, Kinet JP. Family of disulphide-linked dimers containing the zeta and eta chains of the T-cell receptor and the gamma chain of Fc receptors. Nature. 1990;347(6289):189-191.
Vivier E, Rochet N, Kochan JP, Presky DH, Schlossman SF, Anderson P. Structural similarity between Fc receptors and T cell receptors. Expression of the gamma-subunit of Fc epsilon RI in human T cells, natural killer cells and thymocytes. J Immunol. 1991;147(12):4263-4270.
Krishnan S, Warke VG, Nambiar MP, Tsokos GC, Farber DL. The FcR gamma subunit and Syk kinase replace the CD3 zeta-chain and ZAP-70 kinase in the TCR signaling complex of human effector CD4 T cells. J Immunol. 2003;170(8):4189-4195.
Ohno H, Ono S, Hirayama N, Shimada S, Saito T. Preferential usage of the Fc receptor gamma chain in the T cell antigen receptor complex by gamma/delta T cells localized in epithelia. J Exp Med. 1994;179(1):365-369.
Curnow SJ, Boyer C, Buferne M, Schmitt-Verhulst AM. TCR-associated zeta-Fc epsilon RI gamma heterodimers on CD4-CD8- NK1.1+ T cells selected by specific class I MHC antigen. Immunity. 1995;3(4):427-438.
Ohno H, Aoe T, Ra C, Yamamoto T, Saito T. TCR isoform containing the Fc receptor gamma chain exhibits structural and functional differences from isoform containing CD3 zeta. Int Immunol. 1993;5(11):1403-1411.
Krangel MS, Bierer BE, Devlin P, et al. T3 glycoprotein is functional although structurally distinct on human T-cell receptor gamma T lymphocytes. Proc Natl Acad Sci USA. 1987;84(11):3817-3821.
Alarcon B, de Vries J, Pettey C, et al. The T-cell receptor gamma chain-CD3 complex: implication in the cytotoxic activity of a CD3+ CD4− CD8− human natural killer clone. Proc Natl Acad Sci USA. 1987;84(11):3861-3865.
Hayes SM, Laky K, El-Khoury D, Kappes DJ, Fowlkes BJ, Love PE. Activation-induced modification in the CD3 complex of the gammadelta T cell receptor. J Exp Med. 2002;196(10):1355-1361.
Dong D, Zheng L, Lin J, et al. Structural basis of assembly of the human TCR-CD3 complex. Nature. 2019;573:546-552.
van Neerven J, Coligan JE, Koning F. Structural comparison of alpha/beta and gamma/delta T cell receptor-CD3 complexes reveals identical subunit interactions but distinct cross-linking patterns of T cell receptor chains. Eur J Immunol. 1990;20(9):2105-2111.
Brenner MB, Trowbridge IS, Strominger JL. Cross-linking of human T cell receptor proteins: association between the T cell idiotype β subunit and the T3 glycoprotein heavy subunit. Cell. 1985;40(1):183-190.
Marrack P, Scott-Browne JP, Dai S, Gapin L, Kappler JW. Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu Rev Immunol. 2008;26:171-203.
Garcia KC, Adams JJ, Feng D, Ely LK. The molecular basis of TCR germline bias for MHC is surprisingly simple. Nat Immunol. 2009;10(2):143-147.
Rudolph MG, Stanfield RL, Wilson IA. How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol. 2006;24:419-466.
Adams JJ, Narayanan S, Liu B, et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity. 2011;35(5):681-693.
Høydahl LS, Frick R, Sandlie I, Løset GÅ. Targeting the MHC ligandome by use of TCR-like antibodies. Antibodies. 2019;8(2):32.
Doyle C, Strominger JL. Interaction between CD4 and class II MHC molecules mediates cell adhesion. Nature. 1987;330(6145):256-259.
Norment AM, Salter RD, Parham P, Engelhard VH, Littman DR. Cell-cell adhesion mediated by CD8 and MHC class I molecules. Nature. 1988;336(6194):79-81.
Veillette A, Bookman MA, Horak EM, Bolen JB. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell. 1988;55(2):301-308.
van Laethem F, Sarafova SD, Park J-H, et al. Deletion of CD4 and CD8 coreceptors permits generation of alphabetaT cells that recognize antigens independently of the MHC. Immunity. 2007;27(5):735-750.
Chowdhary VR, Krogman A, Tilahun AY, Alexander MP, David CS, Rajagopalan G. Concomitant disruption of CD4 and CD8 genes facilitates the development of double negative αβ TCR+ peripheral T cells that respond robustly to staphylococcal superantigen. J Immunol. 2017;198(11):4413-4424.
Doucey M-A, Goffin L, Naeher D, et al. CD3 delta establishes a functional link between the T cell receptor and CD8. J Biol Chem. 2003;278(5):3257-3264.
Bäckström BT, Müller U, Hausmann B, Palmer E. Positive selection through a motif in the alphabeta T cell receptor. Science. 1998;281(5378):835-838.
Born WK, Kemal Aydintug M, O'Brien RL. Diversity of γδ T-cell antigens. Cell Mol Immunol. 2012;10(1):13-20.
Vantourout P, Hayday A. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat Rev Immunol. 2013;13(2):88-100.
Vermijlen D, Gatti D, Kouzeli A, Rus T, Eberl M. γδ T cell responses: how many ligands will it take till we know. Semin Cell Dev Biol. 2018;84:75-86.
Constant P, Davodeau F, Peyrat MA, et al. Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science. 1994;264(5156):267-270.
Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vgamma2Vdelta2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev. 2007;215:59-76.
Harly C, Guillaume Y, Nedellec S, et al. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood. 2012;120(11):2269-2279.
Karunakaran MM, Herrmann T. The Vγ9Vδ2 T cell antigen receptor and butyrophilin-3 A1: models of interaction, the possibility of co-evolution, and the case of dendritic epidermal T cells. Front Immunol. 2014;5:648.
De Libero G, Lau S-Y, Mori L. Phosphoantigen presentation to TCR γδ cells, a conundrum getting less gray zones. Front Immunol. 2015;5:679.
Gu S, Nawrocka W, Adams EJ. Sensing of pyrophosphate metabolites by Vγ9Vδ2 T cells. Front Immunol. 2014;5:688.
Vavassori S, Kumar A, Wan GS, et al. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat Immunol. 2013;14(9):908-916.
Sandstrom A, Peigné C-M, Léger A, et al. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity. 2014;40(4):490-500.
Nguyen K, Li J, Puthenveetil R, et al. The butyrophilin 3A1 intracellular domain undergoes a conformational change involving the juxtamembrane region. FASEB J. 2017;31(11):4697-4706.
Melandri D, Zlatareva I, Chaleil RAG, et al. The γδTCR combines innate immunity with adaptive immunity by utilizing spatially distinct regions for agonist selection and antigen responsiveness. Nat Immunol. 2018;19(12):1352-1365.
Rudolph MG, Wilson IA. The specificity of TCR/pMHC interaction. Curr Opin Immunol. 2002;14(1):52-65.
Chien YH, Jores R, Crowley MP. Recognition by gamma/delta T cells. Annu Rev Immunol. 1996;14:511-532.
Rock EP, Sibbald PR, Davis MM, Chien YH. CDR3 length in antigen-specific immune receptors. J Exp Med. 1994;179(1):323-328.
Adams EJ, Chien Y-h, Garcia KC. Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science. 2005;308(5719):227-231.
Gil D, Schamel WWA, Montoya M, Sánchez-Madrid F, Alarcón B. Recruitment of Nck by CD3 epsilon reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell. 2002;109(7):901-912.
Paensuwan P, Hartl FA, Yousefi OS, et al. Nck binds to the T cell antigen receptor using its SH3.1 and SH2 domains in a cooperative manner, promoting TCR functioning. J Immunol. 2016;196(1):448-458.
Minguet S, Swamy M, Alarcón B, Luescher IF, Schamel WWA. Full activation of the T cell receptor requires both clustering and conformational changes at CD3. Immunity. 2007;26(1):43-54.
Martínez-Martín N, Risueño RM, Morreale A, et al. Cooperativity between T cell receptor complexes revealed by conformational mutants of CD3epsilon. Sci Signal. 2009;2(83):ra43.
Roy E, Togbe D, Holdorf AD, et al. Nck adaptors are positive regulators of the size and sensitivity of the T-cell repertoire. Proc Natl Acad Sci U S A. 2010;107(35):15529-15534.
Roy E, Togbe D, Holdorf A, et al. Fine tuning of the threshold of T cell selection by the Nck adapters. J Immunol. 2010;185(12):7518-7526.
Borroto A, Arellano I, Dopfer EP, et al. Nck recruitment to the TCR required for ZAP70 activation during thymic development. J Immunol. 2013;190(3):1103-1112.
Blanco R, Borroto A, Schamel W, Pereira P, Alarcon B. Conformational changes in the T cell receptor differentially determine T cell subset development in mice. Sci Signal. 2014;7(354):ra115.
Carding SR, Egan PJ. Gammadelta T cells: functional plasticity and heterogeneity. Nat Rev Immunol. 2002;2(5):336-345.
Prinz I, Silva-Santos B, Pennington DJ. Functional development of γδ T cells. Eur J Immunol. 2013;43(8):1988-1994.
Asarnow DM, Kuziel WA, Bonyhadi M, Tigelaar RE, Tucker PW, Allison JP. Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell. 1988;55(5):837-847.
Ferrero I, Wilson A, Beermann F, Held W, MacDonald HR. T cell receptor specificity is critical for the development of epidermal gammadelta T cells. J Exp Med. 2001;194(10):1473-1483.
Pereira P, Boucontet L. Innate NKTγδ and NKTαβ cells exert similar functions and compete for a thymic niche. Eur J Immunol. 2012;42(5):1272-1281.
Gerber DJ, Azuara V, Levraud JP, Huang SY, Lembezat MP, Pereira P. IL-4-producing gamma delta T cells that express a very restricted TCR repertoire are preferentially localized in liver and spleen. J Immunol. 1999;163(6):3076-3082.
Hayday A, Gibbons D. Brokering the peace: the origin of intestinal T cells. Mucosal Immunol. 2008;1(3):172-174.
Dopfer EP, Hartl FA, Oberg H-H, et al. The CD3 conformational change in the γδ T cell receptor is not triggered by antigens but can be enforced to enhance tumor killing. Cell Rep. 2014;7(5):1704-1715.
Correia DV, d'Orey F, Cardoso BA, et al. Highly active microbial phosphoantigen induces rapid yet sustained MEK/Erk- and PI-3K/Akt-mediated signal transduction in anti-tumor human gammadelta T-cells. PLoS ONE. 2009;4(5):e5657.
Tao C, Shao H, Zhang W, et al. γδTCR immunoglobulin constant region domain exchange in human αβTCRs improves TCR pairing without altering TCR gene-modified T cell function. Mol Med Rep. 2017;15(4):1555-1564.
Ulivieri C, Peter A, Orsini E, Palmer E, Baldari CT. Defective signaling to Fyn by a T cell antigen receptor lacking the alpha -chain connecting peptide motif. J Biol Chem. 2001;276(5):3574-3580.
Werlen G, Hausmann B, Palmer E. A motif in the alphabeta T-cell receptor controls positive selection by modulating ERK activity. Nature. 2000;406(6794):422-426.
Bäckström BT, Milia E, Peter A, Jaureguiberry B, Baldari CT, Palmer E. A motif within the T cell receptor alpha chain constant region connecting peptide domain controls antigen responsiveness. Immunity. 1996;5(5):437-447.
Boyden LM, Lewis JM, Barbee SD, et al. Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal gammadelta T cells. Nat Genet. 2008;40(5):656-662.
Juraske C, Wipa P, Morath A, et al. Anti-CD3 Fab fragments enhance tumor killing by human γδ T cells independent of nck recruitment to the γδ T cell antigen receptor. Front Immunol. 2018;9:1579.
Molnár E, Swamy M, Holzer M, et al. Cholesterol and sphingomyelin drive ligand-independent T-cell antigen receptor nanoclustering*. J Biol Chem. 2012;287(51):42664-42674.
Schamel WWA, Alarcón B. Organization of the resting TCR in nanoscale oligomers. Immunol Rev. 2013;251(1):13-20.
Fahmy TM, Bieler JG, Edidin M, Schneck JP. Increased TCR avidity after T cell activation: a mechanism for sensing low-density antigen. Immunity. 2001;14(2):135-143.
Drake DR, Braciale TJ. Cutting edge: lipid raft integrity affects the efficiency of MHC class I tetramer binding and cell surface TCR arrangement on CD8+ T cells. J Immunol. 2001;166(12):7009-7013.
Kumar R, Ferez M, Swamy M, et al. Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. Immunity. 2011;35(3):375-387.
Swamy M, Beck-Garcia K, Beck-Garcia E, et al. A cholesterol-based allostery model of T cell receptor phosphorylation. Immunity. 2016;44(5):1091-1101.
Chen Y, Shao L, Ali Z, Cai J, Chen ZW. NSOM/QD-based nanoscale immunofluorescence imaging of antigen-specific T-cell receptor responses during an in vivo clonal Vγ2Vδ2 T-cell expansion. Blood. 2008;111(8):4220-4232.
Cheng H-Y, Wu R, Gebre AK, et al. Increased cholesterol content in gammadelta (γδ) T lymphocytes differentially regulates their activation. PLoS ONE. 2013;8(5):e63746.
Wang F, Beck-García K, Zorzin C, Schamel WWA, Davis MM. Inhibition of T cell receptor signaling by cholesterol sulfate, a naturally occurring derivative of membrane cholesterol. Nat Immunol. 2016;17(7):844-850.
Petersen TR, Gülland S, Bettelli E, Kuchroo V, Palmer E, Bäckström BT. A chimeric T cell receptor with super-signaling properties. Int Immunol. 2004;16(7):889-894.
Hayes SM, Li L, Love PE. TCR signal strength influences alphabeta/gammadelta lineage fate. Immunity. 2005;22(5):583-593.
Laird RM, Hayes SM. Profiling of the early transcriptional response of murine gammadelta T cells following TCR stimulation. Mol Immunol. 2009;46(11-12):2429-2438.
Laird RM, Laky K, Hayes SM. Unexpected role for the B cell-specific Src family kinase B lymphoid kinase in the development of IL-17-producing γδ T cells. J Immunol. 2010;185(11):6518-6527.
Aivazian D, Stern LJ. Phosphorylation of T cell receptor zeta is regulated by a lipid dependent folding transition. Nat Struct Biol. 2000;7(11):1023-1026.
Xu C, Gagnon E, Call ME, et al. Regulation of T cell receptor activation by dynamic membrane binding of the CD3ε cytoplasmic tyrosine-based motif. Cell. 2008;135(4):702-713.
Gagnon E, Schubert DA, Gordo S, Chu HH, Wucherpfennig KW. Local changes in lipid environment of TCR microclusters regulate membrane binding by the CD3ε cytoplasmic domain. J Exp Med. 2012;209(13):2423-2439.
Shi X, Bi Y, Yang W, et al. Ca2+ regulates T-cell receptor activation by modulating the charge property of lipids. Nature. 2013;493(7430):111-115.
Lü H-Z, Zhu A-Y, Chen Y, Tang J, Li B-Q. Formation and aggregation of lipid rafts in γδ T cells following stimulation with Mycobacterium tuberculosis antigens. Tohoku J Exp Med. 2011;223(3):193-198.
Zhong L, Zhang Z, Lu X, Liu S, Chen CY, Chen ZW. NSOM/QD-based visualization of GM1 serving as platforms for TCR/CD3 mediated T-cell activation. Biomed Res Int. 2013;2013:276498.
Heilig JS, Tonegawa S. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature. 1986;322(6082):836-840.
LeFranc MP, Forster A, Baer R, Stinson MA, Rabbitts TH. Diversity and rearrangement of the human T cell rearranging gamma genes: nine germ-line variable genes belonging to two subgroups. Cell. 1986;45(2):237-246.
Contributed Indexing:: Keywords: CD3; assembly; cholesterol; glycosylation; nanoclusters; proline rich sequence
Substance Nomenclature:: 0 (Antibodies)
0 (CD3 Complex)
0 (CD3E protein, human)
0 (Ligands)
0 (Receptors, Antigen, T-Cell, alpha-beta)
0 (Receptors, Antigen, T-Cell, gamma-delta)
Entry Date(s):: Date Created: 20200130 Date Completed: 20201104 Latest Revision: 20201104
Update Code:: 20240105
DOI:: 10.1002/JLB.2MR1219-233R
PMID:: 31994778
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There are 2 populations of T lymphocytes, αβ T and γδ T cells, that can be distinguished by the expression of either an αβ TCR or a γδ TCR, respectively. Pairing of the Ag binding heterodimer, which consists of TCR-α/TCR-β (TCRαβ) or TCR-γ/TCR-δ (TCRγδ), with proteins of the CD3 complex forms the complete αβ or γδ TCR. Despite some similarities in the structure of TCRαβ and TCRγδ and the shared subunits of the CD3 complex, the 2 receptors differ in important aspects. These include the assembly geometry of the complex, the glycosylation pattern, the plasma membrane organization, as well as the accessibility of signaling motifs in the CD3 intracellular tails. These differences are reflected in the different demands and outcomes of ligand-induced signaling. It was shown that exposure of the proline-rich sequence (PRS) in CD3ε occurs with all activating αβ TCR ligands and is required to induce αβ TCR signaling. In sharp contrast, CD3ε PRS exposure was not induced by binding of those ligands to the γδ TCR that have been studied. Further, signaling by the γδ TCR occurs independently of CD3ε PRS exposure. Interestingly, it can be enhanced by anti-CD3ε Ab-induced enforcement of CD3ε PRS exposure. This review contrasts these two similar, but different immune receptors.
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