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Γδ T Cell Update: Adaptate Orchestrators of Immune Surveillance δγ T Cell Update: Adaptate Orchestrators of Immune Surveillance Adrian C. Hayday This information is current as J Immunol 2019; 203:311-320; ; of September 29, 2021. doi: 10.4049/jimmunol.1800934 http://www.jimmunol.org/content/203/2/311 Downloaded from References This article cites 136 articles, 58 of which you can access for free at: http://www.jimmunol.org/content/203/2/311.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average by guest on September 29, 2021 Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. gd T Cell Update: Adaptate Orchestrators of Immune Surveillance Adrian C. Hayday As interest in gd T cells grows rapidly, what key points exclude such reactivities from their repertoire (4). The few are emerging, and where is caution warranted? gd Tcells TCR gd Ags so far characterized are structurally diverse, fulfill critical functions, as reflected in associations with including MHC, CD1, several other cell-bound Ags, vaccine responsiveness and cancer survival in humans and histidyl-tRNA synthetase, and haptens that may modify cell ever more phenotypes of gd T cell–deficient mice, in- surface proteins (5, 6). This breadth seemingly reflects an cluding basic physiological deficiencies. Such phenotypes enormous potential for diversity, particularly of TCRd (7). reflect activities of distinct gd T cell subsets, whose ori- Moreover, this potential has been further increased in Xen- gins offer interesting insights into lymphocyte develop- opus by inclusion into the TCRd locus of Ig–VH gene seg- Downloaded from ment but whose variable evolutionary conservation can ments (8) and in marsupials and sharks by the generation of obfuscate translation of knowledge from mice to humans. TCRd-based 3-Ig-domain receptor chains that pair with By contrast, an emerging and conserved feature of TCRg to form TCRm and new Ag receptor–TCR mole- gd T cells is their “adaptate” biology: an integration of cules, respectively (9, 10). Thus, a major challenge is to gd adaptive clonally-restricted specificities, innate tissue- reconcile roles for T cells in immunosurveillance with an http://www.jimmunol.org/ sensing, and unconventional recall responses that collec- unparalleled potential for diversity. Additionally, gd T cells may expand the spatial and temporal tively strengthen host resistance to myriad challenges. ranges of immune responsiveness by being activated in ana- Central to adaptate biology are butyrophilins and other tomical sites and/or ontogenetic periods not well served by gd cell regulators, the study of which should greatly en- B cells and ab T cells (11). Although gray short-tailed opos- hance our understanding of tissue immunogenicity and sums may be an exception (12), many gd T cell subsets mature immunosurveillance and guide intensifying clinical interest prior to ab T cell maturation (13), with further examples in gd cells and other unconventional lymphocytes. The continuing to emerge in mice and in humans (14–16). Pre- Journal of Immunology, 2019, 203: 311–320. dictably, therefore, some gd T cell phenotypes are most overt by guest on September 29, 2021 prior to adulthood (17, 18). unning like a central artery through the biology of Furthermore, the rapid response kinetics of gd T cells (19) gd T cells is one major question, namely, what may critically regulate tissue immunogenicity by altering the R unique host benefit is contributed by a highly con- local milieu so as to accommodate time-delayed adaptive re- served third lineage of cells that, together with B cells and ab sponses of B cells and ab T cells while promoting key ele- T cells, has somatically diversified surface receptors (1)? The ments of tissue repair and regeneration (20). Conversely, question’s significance was starkly reinforced when a wholly dysregulation of such activities might fuel inflammatory unrelated molecular mechanism in jawless vertebrates (agna- pathologic conditions, potentially underpinning ever more thans) was found to likewise diversify three cell lineages (2). causal implications of murine gd T cells in experimental al- lergic encephalomyelitis (a mouse model of multiple sclero- gd T cell uniqueness sis), type I diabetes, skin inflammation, and cancer (21–26). For 25 years, gd cells have highlighted atypical lymphoid Notwithstanding these possibilities, our perspectives on how effector functions, such as keratinocyte growth factor pro- gd T cells expand immunological range will likely require us duction (3), but their primary role may be to expand the to think more laterally about the host response to infection breadth of immune responsiveness. Unlike ab Tcells, and tissue dysregulation. To illustrate this, we shall consider gd T cells are not limited to recognition of peptides pre- emerging data depicting three modes of gd T cell response sented by MHC proteins, lipids presented by CD1, and (Fig. 1), none of which is easily accommodated by today’s metabolites presented by MR1, although this does not immunology textbooks. Peter Gorer Department of Immunobiology, King’s College London, London SE1 9RT, Abbreviations used in this article: BTN3A, butyrophilin 3A; Btnl, Btn-like; DAMP, United Kingdom; and Francis Crick Institute, London NW1 1AT, United Kingdom danger-associated molecular pattern; DETC, dendritic epidermal T cell; EPCR, epithe- lial protein C receptor; HV4, hypervariable region 4; IEL, intraepithelial lymphocyte; ORCID: 0000-0002-9495-5793 (A.C.H.). ILC, innate lymphoid cell; LN, lymph node; LP, lamina propria; PAg, phosphoantigen; Received for publication July 10, 2018. Accepted for publication May 2, 2019. Treg, T regulatory. This work was supported by the Wellcome Trust and the Francis Crick Institute. Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 Address correspondence and reprint requests to Prof. Adrian C. Hayday, King’s College Faculty of Life Sciences and Medicine, 2nd Floor, Borough Wing, Guy’s Hospital, London SE1 9RT, U.K. E-mail address: [email protected] www.jimmunol.org/cgi/doi/10.4049/jimmunol.1800934 312 BRIEF REVIEWS: gd T CELL BIOLOGY characterized expressed a human Vg4Vd5 TCR specific for epithelial protein C receptor (EPCR), a CD1-like protein that can be upregulated by CMV infection and cell transformation (6, 35). With current knowledge, this adaptive response seems puz- zling: how did EPCR-reactive cells avoid immunological tol- erance of self? How was their expansion favored versus the potential expansion of gd cell clones with different specificities (e.g., CMV or self)? How do they finely distinguish virus- infected and/or transformed cells from healthy cells? And ul- timately, how do they confer host benefit? Moreover, the same questions pertain to other self-reactive gd T cells, including a human glioblastoma-reactive clone specific for annexin A2, whose surface expression is likewise promoted by CMV (36). This puzzling scenario also arose in Lyme disease, for which FIGURE 1. Mouse and human gd T cells display at least three types of the etiologic agent is Borrelia burgdorferi. Relative to wild-type 2/2 response: durable adaptive clonal expansion of gd T cells, durable quasi- mice, Borrelia-infected TCRd mice display increased bac- adaptive expansions, and durable innate repertoire selection. terial burden and cardiac inflammation, associated with greatly Downloaded from diminished ab T cell and B cell expansions and reduced anti- Borrelia serum Abs, cytokines, and chemokines (37). Seemingly How and when do gd T cells respond? consistent with this important role of gd Tcells,humanΤ cells Adaptive responses. Recent analyses of human peripheral blood expressing the Vd1 gene segment were expanded in inflamed and liver revealed large, durable, subject-specific expansions, synovial joints of patients with Lyme disease. However, rather commonly dominated by a few highly diverse gd TCRs. than being Borrelia-reactive, the expanded cells were responsive http://www.jimmunol.org/ Moreover, the expansions were enriched in CD27loCX3CR1+ to myelomonocytic cells making TLR-dependent responses granzyme-expressing cells, consistent with clonal naive-to- to Borrelia (38), and their Vd1 TCRs bound to activated, effector differentiation, a signature of adaptive immunity uninfected monocytes and lymphocytes (R. Budd, personal (27–29). communication). The clones’ specificities have yet to be deduced, but, given In sum, seemingly prototypic adaptive responses have so far the potential for diversity in TCRgd, they could be reasonably identified self-reactive rather than pathogen-specific gd cells, expected to include microbe-specific determinants reflecting albeit that such studies are in their infancy. Assuredly, not all subject-specific environmental exposures. Potentially consis- TCRgd reactivities will be self-reactive,
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