TRM maintenance is regulated by tissue damage via P2RX7

Science Immunology

Volumn 3, Issue 30, 2018, Pages

  Stark, Regina ^a,b   Wesselink, Thomas H ^a   Behr, Felix M ^a,b   Kragten, Natasja A M ^a   Arens, Ramon ^c   Koch Nolte, Friedrich ^d   van Gisbergen, Klaas P J M ^a,b   van Lier, René A W ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AIM2 PROTEIN; CD103 ANTIGEN; CHEMOKINE RECEPTOR CXCR6; INTERLEUKIN 12; INTERLEUKIN 33; L SELECTIN; P2RX7 PROTEIN; P2RY10 PROTEIN; PEPTIDES AND PROTEINS; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOBIT; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; P2RX7 PROTEIN, MOUSE; PURINERGIC P2X7 RECEPTOR;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; LIVER INJURY; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOCYTE DIFFERENTIATION; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; SIGNAL TRANSDUCTION; TISSUE RESIDENT MEMORY T LYMPHOCYTE; UPREGULATION; ANIMAL; C57BL MOUSE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KNOCKOUT MOUSE; LIVER; LYMPHOCYTE; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; IMMUNOLOGIC MEMORY; LIVER; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, PURINERGIC P2X7;

EID: 85059254087     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aau1022     Document Type: Article

References (60)

1. T. Gebhardt, L. M. Wakim, L. Eidsmo, P. C. Reading, W. R. Heath, F. R. Carbone, Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524–530 (2009).
2. + TRM cells providing global skin immunity. Nature 483, 227–231 (2012).
3. L. K. Mackay, A. T. Stock, J. Z. Ma, C. M. Jones, S. J. Kent, S. N. Mueller, W. R. Heath, F. R. Carbone, T. Gebhardt, Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc. Natl. Acad. Sci. U.S.A. 109, 7037–7042 (2012).
4. J. M. Schenkel, K. A. Fraser, L. K. Beura, K. E. Pauken, V. Vezys, D. Masopust, Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science 346, 98–101 (2014).
5. + T cells trigger a state of tissue-wide pathogen alert. Science 346, 101–105 (2014).
6. S. R. McMaster, J. J. Wilson, H. Wang, J. E. Kohlmeier, Airway-resident memory CD8 T cells provide antigen-specific protection against respiratory virus challenge through rapid IFN- production. J. Immunol. 195, 203–209 (2015).
7. D. Tang, R. Kang, C. B. Coyne, H. J. Zeh, M. T. Lotze, PAMPs and DAMPs: Signal 0s that spur autophagy and immunity. Immunol. Rev. 249, 158–175 (2012).
8. G. Y. Chen, G. Nunez, Sterile inflammation: Sensing and reacting to damage. Nat. Rev. Immunol. 10, 826–837 (2010).
9. + T cells is independent of glycolysis. J. Immunol. 196, 3695–3705 (2016).
10. A. Cottalorda, C. Verschelde, A. Marcais, M. Tomkowiak, P. Musette, S. Uematsu, S. Akira, J. Marvel, N. Bonnefoy-Berard, TLR2 engagement on CD8 T cells lowers the threshold for optimal antigen-induced T cell activation. Eur. J. Immunol. 36, 1684–1693 (2006).
11. B. C. Mercier, A. Cottalorda, C. A. Coupet, J. Marvel, N. Bonnefoy-Berard, TLR2 engagement on CD8 T cells enables generation of functional memory cells in response to a suboptimal TCR signal. J. Immunol. 182, 1860–1867 (2009).
12. B. C. Mercier, E. Ventre, M. L. Fogeron, A. L. Debaud, M. Tomkowiak, J. Marvel, N. Bonnefoy, NOD1 cooperates with TLR2 to enhance T cell receptor-mediated activation in CD8 T cells. PLOS ONE 7, e42170 (2012).
13. M. Quigley, J. Martinez, X. Huang, Y. Yang, A critical role for direct TLR2-MyD88 signaling in CD8 T-cell clonal expansion and memory formation following vaccinia viral infection. Blood 113, 2256–2264 (2009).
14. T. Woehrle, L. Yip, A. Elkhal, Y. Sumi, Y. Chen, Y. Yao, P. A. Insel, W. G. Junger, Pannexin-1 hemichannel–mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 116, 3475–3484 (2010).
15. B. Rissiek, F. Haag, O. Boyer, F. Koch-Nolte, S. Adriouch, P2X7 on mouse T cells: One channel, many functions. Front. Immunol. 6, 204 (2015).
16. + T cells. Nature 559, 264–268 (2018).
17. + T cell survival and fitness. Immunity 37, 235–248 (2012).
18. + T cells. J. Immunol. 198, 2260–2268 (2017).
19. B. Larkin, V. Ilyukha, M. Sorokin, A. Buzdin, E. Vannier, A. Poltorak, Cutting edge: Activation of STING in T cells induces type I IFN responses and cell death. J. Immunol. 199, 397–402 (2017).
20. F. Di Virgilio, D. Dal Ben, A. C. Sarti, A. L. Giuliani, S. Falzoni, The P2X7 receptor in infection and inflammation. Immunity 47, 15–31 (2017).
21. +-dependent signalling. FEBS Lett. 585, 1651–1656 (2011).
22. + released during inflammation participates in T cell homeostasis by inducing ART2-mediated death of naive T cells in vivo. J. Immunol. 179, 186–194 (2007).
23. P. Pellegatti, L. Raffaghello, G. Bianchi, F. Piccardi, V. Pistoia, F. Di Virgilio, Increased level of extracellular ATP at tumor sites: In vivo imaging with plasma membrane luciferase. PLOS ONE 3, e2599 (2008).
24. K. Wilhelm, J. Ganesan, T. Muller, C. Durr, M. Grimm, A. Beilhack, C. D. Krempl, S. Sorichter, U. V. Gerlach, E. Juttner, A. Zerweck, F. Gartner, P. Pellegatti, F. Di Virgilio, D. Ferrari, N. Kambham, P. Fisch, J. Finke, M. Idzko, R. Zeiser, Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat. Med. 16, 1434–1438 (2010).
25. M. Idzko, D. Ferrari, H. K. Eltzschig, Nucleotide signalling during inflammation. Nature 509, 310–317 (2014).
26. W. G. Junger, Immune cell regulation by autocrine purinergic signalling. Nat. Rev. Immunol. 11, 201–212 (2011).
27. M. Seman, S. Adriouch, F. Scheuplein, C. Krebs, D. Freese, G. Glowacki, P. Deterre, F. Haag, F. Koch-Nolte, NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 19, 571–582 (2003).
28. F. Haag, S. Adriouch, A. Brass, C. Jung, S. Moller, F. Scheuplein, P. Bannas, M. Seman, F. Koch-Nolte, Extracellular NAD and ATP: Partners in immune cell modulation. Purinergic Signal. 3, 71–81 (2007).
29. L. K. Mackay, M. Minnich, N. A. M. Kragten, Y. Liao, B. Nota, C. Seillet, A. Zaid, K. Man, S. Preston, D. Freestone, A. Braun, E. Wynne-Jones, F. M. Behr, R. Stark, D. G. Pellicci, D. I. Godfrey, G. T. Belz, M. Pellegrini, T. Gebhardt, M. Busslinger, W. Shi, F. R. Carbone, R. A. W. van Lier, A. Kallies, K. P. J. M. van Gisbergen, Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352, 459–463 (2016).
30. M. Salmi, S. Jalkanen, Cell-surface enzymes in control of leukocyte trafficking. Nat. Rev. Immunol. 5, 760–771 (2005).
31. + T cells to nucleotides indicates P2X7 as a regulator for intestinal T cell responses. J. Immunol. 181, 3861–3869 (2008).
32. B. Rissiek, W. Danquah, F. Haag, F. Koch-Nolte, Technical advance: A new cell preparation strategy that greatly improves the yield of vital and functional Tregs and NKT cells. J. Leukoc. Biol. 95, 543–549 (2014).
33. + T cells form a front-line defense against malaria liver-stage infection. Immunity 45, 889–902 (2016).
34. B. Rissiek, M. Lukowiak, F. Raczkowski, T. Magnus, H.-W. Mittrücker, F. Koch-Nolte, In vivo blockade of murine ARTC2.2 during cell preparation preserves the vitality and function of liver tissue-resident memory T cells. Front. Immunol. 9, 1580 (2018).
35. + tissue-resident memory T cells. Cell Rep. 19, 114–124 (2017).
36. + T cells at the site of tissue regeneration enable CD69-independent maintenance. J. Exp. Med. 213, 3057–3073 (2016).
37. H. Shin, A. Iwasaki, A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491, 463–467 (2012).
38. N. Iijima, A. Iwasaki, A local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells. Science 346, 93–98 (2014).
39. + lung-resident memory T cells. Nat. Immunol. 17, 1467–1478 (2016).
40. N. A. M. Kragten, F. M. Behr, F. A. Vieira Braga, E. B. M. Remmerswaal, T. H. Wesselink, A. E. Oja, P. Hombrink, A. Kallies, R. A. W. van Lier, R. Stark, K. P. J. M. van Gisbergen, Blimp-1 induces and Hobit maintains the cytotoxic mediator granzyme B in CD8 T cells. Eur. J. Immunol. 48, 1644–1662 (2018).
41. C. O. Park, T. S. Kupper, The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat. Med. 21, 688–697 (2015).
42. M. Proietti, V. Cornacchione, T. Rezzonico Jost, A. Romagnani, C. E. Faliti, L. Perruzza, R. Rigoni, E. Radaelli, F. Caprioli, S. Preziuso, B. Brannetti, M. Thelen, K. D. McCoy, E. Slack, E. Traggiai, F. Grassi, ATP-gated ionotropic P2X7 receptor controls follicular T helper cell numbers in Peyer's patches to promote host-microbiota mutualism. Immunity 41, 789–801 (2014).
43. S. L. Park, A. Zaid, J. L. Hor, S. N. Christo, J. E. Prier, B. Davies, Y. O. Alexandre, J. L. Gregory, T. A. Russell, T. Gebhardt, F. R. Carbone, D. C. Tscharke, W. R. Heath, S. N. Mueller, L. K. Mackay, Local proliferation maintains a stable pool of tissue-resident memory T cells after antiviral recall responses. Nat. Immunol. 19, 183–191 (2018).
44. R. M. Zinkernagel, E. Haenseler, T. Leist, A. Cerny, H. Hengartner, A. Althage, T cell-mediated hepatitis in mice infected with lymphocytic choriomeningitis virus. Liver cell destruction by H-2 class I-restricted virus-specific cytotoxic T cells as a physiological correlate of the 51Cr-release assay? J. Exp. Med. 164, 1075–1092 (1986).
45. + tissue-resident memory T cells of skin. Nat. Immunol. 14, 1294–1301 (2013).
46. A. Zaid, L. K. Mackay, A. Rahimpour, A. Braun, M. Veldhoen, F. R. Carbone, J. H. Manton, W. R. Heath, S. N. Mueller, Persistence of skin-resident memory T cells within an epidermal niche. Proc. Natl. Acad. Sci. U.S.A. 111, 5307–5312 (2014).
47. A. Yoshizawa, K. Bi, D. B. Keskin, G. Zhang, B. Reinhold, E. L. Reinherz, TCR-pMHC encounter differentially regulates transcriptomes of tissue-resident CD8 T cells. Eur. J. Immunol. 48, 128–150 (2018).
48. E. M. Steinert, J. M. Schenkel, K. A. Fraser, L. K. Beura, L. S. Manlove, B. Z. Igyarto, P. J. Southern, D. Masopust, Quantifying memory CD8 T cells reveals regionalization of immunosurveillance. Cell 161, 737–749 (2015).
49. + regulatory T cell compartment through the ART2–P2X7 pathway. J. Exp. Med. 207, 2561–2568 (2010).
50. + regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: A role for P2X7 receptors. J. Immunol. 175, 3075–3083 (2005).
51. H. Kawamura, F. Aswad, M. Minagawa, S. Govindarajan, G. Dennert, P2X7 receptors regulate NKT cells in autoimmune hepatitis. J. Immunol. 176, 2152–2160 (2006).
52. S. Hashimoto-Hill, L. Friesen, M. Kim, C. H. Kim, Contraction of intestinal effector T cells by retinoic acid-induced purinergic receptor P2X7. Mucosal Immunol. 10, 912–923 (2017).
53. H. Georgiev, I. Ravens, G. Papadogianni, B. Malissen, R. Forster, G. Bernhardt, Blocking the ART2.2/P2X7-system is essential to avoid a detrimental bias in functional CD4 T cell studies. Eur. J. Immunol. 48, 1078–1081 (2018).
54. M. Kuhny, T. Hochdorfer, C. K. Ayata, M. Idzko, M. Huber, CD39 is a negative regulator of P2X7-mediated inflammatory cell death in mast cells. Cell Commun. Signal. 12, 40 (2014).
55. S. Deaglio, K. M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J. F. Chen, K. Enjyoji, J. Linden, M. Oukka, V. K. Kuchroo, T. B. Strom, S. C. Robson, Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204, 1257–1265 (2007).
56. + immune regulatory cells, promotes T-cell expansion, and skews T-cell repertoire in multiple myeloma. Blood 128, 384–394 (2016).
57. A. P. Ganesan, J. Clarke, O. Wood, E. M. Garrido-Martin, S. J. Chee, T. Mellows, D. Samaniego-Castruita, D. Singh, G. Seumois, A. Alzetani, E. Woo, P. S. Friedmann, E. V. King, G. J. Thomas, T. Sanchez-Elsner, P. Vijayanand, C. H. Ottensmeier, Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer. Nat. Immunol. 18, 940–950 (2017).
58. + T cell-mediated tumour immunotherapy. Nat. Commun. 8, 15327 (2017).
59. + T cells with enhanced protective function. Immunity 40, 747–757 (2014).
60. F. Koch-Nolte, J. Reyelt, B. Schößow, N. Schwarz, F. Scheuplein, S. Rothenburg, F. Haag, V. Alzogaray, A. Cauerhff, F. A. Goldbaum, Single domain antibodies from llama effectively and specifically block T cell ecto-ADP-ribosyltransferase ART2.2 in vivo. FASEB J. 21, 3490–3498 (2007).