Human intrahepatic CD69 + CD8+ T cells have a tissue resident memory T cell phenotype with reduced cytolytic capacity

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Stelma, Femke ^a   De Niet, Annikki ^a   Sinnige, Marjan J ^a   Van Dort, Karel A ^a   Van Gisbergen, Klaas P J M ^b   Verheij, Joanne ^a   Van Leeuwen, Ester M M ^a   Kootstra, Neeltje A ^a   Reesink, Hendrik W ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b SANQUIN RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA E INTEGRINS; ALPHA INTEGRIN; CD69 ANTIGEN; KLF2 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; LECTIN; LEUKOCYTE ANTIGEN; S1PR1 PROTEIN, HUMAN; SPHINGOSINE 1 PHOSPHATE RECEPTOR; T LYMPHOCYTE ANTIGEN;

ADULT; AGED; CD8+ T LYMPHOCYTE; CHRONIC HEPATITIS B; CHRONIC HEPATITIS C; FEMALE; GENETICS; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LIVER; MALE; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PATHOLOGY; PHENOTYPE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEPATITIS B, CHRONIC; HEPATITIS C, CHRONIC; HUMANS; IMMUNOLOGIC MEMORY; INTEGRIN ALPHA CHAINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; LIVER; MALE; MIDDLE AGED; PHENOTYPE; RECEPTORS, LYSOSPHINGOLIPID;

EID: 85025586725     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-06352-3     Document Type: Article

References (45)

1. Knolle, P. A. & Thimme, R. Hepatic immune regulation and its involvement in viral hepatitis infection. Gastroenterology 146, 1193-1207 (2014).
2. Hamann, D. et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186, 1407-1418 (1997).
3. Sathaliyawala, T. et al. Distribution and Compartmentalization of Human Circulating and Tissue-Resident Memory T Cell Subsets. Immunity 38, 187-197 (2013).
4. Watanabe, R. et al. Human skin is protected by four functionally and phenotypically discrete populations of resident and recirculating memory T cells. Sci. Transl. Med. 7, 279ra39 (2015).
5. Park, C. O. & Kupper, T. S. The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat. Med. 21, 688-97 (2015).
6. Farber, D. L., Yudanin, N. A. & Restifo, N. P. Human memory T cells: generation, compartmentalization and homeostasis. Nat. Rev. Immunol. 14, 24-35 (2014).
7. Thome, J. J. C. et al. Spatial Map of Human T Cell Compartmentalization and Maintenance over Decades of Life. Cell 159, 814-828 (2014).
8. Morrot, A., Hafalla, J. C. R., Cockburn, I. A., Carvalho, L. H. & Zavala, F. IL-4 receptor expression on CD8+ T cells is required for the development of protective memory responses against liver stages of malaria parasites. J. Exp. Med. 202, 551-560 (2005).
9. Abrignani, S. Bystander activation by cytokines of intrahepatic T cells in chronic viral hepatitis. Semin. Liver Dis. 17, 319-22 (1997).
10. Stegmann, K. A. et al. CXCR6 marks a novel subset of T-bet lo Eomes hi natural killer cells residing in human liver. Sci. Rep. 6, 26157 (2016).
11. Skon, C. N. et al. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat. Immunol. 14, 1285-93 (2013).
12. Shiow, L. R. et al. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440, 540-544 (2006).
13. Mackay, L. K. et al. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science. 352, 459-63 (2016).
14. Heydtmann, M. et al. CXC chemokine ligand 16 promotes integrin-mediated adhesion of liver-infiltrating lymphocytes to cholangiocytes and hepatocytes within the inflamed human liver. J. Immunol. 174, 1055-1062 (2005).
15. + T cells specific for infectious pathogens. J. Infect. Dis. 210, 1508-1516 (2014).
16. Reantragoon, R. et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 210, 2305-2320 (2013).
17. Moran, A. E. et al. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J Exp Med 208, 1279-1289 (2011).
18. Appay, V., Van Lier, R. A. W., Sallusto, F. & Roederer, M. Phenotype and function of human T lymphocyte subsets: Consensus and issues. Cytom. Part A 73, 975-983 (2008).
19. Gupta, S. & Gollapudi, S. Effector Memory CD8+ T Cells Are Resistant to Apoptosis. Ann. N.Y. Acad. Sci. 1109, 145-150 (2007).
20. Smith, C. et al. Endogenous antigen presentation impacts on T-box transcription factor expression and functional maturation of CD8+ T cells. Blood 120, 3237-3245 (2012).
21. Vieira Braga, F. A. et al. Blimp-1 homolog Hobit identifies effector-type lymphocytes in humans. Eur. J. Immunol. 45, 2945-2958 (2015).
22. Mackay, L. K. et al. T-box Transcription Factors Combine with the Cytokines TGF-b and IL-15 to Control Tissue-Resident Memory T Cell Fate. Immunity 43, 1101-1111 (2015).
23. Steinert, E. M. et al. Quantifying Memory CD8 T Cells Reveals Regionalization of Immunosurveillance. Cell 161, 737-749 (2015).
24. Casey, K. A. et al. Antigen-Independent Differentiation and Maintenance of Effector-like Resident Memory T Cells in Tissues. J. Immunol. 188, 4866-4875 (2012).
25. Shimizu, Y. et al. Preferential accumulation of CD103+ T cells in human livers; its association with extrathymic T cells. J. Hepatol. 39, 918-924 (2003).
26. Ledgerwood, L. G. et al. The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat. Immunol. 9, 42-53 (2008).
27. Tse, S.-W., Cockburn, I. A., Zhang, H., Scott, A. L. & Zavala, F. Unique transcriptional profile of liver-resident memory CD8+ T cells induced by immunization with malaria sporozoites. Genes Immun. 14, 302-9 (2013).
28. Geissmann, F. et al. Intravascular immune surveillance by CXCR6 + NKT cells patrolling liver sinusoids. PLoS Biol. 3, e113 (2005).
29. Weninger, W., Crowley, M. A., Manjunath, N. & von Andrian, U. H. Migratory properties of naive, effector, and memory CD8(+) T cells. J. Exp. Med. 194, 953-966 (2001).
30. Mackay, C. R., Marston, W. L. & Dudler, L. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J. Exp. Med. 171, 801-17 (1990).
31. de Bree, G. J. et al. Selective accumulation of differentiated CD8+ T cells specific for respiratory viruses in the human lung. J. Exp. Med. 202, 1433-42 (2005).
32. Wakim, L. M. et al. The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J. Immunol. 189, 3462-71 (2012).
33. Crispe, I. N., Dao, T., Klugewitz, K., Mehal, W. Z. & Metz, D. P. The liver as a site of T-cell apoptosis: graveyard, or killing field? Immunol. Rev. 174, 47-62 (2000).
34. Schaerli, P. et al. A skin-selective homing mechanism for human immune surveillance T cells. J. Exp. Med. 199, 1265-1275 (2004).
35. Smolders, J. et al. Characteristics of differentiated CD8+ and CD4+ T cells present in the human brain. Acta Neuropathol. 126, 525-535 (2013).
36. + T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung. J. Clin. Invest. 121, 2254-63 (2011).
37. Kurioka, A., Walker, L. J., Klenerman, P. & Willberg, C. B. MAIT cells: new guardians of the liver. Clin. Transl. Immunol. 6, e132 (2017).
38. Maini, M. K. et al. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191, 1269-80 (2000).
39. Hersperger, A. R. et al. Increased HIV-specific CD8+ T-cell cytotoxic potential in HIV elite controllers is associated with T-bet expression. Blood 117, 3799-3809 (2011).
40. Intlekofer, A. M. et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6, 1236-1244 (2005).
41. Pearce, E. L. et al. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science. 302, 1041-1043 (2003).
42. van Gisbergen, K. P. J. M. et al. Mouse Hobit is a homolog of the transcriptional repressor Blimp-1 that regulates NKT cell effector differentiation. Nat. Immunol. 13, 864-871 (2012).
43. Hombrink, P. et al. Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells. Nat Immunol 17, 1467-1478 (2016).
44. van den Brand, M. et al. Sequential immunohistochemistry: A promising new tool for the pathology laboratory. Histopathology 65, 651-657 (2014).
45. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).