Library Subscription: Guest
Critical Reviews™ in Immunology

Published 6 issues per year

ISSN Print: 1040-8401

ISSN Online: 2162-6472

The Impact Factor measures the average number of citations received in a particular year by papers published in the journal during the two preceding years. 2017 Journal Citation Reports (Clarivate Analytics, 2018) IF: 1.3 To calculate the five year Impact Factor, citations are counted in 2017 to the previous five years and divided by the source items published in the previous five years. 2017 Journal Citation Reports (Clarivate Analytics, 2018) 5-Year IF: 2.6 The Eigenfactor score, developed by Jevin West and Carl Bergstrom at the University of Washington, is a rating of the total importance of a scientific journal. Journals are rated according to the number of incoming citations, with citations from highly ranked journals weighted to make a larger contribution to the eigenfactor than those from poorly ranked journals. Eigenfactor: 0.00079 The Journal Citation Indicator (JCI) is a single measurement of the field-normalized citation impact of journals in the Web of Science Core Collection across disciplines. The key words here are that the metric is normalized and cross-disciplinary. JCI: 0.24 SJR: 0.429 SNIP: 0.287 CiteScore™:: 2.7 H-Index: 81

Indexed in

Tissue-Resident Memory T Cells: Sheltering-in-Place for Host Defense

Volume 40, Issue 5, 2020, pp. 423-440
DOI: 10.1615/CritRevImmunol.2020035522
Get accessGet access

ABSTRACT

A silent revolution has occurred in our understanding of how T cell-mediated immunity protects the host from recrudescent pathogens and how it fits into occurrences of autoimmunity and allergies. Under the new paradigm, the hitherto unknown noncirculatory, tissue-resident memory T cells (TRM ) constitute the host defense sentinels posted in diverse anatomic compartments and they are the key actors in protection against reinfections, tissue surveillance, cancer, and in many cases in autoimmunity and allergy in both animal models and humans. This contrasts with the previously held view that circulating memory T cells (TcircM) transitioning through the peripheral tissue are the main defenders against reinfections and are underlying agents in autoimmune reactions. TRM, elicited after primary pathogen encounter in a given tissue, are now known to be stably positioned in the respective barrier (skin, lungs, gut, female reproductive tract mucosa, liver, etc.) or nonbarrier (brain, kidneys, etc.) peripheral tissues. TRM represent a rapid, tissue-autonomous, first line of robust adaptive immune defense against recurring infections. Following a discussion on the defining characteristics of TRM, this review will focus on how TRM seeding and induction at the site of recurrent pathogen invasion is now, and must continue to be, the governing principle in new vaccine designs. The review will also elaborate on the role of TRM in relapsing and remitting autoimmunity by being prepositioned in the tissue as potent effectors. Many infectious disease vaccines targeted to establish and activate TRM at the infection site in animal models are robustly more effective at host protection relative to their traditional, parenterally administered counterparts that only activate systemic TcircM. Likewise, TRM-centered remedies are being successful in ameliorating T cell mediated autoimmunity in cases in which approaches based on circulatory T cells failed. Thus, the current and emerging TRM discoveries are piloting a new era of TRM-driven strategies focused on activation or inactivation of tissue-localized immunity in vaccines and therapies targeting infectious disease, cancer, autoimmunity, and allergies.

REFERENCES
  1. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;402(6763):34-8. .

  2. Masopust D, Soerens AG. Tissue-resident T cells and other resident leukocytes. Ann Rev Immunol. 2019;37(1):521-46. PubMed PMID: 30726153. .

  3. Mueller SN, Mackay LK. Tissue-resident memory T cells: Local specialists in immune defence. Nat Rev Immunol. 2016;16(2):79-89. .

  4. Szabo PA, Miron M, Farber DL. Location, location, location: Tissue resident memory T cells in mice and humans. Sci Immunol. 2019;4(34):eaas9673. .

  5. Sasson SC, Gordon CL, Christo SN, Klenerman P, Mackay LK. Local heroes or villains: Tissue-resident memory T cells in human health and disease. Cell Mol Immunol. 2020;17(2):113-22. .

  6. Clark RA. Resident memory T cells in human health and disease. Sci Transl Med. 2015;7(269):269rv1-rv1. .

  7. Mackay LK, Stock AT, Ma JZ, Jones CM, Kent SJ, Mueller SN, Heath WR, Carbone FR, Gebhardt T. Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci. 2012;109(18):7037-42. .

  8. Schenkel JM, Fraser KA, Beura LK, Pauken KE, Vezys V, Masopust D. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science. 2014;346(6205):98-101. .

  9. Clark RA, Watanabe R, Teague JE, Schlapbach C, Tawa MC, Adams N, Dorosario AA, Chaney KS, Cutler CS, LeBoeuf NR, Carter JB, Fisher DC, Kupper TS. Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients. Sci Transl Med. 2012;4(117):117ra7-ra7. .

  10. Jiang X, Clark RA, Liu L, Wagers AJ, Fuhlbrigge RC, Kupper TS. Skin infection generates non-migratory memory CD8+ TRM cells providing global skin immunity. Nature. 2012;483(7388):227-31. .

  11. Beura LK, Mitchell JS, Thompson EA, Schenkel JM, Mohammed J, Wijeyesinghe S, Fonseca R, Burbach BJ, Hickman HD, Vezys V, Fife BT, Masopust D. Intravital mucosal imaging of CD8(+) resident memory T cells shows tissue-autonomous recall responses that amplify secondary memory. Nat Immunol. 2018 Feb;19(2):173-82. PubMed PMID: 29311694. PMCID: PMC5896323. Epub 2018/01/10.eng. .

  12. Herndler-Brandstetter D, Ishigame H, Shinnakasu R, Plajer V, Stecher C, Zhao J, Lietzenmayer M, Kroehling L, Takumi A, Kometani K, Inoue T, Kluger Y, Kaech SM, Kurosaki T, Okada T, Flavell RA. KLRG1+ effector CD8+ T cells lose KLRG1, differentiate into all memory T cell lineages, and convey enhanced protective immunity. Immunity. 2018;48(4):716-29.e8. .

  13. Mackay LK, Wynne-Jones E, Freestone D, Pellicci Daniel G, Mielke LA, Newman DM, Braun A, Masson F, Kallies A, Belz Gabrielle T, Carbone FR. T-box transcription factors combine with the cytokines TGF-P and IL-15 to control tissue-resident memory T cell fate. Immunity. 2015;43(6):1101-11. .

  14. Zajac AJ, Harrington LE. Tissue-resident T cells lose their S1P1 exit visas. Cell Mol Immunol. 2014;11(3): 221-3. .

  15. Cheuk S, Schlums H, Gallais Serezal I, Martini E, Chiang SC, Marquardt N, Gibbs A, Detlofsson E, Introini A, Forkel M, Hoog C, Tjernlund A, Michaelsson J, Folkersen L, Mjosberg J, Blomqvist L, Ehrstrom M, Stahle M, Bryceson YT, Eidsmo L. CD49a expression defines tissue-resident CD8+ T cells poised for cytotoxic function in human skin. Immunity. 2017;46(2):287-300. .

  16. Watanabe R, Gehad A, Yang C, Scott LL, Teague JE, Schlapbach C, Elco CP, Huang V, Matos TR, Kupper TS, Clark RA. Human skin is protected by four functionally and phenotypically discrete populations of resident and recirculating memory T cells. Sci Transl Med. 2015;7(279):279ra39-ra39. .

  17. Behr FM, Chuwonpad A, Stark R, van Gisbergen KPJM. Armed and ready: Transcriptional regulation of tissue-resident memory CD8 T cells. Front Immunol. 2018;9(Jul):1770. .

  18. Mackay LK, Minnich M, Kragten NAM, Liao Y, Nota B, Seillet C, Zaid A, Man K, Preston S, Freestone D, Braun A, Wynne-Jones E, Behr FM, Stark R, Pellicci DG, Godfrey DI, Belz GT, Pellegrini M, Gebhardt T, Busslinger M, Shi W, Carbone FR, van Lier RAW, Kallies A, van Gisbergen KPJM. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science. 2016;352(6284):459-63. .

  19. Mackay LK, Rahimpour A, Ma JZ, Collins N, Stock AT, Hafon M-L, Vega-Ramos J, Lauzurica P, Mueller SN, Stefanovic T, Tscharke DC, Heath WR, Inouye M, Carbone FR, Gebhardt T. The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin. Nat Immunol. 2013;14(12):1294-301. .

  20. Skon CN, Lee J-Y, Anderson KG, Masopust D, Hogquist KA, Jameson SC. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol. 2013;14(12):1285-93. .

  21. Beura LK, Fares-Frederickson NJ, Steinert EM, Scott MC, Thompson EA, Fraser KA, Schenkel JM, Vezys V, Maso- pust D. CD4(+) resident memory T cells dominate immunosurveillance and orchestrate local recall responses. J Exp Med. 2019 May 6;216(5):1214-29. PubMed PMID: 30923043. PMCID: PMC6504216. Epub 2019/03/30.eng. .

  22. Oja AE, Piet B, Helbig C, Stark R, van der Zwan D, Blaauwgeers H, Remmerswaal EBM, Amsen D, Jonkers RE, Moerland PD, Nolte MA, van Lier RAW, Hombrink P. Trigger-happy resident memory CD4+ T cells inhabit the human lungs. Mucosal Immunol. 2018;11(3):654-67. .

  23. Pizzolla A, Nguyen THO, Sant S, Jaffar J, Loudovaris T, Mannering SI, Thomas PG, Westall GP, Kedzierska K, Wakim LM. Influenza-specific lung-resident memory T cells are proliferative and polyfunctional and maintain diverse TCR profiles. J Clin Invest. 2018; 128(2):721-33. .

  24. Steinbach K, Vincenti I, Kreutzfeldt M, Page N, Muschaweckh A, Wagner I, Drexler I, Pinschewer D, Korn T, Merkler D. Brain-resident memory T cells represent an autonomous cytotoxic barrier to viral infection. J Exper Med. 2016;213(8):1571-87. .

  25. Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefranjois L, Farber DL. Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol. 2011;187(11):5510-4. .

  26. Pizzolla A, Wakim LM. Memory T cell dynamics in the lung during influenza virus infection. J Immunol. 2019;202(2):374-81. .

  27. Perdomo C, Zedler U, Kuhl AA, Lozza L, Saikali P, Sander LE, Vogelzang A, Kaufmann SHE, Kupz A. Mucosal BCG vaccination induces protective lung-resident memory T cell populations against tuberculosis. mBio. 2016;7(6):e01686-16. .

  28. Wu T, Hu Y, Lee Y-T, Bouchard KR, Benechet A, Khanna K, Cauley LS. Lung-resident memory CD8 T cells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection. J Leukocyte Biol. 2014;95(2):215-24. .

  29. Fernandez-Ruiz D, Ng WY, Holz LE, Ma JZ, Zaid A, Wong YC, Lau LS, Mollard V, Cozijnsen A, Collins N, Li J, Davey GM, Kato Y, Devi S, Skandari R, Pauley M, Manton JH, Godfrey DI, Braun A, Tay SS, Tan PS, Bowen DG, Koch-Nolte F, Rissiek B, Carbone FR, Crabb BS, Lahoud M, Cockburn IA, Mueller SN, Bertolino P, McFadden GI, Caminschi I, Heath WR. Liver-resident memory CD8+ T cells form a front-line defense against malaria liver-stage infection. Immunity. 2016;45(4):889-902. .

  30. Zens KD, Chen JK, Farber DL. Vaccine-generated lung tissue-resident memory T cells provide hetero-subtypic protection to influenza infection. JCI Insight. 2016;1(10):e85832. PubMed PMID: 27468427.eng. .

  31. Bhushan M, Bleiker TO, Ballsdon AE, Allen MH, Sopwith M, Robinson MK, Clarke C, Weller RPJB, Graham-Brown RAC, Keefe M, Barker JNWN, Griffiths CEM. Anti-E-selectin is ineffective in the treatment of psoriasis: A randomized trial. Br J Dermatol. 2002;146(5):824-31. .

  32. Cheuk S, Wiken M, Blomqvist L, Nylen S, Talme T, Stahle M, Eidsmo L. Epidermal Th22 and Tc17 cells form a localized disease memory in clinically healed psoriasis. J Immunol. 2014;192(7):3111-20. .

  33. Richmond JM, Strassner JP, Zapata L, Garg M, Riding RL, Refat MA, Fan X, Azzolino V, Tovar-Garza A, Tsurushita N, Pandya AG, Tso JY, Harris JE. Antibody blockade of IL-15 signaling has the potential to durably reverse vitiligo. Sci Transl Med. 2018;10(450):eaam7710. .

  34. Fransen NL, Hsiao C-C, van der Poel M, Engelenburg HJ, Verdaasdonk K, Vincenten MCJ, Remmerswaal EBM, Kuhlmann T, Mason MRJ, Hamann J, Smolders J, Huitinga I. Tissue-resident memory T cells invade the brain parenchyma in multiple sclerosis white matter lesions. Brain. 2020;143(6):1714-30. .

  35. Smolders J, Heutinck KM, Fransen NL, Remmerswaal EBM, Hombrink P, ten Berge IJM, van Lier RAW, Huitinga I, Hamann J. Tissue-resident memory T cells populate the human brain. Nat Commun. 2018;9(1):4593. .

  36. Takamura S, Yagi H, Hakata Y, Motozono C, McMaster SR, Masumoto T, Fujisawa M, Chikaishi T, Komeda J, Itoh J, Umemura M, Kyusai A, Tomura M, Nakayama T, Woodland DL, Kohlmeier JE, Miyazawa M. Specific niches for lung-resident memory CD8+ T cells at the site of tissue regeneration enable CD69-independent maintenance. J Exper Med. 2016;213(13):3057-73. .

  37. Slutter B, Van Braeckel-Budimir N, Abboud G, Varga SM, Salek-Ardakani S, Harty JT. Dynamics of influenza-induced lung-resident memory T cells underlie waning heterosubtypic immunity. Sci Immunol. 2017 Jan 6;2(7). PubMed PMID: 28783666. PMCID: PMC5590757. Epub 2017/08/08.eng. .

  38. Hayward SL, Scharer CD, Cartwright EK, Takamura S, Li Z-RT, Boss JM, Kohlmeier JE. Environmental cues regulate epigenetic reprogramming of airway-resident memory CD8(+) T cells. Nat Immunol. 2020;21(3):309-20. PubMed PMID: 31953534. Epub 2020/01/17.eng. .

  39. Clemens EB, Van de Sandt C, Wong SS, Wakim LM, Valkenburg SA. Harnessing the power of T cells: The promising hope for a universal influenza vaccine. Vaccines. 2018;6(2):18. PubMed PMID: doi:10.3390/ vaccines6020018. .

  40. Purwar R, Campbell J, Murphy G, Richards WG, Clark RA, Kupper TS. Resident memory T Cells (TRM) are abundant in human lung: Diversity, function, and antigen specificity. PLoS One. 2011;6(1):e16245. .

  41. Hombrink P, Helbig C, Backer RA, Piet B, Oja AE, Stark R, Brasser G, Jongejan A, Jonkers RE, Nota B, Basak O, Clevers HC, Moerland PD, Amsen D, van Lier RAW. Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells. Nat Immunol. 2016;17(12):1467-78. .

  42. Snyder ME, Farber DL. Human lung tissue resident memory T cells in health and disease. Curr Opin Immunol. 2019;59:101-8. .

  43. Jozwik A, Habibi MS, Paras A, Zhu J, Guvenel A, Dhariwal J, Almond M, Wong EHC, Sykes A, Maybeno M, Del Rosario J, Trujillo-Torralbo M-B, Mallia P, Sidney J, Peters B, Kon OM, Sette A, Johnston SL, Openshaw PJ, Chiu C. RSV-specific airway resident memory CD8+ T cells and differential disease severity after experimental human infection. Nat Commun. 2015;6(1):10224. .

  44. Pizzolla A, Nguyen THO, Smith JM, Brooks AG, Kedzierska K, Heath WR, Reading PC, Wakim LM. Resident memory CD8+ T cells in the upper respiratory tract prevent pulmonary influenza virus infection. Sci Immunol. 2017;2(12):eaam6970. .

  45. Hassan AO, Kafai NM, Dmitriev IP, Fox JM, Smith BK, Harvey IB, Chen RE, Winkler ES, Wessel AW, Case JB, Kashentseva E, McCune TB, Bailey AL, Zhao H, Van-Blargan LA, Dai Y, Ma M, Adams LJ, Shrihari S, Danis JE, Gralinski LE, Hou YJ, Schafer A, Kim AS, Keeler SP, Weiskopf D, Baric RS, Holtzman MJ, Fremont DH, Curiel DT, Diamond, MS. A single-dose intranasal ChAd vaccine protects upper and lower respiratory tracts against SARS-CoV-2. Cell. 2020;183(1):169-84.e13. .

  46. Koutsakos M, Illing PT, Nguyen THO, Mifsud NA, Crawford JC, Rizzetto S, Eltahla AA, Clemens EB, Sant S, Chua BY, Wong CY, Allen EK, Teng D, Dash P, Boyd DF, Grzelak L, Zeng W, Hurt AC, Barr I, Rockman S, Jackson DC, Kotsimbos TC, Cheng AC, Richards M, Westall GP, Loudovaris T, Mannering SI, Elliott M, Tangye SG, Wakim LM, Rossjohn J, Vijaykrishna D, Luciani F, Thomas PG, Gras S, Purcell AW, Kedzierska K. Human CD8+ T cell cross-reactivity across influenza A, B and C viruses. Nat Immunol. 2019;20(5):613-25. .

  47. Deliyannis G, Kedzierska K, Lau YF, Zeng W, Turner SJ, Jackson DC, Brown LE. Intranasal lipopeptide primes lung-resident memory CD8+ T cells for long-term pulmonary protection against influenza. Eur J Immunol. 2006;36(3):770-8. .

  48. Gasper DJ, Neldner B, Plisch EH, Rustom H, Carrow E, Imai H, Kawaoka Y, Suresh M. Effective respiratory CD8 t-cell immunity to influenza virus induced by intranasal carbomer-lecithin-adjuvanted non-replicating vaccines. Plos Pathogens. 2016;12(12):e1006064. .

  49. Gilchuk P, Hill TM, Guy C, McMaster SR, Boyd KL, Rabacal WA, Lu P, Shyr Y, Kohlmeier JE, Sebzda E, Green DR, Joyce S. A distinct lung-interstitium-resident memory CD8+ T cell subset confers enhanced protection to lower respiratory tract infection. Cell Rep. 2016;16(7): 1800-9. .

  50. Wakim LM, Smith J, Caminschi I, Lahoud MH, Villadangos JA. Antibody-targeted vaccination to lung dendritic cells generates tissue-resident memory CD8 T cells that are highly protective against influenza virus infection. Mucosal Immunol. 2015;8(5):1060-71. .

  51. Haddadi S, Vaseghi-Shanjani M, Yao Y, Afkhami S, D'Agostino MR, Zganiacz A, Jeyanathan M, Xing Z. Mucosal-pull induction of lung-resident memory CD8 T cells in parenteral TB vaccine-primed hosts requires cognate antigens and CD4 T cells. Front Immunol. 2019;10(Sep):2075. .

  52. Florido M, Muflihah H, Lin LCW, Xia Y, Sierro F, Palendira M, Feng CG, Bertolino P, Stambas J, Triccas JA, Britton WJ. Pulmonary immunization with a recombinant influenza A virus vaccine induces lung-resident CD4+ memory T cells that are associated with protection against tuberculosis. Mucosal Immunol. 2018;11(6):1743-52. .

  53. Bull NC, Stylianou E, Kaveh DA, Pinpathomrat N, Pasricha J, Harrington-Kandt R, Garcia-Pelayo MC, Hogarth PJ, McShane H. Enhanced protection conferred by mucosal BCG vaccination associates with presence of antigen-specific lung tissue-resident PD-1+ KLRG1-CD4+ T cells. Mucosal Immunol. 2019;12(2):555-64. .

  54. Jeyanathan M, Yao Y, Afkhami S, Smaill F, Xing Z. New tuberculosis vaccine strategies: Taking aim at unnatural immunity. Trends Immunol. 2018;39(5):419-33. .

  55. Ogongo P, Porterfield JZ, Leslie A. Lung tissue resident memory T-cells in the immune response to Mycobacterium tuberculosis. Front Immunol. 2019;10:992. PubMed PMID: 31130965.eng. .

  56. Darrah PA, Zeppa JJ, Maiello P, Hackney JA, Wadsworth MH, Hughes TK, Pokkali S, Swanson PA, Grant NL, Rodgers MA, Kamath M, Causgrove CM, Laddy DJ, Bonavia A, Casimiro D, Lin PL, Klein E, White AG, Scanga CA, Shalek AK, Roederer M, Flynn JL, Seder RA. Prevention of tuberculosis in macaques after intravenous BCG immunization. Nature. 2020;577(7788):95-102. .

  57. Barclay WR, Anacker RL, Brehmer W, Leif W, Ribi E. Aerosol-induced tuberculosis in subhuman primates and the course of the disease after intravenous BCG vaccination. Infect Immun. 1970;2(5):574-82. .

  58. Yang Q, Zhang M, Chen Q, Chen W, Wei C, Qiao K, Ye T, Deng G, Li J, Zhu J, Cai Y, Chen X, Ma L. Cutting edge: Characterization of human tissue-resident memory T cells at different infection sites in patients with tuberculosis. J Immunol. 2020;204(9):2331-6. .

  59. Valencia-Hernandez AM, Ng WY, Ghazanfari N, Ghilas S, de Menezes MN, Holz LE, Huang C, English K, Naung M, Tan PS, Tullett KM, Steiner TM, Enders MH, Beattie L, Chua YC, Jones CM, Cozijnsen A, Mollard V, Cai Y, Bowen DG, Purcell AW, La Grata NL, Villadangos JA, de Koning-Ward T, Barry AE, Barchet W, Cockburn IA, McFadden GI, Gras S, Lahoud MH, Bertolino P, Schit- tenhelm RB, Caminschi I, Heath WR, Fernandez-Ruiz D. A natural peptide antigen within the plasmodium ribosomal protein RPL6 confers liver TRM cell-mediated immunity against malaria in mice. Cell Host Microbe. 2020;27(6):950-62e7. .

  60. Kamala T, Nanda NK. Protective response to Leishmania major in BALB/c mice requires antigen processing in the absence of DM. J Immunol. 2009;182(8):4882-90. PubMed PMID: 19342667.eng. .

  61. Pagan AJ, Peters NC, Debrabant A, Ribeiro-Gomes F, Pepper M, Karp CL, Jenkins MK, Sacks DL. Tracking antigen-specific CD4+ T cells throughout the course of chronic Leishmania major infection in resistant mice. Eur J Immunol. 2013 Feb;43(2):427-38. PubMed PMID: 23109292. PMCID: PMC4086308. Epub 2012/10/31.eng. .

  62. Glennie ND, Volk SW, Scott P. Skin-resident CD4+ T cells protect against Leishmania major by recruiting and activating inflammatory monocytes. PLoS Pathogens. 2017;13(4):e1006349. .

  63. Nanda NK, Inbar I. Tissue resident memory T cells in a mouse model of cutaneous Leishmaniasis. 2020. In preparation. .

  64. Boniface K, Jacquemin C, Darrigade A-S, Dessarthe B, Martins C, Boukhedouni N, Vernisse C, Grasseau A, Thiolat D, Rambert J, Lucchese F, Bertolotti A, Ezzedine K, Taieb A, Seneschal J. Vitiligo skin is imprinted with resident memory CD8 T cells expressing CXCR3. J Invest Dermatol. 2018;138(2):355-64. .

  65. Hueber W, Patel DD, Dryja T, Wright AM, Koroleva I, Bruin G, Antoni C, Draelos Z, Gold MH, Durez P, Tak PP, Gomez-Reino JJ, Foster CS, Kim RY, Samson CM, Falk NS, Chu DS, Callanan D, Nguyen QD, Rose K, Haider A, Di Padova F. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med. 2010;2(52):52ra72. .

  66. Harris JE, Harris TH, Weninger W, Wherry EJ, Hunter CA, Turka LA. A mouse model of vitiligo with focused epidermal depigmentation requires IFN-y for autoreactive CD8+ T-cell accumulation in the skin. J Invest Dermatol. 2012;132(7):1869-76. .

  67. van den Boorn JG, Konijnenberg D, Dellemijn TA, van der Veen JP, Bos JD, Melief CJ, Vyth-Dreese FA, Luiten RM. Autoimmune destruction of skin melanocytes by perilesional T cells from vitiligo patients. J Invest Dermatol. 2009 Sep;129(9):2220-32. PubMed PMID: 19242513. Epub 2009/02/27.eng. .

  68. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol. 2009;10(5):524-30. .

  69. Zhang N, Bevan MJ. Transforming growth factor-P signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity. 2013;39(4):687-96. .

  70. Meresse B, Chen Z, Ciszewski C, Tretiakova M, Bhagat G, Krausz TN, Raulet DH, Lanier LL, Groh V, Spies T, Ebert EC, Green PH, Jabri B. Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway cnverts CTL into lymphokine-activated killer cells in celiac disease. Immunity. 2004;21(3):357-66. .

  71. Sakkas LI, Zafiriou E, Bogdanos DP. Mini Review: New treatments in psoriatic arthritis. Focus on the IL-23/17 axis. Front Pharmacol. 2019;10(Aug):872. .

  72. Machado-Santos J, Saji E, Troscher AR, Paunovic M, Liblau R, Gabriely G, Bien CG, Bauer J, Lassmann H. The compartmentalized inflammatory response in the multiple sclerosis brain is composed of tissue-resident CD8+ T lymphocytes and B cells. Brain. 2018;141(7):2066-82. .

  73. Segal BM. The diversity of encephalitogenic CD4+ T cells in multiple sclerosis and its animal models. J Clin Med. 2019;8(1):120. PubMed PMID: doi:10.3390/jcm8010120. .

  74. Bird L. MS signature TH cell subset. Nat Rev Immunol. 2019;19(9):536-7. .

  75. Hohlfeld R, Dornmair K, Meinl E, Wekerle H. The search for the target antigens of multiple sclerosis, part 1 : Auto-reactive CD4+ T lymphocytes as pathogenic effectors and therapeutic targets. Lancet Neurol. 2016;15(2):198-209. .

  76. Cao Y, Goods BA, Raddassi K, Nepom GT, Kwok WW, Love JC, Hafler DA. Functional inflammatory profiles distinguish myelin-reactive T cells from patients with multiple sclerosis. Sci Transl Med. 2015;7(287):287ra74. .

  77. Smolders J, Fransen NL, Hsiao CC, Hamann J, Huitinga I. Perivascular tissue resident memory T cells as therapeutic target in multiple sclerosis. Expert Rev Neurother. 2020 Aug;20(8):835-48. doi: 10.1080/14737175.2020.1776609. Epub 2020 Jun 30. PMID: 32476499. .

  78. van Nierop GP, van Luijn MM, Michels SS, Melief MJ, Janssen M, Langerak AW, Ouwendijk WJD, Hintzen RQ, Verjans GMGM. Phenotypic and functional characterization of T cells in white matter lesions of multiple sclerosis patients. Acta Neuropathol. 2017 Sep;134(3):383-401. doi: 10.1007/s00401-017-1744-4. Epub 2017 Jun 17. PMID: 28624961; PMCID: PMC5563341. .

  79. Wakim LM, Woodward-Davis A, Liu R, Hu Y, Villadan- gos J, Smyth G, Bevan MJ. The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J Immunol. 2012;189(7):3462-71. .

  80. Shwetank, Frost EL, Mockus TE, Ren HM, Toprak M, Lauver MD, Netherby-Winslow CS, Jin G, Cosby JM, Evavold BD, Lukacher AE. PD-1 dynamically regulates inflammation and development of brain-resident memory CD8 T cells during persistent viral encephalitis. Front Im-munol. 2019;10(Apr):783. .

  81. Schaller AS, Fonnes M, Nazerai L, Christensen JP, Thomsen AR. Local antigen encounter is essential for establishing persistent CD8+ T-cell memory in the CNS. Front Immunol. 2019;10(Mar):351. .

  82. Haile Y, Simmen KC, Pasichnyk D, Touret N, Simmen T, Lu J-Q, Bleackley RC, Giuliani F. Granule-derived Granzyme B Mediates the vulnerability of human neurons to T cell-induced neurotoxicity. J Immunol. 2011;187(9):4861-72. .

  83. Giuliani F, Goodyer CG, Antel JP, Yong VW. Vulnerability of human neurons to T cell-mediated cytotoxicity. J Immunol. 2003;171(1):368-79. .

  84. Duraes J, Coutinho I, Mariano A, Geraldo A, Macario MC. Demyelinating disease of the central nervous system associated with Pembrolizumab treatment for metastatic melanoma. Mult Scler. 2019 Jun;25(7):1005-8. doi: 10.1177/1352458518803724. Epub 2018 Oct 12. PMID: 30311534. .

  85. Weisberg SP, Carpenter DJ, Chait M, Dogra P, Gartrell-Corrado RD, Chen AX, Campbell S, Liu W, Saraf P, Snyder ME, Kubota M, Danzl NM, Schrope BA, Rabadan R, Saenger Y, Chen X, Farber DL. Tissue-resident memory T cells mediate immune homeostasis in the human pancreas through the PD-1/PD-L1 pathway. Cell Rep. 2019 Dec 17;29(12):3916-32.e5. doi: 10.1016/j.celrep.2019.11.056. PMID: 31851923; PMCID: PMC6939378. .

  86. Ho AW, Kupper TS. T cells and the skin: From protective immunity to inflammatory skin disorders. Nat Rev Immunol. 2019;19(8):490-502. .

CITED BY
  1. Betjes Michiel G. H., Uremia-Associated Immunological Aging and Severity of COVID-19 Infection, Frontiers in Medicine, 8, 2021. Crossref

Forthcoming Articles

Identification of key chondrocyte apoptosis-related genes in osteoarthritis based on weighted gene co-expression network analysis and experimental verification Wei Wang, Junyi Hong, Tianyi Cao, Fusheng Ye, Junwei Gao, Shumei Qin Anoikis and Mitophagy-Related Gene Signature for Predicting the Survival and Tumor Cell Progression in Colon Cancer Jian Shen, Minzhe Li Exploring the mechanism of Isoforskolin against asthma based on network pharmacology and experimental verification Yan Fang, Shibo Sun, Chuang Xiao, Min Li, Yuanyuan Zheng, Anju Zu, Zhuang Luo Identification of a novel five-gene prognostic model for laryngeal cancer associated with mitophagy using integrated bioinformatics analysis and experimental verification Dong Song, Lun Dong, Mei Wang, Xiaoping Gao Function of steroid receptor coactivators (SRCs) in T cells and cancers: Implications for cancer immunotherapy Wencan Zhang, Xu Cao, Hongmin Wu, Xiancai Zhong, Yun Shi, Zuoming Sun Electroacupuncture Alleviates Ischemic Stroke by Activating the mTOR/SREBP1 Pathway Jiawang Lang, Jianchang Luo, Luodan Wang, Wenbin Xu, Jie Jia, Zhipeng Zhao, Boxu Lang KIAA1429 induces the m6A modification of LINC01106 to enhance the malignancy of lung adenocarcinoma cell via JAK/STAT3 pathway Di Xu, Ziming Wang, Fajiu Li Effects of different doses of dexmedetomidine on the prevention of postoperative sleep disturbance and serum neurotransmitter level in patients under general anesthesia Huifei Lu, Fei He, Ying Huang, Zhongliang Wei
Begell Digital Portal Begell Digital Library eBooks Journals References & Proceedings Research Collections Prices and Subscription Policies Begell House Contact Us Language English 中文 Русский Português German French Spain