Tissue-Resident T Cells and Other Resident Leukocytes

Annual Review of Immunology

Volumn 37, Issue , 2019, Pages 521-546

  Masopust, David ^a   Soerens, Andrew G ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

immunity; lymphoid cells; memory; residence; T lymphocytes

Indexed keywords

CANCER CONTROL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; HOMEOSTASIS; HUMAN; IMMUNITY; LEUKOCYTE; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; LYMPHOID CELL; MACROPHAGE; MEMORY T LYMPHOCYTE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REVIEW; ANIMAL; ANTIBODY SPECIFICITY; B LYMPHOCYTE; CELL MOTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INNATE IMMUNITY; PHYSIOLOGY;

ANIMALS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; LEUKOCYTES; MACROPHAGES; ORGAN SPECIFICITY;

EID: 85065044573     PISSN: 07320582     EISSN: 15453278     Source Type: Book Series    
DOI: 10.1146/annurev-immunol-042617-053214     Document Type: Review

References (143)

1. Gowans JL, Knight EJ. 1964. The route of re-circulation of lymphocytes in the rat. Proc. R. Soc. Lond. B 159(975):257-82
2. Gowans JL. 1959. The recirculation of lymphocytes from blood to lymph in the rat. J. Physiol. 146(1):54-69
3. Bianconi E, Piovesan A, Facchin F, Beraudi A, Casadei R, et al. 2013. An estimation of the number of cells in the human body. Ann. Hum. Biol. 40(6):463-71
4. Cahill RN, Poskitt DC, Frost DC, Trnka Z. 1977. Two distinct pools of recirculating T lymphocytes: migratory characteristics of nodal and intestinal T lymphocytes. J. Exp. Med. 145(2):420-28
5. Mackay CR, Kimpton WG, Brandon MR, Cahill RN. 1988. Lymphocyte subsets show marked differences in their distribution between blood and the afferent and efferent lymph of peripheral lymph nodes. J. Exp. Med. 167(6):1755-65
6. Mackay CR, Marston WL, Dudler L. 1990. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J. Exp. Med. 171(3):801-17
7. Gallatin WM, Weissman IL, Butcher EC. 1983.A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304(5921):30-34
8. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I, et al. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99(1):23-33
9. Picker LJ, Michie SA, Rott LS, Butcher EC. 1990.A unique phenotype of skin-associated lymphocytes in humans: preferential expression of the HECA-452 epitope by benign andmalignant T cells at cutaneous sites. Am. J. Pathol. 136(5):1053-68
10. Fuhlbrigge RC, Kieffer JD, Armerding D, Kupper TS. 1997. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature 389(6654):978-81
11. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, et al. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424(6944):88-93
12. 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 74(1):185-95
13. Springer TA. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76(2):301-14
14. Kunkel EJ, Butcher EC. 2002. Chemokines and the tissue-specific migration of lymphocytes. Immunity 16(1):1-4
15. Butcher EC, Picker LJ. 1996. Lymphocyte homing and homeostasis. Science 272(5258):60-66
16. von Andrian UH, Mackay CR. 2000. T-cell function and migration: two sides of the same coin. N. Engl. J. Med. 343(14):1020-34
17. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401(6754):708-12
18. Kim SK, Schluns KS, Lefrancois L. 1999. Induction and visualization of mucosal memory CD8 T cells following systemic virus infection. J. Immunol. 163(8):4125-32
19. Reinhardt RL, Khoruts A, Merica R, Zell T, Jenkins MK. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature 410(6824):101-5
20. Masopust D. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291(5512):2413-17
21. + T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166(3):1813-22
22. + T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167(6):3293-99
23. Zeitz M, Greene WC, Peffer NJ, James SP. 1988. Lymphocytes isolated from the intestinal lamina propria of normal nonhuman primates have increased expression of genes associated with T-cell activation. Gastroenterology 94(3):647-55
24. Kim SK, Reed DS, Heath WR, Carbone F, Lefrancois L. 1997. Activation and migration of CD8 T cells in the intestinal mucosa. J. Immunol. 159(9):4295-4306
25. Bunting CH, Huston J. 1921. Fate of the lymphocyte. J. Exp. Med. 33(5):593-600
26. Masopust D, Jiang J, Shen H, Lefrancois L. 2001. Direct analysis of the dynamics of the intestinal mucosa CD8 T cell response to systemic virus infection. J. Immunol. 166(4):2348-56
27. 1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity 20(2):167-79
28. Teraki Y, Moriya N, Shiohara T. 1994. Drug-induced expression of intercellular adhesion molecule-1 on lesional keratinocytes in fixed drug eruption. Am. J. Pathol. 145(3):550-60
29. Boyman O, Hefti HP, Conrad C, Nickoloff BJ, Suter M, Nestle FO. 2004. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factoralpha. J. Exp. Med. 199(5):731-36
30. + T cells are resident in normal skin. J. Immunol. 176(7):4431-39
31. Masopust D, Vezys V, Usherwood EJ, Cauley LS, Olson S, et al. 2004. Activated primary and memory CD8Tcells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J. Immunol. 172(8):4875-82
32. Masopust D, Choo D, Vezys V, Wherry EJ, Duraiswamy J, et al. 2010. Dynamic T cell migration program provides resident memory within intestinal epithelium. J. Exp. Med. 207(3):553-64
33. Klonowski KD, Williams KJ, Marzo AL, Blair DA, Lingenheld EG, Lefrancois L. 2004. Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 20(5):551-62
34. + T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 18(5):593-603
35. Wakim LM, Waithman J, Van Rooijen N, Heath WR, Carbone FR. 2008. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319(5860):198-202
36. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. 2009. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10(5):524-30
37. Wakim LM, Woodward-Davis A, Bevan MJ. 2010. Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. PNAS 107(42):17872-79
38. + T cells. Nature 477(7363):216-19
39. + memory T cells exhibit combined cluster-mediated retention and equilibration with the circulation. Nat. Commun. 7:11514
40. Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrancois L, Farber DL. 2011. Cutting edge: Tissueretentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J. Immunol. 187(11):5510-14
41. RM cells providing global skin immunity. Nature 483(7388):227-31
42. + T cells enhance protection against Leishmania major infection. J. Exp. Med. 212(9):1405-14
43. Shin H, Iwasaki A. 2012. A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491(7424):463-67
44. Iijima N, Iwasaki A. 2014. A local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells. Science 346(6205):93-98
45. Steinert EM, Schenkel JM, Fraser KA, Beura LK, Manlove LS, et al. 2015. Quantifying memory CD8 T cells reveals regionalization of immunosurveillance. Cell 161(4):737-49
46. + T cells form a front-line defense against malaria liver-stage infection. Immunity 45(4):889-902
47. Stary G, Olive A, Radovic-Moreno AF, Gondek D, Alvarez D, et al. 2015. A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells. Science 348(6241):aaa8205-5
48. Shiow LR, Rosen DB, Brdičkova N, Xu Y, An J, et al. 2006. CD69 acts downstream of interferonalpha/ beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440(7083):540-44
49. Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, et al. 2016. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532(7600):512-16
50. Beura LK, Wijeyesinghe S, Thompson EA, Macchietto MG, Rosato PC, et al. 2018. T cells in nonlymphoid tissues give rise to lymph-node-resident memory T cells. Immunity 48(2):327-38.e5
51. Hofmann M, Pircher H. 2011. E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands. PNAS 108(40):16741-46
52. Finerty JC. 1952. Parabiosis in physiological studies. Physiol. Rev. 32(3):277-302
53. Tomura M, Yoshida N, Tanaka J, Karasawa S, Miwa Y, et al. 2008. Monitoring cellular movement in vivo with photoconvertible fluorescence protein "Kaede" transgenic mice. PNAS 105(31):10871-76
54. Ely KH, Cookenham T, Roberts AD, Woodland DL. 2006. Memory T cell populations in the lung airways are maintained by continual recruitment. J. Immunol. 176(1):537-43
55. Luettig B, Pape L, Bode U, Bell EB, Sparshott SM, et al. 1999. Naive and memory T lymphocytes migrate in comparable numbers through normal rat liver: Activated T cells accumulate in the periportal field. J. Immunol. 163(8):4300-7
56. Cose S, Brammer C, Khanna KM, Masopust D, Lefrancois L. 2006. Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur. J. Immunol. 36(6):1423-33
57. Harp JR, Onami TM. 2010. Naive T cells re-distribute to the lungs of selectin ligand deficient mice. PLOS ONE 5(6):e10973
58. Caucheteux SM, Torabi-Parizi P, Paul WE. 2013. Analysis of naive lung CD4 T cells provides evidence of functional lung to lymph node migration. PNAS 110(5):1821-26
59. + T cells within the liver. J. Immunol. 166(9):5430-38
60. + T cells into the interstitium of the normal lung. J. Clin. Investig. 115(12):3473-83
61. Anderson KG, Sung H, Skon CN, Lefrancois L, Deisinger A, et al. 2012. Cutting edge: Intravascular staining redefines lung CD8 T cell responses. J. Immunol. 189(6):2702-6
62. Anderson KG, Mayer-Barber K, Sung H, Beura L, James BR, et al. 2014. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat. Protoc. 9(1):209-22
63. Doerschuk CM, Beyers N, Coxson HO, Wiggs B, Hogg JC. 1993. Comparison of neutrophil and capillary diameters and their relation to neutrophil sequestration in the lung. J. Appl. Physiol. 74(6):3040-45
64. RM) are abundant in human lung: diversity, function, and antigen specificity. PLOS ONE 6(1):e16245
65. Gerner MY, Kastenmuller W, Ifrim I, Kabat J, Germain RN. 2012. Histo-cytometry: a method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes. Immunity 37(2):364-76
66. Li W, Germain RN, Gerner MY. 2017. Multiplex, quantitative cellular analysis in large tissue volumes with clearing-enhanced 3D microscopy (Ce3D). PNAS 114(35):E7321-30
67. McNamee EN, Korns Johnson D, Homann D, Clambey ET. 2013. Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function. Immunol. Res. 55(1-3):58-70
68. Buck MD, O'Sullivan D, Pearce EL. 2015. Tcellmetabolism drives immunity. J. Exp. Med. 212(9):1345-60
69. Pan Y, Tian T, Park CO, Lofftus SY, Mei S, et al. 2017. Survival of tissue-resident memory T cells requires exogenous lipid uptake and metabolism. Nature 543(7644):252-56
70. + T-cell activation mediated by cytokines. PNAS 109(25):9971-76
71. Mackay LK, Braun A, Macleod BL, Collins N, Tebartz C, et al. 2015. Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J. Immunol. 194(5):2059-63
72. + T cells. Nat. Immunol. 14(12):1285-93
73. + tissue-resident memory T cells of skin. Nat. Immunol. 14(12):1294-301
74. Wakim LM, Woodward-Davis A, Liu R, Hu Y, Villadangos J, et al. 2012. The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J. Immunol. 189(7):3462-71
75. 5 expression in NK cells promotes egress from lymph nodes and bone marrow. J. Exp. Med. 206(11):2469-81
76. Mackay LK, Wynne-Jones E, Freestone D, Pellicci DG, Mielke LA, et al. 2015. T-box transcription factors combine with the cytokines TGF-β and IL-15 to control tissue-resident memory T cell fate. Immunity 43(6):1101-11
77. Mackay LK, Minnich M, Kragten NAM, Liao Y, Nota B, et al. 2016. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352(6284):459-63
78. Li J, Olshansky M, Carbone FR, Ma JZ. 2016. Transcriptional analysis of T cells resident in human skin. PLOS ONE 11(1):e0148351
79. + lung-resident memory T cells. Nat. Immunol. 17(12):1467-78
80. Kumar BV, Ma W, Miron M, Granot T, Guyer RS, et al. 2017. Human tissue-resident memory T cells are defined by core transcriptional and functional signatures in lymphoid and mucosal sites. Cell Rep. 20(12):2921-34
81. Schenkel JM, Fraser KA, Casey KA, Beura LK, Pauken KE, et al. 2016. IL-15-independent maintenance of tissue-resident and boosted effector memory CD8 T cells. J. Immunol. 196(9):3920-26
82. Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, et al. 2012. Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J. Immunol. 188(10):4866-75
83. Zhang N, Bevan MJ. 2013. Transforming growth factor-βsignaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity 39(4):687-96
84. + T cells mediate local immunity. Eur. J. Immunol. 43(9):2295-304
85. Masopust D, Vezys V, Wherry EJ, Barber DL, Ahmed R. 2006. Cutting edge: gut microenvironment promotes differentiation of a unique memory CD8 T cell population. J. Immunol. 176(4):2079-83
86. Li H, Liu J, Carville A, Mansfield KG, Lynch D, Barouch DH. 2011. Durable mucosal simian immunodeficiency virus-specific effector memory T lymphocyte responses elicited by recombinant adenovirus vectors in rhesus monkeys. J. Virol. 85(21):11007-15
87. RM) cells in the absence of persisting local antigen presentation. PNAS 109(18):7037-42
88. Liang S, Mozdzanowska K, Palladino G, Gerhard W. 1994. Heterosubtypic immunity to influenza type A virus in mice: effector mechanisms and their longevity. J. Immunol. 152(4):1653-61
89. Slutter B, Van Braeckel-Budimir N, Abboud G, Varga SM, Salek-Ardakani S, Harty JT. 2017. Dynamics of influenza-induced lung-resident memory T cells underlie waning heterosubtypic immunity. Sci. Immunol. 2(7):eaag2031
90. + T cells at the site of tissue regeneration enable CD69-independent maintenance. J. Exp. Med. 213(13):3057-73
91. RM) are indispensable for optimal cross-protection against pulmonary virus infection. J. Leukoc. Biol. 95(2):215-24
92. + T cells and differential disease severity after experimental human infection. Nat. Commun. 6:10224.
93. + T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 195(1):135-41
94. Mikhak Z, Strassner JP, Luster AD. 2013. Lung dendritic cells imprint T cell lung homing and promote lung immunity through the chemokine receptor CCR4. J. Exp. Med. 210(9):1855-69
95. + Tlymphocytes to mucosal surfaces following intramuscular vaccination. J. Immunol. 181(6):4188-98
96. + T cells but not rested effectors to migrate to non-lymphoid sites in the absence of inflammation. J. Biol. Chem. 282(9):6106-15
97. + T cell trafficking after live viral immunization. Immunity 25(3):511-20
98. Wakim LM, Smith J, Caminschi I, Lahoud MH, Villadangos JA. 2015. Antibody-targeted vaccination to lung dendritic cells generates tissue-resident memory CD8 T cells that are highly protective against influenza virus infection. Mucosal Immunol. 8(5):1060-71
99. McMaster SR, Wein AN, Dunbar PR, Hayward SL, Cartwright EK, et al. 2018. Pulmonary antigen encounter regulates the establishment of tissue-resident CD8 memory T cells in the lung airways and parenchyma. Mucosal Immunol. 11(4):1071-78
100. + T cells with enhanced protective function. Immunity 40(5):747-57
101. + T cells. J. Exp. Med. 213(13):3075-86
102. + T cell formation during viral infection. J. Exp. Med. 213(6):951-66
103. Gerlach C, Moseman EA, Loughhead SM, Alvarez D, Zwijnenburg AJ, et al. 2016. The Chemokine receptor CX3CR1 defines three antigen-experienced CD8 T cell subsets with distinct roles in immune surveillance and homeostasis. Immunity 45(6):1270-84
104. Kinnear E, Lambert L, McDonald JU, Cheeseman HM, Caproni LJ, Tregoning JS. 2018. Airway T cells protect against RSV infection in the absence of antibody. Mucosal Immunol. 11(1):249-56
105. Smith NM, Wasserman GA, Coleman FT, Hilliard KL, Yamamoto K, et al. 2018. Regionally compartmentalized resident memory T cells mediate naturally acquired protection against pneumococcal pneumonia. Mucosal Immunol. 11(1):220-35
106. Hansen SG, Zak DE, Xu G, Ford JC, Marshall EE, et al. 2018. Prevention of tuberculosis in rhesus macaques by a cytomegalovirus-based vaccine. Nat. Med. 24(2):130-43
107. Conti HR, Peterson AC, Brane L, Huppler AR, Hernandez-Santos N, et al. 2014. Oral-resident natural Th17 cells and γδT cells control opportunistic Candida albicans infections. J. Exp. Med. 211(10):2075-84
108. + skinresident T cells in human herpes virus infection. Nature 497(7450):494-97
109. + T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J. Exp. Med. 204(3):595-603
110. + T cells continuously patrol skin epithelia to quickly recognize local antigen. PNAS 109(48):19739-44
111. + resident memory T cells shows tissue-autonomous recall responses that amplify secondary memory. Nat. Immunol. 19(2):173-82
112. McNamara HA, Cai Y, Wagle MV, Sontani Y, Roots CM. 2017. Up-regulation of LFA-1 allows liverresident memory T cells to patrol and remain in the hepatic sinusoids. Sci. Immunol. 2:eaaj1996
113. Miller MJ, Wei SH, Parker I, Cahalan MD. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296:1869-73
114. + T cells. Nat. Immunol. 14(5):509-13
115. Schenkel JM, Fraser KA, Beura LK, Pauken KE, Vezys V, Masopust D. 2014. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science 346(6205):98-101
116. + T cells trigger a state of tissue-wide pathogen alert. Science 346(6205):101-5
117. Tan H-X, Wheatley AK, Esterbauer R, Jegaskanda S, Glass JJ, et al. 2018. Induction of vaginal-resident HIV-specific CD8 T cells with mucosal prime-boost immunization. Mucosal Immunol. 11(3):994-1007
118. Park SL, Zaid A, Hor JL, Christo SN, Prier JE, et al. 2018. Local proliferation maintains a stable pool of tissue-resident memory T cells after antiviral recall responses. Nat. Immunol. 19(2):183-91
119. + tumor infiltrating lymphocytes predict a favorable prognosis in urothelial cell carcinoma of the bladder. J. Urol. 194(2):556-62
120. + tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J. Immunol. 194(7):3475-86
121. Boddupalli CS, Bar N, Kadaveru K, Krauthammer M, Pornputtapong N, et al. 2016. Interlesional diversity of T cell receptors in melanoma with immune checkpoints enriched in tissue-resident memory T cells. JCI Insight 1(21):e88955
122. Ganesan A-P, Clarke J, Wood O, Garrido-Martin EM, Chee SJ, et al. 2017. Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer. Nat. Immunol. 18(8):940-50
123. + tumor-infiltrating lymphocytes in pulmonary squamous cell carcinoma. Oncotarget 8(8):13762-69
124. Webb JR, Milne K, Watson P, Deleeuw RJ, Nelson BH. 2014. Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer. Clin. Cancer Res. 20(2):434-44
125. + cells by multiepitope imaging. Clin. Exp. Immunol. 112(1):21-26
126. + T cell responses to HLA-A2 restricted MAGE-A3 p271-279 peptide in hepatocellular carcinoma patients without vaccination. Cancer Immunol. Immunother. 56(12):1945-54
127. Nizard M, Roussel H, Tartour E. 2016. Resident memory T cells as surrogate markers of the efficacy of cancer vaccines. Clin. Cancer Res. 22(3):530-32
128. Malik BT, Byrne KT, Vella JL, Zhang P, Shabaneh TB, et al. 2017. Resident memory T cells in the skin mediate durable immunity to melanoma. Sci. Immunol. 2(10):eaam6346
129. + T cell residency in non-lymphoid tissues and tumours. Nature 552(7684):253-57
130. Hondowicz BD, An D, Schenkel JM, Kim KS, Steach HR, et al. 2016. Interleukin-2-dependent allergenspecific tissue-resident memory cells drive asthma. Immunity 44(1):155-66
131. Cheuk S, Wiken M, Blomqvist L, Nylen S, Talme T, et al. 2014. Epidermal Th22 and Tc17 cells form a localized disease memory in clinically healed psoriasis. J. Immunol. 192(7):3111-20
132. + T cells poised for cytotoxic function in human skin. Immunity 46(2):287-300
133. Kleinschek MA, Boniface K, Sadekova S, Grein J, Murphy EE, et al. 2009. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J. Exp. Med. 206(3):525-34
134. Sasaki K, Bean A, Shah S, Schutten E, Huseby PG, et al. 2014. Relapsing-remitting central nervous system autoimmunity mediated by GFAP-specific CD8 T cells. J. Immunol. 192(7):3029-42
135. Yednock TA, Rosen SD. 1989. Lymphocyte homing. Adv. Immunol. 44:313-78
136. Kotas ME, Locksley RM. 2018. Why innate lymphoid cells? Immunity 48(6):1081-90
137. Gasteiger G, Fan X, Dikiy S, Lee SY, Rudensky AY. 2015. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 350(6263):981-85
138. Huang Y, Mao K, Chen X, Sun M-A, Kawabe T, et al. 2018. S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense. Science 359(6371):114-19
139. Ginhoux F, Guilliams M. 2016. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44(3):439-49
140. McDonald BD, Jabri B, Bendelac A. 2018. Diverse developmental pathways of intestinal intraepithelial lymphocytes. Nat. Rev. Immunol. 18(8):514-25
141. Onodera T, Takahashi Y, Yokoi Y, Ato M, Kodama Y, et al. 2012. Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. PNAS 109(7):2485-90
142. Landsverk OJB, Snir O, Casado RB, Richter L, Mold JE, et al. 2017. Antibody-secreting plasma cells persist for decades in human intestine. J. Exp. Med. 214(2):309-17
143. Lim WA, June CH. 2017. The principles of engineering immune cells to treat cancer. Cell 168(4):724-40