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Published in: Seminars in Immunopathology 6/2022

Open Access 11-04-2022 | Kidney Cancer | Review

Tissue-resident memory T cells in the kidney

Authors: Nariaki Asada, Pauline Ginsberg, Nicola Gagliani, Hans-Willi Mittrücker, Ulf Panzer

Published in: Seminars in Immunopathology | Issue 6/2022

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Abstract

The identification of tissue-resident memory T cells (TRM cells) has significantly improved our understanding of immunity. In the last decade, studies have demonstrated that TRM cells are induced after an acute T-cell response, remain in peripheral organs for several years, and contribute to both an efficient host defense and autoimmune disease. TRM cells are found in the kidneys of healthy individuals and patients with various kidney diseases. A better understanding of these cells and their therapeutic targeting might provide new treatment options for infections, autoimmune diseases, graft rejection, and cancer. In this review, we address the definition, phenotype, and developmental mechanisms of TRM cells. Then, we further discuss the current understanding of TRM cells in kidney diseases, such as infection, autoimmune disease, cancer, and graft rejection after transplantation.
Literature
2.
go back to reference Netea MG, Domínguez-Andrés J, Barreiro LB, Chavakis T, Divangahi M, Fuchs E, Joosten LAB, van der Meer JWM, Mhlanga MM, Mulder WJM, Riksen NP, Schlitzer A, Schultze JL, Stabell Benn C, Sun JC, Xavier RJ, Latz E (2020) Defining trained immunity and its role in health and disease. Nat Rev Immunol 20:375–388PubMedPubMedCentralCrossRef Netea MG, Domínguez-Andrés J, Barreiro LB, Chavakis T, Divangahi M, Fuchs E, Joosten LAB, van der Meer JWM, Mhlanga MM, Mulder WJM, Riksen NP, Schlitzer A, Schultze JL, Stabell Benn C, Sun JC, Xavier RJ, Latz E (2020) Defining trained immunity and its role in health and disease. Nat Rev Immunol 20:375–388PubMedPubMedCentralCrossRef
3.
go back to reference Sallusto F, Geginat J, Lanzavecchia A (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22:745–763PubMedCrossRef Sallusto F, Geginat J, Lanzavecchia A (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22:745–763PubMedCrossRef
5.
go back to reference Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708–712PubMedCrossRef Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708–712PubMedCrossRef
7.
go back to reference 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 10:524–530PubMedCrossRef 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 10:524–530PubMedCrossRef
8.
go back to reference Masopust D, Choo D, Vezys V, Wherry EJ, Duraiswamy J, Akondy R, Wang J, Casey KA, Barber DL, Kawamura KS, Fraser KA, Webby RJ, Brinkmann V, Butcher EC, Newell KA, Ahmed R (2010) Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med 207:553–564PubMedPubMedCentralCrossRef Masopust D, Choo D, Vezys V, Wherry EJ, Duraiswamy J, Akondy R, Wang J, Casey KA, Barber DL, Kawamura KS, Fraser KA, Webby RJ, Brinkmann V, Butcher EC, Newell KA, Ahmed R (2010) Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med 207:553–564PubMedPubMedCentralCrossRef
9.
go back to reference Anderson KG, Mayer-Barber K, Sung H, Beura L, James BR, Taylor JJ, Qunaj L, Griffith TS, Vezys V, Barber DL, Masopust D (2014) Intravascular staining for discrimination of vascular and tissue leukocytes. Nat Protoc 9:209–222PubMedPubMedCentralCrossRef Anderson KG, Mayer-Barber K, Sung H, Beura L, James BR, Taylor JJ, Qunaj L, Griffith TS, Vezys V, Barber DL, Masopust D (2014) Intravascular staining for discrimination of vascular and tissue leukocytes. Nat Protoc 9:209–222PubMedPubMedCentralCrossRef
10.
go back to reference Steinert EM, Schenkel JM, Fraser KA, Beura LK, Manlove LS, Igyártó BZ, Southern PJ, Masopust D (2015) Quantifying Memory CD8 T Cells Reveals Regionalization of Immunosurveillance. Cell 161:737–749PubMedPubMedCentralCrossRef Steinert EM, Schenkel JM, Fraser KA, Beura LK, Manlove LS, Igyártó BZ, Southern PJ, Masopust D (2015) Quantifying Memory CD8 T Cells Reveals Regionalization of Immunosurveillance. Cell 161:737–749PubMedPubMedCentralCrossRef
11.
go back to reference Dornieden T, Sattler A, Pascual Reguant A, Ruhm A, Thiel L, Bergmann Y, Thole L, Kohler R, Kuhl A, Hauser A, Boral S, Friedersdorff F, Kotsch K. 2021. Signatures and Specificity of Tissue-resident Lymphocytes Identified in Human Renal Peri-tumor and Tumor Tissue. J Am Soc Nephrol Dornieden T, Sattler A, Pascual Reguant A, Ruhm A, Thiel L, Bergmann Y, Thole L, Kohler R, Kuhl A, Hauser A, Boral S, Friedersdorff F, Kotsch K. 2021. Signatures and Specificity of Tissue-resident Lymphocytes Identified in Human Renal Peri-tumor and Tumor Tissue. J Am Soc Nephrol
12.
go back to reference de Leur K, Dieterich M, Hesselink DA, Corneth OBJ, Dor F, de Graav GN, Peeters AMA, Mulder A, Kimenai H, Claas FHJ, Clahsen-van Groningen MC, van der Laan LJW, Hendriks RW, Baan CC (2019) Characterization of donor and recipient CD8+ tissue-resident memory T cells in transplant nephrectomies. Sci Rep 9:5984PubMedPubMedCentralCrossRef de Leur K, Dieterich M, Hesselink DA, Corneth OBJ, Dor F, de Graav GN, Peeters AMA, Mulder A, Kimenai H, Claas FHJ, Clahsen-van Groningen MC, van der Laan LJW, Hendriks RW, Baan CC (2019) Characterization of donor and recipient CD8+ tissue-resident memory T cells in transplant nephrectomies. Sci Rep 9:5984PubMedPubMedCentralCrossRef
13.
go back to reference Bartolomé-Casado R, Landsverk OJB, Chauhan SK, Richter L, Phung D, Greiff V, Risnes LF, Yao Y, Neumann RS, Yaqub S, Øyen O, Horneland R, Aandahl EM, Paulsen V, Sollid LM, Qiao SW, Baekkevold ES, Jahnsen FL (2019) Resident memory CD8 T cells persist for years in human small intestine. J Exp Med 216:2412–2426PubMedPubMedCentralCrossRef Bartolomé-Casado R, Landsverk OJB, Chauhan SK, Richter L, Phung D, Greiff V, Risnes LF, Yao Y, Neumann RS, Yaqub S, Øyen O, Horneland R, Aandahl EM, Paulsen V, Sollid LM, Qiao SW, Baekkevold ES, Jahnsen FL (2019) Resident memory CD8 T cells persist for years in human small intestine. J Exp Med 216:2412–2426PubMedPubMedCentralCrossRef
14.
go back to reference Snyder ME, Finlayson MO, Connors TJ, Dogra P, Senda T, Bush E, Carpenter D, Marboe C, Benvenuto L, Shah L, Robbins H, Hook JL, Sykes M, D'Ovidio F, Bacchetta M, Sonett JR, Lederer DJ, Arcasoy S, Sims PA, Farber DL. 2019. Generation and persistence of human tissue-resident memory T cells in lung transplantation. Sci Immunol 4 Snyder ME, Finlayson MO, Connors TJ, Dogra P, Senda T, Bush E, Carpenter D, Marboe C, Benvenuto L, Shah L, Robbins H, Hook JL, Sykes M, D'Ovidio F, Bacchetta M, Sonett JR, Lederer DJ, Arcasoy S, Sims PA, Farber DL. 2019. Generation and persistence of human tissue-resident memory T cells in lung transplantation. Sci Immunol 4
15.
go back to reference Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, Casey KA, Thompson EA, Fraser KA, Rosato PC, Filali-Mouhim A, Sekaly RP, Jenkins MK, Vezys V, Haining WN, Jameson SC, Masopust D (2016) Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532:512–516PubMedPubMedCentralCrossRef Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, Casey KA, Thompson EA, Fraser KA, Rosato PC, Filali-Mouhim A, Sekaly RP, Jenkins MK, Vezys V, Haining WN, Jameson SC, Masopust D (2016) Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532:512–516PubMedPubMedCentralCrossRef
16.
go back to reference Turner JE, Becker M, Mittrucker HW, Panzer U (2018) Tissue-Resident Lymphocytes in the Kidney. J Am Soc Nephrol 29:389–399PubMedCrossRef Turner JE, Becker M, Mittrucker HW, Panzer U (2018) Tissue-Resident Lymphocytes in the Kidney. J Am Soc Nephrol 29:389–399PubMedCrossRef
17.
go back to reference van der Putten C, Remmerswaal EBM, Terpstra ML, van der Bom ND, Kers J, Ten Berge IJM, Geerlings SE, van Lier RAW, Bemelman FJ, van Aalderen MC. 2021. CD8 and CD4 T Cell Populations in Human Kidneys. Cells 10 van der Putten C, Remmerswaal EBM, Terpstra ML, van der Bom ND, Kers J, Ten Berge IJM, Geerlings SE, van Lier RAW, Bemelman FJ, van Aalderen MC. 2021. CD8 and CD4 T Cell Populations in Human Kidneys. Cells 10
18.
go back to reference Krebs CF, Reimers D, Zhao Y, Paust HJ, Bartsch P, Nunez S, Rosemblatt MV, Hellmig M, Kilian C, Borchers A, Enk LUB, Zinke M, Becker M, Schmid J, Klinge S, Wong MN, Puelles VG, Schmidt C, Bertram T, Stumpf N, Hoxha E, Meyer-Schwesinger C, Lindenmeyer MT, Cohen CD, Rink M, Kurts C, Franzenburg S, Koch-Nolte F, Turner JE, Riedel JH, Huber S, Gagliani N, Huber TB, Wiech T, Rohde H, Bono MR, Bonn S, Panzer U, Mittrucker HW. 2020. Pathogen-induced tissue-resident memory TH17 (TRM17) cells amplify autoimmune kidney disease. Sci Immunol 5 Krebs CF, Reimers D, Zhao Y, Paust HJ, Bartsch P, Nunez S, Rosemblatt MV, Hellmig M, Kilian C, Borchers A, Enk LUB, Zinke M, Becker M, Schmid J, Klinge S, Wong MN, Puelles VG, Schmidt C, Bertram T, Stumpf N, Hoxha E, Meyer-Schwesinger C, Lindenmeyer MT, Cohen CD, Rink M, Kurts C, Franzenburg S, Koch-Nolte F, Turner JE, Riedel JH, Huber S, Gagliani N, Huber TB, Wiech T, Rohde H, Bono MR, Bonn S, Panzer U, Mittrucker HW. 2020. Pathogen-induced tissue-resident memory TH17 (TRM17) cells amplify autoimmune kidney disease. Sci Immunol 5
19.
go back to reference Mackay LK, Braun A, Macleod BL, Collins N, Tebartz C, Bedoui S, Carbone FR, Gebhardt T (2015) Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J Immunol 194:2059–2063PubMedCrossRef Mackay LK, Braun A, Macleod BL, Collins N, Tebartz C, Bedoui S, Carbone FR, Gebhardt T (2015) Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention. J Immunol 194:2059–2063PubMedCrossRef
20.
go back to reference Shiow LR, Rosen DB, Brdicková N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M (2006) CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544PubMedCrossRef Shiow LR, Rosen DB, Brdicková N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M (2006) CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544PubMedCrossRef
21.
go back to reference Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, Datsi A, This S, Danne C, Campion S, Duncan SH, Owens BMJ, Uhlig HH, McMichael A, Bergthaler A, Teichmann SA, Keshav S, Powrie F (2017) Circulating and Tissue-Resident CD4(+) T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function Is Altered During Inflammation. Gastroenterology 153:1320–37.e16PubMedCrossRef Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, Datsi A, This S, Danne C, Campion S, Duncan SH, Owens BMJ, Uhlig HH, McMichael A, Bergthaler A, Teichmann SA, Keshav S, Powrie F (2017) Circulating and Tissue-Resident CD4(+) T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function Is Altered During Inflammation. Gastroenterology 153:1320–37.e16PubMedCrossRef
22.
go back to reference Park JG, Na M, Kim MG, Park SH, Lee HJ, Kim DK, Kwak C, Kim YS, Chang S, Moon KC, Lee DS, Han SS (2020) Immune cell composition in normal human kidneys. Sci Rep 10:15678PubMedPubMedCentralCrossRef Park JG, Na M, Kim MG, Park SH, Lee HJ, Kim DK, Kwak C, Kim YS, Chang S, Moon KC, Lee DS, Han SS (2020) Immune cell composition in normal human kidneys. Sci Rep 10:15678PubMedPubMedCentralCrossRef
23.
go back to reference Szabo PA, Miron M, Farber DL. 2019. Location, location, location: Tissue resident memory T cells in mice and humans. Sci Immunol 4 Szabo PA, Miron M, Farber DL. 2019. Location, location, location: Tissue resident memory T cells in mice and humans. Sci Immunol 4
24.
go back to reference Mackay LK, Rahimpour A, Ma JZ, Collins N, Stock AT, Hafon ML, Vega-Ramos J, Lauzurica P, Mueller SN, Stefanovic T, Tscharke DC, Heath WR, Inouye M, Carbone FR, Gebhardt T (2013) The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat Immunol 14:1294–1301PubMedCrossRef Mackay LK, Rahimpour A, Ma JZ, Collins N, Stock AT, Hafon ML, Vega-Ramos J, Lauzurica P, Mueller SN, Stefanovic T, Tscharke DC, Heath WR, Inouye M, Carbone FR, Gebhardt T (2013) The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat Immunol 14:1294–1301PubMedCrossRef
25.
go back to reference Zhang N, Bevan MJ (2013) Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity 39:687–696PubMedPubMedCentralCrossRef Zhang N, Bevan MJ (2013) Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity 39:687–696PubMedPubMedCentralCrossRef
26.
go back to reference Kunkel EJ, Boisvert J, Murphy K, Vierra MA, Genovese MC, Wardlaw AJ, Greenberg HB, Hodge MR, Wu L, Butcher EC, Campbell JJ (2002) Expression of the chemokine receptors CCR4, CCR5, and CXCR3 by human tissue-infiltrating lymphocytes. Am J Pathol 160:347–355PubMedPubMedCentralCrossRef Kunkel EJ, Boisvert J, Murphy K, Vierra MA, Genovese MC, Wardlaw AJ, Greenberg HB, Hodge MR, Wu L, Butcher EC, Campbell JJ (2002) Expression of the chemokine receptors CCR4, CCR5, and CXCR3 by human tissue-infiltrating lymphocytes. Am J Pathol 160:347–355PubMedPubMedCentralCrossRef
27.
go back to reference Kumar BV, Ma W, Miron M, Granot T, Guyer RS, Carpenter DJ, Senda T, Sun X, Ho SH, Lerner H, Friedman AL, Shen Y, Farber DL (2017) Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites. Cell Rep 20:2921–2934PubMedPubMedCentralCrossRef Kumar BV, Ma W, Miron M, Granot T, Guyer RS, Carpenter DJ, Senda T, Sun X, Ho SH, Lerner H, Friedman AL, Shen Y, Farber DL (2017) Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites. Cell Rep 20:2921–2934PubMedPubMedCentralCrossRef
28.
go back to reference Liao W, Liu Y, Ma C, Wang L, Li G, Mishra S, Srinivasan S, Fan KK, Wu H, Li Q, Zhao M, Liu X, Demel EL, Zhang X, Qiu Y, Lu Q, Zhang N. 2021. The downregulation of IL-18R defines bona fide kidney-resident CD8(+) T cells. iScience 24: 101975 Liao W, Liu Y, Ma C, Wang L, Li G, Mishra S, Srinivasan S, Fan KK, Wu H, Li Q, Zhao M, Liu X, Demel EL, Zhang X, Qiu Y, Lu Q, Zhang N. 2021. The downregulation of IL-18R defines bona fide kidney-resident CD8(+) T cells. iScience 24: 101975
29.
go back to reference Mueller SN, Mackay LK (2016) Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol 16:79–89PubMedCrossRef Mueller SN, Mackay LK (2016) Tissue-resident memory T cells: local specialists in immune defence. Nat Rev Immunol 16:79–89PubMedCrossRef
30.
go back to reference Ma C, Mishra S, Demel EL, Liu Y, Zhang N (2017) TGF-β Controls the Formation of Kidney-Resident T Cells via Promoting Effector T Cell Extravasation. J Immunol 198:749–756PubMedCrossRef Ma C, Mishra S, Demel EL, Liu Y, Zhang N (2017) TGF-β Controls the Formation of Kidney-Resident T Cells via Promoting Effector T Cell Extravasation. J Immunol 198:749–756PubMedCrossRef
31.
go back to reference Beura LK, Anderson KG, Schenkel JM, Locquiao JJ, Fraser KA, Vezys V, Pepper M, Masopust D (2015) Lymphocytic choriomeningitis virus persistence promotes effector-like memory differentiation and enhances mucosal T cell distribution. J Leukoc Biol 97:217–225PubMedCrossRef Beura LK, Anderson KG, Schenkel JM, Locquiao JJ, Fraser KA, Vezys V, Pepper M, Masopust D (2015) Lymphocytic choriomeningitis virus persistence promotes effector-like memory differentiation and enhances mucosal T cell distribution. J Leukoc Biol 97:217–225PubMedCrossRef
32.
go back to reference Frost EL, Kersh AE, Evavold BD, Lukacher AE (2015) Cutting Edge: Resident Memory CD8 T Cells Express High-Affinity TCRs. J Immunol 195:3520–3524PubMedCrossRef Frost EL, Kersh AE, Evavold BD, Lukacher AE (2015) Cutting Edge: Resident Memory CD8 T Cells Express High-Affinity TCRs. J Immunol 195:3520–3524PubMedCrossRef
33.
go back to reference Skon CN, Lee JY, Anderson KG, Masopust D, Hogquist KA, Jameson SC (2013) Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 14:1285–1293PubMedPubMedCentralCrossRef Skon CN, Lee JY, Anderson KG, Masopust D, Hogquist KA, Jameson SC (2013) Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 14:1285–1293PubMedPubMedCentralCrossRef
34.
go back to reference Walsh DA, Borges da Silva H, Beura LK, Peng C, Hamilton SE, Masopust D, Jameson SC (2019) The Functional Requirement for CD69 in Establishment of Resident Memory CD8<sup>+</sup> T Cells Varies with Tissue Location. J Immunol 203:946–955PubMedCrossRef Walsh DA, Borges da Silva H, Beura LK, Peng C, Hamilton SE, Masopust D, Jameson SC (2019) The Functional Requirement for CD69 in Establishment of Resident Memory CD8<sup>+</sup> T Cells Varies with Tissue Location. J Immunol 203:946–955PubMedCrossRef
35.
go back to reference Mani V, Bromley SK, Äijö T, Mora-Buch R, Carrizosa E, Warner RD, Hamze M, Sen DR, Chasse AY, Lorant A, Griffith JW, Rahimi RA, McEntee CP, Jeffrey KL, Marangoni F, Travis MA, Lacy-Hulbert A, Luster AD, Mempel TR. 2019. Migratory DCs activate TGF-β to precondition naïve CD8(+) T cells for tissue-resident memory fate. Science 366 Mani V, Bromley SK, Äijö T, Mora-Buch R, Carrizosa E, Warner RD, Hamze M, Sen DR, Chasse AY, Lorant A, Griffith JW, Rahimi RA, McEntee CP, Jeffrey KL, Marangoni F, Travis MA, Lacy-Hulbert A, Luster AD, Mempel TR. 2019. Migratory DCs activate TGF-β to precondition naïve CD8(+) T cells for tissue-resident memory fate. Science 366
36.
go back to reference Mackay LK, Minnich M, Kragten NA, 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 RA, Kallies A, van Gisbergen KP (2016) Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352:459–463PubMedCrossRef Mackay LK, Minnich M, Kragten NA, 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 RA, Kallies A, van Gisbergen KP (2016) Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352:459–463PubMedCrossRef
37.
go back to reference Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, Lucas PJ, Artis D, Wherry EJ, Hogquist K, Vezys V, Masopust D (2012) Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol 188:4866–4875PubMedCrossRef Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, Lucas PJ, Artis D, Wherry EJ, Hogquist K, Vezys V, Masopust D (2012) Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol 188:4866–4875PubMedCrossRef
38.
go back to reference Schenkel JM, Fraser KA, Casey KA, Beura LK, Pauken KE, Vezys V, Masopust D (2016) IL-15-Independent Maintenance of Tissue-Resident and Boosted Effector Memory CD8 T Cells. J Immunol 196:3920–3926PubMedCrossRef Schenkel JM, Fraser KA, Casey KA, Beura LK, Pauken KE, Vezys V, Masopust D (2016) IL-15-Independent Maintenance of Tissue-Resident and Boosted Effector Memory CD8 T Cells. J Immunol 196:3920–3926PubMedCrossRef
39.
go back to reference Mackay LK, Wynne-Jones E, Freestone D, Pellicci DG, Mielke LA, Newman DM, Braun A, Masson F, Kallies A, Belz GT, Carbone FR (2015) T-box Transcription Factors Combine with the Cytokines TGF-β and IL-15 to Control Tissue-Resident Memory T Cell Fate. Immunity 43:1101–1111PubMedCrossRef Mackay LK, Wynne-Jones E, Freestone D, Pellicci DG, Mielke LA, Newman DM, Braun A, Masson F, Kallies A, Belz GT, Carbone FR (2015) T-box Transcription Factors Combine with the Cytokines TGF-β and IL-15 to Control Tissue-Resident Memory T Cell Fate. Immunity 43:1101–1111PubMedCrossRef
40.
go back to reference Holz LE, Prier JE, Freestone D, Steiner TM, English K, Johnson DN, Mollard V, Cozijnsen A, Davey GM, Godfrey DI, Yui K, Mackay LK, Lahoud MH, Caminschi I, McFadden GI, Bertolino P, Fernandez-Ruiz D, Heath WR (2018) CD8(+) T Cell Activation Leads to Constitutive Formation of Liver Tissue-Resident Memory T Cells that Seed a Large and Flexible Niche in the Liver. Cell Rep 25:68-79.e4PubMedCrossRef Holz LE, Prier JE, Freestone D, Steiner TM, English K, Johnson DN, Mollard V, Cozijnsen A, Davey GM, Godfrey DI, Yui K, Mackay LK, Lahoud MH, Caminschi I, McFadden GI, Bertolino P, Fernandez-Ruiz D, Heath WR (2018) CD8(+) T Cell Activation Leads to Constitutive Formation of Liver Tissue-Resident Memory T Cells that Seed a Large and Flexible Niche in the Liver. Cell Rep 25:68-79.e4PubMedCrossRef
41.
go back to reference 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 RA (2016) Programs for the persistence, vigilance and control of human CD8(+) lung-resident memory T cells. Nat Immunol 17:1467–1478PubMedCrossRef 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 RA (2016) Programs for the persistence, vigilance and control of human CD8(+) lung-resident memory T cells. Nat Immunol 17:1467–1478PubMedCrossRef
42.
go back to reference van der Gracht ETI, Behr FM, Arens R. 2021. Functional Heterogeneity and Therapeutic Targeting of Tissue-Resident Memory T Cells. Cells 10 van der Gracht ETI, Behr FM, Arens R. 2021. Functional Heterogeneity and Therapeutic Targeting of Tissue-Resident Memory T Cells. Cells 10
43.
go back to reference Milner JJ, Toma C, Yu B, Zhang K, Omilusik K, Phan AT, Wang D, Getzler AJ, Nguyen T, Crotty S, Wang W, Pipkin ME, Goldrath AW (2017) Runx3 programs CD8(+) T cell residency in non-lymphoid tissues and tumours. Nature 552:253–257PubMedPubMedCentralCrossRef Milner JJ, Toma C, Yu B, Zhang K, Omilusik K, Phan AT, Wang D, Getzler AJ, Nguyen T, Crotty S, Wang W, Pipkin ME, Goldrath AW (2017) Runx3 programs CD8(+) T cell residency in non-lymphoid tissues and tumours. Nature 552:253–257PubMedPubMedCentralCrossRef
44.
go back to reference Behr FM, Chuwonpad A, Stark R, van Gisbergen K (2018) Armed and Ready: Transcriptional Regulation of Tissue-Resident Memory CD8 T Cells. Front Immunol 9:1770PubMedPubMedCentralCrossRef Behr FM, Chuwonpad A, Stark R, van Gisbergen K (2018) Armed and Ready: Transcriptional Regulation of Tissue-Resident Memory CD8 T Cells. Front Immunol 9:1770PubMedPubMedCentralCrossRef
45.
go back to reference Li C, Zhu B, Son YM, Wang Z, Jiang L, Xiang M, Ye Z, Beckermann KE, Wu Y, Jenkins JW, Siska PJ, Vincent BG, Prakash YS, Peikert T, Edelson BT, Taneja R, Kaplan MH, Rathmell JC, Dong H, Hitosugi T, Sun J (2019) The Transcription Factor Bhlhe40 Programs Mitochondrial Regulation of Resident CD8(+) T Cell Fitness and Functionality. Immunity 51:491-507.e7PubMedPubMedCentralCrossRef Li C, Zhu B, Son YM, Wang Z, Jiang L, Xiang M, Ye Z, Beckermann KE, Wu Y, Jenkins JW, Siska PJ, Vincent BG, Prakash YS, Peikert T, Edelson BT, Taneja R, Kaplan MH, Rathmell JC, Dong H, Hitosugi T, Sun J (2019) The Transcription Factor Bhlhe40 Programs Mitochondrial Regulation of Resident CD8(+) T Cell Fitness and Functionality. Immunity 51:491-507.e7PubMedPubMedCentralCrossRef
46.
go back to reference Kim JH, Han JW, Choi YJ, Rha MS, Koh JY, Kim KH, Kim CG, Lee YJ, Kim AR, Park J, Kim HK, Min BS, Seo SI, Kang M, Park HJ, Han DH, Kim SI, Kim MS, Lee JG, Lee DH, Kim W, Park JY, Park SH, Joo DJ, Shin EC (2020) Functions of human liver CD69(+)CD103(-)CD8(+) T cells depend on HIF-2α activity in healthy and pathologic livers. J Hepatol 72:1170–1181PubMedCrossRef Kim JH, Han JW, Choi YJ, Rha MS, Koh JY, Kim KH, Kim CG, Lee YJ, Kim AR, Park J, Kim HK, Min BS, Seo SI, Kang M, Park HJ, Han DH, Kim SI, Kim MS, Lee JG, Lee DH, Kim W, Park JY, Park SH, Joo DJ, Shin EC (2020) Functions of human liver CD69(+)CD103(-)CD8(+) T cells depend on HIF-2α activity in healthy and pathologic livers. J Hepatol 72:1170–1181PubMedCrossRef
47.
go back to reference Schödel J, Ratcliffe PJ (2019) Mechanisms of hypoxia signalling: new implications for nephrology. Nat Rev Nephrol 15:641–659PubMedCrossRef Schödel J, Ratcliffe PJ (2019) Mechanisms of hypoxia signalling: new implications for nephrology. Nat Rev Nephrol 15:641–659PubMedCrossRef
49.
go back to reference Pan Y, Tian T, Park CO, Lofftus SY, Mei S, Liu X, Luo C, O’Malley JT, Gehad A, Teague JE, Divito SJ, Fuhlbrigge R, Puigserver P, Krueger JG, Hotamisligil GS, Clark RA, Kupper TS (2017) Survival of tissue-resident memory T cells requires exogenous lipid uptake and metabolism. Nature 543:252–256PubMedPubMedCentralCrossRef Pan Y, Tian T, Park CO, Lofftus SY, Mei S, Liu X, Luo C, O’Malley JT, Gehad A, Teague JE, Divito SJ, Fuhlbrigge R, Puigserver P, Krueger JG, Hotamisligil GS, Clark RA, Kupper TS (2017) Survival of tissue-resident memory T cells requires exogenous lipid uptake and metabolism. Nature 543:252–256PubMedPubMedCentralCrossRef
50.
go back to reference Park SL, Zaid A, Hor JL, Christo SN, Prier JE, Davies B, Alexandre YO, Gregory JL, Russell TA, Gebhardt T, Carbone FR, Tscharke DC, Heath WR, Mueller SN, Mackay LK (2018) Local proliferation maintains a stable pool of tissue-resident memory T cells after antiviral recall responses. Nat Immunol 19:183–191PubMedCrossRef Park SL, Zaid A, Hor JL, Christo SN, Prier JE, Davies B, Alexandre YO, Gregory JL, Russell TA, Gebhardt T, Carbone FR, Tscharke DC, Heath WR, Mueller SN, Mackay LK (2018) Local proliferation maintains a stable pool of tissue-resident memory T cells after antiviral recall responses. Nat Immunol 19:183–191PubMedCrossRef
51.
go back to reference Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrançois L, Farber DL (2011) Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol 187:5510–5514PubMedCrossRef Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrançois L, Farber DL (2011) Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol 187:5510–5514PubMedCrossRef
53.
go back to reference Roberts KB (2011) Urinary tract infection: clinical practice guideline for the diagnosis and management of the initial UTI in febrile infants and children 2 to 24 months. Pediatrics 128:595–610PubMedCrossRef Roberts KB (2011) Urinary tract infection: clinical practice guideline for the diagnosis and management of the initial UTI in febrile infants and children 2 to 24 months. Pediatrics 128:595–610PubMedCrossRef
54.
go back to reference Ohnishi T, Asada N, Furuichi M, Sekiguchi S, Awazu M, Hori N, Kamimaki I (2020) A novel screening method for pediatric urinary tract infection using ordinary diapers. Sci Rep 10:19342PubMedPubMedCentralCrossRef Ohnishi T, Asada N, Furuichi M, Sekiguchi S, Awazu M, Hori N, Kamimaki I (2020) A novel screening method for pediatric urinary tract infection using ordinary diapers. Sci Rep 10:19342PubMedPubMedCentralCrossRef
55.
go back to reference Fogo AB, Lusco MA, Najafian B, Alpers CE (2016) AJKD Atlas of Renal Pathology: Cytomegalovirus Infection. Am J Kidney Dis 68:e35–e36PubMedCrossRef Fogo AB, Lusco MA, Najafian B, Alpers CE (2016) AJKD Atlas of Renal Pathology: Cytomegalovirus Infection. Am J Kidney Dis 68:e35–e36PubMedCrossRef
56.
go back to reference Smith CJ, Caldeira-Dantas S, Turula H, Snyder CM (2015) Murine CMV Infection Induces the Continuous Production of Mucosal Resident T Cells. Cell Rep 13:1137–1148PubMedPubMedCentralCrossRef Smith CJ, Caldeira-Dantas S, Turula H, Snyder CM (2015) Murine CMV Infection Induces the Continuous Production of Mucosal Resident T Cells. Cell Rep 13:1137–1148PubMedPubMedCentralCrossRef
57.
go back to reference Beura LK, Fares-Frederickson NJ, Steinert EM, Scott MC, Thompson EA, Fraser KA, Schenkel JM, Vezys V, Masopust D (2019) CD4(+) resident memory T cells dominate immunosurveillance and orchestrate local recall responses. J Exp Med 216:1214–1229PubMedPubMedCentralCrossRef Beura LK, Fares-Frederickson NJ, Steinert EM, Scott MC, Thompson EA, Fraser KA, Schenkel JM, Vezys V, Masopust D (2019) CD4(+) resident memory T cells dominate immunosurveillance and orchestrate local recall responses. J Exp Med 216:1214–1229PubMedPubMedCentralCrossRef
58.
go back to reference van Aalderen MC, Heutinck KM, Huisman C, ten Berge IJ (2012) BK virus infection in transplant recipients: clinical manifestations, treatment options and the immune response. Neth J Med 70:172–183PubMed van Aalderen MC, Heutinck KM, Huisman C, ten Berge IJ (2012) BK virus infection in transplant recipients: clinical manifestations, treatment options and the immune response. Neth J Med 70:172–183PubMed
59.
go back to reference van Aalderen MC, Remmerswaal EB, Heutinck KM, Ten Brinke A, Feltkamp MC, van der Weerd NC, van der Pant KA, Bemelman FJ, van Lier RA, Ten Berge IJ. 2016. Clinically Relevant Reactivation of Polyomavirus BK (BKPyV) in HLA-A02-Positive Renal Transplant Recipients Is Associated with Impaired Effector-Memory Differentiation of BKPyV-Specific CD8+ T Cells. PLoS Pathog 12: e1005903 van Aalderen MC, Remmerswaal EB, Heutinck KM, Ten Brinke A, Feltkamp MC, van der Weerd NC, van der Pant KA, Bemelman FJ, van Lier RA, Ten Berge IJ. 2016. Clinically Relevant Reactivation of Polyomavirus BK (BKPyV) in HLA-A02-Positive Renal Transplant Recipients Is Associated with Impaired Effector-Memory Differentiation of BKPyV-Specific CD8+ T Cells. PLoS Pathog 12: e1005903
60.
go back to reference van Aalderen MC, Remmerswaal EB, Heutinck KM, ten Brinke A, Pircher H, van Lier RA, ten Berge IJ (2013) Phenotypic and functional characterization of circulating polyomavirus BK VP1-specific CD8+ T cells in healthy adults. J Virol 87:10263–10272PubMedPubMedCentralCrossRef van Aalderen MC, Remmerswaal EB, Heutinck KM, ten Brinke A, Pircher H, van Lier RA, ten Berge IJ (2013) Phenotypic and functional characterization of circulating polyomavirus BK VP1-specific CD8+ T cells in healthy adults. J Virol 87:10263–10272PubMedPubMedCentralCrossRef
61.
go back to reference 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 factor-alpha. J Exp Med 199:731–736PubMedPubMedCentralCrossRef 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 factor-alpha. J Exp Med 199:731–736PubMedPubMedCentralCrossRef
62.
go back to reference Cheuk S, Wikén M, Blomqvist L, Nylén S, Talme T, Ståhle M, Eidsmo L (2014) Epidermal Th22 and Tc17 cells form a localized disease memory in clinically healed psoriasis. J Immunol 192:3111–3120PubMedPubMedCentralCrossRef Cheuk S, Wikén M, Blomqvist L, Nylén S, Talme T, Ståhle M, Eidsmo L (2014) Epidermal Th22 and Tc17 cells form a localized disease memory in clinically healed psoriasis. J Immunol 192:3111–3120PubMedPubMedCentralCrossRef
63.
go back to reference Matos TR, O’Malley JT, Lowry EL, Hamm D, Kirsch IR, Robins HS, Kupper TS, Krueger JG, Clark RA (2017) Clinically resolved psoriatic lesions contain psoriasis-specific IL-17-producing αβ T cell clones. J Clin Invest 127:4031–4041PubMedPubMedCentralCrossRef Matos TR, O’Malley JT, Lowry EL, Hamm D, Kirsch IR, Robins HS, Kupper TS, Krueger JG, Clark RA (2017) Clinically resolved psoriatic lesions contain psoriasis-specific IL-17-producing αβ T cell clones. J Clin Invest 127:4031–4041PubMedPubMedCentralCrossRef
64.
go back to reference Couzi L, Merville P, Deminière C, Moreau JF, Combe C, Pellegrin JL, Viallard JF, Blanco P (2007) Predominance of CD8+ T lymphocytes among periglomerular infiltrating cells and link to the prognosis of class III and class IV lupus nephritis. Arthritis Rheum 56:2362–2370PubMedCrossRef Couzi L, Merville P, Deminière C, Moreau JF, Combe C, Pellegrin JL, Viallard JF, Blanco P (2007) Predominance of CD8+ T lymphocytes among periglomerular infiltrating cells and link to the prognosis of class III and class IV lupus nephritis. Arthritis Rheum 56:2362–2370PubMedCrossRef
65.
go back to reference O’Sullivan KM, Lo CY, Summers SA, Elgass KD, McMillan PJ, Longano A, Ford SL, Gan PY, Kerr PG, Kitching AR, Holdsworth SR (2015) Renal participation of myeloperoxidase in antineutrophil cytoplasmic antibody (ANCA)-associated glomerulonephritis. Kidney Int 88:1030–1046PubMedCrossRef O’Sullivan KM, Lo CY, Summers SA, Elgass KD, McMillan PJ, Longano A, Ford SL, Gan PY, Kerr PG, Kitching AR, Holdsworth SR (2015) Renal participation of myeloperoxidase in antineutrophil cytoplasmic antibody (ANCA)-associated glomerulonephritis. Kidney Int 88:1030–1046PubMedCrossRef
66.
go back to reference Masutani K, Akahoshi M, Tsuruya K, Tokumoto M, Ninomiya T, Kohsaka T, Fukuda K, Kanai H, Nakashima H, Otsuka T, Hirakata H (2001) Predominance of Th1 immune response in diffuse proliferative lupus nephritis. Arthritis Rheum 44:2097–2106PubMedCrossRef Masutani K, Akahoshi M, Tsuruya K, Tokumoto M, Ninomiya T, Kohsaka T, Fukuda K, Kanai H, Nakashima H, Otsuka T, Hirakata H (2001) Predominance of Th1 immune response in diffuse proliferative lupus nephritis. Arthritis Rheum 44:2097–2106PubMedCrossRef
67.
go back to reference Zhou M, Guo C, Li X, Huang Y, Li M, Zhang T, Zhao S, Wang S, Zhang H, Yang N. 2020. JAK/STAT signaling controls the fate of CD8(+)CD103(+) tissue-resident memory T cell in lupus nephritis. J Autoimmun 109: 102424 Zhou M, Guo C, Li X, Huang Y, Li M, Zhang T, Zhao S, Wang S, Zhang H, Yang N. 2020. JAK/STAT signaling controls the fate of CD8(+)CD103(+) tissue-resident memory T cell in lupus nephritis. J Autoimmun 109: 102424
68.
go back to reference Krebs CF, Paust HJ, Krohn S, Koyro T, Brix SR, Riedel JH, Bartsch P, Wiech T, Meyer-Schwesinger C, Huang J, Fischer N, Busch P, Mittrücker HW, Steinhoff U, Stockinger B, Perez LG, Wenzel UO, Janneck M, Steinmetz OM, Gagliani N, Stahl RAK, Huber S, Turner JE, Panzer U (2016) Autoimmune Renal Disease Is Exacerbated by S1P-Receptor-1-Dependent Intestinal Th17 Cell Migration to the Kidney. Immunity 45:1078–1092PubMedPubMedCentralCrossRef Krebs CF, Paust HJ, Krohn S, Koyro T, Brix SR, Riedel JH, Bartsch P, Wiech T, Meyer-Schwesinger C, Huang J, Fischer N, Busch P, Mittrücker HW, Steinhoff U, Stockinger B, Perez LG, Wenzel UO, Janneck M, Steinmetz OM, Gagliani N, Stahl RAK, Huber S, Turner JE, Panzer U (2016) Autoimmune Renal Disease Is Exacerbated by S1P-Receptor-1-Dependent Intestinal Th17 Cell Migration to the Kidney. Immunity 45:1078–1092PubMedPubMedCentralCrossRef
69.
go back to reference Tilstra JS, Avery L, Menk AV, Gordon RA, Smita S, Kane LP, Chikina M, Delgoffe GM, Shlomchik MJ (2018) Kidney-infiltrating T cells in murine lupus nephritis are metabolically and functionally exhausted. J Clin Invest 128:4884–4897PubMedPubMedCentralCrossRef Tilstra JS, Avery L, Menk AV, Gordon RA, Smita S, Kane LP, Chikina M, Delgoffe GM, Shlomchik MJ (2018) Kidney-infiltrating T cells in murine lupus nephritis are metabolically and functionally exhausted. J Clin Invest 128:4884–4897PubMedPubMedCentralCrossRef
70.
go back to reference Arazi A, Rao DA, Berthier CC, Davidson A, Liu Y, Hoover PJ, Chicoine A, Eisenhaure TM, Jonsson AH, Li S, Lieb DJ, Zhang F, Slowikowski K, Browne EP, Noma A, Sutherby D, Steelman S, Smilek DE, Tosta P, Apruzzese W, Massarotti E, Dall’Era M, Park M, Kamen DL, Furie RA, Payan-Schober F, Pendergraft WF 3rd, McInnis EA, Buyon JP, Petri MA, Putterman C, Kalunian KC, Woodle ES, Lederer JA, Hildeman DA, Nusbaum C, Raychaudhuri S, Kretzler M, Anolik JH, Brenner MB, Wofsy D, Hacohen N, Diamond B (2019) The immune cell landscape in kidneys of patients with lupus nephritis. Nat Immunol 20:902–914PubMedPubMedCentralCrossRef Arazi A, Rao DA, Berthier CC, Davidson A, Liu Y, Hoover PJ, Chicoine A, Eisenhaure TM, Jonsson AH, Li S, Lieb DJ, Zhang F, Slowikowski K, Browne EP, Noma A, Sutherby D, Steelman S, Smilek DE, Tosta P, Apruzzese W, Massarotti E, Dall’Era M, Park M, Kamen DL, Furie RA, Payan-Schober F, Pendergraft WF 3rd, McInnis EA, Buyon JP, Petri MA, Putterman C, Kalunian KC, Woodle ES, Lederer JA, Hildeman DA, Nusbaum C, Raychaudhuri S, Kretzler M, Anolik JH, Brenner MB, Wofsy D, Hacohen N, Diamond B (2019) The immune cell landscape in kidneys of patients with lupus nephritis. Nat Immunol 20:902–914PubMedPubMedCentralCrossRef
71.
go back to reference Bertolo M, Baumgart S, Durek P, Peddinghaus A, Mei H, Rose T, Enghard P, Grützkau A (2020) Deep Phenotyping of Urinary Leukocytes by Mass Cytometry Reveals a Leukocyte Signature for Early and Non-Invasive Prediction of Response to Treatment in Active Lupus Nephritis. Front Immunol 11:256PubMedPubMedCentralCrossRef Bertolo M, Baumgart S, Durek P, Peddinghaus A, Mei H, Rose T, Enghard P, Grützkau A (2020) Deep Phenotyping of Urinary Leukocytes by Mass Cytometry Reveals a Leukocyte Signature for Early and Non-Invasive Prediction of Response to Treatment in Active Lupus Nephritis. Front Immunol 11:256PubMedPubMedCentralCrossRef
72.
go back to reference Park SL, Gebhardt T, Mackay LK (2019) Tissue-Resident Memory T Cells in Cancer Immunosurveillance. Trends Immunol 40:735–747PubMedCrossRef Park SL, Gebhardt T, Mackay LK (2019) Tissue-Resident Memory T Cells in Cancer Immunosurveillance. Trends Immunol 40:735–747PubMedCrossRef
73.
go back to reference Díaz-Montero CM, Rini BI, Finke JH (2020) The immunology of renal cell carcinoma. Nat Rev Nephrol 16:721–735PubMedCrossRef Díaz-Montero CM, Rini BI, Finke JH (2020) The immunology of renal cell carcinoma. Nat Rev Nephrol 16:721–735PubMedCrossRef
74.
go back to reference Chevrier S, Levine JH, Zanotelli VRT, Silina K, Schulz D, Bacac M, Ries CH, Ailles L, Jewett MAS, Moch H, van den Broek M, Beisel C, Stadler MB, Gedye C, Reis B, Pe’er D, Bodenmiller B (2017) An Immune Atlas of Clear Cell Renal Cell Carcinoma. Cell 169:736–49.e18PubMedPubMedCentralCrossRef Chevrier S, Levine JH, Zanotelli VRT, Silina K, Schulz D, Bacac M, Ries CH, Ailles L, Jewett MAS, Moch H, van den Broek M, Beisel C, Stadler MB, Gedye C, Reis B, Pe’er D, Bodenmiller B (2017) An Immune Atlas of Clear Cell Renal Cell Carcinoma. Cell 169:736–49.e18PubMedPubMedCentralCrossRef
75.
go back to reference Geissler K, Fornara P, Lautenschläger C, Holzhausen HJ, Seliger B, Riemann D. 2015. Immune signature of tumor infiltrating immune cells in renal cancer. Oncoimmunology 4: e985082 Geissler K, Fornara P, Lautenschläger C, Holzhausen HJ, Seliger B, Riemann D. 2015. Immune signature of tumor infiltrating immune cells in renal cancer. Oncoimmunology 4: e985082
76.
go back to reference Kawashima A, Kanazawa T, Kidani Y, Yoshida T, Hirata M, Nishida K, Nojima S, Yamamoto Y, Kato T, Hatano K, Ujike T, Nagahara A, Fujita K, Morimoto-Okazawa A, Iwahori K, Uemura M, Imamura R, Ohkura N, Morii E, Sakaguchi S, Wada H, Nonomura N (2020) Tumour grade significantly correlates with total dysfunction of tumour tissue-infiltrating lymphocytes in renal cell carcinoma. Sci Rep 10:6220PubMedPubMedCentralCrossRef Kawashima A, Kanazawa T, Kidani Y, Yoshida T, Hirata M, Nishida K, Nojima S, Yamamoto Y, Kato T, Hatano K, Ujike T, Nagahara A, Fujita K, Morimoto-Okazawa A, Iwahori K, Uemura M, Imamura R, Ohkura N, Morii E, Sakaguchi S, Wada H, Nonomura N (2020) Tumour grade significantly correlates with total dysfunction of tumour tissue-infiltrating lymphocytes in renal cell carcinoma. Sci Rep 10:6220PubMedPubMedCentralCrossRef
77.
go back to reference Fridman WH, Pagès F, Sautès-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298–306PubMedCrossRef Fridman WH, Pagès F, Sautès-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298–306PubMedCrossRef
78.
go back to reference Nakano O, Sato M, Naito Y, Suzuki K, Orikasa S, Aizawa M, Suzuki Y, Shintaku I, Nagura H, Ohtani H (2001) Proliferative activity of intratumoral CD8(+) T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res 61:5132–5136PubMed Nakano O, Sato M, Naito Y, Suzuki K, Orikasa S, Aizawa M, Suzuki Y, Shintaku I, Nagura H, Ohtani H (2001) Proliferative activity of intratumoral CD8(+) T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res 61:5132–5136PubMed
79.
go back to reference Zhou J, Liu L, Yang T, Lu B (2018) Prognostic and therapeutic value of CD103(+) cells in renal cell carcinoma. Exp Ther Med 15:4979–4986PubMedPubMedCentral Zhou J, Liu L, Yang T, Lu B (2018) Prognostic and therapeutic value of CD103(+) cells in renal cell carcinoma. Exp Ther Med 15:4979–4986PubMedPubMedCentral
80.
81.
go back to reference Wang J, Li X, Wu X, Wang Z, Zhang C, Cao G, Zhang X, Peng F, Yan T (2019) Role of immune checkpoint inhibitor-based therapies for metastatic renal cell carcinoma in the first-line setting: A Bayesian network analysis. EBioMedicine 47:78–88PubMedPubMedCentralCrossRef Wang J, Li X, Wu X, Wang Z, Zhang C, Cao G, Zhang X, Peng F, Yan T (2019) Role of immune checkpoint inhibitor-based therapies for metastatic renal cell carcinoma in the first-line setting: A Bayesian network analysis. EBioMedicine 47:78–88PubMedPubMedCentralCrossRef
82.
go back to reference Park SL, Buzzai A, Rautela J, Hor JL, Hochheiser K, Effern M, McBain N, Wagner T, Edwards J, McConville R, Wilmott JS, Scolyer RA, Tüting T, Palendira U, Gyorki D, Mueller SN, Huntington ND, Bedoui S, Hölzel M, Mackay LK, Waithman J, Gebhardt T (2019) Tissue-resident memory CD8(+) T cells promote melanoma-immune equilibrium in skin. Nature 565:366–371PubMedCrossRef Park SL, Buzzai A, Rautela J, Hor JL, Hochheiser K, Effern M, McBain N, Wagner T, Edwards J, McConville R, Wilmott JS, Scolyer RA, Tüting T, Palendira U, Gyorki D, Mueller SN, Huntington ND, Bedoui S, Hölzel M, Mackay LK, Waithman J, Gebhardt T (2019) Tissue-resident memory CD8(+) T cells promote melanoma-immune equilibrium in skin. Nature 565:366–371PubMedCrossRef
83.
go back to reference Malik BT, Byrne KT, Vella JL, Zhang P, Shabaneh TB, Steinberg SM, Molodtsov AK, Bowers JS, Angeles CV, Paulos CM, Huang YH, Turk MJ. 2017. Resident memory T cells in the skin mediate durable immunity to melanoma. Sci Immunol 2 Malik BT, Byrne KT, Vella JL, Zhang P, Shabaneh TB, Steinberg SM, Molodtsov AK, Bowers JS, Angeles CV, Paulos CM, Huang YH, Turk MJ. 2017. Resident memory T cells in the skin mediate durable immunity to melanoma. Sci Immunol 2
84.
go back to reference Patel SP, Kurzrock R (2015) PD-L1 Expression as a Predictive Biomarker in Cancer Immunotherapy. Mol Cancer Ther 14:847–856PubMedCrossRef Patel SP, Kurzrock R (2015) PD-L1 Expression as a Predictive Biomarker in Cancer Immunotherapy. Mol Cancer Ther 14:847–856PubMedCrossRef
85.
go back to reference Lemery S, Keegan P, Pazdur R (2017) First FDA Approval Agnostic of Cancer Site - When a Biomarker Defines the Indication. N Engl J Med 377:1409–1412PubMedCrossRef Lemery S, Keegan P, Pazdur R (2017) First FDA Approval Agnostic of Cancer Site - When a Biomarker Defines the Indication. N Engl J Med 377:1409–1412PubMedCrossRef
86.
go back to reference McDermott DF, Huseni MA, Atkins MB, Motzer RJ, Rini BI, Escudier B, Fong L, Joseph RW, Pal SK, Reeves JA, Sznol M, Hainsworth J, Rathmell WK, Stadler WM, Hutson T, Gore ME, Ravaud A, Bracarda S, Suárez C, Danielli R, Gruenwald V, Choueiri TK, Nickles D, Jhunjhunwala S, Piault-Louis E, Thobhani A, Qiu J, Chen DS, Hegde PS, Schiff C, Fine GD, Powles T (2018) Publisher Correction: Clinical activity and molecular correlates of response to atezolizumab alone or in combination with bevacizumab versus sunitinib in renal cell carcinoma. Nat Med 24:1941PubMedCrossRef McDermott DF, Huseni MA, Atkins MB, Motzer RJ, Rini BI, Escudier B, Fong L, Joseph RW, Pal SK, Reeves JA, Sznol M, Hainsworth J, Rathmell WK, Stadler WM, Hutson T, Gore ME, Ravaud A, Bracarda S, Suárez C, Danielli R, Gruenwald V, Choueiri TK, Nickles D, Jhunjhunwala S, Piault-Louis E, Thobhani A, Qiu J, Chen DS, Hegde PS, Schiff C, Fine GD, Powles T (2018) Publisher Correction: Clinical activity and molecular correlates of response to atezolizumab alone or in combination with bevacizumab versus sunitinib in renal cell carcinoma. Nat Med 24:1941PubMedCrossRef
87.
go back to reference Nizard M, Roussel H, Diniz MO, Karaki S, Tran T, Voron T, Dransart E, Sandoval F, Riquet M, Rance B, Marcheteau E, Fabre E, Mandavit M, Terme M, Blanc C, Escudie JB, Gibault L, Barthes FLP, Granier C, Ferreira LCS, Badoual C, Johannes L, Tartour E (2017) Induction of resident memory T cells enhances the efficacy of cancer vaccine. Nat Commun 8:15221PubMedPubMedCentralCrossRef Nizard M, Roussel H, Diniz MO, Karaki S, Tran T, Voron T, Dransart E, Sandoval F, Riquet M, Rance B, Marcheteau E, Fabre E, Mandavit M, Terme M, Blanc C, Escudie JB, Gibault L, Barthes FLP, Granier C, Ferreira LCS, Badoual C, Johannes L, Tartour E (2017) Induction of resident memory T cells enhances the efficacy of cancer vaccine. Nat Commun 8:15221PubMedPubMedCentralCrossRef
88.
go back to reference Braun DA, Bakouny Z, Hirsch L, Flippot R, Van Allen EM, Wu CJ, Choueiri TK (2021) Beyond conventional immune-checkpoint inhibition - novel immunotherapies for renal cell carcinoma. Nat Rev Clin Oncol 18:199–214PubMedPubMedCentralCrossRef Braun DA, Bakouny Z, Hirsch L, Flippot R, Van Allen EM, Wu CJ, Choueiri TK (2021) Beyond conventional immune-checkpoint inhibition - novel immunotherapies for renal cell carcinoma. Nat Rev Clin Oncol 18:199–214PubMedPubMedCentralCrossRef
89.
go back to reference Halloran PF (2010) T cell-mediated rejection of kidney transplants: a personal viewpoint. Am J Transplant 10:1126–1134PubMedCrossRef Halloran PF (2010) T cell-mediated rejection of kidney transplants: a personal viewpoint. Am J Transplant 10:1126–1134PubMedCrossRef
90.
go back to reference Venner JM, Famulski KS, Badr D, Hidalgo LG, Chang J, Halloran PF (2014) Molecular landscape of T cell-mediated rejection in human kidney transplants: prominence of CTLA4 and PD ligands. Am J Transplant 14:2565–2576PubMedCrossRef Venner JM, Famulski KS, Badr D, Hidalgo LG, Chang J, Halloran PF (2014) Molecular landscape of T cell-mediated rejection in human kidney transplants: prominence of CTLA4 and PD ligands. Am J Transplant 14:2565–2576PubMedCrossRef
91.
go back to reference Heeger PS, Greenspan NS, Kuhlenschmidt S, Dejelo C, Hricik DE, Schulak JA, Tary-Lehmann M (1999) Pretransplant frequency of donor-specific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J Immunol 163:2267–2275PubMed Heeger PS, Greenspan NS, Kuhlenschmidt S, Dejelo C, Hricik DE, Schulak JA, Tary-Lehmann M (1999) Pretransplant frequency of donor-specific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J Immunol 163:2267–2275PubMed
92.
go back to reference Hricik DE, Rodriguez V, Riley J, Bryan K, Tary-Lehmann M, Greenspan N, Dejelo C, Schulak JA, Heeger PS (2003) Enzyme linked immunosorbent spot (ELISPOT) assay for interferon-gamma independently predicts renal function in kidney transplant recipients. Am J Transplant 3:878–884PubMedCrossRef Hricik DE, Rodriguez V, Riley J, Bryan K, Tary-Lehmann M, Greenspan N, Dejelo C, Schulak JA, Heeger PS (2003) Enzyme linked immunosorbent spot (ELISPOT) assay for interferon-gamma independently predicts renal function in kidney transplant recipients. Am J Transplant 3:878–884PubMedCrossRef
93.
go back to reference Abou-Daya KI, Tieu R, Zhao D, Rammal R, Sacirbegovic F, Williams AL, Shlomchik WD, Oberbarnscheidt MH, Lakkis FG. 2021. Resident memory T cells form during persistent antigen exposure leading to allograft rejection. Sci Immunol 6 Abou-Daya KI, Tieu R, Zhao D, Rammal R, Sacirbegovic F, Williams AL, Shlomchik WD, Oberbarnscheidt MH, Lakkis FG. 2021. Resident memory T cells form during persistent antigen exposure leading to allograft rejection. Sci Immunol 6
Metadata
Title
Tissue-resident memory T cells in the kidney
Authors
Nariaki Asada
Pauline Ginsberg
Nicola Gagliani
Hans-Willi Mittrücker
Ulf Panzer
Publication date
11-04-2022
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 6/2022
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-022-00927-7

Other articles of this Issue 6/2022

Seminars in Immunopathology 6/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.