Journal of Shandong University (Health Sciences) ›› 2021, Vol. 59 ›› Issue (9): 15-21.doi: 10.6040/j.issn.1671-7554.0.2021.0874

Previous Articles     Next Articles

Maintenance and function of tissue resident memory T cells in the kidney

YI Fan, LI Liang   

  1. Department of Pharmacology, School of Basic Medical Sciences, Shandong University, Jinan 250012, Shandong, China
  • Published:2021-10-15

RichHTML

11

PDF (PC)

173

Abstract: Tissue resident memory T cells (T-RM), a recently discovered type of T lymphocytes, do not participate in systemic circulation but reside in organs. T-RM possess a unique differentiation regulation mechanism and contribute to immunomodulatory effect. They play an important role in the occurrence and development of many kinds of diseases and are expected to become a new therapeutic target. T-RM have also been found in the kidney. This review will focus on the formation, biological characteristics and maintenance of T-RM in the kidney and the role of T-RMin kidney diseases.

CLC Number: 

  • R692
[1] Jiang X, Clark RA, Liu L, et al. Skin infection generates non-migratory memory CD8+ T(RM)cells providing global skin immunity [J]. Nature, 2012, 483(7388): 227-231.
[2] Glennie ND, Yeramilli VA, Beiting DP, et al. Skin-resident memory CD4+ T cells enhance protection against Leishmania major infection [J]. J Exp Med, 2015, 212(9): 1405-1414.
[3] Pizzolla A, Nguyen THO, Smith JM, et al. Resident memory CD8(+)T cells in the upper respiratory tract prevent pulmonary influenza virus infection [J]. Sci Immunol, 2017, 2(12): eaam6970. doi: 10.1126/sciimmunol.aam6970.
[4] Rodriguez-Garcia M, Shen Z, Fortier JM, et al. Differential cytotoxic function of resident and non-resident CD8+ T cells in the human female reproductive tract before and after menopause [J]. Front Immunol, 2020, 11: 1096. doi: 10.3389/fimmu.2020.01096.
[5] Zundler S, Becker E, Spocinska M, et al. Hobit- and Blimp-1-driven CD4(+)tissue-resident memory T cells control chronic intestinal inflammation [J]. Nat Immunol, 2019, 20(3): 288-300.
[6] Mueller SN, Mackay LK. Tissue-resident memory T cells: local specialists in immune defence [J]. Nat Rev Immunol, 2016, 16(2): 79-89.
[7] Okla K, Farber DL, Zou W. Tissue-resident memory T cells in tumor immunity and immunotherapy [J]. J Exp Med, 2021, 218(4):e20201605. doi: 10.1084/jem.20201605.
[8] Mueller SN, Gebhardt T, Carbone FR, et al. Memory T cell subsets, migration patterns, and tissue residence [J]. Annu Rev Immunol, 2013, 31: 137-161. doi: 10.1146/annurev-immunol-032712-095954.
[9] Schenkel JM, Masopust D. Tissue-resident memory T cells [J]. Immunity, 2014, 41(6): 886-897.
[10] Gebhardt T, Mueller SN, HEATH WR, et al. Peripheral tissue surveillance and residency by memory T cells [J]. Trends Immunol, 2013, 34(1): 27-32.
[11] Hogan RJ, Usherwood EJ, Zhong W, et al. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections [J]. J Immunol, 2001, 166(3): 1813-1822.
[12] Masopust D, Vezys V, Marzo AL, et al. Preferential localization of effector memory cells in nonlymphoid tissue [J]. Science, 2001, 291(5512): 2413-2417.
[13] Gebhardt T, Wakim LM, Eidsmo L, et al. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus [J]. Nat Immunol, 2009, 10(5): 524-530.
[14] Teijaro JR, Turner D, Pham Q, et al. Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection [J]. J Immunol, 2011, 187(11): 5510-5514.
[15] Casey KA, Fraser KA, Schenkel JM, et al. Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues [J]. J Immunol, 2012, 188(10): 4866-4875.
[16] Shin H, Iwasaki A. Tissue-resident memory T cells [J]. Immunol Rev, 2013, 255(1): 165-181.
[17] Intlekofer AM, Takemoto N, Wherry EJ, et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin [J]. Nat Immunol, 2005, 6(12): 1236-1244.
[18] Bromley SK, Thomas SY, Luster AD. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics [J]. Nat Immunol, 2005, 6(9): 895-901.
[19] Skon CN, Lee JY, Anderson KG, et al. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells [J]. Nat Immunol, 2013, 14(12): 1285-1293.
[20] Mackay LK, Braun A, Macleod BL, et al. Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention [J]. J Immunol, 2015, 194(5): 2059-2063.
[21] Mackay LK, Rahimpour A, Ma JZ, et al. The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin [J]. Nat Immunol, 2013, 14(12): 1294-1301. doi: 10.1038/ni.2744.
[22] Stelma F, De Niet A, Sinnige MJ, et al. Human intrahepatic CD69 + CD8+ T cells have a tissue resident memory T cell phenotype with reduced cytolytic capacity [J]. Sci Rep, 2017, 7(1): 6172. doi: 10.1038/s41598-017-06352-3.
[23] Ma C, Mishra S, Demel EL, et al. TGF-beta controls the formation of kidney-resident T cells via promoting effector T cell extravasation [J]. J Immunol, 2017, 198(2): 749-756.
[24] Soukou S, Huber S, Krebs CF. T cell plasticity in renal autoimmune disease [J]. Cell Tissue Res, 2021,1-11. doi: 10.1007/s00441-021-03466-z.
[25] Suarez-Fueyo A, Bradley SJ, Klatzmann D, et al. T cells and autoimmune kidney disease [J]. Nat Rev Nephrol, 2017, 13(6): 329-343.
[26] Li Q, Wang Z, Zhang Y, et al. NLRC5 deficiency protects against acute kidney injury in mice by mediating carcinoembryonic antigen-related cell adhesion molecule 1 signaling [J]. Kidney Int, 2018, 94(3): 551-566.
[27] Cibrian D, Sanchez-Madrid F. CD69: from activation marker to metabolic gatekeeper [J]. Eur J Immunol, 2017, 47(6): 946-953.
[28] Topham DJ, Reilly EC. Tissue-resident memory CD8+T cells: from phenotype to function [J]. Front Immunol, 2018, 9: 515. doi: 10.3389/fimmu.2018.00515.
[29] Van Der Putten C, Remmerswaal EBM, Terpstra ML, et al. CD8 and CD4 T Cell Populations in Human Kidneys [J]. Cells, 2021, 10(2):288. doi: 10.3390/cells10020288.
[30] Dornieden T, Sattler A, Pascual-Reguant A, et al. Signatures and specificity of tissue-resident lymphocytes identified in human renal peri-tumor and tumor tissue [J]. J Am Soc Nephrol, 2021, 32(9):2223-2241.
[31] Mackay LK, Minnich M, Kragten NA, et al. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes [J]. Science, 2016, 352(6284): 459- 463.
[32] Milner JJ, Toma C, Yu B, et al. Runx3 programs CD8+T cell residency in non-lymphoid tissues and tumours [J]. Nature, 2017, 552(7684): 253-257.
[33] Van Aalderen MC, Remmerswaal EB, Heutinck KM, et al. 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 [J]. PLoS Pathog, 2016, 12(10): e1005903. doi: 10.1371/journal.ppat.1005903.
[34] Iijima N, Iwasaki A. Tissue instruction for migration and retention of TRM cells [J]. Trends Immunol, 2015, 36(9): 556-564.
[35] Turner JE, Becker M, Mittrucker HW, et al. Tissue-resident lymphocytes in the kidney [J]. J Am Soc Nephrol, 2018, 29(2): 389-399.
[36] Mackay LK, Wynne-Jones E, Freestone D, et al. T-box transcription factors combine with the cytokines TGF-beta and IL-15 to control tissue-resident memory T cell fate [J]. Immunity, 2015, 43(6): 1101-1111.
[37] Jabri B, Abadie V. IL-15 functions as a danger signal to regulate tissue-resident T cells and tissue destruction [J]. Nat Rev Immunol, 2015, 15(12): 771-783.
[38] Pallett LJ, Davies J, Colbeck EJ, et al. IL-2(high)tissue-resident T cells in the human liver: Sentinels for hepatotropic infection [J]. J Exp Med, 2017, 214(6): 1567-1580.
[39] Weiler M, Rogashev B, Einbinder T, et al. Interleukin-15, a leukocyte activator and growth factor, is produced by cortical tubular epithelial cells [J]. J Am Soc Nephrol, 1998, 9(7): 1194-1201.
[40] Schenkel JM, Fraser KA, Casey KA, et al. IL-15-Independent maintenance of tissue-resident and boosted effector memory CD8 T cells [J]. J Immunol, 2016, 196(9): 3920-3926.
[41] Li MO, Flavell RA. TGF-beta: a master of all T cell trades [J]. Cell, 2008, 134(3): 392-404.
[42] Zhou M, Guo C, Li X, et al. JAK/STAT signaling controls the fate of CD8+CD103+ tissue-resident memory T cell in lupus nephritis [J]. J Autoimmun, 2020, 109: 102424. doi: 10.1016/j.jaut.2020.102424.
[43] Wu H, Liao W, Li Q, et al. Pathogenic role of tissue-resident memory T cells in autoimmune diseases [J]. Autoimmun Rev, 2018, 17(9): 906-911.
[44] Willemsen M, Linkute R, Luiten RM, et al. Skin-resident memory T cells as a potential new therapeutic target in vitiligo and melanoma [J]. Pigment Cell Melanoma Res, 2019, 32(5): 612-622.
[45] Park S, Park J, Kim E, et al. The capicua/ETS translocation variant 5 axis regulates liver-resident memory CD8+T-cell development and the pathogenesis of liver injury [J]. Hepatology, 2019, 70(1): 358-371.
[46] Jung J, Lee JS, Kim YG, et al. Synovial fluid CD69+CD8+ T cells with tissue-resident phenotype mediate perforin-dependent citrullination in rheumatoid arthritis [J]. Clin Transl Immunology, 2020, 9(6): e1140. doi: 10.1002/cti2.1140.
[47] Winchester R, Wiesendanger M, Zhang HZ, et al. Immunologic characteristics of intrarenal T cells: trafficking of expanded CD8+ T cell beta-chain clonotypes in progressive lupus nephritis [J]. Arthritis Rheum, 2012, 64(5): 1589-1600.
[48] Zhou G, Fujio K, Sadakata A, et al. Identification of systemically expanded activated T cell clones in MRL/lpr and NZB/W F1 lupus model mice [J]. Clin Exp Immunol, 2004, 136(3): 448-455.
[49] Kato T, Kurokawa M, Sasakawa H, et al. Analysis of accumulated T cell clonotypes in patients with systemic lupus erythematosus [J]. Arthritis Rheum, 2000, 43(12): 2712-2721.
[50] Chen PM, Wilson PC, Shyer JA, et al. Kidney tissue hypoxia dictates T cell-mediated injury in murine lupus nephritis [J]. Sci Transl Med, 2020, 12(538):eaay1620. doi: 10.1126/scitranslmed.aay1620.
[51] Konstantinov KN, Ulff-Moller CJ, Tzamaloukas AH. Infections and antineutrophil cytoplasmic antibodies: triggering mechanisms [J]. Autoimmun Rev, 2015, 14(3): 201-203.
[52] Paust HJ, Turner JE, Steinmetz OM, et al. The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis [J]. J Am Soc Nephrol, 2009, 20(5): 969-979.
[53] Krebs CF, Reimers D, Zhao Y, et al. Pathogen-induced tissue-resident memory TH17(TRM17)cells amplify autoimmune kidney disease [J]. Sci Immunol, 2020, 5(50):eaba 4163. doi: 10.1126/sciimmunol.aba4163.
[54] Savas P, Virassamy B, Ye C, et al. Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis [J]. Nat Med, 2018, 24(7): 986-993.
[55] Clarke J, Panwar B, Madrigal A, et al. Single-cell transcriptomic analysis of tissue-resident memory T cells in human lung cancer [J]. J Exp Med, 2019, 216(9): 2128-2149.
[56] Park SL, Gebhardt T, Mackay LK. Tissue-resident memory T cells in cancer immunosurveillance [J]. Trends Immunol, 2019, 40(8): 735-747.
[57] Nishida K, Kawashima A, Kanazawa T, et al. Clinical importance of the expression of CD4+CD8+ T cells in renal cell carcinoma [J]. Int Immunol, 2020, 32(5): 347-357.
[58] Krishna C, Dinatale RG, Kuo F, et al. Single-cell sequencing links multiregional immune landscapes and tissue-resident T cells in ccRCC to tumor topology and therapy efficacy [J]. Cancer Cell, 2021, 39(5): 662-677.
[59] De Leur K, Dieterich M, Hesselink DA, et al. Characterization of donor and recipient CD8+ tissue-resident memory T cells in transplant nephrectomies [J]. Sci Rep, 2019, 9(1): 5984. doi: 10.1038/s41598-019-42401-9.
[60] Abou-Daya KI, Tieu R, Zhao D, et al. Resident memory T cells form during persistent antigen exposure leading to allograft rejection [J]. Sci Immunol, 2021, 6(57). doi: 10.1126/sciimmunol.abc8122.
[61] Miller BC, Sen DR, Al Abosy R, et al. Subsets of exhausted CD8(+)T cells differentially mediate tumor control and respond to checkpoint blockade [J]. Nat Immunol, 2019, 20(3): 326-336.
[62] 余思菲, 吴长有. 组织定居记忆性T细胞的免疫学特征研究进展 [J]. 中国免疫学杂志, 2017, 33(7): 1093-1100. YU Sifei, WU Changyou. Advances in the study of the immunological characteristics of tissue-resident memory T cells(in Chinese)[J]. Chinese Journal of Immunolo, 2017, 33(7): 1093-1100.
[1] . [J]. Journal of Shandong University (Health Sciences), 2020, 1(8): 123-124.
[2] . [J]. Journal of Shandong University (Health Sciences), 2018, 56(10): 119-121.
[3] XIANG Chunhong, LÜ Li, JIANG Bei, XIAO Xiaoyan, HU Zhao. Mechanism of EGCG protecting high-glucose-induced HK-2 cell apoptosis by suppressing endoplasmic reticulum stress [J]. Journal of Shandong University (Health Sciences), 2017, 55(12): 1-6.
[4] ZHOU Miao, XIA Tongyao, SUN Ailing, LI Ming, SHEN Zhenwei, BIAN Weiwei, JIANG Zheng, KANG Fengling, LIU Xiaojuan, XUE Fuzhong, LIU Jing. Risk prediction model of chronic kidney disease in health management population [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2017, 55(6): 98-103.
[5] SHEN Zhenwei, JI Xiaokang, WANG Qinglian, LI Jie, XUE Fuzhong, LIU Jing. Association between nonalcoholic fatty liver disease and chronic kidney disease: a retrospective cohort study [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2016, 54(7): 43-49.
[6] HUANG Zhilong, LIU Shuai, WANG Jianwei, HAN Liping, WANG Xiaoqing, LI Xin, BI Dongbin, XIE Fang, NIU Zhihong. Role and possible mechanism of autophagy in ubenimex-induced cell death of renal cell carcinoma [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2015, 53(9): 58-64.
[7] . [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(S2): 68-68.
[8] . [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(S2): 121-122.
[9] YANG Zhiying, LIU Xiangchun, GUAN Guangju. Expression changes of methionine sulfoxide reductase B1 in the kidneys of instreptozocin-induced diabetic mice and its relationship with oxidative stress [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(10): 29-34.
[10] . [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(8): 111-112.
[11] QUE Xinxiang, DING Sentai, WU Fei, BI Dongbin, LÜ Jiaju, DING Kejia. Expressions of TGF-β1 and α-SMA in autosomal dominant polycystic kidney disease [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(7): 78-81.
[12] ZHAO Long, GUAN Guangju. Meta-analysis for consumption of cruciferous vegetables and the morbidity risk of renal cell carcinoma [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(7): 82-89.
[13] ZHANG Jin-hang1, ZHANG Lu-wei1, LIU Xin-nong2, TIAN Jun1. Expression of Tribble3 in db/db mice  renal tissues and the possible role in renal fibrosis [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2014, 52(2): 38-43.
[14] LIU Zhao1, DING Sen-tai1, WU Hai-hu1, LI Jia-mei2, SUN Liang1, DING Ke-jia1, NIU Zhi-hong1, BI Dong-bin1, SU Jing-ran3, L Jia-ju1. Diagnosis and treatment of invasive renal parenchyma urothelial carcinoma [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2013, 51(10): 93-97.
[15] GE Jun-ke, ZHAO Sheng-tian. Protective effect of bone marrow mesenchymal stem cells and CD133+ renal cells on acute renal injury [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2013, 51(9): 55-59.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
[1] WANG Huan-liang,SUN Bao-zhu,DU Hong-mei,ZHOU Chang-qing,ZHANG Li. Controlling the depth of propofol anesthesia using the bispectral indexand the systolic blood pressure[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2006, 44(5): 471 -474 .
[2] SONG Yong-hong,MA Chun-hong,LV Hong-juan,ZHU Chuan-fu,NIE Xiang-min,WANG Mei,LIU Yan,ZHANG Ping. HLA allele polymorphism in northern Hans of China[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2007, 45(6): 546 -553 .
[3] HUANGQing,TIAN Hui,LI Lin,LIANG Fei,LIU Xi-xian. [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2006, 44(6): 556 -559 .
[4] ZHU Mei-jia,HAN Ju,WANG Xin-yi,LU Wei,WANG Ai-hua,GUAN Xin-hua,CAO Xia,CAO Bing-zhen. [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2006, 44(8): 834 -839 .
[5] HOU Xiao-yang,BU Pei-li,ZHANG Yun,FENG Jin-bo,LIU Chun-xi,LI Chuan-bao,HAO Ming-xiu. Peroxisome proliferatorsactivated receptor α play a critical role in the inhibition of myocardial fibrosis induced by AngⅡ in vitro[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2007, 45(7): 665 -668 .
[6] ZENG Ji-ping,WANG Li-na,WANG Li-xiang,REN Xiao-hui,ZHANG Meng-ye,XIA Wen,CUI Xing. [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2006, 44(5): 467 -470 .
[7] SHU Ya,QI Feng. Jaw thrust device (JTD) on obesity patients for maintaining the airway patency during general anesthesia induction[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2007, 45(10): 1072 -1074 .
[8] YU Hui1,2, CHEN Shaohua1, ZHAO Jiajun2, GAO Ling3
. Effects of ethanol on glycogen content, GSK3β，
and PAMPK of L02 cells[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2009, 47(04): 75 -78 .
[9] SONG Hai-yan, WU Yu-ling, ZHANG Yan-ping. Protective effect of oyster extract on apoptotic cells in neural tube defect induced by hyperthermia[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2007, 45(2): 113 -116 .
[10] . Susceptibilityweighted imaging of diffuse axonal injury: a correlative
study of lesionnumber and Glasgow Score Scale[J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2009, 47(10): 126 -129 .
Copyright 2018 © Editorial office of Journal of Shandong University (Health Sciences)
Supported by Beijing Magtech Co.Ltd