ABC transporters and NR4A1 identify a quiescent subset of tissue-resident memory T cells

Journal of Clinical Investigation

Volumn 126, Issue 10, 2016, Pages 3905-3916

  Boddupalli, Chandra Sekhar ^a   Nair, Shiny ^a   Gray, Simon M ^a   Nowyhed, Heba N ^b   Verma, Rakesh ^a   Gibson, Joanna A ^a   Abraham, Clara ^a   Narayan, Deepak ^a   Vasquez, Juan ^a   Hedrick, Catherine C ^b   Flavell, Richard A ^a,c   Dhodapkar, Kavita M ^a   Kaech, Susan M ^a,c   Dhodapkar, Madhav V ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; HISTONE; NUCLEAR RECEPTOR NUR77; NR4A1 PROTEIN, HUMAN; TRANSCRIPTOME;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL CYCLE G0 PHASE; CONTROLLED STUDY; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE SUBPOPULATION; ADOPTIVE TRANSFER; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGICAL MEMORY; KNOCKOUT MOUSE; METABOLISM; NONOBESE DIABETIC MOUSE; SCID MOUSE; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELLS, CULTURED; HUMANS; IMMUNOLOGIC MEMORY; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; ORGAN SPECIFICITY; RESTING PHASE, CELL CYCLE; T-LYMPHOCYTES; TRANSCRIPTOME;

EID: 84991737337     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85329     Document Type: Article

References (45)

1. Hammarlund E, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med. 2003;9(9):1131-1137.
2. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401(6754):708-712.
3. Mueller SN, Gebhardt T, Carbone FR, Heath WR. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol. 2013;31:137-161.
4. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol. 2009;10(5):524-530.
5. Schenkel JM, Masopust D. Tissue-resident memory T cells. Immunity. 2014;41(6):886-897.
6. Masopust D, Vezys V, Marzo AL, Lefrançois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science. 2001;291(5512):2413-2417.
7. Steinert EM, et al. Quantifying Memory CD8 T Cells Reveals Regionalization of Immunosurveillance. Cell. 2015;161(4):737-749.
8. Thome JJ, et al. Spatial map of human T cell compartmentalization and maintenance over decades of life. Cell. 2014;159(4):814-828.
9. Gaide O, et al. Common clonal origin of central and resident memory T cells following skin immunization. Nat Med. 2015;21(6):647-653.
10. Mackay LK, et al. The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat Immunol. 2013;14(12):1294-1301.
11. Fearon DT, Manders P, Wagner SD. Arrested differentiation, the self-renewing memory lymphocyte, and vaccination. Science. 2001;293(5528):248-250.
12. Luckey CJ, Bhattacharya D, Goldrath AW, Weissman IL, Benoist C, Mathis D. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc Natl Acad Sci U S A. 2006;103(9):3304-3309.
13. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183(4):1797-1806.
14. Weksberg DC, Chambers SM, Boles NC, Goodell MA. CD150-side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood. 2008;111(4):2444-2451.
15. Zhou S, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 2001;7(9):1028-1034.
16. Doyle MJ, et al. Abcg2 labels multiple cell types in skeletal muscle and participates in muscle regeneration. J Cell Biol. 2011;195(1):147-163.
17. Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood. 2002;99(2):507-512.
18. Fatima S, Zhou S, Sorrentino BP. Abcg2 expression marks tissue-specific stem cells in multiple organs in a mouse progeny tracking model. Stem Cells. 2012;30(2):210-221.
19. Tarling EJ, de Aguiar Vallim TQ, Edwards PA. Role of ABC transporters in lipid transport and human disease. Trends Endocrinol Metab. 2013;24(7):342-350.
20. Turtle CJ, Swanson HM, Fujii N, Estey EH, Riddell SR. A distinct subset of self-renewing human memory CD8+ T cells survives cytotoxic chemotherapy. Immunity. 2009;31(5):834-844.
21. Dusseaux M, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 2011;117(4):1250-1259.
22. Land RH, et al. The orphan nuclear receptor NR4A1 specifies a distinct subpopulation of quiescent myeloid-biased long-term HSCs. Stem Cells. 2015;33(1):278-288.
23. Sirin O, Lukov GL, Mao R, Conneely OM, Goodell MA. The orphan nuclear receptor Nurr1 restricts the proliferation of haematopoietic stem cells. Nat Cell Biol. 2010;12(12):1213-1219.
24. Liu Y, et al. p53 regulates hematopoietic stem cell quiescence. Cell Stem Cell. 2009;4(1):37-48.
25. Foudi A, et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol. 2009;27(1):84-90.
26. Wilson A, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.
27. Li J, Olshansky M, Carbone FR, Ma JZ. Transcriptional Analysis of T Cells Resident in Human Skin. PLoS ONE. 2016;11(1):e0148351.
28. Sekiya T, et al. Nr4a receptors are essential for thymic regulatory T cell development and immune homeostasis. Nat Immunol. 2013;14(3):230-237.
29. Winoto A, Littman DR. Nuclear hormone receptors in T lymphocytes. Cell. 2002;109 Suppl:S57-S66.
30. Morton AM, Sefik E, Upadhyay R, Weissleder R, Benoist C, Mathis D. Endoscopic photoconversion reveals unexpectedly broad leukocyte trafficking to and from the gut. Proc Natl Acad Sci U S A. 2014;111(18):6696-6701.
31. Alp OS, Radbruch A. The lifestyle of memory CD8(+) T cells. Nat Rev Immunol. 2016;16(4):271.
32. Sercan Alp O, et al. Memory CD8(+) T cells colocalize with IL-7(+) stromal cells in bone marrow and rest in terms of proliferation and transcription. Eur J Immunol. 2015;45(4):975-987.
33. Nakamura-Ishizu A, Takizawa H, Suda T. The analysis, roles and regulation of quiescence in hematopoietic stem cells. Development. 2014;141(24):4656-4666.
34. Allam A, et al. The CD8+ memory T-cell state of readiness is actively maintained and reversible. Blood. 2009;114(10):2121-2130.
35. Veiga-Fernandes H, Rocha B. High expression of active CDK6 in the cytoplasm of CD8 memory cells favors rapid division. Nat Immunol. 2004;5(1):31-37.
36. Liu ZG, Smith SW, McLaughlin KA, Schwartz LM, Osborne BA. Apoptotic signals delivered through the T-cell receptor of a T-cell hybrid require the immediate-early gene nur77. Nature. 1994;367(6460):281-284.
37. Nowyhed HN, Huynh TR, Thomas GD, Blatchley A, Hedrick CC. Cutting Edge: The Orphan Nuclear Receptor Nr4a1 Regulates CD8+ T Cell Expansion and Effector Function through Direct Repression of Irf4. J Immunol. 2015;195(8):3515-3519.
38. Hanna RN, et al. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C-monocytes. Nat Immunol. 2011;12(8):778-785.
39. June CH, Riddell SR, Schumacher TN. Adoptive cellular therapy: a race to the finish line. Sci Transl Med. 2015;7(280):280ps7.
40. Maus MV, Grupp SA, Porter DL, June CH. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood. 2014;123(17):2625-2635.
41. Pircher H, Bürki K, Lang R, Hengartner H, Zinkernagel RM. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature. 1989;342(6249):559-561.
42. Watanabe R, et al. Human skin is protected by four functionally and phenotypically discrete populations of resident and recirculating memory T cells. Sci Transl Med. 2015;7(279):279ra39.
43. Nair S, et al. Type II NKT-TFH cells against Gaucher lipids regulate B-cell immunity and inflammation. Blood. 2015;125(8):1256-1271.
44. Sehgal K, et al. Clinical and pharmacodynamic analysis of pomalidomide dosing strategies in myeloma: impact of immune activation and cereblon targets. Blood. 2015;125(26):4042-4051.
45. Das R, et al. Combination therapy with anti-CTLA-4 and anti-PD-1 leads to distinct immunologic changes in vivo. J Immunol. 2015;194(3):950-959.