Quantifying memory CD8 T cells reveals regionalization of immunosurveillance

Cell

Volumn 161, Issue 4, 2015, Pages 737-749

  Steinert, Elizabeth M ^a,b   Schenkel, Jason M ^a,b   Fraser, Kathryn A ^a,b   Beura, Lalit K ^a,b   Manlove, Luke S ^b   Igyártó, Botond Z ^a,b   Southern, Peter J ^a   Masopust, David ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; LECTIN; LEUKOCYTE ANTIGEN; T LYMPHOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOSURVEILLANCE; INFLAMMATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ARENAVIRUS INFECTION; C57BL MOUSE; CELL MOTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL MONITORING; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; METABOLISM; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ARENAVIRIDAE INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; IMMUNOLOGIC MEMORY; INFLAMMATION; LECTINS, C-TYPE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MONITORING, IMMUNOLOGIC; T-LYMPHOCYTE SUBSETS;

EID: 84928904487     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.03.031     Document Type: Article

References (46)

1. J.D. Altman, P.A. Moss, P.J. Goulder, D.H. Barouch, M.G. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis Phenotypic analysis of antigen-specific T lymphocytes Science 274 1996 94 96
2. K.G. Anderson, K. Mayer-Barber, H. Sung, L. Beura, B.R. James, J.J. Taylor, L. Qunaj, T.S. Griffith, V. Vezys, D.L. Barber, and D. Masopust Intravascular staining for discrimination of vascular and tissue leukocytes Nat. Protoc. 9 2014 209 222
3. K.A. Casey, K.A. Fraser, J.M. Schenkel, A. Moran, M.C. Abt, L.K. Beura, P.J. Lucas, D. Artis, E.J. Wherry, and K. Hogquist Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues J. Immunol. 188 2012 4866 4875
4. R.A. Clark, B. Chong, N. Mirchandani, N.K. Brinster, K. Yamanaka, R.K. Dowgiert, and T.S. Kupper The vast majority of CLA+ T cells are resident in normal skin J. Immunol. 176 2006 4431 4439
5. M.K. Collins, C.-S. Tay, and A. Erlebacher Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice J. Clin. Invest. 119 2009 2062 2073
6. T.E. Decoursey, K.G. Chandy, S. Gupta, and M.D. Cahalan Mitogen induction of ion channels in murine T lymphocytes J. Gen. Physiol. 89 1987 405 420
7. R.B. Doctor, N.J. Serkova, K.M. Hasebroock, I. Zafar, and C.L. Edelstein Distinct patterns of kidney and liver cyst growth in pkd2(WS25/-) mice Nephrol. Dial. Transplant. 25 2010 3496 3504
8. M. dos Anjos Pires, C. Palmeira, P. Rodrigues, C. Lopes, and F. Oliveira-Torres Establishment of a diploid reference value for DNA ploidy analysis by image cytometry in mouse cells Anal. Quant. Cytol. Histol. 23 2001 427 432
9. D.L. Farber, N.A. Yudanin, and N.P. Restifo Human memory T cells: generation, compartmentalization and homeostasis Nat. Rev. Immunol. 14 2014 24 35
10. + T cells into the interstitium of the normal lung J. Clin. Invest. 115 2005 3473 3483
11. V.V. Ganusov, and R.J. De Boer Do most lymphocytes in humans really reside in the gut? Trends Immunol. 28 2007 514 518
12. T. Gebhardt, L.M. Wakim, L. Eidsmo, P.C. Reading, W.R. Heath, and F.R. Carbone Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus Nat. Immunol. 10 2009 524 530
13. J.E. Horbul, S.C. Schmechel, B.R. Miller, S.A. Rice, and P.J. Southern Herpes simplex virus-induced epithelial damage and susceptibility to human immunodeficiency virus type 1 infection in human cervical organ culture PLoS ONE 6 2011 e22638 10.1371/journal.pone.0022638
14. X. Jiang, R.A. Clark, L. Liu, A.J. Wagers, R.C. Fuhlbrigge, and T.S. Kupper Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity Nature 483 2012 227 231
15. D.R. Kaufman, J. Liu, A. Carville, K.G. Mansfield, M.J.E. Havenga, J. Goudsmit, and D.H. Barouch Trafficking of antigen-specific CD8+ T lymphocytes to mucosal surfaces following intramuscular vaccination J. Immunol. 181 2008 4188 4198
16. K.M. Khanna, J.T. McNamara, and L. Lefrançois In situ imaging of the endogenous CD8 T cell response to infection Science 318 2007 116 120
17. K.D. Klonowski, K.J. Williams, A.L. Marzo, D.A. Blair, E.G. Lingenheld, and L. Lefrançois Dynamics of blood-borne CD8 memory T cell migration in vivo Immunity 20 2004 551 562
18. Y.T. Lee, J.E. Suarez-Ramirez, T. Wu, J.M. Redman, K. Bouchard, G.A. Hadley, and L.S. Cauley Environmental and antigen receptor-derived signals support sustained surveillance of the lungs by pathogen-specific cytotoxic T lymphocytes J. Virol. 85 2011 4085 4094
19. L. Liu, R.C. Fuhlbrigge, K. Karibian, T. Tian, and T.S. Kupper Dynamic programming of CD8+ T cell trafficking after live viral immunization Immunity 25 2006 511 520
20. L.K. Mackay, A. Rahimpour, J.Z. Ma, N. Collins, A.T. Stock, M.-L. Hafon, J. Vega-Ramos, P. Lauzurica, S.N. Mueller, and T. Stefanovic The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin Nat. Immunol. 14 2013 1294 1301
21. A.L. Marzo, K.D. Klonowski, A. Le Bon, P. Borrow, D.F. Tough, and L. Lefrançois Initial T cell frequency dictates memory CD8+ T cell lineage commitment Nat. Immunol. 6 2005 793 799
22. D. Masopust, and J.M. Schenkel The integration of T cell migration, differentiation and function Nat. Rev. Immunol. 13 2013 309 320
23. D. Masopust, V. Vezys, A.L. Marzo, and L. Lefrançois Preferential localization of effector memory cells in nonlymphoid tissue Science 291 2001 2413 2417
24. D. Masopust, V. Vezys, E.J. Usherwood, L.S. Cauley, S. Olson, A.L. Marzo, R.L. Ward, D.L. Woodland, and L. Lefrançois Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin J. Immunol. 172 2004 4875 4882
25. D. Masopust, V. Vezys, E.J. Wherry, D.L. Barber, and R. Ahmed Cutting edge: gut microenvironment promotes differentiation of a unique memory CD8 T cell population J. Immunol. 176 2006 2079 2083
26. D. Masopust, D. Choo, V. Vezys, E.J. Wherry, J. Duraiswamy, R. Akondy, J. Wang, K.A. Casey, D.L. Barber, and K.S. Kawamura Dynamic T cell migration program provides resident memory within intestinal epithelium J. Exp. Med. 207 2010 553 564
27. S.N. Mueller, T. Gebhardt, F.R. Carbone, and W.R. Heath Memory T cell subsets, migration patterns, and tissue residence Annu. Rev. Immunol. 31 2013 137 161
28. K. Murali-Krishna, J.D. Altman, M. Suresh, D.J. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection Immunity 8 1998 177 187
29. Y. Nakanishi, B. Lu, C. Gerard, and A. Iwasaki CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help Nature 462 2009 510 513
30. R.L. Nutter, D.S. Gridley, J.M. Slater, and P.J. McMillan Responses of mouse spleen morphology to the growth of subcutaneously injected virally transformed cells Anat. Rec. 197 1980 363 368
31. L. Peaudecerf, and B. Rocha Role of the gut as a primary lymphoid organ Immunol. Lett. 140 2011 1 6
32. R.L. Reinhardt, A. Khoruts, R. Merica, T. Zell, and M.K. Jenkins Visualizing the generation of memory CD4 T cells in the whole body Nature 410 2001 101 105
33. B. Rocha, P. Vassalli, and D. Guy-Grand The V beta repertoire of mouse gut homodimeric alpha CD8+ intraepithelial T cell receptor alpha/beta + lymphocytes reveals a major extrathymic pathway of T cell differentiation J. Exp. Med. 173 1991 483 486
34. F. Sallusto, D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia Two subsets of memory T lymphocytes with distinct homing potentials and effector functions Nature 401 1999 708 712
35. L.F. Scheller, R.A. Wirtz, and A.F. Azad Susceptibility of different strains of mice to hepatic infection with Plasmodium berghei Infect. Immun. 62 1994 4844 4847
36. J.M. Schenkel, K.A. Fraser, V. Vezys, and D. Masopust Sensing and alarm function of resident memory CD8 T cells Nat. Immunol. 14 2013 509 513
37. J.M. Schenkel, K.A. Fraser, and D. Masopust Cutting edge: resident memory CD8 T cells occupy frontline niches in secondary lymphoid organs J. Immunol. 192 2014 2961 2964
38. W.S. Selby, G. Janossy, M. Bofill, and D.P. Jewell Intestinal lymphocyte subpopulations in inflammatory bowel disease: an analysis by immunohistological and cell isolation techniques Gut 25 1984 32 40
39. H. Shin, and A. Iwasaki A vaccine strategy that protects against genital herpes by establishing local memory T cells Nature 491 2012 463 467
40. C.N. Skon, J.Y. Lee, K.G. Anderson, D. Masopust, K.A. Hogquist, and S.C. Jameson Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells Nat. Immunol. 14 2013 1285 1293
41. P.K. Suvas, H.M. Dech, F. Sambira, J. Zeng, and T.M. Onami Systemic and mucosal infection program protective memory CD8 T cells in the vaginal mucosa J. Immunol. 179 2007 8122 8127
42. J.R. Teijaro, D. Turner, Q. Pham, E.J. Wherry, L. Lefrançois, and D.L. Farber Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection J. Immunol. 187 2011 5510 5514
43. J.J.C. Thome, N. Yudanin, Y. Ohmura, M. Kubota, B. Grinshpun, T. Sathaliyawala, T. Kato, H. Lerner, Y. Shen, and D.L. Farber Spatial map of human T cell compartmentalization and maintenance over decades of life Cell 159 2014 814 828
44. W. Van den Broeck, A. Derore, and P. Simoens Anatomy and nomenclature of murine lymph nodes: Descriptive study and nomenclatory standardization in BALB/cAnNCrl mice J. Immunol. Methods 312 2006 12 19
45. E.J. Wherry, V. Teichgräber, T.C. Becker, D. Masopust, S.M. Kaech, R. Antia, U.H. von Andrian, and R. Ahmed Lineage relationship and protective immunity of memory CD8 T cell subsets Nat. Immunol. 4 2003 225 234
46. RM) are indispensable for optimal cross-protection against pulmonary virus infection J. Leukoc. Biol. 95 2014 215 224