CXCR5+ follicular cytotoxic T cells control viral infection in B cell follicles

Nature Immunology

Volumn 17, Issue 10, 2016, Pages 1187-1196

  Leong, Yew Ann ^a   Chen, Yaping ^a   Ong, Hong Sheng ^a   Wu, Di ^b   Man, Kevin ^c,d   Deleage, Claire ^e   Minnich, Martina ^f   Meckiff, Benjamin J ^g   Wei, Yunbo ^h   Hou, Zhaohua ^h   Zotos, Dimitra ^c,d   Fenix, Kevin A ⁱ   Atnerkar, Anurag ^a   Preston, Simon ^c,d   Chipman, Jeffrey G ^j   Beilman, Greg J ^j   Allison, Cody C ^c,d   Sun, Lei ^k   Wang, Peng ^k   Xu, Jiawei ^l   Toe, Jesse G ^c,d   Lu, Hao K ^d   Tao, Yong ^m   Palendira, Umaimainthan ⁿ   Dent, Alexander L ^o   Landay, Alan L ^p   Pellegrini, Marc ^c,d   Comerford, Iain ⁱ   McColl, Shaun R ⁱ   Schacker, Timothy W ^j   Long, Heather M ^g   Estes, Jacob D ^e   Busslinger, Meinrad ^f   Belz, Gabrielle T ^c,d   Lewin, Sharon R ^d,q   Kallies, Axel ^c,d   Yu, Di ^a,h,q   more..

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^f RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^g UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^h QILU UNIVERSITY OF TECHNOLOGY   (China)

ⁱ UNIVERSITY OF ADELAIDE   (Australia)

^j UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^k CAPITAL MEDICAL UNIVERSITY   (China)

^l The University of North Carolina at Chapel Hill   (United States)

^m CAPITAL MEDICAL UNIVERSITY   (China)

ⁿ CENTENARY INSTITUTE   (Australia)

^o INDIANA UNIVERSITY   (United States)

^p RUSH UNIVERSITY MEDICAL CENTER   (United States)

^q MONASH UNIVERSITY   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CHEMOKINE RECEPTOR CXCR5; INHIBITOR OF DIFFERENTIATION 2; INHIBITOR OF DIFFERENTIATION 3; PROTEIN BCL 6; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR E2A; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BCL6 PROTEIN, MOUSE; CXCR5 PROTEIN, HUMAN; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HNF1A PROTEIN, MOUSE; PRDM1 PROTEIN, MOUSE; TCF3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CXCR5 GENE; CYTOTOXIC T LYMPHOCYTE; FOLLICULAR CYTOTOXIC T CELL; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; INFECTION CONTROL; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR GENE; TRANSCRIPTION REGULATION; VIRUS INFECTION; ANIMAL; ARENAVIRUS INFECTION; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; EPSTEIN BARR VIRUS INFECTION; GENETICS; GERMINAL CENTER; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; ARENAVIRIDAE INFECTIONS; B-LYMPHOCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION REGULATION; GERMINAL CENTER; HEPATOCYTE NUCLEAR FACTOR 1-ALPHA; HIV; HUMANS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-BCL-6; RECEPTORS, CXCR5; T-LYMPHOCYTES, CYTOTOXIC; TRANSCRIPTION FACTORS;

EID: 84981285538     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3543     Document Type: Article

References (62)

1. Mueller, S.N., Gebhardt, T., Carbone, F.R., & Heath, W.R. Memory T cell subsets, migra tion patterns, and tissue residence. Annu. Rev. Immunol. 31, 137-161 (2013).
2. Vinuesa, C.G., Linterman, M.A., Yu, D., & MacLennan, I.C. Follicular helper T cells. Annu. Rev. Immunol. 34, 335-368 (2016
3. Barton, E., Mandal, P., & Speck, S.H. Pathogenesis and host control of gammaherpes viruses: lessons from the mouse. Annu. Rev. Immunol. 29, 351-397 (2011).
4. Lindqvist, M., et al. Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J. Clin. Invest. 122, 3271-3280 (2012).
5. Petrovas, C., et al. CD4 T follicular helper cell dynamics during SIV infection. J. Clin. Invest. 122, 3281-3294 (2012).
6. Perreau, M., et al. Follicular helper T cells serve as the major CD4 T cell compart ment for HIV-1 infection, replication, and production. J. Exp. Med. 210, 143-156 (2013).
7. Pissani, F., & Streeck, H. Emerging concepts on T follicular helper cell dynamics in HIV infection. Trends Immunol. 35, 278-286 (2014).
8. Banga, R., et al. PD-1+ and follicular helper T cells are responsible for persis tent HIV-1 transcription in treated aviremic individuals. Nat. Med. 22, 754-761 (2016).
9. Kaech, S.M., & Cui, W. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 12, 749-761 (2012).
10. Chang, J.T., Wherry, E.J., & Goldrath, A.W. Molecular regulation of effector and memory T cell differentiation. Nat. Immunol. 15, 1104-1115 (2014).
11. Wherry, E.J., & Kurachi, M. Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 15, 486-499 (2015).
12. Paley, M.A., et al. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science 338, 1220-1225 (2012).
13. Shin, H., et al. A role for the transcriptional repressor Blimp-1 in CD8+ T cell exhaustion during chronic viral infection. Immunity 31, 309-320 (2009).
14. Kao, C., et al. Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat. Immunol. 12, 663-671 (2011).
15. Masopust, D., & Schenkel, J.M. The integration of T cell migration, differentiation and function. Nat. Rev. Immunol. 13, 309-320 (2013).
16. Griffith, J.W., Sokol, C.L., & Luster, A.D. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32, 659-702 (2014).
17. Sallusto, F. Heterogeneity of human CD4+ T cells against microbes. Annu. Rev. Immunol. 34, 317-334 (2016).
18. Vinuesa, C.G., & Cyster, J.G. How T cells earn the follicular rite of passage. Immunity 35, 671-680 (2011).
19. Weinmann, A.S. Regulatory mechanisms that control T-follicular helper and T-helper 1 cell flexibility. Immunol. Cell Biol. 92, 34-39 (2014).
20. Hong, J.J., Amancha, P.K., Rogers, K., Ansari, A.A., & Villinger, F. Spatial alterations between CD4+ T follicular helper, B, and CD8+ T cells during simian immunodeficiency virus infection: T/B cell homeostasis, activation, and potential mechanism for viral escape. J. Immunol. 188, 3247-3256 (2012).
21. Fukazawa, Y., et al. B cell follicle sanctuary permits persistent productive simian immu nodeficiency virus infection in elite controllers. Nat. Med. 21, 132-139 (2015).
22. Quigley, M.F., Gonzalez, V.D., Granath, A., Andersson, J., & Sandberg, J.K. CXCR5+ CCR7-CD8 T cells are early effector memory cells that infiltrate tonsil B cell follicles. Eur. J. Immunol. 37, 3352-3362 (2007).
23. Zhou, X., Ramachandran, S., Mann, M., & Popkin, D.L. Role of lymphocytic chorio meningitis virus (LCMV) in understanding viral immunology: past, present and future. Viruses 4, 2650-2669 (2012).
24. Kyburz, D., et al. T cell immunity after a viral infection versus T cell tolerance induced by soluble viral peptides. Eur. J. Immunol. 23, 1956-1962 (1993).
25. Hogquist, K.A., et al. T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27 (1994).
26. Homann, D., McGavern, D.B., & Oldstone, M.B. Visualizing the viral burden: phenotypic and functional alterations of T cells and APCs during persistent infection. J. Immunol. 172, 6239-6250 (2004
27. Baca Jones, C., et al. Direct infection of dendritic cells during chronic viral infection suppresses antiviral T cell proliferation and induces IL-10 expression in CD4 T cells. PLoS One 9, e90855 (2014).
28. Oxenius, A., Bachmann, M.F., Zinkernagel, R.M., & Hengartner, H. Virus-specific MHC-class II-restricted TCR-Transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 28, 390-400 (1998).
29. Afshar-Sterle, S., et al. Fas ligand-mediated immune surveillance by T cells is essential for the control of spontaneous B cell lymphomas. Nat. Med. 20, 283-290 (2014).
30. Gaspar, M., et al. Murid herpesvirus-4 exploits dendritic cells to infect B cells. PLoS Pathog. 7, e1002346 (2011).
31. Kim, H.J., Verbinnen, B., Tang, X., Lu, L., & Cantor, H. Inhibition of follicular T-helper cells by CD8+ regulatory T cells is essential for self tolerance. Nature 467, 328-332 (2010).
32. Johnston, R.J., et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325, 1006-1010 (2009).
33. Nurieva, R.I., et al. Bcl6 mediates the development of T follicular helper cells. Science 325, 1001-1005 (2009).
34. Yu, D., et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31, 457-468 (2009).
35. Miyazaki, M., et al. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat. Immunol. 12, 992-1001 (2011).
36. Choi, Y.S., et al. LEF-1 and TCF-1 orchestrate TFH differentiation by regulating differ entiation circuits upstream of the transcriptional repressor Bcl6. Nat. Immunol. 16, 980-990 (2015).
37. Wu, T., et al. TCF1 is required for the T follicular helper cell response to viral infection. Cell Reports 12, 2099-2110 (2015).
38. Xu, L., et al. The transcription factor TCF-1 initiates the differentiation of TFH cells during acute viral infection. Nat. Immunol. 16, 991-999 (2015).
39. Shaw, L.A., et al. Id2 reinforces TH1 differentiation and inhibits E2A to repress TFH differentiation. Nat. Immunol. 17, 834-843 (2016).
40. Xin, A., et al. A combinatorial threshold model for effector differentiation of CD8+ T cells mediated by Blimp-1 and T-bet. Nat. Immunol. 17, 422-432 (2016).
41. Chen, Y., & Yu, D. TCF-1 at the Tfh and Th1 Divergence. Trends Immunol. 36, 758-760 (2015).
42. Ji, Y., et al. Repression of the DNA-binding inhibitor Id3 by Blimp-1 limits the formation of memory CD8+ T cells. Nat. Immunol. 12, 1230-1237 (2011).
43. Masson, F., et al. Id2-mediated inhibition of E2A represses memory CD8+ T cell dif ferentiation. J. Immunol. 190, 4585-4594 (2013).
44. Hatzi, K., et al. BCL6 orchestrates Tfh cell differentiation via multiple distinct mecha nisms. J. Exp. Med. 212, 539-553 (2015).
45. Liu, X., et al. Genome-wide analysis identifies Bcl6-controlled regulatory networks during T follicular helper cell differentiation. Cell Rep. 14, 1735-1747 (2016).
46. Shaffer, A.L., et al. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17, 51-62 (2002).
47. Oestreich, K.J., Mohn, S.E., & Weinmann, A.S. Molecular mechanisms that control the expression and activity of Bcl-6 in TH1 cells to regulate flexibility with a TFH-like gene profile. Nat. Immunol. 13, 405-411 (2012).
48. Kallies, A., Xin, A., Belz, G.T., & Nutt, S.L. Blimp-1 transcription factor is required for the differentiation of effector CD8+ T cells and memory responses. Immunity 31, 283-295 (2009).
49. Rutishauser, R.L., et al. Transcriptional repressor Blimp-1 promotes CD8+ T cell termi nal differentiation and represses the acquisition of central memory T cell properties. Immunity 31, 296-308 (2009).
50. Mackay, L.K., et al. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352, 459-463 (2016
51. Junying, J., et al. Absence of Epstein-Barr virus DNA in the tumor cells of European hepatocellular carcinoma. Virology 306, 236-243 (2003).
52. Hollister, K., et al. Insights into the role of Bcl6 in follicular Th cells using a new con ditional mutant mouse model. J. Immunol. 191, 3705-3711 (2013).
53. Steinke, F.C., et al. TCF-1 and LEF-1 act upstream of Th-POK to promote the CD4+ T cell fate and interact with Runx3 to silence Cd4 in CD8+ T cells. Nat. Immunol. 15, 646-656 (2014).
54. Kallies, A., et al. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 200, 967-977 (2004).
55. Jackson, J.T., et al. Id2 expression delineates differential checkpoints in the genetic program of CD8a+ and CD103+ dendritic cell lineages. EMBO J. 30, 2690-2704 (2011).
56. Lüthje, K., et al. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat. Immunol. 13, 491-498 (2012).
57. Minnich, M., et al. Multifunctional role of the transcription factor Blimp-1 in coordinat ing plasma cell differentiation. Nat. Immunol. 17, 331-343 (2016).
58. Korns Johnson, D., & Homann, D. Accelerated and improved quantification of lym phocytic choriomeningitis virus (LCMV) titers by flow cytometry. PLoS One 7, e37337 (2012).
59. Hislop, A.D., Annels, N.E., Gudgeon, N.H., Leese, A.M., & Rickinson, A.B. Epitope-specific evolution of human CD8+ T cell responses from primary to persistent phases of Epstein-Barr virus infection. J. Exp. Med. 195, 893-905 (2002).
60. Deleage, C., et al. Defining HIV and SIV reservoirs in lymphoid tissues. Pathog. Immun. 1, 68-106 (2016).
61. Jedema, I., van der Werff, N.M., Barge, R.M., Willemze, R., & Falkenburg, J.H. New CFSE-based assay to determine susceptibility to lysis by cytotoxic T cells of leukemic precursor cells within a heterogeneous target cell population. Blood 103, 2677-2682 (2004).
62. Xing, S., et al. Tcf1 and Lef1 transcription factors establish CD8+ T cell identity through intrinsic HDAC activity. Nat. Immunol. 17, 695-703 (2016