Follicular Helper T Cells are Essential for the Elimination of Plasmodium Infection

EBioMedicine

Volumn 24, Issue , 2017, Pages 216-230

  Pérez Mazliah, Damián ^a   Nguyen, Minh Phuong ^a   Hosking, Caroline ^a   McLaughlin, Sarah ^a   Lewis, Matthew D ^a   Tumwine, Irene ^a   Levy, Prisca ^a   Langhorne, Jean ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

Follicular helper T (Tfh) cells; GC B cells; Plasmodium; Signaling Lymphocyte Activation Molecule (SLAM) Associated Protein (SAP); Vector transmission

Indexed keywords

CD19 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 21; PROTEIN BCL 6; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; TRANSCRIPTION FACTOR; BCL6 PROTEIN, MOUSE; IMMUNOGLOBULIN G;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BCL6 GENE; CONTROLLED STUDY; DISEASE TRANSMISSION; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; FEMALE; FLOW CYTOMETRY; GENE; GERMINAL CENTER; GIEMSA STAIN; MOSQUITO BITE; MOUSE; NONHUMAN; PLASMODIUM CHABAUDI; PLASMODIUM CHABAUDI INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TFH CELL; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; FOLLICULAR DENDRITIC CELL; GENE DELETION; GENETICS; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALARIA; METABOLISM;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DENDRITIC CELLS, FOLLICULAR; GENE DELETION; IMMUNOGLOBULIN G; LYMPHOCYTE ACTIVATION; MALARIA; MICE; MICE, INBRED C57BL; PLASMODIUM CHABAUDI; PROTO-ONCOGENE PROTEINS C-BCL-6; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 85028855812     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2017.08.030     Document Type: Article

References (67)

1. Achtman, A.H., et al. Plasmodium chabaudi chabaudi infection in mice induces strong B cell responses and striking but temporary changes in splenic cell distribution. J. Immunol. 171:1 (2003), 317–324.
2. Achtman, A.H., et al. Malaria-specific antibody responses and parasite persistence after infection of mice with Plasmodium chabaudi chabaudi. Parasite Immunol. 29:9 (2007), 435–444.
3. Allen, C.D.C., Okada, T., Cyster, J.G., Germinal-center organization and cellular dynamics. Immunity 27:2 (2007), 190–202.
4. Bauquet, A.T., et al. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat. Immunol. 10:2 (2009), 167–175.
5. Breitfeld, D., et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J. Exp. Med. 192:11 (2000), 1545–1552.
6. Burns, J.M., Dunn, P.D., Russo, D.M., Protective immunity against Plasmodium yoelii malaria induced by immunization with particulate blood-stage antigens. Infect. Immun. 65:8 (1997), 3138–3145.
7. Butler, N.S., et al. Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nat. Immunol. 13:2 (2012), 188–195.
8. Cannons, J.L., et al. SAP regulates T cell–mediated help for humoral immunity by a mechanism distinct from cytokine regulation. J. Exp. Med. 203:6 (2006), 1551–1565.
9. Cannons, J.L., et al. Optimal germinal center responses require a multistage T cell: B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32:2 (2010), 253–265.
10. Cannons, J.L., Tangye, S.G., Schwartzberg, P.L., SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 29 (2011), 665–705.
11. Carpio, V.H., et al. IFN-γ and IL-21 double producing T cells are Bcl6-independent and survive into the memory phase in plasmodium chabaudi infection. PLoS One, 10(12), 2015, e0144654.
12. Choi, Y.S., et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34:6 (2011), 932–946.
13. Cohen, S., et al. Gamma-globulin and acquired immunity to human malaria. Nature 192 (1961), 733–737.
14. Conway, D.J., et al. A principal target of human immunity to malaria identified by molecular population genetic and immunological analyses. Nat. Med. 6:6 (2000), 689–692.
15. Crotty, S., T follicular helper cell differentiation, function, and roles in disease. Immunity 41:4 (2014), 529–542.
16. Crotty, S., et al. SAP is required for generating long-term humoral immunity. Nature 421:6920 (2003), 282–287.
17. Crotty, S., et al. Hypogammaglobulinemia and exacerbated CD8 T-cell-mediated immunopathology in SAP-deficient mice with chronic LCMV infection mimics human XLP disease. Blood 108:9 (2006), 3085–3093.
18. Czar, M.J., et al. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc. Natl. Acad. Sci. U. S. A. 98:13 (2001), 7449–7454.
19. Deenick, E.K., et al. Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 33:2 (2010), 241–253.
20. Fowkes, F.J.I., et al. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Med., 7(1), 2010, e1000218.
21. Hansen, D.S., et al. Emerging concepts in T follicular helper cell responses to malaria. Int. J. Parasitol. 47:2–3 (2017), 105–110.
22. Hiramatsu, Y., et al. c-Maf activates the promoter and enhancer of the IL-21 gene, and TGF-beta inhibits c-Maf-induced IL-21 production in CD4 + T cells. J. Leukoc. Biol. 87:4 (2010), 703–712.
23. Hu, J., Havenar-Daughton, C., Crotty, S., Modulation of SAP dependent T:B cell interactions as a strategy to improve vaccination. Curr. Opin. Virol. 3:3 (2013), 363–370.
24. Johnston, R.J., et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science (New York, N.Y.) 325:5943 (2009), 1006–1010.
25. Kaji, T., Ishige, A., Hikida, M., Taka, J., Hijikata, A., Kubo, M., Nagashima, T., Takahashi, Y., Kurosaki, T., Okada, M., Ohara, O., Rajewsky, K., Takemori, T., Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J. Exp. Med. 209:11 (2012), 2079–2097.
26. Kamperschroer, C., et al. SAP is required for Th cell function and for immunity to influenza. J. Immunol. 177:8 (2006), 5317–5327.
27. Kerfoot, S.M., et al. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 34:6 (2011), 947–960.
28. Kim, C.H., et al. Subspecialization of CXCR5 + T cells: B helper activity is focused in a germinal center-localized subset of CXCR5 + T cells. J. Exp. Med. 193:12 (2001), 1373–1381.
29. Kroenke, M.A., et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J. Immunol. 188:8 (2012), 3734–3744.
30. Langhorne, J., et al. Frequencies of CD4 + T cells reactive with Plasmodium chabaudi chabaudi: distinct response kinetics for cells with Th1 and Th2 characteristics during infection. Int. Immunol. 1:4 (1989), 416–424.
31. Lee, P.P., et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15:5 (2001), 763–774.
32. Lee, S.K., et al. B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J. Exp. Med. 208:7 (2011), 1377–1388.
33. Linterman, M.A., et al. Foxp3 + follicular regulatory T cells control the germinal center response. Nat. Med. 17:8 (2011), 975–982.
34. Liu, X., et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. J. Exp. Med. 31:3 (2009), 457–468.
35. Liu, D., et al. T-B-cell entanglement and ICOSL-driven feed-forward regulation of germinal centre reaction. Nature 517:7533 (2015), 214–218.
36. Matar, C.G., et al. Gammaherpesvirus co-infection with malaria suppresses anti-parasitic humoral immunity. PLoS Pathog., 11(5), 2015, e1004858.
37. McCausland, M.M., et al. SAP regulation of follicular helper CD4 T cell development and humoral immunity is independent of SLAM and Fyn kinase. J. Immunol. 178:2 (2007), 817–828.
38. Morra, M., et al. Defective B cell responses in the absence of SH2D1A. Proc. Natl. Acad. Sci. U. S. A. 102:13 (2005), 4819–4823.
39. Moyron-Quiroz, J.E., et al. The smallpox vaccine induces an early neutralizing IgM response. Vaccine 28:1 (2009), 140–147.
40. Ndungu, F.M., et al. Functional memory B cells and long-lived plasma cells are generated after a single Plasmodium chabaudi infection in mice. PLoS Pathog., 5(12), 2009, e1000690.
41. Nurieva, R.I., et al. Bcl6 mediates the development of T follicular helper cells. Science (New York, N.Y.) 325:5943 (2009), 1001–1005.
42. Obeng-Adjei, N., et al. Circulating Th1-cell-type Tfh cells that exhibit impaired B cell help are preferentially activated during acute malaria in children. Cell Rep., 2015, 1–34.
43. Okada, T., et al. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol., 3(6), 2005, e150.
44. Osier, F.H.A., et al. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect. Immun. 76:5 (2008), 2240–2248.
45. Pérez-Mazliah, D., et al. Disruption of IL-21 signaling affects T cell-B cell interactions and abrogates protective humoral immunity to malaria. PLoS Pathog., 11(3), 2015, e1004715.
46. Qi, H., From SAP-less T cells to helpless B cells and back: dynamic T-B cell interactions underlie germinal center development and function. Immunol. Rev. 247:1 (2012), 24–35.
47. Qi, H., T follicular helper cells in space-time. Nat. Rev. Immunol. 16:10 (2016), 612–625.
48. Qi, H., et al. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455:7214 (2008), 764–769.
49. Quin, S.J., Langhorne, J., Different regions of the malaria merozoite surface protein 1 of Plasmodium chabaudi elicit distinct T-cell and antibody isotype responses. Infect. Immun. 69:4 (2001), 2245–2251.
50. Reinhardt, R.L., Liang, H.-E., Locksley, R.M., Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10:4 (2009), 385–393.
51. Ryg-Cornejo, V., et al. Severe malaria infections impair germinal center responses by inhibiting T follicular helper cell differentiation. Cell Rep., 2015, 1–29.
52. Sabchareon, A., et al. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am. J. Trop. Med. Hyg. 45:3 (1991), 297–308.
53. Schaerli, P., et al. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192:11 (2000), 1553–1562.
54. Schindelin, J., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9:7 (2012), 676–682.
55. Shinkai, Y., et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:5 (1992), 855–867.
56. Shulman, Z., et al. Dynamic signaling by T follicular helper cells during germinal center B cell selection. Science (New York, N.Y.) 345:6200 (2014), 1058–1062.
57. Spence, P.J., et al. Mosquito transmission of the rodent malaria parasite Plasmodium chabaudi. Malar. J., 11(1), 2012, 1.
58. Spence, P.J., et al. Vector transmission regulates immune control of Plasmodium virulence. Nature 498:7453 (2013), 228–231.
59. Spolski, R., Leonard, W.J., Interleukin-21: a double-edged sword with therapeutic potential. Nat. Rev. Drug Discov. 13:5 (2014), 379–395.
60. Unkeless, J.C., Unkeless, J.C., Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J. Exp. Med. 150:3 (1979), 580–596.
61. Vinuesa, C.G., et al. Follicular helper T cells. Annu. Rev. Immunol. 34:1 (2016), 335–368.
62. von der Weid, T., Honarvar, N., Langhorne, J., Gene-targeted mice lacking B cells are unable to eliminate a blood stage malaria infection. J. Immunol. 156:7 (1996), 2510–2516.
63. Wikenheiser, D.J., et al. The costimulatory molecule ICOS regulates host Th1 and follicular Th cell differentiation in response to Plasmodium chabaudi chabaudi AS infection. J. Immunol. 196:2 (2016), 778–791.
64. Wu, C., et al. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2:5 (2001), 410–414.
65. Xu, H., et al. Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility. Nature 496:7446 (2013), 523–527.
66. Yusuf, I., et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 185:1 (2010), 190–202.
67. Zander, R.A., et al. PD-1 co-inhibitory and OX40 co-stimulatory crosstalk regulates helper T cell differentiation and anti-plasmodium humoral immunity. Cell Host Microbe 17:5 (2015), 628–641.