Recognition of microbial viability via TLR8 drives T FH cell differentiation and vaccine responses

Nature Immunology

Volumn 19, Issue 4, 2018, Pages 386-396

  Ugolini, Matteo ^a   Gerhard, Jenny ^a   Burkert, Sanne ^a   Jensen, Kristoffer Jarlov ^b,c   Georg, Philipp ^a   Ebner, Friederike ^d   Volkers, Sarah M ^a   Thada, Shruthi ^a,e   Dietert, Kristina ^d   Bauer, Laura ^f   Schäfer, Alexander ^g   Helbig, Elisa T ^a   Opitz, Bastian ^a,h   Kurth, Florian ^a   Sur, Saubashya ^a   Dittrich, Nickel ^a   Gaddam, Sumanlatha ^e,i   Conrad, Melanie L ^a   Benn, Christine S ^b,j   Blohm, Ulrike ^g   Gruber, Achim D ^d   Hutloff, Andreas ^f   Hartmann, Susanne ^d   Boekschoten, Mark V ^k   Müller, Michael ^k,l   Jungersen, Gregers ^c   Schumann, Ralf R ^a   Suttorp, Norbert ^a,h   Sander, Leif E ^a,h   more..

^a BERLIN INSTITUTE OF HEALTH   (Germany)

^b STATENS SERUM INSTITUT   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e Bhagwan Mahavir Medical Research Centre   (India)

^f Chronic Immune Reactions German Rheumatism Research Centre A Leibniz Institute   (Germany)

^g FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^h German Center for Lung Research   (Germany)

ⁱ OSMANIA UNIVERSITY   (India)

^j ODENSE UNIVERSITY HOSPITAL   (Denmark)

^k WAGENINGEN UNIVERSITY   (Netherlands)

^l UNIVERSITY OF EAST ANGLIA   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; BCG VACCINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 23; INTERLEUKIN 6; SALMONELLOSIS VACCINE; TOLL LIKE RECEPTOR 8; TUMOR NECROSIS FACTOR; LIVE VACCINE; TLR8 PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM DETECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOMESTIC PIG; EXTRAPULMONARY TUBERCULOSIS; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNIZATION; INNATE IMMUNITY; LUNG TUBERCULOSIS; LYMPHOCYTE DIFFERENTIATION; MAJOR CLINICAL STUDY; MICROBIAL VIABILITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SALMONELLOSIS; SINGLE NUCLEOTIDE POLYMORPHISM; TFH CELL; TREATMENT RESPONSE; VACCINATION; ANIMAL; ANTIBODY PRODUCTION; CELL DIFFERENTIATION; FEMALE; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; PIG;

ADULT; ANIMALS; ANTIBODY FORMATION; CELL DIFFERENTIATION; FEMALE; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MICROBIAL VIABILITY; SWINE; T-LYMPHOCYTES, HELPER-INDUCER; TOLL-LIKE RECEPTOR 8; VACCINES, ATTENUATED;

EID: 85044220410     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/s41590-018-0068-4     Document Type: Article

References (55)

1. Barquet, N. &Domingo, P. Smallpox: the triumph over the most terrible of the ministers of death. Ann. Intern. Med. 127, 635-642 (1997).
2. Plotkin, S. A. &Plotkin, S. L. The development of vaccines: how the past led to the future. Nat. Rev. Microbiol. 9, 889-893 (2011).
3. Minor, P. D. Live attenuated vaccines: Historical successes and current challenges. Virology 479-480, 379-392 (2015).
4. De Gregorio, E. &Rappuoli, R. From empiricism to rational design: a personal perspective of the evolution of vaccine development. Nat. Rev. Immunol. 14, 505-514 (2014).
5. Rauh, L. W. &Schmidt, R. Measles immunization with killed virus vaccine. Serum antibody titers and experience with exposure to measles epidemic. Am. J. Dis. Child. 109, 232-237 (1965).
6. Blander, J. M. &Sander, L. E. Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 12, 215-225 (2012).
7. Sander, L. E. et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474, 385-389 (2011).
8. Iwasaki, A. &Medzhitov, R. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16, 343-353 (2015).
9. Crotty, S. T follicular helper cell differentiation, function, and roles in disease. Immunity 41, 529-542 (2014).
10. Vinuesa, C. G., Linterman, M. A., Yu, D. &MacLennan, I. C. Follicular helper T cells. Annu. Rev. Immunol. 34, 335-368 (2016).
11. 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).
12. Nurieva, R. I. et al. Bcl6 mediates the development of T follicular helper cells. Science 325, 1001-1005 (2009).
13. Linterman, M. A. et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207, 353-363 (2010).
14. Weber, J. P. et al. ICOS maintains the T follicular helper cell phenotype by down-regulating Kruppel-like factor 2. J. Exp. Med. 212, 217-233 (2015).
15. 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, 1545-1552 (2000).
16. Schaerli, P. et al. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192, 1553-1562 (2000).
17. Ueno, H., Banchereau, J. &Vinuesa, C. G. Pathophysiology of T follicular helper cells in humans and mice. Nat. Immunol. 16, 142-152 (2015).
18. Cucak, H., Yrlid, U., Reizis, B., Kalinke, U. &Johansson-Lindbom, B. Type I interferon signaling in dendritic cells stimulates the development of lymph-node-resident T follicular helper cells. Immunity 31, 491-501 (2009).
19. Batten, M. et al. IL-27 supports germinal center function by enhancing IL-21 production and the function of T follicular helper cells. J. Exp. Med. 207, 2895-2906 (2010).
20. Schmitt, N. et al. The cytokine TGF-β co-opts signaling via STAT3-STAT4 to promote the differentiation of human TFH cells. Nat. Immunol. 15, 856-865 (2014).
21. Jacquemin, C. et al. OX40 ligand contributes to human lupus pathogenesis by promoting T follicular helper response. Immunity 42, 1159-1170 (2015).
22. Eigenbrod, T., Pelka, K., Latz, E., Kreikemeyer, B. &Dalpke, A. H. TLR8 senses bacterial RNA in human monocytes and plays a nonredundant role for recognition of Streptococcus pyogenes. J. Immunol. 195, 1092-1099 (2015).
23. Bergstrom, B. et al. TLR8 senses Staphylococcus aureus RNA in human primary monocytes and macrophages and induces IFN-β production via a TAK1-IKKβ-IRF5 signaling pathway. J. Immunol. 195, 1100-1111 (2015).
24. Meurens, F., Summerfield, A., Nauwynck, H., Saif, L. &Gerdts, V. The pig: a model for human infectious diseases. Trends Microbiol. 20, 50-57 (2012).
25. Mair, K. H. et al. The porcine innate immune system: an update. Dev. Comp. Immunol. 45, 321-343 (2014).
26. Zhu, J., Lai, K., Brownile, R., Babiuk, L. A. &Mutwiri, G. K. Porcine TLR8 and TLR7 are both activated by a selective TLR7 ligand, imiquimod. Mol. Immunol. 45, 3238-3243 (2008).
27. Springer S., Lindner T., Steinbach G., Selbitz H. J. Investigation of the efficacy of a genetically-stabile live Salmonella typhimurium vaccine for use in swine. Berl. Munch. Tierarztl. Wochenschr. 114,342-345 (2001).
28. Sinkora, M., Stepanova, K. &Sinkorova, J. Different anti-CD21 antibodies can be used to discriminate developmentally and functionally different subsets of B lymphocytes in circulation of pigs. Dev. Comp. Immunol. 39, 409-418 (2013).
29. Oh, D. Y. et al. A functional toll-like receptor 8 variant is associated with HIV disease restriction. J. Infect. Dis. 198, 701-709 (2008).
30. Wang, C. H. et al. TLR7 and TLR8 gene variations and susceptibility to hepatitis C virus infection. PLoS One 6, e26235 (2011).
31. Tanji, H., Ohto, U., Shibata, T., Miyake, K. &Shimizu, T. Structural reorganization of the Toll-like receptor 8 dimer induced by agonistic ligands. Science 339, 1426-1429 (2013).
32. Davila, S. et al. Genetic association and expression studies indicate a role of toll-like receptor 8 in pulmonary tuberculosis. PLoS Genet. 4, e1000218 (2008).
33. Schmitt, N. et al. Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12. Immunity 31, 158-169 (2009).
34. Hochrein, H. et al. Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells. J. Exp. Med. 192, 823-833 (2000).
35. Jones, S. C., Brahmakshatriya, V., Huston, G., Dibble, J. &Swain, S. L. TLR-activated dendritic cells enhance the response of aged naive CD4 T cells via an IL-6-dependent mechanism. J. Immunol. 185, 6783-6794 (2010).
36. Chakarov, S. &Fazilleau, N. Monocyte-derived dendritic cells promote T follicular helper cell differentiation. EMBO Mol. Med. 6, 590-603 (2014).
37. Heil, F. et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303, 1526-1529 (2004).
38. Schmitt, N. et al. IL-12 receptor beta1 deficiency alters in vivo T follicular helper cell response in humans. Blood 121, 3375-3385 (2013).
39. Barbet, G. et al. Sensing microbial viability through bacterial RNA augments T follicular helper cell and antibody responses. Immunity (in the press).
40. Dowling, D. J. et al. TLR7/8 adjuvant overcomes newborn hyporesponsiveness to pneumococcal conjugate vaccine at birth. JCI Insight 2, e91020 (2017).
41. Dowling, D. J. et al. Toll-like receptor 8 agonist nanoparticles mimic immunomodulating effects of the live BCG vaccine and enhance neonatal innate and adaptive immune responses. J. Allergy Clin. Immunol. 140, 1339-1350 (2017).
42. Fairbairn, L., Kapetanovic, R., Sester, D. P. &Hume, D. A. The mononuclear phagocyte system of the pig as a model for understanding human innate immunity and disease. J. Leukoc. Biol. 89, 855-871 (2011).
43. Landers, T. F., Cohen, B., Wittum, T. E. &Larson, E. L. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep. 127, 4-22 (2012).
44. Colditz, G. A. et al. Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. J. Am. Med. Assoc. 271, 698-702 (1994).
45. de Beaucoudrey, L. et al. Revisiting human IL-12Rβ deficiency: a survey of 141 patients from 30 countries. Medicine (Baltimore) 89, 381-402 (2010).
46. Picard, C. et al. Clinical features and outcome of patients with IRAK-4 and MyD88 deficiency. Medicine (Baltimore) 89, 403-425 (2010).
47. Ma, C. S. et al. Functional STAT3 deficiency compromises the generation of human T follicular helper cells. Blood 119, 3997-4008 (2012).
48. Ma, C. S. et al. Monogenic mutations differentially affect the quantity and quality of T follicular helper cells in patients with human primary immunodeficiencies. J. Allergy Clin. Immunol. 136, 993-1006 (2015).
49. Rao, D. A. et al. Pathologically expanded peripheral T helper cell subset drives B cells in rheumatoid arthritis. Nature 542, 110-114 (2017).
50. Lin, K. et al. MADMAX-Management and analysis database for multiple ~omics experiments. J. Integr. Bioinform. 8, 160 (2011).
51. Dai, M. et al. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175 (2005).
52. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density ol array probe level data. Biostatistics 4, 249-264 (2003).
53. Sartor, M. A. et al. Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics 7, 538 (2006).
54. Storey, J. D. &Tibshirani, R. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100, 9440-9445 (2003).
55. Dittrich, N. et al. Toll-like receptor 1 variations influence susceptibility and immune response to Mycobacterium tuberculosis. Tuberculosis (Edinb.) 95, 328-335 (2015).