CD28 expression is required after T cell priming for helper T cell responses and protective immunity to infection

eLife

Volumn 3, Issue October2014, 2014, Pages 1-21

  Linterman, Michelle A ^a,b,e   Denton, Alice E ^b,c   Divekar, Devina P ^a,b,f   Zvetkova, Ilona ^c   Kane, Leanne ^d   Ferreira, Cristina ^e   Veldhoen, Marc ^e   Clare, Simon ^d   Dougan, Gordon ^d   Espéli, Marion ^a,b,g   Smith, Kenneth G C ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e BABRAHAM INSTITUTE   (United Kingdom)

^f UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^g Universite Paris Sud   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD134 ANTIGEN; CD28 ANTIGEN; CRE RECOMBINASE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTEGRASE; LIGAND; TNFRSF4 PROTEIN, MOUSE;

ANIMAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR IMMUNITY; CITROBACTER RODENTIUM; CROSS PRESENTATION; ENTEROBACTERIACEAE INFECTION; HELPER CELL; IMMUNITY; IMMUNOLOGY; INFLUENZA A VIRUS; METABOLISM; MICROBIOLOGY; MOUSE; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD28; CELL DIFFERENTIATION; CELL PROLIFERATION; CITROBACTER RODENTIUM; CROSS-PRIMING; ENTEROBACTERIACEAE INFECTIONS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNITY; IMMUNITY, CELLULAR; INFLUENZA A VIRUS; INTEGRASES; LIGANDS; MICE; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, OX40; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84928203976     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03180     Document Type: Article

References (60)

1. Aberg JA. 2012. Aging, inflammation, and HIV infection. Topics in Antiviral Medicine 20:101-105.
2. Attridge K, Kenefeck R, Wardzinski L, Qureshi OS, Wang CJ, Manzotti C, Okkenhaug K, Walker LS. 2014. IL-21 promotes CD4 T Cell responses by phosphatidylinositol 3-kinase-dependent upregulation of CD86 on B cells. Journal of Immunology 192:2195-2201. doi: 10.4049/jimmunol.1302082.
3. Baumjohann D, Okada T, Ansel KM. 2011. Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. The Journal of Immunology 187:2089-2092. doi: 10.4049/jimmunol.1101393.
4. Beima KM, Miazgowicz MM, Lewis MD, Yan PS, Huang TH, Weinmann AS. 2006. T-bet binding to newly identified target gene promoters is cell type-independent but results in variable context-dependent functional effects. The Journal of Biological Chemistry 281:11992-12000. doi: 10.1074/jbc.M513613200.
5. Belz GT, Wodarz D, Diaz G, Nowak MA, Doherty PC. 2002. Compromised influenza virus-specific CD8(+)-T-cell memory in CD4(+)-T-cell-deficient mice. Journal of Virology 76:12388-12393. doi: 10.1128/JVI.76.23.12388-12393.2002.
6. Bertram EM, Lau P, Watts TH. 2002. Temporal segregation of 4-1BB versus CD28-mediated costimulation: 4-1BB ligand influences T cell numbers late in the primary response and regulates the size of the T cell memory response following influenza infection. The Journal of Immunology 168:3777-3785. doi: 10.4049/jimmunol.168.8.3777.
7. Boise LH, Minn AJ, Noel PJ, June CH, Accavitti MA, Lindsten T, Thompson CB. 1995. CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 3:87-98. doi: 10.1016/1074-7613(95)90161-2.
8. Borowski AB, Boesteanu AC, Mueller YM, Carafides C, Topham DJ, Altman JD, Jennings SR, Katsikis PD. 2007. Memory CD8+ T cells require CD28 costimulation. The Journal of Immunology 179:6494-6503. doi: 10.4049/jimmunol.179.10.6494.
9. Broux B, Markovic-Plese S, Stinissen P, Hellings N. 2012. Pathogenic features of CD4+CD28-T cells in immune disorders. Trends in Molecular Medicine 18:446-453. doi: 10.1016/j.molmed.2012.06.003.
10. Bry L, Brigl M, Brenner MB. 2006. CD4+-T-cell effector functions and costimulatory requirements essential for surviving mucosal infection with Citrobacter rodentium. Infection and Immunity 74:673-681. doi: 10.1128/IAI.74.1.673-681.2006.
11. Carreno BM, Carter LL, Collins M. 2005. Therapeutic opportunities in the B7/CD28 family of ligands and receptors. Current Opinion in Pharmacology 5:424-430. doi: 10.1016/j.coph.2005.02.003.
12. Choi YS, Kageyama R, Eto D, Escobar TC, Johnston RJ, Monticelli L, Lao C, Crotty S. 2011. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34:932-946. doi: 10.1016/j.immuni.2011.03.023.
13. Chung Y, Tanaka S, Chu F, Nurieva RI, Martinez GJ, Rawal S, Wang YH, Lim H, Reynolds JM, Zhou XH, Fan HM, Liu ZM, Neelapu SS, Dong C. 2011. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nature Medicine 17:983-988. doi: 10.1038/nm.2426.
14. Crotty S. 2011. Follicular helper CD4 T Cells (T(FH)). Annual Review of Immunology 29:621-663. doi: 10.1146/annurev-immunol-031210-101400.
15. Cubas RA, Mudd JC, Savoye AL, Perreau M, van Grevenynghe J, Metcalf T, Connick E, Meditz A, Freeman GJ, Abesada-Terk G Jnr, Jacobson JM, Brooks AD, Crotty S, Estes JD, Pantaleo G, Lederman MM, Haddad EK. 2013. Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nature Medicine 19:494-499. doi: 10.1038/nm.3109.
16. Deenick EK, Chan A, Ma CS, Gatto D, Schwartzberg PL, Brink R, Tangye SG. 2010. Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 33:241-253. doi: 10.1016/j.immuni.2010.07.015.
17. Diehn M, Alizadeh AA, Rando OJ, Liu CL, Stankunas K, Botstein D, Crabtree GR, Brown PO. 2002. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proceedings of the National Academy of Sciences of USA 99:11796-11801. doi: 10.1073/pnas.092284399.
18. Ferguson SE, Han S, Kelsoe G, Thompson CB. 1996. CD28 is required for germinal center formation. The Journal of Immunology 156:4576-4581.
19. Flynn KJ, Riberdy JM, Christensen JP, Altman JD, Doherty PC. 1999. In vivo proliferation of naive and memory influenza-specific CD8(+) T cells. Proceedings of the National Academy of Sciences of USA 96:8597-8602. doi: 10.1073/pnas.96.15.8597.
20. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR, Elstrom RL, June CH, Thompson CB. 2002. The CD28 signaling pathway regulates glucose metabolism. Immunity 16:769-777. doi: 10.1016/S1074-7613(02)00323-0.
21. Good-Jacobson KL, Song E, Anderson S, Sharpe AH, Shlomchik MJ. 2012. CD80 expression on B cells regulates murine T follicular helper development, germinal center B cell survival, and plasma cell generation. The Journal of Immunology 188:4217-4225. doi: 10.4049/jimmunol.1102885.
22. Gramaglia I, Weinberg AD, Lemon M, Croft M. 1998. Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. Journal of Immunology 161:6510-6517.
23. Green JM, Noel PJ, Sperling AI, Walunas TL, Gray GS, Bluestone JA, Thompson CB. 1994. Absence of B7-dependent responses in CD28-deficient mice. Immunity 1:501-508. doi: 10.1016/1074-7613(94)90092-2.
24. Han S, Hathcock K, Zheng B, Kepler TB, Hodes R, Kelsoe G. 1995. Cellular interaction in germinal centers. Roles of CD40 ligand and B7-2 in established germinal centers. The Journal of Immunology 155:556-567.
25. Harding FA, McArthur JG, Gross JA, Raulet DH, Allison JP. 1992. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356:607-609. doi: 10.1038/356607a0.
26. Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, Fujikado N, Tanahashi Y, Akitsu A, Kotaki H, Sudo K, Nakae S, Sasakawa C, Iwakura Y. 2009. Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30:108-119. doi: 10.1016/j.immuni.2008.11.009.
27. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. 2008. PD-1 and its ligands in tolerance and immunity. Annual Review of Immunology 26:677-704. doi: 10.1146/annurev.immunol.26.021607.090331.
28. King CL, Xianli J, June CH, Abe R, Lee KP. 1996. CD28-deficient mice generate an impaired Th2 response to Schistosoma mansoni infection. European Journal of Immunology 26:2448-2455. doi: 10.1002/eji.1830261027.
29. Klinger M, Kim JK, Chmura SA, Barczak A, Erle DJ, Killeen N. 2009. Thymic OX40 expression discriminates cells undergoing strong responses to selection ligands. Journal of Immunology 182:4581-4589. doi: 10.4049/jimmunol.0900010.
30. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, Campbell DJ. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nature Immunology 10:595-602. doi: 10.1038/ni.1731.
31. Lafferty KJ, Cunningham AJ. 1975. A new analysis of allogeneic interactions. The Australian Journal of Experimental Biology and Medical Science 53:27-42. doi: 10.1038/icb.1975.3.
32. Linterman MA. 2014. How T follicular helper cells and the germinal centre response change with age. Immunology and Cell Biology 92:72-79. doi: 10.1038/icb.2013.77.
33. Linterman MA, Liston A, Vinuesa CG. 2012. T-follicular helper cell differentiation and the co-option of this pathway by non-helper cells. Immunological Reviews 247:143-159. doi: 10.1111/j.1600-065X.2012.01121.x.
34. Linterman MA, Pierson W, Lee SK, Kallies A, Kawamoto S, Rayner TF, Srivastava M, Divekar DP, Beaton L, Hogan JJ, Fagarasan S, Liston A, Smith KG, Vinuesa CG. 2011. Foxp3(+) follicular regulatory T cells control the germinal center response. Nature Medicine 17:975-982. doi: 10.1038/nm.2425.
35. Mallett S, Fossum S, Barclay AN. 1990. Characterization of the MRC OX40 antigen of activated CD4 positive T lymphocytes-a molecule related to nerve growth factor receptor. The EMBO Journal 9:1063-1068.
36. Marelli-Berg FM, Okkenhaug K, Mirenda V. 2007. A two-signal model for T cell trafficking. Trends in Immunology 28:267-273. doi: 10.1016/j.it.2007.04.008.
37. Martinez-Llordella M, Esensten JH, Bailey-Bucktrout SL, Lipsky RH, Marini A, Chen J, Mughal M, Mattson MP, Taub DD, Bluestone JA. 2013. CD28-inducible transcription factor DEC1 is required for efficient autoreactive CD4+ T cell response. The Journal of Experimental Medicine 210:1603-1619. doi: 10.1084/jem.20122387.
38. McAdam AJ, Chang TT, Lumelsky AE, Greenfield EA, Boussiotis VA, Duke-Cohan JS, Chernova T, Malenkovich N, Jabs C, Kuchroo VK, Ling V, Collins M, Sharpe AH, Freeman GJ. 2000. Mouse inducible costimulatory molecule (ICOS) expression is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells. The Journal of Immunology 165:5035-5040. doi: 10.4049/jimmunol.165.9.5035.
39. Mittrucker HW, Shahinian A, Bouchard D, Kundig TM, Mak TW. 1996. Induction of unresponsiveness and impaired T cell expansion by staphylococcal enterotoxin B in CD28-deficient mice. The Journal of Experimental Medicine 183:2481-2488. doi: 10.1084/jem.183.6.2481.
40. Ndlovu H, Darby M, Froelich M, Horsnell W, Luhder F, Hunig T, Brombacher F. 2014. Inducible deletion of CD28 prior to secondary nippostrongylus brasiliensis infection impairs worm expulsion and recall of protective memory CD4(+) T cell responses. PLOS Pathogens 10:e1003906. doi: 10.1371/journal.ppat.1003906.
41. Riley JL, Mao M, Kobayashi S, Biery M, Burchard J, Cavet G, Gregson BP, June CH, Linsley PS. 2002. Modulation of TCR-induced transcriptional profiles by ligation of CD28, ICOS, and CTLA-4 receptors. Proceedings of the National Academy of Sciences of USA 99:11790-11795. doi: 10.1073/pnas.162359999.
42. Roman E, Miller E, Harmsen A, Wiley J, Von Andrian UH, Huston G, Swain SL. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. The Journal of Experimental Medicine 196:957-968. doi: 10.1084/jem.20021052.
43. Sage PT, Francisco LM, Carman CV, Sharpe AH. 2013. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nature Immunology 14:152-161. doi: 10.1038/ni.2496.
44. Salek-Ardakani S, Choi YS, Rafii-El-Idrissi Benhnia M, Flynn R, Arens R, Shoenberger S, Crotty S, Croft M, Salek-Ardakani S. 2011. B cell-specific expression of B7-2 is required for follicular Th cell function in response to vaccinia virus. The Journal of Immunology 186:5294-5303. doi: 10.4049/jimmunol.1100406.
45. Salomon B, Bluestone JA. 2001. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annual Review of Immunology 19:225-252. doi: 10.1146/annurev.immunol.19.1.225.
46. Sarawar SR, Doherty PC. 1994. Concurrent production of interleukin-2, interleukin-10, and gamma interferon in the regional lymph nodes of mice with influenza pneumonia. Journal of Virology 68:3112-3119.
47. Scalapino KJ, Daikh DI. 2008. CTLA-4: a key regulatory point in the control of autoimmune disease. Immunological Reviews 223:143-155. doi: 10.1111/j.1600-065X.2008.00639.x.
48. Schweitzer AN, Sharpe AH. 1998. Studies using antigen-presenting cells lacking expression of both B7-1 (CD80) and B7-2 (CD86) show distinct requirements for B7 molecules during priming versus restimulation of Th2 but not Th1 cytokine production. The Journal of Immunology 161:2762-2771.
49. Shahinian A, Pfeffer K, Lee KP, Kundig TM, Kishihara K, Wakeham A, Kawai K, Ohashi PS, Thompson CB, Mak TW. 1993. Differential T cell costimulatory requirements in CD28-deficient mice. Science 261:609-612. doi: 10.1126/science.7688139.
50. Shiomi H, Masuda A, Nishiumi S, Nishida M, Takagawa T, Shiomi Y, Kutsumi H, Blumberg RS, Azuma T, Yoshida M. 2010. Gamma interferon produced by antigen-specific CD4+ T cells regulates the mucosal immune responses to Citrobacter rodentium infection. Infection and Immunity 78:2653-2666. doi: 10.1128/IAI.01343-09.
51. Sonnenberg GF, Monticelli LA, Elloso MM, Fouser LA, Artis D. 2011. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 34:122-134. doi: 10.1016/j.immuni.2010.12.009.
52. Tripp RA, Sarawar SR, Doherty PC. 1995. Characteristics of the influenza virus-specific CD8+ T cell response in mice homozygous for disruption of the H-2lAb gene. The Journal of Immunology 155:2955-2959.
53. Walker LS, Gulbranson-Judge A, Flynn S, Brocker T, Raykundalia C, Goodall M, Forster R, Lipp M, Lane P. 1999. Compromised OX40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. The Journal of Experimental Medicine 190:1115-1122. doi: 10.1084/jem.190.8.1115.
54. Walker LS, Wiggett HE, Gaspal FM, Raykundalia CR, Goodall MD, Toellner KM, Lane PJ. 2003. Established T cell-driven germinal center B cell proliferation is independent of CD28 signaling but is tightly regulated through CTLA-4. The Journal of Immunology 170:91-98. doi: 10.4049/jimmunol.170.1.91.
55. Walunas TL, Sperling AI, Khattri R, Thompson CB, Bluestone JA. 1996. CD28 expression is not essential for positive and negative selection of thymocytes or peripheral T cell tolerance. Journal of Immunology 156:1006-1013.
56. Weng NP, Akbar AN, Goronzy J. 2009. CD28(-) T cells: their role in the age-associated decline of immune function. Trends in Immunology 30:306-312. doi: 10.1016/j.it.2009.03.013.
57. Wing JB, Sakaguchi S. 2014. Foxp3(+) T(reg) cells in humoral immunity. International Immunology 26:61-69. doi: 10.1093/intimm/dxt060.
58. Wollenberg I, Agua-Doce A, Hernandez A, Almeida C, Oliveira VG, Faro J, Graca L. 2011. Regulation of the germinal center reaction by Foxp3+ follicular regulatory T cells. The Journal of Immunology 187:4553-4560. doi: 10.4049/jimmunol.1101328.
59. Zhang R, Huynh A, Whitcher G, Chang J, Maltzman JS, Turka LA. 2013. An obligate cell-intrinsic function for CD28 in Tregs. The Journal of Clinical Investigation 123:580-593. doi: 10.1172/JCI65013.
60. Zhu J, Paul WE. 2010. Heterogeneity and plasticity of T helper cells. Cell Research 20:4-12. doi: 10.1038/cr.2009.138.