CD8+ T cell exhaustion, suppressed gamma interferon production, and delayed memory response induced by chronic Brucella melitensis infection

Infection and Immunity

Volumn 83, Issue 12, 2015, Pages 4759-4771

  Durward Diioia, Marina ^a,b   Harms, Jerome ^b   Khan, Mike ^c   Hall, Cherisse ^c   Smith, Judith A ^c   Splitter, Gary A ^b  

^a MIDWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 7 RECEPTOR; LYMPHOCYTE ACTIVATION GENE 3; PROGRAMMED DEATH 1 RECEPTOR; UNCLASSIFIED DRUG; CD223 ANTIGEN; LEUKOCYTE ANTIGEN; PDCD1 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRUCELLA MELITENSIS; BRUCELLOSIS; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; INTERFERON PRODUCTION; MEMORY CELL; MORBIDITY; MOUSE; NONHUMAN; PERSISTENT INFECTION; PRIMARY INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; CHRONIC DISEASE; CLONAL ANERGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LYMPHOCYTE COUNT; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSPLANTATION;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD; BRUCELLA MELITENSIS; BRUCELLOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; CLONAL ANERGY; FEMALE; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; LYMPHOCYTE COUNT; MICE; MICE, INBRED BALB C; PROGRAMMED CELL DEATH 1 RECEPTOR; SIGNAL TRANSDUCTION;

EID: 84949655046     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01184-15     Document Type: Article

References (60)

1. Maudlin I, Eisler MC, Welburn SC. 2009. Neglected and endemic zoonoses. Philos Trans R Soc Lond B Biol Sci 364:2777-2787. http://dx.doi.org/10.1098/rstb.2009.0067.
2. Maudlin I, Weber-Mosdorf S. 2005. The control of neglected zoonotic diseases: a route to poverty alleviation. Report of a joint WHO/DFIDAHP meeting with the participation of FAO and OIE. World Health Organization, Geneva, Switzerland.
3. Smith JA, Khan M, Magnani DD, Harms JS, Durward M, Radhakrishnan GK, Liu YP, Splitter GA. 2013. Brucella induces an unfolded protein response via TcpB that supports intracellular replication in macrophages. PLoS Pathog 9:e1003785. http://dx.doi.org/10.1371/journal.ppat.1003785.
4. Radhakrishnan GK, Yu Q, Harms JS, Splitter GA. 2009. Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J Biol Chem 284:9892-9898. http://dx.doi.org/10.1074/jbc.M805458200.
5. Ko J, Splitter GA. 2003. Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and humans. Clin Microbiol Rev 16:65-78. http://dx.doi.org/10.1128/CMR.16.1.65-78.2003.
6. Baldwin CL, Goenka R. 2006. Host immune responses to the intracellular bacteria Brucella: does the bacteria instruct the host to facilitate chronic infection? Crit Rev Immunol 26:407-442. http://dx.doi.org/10.1615/CritRevImmunol.v26.i5.30.
7. Durward M, Radhakrishnan G, Harms J, Bareiss C, Magnani D, Splitter GA. 2012. Active evasion of CTL mediated killing and low quality responding CD8+T cells contribute to persistence of brucellosis. PLoS One 7:e34925. http://dx.doi.org/10.1371/journal.pone.0034925.
8. Franco MP, Mulder M, Smits HL. 2007. Persistence and relapse in brucellosis and need for improved treatment. Trans R Soc Trop Med Hyg 101:854-855. http://dx.doi.org/10.1016/j.trstmh.2007.05.016.
9. Oliveira S, Giambartolomei G, Cassataro J. 2011. Confronting the barriers to develop novel vaccines against brucellosis. Expert Rev Vaccines 10:1291-1305. http://dx.doi.org/10.1586/erv.11.110.
10. Woolard SN, Kumaraguru U. 2010 Viral vaccines and CTL response. J Biomed Biotechnol 2010:141657. http://dx.doi.org/10.1155/2010/141657.
11. Anikeeva N, Sykulev Y. 2011. Mechanisms controlling granule-mediated cytolytic activity of cytotoxic T lymphocytes. Immunol Res 51:183-194. http://dx.doi.org/10.1007/s12026-011-8252-8.
12. Zhang N, Bevan MJ. 2011. CD8(+) T cells: foot soldiers of the immune system. Immunity 35:161-168. http://dx.doi.org/10.1016/j.immuni.2011.07.010.
13. Durward MA, Harms J, Magnani DM, Eskra L, Splitter GA. 2010. Discordant Brucella melitensis antigens yield cognate CD8+ T cells in vivo. Infect Immun 78:168-176. http://dx.doi.org/10.1128/IAI.00994-09.
14. Cox MA, Harrington LE, Zajac AJ. 2011. Cytokines and the inception of CD8 T cell responses. Trends Immunol 32:180-186. http://dx.doi.org/10.1016/j.it.2011.01.004.
15. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E. 2013. The who's who of T-cell differentiation: human memory T-cell subsets. Eur J Immunol 43:2797-2809. http://dx.doi.org/10.1002/eji.201343751.
16. Obar JJ, Lefrancois L. 2010. Early events governing memory CD8+ T-cell differentiation. Int Immunol 22:619-625. http://dx.doi.org/10.1093/intimm/dxq053.
17. Cox MA, Zajac AJ. 2010. Shaping successful and unsuccessful CD8 T cell responses following infection. J Biomed Biotechnol 2010:159152. http://dx.doi.org/10.1155/2010/159152.
18. Youngblood B, Davis CW, Ahmed R. 2010. Making memories that last a lifetime: heritable functions of self-renewing memory CD8 T cells. Int Immunol 22:797-803. http://dx.doi.org/10.1093/intimm/dxq437.
19. Jung YW, Rutishauser RL, Joshi NS, Haberman AM, Kaech SM. 2010. Differential localization of effector and memory CD8 T cell subsets in lymphoid organs during acute viral infection. J Immunol 185:5315-5325. http://dx.doi.org/10.4049/jimmunol.1001948.
20. Cui W, Kaech SM. 2010. Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol Rev 236:151-166. http://dx.doi.org/10.1111/j.1600-065X.2010.00926.x.
21. Kaech SM, Cui W. 2012. Transcriptional control of effector and memory CD8+T cell differentiation. Nat Rev Immunol 12:749-761. http://dx.doi.org/10.1038/nri3307.
22. Sarkar S, Kalia V, Haining WN, Konieczny BT, Subramaniam S, Ahmed R. 2008. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med 205:625-640. http://dx.doi.org/10.1084/jem.20071641.
23. D'Cruz LM, Rubinstein MP, Goldrath AW. 2009. Surviving the crash: transitioning from effector to memory CD8+ T cell. Semin Immunol 21:92-98. http://dx.doi.org/10.1016/j.smim.2009.02.002.
24. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, Larsen CP, Ahmed R. 2009. mTOR regulates memory CD8 T-cell differentiation. Nature 460:108-112. http://dx.doi.org/10.1038/nature08155.
25. Schietinger A, Greenberg PD. 2014. Tolerance and exhaustion: defining mechanisms of T cell dysfunction. Trends Immunol 35:51-60. http://dx.doi.org/10.1016/j.it.2013.10.001.
26. Wherry EJ. 2011. T cell exhaustion. Nat Immunol 131:492-499. http://dx.doi.org/10.1038/ni.2035.
27. West EE, Youngblood B, Tan WG, Jin HT, Araki K, Alexe G, Konieczny BT, Calpe S, Freeman GJ, Terhorst C, Haining WN, Ahmed R. 2011. Tight regulation of memory CD8(+) T cells limits their effectiveness during sustained high viral load. Immunity 35:285-298. http://dx.doi.org/10.1016/j.immuni.2011.05.017.
28. Vitry MA, De Trez C, Goriely S, Dumoutier L, Akira S, Ryffel B, Carlier Y, Letesson JJ, Muraille E. 2012. Crucial role of gamma interferon-producing CD4+ Th1 cells but dispensable function of CD8+ T cell, B cell, Th2, and Th17 responses in the control of Brucella melitensis infection in mice. Infect Immun 80:4271-4280. http://dx.doi.org/10.1128/IAI.00761-12.
29. Rajashekara G, Glover DA, Krepps M, Splitter GA. 2005. Temporal analysis of pathogenic events in virulent and avirulent Brucella melitensis infections. Cell Microbiol 7:1459-1473. http://dx.doi.org/10.1111/j.1462-5822.2005.00570.x.
30. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
31. Youngblood B, Hale JS, Ahmed R. 2013. T-cell memory differentiation: insights from transcriptional signatures and epigenetics. Immunology 139:277-284. http://dx.doi.org/10.1111/imm.12074.
32. Kim EH, Sullivan JA, Plisch EH, Tejera MM, Jatzek A, Choi KY, Suresh M. 2012. Signal integration by Akt regulates CD8 T cell effector and memory differentiation. J Immunol 188:4305-4314. http://dx.doi.org/10.4049/jimmunol.1103568.
33. Franco MP, Mulder M, Gilman RH, Smits HL. 2007. Human brucellosis. Lancet Infect Dis 7:775-786. http://dx.doi.org/10.1016/S1473-3099(07)70286-4.
34. Barrionuevo P, Delpino MV, Pozner RG, Velasquez LN, Cassataro J, Giambartolomei GH. 2013. Brucella abortus induces intracellular retention of MHC-I molecules in human macrophages down-modulating cytotoxic CD8(+) T cell responses. Cell Microbiol 15:487-502. http://dx.doi.org/10.1111/cmi.12058.
35. West EE, Jin HT, Rasheed AU, Penaloza-Macmaster P, Ha SJ, Tan WG, Youngblood B, Freeman GJ, Smith KA, Ahmed R. 2013. PD-L1 blockade synergizes with IL-2 therapy in reinvigorating exhausted T cells. J Clin Invest 123:2604-2615. http://dx.doi.org/10.1172/JCI67008.
36. Hofmeyer KA, Jeon H, Zang X. 2011. The PD-1/PD-L1 (B7-H1) pathway in chronic infection-induced cytotoxicTlymphocyte exhaustion. J Biomed Biotechnol 2011:451694. http://dx.doi.org/10.1155/2011/451694.
37. Liu J, Zhang E, Ma Z, Wu W, Kosinska A, Zhang X, Moller I, Seiz P, Glebe D, Wang B, Yang D, Lu M, Roggendorf M. 2014. Enhancing virus-specific immunity in vivo by combining therapeutic vaccination and PD-L1 blockade in chronic hepadnaviral infection. PLoS Pathog 10: e1003856. http://dx.doi.org/10.1371/journal.ppat.1003856.
38. Esch KJ, Juelsgaard R, Martinez PA, Jones DE, Petersen CA. 2013. Programmed death 1-mediated T cell exhaustion during visceral leishmaniasis impairs phagocyte function. J Immunol 191:5542-5550. http://dx.doi.org/10.4049/jimmunol.1301810.
39. Ko J, Gendron-Fitzpatrick A, Splitter GA. 2002. Susceptibility of IFN regulatory factor-1 and IFN consensus sequence binding protein-deficient mice to brucellosis. J Immunol 168:2433-2440. http://dx.doi.org/10.4049/jimmunol.168.5.2433.
40. Kulpa DA, Lawani M, Cooper A, Peretz Y, Ahlers J, Sekaly RP. 2013. PD-1 coinhibitory signals: the link between pathogenesis and protection. Semin Immunol 25:219-227. http://dx.doi.org/10.1016/j.smim.2013.02.002.
41. Sierro S, Romero P, Speiser DE. 2011. The CD4-like molecule LAG-3, biology and therapeutic applications. Expert Opin Ther Targets 15:91-101. http://dx.doi.org/10.1517/14712598.2011.540563.
42. Choi S, Schwartz RH. 2007. Molecular mechanisms for adaptive tolerance and other T cell anergy models. Semin Immunol 19:140-152. http://dx.doi.org/10.1016/j.smim.2007.02.005.
43. Lutz MB, Kurts C. 2009. Induction of peripheral CD4+ T-cell tolerance and CD8+ T-cell cross-tolerance by dendritic cells. Eur J Immunol 39: 2325-2330. http://dx.doi.org/10.1002/eji.200939548.
44. Mescher MF, Agarwal P, Casey KA, Hammerbeck CD, Xiao Z, Curtsinger JM. 2007. Molecular basis for checkpoints in the CD8 T cell response: tolerance versus activation. Semin Immunol 19:153-161. http://dx.doi.org/10.1016/j.smim.2007.02.007.
45. Shakhar G, Lindquist RL, Skokos D, Dudziak D, Huang JH, Nussenzweig MC, Dustin ML. 2005. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat Immunol 6:707-714. http://dx.doi.org/10.1038/ni1210.
46. Mescher MF, Popescu FE, Gerner M, Hammerbeck CD, Curtsinger JM. 2007. Activation-induced non-responsiveness (anergy) limits CD8 T cell responses to tumors. Semin Cancer Biol 17:299-308. http://dx.doi.org/10.1016/j.semcancer.2007.06.008.
47. Wyckoff JH, III, Howland JL, Scott CM, Smith RA, Confer AW. 2005. Recombinant bovine interleukin 2 enhances immunity and protection induced by Brucella abortus vaccines in cattle. Vet Microbiol 111:77-87. http://dx.doi.org/10.1016/j.vetmic.2005.09.004.
48. Vitry MA, Hanot Mambres D, De Trez C, Akira S, Ryffel B, Letesson JJ, Muraille E. 2014. Humoral immunity and CD4+ Th1 cells are both necessary for a fully protective immune response upon secondary infection with Brucella melitensis. J Immunol 192:3740-3752. http://dx.doi.org/10.4049/jimmunol.1302561.
49. Casadevall A, Pirofski LA. 2006. A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv Immunol 91:1-44. http://dx.doi.org/10.1016/S0065-2776(06)91001-3.
50. Goenka R, Parent MA, Elzer PH, Baldwin CL. 2011. B cell-deficient mice display markedly enhanced resistance to the intracellular bacterium Brucella abortus. J Infect Dis 203:1136-1146. http://dx.doi.org/10.1093/infdis/jiq171.
51. Goenka R, Guirnalda PD, Black SJ, Baldwin CL. 2012. B lymphocytes provide an infection niche for intracellular bacterium Brucella abortus. J Infect Dis 206:91-98. http://dx.doi.org/10.1093/infdis/jis310.
52. Splitter G, Harms J, Petersen E, Magnani D, Durward M, Rajashekara G, Radhakrishnan G. 2014. Studying host-pathogen interaction events in living mice visualized in real time using biophotonic imaging. Methods Mol Biol 1197:67-85. http://dx.doi.org/10.1007/978-1-4939-1261-2_4.
53. Boer MC, van Meijgaarden KE, Joosten SA, Ottenhoff TH. 2014. CD8+ regulatory T cells, and not CD4+T cells, dominate suppressive phenotype and function after in vitro live Mycobacterium bovis-BCG activation of human cells. PLoS One 9:e94192. http://dx.doi.org/10.1371/journal.pone.0094192.
54. Sakaguchi S, Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T. 2009. Regulatory T cells: how do they suppress immune responses? Int Immunol 21:1105-1111. http://dx.doi.org/10.1093/intimm/dxp095.
55. Corsetti PP, de Almeida LA, Carvalho NB, Azevedo V, Silva TM, Teixeira HC, Faria AC, Oliveira SC. 2013. Lack of endogenous IL-10 enhances production of proinflammatory cytokines and leads to Brucella abortus clearance in mice. PLoS One 8:e74729. http://dx.doi.org/10.1371/journal.pone.0074729.
56. Pasquali P, Thornton AM, Vendetti S, Pistoia C, Petrucci P, Tarantino M, Pesciaroli M, Ruggeri F, Battistoni A, Shevach EM. 2010. CD4+CD25+ T regulatory cells limit effector T cells and favor the progression of brucellosis in BALB/c mice. Microbes Infect 12:3-10. http://dx.doi.org/10.1016/j.micinf.2009.09.005.
57. Oliveira SC, Splitter GA. 1995. CD8+ type 1 CD44hi CD45 RBlo T lymphocytes control intracellular Brucella abortus infection as demonstrated in major histocompatibility complex class I-and class IIdeficient mice. Eur J Immunol 25:2551-2557. http://dx.doi.org/10.1002/eji.1830250922.
58. Martirosyan A, Gorvel JP. 2013. Brucella evasion of adaptive immunity. Future Microbiol 8:147-154. http://dx.doi.org/10.2217/fmb.12.140.
59. Badowski M, Shultz CL, Eason Y, Ahmad N, Harris DT. 2014. The influence of intrinsic and extrinsic factors on immune system aging. Immunobiology 219:482-485. http://dx.doi.org/10.1016/j.imbio.2014.02.008.
60. Renkema KR, Li G, Wu A, Smithey MJ, Nikolich-Zugich J. 2014. Two separate defects affecting true naive or virtual memory T cell precursors combine to reduce naive T cell responses with aging. J Immunol 192:151-159. http://dx.doi.org/10.4049/jimmunol.1301453.