Nasal vaccination stimulates CD8+ T cells for potent protection against mucosal Brucella melitensis challenge

Immunology and Cell Biology

Volumn 94, Issue 5, 2016, Pages 496-508

  Clapp, Beata ^a   Yang, Xinghong ^a   Thornburg, Theresa ^b   Walters, Nancy ^b   Pascual, David W ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRUCELLA MELITENSIS VACCINE; BRUCELLA VACCINE; CHEMOKINE RECEPTOR CCR7; CYTOKINE; GAMMA INTERFERON; GRANZYME B; HERMES ANTIGEN; INTERLEUKIN 17; L SELECTIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; BACTERIAL VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIAL VIRULENCE; BRUCELLA MELITENSIS; BRUCELLOSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; FEMALE; IMMUNIZATION; IN VIVO STUDY; LUNG; LUNG INFECTION; LYMPH NODE; MEMORY T LYMPHOCYTE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PROTEIN FOLDING; RESPIRATORY SYSTEM; SPLEEN; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; NOSE MUCOSA; PATHOLOGY; PHYSIOLOGY; VACCINATION;

ANIMALS; BACTERIAL VACCINES; BRUCELLA MELITENSIS; BRUCELLOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; FEMALE; IMMUNOLOGIC MEMORY; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; LUNG; MICE, INBRED BALB C; MICE, INBRED C57BL; NASAL MUCOSA; SPLEEN; VACCINATION;

EID: 84956932108     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.5     Document Type: Article

References (67)

1. Corbel M. Brucellosis: an overview. Emerg Infect Dis 1997; 3: 213-221
2. Whatmore AM. Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect Genet Evol 2009; 9: 1168-1184
3. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. The new global map of human brucellosis. Lancet Infect Dis 2006; 6: 91-99
4. Dean AS, Crump L, Greter H, Schelling E, Zinsstag J. Global burden of human brucellosis: a systematic review of disease frequency. PLoS Negl Trop Dis 2012; 6: e1865
5. Roth F, Zinsstag J, Orkhon D, Chimed-Ochir G, Hutton G, Cosivi O, et al. Human health benefits from livestock vaccination for brucellosis: case study. Bull World Health Organ 2003; 81: 867-876
6. Yang X, Skyberg JA, Cao L, Clapp B, Thornburg T, Pascual DW. Progress in Brucella vaccine development. Front Biol (Beijing) 2013; 8: 60-77
7. Alexander B, Schnurrenberger PR, Brown RR. Numbers of Brucella abortus in the placenta, umbilicus and fetal fluid of two naturally infected cows. Vet Rec 1981; 108: 500
8. Godfroid J, Scholz HC, Barbier T, Nicolas C, Wattiau P, Fretin D, et al. Brucellosis at the animal/ecosystem/human interface at the beginning of the 21st century. Prev Vet Med 2011; 102: 118-131
9. Gorvel JP, Moreno E, Moriyon I. Is Brucella an enteric pathogen?. Nat Rev Microbiol 2009; 7: 250
10. Olsen SC. Recent developments in livestock and wildlife brucellosis vaccination. Rev Sci Technol 2013; 32: 207-217
11. Dabral N, Moreno-Lafont M, Sriranganathan N, Vemulapalli R. Oral immunization of mice with gamma-irradiated Brucella neotomae induces protection against intraperitoneal and intranasal challenge with virulent B. abortus 2308. PLoS ONE 2014; 9: e107180
12. Clapp B, Skyberg JA, Yang X, Thornburg T, Walters N, Pascual DW. Protective live oral brucellosis vaccines stimulate Th1 and Th17 cell responses. Infect Immun 2011; 79: 4165-4174
13. Izadjoo MJ, Bhattacharjee AK, Paranavitana CM, Hadfield TL, Hoover DL. Oral vaccination with Brucella melitensis WR201 protects mice against intranasal challenge with virulent Brucella melitensis 16M. Infect Immun 2004; 72: 4031-4039
14. Pasquali P, Rosanna A, Pistoia C, Petrucci P, Ciuchini F. Brucella abortus RB51 induces protection in mice orally infected with the virulent strain B. abortus 2308. Infect Immun 2003; 71: 2326-2330
15. González-González E, García-Hernàndez AL, Flores-Mejía R, López-Santiago R, Moreno-Fierros L. The protoxin Cry1Ac of Bacillus thuringienis improves the protection conferred by intranasal immunization with Brucella abortus RB51 in a mouse model. Vet Microbiol 2015; 175: 382-388
16. Surendran N, Sriranganathan N, Lawler H, Boyle SM, Hiltbold EM, Heid B, et al. Efficacy of vaccination strategies against intranasal challenge with Brucella abortus in BALB/c mice. Vaccine 2011; 29: 2749-2755
17. Surendran N, Sriranganathan N, Boyle SM, Hiltbolt EM, Tenpenny N, Walker M, et al. Protection to respiratory challenge of Brucella abortus strain 2308 in the lung. Vaccine 2013; 31: 4103-4110
18. Zhan Y, Cheers C. Control of IL-12 and IFN-? in response to live or dead bacteria by TNF and other factors. J Immunol 1998; 161: 1447-1453
19. Skyberg JA, Thornburg T, Rollins MC, Huarte E, Jutila M, Pascual DW. Murine and bovine 'd T cells enhance innate immunity against Brucella abortus infections. PLoS ONE 2011; 6: e21978
20. He Y, Vemulapalli R, Zeytun A, Schurig GG. Induction of specific cytotoxic lymphocytes in mice vaccinated with Brucella abortus RB51. Infect Immun 2001; 69: 5502-5508
21. Pasquevich KA, Estein SM, Garcia Samartino C, Zwerdling A, Coria LM, Barrionuevo P, et al. Immunization with recombinant Brucella species outer membrane protein OMP16 or OMP19 in adjuvant induces specific CD4+ and CD8+ T cells as well as systemic and oral protection against Brucella abortus infection. Infect Immun 2009; 77: 436-445
22. Goel D, Rajendran V, Ghosh PC, Bhatnagar R. Cell mediated immune response after challenge in Omp25 liposome immunized mice contributes to protection against Brucella abortus 544. Vaccine 2013; 31: 1231-1237
23. Vitry MA, Hanot Mambres D, De Trez C, Akira S, Ryffel B, Letesson JJ, et al. Humoral immunity and CD4+ Th1 cells are both necessary for a fully protective immune response upon secondary infection with Brucella melitensis. J Immunol 2014; 192: 3740-3752
24. Vitry MA, De Trez C, Goriely S, Dumoutier L, Akira S, Ryffel B, et al. 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 2012; 80: 4271-4280
25. Yingst SL, Izadjoo M, Hoover DL. CD8 knockout mice are protected from challenge by vaccination with WR201, a live attenuated mutant of Brucella melitensis. Clin Dev Immunol 2013; 2013: 686919
26. Oliveira SC, Harms JS, Banai M, Splitter GA. Recombinant Brucella abortus proteins that induce proliferation and gamma-interferon secretion by CD4+ T cells from Brucella-vaccinated mice and delayed-Type hypersensitivity in sensitized guinea pigs. Cell Immunol 1993; 172: 262-268
27. Oliveira SC, Splitter GA. CD8+ type 1 CD44hi CD45 RBlo T lymphocytes control intracellular Brucella abortus infection as demonstrated in major histocompatibility complex class I-And class II-deficient mice. Eur J Immunol 1995; 25: 2551-2557
28. Cassataro J, Velikovsky CA, de la Barrera S, Estein SM, Bruno L, Bowden R, et al. A DNA vaccine coding for the Brucella outer membrane protein 31 confers protection against B. melitensis and B. ovis infection by eliciting a specific cytotoxic response. Infect Immun 2005; 73: 6537-6546
29. Hu XD, Chen ST, Li JY, Yu DH, Zhang Y, Cai H. An IL-15 adjuvant enhances the efficacy of a combined DNA vaccine against Brucella by increasing the CD8+ cytotoxic T cell response. Vaccine 2010; 28: 2408-2415
30. Jain S, Afley P, Dohre SK, Saxena N, Kumar S. Evaluation of immunogenicity and protective efficacy of a plasmid DNA vaccine encoding ribosomal protein L9 of Brucella abortus in BALB/c mice. Vaccine 2014; 32: 4537-4542
31. Rajashekara G, Glover DA, Krepps M, Splitter GA. Temporal analysis of pathogenic events in virulent and avirulent Brucella melitensis infections. Cell Microbiol 2005; 7: 1459-1473
32. Santosuosso M, Zhang X, McCormick S, Wang J, Hitt M, Xing Z. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J Immunol 2005; 174: 7986-7994
33. Murphy EA, Sathiyaseelan J, Parent MA, Zou B, Baldwin CL. Interferon-? is crucial for surviving a Brucella abortus infection in both resistant C57BL/6 and susceptible BALB/c mice. Immunol 2001; 103: 511-518
34. Lazarevic V, Glimcher LH. T-bet in disease. Nat Immunol 2011; 12: 597-606
35. Corsetti PP, de Almeida LA, Carvalho NB, Azevedo V, Silva TM, Teixeira HC, et al. Lack of endogenous IL-10 enhances production of proinflammatory cytokines and leads to Brucella abortus clearance in mice. PLoS ONE 2013; 8: e74729
36. Pasquevich KA, Ibanez AE, Coria LM, Samartino SG, Estein SM, Zwerdling A, et al. An oral vaccine based on U-Omp 19 induces protection against B. abortus mucosal challenge by inducing an adaptive IL-17 immune response in mice. PLoS ONE 2011; 6: e16203
37. Hoover DL, Crawford RM, Van de Verg LL, Izadjoo MJ, Bhattacharjee AK, Paranavitana CM, et al. Protection of mice against brucellosis by vaccination with Brucella melitensis WR201 (16M?purEK). Infect Immun 1999; 67: 5877-5884
38. Kahl-McDonagh MM, Arenas-Gamboa AM, Ficht TA. Aerosol infection of BALB/c mice with Brucella melitensis and Brucella abortus and protective efficacy against aerosol challenge. Infect Immun 2007; 75: 4923-4932
39. Chen L, Wang J, Zganiacz A, Xing Z. Single intranasal mucosal Mycobacterium bovis BCG vaccination confers improved protection compared to subcutaneous vaccination against pulmonary tuberculosis. Infect Immun 2004; 72: 238-246
40. Paix'o TA, Roux CM, den Hartigh A, Sankaran-Walters S, Dandekar S, Santos R, et al. Establishment of systemic Brucella melitensis infection through the digestive tract requires urease, the type IV secretion system, and lipopolysaccharide O antigen. Infect Immun 2009; 77: 4197-4208
41. Ackermann MR, Cheville NF, Deyoe BL. Bovine ileal dome lymphoepithelial cells: endocytosis and transport of Brucella abortus strain 19. Vet Pathol 1988; 25: 28-35
42. Sangari FJ, Seoane A, Rodriguez MC, Aguero J, Garcia Lobo JM. Characterization of the urease operon of Brucella abortus and assessment of its role in virulence of the bacterium. Infect Immun 2007; 75: 774-780
43. Plommet M. Studies on experimental brucellosis in cows in France. In: R.M. Crawford and R.J. Hidalgo (Eds.) Bovine Brucellosis. Texas A&M Univ. Press: College Station, TX, USA and London, UK, 1977, pp 116-134
44. Zachou K, Papamichalis PA, Dalekos GN. Severe pharyngitis in stockbreeders: an unusual presentation of brucellosis. Occup Med (Lond) 2008; 58: 305-307
45. von Bargen K, Gagnaire A, Arce-Gorvel V, de Bovis B, Baudimont F, Chasson L, et al. Cervical lymph nodes as a selective niche for Brucella during oral infections. PLoS ONE 2015; 10: e121790
46. Davis SS. Nasal vaccines. Adv Drug Deliv Rev 2001; 51: 21-42
47. Skyberg JA, Thornburg T, Kochetkova I, Layton W, Callis G, Rollins MF, et al. IFN-?-deficient mice develop IL-1-dependent cutaneous and musculoskeletal inflammation during experimental brucellosis. J Leukoc Biol 2012; 92: 375-387
48. Kolls JK, Khader SA. The role of Th17 cytokines in primary mucosal immunity. Cytokine Growth Factor Rev 2010; 21: 443-448
49. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, Rangel-Moreno J, et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009; 31: 799-810
50. Bai H, Cheng J, Gao X, Joyee AG, Fan Y, Wang S, et al. IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J Immunol 2009; 183: 5886-5895
51. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, Cilley GE, et al. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007; 8: 369-377
52. Gopal R, Rangel-Moreno J, Slight S, Lin Y, Nawar HF, Fallert Junecko BA, et al. Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 2013; 6: 972-984
53. Orgun NN, Mathis MA, Wilson CB, Way SS. Deviation from a strong Th1-dominated to a modest Th17-dominated CD4 T cell response in the absence of IL-12p40 and type I IFNs sustains protective CD8 T cells. J Immunol 2008; 180: 4109-4115
54. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008; 14: 282-289
55. Graham AC, Carr KD, Sieve AN, Indramohan M, Break TJ, Berg RE. IL-22 production is regulated by IL-23 during Listeria monocytogenes infection but is not required for bacterial clearance or tissue protection. PLoS ONE 2011; 6: e17171
56. Paranavitana C, Zelazowska E, DaSilva L, Pittman PR, Nikolich M. Th17 cytokines in recall responses against Francisella tularensis in humans. J Interferon Cytokine Res 2010; 30: 471-476
57. Wilson MS, Feng CG, Barber DL, Yarovinsky F, Cheever AW, Sher A, et al. Redundant and pathogenic roles for IL-22 in mycobacterial, protozoan, and helminth infections. J Immunol 2010; 184: 4378-4390
58. Dhiman R, Periasamy S, Barnes PF, Garg Jaiswal A, Paidipally P, Barnes AB, et al. NK1.1+ cells and IL-22 regulate vaccine-induced protective immunity against challenge with Mycobacterium tuberculosis. J Immunol 2012; 189: 897-905
59. Peng Y, Gao X, Yang J, Shekhar S, Wang S, Fan Y, et al. Interleukin-22 promotes T helper 1 (Th1)/Th17 immunity in chlamydial lung infection. Mol Med 2014; 20: 109-119
60. Adone R, Francia M, Pistoia C, Petrucci P, Pesciaroli M, Pasquali P. Protective role of antibodies induced by Brucella melitensis B115 against B. melitensis and Brucella abortus infections in mice. Vaccine 2012; 30: 3992-3995
61. Durward M, Radhakrishnan G, Harms J, Bareiss C, Magnani D, Splitter GA. Active evasion of CTL mediated killing and low quality responding CD8+ T cells contribute to persistence of brucellosis. PLos ONE 2012; 7: e34925
62. Durward-Diioia M, Harms J, Khan M, Hall C, Smith JA, Splitter GA. CD8+ T cell exhaustion, suppressed gamma interferon production, and delayed memory response induced by chronic Brucella melitensis infection. Infect Immun 2015; 83: 4759-4771
63. Lanzavecchia A, Sallusto F. Dynamics of T lymphocyte responses: intermediates, effectors and memory cells. Science 2000; 290: 92-97
64. Obar JJ, Jellison ER, Sheridan BS, Blair DA, Pham QM, Zickovich JM, Lefrançois L. Pathogen-induced inflammatory environment controls effector and memory CD8+ T cell differentiation. J Immunol 2011; 187: 4967-4978
65. Unsoeld H, Pircher H. Complex memory T-cell phenotypes revealed by coexpression of CD62L and CCR7. J Virol 2005; 79: 4510-4513
66. Walters N, Trunkle T, Sura M, Pascual DW. Enhanced immunoglobulin A response and protection against Salmonella enterica serovar Typhimurium in the absence of the substance P receptor. Infect Immun 2005; 73: 317-324
67. Abboud G, Tahiliani V, Desai P, Varkoly K, Driver J, Hutchinson TE, Salek-Ardakani S. Natural killer cells and innate IFN-' participate in host defense against respiratory vaccinia virus infection. J Virol 2015; 90: 129-141