High mobility group box 1 acts as an adjuvant for tuberculosis subunit vaccines

Immunology

Volumn 142, Issue 1, 2014, Pages 111-123

  Grover, Ajay ^a   Troudt, Jolynn ^a   Foster, Chad ^a   Basaraba, Randall ^a   Izzo, Angelo ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Adjuvants; Antigen presentation; Infection; T cells; Tuberculosis; Vaccines

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; BCG VACCINE; BROMINE DERIVATIVE; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR7; DIOCTADECYLAMMONIUM BROMIDE; DNA VACCINE; EARLY SECRETORY ANTIGENIC TARGET 6; GAMMA INTERFERON; HERMES ANTIGEN; HIGH MOBILITY GROUP B1 PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN EARLY SECRETORY ANTIGENIC TARGET 6 FUSION PROTEIN; HYBRID PROTEIN; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 2; L SELECTIN; PHOSPHORYL LIPID A; SUBUNIT VACCINE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL LOAD; BCG VACCINATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SUSPENSION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; DNA IMMUNIZATION; DRUG FORMULATION; ERYTHROCYTE; FEMALE; FLOW CYTOMETRY; IMMUNOPROPHYLAXIS; LUNG ALVEOLUS CELL; MEMORY T LYMPHOCYTE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE DRUG DOSE; SPLEEN CELL; TH1 CELL; TUBERCULOSIS; VACCINATION;

ADJUVANTS; ANTIGEN PRESENTATION; INFECTION; T CELLS; TUBERCULOSIS; VACCINES;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HMGB1 PROTEIN; IMMUNITY, CELLULAR; IMMUNOLOGIC MEMORY; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; RECOMBINANT FUSION PROTEINS; TH1 CELLS; TIME FACTORS; TUBERCULOSIS VACCINES; TUBERCULOSIS, PULMONARY; VACCINES, SUBUNIT;

EID: 84898007190     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12236     Document Type: Article

References (57)

1. Brennan MJ, Thole J. Tuberculosis vaccines: a strategic blueprint for the next decade. Tuberculosis (Edinb) 2012; 92(Suppl. 1):S6-13.
2. Ernst JD. The immunological life cycle of tuberculosis. Nat Rev Immunol 2012; 12:581-91.
3. Leroux-Roels G. Unmet needs in modern vaccinology: adjuvants to improve the immune response. Vaccine 2010; 28(Suppl. 3):C25-36.
4. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009; 22:240-73.
5. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukocyte Biol 2007; 81:1-5.
6. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11:373-84.
7. Bluestone JA, Mackay CR, O'Shea JJ, Stockinger B. The functional plasticity of T cell subsets. Nat Rev Immunol 2009; 9:811-6.
8. Lanzavecchia A, Sallusto F. The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics. Curr Opin Immunol 2001; 13:291-8.
9. Tang D, Kang R, Coyne CB, Zeh HJ, Lotze MT. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev 2012; 249:158-75.
10. Miyaji EN, Carvalho E, Oliveira ML, Raw I, Ho PL. Trends in adjuvant development for vaccines: DAMPs and PAMPs as potential new adjuvants. Braz J Med Bio Res 2011; 44:500-13.
11. Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immun Cell Bio 2004; 82:488-96.
12. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5:331-42.
13. Ulloa L, Messmer D. High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev 2006; 17:189-201.
14. Messmer D, Yang H, Telusma G, Knoll F, Li J, Messmer B, Tracey KJ, Chiorazzi N. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 2004; 173:307-13.
15. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Bio Chem 2004; 279:7370-7.
16. Dumitriu IE, Baruah P, Valentinis B et al. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 2005; 174:7506-15.
17. Park JS, Gamboni-Robertson F, He Q et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 2006; 290:C917-24.
18. Kokkola R, Andersson A, Mullins G et al. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol 2005; 61:1-9.
19. Rovere-Querini P, Capobianco A, Scaffidi P et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 2004; 5:825-30.
20. Muthumani G, Laddy DJ, Sundaram SG et al. Co-immunization with an optimized plasmid-encoded immune stimulatory interleukin, high-mobility group box 1 protein, results in enhanced interferon-γ secretion by antigen-specific CD8 T cells. Immunol 2009; 128:e612-20.
21. Fagone P, Shedlock DJ, Bao H et al. Molecular adjuvant HMGB1 enhances anti-influenza immunity during DNA vaccination. Gene Ther 2011; 18:1070-7.
22. Grover A, Taylor J, Troudt J, Keyser A, Sommersted K, Schenkel A, Izzo AA. Mycobacterial infection induces the secretion of high-mobility group box 1 protein. Cell Microbiol 2008; 10:1390-404.
23. Brandt L, Elhay M, Rosenkrands I, Lindblad EB, Andersen P. ESAT-6 subunit vaccination against Mycobacterium tuberculosis. Infect Immun 2000; 68:791-5.
24. Olsen AW, Hansen PR, Holm A, Andersen P. Efficient protection against Mycobacterium tuberculosis by vaccination with a single subdominant epitope from the ESAT-6 antigen. Eur J Immunol 2000; 30:1724-32.
25. Weinrich Olsen A, van Pinxteren LA, Meng Okkels L, Birk Rasmussen P, Andersen P. Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85b and ESAT-6. Infect Immun 2001; 69:2773-8.
26. Aagaard C, Hoang T, Dietrich J et al. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 2011; 17:189-94.
27. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon-γ gene-disrupted mice. J Exp Med 1993; 178:2243-7.
28. Hilgers LA, Snippe H. DDA as an immunological adjuvant. Res Immunol 1992; 143:494-503; discussion 74-6.
29. Langermans JA, Doherty TM, Vervenne RA et al. Protection of macaques against Mycobacterium tuberculosis infection by a subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Vaccine 2005; 23:2740-50.
30. Izzo A, Brandt L, Lasco T, Kipnis AP, Orme I. NIH pre-clinical screening program: overview and current status. Tuberculosis 2005; 85:25-8.
31. Billeskov R, Elvang TT, Andersen PL, Dietrich J. The HyVac4 subunit vaccine efficiently boosts BCG-primed anti-mycobacterial protective immunity. PLoS One 2012; 7:e39909.
32. Garcon N, Chomez P, Van Mechelen M. GlaxoSmithKline Adjuvant Systems in vaccines: concepts, achievements and perspectives. Exp Rev Vaccines 2007; 6:723-39.
33. Baldrick P, Richardson D, Elliott G, Wheeler AW. Safety evaluation of monophosphoryl lipid A (MPL): an immunostimulatory adjuvant. Reg Toxicol Pharm 2002; 35:398-413.
34. Mizel SB, Bates JT. Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 2010; 185:5677-82.
35. Eckl-Dorna J, Batista FD. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood 2009; 113:3969-77.
36. Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, Beverley PC, Tchilian EZ. Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J Immunol 2008; 181:4955-64.
37. Lindenstrom T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, Seder RA, Rosenkrands I, Andersen P. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol 2009; 182:8047-55.
38. + T cell responses directed to dominant and subdominant epitopes in ESAT-6 from Mycobacterium tuberculosis. J Immunol 2009; 183:2659-68.
39. Hoang TT, Nansen A, Roy S, Billeskov R, Aagaard C, Elvang T, Dietrich J, Andersen P. Distinct differences in the expansion and phenotype of TB10.4 specific CD8 and CD4 T cells after infection with Mycobacterium tuberculosis. PLoS One 2009; 4:e5928.
40. Dumitriu IE, Bianchi ME, Bacci M, Manfredi AA, Rovere-Querini P. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J leuokocyte Biol 2007; 81:84-91.
41. Grover A, Ahmed MF, Singh B, Verma I, Sharma P, Khuller GK. A multivalent combination of experimental antituberculosis DNA vaccines based on Ag85B and regions of difference antigens. Microb Infect 2006; 8:2390-9.
42. Romano M, Huygen K. DNA vaccines against mycobacterial diseases. Exp Rev Vaccines 2009; 8:1237-50.
43. + T cells after airborne M. tuberculosis infection. J Exp Med 2008; 205:2359-68.
44. Rock KL, Hearn A, Chen CJ, Shi Y. Natural endogenous adjuvants. Spring Sem Immunopath 2005; 26:231-46.
45. Lamb JR, Bal V, Mendez-Samperio P et al. Stress proteins may provide a link between the immune response to infection and autoimmunity. Intl Immunol 1989; 1:191-6.
46. Munk ME, Schoel B, Modrow S, Karr RW, Young RA, Kaufmann SH. T lymphocytes from healthy individuals with specificity to self-epitopes shared by the mycobacterial and human 65-kilodalton heat shock protein. J Immunol 1989; 143:2844-9.
47. Schwartz RH. Acquisition of immunologic self-tolerance. Cell 1989; 57:1073-81.
48. van Eden W, Thole JE, van der Zee R, Noordzij A, van Embden JD, Hensen EJ, Cohen IR. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature 1988; 331:171-3.
49. Young D, Lathigra R, Hendrix R, Sweetser D, Young RA. Stress proteins are immune targets in leprosy and tuberculosis. Proc Natl Acad Sci USA 1988; 85:4267-70.
50. Plotz PH. The autoantibody repertoire: searching for order. Nat Immunol 2003; 3:73-8.
51. Sanford AN, Dietzmann K, Sullivan KE. Apoptotic cells, autoantibodies, and the role of HMGB1 in the subcellular localization of an autoantigen. J Autoimmun 2005; 25:264-71.
52. Barnay-Verdier S, Fattoum L, Borde C, Kaveri S, Gibot S, Marechal V. Emergence of autoantibodies to HMGB1 is associated with survival in patients with septic shock. Inten Care Med 2011; 37:957-62.
53. Tian J, Avalos AM, Mao SY et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007; 8:487-96.
54. Telusma G, Datta S, Mihajlov I et al. Dendritic cell activating peptides induce distinct cytokine profiles. Int Immunol 2006; 18:1563-73.
55. Saenz R, Souza Cda S, Huang CT, Larsson M, Esener S, Messmer D. HMGB1-derived peptide acts as adjuvant inducing immune responses to peptide and protein antigen. Vaccine 2010; 28:7556-62.
56. Yang H, Hreggvidsdottir HS, Palmblad K et al. A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc Natl Acad Sci USA 2010; 107:11942-7.
57. McShane H, Jacobs WR, Fine PE, Reed SG, McMurray DN, Behr M, Williams A, Orme IM. BCG: myths, realities, and the need for alternative vaccine strategies. Tuberculosis (Edinb) 2012; 92:283-8.