613
Views
24
CrossRef citations to date
0
Altmetric
Reviews

Synergy between Th1 and Th2 responses during Mycobacterium tuberculosis infection: A review of current understanding

The paper discusses the importance of simultaneous induction of Th1/Th2 responses to design and develop vaccine against TB

Pages 172-179 | Received 10 Jan 2019, Accepted 11 Jun 2019, Published online: 27 Jun 2019

References

  • World Health Organization (WHO). Global Tuberculosis report, Geneva, Switzerland; 2018.
  • Pai M, Dewan P. Testing and treating the missing millions with tuberculosis. PLOS Med 2015;12(3):e1001805. doi:10.1371/journal.pmed.1001805.
  • Fox GJ, Orlova M, Schurr E. Tuberculosis in Newborns: lessons of the “Lubeck disaster” (1929-1933). PLOS Pathog 2016;12(1):e1005271. doi:10.1371/journal.ppat.1005271.
  • Fine PA, Cameiro IAM, Milstein J, Clements CJ. Issues relating to the use of BCG in immunization programes. A discussion document. WHO/V & B/99.23. Geneva: World Health Organization; 1999.
  • Food and Drug Administration, Guidelines for Industry: for the evaluation of combinations of vaccines for preventable diseases: production, testing and clinical studies, Silver Springs; US Department of Health and Human Services, Food and Drug Administration, Centre for Biologics Evaluation and Research; 1997.
  • Doherty M, Wallis RS, Zumla A. Biomarkers for tuberculosis disease status and diagnosis. Curr Opin Pulm Med 2009;15(3):181–187.
  • Al-Attiyah R, Musta A, Abal AT. Restoration of mycobacterial antigen-induced proliferation and interferon-gamma responses in peripheral mononuclear cells of tuberculosis patients upon effective chemotherapy. FFMS Immunol Med Microbiol 2003;38(3):249–256. doi:10.1016/S0928-8244(03)00166-4.
  • Carrara S, Vincenti D, Petrosillo N. Use of T cell based assay for monitoring efficacy of antituberculosis therapy. Clin Infect Dis 2004;38(5):754–756. doi:10.1086/381754.
  • Abebe F, Belay M, Legesse M, Mihret A, Franken KS. Association of ESAT-6/CFP-10-induced IFN-γ, TNF-α and IL-10 with clinical tuberculosis: evidence from cohorts of pulmonary tuberculosis patients, household contacts and community controls in an endemic setting. Clin Exp Immunol 2017;189(2):241–249. doi:10.1111/cei.12972.
  • Belay M, Legesse M, Mihret A, et al. Pro-and anti-inflammatory cytokines against RV2031 are elevated during latent tuberculosis: a study in cohorts of tuberculosis patients, household contacts and community controls in an endemic setting. PLOS One 2015;10(4):e0124134. doi:10.1371/journal.pone.0124134.
  • Legesse M, Ameni G, Mamo G, Medhin G, Bjune G, Abebe F. Association of the level of IFN-g produced by T cells in response to Mycobacterium tuberculosis-specific antigens with the size of skin indurations among individuals with latent tuberculosis in a highly tuberculosis-endemic setting. Int Immunol. 2012;24(2):71–78. doi:10.1093/intimm/dxr102.
  • Gosset J. Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob Agents Chemother 2003;47:833–836.
  • McDonough KA, Kress Y, Bloom RR. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 1993;61:2763–2773.
  • Cardona PJ. A dynamic reinfection hypothesis of latent tuberculosis infection. Infection 2009;37(2):80–86. doi:10.1007/s15010-008-8087-y.
  • Weed LA, Baggenstoss AH. The isolation of pathogens from tissues of embalmed human bodies. Am J Clin Pathol 1951;21(12):1114–1120. doi:10.1093/ajcp/21.12.1114.
  • Write RC. Mycobacterium tuberculosis in pasteurized milk. BMJ 1967;2:108.
  • El Khechine A, Henry M, Raouly D, Drancourt M. Detection of Mycobacterium tuberculosis complex organisms in the stools of patients with pulmonary tuberculosis. Microbiology 2009;155(7):2384–2389. doi:10.1099/mic.0.026484-0.
  • Ghodbane R, Drancourt M. Non-human sources of Mycobacterium tuberculosis. Tuberculosis (Edinb) 2013;93(6):589–595. doi:10.1016/j.tube.2013.09.005.
  • De Jonge MI, Pehau-Arnaudet G, Fretz MM. ESAT-6 from Mycobacterium tuberculosis dissociates from its putative cheprone CFP-10 under acidic conditions and exhibits membrane-lysing activity. J Bacteriol 2007;16:6028–6034. doi:10.1128/JB.00469-07.
  • Lu LL, Chung AW, Rosebrock T, Gebremichael M, Yu WH, Grace PS. A functional role for antibodies in Tuberculosis. Cell 2016;167(2):433–443. doi:10.1016/j.cell.2016.08.072.
  • Jacob AJ, Mongkolsapaya J, Screaton GR, McShane H, Wilkinson RJ. Antibodies and tuberculosis. Tuberculosis (Edinb) 2016;101:102–113. doi:10.1016/j.tube.2016.08.001.
  • Moore T, Ekworomadu C, Eko F. Fc receptor-mediated antibody regulationof T cell immunity against intracellular pathogens. J Infect Dis 2003;188(4):617–624. doi:10.1086/377134.
  • Casadevall A. To be or not Be a (Functional) antibody against TB. Cell 2016;167(2):306–307. doi:10.1016/j.cell.2016.09.041.
  • Zimmermann N, Thormann V, Hu Bo Kohler AB, Imai-Matsushima A, Locht C. Human isotype-dependent inhibitory antibody responses against Mycobacterium tuberculosis. EMBO Mol Med 2016;8(11):1325–1339. doi:10.15252/emmm.201606330.
  • Zenteno-Cuevas R. Successes and failures in human tuberculosis vaccine development. Exp Opin Biol Ther 2017;17(12):1481–1491. doi:10.1080/14712598.2017.1378641.
  • Cooper AM, Flynn JL. The protective immune response to Mycobacterium tuberculosis. Curr Opin Immunol 1995;7(4):512–516. doi:10.1016/0952-7915(95)80096-4.
  • Flynn JL, Chan J, Triebold KJ. An essential role for interferon-gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 1993;178(6):2249–2254. doi:10.1084/jem.178.6.2249.
  • Kaufmann SH. Future vaccination strategies against tuberculosis: thinking outside the box. Immunity 2010;33(4):567–577. doi:10.1016/j.immuni.2010.09.015.
  • Goonetilleke NP, McShane H, Hannan CM, Anderson RJ, Brookes RH, Hill AVS. Enhanced immunogenicity and protective efficacy against Mycobacterium tuberculosis of bacilli Calmette-Guerin vaccine using mucosal administration and boosting with a recombinant modified vaccinia virus Ankara. J Immunol 2003;171(3):1602–1609. doi:10.4049/jimmunol.171.3.1602.
  • Sharpe SA, McShane H, Dennis MJ, et al. Establishment of an aerosol challenge model of tuberculosis in rhesus macaques and an evaluation of endpoints for vaccine testing. Clin Vaccine Immunol 2010;17(8):1170–1182. doi:10.1128/CVI.00079-10.
  • Tameris MD, Hatherill M, Landry BS, et al. MVA85A 020 Trial Study Team. Safety and efficacy of MVA85A, a new tuberculosis vaccine in infants previously vaccinated with BCG: a randomized placebo controlled phase 2b trail. Lancet 2013;381(9871):1021–1028. doi:10.1016/S0140-6736(13)60177-4.
  • Ndiaye BP, Thienemann F, Ota M. MVA85A o30 trial investigators. Safety, immunogenicity, and efficacy of the candidate tuberculosis vaccine MVA85A in healthy adults infected with HIV-1: a randomized placebo-controlled, phase 2 trial. Lancet Respir Med 2015;3(3):190–200. doi:10.1016/S2213-2600(15)00037-5.
  • Ernst JD. Mechanisms of M. tuberculosis immune evasion as challenges to TB vaccine design. Cell Host Microbe 2018;24(1):34–42. doi:10.1016/j.chom.2018.06.004.
  • Kagina BMN, Abel B, Scriba TJ. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guerin vaccination of newborns. Am J Respir Crit Care Med 2010;182(8):1073–1079. doi:10.1164/rccm.201003-0334OC.
  • Glatman-Freedman A, Casadevall A. Serum therapy for tuberculosis revisited: reappraisal of the role of antibody-mediated immunity against Mycobacterium tuberculosis. Clin Microbiol Rev 1998;11(3):514–532.
  • Casdevall A. Antibodies to Mycobacterium tuberculosis. 2017. N Eng J Med 2017;376:283–285.
  • Bennekov T, Dietrich J, Rosenkrands I, et al. Aletrations of epitope recognition pattern in Ag85A and ESAT-6 has a profound influence on vaccine-induced protection against Mycobacterium tuberculosis. Eur J Immunol 2006;36(12):3346. doi:10.1002/eji.200636128.
  • Belay M, Legesse M, Mihret A, et al. IFNγand IgA against non-methylated heparin-binding hemagglutnin as marker of protective immunity and latent tuberculosis: results of a longitudinal study from an endemic setting. J Infect 2016;72(2):189–200. doi:10.1016/j.jinf.2015.09.040.
  • Guerrero GG, Feunou FP, Locht C. The coiled-coil N.terminal domain of the heparin-binding haemagglutnin is required for humoral and cellular immune responses. Mom Immunol 2008;46(1):116–124. doi:10.1016/j.molimm.2008.07.009.
  • Aleyed E. the Era of the immunoglobulin A Fc receptor FcaRI: its function and potential as target in disease. Immunol Rev 2015;268:123–138.
  • Wang JL, Li TT, Elsheikha HM, et al. Live attenuated Pru cdpk2 strain of Toxoplasma gondii protects against acute, chronic, and congenital toxoplasmosis. J Infect Dis 2018; XX (XX XXXX):1–10.
  • Chen Y, Yu M, Hemandez JA, Li J, Yuan Z-G, Yan H. Immuno-efficacy of DNA vaccines encoding PLP1 and ROP18 against experimental Toxoplasma gondii infection in mice. Exp Parasitol 2018;188:73–76. doi:10.1016/j.exppara.2018.04.003.
  • Bayih AG, Daifalla NS, Gedamu L. Immune response and protective efficacy of a heterologous DNA-protein immunization with Leishmania superoxide dismutase B1. Biomed Res Int 2017. doi:10.1155/2017/2145386.
  • McManus DP, Loukas A. Current status of vaccines for schistosomiasis. Clin Microbiol Rev 2008;21(1):225–242. doi:10.1128/CMR.00046-07.
  • Yang Z, Li W, Yang Z, Pan A, Liao W, Zhou X. A novel antigenic cathepsin B protease induces protective immunity in Trichinella spiralis. Vaccine 2018;36(2):248–255. doi:10.1016/j.vaccine.2017.11.048.
  • Feng L, Niu X, Mei W, et al. Immunogenicity and protective efficacy of EF-Tu and FtsZ of Streptococcus Suis serotype 2 against lethal infection. Vaccine 2018;36(19):2581–2588. doi:10.1016/j.vaccine.2018.03.079.
  • Abkar M, Fasihi-Ramandi M, Koshki H, Lotfi AS. Interperitoneal immunization with Urease loaded N-trimethyl chitosan melitensis and Brucella abortus infections. Immunol Lett. 2018;199:53–60. doi:10.1016/j.imlet.2018.03.004.
  • Im YB, Park WB, Jung M, Kim S, Yoo HS. Evaluation of Th1/Th2-related immune response against recombinant proteins of Brucella abortus infection in mice. J Microbiol Biotechnol. 2016;26(6):1132–1139. doi:10.4014/jmb.1512.12046.
  • Chu CY, Liu CH, Liou JJ, Lee JW, Cheng LT. Development of a subunit vaccine containing recombinant Riemerella anatipestifer outer membrane protein A and CpG ODN adjuvant. Vaccine 2015;33(1):92–99. doi:10.1016/j.vaccine.2014.11.010.
  • Raeven RH, Brummelman J, Pennings JL, van der Maas L, Tilstra W, Helm K. Bordetella pertussis outer membrane visicle vaccine confers equal efficacy in mice with milder inflammatory responses compared to a whole-cell vaccine. Sci Rep 2016;6:1–15. doi:10.1038/srep38240.
  • Jiang H, Hu Y, Yang M, Liu H, Jian G. Enhanced immune response to a dual-promoter anti-caries DNA vaccine orally delivered by attenuated Salmonella typhimurium. Immunobiology 2017;222(5):730–737. doi:10.1016/j.imbio.2017.01.007.
  • Adams GP, Weiner LM. Monoclonal antibody therapy of cancer. Nat Biotechnol. 2005;23(9):1147–1157. doi:10.1038/nbt1137.
  • Nimmerjahn F, Ravetch JV. Antibodies, Fc receptors and cancer. Curr Opin Immunol. 2007;19(2):239–245. doi:10.1016/j.coi.2007.01.005.
  • Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med. 2000;6(4):443–446. doi:10.1038/74704.
  • Weng WK, Levy R. Two immunoglobulin fragment C receptors polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 2003;21(21):3940–3947. doi:10.1200/JCO.2003.05.013.
  • Zhang M, Wen B, Anton OM, Yao Z, Dubois S, Ju W. IL-15 enhanced antibody-dependent cellular cytotoxicity mediated by NK and macrophages. Proc Natl Acad Sci USA 2018;46:E10915–E10924. doi:10.1073/pnas.1811615115.
  • Wittrup KD. Antitumor antibodies can drive therapeutic T cell responses. Trends Cancer 2017;3(9):615–620. doi:10.1016/j.trecan.2017.07.001.
  • Ackhar JM, Chan J, Casadevall A. B cells and antibodies in the defence against Mycobacterium tuberculosis infection. Immunol Rev 2015;264:167–181. doi:10.1111/imr.12276.
  • Abebe F, Bjune G. the protective role of antibody responses during Mycobacterium tuberculosis infection. Clin Exp Immunol 2009;157(2):235–243. doi:10.1111/j.1365-2249.2009.03967.x.
  • Igietseme JU, Eko FO, He Q, Black CM. Antibody regulation of T cell immunity: implications for vaccine strategies against intracellular pathogen. Exp Rev Vaccines 2004;3(1):23–34. doi:10.1586/14760584.3.1.23.
  • de Vallière S, Abate G, Blazevic A, Heuertz RM, Hoft DF. Enhancement of innate and cell-mediated immunity by antimycobacterial antibodies. Infect Immun 2005;73(10):6711–6720. doi:10.1128/IAI.73.10.6711-6720.2005.
  • Brown RM, Cruz O, Brennan M, et al. Lipoarabinomannan-reactive human secretory immunoglobulin response induced by muosal bacilli Calmette-Guerin vaccination. J Infect Dis 2003;187(3):513–517. doi:10.1086/368096.
  • Chen T, Blanc C, Eder AZ, Prados-Rosales R, Souza ACO, et al. Association of human antibodies to arabinomannan with enhanced mycobacterial opsono-phagocytosis and intracellular growth reduction. J Infect Dis 2016;214(2):300–310. doi:10.1093/infdis/jiw141.
  • Casadevall A, Pirofski LA. A reapraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv Immunol 2006;91:1–44.
  • Maglione PJ, Xu J, Casadevall A, Chen J. Fc gamma receptors regulate immune activation and susceptibility during Mycobacterium tuberculosis infection. J Immunol 2008;180(5):3329–3338. doi:10.4049/jimmunol.180.5.3329.
  • Sutherland JS, Loxton AG, Haks MC, et al. Differential gene expresion of activating Fcgamma receptor classifies active tuberculosis regardless of human immunodeficiency virus status or ethnicity. Clin Microbol Infect 2014;20:0230–0238.
  • Machado LR, Bowdrey J, Ngaimisi E, et al. Copy number variation of Fc gamma receptor gene in HIV infected and HIV-tuberculosis co-infected individuals in sub-Saharan Africa. Plos One 2013;8(11):e78165. doi:10.1371/journal.pone.0078165.
  • Hutching CL, Gilbert SC, Hill AVS, Moore AC. Novel protein and poxvirus-based vaccine combinations for simultaneous induction of humoral and cell-mediated immunity. J Immunol 2005;175:599–606. doi:10.4049/jimmunol.175.1.599.
  • Phumiamorn S, Sato H, Kamiyama T, Kurokawa M, Shiraki K. Induction of humoral and cell-mediated immunity to hepatitis B surface antigen by a novel adjuvant activity of Oka varicella vaccine. J Gen Virol 2003;84(Pt 2):287–291. doi:10.1099/vir.0.18692-0.
  • Letvin NL, Barouch DH, Montefiori DC. Prospects for vaccine protection against HIV-1 infection and AIDS. Annu Rev Immunol. 2002;20:73–99. doi:10.1146/annurev.immunol.20.081501.094854.
  • Srivastava IK, Liu MA. Gene vaccines. Ann Intern Med 2003;138(7):550–559.
  • Bachmann MF, Hengartner H, Zinkernagel RM. Immunization with recombinant protein: conditions for cytotoxic T cell and/or antibody induction. Med Microbiol Immunol 1994;183(6):315–324.
  • Agger EM, Cassidy JP, Brady J, Korsholm KS, Vingsbo-Lundberg C, Andersen P. Adjuvant modulation of cytokine balance in Mycobacterium tuberculosis subunit vacines; immunity, pathology and protection. Immunology 2008;124(2):175–185.
  • Lagranderie M, Balazuc A-M, Abolhassani M, et al. Development of mixed Th1/Th2 type immune response and protection against Mycobacterium tuberculosis after rectal or subcutaneous immunization of newborn and adult mice with Mycobacterium bovis BCG. Scand J Immunol 2002;55(3):293–303.
  • Tanghe A, Denis O, Lambrecht B, Motte V, van den Berg T, Huygen K. Tuberculosis DNA vaccine encoding ag85A is immunogenic and protective when administered by intramuscular needle injection but not by epidermal gene gun bombardment. Infect Immun 2000;68(7):3854–3860. doi:10.1128/iai.68.7.3854-3860.2000.
  • Power CA, Wei G, Bretscher PA. Mycobacterial dose defines the Th1/Th2 nature of immune response independently of whether immunization is administered by intravenous, subcutaneous or intradermal route. Infect Immun 1998;66(12):5743–5749.
  • Donnelly JJ, Ulmer JB, Liu MA. Immunization with DNA. J Immunol Methods 1994;176(2):145–152.
  • Bachmann MF, Kündig TM, Kalberer CP, Hengartner H, Zinkernagel RM. Formalin inactivation of vesicular stomatitis virus impairs T cell but not T help independent B cell responses. J Virol 1993;67(7):3917–3922.
  • Huygen K, Content J, Denis O, et al. Immunogenicity and protective efficacy of tuberculosis DNA vaccine. Nat Med 1996;2(8):893–898.
  • Sjetske K, Huber R, Hendriks M, Ronald H, Jacob J, van de K. Immunogenicity of influenza vaccines: evidence for differential effect of secondary vaccination on humoral and cell-mediated immunity. Front Immunol 2019;9:1–12.
  • Kim SK, Ragupathi G, Musselli C, Choi S-J, Park YS, Livingston PO. Comaprison of the effect of different immunological adjuvants on the antibody and T-cell response to immunization with MUCI-KLH and GD3-KLH conjugate cancer vaccines. Vaccine 1999;18(7–8):597–603. doi:10.1016/S0264-410X(99)00316-3.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.