2,634
Views
49
CrossRef citations to date
0
Altmetric
BRIEF REPORT

IFNG-mediated immune responses enhance autophagy against Mycobacterium tuberculosis antigens in patients with active tuberculosis

, , , , , , , , , & show all
Pages 2109-2121 | Received 16 Jan 2014, Accepted 06 Oct 2014, Published online: 28 Jan 2015

References

  • Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 1993; 178:2243-7; PMID:8245795; http://dx.doi.org/10.1084/jem.178.6.2243
  • Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 1993; 178:2249-54; PMID:7504064; http://dx.doi.org/10.1084/jem.178.6.2249
  • Newport MJ, Huxley CM, Huston S, Hawrylowicz CM, Oostra BA, Williamson R, Levin M. A mutation in the interferon-gamma-receptor gene and susceptibility to mycobacterial infection. N Engl J Med 1996; 335:1941-9; PMID:8960473; http://dx.doi.org/10.1056/NEJM199612263352602
  • Holland SM. Interferon gamma, IL-12, IL-12R and STAT-1 immunodeficiency diseases: disorders of the interface of innate and adaptive immunity. Immunol Res 2007; 38:342-6; PMID:17917041; http://dx.doi.org/10.1007/s12026-007-0045-8
  • Flynn JL. Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect 2006; 8:1179-88; PMID:16513383; http://dx.doi.org/10.1016/j.micinf.2005.10.033
  • Sodhi A, Gong J, Silva C, Qian D, Barnes PF. Clinical correlates of interferon gamma production in patients with tuberculosis. Clin Infect Dis: Off Pub Infect Dis Soc Am 1997; 25:617-20; PMID:9314449; http://dx.doi.org/10.1086/513769
  • Nathan CF, Kaplan G, Levis WR, Nusrat A, Witmer MD, Sherwin SA, Job CK, Horowitz CR, Steinman RM, Cohn ZA. Local and systemic effects of intradermal recombinant interferon-gamma in patients with lepromatous leprosy. N Engl J Med 1986; 315:6-15; PMID:3086725; http://dx.doi.org/10.1056/NEJM198607033150102
  • Kaplan G, Nusrat A, Sarno EN, Job CK, McElrath J, Porto JA, Nathan CF, Cohn ZA. Cellular responses to the intradermal injection of recombinant human gamma-interferon in lepromatous leprosy patients. Am J Pathol 1987; 128:345-53; PMID:3113256
  • Harris J, De Haro SA, Master SS, Keane J, Roberts EA, Delgado M, Deretic V. T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 2007; 27:505-17; PMID:17892853; http://dx.doi.org/10.1016/j.immuni.2007.07.022
  • Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66; PMID:15607973; http://dx.doi.org/10.1016/j.cell.2004.11.038
  • Shi CS, Kehrl JH. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci Signal 2010; 3:ra42; PMID:20501938
  • Tanida I, Ueno T, Kominami E. Human light chain 3MAP1LC3B is cleaved at its carboxyl-terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J Biol Chem 2004; 279:47704-10; PMID:15355958; http://dx.doi.org/10.1074/jbc.M407016200
  • Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, et al. A ubiquitin-like system mediates protein lipidation. Nature 2000; 408:488-92; PMID:11100732; http://dx.doi.org/10.1038/35044114
  • Feng CG, Zheng L, Lenardo MJ, Sher A. Interferon-inducible immunity-related GTPase Irgm1 regulates IFN gamma-dependent host defense, lymphocyte survival and autophagy. Autophagy 2009; 5:232-4; PMID:19066452; http://dx.doi.org/10.4161/auto.5.2.7445
  • Intemann CD, Thye T, Niemann S, Browne EN, Amanua Chinbuah M, Enimil A, Gyapong J, Osei I, Owusu-Dabo E, Helm S, et al. Autophagy gene variant IRGM -261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog 2009; 5:e1000577; PMID:19750224; http://dx.doi.org/10.1371/journal.ppat.1000577
  • King KY, Lew JD, Ha NP, Lin JS, Ma X, Graviss EA, Goodell MA. Polymorphic allele of human IRGM1 is associated with susceptibility to tuberculosis in African Americans. PLoS One 2011; 6:e16317; PMID:21283700; http://dx.doi.org/10.1371/journal.pone.0016317
  • Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, MacMicking JD. A family of IFN-gamma-inducible 65-kD GTPases protects against bacterial infection. Science 2011; 332:717-21; PMID:21551061; http://dx.doi.org/10.1126/science.1201711
  • Pasquinelli V, Quiroga MF, Martinez GJ, Zorrilla LC, Musella RM, Bracco MM, Belmonte L, Malbran A, Fainboim L, Sieling PA, et al. Expression of signaling lymphocytic activation molecule-associated protein interrupts IFN-gamma production in human tuberculosis. J Immunol 2004; 172:1177-85; PMID:14707094; http://dx.doi.org/10.4049/jimmunol.172.2.1177
  • Castillo EF, Dekonenko A, Arko-Mensah J, Mandell MA, Dupont N, Jiang S, Delgado-Vargas M, Timmins GS, Bhattacharya D, Yang H, et al. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc Natl Acad Sci U S A 2012; 109:E3168-76; PMID:23093667; http://dx.doi.org/10.1073/pnas.1210500109
  • Goletti D, Petruccioli E, Romagnoli A, Piacentini M, Fimia GM. Autophagy in Mycobacterium tuberculosis infection: a passepartout to flush the intruder out? Cytokine Growth Factor Rev 2013; 24:335-43; PMID:23395260; http://dx.doi.org/10.1016/j.cytogfr.2013.01.002
  • Man N, Chen Y, Zheng F, Zhou W, Wen LP. Induction of genuine autophagy by cationic lipids in mammalian cells. Autophagy 2010; 6:449-54; PMID:20383065; http://dx.doi.org/10.4161/auto.6.4.11612
  • Eng KE, Panas MD, Karlsson Hedestam GB, McInerney GM. A novel quantitative flow cytometry-based assay for autophagy. Autophagy 2010; 6:634-41; PMID:20458170; http://dx.doi.org/10.4161/auto.6.5.12112
  • Jurado JO, Pasquinelli V, Alvarez IB, Pena D, Rovetta AI, Tateosian NL, Romeo HE, Musella RM, Palmero D, Chuluyan HE, et al. IL-17 and IFN-gamma expression in lymphocytes from patients with active tuberculosis correlates with the severity of the disease. J Leukoc Biol 2012; 91:991-1002; PMID:22416258; http://dx.doi.org/10.1189/jlb.1211619
  • Spellberg B, Edwards JE Jr. Type 1Type 2 immunity in infectious diseases. Clin Infect Dis: Off Pub Infect Dis Soc Am 2001; 32:76-102; PMID:11118387; http://dx.doi.org/10.1086/317537
  • Chan ED, Chan J, Schluger NW. What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. Am J Respir Cell Mol Biol 2001; 25:606-12; PMID:11713103; http://dx.doi.org/10.1165/ajrcmb.25.5.4487
  • Dorman SE, Holland SM. Interferon-gamma and interleukin-12 pathway defects and human disease. Cytokine Growth Factor Rev 2000; 11:321-33; PMID:10959079; http://dx.doi.org/10.1016/S1359-6101(00)00010-1
  • Quiroga MF, Pasquinelli V, Martinez GJ, Jurado JO, Zorrilla LC, Musella RM, Abbate E, Sieling PA, Garcia VE. Inducible costimulator: a modulator of IFN-gamma production in human tuberculosis. J Immunol 2006; 176:5965-74; PMID:16670305; http://dx.doi.org/10.4049/jimmunol.176.10.5965
  • Jurado JO, Alvarez IB, Pasquinelli V, Martinez GJ, Quiroga MF, Abbate E, Musella RM, Chuluyan HE, Garcia VE. Programmed death (PD)-1:PD-ligand 1PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. J Immunol 2008; 181:116-25; PMID:18566376; http://dx.doi.org/10.4049/jimmunol.181.1.116
  • Samten B, Thomas EK, Gong J, Barnes PF. Depressed CD40 ligand expression contributes to reduced gamma interferon production in human tuberculosis. Infect Immun 2000; 68:3002-6; PMID:10769003; http://dx.doi.org/10.1128/IAI.68.5.3002-3006.2000
  • Gong JH, Zhang M, Modlin RL, Linsley PS, Iyer D, Lin Y, Barnes PF. Interleukin-10 downregulates Mycobacterium tuberculosis-induced Th1 responses and CTLA-4 expression. Infect Immun 1996; 64:913-8; PMID:8641800
  • Fabri M, Stenger S, Shin DM, Yuk JM, Liu PT, Realegeno S, Lee HM, Krutzik SR, Schenk M, Sieling PA, et al. Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci Trans Med 2011; 3:104ra2; PMID:21998409; http://dx.doi.org/10.1126/scitranslmed.3003045
  • Songane M, Kleinnijenhuis J, Netea MG, van Crevel R. The role of autophagy in host defence against Mycobacterium tuberculosis infection. Tuberculosis (Edinb) 2012; 92:388-96; PMID:22683183; http://dx.doi.org/10.1016/j.tube.2012.05.004
  • Kaufmann SH. How can immunology contribute to the control of tuberculosis? Nat Rev Immunol 2001; 1:20-30; PMID:11905811; http://dx.doi.org/10.1038/35095558
  • Samten B, Ghosh P, Yi AK, Weis SE, Lakey DL, Gonsky R, Pendurthi U, Wizel B, Zhang Y, Zhang M, et al. Reduced expression of nuclear cyclic adenosine 5′-monophosphate response element-binding proteins and IFN-gamma promoter function in disease due to an intracellular pathogen. J Immunol 2002; 168:3520-6; PMID:11907114; http://dx.doi.org/10.4049/jimmunol.168.7.3520
  • Hoft DF, Worku S, Kampmann B, Whalen CC, Ellner JJ, Hirsch CS, Brown RB, Larkin R, Li Q, Yun H, et al. Investigation of the relationships between immune-mediated inhibition of mycobacterial growth and other potential surrogate markers of protective Mycobacterium tuberculosis immunity. J Infect Dis 2002; 186:1448-57; PMID:12404160; http://dx.doi.org/10.1086/344359
  • Elias D, Akuffo H, Britton S. PPD induced in vitro interferon gamma production is not a reliable correlate of protection against Mycobacterium tuberculosis. Trans Royal Soc Trop Med Hygiene 2005; 99:363-8; PMID:15780343; http://dx.doi.org/10.1016/j.trstmh.2004.08.006
  • Marino G, Lopez-Otin C. Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. Cell Mol Life Sci 2004; 61:1439-54; PMID:15197469; http://dx.doi.org/10.1007/s00018-004-4012-4
  • Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 2005; 120:159-62; PMID:15680321
  • Colombo MI, Gutierrez MG, Romano PS. The two faces of autophagy: coxiella and mycobacterium. Autophagy 2006; 2:162-4; PMID:16874070; http://dx.doi.org/10.4161/auto.2827
  • Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser JM, Barry CE 3rd, Freedman VH, Kaplan G. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha beta. Proc Natl Acad Sci U S A 2001; 98:5752-7; PMID:11320211; http://dx.doi.org/10.1073/pnas.091096998
  • Gonzalez-Juarrero M, Shim TS, Kipnis A, Junqueira-Kipnis AP, Orme IM. Dynamics of macrophage cell populations during murine pulmonary tuberculosis. J Immunol 2003; 171:3128-35; PMID:12960339; http://dx.doi.org/10.4049/jimmunol.171.6.3128
  • Bai X, Kim SH, Azam T, McGibney MT, Huang H, Dinarello CA, Chan ED. IL-32 is a host protective cytokine against Mycobacterium tuberculosis in differentiated THP-1 human macrophages. J Immunol 2010; 184:3830-40; PMID:20190143; http://dx.doi.org/10.4049/jimmunol.0901913
  • Altare F, Durandy A, Lammas D, Emile JF, Lamhamedi S, Le Deist F, Drysdale P, Jouanguy E, Doffinger R, Bernaudin F, et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998; 280:1432-5; PMID:9603732; http://dx.doi.org/10.1126/science.280.5368.1432
  • Lerena MC, Colombo MI. Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system. Cell Microbiol 2011; 13:814-35; PMID:21447143; http://dx.doi.org/10.1111/j.1462-5822.2011.01581.x
  • Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, Falasca L, Goletti D, Gafa V, Simeone R, et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 2012; 8:1357-70; PMID:22885411; http://dx.doi.org/10.4161/auto.20881
  • Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, Takatsu K, Ernst JD. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 2008; 205:105-15; PMID:18158321; http://dx.doi.org/10.1084/jem.20071367
  • Harris J, Master SS, De Haro SA, Delgado M, Roberts EA, Hope JC, Keane J, Deretic V. Th1-Th2 polarisation and autophagy in the control of intracellular mycobacteria by macrophages. Vet Immunol Immunopathol 2009; 128:37-43; PMID:19026454; http://dx.doi.org/10.1016/j.vetimm.2008.10.293
  • Park HJ, Lee SJ, Kim SH, Han J, Bae J, Kim SJ, Park CG, Chun T. IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway. Mol Immunol 2011; 48:720-7; PMID:21095008; http://dx.doi.org/10.1016/j.molimm.2010.10.020
  • Jacquel A, Obba S, Solary E, Auberger P. Proper macrophagic differentiation requires both autophagy and caspase activation. Autophagy 2012; 8:1141-3; PMID:22751215; http://dx.doi.org/10.4161/auto.20367

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.