Skip to main content

Advertisement

Log in

Host defense mechanisms against Mycobacterium tuberculosis

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Tuberculosis (TB), which is caused by Mycobacterium tuberculosis (Mtb), remains the leading cause of death worldwide from a single infectious pathogen. Mtb is a paradigmatic intracellular pathogen that primarily invades the lungs after host inhalation of bacteria-containing droplets via the airway. However, the majority of Mtb-exposed individuals can spontaneously control the infection by virtue of a robust immune defense system. The mucosal barriers of the respiratory tract shape the first-line defense against Mtb through various mucosal immune responses. After arriving at the alveoli, the surviving mycobacteria further encounter a set of host innate immune cells that exert multiple cellular bactericidal functions. Adaptive immunity, predominantly mediated by a range of different T cell and B cell subsets, is subsequently activated and participates in host anti-mycobacterial defense. During Mtb infection, host bactericidal immune responses are exquisitely adjusted and balanced by multifaceted mechanisms, including genetic and epigenetic regulation, metabolic regulation and neuroendocrine regulation, which are indispensable for maintaining host immune efficiency and avoiding excessive tissue injury. A better understanding of the integrated and equilibrated host immune defense system against Mtb will contribute to the development of rational TB treatment regimens especially novel host-directed therapeutics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. WHO (2018) Global tuberculosis report 2018. https://www.who.int/tb/publications/global_report/en/. Accessed 18 Sept 2018

  2. Zumla A, Raviglione M, Hafner R, von Reyn CF (2013) Tuberculosis. N Engl J Med 368(8):745–755

    Article  CAS  PubMed  Google Scholar 

  3. Ewer K, Millington KA, Deeks JJ, Alvarez L, Bryant G, Lalvani A (2006) Dynamic antigen-specific T-cell responses after point-source exposure to Mycobacterium tuberculosis. Am J Respir Crit Care Med 174(7):831–839

    Article  CAS  PubMed  Google Scholar 

  4. Ma N, Zalwango S, Malone LL, Nsereko M, Wampande EM, Thiel BA, Okware B, Igo RP Jr, Joloba ML, Mupere E, Mayanja-Kizza H, Boom WH, Stein CM, Tuberculosis Research U (2014) Clinical and epidemiological characteristics of individuals resistant to M. tuberculosis infection in a longitudinal TB household contact study in Kampala, Uganda. BMC Infect Dis 14:352

    Article  PubMed  PubMed Central  Google Scholar 

  5. Stein CM, Zalwango S, Malone LL, Thiel B, Mupere E, Nsereko M, Okware B, Kisingo H, Lancioni CL, Bark CM, Whalen CC, Joloba ML, Boom WH, Mayanja-Kizza H (2018) Resistance and Susceptibility to Mycobacterium tuberculosis Infection and Disease in Tuberculosis Households in Kampala, Uganda. Am J Epidemiol 187(7):1477–1489

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cadena AM, Fortune SM, Flynn JL (2017) Heterogeneity in tuberculosis. Nat Rev Immunol 17(11):691–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lin PL, Rodgers M, Smith L, Bigbee M, Myers A, Bigbee C, Chiosea I, Capuano SV, Fuhrman C, Klein E, Flynn JL (2009) Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 77(10):4631–4642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Lin PL, Ford CB, Coleman MT, Myers AJ, Gawande R, Ioerger T, Sacchettini J, Fortune SM, Flynn JL (2014) Sterilization of granulomas is common in active and latent tuberculosis despite within-host variability in bacterial killing. Nat Med 20(1):75–79

    Article  CAS  PubMed  Google Scholar 

  9. Marakalala MJ, Raju RM, Sharma K, Zhang YJ, Eugenin EA, Prideaux B, Daudelin IB, Chen PY, Booty MG, Kim JH, Eum SY, Via LE, Behar SM, Barry CE 3rd, Mann M, Dartois V, Rubin EJ (2016) Inflammatory signaling in human tuberculosis granulomas is spatially organized. Nat Med 22(5):531–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Jasenosky LD, Scriba TJ, Hanekom WA, Goldfeld AE (2015) T cells and adaptive immunity to Mycobacterium tuberculosis in humans. Immunol Rev 264(1):74–87

    Article  CAS  PubMed  Google Scholar 

  11. Reiling N, Holscher C, Fehrenbach A, Kroger S, Kirschning CJ, Goyert S, Ehlers S (2002) Cutting edge: toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol 169(7):3480–3484

    Article  CAS  PubMed  Google Scholar 

  12. Fremond CM, Yeremeev V, Nicolle DM, Jacobs M, Quesniaux VF, Ryffel B (2004) Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J Clin Invest 114(12):1790–1799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Carlos D, Frantz FG, Souza-Junior DA, Jamur MC, Oliver C, Ramos SG, Quesniaux VF, Ryffel B, Silva CL, Bozza MT, Faccioli LH (2009) TLR2-dependent mast cell activation contributes to the control of Mycobacterium tuberculosis infection. Microbes Infect 11(8–9):770–778

    Article  CAS  PubMed  Google Scholar 

  14. Roy MG, Livraghi-Butrico A, Fletcher AA, McElwee MM, Evans SE, Boerner RM, Alexander SN, Bellinghausen LK, Song AS, Petrova YM, Tuvim MJ, Adachi R, Romo I, Bordt AS, Bowden MG, Sisson JH, Woodruff PG, Thornton DJ, Rousseau K, De la Garza MM, Moghaddam SJ, Karmouty-Quintana H, Blackburn MR, Drouin SM, Davis CW, Terrell KA, Grubb BR, O’Neal WK, Flores SC, Cota-Gomez A, Lozupone CA, Donnelly JM, Watson AM, Hennessy CE, Keith RC, Yang IV, Barthel L, Henson PM, Janssen WJ, Schwartz DA, Boucher RC, Dickey BF, Evans CM (2014) Muc5b is required for airway defence. Nature 505(7483):412–416

    Article  CAS  PubMed  Google Scholar 

  15. Nicholas B, Skipp P, Mould R, Rennard S, Davies DE, O’Connor CD, Djukanovic R (2006) Shotgun proteomic analysis of human-induced sputum. Proteomics 6(15):4390–4401

    Article  CAS  PubMed  Google Scholar 

  16. Whitsett JA, Alenghat T (2015) Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat Immunol 16(1):27–35

    Article  CAS  PubMed  Google Scholar 

  17. AlMatar M, Makky EA, Yakici G, Var I, Kayar B, Koksal F (2018) Antimicrobial peptides as an alternative to anti-tuberculosis drugs. Pharmacol Res 128:288–305

    Article  PubMed  CAS  Google Scholar 

  18. Brandtzaeg P (2013) Secretory IgA: designed for anti-microbial defense. Front Immunol 4:222

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Tjarnlund A, Rodriguez A, Cardona PJ, Guirado E, Ivanyi J, Singh M, Troye-Blomberg M, Fernandez C (2006) Polymeric IgR knockout mice are more susceptible to mycobacterial infections in the respiratory tract than wild-type mice. Int Immunol 18(5):807–816

    Article  PubMed  CAS  Google Scholar 

  20. Falero-Diaz G, Challacombe S, Rahman D, Mistry M, Douce G, Dougan G, Acosta A, Ivanyi J (2000) Transmission of IgA and IgG monoclonal antibodies to mucosal fluids following intranasal or parenteral delivery. Int Arch Allergy Immunol 122(2):143–150

    Article  CAS  PubMed  Google Scholar 

  21. Williams A, Reljic R, Naylor I, Clark SO, Falero-Diaz G, Singh M, Challacombe S, Marsh PD, Ivanyi J (2004) Passive protection with immunoglobulin A antibodies against tuberculous early infection of the lungs. Immunology 111(3):328–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Crapo JD, Barry BE, Gehr P, Bachofen M, Weibel ER (1982) Cell number and cell characteristics of the normal human lung. Am Rev Respir Dis 126(2):332–337

    CAS  PubMed  Google Scholar 

  23. Ghosh MC, Gorantla V, Makena PS, Luellen C, Sinclair SE, Schwingshackl A, Waters CM (2013) Insulin-like growth factor-I stimulates differentiation of ATII cells to ATI-like cells through activation of Wnt5a. Am J Physiol Lung Cell Mol Physiol 305(3):L222–L228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Reuschl AK, Edwards MR, Parker R, Connell DW, Hoang L, Halliday A, Jarvis H, Siddiqui N, Wright C, Bremang S, Newton SM, Beverley P, Shattock RJ, Kon OM, Lalvani A (2017) Innate activation of human primary epithelial cells broadens the host response to Mycobacterium tuberculosis in the airways. PLoS Pathog 13(9):e1006577

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Nouailles G, Dorhoi A, Koch M, Zerrahn J, Weiner J 3rd, Fae KC, Arrey F, Kuhlmann S, Bandermann S, Loewe D, Mollenkopf HJ, Vogelzang A, Meyer-Schwesinger C, Mittrucker HW, McEwen G, Kaufmann SH (2014) CXCL5-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J Clin Invest 124(3):1268–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Eghtesad M, Jackson HE, Cunningham AC (2001) Primary human alveolar epithelial cells can elicit the transendothelial migration of CD14+ monocytes and CD3+ lymphocytes. Immunology 102(2):157–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Veldhuizen R, Nag K, Orgeig S, Possmayer F (1998) The role of lipids in pulmonary surfactant. Biochim Biophys Acta 1408(2–3):90–108

    Article  CAS  PubMed  Google Scholar 

  28. Han S, Mallampalli RK (2015) The role of surfactant in lung disease and host defense against pulmonary infections. Ann Am Thorac Soc 12(5):765–774

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ariki S, Nishitani C, Kuroki Y (2012) Diverse functions of pulmonary collectins in host defense of the lung. J Biomed Biotechnol 2012:532071

    Article  PubMed  PubMed Central  Google Scholar 

  30. Strunk RC, Eidlen DM, Mason RJ (1988) Pulmonary alveolar type II epithelial cells synthesize and secrete proteins of the classical and alternative complement pathways. J Clin Invest 81(5):1419–1426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Beltran-Beck B, de la Fuente J, Garrido JM, Aranaz A, Sevilla I, Villar M, Boadella M, Galindo RC, Perez de la Lastra JM, Moreno-Cid JA, Fernandez de Mera IG, Alberdi P, Santos G, Ballesteros C, Lyashchenko KP, Minguijon E, Romero B, de Juan L, Dominguez L, Juste R, Gortazar C (2014) Oral vaccination with heat inactivated Mycobacterium bovis activates the complement system to protect against tuberculosis. PLoS One 9(5):e98048

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Arcos J, Sasindran SJ, Fujiwara N, Turner J, Schlesinger LS, Torrelles JB (2011) Human lung hydrolases delineate Mycobacterium tuberculosis-macrophage interactions and the capacity to control infection. J Immunol 187(1):372–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Arcos J, Diangelo LE, Scordo JM, Sasindran SJ, Moliva JI, Turner J, Torrelles JB (2015) Lung mucosa lining fluid modification of Mycobacterium tuberculosis to reprogram human neutrophil killing mechanisms. J Infect Dis 212(6):948–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kopf M, Schneider C, Nobs SP (2015) The development and function of lung-resident macrophages and dendritic cells. Nat Immunol 16(1):36–44

    Article  CAS  PubMed  Google Scholar 

  35. Alexis NE, Soukup J, Nierkens S, Becker S (2001) Association between airway hyperreactivity and bronchial macrophage dysfunction in individuals with mild asthma. Am J Physiol Lung Cell Mol Physiol 280(2):L369–L375

    Article  CAS  PubMed  Google Scholar 

  36. Kawano H, Kayama H, Nakama T, Hashimoto T, Umemoto E, Takeda K (2016) IL-10-producing lung interstitial macrophages prevent neutrophilic asthma. Int Immunol 28(10):489–501

    Article  CAS  PubMed  Google Scholar 

  37. Westphalen K, Gusarova GA, Islam MN, Subramanian M, Cohen TS, Prince AS, Bhattacharya J (2014) Sessile alveolar macrophages communicate with alveolar epithelium to modulate immunity. Nature 506(7489):503–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liu CH, Liu H, Ge B (2017) Innate immunity in tuberculosis: host defense vs pathogen evasion. Cell Mol Immunol 14(12):963–975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ehrt S, Schnappinger D (2009) Mycobacterial survival strategies in the phagosome: defence against host stresses. Cell Microbiol 11(8):1170–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Silver RF, Walrath J, Lee H, Jacobson BA, Horton H, Bowman MR, Nocka K, Sypek JP (2009) Human alveolar macrophage gene responses to Mycobacterium tuberculosis strains H37Ra and H37Rv. Am J Respir Cell Mol Biol 40(4):491–504

    Article  CAS  PubMed  Google Scholar 

  41. Gleeson LE, Sheedy FJ, Palsson-McDermott EM, Triglia D, O’Leary SM, O’Sullivan MP, O’Neill LA, Keane J (2016) Cutting edge: Mycobacterium tuberculosis induces aerobic glycolysis in human alveolar macrophages that is required for control of intracellular bacillary replication. J Immunol 196(6):2444–2449

    Article  CAS  PubMed  Google Scholar 

  42. Nicholson S, Bonecini-Almeida Mda G, Lapailva JR, Nathan C, Xie QW, Mumford R, Weidner JR, Calaycay J, Geng J, Boechat N, Linhares C, Rom W, Ho JL (1996) Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med 183(5):2293–2302

    Article  CAS  PubMed  Google Scholar 

  43. Rivas-Santiago B, Hernandez-Pando R, Carranza C, Juarez E, Contreras JL, Aguilar-Leon D, Torres M, Sada E (2008) Expression of cathelicidin LL-37 during Mycobacterium tuberculosis infection in human alveolar macrophages, monocytes, neutrophils, and epithelial cells. Infect Immun 76(3):935–941

    Article  CAS  PubMed  Google Scholar 

  44. Simeone R, Sayes F, Song O, Groschel MI, Brodin P, Brosch R, Majlessi L (2015) Cytosolic access of Mycobacterium tuberculosis: critical impact of phagosomal acidification control and demonstration of occurrence in vivo. PLoS Pathog 11(2):e1004650

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Wassermann R, Gulen MF, Sala C, Perin SG, Lou Y, Rybniker J, Schmid-Burgk JL, Schmidt T, Hornung V, Cole ST, Ablasser A (2015) Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 17(6):799–810

    Article  CAS  PubMed  Google Scholar 

  46. Watson RO, Bell SL, MacDuff DA, Kimmey JM, Diner EJ, Olivas J, Vance RE, Stallings CL, Virgin HW, Cox JS (2015) The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce Type I interferons and activate autophagy. Cell Host Microbe 17(6):811–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wang J, Li BX, Ge PP, Li J, Wang Q, Gao GF, Qiu XB, Liu CH (2015) Mycobacterium tuberculosis suppresses innate immunity by coopting the host ubiquitin system. Nat Immunol 16(3):237–245

    Article  CAS  PubMed  Google Scholar 

  48. Li J, Chai QY, Liu CH (2016) The ubiquitin system: a critical regulator of innate immunity and pathogen-host interactions. Cell Mol Immunol 13(5):560–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Chai Q, Wang X, Qiang L, Zhang Y, Ge P, Lu Z, Zhong Y, Li B, Wang J, Zhang L, Zhou D, Li W, Dong W, Pang Y, Gao GF, Liu CH (2019) A Mycobacterium tuberculosis surface protein recruits ubiquitin to trigger host xenophagy. Nat Commun 10(1):1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Cheng Y, Schorey JS (2013) Exosomes carrying mycobacterial antigens can protect mice against Mycobacterium tuberculosis infection. Eur J Immunol 43(12):3279–3290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Smith VL, Cheng Y, Bryant BR, Schorey JS (2017) Exosomes function in antigen presentation during an in vivo Mycobacterium tuberculosis infection. Sci Rep 7:43578

    Article  PubMed  PubMed Central  Google Scholar 

  52. Getahun H, Gunneberg C, Granich R, Nunn P (2010) HIV infection-associated tuberculosis: the epidemiology and the response. Clin Infect Dis 50(Suppl 3):S201–S207

    Article  PubMed  Google Scholar 

  53. Doyle T, Goujon C, Malim MH (2015) HIV-1 and interferons: who’s interfering with whom? Nat Rev Microbiol 13(7):403–413

    Article  CAS  PubMed  Google Scholar 

  54. Moreira-Teixeira L, Mayer-Barber K, Sher A, O’Garra A (2018) Type I interferons in tuberculosis: foe and occasionally friend. J Exp Med 215(5):1273–1285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Mazzolini J, Herit F, Bouchet J, Benmerah A, Benichou S, Niedergang F (2010) Inhibition of phagocytosis in HIV-1-infected macrophages relies on Nef-dependent alteration of focal delivery of recycling compartments. Blood 115(21):4226–4236

    Article  CAS  PubMed  Google Scholar 

  56. Kyei GB, Dinkins C, Davis AS, Roberts E, Singh SB, Dong C, Wu L, Kominami E, Ueno T, Yamamoto A, Federico M, Panganiban A, Vergne I, Deretic V (2009) Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 186(2):255–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Lawn SD, Wainwright H, Orrell C (2009) Fatal unmasking tuberculosis immune reconstitution disease with bronchiolitis obliterans organizing pneumonia: the role of macrophages. AIDS 23(1):143–145

    Article  PubMed  Google Scholar 

  58. Lai RPJ, Meintjes G, Wilkinson KA, Graham CM, Marais S, Van der Plas H, Deffur A, Schutz C, Bloom C, Munagala I, Anguiano E, Goliath R, Maartens G, Banchereau J, Chaussabel D, O’Garra A, Wilkinson RJ (2015) HIV-tuberculosis-associated immune reconstitution inflammatory syndrome is characterized by Toll-like receptor and inflammasome signalling. Nat Commun 6:8451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Day J, Friedman A, Schlesinger LS (2009) Modeling the immune rheostat of macrophages in the lung in response to infection. Proc Natl Acad Sci USA 106(27):11246–11251

    Article  CAS  PubMed  Google Scholar 

  60. Lavalett L, Rodriguez H, Ortega H, Sadee W, Schlesinger LS, Barrera LF (2017) Alveolar macrophages from tuberculosis patients display an altered inflammatory gene expression profile. Tuberculosis (Edinb) 107:156–167

    Article  CAS  Google Scholar 

  61. Hussell T, Bell TJ (2014) Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 14(2):81–93

    Article  CAS  PubMed  Google Scholar 

  62. Shapouri-Moghaddam A, Mohammadian S, Vazini H, Taghadosi M, Esmaeili SA, Mardani F, Seifi B, Mohammadi A, Afshari JT, Sahebkar A (2018) Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol 233(9):6425–6440

    Article  CAS  PubMed  Google Scholar 

  63. Marino S, Cilfone NA, Mattila JT, Linderman JJ, Flynn JL, Kirschner DE (2015) Macrophage polarization drives granuloma outcome during Mycobacterium tuberculosis infection. Infect Immun 83(1):324–338

    Article  PubMed  CAS  Google Scholar 

  64. Bonecini-Almeida MG, Ho JL, Boechat N, Huard RC, Chitale S, Doo H, Geng J, Rego L, Lazzarini LC, Kritski AL, Johnson WD Jr, McCaffrey TA, Silva JR (2004) Down-modulation of lung immune responses by interleukin-10 and transforming growth factor beta (TGF-beta) and analysis of TGF-beta receptors I and II in active tuberculosis. Infect Immun 72(5):2628–2634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. O’Leary S, O’Sullivan MP, Keane J (2011) IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages. Am J Respir Cell Mol Biol 45(1):172–180

    Article  PubMed  CAS  Google Scholar 

  66. Chang ST, Linderman JJ, Kirschner DE (2005) Multiple mechanisms allow Mycobacterium tuberculosis to continuously inhibit MHC class II-mediated antigen presentation by macrophages. Proc Natl Acad Sci USA 102(12):4530–4535

    Article  CAS  PubMed  Google Scholar 

  67. Hickey AJ, Durham PG, Dharmadhikari A, Nardell EA (2016) Inhaled drug treatment for tuberculosis: past progress and future prospects. J Control Release 240:127–134

    Article  CAS  PubMed  Google Scholar 

  68. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B, Neyrolles O (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197(1):121–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Bafica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A (2005) TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 202(12):1715–1724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Wolf AJ, Linas B, Trevejo-Nunez GJ, Kincaid E, Tamura T, Takatsu K, Ernst JD (2007) Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 179(4):2509–2519

    Article  CAS  PubMed  Google Scholar 

  71. Lai R, Jeyanathan M, Afkhami S, Zganiacz A, Hammill JA, Yao Y, Kaushic C, Xing Z (2018) CD11b(+) dendritic cell-mediated anti-Mycobacterium tuberculosis Th1 activation is counterregulated by CD103(+) Dendritic Cells via IL-10. J Immunol 200(5):1746–1760

    CAS  PubMed  Google Scholar 

  72. Mayer-Barber KD, Andrade BB, Barber DL, Hieny S, Feng CG, Caspar P, Oland S, Gordon S, Sher A (2011) Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 35(6):1023–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Balboa L, Kviatcovsky D, Schierloh P, Garcia M, de la Barrera S, Sasiain MDC (2016) Monocyte-derived dendritic cells early exposed to Mycobacterium tuberculosis induce an enhanced T helper 17 response and transfer mycobacterial antigens. Int J Med Microbiol 306(7):541–553

    Article  CAS  PubMed  Google Scholar 

  74. Ovchinnikova OA, Berge N, Kang C, Urien C, Ketelhuth DF, Pottier J, Drouet L, Hansson GK, Marchal G, Back M, Schwartz-Cornil I, Lagranderie M (2014) Mycobacterium bovis BCG killed by extended freeze-drying induces an immunoregulatory profile and protects against atherosclerosis. J Intern Med 275(1):49–58

    Article  CAS  PubMed  Google Scholar 

  75. Jagannath C, Lindsey DR, Dhandayuthapani S, Xu Y, Hunter RL, Eissa NT (2009) Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat Med 15(3):267–276

    Article  CAS  PubMed  Google Scholar 

  76. Harding JS, Rayasam A, Schreiber HA, Fabry Z, Sandor M (2015) Mycobacterium-infected dendritic cells disseminate granulomatous inflammation. Sci Rep 5:15248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Martineau AR, Newton SM, Wilkinson KA, Kampmann B, Hall BM, Nawroly N, Packe GE, Davidson RN, Griffiths CJ, Wilkinson RJ (2007) Neutrophil-mediated innate immune resistance to mycobacteria. J Clin Invest 117(7):1988–1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Blomgran R, Ernst JD (2011) Lung neutrophils facilitate activation of naive antigen-specific CD4+ T cells during Mycobacterium tuberculosis infection. J Immunol 186(12):7110–7119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Yang CT, Cambier CJ, Davis JM, Hall CJ, Crosier PS, Ramakrishnan L (2012) Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 12(3):301–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Tan BH, Meinken C, Bastian M, Bruns H, Legaspi A, Ochoa MT, Krutzik SR, Bloom BR, Ganz T, Modlin RL, Stenger S (2006) Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J Immunol 177(3):1864–1871

    Article  CAS  PubMed  Google Scholar 

  81. Alvarez-Jimenez VD, Leyva-Paredes K, Garcia-Martinez M, Vazquez-Flores L, Garcia-Paredes VG, Campillo-Navarro M, Romo-Cruz I, Rosales-Garcia VH, Castaneda-Casimiro J, Gonzalez-Pozos S, Hernandez JM, Wong-Baeza C, Garcia-Perez BE, Ortiz-Navarrete V, Estrada-Parra S, Serafin-Lopez J, Wong-Baeza I, Chacon-Salinas R, Estrada-Garcia I (2018) Extracellular vesicles released from Mycobacterium tuberculosis-infected neutrophils promote macrophage autophagy and decrease intracellular mycobacterial survival. Front Immunol 9:272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, Wilkinson KA, Banchereau R, Skinner J, Wilkinson RJ, Quinn C, Blankenship D, Dhawan R, Cush JJ, Mejias A, Ramilo O, Kon OM, Pascual V, Banchereau J, Chaussabel D, O’Garra A (2010) An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466(7309):973–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Mishra BB, Lovewell RR, Olive AJ, Zhang G, Wang W, Eugenin E, Smith CM, Phuah JY, Long JE, Dubuke ML, Palace SG, Goguen JD, Baker RE, Nambi S, Mishra R, Booty MG, Baer CE, Shaffer SA, Dartois V, McCormick BA, Chen X, Sassetti CM (2017) Nitric oxide prevents a pathogen-permissive granulocytic inflammation during tuberculosis. Nat Microbiol 2:17072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Dallenga T, Repnik U, Corleis B, Eich J, Reimer R, Griffiths GW, Schaible UE (2017) M. tuberculosis-induced necrosis of infected neutrophils promotes bacterial growth following phagocytosis by macrophages. Cell Host Microbe 22(4):519–530 e513

    Article  CAS  Google Scholar 

  85. Lowe DM, Demaret J, Bangani N, Nakiwala JK, Goliath R, Wilkinson KA, Wilkinson RJ, Martineau AR (2018) Differential effect of viable versus necrotic neutrophils on Mycobacterium tuberculosis growth and cytokine induction in whole blood. Front Immunol 9:903

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Vacca P, Chiossone L, Mingari MC, Moretta L (2019) Heterogeneity of NK cells and other innate lymphoid cells in human and murine decidua. Front Immunol 10:170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Zitti B, Bryceson YT (2018) Natural killer cells in inflammation and autoimmunity. Cytokine Growth Factor Rev 42:37–46

    Article  CAS  PubMed  Google Scholar 

  88. Vivier E, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie ANJ, Mebius RE, Powrie F, Spits H (2018) Innate lymphoid cells: 10 years on. Cell 174(5):1054–1066

    Article  CAS  PubMed  Google Scholar 

  89. Emgard J, Kammoun H, Garcia-Cassani B, Chesne J, Parigi SM, Jacob JM, Cheng HW, Evren E, Das S, Czarnewski P, Sleiers N, Melo-Gonzalez F, Kvedaraite E, Svensson M, Scandella E, Hepworth MR, Huber S, Ludewig B, Peduto L, Villablanca EJ, Veiga-Fernandes H, Pereira JP, Flavell RA, Willinger T (2018) Oxysterol sensing through the receptor GPR183 promotes the lymphoid-tissue-inducing function of innate lymphoid cells and colonic inflammation. Immunity 48(1):120–132 e128

    Article  CAS  Google Scholar 

  90. Zhong C, Zheng M, Zhu J (2018) Lymphoid tissue inducer-A divergent member of the ILC family. Cytokine Growth Factor Rev 42:5–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Feng CG, Kaviratne M, Rothfuchs AG, Cheever A, Hieny S, Young HA, Wynn TA, Sher A (2006) NK cell-derived IFN-gamma differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. J Immunol 177(10):7086–7093

    Article  CAS  PubMed  Google Scholar 

  92. Kupz A, Zedler U, Staber M, Perdomo C, Dorhoi A, Brosch R, Kaufmann SH (2016) ESAT-6-dependent cytosolic pattern recognition drives noncognate tuberculosis control in vivo. J Clin Invest 126(6):2109–2122

    Article  PubMed  PubMed Central  Google Scholar 

  93. Lai HC, Chang CJ, Lin CS, Wu TR, Hsu YJ, Wu TS, Lu JJ, Martel J, Ojcius DM, Ku CL, Young JD, Lu CC (2018) NK cell-derived IFN-gamma protects against nontuberculous mycobacterial lung infection. J Immunol 201(5):1478–1490

    Article  CAS  PubMed  Google Scholar 

  94. Esin S, Batoni G, Counoupas C, Stringaro A, Brancatisano FL, Colone M, Maisetta G, Florio W, Arancia G, Campa M (2008) Direct binding of human NK cell natural cytotoxicity receptor NKp44 to the surfaces of mycobacteria and other bacteria. Infect Immun 76(4):1719–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Roy Chowdhury R, Vallania F, Yang Q, Lopez Angel CJ, Darboe F, Penn-Nicholson A, Rozot V, Nemes E, Malherbe ST, Ronacher K, Walzl G, Hanekom W, Davis MM, Winter J, Chen X, Scriba TJ, Khatri P, Chien YH (2018) A multi-cohort study of the immune factors associated with M. tuberculosis infection outcomes. Nature 560(7720):644–648

    Article  CAS  PubMed  Google Scholar 

  96. Ardain A, Domingo-Gonzalez R, Das S, Kazer SW, Howard NC, Singh A, Ahmed M, Nhamoyebonde S, Rangel-Moreno J, Ogongo P, Lu L, Ramsuran D, de la Luz Garcia-Hernandez M, Ku T, Darby M, Park E, Karim F, Melocchi L, Madansein R, Dullabh KJ, Dunlap M, Marin-Agudelo N, Ebihara T, Ndung’u T, Kaushal D, Pym AS, Kolls JK, Steyn A, Zuniga J, Horsnell W, Yokoyama WM, Shalek AK, Kloverpris HN, Colonna M, Leslie A, Khader SA (2019) Group 3 innate lymphoid cells mediate early protective immunity against tuberculosis. Nature 5:1

    Google Scholar 

  97. Rigoni A, Colombo MP, Pucillo C (2018) Mast cells, basophils and eosinophils: from allergy to cancer. Semin Immunol 35:29–34

    Article  CAS  PubMed  Google Scholar 

  98. Carlos D, Fremond C, Samarina A, Vasseur V, Maillet I, Ramos SG, Erard F, Quesniaux V, Ohtsu H, Silva CL, Faccioli LH, Ryffel B (2009) Histamine plays an essential regulatory role in lung inflammation and protective immunity in the acute phase of Mycobacterium tuberculosis infection. Infect Immun 77(12):5359–5368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Babu D, Morgan AG, Reiz B, Whittal RM, Almas S, Lacy P, Siraki AG (2019) Eosinophil peroxidase oxidizes isoniazid to form the active metabolite against M. tuberculosis, isoniazid-NAD+. Chem Biol Interact 305:48–53

    Article  CAS  PubMed  Google Scholar 

  100. Randall PJ, Hsu NJ, Quesniaux V, Ryffel B, Jacobs M (2015) Mycobacterium tuberculosis infection of the ‘non-classical immune cell’. Immunol Cell Biol 93(9):789–795

    Article  CAS  PubMed  Google Scholar 

  101. Chai Q, Zhang Y, Liu CH (2018) Mycobacterium tuberculosis: an adaptable pathogen associated with multiple human diseases. Front Cell Infect Microbiol 8:158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Kalsdorf B, Scriba TJ, Wood K, Day CL, Dheda K, Dawson R, Hanekom WA, Lange C, Wilkinson RJ (2009) HIV-1 infection impairs the bronchoalveolar T-cell response to mycobacteria. Am J Respir Crit Care Med 180(12):1262–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Robinson RT, Orme IM, Cooper AM (2015) The onset of adaptive immunity in the mouse model of tuberculosis and the factors that compromise its expression. Immunol Rev 264(1):46–59

    Article  CAS  PubMed  Google Scholar 

  104. Godfrey DI, Uldrich AP, McCluskey J, Rossjohn J, Moody DB (2015) The burgeoning family of unconventional T cells. Nat Immunol 16(11):1114–1123

    Article  CAS  PubMed  Google Scholar 

  105. Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, Affaticati P, Gilfillan S, Lantz O (2003) Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422(6928):164–169

    Article  CAS  PubMed  Google Scholar 

  106. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, Bhati M, Chen Z, Kostenko L, Reantragoon R, Williamson NA, Purcell AW, Dudek NL, McConville MJ, O’Hair RA, Khairallah GN, Godfrey DI, Fairlie DP, Rossjohn J, McCluskey J (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491(7426):717–723

    Article  CAS  PubMed  Google Scholar 

  107. Downey AM, Kaplonek P, Seeberger PH (2019) MAIT cells as attractive vaccine targets. FEBS Lett 593(13):1627–1640

    Article  CAS  PubMed  Google Scholar 

  108. Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, Winata E, Swarbrick GM, Chua WJ, Yu YY, Lantz O, Cook MS, Null MD, Jacoby DB, Harriff MJ, Lewinsohn DA, Hansen TH, Lewinsohn DM (2010) Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol 8(6):e1000407

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, Core M, Levy E, Dusseaux M, Meyssonnier V, Premel V, Ngo C, Riteau B, Duban L, Robert D, Huang S, Rottman M, Soudais C, Lantz O (2010) Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11(8):701–708

    Article  PubMed  CAS  Google Scholar 

  110. Kwon YS, Cho YN, Kim MJ, Jin HM, Jung HJ, Kang JH, Park KJ, Kim TJ, Kee HJ, Kim N, Kee SJ, Park YW (2015) Mucosal-associated invariant T cells are numerically and functionally deficient in patients with mycobacterial infection and reflect disease activity. Tuberculosis (Edinb) 95(3):267–274

    Article  CAS  Google Scholar 

  111. Malka-Ruimy C, Ben Youssef G, Lambert M, Tourret M, Ghazarian L, Faye A, Caillat-Zucman S, Houdouin V (2019) Mucosal-associated invariant T cell levels are reduced in the peripheral blood and lungs of children with active pulmonary tuberculosis. Front Immunol 10:206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Kauffman KD, Sallin MA, Hoft SG, Sakai S, Moore R, Wilder-Kofie T, Moore IN, Sette A, Arlehamn CSL, Barber DL (2018) Limited pulmonary mucosal-associated invariant T cell Accumulation and activation during Mycobacterium tuberculosis infection in rhesus macaques. Infect Immun 86:12

    Article  Google Scholar 

  113. Leeansyah E, Ganesh A, Quigley MF, Sonnerborg A, Andersson J, Hunt PW, Somsouk M, Deeks SG, Martin JN, Moll M, Shacklett BL, Sandberg JK (2013) Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121(7):1124–1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Carreno LJ, Saavedra-Avila NA, Porcelli SA (2016) Synthetic glycolipid activators of natural killer T cells as immunotherapeutic agents. Clin Transl Immunol 5(4):e69

    Article  CAS  Google Scholar 

  115. Kee SJ, Kwon YS, Park YW, Cho YN, Lee SJ, Kim TJ, Lee SS, Jang HC, Shin MG, Shin JH, Suh SP, Ryang DW (2012) Dysfunction of natural killer T cells in patients with active Mycobacterium tuberculosis infection. Infect Immun 80(6):2100–2108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Paquin-Proulx D, Costa PR, Terrassani Silveira CG, Marmorato MP, Cerqueira NB, Sutton MS, O’Connor SL, Carvalho KI, Nixon DF, Kallas EG (2018) Latent Mycobacterium tuberculosis infection is associated with a higher frequency of mucosal-associated invariant t and invariant natural killer T cells. Front Immunol 9:1394

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Wu C, Li Z, Fu X, Yu S, Lao S, Yang B (2015) Antigen-specific human NKT cells from tuberculosis patients produce IL-21 to help B cells for the production of immunoglobulins. Oncotarget 6(30):28633–28645

    Article  PubMed  PubMed Central  Google Scholar 

  118. Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM (2008) Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages, produce interferon-gamma, and kill intracellular bacteria. PLoS Pathog 4(12):e1000239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Gansert JL, Kiessler V, Engele M, Wittke F, Rollinghoff M, Krensky AM, Porcelli SA, Modlin RL, Stenger S (2003) Human NKT cells express granulysin and exhibit antimycobacterial activity. J Immunol 170(6):3154–3161

    Article  CAS  PubMed  Google Scholar 

  120. Chackerian A, Alt J, Perera V, Behar SM (2002) Activation of NKT cells protects mice from tuberculosis. Infect Immun 70(11):6302–6309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Chancellor A, White A, Tocheva AS, Fenn JR, Dennis M, Tezera L, Singhania A, Elliott T, Tebruegge M, Elkington P, Gadola S, Sharpe S, Mansour S (2017) Quantitative and qualitative iNKT repertoire associations with disease susceptibility and outcome in macaque tuberculosis infection. Tuberculosis (Edinb) 105:86–95

    Article  CAS  Google Scholar 

  122. Peng MY, Wang ZH, Yao CY, Jiang LN, Jin QL, Wang J, Li BQ (2008) Interleukin 17-producing gamma delta T cells increased in patients with active pulmonary tuberculosis. Cell Mol Immunol 5(3):203–208

    Article  PubMed  PubMed Central  Google Scholar 

  123. Okamoto Yoshida Y, Umemura M, Yahagi A, O’Brien RL, Ikuta K, Kishihara K, Hara H, Nakae S, Iwakura Y, Matsuzaki G (2010) Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J Immunol 184(8):4414–4422

    Article  CAS  PubMed  Google Scholar 

  124. Leslie DS, Vincent MS, Spada FM, Das H, Sugita M, Morita CT, Brenner MB (2002) CD1-mediated gamma/delta T cell maturation of dendritic cells. J Exp Med 196(12):1575–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Vorkas CK, Wipperman MF, Li K, Bean J, Bhattarai SK, Adamow M, Wong P, Aube J, Juste MAJ, Bucci V, Fitzgerald DW, Glickman MS (2018) Mucosal-associated invariant and gammadelta T cell subsets respond to initial Mycobacterium tuberculosis infection. JCI Insight 3:19

    Article  Google Scholar 

  126. Wykes MN, Lewin SR (2018) Immune checkpoint blockade in infectious diseases. Nat Rev Immunol 18(2):91–104

    Article  CAS  PubMed  Google Scholar 

  127. Lazar-Molnar E, Chen B, Sweeney KA, Wang EJ, Liu W, Lin J, Porcelli SA, Almo SC, Nathenson SG, Jacobs WR Jr (2010) Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc Natl Acad Sci USA 107(30):13402–13407

    Article  CAS  PubMed  Google Scholar 

  128. Barber DL, Mayer-Barber KD, Feng CG, Sharpe AH, Sher A (2011) CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J Immunol 186(3):1598–1607

    Article  CAS  PubMed  Google Scholar 

  129. Sakai S, Kauffman KD, Sallin MA, Sharpe AH, Young HA, Ganusov VV, Barber DL (2016) CD4 T cell-derived IFN-gamma plays a minimal role in control of pulmonary Mycobacterium tuberculosis infection and must be actively repressed by PD-1 to prevent lethal disease. PLoS Pathog 12(5):e1005667

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. Saharia KK, Petrovas C, Ferrando-Martinez S, Leal M, Luque R, Ive P, Luetkemeyer A, Havlir D, Koup RA (2016) Tuberculosis therapy modifies the cytokine profile, maturation state, and expression of inhibitory molecules on Mycobacterium tuberculosis-specific CD4+ T-cells. PLoS One 11(7):e0158262

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. Day CL, Abrahams DA, Bunjun R, Stone L, de Kock M, Walzl G, Wilkinson RJ, Burgers WA, Hanekom WA (2018) PD-1 expression on Mycobacterium tuberculosis-specific CD4 T cells is associated with bacterial load in human tuberculosis. Front Immunol 9:1995

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Picchi H, Mateus C, Chouaid C, Besse B, Marabelle A, Michot JM, Champiat S, Voisin AL, Lambotte O (2018) Infectious complications associated with the use of immune checkpoint inhibitors in oncology: reactivation of tuberculosis after anti PD-1 treatment. Clin Microbiol Infect 24(3):216–218

    Article  CAS  PubMed  Google Scholar 

  133. Barber DL, Sakai S, Kudchadkar RR, Fling SP, Day TA, Vergara JA, Ashkin D, Cheng JH, Lundgren LM, Raabe VN, Kraft CS, Nieva JJ, Cheever MA, Nghiem PT, Sharon E (2019) Tuberculosis following PD-1 blockade for cancer immunotherapy. Sci Transl Med 11:475

    Google Scholar 

  134. Jayaraman P, Jacques MK, Zhu C, Steblenko KM, Stowell BL, Madi A, Anderson AC, Kuchroo VK, Behar SM (2016) TIM3 mediates T cell exhaustion during Mycobacterium tuberculosis infection. PLoS Pathog 12(3):e1005490

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  135. del Barrio L, Sahoo M, Lantier L, Reynolds JM, Ceballos-Olvera I, Re F (2015) Production of anti-LPS IgM by B1a B cells depends on IL-1beta and is protective against lung infection with Francisella tularensis LVS. PLoS Pathog 11(3):e1004706

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  136. Di Niro R, Lee SJ, Vander Heiden JA, Elsner RA, Trivedi N, Bannock JM, Gupta NT, Kleinstein SH, Vigneault F, Gilbert TJ, Meffre E, McSorley SJ, Shlomchik MJ (2015) Salmonella infection drives promiscuous B cell activation followed by extrafollicular affinity maturation. Immunity 43(1):120–131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Lehar SM, Pillow T, Xu M, Staben L, Kajihara KK, Vandlen R, DePalatis L, Raab H, Hazenbos WL, Morisaki JH, Kim J, Park S, Darwish M, Lee BC, Hernandez H, Loyet KM, Lupardus P, Fong R, Yan D, Chalouni C, Luis E, Khalfin Y, Plise E, Cheong J, Lyssikatos JP, Strandh M, Koefoed K, Andersen PS, Flygare JA, Wah Tan M, Brown EJ, Mariathasan S (2015) Novel antibody-antibiotic conjugate eliminates intracellular S. aureus. Nature 527(7578):323–328

    Article  CAS  PubMed  Google Scholar 

  138. Shen P, Fillatreau S (2015) Antibody-independent functions of B cells: a focus on cytokines. Nat Rev Immunol 15(7):441–451

    Article  CAS  PubMed  Google Scholar 

  139. Phuah J, Wong EA, Gideon HP, Maiello P, Coleman MT, Hendricks MR, Ruden R, Cirrincione LR, Chan J, Lin PL, Flynn JL (2016) Effects of B cell depletion on early Mycobacterium tuberculosis infection in cynomolgus macaques. Infect Immun 84(5):1301–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Maglione PJ, Xu J, Chan J (2007) B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis. J Immunol 178(11):7222–7234

    Article  CAS  PubMed  Google Scholar 

  141. Kozakiewicz L, Chen Y, Xu J, Wang Y, Dunussi-Joannopoulos K, Ou Q, Flynn JL, Porcelli SA, Jacobs WR Jr, Chan J (2013) B cells regulate neutrophilia during Mycobacterium tuberculosis infection and BCG vaccination by modulating the interleukin-17 response. PLoS Pathog 9(7):e1003472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Yuan C, Qu ZL, Tang XL, Liu Q, Luo W, Huang C, Pan Q, Zhang XL (2019) Mycobacterium tuberculosis mannose-capped lipoarabinomannan induces IL-10-producing B cells and hinders CD4(+)Th1 immunity. iScience 11:13–30

    Article  CAS  PubMed  Google Scholar 

  143. Benard A, Sakwa I, Schierloh P, Colom A, Mercier I, Tailleux L, Jouneau L, Boudinot P, Al-Saati T, Lang R, Rehwinkel J, Loxton AG, Kaufmann SHE, Anton-Leberre V, O’Garra A, Sasiain MDC, Gicquel B, Fillatreau S, Neyrolles O, Hudrisier D (2018) B cells producing Type I IFN modulate macrophage polarization in tuberculosis. Am J Respir Crit Care Med 197(6):801–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Lund FE, Randall TD (2010) Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat Rev Immunol 10(4):236–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Linge I, Dyatlov A, Kondratieva E, Avdienko V, Apt A, Kondratieva T (2017) B-lymphocytes forming follicle-like structures in the lung tissue of tuberculosis-infected mice: dynamics, phenotypes and functional activity. Tuberculosis (Edinb) 102:16–23

    Article  CAS  Google Scholar 

  146. Wong SC, Puaux AL, Chittezhath M, Shalova I, Kajiji TS, Wang X, Abastado JP, Lam KP, Biswas SK (2010) Macrophage polarization to a unique phenotype driven by B cells. Eur J Immunol 40(8):2296–2307

    Article  CAS  PubMed  Google Scholar 

  147. Maglione PJ, Xu J, Casadevall A, Chan J (2008) Fcγ receptors regulate immune activation and susceptibility during Mycobacterium tuberculosis infection. J Immunol 180(5):3329–3338

    Article  CAS  PubMed  Google Scholar 

  148. Phuah JY, Mattila JT, Lin PL, Flynn JL (2012) Activated B cells in the granulomas of nonhuman primates infected with Mycobacterium tuberculosis. Am J Pathol 181(2):508–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Lu LL, Chung AW, Rosebrock TR, Ghebremichael M, Yu WH, Grace PS, Schoen MK, Tafesse F, Martin C, Leung V, Mahan AE, Sips M, Kumar MP, Tedesco J, Robinson H, Tkachenko E, Draghi M, Freedberg KJ, Streeck H, Suscovich TJ, Lauffenburger DA, Restrepo BI, Day C, Fortune SM, Alter G (2016) A functional role for antibodies in tuberculosis. Cell 167(2):433–443.e414

    Article  CAS  Google Scholar 

  150. Chen T, Blanc C, Eder AZ, Prados-Rosales R, Souza AC, Kim RS, Glatman-Freedman A, Joe M, Bai Y, Lowary TL, Tanner R, Brennan MJ, Fletcher HA, McShane H, Casadevall A, Achkar JM (2016) Association of human antibodies to arabinomannan with enhanced mycobacterial opsonophagocytosis and intracellular growth reduction. J Infect Dis 214(2):300–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Zimmermann N, Thormann V, Hu B, Kohler AB, Imai-Matsushima A, Locht C, Arnett E, Schlesinger LS, Zoller T, Schurmann M, Kaufmann SH, Wardemann H (2016) Human isotype-dependent inhibitory antibody responses against Mycobacterium tuberculosis. EMBO Mol Med 8(11):1325–1339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Snow KJ, Sismanidis C, Denholm J, Sawyer SM, Graham SM (2018) The incidence of tuberculosis among adolescents and young adults: a global estimate. Eur Respir J 51:2

    Article  Google Scholar 

  153. Elkington P, Tebruegge M, Mansour S (2016) Tuberculosis: an infection-initiated autoimmune disease? Trends Immunol 37(12):815–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Ravimohan S, Kornfeld H, Weissman D, Bisson GP (2018) Tuberculosis and lung damage: from epidemiology to pathophysiology. Eur Respir Rev 27:147

    Article  Google Scholar 

  155. Tzelepis F, Blagih J, Khan N, Gillard J, Mendonca L, Roy DG, Ma EH, Joubert P, Jones RG, Divangahi M (2018) Mitochondrial cyclophilin D regulates T cell metabolic responses and disease tolerance to tuberculosis. Sci Immunol 3:23

    Article  Google Scholar 

  156. Cooke GS, Hill AV (2001) Genetics of susceptibility to human infectious disease. Nat Rev Genet 2(12):967–977

    Article  CAS  PubMed  Google Scholar 

  157. Stead WW, Senner JW, Reddick WT, Lofgren JP (1990) Racial differences in susceptibility to infection by Mycobacterium tuberculosis. N Engl J Med 322(7):422–427

    Article  CAS  PubMed  Google Scholar 

  158. Torrelles JB, Azad AK, Henning LN, Carlson TK, Schlesinger LS (2008) Role of C-type lectins in mycobacterial infections. Curr Drug Targets 9(2):102–112

    Article  CAS  PubMed  Google Scholar 

  159. Lopez B, Aguilar D, Orozco H, Burger M, Espitia C, Ritacco V, Barrera L, Kremer K, Hernandez-Pando R, Huygen K, van Soolingen D (2003) A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes. Clin Exp Immunol 133(1):30–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Dormans J, Burger M, Aguilar D, Hernandez-Pando R, Kremer K, Roholl P, Arend SM, van Soolingen D (2004) Correlation of virulence, lung pathology, bacterial load and delayed type hypersensitivity responses after infection with different Mycobacterium tuberculosis genotypes in a BALB/c mouse model. Clin Exp Immunol 137(3):460–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Reed MB, Domenech P, Manca C, Su H, Barczak AK, Kreiswirth BN, Kaplan G, Barry CE 3rd (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431(7004):84–87

    Article  CAS  PubMed  Google Scholar 

  162. Ates LS, Dippenaar A, Ummels R, Piersma SR, van der Woude AD, van der Kuij K, Le Chevalier F, Mata-Espinosa D, Barrios-Payan J, Marquina-Castillo B, Guapillo C, Jimenez CR, Pain A, Houben ENG, Warren RM, Brosch R, Hernandez-Pando R, Bitter W (2018) Mutations in ppe38 block PE_PGRS secretion and increase virulence of Mycobacterium tuberculosis. Nat Microbiol 3(2):181–188

    Article  CAS  PubMed  Google Scholar 

  163. Pareek M, Evans J, Innes J, Smith G, Hingley-Wilson S, Lougheed KE, Sridhar S, Dedicoat M, Hawkey P, Lalvani A (2013) Ethnicity and mycobacterial lineage as determinants of tuberculosis disease phenotype. Thorax 68(3):221–229

    Article  PubMed  Google Scholar 

  164. Ouimet M, Koster S, Sakowski E, Ramkhelawon B, van Solingen C, Oldebeken S, Karunakaran D, Portal-Celhay C, Sheedy FJ, Ray TD, Cecchini K, Zamore PD, Rayner KJ, Marcel YL, Philips JA, Moore KJ (2016) Mycobacterium tuberculosis induces the miR-33 locus to reprogram autophagy and host lipid metabolism. Nat Immunol 17(6):677–686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Dorhoi A, Iannaccone M, Farinacci M, Fae KC, Schreiber J, Moura-Alves P, Nouailles G, Mollenkopf HJ, Oberbeck-Muller D, Jorg S, Heinemann E, Hahnke K, Lowe D, Del Nonno F, Goletti D, Capparelli R, Kaufmann SH (2013) MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J Clin Invest 123(11):4836–4848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Rothchild AC, Sissons JR, Shafiani S, Plaisier C, Min D, Mai D, Gilchrist M, Peschon J, Larson RP, Bergthaler A, Baliga NS, Urdahl KB, Aderem A (2016) MiR-155-regulated molecular network orchestrates cell fate in the innate and adaptive immune response to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 113(41):E6172–E6181

    Article  CAS  PubMed  Google Scholar 

  167. Chen YC, Chao TY, Leung SY, Chen CJ, Wu CC, Fang WF, Wang YH, Chang HC, Wang TY, Lin YY, Zheng YX, Lin MC, Hsiao CC (2017) Histone H3K14 hypoacetylation and H3K27 hypermethylation along with HDAC1 up-regulation and KDM6B down-regulation are associated with active pulmonary tuberculosis disease. Am J Transl Res 9(4):1943–1955

    CAS  PubMed  PubMed Central  Google Scholar 

  168. Seshadri C, Sedaghat N, Campo M, Peterson G, Wells RD, Olson GS, Sherman DR, Stein CM, Mayanja-Kizza H, Shojaie A, Boom WH, Hawn TR, Tuberculosis Research U (2017) Transcriptional networks are associated with resistance to Mycobacterium tuberculosis infection. PLoS One 12(4):e0175844

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  169. Coussens AK, Wilkinson RJ, Martineau AR (2015) Phenylbutyrate is bacteriostatic against Mycobacterium tuberculosis and regulates the macrophage response to infection, synergistically with 25-hydroxy-vitamin D3. PLoS Pathog 11(7):e1005007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  170. Kleinnijenhuis J, Quintin J, Preijers F, Joosten LA, Ifrim DC, Saeed S, Jacobs C, van Loenhout J, de Jong D, Stunnenberg HG, Xavier RJ, van der Meer JW, van Crevel R, Netea MG (2012) Bacille Calmette–Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci USA 109(43):17537–17542

    Article  CAS  PubMed  Google Scholar 

  171. Joosten SA, van Meijgaarden KE, Arend SM, Prins C, Oftung F, Korsvold GE, Kik SV, Arts RJ, van Crevel R, Netea MG, Ottenhoff TH (2018) Mycobacterial growth inhibition is associated with trained innate immunity. J Clin Invest 128(5):1837–1851

    Article  PubMed  PubMed Central  Google Scholar 

  172. Verma D, Parasa VR, Raffetseder J, Martis M, Mehta RB, Netea M, Lerm M (2017) Anti-mycobacterial activity correlates with altered DNA methylation pattern in immune cells from BCG-vaccinated subjects. Sci Rep 7(1):12305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  173. Kaufmann E, Sanz J, Dunn JL, Khan N, Mendonca LE, Pacis A, Tzelepis F, Pernet E, Dumaine A, Grenier JC, Mailhot-Leonard F, Ahmed E, Belle J, Besla R, Mazer B, King IL, Nijnik A, Robbins CS, Barreiro LB, Divangahi M (2018) BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172(1–2):176–190 e119

    Google Scholar 

  174. Kelly B, O’Neill LA (2015) Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Res 25(7):771–784

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  175. Arts RJW, Carvalho A, La Rocca C, Palma C, Rodrigues F, Silvestre R, Kleinnijenhuis J, Lachmandas E, Goncalves LG, Belinha A, Cunha C, Oosting M, Joosten LAB, Matarese G, van Crevel R, Netea MG (2016) Immunometabolic pathways in BCG-induced trained immunity. Cell Rep 17(10):2562–2571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Braverman J, Sogi KM, Benjamin D, Nomura DK, Stanley SA (2016) HIF-1alpha is an essential mediator of IFN-gamma-dependent immunity to Mycobacterium tuberculosis. J Immunol 197(4):1287–1297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Braverman J, Stanley SA (2017) Nitric oxide modulates macrophage responses to Mycobacterium tuberculosis infection through activation of HIF-1alpha and repression of NF-kappaB. J Immunol 199(5):1805–1816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Jo EK, Silwal P, Yuk JM (2019) AMPK-targeted effector networks in mycobacterial infection. Front Microbiol 10:520

    Article  PubMed  PubMed Central  Google Scholar 

  179. Bafica A, Scanga CA, Serhan C, Machado F, White S, Sher A, Aliberti J (2005) Host control of Mycobacterium tuberculosis is regulated by 5-lipoxygenase-dependent lipoxin production. J Clin Invest 115(6):1601–1606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Chen M, Divangahi M, Gan H, Shin DS, Hong S, Lee DM, Serhan CN, Behar SM, Remold HG (2008) Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J Exp Med 205(12):2791–2801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Divangahi M, Chen M, Gan H, Desjardins D, Hickman TT, Lee DM, Fortune S, Behar SM, Remold HG (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 10(8):899–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Divangahi M, Desjardins D, Nunes-Alves C, Remold HG, Behar SM (2010) Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol 11(8):751–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Knight M, Braverman J, Asfaha K, Gronert K, Stanley S (2018) Lipid droplet formation in Mycobacterium tuberculosis infected macrophages requires IFN-gamma/HIF-1alpha signaling and supports host defense. PLoS Pathog 14(1):e1006874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  184. Chang PV, Hao L, Offermanns S, Medzhitov R (2014) The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA 111(6):2247–2252

    Article  CAS  PubMed  Google Scholar 

  185. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL, Marsland BJ (2014) Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20(2):159–166

    Article  CAS  PubMed  Google Scholar 

  186. Allen M, Bailey C, Cahatol I, Dodge L, Yim J, Kassissa C, Luong J, Kasko S, Pandya S, Venketaraman V (2015) Mechanisms of control of Mycobacterium tuberculosis by NK cells: role of glutathione. Front Immunol 6:508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  187. Teskey G, Cao R, Islamoglu H, Medina A, Prasad C, Prasad R, Sathananthan A, Fraix M, Subbian S, Zhong L, Venketaraman V (2018) The synergistic effects of the glutathione precursor, NAC and first-line antibiotics in the granulomatous response against Mycobacterium tuberculosis. Front Immunol 9:2069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Tiwari S, van Tonder AJ, Vilcheze C, Mendes V, Thomas SE, Malek A, Chen B, Chen M, Kim J, Blundell TL, Parkhill J, Weinrick B, Berney M, Jacobs WR Jr (2018) Arginine-deprivation-induced oxidative damage sterilizes Mycobacterium tuberculosis. Proc Natl Acad Sci USA 115(39):9779–9784

    Article  CAS  PubMed  Google Scholar 

  189. Lange SM, McKell MC, Schmidt SM, Zhao J, Crowther RR, Green LC, Bricker RL, Arnett E, Kohler SE, Schlesinger LS, Setchell KDR, Qualls JE (2019) l-Arginine synthesis from l-citrulline in myeloid cells drives host defense against mycobacteria in vivo. J Immunol 202(6):1747–1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Martineau AR, Timms PM, Bothamley GH, Hanifa Y, Islam K, Claxton AP, Packe GE, Moore-Gillon JC, Darmalingam M, Davidson RN, Milburn HJ, Baker LV, Barker RD, Woodward NJ, Venton TR, Barnes KE, Mullett CJ, Coussens AK, Rutterford CM, Mein CA, Davies GR, Wilkinson RJ, Nikolayevskyy V, Drobniewski FA, Eldridge SM, Griffiths CJ (2011) High-dose vitamin D3 during intensive-phase antimicrobial treatment of pulmonary tuberculosis: a double-blind randomised controlled trial. Lancet 377(9761):242–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Campbell GR, Spector SA (2012) Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog 8(5):e1002689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Wheelwright M, Kim EW, Inkeles MS, De Leon A, Pellegrini M, Krutzik SR, Liu PT (2014) All-trans retinoic acid-triggered antimicrobial activity against Mycobacterium tuberculosis is dependent on NPC2. J Immunol 192(5):2280–2290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Hu S, He W, Du X, Huang Y, Fu Y, Yang Y, Hu C, Li S, Wang Q, Wen Q, Zhou X, Zhou C, Zhong XP, Ma L (2018) Vitamin B1 helps to limit Mycobacterium tuberculosis growth via regulating innate immunity in a peroxisome proliferator-activated receptor-gamma-dependent manner. Front Immunol 9:1778

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  194. He W, Hu S, Du X, Wen Q, Zhong XP, Zhou X, Zhou C, Xiong W, Gao Y, Zhang S, Wang R, Yang J, Ma L (2018) Vitamin B5 reduces bacterial growth via regulating innate immunity and adaptive immunity in mice infected with Mycobacterium tuberculosis. Front Immunol 9:365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  195. Vilcheze C, Hartman T, Weinrick B, Jacobs WR Jr (2013) Mycobacterium tuberculosis is extraordinarily sensitive to killing by a vitamin C-induced Fenton reaction. Nat Commun 4:1881

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  196. Brighenti S, Bergman P, Martineau AR (2018) Vitamin D and tuberculosis: where next? J Intern Med

  197. Coussens AK, Wilkinson RJ, Hanifa Y, Nikolayevskyy V, Elkington PT, Islam K, Timms PM, Venton TR, Bothamley GH, Packe GE, Darmalingam M, Davidson RN, Milburn HJ, Baker LV, Barker RD, Mein CA, Bhaw-Rosun L, Nuamah R, Young DB, Drobniewski FA, Griffiths CJ, Martineau AR (2012) Vitamin D accelerates resolution of inflammatory responses during tuberculosis treatment. Proc Natl Acad Sci USA 109(38):15449–15454

    Article  CAS  PubMed  Google Scholar 

  198. Neyrolles O, Wolschendorf F, Mitra A, Niederweis M (2015) Mycobacteria, metals, and the macrophage. Immunol Rev 264(1):249–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Sweetland AC, Jaramillo E, Wainberg ML, Chowdhary N, Oquendo MA, Medina-Marino A, Dua T (2018) Tuberculosis: an opportunity to integrate mental health services in primary care in low-resource settings. Lancet Psychiatry 5(12):952–954

    Article  PubMed  PubMed Central  Google Scholar 

  200. Ban TA (2001) Pharmacotherapy of depression: a historical analysis. J Neural Transm (Vienna) 108(6):707–716

    Article  CAS  Google Scholar 

  201. Diaz A, Bongiovanni B, D’Attilio L, Santucci N, Didoli G, Fernandez RDV, Kovalevski L, Lioi S, Gardenez W, Brandan N, Nannini LJ, Besedovsky H, Del Rey A, Bottasso O, Bay ML (2017) The clinical recovery of tuberculosis patients undergoing specific treatment is associated with changes in the immune and neuroendocrine responses. Pathog Dis 75:7

    Article  CAS  Google Scholar 

  202. Roewe J, Higer M, Riehl DR, Gericke A, Radsak MP, Bosmann M (2017) Neuroendocrine modulation of IL-27 in macrophages. J Immunol 199(7):2503–2514

    Article  CAS  PubMed  Google Scholar 

  203. Boomershine CS, Lafuse WP, Zwilling BS (1999) Beta2-adrenergic receptor stimulation inhibits nitric oxide generation by Mycobacterium avium infected macrophages. J Neuroimmunol 101(1):68–75

    Article  CAS  PubMed  Google Scholar 

  204. Barrios-Payan J, Revuelta A, Mata-Espinosa D, Marquina-Castillo B, Villanueva EB, Gutierrez ME, Perez-Sanchez G, Pavon L, Hernandez-Pando R (2016) The contribution of the sympathetic nervous system to the immunopathology of experimental pulmonary tuberculosis. J Neuroimmunol 298:98–105

    Article  CAS  PubMed  Google Scholar 

  205. Critchley JA, Young F, Orton L, Garner P (2013) Corticosteroids for prevention of mortality in people with tuberculosis: a systematic review and meta-analysis. Lancet Infect Dis 13(3):223–237

    Article  CAS  PubMed  Google Scholar 

  206. Smego RA, Ahmed N (2003) A systematic review of the adjunctive use of systemic corticosteroids for pulmonary tuberculosis. Int J Tuberc Lung Dis 7(3):208–213

    CAS  PubMed  Google Scholar 

  207. Kim JK, Kim YS, Lee HM, Jin HS, Neupane C, Kim S, Lee SH, Min JJ, Sasai M, Jeong JH, Choe SK, Kim JM, Yamamoto M, Choy HE, Park JB, Jo EK (2018) GABAergic signaling linked to autophagy enhances host protection against intracellular bacterial infections. Nat Commun 9(1):4184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  208. Klose CS, Artis D (2019) Neuronal regulation of innate lymphoid cells. Curr Opin Immunol 56:94–99

    Article  CAS  PubMed  Google Scholar 

  209. Tiberi S, du Plessis N, Walzl G, Vjecha MJ, Rao M, Ntoumi F, Mfinanga S, Kapata N, Mwaba P, McHugh TD, Ippolito G, Migliori GB, Maeurer MJ, Zumla A (2018) Tuberculosis: progress and advances in development of new drugs, treatment regimens, and host-directed therapies. Lancet Infect Dis 18(7):e183–e198

    Article  PubMed  Google Scholar 

  210. Mayer-Barber KD, Andrade BB, Oland SD, Amaral EP, Barber DL, Gonzales J, Derrick SC, Shi R, Kumar NP, Wei W, Yuan X, Zhang G, Cai Y, Babu S, Catalfamo M, Salazar AM, Via LE, Barry CE 3rd, Sher A (2014) Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 511(7507):99–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Sanmamed MF, Chen L (2018) A paradigm shift in cancer immunotherapy: from enhancement to normalization. Cell 175(2):313–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2017YFA0505900), the National Natural Science Funds for Distinguished Young Scholar (81825014), the National Natural Science Foundation of China (31830003, 81571954), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB29020000), and the Key Program of Logistics Research (BWS17J030).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qiyao Chai or Cui Hua Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chai, Q., Lu, Z. & Liu, C.H. Host defense mechanisms against Mycobacterium tuberculosis. Cell. Mol. Life Sci. 77, 1859–1878 (2020). https://doi.org/10.1007/s00018-019-03353-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03353-5

Keywords

Navigation