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Latest Comprehensive Knowledge of the Crosstalk between TLR Signaling and Mycobacteria and the Antigens Driving the Process

  • Kim, Jae-Sung (Department of Molecular and Life Science, Hanyang University) ;
  • Kim, Ye-Ram (Department of Molecular and Life Science, Hanyang University) ;
  • Yang, Chul-Su (Department of Molecular and Life Science, Hanyang University)
  • Received : 2019.08.29
  • Accepted : 2019.09.25
  • Published : 2019.10.28

Abstract

Tuberculosis, which is caused by Mycobacterium tuberculosis (Mtb), is among the most pressing worldwide problems. Mtb uniquely interacts with innate immune cells through various pattern recognition receptors. These interactions initiate several inflammatory pathways that play essential roles in controlling Mtb pathogenesis. Although the TLR signaling pathways have essential roles in numerous host's immune defense responses, the role of TLR signaling in the response to Mtb infection is still unclear. This review presents discussions on host-Mtb interactions in terms of Mtb-mediated TLR signaling. In addition, we highlight recent discoveries pertaining to these pathways that may help in new immunotherapeutic opportunities.

Keywords

References

  1. Jeon S, Lim N, Park S, Park M, Kim S. 2018. Comparison of PFGE, IS6110-RFLP, and 24-Locus MIRU-VNTR for molecular epidemiologic typing of Mycobacterium tuberculosis isolates with known epidemic connections. J. Microbiol. Biotechnol. 28: 338-346. https://doi.org/10.4014/jmb.1704.04042
  2. Glaziou P, Floyd K, Raviglione MC. 2018. Global epidemiology of tuberculosis. Semin. Respir. Crit. Care Med. 39: 271-285. https://doi.org/10.1055/s-0038-1651492
  3. Wu S, Wang Y, Zhang M, Shrestha SS, Wang M, He JQ. 2018. Genetic polymorphisms of IL1B, IL6, and TNFalpha in a Chinese Han population with pulmonary tuberculosis. Biomed. Res. Int. 2018: 3010898.
  4. Kim S, Seo H, Mahmud HA, Islam MI, Kim YS, Lyu J, et al. 2017. In vitro effect of DFC-2 on mycolic acid biosynthesis in Mycobacterium tuberculosis. J. Microbiol. Biotechnol. 27: 1932-1941. https://doi.org/10.4014/jmb.1705.05013
  5. Azad AK, Sadee W, Schlesinger LS. 2012. Innate immune gene polymorphisms in tuberculosis. Infect. Immun. 80: 3343-3359. https://doi.org/10.1128/IAI.00443-12
  6. Venketaraman V. 2018. Understanding the host immune response against Mycobacterium tuberculosis Infection, pp. 23-40. Ed. Springer, Switzerland.
  7. Dookie N, Rambaran S, Padayatchi N, Mahomed S, Naidoo K. 2018. Evolution of drug resistance in Mycobacterium tuberculosis: a review on the molecular determinants of resistance and implications for personalized care. J. Antimicrob. Chemother. 73: 1138-1151. https://doi.org/10.1093/jac/dkx506
  8. Kwon BE, Ahn JH, Min S, Kim H, Seo J, Yeo SG, et al. 2018. Development of new preventive and therapeutic vaccines for Tuberculosis. Immune Netw. 18(2): e17. https://doi.org/10.4110/in.2018.18.e17
  9. Queval CJ, Brosch R, Simeone R. 2017. The macrophage: a disputed fortress in the battle against Mycobacterium tuberculosis. Front. Microbiol. 8: 2284. https://doi.org/10.3389/fmicb.2017.02284
  10. Mayer-Barber KD, Barber DL. 2015. Innate and adaptive cellular immune responses to Mycobacterium tuberculosis Infection. Cold Spring Harb. Perspect. Med. 5(12).
  11. van Crevel R, Ottenhoff TH, van der Meer JW. 2002. Innate immunity to Mycobacterium tuberculosis. Clin. Microbiol. Rev. 15: 294-309. https://doi.org/10.1128/CMR.15.2.294-309.2002
  12. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. https://doi.org/10.1016/j.cell.2006.02.015
  13. McClean CM, Tobin DM. 2016. Macrophage form, function, and phenotype in mycobacterial infection: lessons from tuberculosis and other diseases. Pathog Dis. 74(7).
  14. Berrington WR, Hawn TR. 2007. Mycobacterium tuberculosis, macrophages, and the innate immune response: does common variation matter? Immunol. Rev. 219: 167-186. https://doi.org/10.1111/j.1600-065X.2007.00545.x
  15. Ernst JD. 1998. Macrophage receptors for Mycobacterium tuberculosis. Infect. Immun. 66: 1277-1281. https://doi.org/10.1128/IAI.66.4.1277-1281.1998
  16. Ciaramella A, Cavone A, Santucci MB, Amicosante M, Martino A, Auricchio G, et al. 2002. Proinflammatory cytokines in the course of Mycobacterium tuberculosisinduced apoptosis in monocytes/macrophages. J. Infect. Dis. 186: 1277-1282. https://doi.org/10.1086/344645
  17. Moure R, Domingo P, Gallego-Escuredo JM, Villarroya J, Gutierrez Mdel M, Mateo MG, et al. 2016. Impact of elvitegravir on human adipocytes: alterations in differentiation, gene expression and release of adipokines and cytokines. Antiviral Res. 132: 59-65. https://doi.org/10.1016/j.antiviral.2016.05.013
  18. Voskuil MI, Bartek IL, Visconti K, Schoolnik GK. 2011. The response of mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front. Microbiol. 2: 105.
  19. Amaral EP, Lasunskaia EB, D'Imperio-Lima MR. 2016. Innate immunity in tuberculosis: how the sensing of mycobacteria and tissue damage modulates macrophage death. Microbes Infect. 18: 11-20. https://doi.org/10.1016/j.micinf.2015.09.005
  20. Zhai W, Wu F, Zhang Y, Fu Y, Liu Z. 2019. The Immune escape mechanisms of Mycobacterium tuberculosis. Int. J. Mol Sci. 20(2).
  21. Blanc L, Gilleron M, Prandi J, Song OR, Jang MS, Gicquel B, et al. 2017.Mycobacterium tuberculosis inhibits human innate immune responses via the production of TLR2 antagonist glycolipids. Proc. Natl. Acad. Sci. USA 114: 11205-11210. https://doi.org/10.1073/pnas.1707840114
  22. Seo JY, Choi JW, Lee JY, Park YS, Park YI. 2018. Enzyme hydrolysates of ginseng marc polysaccharides promote the phagocytic activity of macrophages via activation of TLR2 and Mer tyrosine kinase. J. Microbiol. Biotechnol. 28: 860-873. https://doi.org/10.4014/jmb.1801.01003
  23. Triantafilou M, Gamper FG, Haston RM, Mouratis MA, Morath S, Hartung T, et al. 2006. Membrane sorting of tolllike receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281: 31002-31011. https://doi.org/10.1074/jbc.M602794200
  24. Lim KH, Staudt LM. 2013. Toll-like receptor signaling. Cold Spring Harb. Perspect Biol. 5: a011247. https://doi.org/10.1101/cshperspect.a011247
  25. Irie T, Muta T, Takeshige K. 2000. TAK1 mediates an activation signal from toll-like receptor(s) to nuclear factorkappaB in lipopolysaccharide-stimulated macrophages. FEBS Lett. 467: 160-164. https://doi.org/10.1016/S0014-5793(00)01146-7
  26. Kawai T, Akira S. 2007. Signaling to NF-kappaB by tolllike receptors. Trends Mol. Med. 13: 460-469. https://doi.org/10.1016/j.molmed.2007.09.002
  27. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384. https://doi.org/10.1038/ni.1863
  28. Vijay K. 2018. Toll-like receptors in immunity and inflammatory diseases: Past, present, and future. Int. Immunopharmacol. 59: 391-412. https://doi.org/10.1016/j.intimp.2018.03.002
  29. Holscher C, Reiling N, Schaible UE, Holscher A, Bathmann C, Korbel D, et al. 2008. Containment of aerogenic Mycobacterium tuberculosis infection in mice does not require MyD88 adaptor function for TLR2, -4 and -9. Eur. J. Immunol. 38: 680-694. https://doi.org/10.1002/eji.200736458
  30. Kleinnijenhuis J, Oosting M, Joosten LA, Netea MG, Van Crevel R. 2011. Innate immune recognition of Mycobacterium tuberculosis. Clin. Dev. Immunol. 2011: 405310.
  31. Basu J, Shin DM, Jo EK. 2012. Mycobacterial signaling through toll-like receptors. Front. Cell Infect. Microbiol. 2: 145.
  32. Mortaz E, Adcock IM, Tabarsi P, Masjedi MR, Mansouri D, Velayati AA, et al. 2015. Interaction of pattern recognition receptors with Mycobacterium Tuberculosis. J. Clin. Immunol. 35: 1-10. https://doi.org/10.1007/s10875-015-0199-4
  33. Hossain MM, Norazmi MN. 2013. Pattern recognition receptors and cytokines in Mycobacterium tuberculosis infection--the double-edged sword? Biomed. Res. Int. 2013: 179174.
  34. Kawai T, Akira S. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650. https://doi.org/10.1016/j.immuni.2011.05.006
  35. Underhill DM, Ozinsky A, Smith KD, Aderem A. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96: 14459-14463. https://doi.org/10.1073/pnas.96.25.14459
  36. Kleinnijenhuis J, Joosten LA, van de Veerdonk FL, Savage N, van Crevel R, Kullberg BJ, et al. 2009. Transcriptional and inflammasome-mediated pathways for the induction of IL-1beta production by Mycobacterium tuberculosis. Eur. J. Immunol. 39: 1914-1922. https://doi.org/10.1002/eji.200839115
  37. Pompei L, Jang S, Zamlynny B, Ravikumar S, McBride A, Hickman SP, et al. 2007. Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs. J. Immunol. 178: 5192-5199. https://doi.org/10.4049/jimmunol.178.8.5192
  38. Lee HM, Shin DM, Kim KK, Lee JS, Paik TH, Jo EK. 2009. Roles of reactive oxygen species in CXCL8 and CCL2 expression in response to the 30-kDa antigen of Mycobacterium tuberculosis. J. Clin. Immunol. 29: 46-56. https://doi.org/10.1007/s10875-008-9222-3
  39. Romero MM, Basile JI, Corra Feo L, Lopez B, Ritacco V, Aleman M. 2016. Reactive oxygen species production by human dendritic cells involves TLR2 and dectin-1 and is essential for efficient immune response against Mycobacteria. Cell Microbiol. 18: 875-886. https://doi.org/10.1111/cmi.12562
  40. Drennan MB, Nicolle D, Quesniaux VJ, Jacobs M, Allie N, Mpagi J, et al. 2004. Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am. J. Pathol. 164: 49-57. https://doi.org/10.1016/S0002-9440(10)63095-7
  41. Reiling N, Holscher C, Fehrenbach A, Kroger S, Kirschning CJ, Goyert S, et al. 2002. Cutting edge: toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol. 169: 3480-3484. https://doi.org/10.4049/jimmunol.169.7.3480
  42. Sugawara I, Yamada H, Li C, Mizuno S, Takeuchi O, Akira S. 2003. Mycobacterial infection in TLR2 and TLR6 knockout mice. Microbiol. Immunol. 47: 327-336. https://doi.org/10.1111/j.1348-0421.2003.tb03404.x
  43. Gopalakrishnan A, Dietzold J, Verma S, Bhagavathula M, Salgame P. 2019. Toll-like receptor 2 prevents neutrophildriven immunopathology during infection with mycobacterium tuberculosis by curtailing CXCL5 production. Infect. Immun. 87(3): pii: e00760-1.
  44. Jung SB, Yang CS, Lee JS, Shin AR, Jung SS, Son JW, et al. 2006. The mycobacterial 38-kilodalton glycolipoprotein antigen activates the mitogen-activated protein kinase pathway and release of proinflammatory cytokines through Toll-like receptors 2 and 4 in human monocytes. Infect. Immun. 74: 2686-2696. https://doi.org/10.1128/IAI.74.5.2686-2696.2006
  45. McBride A, Bhatt K, Salgame P. 2011. Development of a secondary immune response to Mycobacterium tuberculosis is independent of Toll-like receptor 2. Infect. Immun. 79: 1118-1123. https://doi.org/10.1128/IAI.01076-10
  46. Bai W, Liu H, J i Q, Zhou Y, L iang L , Zheng R, et al. 2014. TLR3 regulates mycobacterial RNA-induced IL-10 production through the PI3K/AKT signaling pathway. Cell Signal. 26: 942-950. https://doi.org/10.1016/j.cellsig.2014.01.015
  47. Antonelli LR, Gigliotti Rothfuchs A, Goncalves R, Roffe E, Cheever AW, Bafica A, et al. 2010. Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J. Clin. Invest. 120: 1674-1682. https://doi.org/10.1172/JCI40817
  48. Huang L, Russell DG. 2017. Protective immunity against tuberculosis: what does it look like and how do we find it? Curr. Opin. Immunol. 48: 44-50. https://doi.org/10.1016/j.coi.2017.08.001
  49. Speth MT, Repnik U, Muller E, Spanier J, Kalinke U, Corthay A, et al. 2017. Poly(I:C)-Encapsulating nanoparticles enhance innate immune responses to the Tuberculosis vaccine Bacille Calmette-Guerin (BCG) via synergistic activation of innate immune receptors. Mol. Pharm. 14: 4098-4112. https://doi.org/10.1021/acs.molpharmaceut.7b00795
  50. Liu X, Da Z, Wang Y, Niu H, Li R, Yu H, et al. 2 016 . A novel liposome adjuvant DPC mediates Mycobacterium tuberculosis subunit vaccine well to induce cell-mediated immunity and high protective efficacy in mice. Vaccine 34: 1370-1378. https://doi.org/10.1016/j.vaccine.2016.01.049
  51. Pandey S, Kawai T, Akira S. 2014. Microbial sensing by Toll-like receptors and intracellular nucleic acid sensors. Cold Spring Harb. Perspect. Biol. 7: a016246. https://doi.org/10.1101/cshperspect.a016246
  52. Sepehri Z, Kiani Z, Kohan F, Ghavami S. 2019. Toll-like receptor 4 as an immune receptor against Mycobacterium tuberculosis: a systematic review. Lab. Med. 50: 117-129. https://doi.org/10.1093/labmed/lmy047
  53. Lv J, He X, Wang H, Wang Z, Kelly GT, Wang X, et al. 2017. TLR4-NOX2 axis regulates the phagocytosis and killing of Mycobacterium tuberculosis by macrophages. BMC Pulm. Med. 17: 194. https://doi.org/10.1186/s12890-017-0517-0
  54. Means TK, Jones BW, Schromm AB, Shurtleff BA, Smith JA, Keane J, et al. 2001. Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J. Immunol. 166: 4074-4082. https://doi.org/10.4049/jimmunol.166.6.4074
  55. Doz E, Rose S, Nigou J, Gilleron M, Puzo G, Erard F, et al. 2007. Acylation determines the toll-like receptor (TLR)-dependent positive versus TLR2-, mannose receptor-, and SIGNR1-independent negative regulation of pro-inflammatory cytokines by mycobacterial lipomannan. J. Biol. Chem. 282: 26014-26025. https://doi.org/10.1074/jbc.M702690200
  56. Chang JS, Huggett JF, Dheda K, Kim LU, Zumla A, Rook GA. 2006. Myobacterium tuberculosis induces selective upregulation of TLRs in the mononuclear leukocytes of patients with active pulmonary tuberculosis. J. Immunol. 176: 3010-3018. https://doi.org/10.4049/jimmunol.176.5.3010
  57. Abel B, Thieblemont N, Quesniaux VJ, Brown N, Mpagi J, Miyake K, et al. 2002. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J. Immunol. 169: 3155-3162. https://doi.org/10.4049/jimmunol.169.6.3155
  58. Kleinnijenhuis J, Quintin J, Preijers F, Benn CS, Joosten LA, Jacobs C, et al. 2014. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. J. Innate. Immun. 6: 152-158. https://doi.org/10.1159/000355628
  59. Hilda JN, Selvaraj A, Das SD. 2012. Mycobacterium tuberculosis H37Rv is more effective compared to vaccine strains in modulating neutrophil functions: an in vitro study. FEMS Immunol. Med. Microbiol. 66: 372-381. https://doi.org/10.1111/j.1574-695X.2012.01025.x
  60. Nancy Hilda J, Das S. 2018. Neutrophil CD64, TLR2 and TLR4 expression increases but phagocytic potential decreases during tuberculosis. Tuberculosis (Edinb). 111: 135-142. https://doi.org/10.1016/j.tube.2018.06.010
  61. Branger J, Leemans JC, Florquin S, Weijer S, Speelman P, Van Der Poll T. 2004. Toll-like receptor 4 plays a protective role in pulmonary tuberculosis in mice. Int. Immunol. 16: 509-516. https://doi.org/10.1093/intimm/dxh052
  62. Shim TS, Turner OC, Orme IM. 2003. Toll-like receptor 4 plays no role in susceptibility of mice to Mycobacterium tuberculosis infection. Tuberculosis (Edinb) 83: 367-371. https://doi.org/10.1016/S1472-9792(03)00071-4
  63. Sanchez D, Rojas M, Hernandez I, Radzioch D, Garcia LF, Barrera LF. 2010. Role of TLR2- and TLR4-mediated signaling in Mycobacterium tuberculosis-induced macrophage death. Cell Immunol. 260: 128-136. https://doi.org/10.1016/j.cellimm.2009.10.007
  64. Bao M, Yi Z, Fu Y. 2017. Activation of TLR7 Inhibition of Mycobacterium Tuberculosis Survival by Autophagy in RAW 264.7 Macrophages. J. Cell Biochem. 118: 4222-4229. https://doi.org/10.1002/jcb.26072
  65. Davila S , Hibberd ML, H ari Dass R , Wong H E, Sahiratmadja E, Bonnard C, et al. 2008. Genetic association and expression studies indicate a role of toll-like receptor 8 in pulmonary tuberculosis. PLoS Genet. 4: e1000218. https://doi.org/10.1371/journal.pgen.1000218
  66. Lai Y F, L in TM, Wang CH, Su PY, Wu JT, Lin MC, et al. 2016. Functional polymorphisms of the TLR7 and TLR8 genes contribute to Mycobacterium tuberculosis infection. Tuberculosis (Edinb) 98: 125-131. https://doi.org/10.1016/j.tube.2016.03.008
  67. Tang J, Sun M, Shi G, Xu Y, Han Y, Li X, et al. 2017. Toll-Like receptor 8 agonist strengthens the protective efficacy of ESAT-6 immunization to Mycobacterium tuberculosis infection. Front. Immunol. 8: 1972. https://doi.org/10.3389/fimmu.2017.01972
  68. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745. https://doi.org/10.1038/35047123
  69. Latz E, Schoenemeyer A, Visintin A, Fitzgerald KA, Monks BG, Knetter CF, et al. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5: 190-198. https://doi.org/10.1038/ni1028
  70. Jo EK, Yang CS, Choi CH, Harding CV. 2007. Intracellular signalling cascades regulating innate immune responses to Mycobacteria: branching out from Toll-like receptors. Cell Microbiol. 9: 1087-1098. https://doi.org/10.1111/j.1462-5822.2007.00914.x
  71. Rahman AH, Taylor DK, Turka LA. 2009. The contribution of direct TLR signaling to T cell responses. Immunol. Res. 45: 25-36. https://doi.org/10.1007/s12026-009-8113-x
  72. 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: 1715-1724. https://doi.org/10.1084/jem.20051782
  73. Cervantes JL, Oak E, Garcia J, Liu H, Lorenzini PA, Batra D, et al. 2019. Vitamin D modulates human macrophage response to Mycobacteriumc. Tuberculosis (Edinb) 116S: S131-S137.
  74. Chen Z, Wang W, Liang J, Wang J, Feng S, Zhang G. 2015. Association between toll-like receptors 9 (TLR9) gene polymorphism and risk of pulmonary tuberculosis: metaanalysis. BMC Pulm. Med. 15: 57. https://doi.org/10.1186/s12890-015-0049-4
  75. Graustein AD, Horne DJ, Arentz M, Bang ND, Chau TT, Thwaites GE, et al. 2015. TLR9 gene region polymorphisms and susceptibility to tuberculosis in Vietnam. Tuberculosis (Edinb) 95: 190-196. https://doi.org/10.1016/j.tube.2014.12.009
  76. Bharti D, Kumar A, Mahla RS, Kumar S, Ingle H, Shankar H, et al. 2014. The role of TLR9 polymorphism in susceptibility to pulmonary tuberculosis. Immunogenetics 66: 675-681. https://doi.org/10.1007/s00251-014-0806-1
  77. Yuk JM, Jo EK. 2014. Host immune responses to mycobacterial antigens and their implications for the development of a vaccine to control tuberculosis. Clin. Exp. Vaccine Res. 3: 155-167. https://doi.org/10.7774/cevr.2014.3.2.155
  78. Geluk A, van Meijgaarden KE, Joosten SA, Commandeur S, Ottenhoff TH. 2014. Innovative strategies to identify M. tuberculosis antigens and epitopes using genome-wide analyses. Front. Immunol. 5: 256.
  79. Lindestam Arlehamn CS, Lewinsohn D, Sette A, Lewinsohn D. 2014. Antigens for CD4 and CD8 T cells in tuberculosis. Cold Spring Harb. Perspect. Med. 4: a018465. https://doi.org/10.1101/cshperspect.a018465
  80. Moguche AO, Musvosvi M, Penn-Nicholson A, Plumlee CR, Mearns H, Geldenhuys H, et al. 2017. Antigen availability shapes T cell differentiation and function during tuberculosis. Cell Host Microbe 21: 695-706. https://doi.org/10.1016/j.chom.2017.05.012
  81. Yang JD, Mott D, Sutiwisesak R, Lu YJ, Raso F, Stowell B, et al. 2018. Mycobacterium tuberculosis-specific CD4+ and CD8+ T cells differ in their capacity to recognize infected macrophages. PLoS Pathog. 14: e1007060. https://doi.org/10.1371/journal.ppat.1007060
  82. Commandeur S, van den Eeden SJ, Dijkman K, Clark SO, van Meijgaarden KE, Wilson L, et al. 2014. The in vivo expressed Mycobacterium tuberculosis (IVE-TB) antigen Rv2034 induces CD4(+) T-cells that protect against pulmonary infection in HLA-DR transgenic mice and guinea pigs. Vaccine 32: 3580-3588. https://doi.org/10.1016/j.vaccine.2014.05.005
  83. Li F, Feng L, Jin C, Wu X, Fan L, Xiong S, et al. 2018. LpqT improves mycobacteria survival in macrophages by inhibiting TLR2 mediated inflammatory cytokine expression and cell apoptosis. Tuberculosis (Edinb). 111: 57-66. https://doi.org/10.1016/j.tube.2018.05.007
  84. Su H, Zhu S, Zhu L, Huang W, Wang H, Zhang Z, et al. 2016. Recombinant lipoprotein Rv1016c derived from Mycobacterium tuberculosis is a TLR-2 ligand that induces macrophages apoptosis and inhibits MHC II antigen processing. Front. Cell. Infect. Microbiol. 6: 147.
  85. Drage MG, Tsai HC, Pecora ND, Cheng TY, Arida AR, Shukla S, et al. 2010. Mycobacterium tuberculosis lipoprotein LprG (Rv1411c) binds triacylated glycolipid agonists of Toll-like receptor 2. Nat. Struct. Mol. Biol. 17: 1088-1095. https://doi.org/10.1038/nsmb.1869
  86. Gehring AJ, D obos KM, Belisle J T, Harding C V, B oom WH. 2004. Mycobacterium tuberculosis LprG (Rv1411c): a novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J. Immunol. 173: 2660-2668. https://doi.org/10.4049/jimmunol.173.4.2660
  87. Pecora ND, Gehring AJ, Canaday DH, Boom WH, Harding CV. 2006. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J. Immunol. 177: 422-429. https://doi.org/10.4049/jimmunol.177.1.422
  88. Shin DM, Yuk JM, Lee HM, Lee SH, Son JW, Harding CV, et al. 2010. Mycobacterial lipoprotein activates autophagy via TLR2/1/CD14 and a functional vitamin D receptor signalling. Cell. Microbiol. 12: 1648-1665. https://doi.org/10.1111/j.1462-5822.2010.01497.x
  89. Lancioni CL, Li Q, Thomas JJ, Ding X, Thiel B, Drage MG, et al. 2011. Mycobacterium tuberculosis lipoproteins directly regulate human memory CD4(+) T cell activation via Tolllike receptors 1 and 2. Infect. Immun. 79: 663-673. https://doi.org/10.1128/IAI.00806-10
  90. Sanchez A, Espinosa P, Garcia T, Mancilla R. 2012. The 19 kDa Mycobacterium tuberculosis lipoprotein (LpqH) induces macrophage apoptosis through extrinsic and intrinsic pathways: a role for the mitochondrial apoptosis-inducing factor. Clin. Dev. Immunol. 2012: 950503.
  91. Liu L, Liu J, Niu G, Xu Q, Chen Q. 2015. Mycobacterium tuberculosis 19-kDa lipoprotein induces Toll-like receptor 2-dependent peroxisome proliferator-activated receptor gamma expression and promotes inflammatory responses in human macrophages. Mol. Med. Rep. 11: 2921-2926. https://doi.org/10.3892/mmr.2014.3070
  92. Lopez M, Sly LM, Luu Y, Young D, Cooper H, Reiner NE. 2003. The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J. Immunol. 170: 2409-2416. https://doi.org/10.4049/jimmunol.170.5.2409
  93. Chen ST, Li JY, Zhang Y, Gao X, Cai H. 2012. Recombinant MPT83 derived from Mycobacterium tuberculosis induces cytokine production and upregulates the function of mouse macrophages through TLR2. J. Immunol. 188: 668-677. https://doi.org/10.4049/jimmunol.1102177
  94. Wang L, Zuo M, Chen H, Liu S, Wu X, Cui Z, et al. 2017. Mycobacterium tuberculosis lipoprotein MPT83 induces apoptosis of infected macrophages by activating the TLR2/p38/COX-2 signaling pathway. J. Immunol. 198: 4772-4780. https://doi.org/10.4049/jimmunol.1700030
  95. Elass E, Aubry L, Masson M, Denys A, Guerardel Y, Maes E, et al. 2005. Mycobacterial lipomannan induces matrix metalloproteinase-9 expression in human macrophagic cells through a Toll-like receptor 1 (TLR1)/TLR2- and CD14-dependent mechanism. Infect. Immun. 73: 7064-7068. https://doi.org/10.1128/IAI.73.10.7064-7068.2005
  96. Gilleron M, Nigou J, Nicolle D, Quesniaux V, Puzo G. 2006. The acylation state of mycobacterial lipomannans modulates innate immunity response through toll-like receptor 2. Chem. Biol. 13: 39-47. https://doi.org/10.1016/j.chembiol.2005.10.013
  97. Puissegur MP, Lay G, Gilleron M, Botella L, Nigou J, Marrakchi H, et al. 2007. Mycobacterial lipomannan induces granuloma macrophage fusion via a TLR2-dependent, ADAM9- and beta1 integrin-mediated pathway. J. Immunol. 178: 3161-3169. https://doi.org/10.4049/jimmunol.178.5.3161
  98. Tapping RI, Tobias PS. 2003. Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling. J. Endotoxin Res. 9: 264-268. https://doi.org/10.1177/09680519030090040801
  99. Bansal K, Elluru SR, Narayana Y, Chaturvedi R, Patil SA, Kaveri SV, et al. 2010. PE_PGRS antigens of Mycobacterium tuberculosis induce maturation and activation of human dendritic cells. J. Immunol. 184: 3495-3504. https://doi.org/10.4049/jimmunol.0903299
  100. Chaturvedi R, Bansal K, Narayana Y, Kapoor N, Sukumar N, Togarsimalemath SK, et al. 2010. The multifunctional PE_PGRS11 protein from Mycobacterium tuberculosis plays a role in regulating resistance to oxidative stress. J. Biol. Chem. 285: 30389-30403. https://doi.org/10.1074/jbc.M110.135251
  101. Basu S, Pathak SK, Banerjee A, Pathak S, Bhattacharyya A, Yang Z, et al. 2007. Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-alpha. J. Biol. Chem. 282: 1039-1050. https://doi.org/10.1074/jbc.M604379200
  102. Palucci I, Camassa S, Cascioferro A, Sali M, Anoosheh S, Zumbo A, et al. 2016. PE_PGRS33 contributes to Mycobacterium tuberculosis entry in macrophages through interaction with TLR2. PLoS One 11: e0150800. https://doi.org/10.1371/journal.pone.0150800
  103. Vani J, Shaila MS, Trinath J, Balaji KN, Kaveri SV, Bayry J. 2013. Mycobacterium tuberculosis cell wall-associated Rv3812 protein induces strong dendritic cell-mediated interferon gamma responses and exhibits vaccine potential. J. Infect. Dis. 208: 1034-1036. https://doi.org/10.1093/infdis/jit281
  104. Huang Y, Wang Y, Bai Y, Wang ZG, Yang L, Zhao D. 2010. Expression of PE_PGRS 62 protein in Mycobacterium smegmatis decrease mRNA expression of proinflammatory cytokines IL-1beta, IL-6 in macrophages. Mol. Cell. Biochem. 340: 223-229. https://doi.org/10.1007/s11010-010-0421-x
  105. Bhat KH, Chaitanya CK, Parveen N, Varman R, Ghosh S, Mukhopadhyay S. 2012. Proline-proline-glutamic acid (PPE) protein Rv1168c of Mycobacterium tuberculosis augments transcription from HIV-1 long terminal repeat promoter. J. Biol. Chem. 287: 16930-16946. https://doi.org/10.1074/jbc.M111.327825
  106. Ahmed A, Dolasia K, Mukhopadhyay S. 2018. Mycobacterium tuberculosis PPE18 protein reduces inflammation and increases survival in animal model of sepsis. J. Immunol. 200: 3587-3598. https://doi.org/10.4049/jimmunol.1602065
  107. Nair S, Ramaswamy PA, Ghosh S, Joshi DC, Pathak N, Siddiqui I, et al. 2009. The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage. J. Immunol. 183: 6269-6281. https://doi.org/10.4049/jimmunol.0901367
  108. Tiwari B, Soory A, Raghunand TR. 2014. An immunomodulatory role for the Mycobacterium tuberculosis region of difference 1 locus proteins PE35 (Rv3872) and PPE68 (Rv3873). FEBS J. 281: 1556-1570. https://doi.org/10.1111/febs.12723
  109. Su H, Kong C, Zhu L, Huang Q, Luo L, Wang H, et al. 2015. PPE26 induces TLR2-dependent activation of macrophages and drives Th1-type T-cell immunity by triggering the cross-talk of multiple pathways involved in the host response. Oncotarget 6: 38517-38537. https://doi.org/10.18632/oncotarget.5956
  110. Deng W, Li W, Zeng J, Zhao Q, Li C, Zhao Y, et al. 2014. Mycobacterium tuberculosis PPE family protein Rv1808 manipulates cytokines profile via co-activation of MAPK and NF-kappaB signaling pathways. Cell. Physiol. Biochem. 33: 273-288. https://doi.org/10.1159/000356668
  111. Su H, Zhang Z, Liu Z, Peng B, Kong C, Wang H, et al. 2018. Mycobacterium tuberculosis PPE60 antigen drives Th1/Th17 responses via Toll-like receptor 2-dependent maturation of dendritic cells. J. Biol. Chem. 293: 10287-10302. https://doi.org/10.1074/jbc.RA118.001696
  112. Parveen N, Varman R, Nair S, Das G, Ghosh S, Mukhopadhyay S. 2013. Endocytosis of Mycobacterium tuberculosis heat shock protein 60 is required to induce interleukin-10 production in macrophages. J. Biol. Chem. 288: 24956-24971. https://doi.org/10.1074/jbc.M113.461004
  113. Khan N, Alam K, Mande SC, Valluri VL, Hasnain SE, Mukhopadhyay S. 2008. Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages. Cell. Microbiol. 10: 1711-1722. https://doi.org/10.1111/j.1462-5822.2008.01161.x
  114. Singh PP, LeMaire C, Tan JC, Zeng E, Schorey JS. 2011. Exosomes released from M. tuberculosis infected cells can suppress IFN-gamma mediated activation of naive macrophages. PLoS One. 6: e18564. https://doi.org/10.1371/journal.pone.0018564
  115. Bednarska K, Kielbik M, Sulowska Z, Dziadek J, Klink M. 2014. Cholesterol oxidase binds TLR2 and modulates functional responses of human macrophages. Mediators Inflamm. 2014: 498395. https://doi.org/10.1155/2014/498395
  116. Byun EH, Kim WS, Kim JS, Jung ID, Park YM, Kim HJ, et al. 2012. Mycobacterium tuberculosis Rv0577, a novel TLR2 agonist, induces maturation of dendritic cells and drives Th1 immune response. FASEB J. 26: 2695-2711. https://doi.org/10.1096/fj.11-199588
  117. Madan-Lala R, Peixoto KV, Re F, Rengarajan J. 2011. Mycobacterium tuberculosis Hip1 dampens macrophage proinflammatory responses by limiting toll-like receptor 2 activation. Infect. Immun. 79: 4828-4838. https://doi.org/10.1128/IAI.05574-11
  118. Madan-Lala R, Sia JK, King R, Adekambi T, Monin L, Khader SA, et al. 2014. Mycobacterium tuberculosis impairs dendritic cell functions through the serine hydrolase Hip1. J. Immunol. 192: 4263-4272. https://doi.org/10.4049/jimmunol.1303185
  119. Bandyopadhyay U, Chadha A, Gupta P, Tiwari B, Bhattacharyya K, Popli S, et al. 2017. Suppression of Tolllike receptor 2-mediated proinflammatory responses by Mycobacterium tuberculosis protein Rv3529c. J. Leukoc Biol. 102: 1249-1259. https://doi.org/10.1189/jlb.4A0217-042R
  120. Kumar A, Singh SM, Singh R, Kaur J. 2017. Rv0774c, an iron stress inducible, extracellular esterase is involved in immune-suppression associated with altered cytokine and TLR2 expression. Int. J. Med. Microbiol. 307: 126-138. https://doi.org/10.1016/j.ijmm.2017.01.003
  121. Liu Y, Li JY, Chen ST, Huang HR, Cai H. 2016. The rLrp of Mycobacterium tuberculosis inhibits proinflammatory cytokine production and downregulates APC function in mouse macrophages via a TLR2-mediated PI3K/Akt pathway activation-dependent mechanism. Cell. Mol. Immunol. 13: 729-746. https://doi.org/10.1038/cmi.2015.58
  122. Gao X, Wu C, He W, Wang X, Li Y, Wang Y, et al. 2019. DosR antigen Rv1737c induces activation of macrophages dependent on the TLR2 pathway. Cell. Immunol. 344: 103947. https://doi.org/10.1016/j.cellimm.2019.103947
  123. Peddireddy V, Doddam SN, Qureshi IA, Yerra P, Ahmed N. 2016. A putative nitroreductase from the DosR regulon of Mycobacterium tuberculosis induces pro-inflammatory cytokine expression via TLR2 signaling pathway. Sci. Rep. 6: 24535. https://doi.org/10.1038/srep24535
  124. Yihao D, Hongyun H, Maodan T. 2015. Latency-associated protein Rv2660c of Mycobacterium tuberculosis augments expression of proinflammatory cytokines in human macrophages by interacting with TLR2. Infect. Dis. (Lond) 47: 168-177. https://doi.org/10.3109/00365548.2014.982167
  125. Kim WS, Kim JS, Cha SB, Kim H, Kwon KW, Kim SJ, et al. 2016. Mycobacterium tuberculosis Rv3628 drives Th1-type T cell immunity via TLR2-mediated activation of dendritic cells and displays vaccine potential against the hypervirulent Beijing K strain. Oncotarget 7: 24962-24982. https://doi.org/10.18632/oncotarget.8771
  126. Kumar A, Lewin A, Rani PS, Qureshi IA, Devi S, Majid M, et al. 2013. Dormancy associated translation inhibitor (DATIN/Rv0079) of Mycobacterium tuberculosis interacts with TLR2 and induces proinflammatory cytokine expression. Cytokine 64: 258-264. https://doi.org/10.1016/j.cyto.2013.06.310
  127. Saraav I, Singh S, Pandey K, Sharma M, Sharma S. 2017. Mycobacterium tuberculosis MymA is a TLR2 agonist that activate macrophages and a TH1 response. Tuberculosis (Edinb). 106: 16-24. https://doi.org/10.1016/j.tube.2017.05.005
  128. Prados-Rosales R, Baena A, Martinez LR, Luque-Garcia J, Kalscheuer R, Veeraraghavan U, et al. 2011. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Invest. 121: 1471-1483. https://doi.org/10.1172/JCI44261
  129. Ko A, Wui SR, Ryu JI, Lee YJ, Hien DTT, RheeI, et al. 2018. Potentiation of Th1-type immune responses to Mycobacterium tuberculosis antigens in mice by cationic liposomes combined with De-O-Acylated Lipooligosaccharide. J. Microbiol. Biotechnol. 28: 136-144. https://doi.org/10.4014/jmb.1709.09009
  130. Sun F, Oh S, Kim J, Kato T, Kim HJ, Lee J, et al. 2017. Enhanced internalization of Macromolecular drugs into Mycobacterium smegmatis with the assistance of silver nanoparticles. J. Microbiol. Biotechnol. 27: 1483-1490. https://doi.org/10.4014/jmb.1612.12041
  131. Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV. 2006. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J. Immunol. 176: 4323-4330. https://doi.org/10.4049/jimmunol.176.7.4323
  132. Choi HG, Choi S, Back YW, Park HS, Bae HS, Choi CH, et al. 2016. Mycobacterium tuberculosis Rv2882c protein induces activation of macrophages through TLR4 and exhibits vaccine potential. PLoS One 11: e0164458. https://doi.org/10.1371/journal.pone.0164458
  133. Kim K, Sohn H, Kim JS, Choi HG, Byun EH, Lee KI, et al. 2012. Mycobacterium tuberculosis Rv0652 s timulates production of tumour necrosis factor and monocytes chemoattractant protein-1 in macrophages through the Toll-like receptor 4 pathway. Immunology 136: 231-240. https://doi.org/10.1111/j.1365-2567.2012.03575.x
  134. Lee SJ, Shin SJ, Lee MH, Lee MG, Kang TH, Park WS, et al. 2014. A potential protein adjuvant derived from Mycobacterium tuberculosis Rv0652 enhances dendritic cellsbased tumor immunotherapy. PLoS One 9: e104351. https://doi.org/10.1371/journal.pone.0104351
  135. Stewart GR, Snewin VA, Walzl G, Hussell T, Tormay P, O'Gaora P, et al. 2001. Overexpression of heat-shock proteins reduces survival of Mycobacterium tuberculosis in the chronic phase of infection. Nat. Med. 7: 732-737. https://doi.org/10.1038/89113
  136. Young DB, Garbe TR. 1991. Heat shock proteins and antigens of Mycobacterium tuberculosis. Infect. Immun. 59: 3086-3093. https://doi.org/10.1128/IAI.59.9.3086-3093.1991
  137. Bulut Y, Michelsen KS, Hayrapetian L, Naiki Y, Spallek R, Singh M, et al. 2005. Mycobacterium tuberculosis heat shock proteins use diverse Toll-like receptor pathways to activate pro-inflammatory signals. J. Biol. Chem. 280: 20961-20967. https://doi.org/10.1074/jbc.M411379200
  138. Kim WS, Jung ID, Kim JS, Kim HM, Kwon KW, Park YM, et al. 2018. Mycobacterium tuberculosis GrpE, A heat-shock stress responsive chaperone, promotes Th1-biased T cell immune response via TLR4-Mediated Activation of dendritic cells. Front. Cell. Infect. Microbiol. 8: 95. https://doi.org/10.3389/fcimb.2018.00095
  139. Kim JS, Kim WS, Choi HG, Jang B, Lee K, Park JH, et al. 2013. Mycobacterium tuberculosis RpfB drives Th1-type T cell immunity via a TLR4-dependent activation of dendritic cells. J. Leukoc Biol. 94: 733-749. https://doi.org/10.1189/jlb.0912435
  140. Choi S, Choi HG, Shin KW, Back YW, Park HS, Lee JH, et al. 2018. Mycobacterium tuberculosis protein Rv3841 activates dendritic cells and contributes to a T Helper 1 immune response. J. Immunol. Res. 2018: 3525302.
  141. Lin J, Chang Q, Dai X, Liu D, Jiang Y, Dai Y. 2019. Early secreted antigenic target of 6-kDa of Mycobacterium tuberculosis promotes caspase-9/caspase-3-mediated apoptosis in macrophages. Mol. Cell. Biochem. 457: 179-189. https://doi.org/10.1007/s11010-019-03522-x
  142. Jang AR, Choi JH, Shin SJ, Park JH. 2018. Mycobacterium tuberculosis ESAT6 induces IFN-beta gene expression in Macrophages via TLRs-mediated signaling. Cytokine 104: 104-109. https://doi.org/10.1016/j.cyto.2017.10.006
  143. Samten B, Wang X, Barnes PF. 2009. Mycobacterium tuberculosis ESX-1 system-secreted protein ESAT-6 but not CFP10 inhibits human T-cell immune responses. Tuberculosis (Edinb) 89 Suppl 1: S74-76. https://doi.org/10.1016/S1472-9792(09)70017-4
  144. Lim YJ, Choi JA, Lee JH, Choi CH, Kim HJ, Song CH. 2015. Mycobacterium tuberculosis 38-kDa antigen induces endoplasmic reticulum stress-mediated apoptosis via tolllike receptor 2/4. Apoptosis 20: 358-370. https://doi.org/10.1007/s10495-014-1080-2
  145. Park HS, Back YW, Shin KW, Bae HS, Lee KI, Choi HG, et al. 2019. Mycobacterium tuberculosis Rv3463 induces mycobactericidal activity in macrophages by enhancing phagolysosomal fusion and exhibits therapeutic potential. Sci. Rep. 9: 4246. https://doi.org/10.1038/s41598-019-38982-0
  146. Faridgohar M, Nikoueinejad H. 2017. New findings of Tolllike receptors involved in Mycobacterium tuberculosis infection. Pathog. Glob. Health. 111: 256-264. https://doi.org/10.1080/20477724.2017.1351080
  147. Weeratunga P, Herath TUB, Kim TH, Lee HC, Kim JH, Lee BH, et al. 2017. Dense granule protein-7 (GRA-7) of Toxoplasma gondii inhibits viral replication in vitro and in vivo. J. Microbiol. 55: 909-917. https://doi.org/10.1007/s12275-017-7392-5
  148. Yang CS, Yuk JM, Lee YH, Jo EK. 2016. Toxoplasma gondii GRA7-induced TRAF6 activation contributes to host protective immunity. Infect. Immun. 84: 339-350. https://doi.org/10.1128/IAI.00734-15
  149. Kim YR, Kim JS, Yun JS, Kim S, Kim SY, Jang K, et al. 2018. Toxoplasma gondii GRA8 induces ATP5A1-SIRT3-mediated mitochondrial metabolic resuscitation: a potential therapy for sepsis. Exp. Mol. Med. 50(3): e464. https://doi.org/10.1038/emm.2017.308
  150. Shi L, Eugenin EA, Subbian S. 2016. Immunometabolism in Tuberculosis. Front. Immunol. 7: 150.

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