Distinct Strategies Employed by Dendritic Cells and Macrophages in Restricting Mycobacterium tuberculosis Infection: Different Philosophies but Same Desire

REFERENCES

• Geissmann F, Manz MG, Jung S, Development of monocytes, macrophages, and dendritic cells. Science 2010; 327:656–661.
   PubMed Web of Science ®Google Scholar
• Foucher ED, Blanchard S, Preisser L, IL-34 induces the differentiation of human monocytes into immunosuppressive macrophages. antagonistic effects of GM-CSF and IFNgamma. PLoS One 2013;8:e56045.
   Google Scholar
• Rivollier A, He J, Kole A, Valatas V, Kelsall BL. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med 2013;209:139–155.
   Web of Science ®Google Scholar
• Guilliams M, Lambrecht BN, Hammad H. Division of labor between lung dendritic cells and macrophages in the defense against pulmonary infections. Mucosal Immunol 2013;6:464–473.
   PubMed Web of Science ®Google Scholar
• Giacomini E, Iona E, Ferroni L, Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J Immunol 2001;166:7033–7041.
   PubMed Web of Science ®Google Scholar
• Gutierrez MG, Master SS, Singh SB, Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004;119:753–766.
   PubMed Web of Science ®Google Scholar
• Chan J, Xing Y, Magliozzo RS, Bloom BR. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med 1992;175:1111–1122.
   PubMed Web of Science ®Google Scholar
• Liu PT, Modlin RL. Human macrophage host defense against Mycobacterium tuberculosis. Curr Opin Immunol 2008;20:371–376.
   PubMed Web of Science ®Google Scholar
• Fratazzi C, Arbeit RD, Carini C, Macrophage apoptosis in mycobacterial infections. J Leukoc Biol 1999;66:763–764.
   PubMed Web of Science ®Google Scholar
• Behar SM, Martin CJ, Booty MG, Apoptosis is an innate defense function of macrophages against Mycobacterium tuberculosis. Mucosal Immunol 2011;4:279–287.
   PubMed Web of Science ®Google Scholar
• Tian T, Woodworth J, Skold M, Behar SM. In vivo depletion of CD11c+ cells delays the CD4+ T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J Immunol 2005;175:3268–3272.
   PubMed Web of Science ®Google Scholar
• Buettner M, Meinken C, Bastian M, Inverse correlation of maturity and antibacterial activity in human dendritic cells. J Immunol 2005;174:4203–4209.
   PubMed Web of Science ®Google Scholar
• Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245–252.
   PubMed Web of Science ®Google Scholar
• Wolf AJ, Linas B, Trevejo-Nunez GJ, Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 2007;179:2509–2519.
   PubMed Web of Science ®Google Scholar
• Wolf AJ, Desvignes L, Linas B, Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 2008;205:105–115.
   PubMed Web of Science ®Google Scholar
• Croft M, Bradley LM, Swain SL. Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J Immunol 1994;152:2675–2685.
   PubMed Web of Science ®Google Scholar
• Winau F, Weber S, Sad S, Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 2006;24:105–117.
   PubMed Web of Science ®Google Scholar
• Albert ML, Sauter B, Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 1998;392:86–89.
   PubMed Web of Science ®Google Scholar
• Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783–801.
   PubMed Web of Science ®Google Scholar
• Taylor PR, Martinez-Pomares L, Stacey M, Macrophage receptors and immune recognition. Annu Rev Immunol 2005;23:901–944.
   PubMed Web of Science ®Google Scholar
• Janeway CA, Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002;20:197–216.
   PubMed Web of Science ®Google Scholar
• Jo EK. Mycobacterial interaction with innate receptors: TLRs, C-type lectins, NLRs. Curr Opin Infect Dis 2008;21:279–86.
   PubMed Web of Science ®Google Scholar
• Medzhitov R, Janeway C, Jr. The Toll receptor family and microbial recognition. Trends Microbiol 2000;8:452–456.
   PubMed Web of Science ®Google Scholar
• Saiga H, Shimada Y, Takeda K. Innate immune effectors in mycobacterial infection. Clin Dev Immunol 2011;2011:347594.
   PubMedGoogle Scholar
• Heldwein KA, Fenton MJ. The role of Toll-like receptors in immunity against mycobacterial infection. Microbes Infect 2002;4:937–944.
   PubMed Web of Science ®Google Scholar
• Kleinnijenhuis J, Oosting M, Joosten LA, Innate immune recognition of Mycobacterium tuberculosis. Clin Dev Immunol 2011:405310.
   PubMedGoogle Scholar
• Stenger S, Modlin RL. Control of Mycobacterium tuberculosis through mammalian Toll-like receptors. Curr Opin Immunol 2002;14:452–457.
   PubMed Web of Science ®Google Scholar
• Kleinnijenhuis J, Oosting M, Joosten LA, Innate immune recognition of Mycobacterium tuberculosis. Clin Dev Immunol 2011;2011:405310.
   PubMedGoogle Scholar
• Pompei L, Jang S, Zamlynny B, Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs. J Immunol 2007;178:5192–5199.
   PubMed Web of Science ®Google Scholar
• Zanoni I, Granucci F. Differences in lipopolysaccharide-induced signaling between conventional dendritic cells and macrophages. Immunobiology 2010;215:709–712.
   PubMed Web of Science ®Google Scholar
• Pai RK, Convery M, Hamilton TA, Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 2003;171:175–184.
   PubMed Web of Science ®Google Scholar
• Kusner DJ. Mechanisms of mycobacterial persistence in tuberculosis. Clin Immunol 2005;114:239–247.
   PubMed Web of Science ®Google Scholar
• Houben EN, Nguyen L, Pieters J. Interaction of pathogenic mycobacteria with the host immune system. Curr Opin Microbiol 2006;9:76–85.
   PubMed Web of Science ®Google Scholar
• Balboa L, Romero MM, Yokobori N, Mycobacterium tuberculosis impairs dendritic cell response by altering CD1b, DC-SIGN and MR profile. Immunol Cell Biol 2010;88:716–726.
   PubMed Web of Science ®Google Scholar
• Siddiqui KF, Amir M, Gurram RK, Latency-associated protein Acr1 impairs dendritic cell maturation and functionality: a possible mechanism of immune evasion by Mycobacterium tuberculosis. J Infect Dis 2014;209:1436–1445.
   PubMed Web of Science ®Google Scholar
• Mariotti S, Teloni R, Iona E, Mycobacterium tuberculosis subverts the differentiation of human monocytes into dendritic cells. Eur J Immunol 2002;32:3050–3058.
   PubMed Web of Science ®Google Scholar
• Remoli ME, Giacomini E, Petruccioli E, Bystander inhibition of dendritic cell differentiation by Mycobacterium tuberculosis-induced IL-10. Immunol Cell Biol 2011;89:437–446.
   PubMed Web of Science ®Google Scholar
• Kang PB, Azad AK, Torrelles JB, The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 2005;202:987–999.
   PubMed Web of Science ®Google Scholar
• Tailleux L, Schwartz O, Herrmann JL, DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 2003;197:121–127.
   PubMed Web of Science ®Google Scholar
• Khan N, Gowthaman U, Pahari S, Agrewala JN. Manipulation of costimulatory molecules by intracellular pathogens: veni, vidi, vici!! PLoS Pathog 2012;8:e1002676.
   Google Scholar
• Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009;30:646–655.
   PubMed Web of Science ®Google Scholar
• Demangel C, Britton WJ. Interaction of dendritic cells with mycobacteria: where the action starts. Immunol Cell Biol 2000;78:318–324.
   PubMed Web of Science ®Google Scholar
• Khader SA, Partida-Sanchez S, Bell G, Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J Exp Med 2006;203:1805–1815.
   PubMed Web of Science ®Google Scholar
• Cooper AM. Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 2009;27:393–422.
   PubMed Web of Science ®Google Scholar
• Herbst S, Schaible UE, Schneider BE. Interferon gamma activated macrophages kill mycobacteria by nitric oxide induced apoptosis. PLoS One 2011;6:e19105.
   Google Scholar
• Ottenhoff TH. New pathways of protective and pathological host defense to mycobacteria. Trends Microbiol 2012;20:419–28.
   PubMed Web of Science ®Google Scholar
• Khader SA, Bell GK, Pearl JE, IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007;8:369–377.
   PubMed Web of Science ®Google Scholar
• Scriba TJ, Kalsdorf B, Abrahams DA, Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J Immunol 2008;180:1962–1970.
   PubMed Web of Science ®Google Scholar
• Torrado E, Cooper AM. IL-17 and Th17 cells in tuberculosis. Cytokine Growth Factor Rev 2010;21:455–462.
   PubMed Web of Science ®Google Scholar
• Sakaguchi S, Miyara M, Costantino CM, Hafler DA. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 2010;10:490–500.
   PubMed Web of Science ®Google Scholar
• Tailleux L, Waddell SJ, Pelizzola M, Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One 2008;3:e1403.
   Google Scholar
• Jang S, Uzelac A, Salgame P. Distinct chemokine and cytokine gene expression pattern of murine dendritic cells and macrophages in response to Mycobacterium tuberculosis infection. J Leukoc Biol 2008;84:1264–1270.
   PubMed Web of Science ®Google Scholar
• Hickman SP, Chan J, Salgame P. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 2002;168:4636–4642.
   PubMed Web of Science ®Google Scholar
• Zhou L, Nazarian AA, Smale ST. Interleukin-10 inhibits interleukin-12 p40 gene transcription by targeting a late event in the activation pathway. Mol Cell Biol 2004;24:2385–2396.
   PubMed Web of Science ®Google Scholar
• Murray PJ. The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc Natl Acad Sci U S A 2005;102:8686–8691.
   PubMed Web of Science ®Google Scholar
• Cao S, Liu J, Chesi M, Differential regulation of IL-12 and IL-10 gene expression in macrophages by the basic leucine zipper transcription factor c-Maf fibrosarcoma. J Immunol 2002;169:5715–5725.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Suda T, Naito T, Impaired toll-like receptor 9 expression in alveolar macrophages with no sensitivity to CpG DNA. Am J Respir Crit Care Med 2005;171:707–713.
   PubMed Web of Science ®Google Scholar
• Rothfuchs AG, Bafica A, Feng CG, Dectin-1 interaction with Mycobacterium tuberculosis leads to enhanced IL-12p40 production by splenic dendritic cells. J Immunol 2007;179:3463–3471.
   PubMed Web of Science ®Google Scholar
• Sanjuan MA, Rao N, Lai KT, CpG-induced tyrosine phosphorylation occurs via a TLR9-independent mechanism and is required for cytokine secretion. J Cell Biol 2006;172:1057–1068.
   PubMed Web of Science ®Google Scholar
• LeibundGut-Landmann S, Gross O, Robinson MJ, Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 2007;8:630–638.
   PubMed Web of Science ®Google Scholar
• Underhill DM, Ozinsky A, Smith KD, Aderem A. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc Natl Acad Sci U S A 1999;96:14459–14463.
   PubMed Web of Science ®Google Scholar
• Roach DR, Bean AG, Demangel C, TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J Immunol 2002;168:4620–4627.
   PubMed Web of Science ®Google Scholar
• Flynn JL, Chan J, Lin PL. Macrophages and control of granulomatous inflammation in tuberculosis. Mucosal Immunol 2011;4:271–278.
   PubMed Web of Science ®Google Scholar
• Saunders BM, Cooper AM. Restraining mycobacteria: role of granulomas in mycobacterial infections. Immunol Cell Biol 2000;78:334–341.
   PubMed Web of Science ®Google Scholar
• Ordway D, Harton M, Henao-Tamayo M, Enhanced macrophage activity in granulomatous lesions of immune mice challenged with Mycobacterium tuberculosis. J Immunol 2006;176:4931–4939.
   PubMed Web of Science ®Google Scholar
• Sallusto F, Lanzavecchia A. Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol Rev 2000;177:134–140.
   PubMed Web of Science ®Google Scholar
• Cyster JG. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol 2005;23:127–159.
   PubMed Web of Science ®Google Scholar
• Cyster JG. Chemokines and cell migration in secondary lymphoid organs. Science 1999;286:2098–2102.
   PubMed Web of Science ®Google Scholar
• Parker LC, Whyte MK, Vogel SN, Toll-like receptor (TLR)2 and TLR4 agonists regulate CCR expression in human monocytic cells. J Immunol 2004;172:4977–4986.
   PubMed Web of Science ®Google Scholar
• Lehner M, Morhart P, Stilper A, Efficient chemokine-dependent migration and primary and secondary IL-12 secretion by human dendritic cells stimulated through Toll-like receptors. J Immunother 2007;30:312–322.
   PubMed Web of Science ®Google Scholar
• Bhatt K, Hickman SP, Salgame P. Cutting edge: a new approach to modeling early lung immunity in murine tuberculosis. J Immunol 2004;172:2748–2751.
   PubMed Web of Science ®Google Scholar
• Sallusto F, Palermo B, Lenig D, Distinct patterns and kinetics of chemokine production regulate dendritic cell function. Eur J Immunol 1999;29:1617–1625.
   PubMed Web of Science ®Google Scholar
• Benvenuti F, Lagaudriere-Gesbert C, Grandjean I, Dendritic cell maturation controls adhesion, synapse formation, and the duration of the interactions with naive T lymphocytes. J Immunol 2004;172:292–301.
   PubMed Web of Science ®Google Scholar
• Hugues S, Fetler L, Bonifaz L, Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat Immunol 2004;5:1235–42.
   PubMed Web of Science ®Google Scholar
• Henry CJ, Ornelles DA, Mitchell LM, IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J Immunol 2008;181:8576–8584.
   PubMed Web of Science ®Google Scholar
• Mackay CR. Homing of naive, memory and effector lymphocytes. Curr Opin Immunol 1993;5:423–427.
   PubMed Web of Science ®Google Scholar
• Kim CH, Broxmeyer HE. Chemokines: signal lamps for trafficking of T and B cells for development and effector function. J Leukoc Biol 1999;65:6–15.
   PubMed Web of Science ®Google Scholar
• Iellem A, Mariani M, Lang R, Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med 2001;194:847–53.
   PubMed Web of Science ®Google Scholar
• Algood HM, Lin PL, Flynn JL. Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis. Clin Infect Dis 2005;41 Suppl 3:S189–S193.
   Google Scholar
• Ameixa C, Friedland JS. Interleukin-8 secretion from Mycobacterium tuberculosis-infected monocytes is regulated by protein tyrosine kinases but not by ERK1/2 or p38 mitogen-activated protein kinases. Infect Immun 2002;70:4743–4746.
   PubMed Web of Science ®Google Scholar
• Larsen CG, Thomsen MK, Gesser B, The delayed-type hypersensitivity reaction is dependent on IL-8. Inhibition of a tuberculin skin reaction by an anti-IL-8 monoclonal antibody. J Immunol 1995;155:2151–2157.
   PubMed Web of Science ®Google Scholar
• Reiner SL. Development in motion: helper T cells at work. Cell 2007;129:33–36.
   PubMed Web of Science ®Google Scholar
• McBride A, Konowich J, Salgame P. Host defense and recruitment of Foxp3(+) T regulatory cells to the lungs in chronic Mycobacterium tuberculosis infection requires toll-like receptor 2. PLoS Pathog 2013;9(6): e1003397.
   Google Scholar
• Chodisetti SB, Gowthaman U, Rai PK, Triggering through toll-like receptor 2 limits chronically stimulated T-helper type 1 cells from undergoing exhaustion. J Infect Dis 2015;211:486–96.
   PubMed Web of Science ®Google Scholar
• Carvalho LP, Petritus PM, Trochtenberg AL, Lymph node hypertrophy following Leishmania major infection is dependent on TLR9. J Immunol 2012;188:1394–1401.
   PubMed Web of Science ®Google Scholar
• Mueller P, Pieters J. Modulation of macrophage antimicrobial mechanisms by pathogenic mycobacteria. Immunobiology 2006;211:549–556.
   PubMed Web of Science ®Google Scholar
• Kushwah R, Hu J. Dendritic cell apoptosis: regulation of tolerance versus immunity. J Immunol 2010;185:795–802.
   PubMed Web of Science ®Google Scholar
• De Smedt T, Pajak B, Muraille E, Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J Exp Med 1996;184:1413–1424.
   PubMed Web of Science ®Google Scholar
• Stafford JL, Neumann NF, Belosevic M. Macrophage-mediated innate host defense against protozoan parasites. Crit Rev Microbiol 2002;28:187–248.
   PubMed Web of Science ®Google Scholar
• Armstrong JA, Hart PD. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 1971;134:713–740.
   PubMed Web of Science ®Google Scholar
• Barker LP, George KM, Falkow S, Small PL. Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages. Infect Immun 1997;65:1497–1504.
   PubMed Web of Science ®Google Scholar
• Hasan Z, Schlax C, Kuhn L, Isolation and characterization of the mycobacterial phagosome: segregation from the endosomal/lysosomal pathway. Mol Microbiol 1997;24:545–553.
   PubMed Web of Science ®Google Scholar
• Chan J, Fan XD, Hunter SW, Lipoarabinomannan, a possible virulence factor involved in persistence of Mycobacterium tuberculosis within macrophages. Infect Immun 1991;59:1755–1761.
   PubMed Web of Science ®Google Scholar
• Nagabhushanam V, Solache A, Ting LM, Escaron CJ, Innate inhibition of adaptive immunity: mycobacterium tuberculosis-induced IL-6 inhibits macrophage responses to IFN-gamma. J Immunol 2003;171:4750–4757.
   PubMed Web of Science ®Google Scholar
• Soualhine H, Deghmane AE, Sun J, Mycobacterium bovis bacillus Calmette-Guerin secreting active cathepsin S stimulates expression of mature MHC class II molecules and antigen presentation in human macrophages. J Immunol 2007;179:5137–5145.
   PubMed Web of Science ®Google Scholar
• Gehring AJ, Dobos KM, Belisle JT, Mycobacterium tuberculosis LprG (Rv1411c): a novel TLR-2 ligand that inhibits human macrophage class II MHC antigen processing. J Immunol 2004;173:2660–2668.
   PubMed Web of Science ®Google Scholar
• Fulton SA, Reba SM, Pai RK, Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. Infect Immun 2004;72:2101–2110.
   PubMed Web of Science ®Google Scholar
• Pathak SK, Basu S, Basu KK, Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat Immunol 2007;8:610–618.
   PubMed Web of Science ®Google Scholar
• Mariotti S, Teloni R, Iona E, Mycobacterium tuberculosis diverts alpha interferon-induced monocyte differentiation from dendritic cells into immunoprivileged macrophage-like host cells. Infect Immun 2004;72:4385–4392.
   PubMed Web of Science ®Google Scholar
• Siddiqui KF, Amir M, Gurram RK, Latency associated protein acr1 impairs dendritic cells maturation and functionality: a possible mechanism of immune evasion by mycobacterium tuberculosis. J Infect Dis 2014;209:1436–45.
   PubMed Web of Science ®Google Scholar
• Schlesinger LS, Bellinger-Kawahara CG, Payne NR, Horwitz MA. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 1990;144:2771–2780.
   PubMed Web of Science ®Google Scholar
• Malik ZA, Denning GM, Kusner DJ. Inhibition of Ca(2+) signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J Exp Med 2000;191:287–302.
   PubMed Web of Science ®Google Scholar
• Gowthaman U, Singh V, Zeng W, Promiscuous peptide of 16 kDa antigen linked to Pam2Cys protects against Mycobacterium tuberculosis by evoking enduring memory T-cell response. J Infect Dis 2011;204:1328–1338.
   PubMed Web of Science ®Google Scholar