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Pathogenesis of Mycobacterium tuberculosis and its Interaction with the Host Organism pp 189–209Cite as

Surviving the Macrophage: Tools and Tricks Employed by Mycobacterium tuberculosis

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Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 374))

Abstract

Mycobacterium tuberculosis has evolved to withstand one of the most inhospitable cells within the human body, namely the macrophage, a cell that is normally geared toward the destruction of any invading microbe. How M. tuberculosis achieves this is still incompletely understood; however, a number of mechanisms are now known that provide advantages to M. tuberculosis for its survival and proliferation inside the macrophage. While some of these mechanisms are mediated by factors released by M. tuberculosis, others rely on host components that are being hijacked to benefit survival of M. tuberculosis within the macrophage as well to avoid the generation of an effective immune response. Here, we describe several of these mechanisms, also pointing out the potential usage of this knowledge toward the development of novel strategies to treat tuberculosis. Furthermore, we attempt to put the ‘macrophage niche’ into context with other intracellular pathogens and discuss some of the generalities as well as specializations that M. tuberculosis employs to survive.

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References

  • Abdallah AM, Gey van Pittius NC, Champion PA et al (2007) Type VII secretion–mycobacteria show the way. Nat Rev Microbiol 5:883–891

    Article  PubMed  CAS  Google Scholar 

  • Adams JS, Ren S, Liu PT et al (2009) Vitamin d-directed rheostatic regulation of monocyte antibacterial responses. J Immunol 182:4289–4295

    Article  PubMed  CAS  Google Scholar 

  • Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17:593–623

    Article  PubMed  CAS  Google Scholar 

  • Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783–801

    Article  PubMed  CAS  Google Scholar 

  • Allen LA, Schlesinger LS, Kang B (2000) Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J Exp Med 191:115–128

    Article  PubMed  CAS  Google Scholar 

  • Armstrong JA, Hart PD (1971) Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 134:713–740

    Article  PubMed  CAS  Google Scholar 

  • Av-Gay Y, Everett M (2000) The eukaryotic-like Ser/Thr protein kinases of M. tuberculosis. Trends Microbiol 8:238–244

    Article  PubMed  CAS  Google Scholar 

  • Av-Gay Y, Sobouti R (2000) Cholesterol is accumulated by mycobacteria but its degradation is limited to non-pathogenic fast-growing mycobacteria. Can J Microbiol 46:826–831

    Article  PubMed  CAS  Google Scholar 

  • Bach H, Papavinasasundaram KG, Wong D, Hmama Z, Av-Gay Y (2008) M. tuberculosis virulence is mediated by PtpA dephosphorylation of human vacuolar protein sorting 33B. Cell Host Microbe 3:316–322

    Article  PubMed  CAS  Google Scholar 

  • Be NA, Bishai WR, Jain SK (2012) Role of M. tuberculosis pknD in the pathogenesis of central nervous system tuberculosis. BMC Microbiol 12:7

    Article  PubMed  CAS  Google Scholar 

  • Berthet FX, Lagranderie M, Gounon P et al (1998) Attenuation of virulence by disruption of the M. tuberculosis erp gene. Science 282:759–762

    Article  PubMed  CAS  Google Scholar 

  • Boehm U, Klamp T, Groot M, Howard JC (1997) Cellular responses to interferon-gamma. Annu Rev Immunol 15:749–795

    Article  PubMed  CAS  Google Scholar 

  • Briken V, Porcelli SA, Besra GS, Kremer L (2004) Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53:391–403

    Article  PubMed  CAS  Google Scholar 

  • Brodin P, Majlessi L, Marsollier L et al (2006) Dissection of ESAT-6 system 1 of M. tuberculosis and impact on immunogenicity and virulence. Infect Immun 74:88–98

    Article  PubMed  CAS  Google Scholar 

  • Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221–17224

    Article  PubMed  CAS  Google Scholar 

  • Chakraborty P, Sturgill-Koszycki S, Russell DG (1994) Isolation and characterization of pathogen-containing phagosomes. Methods Cell Biol 45:261–276

    Article  PubMed  CAS  Google Scholar 

  • Chen JM, Boy-Rottger S, Dhar N et al (2012) EspD is critical for the virulence-mediating ESX-1 secretion system in M. tuberculosis. J Bacteriol 194:884–893

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Pieters J (2010) Novel proteasome inhibitors as potential drugs to combat tuberculosis. J Mol Cell Biol 2:173–175

    Article  PubMed  CAS  Google Scholar 

  • Cole ST, Eiglmeier K, Parkhill J et al (2001) Massive gene decay in the leprosy bacillus. Nature 409:1007–1011

    Article  PubMed  CAS  Google Scholar 

  • Combaluzier B, Mueller P, Massner J, Finke D, Pieters J (2009) Coronin 1 is essential for IgM-mediated Ca2+ mobilization in B cells but dispensable for the generation of immune responses in vivo. J Immunol 182:1954–1961

    Article  PubMed  CAS  Google Scholar 

  • Cosma CL, Klein K, Kim R, Beery D, Ramakrishnan L (2006) Mycobacterium marinum Erp is a virulence determinant required for cell wall integrity and intracellular survival. Infect Immun 74:3125–3133

    Article  PubMed  CAS  Google Scholar 

  • Cowley S, Ko M, Pick N et al (2004) The M. tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol 52:1691–1702

    Article  PubMed  CAS  Google Scholar 

  • Cywes C, Hoppe HC, Daffe M, Ehlers MR (1997) Nonopsonic binding of M. tuberculosis to complement receptor type 3 is mediated by capsular polysaccharides and is strain dependent. Infect Immun 65:4258–4266

    PubMed  CAS  Google Scholar 

  • Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF (2003) The proteasome of M. tuberculosis is required for resistance to nitric oxide. Science 302:1963–1966

    Article  PubMed  CAS  Google Scholar 

  • Davies DG, Chakrabarty AM, Geesey GG (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl Environ Microbiol 59:1181–1186

    PubMed  CAS  Google Scholar 

  • de Jonge MI, Pehau-Arnaudet G, Fretz MM et al (2007) ESAT-6 from M. tuberculosis dissociates from its putative chaperone CFP-10 under acidic conditions and exhibits membrane-lysing activity. J Bacteriol 189:6028–6034

    Article  PubMed  CAS  Google Scholar 

  • Deghmane AE, Soualhine H, Bach H et al (2007) Lipoamide dehydrogenase mediates retention of coronin-1 on BCG vacuoles, leading to arrest in phagosome maturation. J Cell Sci 120:2796–2806

    Article  PubMed  CAS  Google Scholar 

  • Deretic V, Singh S, Master S et al (2006) Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol 8:719–727

    Article  PubMed  CAS  Google Scholar 

  • Desjardins M, Descoteaux A (1997) Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan. J Exp Med 185:2061–2068

    Article  PubMed  CAS  Google Scholar 

  • DiGiuseppe Champion PA, Cox JS (2007) Protein secretion systems in Mycobacteria. Cell Microbiol 9:1376–1384

    Article  CAS  Google Scholar 

  • Drennan MB, Nicolle D, Quesniaux VJ et al (2004) Toll-like receptor 2-deficient mice succumb to M. tuberculosis infection. Am J Pathol 164:49–57

    Article  PubMed  CAS  Google Scholar 

  • Ehlers S (2010) DC-SIGN and mannosylated surface structures of M. tuberculosis: a deceptive liaison. Eur J Cell Biol 89:95–101

    Article  PubMed  CAS  Google Scholar 

  • Fabri M, Stenger S, Shin DM et al (2011) Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci Transl Med 3:104ra102

    Google Scholar 

  • Feng CG, Collazo-Custodio CM, Eckhaus M et al (2004) Mice deficient in LRG-47 display increased susceptibility to mycobacterial infection associated with the induction of lymphopenia. J Immunol 172:1163–1168

    PubMed  CAS  Google Scholar 

  • Ferrari G, Langen H, Naito M, Pieters J (1999) A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97:435–447

    Article  PubMed  CAS  Google Scholar 

  • Foger N, Rangell L, Danilenko DM, Chan AC (2006) Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 313:839–842.

    Article  PubMed  CAS  Google Scholar 

  • Fortune SM, Jaeger A, Sarracino DA et al (2005) Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci USA 102:10676–10681

    Article  PubMed  CAS  Google Scholar 

  • Franchi L, Amer A, Body-Malapel M et al (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7:576–582

    Article  PubMed  CAS  Google Scholar 

  • Fratti RA, Chua J, Vergne I, Deretic V (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 100:5437–5442

    Article  PubMed  CAS  Google Scholar 

  • Ganaie AA, Lella RK, Solanki R, Sharma C (2011) Thermostable hexameric form of Eis (Rv2416c) protein of M. tuberculosis plays an important role for enhanced intracellular survival within macrophages. PLoS One 6:e27590

    Article  PubMed  CAS  Google Scholar 

  • Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, Brown EJ (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53:1677–1693

    Article  PubMed  CAS  Google Scholar 

  • Gatfield J, Pieters J (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288:1647–1650

    Article  PubMed  CAS  Google Scholar 

  • Gatfield J, Pieters J (2003) Molecular mechanisms of host-pathogen interaction: Entry and survival of mycobacteria in macrophages. Adv Immunol 82:45–96

    Google Scholar 

  • Gatfield J, Albrecht I, Zanolari B, Steinmetz MO, Pieters J (2005) Association of the Leukocyte Plasma Membrane with the Actin Cytoskeleton through Coiled Coil-mediated Trimeric Coronin 1 Molecules. Mol Biol Cell 16:2786–2798

    Article  PubMed  CAS  Google Scholar 

  • Gengenbacher M, Kaufmann SH (2012) Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev 36:514–532

    Article  PubMed  CAS  Google Scholar 

  • Goldberg DE, Siliciano RF, Jacobs WR, Jr (2012) Outwitting evolution: fighting drug-resistant TB, malaria, and HIV. Cell 148:1271–1283

    Article  PubMed  CAS  Google Scholar 

  • Greenstein AE, MacGurn JA, Baer CE, Falick AM, Cox JS, Alber T (2007) M. tuberculosis Ser/Thr protein kinase D phosphorylates an anti–anti-sigma factor homolog. PLoS Pathog 3:e49

    Article  PubMed  CAS  Google Scholar 

  • Grinstein S (2010) Imaging signal transduction during phagocytosis: phospholipids, surface charge, and electrostatic interactions. Am J Physiol. Cell Physiol 299:C876–881

    Article  PubMed  CAS  Google Scholar 

  • Grundner C, Gay LM, Alber T (2005) Mycobacterium tuberculosis serine/threonine kinases PknB, PknD, PknE, and PknF phosphorylate multiple FHA domains. Protein Sci 14:1918–1921

    Article  PubMed  CAS  Google Scholar 

  • Hackstadt T, Fischer ER, Scidmore MA, Rockey DD, Heinzen RA (1997) Origins and functions of the chlamydial inclusion. Trends Microbiol 5:288–293

    Article  PubMed  CAS  Google Scholar 

  • Han G, Zhang C–C (2001) On the origin of Ser/Thr kinases in a prokaryote. FEMS Microbiol Lett 200:79–84

    Article  PubMed  CAS  Google Scholar 

  • Harris J, De Haro SA, Master SS, Keane J, Roberts EA, Delgado M, Deretic V (2007) T helper 2 cytokines inhibit autophagic control of intracellular M. tuberculosis. Immunity 27:505–517

    Article  PubMed  CAS  Google Scholar 

  • Hasan Z, Schlax C, Kuhn L, Lefkovits I, Young D, Thole J, Pieters J (1997) Isolation and characterization of the mycobacterial phagosome: segregation from the endosomal/lysosomal pathway. Mol Microbiol 24:545–553

    PubMed  CAS  Google Scholar 

  • Hassett DJ (1996) Anaerobic production of alginate by Pseudomonas aeruginosa: alginate restricts diffusion of oxygen. J Bacteriol 178:7322–7325

    PubMed  CAS  Google Scholar 

  • Hemmi H, Takeuchi O, Kawai T et al (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408:740–745

    Article  PubMed  CAS  Google Scholar 

  • Henry SC, Daniell X, Indaram M et al (2007) Impaired macrophage function underscores susceptibility to Salmonella in mice lacking Irgm1 (LRG-47). J Immunol 179:6963–6972

    PubMed  CAS  Google Scholar 

  • Houben EN, Nguyen L, Pieters J (2006) Interaction of pathogenic mycobacteria with the host immune system. Curr Opin Microbiol 9:76–85

    Article  PubMed  CAS  Google Scholar 

  • Houben EN, Walburger A, Ferrari G et al (2009) Differential expression of a virulence factor in pathogenic and non-pathogenic mycobacteria. Mol Microbiol 72:41–52

    Article  PubMed  CAS  Google Scholar 

  • Hughes EA, Galan JE (2002) Immune response to Salmonella: location, location, location? Immunity 16:325–328

    Article  PubMed  CAS  Google Scholar 

  • Hunn JP, Howard JC (2010) The mouse resistance protein Irgm1 (LRG-47): a regulator or an effector of pathogen defense? PLoS Pathog 6:e1001008

    Article  PubMed  CAS  Google Scholar 

  • Hurme R, Cossart P (1999) Invasion of mammalian cells by Listeria monocytogenes. In: Gordon S (ed) Phagocytosis: Microbial invasion. JAI Press Inc., Stamford, pp 59–79

    Chapter  Google Scholar 

  • Iniesta V, Gomez-Nieto LC, Corraliza I (2001) The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J Exp Med 193:777–784

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa E, Ishikawa T, Morita YS et al (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 206:2879–2888

    Article  PubMed  CAS  Google Scholar 

  • Janeway CA, Jr., Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216

    Article  PubMed  CAS  Google Scholar 

  • Jayachandran R, Sundaramurthy V, Combaluzier B et al (2007) Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell 130:37–50

    Article  PubMed  CAS  Google Scholar 

  • Jayachandran R, Gatfield J, Massner J, Albrecht I, Zanolari B, Pieters J (2008) RNA interference in J774 macrophages reveals a role for Coronin 1 in mycobacterial trafficking but not in actin-dependent processes. Mol Biol Cell 19:1241–1251

    Article  PubMed  CAS  Google Scholar 

  • Kang CM, Abbott DW, Park ST, Dascher CC, Cantley LC, Husson RN (2005) The M. tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev 19:1692–1704

    Article  PubMed  CAS  Google Scholar 

  • Kaye PM, Rogers NJ, Curry AJ, Scott JC (1994) Deficient expression of co-stimulatory molecules on Leishmania-infected macrophages. Eur J Immunol 24:2850–2854

    Article  PubMed  CAS  Google Scholar 

  • Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, MacMicking JD (2011) A family of IFN-gamma-inducible 65-kD GTPases protects against bacterial infection. Science 332:717–721

    Article  PubMed  CAS  Google Scholar 

  • Kim KH, An DR, Song J et al (2012) Mycobacterium tuberculosis Eis protein initiates suppression of host immune responses by acetylation of DUSP16/MKP-7. Proc Natl Acad Sci USA 109:7729–7734

    Article  PubMed  CAS  Google Scholar 

  • Kima PE, Soong L, Chicharro C, Ruddle NH, McMahon-Pratt D (1996) Leishmania-infected macrophages sequester endogenously synthesized parasite antigens from presentation to CDCD4+ T cells. Eur J Immunol 26:3163–3169

    Article  PubMed  CAS  Google Scholar 

  • Kleinnijenhuis J, Oosting M, Plantinga TS, van der Meer JW, Joosten LA, Crevel RV, Netea MG (2011) Autophagy modulates the M. tuberculosis-induced cytokine response. Immunology 134:341–348

    Article  PubMed  CAS  Google Scholar 

  • Klepp LI, Soria M, Blanco FC, Bianco MV, Santangelo MP, Cataldi AA, Bigi F (2009) Identification of two proteins that interact with the Erp virulence factor from M. tuberculosis by using the bacterial two-hybrid system. BMC Mol Biol 10:3

    Article  PubMed  CAS  Google Scholar 

  • Lahiri A, Eswarappa SM, Das P, Chakravortty D (2010) Altering the balance between pathogen containing vacuoles and lysosomes: a lesson from Salmonella. Virulence 1:325–329

    Article  PubMed  Google Scholar 

  • Lang C, Hildebrandt A, Brand F, Opitz L, Dihazi H, Luder CG (2012) Impaired chromatin remodelling at STAT1-regulated promoters leads to global unresponsiveness of Toxoplasma gondii-Infected macrophages to IFN-gamma. PLoS Pathog 8:e1002483

    Article  PubMed  CAS  Google Scholar 

  • Le Cabec V, Cols C, Maridonneau-Parini I (2000) Nonopsonic phagocytosis of zymosan and M. kansasii by CR3 (CD11b/CD18) involves distinct molecular determinants and is or is not coupled with NADPH oxidase activation. Infect Immun 68:4736–4745

    Article  PubMed  Google Scholar 

  • Le Cabec V, Carreno S, Moisand A, Bordier C, Maridonneau-Parini I (2002) Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively. J Immunol 169:2003–2009

    PubMed  Google Scholar 

  • Lemeland JF, Allaire R, Boiron H (1974) [Hemolysin of Listeria monocytogenes (listeriolysin)]. Pathol Biol (Paris) 22:763–770

    CAS  Google Scholar 

  • Lin G, Li D, de Carvalho LP et al (2009) Inhibitors selective for mycobacterial versus human proteasomes. Nature 461:621–626

    Article  PubMed  CAS  Google Scholar 

  • Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJ, Yap GS (2006) Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 203:2063–2071

    Article  PubMed  CAS  Google Scholar 

  • Lingwood D, Kaiser HJ, Levental I, Simons K (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem Soc Trans 37:955–960

    Article  PubMed  CAS  Google Scholar 

  • Liu PT, Stenger S, Li H et al (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311:1770–1773

    Article  PubMed  CAS  Google Scholar 

  • Liu PT, Stenger S, Tang DH, Modlin RL (2007) Cutting edge: vitamin D-mediated human antimicrobial activity against M. tuberculosis is dependent on the induction of cathelicidin. J Immunol 179:2060–2063

    PubMed  CAS  Google Scholar 

  • MacGurn JA, Cox JS (2007) A genetic screen for M. tuberculosis mutants defective for phagosome maturation arrest identifies components of the ESX-1 secretion system. Infect Immun 75:2668–2678

    Article  PubMed  CAS  Google Scholar 

  • MacMicking JD, Taylor GA, McKinney JD (2003) Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 302:654–659

    Article  PubMed  CAS  Google Scholar 

  • Mahdavi J, Sonden B, Hurtig M et al (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297:573–578

    Article  PubMed  CAS  Google Scholar 

  • Majlessi L, Brodin P, Brosch R et al (2005) Influence of ESAT-6 secretion system 1 (RD1) of M. tuberculosis on the interaction between mycobacteria and the host immune system. J Immunol 174:3570-3579.

    PubMed  CAS  Google Scholar 

  • Malik ZA, Denning GM, Kusner DJ (2000) Inhibition of Ca(2 +) signaling by M. tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J Exp Med 191:287–302

    Article  PubMed  CAS  Google Scholar 

  • Malik ZA, Thompson CR, Hashimi S, Porter B, Iyer SS, Kusner DJ (2003) Cutting edge: M. tuberculosis blocks Ca2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol 170:2811–2815

    PubMed  CAS  Google Scholar 

  • Master SS, Rampini SK, Davis AS et al (2008) Mycobacterium tuberculosis prevents inflammasome activation. Cell Host Microbe 3:224–232

    Article  PubMed  CAS  Google Scholar 

  • Mauel J (1990) Macrophage-parasite interactions in Leishmania infections. J Leukoc Biol 47:187–193

    PubMed  CAS  Google Scholar 

  • Meresse S, Steele-Mortimer O, Moreno E, Desjardins M, Finlay B, Gorvel JP (1999) Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat Cell Biol 1:E183–188

    Article  PubMed  CAS  Google Scholar 

  • Mueller P, Massner J, Jayachandran R et al (2008) Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering. Nat Immunol 9:424–431

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay R, Jia J, Arif A, Ray PS, Fox PL (2009) The GAIT system: a gatekeeper of inflammatory gene expression. Trends Biochem Sci 34:324–331

    Article  PubMed  CAS  Google Scholar 

  • Nathan C (2006) Role of iNOS in human host defense. Science 312:1874–1875; author reply 1874–1875

    Google Scholar 

  • Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97:8841–8848

    Article  PubMed  CAS  Google Scholar 

  • North RJ (1974) T cell dependence of macrophage activation and mobilization during infection with M. tuberculosis. Infect Immun 10:66–71

    PubMed  CAS  Google Scholar 

  • Parkhill J, Dougan G, James KD et al (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848–852

    Article  PubMed  CAS  Google Scholar 

  • Peyron P, Bordier C, N’Diaye EN, Maridonneau-Parini I (2000) Nonopsonic phagocytosis of M. kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol-anchored proteins. J Immunol 165:5186–5191

    PubMed  CAS  Google Scholar 

  • Philips JA (2008) Mycobacterial manipulation of vacuolar sorting. Cell Microbiol 10:2408–2415

    Article  PubMed  CAS  Google Scholar 

  • Pieters J (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3:399–407

    Article  PubMed  CAS  Google Scholar 

  • Pieters J, Ploegh H (2003) Microbiology. Chemical warfare and mycobacterial defense. Science 302:1900–1902

    Article  PubMed  CAS  Google Scholar 

  • Ponting CP, Aravind L, Schultz J, Bork P, Koonin EV (1999) Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J Mol Biol 289:729–745

    Article  PubMed  CAS  Google Scholar 

  • Raoust E, Balloy V, Garcia-Verdugo I, Touqui L, Ramphal R, Chignard M (2009) Pseudomonas aeruginosa LPS or flagellin are sufficient to activate TLR-dependent signaling in murine alveolar macrophages and airway epithelial cells. PLoS One 4:e7259

    Article  PubMed  CAS  Google Scholar 

  • Reid DM, Gow NA, Brown GD (2009) Pattern recognition: recent insights from Dectin-1. Curr Opin Immunol 21:30–37

    Article  PubMed  CAS  Google Scholar 

  • Restrepo CI, Dong Q, Savov J, Mariencheck WI, Wright JR (1999) Surfactant protein D stimulates phagocytosis of Pseudomonas aeruginosa by alveolar macrophages. Am J Respir Cell Mol Biol 21:576–585

    Article  PubMed  CAS  Google Scholar 

  • Rohde K, Yates RM, Purdy GE, Russell DG (2007) Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 219:37–54

    Article  PubMed  CAS  Google Scholar 

  • Rosales-Reyes R, Alpuche-Aranda C, Ramirez-Aguilar Mde L, Castro-Eguiluz AD, Ortiz-Navarrete V (2005) Survival of Salmonella enterica serovar Typhimurium within late endosomal-lysosomal compartments of B lymphocytes is associated with the inability to use the vacuolar alternative major histocompatibility complex class I antigen-processing pathway. Infect Immun 73:3937–3944

    Article  PubMed  CAS  Google Scholar 

  • Roth MG (2004) Phosphoinositides in constitutive membrane traffic. Physiol Rev 84:699–730

    Article  PubMed  CAS  Google Scholar 

  • Rybakin V, Clemen CS (2005) Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. Bioessays 27:625–632

    Article  PubMed  CAS  Google Scholar 

  • Ryffel B, Jacobs M, Parida S, Botha T, Togbe D, Quesniaux V (2006) Toll-like receptors and control of mycobacterial infection in mice. Novartis Found Symp 279:127–139; discussion 139–141, 216–129

    Google Scholar 

  • Saiga H, Shimada Y, Takeda K (2011) Innate immune effectors in mycobacterial infection. Clin Dev Immunol 2011:347594

    PubMed  Google Scholar 

  • Saleh MT, Belisle JT (2000) Secretion of an acid phosphatase (SapM) by M. tuberculosis that is similar to eukaryotic acid phosphatases. J Bacteriol 182:6850–6853

    Article  PubMed  CAS  Google Scholar 

  • Schafer G, Jacobs M, Wilkinson RJ, Brown GD (2009) Non-opsonic recognition of M. tuberculosis by phagocytes. J Innate Immun 1:231–243

    Article  PubMed  CAS  Google Scholar 

  • Scherr N, Honnappa S, Kunz G, et al. (2007) Structural basis for the specific inhibition of protein kinase G, a virulence factor of M. tuberculosis. Proc Natl Acad Sci USA 104:12151–12156

    Article  PubMed  CAS  Google Scholar 

  • Scherr N, Jayachandran R, Mueller P, Pieters J (2009a) Interference of M. tuberculosis with macrophage responses. Indian J Exp Biol 47:401–406

    PubMed  CAS  Google Scholar 

  • Scherr N, Muller P, Perisa D, Combaluzier B, Jeno P, Pieters J (2009b) Survival of pathogenic mycobacteria in macrophages is mediated through autophosphorylation of protein kinase G. J Bacteriol 191:4546–4554

    Article  PubMed  CAS  Google Scholar 

  • Schorey JS, Carroll MC, Brown EJ (1997) A macrophage invasion mechanism of pathogenic mycobacteria. Science 277:1091–1093

    Article  PubMed  CAS  Google Scholar 

  • Shenoy AR, Wellington DA, Kumar P, Kassa H, Booth CJ, Cresswell P, MacMicking JD (2012) GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 336:481–485

    Article  PubMed  CAS  Google Scholar 

  • Shiloh MU, Nathan CF (2000) Reactive nitrogen intermediates and the pathogenesis of Salmonella and mycobacteria. Curr Opin Microbiol 3:35–42

    Article  PubMed  CAS  Google Scholar 

  • Shin DM, Jeon BY, Lee HM et al (2010) Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 6:e1001230

    Article  PubMed  CAS  Google Scholar 

  • Sibley LD, Hunter SW, Brennan PJ, Krahenbuhl JL (1988) Mycobacterial lipoarabinomannan inhibits gamma interferon-mediated activation of macrophages. Infect Immun 56:1232–1236

    PubMed  CAS  Google Scholar 

  • Sibley LD, Adams LB, Krahenbuhl JL (1990) Inhibition of interferon-gamma-mediated activation in mouse macrophages treated with lipoarabinomannan. Clin Exp Immunol 80:141–148

    PubMed  CAS  Google Scholar 

  • Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572

    Article  PubMed  CAS  Google Scholar 

  • Singh SB, Davis AS, Taylor GA, Deretic V (2006) Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313:1438–1441

    Article  PubMed  CAS  Google Scholar 

  • Smith J, Manoranjan J, Pan M et al (2008) Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in M. marinum escape from the vacuole. Infect Immun 76:5478–5487

    Article  PubMed  CAS  Google Scholar 

  • Soldati T, Neyrolles O (2012) Mycobacteria and the intraphagosomal environment: take it with a pinch of salt(s)! Traffic 13:1042–1052

    Google Scholar 

  • Steinberg BE, Grinstein S (2008) Pathogen destruction versus intracellular survival: the role of lipids as phagosomal fate determinants. J Clin Invest 118:2002–2011

    Article  PubMed  CAS  Google Scholar 

  • Sturgill-Koszycki S, Schlesinger PH, Chakraborty P et al (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678–681

    Article  PubMed  CAS  Google Scholar 

  • Tateda K, Ishii Y, Horikawa M et al (2003) The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun 71:5785–5793

    Article  PubMed  CAS  Google Scholar 

  • Taylor GA, Feng CG, Sher A (2004) p47 GTPases: regulators of immunity to intracellular pathogens. Nat Rev Immunol 4:100–109

    Article  PubMed  CAS  Google Scholar 

  • Thakur M, Chakraborti PK (2008) Ability of PknA, a mycobacterial eukaryotic-type serine/threonine kinase, to transphosphorylate MurD, a ligase involved in the process of peptidoglycan biosynthesis. Biochem J 415:27–33

    Article  PubMed  CAS  Google Scholar 

  • Thakur M, Chaba R, Mondal AK, Chakraborti PK (2008) Interdomain interaction reconstitutes the functionality of PknA, a eukaryotic type Ser/Thr kinase from M. tuberculosis. J Biol Chem 283:8023–8033

    Article  PubMed  CAS  Google Scholar 

  • Tilney LG, Portnoy DA (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109:1597–1608

    Article  PubMed  CAS  Google Scholar 

  • Torrelles JB, Azad AK, Schlesinger LS (2006) Fine discrimination in the recognition of individual species of phosphatidyl-myo-inositol mannosides from M. tuberculosis by C-type lectin pattern recognition receptors. J Immunol 177:1805–1816

    PubMed  CAS  Google Scholar 

  • Townsend SM, Kramer NE, Edwards R et al (2001) Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 69:2894–2901

    Article  PubMed  CAS  Google Scholar 

  • Tracy Tan WLLDCASGJL (2006) The ESAT-6/CFP-10 secretion system of <i> M. marinum </i> modulates phagosome maturation. Cellular Microbiology 8:1417–1429

    Article  CAS  Google Scholar 

  • Uematsu S, Akira S (2006) Innate immune recognition of viral infection. Uirusu 56:1–8

    Article  PubMed  CAS  Google Scholar 

  • van der Wel N, Hava D, Houben D et al (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:1287–1298

    Article  PubMed  CAS  Google Scholar 

  • Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V (2004) Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 15:751–760

    Article  PubMed  CAS  Google Scholar 

  • Vergne I, Chua J, Lee HH, Lucas M, Belisle J, Deretic V (2005) Mechanism of phagolysosome biogenesis block by viable M. tuberculosis. Proc Natl Acad Sci USA 102:4033–4038

    Article  PubMed  CAS  Google Scholar 

  • Vieira OV, Botelho RJ, Grinstein S (2002) Phagosome maturation: aging gracefully. Biochem J 366:689–704

    PubMed  CAS  Google Scholar 

  • Waddell SJ, Popper SJ, Rubins KH, Griffiths MJ, Brown PO, Levin M, Relman DA (2010) Dissecting interferon-induced transcriptional programs in human peripheral blood cells. PLoS One 5:e9753

    Article  PubMed  CAS  Google Scholar 

  • Wain J, Pham VB, Ha V, et al. (2001) Quantitation of bacteria in bone marrow from patients with typhoid fever: relationship between counts and clinical features. J Clin Microbiol 39:1571–1576

    Article  PubMed  CAS  Google Scholar 

  • Walburger A, Koul A, Ferrari G et al (2004) Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304:1800–1804

    Article  PubMed  CAS  Google Scholar 

  • Warner DF, Mizrahi V (2007) The survival kit of M. tuberculosis. Nat Med 13:282–284

    Article  PubMed  CAS  Google Scholar 

  • Wehenkel A, Bellinzoni M, Grana M et al (2008) Mycobacterial Ser/Thr protein kinases and phosphatases: physiological roles and therapeutic potential. Biochim Biophys Acta 1784:193–202

    Article  PubMed  CAS  Google Scholar 

  • Wei J, Dahl JL, Moulder JW, Roberts EA, O’Gaora P, Young DB, Friedman RL (2000) Identification of a M. tuberculosis gene that enhances mycobacterial survival in macrophages. J Bacteriol 182:377–384

    Article  PubMed  CAS  Google Scholar 

  • Welin A, Lerm M (2011) Inside or outside the phagosome? The controversy of the intracellular localization of M. tuberculosis. Tuberculosis (Edinb)

    Google Scholar 

  • Winslow MM, Neilson JR, Crabtree GR (2003) Calcium signalling in lymphocytes. Curr Opin Immunol 15:299–307

    Article  PubMed  CAS  Google Scholar 

  • Yadav M, Schorey JS (2006) The beta-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108:3168–3175

    Article  PubMed  CAS  Google Scholar 

  • Zheng PY, Jones NL (2003) Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell Microbiol 5:25–40

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Research in the laboratory of Jean Pieters is funded by the Swiss National Science Foundation and the Optimus Foundation. Somdeb BoseDasgupta is a recipient of an EMBO Long Term Fellowship and Rajesh Jayachandran is a Cloetta Medical Research fellow.

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Authors and Affiliations

  1. Biozentrum, University of Basel, Klingelbergstrasse 50/70, 4056, Basel, Switzerland

    Rajesh Jayachandran, Somdeb BoseDasgupta & Jean Pieters

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  1. Rajesh Jayachandran
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  2. Somdeb BoseDasgupta
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  3. Jean Pieters
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Correspondence to Jean Pieters .

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  1. Biozentrum, University of Basel, Basel, Switzerland

    Jean Pieters

  2. Laboratory of Microbiology and Microsystems, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, Switzerland

    John D. McKinney

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Jayachandran, R., BoseDasgupta, S., Pieters, J. (2012). Surviving the Macrophage: Tools and Tricks Employed by Mycobacterium tuberculosis . In: Pieters, J., McKinney, J. (eds) Pathogenesis of Mycobacterium tuberculosis and its Interaction with the Host Organism. Current Topics in Microbiology and Immunology, vol 374. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2012_273

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