Skip to main content
Log in

Survival of intracellular pathogens within macrophages

  • Focus on Cellular Biochemistry
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The threat caused by intracellular pathogens increases as conventional drag treatments are less and less effective against a wide range of microorganisms. Understanding the molecular mechanisms used by intracellular pathogens to avoid killing and degradation in their host cells is likely to point at new ways to threat infectious diseases. We discuss some of the strategies used by various microorganisms to avoid killing and degradation in phagolysosomes. Interestingly, it appears that microbes have a lot to teach us about the cell biology and molecular mechanisms of organelle sorting in macrophages.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agranoff DD, Krishna S (1998) Metal ion homeostasis and intracellular parasitism. Mol Microbiol 28: 403–412

    Google Scholar 

  • Alexander J, Vickerman K (1975) Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana-infected macrophages. J Protozool 22: 502–508

    Google Scholar 

  • Alpuche-Aranda CM, Swanson JA, Loomis WP, Miller SI (1992)Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc Natl Acad Sci USA 89: 10079–10083

    Google Scholar 

  • —, Racoosin EL, Swanson JA, Miller SI (1994)Salmonella stimulates macropinocytosis and persists within spacious phagosomes. J Exp Med 179: 601–608

    Google Scholar 

  • Alvarez-Dominguez C, Barbieri AM, Beron W, Wandinger-Ness A, Stahl PD (1996) Phagocytosed liveListeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J Biol Chem 271: 13834–13843

    Google Scholar 

  • —, Roberts R, Stahl PD (1997) InternalizedListeria monocytogenes modulates trafficking and delays maturation of the phagosome. J Cell Sci 110: 731–743

    Google Scholar 

  • Andrews HL, Vogel JP, Isberg RR (1998) Identification of linkedLegionella pneumophilia genes essential for intracellular growth and evasion of the endocytic pathway. Infect Immun 66: 950–958

    Google Scholar 

  • Aniento F, Gu F, Parton RG, Gruenberg J (1996) An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 133: 29–41

    Google Scholar 

  • Antoine JC, Prina E, Jouanne C, Bongrand P (1990) Parasitophorous vacuoles ofLeishmania amazonensis-infected macrophages maintain an acidic pH. Infect Immun 58: 779–787

    Google Scholar 

  • —, Jouanne C, Lang T, Prina E, de Chastellier C, Frehel C (1991) Localization of major histocompatibility complex class II molecules in phagolysosomes of murine macrophages infected withLeishmania amazonensis. Infect Immun 59: 764–775

    Google Scholar 

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

    Google Scholar 

  • Baca OG, Li YP, Kumar H (1994) Survival of the Q fever agentCoxiella burnetii in the phagolysosome. Trends Microbiol 2: 476–480

    Google Scholar 

  • Barker LP, George KM, Falkow S, Small PLC (1997) Differential trafficking of live and deadMycobacterium marinum organisms in macrophages. Infect Immun 65: 1497–1504

    Google Scholar 

  • Bäumler AJ, Kusters JG, Stojiljkovick I, Heffron F (1994)Salmonella typhimurium loci involved in survival within macrophages. Infect Immun 62: 1623–1630

    Google Scholar 

  • Beron W, Alvarez-Dominguez C, Mayorga L, Stahl PD (1995) Membrane trafficking along the phagocytic pathway. Trends Cell Biol 5: 100–104

    Google Scholar 

  • Biederbick A. Kern HF, Elsasser HP (1995) Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66: 3–14

    Google Scholar 

  • Blocker A, Severin FF, Burkhardt JK, Bingham JB, Yu H, Olivo JC, Schroer TA, Hyman AA, Griffiths G (1997) Molecular requirements for bi-directional movement of phagosomes along microtubules. J Cell Biol 137: 113–129

    Google Scholar 

  • —, Griffiths G, Olivo JC, Hyman AA, Severin FF (1998) A role for microtubule dynamics in phagosome movement. J Cell Sci 111: 303–312

    Google Scholar 

  • Boucher JC, Martinez-Salazar J, Schurr MJ, Mudd MH, Yu H, Derectic V (1996) Two distinct loci affecting conversion to mucoidy inPseudomonas aeruginosa in cystic fibrosis encode homologues of the serine protease HtrA. J Bacteriol 178: 511–523

    Google Scholar 

  • Bradley DJ (1977) Regulation ofLeishmania populations within the host II: genetic control of acute susceptibility of mice toLeishmania donovani infection. Clin Exp Immunol 30: 130–140

    Google Scholar 

  • Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715–718

    Google Scholar 

  • Buchmeier NA, Heffron F (1991) Inhibition of macrophage phagosome-lysosome fusion bySalmonella typhimurium. Infect Immun 59: 2232–2238

    Google Scholar 

  • Burkhardt J, Huber LA, Dieplinger H, Blocker A, Griffiths G, Desjardins M (1995) Gaining insight into a complex organelle, the phagosome, using two-dimensional gel electrophoresis. Electrophoresis 16: 2249–2257

    Google Scholar 

  • Burton PR, Stueckemann J, Welsh RM, Paretsky D (1978) Some ultrastructural effects of persistent infections by therickettsia Coxiella burnetii in mouse L cells and green monkey kidney (Vero) cells. Infect Immun 21: 556–566

    Google Scholar 

  • Cellier M, Prive G, Belouchi A, Kwan T, Rodrigues V, Chia W, Gros P (1995) Nramp defines a family of membrane proteins. Proc Natl Acad Sci USA 92: 10089–10093

    Google Scholar 

  • —, Belouchi A, Gros P (1996) Resistance to intracellular infections: comparative genomic analysis of Nramp. Trends Genet 12: 201–204

    Google Scholar 

  • —, Shustik C, Dalton W, Rich E, Hu J, Malo D, Schurr E, Gros P (1997) Expression of the human NRAMP1 gene in professional primary phagocytes: studies in blood cells and in HL-60 promyelocytic leukemia. J Leukoc Biol 61: 96–105

    Google Scholar 

  • Chang KP, Dwyer DM (1976) Multiplication of a human parasite (Leishmania donovani) in phagolysosomes of hamster macrophages in vitro. Science 193: 678–680

    Google Scholar 

  • Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62: 317–329

    Google Scholar 

  • Clemens DL, Horwitz MA (1995) Characterization of theMycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257–270

    Google Scholar 

  • — — (1996) TheMycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 184: 1349–1355

    Google Scholar 

  • Clerc PL, Ryter A, Mounier J, Sansonetti PJ (1987) Plasmid-mediated early killing of eukaryotic cells byShigella flexneri as studied by infection of J774 macrophages. Infect Immun 55: 521–527

    Google Scholar 

  • Cooper J, Walker RD (1998) Listeriosis. Vet Clin North Am Food Anim Pract 14: 113–125

    Google Scholar 

  • de Carvahlo L, de Souza W (1989) Cytochemical localization of plasma membrane enzyme markers during internalization of tachyzoites ofToxoplasma gondii by macrophages. J Protozool 36: 164–170

    Google Scholar 

  • de Chastellier C, Frehel C, Offredo C, Skamene E (1993) Implication of phagosome-lysosome fusion in restriction ofMycobacterium avium growth in bone marrow macrophages from genetically resistant mice. Infect Immun 61: 3775–3784

    Google Scholar 

  • —, Lang T, Thilo L (1995) Phagocytic processing of the macrophage endoparasite,Mycobacterium avium, in comparison to phagosomes which containBacillus subtilis or latex beads. Eur J Cell Biol 68: 167–182

    Google Scholar 

  • Denis M (1991) Interferon-gamma-treated murine macrophages inhibit growth of tubercle bacilli via the generation of reactive nitrogen intermediates. Cell Immunol 132: 150–157

    Google Scholar 

  • Deretic V, Via LE, Fratti RA, Deretic D (1997) Mycobacterial phagosome maturation, rab proteins, and intracellular trafficking. Electrophoresis 18: 2542–2547

    Google Scholar 

  • Desjardins M (1995) Biogenesis of phagolysosomes: the kiss and run hypothesis. Trends Cell Biol 5: 183–186

    Google Scholar 

  • —, Descoteaux A (1997) Inhibition of phagolysosomal biogenesis by theLeishmania lipophosphoglycan. J Exp Med 185: 2061–2068

    Google Scholar 

  • —, Huber LA, Parton RG, Griffiths G (1994a) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124: 677–688

    Google Scholar 

  • —, Celis JE, van Meer G, Dieplinger H, Jahraus A, Griffiths G, Huber LA (1994b) Molecular characterization of phagosomes. J Biol Chem 269: 32194–32200

    Google Scholar 

  • —, Nzala NN, Corsini R, Rondeau C (1997) Maturation of phagosomes is accompanied by changes in their fusion properties and size-selective acquisition of solute materials from endosomes. J Cell Sci 110: 2303–2314

    Google Scholar 

  • De Souza Leao S, Lang T, Prina E, Hellio R, Antoine JC (1995) IntracellularLeishmania amazonensis amastigotes internalize and degrade MHC class II molecules of their host cells. J Cell Sci 108: 3219–3231

    Google Scholar 

  • Dobrowolski JM, Sibley LD (1996)Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933–939

    Google Scholar 

  • Dunn WA (1990a) Studies on the mechanism of autophagy: formation of the autophagic vacuole. J Cell Biol 110: 1923–1933

    Google Scholar 

  • — (1990b) Studies on the mechanism of autophagy: maturation of the autophagic vacuole. J Cell Biol 110: 1935–1945

    Google Scholar 

  • Ehlers MR, Daffe M (1998) Interactions betweenMycobacterium tuberculosis and host cells: are mycobacterial sugars the key? Trends Microbiol 6: 328–335

    Google Scholar 

  • Elzer PH, Phillips RW, Roberston GT, Roop RM II (1996) The Htr A stress response contributes to resistance ofBrucella abortus to killing by murine phagocytes. Infect Immun 64: 4838–4841

    Google Scholar 

  • Feng Y, Press B, Wandinger-Ness A (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 31: 1435–1452

    Google Scholar 

  • Finlay BB (1994) Cell biology ofSalmonella pathogenesis. In: Miller VL, Kaper JB, Portnoy DA, Isberg RR (eds) Molecular genetics of bacterial pathogenesis. American Society for Microbiology, Washington, DC, pp 249–261

    Google Scholar 

  • —, Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136–169

    Google Scholar 

  • Fleming MD, Trenor CC III, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC (1997) Microcytic anemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16: 383–386

    Google Scholar 

  • —, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC (1998) Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc Natl Acad Sci USA 95: 1148–1153

    Google Scholar 

  • Flesch IEA, Kaufman SHE (1987) Mycobacterial growth inhibition by interferon-gamma-activated bone marrow macrophages and differential susceptibility among strains ofMycobacterium tuberculosis. J Immunol 138: 4408–4413

    Google Scholar 

  • Flohe S, Lang T, Moll H (1997) Synthesis, stability, and subcellular distribution of major histocompatibility complex class II molecules in Langerhans cells infected withLeishmania major. Infect Immun 65: 3444–3450

    Google Scholar 

  • Gaillard JL, Berche P, Mounier J, Richard S, Sansonetti P (1987) In vitro model of penetration and intracellular growth ofListeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun 55: 2822–2829

    Google Scholar 

  • Garcia-del Portillo F, Finlay BB (1995) Targeting ofSalmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 129: 81–97

    Google Scholar 

  • Geoffroy C, Gaillard JL, Aloug JE, Berche P (1987) Purification, characterization and toxicity of the sulfhydryl-activated hemolysin listeriolysin O fromListeria monocytogenes. Infect Immun 55: 1641–1646

    Google Scholar 

  • Germain RN (1995) The biochemistry and cell biology of antigen presentation by MHC class I and class II molecules: implications for development of combination vaccines. Ann N Y Acad Sci 754: 114–125

    Google Scholar 

  • Gordon AH, Hart PD, Young MR (1980) Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286: 79–80

    Google Scholar 

  • Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) Rab5 controls early endosome fusion in vitro. Cell 64: 915–925

    Google Scholar 

  • Gros P, Skamene E, Forget A (1981) Genetic control of natural resistance toMycobacterium bovis (BCG) in mice. J Immunol 127: 2417–2421

    Google Scholar 

  • Gruenberg J, Maxfield FR (1995) Membrane transport in the endocytic pathway. Curr Opin Cell Biol 7: 552–563

    Google Scholar 

  • Gruenheid S, Pinner E, Desjardins M, Gros P (1997) Natural resistance to infection with intracellular pathogens: the Nrampl protein is recruited to the membrane of the phagosome. J Exp Med 185: 717–730

    Google Scholar 

  • Harding CV, Song R, Griffin J, France J, Wick MJ, Pfeifer JD, Geuze HJ (1995) Processing of bacterial antigens for presentation to class I and II MHC-restricted T lymphocytes. Infect Agents Dis 4: 1–12

    Google Scholar 

  • Hart PD, Young MR, Jordan MM, Perkins WJ, Geisow MJ (1983) Chemical inhibitors of phagosome-lysosome fusion in cultured macrophages also inhibit saltatory lysosomal movements: a combined microscopic and computer study. J Exp Med 158: 477–492

    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

    Google Scholar 

  • Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T (1996) Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles ofCoxiella burnetii andChlamydia trachomatis. Infect Immun 64: 796–809

    Google Scholar 

  • High N, Mounier J, Prévost MC, Sansonetti PJ (1992) IpaB ofShigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J 11: 1991–1999

    Google Scholar 

  • Horwitz MA (1983a) The Legionnaires' disease bacterium (Legionella pneumophilia) inhibits phagosome lysosome fusion in human monocytes. J Exp Med 158: 2108–2126

    Google Scholar 

  • — (1983b) Formation of a novel phagosome by Legionnaires' disease bacterium (Legionella pneumophilia) in human monocytes. J Exp Med 158: 1319–1331

    Google Scholar 

  • — (1984) Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophilia) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36: 27–33

    Google Scholar 

  • —, Maxfield FR (1984)Legionella pneumophilia inhibits acidification of its phagosome in human monocytes. J Cell Biol 99: 1936–1943

    Google Scholar 

  • Ishibashi Y, Arai T (1990) Specific inhibition of phagosomelysosome fusion in murine macrophages mediated bySalmonella typhimurium infections. FEMS Microbiol Immunol 64: 3745–3752

    Google Scholar 

  • Jahraus A, Storrie B, Griffiths G, Desjardins M (1994) Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment. J Cell Sci 107: 145–157

    Google Scholar 

  • Johnson K, Charles I, Dougan G, Pickard D, O'Gaora P, Costa G, Ali T, Miller I, Hormaeche C (1991) The role of a stress-response protein inSalmonella typhimurium virulence. Mol Microbiol 5: 401–407

    Google Scholar 

  • Joiner KA (1992) The parasitophorous vacuole membrane surroundingToxoplasma gondii: a specialized interface between parasite and cell. In: Smith JL (ed) Toxoplasmosis. Springer, Berlin Heidelberg New York Tokyo, pp 73–81

    Google Scholar 

  • Joiner KA, Furhman SA, Miettinnen H, Kasper LL, Mellman I (1990)Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249: 641–646

    Google Scholar 

  • Jones TC, Hirsch JG (1972) The interaction betweenToxoplasma gondii and mammalians cells I: mechanism of entry and intracellular fate of the parasite. J Exp Med 136: 1157–1172

    Google Scholar 

  • Kirby JE, Isberg RR (1998) Legionnaires' disease: the pore macrophage and the legion of terror within. Trends Microbiol 6: 256–258

    Google Scholar 

  • —, Vogel JP, Andrews HL, Isberg, RR (1998) Evidence for poreforming ability byLegionella pneumophilia. Mol Microbiol 27: 323–326

    Google Scholar 

  • Kreutzer DL, Dreyfus LA, Robertson DC (1979) Interaction of polymorphonuclear leukocytes with smooth and rough strains ofBrucella abortus. Infect Immun 23: 737–742

    Google Scholar 

  • Lang T, de Chastellier C, Ryter A, Thilo L (1988) Endocytic membrane traffic with respect to phagosomes in macrophages infected with non-pathogenic bacteria: phagosomal membrane acquires the same composition as lysosomal membrane. Eur J Cell Biol 46: 39–50

    Google Scholar 

  • — —, Frehel C, Hellio R, Metezeau P, de Souza Leao S, Antoine JC (1994a) Distribution of MHC class I and of MHC class II molecules in macrophages infected withLeishmania amazonensis. J Cell Sci 107: 69–82

    Google Scholar 

  • —, Hellio R, Kaye PM, Antoine JC (1994b)Leishmania donovani-infected macrophages: characterization of the parasitophorous vacuole and potential role of this organelle in antigen presentation. J Cell Sci 107: 2137–2150

    Google Scholar 

  • Leid RW, Suquet CM, Tanigoshi L (1989) Oxygen detoxifying enzymes in parasites: a review. Acta Leiden 57: 107–114

    Google Scholar 

  • Leimeister-Wacher M, Domann E, Chakraborty T (1991) Detection of a gene encoding a phosphatidylinositol-specific phospholipase C that is co-ordinately expressed with listeriolysin inListeria monocytogenes. Mol Microbiol 5: 361–366

    Google Scholar 

  • Li SR, Dorrel N, Everest PH, Dougan G, Wren BW (1996) Construction and characterization of a Yersinia enterocolita O:8 high-temperature requirement A (HtrA) isogenic mutant. Infect Immun 64: 2088–2094

    Google Scholar 

  • Li YP, Curley G, Lopez M. Chavez M, Glew R, Aragon A, Kumar H, Baca OG (1996) Protein-tyrosine phosphatase activity ofCoxiella burnetii that inhibits human neutrophils. Acta Virol 40: 263–272

    Google Scholar 

  • Martinez de Tejada G, Pizzaro-Cerdá J, Moreno E, Moriyon I (1995) The outer membranes ofBrucella spp. are resistant to bactericidal cationic peptides. Infect Immun 63: 3054–3061

    Google Scholar 

  • Maurin M, Benoliel AM, Bongrand P, Raoult D (1992) Phagolysosomes ofCoxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect Immun 60: 5013–5016

    Google Scholar 

  • Mayorga LS, Bertini F, Stahl PD (1991) Fusion of newly formed phagosomes with endosomes in intact cells and in a cell-free system. J Biol Chem 266: 6511–6517

    Google Scholar 

  • McDade JE, Shepard CC, Fraser DW, Tsai TR, Redus MA, Dowdle WR (1977) Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297: 1197–1203

    Google Scholar 

  • McNeely TB, Turco SJ (1990) Requirement of lipophosphoglycan for intracellular survival ofLeishmania donovani within human monocytes. J Immunol 144: 2745–2750

    Google Scholar 

  • Menard R, Dehio C, Sansonetti PJ (1996) Bacterial entry into epithelial cells: the paradigm ofShigella. Trends Microbiol 4: 220–226

    Google Scholar 

  • Mengaud J, Braun-Breton C, Cossart P (1991) Identification of phosphatidylinositol-specific phospholipase C activity inListeria monocytogenes, a novel type of virulence factor? Mol Microbiol 5: 367–372

    Google Scholar 

  • Méresse S, Gorvel JP, Chavrier P (1995) The GTPase rab7 is involved in the transport between late endosomes and lysosomes. J Cell Sci 108: 3340–3358

    Google Scholar 

  • Miao L, Stafford A, Nir S, Turco SJ, Flanagan TD, Epand RM (1995) Potent inhibition of viral fusion by the lipophosphoglycan ofLeishmania donovani. Biochemistry 34: 4676–4683

    Google Scholar 

  • Mordue DG, Sibley LD (1997) Intracellular fate of vacuoles containingToxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J Immunol 159: 4452–4459

    Google Scholar 

  • Morisaki JH, Heuser JE, Sibley LD (1995) Invasion ofToxoplasma gondii occurs by active penetration of the host cell. J Cell Sci 108: 2457–2464

    Google Scholar 

  • Oh YK, Alpuche-Aranda C, Berthiaume E, Jinks T, Miller SI, Swanson J (1996) Rapid and complete fusion of macrophage lysosomes with phagosomes containingSalmonella typhimurium. Infect Immun 64: 3877–3833

    Google Scholar 

  • Pacheco-Soares C, De Souza W (1998) Redistribution of parasite and host cell membrane components duringToxoplasma gondii invasion. Cell Struct Funct 23: 159–168

    Google Scholar 

  • Pimenta PF, Saraiva EM, Sacks DL (1991) The comparative fine structure and surface glycoconjugate expression of three life stages ofLeishmania major. Exp Parasitol 72: 191–204

    Google Scholar 

  • Pitt A, Mayorga LS, Stahl PD, Schwartz AL (1992a) Alterations in the protein composition of maturing phagosomes. J Clin Invest 90: 1978–1983

    Google Scholar 

  • — —, Schwartz AL, Stahl PD (1992b) Transport of phagosomal components to an endosomal compartment. J Biol Chem 267: 126–132

    Google Scholar 

  • Pizarro-Cerdá J, Moreno E, Desjardins M, Gorvel JP (1997) When intracellular pathogens invade the frontiers of cell biology and immunology. Histol Histopathol 12: 1027–1038

    Google Scholar 

  • — —, Sanguedolce V, Mege JL, Gorvel JP (1998a) VirulentBrucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387–2392

    Google Scholar 

  • —, Méresse S, Parton RG, van der Goot FG, Sola-Landa A, Lopez-Goni I, Moreno E, Gorvel JP (1998b)Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of non-professional phagocytes. Infect Immun 66: 5711–5724

    Google Scholar 

  • Pizon V, Desjardins M, Bucci C, Parton RG, Zerial M (1994) Association of Rap1a and Rap1b proteins with late endocytic/phagocytic compartments and Rap2a with the Golgi complex. J Cell Sci 107: 1661–1670

    Google Scholar 

  • Plant J, Glynn AA (1976) Genetics of resistance to infection withSalmonella typhimurium in mice. J Infect Dis 133: 72–78

    Google Scholar 

  • Portnoy DA, Jacks PS, Hinrichs DJ (1988) Role of hemolysin for the intracellular growth ofListeria monocytogenes. J Exp Med 167: 1459–1471

    Google Scholar 

  • Prina E, Antoine JC, Wiederanders B, Kirschke H (1990) Localization and activity of various lysosomal proteases inLeishmania amazonensis-infected macrophages. Infect Immun 58: 1730–1737

    Google Scholar 

  • —, Lang T, Glaichenhaus N, Antoine JC (1996) Presentation of the protective parasite antigen LACK byLeishmania-infected macrophages. J Immunol 156: 4318–4327

    Google Scholar 

  • Pupkis MF, Tetley L, Coombs GH (1986)Leishmania mexicana: amastigote hydrolases in unusual lysosomes. Exp Parasitol 62: 29–39

    Google Scholar 

  • Rabinovitch M, Veras PS (1996) Cohabitation ofLeishmania amazonensis andCoxiella burnetii. Trends Microbiol 4: 158–161

    Google Scholar 

  • —, Topper G, Cristello P, Rich A (1985) Receptor-mediated entry of peroxidases into the parasitophorous vacuoles of macrophages infected withLeishmania mexicana amazonensis. J Leukoc Biol 37: 247–261

    Google Scholar 

  • Rathman M, Sjaastad MD, Falkow S (1996) Acidification of phagosomes containingSalmonella typhimurium in murine macrophages. Infect Immun 64: 2765–2773

    Google Scholar 

  • —, Barker LP, Falkow S (1997) The unique trafficking pattern ofSalmonella typhimurium-containing phagosomes in murine macrophages is independent of the mechanism of bacterial entry. Infect Immun 65: 1475–1485

    Google Scholar 

  • Riley N, Robertson DC (1984) Brucellacidal activity of human and bovine polymorphonuclear leukocytes granule extracts against smooth and rough strains ofBrucella abortus. Infect Immun 46: 231–236

    Google Scholar 

  • Rittig MG, Schroppel K, Seack KH, Sander U, N'Diaye EN, Maridonneau-Parini I, Solbach W, Bogdan C (1998) Coiling phagocytosis of trypanosomatids and fungal cells. Infect Immun 66: 4331–4339

    Google Scholar 

  • Rook GAW, Steele J, Ainsworth M, Champion BR (1986) Activation of macrophages to inhibit proliferation ofMycobacterium tuberculosis: comparison of the effect of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages. Immunology 59: 333–338

    Google Scholar 

  • Roy CR, Isberg RI (1997) Topology ofLegionella pneumophilia DotA: an inner membrane protein required for replication in macrophages. Infect Immun 65: 571–578

    Google Scholar 

  • —, Berger KH, Isberg RR (1998)Legionella pneumophilia DotA is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28: 663–674

    Google Scholar 

  • Russell DG, Xu S, Chakraborty P (1992) Intracellular trafficking and the parasitophorous vacuole ofLeishmania mexicana-infected macrophages. J Cell Sci 103: 1193–1210

    Google Scholar 

  • —, Dant J, Sturgill-Koszycki S (1996)Mycobacterium avium- andMycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from host cell plasmalemma. J Immunol 156: 4764–4773

    Google Scholar 

  • Schaible UE, Sturgill-Koszycki S, Schlesinger PH, Russell DG (1998) Cytokine activation leads to acidification and increases maturation ofMycobacterium avium-containing phagosomes in murine macrophages. J Immunol 160: 1290–1296

    Google Scholar 

  • Scianimanico S, Pasquali C, Lavoie J, Huber LA, Gorvel JP, Desjardins M (1997) Two-dimensional gel electrophoresis analysis of endovacuolar organelles. Electrophoresis 18: 2566–2572

    Google Scholar 

  • Segal G, Shuman HA (1998) How is the intracellular fate ofLegionella pneumophilia phagosome determined? Trends Microbiol 6: 253–255

    Google Scholar 

  • Shepherd VL, Stahl PD, Bernd P, Rabinovitch M (1983) Receptor-mediated entry of beta-glucuronidase into the parasitophorous vacuoles of macrophages infected withLeishmania mexicana amazonensis. J Exp Med 157: 1471–1482

    Google Scholar 

  • Sibley LD, Weidner E, Krahenbuhl JL (1985) Phagosome acidification blocked by intracellularToxoplasma gondii. Nature 315: 416–419

    Google Scholar 

  • Sinai AP, Joiner KA (1997) Safe haven: the cell biology of non-fusogenic pathogen vacuoles. Annu Rev Microbiol 51: 415–462

    Google Scholar 

  • —, Webster P, Joiner KA (1997) Association of host cell endoplasmic reticulum and mitochondria withToxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 110: 2117–2128

    Google Scholar 

  • Small PL, Ramakrishnan L, Falkow S (1994) Remodeling schemes of intracellular pathogens. Science 263: 637–639

    Google Scholar 

  • Storrie B, Desjardins M (1996) The biogenesis of lysosomes: is it a kiss and run, continuous fusion and fission process? Bioessays 18: 895–903

    Google Scholar 

  • Sturgill-Koszycki S, Schlesinger PD, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG (1994) Lack of acidification inMycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263: 678–681

    Google Scholar 

  • —, Schaible UE, Russell DG (1996)Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 15: 6960–6968

    Google Scholar 

  • —, Haddix PL, Russell DG (1997) The interaction betweenMycobacterium and the macrophage analyzed by two-dimensional poly-acrylamide gel electrophoresis. Electrophoresis 18: 2558–2565

    Google Scholar 

  • Supek F, Supekova L, Nelson H, Nelson N (1996) A yeast manganese transporter related to the macrophage protein involved in conferring resistance toMycobacteria. Proc Natl Acad Sci USA 93: 5105–5110

    Google Scholar 

  • Swanson MS, Isberg RR (1995) Association ofLegionella pneumophilia with the macrophage endoplasmic reticulum. Infect Immun 63: 3609–3620

    Google Scholar 

  • Theriot JA (1995) The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol 11: 213–239

    Google Scholar 

  • Tolson DL, Turco SJ, Pearson TW (1990) Expression of a repeating phosphorylated disaccharide lipophosphoglycan epitope on the surface of macrophages infected withLeishmania donovani. Infect Immun 58: 3500–3507

    Google Scholar 

  • Trotter PJ, Voelker DR (1994) Lipid transport processes in eukaryotic cells. Biochim Biophys Acta 1213: 241–262

    Google Scholar 

  • Vance JE, Shiao YJ (1996) Intracellular trafficking of phospholipids: import of phosphatidylserine into mitochondria. Anticancer Res 16: 1333–1340

    Google Scholar 

  • Vasquez-Boland JA, Kocks C, Dramsi S, Ohayon H, Geoffroy C, Mengaud J, Cossart P (1992) Nucleotide sequence of the lecithinase operon ofListeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect Immun 60: 219–230

    Google Scholar 

  • Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA, Deretic V (1997) Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 272: 13326–13331

    Google Scholar 

  • —, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D, Deretic V (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111: 897–905

    Google Scholar 

  • Vogel JP, Andrew HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system ofLegionella pneumophilia. Science 279: 873–875

    Google Scholar 

  • Xu S, Cooper A, Sturgill-Koszycki S, van Heyningen T, Chatterjee D, Orme I, Allen P, Russell DG (1994) Intracellular trafficking inMycobacterium tuberculosis andMycobacterium avium-infected macrophages. J Immunol 153: 2568–2578

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dermine, J.F., Desjardins, M. Survival of intracellular pathogens within macrophages. Protoplasma 210, 11–24 (1999). https://doi.org/10.1007/BF01314950

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01314950

Keywords

Navigation