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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Agranoff DD, Krishna S (1998) Metal ion homeostasis and intracellular parasitism. Mol Microbiol 28: 403–412
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
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
—, Racoosin EL, Swanson JA, Miller SI (1994)Salmonella stimulates macropinocytosis and persists within spacious phagosomes. J Exp Med 179: 601–608
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
—, Roberts R, Stahl PD (1997) InternalizedListeria monocytogenes modulates trafficking and delays maturation of the phagosome. J Cell Sci 110: 731–743
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
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
Antoine JC, Prina E, Jouanne C, Bongrand P (1990) Parasitophorous vacuoles ofLeishmania amazonensis-infected macrophages maintain an acidic pH. Infect Immun 58: 779–787
—, 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
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
Baca OG, Li YP, Kumar H (1994) Survival of the Q fever agentCoxiella burnetii in the phagolysosome. Trends Microbiol 2: 476–480
Barker LP, George KM, Falkow S, Small PLC (1997) Differential trafficking of live and deadMycobacterium marinum organisms in macrophages. Infect Immun 65: 1497–1504
Bäumler AJ, Kusters JG, Stojiljkovick I, Heffron F (1994)Salmonella typhimurium loci involved in survival within macrophages. Infect Immun 62: 1623–1630
Beron W, Alvarez-Dominguez C, Mayorga L, Stahl PD (1995) Membrane trafficking along the phagocytic pathway. Trends Cell Biol 5: 100–104
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
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
—, Griffiths G, Olivo JC, Hyman AA, Severin FF (1998) A role for microtubule dynamics in phagosome movement. J Cell Sci 111: 303–312
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
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
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
Buchmeier NA, Heffron F (1991) Inhibition of macrophage phagosome-lysosome fusion bySalmonella typhimurium. Infect Immun 59: 2232–2238
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
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
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
—, Belouchi A, Gros P (1996) Resistance to intracellular infections: comparative genomic analysis of Nramp. Trends Genet 12: 201–204
—, 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
Chang KP, Dwyer DM (1976) Multiplication of a human parasite (Leishmania donovani) in phagolysosomes of hamster macrophages in vitro. Science 193: 678–680
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
Clemens DL, Horwitz MA (1995) Characterization of theMycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257–270
— — (1996) TheMycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 184: 1349–1355
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
Cooper J, Walker RD (1998) Listeriosis. Vet Clin North Am Food Anim Pract 14: 113–125
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
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
—, 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
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
Deretic V, Via LE, Fratti RA, Deretic D (1997) Mycobacterial phagosome maturation, rab proteins, and intracellular trafficking. Electrophoresis 18: 2542–2547
Desjardins M (1995) Biogenesis of phagolysosomes: the kiss and run hypothesis. Trends Cell Biol 5: 183–186
—, Descoteaux A (1997) Inhibition of phagolysosomal biogenesis by theLeishmania lipophosphoglycan. J Exp Med 185: 2061–2068
—, 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
—, Celis JE, van Meer G, Dieplinger H, Jahraus A, Griffiths G, Huber LA (1994b) Molecular characterization of phagosomes. J Biol Chem 269: 32194–32200
—, 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
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
Dobrowolski JM, Sibley LD (1996)Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933–939
Dunn WA (1990a) Studies on the mechanism of autophagy: formation of the autophagic vacuole. J Cell Biol 110: 1923–1933
— (1990b) Studies on the mechanism of autophagy: maturation of the autophagic vacuole. J Cell Biol 110: 1935–1945
Ehlers MR, Daffe M (1998) Interactions betweenMycobacterium tuberculosis and host cells: are mycobacterial sugars the key? Trends Microbiol 6: 328–335
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
Feng Y, Press B, Wandinger-Ness A (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 31: 1435–1452
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
—, Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136–169
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
—, 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
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
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
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
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
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
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
Gordon AH, Hart PD, Young MR (1980) Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286: 79–80
Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) Rab5 controls early endosome fusion in vitro. Cell 64: 915–925
Gros P, Skamene E, Forget A (1981) Genetic control of natural resistance toMycobacterium bovis (BCG) in mice. J Immunol 127: 2417–2421
Gruenberg J, Maxfield FR (1995) Membrane transport in the endocytic pathway. Curr Opin Cell Biol 7: 552–563
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
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
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
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
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
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
Horwitz MA (1983a) The Legionnaires' disease bacterium (Legionella pneumophilia) inhibits phagosome lysosome fusion in human monocytes. J Exp Med 158: 2108–2126
— (1983b) Formation of a novel phagosome by Legionnaires' disease bacterium (Legionella pneumophilia) in human monocytes. J Exp Med 158: 1319–1331
— (1984) Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophilia) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36: 27–33
—, Maxfield FR (1984)Legionella pneumophilia inhibits acidification of its phagosome in human monocytes. J Cell Biol 99: 1936–1943
Ishibashi Y, Arai T (1990) Specific inhibition of phagosomelysosome fusion in murine macrophages mediated bySalmonella typhimurium infections. FEMS Microbiol Immunol 64: 3745–3752
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
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
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
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
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
Kirby JE, Isberg RR (1998) Legionnaires' disease: the pore macrophage and the legion of terror within. Trends Microbiol 6: 256–258
—, Vogel JP, Andrews HL, Isberg, RR (1998) Evidence for poreforming ability byLegionella pneumophilia. Mol Microbiol 27: 323–326
Kreutzer DL, Dreyfus LA, Robertson DC (1979) Interaction of polymorphonuclear leukocytes with smooth and rough strains ofBrucella abortus. Infect Immun 23: 737–742
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
— —, 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
—, 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
Leid RW, Suquet CM, Tanigoshi L (1989) Oxygen detoxifying enzymes in parasites: a review. Acta Leiden 57: 107–114
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
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
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
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
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
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
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
McNeely TB, Turco SJ (1990) Requirement of lipophosphoglycan for intracellular survival ofLeishmania donovani within human monocytes. J Immunol 144: 2745–2750
Menard R, Dehio C, Sansonetti PJ (1996) Bacterial entry into epithelial cells: the paradigm ofShigella. Trends Microbiol 4: 220–226
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
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
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
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
Morisaki JH, Heuser JE, Sibley LD (1995) Invasion ofToxoplasma gondii occurs by active penetration of the host cell. J Cell Sci 108: 2457–2464
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
Pacheco-Soares C, De Souza W (1998) Redistribution of parasite and host cell membrane components duringToxoplasma gondii invasion. Cell Struct Funct 23: 159–168
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
Pitt A, Mayorga LS, Stahl PD, Schwartz AL (1992a) Alterations in the protein composition of maturing phagosomes. J Clin Invest 90: 1978–1983
— —, Schwartz AL, Stahl PD (1992b) Transport of phagosomal components to an endosomal compartment. J Biol Chem 267: 126–132
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
— —, Sanguedolce V, Mege JL, Gorvel JP (1998a) VirulentBrucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387–2392
—, 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
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
Plant J, Glynn AA (1976) Genetics of resistance to infection withSalmonella typhimurium in mice. J Infect Dis 133: 72–78
Portnoy DA, Jacks PS, Hinrichs DJ (1988) Role of hemolysin for the intracellular growth ofListeria monocytogenes. J Exp Med 167: 1459–1471
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
—, Lang T, Glaichenhaus N, Antoine JC (1996) Presentation of the protective parasite antigen LACK byLeishmania-infected macrophages. J Immunol 156: 4318–4327
Pupkis MF, Tetley L, Coombs GH (1986)Leishmania mexicana: amastigote hydrolases in unusual lysosomes. Exp Parasitol 62: 29–39
Rabinovitch M, Veras PS (1996) Cohabitation ofLeishmania amazonensis andCoxiella burnetii. Trends Microbiol 4: 158–161
—, 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
Rathman M, Sjaastad MD, Falkow S (1996) Acidification of phagosomes containingSalmonella typhimurium in murine macrophages. Infect Immun 64: 2765–2773
—, 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
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
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
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
Roy CR, Isberg RI (1997) Topology ofLegionella pneumophilia DotA: an inner membrane protein required for replication in macrophages. Infect Immun 65: 571–578
—, 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
Russell DG, Xu S, Chakraborty P (1992) Intracellular trafficking and the parasitophorous vacuole ofLeishmania mexicana-infected macrophages. J Cell Sci 103: 1193–1210
—, 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
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
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
Segal G, Shuman HA (1998) How is the intracellular fate ofLegionella pneumophilia phagosome determined? Trends Microbiol 6: 253–255
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
Sibley LD, Weidner E, Krahenbuhl JL (1985) Phagosome acidification blocked by intracellularToxoplasma gondii. Nature 315: 416–419
Sinai AP, Joiner KA (1997) Safe haven: the cell biology of non-fusogenic pathogen vacuoles. Annu Rev Microbiol 51: 415–462
—, 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
Small PL, Ramakrishnan L, Falkow S (1994) Remodeling schemes of intracellular pathogens. Science 263: 637–639
Storrie B, Desjardins M (1996) The biogenesis of lysosomes: is it a kiss and run, continuous fusion and fission process? Bioessays 18: 895–903
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
—, 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
—, Haddix PL, Russell DG (1997) The interaction betweenMycobacterium and the macrophage analyzed by two-dimensional poly-acrylamide gel electrophoresis. Electrophoresis 18: 2558–2565
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
Swanson MS, Isberg RR (1995) Association ofLegionella pneumophilia with the macrophage endoplasmic reticulum. Infect Immun 63: 3609–3620
Theriot JA (1995) The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol 11: 213–239
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
Trotter PJ, Voelker DR (1994) Lipid transport processes in eukaryotic cells. Biochim Biophys Acta 1213: 241–262
Vance JE, Shiao YJ (1996) Intracellular trafficking of phospholipids: import of phosphatidylserine into mitochondria. Anticancer Res 16: 1333–1340
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
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
—, 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
Vogel JP, Andrew HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system ofLegionella pneumophilia. Science 279: 873–875
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
Author information
Authors and Affiliations
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01314950