The Journal of Membrane Biology

, Volume 193, Issue 3, pp 137–152

Phagosome Maturation: A Few Bugs in the System

Article

Abstract

Cells of the innate immune system ingest and destroy invading microorganisms by initially engulfing them into a specialized vacuole, known as the phagosome. The membrane of the forming phagosome is similar to the plasmalemma and its contents resemble the extracellular milieu. As such, the nascent phagosome is not competent to kill and eliminate the ingested microorganisms. However, shortly after sealing, the phagosome undergoes a series of rapid and extensive changes in its composition, the result of a sophisticated sequence of membrane fusion and fission reactions. Understanding the molecular basis of these events is of particular importance, since they are often the target of disruption by intracellular parasites such as Mycobacterium, Salmonella and Legionella. The objective of this review is to summarize the current knowledge of the molecular mechanisms underlying phagosomal maturation and its subversion by parasitic microorganisms.

Keywords

Phagosome Macrophage Rab SNARE Phosphoinositides Salmonella Mycobacterium 

References

  1. 1.
    Adam, T. 2001Exploitation of host factors for efficient infection by Shigella.Int. J. Med. Microbiol.291287298Google Scholar
  2. 2.
    Aderem, A. 2002How to eat something bigger than your head.Cell11058Google Scholar
  3. 3.
    Aderem, A., Underhill, D.M. 1999Mechanisms of phagocytosis in macrophages.Annu. Rev. Immunol.17593623CrossRefGoogle Scholar
  4. 4.
    Allaoui, A., Mounier, J., Prevost, M.C., Sansonetti, P.J., Parsot, C. 1992icsB: a Shigellaflexneri virulence gene necessary for the lysis of protrusions during intercellular spread.Mol. Microbiol.616051616Google Scholar
  5. 5.
    Allen, L.A., Aderem, A. 1996Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages.J. Exp. Med.184627637Google Scholar
  6. 6.
    Allen, L.A., Yang, C., Pessin, J.E. 2002Rate and extent of phagocytosis in macrophages lacking vamp3.J. Leukoc. Biol.72217221Google Scholar
  7. 7.
    Alvarez-Dominguez, C., Barbieri, A.M., Beron, W., Wandinger-Ness, A., Stahl, P.D. 1996Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion.J. Biol. Chem.2711383413843CrossRefGoogle Scholar
  8. 8.
    Andrews, N.W. 1993Living dangerously: how Trypanosoma cruzi uses lysosomes to get inside host cells, and then escapes into the cytoplasm.Biol. Res.266567Google Scholar
  9. 9.
    Antonin, W., Holroyd, C., Fasshauer, D., Pabst, S., Von Mollard, G.F., Jahn, R. 2000A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function.Embo. J.1964536464CrossRefGoogle Scholar
  10. 10.
    Armstrong, J.A., Hart, P.D. 1975Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival.J. Exp. Med.142116MATHGoogle Scholar
  11. 11.
    Astarie-Dequeker, C., Carreno, S., Cougoule, C., Maridonneau-Parini, I. 2002The protein tyrosine kinase Hck is located on lysosomal vesicles that are physically and functionally distinct from CD63-positive lysosomes in human macrophages.J. Cell. Sci.1158189Google Scholar
  12. 12.
    Astarie-Dequeker, C., N’Diaye, E.N., Le Cabec, V., Rittig, M.G., Prandi, J., Maridonneau-Parini, I. 1999The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages.Infect. Immun.67469477Google Scholar
  13. 13.
    Bangs, P., Franc, N., White, K. 2000Molecular mechanisms of cell death and phagocytosis in Drosophila.Cell Death Differ.710271034CrossRefGoogle Scholar
  14. 14.
    Beron, W., Alvarez-Dominguez, C., Mayorga, L., Stahl, P.D. 1995Membrane trafficking along the phagocytic pathway.Trends Cell Biol.5100104CrossRefGoogle Scholar
  15. 15.
    Beuzon, C.R., Meresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S.R., Ryder, T.A., Boucrot, E., Holden, D.W. 2000Salmonella maintains the integrity of its intracellular vacuole through the action of SifA.Embo J.1932353249CrossRefGoogle Scholar
  16. 16.
    Beuzon, C.R., Salcedo, S.P., Holden, D.W. 2002Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines.Microbiology14827052715Google Scholar
  17. 17.
    Botelho, R.J., Hackam, D.J., Schreiber, A.D., Grinstein, S. 2000Role of COPI in phagosome maturation.J. Biol. Chem.2751571715727CrossRefGoogle Scholar
  18. 18.
    Brumell, J.H., Goosney, D.L., Finlay, B.B. 2002aSifA, a Type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules.Traffic3407415Google Scholar
  19. 19.
    Brumell, J.H., Rosenberger, C.M., Gotto, G.T., Marcus, S.L., Finlay, B.B. 2001aSifA permits survival and replication of Salmonella typhimurium in murine macrophages.Cell Microbiol.37584Google Scholar
  20. 20.
    Brumell, J.H., Tang, P., Mills, S.D., Finlay, B.B. 2001bCharacterization of Salmonella-induced filaments (Sifs) reveals a delayed interaction between Salmonella-containing vacuoles and late endocytic compartments.Traffic2643653Google Scholar
  21. 21.
    Brumell, J.H., Tang, P., Zaharik, M.L., Finlay, B.B. 2002bDisruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovartyphimurium in the cytosol of epithelial cells.Infect. Immun.7032643270Google Scholar
  22. 22.
    Bucci, C., Parton, R.G., Mather, I.H., Stunnenberg, H., Simons, K., Hoflack, B., Zerial, M. 1992The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway.Cell70715728Google Scholar
  23. 23.
    Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., van Deurs, B. 2000Rab7: a key to lysosome biogenesis.Mol. Biol. Cell11467480Google Scholar
  24. 24.
    Burd, C.G., Emr, S.D. 1998Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains.Mol. Cell2157162Google Scholar
  25. 25.
    Callaghan, J., Simonsen, A., Gaullier, J.M., Toh, B.H., Stenmark, H. 1999The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer.Biochem. J.338539543CrossRefGoogle Scholar
  26. 26.
    Camilli, A., Tilney, L.G., Portnoy, D.A. 1993Dual roles of plcA in Listeria monocytogenes pathogenesis.Mol. Microbiol.8143157Google Scholar
  27. 27.
    Cantalupo, G., Alifano, P., Roberti, V., Bruni, C.B., Bucci, C. 2001Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes.Embo J.20683693CrossRefGoogle Scholar
  28. 28.
    Cardelli, J. 2001Phagocytosis and macropinocytosis in dictyostelium: phosphoinositide-based processes, biochemically distinct.Traffic2311320CrossRefGoogle Scholar
  29. 29.
    Carruthers, V.B. 2002Host cell invasion by the opportunistic pathogen Toxoplasma gondii.Acta Trop.81111122CrossRefGoogle Scholar
  30. 30.
    Catron, D.M., Sylvester, M.D., Lange, Y., Kadekoppala, M., Jones, B.D., Monack, D.M., Falkow, S., Haldar, K. 2002The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55.Cell Microbiol.4315328CrossRefGoogle Scholar
  31. 31.
    Christoforidis, S., McBride, H.M., Burgoyne, R.D., Zerial, M. 1999aThe Rab5 effector EEA1 is a core component of endosome docking.Nature397621625Google Scholar
  32. 32.
    Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S.C., Waterfield, M.D., Backer, J.M., Zerial, M. 1999bPhosphatidylinositol-3-OH kinases are Rab5 effectors.Nat. Cell Biol.1249252Google Scholar
  33. 33.
    Cirillo, D.M., Valdivia, R.H., Monack, D.M., Falkow, S. 1998Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival.Mol. Microbiol.30175188CrossRefGoogle Scholar
  34. 34.
    Clemens, D.L., Horwitz, M.A. 1995Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited.J. Exp. Med.181257270Google Scholar
  35. 35.
    Clemens, D.L., Lee, B.Y., Horwitz, M.A. 2002The Mycobacterium tuberculosis phagosome in human macrophages is isolated from the host cell cytoplasm.Infect. Immun.7058005807CrossRefGoogle Scholar
  36. 36.
    Collins, R.F., Schreiber, A.D., Grinstein, S., Trimble, W.S. 2002Syntaxins 13 and 7 function at distinct steps during phagocytosis.J. Immunol.16932503250Google Scholar
  37. 37.
    Cuellar-Mata, P., Jabado, N., Liu, J., Furuya, W., Finlay, B.B., Gros, P., Grinstein, S. 2002Nrampl modifies the fusion of Salmonella typhimurium-containing vacuoles with cellular endomembranes in macrophages.J. Biol. Chem.27722582265CrossRefGoogle Scholar
  38. 38.
    Cywes, C., Hoppe, H.C., Daffe, M., Ehlers, M.R. 1997Nonopsonic binding of Mycobacterium tuberculosis to complement receptor type 3 is mediated by capsular polysaccharides and is strain dependent.Infect. Immun.6542584266Google Scholar
  39. 39.
    Daeron, M. 1997Fc receptor biology.Annu. Rev. Immunol.15203234CrossRefGoogle Scholar
  40. 40.
    Deiwick, J., Nikolaus, T., Erdogan, S., Hensel, M. 1999Environmental regulation of Salmonella pathogenicity island 2 gene expression.Mol. Microbiol.3117591773CrossRefGoogle Scholar
  41. 41.
    Dermine, J.F., Scianimanico, S., Prive, C., Descoteaux, A., Desjardins, M. 2000Leishmania promastigotes require lipophosphoglycan to actively modulate the fusion properties of phagosomes at an early step of phagocytosis.Cell Microbiol.2115126CrossRefGoogle Scholar
  42. 42.
    Desjardins, M. 1995Biogenesis of phagolysosomes: the “kiss-and-run” hypothesis.Trends Cell Biol.5183186CrossRefGoogle Scholar
  43. 43.
    Desjardins, M., Huber, L.A., Parton, R.G., Griffiths, G. 1994Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus.J. Cell biol.124677688Google Scholar
  44. 44.
    Desjardins, M., Nzala, N.N., Corsini, R., Rondeau, C. 1997Maturation of phagosomes is accompanied by changes in their fusion properties and size-selective acquisition of solute materials from endosomes.J. Cell Sci.11023032314Google Scholar
  45. 45.
    D’Hondt, K., Heese-Peck, A., Riezman, H. 2000Protein and lipid requirements for endocytosis.Annu. Rev. Genet.34255295CrossRefGoogle Scholar
  46. 46.
    Diamond, M.S., Garcia-Aguilar, J., Bickford, J.K., Corbi, A.L., Springer, T.A. 1993The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands.J. Cell Biol.12010311043Google Scholar
  47. 47.
    Duclos, S., Desjardins, M. 2000Subversion of a young phagosome: the survival strategies of intracellular pathogens.Cell Microbiol.2365377CrossRefGoogle Scholar
  48. 48.
    El-Etr, S.H., Cirillo, J.D. 2001Entry mechanisms of mycobacteria.Front. Biosci.6D737D747Google Scholar
  49. 49.
    Ellson, C.D., Anderson, K.E., Morgan, G., Chilvers, E.R., Lipp, P., Stephens, L.R., Hawkins, P.T. 2001Phosphatidylinositol 3-phosphate is generated in phagosomal membranes.Curr. Biol.1116311635CrossRefGoogle Scholar
  50. 50.
    Feng, Y., Press, B., Wandinger-Ness, A. 1995Rab7: an important regulator of late endocytic membrane traffic.J. Cell Biol.13114351452Google Scholar
  51. 51.
    Franc, N.C., White, K., Ezekowitz, R.A. 1999Phagocytosis and development: back to the future.Curr. Opin. Immunol.114752CrossRefGoogle Scholar
  52. 52.
    Francis, C.L., Ryan, T.A., Jones, B.D., Smith, S.J., Falkow, S. 1993Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria.Nature364639642PubMedGoogle Scholar
  53. 53.
    Fratti, R.A., Backer, J.M., Gruenberg, J., Corvera, S., Deretic, V. 2001Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest.J. Cell Biol.154631644CrossRefGoogle Scholar
  54. 54.
    Fratti, R.A., Chua, J., Deretic, V. 2002Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest.J. Biol. Chem.2771732017326CrossRefGoogle Scholar
  55. 55.
    Freeman, J.A., Rappl, C., Kuhle, V., Hensel, M., Miller, S.I. 2002SpiC is required for translocation of Salmonella pathogenicity island 2 effectors and secretion of translocon proteins SseB and SseC.J. Bacteriol.18449714980CrossRefGoogle Scholar
  56. 56.
    Fu, Y., Galan, J.E. 1998The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton.Mol. Microbiol.27359368CrossRefGoogle Scholar
  57. 57.
    Funato, K., Beron, W., Yang, C.Z., Mukhopadhyay, A., Stahl, P.D. 1997Reconstitution of phagosome-lysosome fusion in streptolysin O-permeabilized cells.J. Biol. Chem.2721614716151CrossRefGoogle Scholar
  58. 58.
    Futter, C.E., Collinson, L.M., Backer, J.M., Hopkins, C.R. 2001Human VPS34 is required for internal vesicle formation within multivesicular endosomes.J. Cell Biol.15512511261CrossRefGoogle Scholar
  59. 59.
    Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P.H., Steele-Mortimer, O., Paiement, J., Bergeron, J.J., Desjardins, M. 2002Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages.Cell110119131PubMedGoogle Scholar
  60. 60.
    Gaillard, J.L., Berche, P., Mounier, J., Richard, S., Sansonetti, P. 1987In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2.Infect. Immun.5528222929Google Scholar
  61. 61.
    Galan, J.E., Curtiss 3rd, R. 1989Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells.Proc. Natl. Acad. Sci. USA8663836387Google Scholar
  62. 62.
    Garcia Vescovi, E., Soncini, F.C., Groisman, E.A. 1996Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence.Cell84165174Google Scholar
  63. 63.
    Garcia-del Portillo, F., Zwick, M.B., Leung, K.Y., Finlay, B.B. 1993Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells.Proc. Natl. Acad. Sci. USA901054410548Google Scholar
  64. 64.
    Garin, J., Diez, R., Kieffer, S., Dermine, J.F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C., Desjardins, M. 2001The phagosome proteome. Insight into phagosome functions.J. Cell Biol.152165180CrossRefGoogle Scholar
  65. 65.
    Garner, M.J., Hayward, R.D., Koronakis, V. 2002The Salmonella pathogenicity island 1 secretion system directs cellular cholesterol redistribution during mammalian cell entry and intracellular trafficking.Cell Microbiol.4153165CrossRefGoogle Scholar
  66. 66.
    Garvis, S.G., Beuzon, C.R., Holden, D.W. 2001A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages.Cell Microbiol.3731744CrossRefGoogle Scholar
  67. 67.
    Gaullier, J.M., Simonsen, A., D’Arrigo, A., Bremnes, B., Stenmark, H., Aasland, R. 1998FYVE fingers bind PtdIns(3)P.Nature394432433CrossRefGoogle Scholar
  68. 68.
    Gessner, J.E., Heiken, H., Tamm, A., Schmidt, R.E. 1998The IgG Fc receptor family.Ann. Hematol.76231248CrossRefGoogle Scholar
  69. 69.
    Goldfine, H., Wadsworth, S.J., Johnston, N.C. 2000Activation of host phospholipases C and D in macrophages after infection with Listeria monocytogenes.Infect. Immun.6857355741CrossRefGoogle Scholar
  70. 70.
    Grieshaber, S., Swanson, J.A., Hackstadt, T. 2002Determination of the physical environment within the Chlamydia trachomatis inclusion using ion-selective ratiometric probes.Cell Microbiol.4273283CrossRefGoogle Scholar
  71. 71.
    Gruenberg, J. 2001The endocytic pathway: a mosaic of domains.Nat. Rev. Mol. Cell Biol.2721730CrossRefGoogle Scholar
  72. 72.
    Hackstadt, T. 2000Redirection of host vesicle trafficking pathways by intracellular parasites.Traffic19399CrossRefGoogle Scholar
  73. 73.
    Hackstadt, T., Rockey, D.D., Heinzen, R.A., Scidmore, M.A. 1996Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane.Embo J.15964977Google Scholar
  74. 74.
    Hackstadt, T., Scidmore-Carlson, M.A., Shaw, E.I., Fischer, E.R. 1999The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion.Cell Microbiol.1119130CrossRefGoogle Scholar
  75. 75.
    Hampton, M.B., Kettle, A.J., Winterbourn, C.C. 1998Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing.Blood9230073017PubMedGoogle Scholar
  76. 76.
    Hardt, W.D., Chen, L.M., Schuebel, K.E., Bustelo, X.R., Galan, J.E. 1998S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells.Cell93815826Google Scholar
  77. 77.
    Harrison, R.E., Grinstein, S. 2002. RILP and phagosomes.Google Scholar
  78. 78.
    Hay, J.C. 2001SNARE complex structure and function.Exp. Cell Res.2711021CrossRefGoogle Scholar
  79. 79.
    Hayward, R.D., Koronakis, V. 1999Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella.Embo J.1849264934CrossRefGoogle Scholar
  80. 80.
    Hensel, M, Shea, J.E., Waterman, S.R., Mundy, R., Nikolaus, T., Banks, G., Vazquez-Torres, A., Gleeson, C., Fang, F.C., Holden, D.W. 1998Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages.Mol. Microbiol.30163174CrossRefGoogle Scholar
  81. 81.
    Hoffmann, P.R., deCathelineau, A.M., Ogden, C.A., Leverrier, Y., Bratton, D.L., Daleke, D.L., Ridley, A.J., Fadok, V.A., Henson, P.M. 2001Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells.J. Cell Biol.155649659CrossRefGoogle Scholar
  82. 82.
    Holm, A., Tejle, K., Magnusson, K.E., Descoteaux, A., Rasmusson, B. 2001Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: correlation with impaired translocation of PKCalpha and defective phagosome maturation.Cell Microbiol.3439447CrossRefGoogle Scholar
  83. 83.
    Jahraus, A., Tjelle, T.E., Berg, T., Habermann, A., Storrie, B., Ullrich, O., Griffiths, G. 1998In vitro fusion of phagosomes with different endocytic organelles from J774 macrophages.J. Biol. Chem.2133037930390CrossRefGoogle Scholar
  84. 84.
    Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R., Neefjes, J. 2001The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors.Curr. Biol.1116801685CrossRefGoogle Scholar
  85. 85.
    Kadurugamuwa, J.L., Rohde, M., Wehland, J., Timmis, K.N. 1991Intercellular spread of Shigella flexneri through a monolayer mediated by membranous protrusions and associated with reorganization of the cytoskeletal protein vinculin.Infect. Immun.5934633471Google Scholar
  86. 86.
    Kanai, F., Liu, H., Field, S.J., Akbary, H., Matsuo, T., Brown, G.E., Cantley, L.C., Yaffe, M.B. 2001The PX domains of p47phox and p40phox bind to lipid products of PI(3)K.Nat. Cell Biol.3675678CrossRefGoogle Scholar
  87. 87.
    Katz, S.M., Hashemi, S. 1982Electron microscopic examination of the inflammatory response to Legionella pneumophila in guinea pigs.Lab. Invest.462432Google Scholar
  88. 88.
    Kobayashi, T., Beuchat, M.H., Lindsay, M., Frias, S., Palmiter, R.D., Sakuraba, H., Parton, R.G., Gruenberg, J. 1999Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport.Nat. Cell Biol.11138CrossRefMATHGoogle Scholar
  89. 89.
    Kwiatkowska, K., Sobota, A. 1999Signaling pathways in phagocytosis.Bioessays21422431CrossRefPubMedGoogle Scholar
  90. 90.
    Lawe, D.C., Patki, V., Heller-Harrison, R., Lambright, D., Corvera, S. 2000The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization.J. Biol. Chem.21536993705CrossRefGoogle Scholar
  91. 91.
    Le Cabec, V., Carreno, S., Moisand, A., Bordier, C., Maridonneau-Parini, I. 2002Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively.J. Immunol.16920032009Google Scholar
  92. 92.
    Lennartz, M.R. 1999Phospholipases and phagocytosis: the role of phospholipid-derived second messengers in phagocytosis.Int. J. Biochem. Cell Biol.31415430CrossRefGoogle Scholar
  93. 93.
    Littleton, J.T., Barnard, R.J., Titus, S.A., Slind, J., Chapman, E.R., Ganetzky, B. 2001SNARE-complex disassembly by NSF follows synaptic-vesicle fusion.Proc. Natl. Acad. Sci. USA98122338CrossRefGoogle Scholar
  94. 94.
    Lorenzen, D.R., Gunther, D., Pandit, J., Rudel, T., Brandt, E., Meyer, T.F. 2000Neisseriagonorrhoeae porin modifies the oxidative burst of human professional phagocytes.Infect. Immun.6862156222CrossRefGoogle Scholar
  95. 95.
    Luhrmann, A., Streker, K., Schuttfort, A., Daniels, J.J., Haas, A. 2001Afipia felis induces uptake by macrophages directly into a nonendocytic compartment.Proc. Natl. Acad. Sci. USA9872717276CrossRefGoogle Scholar
  96. 96.
    Luzio, J.P., Rous, B.A., Bright, N.A., Pryor, P.R., Mullock, B.M., Piper, R.C. 2000Lysosome-endosome fusion and lysosome biogenesis.J. Cell Sci.11315151524Google Scholar
  97. 97.
    May, R.C. 2001Phagocytosis in C. elegans: CED-1 reveals its secrets.Trends Cell Biol.11150CrossRefGoogle Scholar
  98. 98.
    May, R.C., Machesky, L.M. 2001Phagocytosis and the actin cytoskeleton.J. Cell Sci.11410611077Google Scholar
  99. 99.
    Mayorga, L.S., Bertini, F., Stahl, P.D. 1991Fusion of newly formed phagosomes with endosomes in intact cells and in a cell-free system.J. Biol. Chem.26665116517Google Scholar
  100. 100.
    McBride, H.M., Rybin, V., Murphy, C., Giner, A., Teasdale, R., Zerial, M. 1999Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13.Cell98377386PubMedGoogle Scholar
  101. 101.
    Mellman, I. 1996Endocytosis and molecular sorting.Annu. Rev. Cell Dev. Biol.12575625PubMedGoogle Scholar
  102. 102.
    Meresse, S., Steele-Mortimer, O., Finlay, B.B., Gorvel, J.P. 1999aThe rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells.Embo J.1843944403Google Scholar
  103. 103.
    Meresse, S., Steele-Mortimer, O., Moreno, E., Desjardins, M., Finlay, B., Gorvel, J.P. 1999bControlling the maturation of pathogen-containing vacuoles: a matter of life and death.Nat. Cell Biol.1E183E188Google Scholar
  104. 104.
    Mills, I.G., Urbe, S., Clague, M.J. 2001Relationships between EEA1 binding partners and their role in endosome fusion.J. Cell Sci.11419591965Google Scholar
  105. 105.
    Misra, S., Miller, G.J., Hurley, J.H. 2001Recognizing phosphatidylinositol 3-phosphate.Cell107559562Google Scholar
  106. 106.
    Monack, D.M., Theriot, J.A. 2001Actin-based motility is sufficient for bacterial membrane protrusion formation and host cell uptake.Cell Microbiol.3633647CrossRefGoogle Scholar
  107. 107.
    Mosleh, I.M., Huber, L.A., Steinlein, P., Pasquali, C., Gunther, D., Meyer, T.F. 1998Neisseria gonorrhoeae porin modulates phagosome maturation.J. Biol. Chem.2733533235338CrossRefGoogle Scholar
  108. 108.
    Mukherjee, S., Ghosh, R.N., Maxfield, F.R. 1997Endocytosis.Physiol. Rev.77759803PubMedGoogle Scholar
  109. 109.
    Mukherjee, K., Parashuraman, S., Raje, M., Mukhopadhyay, A. 2001SopE acts as an Rab5-specific nucleotide exchange factor and recruits non-prenylated Rab5 on Salmonella-containing phagosomes to promote fusion with early endosomes.J. Biol. Chem.2762360723615CrossRefGoogle Scholar
  110. 110.
    Mukherjee, K., Siddiqi, S.A., Hashim, S., Raje, M., Basu, S.K., Mukhopadhyay, A. 2000Live Salmonella recruits N-ethylmaleimide-sensitive fusion protein on phagosomal membrane and promotes fusion with early endosome.J. Cell Biol148741753CrossRefGoogle Scholar
  111. 111.
    Muller, W.A., Steinman, R.M., Cohn, Z.A. 1980The membrane proteins of the vacuolar system. II. Bidirectional flow between secondary lysosomes and plasma membrane.J. Cell Biol.86304314Google Scholar
  112. 112.
    Nagai, H., Kagan, J.C., Zhu, X., Kahn, R.A., Roy, C.R. 2002A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes.Science295679682CrossRefPubMedGoogle Scholar
  113. 113.
    Ochman, H., Soncini, F.C., Solomon, F., Groisman, E.A. 1996Identification of a pathogenicity island required for Salmonella survival in host cells.Proc. Natl. Acad. Sci. USA9378007804CrossRefGoogle Scholar
  114. 114.
    Ofek, I., Goldhar, J., Keisari, Y., Sharon, N. 1995Nonopsonic phagocytosis of microorganisms.Annu. Rev. Microbiol.49239276CrossRefGoogle Scholar
  115. 115.
    Oh, Y.K., Alpuche-Aranda, C., Berthiaume, E., Jinks, T., Miller, S.I., Swanson, J.A. 1996Rapid and complete fusion of macrophage lysosomes with phagosomes containing Salmonella typhimurium.Infect. Immun.6438773883Google Scholar
  116. 116.
    Page, A.L., Ohayon, H., Sansonetti, P.J., Parsot, C. 1999The secreted IpaB and IpaC invasins and their cytoplasmic chaperone IpgC are required for intercellular dissemination of Shigella flexneri.Cell Microbiol.1183193CrossRefGoogle Scholar
  117. 117.
    Panaretou, C., Domin, J., Cockcroft, S., Waterfield, M.D. 1997Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 3-kinase. Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex.J. Biol. Chem.27224772485CrossRefGoogle Scholar
  118. 118.
    Pasula, R., Wisniowski, P., Martin 2nd, W.J. 2002Fibronectin facilitates Mycobacterium tuberculosis attachment to murine alveolar macrophages.Infect. Immun.7012871292CrossRefGoogle Scholar
  119. 119.
    Pattni, K., Jepson, M., Stenmark, H., Banting, G. 2001A PtdIns(3)P-specific probe cycles on and off host cell membranes during Salmonella invasion of mammalian cells.Curr. Biol.1116361642CrossRefGoogle Scholar
  120. 120.
    Perskvist, N., Roberg, K., Kulyte, A., Stendahl, O. 2002Rab5a GTPase regulates fusion between pathogen-containing phagosomes and cytoplasmic organelles in human neutrophils.J. Cell Sci.11513211330Google Scholar
  121. 121.
    Petty, H.R., Todd 3rd., R.F. 1993Receptor-receptor interactions of complement receptor type 3 in neutrophil membranes.J. Leukoc. Biol.54492494Google Scholar
  122. 122.
    Pitt, A., Mayorga, L.S., Schwartz, A.L., Stahl, P.D. 1992aTransport of phagosomal components to an endosomal compartment.J. Biol. Chem.267126132Google Scholar
  123. 123.
    Pitt, A., Mayorga, L.S., Stahl, P.D., Schwartz, A.L. 1992bAlterations in the protein composition of maturing phagosomes.J. Clin. Invest.9019781983Google Scholar
  124. 124.
    Portnoy, D.A., Auerbuch, V., Glomski, I.J. 2002The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity.J. Cell Biol.158409414CrossRefGoogle Scholar
  125. 125.
    Rabinovitch, M. 1995Professional and non-professional phagocytes: an introduction.Trends Cell Biol.58587CrossRefGoogle Scholar
  126. 126.
    Rao, S.P., Ogata, K., Catanzaro, A. 1993Mycobacterium avium-M. intracellulare binds to the integrin receptor alpha v beta 3 on human monocytes and monocyte-derived macrophages.Infect. Immun.61663670Google Scholar
  127. 127.
    Row, P.E., Reaves, B.J., Domin, J., Luzio, J.P., Davidson, H.W. 2001Overexpression of a rat kinase-deficient phosphoinositide 3-kinase, Vps34p, inhibits cathepsin D maturation.Biochem. J.353655661CrossRefGoogle Scholar
  128. 128.
    Roy, C.R., Berger, K.H., Isberg, R.R. 1998Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake.Mol. Microbiol.28663674CrossRefGoogle Scholar
  129. 129.
    Ruiz-Albert, J., Yu, X.J., Beuzon, C.R., Blakey, A.N., Galyov, E.E., Holden, D.W. 2002Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane.Mol. Microbiol.44645661CrossRefGoogle Scholar
  130. 130.
    Schlesinger, L.S. 1993Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors.J. Immunol.15029202930Google Scholar
  131. 131.
    Schlesinger, L.S., Bellinger-Kawahara, C.G., Payne, N.R., Horwitz, M.A. 1990Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3.J. Immunol.14427712780Google Scholar
  132. 132.
    Schu, P.V., Takegawa, K., Fry, M.J., Stack, J.H., Waterfield, M.D., Emr, S.D. 1993Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting.Science2608891Google Scholar
  133. 133.
    Schutt, C. 1999Fighting infection: the role of lipopolysaccharide binding proteins CD14 and LBP.Pathobiology67227229CrossRefGoogle Scholar
  134. 134.
    Scianimanico, S., Desrosiers, M., Dermine, J.F., Meresse, S., Descoteaux, A., Desjardins, M. 1999Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes.Cell Microbiol.11932CrossRefGoogle Scholar
  135. 135.
    Scott, C.C., Cuellar-Mata, P., Matsuo, T., Davidson, H.W., Grinstein, S. 2002Role of 3-phosphoinositides in the maturation of Salmonella-containing vacuoles within host cells.J. Biol. Chem.2771277012776CrossRefGoogle Scholar
  136. 136.
    Shpetner, H., Joly, M., Hartley, D., Corvera, S. 1996Potential sites of PI-3 kinase function in the endocytic pathway revealed by the PI-3 kinase inhibitor, wortmannin.J. Cell Biol.132595605Google Scholar
  137. 137.
    Sollner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H., Rothman, J.E. 1993A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion.Cell75409418Google Scholar
  138. 138.
    Somsel Rodman, J., Wandinger-Ness, A. 2000Rab GTPases coordinate endocytosis.J. Cell Sci.113183192Google Scholar
  139. 139.
    Steele-Mortimer, O., Meresse, S., Gorvel, J.P., Toh, B.H., Finlay, B.B. 1999Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway.Cell Microbiol.13349CrossRefGoogle Scholar
  140. 140.
    Steele-Mortimer, O., St-Louis, M., Olivier, M., Finlay, B.B. 2000Vacuole acidification is not required for survival of Salmonella enterica serovar typhimurium within cultured macrophages and epithelial cells.Infect. Immun.6854015404CrossRefGoogle Scholar
  141. 141.
    Stein, M.A., Leung, K.Y., Zwick, M., Garcia-del Portillo, F., Finlay, B.B. 1996Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells.Mol. Microbiol.20151164Google Scholar
  142. 142.
    Steinert, M., Hentschel, U., Hacker, J. 2002Legionella pneumophila: an aquatic microbe goes astray.FEMS Microbiol. Rev.26149162CrossRefGoogle Scholar
  143. 143.
    Stephens, L., Ellson, C., Hawkins, P. 2002Roles of PI3Ks in leukocyte chemotaxis and phagocytosis.Curr. Opin. Cell Biol.14203213CrossRefGoogle Scholar
  144. 144.
    Stokes, R.W., Haidl, I.D., Jefferies, W.A., Speert, D.P. 1993Mycobacteria-macrophage interactions. Macrophage phenotype determines the nonopsonic binding of Mycobacterium tuberculosis to murine macrophages.J. Immunol.15170677076Google Scholar
  145. 145.
    Subtil, A., Parsot, C., Dautry-Varsat, A. 2001Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery.Mol. Microbiol.39792800CrossRefGoogle Scholar
  146. 146.
    Swanson, M.S., Isberg, R.R. 1995Association of Legionella pneumophila with the macrophage endoplasmic reticulum.Infect. Immun.6336093620Google Scholar
  147. 147.
    Swanton, E., Bishop, N., Sheehan, J., High, S., Woodman, P. 2000Disassembly of membrane-associated NSF 20S complexes is slow relative to vesicle fusion and is Ca(2+)-independent.J. Cell Sci.11317831791Google Scholar
  148. 148.
    Tapper, H., Furuya, W., Grinstein, S. 2002Localized exocytosis of primary (lysosomal) granules during phagocytosis: role of Ca2+-dependent tyrosine phosphorylation and microtubules.J. Immunol.16852875296Google Scholar
  149. 149.
    Teitelbaum, R., Cammer, M., Maitland, M.L., Freitag, N.E., Condeelis, J., Bloom, B.R. 1999Mycobacterial infection of macrophages results in membrane-permeable phagosomes.Proc. Natl. Acad. Sci. USA961519015195CrossRefGoogle Scholar
  150. 150.
    Terebiznik, M.R., Vieira, O.V., Marcus, S.L., Slade, A., Yip, C.M., Trimble, W.S., Meyer, T., Finlay, B.B., Grinstein, S. 2002Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella.Nat. Cell Biol.4766773CrossRefGoogle Scholar
  151. 151.
    Thornton, B.P., Vetvicka, V., Pitman, M., Goldman, R.C., Ross, G.D. 1996Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18).J. Immunol.15612351246Google Scholar
  152. 152.
    Tilney, L.G., Harb, O.S., Connelly, P.S., Robinson, C.G., Roy, C.R. 2001How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane.J. Cell Sci.11446374650Google Scholar
  153. 153.
    Tjelle, T.E., Lovdal, T., Berg, T. 2000Phagosome dynamics and function.Bioessays22255263CrossRefGoogle Scholar
  154. 154.
    Uchiya, K., Barbieri, M.A., Funato, K., Shah, A.H., Stahl, P.D., Groisman, E.A. 1999A Salmonella virulence protein that inhibits cellular trafficking.Embo J.1839243933CrossRefGoogle Scholar
  155. 155.
    Underhill, D.M., Ozinsky, A. 2002Phagocytosis of microbes: complexity in action.Annu. Rev. Immunol.20825852CrossRefGoogle Scholar
  156. 156.
    Vanhaesebroeck, B., Waterfield, M.D. 1999Signaling by distinct classes of phosphoinositide 3-kinases.Exp. Cell Res.253239254CrossRefGoogle Scholar
  157. 157.
    Via, L.E., Deretic, D., Ulmer, R.J., Hibler, N.S., Huber, L.A., Deretic, V. 1997Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7.J. Biol. Chem.2721332613331CrossRefGoogle Scholar
  158. 158.
    Via, L.E., Fratti, R.A., McFalone, M., Pagan-Ramos, E., Deretic, D., Deretic, V. 1998Effects of cytokines on mycobacterial phagosome maturation.J. Cell Sci.111897905Google Scholar
  159. 159.
    Vieira, O.V., Botelho, R.J., Grinstein, S. 2002Phagosome maturation: aging gracefully.Biochem. J.In pressCrossRefPubMedGoogle Scholar
  160. 160.
    Vieira, O.V., Botelho, R.J., Rameh, L., Brachmann, S.M., Matsuo, T., Davidson, H.W., Schreiber, A., Backer, J.M., Cantley, L.C., Grinstein, S. 2001Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation.J. Cell Biol.1551925CrossRefGoogle Scholar
  161. 161.
    Volinia, S., Dhand, R., Vanhaesebroeck, B., MacDougall, L.K., Stein, R., Zvelebil, M.J., Domin, J., Panaretou, C., Waterfield, M.D. 1995A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system.Embo J.1433393348Google Scholar
  162. 162.
    Wade, N., Bryant, N.J., Connolly, L.M., Simpson, R.J., Luzio, J.P., Piper, R.C., James, D.E. 2001Syntaxin 7 complexes with mouse Vps10p tail interactor 1b, syntaxin 6, vesicle-associated membrane protein (VAMP)8, and VAMP7 in b16 melanoma cells.J. Biol. Chem.2761982019827CrossRefGoogle Scholar
  163. 163.
    Walker, D.H., Feng, H.M., Popov, V.L. 2001Rickettsial phospholipase A2 as a pathogenic mechanism in a model of cell injury by typhus and spotted fever group rickettsiae.Am. J. Trop. Med. Hyg.65936942Google Scholar
  164. 164.
    Wilkowsky, S.E., Barbieri, M.A., Stahl, P.D., Isola, E.L. 2002Regulation of Trypanosoma cruzi invasion of nonphagocytic cells by the endocytically active GTPases dynamin, Rab5, and Rab7.Biochem. Biophys. Res. Commun.291516521CrossRefGoogle Scholar
  165. 165.
    Xu, Y., Hortsman, H., Sect, L., Wong, S.H., Hong, W. 2001SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P.Nat. Cell Biol.3658666CrossRefGoogle Scholar
  166. 166.
    Yefenof, E. 2000Complement receptor 3 (CR3): a public transducer of innate immunity signals in macrophages.Adv. Exp. Med. Biol.4791525Google Scholar
  167. 167.
    Yu, X.J., Ruiz-Albert, J., Unsworth, K.E., Garvis, S., Liu, M., Holden, D.W. 2002SpiC is required for secretion of Salmonella Pathogenicity Island 2 type III secretion system proteins.Cell Microbiol.4531540CrossRefMATHGoogle Scholar
  168. 168.
    Zhou, D., Mooseker, M.S., Galan, J.E. 1999Role of the S. typhimurium actin-binding protein SipA in bacterial internalization.Science28320922095CrossRefGoogle Scholar
  169. 169.
    Zimmerli, S., Edwards, S., Ernst, J.D. 1996Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages.Am. J. Respir. Cell. Mol. Biol.15760770Google Scholar

Copyright information

© Springer-Verlag New York Inc. 2003

Authors and Affiliations

  1. 1.Programme in Cell Biology, The Hospital for Sick Children and Department of BiochemistryUniversity of Toronto, 555 University Avenue, Toronto, OntarioCanada

Personalised recommendations