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Membrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuoles

dc.contributor.authorShaughnessy, Lee M.en_US
dc.contributor.authorHoppe, Adam D.en_US
dc.contributor.authorChristensen, Kenneth A.en_US
dc.contributor.authorSwanson, Joel A.en_US
dc.date.accessioned2010-06-01T19:31:07Z
dc.date.available2010-06-01T19:31:07Z
dc.date.issued2006-05en_US
dc.identifier.citationShaughnessy, Lee M.; Hoppe, Adam D.; Christensen, Kenneth A.; Swanson, Joel A. (2006). "Membrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuoles." Cellular Microbiology 8(5): 781-792. <http://hdl.handle.net/2027.42/72656>en_US
dc.identifier.issn1462-5814en_US
dc.identifier.issn1462-5822en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/72656
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=16611227&dopt=citationen_US
dc.description.abstractListeria monocytogenes ( Lm ) evade microbicidal defences inside macrophages by secreting a pore-forming cytolysin listeriolysin O (LLO), which allows Lm to escape vacuoles. LLO also inhibits Lm vacuole fusion with lysosomes, which indicates LLO alters vacuole chemistry prior to release of Lm into cytoplasm. Using fluorescent probes to measure membrane permeability, calcium and pH, we identified small membrane perforations in vacuoles containing wild-type but not LLO-deficient ( hly- ) Lm . The small membrane perforations released small fluorescent molecules and persisted for several minutes before expanding to allow exchange of larger fluorescent molecules. Macropinosomes and hly- Lm vacuoles acidified and increased their calcium content ([Ca 2+ ] vac ) within minutes of formation; however, the small perforations made by LLO-expressing bacteria increased vacuolar pH and decreased [Ca 2+ ] vac shortly after infection. Experimental increases in vacuolar pH inhibited Lm vacuole fusion with lysosomes. The timing of perforation indicated that LLO-dependent delays of Lm vacuole maturation result from disruption of ion gradients across vacuolar membranes.en_US
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dc.publisherBlackwell Publishing Ltden_US
dc.rights© 2005 The Authors; Journal compilation © 2005 Blackwell Publishing Ltden_US
dc.titleMembrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuolesen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biologyen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109-0620, USA.en_US
dc.contributor.affiliationotherDepartment of Chemistry, Clemson University, Clemson, SC 29634, USA.en_US
dc.identifier.pmid16611227en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/72656/1/j.1462-5822.2005.00665.x.pdf
dc.identifier.doi10.1111/j.1462-5822.2005.00665.xen_US
dc.identifier.sourceCellular Microbiologyen_US
dc.identifier.citedreferenceLuzio, J. P., Poupon, V., Lindsay, M. R., Mullock, B. M., Piper, R. C., Pryor, P. R. ( 2003 ) Membrane dynamics and the biogenesis of lysosomes. Mol Membr Biol 20: 141 – 154.en_US
dc.identifier.citedreferenceMellman, I., Fuchs, R., Helenius, A. ( 1986 ) Acidification of the endocytic and exocytic pathways. Ann Rev Biochem 55: 663 – 700.en_US
dc.identifier.citedreferenceMeresse, S., Steele-Mortimer, O., Moreno, E., Desjardins, M., Finlay, B., Gorvel, J. -P. ( 1999 ) Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nature Cell Biol 1: E183 – E188.en_US
dc.identifier.citedreferenceMyers, J. T., Tsang, A. W., Swanson, J. A. ( 2003 ) Localized reactive oxygen and nitrogen intermediates inhibit escape of Listeria monocytogenes from vacuoles in activated macrophages. J Immunol 171: 5447 – 5453.en_US
dc.identifier.citedreferencePeters, C., Mayer, A. ( 1998 ) Ca 2+ /calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 396: 575 – 580.en_US
dc.identifier.citedreferencePortnoy, D. A., Jacks, P. S., Hinrichs, D. J. ( 1988 ) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459 – 1471.en_US
dc.identifier.citedreferencePortnoy, D. A., Tweten, R. K., Kehoe, M., Bielecki, J. ( 1992 ) Capacity of Listeriolysin O, Streptolysin O, and Perfringolysin O to mediate growth of Bacillus subtilis within mammalian cells. Infect Immun 60: 2710 – 2717.en_US
dc.identifier.citedreferencePryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R., Luzio, J. P. ( 2000 ) The role of intraorganellar Ca 2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol 149: 1053 – 1062.en_US
dc.identifier.citedreferenceReeves, E. P., Lu, H., Jacobs, H. L., Messina, C. G. M., Bolsover, S., Gabella, G., et al. ( 2002 ) Killing activity of neutrophils is mediated through activation of proteases by K + flux. Nature 416: 291 – 297.en_US
dc.identifier.citedreferenceRossjohn, J., Feil, S. C., McKinstry, W. J., Tweten, R. K., Parker, M. W. ( 1997 ) Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 89: 685 – 692.en_US
dc.identifier.citedreferenceSansonetti, P. ( 2001 ) Phagocytosis of bacterial pathogens: implications in the host response. Semin Immunol 13: 381 – 390.en_US
dc.identifier.citedreferenceScott, C. C., Botelho, R. J., Grinstein, S. ( 2003 ) Phagosome maturation: a few bugs in the system. J Membr Biol 193: 137 – 152.en_US
dc.identifier.citedreferenceSmith, G. A., Marquis, H., Jones, S., Johnston, N. C., Portnoy, D. A., Goldfine, H. ( 1995 ) The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect Immun 63: 4231 – 4237.en_US
dc.identifier.citedreferenceTapper, H., Sundler, R. ( 1995 ) Bafilomycin A1 inhibits lysosomal, phagosomal, and plasma membrane H(+)-ATPase and induces lysosomal enzyme secretion in macrophages. J Cell Physiol 163: 137 – 144.en_US
dc.identifier.citedreferenceTsang, A. W., Oestergaard, K., Myers, J. T., Swanson, J. A. ( 2000 ) Altered membrane trafficking in bone marrow-derived macrophages. J Leukoc Biol 68: 487 – 494.en_US
dc.identifier.citedreferenceUnderhill, D. M., Ozinsky, A. ( 2002 ) Phagocytosis of microbes: complexity in action. Annu Rev Immunol 20: 825 – 852.en_US
dc.identifier.citedreferenceVazquez-Boland, J. -A., Kocks, C., Dramsi, S., Ohayon, H., Geoffroy, C., Mengaud, J., Cossart, P. ( 1992 ) Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect Immun 60: 219 – 230.en_US
dc.identifier.citedreferenceVieira, O. V., Botelho, R. J., Grinstein, S. ( 2002 ) Phagosome maturation: aging gracefully. Biochem J 366: 689 – 704.en_US
dc.identifier.citedreferenceWadsworth, S. J., Goldfine, H. ( 2002 ) Mobilization of protein kinase C in macrophages induced by Listeria monocytogenes affects its internalization and escape from the phagosome. Infect Immun 70: 4650 – 4660.en_US
dc.identifier.citedreferencevan Weert, A. W. M., Dunn, K. W., Geuze, H. J., Maxfield, F. R., Stoorvogel, W. ( 1995 ) Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 130: 821 – 834.en_US
dc.identifier.citedreferenceBeauregard, K. E., Lee, K. -D., Collier, R. J., Swanson, J. A. ( 1997 ) pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J Exp Med 186: 1159 – 1163.en_US
dc.identifier.citedreferenceBerridge, M. J., Lipp, P., Bootman, M. D. ( 2000 ) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11 – 21.en_US
dc.identifier.citedreferenceBielecki, J., Youngman, P., Connelly, P., Portnoy, D. A. ( 1990 ) Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature 345: 175 – 176.en_US
dc.identifier.citedreferenceChristensen, K. A., Myers, J. T., Swanson, J. A. ( 2002 ) pH-dependent regulation of lysosomal calcium in macrophages. J Cell Sci 115: 599 – 607.en_US
dc.identifier.citedreferenceColombo, M. I., Beron, W., Stahl, P. D. ( 1997 ) Calmodulin regulates endosome fusion. J Biol Chem 272: 7707 – 7712.en_US
dc.identifier.citedreferenceCossart, P., Vicente, M. F., Mengaud, J., Baquero, F., Perez-Diaz, J. C., Berche, P. ( 1989 ) Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun 57: 3629 – 3636.en_US
dc.identifier.citedreferenceDesjardins, M., Huber, L. A., Parton, R. G., Griffiths, G. ( 1994 ) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124: 677 – 688.en_US
dc.identifier.citedreferencevan Deurs, B., Holm, P. K., Sandvig, K. ( 1996 ) Inhibition of the vacuolar H(+)-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in HEp-2 cells. Eur J Cell Biol 69: 343 – 350.en_US
dc.identifier.citedreferenceDuclos, S., Desjardins, M. ( 2000 ) Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2: 365 – 377.en_US
dc.identifier.citedreferenceGedde, M. M., Higgins, D. E., Tilney, L. G., Portnoy, D. A. ( 2000 ) Role of listeriolysin O in cell-to-cell spread of Listeria monocytogenes. Infect Immun 68: 999 – 1003.en_US
dc.identifier.citedreferenceGordon, A. H., Hart, P. D., Young, M. R. ( 1980 ) Ammonia inhibits phagosome–lysosome fusion in macrophages. Nature 286: 79 – 80.en_US
dc.identifier.citedreferenceGrynkiewicz, G., Poenie, M., Tsien, R. Y. ( 1985 ) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440 – 3450.en_US
dc.identifier.citedreferenceHakansson, A., Bentley, C. C., Shakhnovic, E. A., Wessels, M. R. ( 2005 ) Cytolysin-dependent evasion of lysosomal killing. Proc of the Natl Acad Sci USA.en_US
dc.identifier.citedreferenceHenry, R., Shaughnessy, L., Loessner, M. J., Alberti-Segui, C., Higgins, D. E., Swanson, J. A. ( 2006 ) Cytolysin-dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cell Microbiol 8: 107 – 119.en_US
dc.identifier.citedreferenceHeuck, A. P., Tweten, R. K., Johnson, A. E. ( 2003 ) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J Biol Chem 278: 31218 – 31225.en_US
dc.identifier.citedreferenceHolroyd, C., Kistner, U., Annaert, W., Jahn, R. ( 1999 ) Fusion of endosomes involved in synaptic vesicle recycling. Mol Biol Cell 10: 3035 – 3044.en_US
dc.identifier.citedreferenceHoppe, A., Christensen, K. A., Swanson, J. A. ( 2002 ) Fluorescence resonance energy transfer-based stoichiometry in living cells. Biophys J 83: 3652 – 3664.en_US
dc.identifier.citedreferenceJones, S., Portnoy, D. A. ( 1994 ) Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect Immun 62: 5608 – 5613.en_US
dc.identifier.citedreferenceKornfeld, S., Mellman, I. ( 1989 ) The biogenesis of lysosomes. Annu Rev Cell Biol 5: 483 – 525.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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