Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages
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We have used endocytic and phagocytic tracers in an EM immunocytochemical study to define the compartments of the phagocytic and endocytic pathways in mouse peritoneal macrophages. Endocytosed BSA-gold appeared successively in early endosomes, spherical endosomal vesicles, a late endosomal tubuloreticular compartment (TC), and terminal lysosomes. The TC appeared as an elaborate structure enriched for the lysosomal membrane glycoproteins Lamp 1 and Lamp 2, and expressing significant levels of rab7, a late endosome-specific GTP-binding protein. The cation-independent mannose-6-phosphate receptor was restricted to specialized regions of the TC that were predominantly adjacent to the Golgi complex. Both the early endosome and the TC had coated bud structures whose composition and function are presently unknown. Phagolysosomes containing latex beads expressed the same membrane antigens and received endocytic tracers simultaneously with the TC. Since the membrane surrounding both organelles was also in direct continuity, we assume that both structures form one functional compartment. Macrosialin, an antigen confined to macrophages and dendritic cells, was heavily expressed in TC and phagolysosomal membranes with low levels being detected in other endosomal compartments and on the cell surface. Treatment of cells with wheat germ agglutinin drastically altered the morphology of the TC, giving rise to sheets of tightly adherent membrane and greatly expanded vesicles, in which cell-associated wheat germ agglutinin was concentrated. The spherical endosomal carrier vesicles loaded with internalized gold tracers clustered nearby, often making contact without fusing. Since the delivery of endocytic tracer to the TC was significantly delayed these experiments suggest that the lectin is somehow preventing the endosome vesicles from fusing with the TC. Collectively, our data argue first that the PLC is equivalent to the "tubular lysosomes" commonly described in macrophages, and second that the meeting of the phagocytic and endocytic pathway occurs in this compartment.
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The movement of phagosomes along microtubules likely facilitates the interaction of phagosomes with endosomes and lysosomes.
“Earlier studies on the phagocytosis of latex beads by macrophages concluded that the movement of the phagosomes along microtubules likely facilitates the interaction of phagosomes with endosomes and lysosomes (Rabinowitz et al., 1992; Desjardins et al., 1994).”
From Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis (2015) · cites this paper as Rabinowitz et al., 1992
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Cites
Receptor-Mediated Endocytosis: Concepts Emerging from the LDL Receptor System
Goldstein, J. L., Brown, M. S., Anderson, R. G. W., Russell, D. W., & Schneider, W. J. (1985) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.01.110185.000245 · Cited by 1,600 · see citing works
Kornfeld, S. A., & Mellman, I. (1989) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.05.110189.002411 · Cited by 1,593 · see citing works
A new method of preparing gold probes for multiple-labeling cytochemistry.
Slot, J. W., & Geuze, H. J. (1985) · PubMed · Cited by 1,419 · see citing works
Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments
Chavrier, P., Parton, R. G., Hauri, H. P., Simons, K., & Zerial, M. (1990) · Cell · doi:10.1016/0092-8674(90)90369-p · Cited by 1,166 · see citing works
rab5 controls early endosome fusion in vitro
Gorvel, J., Chavrier, P., Zerial, M., & Gruenberg, J. E. (1991) · Cell · doi:10.1016/0092-8674(91)90316-q · Cited by 1,094 · see citing works
Armstrong, J. A., & Hart, P. D. (1971) · The Journal of Experimental Medicine · doi:10.1084/jem.134.3.713 · Cited by 991 · see citing works
Slot, J. W., Geuze, H. J., Gigengack, S., Lienhard, G. E., & James, D. E. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.113.1.123 · Cited by 862 · see citing works
The mannose 6-phosphate receptor and the biogenesis of lysosomes
Griffiths, G. W., Hoflack, B., Simons, K., Mellman, I., & Kornfeld, S. A. (1988) · Cell · doi:10.1016/s0092-8674(88)80026-6 · Cited by 856 · see citing works
Self-citationPeters, P. J., Neefjes, J., Oorschot, V. M. J., Ploegh, H. L., & Geuze, H. J. (1991) · Nature · doi:10.1038/349669a0 · Cited by 658 · see citing works
Membrane flow during pinocytosis. A stereologic analysis.
Steinman, R. M., Brodie, S. E., & Cohn, Z. A. (1976) · The Journal of Cell Biology · doi:10.1083/jcb.68.3.665 · Cited by 644 · see citing works
Griffin, F. M., Griffin, J. A., Leider, J. E., & Silverstein, S. C. (1975) · The Journal of Experimental Medicine · doi:10.1084/jem.142.5.1263 · Cited by 588 · see citing works
Gruenberg, J. E., Griffiths, G. W., & Howell, K. E. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.4.1301 · Cited by 586 · see citing works
Self-citationTHE INTERACTION BETWEEN TOXOPLASMA GONDII AND MAMMALIAN CELLS
Jones, T. C., & Hirsch, J. G. (1972) · The Journal of Experimental Medicine · doi:10.1084/jem.136.5.1173 · Cited by 521 · see citing works
Identification of two lysosomal membrane glycoproteins.
Chen, J. W., Murphy, T. L., Willingham, M. C., Pastan, I. H., & August, J. T. (1985) · The Journal of Cell Biology · doi:10.1083/jcb.101.1.85 · Cited by 485 · see citing works
On the preparation of cryosections for immunocytochemistry
Griffiths, G. W., McDowall, A. W., Back, R., & Dubochet, J. (1984) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(84)80024-6 · Cited by 461 · see citing works
Self-citationJoiner, K. A., Fuhrman, S. A., Miettinen, H. M., Kasper, L. H., & Mellman, I. (1990) · Science · doi:10.1126/science.2200126 · Cited by 447 · see citing works
THE INTERACTION OF SOLUBLE HORSERADISH PEROXIDASE WITH MOUSE PERITONEAL MACROPHAGES IN VITRO
Steinman, R. M., & Cohn, Z. A. (1972) · The Journal of Cell Biology · doi:10.1083/jcb.55.1.186 · Cited by 427 · see citing works
Steinman, R. M., Silver, J., & Cohn, Z. A. (1974) · The Journal of Cell Biology · doi:10.1083/jcb.63.3.949 · Cited by 389 · see citing works
Membrane Traffic in Endocytosis: Insights from Cell-Free Assays
Grüenberg, J., & Howell, K. E. (1989) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.05.110189.002321 · Cited by 372 · see citing works
Guagliardi, L. E., Koppelman, B., Blum, J. S., Marks, M. S., Cresswell, P., & Brodsky, F. M. (1990) · Nature · doi:10.1038/343133a0 · Cited by 370 · see citing works
A quantitative analysis of the endocytic pathway in baby hamster kidney cells.
Griffiths, G., Back, R., & Marsh, M. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.6.2703 · Cited by 324 · see citing works
Self-citationFriis, R. R. (1972) · Journal of Bacteriology · doi:10.1128/jb.110.2.706-721.1972 · Cited by 321 · see citing works
Goren, M. B., Hart, P. D., Young, M. R., & Armstrong, J. A. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.7.2510 · Cited by 310 · see citing works
Bomsel, M., Parton, R. G., Kuznetsov, S. A., Schroer, T. A., & Gruenberg, J. E. (1990) · Cell · doi:10.1016/0092-8674(90)90117-w · Cited by 298 · see citing works
Swanson, J. A., Bushnell, A. F., & Silverstein, S. C. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.7.1921 · Cited by 274 · see citing works
THE PARTICULATE HYDROLASES OF MACROPHAGES
Cohn, Z. A., & Wiener, E. (1963) · The Journal of Experimental Medicine · doi:10.1084/jem.118.6.1009 · Cited by 268 · see citing works
Geisow, M. J., Hart, P. D., & Young, M. R. (1981) · The Journal of Cell Biology · doi:10.1083/jcb.89.3.645 · Cited by 248 · see citing works
Lippincott‐Schwartz, J., & Fambrough, D. M. (1987) · Cell · doi:10.1016/0092-8674(87)90543-5 · Cited by 244 · see citing works
Phorbol esters stimulate macropinocytosis and solute flow through macrophages
Swanson, J. A. (1989) · Journal of Cell Science · doi:10.1242/jcs.94.1.135 · Cited by 243 · see citing works
Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles.
Geuze, H. J., Stoorvogel, W., Strous, G. J., Slot, J. W., Zijderhand-Bleekemolen, J. E., & Mellman, I. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.107.6.2491 · Cited by 243 · see citing works
Racoosin, E. L., & Swanson, J. A. (1989) · The Journal of Experimental Medicine · doi:10.1084/jem.170.5.1635 · Cited by 240 · see citing works
Rabinowitz, S. S., & Gordon, S. (1991) · The Journal of experimental medicine · doi:10.1084/jem.174.4.827 · Cited by 233 · see citing works
Self-citationThe dissociation of the attachment and ingestion phases of phagocytosis by macrophages
Rabinovitch, M. (1967) · Experimental Cell Research · doi:10.1016/0014-4827(67)90405-3 · Cited by 225 · see citing works
Parton, R. G., Prydz, K., Bomsel, M., Simons, K., & Griffiths, G. W. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.6.3259 · Cited by 222 · see citing works
Self-citationEFFECTS OF CONCANAVALIN A ON MOUSE PERITONEAL MACROPHAGES
Edelson, P. J., & Cohn, Z. A. (1974) · The Journal of Experimental Medicine · doi:10.1084/jem.140.5.1364 · Cited by 216 · see citing works
Griffiths, G. O., & Hoppeler, H. H. (1986) · Journal of Histochemistry & Cytochemistry · doi:10.1177/34.11.3534077 · Cited by 191 · see citing works
Self-citationSEGMENTAL RESPONSE OF THE MACROPHAGE PLASMA MEMBRANE TO A PHAGOCYTIC STIMULUS
Griffin, F. M., & Silverstein, S. C. (1974) · The Journal of Experimental Medicine · doi:10.1084/jem.139.2.323 · Cited by 179 · see citing works
Chen, J. W., Cha, Y., Yüksel, K. Ü., Gracy, R. W., & August, J. T. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)68370-x · Cited by 159 · see citing works
Griffiths, G. W., Matteoni, R., Back, R., & Hoflack, B. (1990) · Journal of Cell Science · doi:10.1242/jcs.95.3.441 · Cited by 155 · see citing works
Self-citationFusion of newly formed phagosomes with endosomes in intact cells and in a cell-free system.
Mayorga, L. S., Bertini, F., & Stahl, P. D. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)38147-x · Cited by 139 · see citing works
Plasticity of the tubular lysosomal compartment in macrophages
Knapp, P. E., & Swanson, J. A. (1990) · Journal of Cell Science · doi:10.1242/jcs.95.3.433 · Cited by 101 · see citing works
Smith, M. J., & Koch, G. L. E. (1987) · Journal of Cell Science · doi:10.1242/jcs.87.1.113 · Cited by 94 · see citing works
Kielian, M. C., Steinman, R. M., & Cohn, Z. A. (1982) · The Journal of Cell Biology · doi:10.1083/jcb.93.3.866 · Cited by 71 · see citing works
EFFECTS OF CONCANAVALIN A ON MOUSE PERITONEAL MACROPHAGES
Edelson, P. J., & Cohn, Z. A. (1974) · The Journal of Experimental Medicine · doi:10.1084/jem.140.5.1387 · Cited by 66 · see citing works
Maintenance of granuloma macrophages in serum-free medium
Fauve, R. M., Jusforgues, H., & Hevin, B. (1983) · Journal of Immunological Methods · doi:10.1016/0022-1759(83)90442-8 · Cited by 64 · see citing works
A differential response elicited in macrophages on interaction with lectins
Goldman, R., Sharon, N., & Lotan, R. (1976) · Experimental Cell Research · doi:10.1016/0014-4827(76)90598-x · Cited by 63 · see citing works
Hart, P. D., & Young, M. R. (1979) · Experimental Cell Research · doi:10.1016/0014-4827(79)90160-5 · Cited by 54 · see citing works
The structure of organelles of the endocytic pathway in hydrated cryosections of cultured cells.
McDowall, A. W., Gruenberg, J. E., Römisch, K., & Griffiths, G. W. (1989) · PubMed · Cited by 43 · see citing works
Self-citationAssembly of Lysosomes: Perspectives from Comparative Molecular Cell Biology
Storrie, B. (1988) · International review of cytology · doi:10.1016/s0074-7696(08)61731-3 · Cited by 35 · see citing works
Modified lysosomal compartment as carrier of slowly and non-degradable tracers in macrophages.
Tassin, M. T., Lang, T., Antoine, J. C., Hellio, R., & Ryter, A. (1990) · PubMed · Cited by 33 · see citing works
Modulation of phagosome-lysosome fusion in mouse macrophages.
Kielian, M. C., & Cohn, Z. A. (1981) · The Journal of Experimental Medicine · doi:10.1084/jem.153.4.1015 · Cited by 30 · see citing works
Rabinowitz, S. S., & Gordon, S. (1989) · Journal of Cell Science · doi:10.1242/jcs.93.4.623 · Cited by 30 · see citing works
Self-citationIdentification of a membrane glycoprotein found primarily in the prelysosomal endosome compartment.
Park, J. E., Lopez, J. M., Cluett, E. B., & Brown, W. J. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.112.2.245 · Cited by 18 · see citing works
The Compartments of the Endocytic Pathway
Griffiths, G. W. (1992) · Springer eBooks · doi:10.1007/978-3-642-84295-5_9 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion
Mauthe, M., Orhon, I., Rocchi, C., Zhou, X., Luhr, M., Hijlkema, K.-J., Coppes, R. P., Engedal, N., Mari, M., & Reggiori, F. (2018) · Autophagy · doi:10.1080/15548627.2018.1474314 · Cited by 2,122 · see citing works
ENDOCYTOSIS AND MOLECULAR SORTING
Mellman, I. (1996) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.12.1.575 · Cited by 1,521 · see citing works
CAPTURE AND PROCESSING OF EXOGENOUS ANTIGENS FOR PRESENTATION ON MHC MOLECULES
Watts, C. K. W. (1997) · Annual Review of Immunology · doi:10.1146/annurev.immunol.15.1.821 · Cited by 754 · see citing works
Lewis A. Conner Memorial Lecture
Steinberg, D. H. (1997) · Circulation · doi:10.1161/01.cir.95.4.1062 · Cited by 743 · see citing works
The endocytic pathway: a mosaic of domains
Gruenberg, J. E. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35096054 · Cited by 703 · see citing works
Clemens, D. L., & Horwitz, M. A. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.181.1.257 · Cited by 681 · see citing works
In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles
Reddy, S. T., Rehor, A., Schmoekel, H. G., Hubbell, J. A., & Swartz, M. A. (2006) · Journal of Controlled Release · doi:10.1016/j.jconrel.2006.01.006 · Cited by 680 · see citing works
Desjardins, M., Huber, L., Parton, R., & Griffiths, G. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.5.677 · Cited by 673 · see citing works
Self-citationRab 7: an important regulator of late endocytic membrane traffic.
Feng, Y., Press, B., & Wandinger‐Ness, A. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.6.1435 · Cited by 637 · see citing works
Dendritic cells in the T‐cell areas of lymphoid organs
Steinman, R. M., Pack, M., & Inaba, K. (1997) · Immunological Reviews · doi:10.1111/j.1600-065x.1997.tb00956.x · Cited by 550 · see citing works
Lysosomes Behave as Ca2+-regulated Exocytic Vesicles in Fibroblasts and Epithelial Cells
Rodrı́guez, A., Webster, P. C., Ortego, J., & Andrews, N. W. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.1.93 · Cited by 532 · see citing works
Infectious HIV-1 assembles in late endosomes in primary macrophages
Pelchen–Matthews, A., Kramer, B., & Marsh, M. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200304008 · Cited by 491 · see citing works
NGF Signaling in Sensory Neurons
Delcroix, J., Valletta, J. S., Wu, C., Hunt, S. J., Kowal, A. S., & Mobley, W. C. (2003) · Neuron · doi:10.1016/s0896-6273(03)00397-0 · Cited by 455 · see citing works
Gruenheid, S., Pinner, E., Desjardins, M., & Gros, P. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.4.717 · Cited by 428 · see citing works
Pizarro‐Cerdá, J., Méresse, S., Parton, R. G., van der Goot, G., Sola‐Landa, A., López‐Goñi, I., Moreno, E., & Gorvel, J. (1998) · Infection and Immunity · doi:10.1128/iai.66.12.5711-5724.1998 · Cited by 428 · see citing works
The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin.
Takei, K., Mundigl, O., DANIELL, L. W., & Camilli, P. V. D. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.133.6.1237 · Cited by 416 · see citing works
Aniento, F. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.6.1373 · Cited by 404 · see citing works
Tardieux, I., Webster, P. C., Ravesloot, J. H., Boron, W. F., Lunn, J. A., Heuser, J. E., & Andrews, N. W. (1992) · Cell · doi:10.1016/s0092-8674(05)80061-3 · Cited by 387 · see citing works
Ramprasad, M. P., Terpstra, V., Kondratenko, N., Quehenberger, O., & Steinberg, D. H. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14833 · Cited by 382 · see citing works
Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network
Schmelz, M., Sodeik, B., Ericsson, M., Wolffe, E. J., Shida, H., Hiller, G., & Griffiths, G. W. (1994) · Journal of Virology · doi:10.1128/jvi.68.1.130-147.1994 · Cited by 382 · see citing works
Self-citationA novel class of clathrin-coated vesicles budding from endosomes.
Stoorvogel, W., Oorschot, V. M. J., & Geuze, H. J. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.132.1.21 · Cited by 358 · see citing works
Roy, C. R., Berger, K. H., & Isberg, R. R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00841.x · Cited by 357 · see citing works
Endolysosomal proteolysis and its regulation
Pillay, C. S., Elliott, E., & Dennison, C. (2002) · Biochemical Journal · doi:10.1042/0264-6021:3630417 · Cited by 341 · see citing works
Magnetically labeled cells can be detected by MR imaging
Weissleder, R., Cheng, H., Bogdanova, A., & Bogdanov, A. A., Jr. (1997) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.1880070140 · Cited by 338 · see citing works
Macropinosome maturation and fusion with tubular lysosomes in macrophages.
Racoosin, E. L., & Swanson, J. A. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.5.1011 · Cited by 335 · see citing works
The coordination of signaling during Fc receptor-mediated phagocytosis
Swanson, J. A., & Hoppe, A. D. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0804439 · Cited by 326 · see citing works
Ramprasad, M. P., Fischer, W., Witztum, J. L., Sambrano, G. R., Quehenberger, O., & Steinberg, D. H. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.21.9580 · Cited by 311 · see citing works
Clemens, D. L., & Horwitz, M. A. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.4.1349 · Cited by 304 · see citing works
The rab7 gtpase resides on a vesicular compartment connected to lysosomes
Méresse, S., Gorvel, J., & Chavrier, P. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.11.3349 · Cited by 293 · see citing works
Inhibition of Phagolysosomal Biogenesis by the Leishmania Lipophosphoglycan
Desjardins, M., & Descoteaux, A. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.12.2061 · Cited by 289 · see citing works
Particulate vaccines: on the quest for optimal delivery and immune response
Temmerman, M. D., Rejman, J., Demeester, J., Irvine, D. J., Gander, B. A., & Smedt, S. C. D. (2011) · Drug Discovery Today · doi:10.1016/j.drudis.2011.04.006 · Cited by 288 · see citing works
Phagocytosis and comparative innate immunity: learning on the fly
Stuart, L. M., & Ezekowitz, R. A. B. (2008) · Nature reviews. Immunology · doi:10.1038/nri2240 · Cited by 288 · see citing works
Cytoplasmic coat proteins involved in endosome function
Whitney, J. A., Gomez, M., Sheff, D. R., Kreis, T. E., & Mellman, I. (1995) · Cell · doi:10.1016/0092-8674(95)90183-3 · Cited by 281 · see citing works
Molecular characterization of phagosomes.
Desjardins, M., Celis, J. E., Gerrit van, M. E. E. R., Dieplinger, H., Jahraus, A., Griffiths, G. W., & Huber, L. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)31620-x · Cited by 279 · see citing works
Self-citationHIV-1 Buds Predominantly at the Plasma Membrane of Primary Human Macrophages
Welsch, S., Keppler, O. T., Habermann, A., Allespach, I., Krijnse‐Locker, J., & Kräusslich, H. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030036 · Cited by 272 · see citing works
Haas, A., Scheglmann, D., Lazar, T. A., Gallwitz, D., & Wickner, W. T. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00210.x · Cited by 267 · see citing works
Biogenesis of phagolysosomes: the 'kiss and run' hypothesis
Desjardins, M. (1995) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)88989-8 · Cited by 266 · see citing works
del Portillo, F. G., & Finlay, B. B. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.129.1.81 · Cited by 261 · see citing works
Astarie‐Dequeker, C., N’Diaye, E.-N., Cabec, V. L., Rittig, M. G., Prandi, J., & Maridonneau‐Parini, I. (1999) · Infection and Immunity · doi:10.1128/iai.67.2.469-477.1999 · Cited by 250 · see citing works
The rab7 GTPase controls the maturation of Salmonella typhimurium‐containing vacuoles in HeLa cells
Méresse, S., Steele‐Mortimer, O., Finlay, B. B., & Gorvel, J. (1999) · The EMBO Journal · doi:10.1093/emboj/18.16.4394 · Cited by 234 · see citing works
SAFE HAVEN: The Cell Biology of Nonfusogenic Pathogen Vacuoles
Sinai, A. P., & Joiner, K. A. (1997) · Annual Review of Microbiology · doi:10.1146/annurev.micro.51.1.415 · Cited by 226 · see citing works
Macrosialin, a mouse macrophage-restricted glycoprotein, is a member of the lamp/lgp family
Holness, C. L. L., da Silva, R. P., Fawcett, J., Gordon, S., & Simmons, D. L. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)98400-0 · Cited by 217 · see citing works
Self-citationFlannagan, R. S., Heit, B., & Heinrichs, D. E. (2015) · Cellular Microbiology · doi:10.1111/cmi.12527 · Cited by 216 · see citing works
The Chlamydial Inclusion: Escape from the Endocytic Pathway
Fields, K. A., & Hackstadt, T. (2002) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.18.012502.105845 · Cited by 215 · see citing works
Intracellular transport of MHC class II molecules
Neefjes, J., & Ploegh, H. L. (1992) · Immunology Today · doi:10.1016/0167-5699(92)90123-o · Cited by 215 · see citing works
Zeng, Q., Si, X., Horstmann, H., Xu, Y., Hong, W., & Pallen, C. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000453200 · Cited by 210 · see citing works
Self-citationMordue, D. G., Håkansson, S., Niesman, I. R., & Sibley, L. D. (1999) · Experimental Parasitology · doi:10.1006/expr.1999.4412 · Cited by 209 · see citing works
Yolk-sac–derived macrophages regulate fetal testis vascularization and morphogenesis
DeFalco, T., Bhattacharya, I., Williams, A. V., Sams, D. M., & Capel, B. (2014) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1400057111 · Cited by 173 · see citing works
Lysosomal Enzyme Trafficking between Phagosomes, Endosomes, and Lysosomes in J774 Macrophages
Claus, V., Jahraus, A., Tjelle, T. E., Berg, T., Kirschke, H., Faulstich, H., & Griffiths, G. W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.16.9842 · Cited by 205 · see citing works
Self-citationPieters, J., Bakke, O., & Dobberstein, B. (1993) · Journal of Cell Science · doi:10.1242/jcs.106.3.831 · Cited by 204 · see citing works
Histoplasma capsulatum modulates the acidification of phagolysosomes.
Eissenberg, L. G., Goldman, W. E., & Schlesinger, P. H. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.177.6.1605 · Cited by 200 · see citing works
Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes
Hille-Rehfeld, A. (1995) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(95)00004-b · Cited by 249 · see citing works
What transgenic mice tell us about neurodegenerative disease
Gurney, M. E. (2000) · BioEssays · doi:10.1002/(sici)1521-1878(200003)22:3 · Cited by 38 · see citing works
Antigen Markers of Macrophage Differentiation in Murine Tissues
Gordon, S., Lawson, L. J., Rabinowitz, S. S., Crocker, P. R., Morris, L., & Perry, V. H. (1992) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-77377-8_1 · Cited by 187 · see citing works
Self-citationConfrontation between Intracellular Bacteria and the Immune System
Schaible, U. E., Collins, H., & Kaufmann, S. H. E. (1998) · Advances in immunology · doi:10.1016/s0065-2776(08)60405-8 · Cited by 182 · see citing works
Campylobacter jejuni Survives within Epithelial Cells by Avoiding Delivery to Lysosomes
Watson, R. O., & Galán, J. E. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.0040014 · Cited by 181 · see citing works
de Chastellier, C., & Berche, P. (1994) · Infection and Immunity · doi:10.1128/iai.62.2.543-553.1994 · Cited by 181 · see citing works
Duclos, S., Diez, R., Garin, J., Papadopoulou, B., Descoteaux, A., Stenmark, H., & Desjardins, M. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.19.3531 · Cited by 175 · see citing works
Tjelle, T. E., Brech, A., Juvet, L. K., Griffiths, G. W., & Berg, T. (1996) · Journal of Cell Science · doi:10.1242/jcs.109.12.2905 · Cited by 170 · see citing works
Self-citationScianimanico, S., Desrosiers, M., Dermine, J.-F., Méresse, S., Descoteaux, A., & Desjardins, M. (1999) · Cellular Microbiology · doi:10.1046/j.1462-5822.1999.00002.x · Cited by 169 · see citing works
Russell, D. G., Xu, S., & Chakraborty, P. (1992) · Journal of Cell Science · doi:10.1242/jcs.103.4.1193 · Cited by 169 · see citing works
Palokangas, H., Mulari, M. T. K., & Väänänen, H. K. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.15.1767 · Cited by 168 · see citing works
Pizon, V., Desjardins, M., Bucci, C., Parton, R. G., & Zerial, M. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.6.1661 · Cited by 165 · see citing works
Harding, C. V., & Geuze, H. J. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.3.531 · Cited by 164 · see citing works
Kühnel, M., Goethe, R., Habermann, A., Mueller, E., Rohde, M., Griffiths, G., & Valentin‐Weigand, P. (2001) · Cellular Microbiology · doi:10.1046/j.1462-5822.2001.00139.x · Cited by 161 · see citing works
Self-citationSize of IgG-Opsonized Particles Determines Macrophage Response during Internalization
Koval, M. H., Preiter, K., Adles, C., Stahl, P. D., & Steinberg, T. H. (1998) · Experimental Cell Research · doi:10.1006/excr.1998.4110 · Cited by 161 · see citing works
Intracellular Trafficking ofBrucella abortusin J774 Macrophages
Arenas, G. N., Staskevich, A. S., Aballay, A., & Mayorga, L. S. (2000) · Infection and Immunity · doi:10.1128/iai.68.7.4255-4263.2000 · Cited by 161 · see citing works
Rathman, M., Barker, L. P., & Falkow, S. (1997) · Infection and Immunity · doi:10.1128/iai.65.4.1475-1485.1997 · Cited by 160 · see citing works
Kuhle, V., & Hensel, M. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-4248-z · Cited by 159 · see citing works
Localisation of Nramp1 in macrophages: Modulation with activation and infection
Searle, S., Bright, N. A., Roach, T. I. A., Atkinson, P. G. P., Barton, C. H., Meloen, R. H., & Blackwell, J. M. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.19.2855 · Cited by 158 · see citing works
Courret, N., Fréhel, C., Gouhier, N., Pouchelet, M., Prina, E., Roux, P., & Antoine, J.-C. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.11.2303 · Cited by 154 · see citing works
Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport.
Rodrı́guez, A., Samoff, E., Rioult, M. G., Chung, A., & Andrews, N. W. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.134.2.349 · Cited by 149 · see citing works
Characterization of the microglial response in murine scrapie
Williams, A. E., Lawson, L. J., Perry, V. H., & Fraser, H. (1994) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1994.tb00956.x · Cited by 148 · see citing works
MHC class II-restricted antigen processing and presentation
Pieters, J. (2000) · Advances in immunology · doi:10.1016/s0065-2776(00)75004-8 · Cited by 147 · see citing works
Hashim, S., Mukherjee, K., Raje, M., Basu, S. K., & Mukhopadhyay, A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.21.16281 · Cited by 145 · see citing works
Subversion of a young phagosome: the survival strategies of intracellular pathogens. Microreview
Duclos, S., & Desjardins, M. (2000) · Cellular Microbiology · doi:10.1046/j.1462-5822.2000.00066.x · Cited by 144 · see citing works
Infection Genomics:Nramp1as a Major Determinant of Natural Resistance to Intracellular Infections
Skamene, E., Schurr, E., & Gros, P. (1998) · Annual Review of Medicine · doi:10.1146/annurev.med.49.1.275 · Cited by 139 · see citing works
Intracellular Magnetic Labeling of Lymphocytes for In Vivo Trafficking Studies
Schoepf, U. J., Marecos, E., Melder, R. J., Jain, R. K., & Weissleder, R. (1998) · BioTechniques · doi:10.2144/98244rr01 · Cited by 133 · see citing works
Localization of five annexins in J774 macrophages and on isolated phagosomes
Diakonova, M., Gerke, V., Ernst, J., Liautard, J., Vusse, G. J., & Griffiths, G. W. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.10.1199 · Cited by 132 · see citing works
Self-citationDifferent fates of phagocytosed particles after delivery into macrophage lysosomes.
Oh, Y., & Swanson, J. A. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.132.4.585 · Cited by 130 · see citing works
Zuckman, D. M., Hung, J. B., & Roy, C. R. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01410.x · Cited by 129 · see citing works
Membrane trafficking along the phagocytic pathway
Berón, W., Alvarez-Dominguez, C., Mayorga, L., & Stahl, P. D. (1995) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)88958-8 · Cited by 129 · see citing works
Burkhardt, J. K., Wiebel, F. A., Hester, S., & Argon, Y. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.6.1845 · Cited by 128 · see citing works
Desjardins, M., Nzala, N. N., Corsini, R., & Rondeau, C. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.18.2303 · Cited by 127 · see citing works
Morphology and Dynamics of Clathrin/GGA1-coated Carriers Budding from the Trans -Golgi Network
Puertollano, R., van der Wel, N. N., Greene, L. E., Eisenberg, E., Peters, P. J., & Bonifacino, J. S. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.02-07-0109 · Cited by 126 · see citing works
Marion, S., Laurent, C., & Guillén, N. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00573.x · Cited by 125 · see citing works
In Vitro Fusion of Phagosomes with Different Endocytic Organelles from J774 Macrophages
Jahraus, A., Tjelle, T. E., Berg, T., Habermann, A., Storrie, B., Ullrich, O., & Griffiths, G. W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.46.30379 · Cited by 124 · see citing works
Self-citationMolecular immunobiology of macrophages: recent progress
Gordon, S., Clarke, S., Greaves, D. R., & Doyle, A. (1995) · Current Opinion in Immunology · doi:10.1016/0952-7915(95)80025-5 · Cited by 120 · see citing works
Self-citationDynamic life and death interactions between Mycobacterium smegmatis and J774 macrophages
Anes, E., Peyron, P., Staali, L., Jordão, L., Gutierrez, M. G., Kress, H., Hagedorn, M., Maridonneau‐Parini, I., Skinner, M. A., Wildeman, A. G., et al. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2005.00675.x · Cited by 119 · see citing works
Self-citationJahraus, A., Storrie, B., Griffiths, G., & Desjardins, M. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.1.145 · Cited by 119 · see citing works
Self-citationLamothe, J., Huynh, K. K., Grinstein, S., & Valvano, M. A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00766.x · Cited by 115 · see citing works
Balestrieri, B., Hsu, V. W., Gilbert, H.-Y., Leslie, C. C., Han, W. K., Bonventre, J. V., & Arm, J. P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m508314200 · Cited by 114 · see citing works
Alix regulates cortical actin and the spatial distribution of endosomes
Cabezas, A., Bache, K. G., Brech, A., & Stenmark, H. (2005) · Journal of Cell Science · doi:10.1242/jcs.02382 · Cited by 113 · see citing works
Morrison, D. C., Danner, R. L., Dinarello, C. A., Munford, R. S., Natanson, C., Pollack, M., Spitzer, J. J., Ulevitch, R. J., Vogel, S. N., & McSweegan, E. F. (1994) · Journal of Endotoxin Research · doi:10.1177/096805199400100201 · Cited by 110 · see citing works
Cieutat, A.-M., Lobel, P., August, J. T., Kjeldsen, L., Sengeløv, H., Borregaard, N., & Bainton, D. F. (1998) · Blood · doi:10.1182/blood.v91.3.1044.1044_1044_1058 · Cited by 108 · see citing works
Alvarez-Domı́nguez, C., Roberts, R., & Stahl, P. D. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.6.731 · Cited by 105 · see citing works
Myosin Va bound to phagosomes binds to F-actin and delays microtubule-dependent motility
Al-Haddad, A., Shonn, M. A., Redlich, B., Blocker, A., Burkhardt, J. K., Yu, H., Hammer, J. A., Weiss, D. G., Steffen, W., Griffiths, G., et al. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.9.2742 · Cited by 102 · see citing works
Self-citationSILVA, R. P. D., & GORDON, S. (1999) · Biochemical Journal · doi:10.1042/bj3380687 · Cited by 101 · see citing works
Self-citationMyosin IB from Entamoeba histolytica is involved in phagocytosis of human erythrocytes
Voigt, H., Olivo‐Marín, J., Sansonetti, P. J., & Guillén, N. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.8.1191 · Cited by 98 · see citing works
Joshi, A., Sturgill-Koszycki, S., & Swanson, M. S. (2001) · Cellular Microbiology · doi:10.1046/j.1462-5822.2001.00093.x · Cited by 97 · see citing works
- Authors
- Rabinowitz, S., Horstmann, H., Gordon, S., & Griffiths, G.
- Affiliations
- University of Oxford (GB)
- Venue
- The Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 1992-01-01
- Volume
- 116
- Issue
- 1
- Pages
- 95-112
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2289258
- OpenAlex
- W2171821916
- Cited by
- 271
- References
- 54
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 3 · 2018: 1 · 2016: 1 · 2015: 5 · 2014: 4 · 2013: 3 · 2012: 2
- FWCI
- 10.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- peritoneal macrophages, endocytic pathway, phagolysosomes, late endosomes, lysosomes, LAMP1, LAMP2, Rab7, mannose 6-phosphate receptor, wheat germ agglutinin, endosome fusion
- MeSH terms
- Animals, Cells, Cultured, Endocytosis, Lysosomes, Macrophages, Male, Membrane Glycoproteins, Mice, Inbred C57BL, Microscopy, Electron, Models, Biological, Phagocytosis, Wheat Germ Agglutinins, Biomarkers, Antigens, CD, Fluorescein-5-isothiocyanate, Mice, Lysosomal Membrane Proteins
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