Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes

doi:10.1084/jem.179.2.601

This Article

	Full Text (PDF, 1708K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Alpuche-Aranda, C. M.
	Articles by Miller, S. I.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Alpuche-Aranda, C. M.
	Articles by Miller, S. I.


Social Bookmarking

	What's this?

ARTICLES

Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes

CM Alpuche-Aranda, EL Racoosin, JA Swanson and SI Miller
Infectious Disease Unit, Massachusetts General Hospital, Boston 02114.

Light microscopic studies of phagocytosis showed that Salmonella typhimurium entered mouse macrophages enclosed in spacious phagosomes (SP). Viewed by time-lapse video microscopy, bone marrow-derived macrophages exposed to S. typhimurium displayed generalized plasma membrane ruffling and macropinocytosis. Phagosomes containing Salmonella were morphologically indistinguishable from macropinosomes. SP formation was observed after several methods of bacterial opsonization, although bacteria opsonized with specific IgG appeared initially in small phagosomes that later enlarged. In contrast to macropinosomes induced by growth factors, which shrink completely within 15 min, SP persisted in the cytoplasm, enlarging often by fusion with macropinosomes or other SP. A Salmonella strain containing a constitutive mutation in the phoP virulence regulatory locus (PhoPc) induced significantly fewer SP. Similar to Yersinia enterocolitica, PhoPc bacteria entered macrophages in close-fitting phagosomes, consistent with that expected for conventional receptor-mediated phagocytosis. These results suggest that formation of SP contributes to Salmonella survival and virulence.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Bujny, M. V., Ewels, P. A., Humphrey, S., Attar, N., Jepson, M. A., Cullen, P. J. (2008). Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection. J. Cell Sci. 121: 2027-2036 [Abstract] [Full Text]
Subramanian, S., Roberts, C. L., Hart, C. A., Martin, H. M., Edwards, S. W., Rhodes, J. M., Campbell, B. J. (2008). Replication of Colonic Crohn's Disease Mucosal Escherichia coli Isolates within Macrophages and Their Susceptibility to Antibiotics. Antimicrob. Agents Chemother. 52: 427-434 [Abstract] [Full Text]
Guo, A., Lasaro, M. A., Sirard, J.-C., Kraehenbuhl, J.-P., Schifferli, D. M. (2007). Adhesin-dependent binding and uptake of Salmonella enterica serovar Typhimurium by dendritic cells. Microbiology 153: 1059-1069 [Abstract] [Full Text]
Aguirre, A., Cabeza, M. L., Spinelli, S. V., McClelland, M., Garcia Vescovi, E., Soncini, F. C. (2006). PhoP-Induced Genes within Salmonella Pathogenicity Island 1.. J. Bacteriol. 188: 6889-6898 [Abstract] [Full Text]
Knodler, L. A., Bestor, A., Ma, C., Hansen-Wester, I., Hensel, M., Vallance, B. A., Steele-Mortimer, O. (2005). Cloning Vectors and Fluorescent Proteins Can Significantly Inhibit Salmonella enterica Virulence in Both Epithelial Cells and Macrophages: Implications for Bacterial Pathogenesis Studies. Infect. Immun. 73: 7027-7031 [Abstract] [Full Text]
Clemens, D. L., Lee, B.-Y., Horwitz, M. A. (2005). Francisella tularensis Enters Macrophages via a Novel Process Involving Pseudopod Loops. Infect. Immun. 73: 5892-5902 [Abstract] [Full Text]
Rosales-Reyes, R., Alpuche-Aranda, C., Ramirez-Aguilar, M. d. l. L., Castro-Eguiluz, A. D., Ortiz-Navarrete, V. (2005). Survival of Salmonella enterica Serovar Typhimurium within Late Endosomal-Lysosomal Compartments of B Lymphocytes Is Associated with the Inability To Use the Vacuolar Alternative Major Histocompatibility Complex Class I Antigen-Processing Pathway. Infect. Immun. 73: 3937-3944 [Abstract] [Full Text]
Kruth, H. S., Jones, N. L., Huang, W., Zhao, B., Ishii, I., Chang, J., Combs, C. A., Malide, D., Zhang, W.-Y. (2005). Macropinocytosis Is the Endocytic Pathway That Mediates Macrophage Foam Cell Formation with Native Low Density Lipoprotein. J. Biol. Chem. 280: 2352-2360 [Abstract] [Full Text]
Panthel, K., Meinel, K. M., Domenech, V. E. S., Retzbach, H., Igwe, E. I., Hardt, W.-D., Russmann, H. (2005). Salmonella Pathogenicity Island 2-Mediated Overexpression of Chimeric SspH2 Proteins for Simultaneous Induction of Antigen-Specific CD4 and CD8 T Cells. Infect. Immun. 73: 334-341 [Abstract] [Full Text]
Takumi, K., Garssen, J., de Jonge, R., de Jong, W., Havelaar, A. (2005). Release kinetics and cell trafficking in relation to bacterial growth explain the time course of blood neutrophils and monocytes during primary Salmonella infection. Int Immunol 17: 85-93 [Abstract] [Full Text]
Hernandez, L. D., Hueffer, K., Wenk, M. R., Galan, J. E. (2004). Salmonella Modulates Vesicular Traffic by Altering Phosphoinositide Metabolism. Science 304: 1805-1807 [Abstract] [Full Text]
Drevets, D. A., Leenen, P. J. M., Greenfield, R. A. (2004). Invasion of the Central Nervous System by Intracellular Bacteria. Clin. Microbiol. Rev. 17: 323-347 [Abstract] [Full Text]
Baud, D., Benyacoub, J., Revaz, V., Kok, M., Ponci, F., Bobst, M., Curtiss, R. III, De Grandi, P., Nardelli-Haefliger, D. (2004). Immunogenicity against Human Papillomavirus Type 16 Virus-Like Particles Is Strongly Enhanced by the PhoPc Phenotype in Salmonella enterica Serovar Typhimurium. Infect. Immun. 72: 750-756 [Abstract] [Full Text]
Salter, R. D., Tuma-Warrino, R. J., Hu, P. Q., Watkins, S. C. (2004). Rapid and extensive membrane reorganization by dendritic cells following exposure to bacteria revealed by high-resolution imaging. J. Leukoc. Biol. 75: 240-243 [Abstract] [Full Text]
Parikh, S. S., Litherland, S. A., Clare-Salzler, M. J., Li, W., Gulig, P. A., Southwick, F. S. (2003). CapG-/- Mice Have Specific Host Defense Defects That Render Them More Susceptible than CapG+/+ Mice to Listeria monocytogenes Infection but Not to Salmonella enterica Serovar Typhimurium Infection. Infect. Immun. 71: 6582-6590 [Abstract] [Full Text]
Cano, D. A., Pucciarelli, M. G., Martinez-Moya, M., Casadesus, J., Garcia-del Portillo, F. (2003). Selection of Small-Colony Variants of Salmonella enterica Serovar Typhimurium in Nonphagocytic Eucaryotic Cells. Infect. Immun. 71: 3690-3698 [Abstract] [Full Text]
Sanowar, S., Martel, A., Moual, H. L. (2003). Mutational Analysis of the Residue at Position 48 in the Salmonella enterica Serovar Typhimurium PhoQ Sensor Kinase. J. Bacteriol. 185: 1935-1941 [Abstract] [Full Text]
Ibrahim-Granet, O., Philippe, B., Boleti, H., Boisvieux-Ulrich, E., Grenet, D., Stern, M., Latge, J. P. (2003). Phagocytosis and Intracellular Fate of Aspergillus fumigatus Conidia in Alveolar Macrophages. Infect. Immun. 71: 891-903 [Abstract] [Full Text]
Araki, N., Hatae, T., Furukawa, A., Swanson, J. A. (2003). Phosphoinositide-3-kinase-independent contractile activities associated with Fc{gamma}-receptor-mediated phagocytosis and macropinocytosis in macrophages. J. Cell Sci. 116: 247-257 [Abstract] [Full Text]
Igwe, E. I., Geginat, G., Russmann, H. (2002). Concomitant Cytosolic Delivery of Two Immunodominant Listerial Antigens by Salmonella enterica Serovar Typhimurium Confers Superior Protection against Murine Listeriosis. Infect. Immun. 70: 7114-7119 [Abstract] [Full Text]
John, B., Rajagopal, D., Pashine, A., Rath, S., George, A., Bal, V. (2002). Role of IL-12-Independent and IL-12-Dependent Pathways in Regulating Generation of the IFN-{gamma} Component of T Cell Responses to Salmonella typhimurium. J. Immunol. 169: 2545-2552 [Abstract] [Full Text]
Gasper, N. A., Petty, C. C., Schrum, L. W., Marriott, I., Bost, K. L. (2002). Bacterium-Induced CXCL10 Secretion by Osteoblasts Can Be Mediated in Part through Toll-Like Receptor 4. Infect. Immun. 70: 4075-4082 [Abstract] [Full Text]
Pascual, D. W., Trunkle, T., Sura, J. (2002). Fimbriated Salmonella enterica Serovar Typhimurium Abates Initial Inflammatory Responses by Macrophages. Infect. Immun. 70: 4273-4281 [Abstract] [Full Text]
Prouty, A. M., Van Velkinburgh, J. C., Gunn, J. S. (2002). Salmonella enterica Serovar Typhimurium Resistance to Bile: Identification and Characterization of the tolQRA Cluster. J. Bacteriol. 184: 1270-1276 [Abstract] [Full Text]
Takumi, K., Garssen, J., Havelaar, A. (2002). A quantitative model for neutrophil response and delayed-type hypersensitivity reaction in rats orally inoculated with various doses of Salmonella Enteritidis. Int Immunol 14: 111-119 [Abstract] [Full Text]
Watarai, M., Derre, I., Kirby, J., Growney, J. D., Dietrich, W. F., Isberg, R. R. (2001). Legionella pneumophila Is Internalized by a Macropinocytotic Uptake Pathway Controlled by the Dot/Icm System and the Mouse Lgn1 Locus. JEM 194: 1081-1096 [Abstract] [Full Text]
Glasser, A.-L., Boudeau, J., Barnich, N., Perruchot, M.-H., Colombel, J.-F., Darfeuille-Michaud, A. (2001). Adherent Invasive Escherichia coli Strains from Patients with Crohn's Disease Survive and Replicate within Macrophages without Inducing Host Cell Death. Infect. Immun. 69: 5529-5537 [Abstract] [Full Text]
Rupper, A., Lee, K., Knecht, D., Cardelli, J. (2001). Sequential Activities of Phosphoinositide 3-Kinase, PKB/Akt, and Rab7 during Macropinosome Formation in Dictyostelium. Mol. Biol. Cell 12: 2813-2824 [Abstract] [Full Text]
Witke, W., Li, W., Kwiatkowski, D. J., Southwick, F. S. (2001). Comparisons of CapG and gelsolin-null macrophages: demonstration of a unique role for CapG in receptor-mediated ruffling, phagocytosis, and vesicle rocketing. JCB 154: 775-784 [Abstract] [Full Text]
Gallois, A., Klein, J. R., Allen, L.-A. H., Jones, B. D., Nauseef, W. M. (2001). Salmonella Pathogenicity Island 2-Encoded Type III Secretion System Mediates Exclusion of NADPH Oxidase Assembly from the Phagosomal Membrane. J. Immunol. 166: 5741-5748 [Abstract] [Full Text]
Goodier, R. I., Ahmer, B. M. M. (2001). SirA Orthologs Affect both Motility and Virulence. J. Bacteriol. 183: 2249-2258 [Abstract] [Full Text]
Groisman, E. A. (2001). The Pleiotropic Two-Component Regulatory System PhoP-PhoQ. J. Bacteriol. 183: 1835-1842 [Full Text]
Niedergang, F., Sirard, J.-C., Blanc, C. T., Kraehenbuhl, J.-P. (2000). Entry and survival of Salmonella typhimurium in dendritic cells and presentation of recombinant antigens do not require macrophage-specific virulence factors. Proc. Natl. Acad. Sci. USA 97: 14650-14655 [Abstract] [Full Text]
Svensson, M., Johansson, C., Wick, M. J. (2000). Salmonella enterica Serovar Typhimurium-Induced Maturation of Bone Marrow-Derived Dendritic Cells. Infect. Immun. 68: 6311-6320 [Abstract] [Full Text]
Amyere, M., Payrastre, B., Krause, U., Smissen, P. V. D., Veithen, A., Courtoy, P. J. (2000). Constitutive Macropinocytosis in Oncogene-transformed Fibroblasts Depends on Sequential Permanent Activation of Phosphoinositide 3-Kinase and Phospholipase C. Mol. Biol. Cell 11: 3453-3467 [Abstract] [Full Text]
Edwards, J. L., Shao, J. Q., Ault, K. A., Apicella, M. A. (2000). Neisseria gonorrhoeae Elicits Membrane Ruffling and Cytoskeletal Rearrangements upon Infection of Primary Human Endocervical and Ectocervical Cells. Infect. Immun. 68: 5354-5363 [Abstract] [Full Text]
Hashim, S., Mukherjee, K., Raje, M., Basu, S. K., Mukhopadhyay, A. (2000). Live Salmonella Modulate Expression of Rab Proteins to Persist in a Specialized Compartment and Escape Transport to Lysosomes. J. Biol. Chem. 275: 16281-16288 [Abstract] [Full Text]
Garcia-Del Portillo, F., Jungnitz, H., Rohde, M., Guzman, C. A. (2000). Interaction of Salmonella enterica Serotype Typhimurium with Dendritic Cells Is Defined by Targeting to Compartments Lacking Lysosomal Membrane Glycoproteins. Infect. Immun. 68: 2985-2991 [Abstract] [Full Text]
Schwan, W. R., Huang, X.-Z., Hu, L., Kopecko, D. J. (2000). Differential Bacterial Survival, Replication, and Apoptosis-Inducing Ability of Salmonella Serovars within Human and Murine Macrophages. Infect. Immun. 68: 1005-1013 [Abstract] [Full Text]
Mukherjee, K., Siddiqi, S. A., Hashim, S., Raje, M., Basu, S. K., Mukhopadhyay, A. (2000). Live Salmonella Recruits N-Ethylmaleimide-sensitive Fusion Protein on Phagosomal Membrane and Promotes Fusion with Early Endosome. JCB 148: 741-754 [Abstract] [Full Text]
SANGARI, F. J., GOODMAN, J. R., BERMUDEZ, L. E. (2000). Ultrastructural study of Mycobacterium avium infection of HT-29 human intestinal epithelial cells. J Med Microbiol 49: 139-147 [Abstract] [Full Text]
Duclos, S, Diez, R, Garin, J, Papadopoulou, B, Descoteaux, A, Stenmark, H, Desjardins, M (2000). Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J. Cell Sci. 113: 3531-3541 [Abstract]
Grant, T., Bennett-Wood, V., Robins-Browne, R. M. (1999). Characterization of the Interaction between Yersinia enterocolitica Biotype 1A and Phagocytes and Epithelial Cells In Vitro. Infect. Immun. 67: 4367-4375 [Abstract] [Full Text]
Pashine, A., John, B., Rath, S., George, A., Bal, V. (1999). Th1 dominance in the immune response to live Salmonella typhimurium requires bacterial invasiveness but not persistence. Int Immunol 11: 481-489 [Abstract] [Full Text]
Swanson, J., Johnson, M., Beningo, K, Post, P, Mooseker, M, Araki, N (1999). A contractile activity that closes phagosomes in macrophages. J. Cell Sci. 112: 307-316 [Abstract]
Shea, J. E., Beuzon, C. R., Gleeson, C., Mundy, R., Holden, D. W. (1999). Influence of the Salmonella typhimurium Pathogenicity Island 2�Type III Secretion System on Bacterial Growth in the Mouse. Infect. Immun. 67: 213-219 [Abstract] [Full Text]
Meconi, S., Jacomo, V., Boquet, P., Raoult, D., Mege, J.-L., Capo, C. (1998). Coxiella burnetii Induces Reorganization of the Actin Cytoskeleton in Human Monocytes. Infect. Immun. 66: 5527-5533 [Abstract] [Full Text]
Jungnitz, H., West, N. P., Walker, M. J., Chhatwal, G. S., Guzman, C. A. (1998). A Second Two-Component Regulatory System of Bordetella bronchiseptica Required for Bacterial Resistance to Oxidative Stress, Production of Acid Phosphatase, and In Vivo Persistence. Infect. Immun. 66: 4640-4650 [Abstract] [Full Text]
Vassiloyanakopoulos, A. P., Okamoto, S., Fierer, J. (1998). The crucial role of polymorphonuclear leukocytes in resistance to Salmonella dublin infections in genetically susceptible and resistant mice. Proc. Natl. Acad. Sci. USA 95: 7676-7681 [Abstract] [Full Text]
Huang, X.-Z., Tall, B., Schwan, W. R., Kopecko, D. J. (1998). Physical Limitations on Salmonella typhi Entry into Cultured Human Intestinal Epithelial Cells. Infect. Immun. 66: 2928-2937 [Abstract] [Full Text]
Soo, S.-S., Villarreal-Ramos, B., Khan, C. M.�A., Hormaeche, C. E., Blackwell, J. M. (1998). Genetic Control of Immune Response to Recombinant Antigens Carried by an Attenuated Salmonella typhimurium Vaccine Strain: Nramp1 Influences T-Helper Subset Responses and Protection against Leishmanial Challenge. Infect. Immun. 66: 1910-1917 [Abstract] [Full Text]
Veithen, A, Amyere, M, Van Der Smissen, P, Cupers, P, Courtoy, P. (1998). Regulation of macropinocytosis in v-Src-transformed fibroblasts: cyclic AMP selectively promotes regurgitation of macropinosomes. J. Cell Sci. 111: 2329-2335 [Abstract]
Beauregard, K. E., Lee, K.-D., Collier, R. J., Swanson, J. A. (1997). pH-dependent Perforation of Macrophage Phagosomes by Listeriolysin O from Listeria monocytogenes. JEM 186: 1159-1163 [Abstract] [Full Text]
Gruenheid, S., Pinner, E., Desjardins, M., Gros, P. (1997). Natural Resistance to Infection with Intracellular Pathogens: The Nramp1 Protein Is Recruited to the Membrane of the Phagosome. JEM 185: 717-730 [Abstract] [Full Text]
Veithen, A, Cupers, P, Baudhuin, P, Courtoy, P. (1996). v-Src induces constitutive macropinocytosis in rat fibroblasts. J. Cell Sci. 109: 2005-2012 [Abstract]
Zhu, Z., Bao, Z., Li, J. (1995). MacMARCKS Mutation Blocks Macrophage Phagocytosis of Zymosan. J. Biol. Chem. 270: 17652-17655 [Abstract] [Full Text]
Morisaki, J., Heuser, J., Sibley, L. (1995). Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108: 2457-2464 [Abstract]
Small, P., Ramakrishnan, L, Falkow, S (1994). Remodeling schemes of intracellular pathogens. Science 263: 637-639
Kuwae, A., Yoshida, S., Tamano, K., Mimuro, H., Suzuki, T., Sasakawa, C. (2001). Shigella Invasion of Macrophage Requires the Insertion of IpaC into the Host Plasma Membrane. FUNCTIONAL ANALYSIS OF IpaC. J. Biol. Chem. 276: 32230-32239 [Abstract] [Full Text]