This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Arenas, G. N.
Right arrow Articles by Mayorga, L. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Arenas, G. N.
Right arrow Articles by Mayorga, L. S.
Right arrowPubmed/NCBI databases
*Compound via MeSH
*Substance via MeSH

 Previous Article  |  Next Article 

Infection and Immunity, July 2000, p. 4255-4263, Vol. 68, No. 7
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Intracellular Trafficking of Brucella abortus in J774 Macrophages

Graciela N. Arenas,1 Ana Sandra Staskevich,2 Alejandro Aballay,2 and Luis S. Mayorga2,*

Instituto de Histología y Embriología (U.N. Cuyo-CONICET)2 and Cátedra de Microbiología,1 Facultad de Ciencias Médicas, Universidad Nacional de Cuyo, Casilla de Correo 56, Mendoza (5500), Argentina

Received 11 April 2000/Accepted 25 April 2000

Brucella abortus is a facultative intracellular bacterium capable of surviving inside professional and nonprofessional phagocytes. The microorganism remains in membrane-bound compartments that in several cell types resemble modified endoplasmic reticulum structures. To monitor the intracellular transport of B. abortus in macrophages, the kinetics of fusion of phagosomes with preformed lysosomes labeled with colloidal gold particles was observed by electron microscopy. The results indicated that phagosomes containing live B. abortus were reluctant to fuse with lysosomes. Furthermore, newly endocytosed material was not incorporated into these phagosomes. These observations indicate that the bacteria strongly affect the normal maturation process of macrophage phagosomes. However, after overnight incubation, a significant percentage of the microorganisms were found in large phagosomes containing gold particles, resembling phagolysosomes. Most of the Brucella bacteria present in phagolysosomes were not morphologically altered, suggesting that they can also resist the harsh conditions prevalent in this compartment. About 50% colocalization of B. abortus with LysoSensor, a weak base that accumulates in acidic compartments, was observed, indicating that the B. abortus bacteria do not prevent phagosome acidification. In contrast to what has been described for HeLa cells, only a minor percentage of the microorganisms were found in compartments labeled with monodansylcadaverine, a marker for autophagosomes, and with DiOC6 (3,3'-dihexyloxacarbocyanine iodide), a marker for the endoplasmic reticulum. These results indicate that B. abortus bacteria alter phagosome maturation in macrophages. However, acidification does occur in these phagosomes, and some of them can eventually mature to phagolysosomes.


* Corresponding author. Mailing address: Casilla de Correo 56, 5500 Mendoza, Argentina. Phone: 54 261 4494143. Fax: 54 261 4494117. E-mail: lmayorga{at}fmed2.uncu.edu.ar or lmayorga2{at}hotmail.com.


Infection and Immunity, July 2000, p. 4255-4263, Vol. 68, No. 7
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Magnani, D. M., Harms, J. S., Durward, M. A., Splitter, G. A. (2009). Nondividing but Metabolically Active Gamma-Irradiated Brucella melitensis Is Protective against Virulent B. melitensis Challenge in Mice. Infect. Immun. 77: 5181-5189 [Abstract] [Full Text]  
  • Bourg, G., Sube, R., O'Callaghan, D., Patey, G. (2009). Interactions between Brucella suis VirB8 and Its Homolog TraJ from the Plasmid pSB102 Underline the Dynamic Nature of Type IV Secretion Systems. J. Bacteriol. 191: 2985-2992 [Abstract] [Full Text]  
  • Rambow-Larsen, A. A., Rajashekara, G., Petersen, E., Splitter, G. (2008). Putative Quorum-Sensing Regulator BlxR of Brucella melitensis Regulates Virulence Factors Including the Type IV Secretion System and Flagella. J. Bacteriol. 190: 3274-3282 [Abstract] [Full Text]  
  • Valderas, M. W., Barrow, W. W. (2008). Establishment of a method for evaluating intracellular antibiotic efficacy in Brucella abortus-infected Mono Mac 6 monocytes. J Antimicrob Chemother 61: 128-134 [Abstract] [Full Text]  
  • Toyooka, K., Takai, S., Kirikae, T. (2005). Rhodococcus equi can survive a phagolysosomal environment in macrophages by suppressing acidification of the phagolysosome. J Med Microbiol 54: 1007-1015 [Abstract] [Full Text]  
  • Lavigne, J.-P., Patey, G., Sangari, F. J., Bourg, G., Ramuz, M., O'Callaghan, D., Michaux-Charachon, S. (2005). Identification of a New Virulence Factor, BvfA, in Brucella suis. Infect. Immun. 73: 5524-5529 [Abstract] [Full Text]  
  • Bandara, A. B., Sriranganathan, N., Schurig, G. G., Boyle, S. M. (2005). Carboxyl-Terminal Protease Regulates Brucella suis Morphology in Culture and Persistence in Macrophages and Mice. J. Bacteriol. 187: 5767-5775 [Abstract] [Full Text]  
  • Pappas, G., Akritidis, N., Bosilkovski, M., Tsianos, E. (2005). Brucellosis. NEJM 352: 2325-2336 [Full Text]  
  • Bellaire, B. H, Roop, R. M. II, Cardelli, J. A. (2005). Opsonized Virulent Brucella abortus Replicates within Nonacidic, Endoplasmic Reticulum-Negative, LAMP-1-Positive Phagosomes in Human Monocytes. Infect. Immun. 73: 3702-3713 [Abstract] [Full Text]  
  • Kim, S., Watanabe, K., Suzuki, H., Watarai, M. (2005). Roles of Brucella abortus SpoT in morphological differentiation and intramacrophagic replication. Microbiology 151: 1607-1617 [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]  
  • Pei, J., Ficht, T. A. (2004). Brucella abortus Rough Mutants Are Cytopathic for Macrophages in Culture. Infect. Immun. 72: 440-450 [Abstract] [Full Text]  
  • Lestrate, P., Dricot, A., Delrue, R.-M., Lambert, C., Martinelli, V., De Bolle, X., Letesson, J.-J., Tibor, A. (2003). Attenuated Signature-Tagged Mutagenesis Mutants of Brucella melitensis Identified during the Acute Phase of Infection in Mice. Infect. Immun. 71: 7053-7060 [Abstract] [Full Text]  
  • Rittig, M. G., Kaufmann, A., Robins, A., Shaw, B., Sprenger, H., Gemsa, D., Foulongne, V., Rouot, B., Dornand, J. (2003). Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J. Leukoc. Biol. 74: 1045-1055 [Abstract] [Full Text]  
  • Celli, J., de Chastellier, C., Franchini, D.-M., Pizarro-Cerda, J., Moreno, E., Gorvel, J.-P. (2003). Brucella Evades Macrophage Killing via VirB-dependent Sustained Interactions with the Endoplasmic Reticulum. JEM 198: 545-556 [Abstract] [Full Text]  
  • Eto, K., Yamashita, T., Hirose, K., Tsubamoto, Y., Ainscow, E. K., Rutter, G. A., Kimura, S., Noda, M., Iino, M., Kadowaki, T. (2003). Glucose metabolism and glutamate analog acutely alkalinize pH of insulin secretory vesicles of pancreatic {beta}-cells. Am. J. Physiol. Endocrinol. Metab. 285: E262-E271 [Abstract] [Full Text]  
  • Kim, S., Watarai, M., Kondo, Y., Erdenebaatar, J., Makino, S.-i., Shirahata, T. (2003). Isolation and Characterization of Mini-Tn5Km2 Insertion Mutants of Brucella abortus Deficient in Internalization and Intracellular Growth in HeLa Cells. Infect. Immun. 71: 3020-3027 [Abstract] [Full Text]  
  • Gross, A., Bouaboula, M., Casellas, P., Liautard, J.-P., Dornand, J. (2003). Subversion and Utilization of the Host Cell Cyclic Adenosine 5'-Monophosphate/Protein Kinase A Pathway by Brucella During Macrophage Infection. J. Immunol. 170: 5607-5614 [Abstract] [Full Text]  
  • Rouot, B., Alvarez-Martinez, M.-T., Marius, C., Menanteau, P., Guilloteau, L., Boigegrain, R.-A., Zumbihl, R., O'Callaghan, D., Domke, N., Baron, C. (2003). Production of the Type IV Secretion System Differs among Brucella Species as Revealed with VirB5- and VirB8-Specific Antisera. Infect. Immun. 71: 1075-1082 [Abstract] [Full Text]  
  • Porte, F., Naroeni, A., Ouahrani-Bettache, S., Liautard, J.-P. (2003). Role of the Brucella suis Lipopolysaccharide O Antigen in Phagosomal Genesis and in Inhibition of Phagosome-Lysosome Fusion in Murine Macrophages. Infect. Immun. 71: 1481-1490 [Abstract] [Full Text]  
  • Ko, J., Splitter, G. A. (2003). Molecular Host-Pathogen Interaction in Brucellosis: Current Understanding and Future Approaches to Vaccine Development for Mice and Humans. Clin. Microbiol. Rev. 16: 65-78 [Abstract] [Full Text]  
  • Kohler, S., Foulongne, V., Ouahrani-Bettache, S., Bourg, G., Teyssier, J., Ramuz, M., Liautard, J.-P. (2002). The analysis of the intramacrophagic virulome of Brucella suis deciphers the environment encountered by the pathogen inside the macrophage host cell. Proc. Natl. Acad. Sci. USA 99: 15711-15716 [Abstract] [Full Text]  
  • Tibor, A., Wansard, V., Bielartz, V., Delrue, R.-M., Danese, I., Michel, P., Walravens, K., Godfroid, J., Letesson, J.-J. (2002). Effect of omp10 or omp19 Deletion on Brucella abortus Outer Membrane Properties and Virulence in Mice. Infect. Immun. 70: 5540-5546 [Abstract] [Full Text]  
  • Paulsen, I. T., Seshadri, R., Nelson, K. E., Eisen, J. A., Heidelberg, J. F., Read, T. D., Dodson, R. J., Umayam, L., Brinkac, L. M., Beanan, M. J., Daugherty, S. C., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Nelson, W. C., Ayodeji, B., Kraul, M., Shetty, J., Malek, J., Van Aken, S. E., Riedmuller, S., Tettelin, H., Gill, S. R., White, O., Salzberg, S. L., Hoover, D. L., Lindler, L. E., Halling, S. M., Boyle, S. M., Fraser, C. M. (2002). The Brucellasuis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 99: 13148-13153 [Abstract] [Full Text]  
  • Sun, Y.-H., den Hartigh, A. B., Santos, R. d. L., Adams, L. G., Tsolis, R. M. (2002). virB-Mediated Survival of Brucella abortus in Mice and Macrophages Is Independent of a Functional Inducible Nitric Oxide Synthase or NADPH Oxidase in Macrophages. Infect. Immun. 70: 4826-4832 [Abstract] [Full Text]  
  • Watarai, M., Makino, S.-i., Shirahata, T. (2002). An essential virulence protein of Brucella abortus, VirB4, requires an intact nucleoside-triphosphate-binding domain. Microbiology 148: 1439-1446 [Abstract] [Full Text]  
  • Naroeni, A., Porte, F. (2002). Role of Cholesterol and the Ganglioside GM1 in Entry and Short-Term Survival of Brucella suis in Murine Macrophages. Infect. Immun. 70: 1640-1644 [Abstract] [Full Text]  
  • Almiron, M., Martinez, M., Sanjuan, N., Ugalde, R. A. (2001). Ferrochelatase Is Present in Brucella abortus and Is Critical for Its Intracellular Survival and Virulence. Infect. Immun. 69: 6225-6230 [Abstract] [Full Text]  
  • Rittig, M. G., Alvarez-Martinez, M.-T., Porte, F., Liautard, J.-P., Rouot, B. (2001). Intracellular Survival of Brucella spp. in Human Monocytes Involves Conventional Uptake but Special Phagosomes. Infect. Immun. 69: 3995-4006 [Abstract] [Full Text]  
  • Endley, S., McMurray, D., Ficht, T. A. (2001). Interruption of the cydB Locus in Brucella abortus Attenuates Intracellular Survival and Virulence in the Mouse Model of Infection. J. Bacteriol. 183: 2454-2462 [Abstract] [Full Text]  
  • Naroeni, A., Jouy, N., Ouahrani-Bettache, S., Liautard, J.-P., Porte, F. (2001). Brucella suis-Impaired Specific Recognition of Phagosomes by Lysosomes due to Phagosomal Membrane Modifications. Infect. Immun. 69: 486-493 [Abstract] [Full Text]  
  • Luhrmann, A., Streker, K., Schuttfort, A., Daniels, J. J. D., Haas, A. (2001). Afipia felis induces uptake by macrophages directly into a nonendocytic compartment. Proc. Natl. Acad. Sci. USA 98: 7271-7276 [Abstract] [Full Text]