Previous Article | Next Article 
Infection and Immunity, September 1999, p. 4427-4434, Vol. 67, No. 9
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Intracellular Growth in Acanthamoeba
castellanii Affects Monocyte Entry Mechanisms and Enhances
Virulence of Legionella pneumophila
Jeffrey D.
Cirillo,1,*
Suat L. G.
Cirillo,1
Ling
Yan,1
Luiz E.
Bermudez,2
Stanley
Falkow,3 and
Lucy S.
Tompkins3
Department of Veterinary and Biomedical
Sciences, University of Nebraska, Lincoln, Lincoln, Nebraska
685831; Department of Microbiology and
Immunology, Stanford University School of Medicine, Stanford,
California 943053; and Kuzell Institute
for Arthritis and Infectious Diseases, California Pacific Medical
Center, San Francisco, California 941152
Received 17 March 1999/Returned for modification 6 May
1999/Accepted 3 June 1999
Since Legionella pneumophila is an intracellular
pathogen, entry into and replication within host cells are thought to
be critical to its ability to cause disease. L. pneumophila
grown in one of its environmental hosts, Acanthamoeba
castellanii, is phenotypically different from L. pneumophila grown on standard laboratory medium (BCYE agar).
Although amoeba-grown L. pneumophila displays enhanced
entry into monocytes compared to BCYE-grown bacteria, the mechanisms of
entry used and the effects on virulence have not been examined. To
explore whether amoeba-grown L. pneumophila differs from
BCYE-grown L. pneumophila in these characteristics, we
examined entry into monocytes, replication in activated macrophages, and virulence in mice. Entry of amoeba-grown L. pneumophila
into monocytes occurred more frequently by coiling phagocytosis, was less affected by complement opsonization, and was less sensitive to
microtubule and microfilament inhibitors than was entry of BCYE-grown
bacteria. In addition, amoeba-grown L. pneumophila displays
increased replication in monocytes and is more virulent in A/J, C57BL/6
Beige, and C57BL/6 mice. These data demonstrate for the first time that
the intra-amoebal growth environment affects the entry mechanisms and
virulence of L. pneumophila.
*
Corresponding author. Mailing address: Department of
Veterinary and Biomedical Sciences, University of Nebraska, Lincoln, 203 VBS, Fair and East Campus Loop, Lincoln, NE 68583. Phone: (402)
472-8587. Fax: (402) 472-9690. E-mail: jcirillo1{at}unl.edu.
Infection and Immunity, September 1999, p. 4427-4434, Vol. 67, No. 9
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Aurass, P., Pless, B., Rydzewski, K., Holland, G., Bannert, N., Flieger, A.
(2009). bdhA-patD Operon as a Virulence Determinant, Revealed by a Novel Large-Scale Approach for Identification of Legionella pneumophila Mutants Defective for Amoeba Infection. Appl. Environ. Microbiol.
75: 4506-4515
[Abstract]
[Full Text]
-
Cirillo, S. L. G., Subbian, S., Chen, B., Weisbrod, T. R., Jacobs, W. R. Jr., Cirillo, J. D.
(2009). Protection of Mycobacterium tuberculosis from Reactive Oxygen Species Conferred by the mel2 Locus Impacts Persistence and Dissemination. Infect. Immun.
77: 2557-2567
[Abstract]
[Full Text]
-
Bleasdale, B., Lott, P. J., Jagannathan, A., Stevens, M. P., Birtles, R. J., Wigley, P.
(2009). The Salmonella Pathogenicity Island 2-Encoded Type III Secretion System Is Essential for the Survival of Salmonella enterica Serovar Typhimurium in Free-Living Amoebae. Appl. Environ. Microbiol.
75: 1793-1795
[Abstract]
[Full Text]
-
Vaerewijck, M. J. M., Sabbe, K., Bare, J., Houf, K.
(2008). Microscopic and Molecular Studies of the Diversity of Free-Living Protozoa in Meat-Cutting Plants. Appl. Environ. Microbiol.
74: 5741-5749
[Abstract]
[Full Text]
-
Park, B., Subbian, S., El-Etr, S. H., Cirillo, S. L. G., Cirillo, J. D.
(2008). Use of Gene Dosage Effects for a Whole-Genome Screen To Identify Mycobacterium marinum Macrophage Infection Loci. Infect. Immun.
76: 3100-3115
[Abstract]
[Full Text]
-
Danelishvili, L., Wu, M., Stang, B., Harriff, M., Cirillo, S., Cirillo, J., Bildfell, R., Arbogast, B., Bermudez, L. E.
(2007). Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection. Proc. Natl. Acad. Sci. USA
104: 11038-11043
[Abstract]
[Full Text]
-
Bandyopadhyay, P., Liu, S., Gabbai, C. B., Venitelli, Z., Steinman, H. M.
(2007). Environmental Mimics and the Lvh Type IVA Secretion System Contribute to Virulence-Related Phenotypes of Legionella pneumophila. Infect. Immun.
75: 723-735
[Abstract]
[Full Text]
-
Inglis, T. J. J., Sagripanti, J.-L.
(2006). Environmental Factors That Affect the Survival and Persistence of Burkholderia pseudomallei. Appl. Environ. Microbiol.
72: 6865-6875
[Full Text]
-
Chang, B., Kura, F., Amemura-Maekawa, J., Koizumi, N., Watanabe, H.
(2005). Identification of a Novel Adhesion Molecule Involved in the Virulence of Legionella pneumophila. Infect. Immun.
73: 4272-4280
[Abstract]
[Full Text]
-
Shadrach, W. S., Rydzewski, K., Laube, U., Holland, G., Ozel, M., Kiderlen, A. F., Flieger, A.
(2005). Balamuthia mandrillaris, Free-Living Ameba and Opportunistic Agent of Encephalitis, Is a Potential Host for Legionella pneumophila Bacteria. Appl. Environ. Microbiol.
71: 2244-2249
[Abstract]
[Full Text]
-
Zhang, H., Gomez-Garcia, M. R., Brown, M. R. W., Kornberg, A.
(2005). Inorganic polyphosphate in Dictyostelium discoideum: Influence on development, sporulation, and predation. Proc. Natl. Acad. Sci. USA
102: 2731-2735
[Abstract]
[Full Text]
-
Dessi, D., Delogu, G., Emonte, E., Catania, M. R., Fiori, P. L., Rappelli, P.
(2005). Long-Term Survival and Intracellular Replication of Mycoplasma hominis in Trichomonas vaginalis Cells: Potential Role of the Protozoon in Transmitting Bacterial Infection. Infect. Immun.
73: 1180-1186
[Abstract]
[Full Text]
-
Molmeret, M., Horn, M., Wagner, M., Santic, M., Abu Kwaik, Y.
(2005). Amoebae as Training Grounds for Intracellular Bacterial Pathogens. Appl. Environ. Microbiol.
71: 20-28
[Full Text]
-
Del Poeta, M.
(2004). Role of Phagocytosis in the Virulence of Cryptococcus neoformans. Eukaryot Cell
3: 1067-1075
[Full Text]
-
Bandyopadhyay, P., Xiao, H., Coleman, H. A., Price-Whelan, A., Steinman, H. M.
(2004). Icm/Dot-Independent Entry of Legionella pneumophila into Amoeba and Macrophage Hosts. Infect. Immun.
72: 4541-4551
[Abstract]
[Full Text]
-
Tezcan-Merdol, D., Ljungstrom, M., Winiecka-Krusnell, J., Linder, E., Engstrand, L., Rhen, M.
(2004). Uptake and Replication of Salmonella enterica in Acanthamoeba rhysodes. Appl. Environ. Microbiol.
70: 3706-3714
[Abstract]
[Full Text]
-
Yan, L., Cerny, R. L., Cirillo, J. D.
(2004). Evidence that hsp90 Is Involved in the Altered Interactions of Acanthamoeba castellanii Variants with Bacteria. Eukaryot Cell
3: 567-578
[Abstract]
[Full Text]
-
Scola, B. L., Birtles, R. J., Greub, G., Harrison, T. J., Ratcliff, R. M., Raoult, D.
(2004). Legionella drancourtii sp. nov., a strictly intracellular amoebal pathogen. Int. J. Syst. Evol. Microbiol.
54: 699-703
[Abstract]
[Full Text]
-
Greub, G., Raoult, D.
(2004). Microorganisms Resistant to Free-Living Amoebae. Clin. Microbiol. Rev.
17: 413-433
[Abstract]
[Full Text]
-
Welsh, C. T., Summersgill, J. T., Miller, R. D.
(2004). Increases in c-Jun N-Terminal Kinase/Stress-Activated Protein Kinase and p38 Activity in Monocyte-Derived Macrophages following the Uptake of Legionella pneumophila. Infect. Immun.
72: 1512-1518
[Abstract]
[Full Text]
-
Rossier, O., Starkenburg, S. R., Cianciotto, N. P.
(2004). Legionella pneumophila Type II Protein Secretion Promotes Virulence in the A/J Mouse Model of Legionnaires' Disease Pneumonia. Infect. Immun.
72: 310-321
[Abstract]
[Full Text]
-
Ridenour, D. A., Cirillo, S. L. G., Feng, S., Samrakandi, M. M., Cirillo, J. D.
(2003). Identification of a Gene That Affects the Efficiency of Host Cell Infection by Legionella pneumophila in a Temperature-Dependent Fashion. Infect. Immun.
71: 6256-6263
[Abstract]
[Full Text]
-
Greub, G., Mege, J.-L., Raoult, D.
(2003). Parachlamydia acanthamoeba Enters and Multiplies within Human Macrophages and Induces Their Apoptosis. Infect. Immun.
71: 5979-5985
[Abstract]
[Full Text]
-
Roig, J., Rello, J.
(2003). Legionnaires' disease: a rational approach to therapy. J Antimicrob Chemother
51: 1119-1129
[Abstract]
[Full Text]
-
Marciano-Cabral, F., Cabral, G.
(2003). Acanthamoeba spp. as Agents of Disease in Humans. Clin. Microbiol. Rev.
16: 273-307
[Abstract]
[Full Text]
-
Faulkner, G., Garduno, R. A.
(2002). Ultrastructural Analysis of Differentiation in Legionella pneumophila. J. Bacteriol.
184: 7025-7041
[Abstract]
[Full Text]
-
Garduno, R. A., Garduno, E., Hiltz, M., Hoffman, P. S.
(2002). Intracellular Growth of Legionella pneumophila Gives Rise to a Differentiated Form Dissimilar to Stationary-Phase Forms. Infect. Immun.
70: 6273-6283
[Abstract]
[Full Text]
-
Robey, M., Cianciotto, N. P.
(2002). Legionella pneumophila feoAB Promotes Ferrous Iron Uptake and Intracellular Infection. Infect. Immun.
70: 5659-5669
[Abstract]
[Full Text]
-
Schuster, F. L.
(2002). Cultivation of Pathogenic and Opportunistic Free-Living Amebas. Clin. Microbiol. Rev.
15: 342-354
[Abstract]
[Full Text]
-
Fields, B. S., Benson, R. F., Besser, R. E.
(2002). Legionella and Legionnaires' Disease: 25 Years of Investigation. Clin. Microbiol. Rev.
15: 506-526
[Abstract]
[Full Text]
-
Cirillo, S. L. G., Yan, L., Littman, M., Samrakandi, M. M., Cirillo, J. D.
(2002). Role of the Legionella pneumophila rtxA gene in amoebae. Microbiology
148: 1667-1677
[Abstract]
[Full Text]
-
Samrakandi, M. M., Cirillo, S. L. G., Ridenour, D. A., Bermudez, L. E., Cirillo, J. D.
(2002). Genetic and Phenotypic Differences between Legionella pneumophila Strains. J. Clin. Microbiol.
40: 1352-1362
[Abstract]
[Full Text]
-
Molmeret, M., Alli, O. A. T., Zink, S., Flieger, A., Cianciotto, N. P., Kwaik, Y. A.
(2002). icmT Is Essential for Pore Formation-Mediated Egress of Legionella pneumophila from Mammalian and Protozoan Cells. Infect. Immun.
70: 69-78
[Abstract]
[Full Text]
-
Brown, M. R. W., Smith, A. W.
(2001). Dormancy and persistence in chronic infection: role of the general stress response in resistance to chemotherapy. J Antimicrob Chemother
48: 141-142
[Full Text]
-
Robey, M., O'Connell, W., Cianciotto, N. P.
(2001). Identification of Legionella pneumophila rcp, a pagP-Like Gene That Confers Resistance to Cationic Antimicrobial Peptides and Promotes Intracellular Infection. Infect. Immun.
69: 4276-4286
[Abstract]
[Full Text]
-
Cirillo, S. L. G., Bermudez, L. E., El-Etr, S. H., Duhamel, G. E., Cirillo, J. D.
(2001). Legionella pneumophila Entry Gene rtxA Is Involved in Virulence. Infect. Immun.
69: 508-517
[Abstract]
[Full Text]
-
Bandyopadhyay, P., Steinman, H. M.
(2000). Catalase-Peroxidases of Legionella pneumophila: Cloning of the katA Gene and Studies of KatA Function. J. Bacteriol.
182: 6679-6686
[Abstract]
[Full Text]
-
Cirillo, S. L. G., Lum, J., Cirillo, J. D.
(2000). Identification of novel loci involved in entry by Legionella pneumophila. Microbiology
146: 1345-1359
[Abstract]
[Full Text]
-
Inglis, T. J. J., Rigby, P., Robertson, T. A., Dutton, N. S., Henderson, M., Chang, B. J.
(2000). Interaction between Burkholderia pseudomallei and Acanthamoeba Species Results in Coiling Phagocytosis, Endamebic Bacterial Survival, and Escape. Infect. Immun.
68: 1681-1686
[Abstract]
[Full Text]