Previous Article | Next Article 
Infection and Immunity, December 1999, p. 6518-6525, Vol. 67, No. 12
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Microtubules Are Associated with Intracellular Movement and
Spread of the Periodontopathogen Actinobacillus
actinomycetemcomitans
Diane Hutchins
Meyer,
John E.
Rose,
Joan E.
Lippmann, and
Paula M.
Fives-Taylor*
Department of Microbiology and Molecular
Genetics, College of Medicine and College of Agricultural and Life
Sciences, University of Vermont, Burlington, Vermont 05405
Received 21 June 1999/Returned for modification 9 August
1999/Accepted 9 September 1999
Actinobacillus actinomycetemcomitans SUNY 465, the
invasion prototype strain, enters epithelial cells by an
actin-dependent mechanism, escapes from the host cell vacuole, and
spreads intracellularly and to adjacent epithelial cells via
intercellular protrusions. Internalized organisms also egress from host
cells into the assay medium via protrusions that are associated with
just a single epithelial cell. Here we demonstrate that agents which
inhibit microtubule polymerization (e.g., colchicine) and those which stabilize polymerized microtubules (e.g., taxol) both increase markedly
the number of intracellular A. actinomycetemcomitans organisms. Furthermore, both colchicine and taxol prevented the egression of A. actinomycetemcomitans from host cells into
the assay medium. Immunofluorescence microscopy revealed that
protrusions that mediate the bacterial spread contain microtubules.
A. actinomycetemcomitans SUNY 465 and 652, strains that are
both invasive and egressive, interacted specifically with the plus ends
(growing ends) of the filaments of microtubule asters in a KB cell
extract. By contrast, neither A. actinomycetemcomitans 523, a strain that is invasive but not egressive, nor Haemophilus
aphrophilus, a noninvasive oral bacterium with characteristics
similar to those of A. actinomycetemcomitans, bound to
microtubules. Together these data suggest that microtubules function in
the spread and movement of A. actinomycetemcomitans and
provide the first evidence that host cell dispersion of an invasive
bacterium may involve the usurption of host cell microtubules.
*
Corresponding author. Mailing address: Stafford Hall,
Department of Microbiology and Molecular Genetics, University of
Vermont, Burlington VT 05405. Phone: (802) 656-1121. Fax: (802)
656-8749. E-mail: pfivesta{at}zoo.uvm.edu.
Infection and Immunity, December 1999, p. 6518-6525, Vol. 67, No. 12
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Handfield, M., Baker, H.V., Lamont, R.J.
(2008). Beyond Good and Evil in the Oral Cavity: Insights into Host-Microbe Relationships Derived from Transcriptional Profiling of Gingival Cells. JDR
87: 203-223
[Abstract]
[Full Text]
-
Lavine, M. D., Arrizabalaga, G.
(2008). Exit from Host Cells by the Pathogenic Parasite Toxoplasma gondii Does Not Require Motility. Eukaryot Cell
7: 131-140
[Abstract]
[Full Text]
-
Inagaki, S., Onishi, S., Kuramitsu, H. K., Sharma, A.
(2006). Porphyromonas gingivalis Vesicles Enhance Attachment, and the Leucine-Rich Repeat BspA Protein Is Required for Invasion of Epithelial Cells by "Tannerella forsythia". Infect. Immun.
74: 5023-5028
[Abstract]
[Full Text]
-
Yilmaz, O., Verbeke, P., Lamont, R. J., Ojcius, D. M.
(2006). Intercellular Spreading of Porphyromonas gingivalis Infection in Primary Gingival Epithelial Cells. Infect. Immun.
74: 703-710
[Abstract]
[Full Text]
-
Richardson, J., Craighead, J. C., Cao, S. L., Handfield, M.
(2005). Concurrence between the gene expression pattern of Actinobacillus actinomycetemcomitans in localized aggressive periodontitis and in human epithelial cells. J Med Microbiol
54: 497-504
[Abstract]
[Full Text]
-
Kozarov, E. V., Dorn, B. R., Shelburne, C. E., Dunn, W. A. Jr, Progulske-Fox, A.
(2005). Human Atherosclerotic Plaque Contains Viable Invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler. Thromb. Vasc. Bio.
25: e17-e18
[Full Text]
-
Matsuyama, T., Kawai, T., Izumi, Y., Taubman, M. A
(2005). Expression of Major Histocompatibility Complex Class II and CD80 by Gingival Epithelial Cells Induces Activation of CD4+ T Cells in Response to Bacterial Challenge. Infect. Immun.
73: 1044-1051
[Abstract]
[Full Text]
-
Rudney, J.D., Chen, R., Sedgewick, G.J.
(2005). Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are Components of a Polymicrobial Intracellular Flora within Human Buccal Cells. JDR
84: 59-63
[Abstract]
[Full Text]
-
Guignot, J., Caron, E., Beuzon, C., Bucci, C., Kagan, J., Roy, C., Holden, D. W.
(2004). Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J. Cell Sci.
117: 1033-1045
[Abstract]
[Full Text]
-
HENDERSON, B., WILSON, M., SHARP, L., WARD, J. M.
(2002). Actinobacillus actinomycetemcomitans. J Med Microbiol
51: 1013-1020
[Full Text]
-
Henderson, B.
(2002). Oral bacterial disease and the science of cellular conversation. JRSM
95: 77-80
[Full Text]
-
Rudney, J. D., Chen, R., Sedgewick, G. J.
(2001). Intracellular Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in Buccal Epithelial Cells Collected from Human Subjects. Infect. Immun.
69: 2700-2707
[Abstract]
[Full Text]
-
Kim, S.-W., Ihn, K.-S., Han, S.-H., Seong, S.-Y., Kim, I.-S., Choi, M.-S.
(2001). Microtubule- and Dynein-Mediated Movement of Orientia tsutsugamushi to the Microtubule Organizing Center. Infect. Immun.
69: 494-500
[Abstract]
[Full Text]
-
Kespichayawattana, W., Rattanachetkul, S., Wanun, T., Utaisincharoen, P., Sirisinha, S.
(2000). Burkholderia pseudomallei Induces Cell Fusion and Actin-Associated Membrane Protrusion: a Possible Mechanism for Cell-to-Cell Spreading. Infect. Immun.
68: 5377-5384
[Abstract]
[Full Text]
-
Guzman-Verri, C., Chaves-Olarte, E., von Eichel-Streiber, C., Lopez-Goni, I., Thelestam, M., Arvidson, S., Gorvel, J.-P., Moreno, E.
(2001). GTPases of the Rho Subfamily Are Required for Brucella abortus Internalization in Nonprofessional Phagocytes. DIRECT ACTIVATION OF Cdc42. J. Biol. Chem.
276: 44435-44443
[Abstract]
[Full Text]