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 Van Kirk, L. S.
Right arrow Articles by Heinzen, R. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Van Kirk, L. S.
Right arrow Articles by Heinzen, R. A.

 Previous Article  |  Next Article 

Infection and Immunity, August 2000, p. 4706-4713, Vol. 68, No. 8
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Ultrastructure of Rickettsia rickettsii Actin Tails and Localization of Cytoskeletal Proteins

Levi S. Van Kirk,1 Stanley F. Hayes,2 and Robert A. Heinzen1,*

Department of Molecular Biology, University of Wyoming, Laramie, Wyoming 82071-3944,1 and Microscopy Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, Hamilton, Montana 598402

Received 19 January 2000/Returned for modification 17 March 2000/Accepted 8 May 2000

Actin-based motility (ABM) is a mechanism for intercellular spread that is utilized by vaccinia virus and the invasive bacteria within the genera Rickettsia, Listeria, and Shigella. Within the Rickettsia, ABM is confined to members of the spotted fever group (SFG), such as Rickettsia rickettsii, the agent of Rocky Mountain spotted fever. Infection by each agent induces the polymerization of host cell actin to form the typical F (filamentous)-actin comet tail. Assembly of the actin tail propels the pathogen through the host cytosol and into cell membrane protrusions that can be engulfed by neighboring cells, initiating a new infectious cycle. Little is known about the structure and morphogenesis of the Rickettsia rickettsii actin tail relative to Shigella and Listeria actin tails. In this study we examined the ultrastructure of the rickettsial actin tail by confocal, scanning electron, and transmission electron microscopy. Confocal microscopy of rhodamine phalloidin-stained infected Vero cells revealed the typhus group rickettsiae, Rickettsia prowazekii and Rickettsia typhi, to have no actin tails and short (~1- to 3-µm) straight or hooked actin tails, respectively. The SFG rickettsia, R. rickettsii, displayed long actin tails (>10 µm) that were frequently comprised of multiple, distinct actin bundles, wrapping around each other in a helical fashion. Transmission electron microscopy, in conjunction with myosin S1 subfragment decoration, revealed that the individual actin filaments of R. rickettsii tails are >1 µm long, arranged roughly parallel to one another, and oriented with the fast-growing barbed end towards the rickettsial pole. Scanning electron microscopy of intracellular rickettsiae demonstrated R. rickettsii to have polar associations of cytoskeletal material and R. prowazekii to be devoid of cytoskeletal interactions. By indirect immunofluorescence, both R. rickettsii and Listeria monocytogenes actin tails were shown to contain the cytoskeletal proteins vasodilator-stimulated phosphoprotein profilin, vinculin, and filamin. However, rickettsial tails lacked ezrin, paxillin, and tropomyosin, proteins that were associated with actin tails of cytosolic or protrusion-bound Listeria. The unique ultrastructural and compositional characteristics of the R. rickettsii actin tail suggest that rickettsial ABM is mechanistically different from previously described microbial ABM systems.

* Corresponding author. Mailing address: Department of Molecular Biology, University of Wyoming, Laramie, WY 82071-3944. Phone: (307) 766-5458. Fax: (307) 766-3875. E-mail: rheinzen{at}uwyo.edu.

Infection and Immunity, August 2000, p. 4706-4713, Vol. 68, No. 8
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Shenoy, V. B., Tambe, D. T., Prasad, A., Theriot, J. A. (2007). A kinematic description of the trajectories of Listeria monocytogenes propelled by actin comet tails. Proc. Natl. Acad. Sci. USA 104: 8229-8234 [Abstract] [Full Text]  
  • VALBUENA, G., WALKER, D. H. (2004). EFFECT OF BLOCKING THE CXCL9/10-CXCR3 CHEMOKINE SYSTEM IN THE OUTCOME OF ENDOTHELIAL-TARGET RICKETTSIAL INFECTIONS. Am J Trop Med Hyg 71: 393-399 [Abstract] [Full Text]  
  • McLeod, M. P., Qin, X., Karpathy, S. E., Gioia, J., Highlander, S. K., Fox, G. E., McNeill, T. Z., Jiang, H., Muzny, D., Jacob, L. S., Hawes, A. C., Sodergren, E., Gill, R., Hume, J., Morgan, M., Fan, G., Amin, A. G., Gibbs, R. A., Hong, C., Yu, X.-j., Walker, D. H., Weinstock, G. M. (2004). Complete Genome Sequence of Rickettsia typhi and Comparison with Sequences of Other Rickettsiae. J. Bacteriol. 186: 5842-5855 [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]  
  • Stamm, L. M., Morisaki, J. H., Gao, L.-Y., Jeng, R. L., McDonald, K. L., Roth, R., Takeshita, S., Heuser, J., Welch, M. D., Brown, E. J. (2003). Mycobacterium marinum Escapes from Phagosomes and Is Propelled by Actin-based Motility. JEM 198: 1361-1368 [Abstract] [Full Text]  
  • Macaluso, K. R., Mulenga, A., Simser, J. A., Azad, A. F. (2003). Differential Expression of Genes in Uninfected and Rickettsia-Infected Dermacentor variabilis Ticks as Assessed by Differential-Display PCR. Infect. Immun. 71: 6165-6170 [Abstract] [Full Text]  
  • Valbuena, G., Bradford, W., Walker, D. H. (2003). Expression Analysis of the T-Cell-Targeting Chemokines CXCL9 and CXCL10 in Mice and Humans with Endothelial Infections Caused by Rickettsiae of the Spotted Fever Group. Am. J. Pathol. 163: 1357-1369 [Abstract] [Full Text]  
  • Fehrenbacher, K., Huckaba, T., Yang, H.-C., Boldogh, I., Pon, L. (2003). Actin comet tails, endosomes and endosymbionts. J. Exp. Biol. 206: 1977-1984 [Abstract] [Full Text]  
  • Harlander, R. S., Way, M., Ren, Q., Howe, D., Grieshaber, S. S., Heinzen, R. A. (2003). Effects of Ectopically Expressed Neuronal Wiskott-Aldrich Syndrome Protein Domains on Rickettsia rickettsii Actin-Based Motility. Infect. Immun. 71: 1551-1556 [Abstract] [Full Text]  
  • Simser, J. A., Palmer, A. T., Fingerle, V., Wilske, B., Kurtti, T. J., Munderloh, U. G. (2002). Rickettsia monacensis sp. nov., a Spotted Fever Group Rickettsia, from Ticks (Ixodes ricinus) Collected in a European City Park. Appl. Environ. Microbiol. 68: 4559-4566 [Abstract] [Full Text]  
  • Radulovic, S., Price, P. W., Beier, M. S., Gaywee, J., Macaluso, J. A., Azad, A. (2002). Rickettsia-Macrophage Interactions: Host Cell Responses to Rickettsia akari and Rickettsia typhi. Infect. Immun. 70: 2576-2582 [Abstract] [Full Text]  
  • Goldberg, M. B. (2001). Actin-Based Motility of Intracellular Microbial Pathogens. Microbiol. Mol. Biol. Rev. 65: 595-626 [Abstract] [Full Text]  
  • Suzuki, T., Sasakawa, C. (2001). Molecular Basis of the Intracellular Spreading of Shigella. Infect. Immun. 69: 5959-5966 [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»