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Cytoskeletal changes in Eimeria bovis-infected host endothelial cells during first merogony

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Abstract

The first merogony of Eimeria bovis takes place in lymphatic endothelial cells of the ileum, resulting in the formation of macromeronts up to 250 μm. In this study, we investigated the host cell cytoskeleton (actin filaments, microtubules, spectrin, vimentin intermediate filaments) associated with parasitic development in vitro by confocal laser scanning microscopy (CLSM) using primary bovine umbilical vein endothelial cells (BUVEC) and bovine spleen lymphatic endothelial cells (BSLEC) as host cells. No prominent changes in the host cell cytoskeleton were detected 1–3 days after E. bovis sporozoite invasion. With ongoing meront maturation a significant increase in microtubules and actin filaments close to the parasitophorous vacuole (PV) was found. Mature macromeronts within the PV were completely enclosed by these cytoskeletal elements. Our findings suggest, that in order to guarantee the survival of the host cell on the enlargement of macromeronts, E. bovis needs not only to augment but also to rearrange its cytoskeletal system.

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Abbreviations

BSA:

bovine serum albumin

BSLEC:

bovine spleen lymphatic endothelial cells

BUVEC:

bovine umbilical vein endothelial cells

CLSM:

confocal laser scanning microscopy

DMSO:

dimethylsulphoxide

ECGM:

endothelial cell growth medium

FCS:

foetal calf serum

PBS:

phosphate-buffered saline

p. i.:

post-infection

PV:

parasitophorous vacuole

RT:

room temperature

References

  • Andrade, E.F., Stumbo, A.C., Monteiro-Leal, L.H., Carvalho, L. and Barbosa, H.S., 2001. Do microtubules around the Toxoplasma gondii-containing parasitophorous vacuole in skeletal muscle cells form a barrier for the phagolysosomal fusion?, Journal of Submicroscopic Cytology and Pathology, 33(3), 337–341

    PubMed  CAS  Google Scholar 

  • Bart, B.J. and Lussky, R.C., 2005. Bart syndrome with associated anomalies, American Journal of Perinatology, 22(2), 365–369

    Article  PubMed  Google Scholar 

  • Bennett, V., 1985. The membrane skeleton of human erythrocytes and its implication for more complex cells, Annual Review of Biochemistry, 54, 273–304

    Article  PubMed  CAS  Google Scholar 

  • Bonnet, C., Boucher, D., Lazereg, S., Pedrotii, B., Islam, K., Denoulet, P. and Larcher, J.C., 2001. Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation, Journal of Biological Chemistry, 276, 12839–12848

    Article  PubMed  CAS  Google Scholar 

  • Coppens, I., Dunn, J.D., Romano, J.D., Pypaert, M., Zhang, H., Boothroyd, J.C. and Joiner, K.A., 2006. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space, Cell, 125, 261–274.

    Article  PubMed  CAS  Google Scholar 

  • Daugschies, A. and Najdrowski, M., 2005. Eimeriosis in cattle: current understanding, Journal of Veterinary Medicine, 52, 417–427

    Article  PubMed  CAS  Google Scholar 

  • Deng, M., Lancto, C.A. and Abrahamsen, M.S., 2004. Cryptosporidium parvum regulation of human epithelial cell expression, International Journal of Parasitology, 34, 73–82

    Article  PubMed  CAS  Google Scholar 

  • Downing, K.H. and Nogales, E., 1998a. Tubulin and microtubule structure, Current Opinion in Cell Biology, 10, 16–22

    Article  PubMed  CAS  Google Scholar 

  • Downing, K.H. and Nogales, E., 1998b. Tubulin structure: insights into microtubule properties and functions, Current Opinion in Structural Biology, 8, 785–791

    Article  PubMed  CAS  Google Scholar 

  • Elliot, D.A. and Clark, D.P., 2000. Cryptosporidium parvum induces host cell actin accumulation at the host-parasite interface, Infection and Immunity, 68, 2315–2322

    Article  Google Scholar 

  • Elliot, D.A., Coleman, D.J., Lane, M.A., May, R.C., Machesky, L.M. and Clark, D.P., 2001. Cryptosporidium parvum infection requires host cell actin polymerization, Infection and Immunity, 69, 5940–5942

    Article  Google Scholar 

  • Faber, J.E., Kollmann, D., Heise, A., Bauer, C., Failing, K., Bürger, H.J. and Zahner, H., 2002. Eimeria infections in cows in the periparturient phase and their calves: oocyst excretion and levels of specific serum and colostrum antibodies, Veterinary Parasitology, 104(1), 1–17

    Article  PubMed  CAS  Google Scholar 

  • Feng, H., Nie, W., Bonilla, R., Widmer, G., Sheoran, A. and Tzipori, S., 2006. Quantitative tracking of Cryptosporidium infection in cell culture, Journal of Parasitology, 92, 1350–1354

    Article  PubMed  Google Scholar 

  • Fiege, N., Klatte, D., Kollmann, D., Zahner, H. and Bürger, H.J., 1992. Eimeria bovis in cattle: colostral transfer of antibodies and immune response to experimental infections, Parasitology Research, 78, 32–38

    Article  PubMed  CAS  Google Scholar 

  • Forney, J.R., DeWall, D.B.,Yang, S., Speer, C.A. and Healy, M.C., 1999. A role for host phoshoinositide 3-kinase and cytoskeletal remodelling during Cryptosporidium parvum infection, Infection and Immunity, 67, 844–852

    PubMed  CAS  Google Scholar 

  • Ghazali, M., Rodier, M.H., el Moudni, B.E., Babin, P., Fernandez, B. and Jacquemin, J.L., 1995. Detection and immunolocalization of human erythrocyte spectrin immunoanalogues in Toxoplasma gondii (Protozoan, Parasite), Journal of Eukaryotic Microbiology, 42, 427–433

    Article  PubMed  CAS  Google Scholar 

  • Halonen, S.K. and Weidner, E., 1994. Overcoating of Toxoplasma parasitophorous vacuoles with host cell vimentin type intermediate filaments, Journal of Eukaryotic Microbiology, 41, 65–71

    Article  PubMed  CAS  Google Scholar 

  • Halonen, S.K., Weiss, L.M. and Chiu, F.C., 1998. Association of host cell intermediate filaments with Toxoplasma gondii cysts in murine astrocytes in vitro, International Journal of Parasitology, 28, 815–823

    Article  PubMed  CAS  Google Scholar 

  • Hammond, D.M., Davis, L.R. and Bowmann, L., 1964. Experimental infections with Eimeria bovis in calves, American Journal of Veterinary Research, 5, 303–311

    Google Scholar 

  • Hammond, D.M. and Fayer, R., 1968. Cultivation of Eimeria bovis in three established cell lines and bovine tracheal cell line culture, Journal of Parasitolology, 54, 559–568

    Article  Google Scholar 

  • Hermosilla, C., Barbisch, B., Heise, A., Kowalik, S. and Zahner, H., 2002. Development of Eimeria bovis in vitro: suitability of several bovine, human and porcine endothelial cell lines, bovine gastrointestinal, Madin-Darby bovine kidney (MDBK) and African green monkey kidney (VERO) cells, Parasitology Research, 88, 301–307

    Article  PubMed  CAS  Google Scholar 

  • Hermosilla, C., Zahner, H. and Taubert, A., 2006. Eimeria bovis modulates adhesion molecule gene transcription in and PMN adhesion to infected bovine endothelial cells, International Journal of Parasitology, 36, 423–431

    Article  PubMed  CAS  Google Scholar 

  • Janmey, P.A., 1991. Mechanical properties of cytoskeletal polymers, Current Opinion in Cell Biology, 3, 4–11

    Article  PubMed  CAS  Google Scholar 

  • Kelly, R., 1990. Microtubules, membrane traffic and cell organization, Cell, 61, 5–7

    Article  PubMed  CAS  Google Scholar 

  • Kreis, T.E., 1990. Role of microtubules in the organization of the Golgi apparatus, Cell Motility and the Cytoskeleton, 15, 67–70

    Article  PubMed  CAS  Google Scholar 

  • Kreitzer, G., Liao, G. and Gundersen, G.G., 1999. Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism, Molecular Biology of the Cell, 10, 1105–1118

    PubMed  CAS  Google Scholar 

  • Lingelbach, K. and Joiner, K.A., 1998. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells, Journal of Cell Science, 111, 1447–1475

    Google Scholar 

  • Matthews, G. and Allen, M., 2005. Epidermolysis bullosa in cattle in the UK, Veterinary Record, 157, 456

    PubMed  Google Scholar 

  • Melo, E.J., Carvalho, T.M. and De Souza, W., 2001. Behavior of microtubules in cells infected with Toxoplasma gondii, Biocell, 25(1), 53–59

    PubMed  CAS  Google Scholar 

  • Morisaki, J.H., Heuser, J.E. and Sibley, L.D., 1995. Invasion of Toxoplasma gondii occurs by active penetration of the host cell, Journal of Cell Science, 108, 2457–2464

    PubMed  CAS  Google Scholar 

  • Morrissette, N.S., Mitra, A., Sept, D. and Sibley, L.D., 2004. Dinitroanilines bind a-tubulin to disrupt microtubules, Molecular Biology of the Cell, 15, 1960–1968

    Article  PubMed  CAS  Google Scholar 

  • Reduker, D.W. and Speer, C.A., 1986. Antigens of in-vitro produced first generation merozoites of Eimeria bovis (Apicomplexa), Journal of Parasitology, 72, 782–785

    Article  PubMed  CAS  Google Scholar 

  • Sibley, L.D., 2003. Toxoplasma gondii: perfecting an intracellular life style, Traffic, 4(9), 581–586

    Article  PubMed  CAS  Google Scholar 

  • Speer, C.A., Reduker, D.W., Burgess, D.E., Whitmire, W.M. and Splitter, G.A., 1985. Lymphokine-induced inhibition of Eimeria bovis and Eimeria papillata (Apicomplexa) in cultured bovine monocytes, Infection and Immunity, 50, 566–571

    PubMed  CAS  Google Scholar 

  • Steinert, P.M. and Roop, D.R., 1988. Molecular and cellular biology of intermediate filaments, Annual Review of Biochemistry, 57, 593–625

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We acknowledge the kind supply of BSLEC by K. Preissner (Justus Liebig University Giessen) and of bovine umbilical cords by H. Bollwein and A. Koch (University of Veterinary Medicine Hannover). We are indebted to B. Hofmann, C. Scheld and M. Buss for their excellent technical assistance in cell culture. Further, we are grateful to K. Failing (Justus Liebig University Giessen) for support in statistical analyses of the data.

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  1. Carlos Hermosilla

    Present address: Department of Pathology and Infectious Diseases, Royal Veterinary College, Herts, AL9 7TA, UK

Authors and Affiliations

  1. Institute of Parasitology, Justus Liebig University Giessen, Rudolf-Buchhheim-Str. 2, 35392, Giessen, Germany

    Carlos Hermosilla, Michael Stowasser, Jan Hillern Behrendt & Horst Zahner

  2. Institute of Animal Physiology, Justus Liebig University Giessen, Giessen, Germany

    Elmar Schröpfer & Ursula Eckstein-Ludwig

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  1. Carlos Hermosilla
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  2. Elmar Schröpfer
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Correspondence to Carlos Hermosilla.

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Hermosilla, C., Schröpfer, E., Stowasser, M. et al. Cytoskeletal changes in Eimeria bovis-infected host endothelial cells during first merogony. Vet Res Commun 32, 521–531 (2008). https://doi.org/10.1007/s11259-008-9054-x

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  • DOI: https://doi.org/10.1007/s11259-008-9054-x

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