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F-actin distribution and function during sexual development in Eimeria maxima

Published online by Cambridge University Press:  24 March 2015

SONJA FRÖLICH  and
MICHAEL WALLACH
SONJA FRÖLICH*
Affiliation:
The iThree Institute, School of Medical and Molecular Biosciences, University of Technology Sydney, PO Box 123, Broadway, Sydney, New South Wales 2007, Australia
MICHAEL WALLACH
Affiliation:
The iThree Institute, School of Medical and Molecular Biosciences, University of Technology Sydney, PO Box 123, Broadway, Sydney, New South Wales 2007, Australia
*
*Corresponding author. The iThree Institute, School of Medical and Molecular Biosciences, University of Technology Sydney, PO Box 123, Broadway, Sydney, New South Wales 2007, Australia. Tel: +61-2-9514-8283. Fax: +61-2-9514-4026. E-mail: [email protected]
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Summary

To determine the involvement of the actin cytoskeleton in macrogametocyte growth and oocyst wall formation, freshly purified macrogametocytes and oocysts were stained with Oregon Green 514 conjugated phalloidin to visualize F-actin microfilaments, while Evans blue staining was used to detect type 1 wall forming bodies (WFB1s) and the outer oocyst wall. The double-labelled parasites were then analysed at various stages of sexual development using three-dimensional confocal microscopy. The results showed F-actin filaments were distributed throughout the entire cytoplasm of mature Eimeria maxima macrogametocytes forming a web-like meshwork of actin filaments linking the type 1 WFBs together into structures resembling ‘beads on a string’. At the early stages of oocyst wall formation, F-actin localization changed in alignment with the egg-shaped morphology of the forming oocysts with F-actin microfilaments making direct contact with the WFB1s. In tissue oocysts, the labelled actin cytoskeleton was situated underneath the forming outer layer of the oocyst wall. Treatment of macrogametocytes in vitro with the actin depolymerizing agents, Cytochalasin D and Latrunculin, led to a reduction in the numbers of mature WFB1s in the cytoplasm of the developing macrogametocytes, indicating that the actin plays an important role in WFB1 transport and oocyst wall formation in E. maxima.

Keywords

actincytoskeletal inhibitorsWFB1 vesicle transportEimeria oocyst3D confocal microscopy
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 855 - 864
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Angrisano, F., Riglar, D. T., Sturm, A., Volz, J. C., Delves, M. J., Zuccala, E. S., Turnbull, L., Dekiwadia, C., Olshina, M. A., Marapana, D. S., Wong, W., Mollard, V., Bradin, C. H., Tonkin, C. J., Gunning, P. W., Ralph, S. A., Whitchurch, C. B., Sinden, R. E., Cowman, A. F., McFadden, G. I. and Baum, J. (2012). Spatial localisation of actin filaments across developmental stages of the malaria parasite. Plos ONE 7, e32188.Google Scholar
Belli, S. I., Lee, M., Thebo, P., Wallach, M. G., Schwartsburd, B. and Smith, N. C. (2002). Biochemical characterisation of the 56 and 82 kDa immunodominant gametocyte antigens from Eimeria maxima . International Journal for Parasitology 32, 805–816.Google Scholar
Belli, S. I., Wallach, M. G., Luxford, C., Davies, M. J. and Smith, N. C. (2003). Roles of tyrosine-rich precursor glycoproteins and dityrosine- and 3,4-dihydroxyphenylalanine-mediated protein cross-linking in development of the oocyst wall in the coccidian parasite Eimeria maxima . Eukaryotic Cell 2, 456–464.Google Scholar
Belli, S. I., Mai, K., Skene, C. D., Gleeson, M. T., Witcombe, D. M., Katrib, M., Finger, A., Wallach, M. G. and Smith, N. C. (2004). Characterisation of the antigenic and immunogenic properties of bacterially expressed, sexual stage antigens of the coccidian parasite, Eimeria maxima . Vaccine 22, 4316–4325.Google Scholar
Belli, S. I., Smith, N. C. and Ferguson, D. J. P. (2006). The coccidian oocyst: a tough nut to crack! Trends in Parasitology 22, 416–423.CrossRefGoogle ScholarPubMed
Belli, S. I., Ferguson, D. J. P., Katrib, M., Slapetova, I., Mai, K., Slapeta, J., Flowers, S. A., Miska, K. B., Tomley, F. M., Shirley, M. W., Wallach, M. G. and Smith, N. C. (2009). Conservation of proteins involved in oocyst wall formation in Eimeria maxima, Eimeria tenella and Eimeria acervulina . International Journal for Parasitology 39, 1063–1070.Google Scholar
Blake, D. P., Alias, H., Billington, K. J., Clark, E. L., Mat-Isa, M. N., Mohamad, A. F., Mohd-Amin, M. R., Tay, Y. L., Smith, A. L., Tomley, F. M. and Wan, K. L. (2012). EmaxDB: availability of a first draft genome sequence for the apicomplexan Eimeria maxima . Molecular and Biochemical Parasitology 184, 48–51.CrossRefGoogle ScholarPubMed
Bulik, D. A., van Ophem, P., Manning, J. M., Shen, Z. J., Newburg, D. S. and Jarroll, E. L. (2000). UDP-N-acetylglucosamine pyrophosphorylase, a key enzyme in encysting Giardia, is allosterically regulated. Journal of Biological Chemistry 275, 14722–14728.Google Scholar
Bushkin, G. G., Motari, E., Magnelli, P., Gubbels, M.-J., Dubey, J. P., Miska, K. B., Bullitt, E., Costello, C. E., Robbins, P. W. and Samuelson, J. (2012). Beta-1,3-Glucan, which can be targeted by drugs, forms a trabecular scaffold in the oocyst walls of Toxoplasma and Eimeria . Mbio 3, e00258–e00312.Google Scholar
Bushkin, G. G., Motari, E., Carpentieri, A., Dubey, J. P., Costello, C. E., Robbins, P. W. and Samuelson, J. (2013). Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria . Mbio 4, e00387–e00313.CrossRefGoogle Scholar
Castillo-Romero, A., Leon-Avila, G., Perez Rangel, A., Cortes Zarate, R., Garcia Tovar, C. and Hernandez, J. M. (2009). Participation of actin on Giardia lamblia growth and encystation. PLoS ONE 4, e7156.Google Scholar
Castillo-Romero, A., Leon-Avila, G., Wang, C. C., Perez Rangel, A., Camacho Nuez, M., Garcia Tovar, C., Ayala-Sumuano, J. T., Luna-Arias, J. P. and Hernandez, J. M. (2010). Rab11 and actin cytoskeleton participate in Giardia lamblia encystation, guiding the specific vesicles to the cyst wall. PLoS Neglected Tropical Diseases 4, e697.Google Scholar
Chatterjee, A., Carpentieri, A., Ratner, D. M., Bullitt, E., Costello, C. E. et al. (2010). Giardia cyst wall protein 1 is a Lectin that binds to curled fibrils of the GalNAc homopolymer. PLoS Pathog 6(8): e1001059. doi:10.1371/journal.ppat.1001059.Google Scholar
Chavez-Munguia, B., Cedillo-Rivera, R. and Martinez-Palomo, A. (2004). The ultrastructure of the cyst wall of Giardia lamblia . Journal of Eukaryotic Microbiology 51, 220–226.Google Scholar
De Souza, W. (2006). Secretory organelles of pathogenic protozoa. Anais Da Academia Brasileira De Ciencias 78, 271–291.CrossRefGoogle Scholar
Ebert, F., Bachmann, A., Nakada-Tsukui, K., Hennings, I., Drescher, B., Nozaki, T., Tannich, E. and Bruchhaus, I. (2008). An Entamoeba cysteine peptidase specifically expressed during encystation. Parasitology International 57, 521–524.Google Scholar
Ellis, J. E., Wyder, M. A., Jarroll, E. L. and Kaneshiro, E. S. (1996). Changes in lipid composition during in vitro encystation and fatty acid desaturase activity of Giardia lamblia . Molecular and Biochemical Parasitology 81, 13–25.Google Scholar
Faso, C., Bischof, S. and Hehl, A. B. (2013). The proteome landscape of Giardia lamblia encystation. PLoS ONE 8(12): e83207. doi:10.1371/journal.pone.0083207.Google Scholar
Ferguson, D. J. P., Belli, S. I., Smith, N. C. and Wallach, M. G. (2003). The development of the macrogamete and oocyst wall in Eimeria maxima: immuno-light and electron microscopy. International Journal for Parasitology 33, 1329–1340.Google Scholar
Fried, M., Mencher, D., Sarshalom, O. and Wallach, M. (1992). Developmental gene-expression of 230-kilodalton macrogamete-specific protein of the avian coccidial parasite, Eimeria maxima . Molecular and Biochemical Parasitology 51, 251–262.CrossRefGoogle ScholarPubMed
Frölich, S., Johnson, M., Robinson, M., Entzeroth, R. and Wallach, M. (2013). The spatial organization and extraction of the wall-forming bodies of Eimeria maxima . Parasitology 140, 876–887.Google Scholar
Frölich, S., Shahparee, A., Wasinger, V. C. and Wallach, M. (2014). In vivo localization of antibodies raised against Eimeria maxima wall forming bodies during sexual intracellular development. Parasitology (2014), 141, 1726–1735, doi:10.1017/S0031182014001012.Google Scholar
Gerwig, G. J., van Kuik, J. A., Leeflang, B. R., Kamerling, J. P., Vliegenthart, J. F. G., Karr, C. D. and Jarroll, E. L. (2002). The Giardia intestinalis filamentous cyst wall contains a novel beta(1–3)-N-acetyl-D-galactosamine polymer: a structural and conformational study. Glycobiology 12, 499–505.Google Scholar
Goddette, D. W. and Frieden, C. (1986). Actin polymerization. The mechanism of action of cytochalasin D. Journal of Biological Chemistry 261, 15974–15980.CrossRefGoogle ScholarPubMed
Herrera-Martinez, M., Hernandez-Ramirez, V. I., Lagunes-Guillen, A. E., Chavez-Munguia, B. and Talamas-Rohana, P. (2013). Actin, RhoA, and Rab11 participation during encystment in Entamoeba invadens . BioMed Research International 2013, 919345–919345.Google Scholar
Hetsko, M. L., McCaffery, J. M., Svard, S. G., Meng, T. C., Que, X. C. and Gillin, F. D. (1998). Cellular and transcriptional changes during excystation of Giardia lamblia in vitro . Experimental Parasitology 88, 172–183.Google Scholar
Katrib, M., Ikin, R. J., Brossier, F., Robinson, M., Slapetova, I., Sharman, P. A., Walker, R. A., Belli, S. I., Tomley, F. M. and Smith, N. C. (2012). Stage-specific expression of protease genes in the apicomplexan parasite, Eimeria tenella . BMC Genomics 13, 685–712.CrossRefGoogle ScholarPubMed
Lanfredi-Rangel, A., Attias, M., Reiner, D. S., Gillin, F. D. and De Souza, W. (2003). Fine structure of the biogenesis of Giardia lamblia encystation secretory vesicles. Journal of Structural Biology 143, 153–163.CrossRefGoogle ScholarPubMed
Luo, W., Yu, C.-H., Lieu, Z. Z., Allard, J., Mogilner, A., Sheetz, M. P. and Bershadsky, A. D. (2013). Analysis of the local organization and dynamics of cellular actin networks. Journal of Cell Biology 202, 1057–1073.Google Scholar
Mai, K., Sharman, P. A., Walker, R. A., Katrib, M., De Souza, D., McConville, M. J., Wallach, M. G., Belli, S. I., Ferguson, D. J. P. and Smith, N. C. (2009). Oocyst wall formation and composition in coccidian parasites. Memorias Do Instituto Oswaldo Cruz 104, 280–288.Google Scholar
Mai, K., Smith, N. C., Feng, Z.-P., Katrib, M., Slapeta, J., Slapetova, I., Wallach, M. G., Luxford, C., Davies, M. J., Zhang, X., Norton, R. S. and Belli, S. I. (2011). Peroxidase catalysed cross-linking of an intrinsically unstructured protein via dityrosine bonds in the oocyst wall of the apicomplexan parasite, Eimeria maxima . International Journal for Parasitology 41, 1157–1164.CrossRefGoogle ScholarPubMed
Makioka, A., Kumagai, M., Ohtomo, H., Kobayashi, S. and Takeuchi, T. (2001). Effect of jasplakinolide on the growth, encystation, and actin cytoskeleton of Entamoeba histolytica and Entamoeba invadens . Journal of Parasitology 87, 399–405.Google Scholar
Matsubayashi, M., Hatta, T., Miyoshi, T., Anisuzzaman, A., Sasai, K., Yamaji, K., Shimura, K., Isobe, T., Kita, K. and Tsuji, N. (2014). Localization of eimeripain, an Eimeria tenella cathepsin B-like cysteine protease, during asexual and sexual intracellular development in chicken ceca. Journal of Veterinary Medical Science 76, 531–537.Google Scholar
Mehlhorn, E. S. A. H. (1971). Fine strucutre of macrogametes and oocysts of coccidia and related organisms. Zeitschrift Fur Parasitenkunde 37, 1–43.Google Scholar
Morton, W. M., Ayscough, K. R. and McLaughlin, P. J. (2000). Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nature Cell Biology 2, 376–378.Google Scholar
Mouafo, A. N., Weck-Heimann, A., Dubremetz, J. F. and Entzeroth, R. (2002). Monoclonal antibodies specific for the two types of wall-forming bodies of Emeria tenella macrogametes (Coccidia, Apicomplexa). Parasitology Research 88, 217–224.Google Scholar
Pittilo, R. M. and Ball, S. J. (1979). Fine structure of the developing macrogamete and oocyst wall formation in Eimeria maxima . Parasitology 79, R34–R34.Google Scholar
Reid, A. J., Blake, D. P., Ansari, H. R., Billington, K., Browne, H. P., Bryant, J., Dunn, M., Hung, S. S., Kawahara, F., Miranda-Saavedra, D., Malas, T. B., Mourier, T., Naghra, H., Nair, M., Otto, T. D., Rawlings, N. D., Rivailler, P., Sanchez-Flores, A., Sanders, M., Subramaniam, C., Tay, Y.-L., Woo, Y., Wu, X., Barrell, B., Dear, P. H., Doerig, C., Gruber, A., Ivens, A. C., Parkinson, J., Rajandream, M.-A. et al. (2014). Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Research 24, 1676–1685.CrossRefGoogle ScholarPubMed
Rieux, A., Gras, S., Lecaille, F., Niepceron, A., Katrib, M., Smith, N. C., Lalmanach, G. and Brossier, F. (2012). Eimeripain, a cathepsin B-like cysteine protease, expressed throughout sporulation of the apicomplexan parasite Eimeria tenella . PLoS ONE 7, e31914.Google Scholar
Samuelson, J., Bushkin, G. G., Chatterjee, A. and Robbins, P. W. (2013). Strategies to discover the structural components of cyst and oocyst walls. Eukaryotic Cell 12, 1578–1587.CrossRefGoogle ScholarPubMed
Selden, L. A., Gershman, L. C. and Estes, J. E. (1980). A proposed mechanism of action of cytochalasin D on muscle actin. Biochemical and Biophysical Research Communications 95, 1854–1860.Google Scholar
Simon, V. R. and Pon, L. A. (1996). Actin-based organelle movement. Experientia 52, 1117–1122.Google Scholar
Wagenbach, G. E., Challey, J. R. and Burns, W. C. (1966). A method for purifying coccidian oocysts employing Chlorox and sulfuric acid-dochromate solution. Journal of Parasitology 52, 1222.CrossRefGoogle Scholar
Walker, R. A., Slapetova, I., Slapeta, J., Miller, C. M. and Smith, N. C. (2010). The Glycosylation pathway of Eimeria tenella is upregulated during gametocyte development and may play a role in oocyst wall formation. Eukaryotic Cell 9, 127–135.CrossRefGoogle ScholarPubMed

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