Open Access
Research Article
Issue
Parasite
Volume 24, 2017
Article Number 50
Number of page(s) 13
DOI https://doi.org/10.1051/parasite/2017049
Published online 06 December 2017
  • Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology, 83(2), 262–271. [CrossRef] [Google Scholar]
  • Bauer C, Dubremetz JF, Entzeroth R. 1995. Characterization of surface antigens of Eimeria nieschulzi (Sporozoa, Eimeriidae) merozoites. Parasitology Research, 81(3), 230-234. [PubMed] [Google Scholar]
  • Belli SI, Lee M, Thebo P, Wallach MG, Schwartsburd B, Smith NC. 2002. Biochemical characterisation of the 56 and 82 kDa immunodominant gametocyte antigens from Eimeria maxima. International Journal for Parasitology, 32(7), 805-816. [CrossRef] [PubMed] [Google Scholar]
  • Belli SI, Witcombe D, Wallach MG, Smith NC. 2002. Functional genomics of gam56: characterisation of the role of a 56 kilodalton sexual stage antigen in oocyst wall formation in Eimeria maxima. International Journal for Parasitology, 32(14), 1727-1737. [CrossRef] [PubMed] [Google Scholar]
  • Belli SI, Wallach MG, Luxford C, Davies MJ, Smith NC. 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(3), 456-464. [CrossRef] [PubMed] [Google Scholar]
  • Belli SI, Wallach MG, Smith NC. 2003. Cloning and characterization of the 82 kDa tyrosine-rich sexual stage glycoprotein, GAM82, and its role in oocyst wall formation in the apicomplexan parasite, Eimeria maxima. Gene, 307, 201-212. [CrossRef] [Google Scholar]
  • Belli SI, Smith NC, Ferguson DJ. 2006. The coccidian oocyst: a tough nut to crack! Trends in Parasitology, 22(9), 416-423. [CrossRef] [PubMed] [Google Scholar]
  • Belli SI, Ferguson DJ, Katrib M, Slapetova I, Mai K, Slapeta J, Flowers SA, Miska KB, Tomley FM, Shirley MW, Wallach MG, Smith NC. 2009. Conservation of proteins involved in oocyst wall formation in Eimeria maxima, Eimeria tenella and Eimeria acervulina. International Journal for Parasitology, 39(10), 1063-1070. [CrossRef] [PubMed] [Google Scholar]
  • Brothers VM, Kuhn I, Paul LS, Gabe JD, Andrews WH, Sias SR, McCaman MT, Dragon EA, Files JG. 1988. Characterization of a surface antigen of Eimeria tenella sporozoites and synthesis from a cloned cDNA in Escherichia coli. Molecular and Biochemical Parasitology, 28(3), 235-247. [CrossRef] [PubMed] [Google Scholar]
  • Bushkin GG, Motari E, Carpentieri A, Dubey JP, Costello CE, Robbins PW, Samuelson J. 2013. Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria. mBio, 4(5), e00387-13. [CrossRef] [Google Scholar]
  • Cantacessi C, Riddell S, Morris GM, Doran T, Woods WG, Otranto D, Gasser RB. 2008. Genetic characterization of three unique operational taxonomic units of Eimeria from chickens in Australia based on nuclear spacer ribosomal DNA. Veterinary Parasitology, 152(3-4), 226–234. [CrossRef] [PubMed] [Google Scholar]
  • Clark EL, Macdonald SE, Thenmozhi V, Kundu K, Garg R, Kumar S, Ayoade S, Fornace KM, Jatau ID, Moftah A, Nolan MJ, Sudhakar NR, Adebambo AO, Lawal IA, Alvarez Zapata R, Awuni JA, Chapman HD, Karimuribo E, Mugasa CM, Namangala B, Rushton J, Suo X, Thangaraj K, Srinivasa Rao AS, Tewari AK, Banerjee PS, Dhinakar Raj G, Raman M, Tomley FM, Blake DP. 2016. Cryptic Eimeria genotypes are common across the southern but not northern hemisphere. International Journal for Parasitology, 46(9), 537-544. [CrossRef] [Google Scholar]
  • Daugschies A, Bialek R, Joachim A, Mundt HC. 2001. Autofluorescence microscopy for the detection of nematode eggs and protozoa, in particular Isospora suis, in swine faeces. Parasitology Research, 87(5), 409-412. [CrossRef] [Google Scholar]
  • Ferguson DJ, Birch-Andersen A, Hutchison WM, Siim JC. 1977. Ultrastructural studies on the endogenous development of Eimeria brunetti. III. Macrogametogony and the macrogamete. Acta Pathologica et Microbiologica Scandinavica. Section B, Microbiology, 85B(1), 78-88. [Google Scholar]
  • Ferguson DJ, Birch-Andersen A, Hutchison WM, Siim JC. 1977. Ultrastructural studies on the endogenous development of Eimeria brunetti. IV. Formation and structure of the oocyst wall. Acta Pathologica et Microbiologica Scandinavica. Section B, Microbiology, 85(3), 201-211. [Google Scholar]
  • Ferguson DJ, Belli SI, Smith NC, Wallach MG. 2003. The development of the macrogamete and oocyst wall in Eimeria maxima: immuno-light and electron microscopy. International Journal for Parasitology, 33(12), 1329-1340. [CrossRef] [PubMed] [Google Scholar]
  • Fried M, Mencher D, Sar-Shalom O, Wallach M. 1992. Developmental gene expression of a 230-kilodalton macrogamete-specific protein of the avian coccidial parasite, Eimeria maxima. Molecular and Biochemical Parasitolology, 51(2), 251-262. [CrossRef] [Google Scholar]
  • Hanig S, Entzeroth R, Kurth M. 2012. Chimeric fluorescent reporter as a tool for generation of transgenic Eimeria (Apicomplexa, Coccidia) strains with stage specific reporter gene expression. Parasitology International, 61(3), 391-398. [CrossRef] [PubMed] [Google Scholar]
  • Hanig S. 2013. Neue Einblicke in die Oozysten-Hüllbildung von Eimeria nieschulzi (Apicomplexa, Coccidia). Dresden, Technische Universität Dresden, Fakultät Mathematik und Naturwissenschaften, Dissertation. [Google Scholar]
  • Hassan MA, Melo MB, Haas B, Jensen KD, Saeij JP. 2012. De novo reconstruction of the Toxoplasma gondii transcriptome improves on the current genome annotation and reveals alternatively spliced transcripts and putative long non-coding RNAs. BMC Genomics, 13, 696. [CrossRef] [Google Scholar]
  • Jonscher E, Erdbeer A, Günther M, Kurth M. 2015. Two COWP-like cysteine rich proteins from Eimeria nieschulzi (coccidia, apicomplexa) are expressed during sporulation and involved in the sporocyst wall formation. Parasites & Vectors, 8, 395. [CrossRef] [Google Scholar]
  • Krücken J, Hosse RJ, Mouafo AN, Entzeroth R, Bierbaum S, Marinovski P, Hain K, Greif G, Wunderlich F. 2008. Excystation of Eimeria tenella sporozoites impaired by antibody recognizing gametocyte/oocyst antigens GAM22 and GAM56. Eukaryotic Cell, 7(2), 202-211. [CrossRef] [Google Scholar]
  • Kurth M, Entzeroth R. 2008. Improved excystation protocol for Eimeria nieschulzi (Apikomplexa, Coccidia). Parasitology Research, 102(4), 819-822. [CrossRef] [PubMed] [Google Scholar]
  • Lal K, Bromley E, Oakes R, Prieto JH, Sanderson SJ, Kurian D, Hunt L, Yates JR3rd Wastling, JM, Sinden RE, Tomley FM. 2009. Proteomic comparison of four Eimeria tenella life cycle stages: unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite. Proteomics, 9(19), 4566–4576. [CrossRef] [Google Scholar]
  • Landers EJ Jr. 1960. Studies on excystation of coccidial oocysts. Journal of Parasitology, 46, 195-200. [CrossRef] [Google Scholar]
  • Lindquist HD, Bennett JW, Hester JD, Ware MW, Dubey JP, Everson WV. 2003. Autofluorescence of Toxoplasma gondii and related coccidian oocysts. Journal of Parasitology, 89(4), 865-867. [CrossRef] [Google Scholar]
  • Liu D, Cao L, Zhu Y, Deng C, Su S, Xu J, Jin W, Li J, Wu L, Tao J. 2014. Cloning and characterization of an Eimeria necatrix gene encoding a gametocyte protein and associated with oocyst wall formation. Parasites & Vectors, 7, 27. [CrossRef] [Google Scholar]
  • Mai K, Sharman PA, Walker RA, Katrib M, De Souza D, McConville MJ, Wallach MG, Belli SI, Ferguson DJ, Smith NC. 2009. Oocyst wall formation and composition in coccidian parasites. Memórias do Instituto Oswaldo Cruz, 104(2), 281-289. [CrossRef] [Google Scholar]
  • Mai K, Smith NC, Feng ZP, Katrib M, Slapeta J, Slapetova I, Wallach MG, Luxford C, Davies MJ, Zhang X, Norton RS, Belli SI. 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(11), 1157–1164. [CrossRef] [PubMed] [Google Scholar]
  • Marquardt WC. 1966. The living, endogenous stages of the rat coccidium, Eimeria nieschulzi. Journal of Protozoology, 13(3), 509–514. [CrossRef] [Google Scholar]
  • Mouafo A. 2001. Characterization of wall forming bodies in macrogamonts and oocyst wall formation in Eimeria tenella (Coccidia, Apicomplexa). Study on the ultrastructure, immuno-localization of proteins and drug effects. Dresden, Technische Universität Dresden, Fakultät Mathematik und Naturwissenschaften, Dissertation. [Google Scholar]
  • Mouafo AN, Weck-Heimann A, Dubremetz JF, Entzeroth R. 2002. Monoclonal antibodies specific for the two types of wall-forming bodies of Eimeria tenella macrogametes (Coccidia, Apicomplexa). Parasitology Research, 88 (3), 217–224. [CrossRef] [PubMed] [Google Scholar]
  • Mülhardt C. 2009. Molekularbiologie/Genomics. Heidelberg: Spektrum Akademischer Verlag. [Google Scholar]
  • Pugatsch T, Mencher D, Wallach M. 1989. Eimeria maxima: isolation of gametocytes and their immunogenicity in mice, rabbits, and chickens. Experimental Parasitology, 68(2), 127–134. [CrossRef] [PubMed] [Google Scholar]
  • Samuelson J, Bushkin GG, Chatterjee A, Robbins PW. 2013. Strategies to discover the structural components of cyst and oocyst walls. Eukaryotic Cell, 12(12), 1578-1587. [CrossRef] [PubMed] [Google Scholar]
  • Schmatz DM, Crane MS, Murray PK. 1984. Purification of Eimeria sporozoites by DE-52 anion exchange chromatography. Journal of Protozoology, 31(1), 181–183. [CrossRef] [Google Scholar]
  • Scholtyseck E, Voigt WH. 1964. Die Bildung der Oocystenhülle bei Eimeria perforans (Sporozoa). Zeitschrift für Zellforschung und Mikroskopische Anatomie, 62, 279-292. [CrossRef] [Google Scholar]
  • Scholtyseck E, Hammond DM, Ernst JV. 1966. Fine structure of the macrogametes of Eimeria perforans, E. stiedae, E. bovis, and E. auburnensis. Journal of Parasitology, 52(5), 975-987. [CrossRef] [Google Scholar]
  • Scholtyseck E, Gönnert R, Haberkorn A. 1969. Die Feinstruktur der Makrogameten des Hühnercoccids Eimeria tenella. Zeitschrift für Parasitenkunde, 33(1), 31-43. [CrossRef] [Google Scholar]
  • Scholtyseck E, Mehlhorn H, Hammond DM. 1971. Fine structure of macrogametes and oocysts of Coccidia and related organisms. Zeitschrift für ParasitenKunde, 37(1), 1-43. [CrossRef] [Google Scholar]
  • Shirley MW. 1995. Eimeria species and strains of chickens, in COST 89/820 Biotechnology: Guidelines on techniques in coccidiosis research. Eckert J, Braun R, Shirley MW, Coudert P, Editors. Luxembourg: Office for Official Publications of the European Communities. p. 1-24. [Google Scholar]
  • Sorber K, Dimon MT, DeRisi JL. 2011. RNA-Seq analysis of splicing in Plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts. Nucleic Acids Research, 39(9), 3820–3835. [CrossRef] [PubMed] [Google Scholar]
  • Stange J, Hepworth MR, Rausch S, Zajic L, Kühl AA, Uyttenhove C, Renauld JC, Hartmann S, Lucius R. 2012. IL-22 mediates host defense against an intestinal intracellular parasite in the absence of IFN-ɣ at the cost of Th17-driven immunopathology. Journal of Immunology, 188(5), 2410–2418. [CrossRef] [Google Scholar]
  • Walker RA, Sharman PA, Miller CM, Lippuner C, Okoniewski M, Eichenberger RM, Ramakrishnan C, Brossier F, Deplazes P, Hehl AB, Smith NC. 2015. RNA Seq analysis of the Eimeria tenella gametocyte transcriptome reveals clues about the molecular basis for sexual reproduction and oocyst biogenesis. BMC Genomics, 16, 94. [CrossRef] [PubMed] [Google Scholar]
  • Walker RA, Niepceron A, Ramakrishnan C, Sedano L, Hehl AB, Brossier F, Smith NC. 2016. Discovery of a tyrosine-rich sporocyst wall protein in Eimeria tenella. Parasites & Vectors, 9, 124. [CrossRef] [PubMed] [Google Scholar]
  • Wallach MG, Mencher D, Yarus S, Pillemer G, Halabi A, Pugatsch T. 1989. Eimeria maxima: identification of gametocyte protein antigens. Experimental Parasitology, 68(1), 49–56. [CrossRef] [PubMed] [Google Scholar]
  • Wheat BE, Jensen JB, Ernst JV, Chobotar B. 1976. Ultrastructure of macrogametogenesis of Eimeria mivati. Zeitschrift für Parasitenkunde, 50(2), 125-136. [CrossRef] [Google Scholar]
  • Wiedmer S, Stange J, Kurth T, Bleiss W, Entzeroth R, Kurth M. 2011. New insights into the excystation process and oocyst morphology of rodent Eimeria species. Protist, 162(4), 668-678. [CrossRef] [PubMed] [Google Scholar]