Advertisement

Modern Approaches in Fascioloides magna Studies

  • Ivica Králová-HromadováEmail author
  • Ludmila Juhásová
  • Eva Bazsalovicsová
Chapter
Part of the SpringerBriefs in Animal Sciences book series (BRIEFSANIMAL)

Abstract

The methods of cellular and molecular biology represent useful and attractive tools that have been applied in identification, taxonomy and systematics of broad spectrum of parasitic organisms over the past decades. The pilot molecular data on Fascioloides magna appeared in 90s of the 20th century. After more than 20 years of molecular and cellular research of F. magna, effective markers for accurate species identification and large-scale population studies, detailed subcellular structure of the parasite, and immunologically active molecules, were detected. This chapter is divided into four sections. First one is dealing with general structure and characterization of ribosomal genes and their utilization in molecular taxonomy and phylogeny of F. magna. Second part is focused on characterization and structure of mitochondrial genes and their application in studies on genetic interrelationships, biogeography, origin and transmission routes of F. magna. Microsatellites, biparentally inherited multilocus markers, are useful population genetics markers described in third subchapter. Data on ultrastructure, karyotype and chromosomal location of ribosomal genes of F. magna are presented in the last part of this chapter. In addition, we provided brief overview on current knowledge of F. magna isoenzyme analyses, excretory/secretory proteins, humoral immune responses during experimental infection with F. magna in selected final hosts, and up to date technologies of transcriptome analysis.

Keywords

Giant liver fluke Ribosomal DNA Mitochondrial DNA Microsatellites Karyotype Transcriptome Excretory/secretory proteins Isoenzyme analysis Molecular taxonomy Phylogeny 

References

  1. Adlard RD, Barker SC, Blair D, Cribb TH (1993) Comparison of the second internal transcribed spacer (ribosomal DNA) from populations and species of Fasciolidae (Digenea). Int J Parasitol 23:423–425. doi: 10.1016/0020-7519(93)90022-Q CrossRefPubMedGoogle Scholar
  2. Andrés JA, Bogdanowicz SM (2011) Isolating microsatellite loci: looking back, looking ahead. In: Orgogozo V, Rockman MV (eds) Molecular methods for evolutionary genetics. Humana Press, New YorkGoogle Scholar
  3. Andrews RH, Chilton NB (1999) Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics. Int J Parasitol 29:213–253. doi: 10.1016/S0020-7519(98)00168-4 CrossRefPubMedGoogle Scholar
  4. Ansorge WJ (2009) Next-generation DNA sequencing techniques. N Biotechnol 25:193–205. doi: 10.1016/j.nbt.2008.12.009 CrossRefGoogle Scholar
  5. Avise JC (1994) Molecular markers, natural history and evolution, 2nd edn. Chapman & Hall, New YorkCrossRefGoogle Scholar
  6. Avise JC, Walker D (1999) Species realities and numbers in sexual vertebrates: perspectives from an asexually transmitted genome. Proc Nat Acad Sci USA 96:992–995. doi: 10.1073/pnas.96.3.992 PubMedCentralCrossRefPubMedGoogle Scholar
  7. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165. doi: 10.1046/j.0962-1083.2001.01436.x CrossRefPubMedGoogle Scholar
  8. Bazsalovicsová E, Králová-Hromadová I, Špakulová M, Reblánová M, Oberhauserová K (2010) Determination of ribosomal internal transcribed spacer 2 (ITS2) interspecific markers in Fasciola hepatica, Fascioloides magna, Dicrocoelium dendriticum and Paramphistomum cervi (Trematoda), parasites of wild and domestic ruminants. Helminthologia 47:76–82. doi: 10.2478/s11687-010-0011-1 CrossRefGoogle Scholar
  9. Bazsalovicsová E, Králová-Hromadová I, Radvánszky J, Beck R (2013) The origin of the giant liver fluke, Fascioloides magna (Trematoda: Fasciolidae) from Croatia determined by high-resolution melting screening of mitochondrial cox1 haplotypes. Parasitol Res 112:2661–2666. doi: 10.1007/s00436-013-3433-0 CrossRefPubMedGoogle Scholar
  10. Bazsalovicsová E, Králová-Hromadová I, Štefka J, Minárik G, Bokorová S, Pybus M (2015) Genetic interrelationships of North American populations of giant liver fluke Fascioloides magna. Parasit Vectors 8:288. doi: 10.1186/s13071-015-0895-1 PubMedCentralCrossRefPubMedGoogle Scholar
  11. Bennett CD, Campbell MN, Cook CJ, Eyre DJ, Nay LM, Nielsen DR, Rasmussen RP, Bernard PS (2003) The LightTyper: high throughput genotyping using fluorescent melting curve analysis. BioTechniques 34:1288–1295PubMedGoogle Scholar
  12. Bildfell RJ, Whipps CM, Gillin CM, Kent ML (2007) DNA-based identification of a hepatic trematode in an elk calf. J Wildl Dis 43:762–769. doi: 10.7589/0090-3558-43.4.762 CrossRefPubMedGoogle Scholar
  13. Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Ann Rev Genet 35:125–148. doi: 10.1146/annurev.genet.35.102401.090231 CrossRefPubMedGoogle Scholar
  14. Bombarová M, Marec F, Nguyen P, Špakulová M (2007) Divergent location of ribosomal genes in chromosomes of fish thornyheaded worms, Pomphorhynchus laevis and Pomphorhynchus tereticollis (Acanthocephala). Genetica 131:141–149. doi: 10.1007/s10709-006-9124-3 CrossRefPubMedGoogle Scholar
  15. Bombarová M, Vítková M, Špakulová M, Koubková B (2009) Telomere analysis of platyhelminths and acanthocephalans by FISH and Southern hybridization. Genome 52:897–903. doi: 10.1139/g09-063 CrossRefPubMedGoogle Scholar
  16. Bombarová M, Špakulová M, Koubková B (2014) New data on the karyotype and chromosomal rDNA location in Paradiplozoon megan (Monogenea, Diplozoidae), gill parasite of chubs. Parasitol Res 113:4111–4116. doi: 10.1007/s00436-014-4082-7 CrossRefPubMedGoogle Scholar
  17. Boore JL (1999) Animal mitochondrial genomes. Nucleid Acid Res 27:1767–1780. doi: 10.1093/nar/27.8.1767 CrossRefGoogle Scholar
  18. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends in Genet 19:709–716. doi: 10.1016/j.tig.2003.10.012 CrossRefGoogle Scholar
  19. Buschiazzo E, Gemmell NJ (2006) The rise, fall and renaissance of microsatellites in eukaryotic genomes. BioEssays 28:1040–1050. doi: 10.1002/bies.20470 CrossRefPubMedGoogle Scholar
  20. Cantacessi C, Mulvenna J, Young ND, Kašný M, Horák P, Aziz A, Hofmann A, Loukas A, Gasser RB (2012) A deep exploration of the transcriptome and excretory/secretory proteome of adult Fascioloides magna. Mol Cell Proteomics 11:1340–1353. doi: 10.1074/mcp.M112.019844 PubMedCentralCrossRefPubMedGoogle Scholar
  21. Collins FH, Paskewitz SM (1996) A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Mol Biol 5:1–9CrossRefPubMedGoogle Scholar
  22. Crimi M, Rigolio R (2008) The mitochondrial genome, a growing interest inside an organelle. Int J Nanomed 3:51–57. doi: 10.2147/ijn.s2482 Google Scholar
  23. Dieringer D, Schlötterer C (2003) Two distinct modes of microsatellite mutation processes: evidence from the complete genomic sequences of nine species. Genome Res 13:2242–2251. doi: 10.1101/gr.1416703 PubMedCentralCrossRefPubMedGoogle Scholar
  24. Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistics. Syst Biol 53:470–484. doi: 10.1080/10635150490445698 CrossRefPubMedGoogle Scholar
  25. Etter PD, Bassham S, Hohenlohe PA, Johnson EA, Cresko WA (2011) SNP discovery and genotyping for evolutionary genetics using RAD sequencing. Methods Mol Biol 772:157–178. doi: 10.1007/978-1-61779-228-1_9 PubMedCentralCrossRefPubMedGoogle Scholar
  26. Feagin JE (2000) Mitochondrial genome diversity in parasites. Int J Parasitol 30:371–390. doi: 10.1016/S0020-7519(99)00190-3 CrossRefPubMedGoogle Scholar
  27. Flegr J (2009) Evoluční biologie, 2nd edn. Academia, Praha (in Czech)Google Scholar
  28. Gibbons JG, Branco AT, Yu S, Lemos B (2014) Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat Commun 5:4850. doi: 10.1038/ncomms5850 CrossRefPubMedGoogle Scholar
  29. Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit RJ (2011) Current trends in microsatellite genotyping. Mol Ecol Res 11:591–611. doi: 10.1111/j.1755-0998.2011.03014.x CrossRefGoogle Scholar
  30. Gundry CN, Vandersteen JG, Reed GH, Pryor RJ, Chen J, Wittwer CT (2003) Amplicon melting analysis with labelled primers: a closed tube method for differentiating homozygotes and heterozygotes. Clin Chem 49:396–406. doi: 10.1373/49.3.396 CrossRefPubMedGoogle Scholar
  31. Halton DW (2004) Microscopy and the helminth parasite. Micron 35:361–390. doi: 10.1016/j.micron.2003.12.001 CrossRefPubMedGoogle Scholar
  32. Hartl DL, Freifelder D, Snyder LA (1988) Basic genetics. Jones and Bartlett Publishers, BostonGoogle Scholar
  33. He R, Kim MJ, Nelson W, Balbuena TS, Kim R, Kramer R, Crow JA, May GD, Thelen JJ, Soderlund CA, Gang DR (2012) Next-generation sequencing-based transcriptomic and proteomic analysis of the common reed, Phragmites australis (Poaceae), reveals genes involved in invasiveness and rhizome specificity. Am J Bot 99:232–247. doi: 10.3732/ajb.1100429 CrossRefPubMedGoogle Scholar
  34. Hearne CM, Ghosh S, Todd JA (1992) Microsatellites for linkage analysis of genetic traits. Trends Genet 8:288–294. doi: 10.1016/0168-9525(92)90256-4 CrossRefPubMedGoogle Scholar
  35. Hillis DM, Davis SK (1986) Evolution of ribosomal DNA: fifty million years of recorded history in the frog genus Rana. Evolution 40:1275–1288. doi: 10.2307/2408953 CrossRefGoogle Scholar
  36. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453CrossRefPubMedGoogle Scholar
  37. Hörweg C, Prosl H, Wille-Piazzai W, Joachim A, Sattmann H (2011) Prevalence of Fascioloides magna in Galba truncatula in the Danube backwater area east of Vienna, Austria. Wien Tierärztl Mschr 98:261–267Google Scholar
  38. Hu M, Chilton NB, Gasser RB (2004) The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress and implications for population genetics and systematics. Adv Parasitol 56:133–212. doi: 10.1016/S0065-308X(03)56003-1 CrossRefPubMedGoogle Scholar
  39. Josko D (2012) Updates in immunoassays: parasitology. Clin Lab Sci 25:185–190PubMedGoogle Scholar
  40. Karamon J, Larska M, Jasik A, Sell B (2015) First report of the giant liver fluke (Fascioloides magna) infection in farmed fallow deer (Dama dama) in Poland—pathomorphological changes and molecular identification. Bull Vet Inst Pulawy 59:339–344. doi: 10.1515/bvip-2015-0050 Google Scholar
  41. Kobayashi T (2011) Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell Mol Life Sci 68:1395–1403. doi: 10.1007/s00018-010-0613-2 PubMedCentralCrossRefPubMedGoogle Scholar
  42. Králová-Hromadová I, Špakulová M, Horáčková E, Turčeková L, Novobilský A, Beck R, Koudela B, Marinculić A, Rajský D, Pybus M (2008) Sequence analysis of ribosomal and mitochondrial genes of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae): intraspecific variation and differentiation from Fasciola hepatica. J Parasitol 94:58–67. doi: 10.1645/GE-1324.1 CrossRefPubMedGoogle Scholar
  43. Králová-Hromadová I, Bazsalovicsová E, Štefka J, Špakulová M, Vávrová S, Szemes T, Tkach V, Trudgett A, Pybus M (2011) Multiple origins of European populations of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae), a liver parasite of ruminants. Int J Parasitol 41:373–383. doi: 10.1016/j.ijpara.2010.10.010 CrossRefPubMedGoogle Scholar
  44. Králová-Hromadová I, Bazsalovicsová E, Demiaszkiewicz AW (2015) Molecular characterization of Fascioloides magna (Trematoda: Fasciolidae) from south-western Poland based on mitochondrial markers. Acta Parasitol 60:544–547. doi: 10.1515/ap-2015-0077 CrossRefPubMedGoogle Scholar
  45. Le TH, Blair D, McManus DP (2000) Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Tropi 77:243–256. doi: 10.1016/S0001-706X(00)00157-1 CrossRefGoogle Scholar
  46. Le TH, Blair D, McManus DP (2001) Complete DNA sequence and gene organization of the mitochondrial genome of the liver fluke, Fasciola hepatica L. (Platyhelminthes; Trematoda). Parasitology 123:609–621CrossRefPubMedGoogle Scholar
  47. Lotfy WM, Brant SV, DeJong RJ, Le TH, Demiaszkiewicz A, Rajapakse RP, Perera VB, Laursen JR, Loker ES (2008) Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). Am J Trop Med Hygeine 79:248–255Google Scholar
  48. Lydeard C, Mulvey M, Aho JM (1989) Genetic variability among natural populations of the liver fluke Fascioloides magna in white-tailed deer, Odocoileus virginianus. Can J Zool 67:2021–2025. doi: 10.1139/z89-287 CrossRefGoogle Scholar
  49. Minárik G, Bazsalovicsová E, Zvijáková Ľ, Štefka J, Pálková L, Králová-Hromadová I (2014) Development and characterization of multiplex panels of polymorphic microsatellite loci in giant liver fluke Fascioloides magna (Trematoda: Fasciolidae), using next generation sequencing. Mol Biochem Parasit 195:30–33. doi: 10.1016/j.molbiopara.2014.06.003 CrossRefGoogle Scholar
  50. Morgan EA (1982) Ribosomal RNA genes in Escherischia coli. In: Busch H, Rothblum L (eds) The cell nucleus: rDNA. Academic Press, New YorkGoogle Scholar
  51. Mulvey M, Aho JM, Lydeard C, Leberg PL, Smith MH (1991) Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45:1628–1640. doi: 10.2307/2409784 CrossRefGoogle Scholar
  52. Nadler SA, De Leon GPP (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138:1688–1709. doi: 10.1017/S003118201000168X CrossRefPubMedGoogle Scholar
  53. Nadler SA, Lindquist RL, Near TJ (1995) Genetic structure of Midwestern Ascaris suum populations: a comparison of isoenzyme and RAPD markers. J Parasitol 81:385–394CrossRefPubMedGoogle Scholar
  54. Naem S, Budke CM, Craig TM (2012) Morphological characterization of adult Fascioloides magna (Trematoda: Fasciolidae): first SEM report. Parasitol Res 2:971–978. doi: 10.1007/s00436-011-2582-2 CrossRefGoogle Scholar
  55. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Ann Rev Genet 39:121–152. doi: 10.1146/annurev.genet.39.073003.112240 PubMedCentralCrossRefPubMedGoogle Scholar
  56. Nguyen P, Sahara K, Yoshido A, Marec F (2010) Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera). Genetica 138:343–354. doi: 10.1007/s10709-009-9424-5
  57. Noller HF (1991) Ribosomal RNA and translation. Ann Rev Biochem 60:191–227. doi: 10.1146/annurev.bi.60.070191.001203 CrossRefPubMedGoogle Scholar
  58. Novobilský A, Kašný M, Mikeš L, Kovařčík K, Koudela B (2007) Humoral immune responses during experimental infection with Fascioloides magna and Fasciola hepatica in goats. Parasitol Res 101:357–364. doi: 10.1007/s00436-007-0463-5 CrossRefPubMedGoogle Scholar
  59. Nunome T, Negoro S, Miyatake K, Hirotaka Y, Fukuoka H (2006) A protocol for construction of microsatellite enriched genomic library. Plant Mol Biol Rep 24:305–312. doi: 10.1007/BF02913457 CrossRefGoogle Scholar
  60. Oberhauserová K, Bazsalovicsová E, Králová-Hromadová I, Major P, Reblánová M (2010) Molecular discrimination of eggs of cervid trematodes using the Teflon (PTFE) technique for eggshell disruption. Helminthologia 47:147–151. doi: 10.2478/s11687-010-0022-y CrossRefGoogle Scholar
  61. Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471–498PubMedCentralPubMedGoogle Scholar
  62. Prokopowich CD, Gregory TR, Crease TJ, Gregory TR, Crease TJ, Crease TJ (2003) The correlation between rDNA copy number and genome size in eukaryotes. Genome 46:48–50. doi: 10.1139/g02-103 CrossRefPubMedGoogle Scholar
  63. Pyziel AM, Demiaszkiewicz AW, Kuligowska I (2014) Molecular identification of Fascioloides magna (Bassi, 1875) from red deer from South-Western Poland (Lower Silesian wilderness) on the basis of internal transcribed spacer 2 (ITS-2). Pol J Vet Sci 17:523–525. doi: 10.2478/pjvs-2014-0077 PubMedGoogle Scholar
  64. Queller DC, Strassmann JE, Hughes CR (1993) Microsatellites and kinship. Trends Ecol Evol 8:285–288. doi: 10.1016/0169-5347(93)90256-O CrossRefPubMedGoogle Scholar
  65. Radvánský J, Bazsalovicsová E, Králová-Hromadová I, Minárik G, Kádaši L (2011) Development of high-resolution melting (HRM) analysis for population studies of Fascioloides magna (Trematoda: Fasciolidae), the giant liver fluke of ruminants. Parasitol Res 108:201–209. doi: 10.1007/s00436-010-2057-x CrossRefPubMedGoogle Scholar
  66. Reblánová M, Špakulová M, Orosová M, Bazsalovicsová E, Rajský D (2010) A description of karyotype of the giant liver fluke Fascioloides magna (Trematoda, Platyhelminthes) and review of Fasciolidae cytogenetics. Helminthologia 47:69–75. doi: 10.2478/s11687-010-0012-0 CrossRefGoogle Scholar
  67. Reblánová M, Špakulová M, Orosová M, Králová-Hromadová I, Bazsalovicsová E, Rajský D (2011) A comparative study of karyotypes and chromosomal location of rDNA genes in important liver flukes Fasciola hepatica and Fascioloides magna (Trematoda: Fasciolidae). Parasitol Res 109:1021–1028. doi: 10.1007/s00436-011-2339-y CrossRefPubMedGoogle Scholar
  68. Ririe KM, Rasmussen RP, Wittwer CT (1997) Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 245:154–160. doi: 10.1006/abio.1996.9916 CrossRefPubMedGoogle Scholar
  69. Sattmann H, Hörweg C, Gaub L, Feix AS, Haider M, Walochnik J, Rabitsch W, Prosl H (2014) Wherefrom and whereabouts of an alien: the American liver fluke Fascioloides magna in Austria: an overview. Wiener Klinische Wochenschrift 126:23–31. doi: 10.1007/s00508-014-0499-3 PubMedCentralCrossRefGoogle Scholar
  70. Schlötterer C (2004) The evolution of molecular markers—just a matter of fashion. Nat Rev Genet 5:63–69. doi: 10.1038/nrg1249 CrossRefPubMedGoogle Scholar
  71. Simon C, Pääbo S, Kocher TD, Wilson AC (1990) Evolution of mitochondrial ribosomal RNA in insects as shown by the polymerase chain reaction. In: Cleeg M, O’Brien S (eds) Molecular evolution. UCLA Symposia on molecular and cellular Biology, new series. Liss, New YorkGoogle Scholar
  72. Tighe PJ, Ryder RR, Todd I, Fairclough LC (2015) ELISA in the multiplex era: potentials and pitfalls. Proteomics Clin Appl 9:406–422. doi: 10.1002/prca.201400130 CrossRefPubMedGoogle Scholar
  73. Wittwer CT, Reed GH, Gundry CN, Vandersteen JG, Pryor RJ (2003) High-resolution genotyping by amplicon melting analysis using LCGreen. Clin Chem 49:853–860. doi: 10.1373/49.6.853 CrossRefPubMedGoogle Scholar
  74. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216CrossRefPubMedGoogle Scholar
  75. Yang Y, Ma H (2009) Western blotting and ELISA techniques. Researcher 1:67–86Google Scholar
  76. Zalapa JE, Cuevas H, Zhu H, Steffan S, Senalik D, Zeldin E, McCown B, Harbut R, Simon P (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99:193–208. doi: 10.3732/ajb.1100394 CrossRefPubMedGoogle Scholar
  77. Zane L, Bargelloni L, Patarnello T (2002) Stretegies for microsatellite isolation: a review. Mol Ecol 11:1–16. doi: 10.1046/j.0962-1083.2001.01418.x CrossRefPubMedGoogle Scholar
  78. Zheng X, Chang QC, Zhang Y, Tian SQ, Lou Y, Duan H, Guo DH, Wang CR, Xing-Quan Zhu XQ (2014) Characterization of the complete nuclear ribosomal DNA sequences of Paramphistomum cervi. Sci World J Article ID 751907. doi: 10.1155/2014/751907

Copyright information

© The Author(s) 2016

Authors and Affiliations

  • Ivica Králová-Hromadová
    • 1
    Email author
  • Ludmila Juhásová
    • 1
  • Eva Bazsalovicsová
    • 1
  1. 1.Institute of ParasitologySlovak Academy of SciencesKošiceSlovakia

Personalised recommendations