Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Differential Expression of Hox and Notch Genes in Larval and Adult Stages of Echinococcus granulosus

  • Dezaki, Ebrahim Saedi (Research Center for Hydatid Disease in Iran, School of Medicine, Kerman University of Medical Sciences) ;
  • Yaghoobi, Mohammad Mehdi (Research Department of Biotechnology, Institute of Sciences and High Technology and Environmental Sciences, Graduate University of Advanced Technology) ;
  • Taheri, Elham (Department of Pathology, School of Medicine, Kerman University of Medical Sciences) ;
  • Almani, Pooya Ghaseminejad (Research Center for Hydatid Disease in Iran, School of Medicine, Kerman University of Medical Sciences) ;
  • Tohidi, Farideh (Research Center for Hydatid Disease in Iran, School of Medicine, Kerman University of Medical Sciences) ;
  • Gottstein, Bruno (Institute of Parasitology, Faculty of Medicine and Vetsuisse Faculty of the University of Bern) ;
  • Harandi, Majid Fasihi (Research Center for Hydatid Disease in Iran, School of Medicine, Kerman University of Medical Sciences)
  • Received : 2016.01.14
  • Accepted : 2016.05.13
  • Published : 2016.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

This investigation aimed to evaluate the differential expression of HoxB7 and notch genes in different developmental stages of Echinococcus granulosus sensu stricto. The expression of HoxB7 gene was observed at all developmental stages. Nevertheless, significant fold differences in the expression level was documented in the juvenile worm with 3 or more proglottids, the germinal layer from infected sheep, and the adult worm from an experimentally infected dog. The notch gene was expressed at all developmental stages of E. granulosus; however, the fold difference was significantly increased at the microcysts in monophasic culture medium and the germinal layer of infected sheep in comparison with other stages. The findings demonstrated that the 2 aforementioned genes evaluated in the present study were differentially expressed at different developmental stages of the parasite and may contribute to some important biological processes of E. granulosus.

Keywords

References

  1. da Silva AM. Human echinococcosis: a neglected disease. Gastroenterol Res Pract 2010; 2010: 1-9.
  2. Moro P, Schantz PM. Echinococcosis: a review. Int J Infect Dis 2009; 13: 125-133. https://doi.org/10.1016/j.ijid.2008.03.037
  3. Smyth JD, Miller HJ, Howkins AB. Further analysis of the factors controlling strobilization, differentiation, and maturation of Echinococcus granulosus in vitro. Exp Parasitol 1967; 21: 31-41. https://doi.org/10.1016/0014-4894(67)90064-1
  4. Smyth JD. Studies on tapeworm physiology. Parasitology 1962; 52: 441-457. https://doi.org/10.1017/S0031182000027256
  5. Smyth JD, Howkins AB, Barton M. Factors controlling the differentiation of the hydatid organism, Echinococcus granulosus, into cystic or strobilar stages in vitro. Nature 1966; 211: 1374-1377. https://doi.org/10.1038/2111374a0
  6. Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Huang Y, Liu J, Kang H, Chen J, Wang L, Chen A, Yu Sh, Gao Z, Jin L, Gu W, Wang Z, Zhao L, Shi B, Wen H, Lin R, K Jones M, Brejova B, Vinar T, Zhao G, McManus DP, Chen Z, Zhou Y, Wang S. The genome of the hydatid tapeworm Echinococcus granulosus. Nat Genet 2013; 45: 1168-1175. https://doi.org/10.1038/ng.2757
  7. Thompson RC, Jenkins DJ. Echinococcus as a model system: biology and epidemiology. Int J Parasitol 2014; 44: 865-877. https://doi.org/10.1016/j.ijpara.2014.07.005
  8. Monteiro KM, de Carvalho MO, Zaha A, Ferreira HB. Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics 2010; 10: 1985-1999. https://doi.org/10.1002/pmic.200900506
  9. Lappin TRJ, Grier DG, Thompson A, Halliday HL. HOX genes: seductive science, mysterious mechanisms. Ulster Med J 2006; 75: 23-31.
  10. Ladam F, Sagerstrom CG. Hox regulation of transcription: more complex(es). Dev Dyn 2014; 243: 4-15. https://doi.org/10.1002/dvdy.23997
  11. Artavanis-Tsakonas S, Matsuno K, Fortini M. Notch signaling. Science 1995; 268: 225-232. https://doi.org/10.1126/science.7716513
  12. Priess JR. Notch signaling in the C. elegans embryo. WormBook: The Online Review of C. elegans Biology 2005: 1-16.
  13. Brehm K, Spiliotis M. Recent advances in the in vitro cultivation and genetic manipulation of Echinococcus multilocularis metacestodes and germinal cells. Exp Parasitol 2008; 119: 506-515. https://doi.org/10.1016/j.exppara.2008.03.007
  14. Smyth JD. Development of monozoic forms of Echinococcus granulosus during in vitro culture. Int J Parasitol 1971; 1: 121-124. https://doi.org/10.1016/0020-7519(71)90004-X
  15. Hajialilo E, Harandi MF, Sharbatkhori M, Mirhendi H, Rostami S. Genetic characterization of Echinococcus granulosus in camels, cattle and sheep from the south-east of Iran indicates the presence of the G3 genotype. J Helminthol 2012; 86: 263-270. https://doi.org/10.1017/S0022149X11000320
  16. Smyth JD, Davies Z. In vitro culture of the strobilar stage of Echinococcus granulosus (sheep strain): a review of basic problems and results. Int J Parasitol 1974; 4: 631-644. https://doi.org/10.1016/0020-7519(74)90028-9
  17. Smyth JD, Howkins AB. An in vitro technique for the production of eggs of Echinococcus granulosus by maturation of partly developed strobila. Parasitology 1966; 56: 763-766. https://doi.org/10.1017/S003118200007178X
  18. Hemphill A, Stettler M, Walker M, Siles-Lucas M, Fink R, Gottstein B. Culture of Echinococcus multilocularis metacestodes: an alternative to animal use. Trends Parasitol 2002; 18: 445-451. https://doi.org/10.1016/S1471-4922(02)02346-2
  19. Rossi A, Marques JM, Gavidia CM, Gonzalez AE, Garcia HH, Chabalgoity JA. Echinococcus granulosus: different cytokine profiles are induced by single versus multiple experimental infections in dogs. Exp. Parasitol 2012; 130: 110-115. https://doi.org/10.1016/j.exppara.2011.12.006
  20. Jenkins DJ, Fraser A, Bradshaw H, Craig PS. Detection of Echinococcus granulosus coproantigens in Australian canids with natural or experimental infection. J Parasitol 2000; 86: 140-145. https://doi.org/10.1645/0022-3395(2000)086[0140:DOEGCI]2.0.CO;2
  21. Espinola SM, Ferreira HB, Zaha A. Validation of suitable reference genes for expression normalization in Echinococcus spp. larval stages. PLoS One 2014; 9: e102228. https://doi.org/10.1371/journal.pone.0102228
  22. Liao WT, Jiang D, Yuan J, Cui YM, Shi XW, Chen CM, Biam XW, Deng YJ, Ding YQ. HOXB7 as a prognostic factor and mediator of colorectal cancer progression. Clin Cancer Res 2011; 17: 3569-3578. https://doi.org/10.1158/1078-0432.CCR-10-2533
  23. Ishii M, Mitsunaga-Nakatsubo K, Kitajima T, Kusunoki S, Shimada H, Akasaka K. Hbox1 and Hbox7 are involved in pattern formation in sea urchin embryos. Dev Growth Differ 1999; 41: 241-252. https://doi.org/10.1046/j.1440-169X.1999.413426.x
  24. Carè A, Valtieri M, Mattia G, Meccia E, Masella B, Luchetti L, Felicetti F, Colombo MP, Peschle C. Enforced expression of HOXB7 promotes hematopoietic stem cell proliferation and myeloid-restricted progenitor differentiation. Oncogene 1999; 18: 1993-2001. https://doi.org/10.1038/sj.onc.1202498
  25. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978; 276: 565-570. https://doi.org/10.1038/276565a0
  26. Wellik DM. Hox genes and vertebrate axial pattern. Curr Top Dev Biol 2009; 88: 257-278.
  27. Kim KH, Lee YS, Jeon HK, Park JK, Kim CB, Eom KS. Hox genes from the tapeworm Taenia asiatica (Platyhelminthes: Cestoda). Biochem Genet 2007; 45: 335-343. https://doi.org/10.1007/s10528-007-9078-x
  28. Sanchez Alvarado A, Newmark PA, Robb SM, Juste R. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 2002; 129: 5659-5665. https://doi.org/10.1242/dev.00167
  29. Olson PD. Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitol Int 2008; 57: 8-17. https://doi.org/10.1016/j.parint.2007.09.007
  30. Koziol U, Lalanne AI, Castillo E. Hox genes in the parasitic platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: evidence for a reduced Hox complement. Biochem Genet 2009; 47: 100-116. https://doi.org/10.1007/s10528-008-9210-6
  31. Roma J, Almazan-Moga A, Sanchez de Toledo J, Gallego S. Notch, wnt, and hedgehog pathways in rhabdomyosarcoma: from single pathways to an integrated network. Sarcoma 2012; 2012: 695603.
  32. Liu J, Sato C, Cerletti M, Wagers A. Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 2010; 92: 367-409.
  33. Deng WM, Althauser C, Ruohola-Baker H. Notch-Delta signaling induces a transition from mitotic cell cycle to endocycle in Drosophila follicle cells. Development 2001; 128: 4737-4746.

Cited by

  1. Calmodulin-specific small interfering RNA induces consistent expression suppression and morphological changes in Echinococcus granulosus vol.9, pp.None, 2016, https://doi.org/10.1038/s41598-019-40656-w
  2. Comparative Transcriptomic Analysis of the Larval and Adult Stages of Taenia pisiformis vol.10, pp.7, 2019, https://doi.org/10.3390/genes10070507
  3. Evolutionary Transformations of the Metazoan Body Plan: Genomic-Morphogenetic Correlations vol.55, pp.7, 2016, https://doi.org/10.1134/s0031030121070042