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Hymenolepis diminuta (Cestoda) induces changes in expression of select genes of Tribolium confusum (Coleoptera)

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Abstract

The flour beetle Tribolium confusum is a common experimental intermediate host for the tapeworm Hymenolepis diminuta, but while many aspects of their host–parasite interactions have been determined to have genetic basis, the genes involved have not been identified. In this paper, we report on the expression of several predicted metabolic and defense-related genes using quantitative polymerase chain reaction 2 weeks after initial infection of the beetle. The expression of heat shock protein 68, a predicted sugar transporter, a pheromone binding protein, and endoglin were up-regulated in infected beetles. The expression of thaumatin-like protein and prophenoloxidase 2/3 was down-regulated in infected beetles, while the mRNA levels of Toll-like receptor 3, Toll-like receptor 4, and lysozyme 4 were not affected by infection with H. diminuta.

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References

  • Altincicek B, Knorr E, Vilcinskas A (2008) Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum. Dev Comp Immunol 32:585–595

    Article  CAS  PubMed  Google Scholar 

  • Brown SJ, Denell RE, Beeman RW (2003) Beetling around the genome. Genet Res 82:155–161

    Article  CAS  PubMed  Google Scholar 

  • Evans WS, Wong A, Hardy M, Currie RW, Vanderwel D (1998) Evidence that the factor used by the tapeworm, Hymenolepis diminuta, to direct the foraging of its intermediate host, Tribolium confusum, is a volatile attractant. J Parasitol 84:1098–1101

    Article  CAS  PubMed  Google Scholar 

  • Gregório EA, Ratcliffe NA (1991) The prophenoloxidase system and in vitro interaction of Trypanosoma rangeli with Rhodnius prolixus and Triatoma infestans. Parasite Immunol 13:551–564

    Article  PubMed  Google Scholar 

  • Haine ER, Pollitt LC, Moret Y, Silva-Jothy MT, Rolff J (2008) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). J Insect Physiol 54:1090–1097

    Article  CAS  PubMed  Google Scholar 

  • Heyneman D, Voge M (1971) Host response of the flour beetle, Tribolium confusum, to infections with Hymenolepis diminuta, H. microstoma, and H. citelli (Cestoda: Hymenolepididae). J Parasitol 57:881–886

    Article  CAS  PubMed  Google Scholar 

  • Keymer AE (1980) The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81:405–421

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    Article  CAS  PubMed  Google Scholar 

  • Lethbridge RC (1971) The hatching of Hymenolepis diminuta eggs and penetration of the hexacanths in Tenebrio molitor beetles. Parasitology 62:445–456

    Article  CAS  PubMed  Google Scholar 

  • Novak M, Modha A, Blackburn BJ (1993) D-[1-13C]Glucose metabolism of Tribolium confusum parasitized by hymenolepid metacestodes. J Invertebr Pathol 62:302–307

    Article  CAS  Google Scholar 

  • Ovelgönne JH, Souren JEM, Weigant FAC, Van Wijk R (1995) Relationship between cadmium-induced expression of heatshock genes, inhibition of protein synthesis and cell death. Toxicology 99:19–30

    Article  PubMed  Google Scholar 

  • Pai A, Yan G (2003) Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle, Tribolium castaneum. J Parasitol 89:516–521

    Article  PubMed  Google Scholar 

  • Reineke A, Löbman S (2005) Gene expression changes in Ephestia kuehniella caterpillars after parasitization by the endoparasitic wasp Venturia canescens analyzed trough cDNA-AFLPs. J Insect Physiol 51:923–932

    Article  CAS  PubMed  Google Scholar 

  • Robb T, Reid ML (1996) Parasite-induced changes in the behavior of cestode-infected beetles: adaptation or simple pathology? Can J Zool 74:1268–1274

    Article  Google Scholar 

  • Ryan MF, O’Ceallachain DP (1976) Aggregation and sex pheromones in the beetle Tribolium confusum. J Insect Physiol 22:1501–1503

    Article  CAS  Google Scholar 

  • Sabatier L, Jouanguy E, Dostert C, Zachary D, Dimarcq J-L, Bulet P, Imler J-L (2003) Two Drosophila molecules related to pheromone/odor-binding proteins induced by viral and bacterial infections. Eur J Biochem 270:3398–3407

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Weber CB, Letarte M, Kunzmann S, Rückert B, Bernabéu C, Blaser K (2005) TGF-β signaling of human T cells is modulated by the ancillary TGF-β receptor endoglin. Int Immunol 17:921–930

    Article  CAS  PubMed  Google Scholar 

  • Shostak AW, Walsh JG, Wong YC (2006) Shape variation of cysticercoids of Hymenolepis diminuta (Cyclophyllidea) from fed, partially fed, and fasted Tribolium confusum (Colepotera). J Parasitol 92:756–763

    Article  PubMed  Google Scholar 

  • Shostak AW, Walsh JG, Wong YC (2008) Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135:1019–1033

    Article  CAS  PubMed  Google Scholar 

  • Torsney E, Charlton R, Parums D, Collis M, Arthur HM (2002) Inducible expression of human endoglin during inflammation and wound healing in vivo. Inflamm Res 51:464–470

    Article  CAS  PubMed  Google Scholar 

  • Tribolium Genome Sequencing Consortium (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–955

    Article  Google Scholar 

  • Ubelaker JE, Cooper NB, Allison VF (1970) Possible defensive mechanism of Hymenolepis diminuta cysticercoids to hemocytes of the beetle Tribolium confusum. J Invertebr Pathol 16:310–312

    Article  CAS  PubMed  Google Scholar 

  • Voge M, Heyneman D (1957) Development of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Hymenolepididae) in the intermediate host Tribolium confusum. Univ Calif Publ Zool 59:549–579

    Google Scholar 

  • Warr W, Meredith JM, Nimmo DD, Basu S, Hurd H, Eggelston P (2006) A tapeworm manipulates vitellogenin expression in the beetle Tenebrio molitor. Insect Mol Biol 15:497–505

    Article  CAS  PubMed  Google Scholar 

  • Yan G, Norman S (1995) Infection of Tribolium beetles with a tapeworm: variation in susceptibility within and between beetle species and among genetic strains. J Parasitol 81:37–42

    Article  CAS  PubMed  Google Scholar 

  • Yan G, Phillips TW (1996) Influence of tapeworm infection on the production of aggregation pheromone and defensive compounds in Tribolium castaneum. J Parasitol 82:1037–1039

    Article  CAS  PubMed  Google Scholar 

  • Yu KH, Kim KN, Lee JH, Lee HS, Kim SH, Cho KY, Nam MH, Lee IH (2002) Comparative study on characteristics of lysozymes from the hemolymph of three lepidopteran larvae, Galleria mellonella, Bombyx mori, Agrius convolvuli. Dev Comp Immunol 26:707–713

    Article  CAS  PubMed  Google Scholar 

  • Zhang GH, Wang J, Shi X, Wang H, Zheng GK, Wong T, Clark W, Wang J, Wang KL (2007) Identification and characterization of insect-specific proteins by genome data analysis. BMC Genomics 8:93

    Article  PubMed  Google Scholar 

  • Zhong D, Pai A, Yan G (2003) Quantitative trait loci for susceptibility to tapeworm infection in the red flour beetle. Genetics 165:1307–1315

    CAS  PubMed  Google Scholar 

  • Zou Z, Evans JD, Lu Z, Zhao P, Williams M, Sumathipala N, Hetru C, Hultmark D, Jiang H (2007) Comparative genomic analysis of the Tribolium immune system. Genome Biol 8:R177

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by an NSERC operating grant to MB and an NSERC PGS-M graduate fellowship to SJH. We thank Dr. B. Andrew Keddie for reading the manuscript and Dr. Patrick C. Hanington for discussions on optimization of the PCR reactions and RNA isolation techniques. The experiments reported herein were conducted in accordance with the laws of Canada.

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Correspondence to Miodrag Belosevic.

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Hitchen, S.J., Shostak, A.W. & Belosevic, M. Hymenolepis diminuta (Cestoda) induces changes in expression of select genes of Tribolium confusum (Coleoptera). Parasitol Res 105, 875–879 (2009). https://doi.org/10.1007/s00436-009-1481-2

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  • DOI: https://doi.org/10.1007/s00436-009-1481-2

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