Influence of the genetic makeup of common carp on the expression of iron-related genes during Trypanoplasma borreli infection

Open access

Abstract

Introduction: Genes related to iron metabolism play an important role in inflammatory response. The objective of this study was to investigate the role of ferritin, transferrin receptors 1a and 1b, and transferrin genes in the response to blood parasite infection in common carp (Cyprinuscarpio L.).

Material and Methods: Two genetically distinct carp groups were used: R3 carp, which are established as being sensitive to parasitic infection, and SA carp (Cyprinus carpio haematopterus) of wild origin. An established challenge model with Trypanoplasma borreli was applied. Challenged carp were sampled to determine their expression levels of transferrin receptors 1a and 1b, ferritin, and transferrin mRNA. Mortality and serum iron concentration were also measured.

Results: The study revealed contrasting differences in the expression profiles of all key iron regulatory genes except the transferrin gene. In the case of other parameters, significant differences were also observed.

Conclusion: Our results demonstrate that the level of parasitic infection depends on the blood iron status. This parameter was related to the origin of the fish.

1. Aisen P., Enns C., Wessling-Resnick M.: Chemistry and biology of eukaryotic iron metabolism. Int J Biochem Cell Biol 2001, 33, 940–959.

2. Bayne C.J., Gerwick L.: The acute phase response and innate immunity of fish. Develop Comp Immunol 2001, 25, 725–743.

3. Bogdan C.: Nitric oxide and the regulation of gene expression. Trends Cell Biol 2001, 11, 66–75.

4. Brucka-Jastrzębska E., Kawczuga D., Rajkowska M., Protasowicki M.: Levels of microelements (Cu, Zn, Fe) and macroelements (Mg, Ca) in freshwater fish. J Elementol 2009, 14, 437–447.

5. Brzuska E.: Artificial propagation of female Hungarian strain 7 carp (Cyprinus carpio) after treatment with carp pituitary homogenate, Ovopel or Dagin. Czech J Anim Sci 2006, 51, 132–141.

6. Elvitigala D.A.S., Premachandra H.K.A., Whang I., Oh M.J., Jung S.J., Park C.J., Lee J.: A teleostean counterpart of ferritin M subunit from rock bream (Oplegnathusfasciatus): An active constituent in iron chelation and DNA protection against oxidative damage, with a modulated expression upon pathogen stress. Fish Shellfish Immunol 2013, 35, 1455–1465.

7. Feng C.Y., Johnson S.C., Hori T.S., Rise M., Hall J.R., Gamperl A.K., Hubert S., Kimball J., Bowman S., Rise M.L.: Identification and analysis of differential expressed genes in immune tissues of Atlantic cod stimulated with formalin-killed, atypical Aeromonassalmonicida. Physiol Genom 2009, 37, 149–163.

8. Forlenza M., Nakao M., Wibowo I., Joerink M., Arts J.A., Savelkoul H.F., Wiegertjes G.F.: Nitric oxide hinders antibody clearance from the surface of Trypanoplasma borreli and increases susceptibility to complement-mediated lysis. Mol Immunol 2009, 46, 3188–3197.

9. Gabay C., Kushner I.: Acute-phase protein and other systemic response to inflammation. New Engl J Med 1999, 340, 448–454.

10. Graham R.M., Chua A.C.G., Herbison C.E., Olynyk J.K., Trinder D.: Liver iron transport. World J Gastroenterol 2007, 13, 4725–4736.

11. Jurecka P., Irnazarow I., Westphal A.H., Forlenza M., Arts J.A.J., Savelhoul H.F.J., Wiegertjes G.F.: Allelic discrimination, three-dimensional analysis end gene expression of multiple transferrin alleles of common carp (Cyprinus carpio L.). Fish Shellfish Immunol 2009, 26, 573–581.

12. Kazuń K., Siwicki A.K.: Propiscine – a new safe anaesthetic for fish. Arch Polish Fisher 2001, 9, 95–102.

13. Liu H., Takano T., Abernathy J., Wang S., Sha Z., Jiang Y., Terhune J., Kucuktas H., Peatman E., Liu Z.: Structure and expression of transferrin gene of channel catfish, Ictalurus punctatus. Fish Shellfish Immunol 2010, 28, 159–166.

14. Liu Y., Yu S., Chai Y., Zhu Q.: Transferrin gene expression in response to LPS challenge and heavy metal exposure in roughskin sculpin (Trachidermus fasciatus). Fish Shellfish Immunol 2012, 32, 223–229.

15. Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402–408.

16. Lu X.J., Chen J., Huang Z.A., Zhuang L., Peng L.Z., Shi Y.H.: Influence of acute cadmium exposure on the liver proteome of a teleost fish, ayu (Plecoglossus altivelis). MolBiol Reports 2012, 39, 2851–2859.

17. Magarinos B., Romalde J.L., Lemos M.L., Barja J.L., Toranzo A.F.: Iron uptake by Pasteurella piscicida and its role in pathogenicity for fish. Appl Environ Microbiol 1994, 60, 2990–2998.

18. Mohd-Shaharuddin N., Mohd-Adnan A., Kua B.C., Nathan S.: Expression profile of immune-related genes in Lates calcarifer infected by Cryptocaryon irritans. Fish Shellfish Immunol 2013, 34, 762–769.

19. Neves J.V., Wilson J.M., Rodrigues P.N.S.: Transferrin and ferritin response to bacterial infection: The role of liver and brain in fish. Develop Comp Immunol 2009, 33, 848–857.

20. Peatman E., Baoprasertkul P., Terhune J., Xu P., Nandi S., Kucuktas H., Li P., Wang S., Somridhivej B., Dunham R., Liu Z.: Expression analysis of the acute phase response in channel catfish (Ictalurus punctatus) after infection with a Gram-negative bacterium. Develop Comp Immunol 2007, 31, 1183–1196.

21. Schreiber G., Tsykin A., Aldred A.R., Thomas T., Fung W.P., Dickson P.W., Cole T., Birch H., de Jong F.A., Milland J.: The acute phase response in the rodent. Ann NY Acad Sci 1989, 557, 61–85.

22. Steinhagen D., Kruse P., Korting W.: Some haematological observations on carp, Cyprinus carpio L., experimentally infected with Trypanoplasma borreli Laveran & Mesnil, 1901 (Protozoa: Kinetoplastida). J Fish Dis 1990, 13, 157–162.

23. Steverding D., Stierhof Y.D., Chaudhri M., Ligtenberg M., Schell D., Beck-Sickinger A.G., Overath P.: ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Europ J Cell Biol 1994, 64, 78–87.

24. Torti F.M., Torti S.V.: Regulation of ferritin genes and protein. Blood 2002, 99, 3505–3516.

25. Vale-Costa S., Gomes-Pereira S., Miguel Teixeira C., Nuno Rodrigues P., Tomás A., Appelberg R., Salomé Gomes M.: Iron overload favors the elimination of Leishmania infantum from mouse tissues through interaction with reactive oxygen and nitrogen species. PLoS Neglected Trop Dis 2013, 7, e2061.

26. Weiss G., Bogdan C., Hentze M.W.: Pathways for regulation of macrophage iron metabolism by the anti-inflammatory cytokines IL-4 and Il-13. J Immunol 1997, 158, 420–425.

27. Wiegertjes G.F., Forlenza M., Joerink M., Scharsack J.P.: Parasite infection revisited. Develop Comp Immunol 2005, 29, 749–758.

28. Woo P.T.K., Ardeli B.F.: Immunity against selected piscine flagellates. Develop Comp Immunol 2014, 43, 268–279.

29. Yang C.G., Liu S.S., Sun B., Wang X.L., Wang N., Chen S.L.: Iron-metabolic function and potential antibacterial role of Hepcidin and its correlated genes (Ferroportin 1 and Transferrin Receptor) in turbot (Scophthalmus maximus). Fish Shellfish Immunol 2013, 34, 744–755.

Journal of Veterinary Research

formerly Bulletin of the Veterinary Institute in Pulawy

Journal Information


IMPACT FACTOR J Vet Res 2017: 0.811

CiteScore 2017: 0.68

SCImago Journal Rank (SJR) 2017: 0.29
Source Normalized Impact per Paper (SNIP) 2017: 0.484

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