Advertisement

Parasitology Research

, Volume 118, Issue 5, pp 1573–1579 | Cite as

Intestinal injury caused by Eimeria spp. impairs the phosphotransfer network and gain weight in experimentally infected chicken chicks

  • Gabriela M. Galli
  • Matheus D. Baldissera
  • Luiz Gustavo Griss
  • Carine F. Souza
  • Bruno F. Fortuoso
  • Marcel M. Boiago
  • Anderson Gris
  • Ricardo E. Mendes
  • Lenita M. Stefani
  • Aleksandro S. da SilvaEmail author
Protozoology - Original Paper
  • 120 Downloads

Abstract

Parasitic infections caused by protozoan belonging to genus Eimeria are considered important for the poultry industry, due to their severe intestinal lesions and high mortality rates, causing significant economic losses. Although several mechanisms of coccidiosis pathogenesis are known, the effects of this infection on intestinal enzymes linked to adenosine triphosphate (ATP) metabolism, as creatine kinase (CK), adenylate kinase (AK), and pyruvate kinase (PK), remain unknown. Thus, the aim of this study was to evaluate whether coccidiosis impairs enzymes linked ATP metabolism in the intestine of chicken chicks. For this, 42 animals that were 2 days old were divided into two groups: uninfected (the negative control group) and experimentally infected on second day of life (the positive control group). On days 5, 10, and 15 post-infection (PI), fecal samples were collected for oocyst counts; intestinal tissue was collected in order to evaluate CK, AK, and PK activities, as well as parameters of the oxidative stress and histopathology. On days 10 and 15 PI, infected animals showed high counts of oocysts in fecal samples and intestinal lesions compared to the control group. Cytosolic CK activity was higher in infected animals on days 10 and 15 PI compared to the control group, while mitochondrial CK activity was lower on days 5, 10, and 15 PI. Also, AK activity was lower in infected animals on days 10 and 15 PI compared to control group, while no differences were observed between groups regarding PK activity. In relation to parameters of oxidative stress, intestinal lipid peroxidation and reactive oxygen species levels were higher in infected animals on days 10 and 15 PI compared to the control group, while non-protein thiol levels were lower on day 10 PI. On the 15th day, infected animals had lower body weight (P < 0.05). Based on this evidence, inhibition of mitochondrial CK activity causes an impairment of intestinal energetic homeostasis possibly through depletion on ATP levels, although the cytosolic CK activity acted as an attempt to restore the mitochondrial ATP levels through a feedback mechanism. Moreover, the impairment on energy metabolism appears to be mediated by excessive production of intestinal ROS, as well as oxidation of lipids and thiol groups.

Keywords

Poultry farm Coccidiosis Oxidative stress Energetic metabolism 

Notes

Acknowledgements

We thank CAPES and CNPq for their financial support.

Compliance with ethical standards

Commission of ethics

All procedures were approved by the Ethical and Animal Welfare Committee (CEUA) from the Universidade do Estado de Santa Catarina (UDESC), under protocol number 3096260917.

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Alekssev AE, Reyes S, Selivanov VA, Dzeja PP, Terzic A (2012) Compartmentation of membrane processes and nucleotide dynamics in diffusion-restricted cardiac cell microenvironment. J Mol Cell Cardiol 52:401–409CrossRefGoogle Scholar
  2. Baldissera MD, Oliveira CB, Rech VC, Rezer JFP, Sagrillo MR, Alves MP, da Silva AS, Leal DBR, Boligon AA, Athayde ML, Da Silva AS, Mendes RE, Monteiro SG (2014) Treatment with essential oil of Achyrocline satureioides in rats infected with Trypanosoma evansi: relationship between protective effect and tissue damage. Pathol Res Pract 210:1068–1074CrossRefGoogle Scholar
  3. Baldissera MD, Souza CF, Grando TH, Dolci GS, Cossetin LF, Moreira KL, DA Veiga ML, DA Rocha MI, Boligon AA, DE Campos MM, Stefani LM, DA Silva AS, Monteiro SG (2017a) Nerolidol-loaded nanospheres prevent hepatic oxidative stress of mice infected by Trypanosoma evansi. Parasitology 144:148–157CrossRefGoogle Scholar
  4. Baldissera MD, Souza CF, Júnior GB, Verdi CM, Moreira KLS, da Rocha MIUM, da Veiga MIUM, Santos RCV, Vizzotto BS, Baldisserotto B (2017b) Aeromonas caviae alters the cytosolic and mitochondrial creatine kinase activities in experimentally infected silver catfish: impairment on renal bioenergetics. Microb Pathog 110:439–443CrossRefGoogle Scholar
  5. Baldissera MD, Souza CF, Baldisserotto B (2018a) Ichthyophthirius multifiliis impairs splenic enzymes of the phosphoryl transfer network in naturally infected Rhamdia quelen: effects on energetic homeostasis. Parasitol Res 117:413–418CrossRefGoogle Scholar
  6. Baldissera MD, Souza CF, Seben D, Sippert LR, Salbego J, Marchesan E, Zanella R, Baldisserotto B, Golombieski J (2018b) Gill bioenergetics dysfunction and oxidative damage induced by thiamethoxam exposure as relevant toxicological mechanisms in freshwater silver catfish Rhamdia quelen. Sci Total Environ 636:420–426CrossRefGoogle Scholar
  7. Biazus AH, Da Silva AS, Bottari NB, Baldissera MD, do Carmo GM, Morsch VM, Schetinger MRC, Casagrande R, Guarda NS, Moresco RN, Stefani LM, Campigotto G, Boiago MM (2017) Fowl typhoid in laying hens cause hepatic oxidative stress. Microb Pathog 103:162–166CrossRefGoogle Scholar
  8. Carrasco AJ, Dzeja PP, Alekssev AE, Pucar D, Zingman LV, Abraham MR, Hodgson D, Bienengraeber M, Puceat M, Janssen E, Wieringa B, Terzic A (2001) Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proc Natl Acad Sci 98:7623–7628CrossRefGoogle Scholar
  9. Dalloul RA, Lillehoj HS (2006) Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Rev Vaccines 5:143–163CrossRefGoogle Scholar
  10. Dzeja PP, Terzic A (2003) Phosphotransfer networks and cellular energetics. J Exp Biol 206:2039–2047CrossRefGoogle Scholar
  11. Dzeja P, Terzic A (2009) Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci 10(4):1729–1772CrossRefGoogle Scholar
  12. Dzeja PP, Vitkevicius KT, Redfield MM, Burnettm JC, Terzic A (1999) Adenylate kinase-catalyzed phosphotransfer in the myocardium: increased contribution in heart failure. Circ Res 84:1137–1143CrossRefGoogle Scholar
  13. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77CrossRefGoogle Scholar
  14. Freitas FLC, Almeida KS, Machado RZ, Machado CR (2008) Lipid and glucose metabolism of broilers (Gallus gallus domesticus) experimentally infected with Eimeria acervulina Tyzzer, 1929 oocysts. Rev Bras Cienc Avic 10:157–162CrossRefGoogle Scholar
  15. Glaser V, Leipnitz G, Straliotto MR, Oliveira J, dos Santos VV, Wannmacher CMD, de Bem AF, Rocha JBT, Farina M, Latini A (2010) Oxidative stress-mediated inhibition of brain creatine kinase activity by methylmercury. Neuro Toxicol 31:454–460Google Scholar
  16. Hughes BP (1962) A method for estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathological sera. Clin Chim Acta 7:597–603CrossRefGoogle Scholar
  17. Janssen E, Dzeja PP, Oerlemans F, Simonetti AW, Heerschap A, de Haan A, Rush PS, Terjung RR, Wieringa B, Terzic A (2000) Adenylate kinase 1 gene deletion disrupts muscle energetic economy despite metabolic rearrangement. EMBO J 19:6371–6381CrossRefGoogle Scholar
  18. Kitessa SM, Nattrass GS, Forder RE, McGrice HA, Wu SB, Hughes RJ (2014) Mucin gene mRNA levels in broilers challenged with Eimeria and/or Clostridium perfringens. Avian Dis 58:408–414Google Scholar
  19. Koinarski V, Gabrashanska M, Georgieva NV, Petkov P (2005) (2005). Antioxidant status of broiler chickens infected with Eimeria acervulina. Rev Méd Vét 156:498–502Google Scholar
  20. Koinarski V, Gabrashanska M, Georgieva N, Petkov P (2006) Antioxidant parameters in Eimeria acervulina infected chicks after treatment with a new zinc compound. Bull Vet Inst Pulawy 50:55–61Google Scholar
  21. Koufen P, Stark G (2000) Free radical induced inactivation of creatine kinase: sites of interaction, protection and recovery. Biochim Biophys Acta 1501:44–50CrossRefGoogle Scholar
  22. Lebel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231CrossRefGoogle Scholar
  23. Leong SF, Lai JKF, Lim L, Clark JB (1981) Energy-metabolism in brain regions of adult and aging rats. J Neurochem 37:1548–1556CrossRefGoogle Scholar
  24. Monteiro SV (2010) Técnicas laboratoriais. In: Monteiro SV. (ed) Parasitologia na Medicina Veterinária. Roca, São Paulo, p.301-312Google Scholar
  25. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefGoogle Scholar
  26. Read SM, Northcote DH (1981) Minimization of variation in the response to different proteins of the Coomassie blue G dye-binding assay for protein. Anal Biochem 116:53–64CrossRefGoogle Scholar
  27. Ritzi MM, Abdelrahman W, van-Heerden K, Mohnl M, Barrett NW, Dalloul RA (2016) Combination of probiotics and coccidiosis vaccine enhances protection against an Eimeria challenge. Vet Res 47:111-115Google Scholar
  28. Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RF, Lopes DC, Ferreira AS, Barreto SLT, Euclides RF (2011) Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais de aves e suínos. 3ªedição, UFV, Viçosa, p. 252 Google Scholar
  29. Schlattner U, Tokarska-Schlattner M, Wallimann T (2006) Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 1762:164–180CrossRefGoogle Scholar
  30. Venkataraman P, Krishnamoorthy G, Selvakumar K, Arunakaran J (2009) Oxidative stress alters creatine kinase system in serum and brain regions of polychlorinated biphenyl (Aroclor 1254)-exposed rats: protective role of melatonin. Basic Clin Pharmacol Toxicol 105:92–97CrossRefGoogle Scholar
  31. Wang H, Chu W, Das SK, Ren Q, Hasstedt SJ, Elbein SC (2002) Liver pyruvate kinase polymorphisms are associated with type 2 diabetes in Northern European Caucasians. Diabetes 51:2861–2865CrossRefGoogle Scholar
  32. Winterbourne CC (2015) Are free radicals involved in thiol-based redox signaling? Free Radic Biol Med 80:164–170CrossRefGoogle Scholar
  33. Xing H, Li S, Wang Z, Gao X, Xu S, Wang X (2012) Oxidative stress response and histopathological changes due to atrazine and chlorpyrifos exposure in common carp. Pestic Biochem Physiol 103:74–80CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Gabriela M. Galli
    • 1
  • Matheus D. Baldissera
    • 2
  • Luiz Gustavo Griss
    • 3
  • Carine F. Souza
    • 4
  • Bruno F. Fortuoso
    • 2
  • Marcel M. Boiago
    • 1
    • 3
  • Anderson Gris
    • 5
  • Ricardo E. Mendes
    • 5
  • Lenita M. Stefani
    • 1
    • 3
  • Aleksandro S. da Silva
    • 1
    • 3
    • 4
    Email author
  1. 1.Graduate Program in Animal ScienceUniversidade do Estado de Santa Catarina (UDESC)ChapecoBrazil
  2. 2.Department of Microbiology and ParasitologyUniversidade Federal de Santa Maria (UFSM)Santa MariaBrazil
  3. 3.Department of Animal ScienceUniversidade do Estado de Santa Catarina (UDESC)ChapecoBrazil
  4. 4.Graduate Program of Toxicological BiochemistryUniversidade Federal de Santa Maria (UFSM)Santa MariaBrazil
  5. 5.Laboratory of Veterinary PathologyInstituto Federal Catarinense – IFCConcordiaBrazil

Personalised recommendations