Folia Parasitologica, vol. 64 (2017)

Folia Parasitologica 64:012 (2017) | 10.14411/fp.2017.012

Gene expression, oxidative stress and apoptotic changes in rabbit ileum experimentally infected with Eimeria intestinalis

Heba M. Abdel-Haleem1, Shawky M. Aboelhadid2, Thabet Sakran1, Gamal El-Shahawy1, Huda El-Fayoumi1, Saleh Al-Quraishy3, Abdel-Azeem S. Abdel-Baki1,3
1 Zoology Department, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt;
2 Parasitology Department, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef, Egypt;
3 Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

Coccidiosis is a parasitic disease caused by protists (apicomplexans) of the genus Eimeria Schneider, 1875 and is considered to be the most important disease faced by rabbit breeders due to its high morbidity. In the present study, the antioxidant status and changes in apoptosis and in the expression of some genes were quantified in rabbits' ilea following infection with Eimeria intestinalis Cheissin, 1948. Rabbits, orally infected with 1 × 105 sporulated oocysts of E. intestinalis, started to shed oocysts in their faeces on 8 days post infection (dpi) and reached maximum excretion on 10 dpi, with approximately 5 million oocysts. This was accompanied by a significant decrease in the live body weight of infected rabbits. Also, malondialdehyde and nitric oxide were significantly increased while catalase and glutathione were significantly decreased in the ileum tissues of the infected rabbits. In addition, a significant increase was observed in the percentages of apoptotic cells in the ilea of the infected rabbits. Furthermore, interleukin-1β and interleukin-2 mRNA levels were significantly down-regulated and mRNA levels of interleukin-6, interferon gamma and inducible nitric oxide synthase were significantly up-regulated, while those of C-reactive protein remained unchanged. We conclude that infection with E. intestinalis induces oxidative stress, a significant increase in the percentage of apoptotic cells and a diverse and robust Th1 and Th1-related cytokine response in the ileum tissues.

Keywords: Coccidia, malondialdehyde, catalase, intestine, Real time PCR, apoptosis

Received: October 28, 2016; Accepted: March 20, 2017; Published online: April 19, 2017


References

  1. Aebi H. 1984: Catalase. In: H.U. Bergmeyer (Ed.), Methods of Enzymatic Analysis. Academic Press, New York, pp. 673-684.
  2. Ahmed W.M., Hassan S.E. 2007: Applied studies on coccidiosis in growing buffalo-calves with special reference to oxidant/antioxidant status. World J. Zool. 2: 40-48.
  3. Alcala-Canto Y., Ibarra-Velarde F. 2008: Cytokine gene expression and NF-kappa B activation following infection of intestinal epithelial cells with Eimeria bovis or Eimeria alabamensis in vitro. Parasite Immunol. 30: 175-179. Go to original source... Go to PubMed...
  4. Badr G., Garraud O., Daghestani M., Al-Khalifa M.S., Richard Y. 2012: Human breast carcinoma cells are induced to apoptosis by samsum ant venom through an IGF-1-dependant pathway, PI3K/AKT and ERK signaling. Cell. Immunol. 273: 10-16. Go to original source... Go to PubMed...
  5. Balicka-Ramisz A., Wróbel M., Adadyńska K. 2014: Epidemiology and economic benefits of treating rabbits coccidiosis in small farms from West Pomerania province, Poland. Ann. Parasitol. 60: 247-251.
  6. Beutler E., Duron O., Kelly B.M. 1963: Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 61: 882-888. Go to PubMed...
  7. Çam Y., Atasever A., Eraslan G., Kibar M., Atalay O., Beyaz L., İnci A., Liman B.C. 2008: Eimeria stiedae: experimental infection in rabbits and the effect of treatment with toltrazuril and ivermectin. Exp. Parasitol. 119: 164-172. Go to original source... Go to PubMed...
  8. Chapman H.D. 1997: Biochemical, genetic and applied aspects of drug resistance in Eimeria parasites of the fowl. Avian Pathol. 26: 221-244. Go to original source... Go to PubMed...
  9. Cornelissen J.B., Swinkels W.J., Boersma W.A., Rebel J.M. 2009: Host response to simultaneous infections with Eimeria acervulina, maxima and tenella: a cumulation of single responses. Vet. Parasitol. 162: 58-66. Go to original source... Go to PubMed...
  10. Dkhil M., Abdel-Baki A.S., Delić D., Wunderlich F., Sies H., Al-Quraishy S. 2011: Eimeria papillata: upregulation of specific miRNA-species in the mouse jejunum. Exp. Parasitol. 127: 581-586. Go to original source... Go to PubMed...
  11. Dkhil M.A., Abdel-Maksoud M.A., Al-Quraishy S., Abdel-Baki A.S., Wunderlich F. 2012: Gene expression in rabbit appendices infected with Eimeria coecicola. Vet. Parasitol. 186: 222-228. Go to original source... Go to PubMed...
  12. Dortay H., Schmöckel S.M., Fettke J., Mueller-Roeber B. 2011: Expression of human C-reactive protein in different systems and its purification from Leishmania tarentolae. Protein Expr. Purif. 78: 55-60. Go to original source... Go to PubMed...
  13. Drouet-Viard F., Coudert P., Licois D., Boivin M. 1997: Vaccination against Eimeria magna coccidiosis using spray dispersion of precocious line oocysts in the nest box. Vet. Parasitol. 70: 61-66. Go to original source... Go to PubMed...
  14. Elfayoumi H., Abdel-Haleem H.M. 2014: Electron microscopic study of the developmental stages of Eimeria intestinalis Cheissin, 1948 in domestic rabbit (Oryctolagus cuniculus) with reference to endodyogeny. J. Egypt. Soc. Parasitol. 44: 531-538. Go to original source... Go to PubMed...
  15. El-Shahawi G.A., El-Fayomi H.M., Abdel-Haleem H.M. 2012. Coccidiosis of domestic rabbit (Oryctolagus cuniculus) in Egypt: light microscopic study. Parasitol. Res. 110: 251-258. Go to original source... Go to PubMed...
  16. Eraslan G., Çam Y., Eren M., Liman B.C. 2004: Changes in malondialdehyde level and catalase activity and effect of toltrazuril on these parameters in chicks infected with Eimeria tenella. Bull. Vet. Inst. Pulawy 48: 251-255.
  17. Fisch S., Gray S., Heyman S., Haldar S.M., Wang B., Pfister O., Cui L., Kumar A., Lin Z., Sen-Banerjee S., Das H., Peterson C.A., Mende U., Burleigh B.A., Zhu Y., Pinto Y., Liao R., Jain M.K. 2007: Kruppel-like factor 15 is a regulator of cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. USA 104: 7074-7079. Go to original source...
  18. Green D.R. 2000: Apoptotic pathways: paper wraps stone blunts scissors. Cell 102: 1-4. Go to original source... Go to PubMed...
  19. Georgieva N.V., Koinarski V., Gadjeva V. 2006: Antioxidant status during the course of Eimeria tenella infection in broiler chickens. Vet. J. 172: 488-492. Go to original source... Go to PubMed...
  20. Hishikawa K., Oemar B.S., Tanner F.C., Nakaki T., Lüscher T.F., Fujii T. 1999: Connective tissue growth factor induces apoptosis in human breast cancer cell line MCF-7. J. Biol. Chem. 274: 37461-37466. Go to original source... Go to PubMed...
  21. Hong Y.H., Lillehoj H.S., Lee S.H., Dalloul R.A., Lillehoj E.P. 2006: Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 114: 209-223. Go to original source... Go to PubMed...
  22. Kaiser P., Rothwell L., Galyov E.E., Barrow P.A., Burnside J., Wigley P. 2000: Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiology 12: 3217-3226. Go to original source... Go to PubMed...
  23. Kang K.W., Wagley Y., Kim H.W., Pokharel Y.R., Chung Y.Y., Chang I.Y., Kim J.J., Moon J.S., Kim Y.K., Nah S.Y., Kang H.S., Oh J.W. 2007: Novel role of IL-6/SIL-6R signaling in the expression of inducible nitric oxide synthase (iNOS) in murine B16, metastatic melanoma clone F10.9, cells. Free Radic. Biol. Med. 42: 215-227. Go to original source... Go to PubMed...
  24. Kvičerová J., Pakandl M., Hypša V. 2008: Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: evolutionary significance of biological and morphological features. Parasitology 135: 443-452. Go to PubMed...
  25. Li M., Ooi H. 2009: Fecal occult blood manifestation of intestinal Eimeria spp. infection in rabbit. Vet. Parasitol. 161: 327-329. Go to original source... Go to PubMed...
  26. Liu J., Deng M., Lancto C.A., Abrahamsen M.S., Rutherford M.S., Enomoto S. 2009: Biphasic modulation of apoptotic pathways in Cryptosporidium parvum infected human intestinal epithelial cells. Infect. Immun. 77: 837-849. Go to original source... Go to PubMed...
  27. Livak K.J., Schmittgen T.D. 2001: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408. Go to original source... Go to PubMed...
  28. Lüder C.K., Stanway R.R., Chaussepied M., Langsley G., Heussler V.T. 2009: Intracellular survival of apicomplexan parasites and host cell modification. Int. J. Parasitol. 39: 163-173. Go to original source... Go to PubMed...
  29. Lüder C.K., Walter W., Beuerle B., Maeurer M.J., Gross U. 2001: Toxoplasma gondii down-regulates MHC class II gene expression and antigen presentation by murine macrophages via interference with nuclear translocation of STAT1alpha. Eur. J. Immunol. 31: 1475-1484. Go to original source... Go to PubMed...
  30. Lynagh G.R., Bailey M., Kaiser P. 2000: Interleukin-6 is produced during both murine and avian Eimeria infections. Vet. Immunol. Immunopathol. 76: 89-102. Go to original source... Go to PubMed...
  31. Maalouf S.W., Talhouk R.S., Schanbacher F.L. 2010: Inflammatory responses in epithelia: endotoxin-induced IL-6 secretion and iNOS/NO production are differentially regulated in mouse mammary epithelial cells. J. Inflamm. 7: 58. Go to original source... Go to PubMed...
  32. MacMicking J., Xie Q.W., Nathan C. 1997: Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350. Go to original source... Go to PubMed...
  33. Major P., Tóth S., Goldová M., Révajová V., Kožárová I., Levkut M., Mojžišová J., Hisira V., Mihok T. 2011: Dynamic of apoptosis of cells in duodenal villi infected with Eimeria acervulina in broiler chickens. Biologia 66: 696-700. Go to original source...
  34. Marnell L., Mold C., Du Clos T.W. 2005: C-reactive protein: ligands, receptors and role in inflammation. Clin. Immunol. 117: 104-111. Go to original source... Go to PubMed...
  35. Metwaly M.S., Dkhil M.A., Al-Quraishy S. 2014: Anti-coccidial and anti-apoptotic activities of palm pollen grains on Eimeria papillata-induced infection in mice. Biologia 69: 254-259. Go to original source...
  36. Metwaly M.S., Dkhil M.A., Gewik M.M., Al-Ghamdy A.O., Al-Quraishy S. 2013: Induced metabolic disturbance and growth depression in rabbits infected with Eimeria coecicola. Parasitol. Res. 112: 3109-3114. Go to original source... Go to PubMed...
  37. Montgomery H.A.C., Dymock J.E. 1961. The determination of nitrite in water. Analyst 86: 414-416.
  38. Ohkawa H., Ohishi N., Yagi K. 1979: Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95: 351-358. Go to original source... Go to PubMed...
  39. Oncel T., Gulegen E., Senlik B., Bakirci S. 2011: Intestinal coccidiosis in angora rabbits (Oryctolagus cuniculus) caused by Eimeria intestinalis, Eimeria perforans and Eimeria coecicola. Yüzüncü Yil Üniversitesi Vet. Fak. Derg. 22: 27-29.
  40. Pakandl M. 2009: Coccidia of rabbit: a review. Folia Parasitol. 56: 153-166. Go to original source... Go to PubMed...
  41. Pakandl M., Hlásková L., Poplštein M., Chromá V., Vodička T., Salát J., Mucksová J. 2008: Dependence of the immune response to coccidiosis on the age of rabbit suckling. Parasitol. Res. 103: 1265-1271. Go to original source... Go to PubMed...
  42. Pakandl M., Sewald B., Drouet-Viard F. 2006: Invasion of the intestinal tract by sporozoites of Eimeria coecicola and Eimeria intestinalis in naive and immune rabbits. Parasitol. Res. 98: 310-316. Go to original source... Go to PubMed...
  43. Rasul A., Ding C., Li X., Khan M., Yi F., Ali M., Ma T. 2012: Dracorhodin perchlorate inhibits PI3K/Akt and NF-κB activation, up-regulates the expression of p53, and enhances apoptosis. Apoptosis 17: 1104-1119. Go to original source... Go to PubMed...
  44. Renaux S., Quéré P., Buzoni-Gatel D., Sewald B., Le Vern Y., Coudert P., Drouet-Viard F. 2003: Dynamics and responsiveness of T-lymphocytes in secondary lymphoid organs of rabbits developing immunity to Eimeria intestinalis. Vet. Parasitol. 110: 181-195. Go to original source... Go to PubMed...
  45. Salminen A., Hyttinen J.M., Kauppinen A., Kaarniranta K. 2012: Context-dependent regulation of autophagy by IKK-NF-κB signaling: impact on the aging process. Int. J. Cell. Biol. 2012: 1-15.
  46. Schito M.L., Barta J.R., Chobotar B. 1996: Comparison of four murine Eimeria species in immunocompetent and immunodeficient mice. J. Parasitol. 82: 255-262. Go to original source... Go to PubMed...
  47. Swaggerty C.L., Kogut M.H., Ferro P.J., Rothwell L., Pevzner I.Y., Kaiser P. 2004: Differential cytokine mRNA expression in heterophils isolated from Salmonella-resistant and -susceptible chickens. Immunology 113: 139-148. Go to original source... Go to PubMed...
  48. Taubert A., Behrendt J.H., Sühwold A., Zahner H., Hermosilla C. 2009: Monocyte- and macrophage-mediated immune reactions against Eimeria bovis. Vet. Parasitol. 164: 141-153. Go to original source... Go to PubMed...
  49. Vadlejch J., Knízková I., Makovcová K., Kunc P., Jankovská I., Janda K., Borkovcová M., Langrová I. 2010: Thermal profile of rabbits infected with Eimeria intestinalis. Vet. Parasitol. 171: 343-345. Go to original source... Go to PubMed...
  50. Yan Z., Ming-Xue Z., Zhi-Yong X., Huan-Cheng X., Xiao-Zhen C., Sha-Sha Y., Wen-Long Z., Shan L., Qiang-Hua L., Rui B. 2015: Relationship between Eimeria tenella development and host cell apoptosis in chickens. Poult. Sci. 94: 2970-2979. Go to original source... Go to PubMed...