Advertisement

Acta Parasitologica

, Volume 63, Issue 1, pp 198–209 | Cite as

Syphacia muris infection in rats attenuates colorectal carcinogenesis through oxidative stress and gene expression alterations. Implications for modulatory effects by Bryostatin-1

  • Elsayed I. SalimEmail author
  • Samar F. Harras
  • Aisha G. Abdalla
  • Mohmmed H. Mona
Article
First Online:

Abstract

Accumulating evidence suggest that some infectious agents may interfere in the natural progression of neoplasia. This study examined the association between chronic infection with adult Syphacia muris parasites and 1,2-dimethylhydrazine (DMH)-induced colorectal carcinogenesis in rats. In addition, the conceivable therapeutic effect of Bryostatin-1, a potent extract of the marine Bryozoan, Bugulane ritina, was investigated against this combined effect.DMH administration has induced aberrant crypt foci (ACF), surrogate biomarkers for colorectal carcinogenesis, while the S. muris infection combined with DMH has significantly increased the total numbers of ACF. Nonetheless, treatment with Bryostatin-1 after infection has significantly reduced the ACF numbers particularly larger ones. This inhibition was concomitant with significant inhibition in the immunohisto-chemical levels of the ki67, Caspase-3 and IgM levels in colorectal epithelium, as well as serum levels of IgM and IgG. Additionally, treatment with Bryostatin-1 after S. muris + DMH has modulated enzymatic antioxidative markers levels of superoxide dismutase and catalase as well as the non-enzymatic antioxidant markers levels of reduced glutathione, lipid peroxidation, nitric oxide and total antioxidant capacity. Further, treatment with Bryostatin-1 has down-regulated the mRNA expression levels of COX-2 and APC genes in colorectal mucosa. In conclusion, infection with S. muris during colorectal carcinogenesis has significantly modulated the oxidative stress markers in the colorectum, while treatment with Bryostatin-1 has exerted significant curative potential. A mechanism could be explained that Bryostatin-1 treatment has reduced oxidative stress markers activities along with affecting host to parasite immunity possibly leading to changes in the COX-2 and APC expression, retarding cellular proliferation and subsequently reducing the colorectal carcinogenesis events.

Keywords

DMH Syphacia muris Bryostatin-1 ROS Rat COX-2 APC IgG IgM Ki67 Caspase-3 ACF 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alberts B., Johnson A., Lewis J., Walter P., Raff M., Roberts K., et al. 2002. Chapter 24. Molecular Biology of the Cell (4th ed.). New York: Garland Science; Molecular Biology of the Cell, 4th edition. ISBN-10: 0-8153-3218-1ISBN-10: 0-8153-4072-9Google Scholar
  2. Alkon D.L., Hongpaisan J., Sun M.K. 2017. Effects of chronic bryo-statin-1 on treatment-resistant depression in rats. European Journal of Pharmacology, PII, S0014-2999(17)30304-7. DOI: 10.1016/j.ejphar.2017.05.001Google Scholar
  3. Atari-Hajipirloo S., Nikanfar S., Heydari A., Noori F., Kheradmand F. 2016. The effect of celecoxib and its combination with imatinib on human HT-29 colorectal cancer cells: Involvement of COX-2, Caspase-3, VEGF and NF-κB genes expression. Cellular and Molecular Biology, 62, 68–74PubMedGoogle Scholar
  4. Balaji C., Muthukumaran J., Nalini N. 2015. Effect of sinapic acid on 1,2 dimethylhydrazine induced aberrant crypt foci, biotrans-forming bacterial enzymes and circulatory oxidative stress status in experimental rat colon carcinogenesis. Bratislavske Lekarske Listy, 116, 560–6PubMedGoogle Scholar
  5. Bastide N.M., Naud N., Nassy G., Vendeuvre J.L., Taché S., Guéraud F., et al. 2017. Red Wine and Pomegranate Extracts Suppress Cured Meat Promotion of Colonic Mucin-Depleted Foci in Carcinogen-Induced Rats. Nutrition and Cancer, 69, 289–298. DOI: 10.1080/01635581.2017.1263745CrossRefGoogle Scholar
  6. Beutler E. (Ed.) 1982. Catalase, In: Red Cell Metabolism, a Manual of Biochemical Methods, Grune and Stratton New York, pp.105–106Google Scholar
  7. Breen L.D., Pučić-Baković M., Vučković F., Reiding K., Trbojević-Akmačić I., Šrajer Gajdošik M., et al. 2016. IgG and IgM gly-cosylation patterns in patients undergoing image-guided tumor ablation. Biochimica et Biophysica Acta, 1860, 1786–94. DOI: 10.1016/j.bbagen.2016.01.011CrossRefGoogle Scholar
  8. Burkhart C.N., Burkhart C.G. 2005. Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). International Journal of Dermatology, 44, 837–40. DOI:10.1111/j.1365-4632.2004.02332.xCrossRefGoogle Scholar
  9. Chahid K., Laglaoui A., Zantar S., Ennabili A. 2015. Antioxidant-enzyme reaction to the oxidative stress due to alpha-cypermethrin, chlorpyriphos, and pirimicarb in tomato (Lycopersicon esculentum Mill.). Environmental Science and Pollution Research, 22, 18115–26. DOI: 10.1007/s11356-015-5024-3CrossRefGoogle Scholar
  10. Davidson S.K., Allen S.W., Lim G.E., Anderson, C.M., Haygood, M.G. 2001. Evidence for the Biosynthesis of Bryostatins by the Bacterial Symbiont “Candidatus Endobugula sertula” of the Bryozoan Bugula neritina. Applied and Environmental Microbiology, 67, 4531–4537. DOI: 10.1128/AEM.67.10.4531-4537. 2001CrossRefGoogle Scholar
  11. DeWitt M., Johnson R.L., Snyder P., Fleet J.C. 2015. The effect of 1,25 dihydroxyvitamin D treatment on the mRNA levels of β catenin target genes in mice with colonic inactivation of both APC alleles. The Journal of Steroid Biochemistry and Molecular Biology, 148, 103–110. DOI: 10.1016/j.jsbmb.2015. 01.009CrossRefGoogle Scholar
  12. Etcheberrigaray R., Tan M., Dewachter I., Kuipéri C., Van der Auwera I., Wera S., et al.. 2004. Therapeutic effects of PKC activators in Alzheimer’s disease transgenic mice. Proceedings of the National Academy of Sciences USA, 101, 11141–11146. DOI: 10.1073/pnas.0403921101CrossRefGoogle Scholar
  13. Fijneman R.J., Peham J.R., van de Wiel M.A., Meijer G.A., Matise I., Velcich A., et al. 2008. Expression of Pla2g2a prevents carcinogenesis in Muc2-deficient mice. Cancer Science, 99, 2113–9. DOI: 10.1111/j.1349-7006.2008.00924.xCrossRefGoogle Scholar
  14. Hale K.J., Manviazar S. 2010. New approaches to the Total Synthesis of Bryostatin Antitumor Macrolides. Chemistry–An Asian Journal, 5, 704–54. DOI: 10.1002/asia.200900634CrossRefGoogle Scholar
  15. Hanley M.P., Hahn M.A., Li A.X., Wu X., Lin J., Wang J., et al. 2017. Genome-wide DNA methylation profiling reveals cancer-associated changes within early colonic neoplasia. Oncogene. DOI: 10.1038/onc.2017.130Google Scholar
  16. Ince S., Kozan E., Kucukkurt I., Bacak E. 2010. The effect of levamisole and levamisole+vitamin C on oxidative damage in rats naturally infected with Syphacia muris. Experimental Parasitology, 124, 448–52. DOI: 10.1016/j.exppara.2009.12.017CrossRefGoogle Scholar
  17. Jacqueline C., Tasiemski A., Sorci G., Ujvari B., Maachi F., Missé D., et al., 2017. Infections and cancer: the “fifty shades of immunity hypothesis”. BMC Cancer, 17, 257. DOI: 10.1186/s12885-017-3234-4CrossRefGoogle Scholar
  18. Jaggi M., Chauhan S.C., Du C., Balaji K.C. 2008. Bryostatin 1 modulates beta-catenin subcellular localization and transcription activity through protein kinase D1 activation. Molecular Cancer Therapeutics, 7, 2703–12. DOI: 10.1158/1535-7163.MCT-08-0119CrossRefGoogle Scholar
  19. Janakiram N.B., Rao C.V. 2014. Inflammation and Cancer, Advances in Experimental Medicine and Biology 816, 25–52, DOI: 10.1007/978-3-0348-0837-8_2CrossRefGoogle Scholar
  20. Jiangbo Z., Xuying W., Yuping Z., Xili M., Yiwen Z., Tianbao Z. 2010. Toxicity of bryostatin-1 on the embryo-fetal development of Sprague-Dawley rats. Birth Defects Research, 89, 171–174. DOI: 10.1002/bdrb.20229PubMedGoogle Scholar
  21. Kello M., Drutovic D., Pilatova M.B., Tischlerova V., Perjesi P., Mojzis J. 2016. Chalcone derivatives cause accumulation of colon cancer cells in the G2/M phase and induce apoptosis. Life Science, 150, 32–8. DOI: 10.1016/j.lfs.2016.02.073CrossRefGoogle Scholar
  22. Mutter R., Wills M. 2000. Chemistry and clinical biology of the bryostatins. Bioorganic & Medicinal Chemistry, 8, 1841–1860CrossRefGoogle Scholar
  23. Kosik-Bogacka D.I., Baranowska-Bosiacka I., Kolasa-Wołosiuk A., Lanocha-Arendarczyk N., Gutowska I, Korbecki J., et al. 2016. The inflammatory effect of infection with Hymenolepis diminuta via the increased expression and activity of COX-1 and COX-2 in the rat jejunum and colon. Experimental Parasitology, 169, 69–76. DOI: 10.1016/j.exppara.2016. 07.009CrossRefGoogle Scholar
  24. Lesko A.C., Goss K.H., Yang F.F., Schwertner A., Hulur I., Onel K., et al. 2015. The APC tumor suppressor is required for epithelial cell polarization and three-dimensional morphogenesis. Biochimica et Biophysica Acta, 1853, 711–23. DOI: 10.1016/j.bbamcr.2014.12.036CrossRefGoogle Scholar
  25. Livak K.J., Schmittgen T.D. 2001. Analysis of relative gene expression data using real time quantitative PCR, the 2DDCT. Methods, 25, 402–408. DOI: 10.1006/meth.2001.1262CrossRefGoogle Scholar
  26. Montgomery J.F., Hum S. 1995. Field diagnosis of nitrite poisoning in cattle by testing aqueous humor samples with urine test strips. Veterinary Record, 137, 593–594PubMedGoogle Scholar
  27. Notarnicola M., Tutino V., De Nunzio V., Dituri F., Caruso M.G., Giannelli G. 2017. Dietary ω-3 Polyunsaturated Fatty Acids Inhibit Tumor Growth in Transgenic Apc<sup>Min/+</sup> Mice, Correlating with CB1 Receptor Up-Regulation. International Journal of Molecular Sciences, 18, E485. DOI: 10.3390/ijms18030485CrossRefGoogle Scholar
  28. Perec-Matysiak A., Okulewicz A., Hildebrand J., Zalesny G. 2006. Helminth parasites of laboratory mice and rats. Wiadomości Parazytologiczne, 52, 99–102PubMedGoogle Scholar
  29. Peterson M.R., Weidner N. 2011. Gastrointestinal neoplasia associated with bowel parasitosis: real or imaginary?, Journal of Tropical Medicine, 2354. DOI: 10.1155/2011/234254Google Scholar
  30. Plummer M., de Martel C., Vignat J., Ferlay J., Bray F., Franceschi S. 2016. Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Global Health, 4, e609–16. DOI: 10.1016/S2214-109X(16)30143-7CrossRefGoogle Scholar
  31. Rana T., Bera A.K., Das S., Bhattacharya D., Pan D., Das S.K. 2016. Inhibition of Oxidative Stress and Enhancement of Cellular Activity by Mushroom Lectins in Arsenic Induced Carcinogenesis. Asian Pacific Journal of Cancer Prevention, 17, 4185–4197PubMedGoogle Scholar
  32. Salim, E.I., Morimura K., Menesi A., El-Lity M., Fukushima S. and Wanibuchi H. 2008. Elevated oxidative stress and DNA damage and repair levels in urinary bladder carcinomas associated with Schistosomiasis. International Journal of Cancer, 123, 601–8. DOI: 10.1002/ijc.23547CrossRefGoogle Scholar
  33. Shiraishi N., Ohta Y., Nishikimi M. 2000. The octapeptide repeat region of prion protein binds Cu(II) in the redox inactive states. Biochemical and Biophysical Research Communications, 267, 398–402. DOI: 10.1006/bbrc.1999.1944CrossRefGoogle Scholar
  34. Sinha A.K. 1972. Colorimetric assay of catalase. Analytical Biochemistry, 47, 389–394CrossRefGoogle Scholar
  35. Staff C., Magnusson C.G., Hojjat-Farsangi M., Mosolits S., Liljefors M., Frödin J.E. 2012. Induction of IgM, IgA and IgE antibodies in colorectal cancer patients vaccinated with a recombinant CEA protein. Journal of Clinical Immunology, 32, 855–65. DOI: 10.1007/s10875-012-9662-7CrossRefGoogle Scholar
  36. Theodoratou E., Thaçi K., Agakov F., Timofeeva M.N., Štambuk J., Pučić-Baković M., et al. 2016. Glycosylation of plasma IgG in colorectal cancer prognosis. Scientific Reports, 6, 28098. DOI: 10.1038/srep28098CrossRefGoogle Scholar
  37. Su L.K., Vogelstein B., Kinzler K.W. 1993. Association of the APC tumor suppressor protein with catenins, Science, 262, 1734–1737CrossRefGoogle Scholar
  38. Sun M.K. and Alkon D.L. 2008. Synergistic effects of chronic bryo-statin-1 and alpha-tocopherol on spatial learning and memory in rats. European Journal of Pharmacology, 584, 328–37. DOI: 10.1016/j.ejphar.2008.02.014CrossRefGoogle Scholar
  39. Wang L., Hu T., Shen J., Zhang L., Chan R.L., et al. 2015. Dihy-drotanshinone I induced apoptosis and autophagy through cas-pase dependent pathway in colon cancer. Phytomedicine, 22, 1079–87. DOI: 10.1016/j.phymed.2015.08.009CrossRefGoogle Scholar
  40. Yamasaki T., Takahashi A., Pan J., Yamaguchi N., Yokoyama K.K. 2009. Phosphorylation of Activation Transcription Factor-2 at Serine 121 by Protein Kinase C Controls c-Jun-mediated Activation of Transcription. The Journal of Biological Chemistry, 284, 8567–81. DOI: 10.1074/jbc.M808719200CrossRefGoogle Scholar
  41. Ye B., Yu-Xia Zhang Y-X., Fei Yang F., Hong-Lei Chen H-L., et al. 2007. Induction of lung lesions in Wistar rats by 4-(methyl-nitrosamino)-1-(3-pyridyl)-1-butanone and its inhibition by aspirin and phenethyl isothiocyanate. BMC Cancer, 7, 90. DOI: 10.1186/1471-2407-7-90CrossRefGoogle Scholar
  42. Yoshioka T., Kawada K., Shimada T., Mori M. 1979. Lipid peroxi-dation in maternal and cord blood and protective mechanism against activated oxygen toxicity in the blood. American Journal of Obstetrics & Gynecology, 135, 372CrossRefGoogle Scholar
  43. Zoon C.K., Wan W., Graham L., Bear H.D. 2017. Expansion of T Cells with Interleukin-21 for Adoptive Immunotherapy of Murine Mammary Carcinoma. International Journal of Molecular Sciences, 18, E270. DOI: 10.3390/ijms18020270CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2018

Authors and Affiliations

  • Elsayed I. Salim
    • 1
    Email author
  • Samar F. Harras
    • 2
  • Aisha G. Abdalla
    • 1
    • 2
  • Mohmmed H. Mona
    • 1
  1. 1.Zoology Department, Faculty of ScienceTanta UniversityTantaEgypt
  2. 2.Faculty of Public HealthBenghazi UniversityLibya

Personalised recommendations

Cite article

Buy options