Skip to main content

Advertisement

Log in

Effects of diets high in corn oil or in extra virgin olive oil on oxidative stress in an experimental model of breast cancer

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Experimental evidence highlights the importance of dietetic factors on breast cancer. In this work we aimed to analyze the effects two oils, corn oil (rich in n-6 polyunsaturated fatty acids -PUFA-) and extra virgin olive oil (EVOO), on oxidative stress in an animal model of breast carcinogenesis. Female rats were fed a low-fat control, a high-corn oil, or a high-EVOO diet from weaning or after induction with 7,12-dimethylbenz[a]anthracene at 53 days. Animals were euthanized at 36, 51, 100 and 246 days of age. We analyzed antioxidant enzymes (mRNA and activity of superoxide dismutase, glutathione peroxidase and catalase), non-enzymatic capacity (oxidized and reduced glutathione) and DNA damage (8-oxo-dG) in tumors and mammary gland at different ages. We also analyzed lipid peroxidation (isoprostanes in serum and lipofuscin in liver). Results indicated a decrease in the enzymatic antioxidant capacity and increased oxidative stress in mammary gland of healthy young animals after a short period of high-fat diets intake, followed by an adaptation to chronic dietary intervention. After induction both diets, especially the one high in n-6 PUFA, increased the oxidized glutathione. In tumors no clear effects of the high-fat diets were observed, although in the long-term lipofuscin and 8-oxo-dG suggested greater oxidative damage by effect of the n-6 PUFA-rich diet. Considering the differential effects of these diets on mammary carcinogenesis that we have previously reported, this study suggests that these high-fat diets could have an effect on oxidative stress that would lead to different signaling pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA-Cancer J Clin 68:394–424

    Article  Google Scholar 

  2. WCRF/AICR - World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. American Institute for Cancer Research, Washington

    Google Scholar 

  3. Escrich E, Solanas M, Moral R (2006) Olive oil, and other dietary lipids in cancer: experimental approaches. In: Quiles JL, Ramirez-Tortosa MC, Yaqoob P (eds) Olive oil and health. CABI Publishing, Oxford, pp 317–374

    Chapter  Google Scholar 

  4. Schwingshackl L, Schwedhelm C, Galbete C, Hoffmann G (2017) Adherence to mediterranean diet and risk of cancer: an updated systematic review and meta-analysis. Nutrients 9:E1063

    Article  Google Scholar 

  5. Foscolou A, Critselis E, Panagiotakos D (2018) Olive oil consumption and human health: a narrative review. Maturitas 118:60–66

    Article  CAS  Google Scholar 

  6. Amel N, Wafa T, Samia D, Yousra B, Issam C, Cheraif I, Attia N, Mohamed H (2016) Extra virgin olive oil modulates brain docosahexaenoic acid level and oxidative damage caused by 2,4-Dichlorophenoxyacetic acid in rats. J Food Sci Technol 53:1454–1464

    Article  CAS  Google Scholar 

  7. Escrich E, Solanas M, Moral R, Escrich R (2011) Modulatory effects and molecular mechanisms of olive oil and other dietary lipids in breast cancer. Curr Pharm Des 17:813–830

    Article  CAS  Google Scholar 

  8. Kumari S, Badana AK, Malla R (2018) Reactive oxygen species: a key constituent in cancer survival. Biomark Insights 13:1177271918755391

    Article  Google Scholar 

  9. Saha SK, Lee SB, Won J, Choi HY et al (2017) Correlation between oxidative stress, nutrition, and cancer initiation. Int J Mol Sci 18:1544

    Article  Google Scholar 

  10. Kryston TB, Georgiev AB, Pissis P, Georgakilas AG (2011) Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 11:193–201

    Article  Google Scholar 

  11. Visioli F, Grande S, Bogani P, Galli C (2004) The role of antioxidants in the Mediterranean diets: focus on cancer. Eur J Cancer Prev 13:337–343

    Article  CAS  Google Scholar 

  12. Presti G, Guarrasi V, Gulotta E, Provenzano F et al (2017) Bioactive compounds from extra virgin olive oils: correlation between phenolic content and oxidative stress cell protection. Biophys Chem 230:109–116

    Article  CAS  Google Scholar 

  13. Escrich R, Costa I, Moreno M, Cubedo M, Vela E, Escrich E, Moral R (2019) A high-corn-oil diet strongly stimulates mammary carcinogenesis, while a high-extra-virgin-olive-oil diet has a weak effect, through changes in metabolism, immune system function and proliferation/apoptosis pathways. J Nutr Biochem 64:218–227

    Article  CAS  Google Scholar 

  14. Cordain L, Eaton SB, Sebastian A, Mann N et al (2005) Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81:341–354

    Article  CAS  Google Scholar 

  15. Escrich E, Solanas M, Segura R (1994) Experimental diets for the study of lipid influence on induced mammary carcinoma in rats: I-diet definition. In vivo 8:1099–1105

    CAS  PubMed  Google Scholar 

  16. Escrich E, Solanas M, Ruiz de Villa MC, Ribalta T, Muntane J, Segura R (1994) Experimental diets for the study of lipid influence on induced mammary carcinoma in rats: II-suitability of the diets. In vivo 8:1107–1111

    CAS  PubMed  Google Scholar 

  17. Solanas M, Hurtado A, Costa I, Moral R, Menendez JA, Colomer R, Escrich E (2002) Effects of a high olive oil diet on the clinical behavior and histopathological features of rat DMBA-induced mammary tumors compared with a high corn oil diet. Int J Oncol 21:745–753

    CAS  PubMed  Google Scholar 

  18. Costa I, Solanas M, Escrich E (2002) Histopathologic characterization of mammary neoplastic lesions induced with 7,12-dimethylbenz(α)antracene in the rat. A comparative analysis with human breast tumours. Arch Pathol Lab Med 126:915–927

    PubMed  Google Scholar 

  19. Venkatraman JT, Pinnavaia L (1998) Effects of saturated, ω-6 and ω-3 lipids on activities of enzymes involved in antioxidant defense in normal rats. Nutr Res 18:341–350

    Article  CAS  Google Scholar 

  20. Cnubben NH, Rietjens IM, Wortelboer H, van Zanden J, van Bladeren PJ (2001) The interplay of glutathione-related processes in antioxidant defense. Environ Toxicol Phar 10:141–152

    Article  CAS  Google Scholar 

  21. Kannan N, Nguyen LV, Makarem M, Dong Y et al (2014) Glutathione-dependent and -independent oxidative stress-control mechanisms distinguish normal human mammary epithelial cell subsets. Proc Natl Acad Sci USA 111:7789–7794

    Article  CAS  Google Scholar 

  22. Moral R, Escrich R, Solanas M, Vela E, Costa I, Ruiz de Villa MC, Escrich E (2011) Diets high in corn oil or extra-virgin olive oil provided from weaning advance sexual maturation and differentially modify susceptibility to mammary carcinogenesis in female rats. Nutr Cancer 63:410–420

    Article  CAS  Google Scholar 

  23. Sospedra I, Moral R, Escrich R, Solanas M, Vela E, Escrich E (2015) Effect of high fat diets on body mass, oleylethanolamide plasma levels and oxytocin expression in growing rats. J Food Sci 80:H1425–H1431

    Article  CAS  Google Scholar 

  24. Solanas M, Grau L, Moral R, Vela E, Escrich R, Escrich E (2010) Dietary olive oil and corn oil differentially affect experimental breast cancer through distinct modulation of the p21Ras signaling and the proliferation-apoptosis balance. Carcinogenesis 31:871–879

    Article  CAS  Google Scholar 

  25. Da Silva MS, Bilodeau JF, Julien P, Rudkowska I (2017) Dietary fats and F2-isoprostanes: A review of the clinical evidence. Crit Rev Food Sci Nutr 57:3929–3941

    Article  Google Scholar 

  26. Brunk UT, Terman A (2002) Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radical Bio Med 33:611–619

    Article  CAS  Google Scholar 

  27. Yeldandi AV, Rao MS, Reddy JK (2000) Hydrogen peroxide generation in peroxisome proliferator-induced oncogenesis. Mutat Res 448:159–177

    Article  CAS  Google Scholar 

  28. Maynard S, Schurman SH, Harboe C, de Souza-Pinto NC, Bohr VA (2009) Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30:2–10

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from “Plan Nacional I +D+I” (AGL2006-07691, AGL2011-24778), “Fundación Patrimonio Comunal Olivarero (FPCO)” (FPCO2008-165.396; FPCO2013-CF611.084), “Agencia para el Aceite de Oliva del Ministerio de Agricultura, Alimentación y Medio Ambiente” (AAO2008-165.471), “Organización Interprofesional del Aceite de Oliva Español (OIAOE)” (OIP2009-165.646), “Departaments de Salut i d’Agricultura, Alimentació i Acció Rural de la Generalitat de Catalunya” (GC2010-165.000), FPCO and OIAOE (FPCO-OIP2016-CS614.268). The sponsors had no role in the study design, data collection and analysis and interpretation of the results. We thank Dr. Eduard Escrich, director of the research group “Grup Multidisciplinari per a l’Estudi del Càncer de Mama”, for providing the means and infrastructure to develop this study.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Montserrat Solanas or Raquel Moral.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethics approval

Institutionally approved experimental animal protocol (CEEAH 566/3616).

Informed consent

All authors have read and approved the manuscript, and all of them are aware of its submission to the Molecular Biology Reports.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Escrich, R., Vela, E., Solanas, M. et al. Effects of diets high in corn oil or in extra virgin olive oil on oxidative stress in an experimental model of breast cancer. Mol Biol Rep 47, 4923–4932 (2020). https://doi.org/10.1007/s11033-020-05492-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-020-05492-6

Keywords

Navigation