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Naturally Occurring Glycoalkaloids in Potatoes Aggravate Intestinal Inflammation in Two Mouse Models of Inflammatory Bowel Disease

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Abstract

Background

Inflammatory bowel disease (IBD) may be initiated following disruption of the intestinal epithelial barrier. This disruption, in turn, permits luminal antigens unfettered access to the mucosal immune system and leads to an uncontrolled inflammatory response. Glycoalkaloids, which are found in potatoes, disrupt cholesterol-containing membranes such as those of the intestinal epithelium. Glycoalkaloid ingestion through potatoes may play a role in the initiation and/or perpetuation of IBD.

Aim

To determine if commercial and high glycoalkaloids containing fried potato skins aggravate intestinal inflammation using two different animal models of IBD.

Methods

Fried potato skins from commercial potatoes containing low/medium glycoalkaloid levels and high glycoalkaloids potatoes were fed for 20 days to interleukin 10 gene-deficient mice and dextran sodium sulfate-induced colitic mice. Intestinal permeability, mucosal cytokine and myeloperoxidase levels and body weight were determined to assess intestinal injury.

Results

Deep frying potato skins markedly increased glycoalkaloid content. Interleukin 10 gene-deficient mice fed fried commercial potato skins with medium glycoalkaloid content exhibited significantly elevated levels of ileal IFN-γ relative to controls. Mice in the dextran sodium sulfate colitis model that were fed the same strain of potatoes demonstrated significantly elevated levels of pro-inflammatory cytokines IFN-γ, TNF-α, and IL-17 in the colon in addition to an enhanced colonic permeability. Inflammatory response was intensified when the mice were fed potatoes with higher glycoalkaloid contents.

Conclusions

Our results demonstrate that consumption of potato skins containing glycoalkaloids can significantly aggravate intestinal inflammation in predisposed individuals.

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References

  1. Chichlowski M, Hale LP. Bacterial-mucosal interactions in inflammatory bowel disease—an alliance gone bad. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1139–G1149.

    Article  CAS  PubMed  Google Scholar 

  2. Madsen KL, Malfair D, Gray D, et al. Interleukin-10 gene-deficient mice develop a primary intestinal permeability defect in response to enteric microflora. Inflamm Bowel Dis. 1999;5(4):262–270.

    Article  CAS  PubMed  Google Scholar 

  3. Berg DJ, Zhang J, Weinstock JV, et al. Rapid development of colitis in NSAID-treated IL-10-deficient mice. Gastroenterology. 2002;123:1527–1542.

    Article  CAS  PubMed  Google Scholar 

  4. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007;117(3):514–521.

    Article  CAS  PubMed  Google Scholar 

  5. Smith DB, Roddick GJ, Jones JL. Potato glycoalkaloids: some unanswered questions. Trends Food Sci Technol. 1996;7:126–131.

    Article  CAS  Google Scholar 

  6. Roddick JG, Weissenberg M, Leonard AL. Membrane disruption and enzyme inhibition by naturally-occurring and modified chacotriose-containing solanum steroidal glycoalkaloids. Phytochemistry. 2001;56(6):603–610.

    Article  CAS  PubMed  Google Scholar 

  7. Mandimika T, Baykus H, Vissers Y, et al. Differential gene expression in intestinal epithelial cells induced by single and mixtures of potato glycoalkaloids. J Agric Food Chem. 2007;55(24):10055–10066.

    Article  CAS  PubMed  Google Scholar 

  8. Keukens EA, de Vrije T, van den Boom C, et al. Molecular basis of glycoalkaloid induced membrane disruption. Biochim Biophys Acta. 1995;1240(2):216–228.

    Article  PubMed  Google Scholar 

  9. Patel B, Schutte R, Sporns P, et al. Potato glycoalkaloids adversely affect intestinal permeability and aggravate inflammatory bowel disease. Inflamm Bowel Dis. 2002;8(5):340–346.

    Article  PubMed  Google Scholar 

  10. Egger B, Bajaj-Elliott M, MacDonald TT, et al. Characterization of acute murine dextran sodium sulphate colitis: cytokine profile and dose dependency. Digestion. 2000;62(4):240–248.

    Article  CAS  PubMed  Google Scholar 

  11. Dieleman LA, Palmen MJ, Akol H, et al. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol. 1998;114(3):p385–p391.

    Article  Google Scholar 

  12. Kühn R, Löhler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263–274.

    Article  PubMed  Google Scholar 

  13. Friedman M. Potato glycoalkaloids and metabolites: roles in the plant and in the diet. J Agric Food Chem. 2006;54(23):8655–8681.

    Article  CAS  PubMed  Google Scholar 

  14. AOAC International. AOAC official methods of analysis. AOAC official method 997.13. Glycoalkaloids (α-solanine and α-chaconine) in potato tubers. In: Trucksess MW, ed. Natural Toxins. Gaithersburg: AOAC; 1997:63–65.

    Google Scholar 

  15. Meddings JB, Gibbons I. Discrimination of site-specific alterations in gastrointestinal permeability in the rat. Gastroenterology. 1998;114(1):83–92.

    Article  CAS  PubMed  Google Scholar 

  16. Sydora BC, Tavernini MM, Doyle JS, et al. Association with selected bacteria does not cause enterocolitis in IL-10 gene-deficient mice despite a systemic immune response. Dig Dis Sci. 2005;50:905–913.

    Article  CAS  PubMed  Google Scholar 

  17. Keukens EA, de Vrije T, Fabrie CH, et al. Dual specificity of sterol-mediated glycoalkaloid induced membrane disruption. Biochim Biophys Acta. 1992;1110(2):127–136.

    Article  CAS  PubMed  Google Scholar 

  18. Sinden SL, Webb RE. Effect of variety and location on the glycoalkaloid content of potatoes. Am J Potato Res. 1972;49(9):334–338.

    Article  CAS  Google Scholar 

  19. Yang SA, Paek SH, Kozukue N, et al. Alpha-chaconine, a potato glycoalkaloid, induces apoptosis of HT-29 human colon cancer cells through caspase-3 activation and inhibition of ERK 1/2 phosphorylation. Food Chem Toxicol. 2006;44(6):839–846.

    Article  CAS  PubMed  Google Scholar 

  20. Mandimika T, Baykus H, Vissers Y, et al. Differential gene expression in intestinal epithelial cells induced by single and mixtures of potato glycoalkaloids. J Agric Food Chem. 2007;55(24):10055–10066.

    Article  CAS  PubMed  Google Scholar 

  21. Ribeiro RA, Cunha FQ, Ferreira SH. Recombinant gamma interferon causes neutrophil migration mediated by the release of a macrophage neutrophil chemotactic factor. Int J Exp Pathol. 1990;71(5):717–725.

    CAS  PubMed  Google Scholar 

  22. Kozukue N, Yoon KS, Byun GI, et al. Distribution of glycoalkaloids in potato tubers of 59 accessions of two wild and five cultivated solanum species. J Agric Food Chem. 2008;56(24):11920–11928.

    Article  CAS  PubMed  Google Scholar 

  23. Mensinga TT, Sips AJ, Rompelberg CJ, et al. Potato glycoalkaloids and adverse effects in humans: an ascending dose study. Regul Toxicol Pharmacol. 2005;41(1):66–72.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Funding

Crohn’s and Colitis Foundation of Canada (CCFC).

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Correspondence to Vadim Iablokov.

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Iablokov, V., Sydora, B.C., Foshaug, R. et al. Naturally Occurring Glycoalkaloids in Potatoes Aggravate Intestinal Inflammation in Two Mouse Models of Inflammatory Bowel Disease. Dig Dis Sci 55, 3078–3085 (2010). https://doi.org/10.1007/s10620-010-1158-9

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  • DOI: https://doi.org/10.1007/s10620-010-1158-9

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