Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2015, Article ID 513429, 13 pages
http://dx.doi.org/10.1155/2015/513429
Research Article

Exposure to Common Food Additive Carrageenan Alone Leads to Fasting Hyperglycemia and in Combination with High Fat Diet Exacerbates Glucose Intolerance and Hyperlipidemia without Effect on Weight

1Department of Medicine, University of Illinois at Chicago, Chicago, IL 60612-4325, USA
2Jesse Brown VA Medical Center, Chicago, IL 60612-3728, USA

Received 4 November 2014; Accepted 3 March 2015

Academic Editor: Ute Christine Rogner

Copyright © 2015 Sumit Bhattacharyya et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Bhattacharyya, I. O-Sullivan, S. Katyal, T. Unterman, and J. K. Tobacman, “Exposure to the common food additive carrageenan leads to glucose intolerance, insulin resistance and inhibition of insulin signalling in HepG2 cells and C57BL/6J mice,” Diabetologia, vol. 55, no. 1, pp. 194–203, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. http://www.cdc.gov/nutrition/everyone/basics/fat/saturatedfat.html.
  3. Harvard School of Public Health, The Nutrition Source. Top Food Choices High in Saturated Fat in the U.S, 2014, http://www.hsph.harvard.edu/nutritionsource/top-food-sources-of-saturated-fat-in-the-us/.
  4. M. Dehghan, A. Mente, K. K. Teo et al., “Relationship between healthy diet and risk of cardiovascular disease among patients on drug therapies for secondary prevention: a prospective cohort study of 31 546 high-risk individuals from 40 countries,” Circulation, vol. 126, no. 23, pp. 2705–2712, 2012. View at Publisher · View at Google Scholar
  5. 2014, http://www.who.int/dietphysicalactivity/diet/en/.
  6. J. West and K. N. Miller, California's Living Marine Resources: A Status Report. Agarophytes and Carrageenophytes, California Department of Fish and Game, 2001.
  7. Britannica Academic, “Algae,” Encyclopædia Britannica, 2010, http://search.eb.com/eb.article-31714.
  8. M. L. Weiner, “Food additive carrageenan: Part II. A critical review of carrageenan in vivo safety studies,” Critical Reviews in Toxicology, vol. 44, no. 3, pp. 244–269, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. J. K. Tobacman, “Review of harmful gastrointestinal effects of carrageenan in animal experiments,” Environmental Health Perspectives, vol. 109, no. 10, pp. 983–994, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Borthakur, S. Bhattacharyya, P. K. Dudeja, and J. K. Tobacman, “Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 292, no. 3, pp. G829–G838, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Bhattacharyya, R. Gill, M.-L. Chen et al., “Toll-like receptor 4 mediates induction of the Bcl10-NFκB-interleukin-8 inflammatory pathway by carrageenan in human intestinal epithelial cells,” The Journal of Biological Chemistry, vol. 283, no. 16, pp. 10550–10558, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Bhattacharyya, P. K. Dudeja, and J. K. Tobacman, “Carrageenan-induced NFκB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10,” Biochimica et Biophysica Acta—General Subjects, vol. 1780, no. 7-8, pp. 973–982, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. V. L. Campo, D. F. Kawano, D. B. D. Silva Jr., and I. Carvalho, “Carrageenans: biological properties, chemical modifications and structural analysis—a review,” Carbohydrate Polymers, vol. 77, no. 2, pp. 167–180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. E. J. Masters, C. N. Grigery, and R. W. Masters, “STARI, or masters disease: lone star tick-vectored lyme-like illness,” Infectious Disease Clinics of North America, vol. 22, no. 2, pp. 361–376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Nuñez, F. Carballada, A. Gonzalez-Quintela, J. Gomez-Rial, M. Boquete, and C. Vidal, “Delayed mammalian meat-induced anaphylaxis due to galactose-α-1,3- galactose in 5 European patients,” Journal of Allergy and Clinical Immunology, vol. 128, no. 5, pp. 1122–1124, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. S. P. Commins, S. M. Satinover, J. Hosen et al., “Delayed anaphylaxis, angioedema, or urticaria after consumption of red meat in patients with IgE antibodies specific for galactose-α-1,3-galactose,” Journal of Allergy and Clinical Immunology, vol. 123, no. 2, pp. 426–433, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. C. H. Chung, B. Mirakhur, E. Chan et al., “Cetuximab-induced anaphylaxis and IgE specific for galactose-α-1,3- galactose,” The New England Journal of Medicine, vol. 358, no. 11, pp. 1109–1117, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. B. A. Macher and U. Galili, “The Galα1,3Galβ1,4GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance,” Biochimica et Biophysica Acta—General Subjects, vol. 1780, no. 2, pp. 75–88, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Tanemura, D. Yin, A. S. Chong, and U. Galili, “Differential immune responses to α-gal epitopes on xenografts and allografts: implications for accommodation in xenotransplantation,” Journal of Clinical Investigation, vol. 105, no. 3, pp. 301–310, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. U. Galili, “The alpha-gal epitope and the anti-Gal antibody in xenotransplantation and in cancer immunotherapy,” Immunology and Cell Biology, vol. 83, no. 6, pp. 674–686, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Teranishi, R. Manez, M. Awwad, and D. K. C. Cooper, “Anti-Galalpha1-3Gal IgM and IgG antibody levels in sera of humans and old world non-human primates,” Xenotransplantation, vol. 9, no. 2, pp. 148–154, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. Z. Gao, D. Hwang, F. Bataille et al., “Serine phosphorylation of insulin receptor substrate 1 by inhibitor κB kinase complex,” Journal of Biological Chemistry, vol. 277, no. 50, pp. 48115–48121, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Perseghin, K. Petersen, and G. I. Shulman, “Cellular mechanism of insulin resistance: potential links with inflammation,” International Journal of Obesity and Related Metabolic Disorders, vol. 27, supplement 3, pp. S6–S11, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Shi, M. V. Kokoeva, K. Inouye, I. Tzameli, H. Yin, and J. S. Flier, “TLR4 links innate immunity and fatty acid-induced insulin resistance,” Journal of Clinical Investigation, vol. 116, no. 11, pp. 3015–3025, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. M. J. Song, K. H. Kim, J. M. Yoon, and J. B. Kim, “Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes,” Biochemical and Biophysical Research Communications, vol. 346, no. 3, pp. 739–745, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. M. K. Mohammad, M. Morran, B. Slotterbeck et al., “Dysregulated Toll-like receptor expression and signaling in bone marrow-derived macrophages at the onset of diabetes in the non-obese diabetic mouse,” International Immunology, vol. 18, no. 7, pp. 1101–1113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. R. F. Tsuji, K. Hoshino, Y. Noro et al., “Suppression of allergic reaction by lambda-carrageenan: toll-like receptor 4/MyD88-dependent and -independent modulation of immunity,” Clinical and Experimental Allergy, vol. 33, no. 2, pp. 249–258, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. J. E. Ayala, D. P. Bracy, C. Malabanan et al., “Hyperinsulinemic-euglycemic clamps in conscious, unrestrained mice,” Journal of Visualized Experiments, no. 57, Article ID e3188, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. http://www.ihcworld.com/_protocols/special_stains/pas.htm.
  30. F. Costa, M. G. Mumolo, M. Bellini et al., “Role of faecal calprotectin as non-invasive marker of intestinal inflammation,” Digestive and Liver Disease, vol. 35, no. 9, pp. 642–647, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. J. A. Potteiger, D. J. Jacobsen, and J. E. Donnelly, “A comparison of methods for analyzing glucose and insulin areas under the cure following nine months of exercise in overweight adults,” International Journal of Obesity, vol. 26, no. 1, pp. 87–89, 2002. View at Google Scholar · View at Scopus
  32. T. G. Willis, D. M. Jadayel, M.-Q. Du et al., “Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types,” Cell, vol. 96, no. 1, pp. 35–45, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. Q. Zhang, R. Siebert, M. Yan et al., “Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32),” Nature Genetics, vol. 22, no. 1, pp. 63–68, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Bhattacharyya and J. K. Tobacman, “Molecular signature of kappa-carrageenan mimics chondroitin-4-sulfate and dermatan sulfate and enables interaction with arylsulfatase B,” Journal of Nutritional Biochemistry, vol. 23, no. 9, pp. 1058–1063, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Yang, S. Bhattacharyya, R. Linhardt, and J. Tobacman, “Exposure to common food additive carrageenan leads to reduced sulfatase activity and increase in sulfated glycosaminoglycans in human epithelial cells,” Biochimie, vol. 94, no. 6, pp. 1309–1316, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. J. K. Tobacman, M. Hinkhouse, and Z. Khalkhali-Ellis, “Steroid sulfatase activity and expression in mammary myoepithelial cells,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 81, no. 1, pp. 65–68, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. E. A. Bergner and L. J. Shapiro, “Increased cholesterol sulfate in plasma and red blood cell membranes of steroid sulfatase deficient patients,” Journal of Clinical Endocrinology and Metabolism, vol. 53, no. 1, pp. 221–223, 1981. View at Publisher · View at Google Scholar · View at Scopus
  38. E. H. Epstein Jr., R. M. Krauss, and C. H. L. Shackleton, “X-linked ichthyosis: increased blood cholesterol sulfate and electrophoretic mobility of low-density lipoprotein,” Science, vol. 214, no. 4521, pp. 659–660, 1981. View at Publisher · View at Google Scholar · View at Scopus
  39. P. M. Elias, M. L. Williams, M. E. Maloney et al., “Stratum corneum lipids in disorders of cornification. Steroid sulfatase and cholesterol sulfate in normal desquamation and the pathogenesis of recessive X-linked ichthyosis,” Journal of Clinical Investigation, vol. 74, no. 4, pp. 1414–1421, 1984. View at Publisher · View at Google Scholar · View at Scopus
  40. M. L. Williams, S. L. Rutherford, and K. R. Feingold, “Effects of cholesterol sulfate on lipid metabolism in cultured human keratinocytes and fibroblasts,” The Journal of Lipid Research, vol. 28, no. 8, pp. 955–967, 1987. View at Google Scholar · View at Scopus
  41. X. Shi, Q. Cheng, L. Xu et al., “Cholesterol sulfate and cholesterol sulfotransferase inhibit gluconeogenesis by targeting hepatocyte nuclear factor 4α,” Molecular and Cellular Biology, vol. 34, no. 3, pp. 485–497, 2014. View at Publisher · View at Google Scholar · View at Scopus