Research Article
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Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines

Year 2024, Volume: 19 Issue: 3, 124 - 131, 29.12.2024
https://doi.org/10.17094/vetsci.1607091

Abstract

The aim of this study was to evaluate the effects of wheat and corn gluten on some histopathologic parameters such as villus atrophy, crypt hyperplasia, lymphocyte plasma neutrophils and immunohistochemical parameters such as trans glutaminase, gliadin and IgA in the small intestine of healthy male rats without HLA-DQ2 and HLA-DQ8 genes. In the study, 21 healthy newborn male Sprague Dawley rats were fed wheat, corn and soy with the addition of 7 rats in each group from one-day age to 60 days of age. Histopathological (villous atrophy, lymphocyte plasma neutrophil, crypt hyperplasia) and immunohistochemical (transglutaminase, gliadin, IgA) parameter analyses were performed in small intestinal tissue samples. As a result of the study, it was found that the small intestinal villus lengths of the wheat gluten group were longer than the other groups (P < .05). Cryptic hyperplasia was detected most in the soybean group and the lowest in the wheat group (P < .05). Gliadin antibody levels were found to be in the soybean group with the highest and the lowest in the wheat group (P < .05). In healthy male rats lacking HLA-DQ2 and HLA-DQ8 genes, the effect of wheat gluten on crypt hyperplasia and gliadin levels in small intestinal tissue was significantly lower than in soy and corn gluten groups, while its effect on villous atrophy, lymphocyte plasma neutrophil and transglutaminase was limited. In addition, the intestinal villus lengths of the wheat gluten group were significantly higher than those of the corn and soybean groups.

References

  • 1. Biesiekierski JR. What is gluten?. J Gastroenterol Hepatol. 2017;31(Suppl 1):78-81.
  • 2. Aziz I, Branchi F, Sanders DS. The rise and fall of gluten!. Proc Nutr Soc. 2015;74(3):221-226.
  • 3.Sapone A, Bai JC, Ciacci C, et al. Spectrum of gluten-related disorders: consensus on new nomenclature and classification. BMC Med. 2012;10(1):1-12.
  • 4.Machado MV. New developments in celiac disease treatment. Int J Mol Sci. 2023;24(2):945.
  • 5. Catassi GN, Pulvirenti A, Monachesi C, Catassi C, Lionetti E. Diagnostic accuracy of IgA anti-transglutaminase and IgG anti-deamidated gliadin for diagnosis of celiac disease in children under two years of age: a systematic review and meta-analysis. Nutrients. 2021;14(1):7.
  • 6. Rubio-Tapia A, Hill ID, Semrad C, Kelly CP, Lebwohl B. American college of gastroenterology guidelines update: Diagnosis and management of celiac disease. Am J Gastroenterol. 2023;118(1):59-76.
  • 7. Abdi F, Zuberi S, Blom JJ, Armstrong D, Pinto-Sanchez MI. Nutritional considerations in celiac disease and non-celiac gluten/wheat sensitivity. Nutrients. 2023;15(6):1475. 8. Sümer SAG, Harmandar FA, Uyar S, Çekin AH. Non-Çölyak gluten duyarlılığı. Güncel Gastroenteroloji. 2015;19(2); 91-97.
  • 9. Sergi C, Vincenzo V, Antonio C. Non-celiac wheat sensitivity: rationality and irrationality of a gluten-free diet in individuals affected with non-celiac disease: a review. BMC Gastroenterol. 2021; 21(1):5.
  • 10. Gümüş R, Uslu S, Aydoğdu U, İmik A, Ekici M. Investigation of the effects of glutens on serum interleukin-1 beta and tumor necrosis factor-alpha levels and the immunohistochemical distribution of CD3 and CD8 receptors in the small intestine in male rats. Brazilian Archives Biol Technol. 2021;64: e21210256.
  • 11. İmik H, Kapakin KAT, Karabulutlu Ö, Gümüş R, Çomaklı S, Özkaraca M. The effects of dietary wheat and corn glutens on the histopathological and immunohistochemical structure of the ovarian tissue and serum and ovarian tissue LH and FSH levels and lipid profiles in rats. Brazilian Archives Biol Technol. 2023;66:e23210726.
  • 12. Kapakin KAT, Kapakin S, Imik H, Gumus R, Eser G. The investigation of the relationship between HSP-27 release and oxidative DNA damage in broiler chickens with tibial dyschondroplasia by using histopathological and immunohistochemical methods. Braz J Poultry Sci. 2019;eRBCA-2019-1091.
  • 13. Iskender H, Dokumacioglu E, Terim Kapakin KA, et al. Effects of oleanolic acid on inflammation and metabolism in diabetic rats. Biotech Histochem. 2022;97(4):269-276.
  • 14. Uni Z, Gal-Garber O, Geyra A, Sklan D, Yahav S. Changes in growth and function of chick small intestine epithelium due to early thermal conditioning. Poultry Sci. 2001;80(4):438-445.
  • 15. Kapakin KAT, Sahin M, Buyuk F, Kapakin S, Gursan N, Saglam YS. Respiratory tract infection induced experimentally by Ornithobacterium rhinotracheale in quails: effects on heat shock proteins and apoptosis. Revue de Med Vet. 2013;164(3):132-140.
  • 16. Kapakin KAT, Gümüş R, İmik H, Kapakin S, Sağlam YS. Effects of ascorbic and α-lipoic acid on secretion of HSP-70 and apoptosis in liver and kidneys of broilers exposed to heat stress. Ankara Univ Vet Fak Derg. 2012;59(4):279-287.
  • 17. SPSS: Statistical Packages for the Social Sciences for Windows release 10.01. SPSS Inc., Chicago.1996.
  • 18.Marsh MN. Gluten, major histocompatibility complex, and the small intestine: a molecular and immunobiologic approach to the spectrum of gluten sensitivity (‘celiac sprue’). Gastroenterol. 1992;102(1):330-354.
  • 19. Sapone A, Lammers KM, Mazzarella G, et al. Differential mucosal IL-17 expression in two gliadin-induced disorders: gluten sensitivity and the autoimmune enteropathy celiac disease. Int Arch Allergy Immunol. 2010;152(1):75-80.
  • 20. Molberg O, Mcadam SN, Körner R, et al. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat Med. 1998;4(6):713-717.
  • 21. Yakan B, Fötüs BG. Yeni doğmuş ve erişkin farede ince bağırsakların histolojik ve histokimyasal kıyaslı yapısı. Erciyes Tıp Derg. 2000;22(1):7-15.
  • 22. Engel E, Guth PH, Nishizaki Y, Kaunitz JD. Barrier function of the gastric mucus gel. Am J Physiol-Gastrointest Liver Physiol. 1995;269(6):G994-G999.
  • 23. Solakoğlu S, Aytekin Y. Temel Histoloji, Junqueira LC, Carneiro J: Basic Histology, text and atlas, eleventh edition. Nobel Tip Kitabevleri, ISBN: 978-975-420-699-9. 2009; 281-317.
  • 24. Kagnoff, MF. "Immunology and inflammation of the gastrointestinal tract." Gastrointestinal and liver disease. Sixth ed. Philadelphia: WB Saunders Company (1998):19-48.
  • 25. Greco N, Pisano A, Mezzatesta L, et al. New Insights and Evidence on “Food Intolerances”: Non-celiac gluten sensitivity and nickel allergic contact mucositis. Nutr. 2023;15(10):2353.
  • 26. Korponay–Szabo IR, Sulkanen S, Halttunen T, et al. Tissue transglutaminase is the target in both rodent and primate tissues for celiac disease-specific autoantibodies. J Pediatric Gastroenterol Nutr. 2000;31(5): 520-527.
  • 27. Kalliokoski S, Piqueras VO, Frias R, et al. Sulic AM, Maatta JA, Kahkönen N, Lindfors K. Transglutaminase 2-specific coeliac disease autoantibodies induce morphological changes and signs of inflammation in the small-bowel mucosa of mice. Amino Acids. 2017;49(3):529-540.
  • 28. Iversen Rasmus, Ludvig MS. The immunobiology and pathogenesis of celiac disease. Ann Rev Pathol. 2023;24(18):47-70.
  • 29. Arentz-Hansen H, Körner R, Molberg O, et al. The intestinal T cell response to α-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J Exp Med. 2000;191(4):603-612.
  • 30. Bürgin-Wolff A, Gaze H, Hadziselimovic F, et al. Antigliadin and antiendomysium antibody determination for coeliac disease. Arch Dis Childhood. 1991;66(8):941-947.
  • 31. Maiuri L, Ciacci C, Ricciardelli I, et al. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. The Lancet. 2003;362 (9377):30-37.
  • 32. Jaskowski TD, Schroder C, Martins TB, Litwin CM, Hill HR. IgA antibodies against endomysium and transglutaminase: a comparison of methods. J Clin Lab Analysis. 2001;15(3):108-111.
  • 33. Matsumoto I, Uchida K, Nakashima K, et al. IgA antibodies against gliadin and tissue transglutaminase in dogs with chronic enteritis and intestinal T-cell lymphoma. Vet Pathol. 2018;55(1):98-107.
  • 34. Smeekens JM, Kulis MD. Mouse models of food allergy in the pursuit of novel treatment modalities. Front Allergy. 2021;15(2):810067.
  • 35.Marietta EV, Murray JA. Animal models to study gluten sensitivity. Semin Immunopathol. 2012;34(4):497-511.

Sağlıklı Rat Bağırsaklarında Buğday ve Mısır Gluteninin İnflamasyon, Transglutaminaz, Gliadin ve IgA Düzeyleri Üzerine Etkisinin Araştırılması

Year 2024, Volume: 19 Issue: 3, 124 - 131, 29.12.2024
https://doi.org/10.17094/vetsci.1607091

Abstract

Bu çalışmada HLA-DQ2 ve HLA-DQ8 genlerine sahip olmayan sağlıklı erkek ratlarda buğday ve mısır gluteninin ince bağırsaklarda villus atrofisi, kript hiperplazisi, lenfosit plazma nötrofil gibi bazı histopatolojik parametreler ile trans glutaminaz, gliadin, IgA gibi immünhistokimyasal parametrelere etkisinin değerlendirilmesi hedeflenmiştir. Çalışmada, 21 adet sağlıklı yeni doğmuş Sprague Dawley cinsi erkek rat bir günlük yaştan 60 günlük yaşa kadar her grupta 7 rat olmak üzere buğday, mısır ve soya eklenerek beslenmişlerdir. İnce bağırsak doku örneklerinde histopatolojik (villöz atrofi, lenfosit plazma nötrofil, kript hiperplazi) ve immunohistokimyasal (transglutaminaz, gliadin, IgA) parametre analizleri yapılmıştır. Çalışma sonucunda buğday gluteni grubunun ince bağırsak villus uzunluklarının diğer gruplardan daha uzun olduğu saptanmıştır (P < ,05). Kript hiperplazisi en fazla soya grubunda, en düşük buğday grubunda tespit edilmiştir (P < ,05). Gliadin antikor seviyesi en yüksek soya grubunda iken en düşük buğday grubunda olduğu tespit edilmiştir (P < ,05). HLA-DQ2 ve HLA-DQ8 genlerine sahip olmayan sağlıklı erkek ratlarda buğday gluteninin ince bağırsak dokusunda kript hiperplazisi ve gliadin değeri soya ve mısır gluteni verilen gruplardan önemli derecede düşük olduğu belirlenirken, villöz atrofisi, lenfosit plazma nötrofil ile transglutaminaz üzerine etkisi sınırlı düzeyde kalmıştır. Ayrıca buğday gluteni verilen grubun bağırsak villus uzunlukları mısır ve soya verilen gruplardan önemli oranda yüksek olduğu tespit edilmiştir.

References

  • 1. Biesiekierski JR. What is gluten?. J Gastroenterol Hepatol. 2017;31(Suppl 1):78-81.
  • 2. Aziz I, Branchi F, Sanders DS. The rise and fall of gluten!. Proc Nutr Soc. 2015;74(3):221-226.
  • 3.Sapone A, Bai JC, Ciacci C, et al. Spectrum of gluten-related disorders: consensus on new nomenclature and classification. BMC Med. 2012;10(1):1-12.
  • 4.Machado MV. New developments in celiac disease treatment. Int J Mol Sci. 2023;24(2):945.
  • 5. Catassi GN, Pulvirenti A, Monachesi C, Catassi C, Lionetti E. Diagnostic accuracy of IgA anti-transglutaminase and IgG anti-deamidated gliadin for diagnosis of celiac disease in children under two years of age: a systematic review and meta-analysis. Nutrients. 2021;14(1):7.
  • 6. Rubio-Tapia A, Hill ID, Semrad C, Kelly CP, Lebwohl B. American college of gastroenterology guidelines update: Diagnosis and management of celiac disease. Am J Gastroenterol. 2023;118(1):59-76.
  • 7. Abdi F, Zuberi S, Blom JJ, Armstrong D, Pinto-Sanchez MI. Nutritional considerations in celiac disease and non-celiac gluten/wheat sensitivity. Nutrients. 2023;15(6):1475. 8. Sümer SAG, Harmandar FA, Uyar S, Çekin AH. Non-Çölyak gluten duyarlılığı. Güncel Gastroenteroloji. 2015;19(2); 91-97.
  • 9. Sergi C, Vincenzo V, Antonio C. Non-celiac wheat sensitivity: rationality and irrationality of a gluten-free diet in individuals affected with non-celiac disease: a review. BMC Gastroenterol. 2021; 21(1):5.
  • 10. Gümüş R, Uslu S, Aydoğdu U, İmik A, Ekici M. Investigation of the effects of glutens on serum interleukin-1 beta and tumor necrosis factor-alpha levels and the immunohistochemical distribution of CD3 and CD8 receptors in the small intestine in male rats. Brazilian Archives Biol Technol. 2021;64: e21210256.
  • 11. İmik H, Kapakin KAT, Karabulutlu Ö, Gümüş R, Çomaklı S, Özkaraca M. The effects of dietary wheat and corn glutens on the histopathological and immunohistochemical structure of the ovarian tissue and serum and ovarian tissue LH and FSH levels and lipid profiles in rats. Brazilian Archives Biol Technol. 2023;66:e23210726.
  • 12. Kapakin KAT, Kapakin S, Imik H, Gumus R, Eser G. The investigation of the relationship between HSP-27 release and oxidative DNA damage in broiler chickens with tibial dyschondroplasia by using histopathological and immunohistochemical methods. Braz J Poultry Sci. 2019;eRBCA-2019-1091.
  • 13. Iskender H, Dokumacioglu E, Terim Kapakin KA, et al. Effects of oleanolic acid on inflammation and metabolism in diabetic rats. Biotech Histochem. 2022;97(4):269-276.
  • 14. Uni Z, Gal-Garber O, Geyra A, Sklan D, Yahav S. Changes in growth and function of chick small intestine epithelium due to early thermal conditioning. Poultry Sci. 2001;80(4):438-445.
  • 15. Kapakin KAT, Sahin M, Buyuk F, Kapakin S, Gursan N, Saglam YS. Respiratory tract infection induced experimentally by Ornithobacterium rhinotracheale in quails: effects on heat shock proteins and apoptosis. Revue de Med Vet. 2013;164(3):132-140.
  • 16. Kapakin KAT, Gümüş R, İmik H, Kapakin S, Sağlam YS. Effects of ascorbic and α-lipoic acid on secretion of HSP-70 and apoptosis in liver and kidneys of broilers exposed to heat stress. Ankara Univ Vet Fak Derg. 2012;59(4):279-287.
  • 17. SPSS: Statistical Packages for the Social Sciences for Windows release 10.01. SPSS Inc., Chicago.1996.
  • 18.Marsh MN. Gluten, major histocompatibility complex, and the small intestine: a molecular and immunobiologic approach to the spectrum of gluten sensitivity (‘celiac sprue’). Gastroenterol. 1992;102(1):330-354.
  • 19. Sapone A, Lammers KM, Mazzarella G, et al. Differential mucosal IL-17 expression in two gliadin-induced disorders: gluten sensitivity and the autoimmune enteropathy celiac disease. Int Arch Allergy Immunol. 2010;152(1):75-80.
  • 20. Molberg O, Mcadam SN, Körner R, et al. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat Med. 1998;4(6):713-717.
  • 21. Yakan B, Fötüs BG. Yeni doğmuş ve erişkin farede ince bağırsakların histolojik ve histokimyasal kıyaslı yapısı. Erciyes Tıp Derg. 2000;22(1):7-15.
  • 22. Engel E, Guth PH, Nishizaki Y, Kaunitz JD. Barrier function of the gastric mucus gel. Am J Physiol-Gastrointest Liver Physiol. 1995;269(6):G994-G999.
  • 23. Solakoğlu S, Aytekin Y. Temel Histoloji, Junqueira LC, Carneiro J: Basic Histology, text and atlas, eleventh edition. Nobel Tip Kitabevleri, ISBN: 978-975-420-699-9. 2009; 281-317.
  • 24. Kagnoff, MF. "Immunology and inflammation of the gastrointestinal tract." Gastrointestinal and liver disease. Sixth ed. Philadelphia: WB Saunders Company (1998):19-48.
  • 25. Greco N, Pisano A, Mezzatesta L, et al. New Insights and Evidence on “Food Intolerances”: Non-celiac gluten sensitivity and nickel allergic contact mucositis. Nutr. 2023;15(10):2353.
  • 26. Korponay–Szabo IR, Sulkanen S, Halttunen T, et al. Tissue transglutaminase is the target in both rodent and primate tissues for celiac disease-specific autoantibodies. J Pediatric Gastroenterol Nutr. 2000;31(5): 520-527.
  • 27. Kalliokoski S, Piqueras VO, Frias R, et al. Sulic AM, Maatta JA, Kahkönen N, Lindfors K. Transglutaminase 2-specific coeliac disease autoantibodies induce morphological changes and signs of inflammation in the small-bowel mucosa of mice. Amino Acids. 2017;49(3):529-540.
  • 28. Iversen Rasmus, Ludvig MS. The immunobiology and pathogenesis of celiac disease. Ann Rev Pathol. 2023;24(18):47-70.
  • 29. Arentz-Hansen H, Körner R, Molberg O, et al. The intestinal T cell response to α-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J Exp Med. 2000;191(4):603-612.
  • 30. Bürgin-Wolff A, Gaze H, Hadziselimovic F, et al. Antigliadin and antiendomysium antibody determination for coeliac disease. Arch Dis Childhood. 1991;66(8):941-947.
  • 31. Maiuri L, Ciacci C, Ricciardelli I, et al. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. The Lancet. 2003;362 (9377):30-37.
  • 32. Jaskowski TD, Schroder C, Martins TB, Litwin CM, Hill HR. IgA antibodies against endomysium and transglutaminase: a comparison of methods. J Clin Lab Analysis. 2001;15(3):108-111.
  • 33. Matsumoto I, Uchida K, Nakashima K, et al. IgA antibodies against gliadin and tissue transglutaminase in dogs with chronic enteritis and intestinal T-cell lymphoma. Vet Pathol. 2018;55(1):98-107.
  • 34. Smeekens JM, Kulis MD. Mouse models of food allergy in the pursuit of novel treatment modalities. Front Allergy. 2021;15(2):810067.
  • 35.Marietta EV, Murray JA. Animal models to study gluten sensitivity. Semin Immunopathol. 2012;34(4):497-511.
There are 34 citations in total.

Details

Primary Language English
Subjects Animal Health Economics and Management
Journal Section Research Articles
Authors

Aybüke İmik 0000-0003-4697-812X

Ceren Gezer 0000-0002-5647-0103

Kübra Asena Terim Kapakin 0000-0002-1740-8657

Publication Date December 29, 2024
Published in Issue Year 2024 Volume: 19 Issue: 3

Cite

APA İmik, A., Gezer, C., & Terim Kapakin, K. A. (2024). Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines. Veterinary Sciences and Practices, 19(3), 124-131. https://doi.org/10.17094/vetsci.1607091
AMA İmik A, Gezer C, Terim Kapakin KA. Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines. Veterinary Sciences and Practices. December 2024;19(3):124-131. doi:10.17094/vetsci.1607091
Chicago İmik, Aybüke, Ceren Gezer, and Kübra Asena Terim Kapakin. “Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines”. Veterinary Sciences and Practices 19, no. 3 (December 2024): 124-31. https://doi.org/10.17094/vetsci.1607091.
EndNote İmik A, Gezer C, Terim Kapakin KA (December 1, 2024) Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines. Veterinary Sciences and Practices 19 3 124–131.
IEEE A. İmik, C. Gezer, and K. A. Terim Kapakin, “Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines”, Veterinary Sciences and Practices, vol. 19, no. 3, pp. 124–131, 2024, doi: 10.17094/vetsci.1607091.
ISNAD İmik, Aybüke et al. “Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines”. Veterinary Sciences and Practices 19/3 (December 2024), 124-131. https://doi.org/10.17094/vetsci.1607091.
JAMA İmik A, Gezer C, Terim Kapakin KA. Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines. Veterinary Sciences and Practices. 2024;19:124–131.
MLA İmik, Aybüke et al. “Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines”. Veterinary Sciences and Practices, vol. 19, no. 3, 2024, pp. 124-31, doi:10.17094/vetsci.1607091.
Vancouver İmik A, Gezer C, Terim Kapakin KA. Investigation of the Effect of Wheat and Corn Gluten on Inflammation, Transglutaminase, Gliadin and IgA Levels in Healthy Rat Intestines. Veterinary Sciences and Practices. 2024;19(3):124-31.

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