High-protein diet differently modifies intestinal goblet cell characteristics and mucosal cytokine expression in ileum and colon

Journal of Nutritional Biochemistry

Volumn 26, Issue 1, 2015, Pages 91-98

  Lan, Annaïg ^a   Andriamihaja, Mireille ^a   Blouin, Jean Marc ^a   Liu, Xinxin ^a   Descatoire, Véronique ^b   Desclée de Maredsous, Caroline ^a   Davila, Anne Marie ^a   Walker, Francine ^b   Tomé, Daniel ^a   Blachier, François ^a  

^a AGROPARISTECH   (France)

^b BICHAT HOSPITAL   (France)

Author keywords

Basal gut inflammatory status; Goblet cells; High protein diet; Intestine; Mucus

Indexed keywords

CYTOKINE; DEFA5 PROTEIN; DEFB1 PROTEIN; GAMMA INTERFERON; IMMUNOGLOBULIN A; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17F; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 6; MUCIN 2; MUCIN 3; MUCIN 4; PROTEIN; PROTEIN ZO1; REG3G PROTEIN; SECRETORY PHOSPHOLIPASE A2; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; MUC3 PROTEIN, RAT; PROTEIN INTAKE; TLR4 PROTEIN, RAT; TRANSFORMING GROWTH FACTOR BETA1; VOLATILE FATTY ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELLULAR DISTRIBUTION; COLON MUCOSA; CONTROLLED STUDY; DOWN REGULATION; FOOD INTAKE; GENE EXPRESSION; GOBLET CELL; ILEUM MUCOSA; INTESTINE CELL; LYMPHOCYTE SUBPOPULATION; MALE; NATURAL KILLER CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN DIET; PROTEIN EXPRESSION; RAT; T LYMPHOCYTE; ADMINISTRATION AND DOSAGE; ANIMAL; CD4+ T LYMPHOCYTE; COLON; DIET; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; ILEUM; IMMUNOHISTOCHEMISTRY; INTESTINE MUCOSA; METABOLISM; PROTEIN INTAKE; TIGHT JUNCTION; UPREGULATION; WISTAR RAT;

ANIMALIA; RATTUS;

ACETATES; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; COLON; DIET; DIETARY PROTEINS; DOWN-REGULATION; ENTEROCYTES; EPITHELIAL CELLS; FATTY ACIDS, VOLATILE; GOBLET CELLS; ILEUM; IMMUNOGLOBULIN A; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-6; INTESTINAL MUCOSA; MALE; MUCIN-3; RATS; RATS, WISTAR; TIGHT JUNCTIONS; TOLL-LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 84926254124     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.09.007     Document Type: Article

References (31)

1. Gibson J.A., Sladen G.E., Dawson A.M. Protein absorption and ammonia production: the effects of dietary protein and removal of the colon. Br J Nutr 1976, 35(1):61-65. [Epub 1976/01/01].
2. Chacko A., Cummings J.H. Nitrogen losses from the human small bowel: obligatory losses and the effect of physical form of food. Gut 1988, 29(6):809-815. [Epub 1988/06/01].
3. Gaudichon C., Bos C., Morens C., Petzke K.J., Mariotti F., Everwand J., et al. Ileal losses of nitrogen and amino acids in humans and their importance to the assessment of amino acid requirements. Gastroenterology 2002, 123(1):50-59. [Epub 2002/07/10].
4. Cummings J.H., Macfarlane G.T. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 1991, 70(6):443-459. [Epub 1991/06/01].
5. Windey K., De Preter V., Verbeke K. Relevance of protein fermentation to gut health. Mol Nutr Food Res 2012, 56(1):184-196. [Epub 2011/11/29].
6. Hughes R., Magee E.A., Bingham S. Protein degradation in the large intestine: relevance to colorectal cancer. Curr Issues Intest Microbiol 2000, 1(2):51-58. [Epub 2001/11/17].
7. Macfarlane G.T., Macfarlane S. Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. J Clin Gastroenterol 2011, 45:S120-S127. [Suppl., Epub 2011/10/14].
8. Ruemmele F.M. Bacterial mucosa cross-talk and pathophysiology of inflammation. J Pediatr Gastroenterol Nutr 2009, 48(Suppl 2):S49-S51. [Epub 2009/03/28].
9. Andriamihaja M., Davila A.M., Eklou-Lawson M., Petit N., Delpal S., Allek F., et al. Colon luminal content and epithelial cell morphology are markedly modified in rats fed with a high-protein diet. Am J Physiol Gastrointest Liver Physiol 2010, 299(5):G1030-G1037. [Epub 2010/08/07].
10. Liu X., Blouin J.M., Santacruz A., Lan A., Andriamihaja M., Wilkanowicz S., et al. High protein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: the increased luminal bulk connection. Am J Physiol Gastrointest Liver Physiol 2014, 307(4):G459-G470.
11. Blachier F., Mariotti F., Huneau J.F., Tome D. Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 2007, 33(4):547-562.
12. Leschelle X., Goubern M., Andriamihaja M., Blottiere H.M., Couplan E., Gonzalez-Barroso M.D., et al. Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim Biophys Acta 2005, 1725(2):201-212. [Epub 2005/07/06].
13. Mouille B., Robert V., Blachier F. Adaptative increase of ornithine production and decrease of ammonia metabolism in rat colonocytes after hyperproteic diet ingestion. Am J Physiol Gastrointest Liver Physiol 2004, 287(2):G344-G351. [Epub 2004/04/06].
14. Peterson L.W., Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014, 14(3):141-153. [Epub 2014/02/26].
15. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008, 8(6):411-420. [Epub 2008/05/13].
16. Guihot G., Blachier F., Colomb V., Morel M.T., Raynal P., Corriol O., et al. Effect of an elemental vs a complex diet on l-citrulline production from l-arginine in rat isolated enterocytes. JPEN J Parenter Enteral Nutr 1997, 21(6):316-323. [Epub 1997/12/24].
17. Kristensen N.B., Pierzynowski S.G., Danfaer A. Net portal appearance of volatile fatty acids in sheep intraruminally infused with mixtures of acetate, propionate, isobutyrate, butyrate, and valerate. J Anim Sci 2000, 78(5):1372-1379. [Epub 2000/06/02].
18. Kim Y.S., Ho S.B. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 2010, 12(5):319-330. [Epub 2010/08/13].
19. Andrianifahanana M., Moniaux N., Batra S.K. Regulation of mucin expression: mechanistic aspects and implications for cancer and inflammatory diseases. Biochim Biophys Acta 2006, 1765(2):189-222. [Epub 2006/02/21].
20. Forstner G., Forstner J., Fahim R. Small intestinal mucin: polymerization and the "link glycopeptide". Symp Soc Exp Biol 1989, 43:259-271. [Epub 1989/01/01].
21. Law G.K., Bertolo R.F., Adjiri-Awere A., Pencharz P.B., Ball R.O. Adequate oral threonine is critical for mucin production and gut function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 2007, 292(5):G1293-G1301. [Epub 2007/01/20].
22. Hamard A., Mazurais D., Boudry G., Le Huerou-Luron I., Seve B., Le Floc'h N. A moderate threonine deficiency affects gene expression profile, paracellular permeability and glucose absorption capacity in the ileum of piglets. J Nutr Biochem 2010, 21(10):914-921. [Epub 2009/12/04].
23. Schaart M.W., Schierbeek H., van der Schoor S.R., Stoll B., Burrin D.G., Reeds P.J., et al. Threonine utilization is high in the intestine of piglets. J Nutr 2005, 135(4):765-770. [Epub 2005/03/30].
24. Dohi T., Fujihashi K., Koga T., Shirai Y., Kawamura Y.I., Ejima C., et al. T helper type-2 cells induce ileal villus atrophy, goblet cell metaplasia, and wasting disease in T cell-deficient mice. Gastroenterology 2003, 124(3):672-682. [Epub 2003/03/04].
25. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118(2):229-241. [Epub 2004/07/21].
26. Santaolalla R., Fukata M., Abreu M.T. Innate immunity in the small intestine. Curr Opin Gastroenterol 2011, 27(2):125-131. [Epub 2011/01/21].
27. Wu Y., Kudsk K.A., DeWitt R.C., Tolley E.A., Li J. Route and type of nutrition influence IgA-mediating intestinal cytokines. Ann Surg 1999, 229(5):662-667. [discussion 7-8. Epub 1999/05/11].
28. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., Hall J., Sun C.M., Belkaid Y., et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007, 204(8):1757-1764. [Epub 2007/07/11].
29. Shan M., Gentile M., Yeiser J.R., Walland A.C., Bornstein V.U., Chen K., et al. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 2013, 342(6157):447-453. [Epub 2013/09/28].
30. Davila A.M., Blachier F., Gotteland M., Andriamihaja M., Benetti P.H., Sanz Y., et al. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host (reprinted from Pharmacological Research vol 68, pg 95-107, 2012). Pharmacol Res 2013, 69(1):114-126.
31. Wrzosek L., Miquel S., Noordine M.L., Bouet S., Chevalier-Curt M.J., Robert V., et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol 2013, 11:61. [Epub 2013/05/23].