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Diabetes-prone BioBreeding rats do not have a normal immune response when weaned to a diet containing fermentable fibre

Published online by Cambridge University Press:  08 March 2007

RoseMarie Stillie ,
Rhonda C. Bell  and
Catherine J. Field
RoseMarie Stillie
Affiliation:
Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada, T6G 2P5
Rhonda C. Bell
Affiliation:
Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada, T6G 2P5
Catherine J. Field*
Affiliation:
Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada, T6G 2P5
*
*Corresponding author: Dr Catherine J. Field, fax +1 780 492 9130, email [email protected]
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Abstract

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Diet is known to modulate the development of diabetes in diabetes-prone BioBreeding (BBdp) rats. The objective of the present study was to determine the effect of fermentable fibre (FF) on immune function in BBdp and diabetes-resistant BioBreeding (BBdr) rats after weaning. Weanling BBdp (thirty-six to thirty-eight per diet) and BBdr rats (thirty to thirty-two per diet) were fed a nutritionally complete, semi-purified, casein-based diet containing either cellulose (control diet, 8 % w/w) or FF (3·2 % cellulose+4·8 % w/w inulin). At 35 d, the small intestine was excised and lymphocytes isolated from spleen, mesenteric lymph nodes and Peyer's patches. Feeding FF to both BBdr and BBdp rats affected the production of anti-inflammatory cytokines (P=0·02). In BBdr rats, feeding FF compared with cellulose resulted in an increased small intestinal length (P=0·0031), higher proliferative (stimulation) index from both splenocytes (P=0·001) and mesenteric lymph nodes (P=0·04), and an increased proportion of CD8+ T-cells in the Peyer's patches (P=0·003). We did not observe an effect of diet on the number of IgA-bearing cells in the jejunum from BBdr rats. Feeding FF to BBdp rats did not affect the same parameters. BBdp rats had both a higher proportion of B-cells in the Peyer's patches (P=0·01) and a higher number of IgA+ cells in the jejunum (P=0·0036) when fed a diet containing FF, a response not observed in BBdr rats. We demonstrate that several aspects of the BBdp immune system respond differently than that of BBdr rats when challenged at weaning with FF.

Keywords

BB ratDiabetesDietary fibreImmune functionWeaning
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 5 , May 2005 , pp. 645 - 653
Copyright
Copyright © The Nutrition Society 2005

References

Andoh, A, Bamba, T & Sasaki, M (1999) Physiological and anti-inflammatory roles of dietary fiber and butyrate in intestinal functions. JPEN J Parenter Enteral Nutr 23, S70–S73.CrossRefGoogle ScholarPubMed
Beales, PE, Elliot, RB, Flohe, S, Hill, JP, Kolb, H, Pozzilli, P, Wang, GS, Wasmuth, H & Scott, FW (2003) A multi-centre, blinded international trial of the effect of A(1) and A(2) beta-casein variants on diabetes incidence in two rodent models of spontaneous Type I diabetes. Diabetologia 45, 1240–1246.CrossRefGoogle Scholar
Buddington, RK, Kelly-Quagliana, K, Buddington, KK & Kimura, Y (2002) Non-digestible oligosaccharides and defense functions: lessons learned from animal models. Br J Nutr 87 Suppl. 2, S231–S239.Google Scholar
Courtois, P, Sener, A, Scott, FW & Malaisse, WJ (2004a) Disaccharidase activity in the intestinal tract of Wistar-Furth, diabetes-resistant and diabetes-prone BioBreeding rats. Br J Nutr 91, 201–209.CrossRefGoogle ScholarPubMed
Courtois, P, Sener, A, Scott, FW & Malaisse, WJ (2004b) Peroxidase activity in the intestinal tract of Wistar-Furth, BBc and BBdp rats. Diabetes Metab Res Rev 20, 305–314.Google Scholar
Crabbe, PA, Bazin, H, Eyssen, H & Heremans, JF (1968) The normal microbial flora as a major stimulus for proliferation of plasma cells synthesizing IgA in the gut. The germ-free intestinal tract. Int Arch Allergy Appl Immunol 34, 362–375.CrossRefGoogle Scholar
Cummins, AG, Eglinton, BA, Gonzalez, A & Roberton, DM (1994) Immune activation during infancy in healthy humans. J Clin Immunol 14, 107–115.CrossRefGoogle ScholarPubMed
Cummins, AG, Labrooy, JT & Shearman, DJ (1989) The effect of cyclosporin A in delaying maturation of the small intestine during weaning in the rat. Clin Exp Immunol 75, 451–456.Google Scholar
Cummins, AG, Thompson, FM & Mayrhofer, G (1991) Mucosal immune activation and maturation of the small intestine at weaning in the hypothymic (nude) rat. J Pediatr Gastroenterol Nutr 12, 361–368.Google Scholar
Edwards, CA & Parrett, AM (2002) Intestinal flora during the first months of life: new perspectives. Br J Nutr 88 Suppl. 1, S11–S18.CrossRefGoogle ScholarPubMed
Elliott, RB, Reddy, SN, Bibby, NJ & Kida, K (1988) Dietary prevention of diabetes in the non-obese diabetic mouse. Diabetologia 31, 62–64.Google Scholar
Field, CJ, Goruk, S & Glen, S (1999a) Effect of diet on the development of the immune system in the BB rat. J Clin Biochem Nutr 26, 119–134.CrossRefGoogle Scholar
Field, CJ, McBurney, MI, Massimino, S, Hayek, MG & Sunvold, GD (1999b) The fermentable fiber content of the diet alters the function and composition of canine gut associated lymphoid tissue. Vet Immunol Immunopathol 72, 325–341.Google Scholar
Hao, WL & Lee, YK (2004) Microflora of the gastrointestinal tract: a review. Methods Mol Biol 268, 491–502.Google ScholarPubMed
Hardin, JA, Donegan, L, Woodman, RC, Trevenen, C & Gall, DG (2002) Mucosal inflammation in a genetic model of spontaneous type I diabetes mellitus. Can J Physiol Pharmacol 80, 1064–1070.CrossRefGoogle Scholar
Hosono, A, Azawa, A, Kato, R, Ohnishi, Y, Nakanishi, Y, Kimura, T & Nakamura, R (2003) Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer's patch cells. Biosci Biotechnol Biochem 67, 758–764.CrossRefGoogle ScholarPubMed
Ishizuka, S & Tanaka, S (2002) Modulation of CD8+ intraepithelial lymphocyte distribution by dietary fiber in the rat large intestine. Exp Biol Med (Maywood) 227, 1017–1021.CrossRefGoogle ScholarPubMed
Kagnoff, MF (1993) Immunology of the intestinal tract. Gastroenterology 105, 1275–1280.CrossRefGoogle ScholarPubMed
Kleessen, B, Hartmann, L & Blaut, M (2001) Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr 86, 291–300.Google Scholar
Kleessen, B, Hartmann, L & Blaut, M (2003) Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. Br J Nutr 89, 597–606.CrossRefGoogle ScholarPubMed
Kudoh, K, Shimizu, J & Ishiyama, A, et al. (1999) Secretion and excretion of immunoglobulin A to cecum and feces differ with type of indigestible saccharides. J Nutr Sci Vitaminol (Tokyo) 45, 173–181.Google Scholar
Kudoh, K, Shimizu, J, Wada, M, Takita, T, Kanke, Y & Innami, S (1998) Effect of indigestible saccharides on B lymphocyte response of intestinal mucosa and cecal fermentation in rats. J Nutr Sci Vitaminol (Tokyo) 44, 103–112.Google Scholar
Like, AA, Butler, L, Williams, RM, Appel, MC, Weringer, EJ & Rossini, AA (1982) Spontaneous autoimmune diabetes mellitus in the BB rat. Diabetes 31, 7–13.Google Scholar
MacFarlane, AJ, Burghardt, KM, Kelly, J, Simell, T, Simell, O, Altosaar, I & Scott, FW (2003) A type 1 diabetes-related protein from wheat ( Triticum aestivum ). cDNA clone of a wheat storage globulin Glb1, linked to islet damage. J Biol Chem 278, 54–63.Google Scholar
Masjedi, M, Tivey, DR, Thompson, FM & Cummins, AG (1999) Activation of the gut-associated lymphoid tissue with expression of interleukin-2 receptors that peaks during weaning in the rat. J Pediatr Gastroenterol Nutr 29, 556–562.Google Scholar
Meddings, JB, Jarand, J, Urbanski, SJ, Hardin, J & Gall, DG (1999) Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am J Physiol 276, G951–G957.Google ScholarPubMed
Menezes, JS, Mucida, DS & Cara, DC, et al. (2003) Stimulation by food proteins plays a critical role in the maturation of the immune system. Int Immunol 15, 447–455.Google Scholar
Nagai, T, Ishizuka, S, Hara, H & Aoyama, Y (2000) Dietary sugar beet fiber prevents the increase in aberrant crypt foci induced by gamma-irradiation in the colorectum of rats treated with an immunosuppressant. J Nutr 130, 1682–1687.Google Scholar
Norris, JM, Barriga, K & Klingensmith, G, et al. (2003) Timing of initial cereal exposure in infancy and risk of islet autoimmunity. JAMA 290, 1713–1720.CrossRefGoogle ScholarPubMed
Ouwehand, A, Isolauri, E & Salminen, S (2002) The role of the intestinal microflora for the development of the immune system in early childhood. Eur J Nutr 41 Suppl. 1, I32–I37.CrossRefGoogle ScholarPubMed
Perrin, IV, Marchesini, M, Rochat, FC, Schiffrin, EJ & Schilter, B (2003) Oligofructose does not affect the development of type 1 diabetes mellitus induced by dietary proteins in the diabetes-prone BB rat model. Diabetes Nutr Metab 16, 94–101.Google Scholar
Pie, S, Lalles, JP, Blazy, F, Laffitte, J, Seve, B & Oswald, IP (2004) Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr 134, 641–647.Google Scholar
Reimer, RA, Glen, S, Field, CJ & McBurney, MI (1998) Proglucagon and glucose transporter mRNA is altered by diet and disease susceptibility in 30-day-old biobreeding (BB) diabetes-prone and normal rats. Pediatr Res 44, 68–73.CrossRefGoogle ScholarPubMed
Rodriguez-Cabezas, ME, Galvez, J & Camuesco, D, et al. (2003) Intestinal anti-inflammatory activity of dietary fiber ( Plantago ovata seeds ) in HLA-B27 transgenic rats. Clin Nutr 22, 463–471.Google Scholar
Roland, N, Nugon-Baudon, L, Andrieux, C & Szylit, O (1995) Comparative study of the fermentative characteristics of inulin and different types of fibre in rats inoculated with a human whole faecal flora. Br J Nutr 74, 239–249.Google Scholar
Roller, M, Rechkemmer, G & Watzl, B (2004) Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr 134, 153–156.Google Scholar
Schley, PD & Field, CJ (2002) The immune-enhancing effects of dietary fibres and prebiotics. Br J Nutr 87 Suppl. 2, S221–S230.Google Scholar
Schmid, S, Koczwara, K, Schwinghammer, S, Lampasona, V, Ziegler, AG & Bonifacio, E (2003) Delayed exposure to wheat and barley proteins reduces diabetes incidence in non-obese diabetic mice. Clin Immunol 111, 108–118.Google Scholar
Scott, FW, Mongeau, R, Kardish, M, Hatina, G, Trick, KD & Wojcinski, Z (1985) Diet can prevent diabetes in the BB rat. Diabetes 34, 1059–1062.Google Scholar
Thompson, FM, Mayrhofer, G & Cummins, AG (1996) Dependence of epithelial growth of the small intestine on T-cell activation during weaning in the rat. Gastroenterology 111, 37–44.CrossRefGoogle ScholarPubMed
Vaarala, O (2002) The gut immune system and type 1 diabetes. Ann N Y Acad Sci 958, 39–46.Google Scholar
Waldmann, TA (1993) The IL-2/IL-2 receptor system: a target for rational immune intervention. Immunol Today 14, 264–270.Google Scholar
Yamada, K, Tokunaga, Y & Ikeda, A, et al. (2003) Effect of dietary fiber on the lipid metabolism and immune function of aged Sprague-Dawley rats. Biosci Biotechnol Biochem 67, 429–433.Google Scholar
Ziegler, AG, Schmid, S, Huber, D, Hummel, M & Bonifacio, E (2003) Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies. JAMA 290, 1721–1728.CrossRefGoogle ScholarPubMed