Hostname: page-component-84b7d79bbc-g78kv Total loading time: 0 Render date: 2024-07-30T02:37:41.021Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary supplementation with ovine serum immunoglobulin is associated with an increased gut luminal mucin concentration in the growing rat

Published online by Cambridge University Press:  15 July 2011

P. Balan ,
K.-S. Han ,
H. Singh  and
P. J. Moughan
P. Balan
Affiliation:
Riddet Institute, Massey University, Private Bag 11 222, Palmerston North, New Zealand
K.-S. Han
Affiliation:
Riddet Institute, Massey University, Private Bag 11 222, Palmerston North, New Zealand
H. Singh
Affiliation:
Riddet Institute, Massey University, Private Bag 11 222, Palmerston North, New Zealand
P. J. Moughan*
Affiliation:
Riddet Institute, Massey University, Private Bag 11 222, Palmerston North, New Zealand
*
†E-mail: p.j.moughan@massey.ac.nz
Get access

Abstract

The mucus layer covering the gut epithelium is pivotal to host defence and is affected by various dietary components. Part of the reported beneficial effect of dietary immunoglobulins (Igs) on gut health may be due to effects on the gut mucus layer. The aim was to determine whether orally administered ovine serum Ig influence goblet cell count, mucin gene expression and digesta mucin protein content in the gut of the growing rat. Fourteen Sprague–Dawley male growing rats were used in a 21-day study and were fed either a casein-based control diet (CON; no Ig) or a similar diet but containing freeze-dried ovine Ig (FDOI). Daily food intake and growth rate were not affected by the dietary treatments. When compared to the rats consuming CON diet, those consuming the FDOI diet had significantly (P < 0.05) more intact and cavitated goblet cells in the intestinal villi. A similar result was found for crypt goblet cells in the small intestine and colon. Ileal Muc2, Muc3, Muc4 and stomach Muc5Ac mRNA expressions for the FDOI animals were higher (P < 0.05) compared to the the CON animals. Mucin protein content was higher (P < 0.05) in the stomach, ileum and colonic digesta of rats fed the FDOI diet. In conclusion, orally administered FDOI influenced gut mucins in the growing rat as evidenced by increased mucin gene expression and digesta mucin protein concentrations as well as an increased goblet cell count.

Keywords

ovine serum immunoglobulinmucin proteinmucin gene expressiongoblet cells
Type
Full Paper
Information
animal , Volume 5 , Issue 12 , 10 November 2011 , pp. 1916 - 1922
Copyright
Copyright © The Animal Consortium 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allori, C, Aguero, G, de Ruiz Holgado, AP, Nader, OM, Perdigon, G 2000. Gut mucosa morphology and microflora changes in malnourished mice after renutrition with milk and administration of Lactobacillus casei. Journal of Food Protection 63, 83–90.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists (AOAC) 2003. Official methods of analysisvol. 1 17th edition. AOAC, Gaithersburg, MD, USA.Google Scholar
Babu, SD, Jayanthi, V, Devaraj, N, Reis, CA, Devaraj, H 2006. Expression profile of mucins (MUC2, MUC5AC and MUC6) in Helicobacter pylori infected preneoplastic and neoplastic human gastric epithelium. Molecular Cancer 19, 5–10.Google Scholar
Balan, P 2011. Effects of orally administered ovine serum immunoglobulin in the normal and Salmonella enteritidis – challenged growing rat. PhD, Massey University.Google Scholar
Balan, P, Han, KS, Rutherfurd, SM, Singh, H, Moughan, PJ 2009. Orally administered ovine serum immunoglobulins influence growth performance, organ weights, and gut morphology in growing rats. Journal of Nutrition 139, 244–249.Google ScholarPubMed
Balan, P, Han, KS, Rutherfurd-Markwick, K, Singh, H, Moughan, PJ 2010. Immunomodulatory effects of ovine serum immunoglobulin in the growing rat. Animal 4, 1702–1708.CrossRefGoogle ScholarPubMed
Balan, P, Han, KS, Rutherfurd-Markwick, K, Singh, H, Moughan, PJ 2011a. Ovine serum immunoglobulin has immunomodulatory effects in growing rats gavaged with Salmonella enteritidis. Journal of Nutrition 141, 950–956.CrossRefGoogle ScholarPubMed
Balan, P, Han, KS, Rutherfurd, SM, Singh, H, Moughan, PJ 2011b. Dietary supplementation with ovine serum immunoglobulin attenuates acute effects on growth, organ weights, gut morphology and intestinal mucin production in the growing rat challenged with Salmonella enteritidis. Animal (in press); doi:10.1017/S1751731111000620.Google ScholarPubMed
Barcelo, A, Claustre, J, Moro, F, Chayvialle, JA, Cuber, JC, Plaisancie, P 2000. Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 46, 218–224.CrossRefGoogle ScholarPubMed
Bosi, P, Casini, L, Finamore, A, Cremokolini, C, Merialdi, G, Trevisi, P, Nobili, F, Mengheri, E 2004. Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. Journal of Animal Science 26, 1764–1772.CrossRefGoogle Scholar
Caballero-Franco, C, Keller, K, De Simone, C, Chadee, K 2007. The VSL3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. American Journal of Physiology Gastrointestinal and Liver Physiology 292, G315–G322.CrossRefGoogle Scholar
Claustre, J, Toumi, F, Trompette, A, Jourdan, G, Guignard, H, Chayvialle, JA, Plaisancie, P 2002. Effects of peptide derived from dietary proteins on mucus secretion in rat jejunum. American Journal of Physiology Gastrointestinal and Liver Physiology 283, G521–G528.Google ScholarPubMed
Corfield, AP, Myerscough, N, Longman, R, Sylvester, P, Arul, S, Pignatelli, M 2000. Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut 47, 589–594.CrossRefGoogle ScholarPubMed
Dharmani, P, Srivastava, V, Kissoon-Singh, V, Chadee, K 2009. Role of intestinal mucins in innate host defense mechanisms against pathogens. Journal of Innate Immunity 1, 123–135.CrossRefGoogle ScholarPubMed
Dock-Nascimento, DB, Junqueira, K, Aguilar-Nascimento, JE 2007. Rapid restoration of colonic globet cells induced by a hydrolyzed diet containing probiotics in experimental malnutrition. Acta Cirurgica Brasileira 22, 72–76.Google Scholar
Forstner, GG 1995. Signal transduction, packaging and secretion of mucins. Annual Review of Physiology 57, 585–605.CrossRefGoogle ScholarPubMed
Forstner, JF, Forstner, GG 1994. Gastrointestinal mucus. In Physiology of the gastrointestinal tract (ed. LR Johnson), pp. 1255–1284. Raven, New York, USA.Google Scholar
Gatnau, R, Paul, PS, Zimmerman, D 1989. Spray dried porcine plasma as a source of immunoglobulins for newborn pigs. Journal of Animal Science 67 (suppl.1), 244.Google Scholar
Hammarstrom, V, Smith, CIE, Hammarstrom, L 1993. Oral immunoglobulin treatment in Campylobacter jejuni enteritis. Lancet 341, 1036.CrossRefGoogle ScholarPubMed
Han, KS, Deglaire, A, Sengupta, R, Moughan, PJ 2008. Hydrolyzed casein influences intestinal mucin gene expression in the rat. Journal of Agricultural and Food Chemistry 56, 5572–5576.CrossRefGoogle ScholarPubMed
Hecht, G 1999. Innate mechanisms of epithelial host defence: spotlight on intestine. American Journal of Physiology 277, 351–358.CrossRefGoogle ScholarPubMed
King, MR, Morel, PCH, Pluske, JR, Hendriks, WH 2008. A comparison of the effects of dietary spray-dried bovine colostrum and animal plasma on growth and intestinal histology in weaner pigs. Livestock Science 119, 167–173.CrossRefGoogle Scholar
Kraehenbuhl, JP, Neutra, MR 1992. Molecular and cellular basis of immune protection of mucosal surfaces. Physiological Reviews 72, 853–879.Google ScholarPubMed
Larsen, FM, Wilson, MN, Moughan, PJ 1994. Dietary fiber viscosity and amino acid digestibility, proteolytic digestive enzyme activity and digestive organ weights in growing rats. Journal of Nutrition 124, 833–841.CrossRefGoogle ScholarPubMed
Linden, SK, Sutton, P, Karlsson, NG, Korolik, V, McGuckin, MA 2008. Mucins in the mucosal barrier to infection. Mucosal Immunology 1, 183–197.CrossRefGoogle ScholarPubMed
McCracken, VJ, Lorenz, RG 2001. The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota: a review. Cellular Microbiology 3, 1–11.CrossRefGoogle Scholar
Moncada, DM, Chadee, K 2002. Production, structure, and function of gastrointestinal mucins. In Infections of the gastrointestinal tract (ed. MJ Blaser), pp. 57–79. Lippincott Williams & Wilkins, Philadelphia, PA, USA.Google Scholar
National Research Council (NRC) 1995. Nutrient requirements of laboratory animals, 4th edition. National Academy Press, Washington, DC, USA.Google Scholar
Pierce, JL, Cromwell, GL, Lindemann, MD, Russell, LE, Weaver, EM 2005. Effects of spray-dried animal plasma and immunoglobulins on performance of early weaned pigs. Journal of Animal Science 83, 2876–2885.CrossRefGoogle ScholarPubMed
Rodriguez, C, Blanch, F, Romano, V, Saborido, N, Rodenas, J, Polo, J 2007. Porcine immunoglobulins survival in the intestinal tract of adult dogs and cats fed dry food kibbles containing spray-dried porcine plasma (SDPP) or porcine immunoglobulin concentrate (PIC). Animal Feed Science and Technology 139, 201–211.CrossRefGoogle Scholar
Sherman, P, Forstner, J, Roomi, N, Khatri, I, Forstner, G 1985. Mucin depletion in the intestine of malnourished rats. American Journal of Physiology 248, 418–423.Google ScholarPubMed
Specian, RD, Oliver, MG 1991. Functional biology of intestinal goblet cells. American Journal of Physiology 260, 183–193.CrossRefGoogle ScholarPubMed
Trompette, A, Blanchard, C, Zoghbi, S, Bara, J, Claustre, J, Jourdan, G, Chayvialle, JA, Plaisance, P 2004. The DHE cell line as a model for studying rat gastro-intestinal mucin expression: effects of dexamethasone. European Journal Cell Biology 83, 347–358.CrossRefGoogle Scholar
van Sandick, JW, van Lanschot, JB, van Felius, L, Haringsma, J, Tytgat, GN, Dekker, W, Drillenburg, P, Offerhaus, GJ, ten Kate, FJ 2002. Intestinal metaplasia of the esophagus or esophagogastric junction: evidence of distinct clinical, pathologic, and histochemical staining features. American Journal of Clinical Pathology 117, 117–125.CrossRefGoogle ScholarPubMed
Warny, M, Fatimi, A, Bostwick, EF, Laine, DC, Lebel, F, LaMont, JT, Pothoulakis, C, Kelly, CP 1999. Bovine immunoglobulin concentrate-clostridium difficile retains C difficile toxin neutralising activity after passage through the human stomach and small intestine. Gut 44, 212–217.CrossRefGoogle ScholarPubMed