Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T02:07:51.909Z Has data issue: false hasContentIssue false
  • English
  • Français

Transient changes of transforming growth factor-β expression in the small intestine of the pig in association with weaning

Published online by Cambridge University Press:  08 March 2007

Jie Mei  and
Ruo-Jun Xu
Jie Mei
Affiliation:
Department of Zoology, The University of Hong Kong, Pokfulam Road, Hong Kong
Ruo-Jun Xu*
Affiliation:
Department of Zoology, The University of Hong Kong, Pokfulam Road, Hong Kong
*
*Corresponding author: Dr Ruo-Jen Xu, fax +852 2559 9114, email xuruojun@hku.hk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

It is well known that early weaning causes marked changes in intestinal structure and function, and transforming growth factor-β (TGF-β) is believed to play an important regulatory role in post-weaning adaptation of the small intestine. The present study examined the distribution and expression intensity of TGF-β in the small intestinal mucosa of pre- and post-weaning pigs using a specific immunostaining technique and Western blot analysis. The level of TGF-β in the intestinal mucosa, as estimated by Western blot analysis, did not change significantly during weaning. However, when examined by the immunostaining technique, TGF-β1 (one of the TGF-β isoforms dominantly expressed in the tissue) at the intestinal villus epithelium, particularly at the apical membrane of the epithelium, decreased significantly 4 d after weaning, while the staining intensity increased significantly at the intestinal crypts compared with that in pre-weaning pigs. These changes were transient, with the immunostaining intensity for TGF-β1 at the intestinal villi and the crypts returning to the pre-weaning level by 8 d post-weaning. The transient decrease in TGF-β1 level at the intestinal villus epithelium was associated with obvious intestinal villus atrophy and marked reduction of mucosal digestive enzyme activities. Furthermore, the number of leucocytes staining positively for TGF-β1 increased significantly in the pig intestinal lamina propria 4 d after weaning. These findings strongly suggest that TGF-β plays an important role in the post-weaning adaptation process in the intestine of the pig.

Keywords

Transforming growth factor-βIntestineWeaning pig
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 1 , January 2005 , pp. 37 - 45
Copyright
Copyright © The Nutrition Society 2005

References

Babyatsky, MW, Rossiter, G & Podolsky, DK (1996) Expression of transforming growth factors alpha and beta in colonic mucosa in inflammatory bowel disease. Gastroenterology 110, 975–984.CrossRefGoogle ScholarPubMed
Barnard, JA, Beauchamp, RD, Coffey, RJ & Moses, HL (1989) Regulation of intestinal epithelial cell growth by transforming growth factor type beta. Proc Natl Acad Sci USA 86, 1578–1582.CrossRefGoogle ScholarPubMed
Barnard, JA, Warwick, GJ & Gold, LI (1993) Localization of transforming growth factor beta isoforms in the normal murine small intestine and colon. Gastroenterology 105, 67–73.CrossRefGoogle ScholarPubMed
Blobe, GC, Schiemann, WP & Lodish, HF (2000) Role of transforming growth factor beta in human disease. N Engl J Med 342, 1350–1358.CrossRefGoogle ScholarPubMed
Ciacci, C, Lind, SE & Podolsky, DK (1993) Transforming growth factor beta regulation of migration in wounded rat intestinal epithelial monolayers. Gastroenterology 105, 93–101.CrossRefGoogle ScholarPubMed
Claud, EC, Savidge, T & Walker, WA (2003) Modulation of human intestinal epithelial cell IL-8 secretion by human milk factors. Pediatr Res 53, 419–425.CrossRefGoogle ScholarPubMed
Czarniecki, CW, Chiu, HH, Wong, GH, McCabe, SM & Palladino, MA (1988) Transforming growth factor-beta 1 modulates the expression of class II histocompatibility antigens on human cells. J Immunol 140, 4217–4223.CrossRefGoogle ScholarPubMed
Dahlqvist, A (1964) Method for assay of intestinal disaccharides. Anal Biochem 7, 18–25.CrossRefGoogle Scholar
Dignass, AU & Sturm, A (2001) Peptide growth factors in the intestine. Eur J Gastroenterol Hepatol 13, 763–770.CrossRefGoogle ScholarPubMed
Forstner, GG, Sabesin, SM & Isselbacher, KJ (1968) Rat intestinal microvillus membranes. Purification and biochemical characterization. Biochem J 106, 381–390.CrossRefGoogle ScholarPubMed
Giles, KW & Myers, A (1964) The role of nucleic acids in the growth of the hypocotyls of lupinus albus under varying light and dark regimes. Biochim Biophys Acta 87, 460–477.Google ScholarPubMed
Gonnella, PA, Chen, Y, Inobe, J, Komagata, Y, Quartulli, M & Weiner, HL (1998) In situ immune response in gut-associated lymphoid tissue (GALT) following oral antigen in TCR-transgenic mice. J Immunol 160, 4708–4718.CrossRefGoogle ScholarPubMed
Gorelik, L & Flavell, RA (2000) Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12, 171–181.CrossRefGoogle Scholar
Hampson, DJ & Kidder, DE (1986) Influence of creep feeding and weaning on brush border enzyme activities in the piglet small intestine. Res Vet Sci 40, 24–31.CrossRefGoogle ScholarPubMed
Hart, AL, Kamm, MA, Knight, SC & Stagg, AJ (2004) Quantitative and functional characteristics of intestinal-homing memory T cells: analysis of Crohn's disease patients and healthy controls. Clin Exp Immunol 135, 137–145.CrossRefGoogle ScholarPubMed
Johnson, LR & Chandler, AM (1973) RNA and DNA of gastric and duodenal mucosa in antrectomized and gastrin-treated rats. Am J Physiol 224, 937–940.CrossRefGoogle ScholarPubMed
Kelly, D, Smyth, JA & McCracken, KJ (1991) Digestive development of the early-weaned pig. 2. Effect of level of food intake on digestive enzyme activity during the immediate post-weaning period. Br J Nutr 65, 181–188.CrossRefGoogle ScholarPubMed
Letterio, JJ & Roberts, AB (1998) Regulation of immune responses by TGF-β. Annu Rev Immunol 16, 137–161.CrossRefGoogle ScholarPubMed
Li, DF, Nelssen, JL, Reddy, PG, Blecha, F, Hancock, JD, Allee, GL, Goodband, RD & Klemm, RD (1990) Transient hypersensitivity to soybean meal in the early-weaned pig. J Anim Sci 68, 1790–1799.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193, 265–275.CrossRefGoogle ScholarPubMed
Massague, J (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6, 597–641.CrossRefGoogle ScholarPubMed
McCartney-Francis, NL & Wahl, SM (1994) Transforming growth factor beta: a matter of life and death. J Leukoc Biol 55, 401–409.CrossRefGoogle ScholarPubMed
McCracken, BA, Gaskins, HR, Ruwe-Kaiser, PJ, Klasing, KC & Jewell, DE (1995) Diet-dependent and diet-independent metabolic responses underlie growth stasis of pigs at weaning. J Nutr 125, 2838–2845.Google ScholarPubMed
McCracken, BA, Spurlock, ME, Roos, MA, Zuckermann, FA & Gaskins, HR (1999) Weaning anorexia may contribute to local inflammation in the piglet small intestine. J Nutr 129, 613–619.CrossRefGoogle ScholarPubMed
McKaig, BC, Hughes, K, Tighe, PJ & Mahida, YR (2002) Differential expression of TGF-beta isoforms by normal and inflammatory bowel disease intestinal myofibroblasts. Am J Physiol Cell Physiol 282, C172–C182.CrossRefGoogle ScholarPubMed
Mei, J, Zhang, YQ, King, D, Sangild, P & Xu, RJ (2004) Distribution and developmental changes of transforming growth factor-beta receptors in the small intestine of the pig. J Anim Vet Adv 3, 89–106.Google Scholar
O'Kane, S & Ferguson, MW (1997) Transforming growth factor betas and wound healing. Int J Biochem Cell Biol 29, 63–78.CrossRefGoogle ScholarPubMed
Penttila, IA, van Spriel, AB, Zhang, MF, Xian, CJ, Steeb, CB, Cummins, AG, Zola, H & Read, LC (1998) Transforming growth factor-beta levels in maternal milk and expression in postnatal rat duodenum and ileum. Pediatr Res 44, 524–531.CrossRefGoogle ScholarPubMed
Penttila, IA, Zhang, MF, Bates, E, Regester, G, Read, LC & Zola, H (2001) Immune modulation in suckling rat pups by a growth factor extract derived from milk whey. J Dairy Res 68, 587–599.CrossRefGoogle ScholarPubMed
Perr, H, Oh, P & Johnson, D (1996) Developmental regulation of transforming growth factor beta-mediated collagen synthesis in human intestinal muscle cells. Gastroenterology 110, 92–101.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Pluske, JR, Williams, IH & Aherne, FX (1996) Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Anim Sci 62, 131–144.CrossRefGoogle Scholar
Pluske, JR, Hampson, DJ & Williams, IH (1997) Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Prod Sci 51, 215–236.CrossRefGoogle Scholar
Proetzel, G, Pawlowski, SA, Wiles, MV, Yin, M, Boivin, GP, Howles, PN, Ding, J, Ferguson, MW & Doetschman, T (1995) Transforming growth factor-beta 3 is required for secondary palate fusion. Nat Genet 11, 409–414.CrossRefGoogle ScholarPubMed
Rao, JN, Li, L, Bass, BL & Wang, JY (2000) Expression of the TGF-beta receptor gene and sensitivity to growth inhibition following polyamine depletion. Am J Physiol Cell Physiol 279, C1034–C1044.CrossRefGoogle ScholarPubMed
Roberts, AB (1995) Transforming growth factor-beta: activity and efficacy in animal models of wound healing. Wound Rep Reg 3, 408–418.CrossRefGoogle ScholarPubMed
Ruifrok, AC, Mason, KA, Lozano, G & Thames, HD (1997) Spatial and temporal patterns of expression of epidermal growth factor, transforming growth factor alpha and transforming growth factor beta 1–3 and their receptors in mouse jejunum after radiation treatment. Radiat Res 147, 1–12.CrossRefGoogle ScholarPubMed
Sanford, LP, Ormsby, I, Gittenberger-de Groot, AC, Sariola, H, Friedman, R, Boivin, GP, Cardell, EL & Doetschman, T (1997) TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124, 2659–2670.CrossRefGoogle ScholarPubMed
Shull, MM, Ormsby, I, Kier, AB, et al. (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359, 693–699.CrossRefGoogle ScholarPubMed
Thompson, FM, Catto-Smith, AG, Moore, D, Davidson, G & Cummins, AG (1998) Epithelial growth of the small intestine in human infants. J Pediatr Gastroenterol Nutr 26, 506–512.Google ScholarPubMed
van Beers-Schreurs, HM, Nabuurs, MJ, Vellenga, L, Kalsbeek-van der Valk, HJ, Wensing, T & Breukink, HJ (1998) Weaning and the weanling diet influence the villus height and crypt depth in the small intestine of pigs and alter the concentrations of short-chain fatty acids in the large intestine and blood. J Nutr 128, 947–953.CrossRefGoogle Scholar
van't Land, B, Meijer, HP, Frerichs, J, Koetsier, M, Jager, D, Smeets, RL, M'Rabet, L & Hoijer, M (2002) Transforming growth factor-beta2 protects the small intestine during methotrexate treatment in rats possibly by reducing stem cell cycling. Br J Cancer 87, 113–118.CrossRefGoogle ScholarPubMed
Walia, B, Wang, L, Merlin, D & Sitaraman, SV (2003) TGF-beta down-regulates IL-6 signaling in intestinal epithelial cells: critical role of SMAD-2. FASEB J 17, 2130–2132.CrossRefGoogle ScholarPubMed
Xu, RJ, Mellor, DJ, Tungthanathanich, P, Birtles, MJ, Reynolds, GW & Simpson, HV (1992) Growth and morphological changes in the small and the large intestine in piglets during the first three days after birth. J Dev Physiol 18, 161–172.Google ScholarPubMed
Xu, RJ, Wang, F & Zhang, SH (2000) Postnatal adaptation of the gastrointestinal tract in neonatal pigs: a possible role of milk-borne growth factors. Livestock Prod Sci 66, 95–107.CrossRefGoogle Scholar
Yue, J & Mulder, KM (2001) Transforming growth factor-beta signal transduction in epithelial cells. Pharmacol Ther 91, 1–34.CrossRefGoogle ScholarPubMed