Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T05:31:20.422Z Has data issue: false hasContentIssue false
  • English
  • Français

Epidermal growth factor promotes intestinal secretory cell differentiation in weaning piglets via Wnt/β-catenin signalling

Published online by Cambridge University Press:  25 October 2019

L. X. Wang ,
F. Zhu ,
J. Z. Li ,
Y. L. Li ,
X. Q. Ding ,
J. Yin ,
X. Xiong  and
H. S. Yang Open the ORCID record for H. S. Yang [Opens in a new window]
L. X. Wang
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China Chinese Academy of Science, Institute of Subtropical Agriculture, Research Center for Healthy Breeding of Livestock and Poultry, Hunan Engineering and Research Center of Animal and Poultry Science and Key Laboratory for Agroecological Processes in Subtropical Region, Scientific Observation and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha City, Hunan 410125, China
F. Zhu
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China Chinese Academy of Science, Institute of Subtropical Agriculture, Research Center for Healthy Breeding of Livestock and Poultry, Hunan Engineering and Research Center of Animal and Poultry Science and Key Laboratory for Agroecological Processes in Subtropical Region, Scientific Observation and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha City, Hunan 410125, China
J. Z. Li
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China
Y. L. Li
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China
X. Q. Ding
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China
J. Yin
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China
X. Xiong
Affiliation:
Chinese Academy of Science, Institute of Subtropical Agriculture, Research Center for Healthy Breeding of Livestock and Poultry, Hunan Engineering and Research Center of Animal and Poultry Science and Key Laboratory for Agroecological Processes in Subtropical Region, Scientific Observation and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha City, Hunan 410125, China
H. S. Yang*
Affiliation:
Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Laboratory of Animal Nutrition and Human Health, College of Life Sciences, Hunan Normal University, Changsha, Hunan 410081, China Chinese Academy of Science, Institute of Subtropical Agriculture, Research Center for Healthy Breeding of Livestock and Poultry, Hunan Engineering and Research Center of Animal and Poultry Science and Key Laboratory for Agroecological Processes in Subtropical Region, Scientific Observation and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha City, Hunan 410125, China
*
†E-mail: yhs@hunnu.edu.cn
Get access

Abstract

Small intestinal epithelium homeostasis involves four principal cell types: enterocytes, goblet, enteroendocrine and Paneth cells. Epidermal growth factor (EGF) has been shown to affect enterocyte differentiation. This study determined the effect of dietary EGF on goblet, enteroendocrine and Paneth cell differentiation in piglet small intestine and potential mechanisms. Forty-two weaned piglets were used in a 2 × 3 factorial design; the major factors were time post-weaning (days 7 and 14) and dietary treatment (0, 200 or 400 µg/kg EGF supplementation). The numbers of goblet and enteroendocrine cells were generally greater with the increase in time post-weaning. Moreover, the supplementation of 200 µg/kg EGF increased (P < 0.01) the number of goblet and enteroendocrine cells in villus and crypt of the piglet small intestine as compared with the control. Dietary supplementation with 200 µg/kg EGF enhanced (P < 0.05) abundances of differentiation-related genes atonal homologue 1, mucin 2 and intestinal trefoil factor 3 messenger RNA (mRNA) as compared with the control. Piglets fed 200 or 400 µg/kg EGF diet had increased (P < 0.05) abundances of growth factor-independent 1, SAM pointed domain containing ETS transcription factor and pancreatic and duodenal homeobox 1 mRNA, but decreased the abundance (P < 0.01) of E74 like ETS transcription factor 3 mRNA as compared with the control. Animals receiving 400 µg/kg EGF diets had enhanced (P < 0.05) abundances of neurogenin3 and SRY-box containing gene 9 mRNA as compared with the control. The mRNA abundance and protein expression of lysozyme, a marker of Paneth cell, were also increased (P < 0.05) in those animals. As compared with the control, dietary supplementation with 200 µg/kg EGF increased the abundance of EGF receptor mRNA and the ratio of non-phospho(p)-β-catenin/β-catenin (P < 0.05) in villus epithelial cells at days 7 and 14. This ratio in crypt epithelial cells was higher (P < 0.05) on the both 200 and 400 µg/kg EGF groups during the same period. Our results demonstrated that dietary EGF stimulated goblet, enteroendocrine and Paneth cell differentiation in piglets during the post-weaning period, partly through EGFR and Wnt/β-catenin signalling.

Keywords

enteroendocrine cellepidermal growth factor receptorgoblet cellPaneth celltranscription factors
Type
Research Article
Information
animal , Volume 14 , Issue 4 , April 2020 , pp. 790 - 798
Copyright
© The Animal Consortium 2019 

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

Barron, L, Sun, R, Aladegbami, B, Erwin, C, Warner, B and Guo, J 2017. Intestinal epithelial-specific mTORC1 activation enhances intestinal adaptation after small bowel resection. Cellular and Molecular Gastroenterology and Hepatology 3, 231–244.CrossRefGoogle ScholarPubMed
Benoit, YD, Lepage, MB, Khalfaoui, T, Tremblay, E, Basora, N, Carrier, JC, Gudas, LJ and Beaulieu, JF 2012. Polycomb repressive complex 2 impedes intestinal cell terminal differentiation. Journal of Cell Science 125, 3454–3463.CrossRefGoogle ScholarPubMed
Chen, CL, Yu, X, James, IO, Zhang, H, Yang, J, Radulescu, A, Zhou, Y and Besner, GE 2012. Heparin-binding EGF-like growth factor protects intestinal stem cells from injury in a rat model of necrotizing enterocolitis. Laboratory Investigation 92, 331–344.CrossRefGoogle Scholar
Cheung, QC, Yuan, ZF, Dyce, PW, Wu, D, Lange, K and Li, JL 2009. Generation of epidermal growth factor-expressing Lactococcus lactis and its enhancement on intestinal development and growth of early-weaned mice. American Journal of Clinical Nutrition 89, 871–879.CrossRefGoogle ScholarPubMed
Clark, JA, Doelle, SM, Halpern, MD, Saunders, TA, Holubec, H, Dvorak, K, Boitano, SA and Dvorak, B 2006. Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. American Journal of Physiology-Gastrointestinal and Liver Physiology 291, 938–949.CrossRefGoogle ScholarPubMed
Clevers, H 2013. The intestinal crypt, a prototype stem cell compartment. Cell 154, 274–284.CrossRefGoogle ScholarPubMed
Gerbe, F, van Es, JH, Makrini, L, Brulin, B, Mellitzer, G, Robine, S, Romagnolo, B, Shroyer, NF, Bourgaux, JF, Pignodel, C, Clevers, H and Jay, P 2011. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. Journal of Cell Biology 192, 767–780.CrossRefGoogle ScholarPubMed
Gonzalez, LM, Williamson, I, Piedrahita, JA, Blikslager, AT and Magness, ST 2013. Cell lineage identification and stem cell culture in a porcine model for the study of intestinal epithelial regeneration. Plos One 8, e66465.CrossRefGoogle Scholar
Hoffmann, W 2007. TFF (trefoil factor family) peptides and their potential roles for differentiation processes during airway remodeling. Current Medicinal Chemistry 14, 2716–2719.CrossRefGoogle ScholarPubMed
Jaeger, LA, Lamar, CH, Cline, TR and Cardona, CJ 1990. Effect of orally administered epidermal growth factor on the jejunal mucosa of weaned pigs. American Journal of Veterinary Research 51, 471–474.Google ScholarPubMed
Kang, P, Toms, DY, Cheung, Q, Gong, J, De, LK and Li, J 2010. Epidermal growth factor-expressing Lactococcus lactis enhances intestinal development of early-weaned pigs. Journal of Nutrition 140, 806–811.CrossRefGoogle ScholarPubMed
Lackeyram, D and Yang, C 2010. Early weaning reduces small intestinal alkaline phosphatase expression in pigs. Journal of Nutrition 140, 461–468.CrossRefGoogle ScholarPubMed
Lee, CH, Hung, HW, Hung, PH and Shieh, YS 2010. Epidermal growth factor receptor regulates β-catenin location, stability, and transcriptional activity in oral cancer. Molecular Cancer 9, 1–12.CrossRefGoogle ScholarPubMed
Liu, CD, Rongione, AJ, Shin, MS, Ashley, SW and McFadden, DW 1996. Epidermal growth factor improves intestinal adaptation during somatostatin administration in vivo. Journal of Surgical Research 63, 163–168.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th revised edition. The National Academies Press, Washington, DC, USA.Google Scholar
Okamoto, R, Matsumoto, T and Watanabe, M 2006. Regeneration of the intestinal epithelia: regulation of bone marrow-derived epithelial cell differentiation towards secretory lineage cells. Human Cell 19, 71–75.CrossRefGoogle ScholarPubMed
Saquisalces, M, Huang, Z, Vila, MF, Li, J, Mielke, JA, Urriola, PE and Shurson, GC 2017. Modulation of intestinal cell differentiation in growing pigs is dependent on the fiber source in the diet. Journal of Animal Science 95, 1179–1190.Google Scholar
Schweiger, M, Steffl, M and Amselgruber, WM 2003. Differential expression of EGF receptor in the pig duodenum during the transition phase from maternal milk to solid food. Journal of Gastroenterology 38, 636.CrossRefGoogle ScholarPubMed
Tang, X, Liu, H, Yang, S, Li, Z, Zhong, J and Fang, R 2016. Epidermal growth factor and intestinal barrier function. Mediators of Inflammation 2016, 1–9.CrossRefGoogle ScholarPubMed
Wang, LX, Zhu, F, Yang, HS, Li, JZ, Li, YL, Ding, XQ, Xiong, X and Yin, YL 2019. Effects of dietary supplementation with epidermal growth factor on nutrient digestibility, intestinal development and expression of nutrient transporters in early-weaned piglets. Journal of Animal Physiology and Animal Nutrition 2019, 1–8.Google Scholar
Wang, S, Guo, C, Zhou, L, Zhang, Z, Huang, Y, Yang, J, Bai, X and Yang, K 2015. Comparison of the biological activities of Saccharomyces cerevisiae-expressed intracellular EGF, extracellular EGF, and tagged EGF in early-weaned pigs. Applied Microbiology & Biotechnology 99, 7125–7135.CrossRefGoogle ScholarPubMed
Xiong, X, Yang, HS, Wang, XC, Hu, Q, Liu, CX, Wu, X, Deng, D, Hou, YQ, Nyachoti, CM and Xiao, DF 2015. Effect of low dosage of chito-oligosaccharide supplementation on intestinal morphology, immune response, antioxidant capacity, and barrier function in weaned piglets. Journal of Animal Science 93, 1089–1097.CrossRefGoogle ScholarPubMed
Yan, SL, Long, LN, Zong, EY, Huang, PF, Li, JZ, Li, YL, Ding, XQ, Xiong, X and Yin, Y L 2018. Dietary sulfur amino acids affect jejunal cell proliferation and functions by affecting antioxidant capacity, Wnt/β-catenin, and the mechanistic target of rapamycin signaling pathways in weaning piglets. Journal of Animal Science 96, 5124–5133.CrossRefGoogle ScholarPubMed
Yang, HS, Xiong, X, Wang, X, Li, TJ and Yin, YL 2016a. Effects of weaning on intestinal crypt epithelial cells in piglets. Scientific Reports 6, 36939.CrossRefGoogle ScholarPubMed
Yang, HS, Xiong, X, Wang, XC, Tan, BE, Li, TJ and Yin, YL 2016b. Effects of weaning on intestinal upper villus epithelial cells of piglets. Plos One 11, e0150216.CrossRefGoogle ScholarPubMed
Yeung, TM, Chia, LA, Kosinski, CM and Kuo, CJ 2011. Regulation of self-renewal and differentiation by the intestinal stem cell niche. Cellular & Molecular Life Sciences 68, 2513–2523.CrossRefGoogle ScholarPubMed
Zhang, L, Zhou, FF, van Laar, T, Zhang, J, van Dam, H and ten Dijke, P 2011. Fas-associated factor 1 antagonizes Wnt signaling by promoting β-catenin degradation. Molecular Biology of the Cell 22, 1617–1624.CrossRefGoogle ScholarPubMed
Zijlstra, RT, Odle, J, Hall, WF, Petschow, BW, Gelberg, HB and Litov, RE 1994. Effect of orally administered epidermal growth factor on intestinal recovery of neonatal pigs infected with rotavirus. Journal of Pediatric Gastroenterology and Nutrition 19, 382–390.CrossRefGoogle ScholarPubMed
Supplementary material: File

Wang et al. supplementary material

Wang et al. supplementary material 1

Download Wang et al. supplementary material(File)
File 23.9 KB
Supplementary material: File

Wang et al. supplementary material

Wang et al. supplementary material 2

Download Wang et al. supplementary material(File)
File 4.8 MB