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Mediators of Inflammation
Volume 2016, Article ID 1927348, 9 pages
http://dx.doi.org/10.1155/2016/1927348
Review Article

Epidermal Growth Factor and Intestinal Barrier Function

1College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128, China
2Hunan Co-Innovation Center of Animal Production Safety, Changsha 410128, China
3Hunan Polytechnic of Environment and Biology, Hengyang 421005, China

Received 5 April 2016; Accepted 26 June 2016

Academic Editor: Dianne Cooper

Copyright © 2016 Xiaopeng Tang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. C. Arrieta, L. Bistritz, and J. B. Meddings, “Alterations in intestinal permeability,” Gut, vol. 55, no. 10, pp. 1512–1520, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Wang, C. Zhang, G. Wu et al., “Glutamine enhances tight junction protein expression and modulates corticotropin-releasing factor signaling in the jejunum of weanling piglets,” The Journal of Nutrition, vol. 145, no. 1, pp. 25–31, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Camilleri, K. Madsen, R. Spiller, B. G. Van Meerveld, and G. N. Verne, “Intestinal barrier function in health and gastrointestinal disease,” Neurogastroenterology and Motility, vol. 24, no. 6, pp. 503–512, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. R. K. Rao and G. Samak, “Role of glutamine in protection of intestinal epithelial tight junctions,” Journal of Epithelial Biology and Pharmacology, vol. 5, supplement 1, pp. 47–54, 2012. View at Google Scholar · View at Scopus
  5. X. Han, H. Song, Y. Wang, Y. Sheng, and J. Chen, “Sodium butyrate protects the intestinal barrier function in peritonitic mice,” International Journal of Clinical and Experimental Medicine, vol. 8, no. 3, pp. 4000–4007, 2015. View at Google Scholar · View at Scopus
  6. N. de Diego-Cabero, A. Mereu, D. Menoyo, J. J. Holst, and I. R. Ipharraguerre, “Bile acid mediated effects on gut integrity and performance of early-weaned piglets,” BMC Veterinary Research, vol. 11, no. 1, article 111, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Yang, C. Hou, X. Zeng, and S. Qiao, “The use of lactic Acid bacteria as a probiotic in Swine diets,” Pathogens, vol. 4, no. 1, pp. 34–45, 2015. View at Publisher · View at Google Scholar
  8. Y.-L. Chen, H.-C. Peng, Y.-C. Hsieh, and S.-C. Yang, “Epidermal growth factor improved alcohol-induced inflammation in rats,” Alcohol, vol. 48, no. 7, pp. 701–706, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Kaur, C. Vaishnavi, P. Ray, M. Singh, and R. Kochhar, “Preliminary investigation on the effect of lactobacillus and epidermal growth factor on tight junction proteins in experimental Clostridium difficile infection,” Advances in Microbiology, vol. 4, no. 8, pp. 425–435, 2014. View at Google Scholar
  10. S. Cohen, “Isolation of a mouse submaxillary gland protein accelerating incisor eruption and eyelid opening in the new-born animal,” The Journal of Biological Chemistry, vol. 237, pp. 1555–1562, 1962. View at Google Scholar
  11. H. F. Zeng and R. C. Harris, “Epidermal growth factor, from gene organization to bedside,” Seminars in Cell & Developmental Biology, vol. 28, pp. 2–11, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. P. B. Alexander, L. Yuan, P. Yang et al., “EGF promotes mammalian cell growth by suppressing cellular senescence,” Cell Research, vol. 25, no. 1, pp. 135–138, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Iwabu, K. Smith, F. D. Allen, D. A. Lauffenburger, and A. Wells, “Epidermal growth factor induces fibroblast contractility and motility via a protein kinase C δ-dependent pathway,” Journal of Biological Chemistry, vol. 279, no. 15, pp. 14551–14560, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. W. Jeong, J. Kim, F. W. Bazer, and G. Song, “Epidermal growth factor stimulates proliferation and migration of porcine trophectoderm cells through protooncogenic protein kinase 1 and extracellular-signal-regulated kinases 1/2 mitogen-activated protein kinase signal transduction cascades during early pregnancy,” Molecular and Cellular Endocrinology, vol. 381, no. 1-2, pp. 302–311, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Bedford, T. Chen, E. Huynh et al., “Epidermal growth factor containing culture supernatant enhances intestine development of early-weaned pigs in vivo: Potential mechanisms involved,” Journal of Biotechnology, vol. 196-197, pp. 9–19, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Arda-Pirincci and S. Bolkent, “The role of epidermal growth factor in prevention of oxidative injury and apoptosis induced by intestinal ischemia/reperfusion in rats,” Acta Histochemica, vol. 116, no. 1, pp. 167–175, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Duh, N. Mouri, D. Warburton, and D. W. Thomas, “EGF regulates early embryonic mouse gut development in chemically defined organ culture,” Pediatric Research, vol. 48, no. 6, pp. 794–802, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. T. M. Brand, M. Iida, C. Li, and D. L. Wheeler, “The nuclear epidermal growth factor receptor signaling network and its role in cancer,” Discovery Medicine, vol. 12, no. 66, pp. 419–432, 2011. View at Google Scholar · View at Scopus
  19. D. N. Lee, W. F. Chang, I. T. Yu, P. W. S. Chiou, and C. F. Weng, “Effects of diets supplemented with recombinant epidermal growth factor and glutamine on gastrointestinal tract development of early-weaned piglets,” Asian-Australasian Journal of Animal Sciences, vol. 21, no. 4, pp. 582–589, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Kang, D. Toms, Y. Yin et al., “Epidermal growth factor-expressing Lactococcus lactis enhances intestinal development of early-weaned pigs,” The Journal of Nutrition, vol. 140, no. 4, pp. 806–811, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Wang, S. Xu, Y. Lin et al., “Recombinant porcine epidermal growth factor-secreting Lactococcus lactis promotes the growth performance of early-weaned piglets,” BMC Veterinary Research, vol. 10, no. 1, article 171, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Xu, D. Wang, P. Zhang et al., “Oral administration of Lactococcus lactis-expressed recombinant porcine epidermal growth factor stimulates the development and promotes the health of small intestines in early-weaned piglets,” Journal of Applied Microbiology, vol. 119, no. 1, pp. 225–235, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Basuroy, A. Seth, B. Elias, A. P. Naren, and R. Rao, “MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide,” Biochemical Journal, vol. 393, no. 1, pp. 69–77, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Samak, S. Aggarwal, and R. K. Rao, “ERK is involved in EGF-mediated protection of tight junctions, but not adherens junctions, in acetaldehyde-treated Caco-2 cell monolayers,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 301, no. 1, pp. G50–G59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. V. García-Hernández, C. Flores-Maldonado, R. Rincon-Heredia et al., “EGF regulates claudin-2 and -4 expression through Src and STAT3 in MDCK cells,” Journal of Cellular Physiology, vol. 230, no. 1, pp. 105–115, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. A. A. Maynard, K. Dvorak, L. Khailova et al., “Epidermal growth factor reduces autophagy in intestinal epithelium and in the rat model of necrotizing enterocolitis,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 299, no. 3, pp. G614–G622, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Buret, M. E. Olson, D. Grant Gall, and J. A. Hardin, “Effects of orally administered epidermal growth factor on enteropathogenic Escherichia coli infection in rabbits,” Infection and Immunity, vol. 66, no. 10, pp. 4917–4923, 1998. View at Google Scholar · View at Scopus
  28. A. G. Buret, K. Mitchell, D. G. Muench, and K. G. E. Scott, “Giardia lamblia disrupts tight junctional ZO-1 and increases permeability in non-transformed human small intestinal epithelial monolayers: effects of epidermal growth factor,” Parasitology, vol. 125, no. 1, pp. 11–19, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. A. G. Buret, A. C. Chin, and K. G. E. Scott, “Infection of human and bovine epithelial cells with Cryptosporidium andersoni induces apoptosis and disrupts tight junctional ZO-1: effects of epidermal growth factor,” International Journal for Parasitology, vol. 33, no. 12, pp. 1363–1371, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Lamb-Rosteski, L. D. Kalischuk, G. D. Inglis, and A. G. Buret, “Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation,” Infection and Immunity, vol. 76, no. 8, pp. 3390–3398, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. N. E. Avissar, H. T. Wang, J.-N. H. Miller, P. Iannoli, and H. C. Sax, “Epidermal growth factor receptor is increased in rabbit intestinal brush border membrane after small bowel resection,” Digestive Diseases and Sciences, vol. 45, no. 6, pp. 1145–1152, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. J. A. Clark, A. T. Clark, R. S. Hotchkiss, T. G. Buchman, and C. M. Coopersmith, “Epidermal growth factor treatment decreases mortality and is associated with improved gut integrity in sepsis,” Shock, vol. 30, no. 1, pp. 36–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Wee, H. Shi, J. Jiang, Y. Wang, and Z. Wang, “EGF stimulates the activation of EGF receptors and the selective activation of major signaling pathways during mitosis,” Cellular Signalling, vol. 27, no. 3, pp. 638–651, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Nojiri, T. Yoshizato, T. Fukami et al., “Clinical significance of amphiregulin and epidermal growth factor in colostrum,” Archives of Gynecology and Obstetrics, vol. 286, no. 3, pp. 643–647, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Cellini, J. Xu, A. Arriaga, and T. L. Buchmiller-Crair, “Effect of epidermal growth factor infusion on fetal rabbit intrauterine growth retardation and small intestinal development,” Journal of Pediatric Surgery, vol. 39, no. 6, pp. 891–897, 2004. View at Google Scholar
  36. D.-N. Lee, T.-Y. Kuo, M.-C. Chen, T.-Y. Tang, F.-H. Liu, and C.-F. Weng, “Expression of porcine epidermal growth factor in Pichia pastoris and its biology activity in early-weaned piglets,” Life Sciences, vol. 78, no. 6, pp. 649–654, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. Q. C. K. Cheung, Z. Yuan, P. W. Dyce, De Wu, K. Delange, and J. Li, “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, vol. 89, no. 3, pp. 871–879, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Wang, C. Guo, L. Zhou et al., “Comparison of the biological activities of Saccharomyces cerevisiae-expressed intracellular EGF, extracellular EGF, and tagged EGF in early-weaned pigs,” Applied Microbiology and Biotechnology, vol. 99, no. 17, pp. 7125–7135, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Wang, L. Zhou, H. Chen et al., “Analysis of the biological activities of Saccharomyces cerevisiae expressing intracellular EGF, extracellular EGF, and tagged EGF in early-weaned rats,” Applied Microbiology and Biotechnology, vol. 99, no. 5, pp. 2179–2189, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Banan, L. J. Zhang, M. Shaikh, J. Z. Fields, A. Farhadi, and A. Keshavarzian, “Inhibition of oxidant-induced nuclear factor-κB activation and inhibitory-κBα degradation and instability of F-actin cytoskeletal dynamics and barrier function by epidermal growth factor: key role of phospholipase-γ isoform,” Journal of Pharmacology and Experimental Therapeutics, vol. 309, no. 1, pp. 356–368, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. J. A. Clark, S. M. Doelle, M. D. Halpern et al., “Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 291, no. 5, pp. G938–G949, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Damiano, A. Morano, V. Ucci et al., “Dual oxidase 2 generated reactive oxygen species selectively mediate the induction of mucins by epidermal growth factor in enterocytes,” The International Journal of Biochemistry & Cell Biology, vol. 60, pp. 8–18, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. K. R. Groschwitz and S. P. Hogan, “Intestinal barrier function: molecular regulation and disease pathogenesis,” Journal of Allergy and Clinical Immunology, vol. 124, no. 1, pp. 3–20, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. Y.-B. Yu and Y.-Q. Li, “Enteric glial cells and their role in the intestinal epithelial barrier,” World Journal of Gastroenterology, vol. 20, no. 32, pp. 11273–11280, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Günzel and A. S. L. Yu, “Claudins and the modulation of tight junction permeability,” Physiological Reviews, vol. 93, no. 2, pp. 525–569, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Wang, G. Wu, Z. Zhou et al., “Glutamine and intestinal barrier function,” Amino Acids, vol. 47, no. 10, pp. 2143–2154, 2015. View at Publisher · View at Google Scholar
  47. K. Matter and M. S. Balda, “Signalling to and from tight junctions,” Nature Reviews Molecular Cell Biology, vol. 4, no. 3, pp. 225–236, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Chen, D. F. Li, Z. L. Dai et al., “l-methionine supplementation maintains the integrity and barrier function of the small-intestinal mucosa in post-weaning piglets,” Amino Acids, vol. 46, no. 4, pp. 1131–1142, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Jung, B.-K. Kang, J.-Y. Kim, K.-S. Shin, C.-S. Lee, and D.-S. Song, “Effects of epidermal growth factor on atrophic enteritis in piglets induced by experimental porcine epidemic diarrhoea virus,” Veterinary Journal, vol. 177, no. 2, pp. 231–235, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Banan, J. Z. Fields, D. A. Talmage, Y. Zhang, and A. Keshavarzian, “PKC-β1 mediates EGF protection of microtubules and barrier of intestinal monolayers against oxidants,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 281, no. 3, pp. G833–G847, 2001. View at Google Scholar · View at Scopus
  51. A. Banan, J. Z. Fields, D. A. Talmage, L. Zhang, and A. Keshavarzian, “PKC-ζ is required in EGF protection of microtubules and intestinal barrier integrity against oxidant injury,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 282, no. 5, pp. G794–G808, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Banan, L. J. Zhang, A. Farhadi, J. Z. Fields, M. Shaikh, and A. Keshavarzian, “PKC-β1 isoform activation is required for EGF-induced NF-κB inactivation and IκBα stabilization and protection of F-actin assembly and barrier function in enterocyte monolayers,” American Journal of Physiology-Cell Physiology, vol. 286, no. 3, pp. C723–C738, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Basuroy, P. Sheth, C. M. Mansbach, and R. K. Rao, “Acetaldehyde disrupts tight junctions and adherens junctions in human colonic mucosa: protection by EGF and l-glutamine,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 289, no. 2, pp. G367–G375, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. P. Sheth, A. Seth, M. Thangavel, S. Basuroy, and R. K. Rao, “Epidermal growth factor prevents acetaldehyde-induced paracellular permeability in Caco-2 cell monolayer,” Alcoholism: Clinical and Experimental Research, vol. 28, no. 5, pp. 797–804, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Suzuki, A. Seth, and R. Rao, “Role of phospholipase Cγ-induced activation of protein kinase Cϵ (PKCϵ) and PKCβI in epidermal growth factor-mediated protection of tight junctions from acetaldehyde in Caco-2 cell monolayers,” The Journal of Biological Chemistry, vol. 283, pp. 3574–3583, 2008. View at Publisher · View at Google Scholar
  56. S. R. Guntaka, G. Samak, A. Seth, N. F. LaRusso, and R. Rao, “Epidermal growth factor protects the apical junctional complexes from hydrogen peroxide in bile duct epithelium,” Laboratory Investigation, vol. 91, no. 9, pp. 1396–1409, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Ogawa, T. Kojima, M. Someya et al., “Epidermal growth factor modulates claudins and tight junctional functions in ovarian cancer cell lines,” Histochemistry and Cell Biology, vol. 138, no. 2, pp. 323–338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Ikari, K. Atomi, A. Takiguchi, Y. Yamazaki, M. Miwa, and J. Sugatani, “Epidermal growth factor increases claudin-4 expression mediated by Sp1 elevation in MDCK cells,” Biochemical and Biophysical Research Communications, vol. 384, no. 3, pp. 306–310, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. H. Okuyama, M. Urao, D. Lee, R. A. Drongowski, and A. G. Coran, “The effect of epidermal growth factor on bacterial translocation in newborn rabbits,” Journal of Pediatric Surgery, vol. 33, no. 2, pp. 225–228, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. S. N. Elliott, J. L. Wallace, W. McKnight et al., “Bacterial colonization and healing of gastric ulcers: the effects of epidermal growth factor,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 278, no. 1, pp. G105–G112, 2000. View at Google Scholar
  61. C. E. Overgaard, B. L. Daugherty, L. A. Mitchell, and M. Koval, “Claudins: control of barrier function and regulation in response to oxidant stress,” Antioxidants and Redox Signaling, vol. 15, no. 5, pp. 1179–1193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Suzuki, “Regulation of intestinal epithelial permeability by tight junctions,” Cellular and Molecular Life Sciences, vol. 70, no. 4, pp. 631–659, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Ulluwishewa, R. C. Anderson, W. C. McNabb, P. J. Moughan, J. M. Wells, and N. C. Roy, “Regulation of tight junction permeability by intestinal bacteria and dietary components,” Journal of Nutrition, vol. 141, no. 5, pp. 769–776, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Geng, J. Li, F. Wang et al., “Epidermal growth factor promotes proliferation and improves restoration after intestinal ischemia-reperfusion injury in rats,” Inflammation, vol. 36, no. 3, pp. 670–679, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Rao, “Oxidative stress-induced disruption of epithelial and endothelial tight junctions,” Frontiers in Bioscience, vol. 13, no. 18, pp. 7210–7226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. J. M. Campbell, J. D. Crenshaw, and J. Polo, “The biological stress of early weaned piglets,” Journal of Animal Science and Biotechnology, vol. 4, no. 1, article 19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Banan, A. Keshavarzian, L. Zhang et al., “NF-κB activation as a key mechanism in ethanol-induced disruption of the F-actin cytoskeleton and monolayer barrier integrity in intestinal epithelium,” Alcohol, vol. 41, no. 6, pp. 447–460, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. R. R. Nair, B. B. Warner, and B. W. Warner, “Role of Epidermal growth factor and other growth factors in the prevention of necrotizing enterocolitis,” Seminars in Perinatology, vol. 32, no. 2, pp. 107–113, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. K. Ludmila, D. Katerina, K. M. Arganbright, C. S. Williams, M. D. Halpern, and D. Bohuslav, “Changes in hepatic cell junctions structure during experimental necrotizing enterocolitis: effect of EGF treatment,” Pediatric Research, vol. 66, no. 2, pp. 140–144, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. M. D. Halpern and P. W. Denning, “The role of intestinal epithelial barrier function in the development of NEC,” Tissue Barriers, vol. 3, no. 1-2, article e1000707, 2015. View at Publisher · View at Google Scholar
  71. M. E. Johansson, H. Sjövall, and G. C. Hansson, “The gastrointestinal mucus system in health and disease,” Nature Reviews Gastroenterology & Hepatology, vol. 10, no. 6, pp. 352–361, 2013. View at Publisher · View at Google Scholar
  72. P. Mannon and W. Reinisch, “Interleukin 13 and its role in gut defence and inflammation,” Gut, vol. 61, no. 12, pp. 1765–1773, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Iwakiri and D. K. Podolsky, “Keratinocyte growth factor promotes goblet cell differentiation through regulation of goblet cell silencer inhibitor,” Gastroenterology, vol. 120, no. 6, pp. 1372–1380, 2001. View at Publisher · View at Google Scholar · View at Scopus
  74. X. De Deken, B. Corvilain, J. E. Dumont, and F. Miot, “Roles of DUOX-mediated hydrogen peroxide in metabolism, host defense, and signaling,” Antioxidants & Redox Signaling, vol. 20, no. 17, pp. 2776–2793, 2014. View at Publisher · View at Google Scholar · View at Scopus