Transforming growth factor-β2 and endotoxin interact to regulate homeostasis via interleukin-8 levels in the immature intestine

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 307, Issue 7, 2014, Pages G689-G699

  Nguyen, Duc Ninh ^a   Sangild, Per T ^a   Østergaard, Mette V ^a   Bering, Stine B ^a   Chatterton, Dereck E W ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Lipopoly saccharide; Necrotizing enterocolitis; Nuclear factor B; Preterm infants

Indexed keywords

ANTIINFECTIVE AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE, E. COLI 026-B6; MITOGEN ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL; ARTIFICIAL MILK; CELL LINE; CELL MOTION; CELL PROLIFERATION; COLOSTRUM; DISEASE MODEL; DRUG EFFECTS; ENTEROCOLITIS, NECROTIZING; GESTATIONAL AGE; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; NEWBORN; PATHOLOGY; PREMATURITY; SIGNAL TRANSDUCTION; SMALL INTESTINE; SWINE; TIME;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; COLOSTRUM; DISEASE MODELS, ANIMAL; ENTEROCOLITIS, NECROTIZING; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GESTATIONAL AGE; HOMEOSTASIS; HUMANS; INFANT FORMULA; INFANT, NEWBORN; INTERLEUKIN-8; INTESTINE, SMALL; LIPOPOLYSACCHARIDES; NF-KAPPA B; PREMATURE BIRTH; SIGNAL TRANSDUCTION; SWINE; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA2;

EID: 84907509814     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00193.2014     Document Type: Article

References (39)

1. Boyd CA, Quigley MA, Brocklehurst P. Donor breast milk versus infant formula for preterm infants: systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed 92: F169-F175, 2007.
2. Chatterton DEW, Nguyen DN, Bering SB, Sangild PT. Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of new-borns. Int J Biochem Cell Biol 45: 1730-1747, 2013.
3. Chatterton DEW, Rasmussen JT, Heegaard CW, Sørensen ES, Petersen TE. In vitro digestion of novel milk protein ingredients for use in infant formulas: research on biological functions. Trends Food Sci Technol 15: 373-383, 2004.
4. Cilieborg MS, Schmidt M, Skovgaard K, Boye M, Weber NR, Heegaard PM, Burrin DG, Sangild PT. Fetal lipopolysaccharide exposure modulates diet-dependent gut maturation and sensitivity to necrotising enterocolitis in pre-term pigs. Br J Nutr 106: 852-861, 2011.
5. Claud EC. Neonatal necrotizing enterocolitis-inflammation and intestinal immaturity. Antiinflamm Antiallergy Agents Med Chem 8: 248-259, 2009.
6. Deva R, Shankaranarayanan P, Ciccoli R, Nigam S. Candida albicans induces selectively transcriptional activation of cyclooxygenase-2 in HeLa cells: pivotal roles of Toll-like receptors, p38 mitogen-activated protein kinase, and NF-kappa B. J Immunol 171: 3047-3055, 2003.
7. Fujihara M, Muroi M, Tanamoto K, Suzuki T, Azuma H, Ikeda H. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol Ther 100: 171-194, 2003.
8. Gauthier SF, Pouliot Y, Maubois JL. Growth factors from bovine milk and colostrum: composition, extraction and biological activities (Abstract). Le Lait 86: 27, 2006.
9. Godlewski MM, Hallay N, Bierła JB, Zabielski R. Molecular mechanism of programmed cell death in the gut epithelium of neonatal piglets. J Physiol Pharmacol 58, Suppl 3: 97-113, 2007.
10. Good M, Siggers RH, Sodhi CP, Afrazi A, Alkhudari F, Egan CE, Neal MD, Yazji I, Jia H, Lin J, Branca MF, Ma C, Prindle T, Grant Z, Shah S, Slagle D, Paredes J, Ozolek J, Gittes GK, Hackam DJ. Amniotic fluid inhibits Toll-like receptor 4 signaling in the fetal and neonatal intestinal epithelium. Proc Natl Acad Sci USA 109: 11330-11335, 2012.
11. Hackam DJ, Good M, Sodhi CP. Mechanisms of gut barrier failure in the pathogenesis of necrotizing enterocolitis: Toll-like receptors throw the switch. Semin Pediatr Surg 22: 76-82, 2013.
12. Hering NA, Andres S, Fromm A, van Tol EA, Amasheh M, Mankertz J, Fromm M, Schulzke JD. Transforming growth factor-, a whey protein component, strengthens the intestinal barrier by upregulating claudin-4 in HT-29/B6 cells. J Nutr 141: 783-789, 2011.
13. Jensen ML, Sangild PT, Lykke M, Schmidt M, Boye M, Jensen BB, Thymann T. Similar efficacy of human banked milk and bovine colostrum to decrease incidence of necrotizing enterocolitis in preterm piglets. Am J Physiol Regul Integr Comp Physiol 305: R4-R12, 2013.
14. Jensen ML, Thymann T, Cilieborg MS, Lykke M, Mølbak L, Jensen BB, Schmidt M, Kelly D, Mulder I, Burrin DG, Sangild PT. Antibiotics modulate intestinal immunity and prevent necrotizing enterocolitis in preterm neonatal piglets. Am J Physiol Gastrointest Liver Physiol 306: G59-G71, 2014.
15. Li Y, Jensen ML, Chatterton DEW, Jensen BB, Thymann T, Kvistgaard AS, Sangild PT. Raw bovine milk improves gut responses to feeding relative to infant formula in preterm piglets. Am J Physiol Gastrointest Liver Physiol 306: G81-G90, 2014.
16. Li Y, Østergaard MV, Jiang P, Chatterton DEW, Thymann T, Kvistgaard AS, Sangild PT. Whey protein processing influences formula-induced gut maturation in preterm pigs. J Nutr 143: 1934-1942, 2013.
17. Lu T, Tian L, Han Y, Vogelbaum M, Stark GR. Dose-dependent cross-talk between the transforming growth factor-beta and interleukin-1 signaling pathways. Proc Natl Acad Sci USA 104: 4365-4370, 2007.
18. Maheshwari A, Kelly DR, Nicola T, Ambalavanan N, Jain SK, Murphy-Ullrich J, Athar M, Shimamura M, Bhandari V, Aprahamian C, Dimmitt RA, Serra R, Ohls RK. TGF-2 Suppresses Macrophage Cytokine Production and Mucosal Inflammatory Responses in the Developing Intestine. Gastroenterology 140: 242-253, 2011.
19. Maheshwari A, Lacson A, Lu W, Fox SE, Barleycorn AA, Christensen RD, Calhoun DA. Interleukin-8/CXCL8 forms an autocrine loop in fetal intestinal mucosa. Pediatr Res 56: 240-249, 2004.
20. Maheshwari A, Lu W, Guida WC, Christensen RD, Calhoun DA. IL-8/CXC ligand 8 survives neonatal gastric digestion as a result of intrinsic aspartyl proteinase resistance. Pediatr Res 57: 438-444, 2005.
21. Maheshwari A, Lu W, Lacson A, Barleycorn AA, Nolan S, Christensen RD, Calhoun DA. Effects of interleukin-8 on the developing human intestine. Cytokine 20: 256-267, 2002.
22. Maheshwari A, Voitenok NN, Akalovich S, Shaik SS, Randolph DA, Sims B, Patel RP, Killingsworth CR, Fallon MB, Ohls RK. Developmental changes in circulating IL-8/CXCL8 isoforms in neonates. Cytokine 46: 12-16, 2009.
23. Manna SK, Ramesh GT. Interleukin-8 induces nuclear transcription factor-kappaB through a TRAF6-dependent pathway. J Biol Chem 280: 7010-7021, 2005.
24. McKaig BC, Makh SS, Hawkey CJ, Podolsky DK, Mahida YR. Normal human colonic subepithelial myofibroblasts enhance epithelial migration (restitution) via TGF-3. Am J Physiol Gastrointest Liver Physiol 276: G1087-G1093, 1999.
25. Mei J, Zhang Y, Wang T, Sangild PT, Xu RJ. Oral ingestion of colostrum alters intestinal transforming growth factor-beta receptor intensity in newborn pigs. Livest Sci 105: 214-222, 2006.
26. Nanthakumar N, Meng D, Goldstein AM, Zhu W, Lu L, Uauy R, Llanos A, Claud EC, Walker WA. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: an immature innate immune response. PLoS ONE 6: e17776, 2011.
27. Nanthakumar NN, Fusunyan RD, Sanderson I, Walker WA. Inflammation in the developing human intestine: a possible pathophysiologic contribution to necrotizing enterocolitis. Proc Natl Acad Sci USA 97: 6043-6048, 2000.
28. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 364: 255-264, 2011.
29. Ozawa T, Miyata M, Nishimura M, Ando T, Ouyang Y, Ohba T, Shimokawa N, Ohnuma Y, Katoh R, Ogawa H, Nakao A. Transforming growth factor-beta activity in commercially available pasteurized cow milk provides protection against inflammation in mice. J Nutr 139: 69-75, 2009.
30. Puiman PJ, Jensen M, Stoll B, Renes IB, de Bruijn ACJM, Dorst K, Schierbeek H, Schmidt M, Boehm G, Burrin DG, Sangild PT, van Goudoever JB. Intestinal threonine utilization for protein and mucin synthesis is decreased in formula-fed preterm pigs. J Nutr 141: 1306-1311, 2011.
31. Rautava S, Lu L, Nanthakumar NN, Dubert-Ferrandon A, Walker WA. TGF-2 induces maturation of immature human intestinal epithelial cells and inhibits inflammatory cytokine responses induced via the NF-B pathway. J Pediatr Gastroenterol Nutr 54: 630-638, 2012.
32. Rautava S, Nanthakumar NN, Dubert-Ferrandon A, Lu L, Rautava J, Walker WA. Breast milk-transforming growth factor-2 specifically at-tenuates IL-1-induced inflammatory responses in the immature human intestine via an SMAD6-and ERK-dependent mechanism. Neonatology 99: 192-201, 2011.
33. Sangild PT, Mei J, Fowden AL, Xu RJ. The prenatal porcine intestine has low transforming growth factor-beta ligand and receptor density and shows reduced trophic response to enteral diets. Am J Physiol Regul Integr Comp Physiol 296: R1053-R1062, 2009.
34. Sangild PT, Siggers RH, Schmidt M, Elnif J, Bjornvad CR, Thymann T, Grondahl ML, Hansen AK, Jensen SK, Boye M, Moelbak L, Buddington RK, Weström BR, Holst JJ, Burrin DG. Diet-and colonization-dependent intestinal dysfunction predisposes to necrotizing en-terocolitis in preterm pigs. Gastroenterology 130: 1776-1792, 2006.
35. Sangild PT, Thymann T, Schmidt M, Stoll B, Burrin DG, Buddington RK. Invited review: the preterm pig as a model in pediatric gastroenterology. J Anim Sci 91: 4713-4729, 2013.
36. Siggers J, Ostergaard MV, Siggers RH, Skovgaard K, Mølbak L, Thymann T, Schmidt M, Møller HK, Purup S, Fink LN, Frøkiær H, Boye M, Sangild PT, Bering SB. Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates. Am J Physiol Gastrointest Liver Physiol 304: G864-G875, 2013.
37. Støy ACF, Heegaard PMH, Thymann T, Bjerre M, Skovgaard K, Boye M, Stoll B, Schmidt M, Jensen BB, Sangild PT. Bovine colostrum improves intestinal function following formula-induced gut inflammation in preterm pigs. Clin Nutr 33: 322-329, 2014.
38. Sullivan S, Schanler RJ, Kim JH, Patel AL, Trawöger R, Kiechl-Kohlendorfer U, Chan GM, Blanco CL, Abrams S, Cotten CM, Laroia N, Ehrenkranz RA, Dudell G, Cristofalo EA, Meier P, Lee ML, Rechtman DJ, Lucas A. An exclusively human milk-based diet is associated with a lower rate of necrotizing enterocolitis than a diet of human milk and bovine milk-based products. J Pediatr 156: 562-567, 2010.
39. Van’t Land B, Meijer HP, Frerichs J, Koetsier M, Jager D, Smeets RL, M’Rabet L, Hoijer M. 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, 2002.