Glutamine downregulates TLR-2 and TLR-4 expression and protects intestinal tract in preterm neonatal rats with necrotizing enterocolitis

Journal of Pediatric Surgery

Volumn 49, Issue 7, 2014, Pages 1057-1063

  Zhou, Wei ^a   Li, Wei ^b   Zheng, Xiao Hui ^b   Rong, Xiao ^a   Huang, Long Guang ^a  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b Taiping People's Hospital of Dongguan)   (China)

Author keywords

Cell apoptosis; Glutamine; Necrotizing enterocolitis; Toll like receptor 2; Toll like receptor 4

Indexed keywords

CASPASE 3; GLUTAMINE; MESSENGER RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TLR4 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ARTIFICIAL MILK; COLD STRESS; COLON; CONTROLLED STUDY; CORRELATIONAL STUDY; DOWN REGULATION; FEEDING; HYPOXIA; ILEUM; IMMUNOHISTOCHEMISTRY; INTESTINE; INTESTINE INJURY; INTESTINE MUCOSA; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; DISEASE MODEL; DRUG EFFECTS; FEMALE; IMMUNOLOGY; METABOLISM; PATHOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; CASPASE 3; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENTEROCOLITIS, NECROTIZING; FEMALE; GLUTAMINE; INTESTINAL MUCOSA; INTESTINES; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84902978166     PISSN: 00223468     EISSN: 15315037     Source Type: Journal    
DOI: 10.1016/j.jpedsurg.2014.02.078     Document Type: Article

References (51)

1. J.A. Lemons, C.R. Bauer, and W. Oh et al. Very low birth weight outcomes of the National Institute of Child health and human development neonatal research network, January 1995 through December 1996. NICHD Neonatal Research Network Pediatrics 107 2001 E1 E8
2. C.J. Hunter, J.S. Upperman, and H.R. Ford et al. Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC) Pediatr Res 63 2008 117 123
3. B. Frost, T. Jilling, and M. Caplan The importance of pro-inflammatory signaling in neonatal necrotizing enterocolitis Semin Perinatol 32 2008 100 106 (Pubitemid 351381163)
4. M.B. Edelson, C.E. Bagwell, and H.J. Rozycki Circulating pro- and counterinflammatory cytokine levels and severity in necrotizing enterocolitis Pediatrics 103 1999 766 771 (Pubitemid 29274469)
5. M.T. Abreu, M. Fukata, and M. Arditi TLR signaling in the gut in health and disease J Immunol 174 2005 4453 4460
6. Y. Liu, L. Zhu, and N.Y. Fatheree et al. Changes in intestinal Toll-like receptors and cytokines precede histological injury in a rat model of necrotizing enterocolitis Am J Physiol Gastrointest Liver Physiol 297 2009 G442 G450
7. N. Nanthakumar, D. Meng, and A.M. Goldstein et al. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: an immature innate immune response PLoS One 6 2011 e17776
8. C.P. Sodhi, M.D. Neal, and R. Siggers et al. Intestinal epithelial Toll-like receptor 4 regulates goblet cell development and is required for necrotizing enterocolitis in mice Gastroenterology 143 2012 708.e1-5 718.e1-5
9. A.P. Houdijk, E.R. Rijnsburger, and J. Jansen et al. Randomised trial of glutamine-enriched enteral nutrition on infectious morbidity in patients with multiple trauma Lancet 352 1998 772 776
10. F. Novak, D.K. Heyland, and A. Avenell et al. Glutamine supplementation in serious illness: a systematic review of the evidence Crit Care Med 30 2002 2022 2029
11. I. Sukhotnik, M. Agam, and R. Shamir et al. Oral glutamine prevents gut mucosal injury and improves mucosal recovery following lipopolysaccharide endotoxemia in a rat J Surg Res 143 2007 379 384 (Pubitemid 350110445)
12. N. Li, K. Liboni, and M.Z. Fang et al. Glutamine decreases lipopolysaccharide-induced intestinal inflammation in infant rats Am J Physiol Gastrointest Liver Physiol 286 2004 G914 G921
13. A. Dilsiz, I. Ciftçi, and T.M. Aktan et al. Enteral glutamine supplementation and dexamenthasone attenuate the local intestinal damage in rats with experimental necrotizing enterocolitis Pediatr Surg Int 19 2003 578 582 (Pubitemid 37408888)
14. A. van den Berg, W.P. Fetter, and E.A. Westerbeek et al. The effect of glutamine-enriched enteral nutrition on intestinal permeability in very-low-birth-weight infants: a randomized controlled trial JPEN J Parenter Enteral Nutr 30 5 2006 408 414
15. K. Bober-Olesińska, and M.K. Kornacka Effects of glutamine supplemented parenteral nutrition on the incidence of necrotizing enterocolitis, nosocomial sepsis and length of hospital stay in very low birth weight infants Med Wieku Rozwoj 9 3 Pt 1 2005 325 333
16. S. Sevastiadou, A. Malamitsi-Puchner, and C. Costalos et al. The impact of oral glutamine supplementation on the intestinal permeability and incidence of necrotizing enterocolitis/septicemia in premature neonates J Matern Fetal Neonatal Med 24 10 2011 1294 1300
17. W. Li, X.H. Zheng, and W. Zhou et al. Regulatory effects of glutamine on Toll-like receptor 4 in neonatal rats with necrotizing enterocolitis Zhongguo Dang Dai Er Ke Za Zhi 13 2011 419 423 [Article in Chinese]
18. N. Auestad, R.A. Korsak, and J.D. Bergstrom et al. Milk-substitutes comparable to rat's milk; their preparation, composition and impact on development and metabolism in the artificially reared rat Br J Nutr 61 1989 495 518 (Pubitemid 19180380)
19. B. Beutler Inferences, questions and possibilities in Toll-like receptor signaling Nature 430 2004 257 263 (Pubitemid 38902439)
20. R. Medzhitov, P. Preston-Hurlburt, and C.A. Janeway Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity Nature 388 1997 394 397 (Pubitemid 27334820)
21. C.J. Kirschning, H. Wesche, and T. Merrill Ayres et al. Human toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide J Exp Med 188 1998 2091 2097 (Pubitemid 28562526)
22. N. Hirata, Y. Yanagawa, and T. Ebihara et al. Selective synergy in antiinflammatory cytokine production upon cooperated signaling via TLR4 and TLR2 in murine conventional dendritic cells Mol Immunol 45 2008 2734 2742
23. Schultz A. Le Mandat, A. Bonnard, and F. Barreau et al. Expression of TLR-2, TLR-4, NOD2 and PNF-kappaB in a neonatal rat model of necrotizing enterocolitis PLoS ONE 2 2007 e1102
24. T.G. Wolfs, J.P. Derikx, and C.M. Hodin et al. Localization of the lipopolysaccharide recognition complex in the human healthy and inflamed premature and adult gut Inflamm Bowel Dis 16 2010 68 75
25. T. Jilling, J. Lu, and M. Jackson et al. Intestinal epithelial apoptosis initiates gross bowel necrosis in an experimental rat model of neonatal necrotizing enterocolitis Pediatr Res 55 2004 622 629 (Pubitemid 38405849)
26. C.P. Sodhi, X.H. Shi, and W.M. Richardson et al. Toll-like receptor-4 inhibits enterocyte proliferation via impaired beta-catenin signaling in necrotizing enterocolitis Gastroenterology 138 2010 185 196
27. M.D. Neal, C.P. Sodhi, and H. Jia et al. Toll-like receptor 4 is expressed on intestinal stem cells and regulates their proliferation and apoptosis via the p53 up-regulated modulator of apoptosis J Biol Chem 287 2012 37296 37308
28. E. LeBouder, J.E. Rey-Nores, and A.C. Raby et al. Modulation of neonatal microbial recognition: TLR-mediated innate immune responses are specifically and differentially modulated by human milk J Immunol 176 2006 3742 3752 (Pubitemid 43364021)
29. S.B. Mkaddem, M. Bens, and A. Vandewalle et al. Differential activation of Toll-like receptor-mediated apoptosis induced by hypoxia Oncotarget 1 2010 741 750
30. N.N. Nanthakumar, R.D. Fusunyan, and I. Sanderson et al. Inflammation in the developing human intestine: a possible pathophysiologic contribution to necrotizing enterocolitis Proc Natl Acad Sci U S A 97 2000 6043 6048 (Pubitemid 30367520)
31. E.C. Claud, L. Lu, and P.M. Anton et al. Developmentally regulated IkappaB expression in intestinal epithelium and susceptibility to flagellin-induced inflammation Proc Natl Acad Sci U S A 101 2004 7404 7408 (Pubitemid 38638045)
32. R. Conejero, A. Bonet, and T. Grau et al. Effect of a glutamine enriched enteral diet on intestinal permeability and infectious morbidity at 28 days in critically ill patients with systemic inflammatory response syndrome: a randomized, single blind, prospective, multicenter study Nutrition 18 9 2002 716 721 (Pubitemid 35286378)
33. A. Kessel, E. Toubi, and E. Pavlotzky et al. Treatment with glutamine is associated with down-regulation of Toll-like receptor-4 and myeloid differentiation factor 88 expression and decrease in intestinal mucosal injury caused by lipopolysaccharide endotoxaemia in a rat Clin Exp Immunol 151 2 2008 341 347
34. S.D. Larson, J. Li, and D.H. Chung et al. Molecular mechanisms contributing to glutamine-mediated intestinal cell survival Am J Physiol Gastrointest Liver Physiol 293 2007 G1262 G1271
35. J.F. Pittet, H. Lee, and D. Morabito et al. Serum levels of Hsp 72 measured early after trauma correlate with survival J Trauma 52 2002 611 617 (Pubitemid 34437214)
36. E.K. Kim, K.Y. Lee, and H.J. Lee et al. Heat shock pretreatment reduces intestinal injury in a neonatal rat model of early necrotizing enterocolitis Neonatology 103 2013 1 6
37. W.Y. Kwon, G.J. Suh, and K.S. Kim et al. Glutamine attenuates acute lung injury by inhibition of high mobility group box protein-1 expression during sepsis Br J Nutr 103 2010 890 898
38. K.D. Singleton, and P.E. Wischmeyer Glutamine's protection against sepsis and lung injury is dependent on heat shock protein 70 expression Am J Physiol Regul Integr Comp Physiol 292 2007 R1839 R1845
39. A. Afrazi, C.P. Sodhi, and M. Good et al. Intracellular heat shock protein-70 negatively regulates TLR4 signaling in the newborn intestinal epithelium J Immunol 188 2012 4543 4557
40. M.D. Neal, C.P. Sodhi, and M. Dyer et al. A critical role for TLR4 induction of autophagy in the regulation of enterocyte migration and the pathogenesis of necrotizing enterocolitis J Immunol 190 2013 3541 3551
41. R.V. Durán, W. Oppliger, and A.M. Robitaille et al. Glutaminolysis activates Rag-mTORC1 signaling Mol Cell 47 2012 349 358
42. S.F. Hsu, C.M. Chao, and W.T. Huang et al. Attenuating heat-induced cellular autophagy, apoptosis and damage in H9c2 cardiomyocytes by pre-inducing HSP70 with heat shock preconditioning Int J Hyperthermia 29 2013 239 247
43. S. Philipsen, and G. Suske A tale of three fingers: the family of mammalian Sp/XKLF transcription factors Nucleic Acids Res 27 1999 2991 3000 (Pubitemid 29355710)
44. K. Ban, and R.A. Kozar Glutamine protects against apoptosis via downregulation of Sp3 in intestinal epithelial cells Am J Physiol Gastrointest Liver Physiol 299 2010 G1344 G1353
45. S. Niederlechner, C. Baird, and B. Petrie Epidermal growth factor receptor expression and signaling are essential in glutamine's cytoprotective mechanism in heat-stressed intestinal epithelial-6 cells Am J Physiol Gastrointest Liver Physiol 304 2013 G543 G552
46. M. Rhoads Glutamine signaling in intestinal cells JPEN J Parenter Enteral Nutr 23 1999 S38 S40
47. C.J. Aprahamian, R.G. Lorenz, and C.M. Harmon et al. Toll-like receptor 2 is protective of ischemia-reperfusion-mediated small-bowel injury in a murine model Pediatr Crit Care Med 9 2008 105 109
48. B. Foligné, S. Nutten, and L. Steidler et al. Recommendations for improved use of the murine TNBS-induced colitis model in evaluating anti-inflammatory properties of lactic acid bacteria: technical and microbiological aspects Dig Dis Sci 51 2006 390 400
49. J. Fan, R.S. Frey, and A.B. Malik TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase J Clin Invest 112 2003 1234 1243 (Pubitemid 38056300)
50. T. Musikacharoen, T. Matsuguchi, and T. Kikuchi et al. NF-kappa B and STAT5 play important roles in the regulation of mouse Toll-like receptor 2 gene expression J Immunol 166 2001 4516 4524 (Pubitemid 32233736)
51. Y. Liu, Y. Wang, and M. Yamakuchi et al. Upregulation of toll-like receptor 2 gene expression in macrophage response to peptidoglycan and high concentration of lipopolysaccharide is involved in NF-kappa b activation Infect Immun 69 2001 2788 2796 (Pubitemid 32332166)