Toll-like receptor 4-mediated lymphocyte influx induces neonatal necrotizing enterocolitis

Journal of Clinical Investigation

Volumn 126, Issue 2, 2016, Pages 495-508

  Egan, Charlotte E ^a,b   Sodhi, Chhinder P ^c,d   Good, Misty ^a   Lin, Joyce ^a   Jia, Hongpeng ^c,d   Yamaguchi, Yukihiro ^c,d   Lu, Peng ^c,d   Ma, Congrong ^a,b   Branca, Maria F ^a,b   Weyandt, Samantha ^a,b   Fulton, William B ^c,d   Niño, Diego F ^c,d   Prindle, Thomas ^c,d   Ozolek, John A ^a   Hackam, David J ^c,d  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS CHILDREN S CENTER   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR9; GRANULOCYTE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 6; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FOXP3; TLR4 PROTEIN, HUMAN; TLR4 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE COURSE; DISEASE SEVERITY; HUMAN; HUMAN CELL; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE MUCOSA; LAMINA PROPRIA; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NECROTIZING ENTEROCOLITIS; NEWBORN; NEWBORN DISEASE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TH17 CELL; TIGHT JUNCTION; ANIMAL; DIET THERAPY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY;

ANIMALS; ENTEROCOLITIS, NECROTIZING; ENTEROCYTES; HUMANS; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; MICE; MICE, KNOCKOUT; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TIGHT JUNCTIONS; TOLL-LIKE RECEPTOR 4;

EID: 84956939804     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83356     Document Type: Article

References (57)

1. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. 2011;364(3):255-264.
2. Lim JC, Golden JM, Ford HR. Pathogenesis of neonatal necrotizing enterocolitis. Pediatr Surg Int. 2015;31(6):509-518.
3. Lu P, Sodhi CP, Hackam DJ. Toll-like receptor regulation of intestinal development and inflammation in the pathogenesis of necrotizing enterocolitis. Pathophysiology. 2014;21(1):81-93.
4. Besner GE. A pain in the NEC: research challenges and opportunities. J Pediatr Surg. 2015;50(1):23-29.
5. Patel RM, Denning PW. Intestinal microbiota and its relationship with necrotizing enterocolitis. Pediatr Res. 2015;78(3):232-238.
6. Sodhi CP, et al. Intestinal epithelial Toll-like receptor 4 regulates goblet cell development and is required for necrotizing enterocolitis in mice. Gastroenterology. 2012;143(3):708-718 e701.
7. Yazji I, et al. Endothelial TLR4 activation impairs intestinal microcirculatory perfusion in necrotizing enterocolitis via eNOS-NOnitrite signaling. Proc Natl Acad Sci U S A. 2013;110(23):9451-9456.
8. Afrazi A, et al. Toll-like receptor 4-mediated endoplasmic reticulum stress in intestinal crypts induces necrotizing enterocolitis. J Biol Chem. 2014;289(14):9584-9599.
9. Good M, et al. Lactobacillus rhamnosus HN001 decreases the severity of necrotizing enterocolitis in neonatal mice and preterm piglets: evidence in mice for a role of TLR9. Am J Physiol Gastrointest Liver Physiol. 2014;306(11):G1021-G1032.
10. Good M, et al. Breast milk protects against the development of necrotizing enterocolitis through inhibition of Toll-like receptor 4 in the intestinal epithelium via activation of the epidermal growth factor receptor. Mucosal Immunol. 2015;8(5):1166-1179.
11. Leaphart CL, et al. A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. Immunol. 2007;179(7):4808-4820.
12. Agrawal V, Jaiswal MK, Ilievski V, Beaman KD, Jilling T, Hirsch E. Platelet-activating factor: a role in preterm delivery and an essential interaction with Toll-like receptor signaling in mice. Biol Reprod. 2014;91(5):119.
13. Soliman A, et al. Platelet-activating factor induces TLR4 expression in intestinal epithelial cells: implication for the pathogenesis of necrotizing enterocolitis. PLoS One. 2010;5(10):e15044.
14. Jilling T, et al. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol. 2006;177(5):3273-3282.
15. Wolfs TG, et al. Endotoxin induced chorioamnionitis prevents intestinal development during gestation in fetal sheep. PLoS One. 2009;4(6):e5837.
16. Neal MD, et al. Discovery and validation of a new class of small molecule Toll-like receptor 4 (TLR4) inhibitors. PLoS One. 2013;8(6):e65779.
17. Good M, et al. Amniotic fluid inhibits Toll-like receptor 4 signaling in the fetal and neonatal intestinal epithelium. Proc Natl Acad Sci U S A. 2012;109(28):11330-11335.
18. Su Y, Besner GE. Heparin-binding EGF-like growth factor (HB-EGF) promotes cell migration and adhesion via focal adhesion kinase. J Surg Res. 2014;189(2):222-231.
19. Ballance WA, Dahms BB, Shenker N, Kliegman RM. Pathology of neonatal necrotizing enterocolitis: a ten-year experience. J Pediatr. 1990;117(1 pt 2):S6-13.
20. Remon JI, et al. Depth of bacterial invasion in resected intestinal tissue predicts mortality in surgical necrotizing enterocolitis. J Perinatol. 2015;35(9):755-762.
21. Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343-353.
22. Hepworth MR, et al. Immune tolerance. Science. 2015;348(6238):1031-1035.
23. von Burg N, et al. Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc Natl Acad Sci U S A. 2014;111(35):12835-12840.
24. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992;68(5):869-877.
25. Kunkel EJ, et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med. 2000;192(5):761-768.
26. Papadakis KA, et al. The role of thymusexpressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J Immunol. 2000;165(9):5069-5076.
27. Lee AY, Eri R, Lyons AB, Grimm MC, Korner H. CC Chemokine Ligand 20 and its cognate receptor CCR6 in mucosal T cell immunology and inflammatory bowel disease: odd couple or axis of evil? Front Immunol. 2013;4:194.
28. Quaroni A, Isselbacher KJ, Ruoslahti E. Fibronectin synthesis by epithelial crypt cells of rat small intestine. Proc Natl Acad Sci U S A. 1978;75(11):5548-5552.
29. Ruemmele FM, et al. Lipopolysaccharide modulation of normal enterocyte turnover by toll-like receptors is mediated by endogenously produced tumour necrosis factor {alpha}. Gut. 2002;51(6):842-848.
30. Qureshi FG, et al. Increased expression and function of integrins in enterocytes by endotoxin impairs epithelial restitution. Gastroenterology. 2005;128(4):1012-1022.
31. Gribar SC, et al. Reciprocal expression and signaling of TLR4 and TLR9 in the pathogenesis and treatment of necrotizing enterocolitis. J Immunol. 2009;182(1):636-646.
32. Chaudhry A, et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science. 2009;326(5955):986-991.
33. Mucida D, et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317(5835):256-260.
34. Lu P, et al. Animal models of gastrointestinal and liver diseases. Am J Physiol Gastrointest Liver Physiol. 2014;306(11):G917-G928.
35. Wolfs TG, et al. Localization of the lipopolysaccharide recognition complex in the human healthy and inflamed premature and adult gut. Inflamm Bowel Dis. 2010;16(1):68-75.
36. 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 U S A. 2000;97(11):6043-6048.
37. Neal MD, et al. Toll-like receptor 4 is expressed on intestinal stem cells and regulates their proliferation and apoptosis via the p53 upregulated modulator of apoptosis. J Biol Chem. 2012;287(44):37296-37308.
38. Deshmukh HS, et al. The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat Med. 2014;20(5):524-530.
39. Verdier J, Ruemmele FM. Molecular mechanisms and cell targets of Th17 cells in the gastrointestinal tract: an innate sense of adaptivity. Int Rev Immunol. 2013;32(5-6):475-492.
40. Troncone E, Marafini I, Pallone F, Monteleone G. Th17 cytokines in inflammatory bowel diseases: discerning the good from the bad. Int Rev Immunol. 2013;32(5-6):526-533.
41. Zhang Z, Zheng M, Bindas J, Schwarzenberger P, Kolls JK. Critical role of IL-17 receptor signaling in acute TNBS-induced colitis. Inflamm Bowel Dis. 2006;12(5):382-388.
42. Yang J, Sundrud MS, Skepner J, Yamagata T. Targeting Th17 cells in autoimmune diseases. Trends Pharmacol Sci. 2014;35(10):493-500.
43. Goto Y, et al. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity. 2014;40(4):594-607.
44. Goto Y, Ivanov II. Intestinal epithelial cells as mediators of the commensal-host immune crosstalk. Immunol Cell Biol. 2013;91(3):204-214.
45. Sano T, et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 responses. Cell. 2015;163(2):381-393.
46. Wang C, Collins M, Kuchroo VK. Effector T cell differentiation: are master regulators of effector T cells still the masters? Curr Opin Immunol. 2015;37:6-10.
47. Reynolds JM, et al. Interleukin-17B antagonizes interleukin-25-mediated mucosal inflammation. Immunity. 2015;42(4):692-703.
48. Raverdeau M, Mills KH. Modulation of T cell and innate immune responses by retinoic acid. J Immunol. 2014;192(7):2953-2958.
49. Si J, Collins SJ. IL-3-induced enhancement of retinoic acid receptor activity is mediated through Stat5, which physically associates with retinoic acid receptors in an IL-3-dependent manner. Blood. 2002;100(13):4401-4409.
50. McElroy SJ, Weitkamp JH. Innate immunity in the small intestine of the preterm infant. Neoreviews. 2011;12(9):e517-e526.
51. Weitkamp JH, et al. Necrotising enterocolitis is characterised by disrupted immune regulation and diminished mucosal regulatory (FOXP3)/effector (CD4, CD8) T cell ratios. Gut. 2013;62(1):73-82.
52. Dingle BM, Liu Y, Fatheree NY, Min J, Rhoads JM, Tran DQ. FoxP3(+) regulatory T cells attenuate experimental necrotizing enterocolitis. PLoS One. 2013;8(12):e82963.
53. Sato T, et al. Single Lgr5 stem cells build cryptvillus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262-265.
54. Shaffiey SA, et al. Intestinal stem cell growth and differentiation on a tubular scaffold with evaluation in small and large animals [published online ahead of print September 23, 2015]. Regen Med. doi:10.2217/rme.15.70.
55. Sodhi CP, et al. Intestinal epithelial TLR-4 activation is required for the development of acute lung injury after trauma/hemorrhagic shock via the release of HMGB1 from the gut. J Immunol. 2015;194(10):4931-4939.
56. Egan CE, Maurer KJ, Cohen SB, Mack M, Simpson KW, Denkers EY. Synergy between intraepithelial lymphocytes and lamina propria T cells drives intestinal inflammation during infection. Mucosal Immunol. 2011;4(6):658-670.
57. Neal MD, et al. A critical role for TLR4 induction of autophagy in the regulation of enterocyte migration and the pathogenesis of necrotizing enterocolitis. J Immunol. 2013;190(7):3541-3551.