Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: A potential role in neonatal necrotizing enterocolitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 4, 2011, Pages

  McElroy, Steven J ^a   Prince, Lawrence S ^a   Weitkamp, Jörn Hendrik ^a   Reese, Jeff ^a   Slaughter, James C ^a   Polk, D Brent ^b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Cytokines; Goblet cells; Intestinal inflammation; Muc2; Mucus secretion

Indexed keywords

MESSENGER RNA; MUCIN 2; MUCIN 3; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL LOSS; CONTROLLED STUDY; GOBLET CELL; HUMAN; HUMAN TISSUE; HYPERSENSITIVITY; ILEUM; IMMATURITY; MOUSE; MUCUS SECRETION; NECROTIZING ENTEROCOLITIS; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE; UPREGULATION;

ANIMALS; ENTEROCOLITIS, NECROTIZING; GOBLET CELLS; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; MUCIN-2; MUCIN-3; MUCINS; MUCUS; PANETH CELLS; PROTO-ONCOGENE PROTEINS C-ETS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80053192711     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00550.2010     Document Type: Article

References (54)

1. Allen A, Bell A, Mantle M, Pearson JP. The structure and physiology of gastrointestinal mucus. Adv Exp Med Biol 144: 115-133, 1982
2. Andrianifahanana M, Moniaux N, Batra SK. Regulation of mucin expression: mechanistic aspects and implications for cancer and inflammatory diseases. Biochim Biophys Acta 1765: 189-222, 2006
3. Bachwich PR, Chensue SW, Larrick JW, Kunkel SL. Tumor necrosis factor stimulates interleukin-1 and prostaglandin E2 production in resting macrophages. Biochem Biophys Res Commun 136: 94-101, 1986
4. Baker SJ, Reddy EP. Modulation of life and death by the TNF receptor superfamily. Oncogene 17: 3261-3270, 1998
5. Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 336: 1066-1071, 1997
6. Buisine MP, Devisme L, Savidge TC, Gespach C, Gosselin B, Porchet N, Aubert JP. Mucin gene expression in human embryonic and fetal intestine. Gut 43: 519-524, 1998
7. Caplan MS, Hsueh W. Necrotizing enterocolitis: role of platelet activating factor, endotoxin, and tumor necrosis factor. J Pediatr 117: S47-51, 1990
8. Caplan MS, Sun XM, Hseuh W, Hageman JR. Role of platelet activating factor and tumor necrosis factor-alpha in neonatal necrotizing enterocolitis. J Pediatr 116: 960-964, 1990
9. Chang HY, Yang X. Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 64: 821-846, 2000
10. Chen G, Korfhagen TR, Xu Y, Kitzmiller J, Wert SE, Maeda Y, Gregorieff A, Clevers H, Whitsett JA. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J Clin Invest 119: 2914-2924, 2009
11. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, Dvorak K, Boitano SA, Dvorak B. Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. Am J Physiol Gastrointest Liver Physiol 291: G938-G949, 2006
12. Corfield AP, Carroll D, Myerscough N, Probert CS. Mucins in the gastrointestinal tract in health and disease. Front Biosci 6: D1321-D1357, 2001
13. Corredor J, Yan F, Shen CC, Tong W, John SK, Wilson G, Whitehead R, Polk DB. Tumor necrosis factor regulates intestinal epithelial cell migration by receptor-dependent mechanisms. Am J Physiol Cell Physiol 284: C953-C961, 2003
14. Fand SB, Thorell B. Spectrophotometry of the periodic acid-Schiff reaction with pituitary hormones in vitro and in histological sections. J Cell Biol 13: 239-247, 1962
15. Fitzgibbons SC, Ching Y, Yu D, Carpenter J, Kenny M, Weldon C, Lillehei C, Valim C, Horbar JD, Jaksic T. Mortality of necrotizing enterocolitis expressed by birth weight categories. J Pediatr Surg 44: 1072-1075; discussion 1075-1076, 2009
16. Forstner G. Signal transduction, packaging and secretion of mucins. Annu Rev Physiol 57: 585-605, 1995
17. Garcia MA, Yang N, Quinton PM. Normal mouse intestinal mucus release requires cystic fibrosis transmembrane regulator-dependent bicarbonate secretion. J Clin Invest 119: 2613-2622, 2009
18. Gendler SJ. MUC1, the renaissance molecule. J Mammary Gland Biol Neoplasia 6: 339-353, 2001
19. Gregorieff A, Stange DE, Kujala P, Begthel H, van den Born M, Korving J, Peters PJ, Clevers H. The ets-domain transcription factor Spdef promotes maturation of goblet and Paneth cells in the intestinal epithelium. Gastroenterology 137: 1333-1345; e1331-1333, 2009
20. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, Taupin D, Thornton DJ, Png CW, Crockford TL, Cornall RJ, Adams R, Kato M, Nelms KA, Hong NA, Florin TH, Goodnow CC, McGuckin MA. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5: e54, 2008
21. Hecht G. Innate mechanisms of epithelial host defense: spotlight on intestine. Am J Physiol Cell Physiol 277: C351-C358, 1999
22. Heller RA, Kronke M. Tumor necrosis factor receptor-mediated signaling pathways. J Cell Biol 126: 5-9, 1994
23. Henning SJ. Ontogeny of enzymes in the small intestine. Annu Rev Physiol 47: 231-245, 1985
24. Holman RC, Stoll BJ, Clarke MJ, Glass RI. The epidemiology of necrotizing enterocolitis infant mortality in the United States. Am J Public Health 87: 2026-2031, 1997
25. Hunter CJ, Upperman JS, Ford HR, Camerini V. Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 63: 117-123, 2008
26. Ikeda H, Sasaki M, Ohira S, Ishikawa A, Sato Y, Harada K, Zen Y, Nakanuma Y. Tumor necrosis factor-alpha induces the aberrant expression of mucus core protein-2 in non-neoplastic biliary epithelial cells via the upregulation of CDX2 in chronic cholangitis. Hepatol Res 38: 1006-1017, 2008
27. Jensen J, Pedersen EE, Galante P, Hald J, Heller RS, Ishibashi M, Kageyama R, Guillemot F, Serup P, Madsen OD. Control of endodermal endocrine development by Hes-1. Nat Genet 24: 36-44, 2000
28. Jilling T, Simon D, Lu J, Meng FJ, Li D, Schy R, Thomson RB, Soliman A, Arditi M, Caplan MS. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 177: 3273-3282, 2006
29. Kaiser GC, Polk DB. Tumor necrosis factor alpha regulates proliferation in a mouse intestinal cell line. Gastroenterology 112: 1231-1240, 1997
30. Kaiser GC, Yan F, Polk DB. Conversion of TNF alpha from antiproliferative to proliferative ligand in mouse intestinal epithelial cells by regulating mitogen-activated protein kinase. Exp Cell Res 249: 349-358, 1999
31. Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol 9: 240-246, 1997
32. Kirkeby S, Moe D, Bog-Hansen T, Garbarsch C, Matthiessen ME. Quantitative PAS assay of some carbohydrate compounds and detergents. J Biochem Biophys Methods 24: 225-238, 1992
33. Kobata R, Tsukahara H, Ohshima Y, Ohta N, Tokuriki S, Tamura S, Mayumi M. High levels of growth factors in human breast milk. Early Hum Dev 84: 67-69, 2008
34. Levine SJ, Larivee P, Logun C, Angus CW, Ognibene FP, Shelhamer JH. Tumor necrosis factor-alpha induces mucin hypersecretion and MUC-2 gene expression by human airway epithelial cells. Am J Respir Cell Mol Biol 12: 196-204, 1995
35. Lin PW, Nasr TR, Stoll BJ. Necrotizing enterocolitis: recent scientific advances in pathophysiology and prevention. Semin Perinatol 32: 70-82, 2008
36. Loetscher H, Schlaeger EJ, Lahm HW, Pan YC, Lesslauer W, Brockhaus M. Purification and partial amino acid sequence analysis of two distinct tumor necrosis factor receptors from HL60 cells. J Biol Chem 265: 20131-20138, 1990
37. Lotz M, Gutle D, Walther S, Menard S, Bogdan C, Hornef MW. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med 203: 973-984, 2006
38. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM. TNF-_-induced increase in intestinal epithelial tight junction permeability requires NF-_B activation. Am J Physiol Gastrointest Liver Physiol 286: G367-G376, 2004
39. McElroy SJ, Frey MR, Yan F, Edelblum KL, Goettel JA, John S, Polk DB. Tumor necrosis factor inhibits ligand-stimulated EGF receptor acti vation through a TNF receptor 1-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 295: G285-G293, 2008
40. McKay DM, Singh PK. Superantigen activation of immune cells evokes epithelial (T84) transport and barrier abnormalities via IFN-gamma and TNF alpha: inhibition of increased permeability, but not diminished secretory responses by TGF-beta2. J Immunol 159: 2382-2390, 1997
41. Mullin JM, Snock KV. Effect of tumor necrosis factor on epithelial tight junctions and transepithelial permeability. Cancer Res 50: 2172-2176, 1990
42. Neu J. Necrotizing enterocolitis: the search for a unifying pathogenic theory leading to prevention. Pediatr Clin North Am 43: 409-432, 1996
43. Noah TK, Kazanjian A, Whitsett J, Shroyer NF. SAM pointed domain ETS factor (SPDEF) regulates terminal differentiation and maturation of intestinal goblet cells. Exp Cell Res 316: 452-465, 2010
44. Oettgen P, Finger E, Sun Z, Akbarali Y, Thamrongsak U, Boltax J, Grall F, Dube A, Weiss A, Brown L, Quinn G, Kas K, Endress G, Kunsch C, Libermann TA. PDEF, a novel prostate epithelium-specific ets transcription factor, interacts with the androgen receptor and activates prostate-specific antigen gene expression. J Biol Chem 275: 1216-1225, 2000
45. Okamoto R, Tsuchiya K, Nemoto Y, Akiyama J, Nakamura T, Kanai T, Watanabe M. Requirement of Notch activation during regeneration of the intestinal epithelia. Am J Physiol Gastrointest Liver Physiol 296: G23-G35, 2009
46. Park KS, Korfhagen TR, Bruno MD, Kitzmiller JA, Wan H, Wert SE, Khurana Hershey GK, Chen G, Whitsett JA. SPDEF regulates goblet cell hyperplasia in the airway epithelium. J Clin Invest 117: 978-988, 2007
47. Perrais M, Pigny P, Copin MC, Aubert JP, Van Seuningen I. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signalregulated kinase cascade and Sp1. J Biol Chem 277: 32258-32267, 2002
48. Sanderson IR, Walker A, NetLibrary Inc. Development of the Gastrointestinal Tract. London, UK: B C Decker, 1999, p. xii and 324
49. Shekels LL, Ho SB. Characterization of the mouse Muc3 membrane bound intestinal mucin 5= coding and promoter regions: regulation by inflammatory cytokines. Biochim Biophys Acta 1627: 90-100, 2003
50. Sherman MP, Bennett SH, Hwang FF, Sherman J, Bevins CL. Paneth cells and antibacterial host defense in neonatal small intestine. Infect Immun 73: 6143-6146, 2005
51. Shub MD, Pang KY, Swann DA, Walker WA. Age-related changes in chemical composition and physical properties of mucus glycoproteins from rat small intestine. Biochem J 215: 405-411, 1983
52. Takeyama K, Dabbagh K, Lee HM, Agusti C, Lausier JA, Ueki IF, Grattan KM, Nadel JA. Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci USA 96: 3081-3086, 1999
53. Williams SJ, Munster DJ, Quin RJ, Gotley DC, McGuckin MA. The MUC3 gene encodes a transmembrane mucin and is alternatively spliced. Biochem Biophys Res Commun 261: 83-89, 1999
54. Yamamoto H, Bai YQ, Yuasa Y. Homeodomain protein CDX2 regulates goblet-specific MUC2 gene expression. Biochem Biophys Res Commun 300: 813-818, 2003.