Active transport of bile acids decreases mucin 2 in neonatal ileum: Implications for development of necrotizing enterocolitis

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Martin, Nina A ^a   Patrick, Sarah K Mount ^a   Estrada, Teresa E ^a   Frisk, Harrison A ^a   Rogan, Daniel T ^a   Dvorak, Bohuslav ^a   Halpern, Melissa D ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; GROWTH FACTOR; MUCIN 2; PROTEIN INHIBITOR; SC 435; TREFOIL FACTOR 3; UNCLASSIFIED DRUG; COLESTYRAMINE;

ACTIVE TRANSPORT; AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE ACID METABOLISM; CONTROLLED STUDY; DRUG EFFECT; EX VIVO STUDY; EXPLANT; ILEUM; IN VIVO STUDY; MOUSE; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; PROTEIN FUNCTION; RAT; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; METABOLISM; MOUSE MUTANT; SPRAGUE DAWLEY RAT; TIME; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BILE ACIDS AND SALTS; BIOLOGICAL TRANSPORT; CHOLESTYRAMINE RESIN; ENTEROCOLITIS, NECROTIZING; GENE EXPRESSION REGULATION; ILEUM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUCIN-2; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 82655183571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027191     Document Type: Article

References (50)

1. Neu J, (1996) Necrotizing enterocolitis: the search for a unifying pathogenic theory leading to prevention. Pediatr Clin North Am 43: 409-432.
2. Lemons JA, Bauer CR, Oh W, Korones SB, Papile LA, et al. (2001) 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: E1.
3. Israel EJ, (1994) Neonatal necrotizing enterocolitis, a disease of the immature intestinal mucosal barrier. Acta Paediatr Suppl 396 pp. 27-32.
4. Schanler RJ, Hurst NM, Lau C, (1999) The use of human milk and breastfeeding in premature infants. Clin Perinatol 26: 379-398, vii.
5. Caplan MS, MacKendrick W, (1993) Necrotizing enterocolitis: a review of pathogenetic mechanisms and implications for prevention. Pediatr Pathol 13: 357-369.
6. Craven PA, Pfanstiel J, Saito R, DeRubertis FR, (1986) Relationship between loss of rat colonic surface epithelium induced by deoxycholate and initiation of the subsequent proliferative response. Cancer Res 46: 5754-5759.
7. Craven PA, DeRubertis FR, (1988) Role of activation of protein kinase C in the stimulation of colonic epithelial proliferation by unsaturated fatty acids. Gastroenterology 95: 676-685.
8. Milovic V, Teller IC, Faust D, Caspary WF, Stein J, (2002) Effects of deoxycholate on human colon cancer cells: apoptosis or proliferation. Eur J Clin Invest 32: 29-34.
9. Halpern MD, Dvorak B, (2008) Does Abnormal Bile Acid Metabolism Contribute to NEC? Semin Perinatol 32: 114-121.
10. Halpern MD, Holubec H, Saunders TA, Dvorak K, Clark JA, et al. (2006) Bile Acids Induce Ileal Damage During Experimental Necrotizing Enterocolitis. Gastroenterology 130: 359-372.
11. Halpern MD, Weitkamp JH, Mount Patrick SK, Dobrenen HJ, Khailova L, et al. (2010) Apical sodium-dependent bile acid transporter upregulation is associated with necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 299: G623-631.
12. Walker WA, (2002) Development of the intestinal mucosal barrier. J Pediatr Gastroenterol Nutr 34 (Suppl 1): S33-39.
13. Einerhand AW, Renes IB, Makkink MK, van der Sluis M, Buller HA, et al. (2002) Role of mucins in inflammatory bowel disease: important lessons from experimental models. Eur J Gastroenterol Hepatol 14: 757-765.
14. Hackam DJ, Upperman JS, Grishin A, Ford HR, (2005) Disordered enterocyte signaling and intestinal barrier dysfunction in the pathogenesis of necrotizing enterocolitis. Semin Pediatr Surg 14: 49-57.
15. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, et al. (2006) Intestinal barrier failure during experimental necrotizing enterocolitis: Protective effect of epidermal growth factor treatment. Am J Physiol Gastrointest Liver Physiol 291: G938-949.
16. Song S, Byrd JC, Koo JS, Bresalier RS, (2005) Bile acids induce MUC2 overexpression in human colon carcinoma cells. Cancer 103: 1606-1614.
17. Klinkspoor JH, Mok KS, Van Klinken BJ, Tytgat GN, Lee SP, et al. (1999) Mucin secretion by the human colon cell line LS174T is regulated by bile salts. Glycobiology 9: 13-19.
18. Shekels LL, Lyftogt CT, Ho SB, (1996) Bile acid-induced alterations of mucin production in differentiated human colon cancer cell lines. Int J Biochem Cell Biol 28: 193-201.
19. Wiedmann TS, Liang W, Herrington H, (2004) Interaction of bile salts with gastrointestinal mucins. Lipids 39: 51-58.
20. Yajima M, Hoshiba J, Terahara M, Yajima T, (2007) Diminishing thymic size and Delayed Appearance of Splenic CD4+ and CD8+ Cells in Artificially Reared Mouse Pups. Bioscience, Biotechnology and Biochemistry 71: 2420-2427.
21. Dvorak B, Halpern MD, Holubec H, Williams CS, McWilliam DL, et al. (2002) Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am J Physiol Gastrointest Liver Physiol 282: G156-164.
22. Halpern MD, Holubec H, Dominguez JA, Williams CS, Meza YG, et al. (2002) Up-regulation of IL-18 and IL-12 in the ileum of neonatal rats with necrotizing enterocolitis. Pediatr Res 51: 733-739.
23. Halpern MD, Dominguez JA, Dvorakova K, Holubec H, Williams CS, et al. (2003) Ileal cytokine dysregulation in experimental necrotizing enterocolitis is reduced by epidermal growth factor. J Pediatr Gastroenterol Nutr 36: 126-133.
24. Halpern MD, Khailova L, Molla-Hosseini D, Arganbright K, Reynolds C, et al. (2008) Decreased development of necrotizing enterocolitis in IL-18-deficient mice. Am J Physiol Gastrointest Liver Physiol 294: G20-26.
25. Halpern MD, Holubec H, Dominguez JA, Meza YG, Williams CS, et al. (2003) Hepatic inflammatory mediators contribute to intestinal damage in necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 284: G695-702.
26. Dvorak B, Halpern MD, Holubec H, Dvorakova K, Dominguez JA, et al. (2003) Maternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr Res 53: 426-433.
27. Dvorak B, Kolinska J, McWilliam DL, Williams CS, Higdon T, et al. (1998) The expression of epidermal growth factor and transforming growth factor-alpha mRNA in the small intestine of suckling rats: organ culture study. FEBS Lett 435: 119-124.
28. Kim YD, Kwon EJ, Park DW, Song SY, Yoon SK, et al. (2002) Interleukin-1beta induces MUC2 and MUC5AC synthesis through cyclooxygenase-2 in NCI-H292 cells. Mol Pharmacol 62: 1112-1118.
29. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, et al. (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5: e54.
30. Podolsky DK, (2000) Mechanisms of regulatory peptide action in the gastrointestinal tract: trefoil peptides. J Gastroenterol 35: 69-74.
31. Suemori S, Lynch-Devaney K, Podolsky DK, (1991) Identification and characterization of rat intestinal trefoil factor: tissue- and cell-specific member of the trefoil protein family. Proc Natl Acad Sci U S A 88: 11017-11021.
32. Taupin D, Podolsky DK, (2003) Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 4: 721-732.
33. Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, et al. (2009) Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 297: G940-949.
34. Bernstein H, Holubec H, Bernstein C, Ignatenko N, Gerner E, et al. (2006) Unique dietary-related mouse model of colitis. Inflamm Bowel Dis 12: 278-293.
35. Muhlbauer M, Allard B, Bosserhoff AK, Kiessling S, Herfarth H, et al. (2004) Differential effects of deoxycholic acid and taurodeoxycholic acid on NF-kappa B signal transduction and IL-8 gene expression in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 286: G1000-1008.
36. Jackson GD, Dai Y, Sewell WA, (2000) Bile mediates intestinal pathology in endotoxemia in rats. Infect Immun 68: 4714-4719.
37. Specian RD, Oliver MG, (1991) Functional biology of intestinal goblet cells. Am J Physiol 260: C183-193.
38. McElroy SJ, Prince LS, Weitkamp JH, Reese J, Slaughter JC, et al. (2011) Tumor Necrosis Factor Receptor 1-Dependent Depletion of Mucus in Immature Small Intestine: A Potential Role in Neonatal Necrotizing Enterocolitis. Am J Physiol Gastrointest Liver Physiol 301: G656-G666.
39. Shub MD, Pang KY, Swann DA, Walker WA, (1983) Age-related changes in chemical composition and physical properties of mucus glycoproteins from rat small intestine. Biochem J 215: 405-411.
40. Lee HY, Crawley S, Hokari R, Kwon S, Kim YS, (2010) Bile acid regulates MUC2 transcription in colon cancer cells via positive EGFR/PKC/Ras/ERK/CREB, PI3K/Akt/IkappaB/NF-kappaB and p38/MSK1/CREB pathways and negative JNK/c-Jun/AP-1 pathway. Int J Oncol 36: 941-953.
41. Wu J, Gong J, Geng J, Song Y, (2008) Deoxycholic acid induces the overexpression of intestinal mucin, MUC2, via NF-kB signaling pathway in human esophageal adenocarcinoma cells. BMC Cancer 8: 333.
42. Perrais M, Pigny P, Ducourouble MP, Petitprez D, Porchet N, et al. (2001) Characterization of human mucin gene MUC4 promoter: importance of growth factors and proinflammatory cytokines for its regulation in pancreatic cancer cells. J Biol Chem 276: 30923-30933.
43. Zhong SP, Ma WY, Quealy JA, Zhang Y, Dong Z, (2001) Organ-specific distribution of AP-1 in AP-1 luciferase transgenic mice during the maturation process. Am J Physiol Regul Integr Comp Physiol 280: R376-381.
44. De Plaen IG, Liu SX, Tian R, Neequaye I, May MJ, et al. (2007) Inhibition of nuclear factor-kappaB ameliorates bowel injury and prolongs survival in a neonatal rat model of necrotizing enterocolitis. Pediatr Res 61: 716-721.
45. Thompson JF, van den Berg M, Stokkers PC, (1994) Developmental regulation of epidermal growth factor receptor kinase in rat intestine. Gastroenterology 107: 1278-1287.
46. Hu Y, Jones C, Gellersen O, Williams VA, Watson TJ, et al. (2007) Pathogenesis of Barrett esophagus: deoxycholic acid up-regulates goblet-specific gene MUC2 in concert with CDX2 in human esophageal cells. Arch Surg 142: 540-544; discussion 544-545.
47. Coleman R, (1987) Bile salts and biliary lipids. Biochem Soc Trans 15 (Suppl): 68S-80S.
48. Coleman R, Lowe P, (1980) Membrane damage caused by bile salts [proceedings]. Biochem Soc Trans 8: 126-127.
49. Klinkspoor JH, Yoshida T, Lee SP, (1998) Bile salts stimulate mucin secretion by cultured dog gallbladder epithelial cells independent of their detergent effect. Biochem J 332 (Pt 1): 257-262.
50. Shneider BL, Setchell KD, Crossman MW, (1997) Fetal and neonatal expression of the apical sodium-dependent bile acid transporter in the rat ileum and kidney. Pediatr Res 42: 189-194.