Impaired mucosal barrier function in the small intestine of the cystic fibrosis mouse

Journal of Pediatric Gastroenterology and Nutrition

Volumn 53, Issue 4, 2011, Pages 371-379

  De Lisle, Robert C ^a   Mueller, Racquel ^a   Boyd, Megan ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Akp3; Akp6; antibiotics; bacterial overgrowth; intestinal alkaline phosphatase; laxative; permeability

Indexed keywords

ALBUMIN; ALKALINE PHOSPHATASE; ALKALINE PHOSPHATASE INTESTINE ISOENZYME; CIPROFLOXACIN; COLYTE; DEXTRAN; MESSENGER RNA; METRONIDAZOLE; RHODAMINE; UNCLASSIFIED DRUG;

ALBUMIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIAL OVERGROWTH; BLOOD LEVEL; CONTROLLED STUDY; CYSTIC FIBROSIS; ENTEROPATHY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION REGULATION; GROWTH INHIBITION; INTESTINE MUCOSA BARRIER FUNCTION IMPAIRMENT; INTESTINE MUCOSA PERMEABILITY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE;

ADMINISTRATION, ORAL; ALKALINE PHOSPHATASE; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL INFECTIONS; BACTERIAL LOAD; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DISEASE MODELS, ANIMAL; INTESTINAL MUCOSA; INTESTINE, SMALL; LAXATIVES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); MURINAE; MUS;

EID: 80053622156     PISSN: 02772116     EISSN: 15364801     Source Type: Journal    
DOI: 10.1097/MPG.0b013e318219c397     Document Type: Article

References (56)

1. Barraclough M, Taylor CJ. Twenty-four hour ambulatory gastric and duodenal pH profiles in cystic fibrosis: Effect of duodenal hyperacidity on pancreatic enzyme function and fat absorption. J Pediatr Gastroenterol Nutr 1996;23:45-50. (Pubitemid 26231032)
2. Quinton PM. Cystic fibrosis: Impaired bicarbonate secretion and mucoviscidosis. Lancet 2008;372:415-7.
3. Boucher RC. Airway surface dehydration in cystic fibrosis: Pathogenesis and therapy. Annu Rev Med 2007;58:157-70. (Pubitemid 46706507)
4. Houwen RH, van der Doef HP, Sermet I, et al. Defining DIOS and constipation in cystic fibrosis with a multicentre study on the incidence, characteristics, and treatment of DIOS. J Pediatr Gastroenterol Nutr 2010;50:38-42.
5. Courtney JM, Bradley J, McCaughan J, et al. Predictors of mortality in adults with cystic fibrosis. Pediatr Pulmonol 2007;42:525-32. (Pubitemid 46870384)
6. Milla CE. Association of nutritional status and pulmonary function in children with cystic fibrosis. Curr Opin Pulm Med 2004;10:505-9. (Pubitemid 39441445)
7. Stallings VA, Stark LJ, Robinson KA, et al. Evidence-based practice recommendations for nutrition-related management of children and adults with cystic fibrosis and pancreatic insufficiency: Results of a systematic review. J Am Diet Assoc 2008;108:832-9. (Pubitemid 351602057)
8. Baker SS, Borowitz D, Duffy L, et al. Pancreatic enzyme therapy and clinical outcomes in patients with cystic fibrosis. J Pediatr 2005;146:189-93. (Pubitemid 40202806)
9. Borowitz D, Durie PR, Clarke LL, et al. Gastrointestinal outcomes and confounders in cystic fibrosis. J Pediatr Gastroenterol Nutr 2005; 41:273-85. (Pubitemid 41285817)
10. Bijvelds MJ, Bronsveld I, Havinga R, et al. Fat absorption in cystic fibrosis mice is impeded by defective lipolysis and postlipolytic events. Am J Physiol Gastrointest Liver Physiol 2005; 288:G646-53. (Pubitemid 40388175)
11. De Lisle RC, Isom KS, Ziemer D, et al. Changes in the exocrine pancreas secondary to altered small intestinal function in the CF mouse. Am J Physiol Gastrointest Liver Physiol 2001; 281:G899-906.
12. Grubb BR, Boucher RC. Pathophysiology of gene-targeted mouse models for cystic fibrosis. Physiol Rev 1999;79:S193-214. (Pubitemid 29058915)
13. Werlin SL, uri-Silbiger I, Kerem E, et al. Evidence of intestinal inflammation in patients with cystic fibrosis. J Pediatr Gastroenterol Nutr 2010;51:304-8.
14. Raia V, Maiuri L, De Ritis G, et al. Evidence of chronic inflammation in morphologically normal small intestine of cystic fibrosis patients. Pediatr Res 2000;47:344-50. (Pubitemid 30127040)
15. Hallberg K, Grzegorczyk A, Larson G, et al. Intestinal permeability in cystic fibrosis in relation to genotype. J Pediatr Gastroenterol Nutr 1997;25:290-5. (Pubitemid 27375419)
16. Norkina O, Burnett TG, De Lisle RC. Bacterial overgrowth in the cystic fibrosis transmembrane conductance regulator null mouse small intestine. Infect Immun 2004;72:6040-9. (Pubitemid 39303719)
17. Canale-Zambrano JC, Auger ML, Haston CK. Toll-like receptor-4 genotype influences the survival of cystic fibrosis mice. Am J Physiol Gastrointest Liver Physiol 2010;299:G381-90.
18. Clarke LL, Gawenis LR, Bradford EM, et al. Abnormal paneth cell granule dissolution and compromised resistance to bacterial colonization in the intestine of CF mice. Am J Physiol Gastrointest Liver Physiol 2004;286:G1050-8. (Pubitemid 38715669)
19. Lisowska A, Wojtowicz J, Walkowiak J. Small intestine bacterial overgrowth is frequent in cystic fibrosis: Combined hydrogen and methane measurements are required for its detection. Acta Biochim Pol 2009;56:631-4.
20. Fridge JL, Conrad C, Gerson L, et al. Risk factors for small bowel bacterial overgrowth in cystic fibrosis. J Pediatr Gastroenterol Nutr 2007;44:212-8. (Pubitemid 46175075)
21. Lewindon PJ, Robb TA, Moore DJ, et al. Bowel dysfunction in cystic fibrosis: Importance of breath testing. J Paediatr Child Health 1998; 34:79-82. (Pubitemid 28158512)
22. O'Brien S, Mulcahy H, Fenlon H, et al. Intestinal bile acid malabsorption in cystic fibrosis. Gut 1993;34:1137-41. (Pubitemid 23245371)
23. Reims A, Strandvik B, Sjovall H. Epithelial electrical resistance as a measure of permeability changes in pediatric duodenal biopsies. J Pediatr Gastroenterol Nutr 2006;43:619-23. (Pubitemid 44863688)
24. Dalzell AM, Freestone NS, Billington D, et al. Small intestinal permeability and orocaecal transit time in cystic fibrosis. Arch Dis Child 1990;65:585-8. (Pubitemid 20193632)
25. Escobar H, Perdomo M, Vasconez F, et al. Intestinal permeability to 51Cr-EDTA and orocecal transit time in cystic fibrosis. J Pediatr Gastroenterol Nutr 1992;14:204-7.
26. Hendriks HJ, van Kreel B, Forget PP. Effects of therapy with lansoprazole on intestinal permeability and inflammation in young cystic fibrosis patients. J Pediatr Gastroenterol Nutr 2001;33:260-5. (Pubitemid 32947326)
27. Purohit V, Bode JC, Bode C, et al. Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: Summary of a symposium. Alcohol 2008;42:349-61.
28. Poelstra K, Bakker WW, Klok PA, et al. Dephosphorylation of endotoxin by alkaline phosphatase in vivo. Am J Pathol 1997; 151:1163-9. (Pubitemid 27424326)
29. Van Biervliet S, Eggermont E, Carchon H, et al. Small intestinal brush border enzymes in cystic fibrosis. Acta Gastroenterol Belg 1999;62:267-71. (Pubitemid 29472854)
30. Van Biervliet S, Eggermont E, Marien P, et al. Combined impact of mucosal damage and of cystic fibrosis on the small intestinal brush border enzyme activities. Acta Clin Belg 2003;58:220-4. (Pubitemid 37339143)
31. De Lisle RC, Roach EA, Norkina O. Eradication of small intestinal bacterial overgrowth in the cystic fibrosis mouse reduces mucus accumulation. J Pediatr Gastroenterol Nutr 2006;42:46-52. (Pubitemid 43061009)
32. Jeffrey I, Durrans D, Wells M, et al. The pathology of meconium ileus equivalent. J Clin Pathol 1983;36:1292-7. (Pubitemid 14205414)
33. Norkina O, Kaur S, Ziemer D, et al. Inflammation of the cystic fibrosis mouse small intestine. Am J Physiol Gastrointest Liver Physiol 2004;286:G1032-41. (Pubitemid 38715667)
34. De Lisle RC, Roach E, Jansson K. Effects of laxative and N-acetylcysteine on mucus accumulation, bacterial load, transit, and inflammation in the cystic fibrosis mouse small intestine. Am J Physiol Gastrointest Liver Physiol 2007;293:G577-84. (Pubitemid 47435389)
35. Bol-Schoenmakers M, Fiechter D, Raaben W, et al. Intestinal alkaline phosphatase contributes to the reduction of severe intestinal epithelial damage. Eur J Pharmacol 2010;633:71-7.
36. Lukas M, Drastich P, Konecny M, et al. Exogenous alkaline phosphatase for the treatment of patients with moderate to severe ulcerative colitis. Inflamm Bowel Dis 2010;16:1180-6.
37. Ramasamy S, Nguyen DD, Eston MA et al. Intestinal alkaline phosphatase has beneficial effects in mouse models of chronic colitis. Inflamm Bowel Dis 2010;17:532-42.
38. Whitehouse JS, Riggle KM, Purpi DP, et al. The protective role of intestinal alkaline phosphatase in necrotizing enterocolitis. J Surg Res 2010;163:79-85.
39. Campbell EL, Macmanus CF, Kominsky DJ et al. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. Proc Natl Acad Sci U S A 2010;107:14298-303.
40. Clarke LL, Gawenis LR, Franklin CL, et al. Increased survival of CFTR knockout mice with an oral osmotic laxative. Lab Anim Sci 1996;46:612-8.
41. Bowers GN Jr, McComb RB. A continuous spectrophotometric method for measuring the activity of serum alkaline phosphatase. Clin Chem 1966;12:70-89.
42. Cesarone CF, Bolognesi C, Santi L. Improved microfluorometric DNA determination in biological material using 33 258 Hoechst. Anal Biochem 1979;100:188-97. (Pubitemid 10157650)
43. Narisawa S, Hoylaerts MF, Doctor KS, et al. A novel phosphatase upregulated in Akp3 knockout mice. Am J Physiol Gastrointest Liver Physiol 2007;293:G1068-77. (Pubitemid 350106561)
44. Shephard MD, Peake MJ, Walmsley RN. Quantitative method for determining serum alkaline phosphatase isoenzyme activity. II. Development and clinical application of method for measuring four serum alkaline phosphatase isoenzymes. J Clin Pathol 1986; 39:1031-8. (Pubitemid 16015992)
45. Malo MS, Alam SN, Mostafa G, et al. Intestinal alkaline phosphatase preserves the normal homeostasis of gut microbiota. Gut 2010; 59:1476-84.
46. Lalles JP. Intestinal alkaline phosphatase: Multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 2010;68:323-32.
47. Malo MS, Biswas S, Abedrapo MA, et al. The pro-inflammatory cytokines, IL-1beta and TNF-alpha, inhibit intestinal alkaline phosphatase gene expression. DNA Cell Biol 2006;25:684-95. (Pubitemid 46052614)
48. Hodin RA, Chamberlain SM, Meng S. Pattern of rat intestinal brush-border enzyme gene expression changes with epithelial growth state. Am J Physiol 1995;269:C385-91.
49. Goldberg RF, Austen WG Jr, Zhang X, et al. Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc Natl Acad Sci U S A 2008;105:3551-6. (Pubitemid 351723590)
50. Lackeyram D, Yang C, Archbold T, et al. Early weaning reduces small intestinal alkaline phosphatase expression in pigs. J Nutr 2010; 140:461-8.
51. Akiba Y, Mizumori M, Guth PH, et al. Duodenal brush border intestinal alkaline phosphatase activity affects bicarbonate secretion in rats. Am J Physiol Gastrointest Liver Physiol 2007;293:G1223-3.
52. Ishii KJ, Akira S. Potential link between the immune system and metabolism of nucleic acids. Curr Opin Immunol 2008; 20:524-9.
53. Nakano T, Inoue I, Koyama I, et al. Disruption of the murine intestinal alkaline phosphatase gene Akp3 impairs lipid transcytosis and induces visceral fat accumulation and hepatic steatosis. Am J Physiol Gastrointest Liver Physiol 2007;292:G1439-4.
54. Bjarnason I, Takeuchi K, Bjarnason A, et al. The G.U.T. of gut. Scand J Gastroenterol 2004;39:807-15. (Pubitemid 39215450)
55. Riordan SM, McIver CJ, Thomas DH, et al. Luminal bacteria and small-intestinal permeability. Scand J Gastroenterol 1997; 32:556-63. (Pubitemid 27314265)
56. Koyama I, Matsunaga T, Harada T, et al. Alkaline phosphatases reduce toxicity of lipopolysaccharides in vivo and in vitro through dephosphorylation. Clin Biochem 2002;35:455-61. (Pubitemid 35284542)