Reduced NHE3-mediated Na+ absorption increases survival and decreases the incidence of intestinal obstructions in cystic fibrosis mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 296, Issue 4, 2009, Pages

  Bradford, Emily M ^a   Sartor, Maureen A ^a   Gawenis, Lara R ^b   Clarke, Lane L ^c   Shull, Gary E ^a  

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

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Cytochrome P 450; Distal intestinal obstructive syndrome; Glutathione transferase; Meconium ileus; Slc9a3

Indexed keywords

GLUTATHIONE; RNA; SODIUM PROTON EXCHANGE PROTEIN 3; TRANSMEMBRANE CONDUCTANCE REGULATOR; SODIUM; SODIUM PROTON EXCHANGE PROTEIN; SODIUM-HYDROGEN EXCHANGER 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL GRANULE; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; CRYPT CELL; CYSTIC FIBROSIS; DIARRHEA; DOWN REGULATION; ENERGY METABOLISM; FEMALE; GENE EXPRESSION; GENOTYPE; GLUTATHIONE METABOLISM; GOBLET CELL; INTESTINE OBSTRUCTION; JEJUNUM; MALE; MEMBRANE FLUIDITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; PROGENY; SMALL INTESTINE; SODIUM ABSORPTION; SURVIVAL RATE; XENOBIOTIC METABOLISM; ANIMAL; CHEMISTRY; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORTALITY; MUTATION; PATHOLOGY; PHYSIOLOGY; STOMACH JUICE;

ANIMALS; CYSTIC FIBROSIS; DIARRHEA; GASTROINTESTINAL CONTENTS; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENOTYPE; INTESTINAL OBSTRUCTION; MICE; MUTATION; SODIUM; SODIUM-HYDROGEN ANTIPORTER;

EID: 67149139397     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90520.2008     Document Type: Article

References (65)

1. + exchangers, NHE-1 and NHE-3, of rat intestine. Expression and localization. J Clin Invest 93: 106-113, 1994.
2. Boucher RC. Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 13: 231-240, 2007.
3. Bruzzese E, Raia V, Gaudiello G, Polito G, Buccigrossi V, Formicola V, Guarino A. Intestinal inflammation is a frequent feature of cystic fibrosis and is reduced by probiotic administration. Aliment Pharmacol Ther 20: 813-819, 2004.
4. Childers M, Eckel G, Himmel A, Caldwell J. A new model of cystic fibrosis pathology: lack of transport of glutathione and its thiocyanate conjugates. Med Hypotheses 68: 101-112, 2007.
5. Clarke LL, Gawenis LR, Bradford EM, Judd LM, Boyle KT, Simpson JE, Shull GE, Tanabe H, Ouellette AJ, Franklin CL, Walker NM. Abnormal Paneth cell granule dissolution and compromised resistance to bacterial colonization in the intestine of CF mice. Am J Physiol Gastrointest Liver Physiol 286: G1050-G1058, 2004.
6. Clarke LL, Gawenis LR, Franklin CL, Harline MC. Increased survival of CFTR knockout mice with an oral osmotic laxative. Lab Anim Sci 46: 612-618, 1996.
7. Dauletbaev N, Viel K, Buhl R, Wagner TO, Bargon J. Glutathione and glutathione peroxidase in sputum samples of adult patients with cystic fibrosis. J Cyst Fibros 3: 119-124, 2004.
8. Day BJ, van Heeckeren AM, Min E, Velsor LW. Role for cystic fibrosis transmembrane conductance regulator protein in a glutathione response to bronchopulmonary pseudomonas infection. Infect Immun 72: 2045-2051, 2004.
9. 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 293: G577-G584, 2007.
10. 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 42: 46-52, 2006.
11. Donaldson SH, Bennett WD, Zeman KL, Knowles MR, Tarran R, Boucher RC. Mucus clearance and lung function in cystic fibrosis with hypertonic saline. N Engl J Med 354: 241-250, 2006.
12. Dray X, Bienvenu T, Desmazes-Dufeu N, Dusser D, Marteau P, Hubert D. Distal intestinal obstruction syndrome in adults with cystic fibrosis. Clin Gastroenterol Hepatol 2: 498-503, 2004.
13. Durie PR, Kent G, Phillips MJ, Ackerley CA. Characteristic multiorgan pathology of cystic fibrosis in a long-living cystic fibrosis transmembrane regulator knockout murine model. Am J Pathol 164: 1481-1493, 2004.
14. Eckman EA, Cotton CU, Kube DM, Davis PB. Dietary changes improve survival of CFTR S489X homozygous mutant mouse. Am J Physiol Lung Cell Mol Physiol 269: L625-L630, 1995.
15. Elkins MR, Robinson M, Rose BR, Harbour C, Moriarty CP, Marks GB, Belousova EG, Xuan W, Bye PT. A controlled trial of long-term inhaled hypertonic saline in patients with cystic fibrosis. N Engl J Med 354: 229-240, 2006.
16. Fahy JV. Remodeling of the airway epithelium in asthma. Am J Respir Crit Care Med 164: S46-S51, 2001.
17. Field M, Rao MC, Chang EB. Intestinal electrolyte transport and diarrheal disease (1). N Engl J Med 321: 800-806, 1989.
18. Gallagher AM, Gottlieb RA. Proliferation, not apoptosis, alters epithelial cell migration in small intestine of CFTR null mice. Am J Physiol Gastrointest Liver Physiol 281: G681-G687, 2001.
19. Gao L, Broughman JR, Iwamoto T, Tomich JM, Venglarik CJ, Forman HJ. Synthetic chloride channel restores glutathione secretion in cystic fibrosis airway epithelia. Am J Physiol Lung Cell Mol Physiol 281: L24-L30, 2001.
20. Gao L, Kim KJ, Yankaskas JR, Forman HJ. Abnormal glutathione transport in cystic fibrosis airway epithelia. Am J Physiol Lung Cell Mol Physiol 277: L113-L118, 1999.
21. Gawenis LR, Hut H, Bot AG, Shull GE, de Jonge HR, Stien X, Miller ML, Clarke LL. Electroneutral sodium absorption and electrogenic anion secretion across murine small intestine are regulated in parallel. Am J Physiol Gastrointest Liver Physiol 287: G1140-G1149, 2004.
22. Gawenis LR, Stien X, Shull GE, Schultheis PJ, Woo AL, Walker NM, Clarke LL. Intestinal NaCl transport in NHE2 and NHE3 knockout mice. Am J Physiol Gastrointest Liver Physiol 282: G776-G784, 2002.
23. Gentzsch M, Choudhury A, Chang XB, Pagano RE, Riordan JR. Misassembled mutant DeltaF508 CFTR in the distal secretory pathway alters cellular lipid trafficking. J Cell Sci 120: 447-455, 2007.
24. Grubb BR, Gabriel SE. Intestinal physiology and pathology in gene-targeted mouse models of cystic fibrosis. Am J Physiol Gastrointest Liver Physiol 273: G258-G266, 1997.
25. + exchanger, by Clostridium difficile toxin B. J Gen Physiol 123: 491-504, 2004.
26. Hirsh AJ, Zhang J, Zamurs A, Fleegle J, Thelin WR, Caldwell RA, Sabater JR, Abraham WM, Donowitz M, Cha B, Johnson KB, St George JA, Johnson MR, Boucher RC. Pharmacological properties of N-(3,5-diamino-6-chloropyrazine- 2-carbonyl)-N-4-[4-(2,3-dihydroxypropoxy) phenyl]butyl-guanidine methanesulfonate (552-02), a novel epithelial sodium channel blocker with potential clinical efficacy for cystic fibrosis lung disease. J Pharmacol Exp Ther 325: 77-88, 2008.
27. Hoogerwerf WA, Tsao SC, Devuyst O, Levine SA, Yun CH, Yip JW, Cohen ME, Wilson PD, Lazenby AJ, Tse CM, Donowitz M. NHE2 and NHE3 are human and rabbit intestinal brush-border proteins. Am J Physiol Gastrointest Liver Physiol 270: G29-G41, 1996.
28. Hudson VM. New insights into the pathogenesis of cystic fibrosis: pivotal role of glutathione system dysfunction and implications for therapy. Treat Respir Med 3: 353-363, 2004.
29. Innes AL, Woodruff PG, Ferrando RE, Donnelly S, Dolganov GM, Lazarus SC, Fahy JV. Epithelial mucin stores are increased in the large airways of smokers with airflow obstruction. Chest 130: 1102-1108, 2006.
30. Kariya C, Leitner H, Min E, van Heeckeren C, van Heeckeren A, Day BJ. A role for CFTR in the elevation of glutathione levels in the lung by oral glutathione administration. Am J Physiol Lung Cell Mol Physiol 292: L1590-L1597, 2007.
31. Kato M. Intestinal first-pass metabolism of CYP3A4 substrates. Drug Metab Pharmacokinet 23: 87-94, 2008.
32. Kearns GL, Crom WR, Karlson KH Jr, Mallory GB Jr, Evans WE. Hepatic drug clearance in patients with mild cystic fibrosis. Clin Pharmacol Ther 59: 529-540, 1996.
33. Kogan I, Ramjeesingh M, Li C, Kidd JF, Wang Y, Leslie EM, Cole SP, Bear CE. CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J 22: 1981-1989, 2003.
34. + exchanger has no apparent effect on diarrheal state of Nhe3-deficient mice. Am J Physiol Gastrointest Liver Physiol 281: G1385-G1396, 2001.
35. - salvage across the luminal membrane of the main pancreatic duct. J Clin Invest 105: 1651-1658, 2000.
36. Linsdell P, Hanrahan JW. Glutathione permeability of CFTR. Am J Physiol Cell Physiol 275: C323-C326, 1998.
37. Lorenz JN, Schultheis PJ, Traynor T, Shull GE, Schnermann J. Micropuncture analysis of single-nephron function in Nhe3-deficient mice. Am J Physiol Renal Physiol 277: F447-F453, 1999.
38. + exchange in canine ileal absorption. Dig Dis Sci 41: 651-659, 1996.
39. Mascarenhas MR. Treatment of gastrointestinal problems in cystic fi-brosis. Curr Treat Options Gastroenterol 6: 427-441, 2003.
40. Mennone A, Biemesderfer D, Negoianu D, Yang CL, Abbiati T, Schultheis PJ, Shull GE, Aronson PS, Boyer JL. Role of sodium/hydrogen exchanger isoform NHE3 in fluid secretion and absorption in mouse and rat cholangiocytes. Am J Physiol Gastrointest Liver Physiol 280: G247-G254, 2001.
41. Muller T, Wijmenga C, Phillips AD, Janecke A, Houwen RH, Fischer H, Ellemunter H, Fruhwirth M, Offner F, Hofer S, Muller W, Booth IW, Heinz-Erian P. Congenital sodium diarrhea is an autosomal recessive disorder of sodium/proton exchange but unrelated to known candidate genes. Gastroenterology 119: 1506-1513, 2000.
42. Norkina O, Kaur S, Ziemer D, De Lisle RC. Inflammation of the cystic fibrosis mouse small intestine. Am J Physiol Gastrointest Liver Physiol 286: G1032-G1041, 2004.
43. Paine MF, Oberlies NH. Clinical relevance of the small intestine as an organ of drug elimination: drug-fruit juice interactions. Expert Opin Drug Metab Toxicol 3: 67-80, 2007.
44. Parker AC, Pritchard P, Preston T, Smyth RL, Choonara I. Enhanced drug metabolism in young children with cystic fibrosis. Arch Dis Child 77: 239-241, 1997.
45. Rey E, Treluyer JM, Pons G. Drug disposition in cystic fibrosis. Clin Pharmacokinet 35: 313-329, 1998.
46. Robert A, Nezamis JE, Lancaster C, Hanchar AJ, Klepper MS. Enteropooling assay: a test for diarrhea produced by prostaglandins. Prostaglandins 11: 809-828, 1976.
47. Roum JH, Buhl R, McElvaney NG, Borok Z, Crystal RG. Systemic deficiency of glutathione in cystic fibrosis. J Appl Physiol 75: 2419-2424, 1993.
48. Sartor MA, Tomlinson CR, Wesselkamper SC, Sivaganesan S, Leikauf GD, Medvedovic M. Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics 7: 538, 2006.
49. Schmidt-Wittig U, Enss ML, Coenen M, Gartner K, Hedrich HJ. Response of rat colonic mucosa to a high fiber diet. Ann Nutr Metab 40: 343-350, 1996.
50. + exchanger isoform 2 gene causes reduced viability of gastric parietal cells and loss of net acid secretion. J Clin Invest 101: 1243-1253, 1998.
51. + exchanger. Nat Genet 19: 282-285, 1998.
52. Seidler U, Rottinghaus I, Hillesheim J, Chen M, Riederer B, Krabbenhoft A, Engelhardt R, Wiemann M, Wang Z, Barone S, Manns MP, Soleimani M. Sodium and chloride absorptive defects in the small intestine in Slc26a6 null mice. Pflügers Arch 455: 757-766, 2008.
53. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3, 2004.
54. Snouwaert JN, Brigman KK, Latour AM, Malouf NN, Boucher RC, Smithies O, Koller BH. An animal model for cystic fibrosis made by gene targeting. Science 257: 1083-1088, 1992.
55. + restriction. Am J Physiol Gastrointest Liver Physiol 281: G1369-G1377, 2001.
56. Vaandrager AB. Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C. Mol Cell Biochem 230: 73-83, 2002.
57. Velsor LW, van Heeckeren A, Day BJ. Antioxidant imbalance in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am J Physiol Lung Cell Mol Physiol 281: L31-L38, 2001.
58. Walker NM, Simpson JE, Levitt RC, Boyle KT, Clarke LL. Talniflumate increases survival in a cystic fibrosis mouse model of distal intestinal obstructive syndrome. J Pharmacol Exp Ther 317: 275-283, 2006.
59. Wang T, Yang CL, Abbiati T, Schultheis PJ, Shull GE, Giebisch G, Aronson PS. Mechanism of proximal tubule bicarbonate absorption in NHE3 null mice. Am J Physiol Renal Physiol 277: F298-F302, 1999.
60. Wang T, Yang CL, Abbiati T, Shull GE, Giebisch G, Aronson PS. Essential role of NHE3 in facilitating formate-dependent NaCl absorption in the proximal tubule. Am J Physiol Renal Physiol 281: F288-F292, 2001.
61. White NM, Jiang D, Burgess JD, Bederman IR, Previs SF, Kelley TJ. Altered cholesterol homeostasis in cultured and in vivo models of cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 292: L476-L486, 2007.
62. + exchanger knockout model of congenital diarrhea. J Biol Chem 277: 49036-49046, 2002.
63. Woo AL, Noonan WT, Schultheis PJ, Neumann JC, Manning PA, Lorenz JN, Shull GE. Renal function in Nhe3-deficient mice with transgenic rescue of small intestinal absorptive defect. Am J Physiol Renal Physiol 284: F1190-F1198, 2003.
64. -/- knockout mouse. Novel model system for a severely compromised oxidative stress response. J Biol Chem 277: 49446-49452, 2002.
65. Zhou L, Dey CR, Wert SE, DuVall MD, Frizzell RA, Whitsett JA. Correction of lethal intestinal defect in a mouse model of cystic fibrosis by human CFTR. Science 266: 1705-1708, 1994.