Epithelial transport in inflammatory bowel diseases

Inflammatory Bowel Diseases

Volumn 20, Issue 6, 2014, Pages 1099-1109

  Ghishan, Fayez K ^a   Kiela, Pawel R ^a  

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

Author keywords

Colitis; Diarrhea; Electrolytes; Epithelial cells; Inflammation; Microbiome; Nutrients

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMINO ACID; ARGININE; BICARBONATE; CALCIUM; CARBOHYDRATE; CYTOKINE; ELECTROLYTE; EPITHELIAL SODIUM CHANNEL; GLUTAMINE; MAGNESIUM; PEPTIDE; PHOSPHORUS; SHORT CHAIN FATTY ACID; TRACE ELEMENT; ZINC;

CROHN DISEASE; DIARRHEA; ENTERITIS; EPITHELIUM; EPITHELIUM CELL; HUMAN; IMMUNE RESPONSE; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MACRONUTRIENT; MALABSORPTION; NONHUMAN; NUTRITIONAL DEFICIENCY; PRIORITY JOURNAL; PROTON SODIUM EXCHANGE; REGULATORY MECHANISM; REVIEW; ULCERATIVE COLITIS; COMPLICATION; INTESTINE MUCOSA; MALNUTRITION; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; COLITIS, ULCERATIVE; CROHN DISEASE; EPITHELIAL CELLS; HUMANS; INTESTINAL MUCOSA; MALNUTRITION;

EID: 84902149501     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000029     Document Type: Review

References (151)

1. Pastorelli L, de Salvo C, Mercado Jr, et al Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front Immunol. 2013; 4: 280.
2. Rescigno M. The intestinal epithelial barrier in the control of homeosta-sis and immunity. Trends Immunol. 2011; 32: 256-264.
3. Caspary WF. Diarrhoea associated with carbohydrate malabsorption. Clin Gastroenterol. 1986; 15: 631-655. (Pubitemid 16009184)
4. Hammer HF, Fine KD, Santa Ana CA, et al Carbohydrate malabsorption. Its measurement and its contribution to diarrhea. J Clin Invest. 1990; 86: 1936-1944.
5. Barrett JS, Irving PM, Shepherd S.J., et al Comparison of the prevalence of fructose and lactose malabsorption across chronic intestinal disorders. Aliment Pharmacol Ther. 2009; 30: 165-174.
6. Coëffier M., Marion-Letellier R, Dechelotte P. Potential for amino acids supplementation during inflammatory bowel diseases. Inflamm Bowel Dis. 2010; 16: 518-524.
7. Fotiadis C, Adamis S, Misiakos E.P., et al The prophylactic effect of L-arginine in acute ischaemic colitis in a rat model of ischaemia/reper-fusion injury. Acta Chir Belgica. 2007; 107: 192-200.
8. Cross RK, Wilson KT Nitric oxide in inflammatory bowel disease. Inflamm Bowel Dis. 2003; 9: 179-189. (Pubitemid 36592449)
9. Coburn LA, Gong X, Singh K., et al L-arginine supplementation improves responses to injury and inflammation in dextran sulfate sodium colitis. PLoS One. 2012; 7:e33546.
10. Singh K, Coburn LA, Barry D.P., et al Deletion of cationic amino acid transporter 2 exacerbates dextran sulfate sodium colitis and leads to an IL-17-predominant T cell response. Am J Physiol Gastrointest Liver Physiol. 2013; 305:G225-G240.
11. Singh K, Coburn LA, Barry D.P., et al L-arginine uptake by cationic amino acid transporter 2 is essential for colonic epithelial cell restitution. Am J Physiol Gastrointest Liver Physiol. 2012; 302:G1061-G1073.
12. Fritz JH. Arginine cools the inflamed gut. Infect Immun. 2013; 81: 3500-3502.
13. Rao RK, Samak G. Role of glutamine in protection of intestinal epithelial tight junctions. J Epithelial Biol Pharmacol. 2012; 5: 47-54.
14. Xue H, Sufit AJ, Wischmeyer PE Glutamine therapy improves outcome of in vitro and in vivo experimental colitis models. JPEN J Parenter Enteral Nutr. 2011; 35: 188-197.
15. Vicario M, Amat C, Rivero M., et al Dietary glutamine affects mucosal functions in rats with mild DSS-induced colitis. J Nutr. 2007; 137: 1931-1937. (Pubitemid 47292741)
16. Ameho CK, Adjei AA, Harrison E.K., et al Prophylactic effect of dietary glutamine supplementation on interleukin 8 and tumour necrosis factor alpha production in trinitrobenzene sulphonic acid induced colitis. Gut. 1997; 41: 487-493. (Pubitemid 27448780)
17. Akobeng AK, Miller V, Stanton J., et al Double-blind randomized controlled trial of glutamine-enriched polymeric diet in the treatment of active Crohn's disease. J Pediatr Gastroenterol Nutr. 2000; 30: 78-84. (Pubitemid 30349950)
18. Akobeng AI, Clayton PE, Miller V, et al Low serum concentrations of insulin-like growth factor-I in children with active Crohn disease: effect of enteral nutritional support and glutamine supplementation. Scand J Gastroenterol. 2002; 37: 1422-1427. (Pubitemid 36051503)
19. Akobeng AK, Richmond K, Miller V., et al Effect of exclusive enteral nutritional treatment on plasma antioxidant concentrations in childhood Crohn's disease. Clin Nutr. 2007; 26: 51-56. (Pubitemid 46179126)
20. Ockenga J, Borchert K, Stuber E., et al Glutamine-enriched total paren-teral nutrition in patients with inflammatory bowel disease. Eur J Clin Nutr. 2005; 59: 1302-1309. (Pubitemid 41655635)
21. Sido B, Seel C, Hochlehnert A., et al Low intestinal glutamine level and low glutaminase activity in Crohn's disease: a rational for glutamine supplementation? Dig Dis Sci. 2006; 51: 2170-2179.
22. Arthur S, Saha P, Sundaram S., et al Regulation of sodium-glutamine cotransport in villus and crypt cells by glucocorticoids during chronic enteritis. Inflamm Bowel Dis. 2012; 18: 2149-2157.
23. Talukder Jr, Boyd B, Griffin A., et al Inflammatory cytokine TNF-alpha inhibits Na(+)-glutamine cotransport in intestinal epithelial cells. Can J Physiol Pharmacol. 2013; 91: 275-284.
24. Ganapathy V, Leibach FH Is intestinal peptide transport energized by a proton gradient? Am J Physiol. 1985; 249:G153-G160. (Pubitemid 16241774)
25. Ganapathy V, Leibach FH Carrier-mediated reabsorption of small pep-tides in renal proximal tubule. Am J Physiol. 1986; 251:F945-F953.
26. Smith DE, Clemencon B, Hediger MA Proton-coupled oligopeptide transporter family SLC15: physiological, pharmacological and pathological implications. Mol Aspects Med. 2013; 34: 323-336.
27. Groneberg DA, Doring F, Eynott P.R., et al Intestinal peptide transport: ex vivo uptake studies and localization of peptide carrier PEPT1. Am J Physiol Gastrointest Liver Physiol. 2001; 281:G697-G704.
28. Jappar D, Wu SP, Hu Y, et al Significance and regional dependency of peptide transporter (PEPT) 1 in the intestinal permeability of glycylsar-cosine: in situ single-pass perfusion studies in wild-type and Pept1 knockout mice. Drug Metab Dispos. 2010; 38: 1740-1746.
29. Walker D, Thwaites DT, Simmons N.L., et al Substrate upregulation of the human small intestinal peptide transporter, hPepT1. J Physiol. 1998; 507(pt 3): 697-706. (Pubitemid 28143571)
30. + channel blockers. Antimicrob Agents Chemother. 2002; 46: 1375-1380. (Pubitemid 34415317)
31. + exchanger. Clin Pharmacol Ther. 1995; 57: 257-264.
32. + exchange activity. Pflugers Archiv. 2002; 445: 139-146. (Pubitemid 35370425)
33. +/oligopeptide transporter 1. Drug Metab Pharmacokinet. 2005; 20: 443-451.
34. Benner J, Daniel H, Spanier B. A glutathione peroxidase, intracellular peptidases and the TOR complexes regulate peptide transporter PEPT-1 in C. elegans. PLoS One. 2011; 6:e25624.
35. Spanier B. Transcriptional and functional regulation of the intestinal peptide transporter PEPT1. J Physiol. 2014; 592: 871-879.
36. Zucchelli M, Torkvist L, Bresso F., et al PepT1 oligopeptide transporter (SLC15A1) gene polymorphism in inflammatory bowel disease. Inflamm Bowel Dis. 2009; 15: 1562-1569.
37. Merlin D, Si-Tahar M, Sitaraman S.V., et al Colonic epithelial hPepT1 expression occurs in inflammatory bowel disease: transport of bacterial peptides influences expression of MHC class 1 molecules. Gastroenter-ology. 2001; 120: 1666-1679. (Pubitemid 32523485)
38. Wojtal KA, Eloranta JJ, Hruz P, et al Changes in mRNA expression levels of solute carrier transporters in inflammatory bowel disease patients. Drug Metab Dispos. 2009; 37: 1871-1877.
39. Buyse M, Charrier L, Sitaraman S., et al Interferon-gamma increases hPepT1-mediated uptake of di-tripeptides including the bacterial tripeptide fMLP in polarized intestinal epithelia. Am J Pathol. 2003; 163: 1969-1977. (Pubitemid 37310027)
40. Vavricka SR, Musch MW, Fujiya M, et al Tumor necrosis factor-alpha and interferon-gamma increase PepT1 expression and activity in the human colon carcinoma cell line Caco-2/bbe and in mouse intestine. Pflugers Archiv. 2006; 452: 71-80.
41. Nduati V, Yan Y, Dalmasso G., et al Leptin transcriptionally enhances peptide transporter (hPepT1) expression and activity via the cAMP-response element-binding protein and Cdx2 transcription factors. J Biol Chem. 2007; 282: 1359-1373. (Pubitemid 47076560)
42. Merlin D, Steel A, Gewirtz A.T., et al hPepT1-mediated epithelial transport of bacteria-derived chemotactic peptides enhances neutrophil- epithelial interactions. J Clin Invest. 1998; 102: 2011-2018. (Pubitemid 29001848)
43. Vavricka SR, Musch MW, Chang J.E., et al hPepT1 transports muramyl dipeptide, activating NF-kappaB and stimulating IL-8 secretion in human colonic Caco2/bbe cells. Gastroenterology. 2004; 127: 1401-1409. (Pubitemid 39457767)
44. Dalmasso G, Nguyen HT, Charrier-Hisamuddin L, et al PepT1 mediates transport of the proinflammatory bacterial tripeptide L-Ala-{gamma}-D-Glu-meso- DAP in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2010; 299:G687-G696.
45. Buyse M, Tsocas A, Walker F., et al PepT1-mediated fMLP transport induces intestinal inflammation in vivo. Am J Physiol Cell Physiol. 2002; 283:C1795-C1800. (Pubitemid 35340612)
46. Dalmasso G, Nguyen HT, Ingersoll S.A., et al The PepT1-NOD2 signaling pathway aggravates induced colitis in mice. Gastroenterology. 2011; 141: 1334-1345.
47. Nguyen HT, Dalmasso G, Powell K.R., et al Pathogenic bacteria induce colonic PepT1 expression: an implication in host defense response. Gas-troenterology. 2009; 137: 1435-1447. e1431-e1432.
48. Wuensch T, Schulz S, Ullrich S., et al The peptide transporter PEPT1 is expressed in distal colon in rodents and humans and contributes to water absorption. Am J Physiol Gastrointest Liver Physiol. 2013; 305:G66-G73.
49. Ingersoll SA, Ayyadurai S, Charania M.A., et al The role and pathophys-iological relevance of membrane transporter PepT1 in intestinal inflammation and inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol. 2012; 302:G484-G492.
50. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990; 70: 567-590. (Pubitemid 20140190)
51. Kiela PR, Kuscuoglu N, Midura A.J., et al Molecular mechanism of rat NHE3 gene promoter regulation by sodium butyrate. Am J Physiol Cell Physiol. 2007; 293:C64-C74. (Pubitemid 47105006)
52. Krishnan S, Rajendran VM, Binder HJ Apical NHE isoforms differentially regulate butyrate-stimulated Na absorption in rat distal colon. Am J Physiol Cell Physiol. 2003; 285:C1246-C1254. (Pubitemid 37296301)
53. Kiela PR, Hines ER, Collins J.F., et al Regulation of the rat NHE3 gene promoter by sodium butyrate. Am J Physiol Gastrointest Liver Physiol. 2001; 281:G947-G956.
54. Musch MW, Bookstein C, Xie Y., et al SCFA increase intestinal Na absorption by induction of NHE3 in rat colon and human intestinal C2/bbe cells. Am J Physiol Gastrointest Liver Physiol. 2001; 280: G687-G693.
55. Hamer HM, Jonkers D, Venema K., et al Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008; 27: 104-119. (Pubitemid 350256609)
56. Davie Jr. Inhibition of histone deacetylase activity by butyrate. J Nutr. 2003; 133: 2485S-2493S.
57. Arpaia N, Campbell C, Fan X., et al Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013; 504: 451-455.
58. Furusawa Y, Obata Y, Fukuda S., et al Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013; 504: 446-450.
59. Singh N, Gurav A, Sivaprakasam S., et al Activation of gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014; 40: 128-139.
60. Wang W, Chen L, Zhou R., et al Increased proportion of bifidobacterium and the lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J Clin Microbiol. 2014; 52: 398-406.
61. Machiels K, Joossens M, Sabino J., et al A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. [published online ahead of print September 10, 2013]. doi:10.1136/gutjnl-2013-304833.
62. Roediger WE. The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet. 1980; 2: 712-715. (Pubitemid 10060060)
63. Roediger WE, Nance S. Metabolic induction of experimental ulcerative colitis by inhibition of fatty acid oxidation. Br J Exp Pathol. 1986; 67: 773-782. (Pubitemid 17212913)
64. Jorgensen J, Mortensen PB Substrate utilization by intestinal mucosal tissue strips from patients with inflammatory bowel disease. Am J Phys-iol Gastrointest Liver Physiol. 2001; 281:G405-G411.
65. Finnie IA, Taylor BA, Rhodes JM Ileal and colonic epithelial metabolism in quiescent ulcerative colitis: increased glutamine metabolism in distal colon but no defect in butyrate metabolism. Gut. 1993; 34: 1552-1558. (Pubitemid 23341847)
66. + absorption during acute colitis in the rabbit. Gastro-enterology. 1994; 106: 1190-1198. (Pubitemid 24129234)
67. Hadjiagapiou C, Schmidt L, Dudeja P.K., et al Mechanism(s) of butyrate transport in Caco-2 cells: role of monocarboxylate transporter 1. Am J Physiol Gastrointest Liver Physiol. 2000; 279:G775-G780.
68. Tamai I, Takanaga H, Maeda H., et al Participation of a proton-cotransporter, MCT1, in the intestinal transport of monocarboxylic acids. Biochem Biophys Res Commun. 1995; 214: 482-489.
69. Kekuda R, Manoharan P, Baseler W., et al Monocarboxylate 4 mediated butyrate transport in a rat intestinal epithelial cell line. Dig Dis Sci. 2013; 58: 660-667.
70. Thibault R, de Coppet P, Daly K, et al Down-regulation of the mono-carboxylate transporter 1 is involved in butyrate deficiency during intestinal inflammation. Gastroenterology. 2007; 133: 1916-1927. (Pubitemid 350180798)
71. Thibault R, Blachier F, Darcy-Vrillon B, et al Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm Bowel Dis. 2010; 16: 684-695.
72. Borthakur A, Priyamvada S, Kumar A., et al A novel nutrient sensing mechanism underlies substrate-induced regulation of monocarboxylate transporter-1. Am J Physiol Gastrointest Liver Physiol. 2012; 303: G1126-G1133.
73. Debongnie JC, Phillips SF Capacity of the human colon to absorb fluid. Gastroenterology. 1978; 74: 698-703. (Pubitemid 8333137)
74. Seidler U, Lenzen H, Cinar A., et al Molecular mechanisms of disturbed electrolyte transport in intestinal inflammation. Ann N Y Acad Sci. 2006; 1072: 262-275. (Pubitemid 44448459)
75. Binder HJ. Mechanisms of diarrhea in inflammatory bowel diseases. Ann N Y Acad Sci. 2009; 1165: 285-293.
76. Tang Y, Forsyth CB, Keshavarzian A. New molecular insights into inflammatory bowel disease-induced diarrhea. Expert Rev Gastroenterol Hepatol. 2011; 5: 615-625.
77. Wenzl HH. Diarrhea in chronic inflammatory bowel diseases. Gastro-enterol Clin North Am. 2012; 41: 651-675.
78. Sandle GI, Higgs N, Crowe P., et al Cellular basis for defective electrolyte transport in inflamed human colon. Gastroenterology. 1990; 99: 97-105. (Pubitemid 20202496)
79. Harris J, Shields R. Absorption and secretion of water and electrolytes by the intact human colon in diffuse untreated proctocolitis. Gut. 1970; 11: 27-33.
80. Rask-Madsen J., Hammersgaard EA, Knudsen E. Rectal electrolyte transport and mucosal permeability in ulcerative colitis and Crohn's disease. J Lab Clin Med. 1973; 81: 342-353.
81. + exchangers in the mammalian gastrointestinal tract. J Physiol Pharmacol. 2006; 57(SUPPL. 7): 51-79. (Pubitemid 46548790)
82. + exchanger isoform 2 gene causes reduced viability of gastric parietal cells and loss of net acid secretion. J Clin Invest. 1998; 101: 1243-1253. (Pubitemid 28145240)
83. + exchanger. Nat Genet. 1998; 19: 282-285. (Pubitemid 28309344)
84. Xu H, Zhang B, Li J., et al Impaired mucin synthesis and bicarbonate secretion in the colon of NHE8 knockout mice. Am J Physiol Gastro-intest Liver Physiol. 2012; 303:G335-G343.
85. Rocha F, Musch MW, Lishanskiy L, et al IFN-gamma downregulates expression of Na(+)/H(+) exchangers NHE2 and NHE3 in rat intestine and human Caco-2/bbe cells. Am J Physiol Cell Physiol. 2001; 280: C1224-C1232.
86. + exchange isoform activities by enteropathogenic E. coli in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2004; 287: G370-G378. (Pubitemid 38955257)
87. Singh V, Raheja G, Borthakur A., et al Lactobacillus acidophilus upre-gulates intestinal NHE3 expression and function. Am J Physiol Gastro-intest Liver Physiol. 2012; 303:G1393-G1401.
88. Barmeyer C, Harren M, Schmitz H., et al Mechanisms of diarrhea in the interleukin-2-deficient mouse model of colonic inflammation. Am J Physiol Gastrointest Liver Physiol. 2004; 286:G244-G252. (Pubitemid 38134035)
89. Sullivan S, Alex P, Dassopoulos T., et al Downregulation of sodium transporters and NHERF proteins in IBD patients and mouse colitis models: potential contributors to IBD-associated diarrhea. Inflamm Bowel Dis. 2009; 15: 261-274.
90. 0-amino-salicylate treatment. Scand J Gastroenterol. 2009; 44: 56-64.
91. Lenzen H, Lunnemann M, Bleich A., et al Downregulation of the NHE3-binding PDZ-adaptor protein PDZK1 expression during cytokine-induced inflammation in interleukin-10-deficient mice. PLoS One. 2012; 7:e40657.
92. Yeruva S, Farkas K, Hubricht J., et al Preserved Na(+)/H(+) exchanger isoform 3 expression and localization, but decreased NHE3 function indicate regulatory sodium transport defect in ulcerative colitis. Inflamm Bowel Dis. 2010; 16: 1149-1161.
93. Farkas K, Yeruva S, Rakonczay Z Jr, et al New therapeutic targets in ulcerative colitis: the importance of ion transporters in the human colon. Inflamm Bowel Dis. 2011; 17: 884-898.
94. Laubitz D, Larmonier CB, Bai A, et al Colonic gene expression profile in NHE3-deficient mice: evidence for spontaneous distal colitis. Am J Physiol Gastrointest Liver Physiol. 2008; 295:G63-G77.
95. Kiela PR, Laubitz D, Larmonier C.B., et al Changes in mucosal homeo-stasis predispose NHE3 knockout mice to increased susceptibility to DSS-induced epithelial injury. Gastroenterology. 2009; 137: 965-975, 975 e1-10.
96. Johansson ME, Gustafsson JK, Holmen-Larsson J, et al Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. 2014; 63: 281-291.
97. Larmonier CB, Laubitz D, Hill F.M., et al Reduced colonic microbial diversity is associated with colitis in NHE3-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2013; 305:G667-677.
98. Engevik MA, Aihara E, Montrose M.H., et al Loss of NHE3 alters gut microbiota composition and influences Bacteroides thetaiotaomicron growth. Am J Physiol Gastrointest Liver Physiol. 2013; 305:G697-G711.
99. Edwards LA, Lucas M, Edwards E.A., et al Aberrant response to commensal Bacteroides thetaiotaomicron in Crohn's disease: an ex vivo human organ culture study. Inflamm Bowel Dis. 2011; 17: 1201-1208.
100. Hansen JJ, Huang Y, Peterson D.A., et al The colitis-associated transcriptional profile of commensal bacteroides thetaiotaomicron enhances adaptive immune responses to a bacterial antigen. PLoS One. 2012; 7:e42645.
101. Xu H, Chen H, Dong J., et al Tumor necrosis factor-{alpha} downregu-lates intestinal NHE8 expression by reducing basal promoter activity. Am J Physiol Cell Physiol. 2009; 296:C489-C497.
102. Liu C, Xu H, Zhang B., et al NHE8 plays an important role in mucosal protection via its effect on bacterial adhesion. Am J Physiol Cell Physiol. 2013; 305:C121-C128.
103. Xiao F, Juric M, Li J., et al Loss of downregulated in adenoma (DRA) impairs mucosal HCO3(-) secretion in murine ileocolonic inflammation. Inflamm Bowel Dis. 2012; 18: 101-111.
104. Juric M, Xiao F, Amasheh S., et al Increased epithelial permeability is the primary cause for bicarbonate loss in inflamed murine colon. Inflamm Bowel Dis. 2013; 19: 904-911.
105. Alrefai WA, Wen X, Jiang W., et al Molecular cloning and promoter analysis of downregulated in adenoma (DRA). Am J Physiol Gastrointest Liver Physiol. 2007; 293:G923-G934. (Pubitemid 350106556)
106. Saksena S, Singla A, Goyal S., et al Mechanisms of transcriptional modulation of the human anion exchanger SLC26A3 gene expression by IFN-{gamma}. Am J Physiol Gastrointest Liver Physiol. 2010; 298: G159-G166.
107. Wang Z, Petrovic S, Mann E., et al Identification of an apical Cl (-)/HCO3(-) exchanger in the small intestine. Am J Physiol Gastrointest Liver Physiol. 2002; 282:G573-G579. (Pubitemid 34651673)
108. 0-flanking region and regulation of expression of human anion exchanger SLC26A6. J Cell Biochem. 2008; 105: 454-466.
109. +-ATPase in ulcerative colitis. J Pathol. 2004; 204: 84-92. (Pubitemid 39214485)
110. Amasheh S, Barmeyer C, Koch C.S., et al Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis. Gastroenterology. 2004; 126: 1711-1720. (Pubitemid 38736336)
111. Zeissig S, Bergann T, Fromm A., et al Altered ENaC expression leads to impaired sodium absorption in the noninflamed intestine in Crohn's disease. Gastroenterology. 2008; 134: 1436-1447. (Pubitemid 351615367)
112. Barmeyer C, Amasheh S, Tavalali S., et al IL-1beta and TNFalpha regulate sodium absorption in rat distal colon. Biochem Biophys Res Commun. 2004; 317: 500-507. (Pubitemid 38452510)
113. Barmeyer C, Horak I, Zeitz M., et al The interleukin-2-deficient mouse model. Pathobiology. 2002; 70: 139-142. (Pubitemid 36184446)
114. Schumann M, Winter S, Wichner K., et al CCR7 deficiency causes diarrhea associated with altered ion transport in colonocytes in the absence of overt colitis. Mucosal Immunol. 2012; 5: 377-387.
115. Bachmann O, Juric M, Seidler U., et al Basolateral ion transporters involved in colonic epithelial electrolyte absorption, anion secretion and cellular homeostasis. Acta Physiol (Oxf). 2011; 201: 33-46.
116. Vagin O, Dada LA, Tokhtaeva E, et al The Na-K-ATPase alpha(1)beta (1) heterodimer as a cell adhesion molecule in epithelia. Am J Physiol Cell Physiol. 2012; 302:C1271-C1281.
117. Rajasekaran SA, Rajasekaran AK Na,K-ATPase and epithelial tight junctions. Front Biosci (Landmark Ed). 2009; 14: 2130-2148.
118. Rajasekaran SA, Barwe SP, Rajasekaran AK Multiple functions of Na, K-ATPase in epithelial cells. Semin Nephrol. 2005; 25: 328-334. (Pubitemid 41749415)
119. Rachmilewitz D, Karmeli F, Sharon P. Decreased colonic Na-K-ATPase activity in active ulcerative colitis. Isr J Med Sci. 1984; 20: 681-684. (Pubitemid 14035879)
120. +)-ATPase activity and degree of mucosal inflammation in inflammatory bowel disease. Dig Dis Sci. 1988; 33: 417-422.
121. Ejderhamn J, Finkel Y, Strandvik B. Na,K-ATPase activity in rectal mucosa of children with ulcerative colitis and Crohn's disease. Scand J Gastroenterol. 1989; 24: 1121-1125. (Pubitemid 19275599)
122. Greig E, Sandle GI Diarrhea in ulcerative colitis. The role of altered colonic sodium transport. Ann N Y Acad Sci. 2000; 915: 327-332. (Pubitemid 32059398)
123. +-ATPase by interferon gamma down-regulates intestinal epithelial transport and barrier function. Gastroenterology. 2001; 120: 1393-1403. (Pubitemid 32322313)
124. +-ATPase expression in human intestinal xenografts in vivo. Am J Physiol Gastrointest Liver Physiol. 2004; 286:G157-G165. (Pubitemid 38055849)
125. +-ATPase activity and molecular events downstream of interferon-gamma receptor stimulation. Br J Pharmacol. 2004; 142: 1281-1292. (Pubitemid 39178882)
126. +-ATPase. J Clin Invest. 2002; 110: 1739-1747. (Pubitemid 35424252)
127. Hwang C, Ross V, Mahadevan U. Micronutrient deficiencies in inflammatory bowel disease: from A to zinc. Inflamm Bowel Dis. 2012; 18: 1961-1981.
128. Alkhouri RH, Hashmi H, Baker R.D., et al Vitamin and mineral status in patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2013; 56: 89-92.
129. Vavricka SR, Rogler G. Intestinal absorption and vitamin levels: is a new focus needed? Dig Dis. 2012; 30(SUPPL. 3): 73-80.
130. Gasche C, Lomer MC, Cavill I, et al Iron, anaemia, and inflammatory bowel diseases. Gut. 2004; 53: 1190-1197. (Pubitemid 38961976)
131. Wang X, Garrick MD, Yang F, et al TNF, IFN-gamma, and endotoxin increase expression of DMT1 in bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2005; 289:L24-L33. (Pubitemid 40863551)
132. Nemeth E, Rivera S, Gabayan V., et al IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest. 2004; 113: 1271-1276. (Pubitemid 39069926)
133. Nicolas G, Chauvet C, Viatte L., et al The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest. 2002; 110: 1037-1044.
134. Dudkowiak R, Neubauer K, Poniewierka E. Hepcidin and its role in inflammatory bowel disease. Adv Clin Exp Med. 2013; 22: 585-591.
135. Bergamaschi G, Di Sabatino A, Albertini R, et al Serum hepcidin in inflammatory bowel diseases: biological and clinical significance. Inflamm Bowel Dis. 2013; 19: 2166-2172.
136. Vagianos K, Bector S, McConnell J., et al Nutrition assessment of patients with inflammatory bowel disease. JPEN J Parenter Enteral Nutr. 2007; 31: 311-319. (Pubitemid 47025695)
137. Ojuawo A, Keith L. The serum concentrations of zinc, copper and selenium in children with inflammatory bowel disease. Cent Afr J Med. 2002; 48: 116-119.
138. Matsui T. Zinc deficiency in Crohn's disease. J Gastroenterol. 1998; 33: 924-925. (Pubitemid 29271566)
139. Ringstad J, Kildebo S, Thomassen Y. Serum selenium, copper, and zinc concentrations in Crohn's disease and ulcerative colitis. Scand J Gastro-enterol. 1993; 28: 605-608. (Pubitemid 23192690)
140. Suwendi E, Iwaya H, Lee J.S., et al Zinc deficiency induces dysregulation of cytokine productions in an experimental colitis of rats. Biomed Res. 2012; 33: 329-336.
141. Ghishan FK, Kiela PR Advances in the understanding of mineral and bone metabolism in inflammatory bowel diseases. Am J Physiol Gastro-intest Liver Physiol. 2011; 300:G191-G201.
142. + transporters. Inflamm Bowel Dis. 2008; 14: 803-811. (Pubitemid 351898065)
143. Thurston RD, Larmonier CB, Majewski P.M., et al Tumor necrosis factor and interferon-gamma down-regulate Klotho in mice with colitis. Gastroenterology. 2010; 138: 1384-1394, 1394 e1381-1382.
144. Radhakrishnan VM, Ramalingam R, Larmonier C.B., et al Post-translational loss of renal TRPV5 calcium channel expression, Ca(2+) wasting, and bone loss in experimental colitis. Gastroenterology. 2013; 145: 613-624.
145. Chen H, Xu H, Dong J., et al Tumor necrosis factor-alpha impairs intestinal phosphate absorption in colitis. Am J Physiol Gastrointest Liver Physiol. 2009; 296:G775-G781.
146. Walder RY, Landau D, Meyer P., et al Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet. 2002; 31: 171-174.
147. Walder RY, Yang B, Stokes J.B., et al Mice defective in Trpm6 show embryonic mortality and neural tube defects. Hum Mol Genet. 2009; 18: 4367-4375.
148. + homeostasis. Science. 2008; 322: 756-760.
149. Hessov I. Magnesium deficiency in Crohn's disease. Clin Nutr. 1990; 9: 297-298. (Pubitemid 20348711)
150. Geerling BJ, Badart-Smook A, Stockbrugger R.W., et al Comprehensive nutritional status in patients with long-standing Crohn disease currently in remission. Am J Clin Nutr. 1998; 67: 919-926. (Pubitemid 28196667)
151. Galland L. Magnesium and inflammatory bowel disease. Magnesium. 1988; 7: 78-83.