NHE8 plays an important role in mucosal protection via its effect on bacterial adhesion

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 1, 2013, Pages

  Liu, Chang ^a   Xu, Hua ^a   Zhang, Bo ^a   Johansson, Malin E V ^b   Li, Jing ^a   Hansson, Gunnar C ^b   Ghishan, Fayez K ^a  

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

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Mucosal layer; NHE8; Salmonella

Indexed keywords

DEXTRAN SULFATE; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MUCIN 2; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 8; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIUM ADHERENCE; CELL STRAIN CACO 2; CONTROLLED STUDY; DESCENDING COLON; LACTOBACILLUS PLANTARUM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA TYPHIMURIUM;

MUCOSAL LAYER; NHE8; SALMONELLA;

ANIMALS; BACTERIA; BACTERIAL ADHESION; CACO-2 CELLS; COLITIS; COLON; CYTOKINES; DEXTRAN SULFATE; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, MUCOSAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; INTESTINAL MUCOSA; MALE; MICE; MICE, KNOCKOUT; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SODIUM-HYDROGEN ANTIPORTER; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); LACTOBACILLUS PLANTARUM; MUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 84879573183     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00101.2013     Document Type: Article

References (45)

1. Barman M, Unold D, Shifley K, Amir E, Hung K, Bos N, Salzman N. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 76: 907-915, 2008.
2. Bell SM, Schreiner CM, Schultheis PJ, Miller ML, Evans RL, Vorhees CV, Shull GE, Scott WJ. Targeted disruption of the murine Nhe1 locus induces ataxia, growth retardation, and seizures. Am J Physiol Cell Physiol 276: C788-C795, 1999.
3. Candela M, Seibold G, Vitali B, Lachenmaier S, Eikmanns BJ, Brigidi P. Real-time PCR quantification of bacterial adhesion to Caco-2 cells: competition between bifidobacteria and enteropathogens. Res Microbiol 156: 887-895, 2005.
4. Collins JF, Xu H, Kiela PR, Zeng J, Ghishan FK. Functional and molecular characterization of NHE3 expression during ontogeny in rat jejunal epithelium. Am J Physiol Cell Physiol 273: C1937-C1946, 1997.
5. Collins JF, Xu H, Kiela PR, Zeng J, Ghishan FK. Ontogeny of basolateral membrane sodium-hydrogen exchange (NHE) activity and mRNA expression of NHE-1 and NHE-4 in rat kidney and jejunum. Biochim Biophys Acta 1369: 247-258, 1998.
6. Cox GA, Lutz CM, Yang CL, Biemesderfer D, Bronson RT, Fu A, Aronson PS, Noebels JL, Frankel WN. Sodium/hydrogen exchanger gene defect in slow-wave epilepsy mutant mice. Cell 91: 139-148, 1997.
7. Ghishan FK, Kiela PR. Small intestinal ion transport. Curr Opin Gastroenterol 28: 130-134, 2011.
8. Goyal S, Mentone S, Aronson PS. Immunolocalization of NHE8 in rat kidney. Am J Physiol Renal Physiol 288: F530-F538, 2005.
9. + exchanger isoform NHE8. Am J Physiol Renal Physiol 284: F467-F473, 2003.
10. Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K. Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol 47: 367-373, 2008.
11. Haraga A, Ohlson MB, Miller SI. Salmonellae interplay with host cells. Nat Rev Microbiol 6: 53-66, 2008.
12. Iijima H, Takahashi I, Kishi D, Kim JK, Kawano S, Hori M, Kiyono H. Alteration of interleukin 4 production results in the inhibition of T helper type 2 cell-dominated inflammatory bowel disease in T cell receptor α-chain-deficient mice. J Exp Med 190: 607-615, 1999.
13. Ince MN, Elliott DE. Immunologic and molecular mechanisms in inflammatory bowel disease. Surg Clin North Am 87: 681-696, 2007.
14. Johansson ME, Gustafsson JK, Holmén-Larsson JM, Jabbar KS, Xia L, Xu H, Ghishan FK, Carvalho FA, Gewirtz AT, Sjövall H, Hansson GC. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and in patients with ulcerative colitis. Gut. In press.
15. Johansson ME, Larsson JM, Hansson GC. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci USA 108 Suppl 1: 4659-4665, 2011.
16. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA 105: 15064-15069, 2008.
17. Kiela PR, Laubitz D, Larmonier CB, Midura-Kiela MT, Lipko MA, Janikashvili N, Bai A, Thurston R, Ghishan FK. Changes in mucosal homeostasis predispose NHE3 knockout mice to increased susceptibility to DSS-induced epithelial injury. Gastroenterology 137: 965-975, 2009.
18. Laubitz D, Larmonier CB, Bai A, Midura-Kiela MT, Lipko MA, Thurston RD, Kiela PR, Ghishan FK. Colonic gene expression profile in NHE3-deficient mice: evidence for spontaneous distal colitis. Am J Physiol Gastrointest Liver Physiol 295: G63-G77, 2008.
19. Linden SK, Florin TH, McGuckin MA. Mucin dynamics in intestinal bacterial infection. PLos One 3: e3952, 2008.
20. Liu C, Zhang ZY, Dong K, Guo XK. Adhesion and immunomodulatory effects of Bifidobacterium lactis HN019 on intestinal epithelial cells INT-407. World J Gastroenterol 16: 2283-2290, 2010.
21. -ΔΔCT method. Methods 25: 402-408, 2001.
22. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R. Development of 16S rRNA-genetargeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68: 5445-5451, 2002.
23. Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148: 257-266, 2002.
24. Orlowski J, Grinstein S. Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflügers Arch 447: 549-565, 2004.
25. Orlowski J, Kandasamy RA, Shull GE. Molecular cloning of putative members of the Na/H exchanger gene family. cDNA cloning, deduced amino acid sequence, and mRNA tissue expression of the rat Na/H exchanger NHE-1 and two structurally related proteins. J Biol Chem 267: 9331-9339, 1992.
26. Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97: 1166-1177, 2004.
27. Sasaki M, Mathis JM, Jennings MH, Jordan P, Wang Y, Ando T, Joh T, Alexander JS. Reversal of experimental colitis disease activity in mice following administration of an adenoviral IL-10 vector. J Inflamm 2: 13, 2005.
28. + exchanger isoform 2 gene causes reduced viability of gastric parietal cells and loss of net acid secretion. J Clin Invest 101: 1243-1253, 1998.
29. + exchanger. Nat Genet 19: 282-285, 1998.
30. Srikanth CV, Mercado-Lubo R, Hallstrom K, McCormick BA. Salmonella effector proteins and host-cell responses. Cell Mol Life Sci 68: 3687-3697, 2011.
31. Trkov M, Avgustin G. An improved 16S rRNA based PCR method for the specific detection of Salmonella enterica. Int J Food Microbiol 80: 67-75, 2003.
32. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Buller HA, Dekker J, Van Seuningen I, Renes IB, Einerhand AW. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131: 117-129, 2006.
33. van Klinken BJ, Einerhand AW, Duits LA, Makkink MK, Tytgat KM, Renes IB, Verburg M, Buller HA, Dekker J. Gastrointestinal expression and partial cDNA cloning of murine Muc2. Am J Physiol Gastrointest Liver Physiol 276: G115-G124, 1999.
34. Xu H, Chen H, Dong J, Li J, Chen R, Uno JK, Ghishan FK. Tumor necrosis factor-α downregulates intestinal NHE8 expression by reducing basal promoter activity. Am J Physiol Cell Physiol 296: C489-C497, 2009.
35. Xu H, Chen H, Dong J, Lynch R, Ghishan FK. Gastrointestinal distribution and kinetic characterization of the sodium-hydrogen exchanger isoform 8 (NHE8). Cell Physiol Biochem 21: 109-116, 2008.
36. Xu H, Chen R, Ghishan FK. Subcloning, localization, and expression of the rat intestinal sodium-hydrogen exchanger isoform 8. Am J Physiol Gastrointest Liver Physiol 289: G36-G41, 2005.
37. Xu H, Li J, Chen H, Wang C, Ghishan FK. NHE8 plays important roles in gastric mucosal protection. Am J Physiol Gastrointest Liver Physiol 304: G257-G261, 2013.
38. Xu H, Li J, Chen R, Zhang B, Wang C, King N, Chen H, Ghishan FK. NHE2X3 DKO mice exhibit gender-specific NHE8 compensation. Am J Physiol Gastrointest Liver Physiol 300: G647-G653, 2011.
39. Xu H, Zhang B, Li J, Chen H, Tooley J, Ghishan FK. Epidermal growth factor inhibits intestinal NHE8 expression via reducing its basal transcription. Am J Physiol Cell Physiol 299: C51-C57, 2010.
40. Xu H, Zhang B, Li J, Chen H, Wang C, Ghishan FK. Transcriptional inhibition of intestinal NHE8 expression by glucocorticoids involves Pax5. Am J Physiol Gastrointest Liver Physiol 299: G921-G927, 2010.
41. Xu H, Zhang B, Li J, Wang C, Chen H, Ghishan FK. Impaired mucin synthesis and bicarbonate secretion in the colon of NHE8 knockout mice. Am J Physiol Gastrointest Liver Physiol 303: G335-G343, 2012.
42. + exchanger gene family: structure and function studies. Am J Physiol Gastrointest Liver Physiol 269: G1-G11, 1995.
43. + exchange. Annu Rev Physiol 67: 411-443, 2005.
44. Zhang ZY, Liu C, Zhu YZ, Wei YX, Tian F, Zhao GP, Guo XK. Safety assessment of Lactobacillus plantarum JDM1 based on the complete genome. Int J Food Microbiol 153: 166-170, 2011.
45. Zhang ZY, Liu C, Zhu YZ, Zhong Y, Zhu YQ, Zheng HJ, Zhao GP, Wang SY, Guo XK. Complete genome sequence of Lactobacillus plantarum JDM1. J Bacteriol 191: 5020-5021, 2009.