Butyrate transcriptionally enhances peptide transporter PepT1 expression and activity

PLoS ONE

Volumn 3, Issue 6, 2008, Pages

  Dalmasso, Guillaume ^a   Nguyen, Hang Thi Thu ^a   Yan, Yutao ^a   Charrier Hisamuddin, Laetitia ^a   Sitaraman, Shanthi V ^a   Merlin, Didier ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; LUCIFERASE; MESSENGER RNA; PEPTIDE TRANSPORTER 1; TRANSCRIPTION FACTOR CDX2; CDX2 PROTEIN, HUMAN; COTRANSPORTER; HISTONE; HOMEODOMAIN PROTEIN; SLC15A1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; APICAL MEMBRANE; ARTICLE; CELL STRAIN CACO 2; CHROMATIN IMMUNOPRECIPITATION; COLITIS; COLON MUCOSA; COMMENSAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; INCUBATION TIME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING; WILD TYPE; ACETYLATION; BINDING SITE; DRUG EFFECT; ENHANCER REGION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

MUS;

ACETYLATION; BINDING SITES; BLOTTING, WESTERN; BUTYRIC ACID; CACO-2 CELLS; CHROMATIN IMMUNOPRECIPITATION; ENHANCER ELEMENTS (GENETICS); HISTONES; HOMEODOMAIN PROTEINS; HUMANS; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYMPORTERS; TRANSCRIPTION, GENETIC;

EID: 49649124650     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002476     Document Type: Article

References (53)

1. Cummings JH (1981) Short chain fatty acids in the human colon. Gut 22: 763-779.
2. Wrong O, Metcalfe-Gibson A, Morrison RB, Ng ST, Howard AV (1965) In Vivo Dialysis of Faeces as a Method of Stool Analysis. I. Technique and Results in Normal Subjects. Clin Sci 28: 357-375.
3. Cummings JH, Pomare EW, Branch WJ, Naylor CP. Macfarlane GT (1978) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28: 1221-1227.
4. Cummings JH, Macfarlane GT (1991) The control and consequences of bacterial fermenation in the human colon. J Appl Bacteriol 70: 443-459.
5. Engelhardt WV, Luciano L, Reale E, Gros G, Rechkemmer G (1989) Transport of SCFA across the large intestinal epithelium of guinea pig. Acta Vet Scand Suppl 86: 103-106.
6. Buyse M, Sitaraman SV, Liu X, Bado A, Merlin D (2002) Luminal leptin enhances CD147/MCT-1-mediated uptake of butyrate in the human intestinal cell line Caco2-BBE. J Biol Chem 277: 28182-28190.
7. Roediger WE, Millard S (1996) Colonocyte metabolism. Gut 38: 792-793.
8. Clausen MR, Mortensen PB (1994) Kinetic studies on the metabolism of short-chain fatty acids and glucose by isolated rat colonocytes. Gastroenterology 106: 423-432.
9. McIntyre A, Gibson PR, Young GP (1993) Butyrate production firom dietary fibre and protection against large bowel cancer in a rat model. Gut 34: 386-391.
10. Gamet L, Daviaud D, Denis-Pouxviel C, Remesy C, Murat JC (1992) Effects of short-chain fatty acids on growth and differentiation of the human colon-cancer cell line HT29. Int J Cancer 52: 286 289.
11. Ruemmele FM, Schwartz S, Seidman EG, Dionne S, Levy E, et al. (2003) Butyrate induced Caco-2 cell apoptosis is mediated via the mitochondrial pathway. Gut 52: 94-100.
12. Liang R, Fei YJ, Prasad PD, Ramamoorthy S, Han H, et al. (1995) Human intestinal H+/peptide cotransporter. Cloning, functional expression, and chromosomal localization. J Biol Chem 270: 6456-6463.
13. Fei YJ, Ganapathy V, Leibach FH (1998) Molecular and structural features of the proton-coupled oligopeptide transporter superfamily. Prog Nucleic Acid Res Mol Biol 58: 239-261.
14. Adibi SA (1997) The oligopeptide transporter (Pept-1) in human intestine: biology and function. Gastroenterology 113: 332-340.
15. Sai Y, Tamai I, Sumikawa H, Hayashi K, Nakanishi T, et al. (1996) Immunolocalization and pharmacological relevance of oligopeptide transporter PepT1 in intestinal absorption of beta-lactam antibiotics. FEBS Lett 392: 25-29.
16. Ogihara H, Saito H, Shin BC, Ferado T, Takenoshita S. et al. (1996) Immunolocalization of H+/peptide cotransporter in rat digestive tract. Biochem Biophys Res Commun 220: 848-852.
17. Smith DE, Pavlova A, Berger UV, Hediger MA, Yang T, et al. (1998) Tubular localization and tissue distribution of peptide transporters in rat kidney. Pharm Res 15: 1244-1249.
18. Ogihara H, Suzuki T, Nagamachi Y, Inui K, Takata K (1999) Peptide transporter in the rat small intestine: ultrastructural localization and the effect of starvation and administration of amino acids. Histochem J 31: 169-174.
19. Tanaka H, Miyamoto KI, Morita K, Haga H, Segawa H, et al. (1998) Regulation of die PepT1 peptide transporter in the rat small intestine in response to 5-fluorouracil-induced injury. Gastroenterology 114: 714-723.
20. Charrier L, Driss A, Yan Y, Nduati V, Klapproth JM, et al. (2006) hPepT1 mediates bacterial tripeptide fMLP uptake in human monocytes. Lab Invest 86: 490-503.
21. Dalmasso G, Charrier-Hisamuddin L, Thu Nguyen HT, Yan Y, Sitaraman S, et al. (2008) PepT1-mediated tripeptide KPV uptake reduces intestinal inflammation. Gastroenterology 134: 166-178.
22. Merlin D, Si-Tahar M, Sitaraman SV, Eastburn K, Williams I, et al. (2001) Colonic epithelial hPepT1 expression occurs in inflammatory bowel disease: transport of bacterial peptides influences expression of MHC class 1 molecules. Gastroenterology 120: 1666-1679.
23. Ziegler TR, Fernandez-Estivariz C, Gu LH, Bazargan N, Umeakunne K, et al. (2002) Distribution of the H+/peptide transporter PepT1 in human intestine: up-regulated expression in the colonic mucosa of patients with short-bowel syndrome. Am J Clin Nutr 75: 922-930.
24. Kiela PR, Kuscuoglu N, Midura AJ, Midura-Kiela MT, Larmonier CB, et al. (2007) Molecular mechanism of rat NHE3 gene promoter regulation by sodium butyrate. Am J Physiol Cell Physiol 293: C64-74.
25. Kiela PR, Hines ER, Collins JF, Ghishan FK (2001) Regulation of the rat NHE3 gene promoter by sodium butyrate. Am J Physiol Gastrointest Liver Physiol 281: G947-956.
26. Zeissig S, Fromm A, Mankertz J, Weiske J, Zeitz M, et al. (2007) Butyrate induces intestinal sodium absorption via Sp3-mediated transcriptional up-regulation of epithelial sodium channels. Gastroenterology 132: 236-248.
27. Nduati V, Yan Y, Dalmasso G, Driss A, Sitaraman S, et al. (2007) Leptin transcriptionally enhances peptide transporter (hPepT1) expression and activity via the cAMP-response element-binding protein and Cdx2 transcription factors. J Biol Chem 282: 1359-1373.
28. Vidali G, Boffa LC, Bradbury EM, Allfrey VG (1978) Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms or histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci U S A 75: 2239-2243.
29. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59: 675-680.
30. Domon-Dell C, Wang Q, Kim S, Kedinger M, Evers BM, et al. (2002) Stimulation of the intestinal Cdx2 homeobox gene by butyrate in colon cancer cells. Gut 50: 525-529
31. Shimakura J, Terada F, Katsura T, Inui K (2005) Characterization of the human peptide transporter PEPT1 promoter: Sp1 functions as a basal transcriptional regulator of human PEPT1. Am J Physiol Gastrointest Liver Physiol 289: G471-477.
32. Shimakura J, Terada T, Shimada Y, Katsura T, Inui K (2006) The transcription factor Cdx2 regulates the intestine-specific expression of human peptide transporter 1 through functional interaction with Spl. Biochem Pharmacol 71: 1581-1588.
33. Mandal M, Olson DJ, Sharma T, Vadlamudi RK, Kumar R (2001) Butyric acid induces apoptosis by up-regulaing Bax expression via stimulation of the c-Jun N-terminal kinase/activation protein-1 pathway in human colon cancer cells. Gastroenterology 120: 71-78.
34. Merlin D, Steel A, Gewirtz AT, Si-Tahar M, Hediger MA, et al. (1998) hPepT1-mediated epithelial transport of bacteria-derived chemotactic peptides enhances neutrophil-epithelial interactions. J Clin Invest 102: 2011-2018.
35. Buyse M, Tsocas A, Walker F, Merlin D, Bado A (2002) PepT1-mediated fMLP transport induces intestinal inflammation in vivo. Am J Physiol Cell Physiol 283: C1795-1800.
36. Chang JG, Hsieh-Li HM, Jong YJ, Wang NM, Tsai CH, et al (2001) Treatment of Spinal muscular atrophy by sodium butyrate. Proc Natl Acad Sci U S A 98: 9808-9813.
37. Minamiyama M, Katsuno M, Adachi H, Waza M, Sang C, et al. (2001) Sodium butyrate ameliorates phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Hum Mol Genet 13: 1183-1192.
38. Roediger WE (1980) Tile colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet 2: 712-715.
39. Den Houd E, Hiele M, Evenepoel P, Peeters M, Ghoos Y, et al. (1998) In vivo butyrate metabolism and colonic permeability in extensive ulcerative colitis. Gastroenterology 115: 584-590.
40. Ahmas MS, Krishnan S, Ramakrishna BS, Mathan M, Pulimood AB, et al. (2000) Bulyrate and glucose metabolism by colonocyte; in experimental colitis in mice. Gut 16: 493-499.
41. Daly K, Cuff MA, Fung F, Shirazi-Beechey SP (2005) The importance of colonic butyrate transport to the regulation of genes associated with colonic tissue homoeostasis. Biochem Soc Trans 33: 733-735.
42. Silberg DG, Swain GP, Suh ER, Traber PG (2000) Cdx1 and cdx2 expression during intestinal development. Gatroenterology 119: 961-971.
43. Mutoh H, Satoh K, Kita H, Sakamoto H, Hayakawa H, et al. (200?) Cdx2 specifies the differentation of morphological as well as functional adsorptive enterocytes of the small intestine. Int J Dev Biol 49: 867-871.
44. Silberg DG, Sullivan J, Kang E, Swain GP, Moffett J, et al. (2002) Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology 122: 689-696.
45. DeCastro M, Nankova BB, Shah P, Patel P, Mally PV, et al. (2005) Short chain fatty acids regulate tyrosine hydroxylase gene expression through a cAMP-dependent signaling pathway. Brain Res Mol Brain Res 142: 28-38.
46. Shah P, Nankova BB, Parab S, La Gamma EF (2006) Short chain fatty acids induce TH gene expression via ERK-dependent phosphorylation of CREB protein. Brain Res 1107: 13-23.
47. Vavricka SR, Musch MW, Chang JE, Nakagawa Y, Phanvijhitsiri K, et al. (2004) hPepT1 transports muramyl dipeptide, activating NF-kappaB and stimulating IL-8 secretion in human colonic Caco2/bbe cells. Gastroenterology 127: 1401-1409.
48. Segain JP, Raingeard de la Bletiere D, Bourreille A, Leray V, Gervois N, et al. (2000) Butyrate inhibits inifammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47: 397-403.
49. Tedelind S, Westberg F, Kjerrulf M, Vidal A (2007) Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World J Gastroenterol 13: 2826-2832.
50. Shi B, Song D, Xue H, Li J, Li N, et al. (2006) Abnormal expression of the peptide transporter PepT1 in the colon of massive bowel resection rat: a potential route for colonic mucosa damage by transport of fMLP. Dig Dis Sci 51: 2087-2093.
51. Shi B, Song D, Xue H, Li N, Li J (2006) PepT1 mediates colon damage by transporting fMLP in rats with bowel resection. J Surg Res 136: 38-44.
52. Daniel H, Morse EL, Adibi SA (1991) The high and low affinity transport systems for dipeptides in kidney brush border membrane respond differently to alterations in pH gradient and membrane potential. J Biol Chem 266: 19917-19924.
53. Nguyen HT, Charrier-Hisamuddin L, Dalmasso G, Hiol A, Sitaraman S, et al. (2007) Association of PepT1 with lipid rafts differently modulates its transport activity in polarized and nonpolarized cells. Am J Physiol Gastrointest Liver Physiol 293: G1155-1165.