Bacterial Metabolite Indole Modulates Incretin Secretion from Intestinal Enteroendocrine L Cells

Cell Reports

Volumn 9, Issue 4, 2014, Pages 1202-1208

  Chimerel, Catalin ^a,b   Emery, Edward ^a   Summers, David K ^a   Keyser, Ulrich ^b   Gribble, Fiona M ^a   Reimann, Frank ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCAGON LIKE PEPTIDE 1; INDOLE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; ADENOSINE DIPHOSPHATE; CALCIUM; INCRETIN; INDOLE DERIVATIVE; ION; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; POTASSIUM CHLORIDE;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CELL METABOLISM; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; HORMONE RELEASE; INTESTINE FLORA; L CELL LINE; MEMBRANE DEPOLARIZATION; MOUSE; NONHUMAN; NUCLEIC ACID SYNTHESIS; OXIDATIVE PHOSPHORYLATION; POTASSIUM CURRENT; PROTEIN INTERACTION; REGULATORY MECHANISM; REPOLARIZATION; SODIUM CURRENT; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COLON; CYTOLOGY; DRUG EFFECTS; ENTEROENDOCRINE CELL; METABOLISM; SECRETION (PROCESS);

BACTERIA (MICROORGANISMS);

ACTION POTENTIALS; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CELLS, CULTURED; COLON; ENTEROENDOCRINE CELLS; GLUCAGON-LIKE PEPTIDE 1; INCRETINS; INDOLES; IONS; MICE; NADP; POTASSIUM CHANNELS, VOLTAGE-GATED; POTASSIUM CHLORIDE;

EID: 84912137874     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.10.032     Document Type: Article

References (40)

1. Avdonin V., Hoshi T. Modification of voltage-dependent gating ofpotassium channels by free form of tryptophan side chain. Biophys. J. 2001, 81:97-106.
2. Aziz A., Anderson G.H. Exendin-4, a GLP-1 receptor agonist, interacts with proteins and their products of digestion to suppress food intake in rats. J.Nutr. 2003, 133:2326-2330.
3. Bansal T., Alaniz R.C., Wood T.K., Jayaraman A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc. Natl. Acad. Sci. USA 2010, 107:228-233.
4. Berg J., Hung Y.P., Yellen G. A genetically encoded fluorescent reporter of ATP:ADP ratio. Nat. Methods 2009, 6:161-166.
5. Bryan G.T. Urinary excretion of indoxyl sulfate (indican) by human subjects ingesting a semisynthetic diet containing variable quantities of L-tryptophan. Am. J. Clin. Nutr. 1966, 19:113-119.
6. Cani P.D., Everard A., Duparc T. Gut microbiota, enteroendocrine functions and metabolism. Curr. Opin. Pharmacol. 2013, 13:935-940.
7. Chimerel C., Murray A.J., Oldewurtel E.R., Summers D.K., Keyser U.F. The effect of bacterial signal indole on the electrical properties of lipid membranes. Chemphyschem 2013, 14:417-423.
8. DeMoss R.D., Moser K. Tryptophanase in diverse bacterial species. J.Bacteriol. 1969, 98:167-171.
9. Devaraj S., Hemarajata P., Versalovic J. The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin. Chem. 2013, 59:617-628.
10. Drucker D.J., Jin T., Asa S.L., Young T.A., Brubaker P.L. Activation of proglucagon gene transcription by protein kinase-A in a novel mouse enteroendocrine cell line. Mol. Endocrinol. 1994, 8:1646-1655.
11. Friedlander R.S., Moss C.E., Mace J., Parker H.E., Tolhurst G., Habib A.M., Wachten S., Cooper D.M., Gribble F.M., Reimann F. Role of phosphodiesterase and adenylate cyclase isozymes in murine colonic glucagon-like peptide 1 secreting cells. Br. J. Pharmacol. 2011, 163:261-271.
12. Garber A., Henry R., Ratner R., Garcia-Hernandez P.A., Rodriguez-Pattzi H., Olvera-Alvarez I., Hale P.M., Zdravkovic M., Bode B. Liraglutide versus glimepiride monotherapy for type 2 diabetes (LEAD-3 Mono): a randomised, 52-week, phase III, double-blind, parallel-treatment trial. Lancet 2009, 373:473-481. LEAD-3 (Mono) Study Group.
13. Gong F., Ito K., Nakamura Y., Yanofsky C. The mechanism of tryptophan induction of tryptophanase operon expression: tryptophan inhibits release factor-mediated cleavage of TnaC-peptidyl-tRNA(Pro). Proc. Natl. Acad. Sci. USA 2001, 98:8997-9001.
14. Gribble F.M., Williams L., Simpson A.K., Reimann F. A novel glucose-sensing mechanism contributing to glucagon-like peptide-1 secretion from the GLUTag cell line. Diabetes 2003, 52:1147-1154.
15. Grynkiewicz G., Poenie M., Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J.Biol. Chem. 1985, 260:3440-3450.
16. Karlin D.A., Mastromarino A.J., Jones R.D., Stroehlein J.R., Lorentz O. Fecal skatole and indole and breath methane and hydrogen in patients with large bowel polyps or cancer. J.Cancer Res. Clin. Oncol. 1985, 109:135-141.
17. Lee J.H., Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 2010, 34:426-444.
18. Marre M., Shaw J., Brändle M., Bebakar W.M., Kamaruddin N.A., Strand J., Zdravkovic M., Le Thi T.D., Colagiuri S. Liraglutide, a once-daily human GLP-1 analogue, added to a sulphonylurea over 26weeks produces greater improvements in glycaemic and weight control compared with adding rosiglitazone or placebo in subjects with Type 2 diabetes (LEAD-1 SU). Diabet. Med. 2009, 26:268-278. LEAD-1 SU study group.
19. Mutch D.M., Fuhrmann J.C., Rein D., Wiemer J.C., Bouillot J.L., Poitou C., Clément K. Metabolite profiling identifies candidate markers reflecting the clinical adaptations associated with Roux-en-Y gastric bypass surgery. PLoS ONE 2009, 4:e7905.
20. Nauck M., Frid A., Hermansen K., Shah N.S., Tankova T., Mitha I.H., Zdravkovic M., Düring M., Matthews D.R. Efficacy and safety comparison of liraglutide, glimepiride, and placebo, all in combination with metformin, in type 2 diabetes: the LEAD (liraglutide effect and action in diabetes)-2 study. Diabetes Care 2009, 32:84-90. LEAD-2 Study Group.
21. Nicholson J.K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., Pettersson S. Host-gut microbiota metabolic interactions. Science 2012, 336:1262-1267.
22. Nyangale E.P., Mottram D.S., Gibson G.R. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J.Proteome Res. 2012, 11:5573-5585.
23. Parker H.E., Adriaenssens A., Rogers G., Richards P., Koepsell H., Reimann F., Gribble F.M. Predominant role of active versus facilitative glucose transport for glucagon-like peptide-1 secretion. Diabetologia 2012, 55:2445-2455.
24. Peters C.T., Choi Y.H., Brubaker P.L., Anderson G.H. A glucagon-like peptide-1 receptor agonist and an antagonist modify macronutrient selection by rats. J.Nutr. 2001, 131:2164-2170.
25. Petersen N., Reimann F., Bartfeld S., Farin H.F., Ringnalda F.C., Vries R.G., van den Brink S., Clevers H., Gribble F.M., de Koning E.J. Generation of L cells in mouse and human small intestine organoids. Diabetes 2014, 63:410-420.
26. Piñero-Fernandez S., Chimerel C., Keyser U.F., Summers D.K. Indole transport across Escherichia coli membranes. J.Bacteriol. 2011, 193:1793-1798.
27. Plaisancié P., Dumoulin V., Chayvialle J.A., Cuber J.C. Luminal glucagon-like peptide-1(7-36) amide-releasing factors in the isolated vascularly perfused rat colon. J.Endocrinol. 1995, 145:521-526.
28. Psichas A., Sleeth M.L., Murphy K.G., Brooks L., Bewick G., Hanyaloglu A.C., Ghatei M.A., Bloom S.R., Frost G. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int. J. Obes. (Lond.) 2014, Published online August 11, 2014. 10.1038/ijo.2014.153.
29. Reimann F., Gribble F.M. Glucose-sensing in glucagon-like peptide-1-secreting cells. Diabetes 2002, 51:2757-2763.
30. Reimann F., Maziarz M., Flock G., Habib A.M., Drucker D.J., Gribble F.M. Characterization and functional role of voltage gated cation conductances in the glucagon-like peptide-1 secreting GLUTag cell line. J.Physiol. 2005, 563:161-175.
31. Reimann F., Habib A.M., Tolhurst G., Parker H.E., Rogers G.J., Gribble F.M. Glucose sensing in L cells: a primary cell study. Cell Metab. 2008, 8:532-539.
32. Smith E.A., Macfarlane G.T. Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J.Appl. Bacteriol. 1996, 81:288-302.
33. Tarasov A.I., Semplici F., Ravier M.A., Bellomo E.A., Pullen T.J., Gilon P., Sekler I., Rizzuto R., Rutter G.A. The mitochondrial Ca2+ uniporter MCU is essential for glucose-induced ATP increases in pancreatic β-cells. PLoS ONE 2012, 7:e39722.
34. Tarini J., Wolever T.M. The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects. Appl. Physiol. Nutr. Metab. 2010, 35:9-16.
35. Tolhurst G., Zheng Y., Parker H.E., Habib A.M., Reimann F., Gribble F.M. Glutamine triggers and potentiates glucagon-like peptide-1 secretion by raising cytosolic Ca2+ and cAMP. Endocrinology 2011, 152:405-413.
36. Tolhurst G., Heffron H., Lam Y.S., Parker H.E., Habib A.M., Diakogiannaki E., Cameron J., Grosse J., Reimann F., Gribble F.M. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 2012, 61:364-371.
37. Wang T.J., Larson M.G., Vasan R.S., Cheng S., Rhee E.P., McCabe E., Lewis G.D., Fox C.S., Jacques P.F., Fernandez C., et al. Metabolite profiles and the risk of developing diabetes. Nat. Med. 2011, 17:448-453.
38. Zariwala H.A., Borghuis B.G., Hoogland T.M., Madisen L., Tian L., De Zeeuw C.I., Zeng H., Looger L.L., Svoboda K., Chen T.W. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging invivo. J.Neurosci. 2012, 32:3131-3141.
39. Zinman B., Gerich J., Buse J.B., Lewin A., Schwartz S., Raskin P., Hale P.M., Zdravkovic M., Blonde L. Efficacy and safety of the human glucagon-like peptide-1 analog liraglutide in combination with metformin and thiazolidinedione in patients with type 2 diabetes (LEAD-4 Met+TZD). Diabetes Care 2009, 32:1224-1230. LEAD-4 Study Investigators.
40. Zuccato E., Venturi M., Di Leo G., Colombo L., Bertolo C., Doldi S.B., Mussini E. Role of bile acids and metabolic activity of colonic bacteria in increased risk of colon cancer after cholecystectomy. Dig. Dis. Sci. 1993, 38:514-519.