The short-chain fatty acid receptor, FFA2, contributes to gestational glucose homeostasis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 10, 2015, Pages 840-851

  Fuller, Miles ^a   Priyadarshini, Medha ^a   Gibbons, Sean M ^b,c   Angueira, Anthony R ^a   Brodsky, Michael ^a   Geoffrey Hayes, M ^a   Kovatcheva Datchary, Petia ^d   Bäckhed, Fredrik ^d   Gilbert, Jack A ^b,c,e,f   Lowe, William L ^a   Layden, Brian T ^a,g  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e MARINE BIOLOGICAL LABORATORY   (United States)

^f ZHEJIANG UNIVERSITY   (China)

^g JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Free fatty acid receptor 2; Gut microbiome; Islets

Indexed keywords

FREE FATTY ACID RECEPTOR 2; G PROTEIN COUPLED RECEPTOR; GLUCOSE; INSULIN; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; FREE FATTY ACID 2 RECEPTOR, MOUSE; VOLATILE FATTY ACID;

ACTINOBACTERIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; CECUM; CELL EXPANSION; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; FEMALE; GLUCOSE HOMEOSTASIS; HYPERGLYCEMIA; IMPAIRED GLUCOSE TOLERANCE; INSULIN RELEASE; INSULIN TOLERANCE TEST; INTESTINE FLORA; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PREGNANCY; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; CLASSIFICATION; FERMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MOLECULAR TYPING; MOLLICUTES; PREGNANCY DIABETES MELLITUS; PRINCIPAL COMPONENT ANALYSIS; SECRETION (PROCESS); STOMACH JUICE; TISSUE CULTURE TECHNIQUE;

ACTINOBACTERIA; ANIMALS; BACTEROIDETES; CECUM; DIABETES, GESTATIONAL; FATTY ACIDS, VOLATILE; FEMALE; FERMENTATION; GASTROINTESTINAL CONTENTS; GASTROINTESTINAL MICROBIOME; INSULIN; INSULIN-SECRETING CELLS; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR TYPING; PREGNANCY; PREGNANCY MAINTENANCE; PRINCIPAL COMPONENT ANALYSIS; RECEPTORS, CELL SURFACE; TENERICUTES; TISSUE CULTURE TECHNIQUES;

EID: 84947282648     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00171.2015     Document Type: Article

References (38)

1. Ahrén B. Islet G protein-coupled receptors as potential targets for treatment of type 2 diabetes. Nat Rev Drug Discov 8: 369-85, 2009.
2. Angueira AR, Ludvik AE, Reddy TE, Wicksteed B, Lowe, WL Jr, Layden BT. New insights into glucose metabolism: lessons learned from 21st century approaches. Diabetes 64: 327-34, 2015.
3. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101: 15718-15723, 2004.
4. Bahar Halpern K, Veprik A, Rubins N, Naaman O, Walker MD. GPR41 gene expression is mediated by internal ribosome entry site (IRES)-dependent translation of a bicistronic mRNA encoding GPR40 and GPR41. J Biol Chem 287: 20154-20163, 2012.
5. Bjursell M, Admyre T, Goransson M, Marley AE, Smith DM, Oscarsson J, Bohlooly YM. Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. Am J Physiol Endocrinol Metab 300: E211-E220, 2011.
6. Bonde L, Vilsboll T, Nielsen T, Bagger JI, Svare JA, Holst JJ, Larsen S, Knop FK. Reduced postprandial GLP-1 responses in women with gestational diabetes mellitus. Diabetes Obes Metab 15: 713-720, 2013.
7. Bouwens L, Rooman I. Regulation of pancreatic beta-cell mass. Physiol Rev 85: 1255-1270, 2005.
8. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278: 11312-11319, 2003.
9. Buchanan TA, Xiang AH. Gestational diabetes mellitus. J Clin Invest 115: 485-491, 2005.
10. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267, 2010.
11. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336, 2010.
12. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. Ultra-high throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621-1624, 2012.
13. Chassaing B, Ley RE, Gewirtz AT. Intestinal epithelial cell toll-like receptor 5 regulates the intestinal microbiota to prevent low-grade inflammation and metabolic syndrome in mice. Gastroenterology 147: 1363-1377, 2014.
14. de Koning EJ, Bonner-Weir S, Rabelink TJ. Preservation of beta-cell function by targeting beta-cell mass. Trends Pharmacol Sci 29: 218-227, 2008.
15. Demirci C, Ernst S, Alvarez-Perez JC, Rosa T, Valle S, Shridhar V, Casinell GP, Alonso L, Vasavada RC, Garcia-Ocana A. Loss HGF/c-Met signaling in pancreatic β-cells leads to incomplete maternal β-cell adaptation and gestational diabetes mellitus. Diabetes 61: 1143-1152, 2012.
16. Hadden DR, McLaughlin C. Normal and abnormal maternal metabolism during pregnancy. Semin Fetal Neonatal Med 14: 66-71, 2009.
17. Insel PA, Wilderman A, Zambon AC, Snead AN, Murray F, Aroonsakool N, McDonald DS, Zhou S, McCann T, Zhang L, Sriram K, Chinn AM, Michkov AV, Lynch RM, Overland AC, Corriden R. G protein-coupled receptor (GPCR) expression in native cells: “novel” endogpcrs as physiologic regulators and therapeutic targets. Mol Pharmacol 88: 181-7, 2015.
18. Karnik SK, Chen H, McLean GW, Heit JJ, Gu X, Zhang AY, Fontaine M, Yen MH, Kim SK. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318: 806-809, 2007.
19. Kebede MA, Alquier T, Latour MG, Poitout V. Lipid receptors and islet function: therapeutic implications? Diabetes Obes Metab 11, Suppl 4: 10-20, 2009.
20. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Backhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150: 470-480, 2012.
21. Layden BT, Angueira AR, Brodsky M, Durai V, Lowe, WL Jr. Short chain fatty acids and their receptors: new metabolic targets. Trans Res 161: 131-140, 2013.
22. Layden BT, Durai V, Newman MV, Marinelarena AM, Ahn CW, Feng G, Lin S, Zhang X, Kaufman DB, Jafari N. Regulation of pancreatic islet gene expression in mouse islets by pregnancy. J Endocrinol 207: 265-279, 2010.
23. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023, 2006.
24. Lozupone C, Knight R. UniFrac: a New phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235, 2005.
25. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282-1286, 2009.
26. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6: 610-618, 2012.
27. McNeils JC, Lee YS, Mayoral R, van der Kant R, Johnson AM, Wollam J, Olefsky JM. GPR43 potentiates beta cell function in obesity. Diabetes. In press.
28. Moffett RC, Vasu S, Thorens B, Drucker DJ, Flatt PR. Incretin receptor null mice reveal key role of GLP-1 but NOT GIP in pancreatic beta cell adaptation to pregnancy. PLOS One 9(6): e96863.
29. Pasek RC, Gannon M. Advancements and challenges in generating accurate animal models of gestational diabetes mellitus. Am J Physiol Endocrinol Metab 305: E1327-E1338, 2013.
30. Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximumlikelihood trees for large alignments. PLoS One 5: e9490, 2010.
31. Priyadarshini M, Layden BT. FFAR3 modulates insulin secretion and global gene expression in mouse islets. Islets In press.
32. Priyadarshini M, Villa SR, Fuller M, Wicksteed B, Mackay CR, Alquier T, Poitout V, Mancebo H, Mirmira RG, Gilchrist A, Layden BT. An acetate-specific GPCR, FFAR2, regulates insulin secretion. Mol Endocrinol 29: 1055-1066, 2015.
33. Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A, et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. Peer J 2: e545, 2014.
34. Rieck S, White P, Schug J, Fox AJ, Smirnova O, Gao N, Gupta RK, Wang ZV, Scherer PE, Keller MP, et al. The transcriptional response of the islet to pregnancy in mice. Mol Endocrinol 23: 1702-1710, 2009.
35. Sorenson RL, Brelje TC. Prolactin receptors are critical to the adaptation of islets to pregnancy. Endocrinology 150: 1566-1569, 2009.
36. Tang C, Ahmed K, Gille A, Lu S, Grone HJ, Tunaru S, Offermanns S. Loss of FFA2 and FFA3 increases insulin secretion and improves glucose tolerance in type 2 diabetes. Nat Med 2: 173-137, 2015.
37. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, Cameron J, Grosse J, Reimann F, Gribble FM. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-proteincoupled receptor FFAR2. Diabetes 61: 364-371, 2012.
38. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267, 2007.