Role of gut microbiota and short chain fatty acids in modulating energy harvest and fat partitioning in youth

Journal of Clinical Endocrinology and Metabolism

Volumn 101, Issue 11, 2016, Pages 4367-4376

  Goffredo, Martina ^a,b   Mass, Kendra ^c   Parks, Elizabeth J ^d   Wagner, David A ^e   McClure, Emily Ann ^c   Graf, Joerg ^c   Savoye, Mary ^a   Pierpont, Bridget ^a   Cline, Gary ^a   Santoro, Nicola ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d University of Missouri   (United States)

^e METABOLIC SOLUTIONS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BUTYRIC ACID; CARBOHYDRATE; DEUTERIUM OXIDE; FRUCTOSE; PROPIONIC ACID; SHORT CHAIN FATTY ACID; VOLATILE FATTY ACID;

ACTINOBACTERIA; ARTICLE; BACTEROIDETES; BODY COMPOSITION; BODY FAT DISTRIBUTION; BODY MASS; CHILD; CONTROLLED STUDY; FEMALE; FIRMICUTES; HUMAN; IN VITRO STUDY; INTESTINE FLORA; INTRAPERITONEAL FAT; LIPOGENESIS; MAJOR CLINICAL STUDY; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; PRIORITY JOURNAL; SUBCUTANEOUS FAT; ABDOMINAL FAT; ADOLESCENT; CHILDHOOD OBESITY; FERMENTATION; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ABDOMINAL FAT; ACTINOBACTERIA; ADOLESCENT; BACTEROIDETES; BODY MASS INDEX; CHILD; FATTY ACIDS, VOLATILE; FEMALE; FERMENTATION; FIRMICUTES; GASTROINTESTINAL MICROBIOME; HUMANS; LIPOGENESIS; MALE; PEDIATRIC OBESITY;

EID: 84994908443     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2016-1797     Document Type: Article

References (48)

1. Boelsen-Robinson T, Gearon E, Peeters A. Incidence of childhood obesity in the United States. N Engl J Med. 2014;370:1659-1660.
2. de Onis M, Blossner M, Borghi E. Global prevalence and trends of overweight and obesity among preschool children. Am J Clin Nutr. 2010;92:1257-1264.
3. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59-65.
4. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242-249.
5. 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 U S A. 2004; 101:15718-15723.
6. Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J Physiol. 2009;587:4153-4158.
7. Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913-916.
8. Kuwahara. A Contributions of colonic short-chain Fatty Acid receptors in energy homeostasis. Front Endocrinol. 2014;5:144.
9. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc 2003;62:67-72.
10. Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol. 2014;121:91-119.
11. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027-1031.
12. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq illumina sequencing platform. Appl Environ Microb. 2013;79:5112-5120.
13. Santoro N, Caprio S, Pierpont B, Name MV, Savoye M, Parks EJ. 2015 Hepatic de novo lipogenesis in obese youth is modulated by a common variant in theGCKRgene. J Clin Endocrinol Metab. 2015; 100:E1125-E1132.
14. DeFilippo C, Cavalieri D, Di PaolaM,et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107: 14691-14696.
15. Schnorr SL, Candela M, Rampelli S, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5:3654.
16. Ou J, Carbonero F, Zoetendal EG, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98:111-120.
17. Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009; 106:2365-2370.
18. Furet JP, Kong LC, Tap J, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59: 3049-3057.
19. VerdamFJ, Fuentes S, de Jonge C, et al.Humanintestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity. 2013;21:E607-E615.
20. Tims S, Derom C, Jonkers DM, et al. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 2013;7:707-717.
21. Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathogen. 2012; 53:100-108.
22. Schwiertz A, Taras D, Schafer K, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010;18:190-195.
23. Everard A, Belzer C, Geurts L, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110:9066-9071.
24. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI. Glycan foraging in vivo by an intestineadapted bacterial symbiont. Science. 2005;307:1955-1959.
25. Brahe LK, Astrup A, Larsen LH. Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obesity Rev. 2013;14:950-959.
26. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28:1221-1227.
27. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325-2340.
28. Solinas G, Boren J, Dulloo AG. De novo lipogenesis in metabolic homeostasis: More friend than foe? Mol Metab. 2015;4:367-377.
29. Brown AJ, Goldsworthy SM, Barnes AA, et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003; 278:11312-11319.
30. Le Poul E, Loison C, Struyf S, et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem. 2003;278:25481-25489.
31. Xiong Y, Miyamoto N, Shibata K, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G proteincoupled receptor GPR41. Proc Natl Acad Sci U S A. 2004;101: 1045-1050.
32. Samuel BS, Shaito A, Motoike T, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A. 2008;105:16767-16772.
33. Yamashita H, Fujisawa K, Ito E, Idei S, Kawaguchi N, Kimoto M, Hiemori M, Tsuji H. Improvement of obesity and glucose tolerance by acetate in type 2 diabetic Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Biosci Biotechnol Biochem. 2007;71:1236-1243.
34. Zydowo MM, Smolenski RT, Swierczynski J. Acetate-induced changes of adenine nucleotide levels in rat liver. Metab Clin Exp. 1993;42:644-648.
35. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL, Tian H, Li Y. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology. 2008;149:4519-4526.
36. GaoZ, Yin J, Zhang J, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58:1509-1517.
37. Chambers ES, Viardot A, Psichas A, et al. 2014 Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut. 2015;64:1744-1754.
38. Chambers ES, Morrison DJ, Frost G. Control of appetite and energy intake by SCFA: what are the potential underlying mechanisms? Proc Nutr Soc. 2015;74:328-336.
39. Nordgaard I, Hansen BS, Mortensen PB. Importance of colonic support for energy absorption as small-bowel failure proceeds.AmJ Clin Nutr. 1996;64:222-231.
40. Nordgaard I, Hansen BS, Mortensen PB. Colon as a digestive organ in patients with short bowel. Lancet. 1994;343:373-376.
41. Kien CL, Kepner J, Grotjohn K, Ault K, McClead RE. Stable isotope model for estimating colonic acetate production in premature infants. Gastroenterology. 1992;102:1458-1466.
42. Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nature reviews. Endocrinology. 2015;11:577-591.
43. Byrne CS, Chambers ES, Morrison DJ, Frost G. The role of short chain fatty acids in appetite regulation and energy homeostasis. Int J Obesity. 2015;39:1331-1338.
44. Lattimer JM, Haub MD. Effects of dietary fiber and its components on metabolic health. Nutrients. 2010;2:1266-1289.
45. Baer DJ, Rumpler WV, Miles CW, Fahey GC, Jr. Dietary fiber decreases the metabolizable energy content and nutrient digestibility of mixed diets fed to humans. The Journal of nutrition 1997;127:579-586.
46. Isken F, Klaus S, Osterhoff M, Pfeiffer AF, Weickert MO. Effects of long-term soluble vs. insoluble dietary fiber intake on high-fat dietinduced obesity in C57BL/6J mice. J Nutr Biochem. 2010;21:278-284.
47. Latulippe ME, Skoog SM. Fructose malabsorption and intolerance: effects of fructose with and without simultaneous glucose ingestion. Crit Rev Food Sci Nutr. 2011;51:583-592.
48. Perry RJ, Peng L, Barry NA, et al. Acetate mediates a microbiomebrain-beta-cell axis to promote metabolic syndrome. Nature. 2016; 534:213-217.