Gut Microbiota and the Gut-Brain Axis: New Insights in the Pathophysiology of Metabolic Syndrome

Psychosomatic Medicine

Volumn 79, Issue 8, 2017, Pages 874-879

  De Clercq, Nicolien C ^a   Frissen, Myrthe N ^a   Groen, Albert K ^a,c,d   Nieuwdorp, Max ^a,b,d  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

gut brain axis; metabolic syndrome; microbiome

Indexed keywords

CHOLECYSTOKININ; GASTROINTESTINAL HORMONE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 2; PEPTIDE YY; SHORT CHAIN FATTY ACID;

BRAIN FUNCTION; CALORIC INTAKE; ENERGY EXPENDITURE; GUT BRAIN AXIS; HORMONE ACTION; HORMONE RELEASE; HUMAN; INDIVIDUALITY; INTESTINE FLORA; INTESTINE TRANSIT TIME; METABOLIC DISORDER; METABOLIC SYNDROME X; MICROBIAL DIVERSITY; NONHUMAN; OBESITY; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; ANIMAL; BRAIN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; GASTROINTESTINAL MICROBIOME; HUMANS; METABOLIC SYNDROME; SIGNAL TRANSDUCTION;

EID: 85019722589     PISSN: 00333174     EISSN: 15347796     Source Type: Journal    
DOI: 10.1097/PSY.0000000000000495     Document Type: Review

References (64)

1. Duca FA, Lam TK. Gut microbiota, nutrient sensing and energy balance. Diabetes Obes Metab 2014;16:68-76
2. Wang YC, McPherson K, Marsh T, Gortmaker SL, Brown M. Health and economic burden of the projected obesity trends in the USA and the UK. Lancet 2011;378:815-25
3. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009;9:313-23
4. Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012;489:242-9
5. Bäckhed 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;101:15718-23
6. 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;444:1027-31
7. Kairupan TS, Amitani H, Cheng KC, Runtuwene J, Asakawa A, Inui A. Role of gastrointestinal hormones in feeding behavior and obesity treatment. J Gastroenterol 2016;51:93-103
8. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012;13:701-12
9. Sender R, Fuchs S,Milo R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 2016;164:337-40
10. Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, Fouhy F, Clarke SF, O'Toole PW, Quigley EM, Stanton C, Ross PR, O'Doherty RM, Shanahan F. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 2010;59:1635-42
11. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005;102:11070-5
12. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. A core gut microbiome in obese and lean twins. Nature 2009;457:480-4
13. Arora T, Bäckhed F. The gut microbiota and metabolic disease: current understanding and future perspectives. J Intern Med 2016;280:339-49
14. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, Peng Y, Zhang D, Jie Z,WuW, Qin Y, XueW, Li J, Han L, Lu D,Wu P, Dai Y, Sun X, Li Z, Tang A, Zhong S, Li X, Chen W, Xu R, Wang M, Feng Q, Gong M, Yu J, Zhang Y, Zhang M, Hansen T, Sanchez G, Raes J, Falony G, Okuda S, Almeida M, LeChatelier E, Renault P, Pons N, Batto JM, Zhang Z, Chen H, Yang R, ZhengW, Li S, Yang H,Wang J, Ehrlich SD, Nielsen R, Pedersen O, Kristiansen K, Wang J. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012;490:55-60
15. Cani PD, NeyrinckAM, Fava F, Knauf C, Burcelin RG, TuohyKM, Gibson GR, Delzenne NM. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007;50:2374-83
16. Tremaroli V, Kovatcheva-Datchary P, Bäckhed F. A role for the gut microbiota in energy harvesting? Gut 2010;59:1589-90
17. Kong LC, Tap J, Aron-Wisnewsky J, Pelloux V, Basdevant A, Bouillot JL, Zucker JD, Doré J, Clément K. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr 2013;98:16-24
18. Liou AP, Paziuk M, Luevano JM Jr., Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med 2013;5:178ra41
19. Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol 2015;11:577-91
20. Cummings JH. Short chain fatty acids in the human colon. Gut 1981;22:763-79
21. Bakker GJ, Zhao J, Herrema H,Nieuwdorp M. Gutmicrobiota and energy expenditure in health and obesity. J Clin Gastroenterol 2015;49:S13-9
22. Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, Vos WM, Hoekstra JB, NieuwdorpM. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012;143:913-6. e7
23. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, CefaluWT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure inmice. Diabetes 2009;58:1509-17
24. Yadav H, Lee JH, Lloyd J, Walter P, Rane SG. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J Biol Chem 2013; 288:25088-97
25. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, DuchamptA, Bäckhed F,MithieuxG.Microbiota-generatedmetabolites promote metabolic benefits via gut-brain neural circuits. Cell 2014;156:84-96
26. Roberge JN, Brubaker PL. Regulation of Intestinal Proglucagon-Derived Peptide Secretion by Glucose-Dependent Insulinotropic Peptide in a Novel Enteroendocrine Loop. Endocrinology 1993;133:233-40
27. Theodorakis MJ, Carlson O, Michopoulos S,DoyleME, Juhaszova M, PetrakiK, Egan JM. Human duodenal enteroendocrine cells: source of both incretin peptides, GLP-1 and GIP. Am J Physiol Endocrinol Metab 2006;290:E550-9
28. Zhou J,Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, Danna SC, Tripathy S, Hegsted M, Keenan MJ. Dietary resistant starch upregulates total GLP-1 and PYYin a sustained day-longmanner through fermentation in rodents. Am J Physiol Endocrinol Metab 2008;295:1160-6
29. Psichas A, Sleeth ML, Murphy KG, Brooks L, Bewick GA, Hanyaloglu AC, Ghatei MA, Bloom SR, 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) 2015;39:424-9
30. Reinehr T, Roth CL. The gut sensor as regulator of body weight. Endocrine 2015; 49:35-50
31. Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterol Motil 2011;23:187-92
32. Bercik P, Denou E, Collins J, JacksonW, Lu J, Jury J, Deng Y, Blennerhassett P, Macri J,McCoy KD, Verdu EF, Collins SM. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011;141:599-609
33. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest 2015;125:926-38
34. Loper HB, La Sala M, Dotson C, Steinle N. Taste perception, associated hormonal modulation, and nutrient intake. Nutr Rev 2015;73:83-91
35. Berthoud HR, Earle T, Zheng H, Patterson LM, Phifer C. Food-related gastrointestinal signals activate caudal brainstem neurons expressing both NMDA and AMPA receptors. Brain Res 2001;915:143-54
36. Ahlman H. N. The gut as the largest endocrine organ in the body. Ann Oncol 2001;12:S63-8
37. Bewick GA, Dhillo WS, Darch SJ, Murphy KG, Gardiner JV, Jethwa PH, Kong WM, Ghatei MA, Bloom SR. Hypothalamic cocaine-and amphetamine-regulated transcript (CART) and agouti-related protein (AgRP) neurons coexpress the NOP1 receptor and nociceptin alters CART and AgRP release. Endocrinology 2005;146:3526-34
38. Bauer PV, Hamr SC, Duca FA. Regulation of energy balance by a gut-brain axis and involvement of the gut microbiota. Cell Mol Life Sci 2016;73:737-55
39. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz M. Central nervous system control of food intake and body weight. Nature 2006;443:289-95
40. Garin MC, Burns CM, Kaul S, Cappola AR. Clinical review: the human experience with ghrelin administration. J Clin Endocrinol Metab 2013;98: 1826-37
41. Wren AM, Small CJ,Ward HL, Murphy KG, Dakin CL, Taheri S, Kennedy AR, Roberts GH, Morgan DG, GhateiMA, Bloom SR. The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 2000;141:4325-8
42. World Health Organization. Obesity and Overweight [fact sheet]. Available at: http://www.who.int/mediacentre/factsheets/fs311/en/. Accessed January 5, 2017
43. Cummings DE. Ghrelin and the short-and long-term regulation of appetite and body weight. Physiol Behav 2006;89:71-84
44. Blom WA, Lluch A, Vinoy S, Stafleu A, van den Berg R, Holst JJ, Kok FJ, Hendriks HF. Effects of gastric emptying on the postprandial ghrelin response. Am J Physiol Endocrinol Metab 2006;290:389-95
45. Alamuddin N, Vetter ML, Ahima RS, Hesson L, Ritter S, Minnick A, Faulconbridge LF, Allison KC, Sarwer DB, Chittams J, Williams NN, Hayes MR, Loughead JW, Gur R,Wadden TA. Changes in fasting and prandial gut and adiposity hormones following vertical sleeve gastrectomy or Roux-en-Ygastric bypass: an 18-month prospective study. Obes Surg 2017;27:1563-72
46. Ledderose C, Kreth S, Beiras-Fernandez A. Ghrelin, a novel peptide hormone in the regulation of energy balance and cardiovascular function. Recent Pat Endocr Metab Immune Drug Discov 2011;5:1-6
47. Queipo-Ortuño MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, Casanueva F, Tinahones FJ. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One 2013;8:e0065465
48. Freeland KR, Wolever TM. Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, peptide YY, ghrelin, adiponectin and tumour necrosis factor-alpha. Br J Nutr 2010;103:460-6
49. Lartigue G, Serre CB, Raybould HE. Vagal afferent neurons in high fat diet-induced obesity; intestinal microflora, gut inflammation and cholecystokinin. Physiol Behav 2011;105:100-5
50. Mitchell VA, Jeong HJ, Drew GM, Vaughan CW. Cholecystokinin exerts an effect via the endocannabinoid systemto inhibitGABAergic transmission inmidbrain periaqueductal gray. Neuropsychopharmacology 2011;36:1801-10
51. Chandra R, Liddle RA. Cholecystokinin. Curr Opin Endocrinol Diabetes Obes 2007;14:63-7
52. Grider JR. Symposium: New Research in Physiology of Cholecystokinin: Nutrition Issues Role of Cholecystokinin in the Regulation of Gastrointestinal Motility1. J Nutr 1994;124(8 Suppl):1334-9
53. Raybould HE. Mechanisms of CCK signaling from gut to brain. Curr Opin Pharmacol 2007;7:570-4
54. Federico A, DallioM, Tolone S, Gravina AG, Patrone V, RomanoM, Tuccillo C, Mozzillo AL, Amoroso V, Misso G,Morelli L, Docimo L, Loguercio C. Gastrointestinal hormones, intestinal microbiota and metabolic homeostasis in obese patients: effect of bariatric surgery. In Vivo 2016;30:321-30
55. Dubé PE, Brubaker PL. Nutrient, neural and endocrine control of glucagon-like peptide secretion. Horm Metab Res 2004;36:755-60
56. Näslund E, Gutniak M, Skogar S, Rössner S, Hellström PM. Glucagon-like peptide 1 increases the period of postprandial satiety and slows gastric emptying in obese men. Am J Clin Nutr 1998;68:525-30
57. Turton MD, O'Shea D, Gunn I, Beak SA, Edwards CM, Meeran K, Choi SJ, Taylor GM, Heath MM, Lambert PD, Wilding JP, Smith DM, Ghatei MA, Herbert J, Bloom SR. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 1996;379:69-72
58. Baggio LL, Drucker DJ. Biology of Incretins: GLP-1 and GIP. Gastroenterology 2007;132:2131-57
59. Dixon JB, Lambert EA, Lambert GW. Neuroendocrine adaptations to bariatric surgery. Mol Cell Endocrinol 2015;418(pt 2):143-52
60. Breton J, TennouneN, Lucas N, Francois M, Legrand R, Jacquemot J, GoichonA, Guérin C, Peltier J, Pestel-Caron M, Chan P, Vaudry D, Rego JC, Liénard F, Pénicaud L, Fioramonti X, Ebenezer IS, Hökfelt T, Déchelotte P, Fetissov SO. Gut commensal E. coli proteins activate host satiety pathways following nutrient-induced bacterial growth. Cell Metab 2016;23:324-34
61. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, Murdock PR, Holder JC, Marshall FH, Szekeres PG, Wilson S, Ignar DM, Foord SM, Wise A, Dowell SJ. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 2003;278:11312-9
62. Karaki S,Mitsui R, HayashiH,Kato I, SugiyaH, Iwanaga T, Furness JB, Kuwahara A. Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res 2006;324:353-60
63. Kim MH, Kang SG, Park JH, Yanagisawa M, Kim CH. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 2013;145:396-406. e10
64. Wichmann A, Allahyar A, Greiner TU, Plovier H, Lundén GO, Larsson T, Drucker DJ, DelzenneNM, Cani PD, Bäckhed F.Microbial modulation of energy availability in the colon regulates intestinal transit. Cell Host Microbe 2013;14: 582-90