Gut microbiota directs PPARγ-driven reprogramming of the liver circadian clock by nutritional challenge

EMBO Reports

Volumn 17, Issue 9, 2016, Pages 1292-1303

  Murakami, Mari ^a   Tognini, Paola ^a   Liu, Yu ^a   Eckel Mahan, Kristin L ^a,b   Baldi, Pierre ^a   Sassone Corsi, Paolo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

circadian clock; liver; microbiota; PPAR

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A DESATURASE 1; AMPICILLIN; BILE ACID; CHOLESTEROL; D BOX BINDING PROTEIN; FARNESOID X RECEPTOR; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 6; GLUCOSE; LIPID; METRONIDAZOLE; NEOMYCIN; NUCLEAR RECEPTOR NR1D1; OLEIC ACID; ORGANIC SOLUTE TRANSPORTER ALPHA; ORGANIC SOLUTE TRANSPORTER BETA; PALMITOLEIC ACID; PALMITOYL COENZYME A HYDROLASE; PER2 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOLIPID TRANSFER PROTEIN; PROTEIN; PYRUVATE CARBOXYLASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION FACTOR ARNTL; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; VANCOMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DYSBIOSIS; FECAL MICROBIOTA TRANSPLANTATION; INTESTINE FLORA; LIPID DIET; LIVER METABOLISM; MALE; MICROBIAL COMMUNITY; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; NUTRITIONAL STATUS; OBESITY; OSCILLATION; PRIORITY JOURNAL;

EID: 84985038266     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201642463     Document Type: Article

References (70)

1. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330: 1349–1354
2. Eckel-Mahan K, Sassone-Corsi P (2013) Metabolism and the circadian clock converge. Physiol Rev 93: 107–135
3. Balsalobre A, Damiola F, Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93: 929–937
4. Giebultowicz JM, Stanewsky R, Hall JC, Hege DM (2000) Transplanted Drosophila excretory tubules maintain circadian clock cycling out of phase with the host. Curr Biol 10: 107–110
5. Krishnan B, Dryer SE, Hardin PE (1999) Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400: 375–378
6. Schibler U, Sassone-Corsi P (2002) A web of circadian pacemakers. Cell 111: 919–922
7. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291: 490–493
8. Whitmore D, Foulkes NS, Strahle U, Sassone-Corsi P (1998) Zebrafish clock rhythmic expression reveals independent peripheral circadian oscillators. Nat Neurosci 1: 701–707
9. Crane BR, Young MW (2014) Interactive features of proteins composing eukaryotic circadian clocks. Annu Rev Biochem 83: 191–219
10. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96: 271–290
11. Mukherji A, Kobiita A, Damara M, Misra N, Meziane H, Champy MF, Chambon P (2015) Shifting eating to the circadian rest phase misaligns the peripheral clocks with the master SCN clock and leads to a metabolic syndrome. Proc Natl Acad Sci USA 112: E6691–E6698
12. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH et al (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466: 627–631
13. Paschos GK, Ibrahim S, Song WL, Kunieda T, Grant G, Reyes TM, Bradfield CA, Vaughan CH, Eiden M, Masoodi M et al (2012) Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med 18: 1768–1777
14. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR et al (2005) Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308: 1043–1045
15. Sahar S, Sassone-Corsi P (2009) Metabolism and cancer: the circadian clock connection. Nat Rev Cancer 9: 886–896
16. Asher G, Sassone-Corsi P (2015) Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161: 84–92
17. Hatori M, Vollmers C, Zarrinpar A, DiTacchio L, Bushong EA, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JA et al (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15: 848–860
18. Kohsaka A, Laposky AD, Ramsey KM, Estrada C, Joshu C, Kobayashi Y, Turek FW, Bass J (2007) High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 6: 414–421
19. Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, Dilag-Penilla SA, Dyar KA, Baldi P, Sassone-Corsi P (2013) Reprogramming of the circadian clock by nutritional challenge. Cell 155: 1464–1478
20. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1: 6ra14
21. Carmody RN, Gerber GK, Luevano JM Jr, Gatti DM, Somes L, Svenson KL, Turnbaugh PJ (2015) Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17: 72–84
22. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559–563
23. Wu M, McNulty NP, Rodionov DA, Khoroshkin MS, Griffin NW, Cheng J, Latreille P, Kerstetter RA, Terrapon N, Henrissat B et al (2015) Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 350: aac5992
24. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3: 213–223
25. Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, Pierre JF, Heneghan AF, Nadimpalli A, Hubert N et al (2015) Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17: 681–689
26. Montagner A, Korecka A, Polizzi A, Lippi Y, Blum Y, Canlet C, Tremblay-Franco M, Gautier-Stein A, Burcelin R, Yen YC et al (2016) Hepatic circadian clock oscillators and nuclear receptors integrate microbiome-derived signals. Sci Rep 6: 20127
27. Garidou L, Pomie C, Klopp P, Waget A, Charpentier J, Aloulou M, Giry A, Serino M, Stenman L, Lahtinen S et al (2015) The gut microbiota regulates intestinal CD4 T cells expressing RORgammat and controls metabolic disease. Cell Metab 22: 100–112
28. Selkrig J, Wong P, Zhang X, Pettersson S (2014) Metabolic tinkering by the gut microbiome: implications for brain development and function. Gut Microbes 5: 369–380
29. Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK (2014) Specialized metabolites from the microbiome in health and disease. Cell Metab 20: 719–730
30. Ohnmacht C, Park JH, Cording S, Wing JB, Atarashi K, Obata Y, Gaboriau-Routhiau V, Marques R, Dulauroy S, Fedoseeva M et al (2015) Mucosal Immunology. The microbiota regulates type 2 immunity through RORgammat(+) T cells. Science 349: 989–993
31. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, Knight R, Ahima RS, Bushman F, Wu GD (2009) High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137: 1716–1724.e2
32. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE et al (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106: 2365–2370
33. Clarke SF, Murphy EF, Nilaweera K, Ross PR, Shanahan F, O'Toole PW, Cotter PD (2012) The gut microbiota and its relationship to diet and obesity: new insights. Gut Microbes 3: 186–202
34. Li F, Jiang C, Krausz KW, Li Y, Albert I, Hao H, Fabre KM, Mitchell JB, Patterson AD, Gonzalez FJ (2013) Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat Commun 4: 2384
35. Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, Angelin B, Hyotylainen T, Oresic M, Backhed F (2013) Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 17: 225–235
36. Parseus A, Sommer N, Sommer F, Caesar R, Molinaro A, Stahlman M, Greiner TU, Perkins R, Backhed F (2016) Microbiota-induced obesity requires farnesoid X receptor. Gut doi:10.1136/gutjnl-2015-310283
37. Reinke H, Asher G (2016) Circadian clock control of liver metabolic functions. Gastroenterology 150: 574–580
38. Tamaru T, Hirayama J, Isojima Y, Nagai K, Norioka S, Takamatsu K, Sassone-Corsi P (2009) CK2alpha phosphorylates BMAL1 to regulate the mammalian clock. Nat Struct Mol Biol 16: 446–448
39. Sahar S, Zocchi L, Kinoshita C, Borrelli E, Sassone-Corsi P (2010) Regulation of BMAL1 protein stability and circadian function by GSK3beta-mediated phosphorylation. PLoS ONE 5: e8561
40. Schadinger SE, Bucher NL, Schreiber BM, Farmer SR (2005) PPARgamma2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. Am J Physiol Endocrinol Metab 288: E1195–E1205
41. Uno K, Katagiri H, Yamada T, Ishigaki Y, Ogihara T, Imai J, Hasegawa Y, Gao J, Kaneko K, Iwasaki H et al (2006) Neuronal pathway from the liver modulates energy expenditure and systemic insulin sensitivity. Science 312: 1656–1659
42. Nielsen R, Pedersen TA, Hagenbeek D, Moulos P, Siersbaek R, Megens E, Denissov S, Borgesen M, Francoijs KJ, Mandrup S et al (2008) Genome-wide profiling of PPARgamma:RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev 22: 2953–2967
43. Siersbaek MS, Loft A, Aagaard MM, Nielsen R, Schmidt SF, Petrovic N, Nedergaard J, Mandrup S (2012) Genome-wide profiling of peroxisome proliferator-activated receptor gamma in primary epididymal, inguinal, and brown adipocytes reveals depot-selective binding correlated with gene expression. Mol Cell Biol 32: 3452–3463
44. Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, Devchand P, Wahli W, Willson TM, Lenhard JM et al (1997) Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc Natl Acad Sci USA 94: 4318–4323
45. Sauma L, Stenkula KG, Kjolhede P, Stralfors P, Soderstrom M, Nystrom FH (2006) PPAR-gamma response element activity in intact primary human adipocytes: effects of fatty acids. Nutrition 22: 60–68
46. Matsusue K, Kusakabe T, Noguchi T, Takiguchi S, Suzuki T, Yamano S, Gonzalez FJ (2008) Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab 7: 302–311
47. Xu X, Park JG, So JS, Lee AH (2015) Transcriptional activation of Fsp27 by the liver-enriched transcription factor CREBH promotes lipid droplet growth and hepatic steatosis. Hepatology 61: 857–869
48. Moffat C, Bhatia L, Nguyen T, Lynch P, Wang M, Wang D, Ilkayeva OR, Han X, Hirschey MD, Claypool SM et al (2014) Acyl-CoA thioesterase-2 facilitates mitochondrial fatty acid oxidation in the liver. J Lipid Res 55: 2458–2470
49. Yazdanyar A, Jiang XC (2012) Liver phospholipid transfer protein (PLTP) expression with a PLTP-null background promotes very low-density lipoprotein production in mice. Hepatology 56: 576–584
50. Leesnitzer LM, Parks DJ, Bledsoe RK, Cobb JE, Collins JL, Consler TG, Davis RG, Hull-Ryde EA, Lenhard JM, Patel L et al (2002) Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry 41: 6640–6650
51. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229–241
52. Mukherji A, Kobiita A, Ye T, Chambon P (2013) Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153: 812–827
53. Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abramson L, Katz MN, Korem T, Zmora N et al (2014) Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159: 514–529
54. Voigt RM, Forsyth CB, Green SJ, Mutlu E, Engen P, Vitaterna MH, Turek FW, Keshavarzian A (2014) Circadian disorganization alters intestinal microbiota. PLoS ONE 9: e97500
55. Zarrinpar A, Chaix A, Yooseph S, Panda S (2014) Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab 20: 1006–1017
56. Yang X, Downes M, Yu RT, Bookout AL, He W, Straume M, Mangelsdorf DJ, Evans RM (2006) Nuclear receptor expression links the circadian clock to metabolism. Cell 126: 801–810
57. Eckel-Mahan KL, Patel VR, Mohney RP, Vignola KS, Baldi P, Sassone-Corsi P (2012) Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci USA 109: 5541–5546
58. Sahar S, Sassone-Corsi P (2012) Regulation of metabolism: the circadian clock dictates the time. Trends Endocrinol Metab 23: 1–8
59. Tontonoz P, Spiegelman BM (2008) Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77: 289–312
60. Green CB, Douris N, Kojima S, Strayer CA, Fogerty J, Lourim D, Keller SR, Besharse JC (2007) Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc Natl Acad Sci USA 104: 9888–9893
61. Grimaldi B, Bellet MM, Katada S, Astarita G, Hirayama J, Amin RH, Granneman JG, Piomelli D, Leff T, Sassone-Corsi P (2010) PER2 controls lipid metabolism by direct regulation of PPARgamma. Cell Metab 12: 509–520
62. Kawai M, Rosen CJ (2010) PPARgamma: a circadian transcription factor in adipogenesis and osteogenesis. Nat Rev Endocrinol 6: 629–636
63. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101: 15718–15723
64. Singh V, Chassaing B, Zhang L, San Yeoh B, Xiao X, Kumar M, Baker MT, Cai J, Walker R, Borkowski K et al (2015) Microbiota-dependent hepatic lipogenesis mediated by stearoyl CoA desaturase 1 (SCD1) promotes metabolic syndrome in TLR5-deficient mice. Cell Metab 22: 983–996
65. den Besten G, Lange K, Havinga R, van Dijk TH, Gerding A, van Eunen K, Muller M, Groen AK, Hooiveld GJ, Bakker BM et al (2013) Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am J Physiol Gastrointest Liver Physiol 305: G900–G910
66. den Besten G, Bleeker A, Gerding A, van Eunen K, Havinga R, van Dijk TH, Oosterveer MH, Jonker JW, Groen AK, Reijngoud DJ et al (2015) Short-chain fatty acids protect against high-fat diet-induced obesity via a PPARgamma-dependent switch from lipogenesis to fat oxidation. Diabetes 64: 2398–2408
67. Luo Y, Chen GL, Hannemann N, Ipseiz N, Kronke G, Bauerle T, Munos L, Wirtz S, Schett G, Bozec A (2015) Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metab 22: 886–894
68. Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509–519
69. Kayala MA, Baldi P (2012) Cyber-T web server: differential analysis of high-throughput data. Nucleic Acids Res 40: W553–W559
70. Carmona-Saez P, Chagoyen M, Tirado F, Carazo JM, Pascual-Montano A (2007) GENECODIS: a web-based tool for finding significant concurrent annotations in gene lists. Genome Biol 8: R3