Metabolomic Modeling to Monitor Host Responsiveness to Gut Microbiota Manipulation in the BTBRT+tf/j Mouse

Journal of Proteome Research

Volumn 15, Issue 4, 2016, Pages 1143-1150

  Klein, Matthias S ^a   Newell, Christopher ^b   Bomhof, Marc R ^a   Reimer, Raylene A ^a,b   Hittel, Dustin S ^b   Rho, Jong M ^a   Vogel, Hans J ^a,b   Shearer, Jane ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

communication; ketogenic diet; Metabolome; metabolomics; microbiota; modeling; mouse

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; BUTYRIC ACID; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; KETONE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SARCOSINE; TAURINE; GLUCOSE BLOOD LEVEL;

AKKERMANSIA MUCINIPHILA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENERGY; CHOW DIET; CLOSTRIDIUM; CLOSTRIDIUM COCCOIDES; CLOSTRIDIUM LEPTUM; CONTROLLED STUDY; DIET; ENERGY METABOLISM; GENOTYPE; GLUCOSE BLOOD LEVEL; HOST; INTESTINE FLORA; KETOGENIC DIET; LACTATE BLOOD LEVEL; LACTOBACILLUS; LIVER METABOLISM; METABOLOME; METABOLOMICS; MICROBE HOST INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BACTEROIDES; BIFIDOBACTERIUM; BIOLOGICAL MODEL; BLOOD; C57BL MOUSE; CECUM; ENTEROBACTERIACEAE; FECES; ISOLATION AND PURIFICATION; LIVER; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BACTEROIDES; BIFIDOBACTERIUM; BLOOD GLUCOSE; CECUM; CLOSTRIDIUM; ENTEROBACTERIACEAE; FECES; GASTROINTESTINAL MICROBIOME; GLUTAMINE; KETOGENIC DIET; KETONES; LACTOBACILLUS; LIVER; METABOLOME; METABOLOMICS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL;

EID: 84963657169     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b01025     Document Type: Article

References (35)

1. Bäckhed, F.; Ding, H.; Wang, T.; Hooper, L. V.; Koh, G. Y.; Nagy, A.; Semenkovich, C. F.; Gordon, J. I. The gut microbiota as an environmental factor that regulates fat storage Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 15718-15723 10.1073/pnas.0407076101
2. Bleau, C.; Karelis, A. D.; St-Pierre, D. H.; Lamontagne, L. Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low-grade inflammation and the development of obesity and diabetes Diabetes/Metab. Res. Rev. 2015, 31, 545-51 10.1002/dmrr.2617
3. MacFabe, D. F. Enteric short-chain fatty acids: microbial messengers of metabolism, mitochondria, and mind: implications in autism spectrum disorders Microb. Ecol. Health Dis. 2015, 26, 28177 10.3402/mehd.v26.28177
4. Frank, D. N.; St. Amand, A. L.; Feldman, R. A.; Boedeker, E. C.; Harpaz, N.; Pace, N. R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 13780-13785 10.1073/pnas.0706625104
5. Karlsson, F. H.; Fåk, F.; Nookaew, I.; Tremaroli, V.; Fagerberg, B.; Petranovic, D.; Bäckhed, F.; Nielsen, J. Symptomatic atherosclerosis is associated with an altered gut metagenome Nat. Commun. 2012, 3, 1245 10.1038/ncomms2266
6. Tremaroli, V.; Bäckhed, F. Functional interactions between the gut microbiota and host metabolism Nature 2012, 489, 242-249 10.1038/nature11552
7. Thomas, C. M.; Versalovic, J. Probiotics-host communication: Modulation of signaling pathways in the intestine Gut Microbes 2010, 1, 148-163 10.4161/gmic.1.3.11712
8. Wikoff, W. R.; Anfora, A. T.; Liu, J.; Schultz, P. G.; Lesley, S. A.; Peters, E. C.; Siuzdak, G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 3698-3703 10.1073/pnas.0812874106
9. Antunes, L. C. M.; Finlay, B. B. A comparative analysis of the effect of antibiotic treatment and enteric infection on intestinal homeostasis Gut Microbes 2011, 2, 105-108 10.4161/gmic.2.2.15610
10. Dunn, L.; Suckling, J. Studies of the genetic variability in wild populations of house mice. I. Analysis of seven alleles at locus T Genetics 1956, 41, 344
11. Karunakaran, S.; Manji, A.; Yan, C. S.; Wu, Z.-J. J.; Clee, S. M. Moo1 obesity quantitative trait locus in BTBR T+ Itpr3tf/J mice increases food intake Physiol. Genomics 2013, 45, 191-199 10.1152/physiolgenomics.00159.2012
12. Stoehr, J. P.; Nadler, S. T.; Schueler, K. L.; Rabaglia, M. E.; Yandell, B. S.; Metz, S. A.; Attie, A. D. Genetic obesity unmasks nonlinear interactions between murine type 2 diabetes susceptibility loci Diabetes 2000, 49, 1946-1954 10.2337/diabetes.49.11.1946
13. Whitehead, G. S.; Walker, J. K. L.; Berman, K. G.; Foster, W. M.; Schwartz, D. A. Allergen-induced airway disease is mouse strain dependent Am. J. Physiol Lung Cell Mol. Physiol 2003, 285, L32-L42 10.1152/ajplung.00390.2002
14. Ruskin, D. N.; Svedova, J.; Cote, J. L.; Sandau, U.; Rho, J. M.; Kawamura, M., Jr; Boison, D.; Masino, S. A. Ketogenic diet improves core symptoms of autism in BTBR mice PLoS One 2013, 8, e65021 10.1371/journal.pone.0065021
15. Bomhof, M. R.; Saha, D. C.; Reid, D. T.; Paul, H. A.; Reimer, R. A. Combined effects of oligofructose and Bifidobacterium animalis on gut microbiota and glycemia in obese rats Obesity 2014, 22, 763-771 10.1002/oby.20632
16. Stoddard, S. F.; Smith, B. J.; Hein, R.; Roller, B. R. K.; Schmidt, T. M. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development Nucleic Acids Res. 2015, 43, D593-D598 10.1093/nar/gku1201
17. Klein, M. S.; Buttchereit, N.; Miemczyk, S. P.; Immervoll, A.-K.; Louis, C.; Wiedemann, S.; Junge, W.; Thaller, G.; Oefner, P. J.; Gronwald, W. NMR metabolomic analysis of dairy cows reveals milk glycerophosphocholine to phosphocholine ratio as prognostic biomarker for risk of ketosis J. Proteome Res. 2012, 11, 1373-1381 10.1021/pr201017n
18. Wu, H.; Southam, A. D.; Hines, A.; Viant, M. R. High-throughput tissue extraction protocol for NMR- and MS-based metabolomics Anal. Biochem. 2008, 372, 204-212 10.1016/j.ab.2007.10.002
19. Thomas, A.; Stevens, A. P.; Klein, M. S.; Hellerbrand, C.; Dettmer, K.; Gronwald, W.; Oefner, P. J.; Reinders, J. Early changes in the liver-soluble proteome from mice fed a nonalcoholic steatohepatitis inducing diet Proteomics 2012, 12, 1437-1451 10.1002/pmic.201100628
20. Gronwald, W.; Klein, M. S.; Kaspar, H.; Fagerer, S. R.; Nürnberger, N.; Dettmer, K.; Bertsch, T.; Oefner, P. J. Urinary metabolite quantification employing 2D NMR spectroscopy Anal. Chem. 2008, 80, 9288-9297 10.1021/ac801627c
21. Klein, M. S.; Almstetter, M. F.; Schlamberger, G.; Nürnberger, N.; Dettmer, K.; Oefner, P. J.; Meyer, H. H. D.; Wiedemann, S.; Gronwald, W. Nuclear magnetic resonance and mass spectrometry-based milk metabolomics in dairy cows during early and late lactation J. Dairy Sci. 2010, 93, 1539-1550 10.3168/jds.2009-2563
22. Technical Note 17: Guidelines for the validation and verification of quantitative and qualitative test methods; National Association of Testing Authorities: Australia, 2013.
23. Hausman, J. A. Specification tests in econometrics Econometrica 1978, 46, 1251-1271 10.2307/1913827
24. Randal Bollinger, R.; Barbas, A. S.; Bush, E. L.; Lin, S. S.; Parker, W. Biofilms in the large bowel suggest an apparent function of the human vermiform appendix J. Theor. Biol. 2007, 249, 826-831 10.1016/j.jtbi.2007.08.032
25. Kossoff, E. H.; Rho, J. M. Ketogenic diets: evidence for short- and long-term efficacy Neurotherapeutics 2009, 6, 406-414 10.1016/j.nurt.2009.01.005
26. Donohoe, D. R.; Garge, N.; Zhang, X.; Sun, W.; OConnell, T. M.; Bunger, M. K.; Bultman, S. J. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon Cell Metab. 2011, 13, 517-526 10.1016/j.cmet.2011.02.018
27. Dupuis, N.; Curatolo, N.; Benoist, J.-F.; Auvin, S. Ketogenic diet exhibits anti-inflammatory properties Epilepsia 2015, 56, e95-e98 10.1111/epi.13038
28. Sullivan, P. G.; Rippy, N. A.; Dorenbos, K.; Concepcion, R. C.; Agarwal, A. K.; Rho, J. M. The ketogenic diet increases mitochondrial uncoupling protein levels and activity Ann. Neurol. 2004, 55, 576-580 10.1002/ana.20062
29. Sokol, H.; Pigneur, B.; Watterlot, L.; Lakhdari, O.; Bermúdez-Humarán, L. G.; Gratadoux, J.-J.; Blugeon, S.; Bridonneau, C.; Furet, J.-P.; Corthier, G.; Grangette, C.; Vasquez, N.; Pochart, P.; Trugnan, G.; Thomas, G.; Blottière, H. M.; Doré, J.; Marteau, P.; Seksik, P.; Langella, P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 16731-16736 10.1073/pnas.0804812105
30. Griffiths, E. A.; Duffy, L. C.; Schanbacher, F. L.; Qiao, H.; Dryja, D.; Leavens, A.; Rossman, J.; Rich, G.; Dirienzo, D.; Ogra, P. L. In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice Dig. Dis. Sci. 2004, 49, 579-589 10.1023/B:DDAS.0000026302.92898.ae
31. Sengupta, R.; Altermann, E.; Anderson, R. C.; McNabb, W. C.; Moughan, P. J.; Roy, N. C. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract Mediators Inflammation 2013, 2013, 237921 10.1155/2013/237921
32. Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J. P.; Druart, C.; Bindels, L. B.; Guiot, Y.; Derrien, M.; Muccioli, G. G.; Delzenne, N. M.; de Vos, W. M.; Cani, P. D. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 9066-9071 10.1073/pnas.1219451110
33. Tsai, G.; Lane, H.-Y.; Yang, P.; Chong, M.-Y.; Lange, N. Glycine transporter I inhibitor, N-methylglycine (sarcosine), added to antipsychotics for the treatment of schizophrenia Biol. Psychiatry 2004, 55, 452-456 10.1016/j.biopsych.2003.09.012
34. Sreekumar, A.; Poisson, L. M.; Rajendiran, T. M.; Khan, A. P.; Cao, Q.; Yu, J.; Laxman, B.; Mehra, R.; Lonigro, R. J.; Li, Y.; Nyati, M. K.; Ahsan, A.; Kalyana-Sundaram, S.; Han, B.; Cao, X.; Byun, J.; Omenn, G. S.; Ghosh, D.; Pennathur, S.; Alexander, D. C.; Berger, A.; Shuster, J. R.; Wei, J. T.; Varambally, S.; Beecher, C.; Chinnaiyan, A. M. Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression Nature 2009, 457, 910-914 10.1038/nature07762
35. Gerard, P. Metabolism of cholesterol and bile acids by the gut microbiota Pathogens 2014, 3, 14-24 10.3390/pathogens3010014