#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Diet modulates cecum bacterial diversity and physiological phenotypes across the BXD mouse genetic reference population


Autoři: Maria Elisa Perez-Munoz aff001;  Autumn M. McKnite aff003;  Evan G. Williams aff004;  Johan Auwerx aff004;  Robert W. Williams aff005;  Daniel A. Peterson aff001;  Daniel C. Ciobanu aff003
Působiště autorů: Department of Pathology, John Hopkins University School of Medicine, Baltimore, Maryland, United States of America aff001;  Department of Agriculture, Food and Nutritional Sciences, University of Alberta, Edmonton, Alberta, Canada aff002;  Animal Science Department, University of Nebraska, Lincoln, Nebraska, United States of America aff003;  Laboratory for Integrative Systems Physiology, Ecole Polytechnique Fédérale de Lausanne, Switzerland aff004;  Department of Genetics, Genomics and Informatics, University of Tennessee Health Science Center, Memphis, Tennessee, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224100

Souhrn

The BXD family has become one of the preeminent genetic reference populations to understand the genetic and environmental control of phenotypic variation. Here we evaluate the responses to different levels of fat in the diet using both chow diet (CD, 13–18% fat) and a high-fat diet (HFD, 45–60% fat). We studied cohorts of BXD strains, both inbred parents C57BL/6J and DBA/2J (commonly known as B6 and D2, respectively), as well as B6D2 and D2B6 reciprocal F1 hybrids. The comparative impact of genetic and dietary factors was analyzed by profiling a range of phenotypes, most prominently their cecum bacterial composition. The parents of the BXDs and F1 hybrids express limited differences in terms of weight and body fat gain on CD. In contrast, the strain differences on HFD are substantial for percent body fat, with DBA/2J accumulating 12.5% more fat than C57BL/6J (P < 0.0001). The F1 hybrids born to DBA/2J dams (D2B6F1) have 10.6% more body fat (P < 0.001) than those born to C57BL/6J dams. Sequence analysis of the cecum microbiota reveals important differences in bacterial composition among BXD family members with a substantial shift in composition caused by HFD. Relative to CD, the HFD induces a decline in diversity at the phylum level with a substantial increase in Firmicutes (+13.8%) and a reduction in Actinobacteria (-7.9%). In the majority of BXD strains, the HFD also increases cecal sIgA (P < 0.0001)—an important component of the adaptive immunity response against microbial pathogens. Host genetics modulates variation in cecum bacterial composition at the genus level in CD, with significant quantitative trait loci (QTLs) for Oscillibacter mapped to Chr 3 (18.7–19.2 Mb, LRS = 21.4) and for Bifidobacterium mapped to Chr 6 (89.21–89.37 Mb, LRS = 19.4). Introduction of HFD served as an environmental suppressor of these QTLs due to a reduction in the contribution of both genera (P < 0.001). Relations among liver metabolites and cecum bacterial composition were predominant in CD cohort, but these correlations do not persist following the shift to HFD. Overall, these findings demonstrate the important impact of environmental/dietary manipulation on the relationships between host genetics, gastrointestinal bacterial composition, immunological parameters, and metabolites—knowledge that will help in the understanding of the causal sources of metabolic disorders.

Klíčová slova:

Bifidobacterium – Diet – Fats – Metabolites – Microbial genetics – Microbiome – Quantitative trait loci – Cecum


Zdroje

1. Williams EG, Wu Y, Jha P, Dubuis S, Blattmann P, Argmann CA, et al. Systems proteomics of liver mitochondria function. Science. 2016;352(6291):aad0189. Epub 2016/06/11. doi: 10.1126/science.aad0189 27284200.

2. Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, et al. The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota. Microbiol Mol Biol Rev. 2017;81(4). Epub 2017/11/10. doi: 10.1128/MMBR.00036-17 29118049.

3. Scarpellini E, Campanale M, Leone D, Purchiaroni F, Vitale G, Lauritano EC, et al. Gut microbiota and obesity. Intern Emerg Med. 2010;5 Suppl 1:S53–6. Epub 2010/10/01. doi: 10.1007/s11739-010-0450-1 20865475.

4. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3(4):213–23. Epub 2008/04/15. doi: 10.1016/j.chom.2008.02.015 18407065.

5. Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J Physiol. 2009;587(Pt 17):4153–8. Epub 2009/06/06. doi: 10.1113/jphysiol.2009.174136 19491241.

6. Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science. 2010;328(5975):228–31. Epub 2010/03/06. doi: 10.1126/science.1179721 20203013.

7. Li H, Wang X, Rukina D, Huang Q, Lin T, Sorrentino V, et al. An Integrated Systems Genetics and Omics Toolkit to Probe Gene Function. Cell Syst. 2018;6(1):90–102 e4. Epub 2017/12/05. doi: 10.1016/j.cels.2017.10.016 29199021.

8. Wang X, Pandey AK, Mulligan MK, Williams EG, Mozhui K, Li Z, et al. Joint mouse-human phenome-wide association to test gene function and disease risk. Nat Commun. 2016;7:10464. Epub 2016/02/03. doi: 10.1038/ncomms10464 26833085.

9. Andreux PA, Williams EG, Koutnikova H, Houtkooper RH, Champy MF, Henry H, et al. Systems genetics of metabolism: the use of the BXD murine reference panel for multiscalar integration of traits. Cell. 2012;150(6):1287–99. Epub 2012/09/04. doi: 10.1016/j.cell.2012.08.012 22939713.

10. McKnite AM, Perez-Munoz ME, Lu L, Williams EG, Brewer S, Andreux PA, et al. Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PLoS One. 2012;7(6):e39191. Epub 2012/06/23. doi: 10.1371/journal.pone.0039191 22723961.

11. Merkwirth C, Jovaisaite V, Durieux J, Matilainen O, Jordan SD, Quiros PM, et al. Two Conserved Histone Demethylases Regulate Mitochondrial Stress-Induced Longevity. Cell. 2016;165(5):1209–23. Epub 2016/05/03. doi: 10.1016/j.cell.2016.04.012 27133168.

12. Wu Y, Williams EG, Dubuis S, Mottis A, Jovaisaite V, Houten SM, et al. Multilayered genetic and omics dissection of mitochondrial activity in a mouse reference population. Cell. 2014;158(6):1415–30. Epub 2014/09/13. doi: 10.1016/j.cell.2014.07.039 25215496.

13. Mantis NJ, Forbes SJ. Secretory IgA: arresting microbial pathogens at epithelial borders. Immunol Invest. 2010;39(4–5):383–406. Epub 2010/05/11. doi: 10.3109/08820131003622635 20450284.

14. Mestecky J, Russell MW. Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol Lett. 2009;124(2):57–62. Epub 2009/06/16. doi: 10.1016/j.imlet.2009.03.013 19524784.

15. Suzuki K, Meek B, Doi Y, Muramatsu M, Chiba T, Honjo T, et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(7):1981–6. Epub 2004/02/10. doi: 10.1073/pnas.0307317101 14766966.

16. Kalim S, Clish CB, Wenger J, Elmariah S, Yeh RW, Deferio JJ, et al. A plasma long-chain acylcarnitine predicts cardiovascular mortality in incident dialysis patients. J Am Heart Assoc. 2013;2(6):e000542. Epub 2013/12/07. doi: 10.1161/JAHA.113.000542 24308938.

17. Las Heras V, Clooney AG, Ryan FJ, Cabrera-Rubio R, Casey PG, Hueston CM, et al. Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection. Microbiome. 2019;7(1):7. Epub 2019/01/20. doi: 10.1186/s40168-019-0621-x 30658700.

18. Diaz-Ochoa VE, Jellbauer S, Klaus S, Raffatellu M. Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis. Front Cell Infect Microbiol. 2014;4:2. Epub 2014/01/31. doi: 10.3389/fcimb.2014.00002 24478990.

19. Gladyshev VN, Arner ES, Berry MJ, Brigelius-Flohe R, Bruford EA, Burk RF, et al. Selenoprotein Gene Nomenclature. J Biol Chem. 2016;291(46):24036–40. Epub 2016/09/21. doi: 10.1074/jbc.M116.756155 27645994.

20. Wang L, Jing J, Yan H, Tang J, Jia G, Liu G, et al. Selenium Pretreatment Alleviated LPS-Induced Immunological Stress Via Upregulation of Several Selenoprotein Encoding Genes in Murine RAW264.7 Cells. Biol Trace Elem Res. 2018;186(2):505–13. Epub 2018/04/20. doi: 10.1007/s12011-018-1333-y 29671252.

21. Kasaikina MV, Kravtsova MA, Lee BC, Seravalli J, Peterson DA, Walter J, et al. Dietary selenium affects host selenoproteome expression by influencing the gut microbiota. FASEB J. 2011;25(7):2492–9. Epub 2011/04/16. doi: 10.1096/fj.11-181990 21493887.

22. Muller M, Banning A, Brigelius-Flohe R, Kipp A. Nrf2 target genes are induced under marginal selenium-deficiency. Genes Nutr. 2010;5(4):297–307. Epub 2010/12/31. doi: 10.1007/s12263-010-0168-8 21189866.

23. Brandsma E, Houben T, Fu J, Shiri-Sverdlov R, Hofker MH. The immunity-diet-microbiota axis in the development of metabolic syndrome. Curr Opin Lipidol. 2015;26(2):73–81. Epub 2015/02/19. doi: 10.1097/MOL.0000000000000154 25692344.

24. Ramirez-Perez O, Cruz-Ramon V, Chinchilla-Lopez P, Mendez-Sanchez N. The Role of the Gut Microbiota in Bile Acid Metabolism. Ann Hepatol. 2017;16 Suppl 1:S21–S6. Epub 2017/11/01. doi: 10.5604/01.3001.0010.5672 31196631.

25. Wahlstrom A. Outside the liver box: The gut microbiota as pivotal modulator of liver diseases. Biochim Biophys Acta Mol Basis Dis. 2019;1865(5):912–9. Epub 2019/04/23. doi: 10.1016/j.bbadis.2018.07.004 31007175.

26. Kunisawa J, Kiyono H. Sphingolipids and Epoxidized Lipid Metabolites in the Control of Gut Immunosurveillance and Allergy. Front Nutr. 2016;3:3. Epub 2016/02/10. doi: 10.3389/fnut.2016.00003 26858949.

27. Fuhrer T, Heer D, Begemann B, Zamboni N. High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal Chem. 2011;83(18):7074–80. Epub 2011/08/13. doi: 10.1021/ac201267k 21830798.

28. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(44):18933–8. Epub 2010/10/13. doi: 10.1073/pnas.1007028107 20937875.


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 1/2024 (znalostní test z časopisu)
nový kurz

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Význam metforminu pro „udržitelnou“ terapii diabetu
Autoři: prof. MUDr. Milan Kvapil, CSc., MBA

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#