Journal of Microbiology and Biotechnology

  • 제27권12호
  • /
  • Pages.2228-2236
  • /
  • 2017
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Difference in the Gut Microbiome between Ovariectomy-Induced Obesity and Diet-Induced Obesity

  • Choi, Sungmi (Department of Public Health Sciences, Graduate School, Korea University) ;
  • Hwang, Yu-Jin (Department of Agrofood Resources, National Institute of Agricultural Science, RDA) ;
  • Shin, Min-Jeong (Department of Public Health Sciences, Graduate School, Korea University) ;
  • Yi, Hana (Department of Public Health Sciences, Graduate School, Korea University)
  • 투고 : 2017.10.10
  • 심사 : 2017.11.07
  • 발행 : 2017.12.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

During menopausal transition, the imbalance of estrogen causes body weight gain. Although gut microbiome dysbiosis has been reported in postmenopausal obesity, it is not clear whether there is any difference in the microbiome profile between dietary-induced obesity and postmenopausal obesity. Therefore, in this study, we analyzed intestinal samples from ovariectomized mice and compared them with those of mice with high-fat diet-induced obesity. To further evaluate the presence of menopause-specific bacteria-gene interactions, we also analyzed the liver transcriptome. Investigation of the 16S rRNA V3-V4 region amplicon sequence profile revealed that menopausal obesity and dietary obesity resulted in similar gut microbiome structures. However, Bifidobacterium animalis was exclusively observed in the ovariectomized mice, which indicated that menopausal obesity resulted in a different intestinal microbiome than dietary obesity. Additionally, several bacterial taxa (Dorea species, Akkermansia muciniphila, and Desulfovibrio species) were found when the ovariectomized mice were treated with a high-fat diet. A significant correlation between the above-mentioned menopause-specific bacteria and the genes for female hormone metabolism was also observed, suggesting the possibility of bacteria-gene interactions in menopausal obesity. Our findings revealed the characteristics of the intestinal microbiome in menopausal obesity in the mouse model, which is very similar to the dietary obesity microbiome but having its own diagnostic bacteria.

키워드

참고문헌

  1. McKinlay SM, Brambilla DJ, Posner JG. 1992. The normal menopause transition. Maturitas 14: 103-115. https://doi.org/10.1016/0378-5122(92)90003-M
  2. Eriksen EF, Colvard DS, Berg NJ, Graham ML, Mann KG, Spelsberg TC, et al. 1988. Evidence of estrogen receptors in normal human osteoblast-like cells. Science 241: 84-86. https://doi.org/10.1126/science.3388021
  3. Lindsay R, Hart DM, Aitken JM, MacDonald EB, Anderson JB, Clarke AC. 1976. Long-term prevention of postmenopausal osteoporosis by oestrogen. Evidence for an increased bone mass after delayed onset of oestrogen treatment. Lancet 1: 1038-1041.
  4. Riggs BL, Khosla S, Melton LJ 3rd. 1998. A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J. Bone Miner. Res. 13: 763-773. https://doi.org/10.1359/jbmr.1998.13.5.763
  5. Paganini-Hill A, Henderson VW. 1994. Estrogen deficiency and risk of Alzheimer's disease in women. Am. J. Epidemiol. 140: 256-261. https://doi.org/10.1093/oxfordjournals.aje.a117244
  6. Yue X, Lu M, Lancaster T, Cao P, Honda S, Staufenbiel M, et al. 2005. Brain estrogen deficiency accelerates $A{\beta}$ plaque formation in an Alzheimer's disease animal model. Proc. Natl. Acad. Sci. USA 102: 19198-19203. https://doi.org/10.1073/pnas.0505203102
  7. Ainslie DA, Morris MJ, Wittert G, Turnbull H, Proietto J, Thorburn AW. 2001. Estrogen deficiency causes central leptin insensitivity and increased hypothalamic neuropeptide Y. Int. J. Obes. Relat. Metab. Disord. 25: 1680-1688. https://doi.org/10.1038/sj.ijo.0801806
  8. Lovejoy JC, Champagne CM, d e Jonge L, X ie H , Smith SR. 2008. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int. J. Obes. 32: 949-958. https://doi.org/10.1038/ijo.2008.25
  9. Shimizu H, Shimomura Y, Nakanishi Y, Futawatari T, Ohtani K, Sato N, et al. 1997. Estrogen increases in vivo leptin production in rats and human subjects. J. Endocrinol. 154: 285-292. https://doi.org/10.1677/joe.0.1540285
  10. Carr MC. 2003. The emergence of the metabolic syndrome with menopause. J. Clin. Endocrinol. Metab. 88: 2404-2411. https://doi.org/10.1210/jc.2003-030242
  11. Dosi R, Bhatt N, Shah P, Patell R. 2014. Cardiovascular disease and menopause. J. Clin. Diagn. Res. 8: 62-64.
  12. Hu FB, Grodstein F, Hennekens CH, Colditz GA, Johnson M, Manson JE, et al. 1999. Age at natural menopause and risk of cardiovascular disease. Arch. Intern. Med. 159: 1061-1066. https://doi.org/10.1001/archinte.159.10.1061
  13. Ramezani Tehrani F, Behboudi-Gandevani S, Ghanbarian A, Azizi F. 2014. Effect of menopause on cardiovascular disease and its risk factors: a 9-year follow-up study. Climacteric 17: 164-172. https://doi.org/10.3109/13697137.2013.828197
  14. Coylewright M, Reckelhoff JF, Ouyang P. 2008. Menopause and hypertension: an age-old debate. Hypertension 51: 952-959. https://doi.org/10.1161/HYPERTENSIONAHA.107.105742
  15. Rappelli A. 2002. Hypertension and obesity after the menopause. J. Hypertens. Suppl. 20: S26-S28.
  16. Nelson HD, Humphrey LL, Nygren P, Teutsch SM, Allan JD. 2002. Postmenopausal hormone replacement therapy: scientific review. JAMA 288: 872-881. https://doi.org/10.1001/jama.288.7.872
  17. Hummelen R, Macklaim JM, Bisanz JE, Hammond JA, McMillan A, Vongsa R, et al. 2011. Vaginal microbiome and epithelial gene array in post-menopausal women with moderate to severe dryness. PLoS One 6: e26602. https://doi.org/10.1371/journal.pone.0026602
  18. Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver MI, et al. 2014. Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause 21: 450-458. https://doi.org/10.1097/GME.0b013e3182a4690b
  19. Cauci S, Driussi S, De Santo D, Penacchioni P, Iannicelli T, Lanzafame P, et al. 2002. Prevalence of bacterial vaginosis and vaginal flora changes in peri- and postmenopausal women. J. Clin. Microbiol. 40: 2147-2152. https://doi.org/10.1128/JCM.40.6.2147-2152.2002
  20. Fuhrman BJ, Feigelson HS, Flores R, Gail MH, Xu X, Ravel J, et al. 2014. Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women. J. Clin. Endocrinol. Metab. 99: 4632-4640. https://doi.org/10.1210/jc.2014-2222
  21. Flores R, Shi J, Fuhrman B, Xu X, Veenstra TD, Gail MH, et al. 2012. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: a cross-sectional study. J. Transl. Med. 10: 253. https://doi.org/10.1186/1479-5876-10-253
  22. Menon R, Watson SE, Thomas LN, Allred CD, Dabney A, Azcarate-Peril MA, et al. 2013. Diet complexity and estrogen receptor beta status affect the composition of the murine intestinal microbiota. Appl. Environ. Microbiol. 79: 5763-5773. https://doi.org/10.1128/AEM.01182-13
  23. Kwa M, Plottel CS, Blaser MJ, Adams S. 2016. The intestinal microbiome and estrogen receptor-positive female breast cancer. J. Natl. Cancer Inst. 108: djw029.
  24. Brahe L K, L e Chatelier E, P rifti E, P ons N, K ennedy S, Hansen T, et al. 2015. Specific gut microbiota features and metabolic markers in postmenopausal women with obesity. Nutr. Diabetes 5: e159. https://doi.org/10.1038/nutd.2015.9
  25. Lawley B, Tannock GW. 2017. Analysis of 16S rRNA gene amplicon sequences using the QIIME software package. Methods Mol. Biol. 1537: 153-163.
  26. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069-5072. https://doi.org/10.1128/AEM.03006-05
  27. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461. https://doi.org/10.1093/bioinformatics/btq461
  28. Hamady M, Lozupone C, Knight R. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4: 17-27. https://doi.org/10.1038/ismej.2009.97
  29. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12: R60. https://doi.org/10.1186/gb-2011-12-6-r60
  30. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67: 1613-1617. https://doi.org/10.1099/ijsem.0.001755
  31. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25: 25-29. https://doi.org/10.1038/75556
  32. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. 2017. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45: D353-D361. https://doi.org/10.1093/nar/gkw1092
  33. The R project for statistical computing. Available from http://www.r-project.org. Accessed 18 September 2017.
  34. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, et al. 2007. Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2: 2366-2382. https://doi.org/10.1038/nprot.2007.324
  35. Cox-York KA, Sheflin AM, Foster MT, Gentile CL, Kahl A, Koch LG, et al. 2015. Ovariectomy results in differential shifts in gut microbiota in low versus high aerobic capacity rats. Physiol. Rep. 3: e12488. https://doi.org/10.14814/phy2.12488
  36. Keenan MJ, Janes M, Robert J, Martin RJ, Raggio AM, McCutcheon KL, et al. 2013. Resistant starch from high amylose maize (HAM-RS2) reduces body fat and increases gut bacteria in ovariectomized (OVX) rats. Obesity 21: 981-984. https://doi.org/10.1002/oby.20109
  37. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, et al. 2009. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137: 1716-1724.e1-2. https://doi.org/10.1053/j.gastro.2009.08.042
  38. Turnbaugh PJ, Baeckhed 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. https://doi.org/10.1016/j.chom.2008.02.015
  39. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108. https://doi.org/10.1126/science.1208344
  40. Rabot S, Membrez M, Blancher F, Berger B, Moine D, Krause L, et al. 2016. High fat diet drives obesity regardless the composition of gut microbiota in mice. Sci. Rep. 6: 32484. https://doi.org/10.1038/srep32484
  41. Liu TW, Park YM, Holscher HD, Padilla J, Scroggins RJ, Welly R, et al. 2015. Physical activity differentially affects the cecal microbiota of ovariectomized female rats selectively bred for high and low aerobic capacity. PLoS One 10: e0136150. https://doi.org/10.1371/journal.pone.0136150
  42. Krebs CJ, Jarvis ED, Pfaff DW. 1999. The 70-kDa heat shock cognate protein (Hsc73) gene is enhanced by ovarian hormones in the ventromedial hypothalamus. Proc. Natl. Acad. Sci. USA 96: 1686-1691. https://doi.org/10.1073/pnas.96.4.1686
  43. Sarvari M, Kallo I, Hrabovszky E, Solymosi N, Liposits Z. 2014. Ovariectomy and subsequent treatment with estrogen receptor agonists tune the innate immune system of the hippocampus in middle-aged female rats. PLoS One 9: e88540. https://doi.org/10.1371/journal.pone.0088540
  44. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 110: 9066-9071. https://doi.org/10.1073/pnas.1219451110
  45. Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS, et al. 2014. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63: 727-735. https://doi.org/10.1136/gutjnl-2012-303839

피인용 문헌

  1. Long-Term Administration of Conjugated Estrogen and Bazedoxifene Decreased Murine Fecal β-Glucuronidase Activity Without Impacting Overall Microbiome Community vol.8, pp.None, 2017, https://doi.org/10.1038/s41598-018-26506-1
  2. Estrogen-mediated gut microbiome alterations influence sexual dimorphism in metabolic syndrome in mice vol.6, pp.1, 2017, https://doi.org/10.1186/s40168-018-0587-0
  3. Impact of Buckwheat Fermented Milk Combined with High‐Fat Diet on Rats’ Gut Microbiota and Short‐Chain Fatty Acids vol.84, pp.12, 2017, https://doi.org/10.1111/1750-3841.14958
  4. Endobolome, a New Concept for Determining the Influence of Microbiota Disrupting Chemicals (MDC) in Relation to Specific Endocrine Pathogenesis vol.11, pp.None, 2017, https://doi.org/10.3389/fmicb.2020.578007
  5. Vaginal Microbiota Profiles of Native Korean Women and Associations with High-Risk Pregnancy vol.30, pp.2, 2017, https://doi.org/10.4014/jmb.1908.08016
  6. The microbiome and gynaecological cancer development, prevention and therapy vol.17, pp.4, 2017, https://doi.org/10.1038/s41585-020-0286-z
  7. Gut microbiome associations with breast cancer risk factors and tumor characteristics: a pilot study vol.182, pp.2, 2020, https://doi.org/10.1007/s10549-020-05702-6
  8. Bone‐protective effects of Lactobacillus plantarum B719‐fermented milk product vol.73, pp.4, 2017, https://doi.org/10.1111/1471-0307.12701
  9. 17β-Estradiol supplementation changes gut microbiota diversity in intact and colorectal cancer-induced ICR male mice vol.10, pp.None, 2017, https://doi.org/10.1038/s41598-020-69112-w
  10. The gut microbiota during the progression of atherosclerosis in the perimenopausal period shows specific compositional changes and significant correlations with circulating lipid metabolites vol.13, pp.1, 2017, https://doi.org/10.1080/19490976.2021.1880220
  11. Alterations in Gut Microbiota Do Not Play a Causal Role in Diet-independent Weight Gain Caused by Ovariectomy vol.5, pp.1, 2021, https://doi.org/10.1210/jendso/bvaa173
  12. Microbiome and PCOS: State-of-Art and Future Aspects vol.22, pp.4, 2017, https://doi.org/10.3390/ijms22042048
  13. Modulation of the Gut Microbiota Structure with Probiotics and Isoflavone Alleviates Metabolic Disorder in Ovariectomized Mice vol.13, pp.6, 2017, https://doi.org/10.3390/nu13061793
  14. Association of clinical characteristics and lifestyle factors with fecal S100/calgranulin concentrations in healthy dogs vol.7, pp.4, 2017, https://doi.org/10.1002/vms3.469
  15. How the Gut Microbiome Links to Menopause and Obesity, with Possible Implications for Endometrial Cancer Development vol.10, pp.13, 2017, https://doi.org/10.3390/jcm10132916
  16. Distinct Changes in Gut Microbiota Are Associated with Estradiol-Mediated Protection from Diet-Induced Obesity in Female Mice vol.11, pp.8, 2017, https://doi.org/10.3390/metabo11080499
  17. Natural and synthetic estrogens specifically alter nicotine demand and cue-induced nicotine seeking in female rats vol.198, pp.None, 2021, https://doi.org/10.1016/j.neuropharm.2021.108756
  18. Lactobacillus intestinalis YT2 restores the gut microbiota and improves menopausal symptoms in ovariectomized rats vol.12, pp.5, 2017, https://doi.org/10.3920/bm2020.0217
  19. Development of a novel model of cholecystectomy in subsequently ovariectomized mice and characterization of metabolic and gastrointestinal phenotypes: a pilot study vol.21, pp.1, 2017, https://doi.org/10.1186/s12876-021-01648-1
  20. Ovariectomy-Induced Dysbiosis May Have a Minor Effect on Bone in Mice vol.9, pp.12, 2017, https://doi.org/10.3390/microorganisms9122563
  21. Cinnamic acid suppresses bone loss via induction of osteoblast differentiation with alteration of gut microbiota vol.101, pp.None, 2017, https://doi.org/10.1016/j.jnutbio.2021.108900