Ovariectomy results in differential shifts in gut microbiota in low versus high aerobic capacity rats

Physiological Reports

Volumn 3, Issue 8, 2015, Pages

  Cox York, Kimberly A ^a   Sheflin, Amy M ^a   Foster, Michelle T ^a   Gentile, Christopher L ^a   Kahl, Amber ^a   Koch, Lauren G ^b   Britton, Steven L ^b   Weir, Tiffany L ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Aerobic capacity; Gut microbiota; Menopause

Indexed keywords

ENDOTOXIN; ESTROGEN; FLUORESCEIN ISOTHIOCYANATE; SHORT CHAIN FATTY ACID; TRIACYLGLYCEROL;

AEROBIC CAPACITY; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; BARNESIELLA; BIFIDOBACTERIUM; BODY COMPOSITION; BODY WEIGHT; CONTROLLED STUDY; FATTY ACID SYNTHESIS; FECES ANALYSIS; FECES MICROFLORA; FEMALE; FOOD INTAKE; GLUCOSE TOLERANCE TEST; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MICROBIAL COLONIZATION; MICROBIAL DIVERSITY; NONHUMAN; OBESITY; OVARIECTOMY; PREVOTELLA; RAT; RUMINOCOCCACEAE; UTERUS WEIGHT;

EID: 85002152688     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12488     Document Type: Article

References (55)

1. Adlercreutz, H., M. O. Pulkkinen, E. K. Hamalainen, and J. T. Korpela. 1984. Studies on the role of intestinal bacteria in metabolism of synthetic and natural steroid hormones. J. Steroid Biochem. 20:217-229.
2. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26:32-46.
3. Britton, S. L., and L. G. Koch. 2001. Animal genetic models for complex traits of physical capacity. Exerc. Sport Sci. Rev. 29:7-14.
4. Burton, F. L., D. Malkova, M. J. Caslake, and J. M. Gill. 2008. Energy replacement attenuates the effects of prior moderate exercise on postprandial metabolism in overweight/obese men. Int. J. Obes. (Lond) 32:481-489.
5. Cani, P. D., R. Bibiloni, C. Knauf, A. Waget, A. M. Neyrinck, N. M. Delzenne, et al. 2008. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470-1481.
6. Choi, J. J., S. Y. Eum, E. Rampersaud, S. Daunert, M. T. Abreu, and M. Toborek. 2013. Exercise attenuates PCBinduced changes in the mouse gut microbiome. Environ. Health Perspect. 121:725-730.
7. Choi, J., K. Chandrasekaran, T. G. Demarest, T. Kristian, S. Xu, K. Vijaykumar, et al. 2014. Brain diabetic neurodegeneration segregates with low intrinsic aerobic capacity. Ann. Clin. Transl. Neurol. 1:589-604.
8. Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117-143.
9. Fernandes, J., W. Su, S. Rahat-Rozenbloom, T. M. Wolever, and E. M. Comelli. 2014. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr. Diabetes 4:e121.
10. Flores, R., J. Shi, B. Fuhrman, X. Xu, T. D. Veenstra, M. H. Gail, et al. 2012. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: a crosssectional study. J. Transl. Med. 10:253.
11. Fuhrman, B. J., H. S. Feigelson, R. Flores, M. H. Gail, X. Xu, J. Ravel, et al. 2014. Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women. J. Clin. Endocrinol. Metab. 99:4632-4640.
12. Gavini, C. K., S. Mukherjee, C. Shukla, S. L. Britton, L. G. Koch, H. Shi, et al. 2014. Leanness and heightened nonresting energy expenditure: role of skeletal muscle activity thermogenesis. Am. J. Physiol. Endocrinol. Metab. 306:E635-E647.
13. Ge, H., X. Li, J. Weiszmann, P. Wang, H. Baribault, J. L. Chen, et al. 2008. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology 149:4519-4526.
14. Gevers, D., S. Kugathasan, L. A. Denson, Y. Vazquez-Baeza, W. Van Treuren, B. Ren, et al. 2014. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 15:382-392.
15. Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125:1401-1412.
16. Gorzek, J. F., K. C. Hendrickson, J. P. Forstner, J. L. Rixen, A. L. Moran, and D. A. Lowe. 2007. Estradiol and tamoxifen reverse ovariectomy-induced physical inactivity in mice. Med. Sci. Sports Exerc. 39:248-256.
17. Hagio, M., M. Matsumoto, T. Yajima, H. Hara, and S. Ishizuka. 2010. Voluntary wheel running exercise and dietary lactose concomitantly reduce proportion of secondary bile acids in rat feces. J. Appl. Physiol. (1985) 109:663-668.
18. Harte, A. L., M. C. Varma, G. Tripathi, K. C. McGee, N. M. Al-Daghri, O. S. Al-Attas, et al. 2012. High fat intake leads to acute postprandial exposure to circulating endotoxin in type 2 diabetic subjects. Diabetes Care 35:375-382.
19. Herd, S. L., A. E. Hardman, L. H. Boobis, and C. J. Cairns. 1998. The effect of 13 weeks of running training followed by 9 d of detraining on postprandial lipaemia. Br. J. Nutr. 80:57-66.
20. Heumann, D., and T. Roger. 2002. Initial responses to endotoxins and Gram-negative bacteria. Clin. Chim. Acta 323:59-72.
21. Howitt, M. R., and W. S. Garrett. 2012. A complex microworld in the gut: gut microbiota and cardiovascular disease connectivity. Nat. Med. 18:1188-1189.
22. Johnsen, V. L., D. D. Belke, C. C. Hughey, D. S. Hittel, R. T. Hepple, L. G. Koch, et al. 2013. Enhanced cardiac protein glycosylation (O-GlcNAc) of selected mitochondrial proteins in rats artificially selected for low running capacity. Physiol. Genomics 45:17-25.
23. Joyner, J. M., L. J. Hutley, and D. P. Cameron. 2000. Glucocorticoid receptors in human preadipocytes: regional and gender differences. J. Endocrinol. 166:145-152.
24. Kim, K. A., W. Gu, I. A. Lee, E. H. Joh, and D. H. Kim. 2012. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS ONE 7:e47713.
25. Kimura, I., K. Ozawa, D. Inoue, T. Imamura, K. Kimura, T. Maeda, et al. 2013. The gut microbiota suppresses insulinmediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 4:1829.
26. Koch, L. G., and S. L. Britton. 2001. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol. Genomics 5:45-52.
27. Koeth, R. A., Z. Wang, B. S. Levison, J. A. Buffa, E. Org, B. T. Sheehy, et al. 2013. Intestinal microbiota metabolism of Lcarnitine, a nutrient in red meat, promotes atherosclerosis Nat. Med. 19:576-585.
28. Kornman, K. S., and W. J. Loesche. 1982. Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect. Immun. 35:256-263.
29. Kuwahara, A. 2014. Contributions of colonic short-chain Fatty Acid receptors in energy homeostasis. Front Endocrinol. (Lausanne) 5: 144.
30. Larsen, N., F. K. Vogensen, F. W. van den Berg, D. S. Nielsen, A. S. Andreasen, B. K. Pedersen, et al. 2010. Gut microbiota in human adults with type 2 diabetes differs from nondiabetic adults. PLoS ONE 5:e9085.
31. Ley, R. E. 2010. Obesity and the human microbiome. Curr. Opin. Gastroenterol. 26:5-11.
32. Liu, W. Y., J. da Lu, X. M. Du, J. Q. Sun, J. Ge, R. W. Wang, et al. 2014. Effect of aerobic exercise and low carbohydrate diet on pre-diabetic non-alcoholic fatty liver disease in postmenopausal women and middle aged men-the role of gut microbiota composition: study protocol for the AELC randomized controlled trial. BMC Public Health 14:48.
33. van Looijer-Langen, M., N. Hotte, L. A. Dieleman, E. Albert, C. Mulder, and K. L. Madsen. 2011. Estrogen receptor-beta signaling modulates epithelial barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 300: G621-G626.
34. Markle, J. G., D. N. Frank, S. Mortin-Toth, C. E. Robertson, L. M. Feazel, U. Rolle-Kampczyk, et al. 2013. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339:1084-1088.
35. Matsumoto, M., R. Inoue, T. Tsukahara, K. Ushida, H. Chiji, N. Matsubara, et al. 2008. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci. Biotechnol. Biochem. 72:572-576.
36. Meissner, M., E. Lombardo, R. Havinga, U. J. Tietge, F. Kuipers, and A. K. Groen. 2011. Voluntary wheel running increases bile acid as well as cholesterol excretion and decreases atherosclerosis in hypercholesterolemic mice. Atherosclerosis 218:323-329.
37. Menon, R., S. E. Watson, L. N. Thomas, C. D. Allred, A. Dabney, M. A. Azcarate-Peril, et al. 2013. Diet complexity and estrogen receptor b status affect the composition of the murine intestinal microbiota. Appl. Environ. Microbiol. 79:5763-5773.
38. Novak, C. M., C. Escande, P. R. Burghardt, M. Zhang, M. T. Barbosa, E. N. Chini, et al. 2010. Spontaneous activity, economy of activity, and resistance to diet-induced obesity in rats bred for high intrinsic aerobic capacity. Horm. Behav. 58:355-367.
39. Oksanen, J., F. Guillaume Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, et al. 2015. vegan: community ecology package. R package version 2.2-1. Available at http://CRAN.R-project.org/package=vegan.
40. Pighon, A., J. Gutkowska, M. Jankowski, R. Rabasa-Lhoret, and J. M. Lavoie. 2011. Exercise training in ovariectomized rats stimulates estrogenic-like effects on expression of genes involved in lipid accumulation and subclinical inflammation in liver. Metabolism 60:629-639.
41. Plottel, C. S., and M. J. Blaser. 2011. Microbiome and malignancy. Cell Host Microbe 10:324-335.
42. Ritchie, R. H., C. H. Leo, C. Qin, E. J. Stephenson, M. A. Bowden, K. D. Buxton, et al. 2013. Low intrinsic exercise capacity in rats predisposes to age-dependent cardiac remodeling independent of macrovascular function. Am. J. Physiol. Heart Circ. Physiol. 304:H729-H739.
43. Rogers, N. H., J. W. 2nd Perfield, K. J. Strissel, M. S. Obin, and A. S. Greenberg. 2009. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 150:2161-2168.
44. Sack, R. B., L. L. Myers, J. Almeido-Hill, D. S. Shoop, W. C. Bradbury, R. Reid, et al. 1992. Enterotoxigenic Bacteroides fragilis: epidemiologic studies of its role as a human diarrhoeal pathogen. J. Diarrhoeal Dis. Res. 10:4-9.
45. Salpeter, S. R., J. M. Walsh, T. M. Ormiston, E. Greyber, N. S. Buckley, and E. E. Salpeter. 2006. Meta-analysis: effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes. Metab. 8:538-554.
46. Seifert, E. L., M. Bastianelli, C. Aguer, C. Moffat, C. Estey, L. G. Koch, et al. 2012. Intrinsic aerobic capacity correlates with greater inherent mitochondrial oxidative and H2O2 emission capacities without major shifts in myosin heavy chain isoform. J. Appl. Physiol. (1985) 113:1624-1634.
47. Sternfeld, B., and S. Dugan. 2011. Physical activity and health during the menopausal transition. Obstet. Gynecol. Clin. North Am. 38:537-566.
48. Tremaroli, V., and F. Backhed. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249.
49. Velagapudi, V. R., R. Hezaveh, C. S. Reigstad, P. Gopalacharyulu, L. Yetukuri, S. Islam, et al. 2010. The gut microbiota modulates host energy and lipid metabolism in mice. J. Lipid Res. 51:1101-1112.
50. Vieira-Potter, V. J., J. Padilla, Y. M. Park, R. J. Welly, R. J. Scroggins, S. L. Britton, et al. 2015. Female rats selectively bred for high intrinsic aerobic fitness are protected from ovariectomy-associated metabolic dysfunction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 6:R530-R542.
51. Viloria, M., E. Lara-Padilla, R. Campos-Rodriguez, A. Jarillo-Luna, H. Reyna-Garfias, P. Lopez-Sanchez, et al. 2011. Effect of moderate exercise on IgA levels and lymphocyte count in mouse intestine. Immunol. Invest. 40:640-656.
52. Waters, R. P., K. J. Renner, C. H. Summers, M. J. Watt, G. L. Forster, L. G. Koch, et al. 2010. Selection for intrinsic endurance modifies endocrine stress responsiveness. Brain Res. 1357:53-61.
53. Wisloff, U., S. M. Najjar, O. Ellingsen, P. M. Haram, S. Swoap, Q. Al-Share, et al. 2005. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307:418-420.
54. Woting, A., N. Pfeiffer, G. Loh, S. Klaus, and M. Blaut. 2014. Clostridium ramosum promotes high-fat dietinduced obesity in gnotobiotic mouse models. MBio 5: e01530-01514.
55. Zhang, C., S. Li, L. Yang, P. Huang, W. Li, S. Wang, et al. 2013. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat. Commun. 4:2163.