Structural modulation of gut microbiota in life-long calorie-restricted mice

Nature Communications

Volumn 4, Issue , 2013, Pages

  Zhang, Chenhong ^a   Li, Shoufeng ^b   Yang, Liu ^b   Huang, Ping ^b   Li, Wenjun ^b   Wang, Shengyue ^c   Zhao, Guoping ^c   Zhang, Menghui ^a   Pang, Xiaoyan ^a   Yan, Zhen ^d,e   Liu, Yong ^b   Zhao, Liping ^a,f  

^a Shanghai Jiao Tong University   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^d UNIVERSITY OF VIRGINIA   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

^f BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPOLYSACCHARIDE BINDING PROTEIN;

ANTIGEN; BACTERIUM; DIET; EXPERIMENTAL STUDY; POLYSACCHARIDE; PROTEIN; RODENT;

ANIMAL EXPERIMENT; ARTICLE; CALORIC RESTRICTION; FEMALE; INTESTINE FLORA; LACTOBACILLUS; LIFESPAN; LOW FAT DIET; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL;

ACUTE-PHASE PROTEINS; AGE FACTORS; ANIMALS; CALORIC RESTRICTION; CARRIER PROTEINS; DIET, FAT-RESTRICTED; DIET, HIGH-FAT; DNA, BACTERIAL; FECES; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; METAGENOME; MICE; MICE, INBRED C57BL; MICROBIOTA; PHYLOGENY;

EID: 84880368918     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3163     Document Type: Article

References (60)

1. McCay, C. M., Crowell, M. F. & Maynard, L. A. The effect of retarded growth upon the length of life span and upon the ultimate body size. J. Nutr. 10, 63-79 (1935).
2. Colman, R. J. et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201-204 (2009).
3. Fontana, L., Meyer, T. E., Klein, S. & Holloszy, J. O. Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans. Proc. Natl Acad. Sci. USA 101, 6659-6663 (2004).
4. Wolf, G. Calorie restriction increases life span: a molecular mechanism. Nutr. Rev. 64, 89-92 (2006).
5. Guarente, L. Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell 132, 171-176 (2008). (Pubitemid 351172441)
6. Wang, Y. et al. Metabonomic investigations of aging and caloric restriction in a life-long dog study. J. Proteome Res. 6, 1846-1854 (2007). (Pubitemid 46814508)
7. Rezzi, S. et al. Metabolic shifts due to long-term caloric restriction revealed in nonhuman primates. Exp. Gerontol. 44, 356-362 (2009).
8. Lederberg, J. Infectious history. Science 288, 287-293 (2000).
9. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010).
10. Goodman, A. L. & Gordon, J. I. Our unindicted coconspirators: human metabolism from a microbial perspective. Cell Metab. 12, 111-116 (2010).
11. Sonnenburg, J. L., Angenent, L. T. & Gordon, J. I. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat. Immunol. 5, 569-573 (2004). (Pubitemid 38811880)
12. van Hylckama Vlieg, J. E., Veiga, P., Zhang, C., Derrien, M. & Zhao, L. Impact of microbial transformation of food on health-from fermented foods to fermentation in the gastro-intestinal tract. Curr. Opin. Biotechnol. 22, 211-219 (2011).
13. Zhang, C. et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 4, 232-241 (2010).
14. Cani, P. D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761-1772 (2007). (Pubitemid 47025442)
15. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022-1023 (2006). (Pubitemid 46018512)
16. Cani, P. D. et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50, 2374-2383 (2007). (Pubitemid 47512397)
17. Murphy, E. F. et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59, 1635-1642 (2010).
18. Turnbaugh, P. J., Backhed, F., Fulton, L. & Gordon, J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213-223 (2008). (Pubitemid 351494716)
19. Cani, P. D. et al. Changes in gut microbiota control metabolic endotoxemiainduced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57, 1470-1481 (2008).
20. Cani, P. D. et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58, 1091-1103 (2009).
21. Na Fei, L. Z. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J. 7, 880-884 (2013).
22. Zhou, B. et al. Midlife gene expressions identify modulators of aging through dietary interventions. Proc. Natl Acad. Sci. USA 109, E1201-E1209 (2012).
23. Knights, D., Costello, E. K. & Knight, R. Supervised classification of human microbiota. FEMS Microbiol. Rev. 35, 343-359 (2011).
24. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).
25. Veiga, P. et al. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl Acad. Sci. USA 107, 18132-18137 (2010).
26. Moore, W. E. & Moore, L. H. Intestinal floras of populations that have a high risk of colon cancer. Appl. Environ. Microbiol. 61, 3202-3207 (1995).
27. Finegold, S. M., Attebery, H. R. & Sutter, V. L. Effect of diet on human fecal flora: comparison of Japanese and American diets. Am. J. Clin. Nutr. 27, 1456-1469 (1974).
28. Mueller, S. et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl. Environ. Microbiol. 72, 1027-1033 (2006). (Pubitemid 43271206)
29. De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA 107, 14691-14696 (2010).
30. Backhed, F. et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl Acad. Sci. USA 101, 15718-15723 (2004). (Pubitemid 39473554)
31. Backhed, F., Manchester, J. K., Semenkovich, C. F. & Gordon, J. I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl Acad. Sci. USA 104, 979-984 (2007). (Pubitemid 46154722)
32. Ley, R. E. et al. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102, 11070-11075 (2005). (Pubitemid 41105994)
33. Mai, V., Colbert, L. H., Perkins, S. N., Schatzkin, A. & Hursting, S. D. Intestinal microbiota: a potential diet-responsive prevention target in ApcMin mice. Mol. Carcinog. 46, 42-48 (2007). (Pubitemid 46095232)
34. Santacruz, A. et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity 17, 1906-1915 (2009).
35. Henderson, A. L., Cao, W. W., Wang, R. F., Lu, M. H. & Cerniglia, C. E. The effect of food restriction on the composition of intestinal microflora in rats. Exp. Gerontol. 33, 239-247 (1998). (Pubitemid 28196405)
36. Kleessen, B., Sykura, B., Zunft, H. J. & Blaut, M. Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am. J. Clin. Nutr. 65, 1397-1402 (1997). (Pubitemid 27187749)
37. Ostan, R. et al. Immunosenescence and immunogenetics of human longevity. Neuroimmunomodulation 15, 224-240 (2008).
38. Guigoz, Y., Dore, J. & Schiffrin, E. J. The inflammatory status of old age can be nurtured from the intestinal environment. Curr. Opin. Clin. Nutr. Metab. Care. 11, 13-20 (2008). (Pubitemid 350295220)
39. Flint, H. J., Duncan, S. H., Scott, K. P. & Louis, P. Interactions and competition within the microbial community of the human colon: links between diet and health. Environ. Microbiol. 9, 1101-1111 (2007). (Pubitemid 46697267)
40. Zareie, M. et al. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 55, 1553-1560 (2006). (Pubitemid 44629200)
41. Bernardeau, M., Guguen, M. & Vernoux, J. P. Beneficial lactobacilli in food and feed: long-term use, biodiversity and proposals for specific and realistic safety assessments. FEMS Microbiol. Rev. 30, 487-513 (2006). (Pubitemid 43855764)
42. Price, L. B. et al. Community analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound microbiota. PLoS One 4, e6462 (2009).
43. Koyuncu, M., Acuner, I. C. & Uyar, M. Deep neck infection due to Lactococcus lactis cremoris: a case report. Eur. Arch. Otorhinolaryngol. 262, 719-721 (2005). (Pubitemid 41428262)
44. Kuehbacher, T. et al. Intestinal TM7 bacterial phylogenies in active inflammatory bowel disease. J. Med. Microbiol. 57, 1569-1576 (2008).
45. Sun, L. et al. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care 33, 1925-1932 (2010).
46. Zweigner, J., Schumann, R. R. & Weber, J. R. The role of lipopolysaccharidebinding protein in modulating the innate immune response. Microbes Infect. 8, 946-952 (2006).
47. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384 (2010).
48. Barrett, E. L. & Richardson, D. S. Sex differences in telomeres and lifespan. Aging Cell 10, 913-921 (2011).
49. Markle, J. G. et al. Sex differences in the gut microbiome drive hormonedependent regulation of autoimmunity. Science 339, 1084-1088 (2013).
50. Morell, V. Zeroing in on how hormones affect the immune system. Science 269, 773-775 (1995).
51. Li, M. et al. Symbiotic gut microbes modulate human metabolic phenotypes. Proc. Natl Acad. Sci. USA 105, 2117-2122 (2008). (Pubitemid 351439474)
52. Gibson, G. R. Dietary modulation of the human gut microflora using the prebiotics oligofructose and inulin. J. Nutr. 129, 1438s-1441s (1999). (Pubitemid 29302775)
53. Naughton, P. J., Mikkelsen, L. L. & Jensen, B. B. Effects of nondigestible oligosaccharides on Salmonella enterica serovar typhimurium and nonpathogenic Escherichia coli in the pig small intestine in vitro. Appl. Environ. Microb. 67, 3391-3395 (2001). (Pubitemid 33641205)
54. Wang, T. et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 6, 320-329 (2012).
55. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380 (2005). (Pubitemid 41613494)
56. McKenna, P. et al. The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog. 4, e20 (2008).
57. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl Acad. Sci. USA 103, 12115-12120 (2006). (Pubitemid 44215820)
58. Zhang, C. et al. Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J. 6, 1848-1857 (2012).
59. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
60. Huse, S. M. et al. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 4, e1000255 (2008).