Advertisement

Biogerontology

, Volume 19, Issue 5, pp 367–383 | Cite as

The effect of dietary lipid on gut microbiota in a senescence-accelerated prone mouse model (SAMP8)

  • Kazushi Yamamoto
  • Mamoru Kushida
  • Tsuyoshi Tsuduki
Research Article

Abstract

Gut microbiota change with aging and diet. In a previous study, it was shown that a moderate-fat diet enriched with fish oil had beneficial effects for elderly patients, so we examined the effect of this diet on aging-related changes in gut microbiota in this study. We used 3-month-old male senescence-accelerated prone mice (SAMP8). The mice were fed a normal diet containing 4 g soybean oil/100 g of diet for 6 months and then divided into 4 groups: (1) the Baseline group, ended breeding at 6 months old; (2) the Control group, continued on a normal diet until 15 months old; (3) the MF group, switched to a moderate-fat diet until 15 months old; and (4) the MF + FO group, switched to a moderate-fat diet enriched with fish oil until 15 months old. When mice were 6 or 15 months old, fecal samples were collected and gut microbiota analysis was performed. Gut microbiota analysis at the genus level showed that bacteria known to increase in association with fatty liver and intestinal inflammation increased with aging. However, this alteration was largely inhibited by the moderate-fat diet enriched with fish oil. On the other hand, there was a decrease with aging in the bacteria that play a role in energy consumption, but this alteration was inhibited by the moderate-fat diet enriched with fish oil. These results suggest that a moderate-fat diet enriched with fish oil has beneficial effects on gut microbiota in aging.

Keywords

Aging Dietary lipid Fish oil Gut microbiota SAMP8 

Notes

Acknowledgements

KY is a research fellow of the Japan Society for the Promotion of Science (JSPS). This work was supported by a Grant-in-Aid for Scientific Research to KY from JSPS (no. 16J00821).

Supplementary material

10522_2018_9764_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 32 kb)

References

  1. Alard J, Lehrter V, Rhimi M, Mangin I, Peucelle V, Abraham AL, Mariadassou M, Maguin E, Waligora-Dupriet AJ, Pot B, Wolowczuk I, Grangette C (2016) Beneficial metabolic effects of selected probiotics on diet-induced obesity and insulin resistance in mice are associated with improvement of dysbiotic gut microbiota. Environ Microbiol 18(5):1484–1497.  https://doi.org/10.1111/1462-2920.13181 CrossRefPubMedGoogle Scholar
  2. Arai Y, Inagaki H, Takayama M, Abe Y, Saito Y, Takebayashi T, Gondo Y, Hirose N (2014) Physical independence and mortality at the extreme limit of life span: supercentenarians study in Japan. J Gerontol A Biol Sci Med Sci 69(4):486–494.  https://doi.org/10.1093/gerona/glt146 CrossRefPubMedGoogle Scholar
  3. Baldwin J, Collins B, Wolf PG, Martinez K, Shen W, Chuang CC, Zhong W, Cooney P, Cockrell C, Chang E, Gaskins HR, McIntosh MK (2016) Table grape consumption reduces adiposity and markers of hepatic lipogenesis and alters gut microbiota in butter fat-fed mice. J Nutr Biochem 27:123–135.  https://doi.org/10.1016/j.jnutbio.2015.08.027 CrossRefPubMedGoogle Scholar
  4. Barnett MP, McNabb WC, Cookson AL, Zhu S, Davy M, Knoch B, Nones K, Hodgkinson AJ, Roy NC (2010) Changes in colon gene expression associated with increased colon inflammation in interleukin-10 gene-deficient mice inoculated with Enterococcus species. BMC Immunol 15(11):39.  https://doi.org/10.1186/1471-2172-11-39 CrossRefGoogle Scholar
  5. Biagi E, Candela M, Turroni S, Garagnani P, Franceschi C, Brigidi P (2013) Ageing and gut microbes: perspectives for health maintenance and longevity. Pharmacol Res 69(1):11–20.  https://doi.org/10.1016/j.phrs.2012.10.005 CrossRefPubMedGoogle Scholar
  6. Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, Consolandi C, Quercia S, Scurti M, Monti D, Capri M, Brigidi P, Candela M (2016) Gut microbiota and extreme longevity. Curr Biol 26(11):1480–1485.  https://doi.org/10.1016/j.cub.2016.04.016 CrossRefPubMedGoogle Scholar
  7. Butterfield DA, Poon HF (2005) The senescence-accelerated prone mouse (SAMP8): a model of age-related cognitive decline with relevance to alterations of the gene expression and protein abnormalities in Alzheimer’s disease. Exp Gerontol 40:774–783CrossRefPubMedGoogle Scholar
  8. Camuesco D, Gálvez J, Nieto A, Comalada M, Rodríguez-Cabezas ME, Concha A, Xaus J, Zarzuelo A (2005) Dietary olive oil supplemented with fish oil, rich in EPA and DHA (n-3) polyunsaturated fatty acids, attenuates colonic inflammation in rats with DSS-induced colitis. J Nutr 135(4):687–694CrossRefPubMedGoogle Scholar
  9. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2):266–267.  https://doi.org/10.1093/bioinformatics/btp636 CrossRefPubMedGoogle Scholar
  10. Chen D, Yang Z, Chen X, Huang Y, Yin B, Guo F, Zhao H, Huang J, Wu Y, Gu R (2015) Effect of Lactobacillus rhamnosus hsryfm 1301 on the gut microbiota and lipid metabolism in rats fed a high-fat diet. J Microbiol Biotechnol 25(5):687–695CrossRefPubMedGoogle Scholar
  11. Cheng IC, Shang HF, Lin TF, Wang TH, Lin HS, Lin SH (2005) Effect of fermented soy milk on the intestinal bacterial ecosystem. World J Gastroenterol 11(8):1225–1227CrossRefPubMedPubMedCentralGoogle Scholar
  12. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald GF, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O’Toole PW (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184.  https://doi.org/10.1038/nature11319 CrossRefPubMedGoogle Scholar
  13. Conley MN, Wong CP, Duyck KM, Hord N, Ho E, Sharpton TJ (2016) Aging and serum MCP-1 are associated with gut microbiome composition in a murine model. PeerJ 4:e1854.  https://doi.org/10.7717/peerj.1854 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cui C, Li Y, Gao H, Zhang H, Han J, Zhang D, Li Y, Zhou J, Lu C, Su X (2017) Modulation of the gut microbiota by the mixture of fish oil and krill oil in high-fat diet-induced obesity mice. PLoS ONE 12(10):e0186216.  https://doi.org/10.1371/journal.pone.0186216 CrossRefPubMedPubMedCentralGoogle Scholar
  15. de Gonzalo-Calvo D, Neitzert K, Fernández M, Vega-Naredo I, Caballero B, García-Macía M, Suárez FM, Rodríguez-Colunga MJ, Solano JJ, Coto-Montes A (2010) Differential inflammatory responses in aging and disease: TNF-alpha and IL-6 as possible biomarkers. Free Radic Biol Med 49(5):733–737.  https://doi.org/10.1016/j.freeradbiomed.2010.05.019 CrossRefPubMedGoogle Scholar
  16. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072CrossRefPubMedPubMedCentralGoogle Scholar
  17. Diao L, Auger C, Konoeda H, Sadri AR, Amini-Nik S, Jeschke MG (2018) Hepatic steatosis associated with decreased β-oxidation and mitochondrial function contributes to cell damage in obese mice after thermal injury. Cell Death Dis 9(5):530.  https://doi.org/10.1038/s41419-018-0531-z CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fleissner CK, Huebel N, Abd El-Bary MM, Loh G, Klaus S, Blaut M (2010) Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr 104(6):919–929.  https://doi.org/10.1017/s0007114510001303 CrossRefPubMedGoogle Scholar
  19. Gruber L, Kisling S, Lichti P, Martin FP, May S, Klingenspor M, Lichtenegger M, Rychlik M, Haller D (2013) High fat diet accelerates pathogenesis of murine Crohn’s disease-like ileitis independently of obesity. PLoS ONE 8(8):e71661.  https://doi.org/10.1371/journal.pone.0071661 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Honma T, Yanaka M, Tsuduki T, Ikeda I (2011) Increased lipid accumulation in liver and white adipose tissue in aging in the SAMP10 mouse. J Nutr Sci Vitaminol (Tokyo) 57:123–129CrossRefGoogle Scholar
  21. Honma T, Shinohara N, Ito J, Kijima R, Sugawara S, Arai T, Tsuduki T, Ikeda I (2012) High-fat diet intake accelerates aging, increases expression of Hsd11b1, and promotes lipid accumulation in liver of SAMP10 mouse. Biogerontology 13:93–103.  https://doi.org/10.1007/s10522-011-9363-2 CrossRefPubMedGoogle Scholar
  22. Honma T, Kitano Y, Kijima R, Jibu Y, Kawakami Y, Tsuduki T, Nakagawa K, Miyazawa T (2013a) Comparison of the health benefits of different eras of Japanese foods: lipid and carbohydrate metabolism focused research. Nippon Shokuhin Kagaku Kogaku Kaishi 60:541–553CrossRefGoogle Scholar
  23. Honma T, Tsuduki T, Sugawara S, Kitano Y, Ito J, Kijima R, Tsubata M, Nakagawa K, Miyazawa T (2013b) Aging decreases antioxidant effects and increases lipid peroxidation in the Apolipoprotein E deficient mouse. J Clin Biochem Nutr 52:234–240.  https://doi.org/10.3164/jcbn.12-85 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kau AL, Martin SM, Lyon W, Hayes E, Caparon MG, Hultgren SJ (2005) Enterococcus faecalis tropism for the kidneys in the urinary tract of C57BL/6 J mice. Infect Immun 73(4):2461–2468CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kimoto-Nira H, Suzuki C, Kobayashi M, Sasaki K, Kurisaki J, Mizumachi K (2007) Anti-ageing effect of a lactococcal strain: analysis using senescence-accelerated mice. Br J Nutr 98(6):1178–1186CrossRefPubMedGoogle Scholar
  26. Kong F, Hua Y, Zeng B, Ning R, Li Y, Zhao J (2016) Gut microbiota signatures of longevity. Curr Biol 26(18):R832–R833.  https://doi.org/10.1016/j.cub.2016.08.015 CrossRefPubMedGoogle Scholar
  27. Langille MG, Meehan CJ, Koenig JE, Dhanani AS, Rose RA, Howlett SE, Beiko RG (2014) Microbial shifts in the aging mouse gut. Microbiome 2(1):50.  https://doi.org/10.1186/s40168-014-0050-9 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lee SM, Han HW, Yim SY (2015) Beneficial effects of soy milk and fiber on high cholesterol diet-induced alteration of gut microbiota and inflammatory gene expression in rats. Food Funct 6(2):492–500.  https://doi.org/10.1039/c4fo00731j CrossRefPubMedGoogle Scholar
  29. Li Q, Zhang Q, Wang C, Tang C, Zhang Y, Li N, Li J (2011) Fish oil enhances recovery of intestinal microbiota and epithelial integrity in chronic rejection of intestinal transplant. PLoS ONE 6(6):e20460.  https://doi.org/10.1371/journal.pone.0020460 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13(6):656–668.  https://doi.org/10.1093/bib/bbs035 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Li M, Ouyang W, Wu X, Zheng Y, Wei Y, An L (2014) Kinetin inhibits apoptosis of aging spleen cells induced by d-galactose in rats. J Vet Sci 15(3):353–359CrossRefPubMedPubMedCentralGoogle Scholar
  32. Liu Z, Chen Z, Guo H, He D, Zhao H, Wang Z, Zhang W, Liao L, Zhang C, Ni L (2016) The modulatory effect of infusions of green tea, oolong tea, and black tea on gut microbiota in high-fat-induced obese mice. Food Funct 7(12):4869–4879CrossRefPubMedGoogle Scholar
  33. Magrone T, Jirillo E (2013) The interaction between gut microbiota and age-related changes in immune function and inflammation. Immun Ageing 10(1):31.  https://doi.org/10.1186/1742-4933-10-31 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mäkivuokko H, Tiihonen K, Tynkkynen S, Paulin L, Rautonen N (2010) The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr 103(2):227–234.  https://doi.org/10.1017/s0007114509991553 CrossRefPubMedGoogle Scholar
  35. Mariat D, Firmesse O, Levenez F, Guimarăes V, Sokol H, Doré J, Corthier G, Furet JP (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9:123.  https://doi.org/10.1186/1471-2180-9-123 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM (2004) Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology 127(1):80–93CrossRefPubMedGoogle Scholar
  37. Monteagudo-Mera A, Arthur JC, Jobin C, Keku T, Bruno-Barcena JM, Azcarate-Peril MA (2016) High purity galacto-oligosaccharides enhance specific Bifidobacterium species and their metabolic activity in the mouse gut microbiome. Benef Microbes 7(2):247–264.  https://doi.org/10.3920/BM2015.0114 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL (2012) IBD-what role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 9(4):219–230.  https://doi.org/10.1038/nrgastro.2012.14 CrossRefPubMedGoogle Scholar
  39. Munyaka PM, Rabbi MF, Khafipour E, Ghia JE (2016) Acute dextran sulfate sodium (DSS)-induced colitis promotes gut microbial dysbiosis in mice. J Basic Microbiol 56(9):986–998.  https://doi.org/10.1002/jobm.201500726 CrossRefPubMedGoogle Scholar
  40. Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao JZ, Abe F, Osawa R (2016) Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol 16:90.  https://doi.org/10.1186/s12866-016-0708-5 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ogata T, Senoo T, Kawano S, Ikeda S (2016) Mitochondrial superoxide dismutase deficiency accelerates chronological aging in the fission yeast Schizosaccharomyces pombe. Cell Biol Int 40(1):100–106.  https://doi.org/10.1002/cbin.10556 CrossRefPubMedGoogle Scholar
  42. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefPubMedGoogle Scholar
  43. Pataky Z, Genton L, Spahr L, Lazarevic V, Terraz S, Gaïa N, Rubbia-Brandt L, Golay A, Schrenzel J, Pichard C (2016) Impact of hypocaloric hyperproteic diet on gut microbiota in overweight or obese patients with nonalcoholic fatty liver disease: a pilot study. Dig Dis Sci 61(9):2721–2731.  https://doi.org/10.1007/s10620-016-4179-1 CrossRefPubMedGoogle Scholar
  44. Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490.  https://doi.org/10.1371/journal.pone.0009490 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Qiao Y, Sun J, Ding Y, Le G, Shi Y (2013) Alterations of the gut microbiota in high-fat diet mice is strongly linked to oxidative stress. Appl Microbiol Biotechnol 97(4):1689–1697.  https://doi.org/10.1007/s00253-012-4323-6 CrossRefPubMedGoogle Scholar
  46. Qiao Y, Sun J, Xia S, Tang X, Shi Y, Le G (2014) Effects of resveratrol on gut microbiota and fat storage in a mouse model with high-fat-induced obesity. Food Funct 5(6):1241–1249.  https://doi.org/10.1039/c3fo60630a CrossRefPubMedGoogle Scholar
  47. Reubsaet FA, Veerkamp JH, Bukkens SG, Trijbels JM, Monnens LA (1988) Acyl-CoA oxidase activity and peroxisomal fatty acid oxidation in rat tissues. Biochim Biophys Acta 958(3):434–442CrossRefPubMedGoogle Scholar
  48. Schaar CE, Dues DJ, Spielbauer KK, Machiela E, Cooper JF, Senchuk M, Hekimi S, Van Raamsdonk JM (2015) Mitochondrial and cytoplasmic ROS have opposing effects on lifespan. PLoS Genet 11(2):e1004972.  https://doi.org/10.1371/journal.pgen.1004972 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Sekita A, Okazaki Y, Katayama T (2016) Dietary phytic acid prevents fatty liver by reducing expression of hepatic lipogenic enzymes and modulates gut microflora in rats fed a high-sucrose diet. Nutrition 32(6):720–722.  https://doi.org/10.1016/j.nut.2016.01.003 CrossRefPubMedGoogle Scholar
  50. Sen T, Cawthon CR, Ihde BT, Hajnal A, DiLorenzo PM, de La Serre CB, Czaja K (2017) Diet-driven microbiota dysbiosis is associated with vagal remodeling and obesity. Physiol Behav 173:305–317.  https://doi.org/10.1016/j.physbeh.2017.02.027 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shinohara N, Tsuduki T, Ito J, Honma T, Kijima R, Sugawara S, Arai T, Yamasaki M, Ikezaki A, Yokoyama M, Nishiyama K, Nakagawa K, Miyazawa T, Ikeda I (2012) Jacaric acid, a linolenic acid isomer with a conjugated triene system, has a strong antitumor effect in vitro and in vivo. Biochim Biophys Acta 1821:980–988.  https://doi.org/10.1016/j.bbalip.2012.04.001 CrossRefPubMedGoogle Scholar
  52. Si H, Zhang L, Liu S, LeRoith T, Virgous C (2014) High corn oil dietary intake improves health and longevity of aging mice. Exp Gerontol 58:244–249.  https://doi.org/10.1016/j.exger.2014.09.001 CrossRefPubMedGoogle Scholar
  53. Tachon S, Zhou J, Keenan M, Martin R, Marco ML (2013) The intestinal microbiota in aged mice is modulated by dietary resistant starch and correlated with improvements in host responses. FEMS Microbiol Ecol 83(2):299–309.  https://doi.org/10.1111/j.1574-6941.2012.01475 CrossRefPubMedGoogle Scholar
  54. Takao M, Hirose N, Arai Y, Mihara B, Mimura M (2016) Neuropathology of supercentenarians—four autopsy case studies. Acta Neuropathol Commun 4(1):97.  https://doi.org/10.1186/s40478-016-0368-6 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Takeda T, Hosokawa M, Takeshita S, Irino M, Higuchi K, Matsushita T, Tomita Y, Yasuhira K, Hamamoto H, Shimizu K, Ishii M, Yamamuro T (1981) A new murine model of accelerated senescence. Mech Ageing Dev 17:183–194CrossRefPubMedGoogle Scholar
  56. Takeda T, Hosokawa M, Higuchi K (1991) Senescence-accelerated mouse (SAM): a novel murine model of accelerated senescence. J Am Geriatr Soc 39:911–919CrossRefPubMedGoogle Scholar
  57. Takeda T, Matsushita T, Kurozumi M, Takemura K, Higuchi K, Hosokawa M (1997) Pathobiology of the senescence-accelerated mouse (SAM). Exp Gerontol 32:117–127CrossRefPubMedGoogle Scholar
  58. Tian Y, Wang H, Yuan F, Li N, Huang Q, He L, Wang L, Liu Z (2016) Perilla oil has similar protective effects of fish oil on high-fat diet-induced nonalcoholic fatty liver disease and gut dysbiosis. Biomed Res Int 2016:9462571.  https://doi.org/10.1155/2016/9462571 PubMedPubMedCentralGoogle Scholar
  59. Tsuduki T, Tokuyama Y, Igarashi M, Miyazawa T (2004) Tumor growth suppression by alpha-eleostearic acid, a linolenic acid isomer with a conjugated triene system, via lipid peroxidation. Carcinogenesis 25:1417–1425CrossRefGoogle Scholar
  60. Tsuduki T, Kambe T, Shibata A, Kawakami Y, Nakagawa K, Miyazawa T (2007) Conjugated EPA activates mutant p53 via lipid peroxidation and induces p53-dependent apoptosis in DLD-1 colorectal adenocarcinoma human cells. Biochim Biophys Acta 1771:20–30CrossRefGoogle Scholar
  61. Tsuduki T, Honma T, Nakagawa K, Ikeda I, Miyazawa T (2011) Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition 27(3):334–337.  https://doi.org/10.1016/j.nut.2010.05.017 CrossRefPubMedGoogle Scholar
  62. Tsuduki T, Kuriyama K, Nakagawa K, Miyazawa T (2013) Tocotrienol (unsaturated vitamin E) suppresses degranulation of mast cells and reduces allergic dermatitis in mice. J Oleo Sci 62:825–834CrossRefPubMedGoogle Scholar
  63. Van Hul M, Geurts L, Plovier H, Druart C, Everard A, Ståhlman M, Rhimi M, Chira K, Teissedre PL, Delzenne NM, Maguin E, Guilbot A, Brochot A, Gerard P, Bäckhed F, Cani PD (2017) Reduced obesity, diabetes and steatosis upon cinnamon and grape pomace are associated with changes in gut microbiota and markers of gut barrier. Am J Physiol Endocrinol Metab.  https://doi.org/10.1152/ajpendo.00107.2017 PubMedGoogle Scholar
  64. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71(3):495–548CrossRefPubMedPubMedCentralGoogle Scholar
  65. Vetrano S, Danese S (2013) Colitis, microbiota, and colon cancer: an infernal triangle. Gastroenterology 144(2):461–463.  https://doi.org/10.1053/j.gastro.2012.12.016 CrossRefPubMedGoogle Scholar
  66. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  67. Watanabe Y, Naito T, Kikuchi K, Amari Y, Uehara Y, Isonuma H, Hisaoka T, Yoshida T, Yaginuma K, Takaya N, Daida H, Hiramatsu K (2011) Infective endocarditis with Lactococcus garvieae in Japan: a case report. J Med Case Rep 5:356.  https://doi.org/10.1186/1752-1947-5-356 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Wijnhoven HA, Schilp J, van Bokhorst-de van der Schueren MA, de Vet HC, Kruizenga HM, Deeg DJ, Ferrucci L, Visser M (2012) Development and validation of criteria for determining undernutrition in community-dwelling older men and women: the short nutritional assessment questionnaire 65+. Clin Nutr 31:351–358.  https://doi.org/10.1016/j.clnu.2011.10.013 CrossRefPubMedGoogle Scholar
  69. Wong VW, Tse CH, Lam TT, Wong GL, Chim AM, Chu WC, Yeung DK, Law PT, Kwan HS, Yu J, Sung JJ, Chan HL (2013) Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis–a longitudinal study. PLoS ONE 8(4):e62885.  https://doi.org/10.1371/journal.pone.0062885 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yamamoto K, Kitano Y, Shuang E, Hatakeyama Y, Sakamoto Y, Honma T, Tsuduki T (2014) Decreased lipid absorption due to reduced pancreatic lipase activity in aging male mice. Biogerontology 15:463–473.  https://doi.org/10.1007/s10522-014-9512-5 CrossRefPubMedGoogle Scholar
  71. Yamamoto K, E S, Hatakeyama Y, Sakamoto Y, Tsuduki T (2015) High-fat diet intake from senescence inhibits the attenuation of cell functions and the degeneration of villi with aging in the small intestine, and inhibits the attenuation of lipid absorption ability in SAMP8 mice. J Clin Biochem Nutr 57(3):204–211.  https://doi.org/10.3164/jcbn.15-60 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Yamamoto K, Iwagaki Y, Watanabe K, Nochi T, Aso H, Tsuduki T (2018) Effects of a moderate-fat diet enriched with fish oil on intestinal lipid absorption in a senescence-accelerated prone mouse model. Nutrition 50:26–35.  https://doi.org/10.1016//j.nut.2017.10.015 CrossRefPubMedGoogle Scholar
  73. Zhan G, Yang N, Li S, Huang N, Fang X, Zhang J, Zhu B, Yang L, Yang C, Luo A (2018) Abnormal gut microbiota composition contributes to cognitive dysfunction in SAMP8 mice. Aging.  https://doi.org/10.18632/aging.101464 Google Scholar
  74. Zhang C, Li S, Yang L, Huang P, Li W, Wang S, Zhao G, Zhang M, Pang X, Yan Z, Liu Y, Zhao L (2013) Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat Commun 4:2163.  https://doi.org/10.1038/ncomms3163 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Zhang L, Wu WK, Gallo RL, Fang EF, Hu W, Ling TK, Shen J, Chan RL, Lu L, Luo XM, Li MX, Chan KM, Yu J, Wong VW, Ng SC, Wong SH, Chan FK, Sung JJ, Chan MT, Cho CH (2016) Critical role of antimicrobial peptide cathelicidin for controlling Helicobacter pylori survival and infection. J Immunol 196(4):1799–1809.  https://doi.org/10.4049/jimmunol.1500021 CrossRefPubMedGoogle Scholar
  76. Zhang W, Zhong W, Sun Q, Sun X, Zhou Z (2018) Adipose-specific lipin1 overexpression in mice protects against alcohol-induced liver injury. Sci Rep 8(1):408.  https://doi.org/10.1038/s41598-017-18837-2 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zhong Y, Nyman M, Fåk F (2015) Modulation of gut microbiota in rats fed high-fat diets by processing whole-grain barley to barley malt. Mol Nutr Food Res 59(10):2066–2076.  https://doi.org/10.1002/mnfr.201500187 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Kazushi Yamamoto
    • 1
  • Mamoru Kushida
    • 1
  • Tsuyoshi Tsuduki
    • 1
  1. 1.Laboratory of Food and Biomolecular Science, Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan

Personalised recommendations