Effect of a long-term high-protein diet on survival, obesity development, and gut microbiota in mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 310, Issue 11, 2016, Pages E886-E899

  Kiilerich, Pia ^a   Myrmel, Lene Secher ^a,b   Fjære, Even ^a,b   Hao, Qin ^a   Hugenholtz, Floor ^c   Sonne, Si Brask ^a   Derrien, Muriel ^c   Pedersen, Lone Møller ^a   Petersen, Rasmus Koefoed ^a   Mortensen, Alicja ^d   Licht, Tine Rask ^d   Rømer, Maria Unni ^a   Vogel, Ulla Birgitte ^e   Waagbø, Linn Jeanette ^b   Giallourou, Natasa ^c   Feng, Qiang ^f   Xiao, Liang ^f   Liu, Chuan ^f   Liaset, Bjørn ^b   Kleerebezem, Michiel ^c,g   Wang, Jun ^a,f,h,i,j   Madsen, Lise ^a,b,f   Kristiansen, Karsten ^a,f   more..

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e NATIONAL RESEARCH CENTRE FOR THE WORKING ENVIRONMENT   (Denmark)

^f BGI SHENZHEN   (China)

^g WAGENINGEN UNIVERSITY   (Netherlands)

^h KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

ⁱ MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

^j UNIVERSITY OF HONG KONG   (Hong Kong)

more..

Author keywords

Gut microbiota; High fat diet; High protein diet; Obesity; Survival

Indexed keywords

BACTERIAL DNA; CARBOHYDRATE; PROTEIN; SUCROSE; PROTEIN INTAKE; SUGAR INTAKE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENERGY; FAT CONTENT; FAT INTAKE; FECES MICROFLORA; FEEDING; FEMALE; GENE; GENE EXPRESSION; GLUCOSE TOLERANCE; INFLAMMATION; INTESTINE FLORA; LIFESPAN; LIPID DIET; LIPID STORAGE; LIVER; LOW FAT DIET; METABOLISM; MOUSE; NONHUMAN; OBESITY; ORAL GLUCOSE TOLERANCE TEST; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DIET; SURVIVAL; TISSUE EXPANSION; WEIGHT GAIN; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; LONGITUDINAL STUDY; PHARMACOKINETICS; PHYSIOLOGY; PROTEIN INTAKE; SUGAR INTAKE; SURVIVAL RATE;

ANIMALS; DIET, FAT-RESTRICTED; DIETARY PROTEINS; DIETARY SUCROSE; FEMALE; GASTROINTESTINAL MICROBIOME; LONGITUDINAL STUDIES; MICE; MICE, INBRED C57BL; OBESITY; SURVIVAL RATE;

EID: 84983631388     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00363.2015     Document Type: Article

References (52)

1. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semen- kovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101: 15718–15723, 2004.
2. Bluher M. Fat tissue and long life. Obesity Facts 1: 176–182, 2008.
3. Bluher M, Kahn BB, Kahn CR. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299: 572–574, 2003.
4. Braak CJFT, Smilauer P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5. 0. Ithaca, NY: Microcomputer Power, 2012, p. 496.
5. Cani PD, Bibiloni R, Knauf C, Neyrinck AM, Neyrinck AM, Delzenne NM, Burcelin R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470–1481, 2008.
6. Carmody RN, Gerber GK, Luevano JM Jr., Gatti DM, Somes L, Svenson KL, Turnbaugh PJ. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17: 72–84, 2015.
7. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HMB, 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. Gut microbiota composition correlates with diet and health in the elderly. Nature 488: 178–184, 2012.
8. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559–563, 2014.
9. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110: 9066–9071, 2013.
10. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257–258, 2007.
11. Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA 309: 71–82, 2013.
12. Freudenberg A, Petzke KJ, Klaus S. Dietary L-leucine and L-alanine supplementation have similar acute effects in the prevention of high-fat diet-induced obesity. Amino Acids 44: 519–528, 2013.
13. Geurts L, Lazarevic V, Derrien M, Everard A, Van Roye M, Knauf C, Valet P, Girard M, Muccioli GG, Francois P, de Vos WM, Schrenzel J, Delzenne NM, Cani PD. Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Front Microbiol 2: 149, 2011.
14. Hao Q, Lillefosse HH, Fjaere E, Myrmel LS, Midtbo LK, Jarlsby RH, Ma T, Jia B, Petersen RK, Sonne SB, Chwalibog A, Froyland L, Liaset B, Kristiansen K, Madsen L. High-glycemic index carbohydrates abrogate the antiobesity effect of fish oil in mice. Am J Physiol Endocrinol Metab 302: E1097–E1112, 2012.
15. Hariri N, Thibault L. High-fat diet-induced obesity in animal models. Nutr Res Rev 23: 270–299, 2010.
16. Harris RBS, Kor H. Insulin insensitivity is rapidly reversed in rats by reducing dietary-fat from 40-percent to 30-percent of energy. J Nutr 122: 1811–1822, 1992.
17. Harrison DE, Archer JR, Astle CM. Effects of food restriction on aging—separation of food-intake and adiposity. Proc Natl Acad Sci Biol 81: 1835–1838, 1984.
18. Hildebrand F, Ebersbach T, Nielsen HB, Li X, Sonne SB, Bertalan M, Dimitrov P, Madsen L, Qin J, Wang J, Raes J, Kristiansen K, Licht TR. A comparative analysis of the intestinal metagenomes present in guinea pigs (Cavia porcellus) and humans (Homo sapiens). BMC Genomics 13: 514, 2012.
19. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, Knight R, Ahima RS, Bushman F, Wu GD. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137: 1716–1724; e1711–e1712, 2009.
20. Hill JO, Melanson EL, Wyatt HT. Dietary fat intake and regulation of energy balance: Implications for obesity. J Nutr 130: 284s–288s, 2000.
21. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421: 182–187, 2003.
22. Keipert S, Voigt A, Klaus S. Dietary effects on body composition, glucose metabolism, and longevity are modulated by skeletal muscle mitochondrial uncoupling in mice. Aging Cell 10: 122–136, 2011.
23. Lahti L, Elo LL, Aittokallio T, Kaski S. Probabilistic analysis of probe reliability in differential gene expression studies with short oligonucleo- tide arrays. Ieee Acm T Comput Bi 8: 217–225, 2011.
24. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto JM, Kennedy S, Leonard P, Li J, Burgdorf K, Grarup N, Jorgensen T, Brandslund I, Nielsen HB, Juncker AS, Bertalan M, Levenez F, Pons N, Rasmussen S, Sunagawa S, Tap J, Tims S, Zoetendal EG, Brunak S, Clement K, Dore J, Kleerebezem M, Kristiansen K, Renault P, Sicheritz-Ponten T, de Vos WM, Zucker JD, Raes J, Hansen T, Bork P, Wang J, Ehrlich SD, Pedersen O. Richness of human gut microbiome correlates with metabolic markers. Nature 500: 541–546, 2013.
25. Levine ME, Suarez JA, Brandhorst S, Balasubramanian P, Cheng CW, Madia F, Fontana L, Mirisola MG, Guevara-Aguirre J, Wan J, Passarino G, Kennedy BK, Wei M, Cohen P, Crimmins EM, Longo VD. Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older popu- lation. Cell Metab 19: 407–417, 2014.
26. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070–11075, 2005.
27. Li H, Durbin R. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25: 1754–1760, 2009.
28. Li R, Grimm SA, Chrysovergis K, Kosak J, Wang X, Du Y, Burk- holder A, Janardhan K, Mav D, Shah R, Eling TE, Wade PA. Obesity, rather than diet, drives epigenomic alterations in colonic epithelium resembling cancer progression. Cell Metab 19: 702–711, 2014.
29. Liang H, Masoro EJ, Nelson JF, Strong R, McMahan CA, Richardson A. Genetic mouse models of extended lifespan. Experimental Gerontology 38: 1353–1364, 2003.
30. Ma T, Liaset B, Hao Q, Petersen RK, Fjaere E, Ngo HT, Lillefosse HH, Ringholm S, Sonne SB, Treebak JT, Pilegaard H, Froyland L, Kristiansen K, Madsen L. Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice. PLoS One 6: e21647, 2011.
31. Madsen L, Kristiansen K. The importance of dietary modulation of cAMP and insulin signaling in adipose tissue and the development of obesity. Ann NY Acad Sci 1190: 1–14, 2010.
32. Madsen L, Pedersen LM, Liaset B, Ma T, Petersen RK, van den Berg S, Pan J, Muller-Decker K, Dulsner ED, Kleemann R, Kooistra T, Doskeland SO, Kristiansen K. cAMP-dependent signaling regulates the adipogenic effect of n-6 polyunsaturated fatty acids. J Biol Chem 283: 7196–7205, 2008.
33. Morens C, Keijzer M, de Vries K, Scheurink A, van Dijk G. Effects of high-fat diets with different carbohydrate-to-protein ratios on energy homeostasis in rats with impaired brain melanocortin receptor activity. Am J Physiol Regul Integr Comp Physiol 289: R156–R163, 2005.
34. Ottaviani E, Ventura N, Mandrioli M, Candela M, Franchini A, Franceschi C. Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. Biogerontology 12: 599–609, 2011.
35. Pettersson US, Walden TB, Carlsson PO, Jansson L, Phillipson M. Female mice are protected against high-fat diet induced metabolic syndrome and increase the regulatory t cell population in adipose tissue. PLoS One 7: 2012.
36. Pichon L, Huneau JF, Fromentin G, Tome D. A high-protein, high-fat, carbohydrate-free diet reduces energy intake, hepatic lipogenesis, and adiposity in rats. J Nutr 136: 1256–1260, 2006.
37. Qin JJ, Li YR, Cai ZM, Li SH, Zhu JF, Zhang F, Liang SS, Zhang WW, Guan YL, Shen DQ, Peng YQ, Zhang DY, Jie ZY, Wu WX, Qin YW, Xue WB, Li JH, Han LC, Lu DH, Wu PX, Dai YL, Sun XJ, Li ZS, Tang AF, Zhong SL, Li XP, Chen WN, Xu R, Wang MB, Feng Q, Gong MH, Yu J, Zhang YY, Zhang M, Hansen T, Sanchez G, Raes J, Falony G, Okuda S, Almeida M, LeChatelier E, Renault P, Pons N, Batto JM, Zhang ZX, Chen H, Yang RF, Zheng WM, Li SG, Yang HM, Wang J, Ehrlich SD, Nielsen R, Pedersen O, Kristiansen K, Wang J. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55–60, 2012.
38. Rajilic-Stojanovic M, Heilig HGHJ, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol 11: 1736–1751, 2009.
39. Regan JC, Partridge L. Gender and longevity: why do men die earlier than women? Comparative and experimental evidence. Best Pract Res Clin Endocrinol Metab 27: 467–479, 2013.
40. Ridaura VK, Faith JJ, Rey FE, Cheng JY, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341: 1079–1049, 2013.
41. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140, 2010.
42. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell 148: 852–871, 2012.
43. Solon-Biet SM, McMahon AC, Ballard JWO, Ruohonen K, Wu LE, Cogger VC, Warren A, Huang X, Pichaud N, Melvin RG, Gokarn R, Khalil M, Turner N, Cooney GJ, Sinclair DA, Raubenheimer D, Le Couteur DG, Simpson SJ. The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab 19: 418–430, 2014.
44. Solon-Biet SM, Walters KA, Simanainen UK, McMahon AC, Ruo- honen K, Ballard JW, Raubenheimer D, Handelsman DJ, Le Couteur DG, Simpson SJ. Macronutrient balance, reproductive function, and lifespan in aging mice. Proc Natl Acad Sci USA 112: 3481–3486, 2015.
45. Sovran B, Loonen LM, Lu P, Hugenholtz F, Belzer C, Stolte EH, Boekschoten MV, van Baarlen P, Kleerebezem M, de Vos P, Dekker J, Renes IB, Wells JM. IL-22-STAT3 pathway plays a key role in the maintenance of ileal homeostasis in mice lacking secreted mucus barrier. Inflamm Bowel Dis 21: 531–542, 2015.
46. Tiihonen K, Ouwehand AC, Rautonen N. Human intestinal microbiota and healthy ageing. Ageing Res Rev 9: 107–116, 2010.
47. Turnbaugh PJ, Baeckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3: 213–223, 2008.
48. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027–1031, 2006.
49. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1: 2009.
50. Turner N, Kowalski GM, Leslie SJ, Risis S, Yang C, Lee-Young RS, Babb JR, Meikle PJ, Lancaster GI, Henstridge DC, White PJ, Krae- gen EW, Marette A, Cooney GJ, Febbraio MA, Bruce CR. Distinct patterns of tissue-specific lipid accumulation during the induction of insulin resistance in mice by high-fat feeding. Diabetologia 56: 1638–1648, 2013.
51. Xiao L, Feng Q, Liang S, Sonne SB, Xia Z, Qiu X, Li X, Long H, Zhang J, Zhang D, Liu C, Fang Z, Chou J, Glanville J, Hao Q, Kotowska D, Colding C, Licht TR, Wu D, Yu J, Sung JJ, Liang Q, Li J, Jia H, Lan Z, Tremaroli V, Dworzynski P, Nielsen HB, Backhed F, Dore J, Le Chatelier E, Ehrlich SD, Lin JC, Arumugam M, Wang J, Madsen L, Kristiansen K. A catalog of the mouse gut metagenome. Nat Biotechnol 33: 1103–1108, 2015.
52. Zhang C, Li S, Yang L, Huang P, Li W, Wang S, Zhao G, Zhang M, Pang X, Yan Z, Liu Y, Zhao L. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat Commun 4: 2163, 2013.