The effects of graded levels of calorie restriction: IX. Global metabolomic screen reveals modulation of carnitines, sphingolipids and bile acids in the liver of C57BL/6 mice

Aging Cell

Volumn 16, Issue 3, 2017, Pages 529-540

  Green, Cara L ^a   Mitchell, Sharon E ^a   Derous, Davina ^a   Wang, Yingchun ^b   Chen, Luonan ^c   Han, Jing Dong J ^d   Promislow, Daniel E L ^e   Lusseau, David ^a   Douglas, Alex ^a   Speakman, John R ^a,b  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^c INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^d Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

aging; bile acid; calorie restriction; carnitine; Metabolomics; sphingolipid

Indexed keywords

ASPARAGINE; BETAINE; BILE ACID; CARNITINE; CATALASE; CERAMIDE; CYSTEINE; FATTY ACID; GLUTAMINE; GLYCEROPHOSPHOLIPID; LEPTIN; LONG CHAIN FATTY ACID; MAJOR URINARY PROTEIN; METHIONINE; NERVE GROWTH FACTOR; NICOTINAMIDE; PHENYLALANINE; PHOSPHOLIPASE; PYRIMIDINE; SATURATED FATTY ACID; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TAUROCHENODEOXYCHOLIC ACID; TAUROCHOLIC ACID; UNCLASSIFIED DRUG; LYSOPHOSPHOLIPID; MAJOR URINARY PROTEINS; PROTEIN; SOMATOMEDIN C; SPHINGOSINE 1-PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY MASS; BODY TEMPERATURE; CALORIC RESTRICTION; COMPARATIVE STUDY; CONTROLLED STUDY; FEEDING; FOOD INTAKE; LIVER METABOLISM; MALE; METABOLOMICS; MOUSE; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; AGING; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DRUG EFFECTS; EATING; GENE EXPRESSION REGULATION; GENETICS; LIVER; METABOLISM; PHYSIOLOGY;

AGING; ANIMALS; BILE ACIDS AND SALTS; CALORIC RESTRICTION; CARNITINE; CATALASE; EATING; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR I; LEPTIN; LIVER; LYSOPHOSPHOLIPIDS; MALE; METABOLOMICS; METHIONINE; MICE; MICE, INBRED C57BL; PROTEINS; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; SPHINGOSINE;

EID: 85011067845     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12570     Document Type: Article

References (88)

1. Babenko NA, Shakhova EG (2014) Long-term food restriction prevents aging-associated sphingolipid turnover dysregulation in the brain. Arch. Gerontol. Geriatr. 58, 420–426.
2. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B (Methodological) 57, 289–300.
3. Bertolotti M, Gabbi C, Anzivino C, Crestani M, Mitro N, Del Puppo M, Godio C, De Fabiani E, Macchioni D, Carulli L, Rossi A, Ricchi M, Loria P, Carulli N (2007) Age-related changes in bile acid synthesis and hepatic nuclear receptor expression. Eur. J. Clin. Invest. 37, 501–508.
4. Blanchard G, Paragon BM, Milliat F, Lutton C (2002) Dietary L-carnitine supplementation in obese cats alters carnitine metabolism and decreases ketosis during fasting and induced hepatic lipidosis. J. Nutr. 132, 204–210.
5. Bozdogan H (1987) Model selection and Akaike's Information Criterion (AIC): The general theory and its analytical extensions. Psychometrika 52, 345–370.
6. Bruss MD, Khambatta CF, Ruby MA, Aggarwal I, Hellerstein MK (2010) Calorie restriction increases fatty acid synthesis and whole body fat oxidation rates. Am. J. Physiol. Endocrinol. Metab. 298, E108–E116.
7. Chiang JYL (2013) Bile acid metabolism and signaling. Comp. Physiol. 3, 1191–1212.
8. Collino S, Martin F-PJ, Montoliu I, Barger JL, Da Silva L, Prolla TA, Weindruch R, Kochhar S (2013) Transcriptomics and metabonomics identify essential metabolic signatures in calorie restriction (CR) regulation across multiple mouse strains. Metabolites 3, 881–911.
9. Colman RJ, Beasley TM, Kemnitz JW, Johnson SC, Weindruch R, Anderson RM (2014) Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nat. Commun. 5, 3557.
10. Conti B, Sanchez-Alavez M, Winsky-Sommerer R, Morale MC, Lucero J, Brownell S, Fabre V, Huitron-Resendiz S, Henriksen S, Zorrilla EP, de Lecea L, Bartfai T (2006) Transgenic mice with a reduced core body temperature have an increased life span. Science 314.
11. de la Cruz J, Burón I, Roncero I (1990) Morphological and functional studies during aging at mitochondrial level. Action of drugs. Int. J. Biochem. Biotechnol. 22, 729–735.
12. De Guzman JM, Ku G, Fahey R, Youm Y-H, Kass I, Ingram DK, Dixit VD, Kheterpal I (2013) Chronic caloric restriction partially protects against age-related alteration in serum metabolome. Age (Dordrecht, Netherlands) 35, 1091–1104.
13. De Livera AM, Bowne JB (2013) Metabolomics: A collection of functions for analysing metabolomics data. R package version 0.1.3. R package.
14. Derous D, Mitchell SE, Green CL, Chen L, Han JJ, Wang Y, Promislow DE, Lusseau D, Speakman JR, Douglas A (2016) The effects of graded levels of calorie restriction: VI. Impact of short-term graded calorie restriction on transcriptomic responses of the hypothalamic hunger and circadian signaling pathways. Aging 8, 642–661.
15. Dong J, Wang H, Wu G, Zhao J, Zhang L, Zuo L, Zhu W, Gong J, Li Y, Gu L, Li J (2014) Oral treatment with SEW2871, a sphingosine-1-phosphate type 1 receptor agonist, ameliorates experimental colitis in interleukin-10 gene deficient mice. Clin. Exp. Immunol. 177, 94–101.
16. Dumitru CA, Zhang Y, Li X, Gulbins E (2007) Ceramide: a novel player in reactive oxygen species-induced signaling? Antioxid. Redox Signal. 9, 1535–1540.
17. van Echten-Deckert G, Hagen-Euteneuer N, Karaca I, Walter J (2014) Sphingosine-1-phosphate: boon and bane for the brain. Cell. Physiol. Biochem. 34, 148–157.
18. Ferland G, Tuchweber B, Perea A, Yousef IM (1989) Effect of aging and dietary restriction on bile acid metabolism in rats. Lipids 24, 842–848.
19. Ferreira JA (2007) The Benjamini-Hochberg method in the case of discrete test statistics. Int. J. Biostat. 3, Article 11.
20. Flanagan JL, Simmons PA, Vehige J, Willcox MD, Garrett Q (2010) Role of carnitine in disease. Nutr. Metab. 7, 30.
21. Fok WC, Bokov A, Gelfond J, Yu Z, Zhang Y, Doderer M, Chen Y, Javors M, Wood WH, Zhang Y, Becker KG, Richardson A, Pérez VI (2014) Combined treatment of rapamycin and dietary restriction has a larger effect on the transcriptome and metabolome of liver. Aging Cell 13, 311–319.
22. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span–from yeast to humans. Science 328, 321–326.
23. Friedman JM (2011) Leptin and the regulation of body weight. Keio J. Med. 60, 1–9.
24. Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid. Redox Signal. 15, 1583–1606.
25. Ge P, Cui Y, Liu F, Luan J, Zhou X, Han J (2015) L-carnitine affects osteoblast differentiation in NIH3T3 fibroblasts by the IGF-1/PI3K/Akt signalling pathway. Biosci. Trends 9, 42–48.
26. Gomez-Muñoz A, Presa N, Gomez-Larrauri A, Rivera I-G, Trueba M, Ordoñez M (2015) Control of inflammatory responses by ceramide, sphingosine 1-phosphate and ceramide 1-phosphate. Prog. Lipid Res. 61, 51–62.
27. Gromski PS, Xu Y, Kotze HL, Correa E, Ellis DI, Armitage EG, Turner ML, Goodacre R (2014) Influence of missing values substitutes on multivariate analysis of metabolomics data. Metabolites 4, 433–452.
28. Herbener GH (1976) A morphometric study of age-dependent changes in mitochondrial population of mouse liver and heart. J. Gerontol. 31, 8–12.
29. Hoffman JM, Soltow QA, Li S, Sidik A, Jones DP, Promislow DEL (2014) Effects of age, sex, and genotype on high-sensitivity metabolomic profiles in the fruit fly, Drosophila melanogaster. Aging Cell 13, 596–604.
30. Huan T, Li L (2015) Counting missing values in a metabolite-intensity data set for measuring the analytical performance of a metabolomics platform. Anal. Chem. 87, 1306–1313.
31. Huang X, Withers BR, Dickson RC (2014) Sphingolipids and lifespan regulation. Biochim. Biophys. Acta 1841, 657–664.
32. Javitt NB (1994) Bile acid synthesis from cholesterol: regulatory and auxiliary pathways. FASEB J. 8, 1308–1311.
33. Johnson SC, Rabinovitch PS, Kaeberlein M (2013) mTOR is a key modulator of ageing and age-related disease. Nature 493, 338–345.
34. Jové M, Naudí A, Ramírez-Núñez O, Portero-Otín M, Selman C, Withers DJ, Pamplona R (2014) Caloric restriction reveals a metabolomic and lipidomic signature in liver of male mice. Aging Cell 13, 828–837.
35. Jun DJ, Lee JH, Choi BH, Koh TK, Ha DC, Jeong MW, Kim KT (2006) Sphingosine-1-phosphate modulates both lipolysis and leptin production in differentiated rat white adipocytes. Endocrinology 147, 5835–5844.
36. Keil G, Cummings E, de Magalhães JP (2015) Being cool: how body temperature influences ageing and longevity. Biogerontology 16, 383–397.
37. Keller J, Couturier A, Haferkamp M, Most E, Eder K (2013) Supplementation of carnitine leads to an activation of the IGF-1/PI3K/Akt signalling pathway and down regulates the E3 ligase MuRF1 in skeletal muscle of rats. Nutr. Metab. 10, 28.
38. Kim S-S, Choi K-M, Kim S, Park T, Cho I-C, Lee J-W, Lee C-K (2016) Whole-transcriptome analysis of mouse adipose tissue in response to short-term caloric restriction. Mol. Genet. Genomics 291, 831–847.
39. Kirkwood TBL (2008) A systematic look at an old problem. Nature 451, 644–647.
40. Knopf JL, Gallagher JF, Held WA (1983) Differential, multihormonal regulation of the mouse major urinary protein gene family in the liver. Mol. Cell. Biol. 3, 2232–2240.
41. Krajcovicová-Kudlácková M, Simoncic R, Béderová A, Babinská K, Béder I (2000) Correlation of carnitine levels to methionine and lysine intake. Physiol. Res. 49, 399–402.
42. Kuhla A, Hahn S, Butschkau A, Lange S, Wree A, Vollmar B (2014) Lifelong caloric restriction reprograms hepatic fat metabolism in mice. J. Gerontol. A Biol. Sci. Med. Sci. 69, 915–922.
43. Lecour S, Van der Merwe E, Opie LH, Sack MN (2006) Ceramide attenuates hypoxic cell death via reactive oxygen species signaling. J. Cardiovasc. Pharmacol. 47, 158–163.
44. Levin BE, Dunn-Meynell AA, Routh VH (1999) Brain glucose sensing and body energy homeostasis: role in obesity and diabetes. Am. J. Physiol. 276, R1223–R1231.
45. Li S, Pozhitkov A, Ryan RA, Manning CS, Brown-Peterson N, Brouwer M (2010) Constructing a fish metabolic network model. Genome Biol. 11, R115.
46. Li S, Park Y, Duraisingham S, Strobel FH, Khan N, Soltow Qa, Jones DP, Pulendran B (2013) Predicting network activity from high throughput metabolomics. PLoS Comput. Biol. 9, e1003123.
47. Lightle SA, Oakley JI, Nikolova-Karakashian MN (2000) Activation of sphingolipid turnover and chronic generation of ceramide and sphingosine in liver during aging. Mech. Ageing Dev. 120, 111–125.
48. Meijer AJ (2003) Amino acids as regulators and components of nonproteinogenic pathways. J. Nutr. 133(6 Suppl 1), 2057S–2062S.
49. Mingorance C, Duluc L, Chalopin M, Simard G, Ducluzeau P-H, Herrera MD, Alvarez de Sotomayor M, Andriantsitohaina R (2012) Propionyl-L-carnitine corrects metabolic and cardiovascular alterations in diet-induced obese mice and improves liver respiratory chain activity. PLoS ONE 7, e34268.
50. Mitchell SE, Delville C, Konstantopedos P, Derous D, Green CL, Chen L, Han J-DJ, Wang Y, Promislow DEL, Douglas A, Lusseau D, Speakman JR (2015a) The effects of graded levels of calorie restriction: III. Impact of short term calorie and protein restriction on mean daily body temperature and torpor use in the C57BL/6 mouse. Oncotarget 6, 18314–18337.
51. Mitchell SE, Delville C, Konstantopedos P, Hurst J, Derous D, Green C, Chen L, Han JJD, Wang Y, Promislow DEL, Lusseau D, Douglas A, Speakman JR (2015b) The effects of graded levels of calorie restriction: II. Impact of short term calorie and protein restriction on circulating hormone levels, glucose homeostasis and oxidative stress in male C57BL/6 mice. Oncotarget 6, 23213–23237.
52. Mitchell SE, Tang Z, Kerbois C, Delville C, Konstantopedos P, Bruel A, Derous D, Green C, Aspden RM, Goodyear SR, Chen L, Han JJD, Wang Y, Promislow DEL, Lusseau D, Douglas A, Speakman JR (2015c) The effects of graded levels of calorie restriction: I. impact of short term calorie and protein restriction on body composition in the C57BL/6 mouse. Oncotarget 6, 15902–15930.
53. Mitchell SE, Delville C, Konstantopedos P, Derous D, Green CL, Wang Y, Han J-DJ, Promislow DEL, Douglas A, Chen L, Lusseau D, Speakman JR (2016a) The effects of graded levels of calorie restriction: V. Impact of short term calorie and protein restriction on physical activity in the C57BL/6 mouse. Oncotarget, 7, 19147–19170.
54. Mitchell SJ, Madrigal-Matute J, Scheibye-Knudsen M, Fang E, Aon M, González-Reyes JA, Cortassa S, Kaushik S, Gonzalez-Freire M, Patel B, Wahl D, Ali A, Calvo-Rubio M, Burón MI, Guiterrez V, Ward TM, Palacios HH, Cai H, Frederick DW, Hine C, Broeskamp F, Habering L, Dawson J, Beasley TM, Wan J, Ikeno Y, Hubbard G, Becker KG, Zhang Y, Bohr VA, Longo DL, Navas P, Ferrucci L, Sinclair DA, Cohen P, Egan JM, Mitchell JR, Baur JA, Allison DB, Anson RM, Villalba JM, Madeo F, Cuervo AM, Pearson KJ, Ingram DK, Bernier M, de Cabo R (2016b) Effects of Sex, Strain, and Energy Intake on Hallmarks of Aging in Mice. Cell Metab. 23, 1093–1112.
55. Navé BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem. J. 344, 427–431.
56. Nogueira LM, Lavigne JA, Chandramouli GVR, Lui H, Barrett JC, Hursting SD (2012) Dose-dependent effects of calorie restriction on gene expression, metabolism, and tumor progression are partially mediated by insulin-like growth factor-1. Cancer Med. 1, 275–288.
57. Pekala J, Patkowska-Sokoła B, Bodkowski R, Jamroz D, Nowakowski P, Lochyński S, Librowski T (2011) L-carnitine–metabolic functions and meaning in humans life. Curr. Drug Metab. 12, 667–678.
58. Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package.
59. Plank M, Wuttke D, van Dam S, Clarke SA, de Magalhães JP (2012) A meta-analysis of caloric restriction gene expression profiles to infer common signatures and regulatory mechanisms. Mol. BioSyst. 8, 1339–1349.
60. Qi Y, Jiang C, Cheng J, Krausz KW, Li T, Ferrell JM, Gonzalez FJ, Chiang JYL (2015) Bile acid signaling in lipid metabolism: metabolomic and lipidomic analysis of lipid and bile acid markers linked to anti-obesity and anti-diabetes in mice. Biochim. Biophys. Acta 1851, 19–29.
61. R Core Team (2015) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
62. Rector RS, Thyfault JP, Uptergrove GM, Morris EM, Naples SP, Borengasser SJ, Mikus CR, Laye MJ, Laughlin MH, Booth FW, Ibdah JA (2010) Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model. J. Hepatol. 52, 727–736.
63. Regev A, Schiff ER (2001) Liver disease in the elderly. Gastroenterol. Clin. North Am. 30, 547–563, x–xi.
64. Rosen ED, Spiegelman BM (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847–853.
65. Schmucker DL, Sanchez H (2011) Liver regeneration and aging: a current perspective. Curr. Gerontol. Geriatr. Res. 2011, 1–8.
66. Selman C, Kerrison ND, Cooray A, Piper MDW, Lingard SJ, Barton RH, Schuster EF, Blanc E, Gems D, Nicholson JK, Thornton JM, Partridge L, Withers DJ (2006) Coordinated multitissue transcriptional and plasma metabonomic profiles following acute caloric restriction in mice. Physiol. Genomics 27, 187–200.
67. Sepe A, Tchkonia T, Thomou T, Zamboni M, Kirkland JL (2011) Aging and regional differences in fat cell progenitors - a mini-review. Gerontology 57, 66–75.
68. Shaham O, Wei R, Wang TJ, Ricciardi C, Lewis GD, Vasan RS, Carr SA, Thadhani R, Gerszten RE, Mootha VK (2008) Metabolic profiling of the human response to a glucose challenge reveals distinct axes of insulin sensitivity. Mol. Syst. Biol. 4, 214.
69. Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J. Clin. Investig. 116, 1793–1801.
70. Silva VRR, Micheletti TO, Pimentel GD, Katashima CK, Lenhare L, Morari J, Mendes MCS, Razolli DS, Rocha GZ, de Souza CT, Ryu D, Prada PO, Velloso LA, Carvalheira JBC, Pauli JR, Cintra DE, Ropelle ER (2014) Hypothalamic S1P/S1PR1 axis controls energy homeostasis. Nat. Commun. 5, 4859.
71. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3 Article 3.
72. Speakman JR, Mitchell SE (2011) Caloric restriction. Mol. Aspects Med. 32, 159–221.
73. Speakman JR, Mitchell SE, Mazidi M (2016) Calories or protein? The effect of dietary restriction on lifespan in rodents is explained by calories alone Exp. Gerontol. 86, 28–38.
74. Stekhoven DJ (2011) Using the missForest Package. R package, pp. 1–11.
75. Stekhoven DJ, Bühlmann P (2012) MissForest–non-parametric missing value imputation for mixed-type data. Bioinformatics (Oxford, England) 28, 112–118.
76. Swindell WR (2012) Dietary restriction in rats and mice: a meta-analysis and review of the evidence for genotype-dependent effects on lifespan. Ageing Res. Rev. 11, 254–270.
77. Tosato M, Zamboni V, Ferrini A, Cesari M (2007) The aging process and potential interventions to extend life expectancy. Clin. Interv. Aging 2, 401–412.
78. Turturro A, Witt WW, Lewis S, Hass BS, Lipman RD, Hart RW (1999) Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. A Biol. Sci. Med. Sci. 54, B492–B501.
79. Van Brocklyn JR, Williams JB (2012) The control of the balance between ceramide and sphingosine-1-phosphate by sphingosine kinase: oxidative stress and the seesaw of cell survival and death. Comp. Biochem. Physiol. Biochem. Mol. Biol. 163, 26–36.
80. Wanichthanarak K, Fahrmann FJ, Grapov D (2015) Genomic, proteomic, and metabolomic data integration strategies. Biomark. Insights 10, 1–6.
81. Wei Y, Wang D, Topczewski F, Pagliassotti MJ (2007) Fructose-mediated stress signaling in the liver: implications for hepatic insulin resistance. J. Nutr. Biochem. 18, 1–9.
82. Weindruch R, Walford RL (1988) The Retardation of Aging and Disease by Dietary Restriction. Springfield, IL, USA: Charles C Thomas Pub Ltd.
83. Westerhuis JA, van Velzen EJJ, Hoefsloot HCJ, Smilde AK (2010) Multivariate paired data analysis: multilevel PLSDA versus OPLSDA. Metabolomics 6, 119–128.
84. Xu Y-C, Yang D-B, Speakman JR, Wang D-H (2014) Oxidative stress in response to natural and experimentally elevated reproductive effort is tissue dependent J Blount (ed.). Funct. Ecol. 28, 402–410.
85. Yang G, Badeanlou L, Bielawski J, Roberts AJ, Hannun YA, Samad F (2009) Central role of ceramide biosynthesis in body weight regulation, energy metabolism, and the metabolic syndrome. Am. J. Physiol. Endocrinol. Metab. 297, E211–E224.
86. Yu BP, Masoro EJ, McMahan CA (1985) Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J. Gerontol. 40, 657–670.
87. Zhang Y, Edwards PA (2008) FXR signaling in metabolic disease. FEBS Lett. 582, 10–18.
88. Zheng S, Hoos L, Cook J, Tetzloff G, Davis H, van Heek M, Hwa JJ (2008) Ezetimibe improves high fat and cholesterol diet-induced non-alcoholic fatty liver disease in mice. Eur. J. Pharmacol. 584, 118–124.