Skip to main content
SpringerLink
Log in

Whole-transcriptome analysis of mouse adipose tissue in response to short-term caloric restriction

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Caloric restriction (CR) has been shown to extend the lifespan of many species by improving cellular function and organismal health. Additionally, fat reduction by CR may play an important role in lengthening lifespan and preventing severe age-related diseases. Interestingly, CR induced the greatest transcriptome change in the epididymal fat of mice in our study. In this transcriptome analysis, we identified and categorized 446 genes that correlated with CR level. We observed down-regulation of several signaling pathways, including insulin/insulin-like growth factor 1 (insulin/IGF-1), epidermal growth factor (EGF), transforming growth factor beta (TGF-β), and canonical wingless-type mouse mammary tumor virus integration site (Wnt). Many genes related to structural features, including extracellular matrix structure, cell adhesion, and the cytoskeleton, were down-regulated, with a strong correlation to the degree of CR. Furthermore, genes related to the cell cycle and adipogenesis were down-regulated. These biological processes are well-identified targets of insulin/IGF-1, EGF, TGF-β, and Wnt signaling. In contrast, genes involved in specific metabolic processes, including the tricarboxylic acid cycle and the electron transport chain were up-regulated. We performed in silico analysis of the promoter sequences of CR-responsive genes and identified two associated transcription factors, Paired-like homeodomain 2 (Pitx2) and Paired box gene 6 (Pax6). Our results suggest that strict regulation of signaling pathways is critical for creating the optimal energy homeostasis to extend lifespan.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CR:

Caloric restriction

IGF:

Insulin-like growth factor

EGF:

Epidermal growth factor

ErbB:

Erythroblastic leukemia viral oncogene homolog

TGF- β:

Transforming growth factor beta

Wnt:

Wingless-type mouse mammary tumor virus integration site

ECM:

Extracellular matrix

TCA:

Tricarboxylic acid

ETC:

Eletron transport chain

References

  • Abdollahi A (2007) LOT1 (ZAC1/PLAGL1) and its family members: mechanisms and functions. J Cell Physiol 210(1):16–25

    Article  CAS  PubMed  Google Scholar 

  • Abe T, Nakajima A, Satoh N, Ohkoshi M, Sakuragi S, Koizumi A (2001) Suppression of experimental autoimmune uveoretinitis by dietary calorie restriction. Jpn J Ophthalmol 45(1):46–52

    Article  CAS  PubMed  Google Scholar 

  • Aga-Mizrachi S, Brutman-Barazani T, Jacob AI, Bak A, Elson A, Sampson SR (2008) Cytosolic protein tyrosine phosphatase-epsilon is a negative regulator of insulin signaling in skeletal muscle. Endocrinology 149(2):605–614

    Article  CAS  PubMed  Google Scholar 

  • Barzilai N, Gabriely I (2001) The role of fat depletion in the biological benefits of caloric restriction. J Nutr 131(3):903S–906S

    CAS  PubMed  Google Scholar 

  • Barzilai N, Gupta G (1999) Revisiting the role of fat mass in the life extension induced by caloric restriction. J Gerontol A Biol Sci Med Sci 54(3):B89–B96 (discussion B97-88)

    Article  CAS  PubMed  Google Scholar 

  • Barzilai N, She L, Liu BQ, Vuguin P, Cohen P, Wang J, Rossetti L (1999) Surgical removal of visceral fat reverses hepatic insulin resistance. Diabetes 48(1):94–98

    Article  CAS  PubMed  Google Scholar 

  • Bertrand HA, Lynd FT, Masoro EJ, Yu BP (1980) Changes in adipose mass and cellularity through the adult life of rats fed ad libitum or a life-prolonging restricted diet. J Gerontol 35(6):827–835

    Article  CAS  PubMed  Google Scholar 

  • Bluher M, Michael MD, Peroni OD, Ueki K, Carter N, Kahn BB, Kahn CR (2002) Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell 3(1):25–38

    Article  CAS  PubMed  Google Scholar 

  • Bluher M, Kahn BB, Kahn CR (2003) Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299(5606):572–574

    Article  PubMed  CAS  Google Scholar 

  • Borisov N, Aksamitiene E, Kiyatkin A, Legewie S, Berkhout J, Maiwald T, Kaimachnikov NP, Timmer J, Hoek JB, Kholodenko BN (2009) Systems-level interactions between insulin-EGF networks amplify mitogenic signaling. Mol Syst Biol 5:256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Briata P, Ilengo C, Corte G, Moroni C, Rosenfeld MG, Chen CY, Gherzi R (2003) The Wnt/beta-catenin–> Pitx2 pathway controls the turnover of Pitx2 and other unstable mRNAs. Mol Cell 12(5):1201–1211

    Article  CAS  PubMed  Google Scholar 

  • Carey JR, Liedo P, Harshman L, Zhang Y, Muller HG, Partridge L, Wang JL (2002) Life history response of Mediterranean fruit flies to dietary restriction. Aging Cell 1(2):140–148

    Article  CAS  PubMed  Google Scholar 

  • Chen XW, Leto D, Xiong T, Yu G, Cheng A, Decker S, Saltiel AR (2011) A Ral GAP complex links PI 3-kinase/Akt signaling to RalA activation in insulin action. Mol Biol Cell 22(1):141–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen JY, Lin JR, Cimprich KA, Meyer T (2012) A two-dimensional ERK-AKT signaling code for an NGF-triggered cell-fate decision. Mol Cell 45(2):196–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiba T, Ezaki O (2010) Dietary restriction suppresses inflammation and delays the onset of stroke in stroke-prone spontaneously hypertensive rats. Biochem Biophys Res Commun 399(1):98–103

    Article  CAS  PubMed  Google Scholar 

  • Choi JS, Lee CK (2013) Maintenance of cellular ATP level by caloric restriction correlates chronological survival of budding yeast. Biochem Biophys Res Commun 439(1):126–131

    Article  CAS  PubMed  Google Scholar 

  • Choi JS, Choi KM, Lee CK (2011) Caloric restriction improves efficiency and capacity of the mitochondrial electron transport chain in Saccharomyces cerevisiae. Biochem Biophys Res Commun 409(2):308–314

    Article  CAS  PubMed  Google Scholar 

  • Choi KM, Kwon YY, Lee CK (2015) Disruption of Snf3/Rgt2 glucose sensors decreases lifespan and caloric restriction effectiveness through Mth1/Std1 by adjusting mitochondrial efficiency in yeast. FEBS Lett 589(3):349–357

    Article  CAS  PubMed  Google Scholar 

  • Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A (2009) Adipogenesis and WNT signalling. Trends Endocrinol Metab 20(1):16–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chujo Y, Fujii N, Okita N, Konishi T, Narita T, Yamada A, Haruyama Y, Tashiro K, Chiba T, Shimokawa I, Higami Y (2013) Caloric restriction-associated remodeling of rat white adipose tissue: effects on the growth hormone/insulin-like growth factor-1 axis, sterol regulatory element binding protein-1, and macrophage infiltration. Age (Dordr) 35(4):1143–1156

    Article  CAS  Google Scholar 

  • Cooper TM, Mockett RJ, Sohal BH, Sohal RS, Orr WC (2004) Effect of caloric restriction on life span of the housefly, Musca domestica. FASEB J 18(13):1591–1593

    CAS  PubMed  Google Scholar 

  • Coppack SW, Fisher RM, Gibbons GF, Humphreys SM, McDonough MJ, Potts JL, Frayn KN (1990) Postprandial substrate deposition in human forearm and adipose tissues in vivo. Clin Sci (Lond) 79(4):339–348

    Article  CAS  Google Scholar 

  • Das M, Gabriely I, Barzilai N (2004) Caloric restriction, body fat and ageing in experimental models. Obes Rev 5(1):13–19

    Article  CAS  PubMed  Google Scholar 

  • Davis LM, Pauly JR, Readnower RD, Rho JM, Sullivan PG (2008) Fasting is neuroprotective following traumatic brain injury. J Neurosci Res 86(8):1812–1822

    Article  CAS  PubMed  Google Scholar 

  • DeClercq V, Taylor C, Zahradka P (2008) Adipose tissue: the link between obesity and cardiovascular disease. Cardiovasc Hematol Disord: Drug Targets 8(3):228–237

    Article  CAS  Google Scholar 

  • Demas GE (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45(3):173–180

    Article  CAS  PubMed  Google Scholar 

  • Dhillon H, Zigman JM, Ye C, Lee CE, McGovern RA, Tang V, Kenny CD, Christiansen LM, White RD, Edelstein EA, Coppari R, Balthasar N, Cowley MA, Chua S Jr, Elmquist JK, Lowell BB (2006) Leptin directly activates SF1 neurons in the VMH, and this action by leptin is required for normal body-weight homeostasis. Neuron 49(2):191–203

    Article  CAS  PubMed  Google Scholar 

  • Douville E, Downward J (1997) EGF induced SOS phosphorylation in PC12 cells involves P90 RSK-2. Oncogene 15(4):373–383

    Article  CAS  PubMed  Google Scholar 

  • Fernandes G, Yunis EJ, Good RA (1976) Influence of diet on survival of mice. Proc Natl Acad Sci USA 73(4):1279–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forster MJ, Morris P, Sohal RS (2003) Genotype and age influence the effect of caloric intake on mortality in mice. FASEB J 17(6):690–692

    PubMed  PubMed Central  Google Scholar 

  • Frayn KN (2002) Adipose tissue as a buffer for daily lipid flux. Diabetologia 45(9):1201–1210

    Article  CAS  PubMed  Google Scholar 

  • Fu C, Hickey M, Morrison M, McCarter R, Han ES (2006) Tissue specific and non-specific changes in gene expression by aging and by early stage CR. Mech Ageing Dev 127(12):905–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabriely I, Ma XH, Yang XM, Atzmon G, Rajala MW, Berg AH, Scherer P, Rossetti L, Barzilai N (2002) Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process? Diabetes 51(10):2951–2958

    Article  CAS  PubMed  Google Scholar 

  • Gardner EM (2005) Caloric restriction decreases survival of aged mice in response to primary influenza infection. J Gerontol A Biol Sci Med Sci 60(6):688–694

    Article  PubMed  Google Scholar 

  • Gehring WJ, Ikeo K (1999) Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet 15(9):371–377

    Article  CAS  PubMed  Google Scholar 

  • Genander M, Halford MM, Xu NJ, Eriksson M, Yu Z, Qiu Z, Martling A, Greicius G, Thakar S, Catchpole T, Chumley MJ, Zdunek S, Wang C, Holm T, Goff SP, Pettersson S, Pestell RG, Henkemeyer M, Frisen J (2009) Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell 139(4):679–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh S, Wanders D, Stone KP, Van NT, Cortez CC, Gettys TW (2014) A systems biology analysis of the unique and overlapping transcriptional responses to caloric restriction and dietary methionine restriction in rats. FASEB J 28(6):2577–2590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gosmain Y, Katz LS, Masson MH, Cheyssac C, Poisson C, Philippe J (2012) Pax6 is crucial for beta-cell function, insulin biosynthesis, and glucose-induced insulin secretion. Mol Endocrinol 26(4):696–709

    Article  CAS  PubMed  Google Scholar 

  • Harper JM, Leathers CW, Austad SN (2006) Does caloric restriction extend life in wild mice? Aging Cell 5(6):441–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison DE, Archer JR (1987) Genetic differences in effects of food restriction on aging in mice. J Nutr 117(2):376–382

    CAS  PubMed  Google Scholar 

  • Higami Y, Pugh TD, Page GP, Allison DB, Prolla TA, Weindruch R (2004) Adipose tissue energy metabolism: altered gene expression profile of mice subjected to long-term caloric restriction. FASEB J 18(2):415–417

    CAS  PubMed  Google Scholar 

  • Higami Y, Barger JL, Page GP, Allison DB, Smith SR, Prolla TA, Weindruch R (2006) Energy restriction lowers the expression of genes linked to inflammation, the cytoskeleton, the extracellular matrix, and angiogenesis in mouse adipose tissue. J Nutr 136(2):343–352

    CAS  PubMed  Google Scholar 

  • Hochberg Y, Benjamini Y (1990) More powerful procedures for multiple significance testing. Stat Med 9(7):811–818

    Article  CAS  PubMed  Google Scholar 

  • Huffman DM, Barzilai N (2009) Role of visceral adipose tissue in aging. Biochim Biophys Acta 1790(10):1117–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucl Acids Res 31(4):e15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin Q, Esteva FJ (2008) Cross-talk between the ErbB/HER family and the type I insulin-like growth factor receptor signaling pathway in breast cancer. J Mammary Gland Biol Neoplasia 13(4):485–498

    Article  PubMed  Google Scholar 

  • Jung H, Lee SK, Jho EH (2011) Mest/Peg1 inhibits Wnt signalling through regulation of LRP6 glycosylation. Biochem J 436(2):263–269

    Article  CAS  PubMed  Google Scholar 

  • Kasumovic MM, Brooks RC, Andrade MC (2009) Body condition but not dietary restriction prolongs lifespan in a semelparous capital breeder. Biol Lett 5(5):636–638

    Article  PubMed  PubMed Central  Google Scholar 

  • Katoh Y, Katoh M (2006) FGF signaling inhibitor, SPRY4, is evolutionarily conserved target of WNT signaling pathway in progenitor cells. Int J Mol Med 17(3):529–532

    CAS  PubMed  Google Scholar 

  • Kawanishi N, Yano H, Yokogawa Y, Suzuki K (2010) Exercise training inhibits inflammation in adipose tissue via both suppression of macrophage infiltration and acceleration of phenotypic switching from M1 to M2 macrophages in high-fat-diet-induced obese mice. Exerc Immunol Rev 16:105–118

    PubMed  Google Scholar 

  • Klein S, Fontana L, Young VL, Coggan AR, Kilo C, Patterson BW, Mohammed BS (2004) Absence of an effect of liposuction on insulin action and risk factors for coronary heart disease. N Engl J Med 350(25):2549–2557

    Article  CAS  PubMed  Google Scholar 

  • Kohonen T, Hynninen J, Kangas J, Laaksonen J (1996) Som pak: the self-organizing map program package. Report A31, Helsinki University of Technology, Laboratory of Computer and Information Science

  • Koza RA, Nikonova L, Hogan J, Rim JS, Mendoza T, Faulk C, Skaf J, Kozak LP (2006) Changes in gene expression foreshadow diet-induced obesity in genetically identical mice. PLoS Genet 2(5):e81

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lagathu C, Christodoulides C, Virtue S, Cawthorn WP, Franzin C, Kimber WA, Nora ED, Campbell M, Medina-Gomez G, Cheyette BN, Vidal-Puig AJ, Sethi JK (2009) Dact1, a nutritionally regulated preadipocyte gene, controls adipogenesis by coordinating the Wnt/beta-catenin signaling network. Diabetes 58(3):609–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laxminarayan KM, Chan BK, Tetaz T, Bird PI, Mitchell CA (1994) Characterization of a cDNA encoding the 43-kDa membrane-associated inositol-polyphosphate 5-phosphatase. J Biol Chem 269(25):17305–17310

    CAS  PubMed  Google Scholar 

  • Lee YL, Lee CK (2008) Transcriptional response according to strength of calorie restriction in Saccharomyces cerevisiae. Mol Cells 26(3):299–307

    CAS  PubMed  Google Scholar 

  • Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JW, Taylor PW, Soran N, Raubenheimer D (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc Natl Acad Sci USA 105(7):2498–2503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee C, Safdie FM, Raffaghello L, Wei M, Madia F, Parrella E, Hwang D, Cohen P, Bianchi G, Longo VD (2010) Reduced levels of IGF-I mediate differential protection of normal and cancer cells in response to fasting and improve chemotherapeutic index. Cancer Res 70(4):1564–1572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141(7):1117–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao CY, Rikke BA, Johnson TE, Diaz V, Nelson JF (2010) Genetic variation in the murine lifespan response to dietary restriction: from life extension to life shortening. Aging Cell 9(1):92–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao CY, Rikke BA, Johnson TE, Gelfond JA, Diaz V, Nelson JF (2011) Fat maintenance is a predictor of the murine lifespan response to dietary restriction. Aging Cell 10(4):629–639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipman RD, Smith DE, Bronson RT, Blumberg J (1995) Is late-life caloric restriction beneficial? Aging (Milano) 7(2):136–139

    CAS  Google Scholar 

  • Lipman RD, Smith DE, Blumberg JB, Bronson RT (1998) Effects of caloric restriction or augmentation in adult rats: longevity and lesion biomarkers of aging. Aging (Milano) 10(6):463–470

    CAS  Google Scholar 

  • Liu HS, Hsu PY, Lai MD, Chang HY, Ho CL, Cheng HL, Chen HT, Lin YJ, Wu TJ, Tzai TS, Chow NH (2010) An unusual function of RON receptor tyrosine kinase as a transcriptional regulator in cooperation with EGFR in human cancer cells. Carcinogenesis 31(8):1456–1464

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu R, Zhou Z, Huang J, Chen C (2011) PMEPA1 promotes androgen receptor-negative prostate cell proliferation through suppressing the Smad3/4-c-Myc-p21 Cip1 signaling pathway. J Pathol 223(5):683–694

    Article  CAS  PubMed  Google Scholar 

  • MacDonald L, Radler M, Paolini AG, Kent S (2011) Calorie restriction attenuates LPS-induced sickness behavior and shifts hypothalamic signaling pathways to an anti-inflammatory bias. Am J Physiol Regul Integr Comp Physiol 301(1):R172–R184

    Article  CAS  PubMed  Google Scholar 

  • Malliri A, Rygiel TP, van der Kammen RA, Song JY, Engers R, Hurlstone AF, Clevers H, Collard JG (2006) The rac activator Tiam1 is a Wnt-responsive gene that modifies intestinal tumor development. J Biol Chem 281(1):543–548

    Article  CAS  PubMed  Google Scholar 

  • Margoni A, Fotis L, Papavassiliou AG (2012) The transforming growth factor-beta/bone morphogenetic protein signalling pathway in adipogenesis. Int J Biochem Cell Biol 44(3):475–479

    Article  CAS  PubMed  Google Scholar 

  • Masoro EJ (2005) Overview of caloric restriction and ageing. Mech Ageing Dev 126(9):913–922

    Article  CAS  PubMed  Google Scholar 

  • Matsubara T, Mita A, Minami K, Hosooka T, Kitazawa S, Takahashi K, Tamori Y, Yokoi N, Watanabe M, Matsuo E, Nishimura O, Seino S (2012) PGRN is a key adipokine mediating high fat diet-induced insulin resistance and obesity through IL-6 in adipose tissue. Cell Metab 15(1):38–50

    Article  CAS  PubMed  Google Scholar 

  • Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, Longo DL, Allison DB, Young JE, Bryant M, Barnard D, Ward WF, Qi W, Ingram DK, de Cabo R (2012) Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489(7415):318–321

    Article  CAS  PubMed  Google Scholar 

  • Millership S, Ninkina N, Rochford JJ, Buchman VL (2013) gamma-synuclein is a novel player in the control of body lipid metabolism. Adipocyte 2(4):276–280

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell JR, Verweij M, Brand K, van de Ven M, Goemaere N, van den Engel S, Chu T, Forrer F, Muller C, de Jong M, van IW, JN IJ, Hoeijmakers JH, de Bruin RW (2010) Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice. Aging Cell 9(1):40–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molleman F, Ding J, Boggs CL, Carey JR, Arlet ME (2009) Does dietary restriction reduce life span in male fruit-feeding butterflies? Exp Gerontol 44(9):601–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moraes RC, Blondet A, Birkenkamp-Demtroeder K, Tirard J, Orntoft TF, Gertler A, Durand P, Naville D, Begeot M (2003) Study of the alteration of gene expression in adipose tissue of diet-induced obese mice by microarray and reverse transcription-polymerase chain reaction analyses. Endocrinology 144(11):4773–4782

    Article  CAS  PubMed  Google Scholar 

  • Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW (2006) Central nervous system control of food intake and body weight. Nature 443(7109):289–295

    Article  CAS  PubMed  Google Scholar 

  • Muzumdar R, Allison DB, Huffman DM, Ma X, Atzmon G, Einstein FH, Fishman S, Poduval AD, McVei T, Keith SW, Barzilai N (2008) Visceral adipose tissue modulates mammalian longevity. Aging Cell 7(3):438–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nacher J, Varea E, Blasco-Ibanez JM, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ, McEwen BS (2005) Expression of the transcription factor Pax 6 in the adult rat dentate gyrus. J Neurosci Res 81(6):753–761

    Article  CAS  PubMed  Google Scholar 

  • Nikolich-Zugich J, Messaoudi I (2005) Mice and flies and monkeys too: caloric restriction rejuvenates the aging immune system of non-human primates. Exp Gerontol 40(11):884–893

    Article  CAS  PubMed  Google Scholar 

  • Niu C, Liang C, Guo J, Cheng L, Zhang H, Qin X, Zhang Q, Ding L, Yuan B, Xu X, Li J, Lin J, Ye Q (2012) Downregulation and growth inhibitory role of FHL1 in lung cancer. Int J Cancer 130(11):2549–2556

    Article  CAS  PubMed  Google Scholar 

  • Okada Y, Sakaue H, Nagare T, Kasuga M (2009) Diet-induced up-regulation of gene expression in adipocytes without changes in DNA methylation. Kobe J Med Sci 54(5):E241–E249

    PubMed  Google Scholar 

  • Okita N, Hayashida Y, Kojima Y, Fukushima M, Yuguchi K, Mikami K, Yamauchi A, Watanabe K, Noguchi M, Nakamura M, Toda T, Higami Y (2012) Differential responses of white adipose tissue and brown adipose tissue to caloric restriction in rats. Mech Ageing Dev 133(5):255–266

    Article  CAS  PubMed  Google Scholar 

  • Oort PJ, Knotts TA, Grino M, Naour N, Bastard JP, Clement K, Ninkina N, Buchman VL, Permana PA, Luo X, Pan G, Dunn TN, Adams SH (2008) Gamma-synuclein is an adipocyte-neuron gene coordinately expressed with leptin and increased in human obesity. J Nutr 138(5):841–848

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pei H, Li L, Fridley BL, Jenkins GD, Kalari KR, Lingle W, Petersen G, Lou Z, Wang L (2009) FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 16(3):259–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plunet WT, Streijger F, Lam CK, Lee JH, Liu J, Tetzlaff W (2008) Dietary restriction started after spinal cord injury improves functional recovery. Exp Neurol 213(1):28–35

    Article  PubMed  Google Scholar 

  • Robertson LT, Mitchell JR (2013) Benefits of short-term dietary restriction in mammals. Exp Gerontol 48(10):1043–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schayek H, Bentov I, Jacob-Hirsch J, Yeung C, Khanna C, Helman LJ, Plymate SR, Werner H (2012) Global methylation analysis identifies PITX2 as an upstream regulator of the androgen receptor and IGF-I receptor genes in prostate cancer. Horm Metab Res 44(7):511–519

    Article  CAS  PubMed  Google Scholar 

  • Sethi JK, Vidal-Puig AJ (2007) Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J Lipid Res 48(6):1253–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sethi JK, Vidal-Puig A (2010) Wnt signalling and the control of cellular metabolism. Biochem J 427(1):1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sima A, Manolescu DC, Bhat P (2011) Retinoids and retinoid-metabolic gene expression in mouse adipose tissues. Biochem Cell Biol 89(6):578–584

    Article  CAS  PubMed  Google Scholar 

  • Skurk T, Alberti-Huber C, Herder C, Hauner H (2007) Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 92(3):1023–1033

    Article  CAS  PubMed  Google Scholar 

  • Speakman JR, Mitchell SE (2011) Caloric restriction. Mol Asp Med 32(3):159–221

    Article  CAS  Google Scholar 

  • Sutphin GL, Kaeberlein M (2008) Dietary restriction by bacterial deprivation increases life span in wild-derived nematodes. Exp Gerontol 43(3):130–135

    Article  CAS  PubMed  Google Scholar 

  • Swindell WR (2009) Genes and gene expression modules associated with caloric restriction and aging in the laboratory mouse. BMC Genom 10:585

    Article  CAS  Google Scholar 

  • Takahashi M, Kamei Y, Ezaki O (2005) Mest/Peg1 imprinted gene enlarges adipocytes and is a marker of adipocyte size. Am J Physiol Endocrinol Metab 288(1):E117–E124

    Article  CAS  PubMed  Google Scholar 

  • Tremblay F, Revett T, Huard C, Zhang Y, Tobin JF, Martinez RV, Gimeno RE (2009) Bidirectional modulation of adipogenesis by the secreted protein Ccdc80/DRO1/URB. J Biol Chem 284(12):8136–8147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathi R, Mishra R (2012) Aging-associated modulation in the expression of Pax6 in mouse brain. Cell Mol Neurobiol 32(2):209–218

    Article  CAS  PubMed  Google Scholar 

  • 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(11):B492–B501

    Article  CAS  PubMed  Google Scholar 

  • Venda LL, Cragg SJ, Buchman VL, Wade-Martins R (2010) alpha-Synuclein and dopamine at the crossroads of Parkinson’s disease. Trends Neurosci 33(12):559–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voigt A, Agnew K, van Schothorst EM, Keijer J, Klaus S (2013) Short-term, high fat feeding-induced changes in white adipose tissue gene expression are highly predictive for long-term changes. Mol Nutr Food Res 57(8):1423–1434

    Article  CAS  PubMed  Google Scholar 

  • Walden TB, Hansen IR, Timmons JA, Cannon B, Nedergaard J (2012) Recruited vs. nonrecruited molecular signatures of brown, “brite,” and white adipose tissues. Am J Physiol Endocrinol Metab 302(1):E19–E31

    Article  CAS  PubMed  Google Scholar 

  • Wang JY, Yeh CL, Chou HC, Yang CH, Fu YN, Chen YT, Cheng HW, Huang CY, Liu HP, Huang SF, Chen YR (2011) Vaccinia H1-related phosphatase is a phosphatase of ErbB receptors and is down-regulated in non-small cell lung cancer. J Biol Chem 286(12):10177–10184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weithoff G (2007) Dietary restriction in two rotifer species: the effect of the length of food deprivation on life span and reproduction. Oecologia 153(2):303–308

    Article  PubMed  Google Scholar 

  • Wellmann A, Fogt F, Hollerbach S, Hahne J, Koenig-Hoffmann K, Smeets D, Brinkmann U (2010) Polymorphisms of the apoptosis-associated gene DP1L1 (deleted in polyposis 1-like 1) in colon cancer and inflammatory bowel disease. J Cancer Res Clin Oncol 136(6):795–802

    Article  CAS  PubMed  Google Scholar 

  • Yabana N, Shibuya M (2002) Adaptor protein APS binds the NH2-terminal autoinhibitory domain of guanine nucleotide exchange factor Vav3 and augments its activity. Oncogene 21(50):7720–7729

    Article  CAS  PubMed  Google Scholar 

  • Yadav H, Quijano C, Kamaraju AK, Gavrilova O, Malek R, Chen W, Zerfas P, Zhigang D, Wright EC, Stuelten C, Sun P, Lonning S, Skarulis M, Sumner AE, Finkel T, Rane SG (2011) Protection from obesity and diabetes by blockade of TGF-beta/Smad3 signaling. Cell Metab 14(1):67–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamagishi T, Bessho M, Yanagida S, Nishizawa K, Kusuhara M, Ohsuzu F, Tamai S (2010) Severe, short-term food restriction improves cardiac function following ischemia/reperfusion in perfused rat hearts. Heart Vessels 25(5):417–425

    Article  PubMed  Google Scholar 

  • Yu BP, Masoro EJ, McMahan CA (1985) Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J Gerontol 40(6):657–670

    Article  CAS  PubMed  Google Scholar 

  • Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4(4):R28

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372(6505):425–432

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Bio and Medical Technology Development Program of the National Research Foundation (NRF) funded by the Ministry of Science, ICT and Future Planning (NRF-2011-0030137), and Cooperative Research Program for Agriculture Science and Technology Development, Rural Development Administration (Project no. PJ01053302), and the Technology Commercialization Support Program, Ministry for Food, Agriculture, Forestry and Fisheries (811003-03-3-SU000), Republic of Korea for CKL, and NRF grant funded by the Korea government (MSIP) (no. 2015064915), Republic of Korea for JWL.

Author information

Authors and Affiliations

  1. Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul, 136-701, Republic of Korea

    Seung-Soo Kim, Kyung-Mi Choi & Cheol-Koo Lee

  2. Department of Food and Nutrition, Yonsei University, Seoul, 120-749, Republic of Korea

    Soyoung Kim & Taesun Park

  3. Subtropical Animal Station, National Institute of Animal Science, Jeju, 690-150, Republic of Korea

    In-Cheol Cho

  4. Department of Statistics, Korea University, Seoul, 136-701, Republic of Korea

    Jae-Won Lee

Authors
  1. Seung-Soo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kyung-Mi Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Soyoung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taesun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. In-Cheol Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jae-Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cheol-Koo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cheol-Koo Lee.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, SS., Choi, KM., Kim, S. et al. Whole-transcriptome analysis of mouse adipose tissue in response to short-term caloric restriction. Mol Genet Genomics 291, 831–847 (2016). https://doi.org/10.1007/s00438-015-1150-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-1150-3

Keywords

Search

Navigation