Skip to main content

Adipose Tissue as a Peripheral Clock

  • Chapter
  • First Online:
Chronobiology and Obesity

Abstract

Adipose tissue is a complex and highly metabolic and endocrine organ, which is capable of expressing and secreting a variety of bioactive peptides, so-called adipokines. These adipokines are involved in coordinating a diversity of biological processes including energy intake and expenditure, insulin resistance, adipocyte differentiation, dyslipidemia, and body fat distribution. One of the most outstanding discoveries in the last year is the presence of an active circadian clock in adipose tissue depots. New data suggest that there is a temporal component in the regulation of all these adipose tissue functions. In fact, studies performed by microarrays have shown that a certain percentage of active genes expressed in adipose tissue in both humans and animal models follow a daily rhythmic pattern. Examples of these genes are clock genes (PER2, CLOCK, CRY1, and BMAL1), adipokine genes (adiponectin and leptin), and glucocorticoid-related genes among others. Thus, an adequate temporal order in the daily pattern of these genes implicated in adipose tissue metabolism could have important consequences not only in body fat distribution but also in the metabolic alterations associated to obesity. Further investigations of circadian rhythms in adipose tissues will provide insight into the physiology of energy homeostasis and the etiology of metabolic diseases such as obesity.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

LEP:

Leptin

LEPR:

Leptin receptor

TNFα:

Tumour necrosis factor alpha

ApM1:

Adipose most abundant gene transcript 1 or adiponectin

Acrp30:

Adipocyte complement-related protein of 30 kDa or adiponectin

GBP28:

Gelatin binding protein of 28 kDa or adiponectin

AdipoQ:

Adiponectin

ADIPOR1:

Adiponectin receptor 1

ADIPOR2:

Adiponectin receptor 2

TZDs:

Thiazolidinediones

IL-6:

Interleukin 6

ASP:

Acylation stimulating protein

PAI-1:

Plasminogen activator inhibitor-1

TGF-beta:

Transforming growth factor-beta

GCs:

Glucocorticoids

HPA:

Hypothalamic–pituitary–adrenal

GR:

Glucocorticoid receptor

11DHC:

11-Dehydrocorticosterone

11βHSD1:

11β-Hydroxysteroid dehydrogenase 1

11βHSD2:

11β-Hydroxysteroid dehydrogenase 2

STAR:

Teroidogenic acute regulatory protein

5αR:

5-α reductase

PPARγ:

Peroxisome proliferator-activated receptor gamma

PCR:

Polymerase reaction chain

AT:

Adipose tissue

WAT:

White adipose tissue

BAT:

Brown adipose tissue

SWAT or SAT:

Subcutaneous adipose tissue

VWAT or VAT:

Visceral adipose tissue

IAAT:

Intra-abdominal adipose tissue

FFAs:

Free fatty acids

TGs:

Triglycerides

MetS:

Metabolic syndrome

SCN:

Suprachiasmatic nucleus

LPL:

Lipoprotein lipase

Pdp1:

PAR domain protein 1

RORα:

RAR-related orphan receptor alpha

PGC1α:

Peroxisome proliferative activated receptor gamma, coactivator 1 alpha

PER2:

Period homolog 2 (Drosophila)

BMAL1 or ARNTL or MOP3:

Aryl hydrocarbon receptor nuclear translocator-like

CLOCK:

Circadian locomotor output cycles kaput

CRY:

Cryptochrome

mRNA:

Messenger ribonucleic acid

CCG:

Clock control genes

ASCs:

Adipose-derived stem cells

ACTH:

Adrenocorticotropic hormone

References

  1. Siiteri PK (1987) Adipose tissue as a source of hormones. Am J Clin Nutr 45(1 Suppl):277–282

    PubMed  CAS  Google Scholar 

  2. 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 372:425–432

    PubMed  CAS  Google Scholar 

  3. Friedman JM (2002) The function of leptin in nutrition, weight, and physiology. Nutr Rev 60(10(Pt 2)):S1–S14, Review

    PubMed  Google Scholar 

  4. Zhang W, Della-Fera MA, Hartzell DL, Hausman D, Baile CA (2008) Adipose tissue gene expression profiles in ob/ob mice treated with leptin. Life Sci 83(1–2):35–42

    PubMed  CAS  Google Scholar 

  5. Kielar D, Clark JS, Ciechanowicz A, Kurzawski G, Sulikowski T, Naruszewicz M (1998) Leptin receptor isoforms expressed in human adipose tissue. Metabolism 47(7):844–847

    PubMed  CAS  Google Scholar 

  6. Saad MF, Riad-Gabriel MG, Khan A, Sharma A, Michael R, Jinagouda SD, Boyadjian R, Steil GM (1998) Diurnal and ultradian rhythmicity of plasma leptin: effects of gender and adiposity. J Clin Endocrinol Metab 83(2):453–459

    PubMed  CAS  Google Scholar 

  7. Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW (2004) Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145:2273–2282

    PubMed  CAS  Google Scholar 

  8. Ruan H, Miles PD, Ladd CM, Ross K, Golub TR, Olefsky JM, Lodish HF (2002) Profiling gene transcription in vivo reveals adipose tissue as an immediate target of tumor necrosis factor-α: implications for insulin resistance. Diabetes 51:3176–3188

    PubMed  CAS  Google Scholar 

  9. Ruan H, Lodish HF (2003) Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor. Cytokine Growth Factor Rev 14:447–455

    PubMed  CAS  Google Scholar 

  10. Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K (1996) cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most abundant Gene transcript 1). Biochem Biophys Res Commun 221:286–289

    PubMed  CAS  Google Scholar 

  11. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF (1995) A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 270:26746–26749

    PubMed  CAS  Google Scholar 

  12. Nakano Y, Tobe T, Choi-Miura NH, Mazda T, Tomita M (1996) Isolation and characterization of GBP28, a novel gelatin-binding protein purified from human plasma. J Biochem (Tokyo) 120:803–812

    CAS  Google Scholar 

  13. Hu E, Liang P, Spiegelman BM (1996) AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem 271:10697–10703

    PubMed  CAS  Google Scholar 

  14. Gil-Campos M, Cañete RR, Gil A (2004) Adiponectin, the missing link in insulin resistance and obesity. Clin Nutr 23:963–974

    PubMed  CAS  Google Scholar 

  15. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423(6941):762–769

    PubMed  CAS  Google Scholar 

  16. Rasmussen MS, Lihn AS, Pedersen SB, Bruun JM, Rasmussen M, Richelsen B (2006) Adiponectin receptors in human adipose tissue: effects of obesity, weight loss, and fat depots. Obesity (Silver Spring) 14(1):28–35

    CAS  Google Scholar 

  17. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312

    PubMed  CAS  Google Scholar 

  18. Banerjee RR, Lazar MA (2003) Resistin: molecular history and prognosis. J Mol Med 81:218–226

    PubMed  CAS  Google Scholar 

  19. Kim KH, Lee K, Moon YS, Sul HS (2001) A cysteine-rich adipose tissue-specific secretory factor inhibits adipocyte differentiation. J Biol Chem 276(14):11252–11256

    PubMed  CAS  Google Scholar 

  20. Adeghate E (2004) An update on the biology and physiology of resistin. Cell Mol Life Sci 61(19–20):2485–2496

    PubMed  CAS  Google Scholar 

  21. Steppan CM, Lazar MA (2004) The current biology of resistin. J Intern Med 255:439–447

    PubMed  CAS  Google Scholar 

  22. Dyck DJ, Heigenhauser GJ, Bruce CR (2006) The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol 186:5–16

    CAS  Google Scholar 

  23. McTernan PG, Kusminski CM, Kumar S (2006) Resistin. Curr Opin Lipidol 17(2):170–175

    PubMed  CAS  Google Scholar 

  24. Fernandez-Real JM, Ricart W (2003) Insulin resistance and chronic cardiovascular inflammatory syndrome. Endocr Rev 24:278–301

    PubMed  CAS  Google Scholar 

  25. Kershaw EE, Flier JS (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89(6):2548–2556

    PubMed  CAS  Google Scholar 

  26. Cianflone K, Xia Z, Chen LY (2003) Critical review of acylation-stimulating protein physiology in humans and rodents. Biochim Biophys Acta 1609:127–143

    PubMed  CAS  Google Scholar 

  27. Flier JS, Cook KS, Usher P, Spiegelman BM (1987) Severely impaired adipsin expression in genetic and acquired obesity. Science 237:405–408

    PubMed  CAS  Google Scholar 

  28. Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, Matsuki Y, Murakami M, Ichisaka T, Murakami H, Watanabe E, Takagi T, Akiyoshi M, Ohtsubo T, Kihara S, Yamashita S, Makishima M, Funahashi T, Yamanaka S, Hiramatsu R, Matsuzawa Y, Shimomura I (2005) Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 307:426–430

    PubMed  CAS  Google Scholar 

  29. Revollo JR (2007) Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab 6:363–375

    PubMed  CAS  Google Scholar 

  30. Frühbeck G (2004) The adipose tissue as a source of vasoactive factors. Curr Med Chem Cardiovasc Hematol Agents 2(3):197–208

    PubMed  Google Scholar 

  31. Maeda K, Okubo K, Shimomura I, Mizuno K, Matsuzawa Y, Matsubara K (1997) Analysis of an expression profile of genes in the human adipose tissue. Gene 190:227–235

    PubMed  CAS  Google Scholar 

  32. Stewart PM, Petersenn S (2009) Rationale for treatment and therapeutic options in Cushing’s disease. Best Pract Res Clin Endocrinol Metab 23(Suppl 1):S15–S22

    PubMed  Google Scholar 

  33. McDonough AK, Curtis JR, Saag KG (2008) The epidemiology of glucocorticoid-associated adverse events. Curr Opin Rheumatol 20:131–137

    PubMed  Google Scholar 

  34. Friedman TC, Mastorakos G, Newman TD, Mullen NM, Horton EG, Costello R, Papadopoulos NM, Chrousos GP (1996) Carbohydrate and lipid metabolism in endogenous hypercortisolism: shared features with metabolic syndrome X and NIDDM. Endocr J 43(6):645–655

    PubMed  CAS  Google Scholar 

  35. Bujalska IJ, Kumar S, Stewart PM (1997) Does central obesity reflect “Cushing’s disease of the omentum”? Lancet 349:1210–1213

    PubMed  CAS  Google Scholar 

  36. Andrew R, Phillips DI, Walker BR (1998) Obesity and gender influence cortisol secretion and metabolism in man. J Clin Endocrinol Metab 83:1806–1809

    PubMed  CAS  Google Scholar 

  37. Strain GW, Zumoff B, Strain JJ, Levin J, Fukushima DK (1980) Cortisol production in obesity. Metabolism 29:980–985

    PubMed  CAS  Google Scholar 

  38. Westerbacka J, Yki-Järvinen H, Vehkavaara S, Häkkinen AM, Andrew R, Wake DJ, Seckl JR, Walker BR (2003) Body fat distribution and cortisol metabolism in healthy men: enhanced 5beta-reductase and lower cortisol/cortisone metabolite ratios in men with fatty liver. J Clin Endocrinol Metab 88:4924–4931

    PubMed  CAS  Google Scholar 

  39. Fraser R, InhGram MC, Anderson NH, Morrison C, Davies E, Connell JM (1999) Cortisol effects on body mass, blood pressure, and cholesterol in the general population. Hypertension 33:1364–1368

    PubMed  CAS  Google Scholar 

  40. García-Prieto MD, Tébar FJ, Nicolás F, Larqué E, Zamora S, Garaulet M (2007) Cortisol secretary pattern and glucocorticoid feedback sensitivity in women from a Mediterranean area: relationship with anthropometric characteristics, dietary intake and plasma fatty acid profile. Clin Endocrinol (Oxf) 66:185–191

    Google Scholar 

  41. Pezzi V, Mathis JM, Rainey WE, Carr BR (2003) Profiling transcript levels for steroidogenic enzymes in fetal tissues. J Steroid Biochem Mol Biol 87:181–189

    PubMed  CAS  Google Scholar 

  42. Schinner S, Willenberg HS, Krause D, Schott M, Lamounier-Zepter V, Krug AW, Ehrhart-Bornstein M, Bornstein SR, Scherbaum WA (2007) Adipocyte-derived products induce the transcription of the StAR promoter and stimulate aldosterone and cortisol secretion from adrenocortical cells through the Wnt-signaling pathway. Int J Obes (Lond) 31:864–870

    CAS  Google Scholar 

  43. Livingstone DE, Jones GC, Smith K, Jamieson PM, Andrew R, Kenyon CJ, Walker BR (2003) Understanding the role of glucocorticoids in obesity: tissue-specific alterations of corticosterone metabolism in obese Zucker rats. Endocrinology 141:560–563

    Google Scholar 

  44. Gerhold DL, Liu F, Jiang G, Li Z, Xu J, Lu M, Sachs JR, Bagchi A, Fridman A, Holder DJ, Doebber TW, Berger J, Elbrecht A, Moller DE, Zhang BB (2002) Gene expression profile of adipocyte differentiation and its regulation by peroxisome proliferator-activated receptor-gamma agonists. Endocrinology 143(6):2106–2118

    PubMed  CAS  Google Scholar 

  45. Tomlinson JW, Moore J, Cooper MS, Bujalska I, Shahmanesh M, Burt C, Strain A, Hewison M, Stewart PM (2001) Regulation of expression of 11beta-hydroxysteroid dehydrogenase type 1 in adipose tissue: tissue-specific induction by cytokines. Endocrinology 142: 1982–1989

    PubMed  CAS  Google Scholar 

  46. Berger J, Tanen M, Elbrecht A, Hermanowski-Vosatka A, Moller DE, Wright SD, Thieringer R (2001) Peroxisome proliferator-activated receptor-gamma ligands inhibit adipocyte 11beta -hydroxysteroid dehydrogenase type 1 expression and activity. J Biol Chem 276(16): 12629–12635

    PubMed  CAS  Google Scholar 

  47. Fawcett DW (1952) A comparison of the histological organization and cytochemical reactions of brown and white adipose tissues. J Morphol 90:363–405

    CAS  Google Scholar 

  48. Napolitano L (1963) The differentiation of white adipose tissue: an electron microscopic study. J Cell Biol 18:663–673

    PubMed  CAS  Google Scholar 

  49. Afzelius BA (1970) Brown adipose tissue: its gross anatomy, histology, and cytology. In: Lindberg O (ed) Brown adipose tissue. Elsevier, Amsterdam, pp 1–31

    Google Scholar 

  50. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359

    PubMed  CAS  Google Scholar 

  51. Garaulet M, Hernandez-Morante JJ, Lujan J, Tebar FJ, Zamora S (2006) Relationship between fat cell size and number and fatty acid composition in adipose tissue from different fat depots in overweight/obese humans. Int J Obes (Lond) 30(6):899–905

    CAS  Google Scholar 

  52. Gil A, Olza J, Gil-Campos M, Gomez-Llorente C, Aguilera CM (2011) Is adipose tissue metabolically different at different sites? Int J Pediatr Obes 6(Suppl 1):13–20, Review

    PubMed  Google Scholar 

  53. Rebuffé-Scrive M, Lundholm K, Björntorp P (1985) Glucocorticoid hormone binding to human adipose tissue. Eur J Clin Invest 15:267–271

    PubMed  Google Scholar 

  54. Freedland ES (2004) Role of critical visceral adipose tissue threshold in metabolic syndrome: implications for controlling dietary carbohydrates: a review. Nutr Metab 1:12

    Google Scholar 

  55. Pedersen SB, Hansen PS, Lund S, Andersen PH, Odgaard A, Richelsen B (1996) Identification of oestrogen receptors and oestrogen receptor mRNA in human adipose tissue. Eur J Clin Invest 26:259

    Google Scholar 

  56. Imbeault P, Couillard C, Tremblay A, Després J-P, Mauriège P (2000) Reduced alpha [2]-adrenergic sensitivity of subcutaneous abdominal adipocytes as a modulator of fasting and post-prandial triglyceride levels in men. J Lipid Res 41:1367

    PubMed  CAS  Google Scholar 

  57. Björntorp P (2000) Metabolic difference between visceral fat and subcutaneous abdominal fat. Diabetes Metab 26(Suppl 3):10–12, Review. French

    PubMed  Google Scholar 

  58. Amer P (1995) Differences in lipolysis between human subcutaneous and omental adipose tissues. Ann Med 27:435–438

    Google Scholar 

  59. Arner P (1997) Obesity and the adipocyte. Regional adipocity in man. J Endocrinol 155:191–192

    PubMed  CAS  Google Scholar 

  60. Hamdy O, Porramatikul S, Al-Ozairi E (2006) Metabolic obesity: the paradox between visceral and subcutaneous fat. Curr Diabetes Rev 2(4):367–373

    PubMed  Google Scholar 

  61. Prasad H, Ryan DA, Celzo MF, Stapleton D (2012) Metabolic syndrome: definition and therapeutic implications. Postgrad Med 124(1):21–30

    PubMed  Google Scholar 

  62. Oh TH, Byeon JS, Myung SJ, Yang SK, Choi KS, Chung JW, Kim B, Lee D, Byun JH, Jang SJ, Kim JH (2008) Visceral obesity as a risk factor for colorectal neoplasm. J Gastroenterol Hepatol 23:411–417

    PubMed  CAS  Google Scholar 

  63. Von Hafe P, Pina F, Pérez A, Tavares M, Barros H (2004) Visceral fat accumulation as a risk factor for prostate cancer. Obes Res 12:1930–1935

    Google Scholar 

  64. Garaulet M, Madrid JA (2009) Chronobiology, genetics and metabolic syndrome. Curr Opin Lipidol 20(2):127–134, Review

    PubMed  CAS  Google Scholar 

  65. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96(2):271–290

    PubMed  CAS  Google Scholar 

  66. Lee C, Etchegaray JP, Cagampang FR, Loudon AS, Reppert SM (2001) Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107(7):855–867

    PubMed  CAS  Google Scholar 

  67. Pevet P, Challet E (2011) Melatonin: both master clock output and internal time-giver in the circadian clocks network. J Physiol Paris 105(4–6):170–182

    PubMed  Google Scholar 

  68. Balsalobre A, Damiola F, Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93(6):929–937

    PubMed  CAS  Google Scholar 

  69. Arble DM, Ramsey KM, Bass J, Turek FW (2010) Circadian disruption and metabolic disease: findings from animal models. Best Pract Res Clin Endocrinol Metab 24(5):785–800

    PubMed  CAS  Google Scholar 

  70. Aoyagi T, Shimba S, Tezuka M (2005) Characteristics of circadian gene expressions in mice white adipose tissue and 3T3-L1 adipocytes. J Health Sci 51:21–32

    CAS  Google Scholar 

  71. Loboda A, Kraft WK, Fine B, Joseph J, Nebozhyn M, Zhang C, He Y, Yang X, Wright C, Morris M, Chalikonda I, Ferguson M, Emilsson V, Leonardson A, Lamb J, Dai H, Schadt E, Greenberg HE, Lum PY (2009) Diurnal variation of the human adipose transcriptome and the link to metabolic disease. BMC Med Genomics 2:7

    PubMed  Google Scholar 

  72. Ptitsyn AA, Zvonic S, Conrad SA, Scott LK, Mynatt RL, Gimble JM (2006) Circadian clocks are resounding in peripheral tissues. PLoS Comput Biol 2(3):e16

    PubMed  Google Scholar 

  73. Bozek K, Relógio A, Kielbasa SM, Heine M, Dame C, Kramer A, Herzel H (2009) Regulation of clock-controlled genes in mammals. PLoS One 4(3):e4882

    PubMed  Google Scholar 

  74. Dallmann R, Viola AU, Tarokh L, Cajochen C, Brown SA (2012) The human circadian metabolome. Proc Natl Acad Sci U S A 109(7):2625–2629

    PubMed  CAS  Google Scholar 

  75. Le Magnen J (1988) Lipogenesis, lipolysis and feeding rhythms. Ann Endocrinol Paris 49(2):98–104, French

    PubMed  Google Scholar 

  76. Gimble JM, Floyd ZE (2009) Fat circadian biology. J Appl Physiol 107(5):1629–1637

    PubMed  Google Scholar 

  77. Sinha MK, Ohanneslan JP, Heiman ML, Kriauclunas A, Stephens TW, Magosin S, Marco C, Caro JF (1996) Nocturnal rise of leptin in lean, obese, and non-insulin-dependent diabetes mellitus subjects. J Clin Invest 97:1344–1347

    PubMed  CAS  Google Scholar 

  78. Gavrila A, Peng CK, Chan JL, Mietus JE, Goldberger AL, Mantzoros CS (2003) Diurnal and ultradian dynamics of serum adiponectin in healthy men: comparison with leptin, circulating soluble leptin receptor, and cortisol patterns. J Clin Endocrinol Metab 88:2838–2843

    PubMed  CAS  Google Scholar 

  79. Langendonk JG, Pijl H, Toornvliet AC, Burggraaf J, Frölich M, Schoemaker RC, Doornbos J, Cohen AF, Meinders AE (1998) Circadian rhythm of plasma leptin levels in upper and lower body obese women: influence of body fat distribution and weight loss. J Clin Endocrinol Metab 83(5):1706–1712

    PubMed  CAS  Google Scholar 

  80. Kalsbeek A, Fliers E, Romijn JA, La Fleur SE, Wortel J, Bakker O, Endert E, Buijs RM (2001) The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology 142:2677–2685

    PubMed  CAS  Google Scholar 

  81. Zvonic S, Ptitsyn AA, Conrad SA, Scott LK, Floyd ZE, Kilroy G, Wu X, Goh BC, Mynatt RL, Gimble JM (2006) Characterization of peripheral circadian clocks in adipose tissues. Diabetes 55(4):962–970

    PubMed  CAS  Google Scholar 

  82. Ando H, Yanagihara H, Hayashi Y, Obi Y, Tsuruoka S, Takamura T, Kaneko S, Fujimura A (2005) Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146(12):5631–5636

    PubMed  CAS  Google Scholar 

  83. Suzuki M, Shimomura Y, Satoh Y (1983) Diurnal changes in lipolytic activity of isolated fat cells and their increased responsiveness to epinephrine and theophylline with meal feeding in rats. J Nutr Sci Vitaminol (Tokyo) 29(4):399–411

    CAS  Google Scholar 

  84. Garaulet M, Madrid JA (2010) Chronobiological aspects of nutrition, metabolic syndrome and obesity. Adv Drug Deliv Rev 62:967–978

    PubMed  CAS  Google Scholar 

  85. Chawla A, Lazar MA (1993) Induction of Rev-ErbAa, an orphan receptor encoded on the opposite strand of the a-thyroid hormone receptor gene, during adipocyte differentiation. J Biol Chem 268:16265–16269

    PubMed  CAS  Google Scholar 

  86. Shimba S, Ishii N, Ohno T, Watabe Y, Hayashi M, Wada T, Aoyagi T, Tezuka M (2005) Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci U S A 102:12071–12076

    PubMed  CAS  Google Scholar 

  87. Benito J, Hoxha V, Lama C, Lazareva AA, Ferveur JF, Hardin PE, Dauwalder B (2010) The circadian output gene takeout is regulated by Pdp1epsilon. Proc Natl Acad Sci U S A 107:2544–2549

    PubMed  Google Scholar 

  88. Sarov-Blat L, So WV, Liu L, Rosbash M (2000) The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell 101:647–656

    PubMed  CAS  Google Scholar 

  89. Gómez-Abellán P, Hernández-Morante JJ, Luján JA, Madrid JA, Garaulet M (2008) Clock genes are implicated in the human metabolic syndrome. Int J Obes (Lond) 32:121–128

    Google Scholar 

  90. Gómez-Abellán P, Madrid JA, Luján JA, Frutos MD, González R, Martínez-Augustín O, de Medina FS, Ordovás JM, Garaulet M (2012) Sexual dimorphism in clock genes expression in human adipose tissue. Obes Surg 22(1):105–112

    PubMed  Google Scholar 

  91. Zanquetta MM, Correa-Giannella ML, Giannella-Neto D, Alonso PA, Guimarães LM, Meyer A, Villares SM (2012) Expression of clock genes in human subcutaneous and visceral adipose tissues. Chronobiol Int 29(3):252–260

    PubMed  CAS  Google Scholar 

  92. Gómez-Santos C, Gómez-Abellán P, Madrid JA, Hernández-Morante JJ, Lujan JA, Ordovas JM, Garaulet M (2009) Circadian rhythm of clock genes in human adipose explants. Obesity (Silver Spring) 17(8):1481–1485

    Google Scholar 

  93. Gómez-Abellán P, Madrid JA, Diez-Noguera A, Luján JA, Ordovás JM, Garaulet M. Resetting of circadian time of CLOCK in human adipose tissue by glucocorticoid signaling. PLoS One. 2012 (in press).

    Google Scholar 

  94. Otway DT, Mäntele S, Bretschneider S, Wright J, Trayhurn P, Skene DJ, Robertson MD, Johnston JD (2011) Rhythmic diurnal gene expression in human adipose tissue from individuals who are lean, overweight, and type 2 diabetic. Diabetes 60(5):1577–1581

    PubMed  CAS  Google Scholar 

  95. Gomez-Santos C, Hernandez-Morante JJ, Margareto J, Larrarte E, Formiguera X, Martínez CM, Garaulet M (2011) Profile of adipose tissue gene expression in premenopausal and postmenopausal women: site-specific differences. Menopause 18(6):675–684

    PubMed  Google Scholar 

  96. Otway DT, Frost G, Johnston JD (2009) Circadian rhythmicity in murine preadipocyte and adipocyte cells. Chronobiol Int 26:1340–1354

    PubMed  CAS  Google Scholar 

  97. Wu X, Zvonic S, Floyd ZE, Kilroy G, Goh BC, Hernandez TL, Eckel RH, Mynatt RL, Gimble JM (2007) Induction of circadian gene expression in human subcutaneous adipose-derived stem cells. Obesity (Silver Spring) 15(11):2560–2570

    CAS  Google Scholar 

  98. Gómez-Abellán P, Gómez-Santos C, Madrid JA, Milagro FI, Campion J, Martínez JA, Ordovás JM, Garaulet M (2010) Circadian expression of adiponectin and its receptors in human adipose tissue. Endocrinology 151(1):115–122

    PubMed  Google Scholar 

  99. Gómez Abellán P, Gómez Santos C, Madrid JA, Milagro FI, Campion J, Martínez JA, Luján JA, Ordovás JM, Garaulet M (2011) Site-specific circadian expression of leptin and its receptor in human adipose tissue. Nutr Hosp 26(6):1394–1401

    PubMed  Google Scholar 

  100. Hernandez-Morante JJ, Gomez-Santos C, Milagro F, Campión J, Martínez JA, Zamora S, Garaulet M (2009) Expression of cortisol metabolism-related genes shows circadian rhythmic patterns in human adipose tissue. Int J Obes (Lond) 33(4):473–480

    CAS  Google Scholar 

  101. Teboul M, Barrat-Petit MA, Li XM, Claustrat B, Formento JL, Delaunay F, Lévi F, Milano G (2005) Atypical patterns of circadian clock gene expression in human peripheral blood mononuclear cells. J Mol Med (Berl) 83(9):693–699

    CAS  Google Scholar 

  102. Boivin DB, James FO, Wu A, Cho-Park PF, Xiong H, Sun ZS (2003) Circadian clock genes oscillate in human peripheral blood mononuclear cells. Blood 102:4143–4145

    PubMed  CAS  Google Scholar 

  103. Khan S, Minihane AM, Talmud PJ, Wright JW, Murphy MC, Williams CM, Griffin BA (2002) Dietary long-chain n-3 PUFAs increase LPL gene expression in adipose tissue of subjects with an atherogenic lipoprotein phenotype. J Lipid Res 43(6):979–985

    PubMed  CAS  Google Scholar 

  104. Welsh DK, Kay SA (2005) Bioluminescence imaging in living organisms. Curr Opin Biotechnol 16(1):73–78

    PubMed  CAS  Google Scholar 

  105. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, Eckel RH, Takahashi JS, Bass J (2005) Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308:1043–1045

    PubMed  CAS  Google Scholar 

  106. Shimba S, Ogawa T, Hitosugi S, Ichihashi Y, Nakadaira Y, Kobayashi M, Tezuka M, Kosuge Y, Ishige K, Ito Y, Komiyama K, Okamatsu-Ogura Y, Kimura K, Saito M (2011) Deficient of a clock gene, brain and muscle Arnt-like protein-1 (BMAL1), induces dyslipidemia and ectopic fat formation. PLoS One 6(9):e25231

    PubMed  CAS  Google Scholar 

  107. Garaulet M, Ordovás JM, Gómez-Abellán P, Martínez JA, Madrid JA (2011) An approximation to the temporal order in endogenous circadian rhythms of genes implicated in human adipose tissue metabolism. J Cell Physiol 226(8):2075–2080

    PubMed  CAS  Google Scholar 

  108. Dietrich MO, Horvath TL (2009) Feeding signals and brain circuitry. Eur J Neurosci 30:1688–1696

    PubMed  Google Scholar 

  109. Kalra SP, Bagnasco M, Otukonyong EE, Dube MG, Kalra PS (2003) Rhythmic, reciprocal ghrelin and leptin signaling: new insight in the development of obesity. Regul Pept 111:1–11

    PubMed  CAS  Google Scholar 

  110. Garaulet M, Hernández-Morante JJ, de Heredia FP, Tébar FJ (2007) Adiponectin, the controversial hormone. Public Health Nutr 10:1145–1150

    PubMed  Google Scholar 

  111. Yang X, Downes M, Yu RT, Bookout AL, He W, Straume M, Mangelsdorf DJ, Evans RM (2006) Nuclear receptor expression links the circadian clock to metabolism. Cell 126:801–810

    PubMed  CAS  Google Scholar 

  112. Peterson RE (1957) Plasma corticosterone and hydrocortisone levels in man. J Clin Endocrinol Metab 17:1150–1157

    PubMed  CAS  Google Scholar 

  113. Henry BA, Clarke IJ (2008) Adipose tissue hormones and the regulation of food intake. J Neuroendocrinol 20:842–849

    PubMed  CAS  Google Scholar 

  114. Yang S, Liu A, Weidenhammer A, Cooksey RC, McClain D, Kim MK, Aguilera G, Abel ED, Chung JH (2009) The role of mPer2 clock gene in glucocorticoid and feeding rhythms. Endocrinology 150:2153–2160

    PubMed  CAS  Google Scholar 

  115. Qin LQ, Li J, Wang Y, Wang J, Xu JY, Kaneko T (2003) The effects of nocturnal life on endocrine circadian patterns in healthy adults. Life Sci 73:2467–2475

    PubMed  CAS  Google Scholar 

  116. Marin P, Darin N, Amemiya T, Andersson B, Jern S, Björntorp P (1992) Cortisol secretion in relation to body fat distribution in obese premenopausal women. Metabolism 41:882–886

    PubMed  CAS  Google Scholar 

  117. Björntorp P (1991) Adipose tissue distribution and function. Int J Obes 15:67–81

    PubMed  Google Scholar 

  118. Hermida RC, Ayala DE, Calvo C, López JE, Fernández JR, Mojón A, Domínguez MJ, Covelo M (2003) Administration-time dependent effects of acetyl-salicylic acid on blood pressure in patients with mild essential hypertension. Med Clin (Barc) 120:686–692

    Google Scholar 

  119. Hermida RC, Calvo C, Ayala DE, López JE, Fernández JR, Mojón A, Domínguez MJ, Covelo M (2003) Seasonal variation in plasma fibrinogen in dipper and non-dipper patients with mildmoderate essential hypertension. Med Clin (Barc) 121:6–11

    Google Scholar 

  120. Johnston JD (2012) Adipose circadian rhythms: translating cellular and animal studies to human physiology. Mol Cell Endocrinol 349(1):45–50

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Purificación Gómez-Abellán Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Gómez-Abellán, P., Garaulet, M. (2013). Adipose Tissue as a Peripheral Clock. In: Garaulet, M., Ordovás, J. (eds) Chronobiology and Obesity. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5082-5_3

Download citation

Publish with us

Policies and ethics