Biological aging alters circadian mechanisms in murine adipose tissue depots

Age

Volumn 35, Issue 3, 2013, Pages 533-547

  Sutton, Gregory M ^a   Ptitsyn, Andrey A ^b   Floyd, Z Elizabeth ^a   Yu, Gang ^a   Wu, Xiying ^a   Hamel, Katie ^a   Shah, Forum S ^a   Centanni, Armand ^a   Eilertsen, Kenneth ^a   Kheterpal, Indu ^a   Newman, Susan ^a   Leonardi, Claudia ^a,e   Freitas, Michael A ^c   Bunnell, Bruce A ^d   Gimble, Jeffrey M ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Brown adipose; Circadian; Liver; Oscillation; Transcriptomics; White adipose

Indexed keywords

CRYPTOCHROME 1; MESSENGER RNA; TRANSCRIPTOME;

AGING; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CRY1 GENE; EPIDIDYMIS FAT; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CODE; GENETIC TRANSCRIPTION; INGUINAL REGION; LIPID STORAGE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSICAL ACTIVITY; RETROPERITONEAL FAT; WHITE ADIPOSE TISSUE;

ADIPOGENESIS; ADIPOSE TISSUE; AGING; ANIMALS; CELL DIFFERENTIATION; CIRCADIAN RHYTHM; DISEASE MODELS, ANIMAL; FOLLOW-UP STUDIES; MALE; MICE; MICE, INBRED C57BL;

EID: 84880570366     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9389-7     Document Type: Article

References (109)

1. Ahmad AM, Guzder R, Wallace AM, Thomas J, Fraser WD, Vora JP (2001) Circadian and ultradian rhythm and leptin pulsatility in adult GH deficiency: effects of GH replacement. J Clin Endocrinol Metab 86:3499-3506
2. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH, Kyriacou CP (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12:540-550
3. Ando H, Yanagihara H, Hayashi Y, Obi Y, Tsuruoka S, Takamura T, Kaneko S, Fujimura A (2005) Rhythmic mRNA expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146:5631-5636
4. Arasaradnam MP, Morgan L, Wright J, Gama R (2002) Diurnal variation in lipoprotein lipase activity. Ann Clin Biochem 39:136-139
5. Atmaca M, Kuloglu M, Tezcan E, Ustundag B (2002) Weight gain and serum leptin levels in patients on lithium treatment. Neuropsychobiology 46:67-69
6. Baptista T, Teneud L, Contreras Q, Alastre T, Burguera JL, de Burguera M, de Baptista E, Weiss S, Hernandez L (1995) Lithium and body weight gain. Pharmacopsychiatry 28:35-44
7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Stat Soc B 57:289-300
8. Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, Johnson KW, Harrison SD, MacDougald OA (2002) Regulation of Wnt signaling during adipogenesis. J Biol Chem 277:30998-31004
9. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA (2005) Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A 102:3324-3329
10. Bray MS, Young ME (2009) The role of cell-specific circadian clocks in metabolism and disease. Obes Rev 10(Suppl 2):6-13
11. Calvani M, Scarfone A, Granato L, Mora EV, Nanni G, Castagneto M, Greco AV, Manco M, Mingrone G (2004) Restoration of adiponectin pulsatility in severely obese subjects after weight loss. Diabetes 53:939-947
12. Cartwright MJ, Tchkonia T, Kirkland JL (2007) Aging in adipocytes: potential impact of inherent, depot-specific mechanisms. Exp Gerontol 42:463-471
13. Cartwright MJ, Schlauch K, Lenburg ME, Tchkonia T, Pirtskhalava T, Cartwright A, Thomou T, Kirkland JL (2010) Aging, depot origin, and preadipocyte gene expression. J Gerontol A Biol Sci Med Sci 65:242-251
14. Chengappa KN, Chalasani L, Brar JS, Parepally H, Houck P, Levine J (2002) Changes in body weight and body mass index among psychiatric patients receiving lithium, valproate, or topiramate: an open-label, nonrandomized chart review. Clin Ther 24:1576-1584
15. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509-1517
16. Davies K (1994) Pressure sores: aetiology, risk factors and assessment scales. Br J Nurs 3:256-262
17. Duffield GE, Best JD, Meurers BH, Bittner A, Loros JJ, Dunlap JC (2002) Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr Biol 12:551-557
18. Elabd C, Chiellini C, Carmona M, Galitzky J, Cochet O, Petersen R, Penicaud L, Kristiansen K, Bouloumie A, Casteilla L, Dani C, Ailhaud G, Amri EZ (2009) Human multipotent adipose-derived stem cells differentiate into functional brown adipocytes. Stem Cells 27:2753-2760
19. Elmslie JL, Mann JI, Silverstone JT, Williams SM, Romans SE (2001) Determinants of overweight and obesity in patients with bipolar disorder. J Clin Psychiatry 62:486-491, quiz 492-483
20. Fagiolini A, Frank E, Houck PR, Mallinger AG, Swartz HA, Buysse DJ, Ombao H, Kupfer DJ (2002) Prevalence of obesity and weight change during treatment in patients with bipolar I disorder. J Clin Psychiatry 63:528-533
21. Fagiolini A, Kupfer DJ, Houck PR, Novick DM, Frank E (2003) Obesity as a correlate of outcome in patients with bipolar I disorder. Am J Psychiatry 160:112-117
22. Fonjallaz P, Ossipow V, Wanner G, Schibler U (1996) The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue-specific expression, but have different target promoter preferences. EMBO J 15:351-362
23. Froy O, Miskin R (2007) The interrelations among feeding, circadian rhythms and ageing. Prog Neurobiol 82:142-150
24. Froy O, Chapnik N, Miskin R (2006) Long-lived alphaMUPA transgenic mice exhibit pronounced circadian rhythms. Am J Physiol Endocrinol Metab 291:E1017-E1024
25. Froy O, Chapnik N, Miskin R (2008) Relationship between calorie restriction and the biological clock: lessons from long-lived transgenic mice. Rejuvenation Res 11:467-471
26. 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 127:905-916
27. Garg A, Agarwal AK (2009) Lipodystrophies: disorders of adipose tissue biology. Biochim Biophys Acta 1791:507-513
28. Gavi SFJ, Melendez MM, Mynarcik DC, Gelato MC, McNurlan MA (2007) Limb fat to trunk fat ratio in elderly persons is a strong determinant of insulin resistance and adiponectin levels. J Gerontol A Biol Sci Med Sci 62:997-1001
29. 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
30. Gimble JM, Floyd ZE (2009) Fat circadian biology. J Appl Physiol 107:1629-1637
31. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME (2006) Playing with bone and fat. J Cell Biochem 98:251-266
32. Gimble JM, Bray MS, Young A (2009) Circadian biology and sleep: missing links in obesity and metabolism? Obes Rev 10(Suppl 2):1-5
33. Goubern M, Portet R (1981) Circadian rhythm and hormonal sensitivity of lipoprotein lipase activity in cold acclimated rats. Horm Metab Res 13:73-77
34. Green CB, Besharse JC (1996) Identification of a novel vertebrate circadian clock-regulated gene encoding the protein nocturnin. Proc Natl Acad Sci U S A 93:14884-14888
35. Green CB, Takahashi JS, Bass J (2008) The meter of metabolism. Cell 134:728-742
36. Hernandez L, Roux KJ, Wong ES, Mounkes LC, Mutalif R, Navasankari R, Rai B, Cool S, Jeong JW, Wang H, Lee HS, Kozlov S, Grunert M, Keeble T, Jones CM, Meta MD, Young SG, Daar IO, Burke B, Perantoni AO, Stewart CL (2010) Functional coupling between the extracellular matrix and nuclear lamina by Wnt signaling in progeria. Dev Cell 19:413-425
37. 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 18:415-417
38. Hirota T, Fukada Y (2004) Resetting mechanism of central and peripheral circadian clocks in mammals. Zool Sci 21:359-368
39. Hogenesch JB, Panda S, Kay S, Takahashi JS (2003) Circadian transcriptional output in the SCN and liver of the mouse. Novartis Found Symp 253:171-180, discussion 152-175, 102-179, 180-173 passim
40. Holmback U, Forslund A, Forslund J, Hambraeus L, Lennernas M, Lowden A, Stridsberg M, Akerstedt T (2002) Metabolic responses to nocturnal eating in men are affected by sources of dietary energy. J Nutr 132:1892-1899
41. Holmback U, Forslund A, Lowden A, Forslund J, Akerstedt T, Lennernas M, Hambraeus L, Stridsberg M (2003) Endocrine responses to nocturnal eating - possible implications for night work. Eur J Nutr 42:75-83
42. Houstek J, Kopecky J, Baudysova M, Janikova D, Pavelka S, Klement P (1990) Differentiation of brown adipose tissue and biogenesis of thermogenic mitochondria in situ and in cell culture. Biochim Biophys Acta 1018:243-247
43. Huffman DM, Barzilai N (2009) Role of visceral adipose tissue in aging. Biochim Biophys Acta 1790:1117-1123
44. Iwahana E, Akiyama M, Miyakawa K, Uchida A, Kasahara J, Fukunaga K, Hamada T, Shibata S (2004) Effect of lithium on the circadian rhythms of locomotor activity and glycogen synthase kinase-3 protein expression in the mouse suprachiasmatic nuclei. Eur J Neurosci 19:2281-2287
45. Jiang Z, Gorenstein NM, Morre DM, Morre DJ (2008) Molecular cloning and characterization of a candidate human growth-related and time-keeping constitutive cell surface hydroquinone (NADH) oxidase. Biochemistry 47:14028-14038
46. Kawai M, Green CB, Lecka-Czernik B, Douris N, Gilbert MR, Kojima S, Ackert-Bicknell C, Garg N, Horowitz MC, Adamo ML, Clemmons DR, Rosen CJ (2010) A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-gamma nuclear translocation. Proc Natl Acad Sci U S A 107:10508-10513
47. Kirkland JL, Hollenberg CH, Gillon WS (1990) Age, anatomic site, and the replication and differentiation of adipocyte precursors. Am J Physiol 258:C206-C210
48. Kirkland JL, Hollenberg CH, Gillon WS (1993) Ageing, differentiation, and gene expression in rat epididymal preadipocytes. Biochem Cell Biol 71:556-561
49. Kirkland JL, Hollenberg CH, Kindler S, Gillon WS (1994) Effects of age and anatomic site on preadipocyte number in rat fat depots. J Gerontol 49:B31-B35
50. Klein PS, Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93:8455-8459
51. Kondratov RV (2007) A role of the circadian system and circadian proteins in aging. Ageing Res Rev 6:12-27
52. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP (2006) Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev 20:1868-1873
53. Kotlar TJ, Borensztajn J (1977) Oscillatory changes in muscle lipoprotein lipase activity of fed and starved rats. Am J Physiol 233:E316-E319
54. Kromkowski J, Hignite H, Morre DM, Morre DJ (2008) Response to lithium of a cell surface ECTO-NOX protein with time-keeping characteristics. Neurosci Lett 438:121-125
55. Kruger C, Kappen C (2010) Expression of cartilage developmental genes in Hoxc8- and Hoxd4-transgenic mice. PLoS One 5:e8978
56. Kumar N, Solt LA, Wang Y, Rogers PM, Bhattacharyya G, Kamenecka TM, Stayrook KR, Crumbley C, Floyd ZE, Gimble JM, Griffin PR, Burris TP (2010) Regulation of adipogenesis by natural and synthetic REV-ERB ligands. Endocrinology 151:3015-3025
57. Lafontan M, Berlan M, Carpene C (1985) Fat cell adrenoceptors: inter- and intraspecific differences and hormone regulation. Int J Obes 9(Suppl 1):117-127
58. Lemberger T, Saladin R, Vazquez M, Assimacopoulos F, Staels B, Desvergne B, Wahli W, Auwerx J (1996) Expression of the peroxisome proliferator-activated receptor alpha gene is stimulated by stress and follows a diurnal rhythm. J Biol Chem 271:1764-1769
59. Liew AW-C, Law N-F, Caoc X-Q, Yan H (2009) Statistical power of Fisher test for the detection of short periodic gene expression profiles. Pattern Recogn 42:549-556
60. Linford NJ, Beyer RP, Gollahon K, Krajcik RA, Malloy VL, Demas V, Burmer GC, Rabinovitch PS (2007) Transcriptional response to aging and caloric restriction in heart and adipose tissue. Aging Cell 6:673-688
61. Lowrey PL, Takahashi JS (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet 5:407-441
62. Marcheva B, Ramsey KM, Affinati A, Bass J (2009) Clock genes and metabolic disease. J Appl Physiol 107:1638-1646
63. Mastronardi CA, Yu WH, McCann SM (2002) Resting and circadian release of nitric oxide is controlled by leptin in male rats. Proc Natl Acad Sci U S A 99:5721-5726
64. Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80:147-154
65. Mitsui S, Yamaguchi S, Matsuo T, Ishida Y, Okamura H (2001) Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev 15:995-1006
66. Monk TH (2005) Aging human circadian rhythms: conventional wisdom may not always be right. J Biol Rhythms 20:366-374
67. Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293:E444-E452
68. Oishi K, Miyazaki K, Kadota K, Kikuno R, Nagase T, Atsumi G, Ohkura N, Azama T, Mesaki M, Yukimasa S, Kobayashi H, Iitaka C, Umehara T, Horikoshi M, Kudo T, Shimizu Y, Yano M, Monden M, Machida K, Matsuda J, Horie S, Todo T, Ishida N (2003) Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J Biol Chem 278:41519-41527
69. Ortega E, Xu X, Koska J, Marie Francisco A, Scalise M, Ferrante AW Jr, Krakoff J (2008) Macrophage content in subcutaneous adipose tissue: associations with adiposity, age, inflammatory markers, and whole-body insulin action in healthy Pima Indians. Diabetes 58:385-393
70. Padiath QS, Paranjpe D, Jain S, Sharma VK (2004) Glycogen synthase kinase 3beta as a likely target for the action of lithium on circadian clocks. Chronobiol Int 21:43-55
71. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002a) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307-320
72. Panda S, Hogenesch JB, Kay SA (2002b) Circadian rhythms from flies to human. Nature 417:329-335
73. Patel DD, Knight BL, Wiggins D, Humphreys SM, Gibbons GF (2001) Disturbances in the normal regulation of SREBP-sensitive genes in PPAR alpha-deficient mice. J Lipid Res 42:328-337
74. Ptitsyn A (2008) Stochastic resonance reveals "pilot light" expression in mammalian genes. PLoS One 3:e1842
75. Ptitsyn AA, Zvonic S, Conrad SA, Scott LK, Mynatt RL, Gimble JM (2006a) Circadian clocks are resounding in peripheral tissues. PLoS Comput Biol 2:e16
76. Ptitsyn AA, Zvonic S, Gimble JM (2006b) Permutation test for periodicity in short time series data. BMC Bioinforma 7(2):S10
77. Ptitsyn AA, Zvonic S, Gimble JM (2007) Digital signal processing reveals circadian baseline oscillation in majority of mammalian genes. PLoS Comput Biol 3:e120
78. Ptitsyn AA, Weil MM, Thamm DH (2008) Systems biology approach to identification of biomarkers for metastatic progression in cancer. BMC Bioinforma 9(9):S8
79. Ptitysn AAZS, Conrad SA, Scott LK, Mynatt ML, Gimble JM (2006) Circadian clocks are resounding in peripheral tissues. PLoS Comput Biol 2:e16
80. Rehnmark S, Nechad M, Herron D, Cannon B, Nedergaard J (1990) Alpha- and beta-adrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J Biol Chem 265:16464-16471
81. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA (2000) Inhibition of adipogenesis by Wnt signaling. Science 289:950-953
82. Ruge T, Wu G, Olivecrona T, Olivecrona G (2004) Nutritional regulation of lipoprotein lipase in mice. Int J Biochem Cell Biol 36:320-329
83. 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 83:453-459
84. Sato TK, Panda S, Kay SA, Hogenesch JB (2003) DNA arrays: applications and implications for circadian biology. J Biol Rhythms 18:96-105
85. Sato TK, Panda S, Miraglia LJ, Reyes TM, Rudic RD, McNamara P, Naik KA, FitzGerald GA, Kay SA, Hogenesch JB (2004) A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43:527-537
86. Savitzky AGM (1964) Smoothing and differentiation of data by simplified least squares procedures. Anal Chem 36:1627-1639
87. Shimba S, Wada T, Hara S, Tezuka M (2004) EPAS1 promotes adipose differentiation in 3T3-L1 cells. J Biol Chem 279:40946-40953
88. Shimba S, Ishii N, Ohta Y, 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
89. Spiegel K, Tasali E, Penev P, Van Cauter E (2004) Brief communication: sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann Intern Med 141:846-850
90. Sutton GM, Perez-Tilve D, Nogueiras R, Fang J, Kim JK, Cone RD, Gimble JM, Tschop MH, Butler AA (2008) The melanocortin-3 receptor is required for entrainment to meal intake. J Neurosci 28:12946-12955
91. Swindell WR (2008) Comparative analysis of microarray data identifies common responses to caloric restriction among mouse tissues. Mech Ageing Dev 129:138-153
92. Swindell WR (2009) Genes and gene expression modules associated with caloric restriction and aging in the laboratory mouse. BMC Genomics 10:585
93. Tchkonia T, Morbeck DE, Von Zglinicki T, Van Deursen J, Lustgarten J, Scrable H, Khosla S, Jensen MD, Kirkland JL (2010) Fat tissue, aging, and cellular senescence. Aging Cell 9:667-684
94. Torra IP, Tsibulsky V, Delaunay F, Saladin R, Laudet V, Fruchart JC, Kosykh V, Staels B (2000) Circadian and glucocorticoid regulation of Rev-erbalpha expression in liver. Endocrinology 141:3799-3806
95. Trayhurn P (2005) Endocrine and signalling role of adipose tissue: new perspectives on fat. Acta Physiol Scand 184:285-293
96. Trayhurn P, Beattie JH (2001) Physiological role of adipose tissue: white adipose tissue as an endocrine and secretory organ. Proc Nutr Soc 60:329-339
97. Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, Iino M, Shigeyoshi Y, Hashimoto S (2002) A transcription factor response element for gene expression during circadian night. Nature 418:534-539
98. Valentinuzzi VS, Scarbrough K, Takahashi JS, Turek FW (1997) Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice. Am J Physiol 273:R1957-R1964
99. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500-1508
100. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518-1525
101. Weinert D, Waterhouse J (1999) Daily activity and body temperature rhythms do not change simultaneously with age in laboratory mice. Physiol Behav 66:605-612
102. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796-1808
103. Wichert S, Fokianos K, Strimmer K (2004) Identifying periodically expressed transcripts in microarray time series data. Bioinformatics 20:5-20
104. Yang X, Enerback S, Smith U (2003) Reduced expression of FOXC2 and brown adipogenic genes in human subjects with insulin resistance. Obes Res 11:1182-1191
105. Yang X, Jansson PA, Nagaev I, Jack MM, Carvalho E, Sunnerhagen KS, Cam MC, Cushman SW, Smith U (2004) Evidence of impaired adipogenesis in insulin resistance. Biochem Biophys Res Commun 317:1045-1051
106. Yildiz BO, Suchard MA, Wong ML, McCann SM, Licinio J (2004) Alterations in the dynamics of circulating ghrelin, adiponectin, and leptin in human obesity. Proc Natl Acad Sci U S A 101:10434-10439
107. Yin L, Wu N, Curtin JC, Qatanani M, Szwergold NR, Reid RA, Waitt GM, Parks DJ, Pearce KH, Wisely GB, Lazar MA (2007) Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 318:1786-1789
108. 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 55:962-970
109. Zvonic S, Ptitsyn AA, Kilroy G, Wu X, Conrad SA, Scott LK, Guilak F, Pelled G, Gazit D, Gimble JM (2007) Circadian oscillation of gene expression in murine calvarial bone. J Bone Miner Res 22:357-365