Modulation of gene expression by 3-iodothyronamine: Genetic evidence for a lipolytic pattern

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Mariotti, Veronica ^a   Melissari, Erika ^a   Iofrida, Caterina ^a   Righi, Marco ^a   Di Russo, Manuela ^a   Donzelli, Riccardo ^a   Saba, Alessandro ^a   Frascarelli, Sabina ^a   Chiellini, Grazia ^a   Zucchi, Riccardo ^a   Pellegrini, Silvia ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

3 IODOTHYRONAMINE; BIOGENIC AMINE; THYROID HORMONE; UNCLASSIFIED DRUG; 3-IODOTHYRONAMINE; THYRONINE DERIVATIVE;

ACSL5 GENE; ADIPOGENESIS; ADIPOSE TISSUE; ADRA2C; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOD GENE; ARTICLE; CEBPB GENE; CONTROLLED STUDY; DMPK GENE; FATTY ACID OXIDATION; G0S2 GENE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HORMONE DETERMINATION; IGFBP2 GENE; IN VIVO STUDY; LDLRAP1 GENE; LIPOLYSIS; LIPOPROTEIN METABOLISM; LIVER; LRP10 GENE; MALE; MICROARRAY ANALYSIS; NOLC1 GENE; NONHUMAN; PEX5 GENE; PMP22 GENE; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCARB1 GENE; SIRT2 GENE; SIRT6 GENE; STAT5B GENE; ANIMAL; DRUG EFFECTS; GENETICS; METABOLISM; WISTAR RAT;

ADIPOSE TISSUE; ANIMALS; GENE EXPRESSION REGULATION; LIPOLYSIS; LIVER; MALE; RATS; RATS, WISTAR; THYRONINES; TRANSCRIPTION, GENETIC;

EID: 84908371005     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106923     Document Type: Article

References (102)

1. Viguerie N, Millet L, Avizou S, Vidal H, Larrouy D, et al. (2002) Regulation of human adipocyte gene expression by thyroid hormone. J Clin Endocrinol Metab 87: 630-634.
2. Hauner H, Entenmann G, Wabitsch M, Gaillard D, Ailhaud G, et al. (1989) Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest 84: 1663-1670.
3. Darimont C, Gaillard D, Ailhaud G, Negrel R (1993) Terminal differentiation of mouse preadipocyte cells: adipogenic and antimitogenic role of triiodothyronine. Mol Cell Endocrinol 98: 67-73.
4. Krotkiewski M (2002) Thyroid hormones in the pathogenesis and treatment of obesity. Eur J Pharmacol 440: 85-98.
5. Chiellini G, Frascarelli S, Ghelardoni S, Carnicelli V, Tobias SC, et al. (2007) Cardiac effects of 3-iodothyronamine: a new aminergic system modulating cardiac function. FASEB J 21: 1597-1608.
6. Braulke LJ, Klingenspor M, DeBarber A, Tobias SC, Grandy DK, et al. (2008) 3-Iodothyronamine: a novel hormone controlling the balance between glucose and lipid utilisation. J Comp Physiol B 178: 167-177.
7. Scanlan TS, Suchland KL, Hart ME, Chiellini G, Huang Y, et al. (2004) 3-Iodothyronamine is an endogenous and rapid-acting derivative of thyroid hormone. Nat Med 10: 638-642.
8. Saba A, Chiellini G, Frascarelli S, Marchini M, Ghelardoni S, et al. (2010) Tissue distribution and cardiac metabolism of 3-iodothyronamine. Endocrinology 151: 5063-5073.
9. Galli E, Marchini M, Saba A, Berti S, Tonacchera M, et al. (2012) Detection of 3-iodothyronamine in human patients: a preliminary study. J Clin Endocrinol Metab 97: E69-74.
10. Wu SY, Green WL, Huang WS, Hays MT, Chopra IJ (2005) Alternate pathways of thyroid hormone metabolism. Thyroid 15: 943-958.
11. Regard JB, Kataoka H, Cano DA, Camerer E, Yin L, et al. (2007) Probing cell type-specific functions of Gi in vivo identifies GPCR regulators of insulin secretion. J Clin Invest 117: 4034-4043.
12. Haviland JA, Reiland H, Butz DE, Tonelli M, Porter WP, et al. (2013) NMRbased metabolomics and breath studies show lipid and protein catabolism during low dose chronic T(1)AM treatment. Obesity (Silver Spring) 21: 2538-2544.
13. Dhillo WS, Bewick GA, White NE, Gardiner JV, Thompson EL, et al. (2009) The thyroid hormone derivative 3-iodothyronamine increases food intake in rodents. Diabetes Obes Metab 11: 251-260.
14. Klieverik LP, Foppen E, Ackermans MT, Serlie MJ, Sauerwein HP, et al. (2009) Central effects of thyronamines on glucose metabolism in rats. J Endocrinol 201: 377-386.
15. Manni ME, De Siena G, Saba A, Marchini M, Dicembrini I, et al. (2012) 3-Iodothyronamine: a modulator of the hypothalamus-pancreas-thyroid axes in mice. Br J Pharmacol 166: 650-658.
16. Manni ME, De Siena G, Saba A, Marchini M, Landucci E, et al. (2013) Pharmacological effects of 3-iodothyronamine (T1AM) in mice include facilitation of memory acquisition and retention and reduction of pain threshold. Br J Pharmacol 168: 354-362.
17. Zucchi R, Chiellini G, Scanlan TS, Grandy DK (2006) Trace amine-associated receptors and their ligands. Br J Pharmacol 149: 967-978.
18. Snead AN, Santos MS, Seal RP, Miyakawa M, Edwards RH, et al. (2007) Thyronamines inhibit plasma membrane and vesicular monoamine transport. ACS Chem Biol 2: 390-398.
19. Smyth G (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer New York:. pp.397-420.
20. Patterson TA, Lobenhofer EK, Fulmer-Smentek SB, Collins PJ, Chu TM, et al. (2006) Performance comparison of one-color and two-color platforms within the Micro Array Quality Control (MAQC) project. Nat Biotechnol 24: 1140-1150.
21. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
22. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Meth) 57: 289-300.
23. Safran M, Chalifa-Caspi V, Shmueli O, Olender T, Lapidot M, et al. (2003) Human Gene-Centric Databases at the Weizmann Institute of Science: Gene Cards, UDB, CroW 21 and HORDE. Nucleic Acids Res 31: 142-146.
24. Draghici S, Khatri P, Bhavsar P, Shah A, Krawetz SA, et al. (2003) Onto-Tools, the toolkit of the modern biologist: Onto-Express, Onto-Compare, Onto-Design and Onto-Translate. Nucleic Acids Res 31: 3775-3781.
25. Khatri P, Draghici S, Ostermeier GC, Krawetz SA (2002) Profiling gene expression using onto-express. Genomics 79: 266-270.
26. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
27. Postic C, Dentin R, Girard J (2004) Role of the liver in the control of carbohydrate and lipid homeostasis. Diabetes Metab 30: 398-408.
28. Havel PJ (2004) Update on adipocyte hormones: regulation of energy balance and carbohydrate/lipid metabolism. Diabetes 53 Suppl 1: S143-151.
29. Yu BL, Zhao SP, Hu JR (2010) Cholesterol imbalance in adipocytes: a possible mechanism of adipocytes dysfunction in obesity. Obes Rev 11: 560-567.
30. Kovanen PT, Nikkilä EA, Miettinen TA (1975) Regulation of cholesterol synthesis and storage in fat cells. J Lipid Res 16: 211-223.
31. Michaely P, Li W, Anderson R, Cohen J, Hobbs H (2004) The modular adaptor protein ARH is required for low density lipoprotein (LDL) binding and internalization but not for LDL receptor clustering in coated pits. J Biol Chem 279: 34023-34031.
32. Sugiyama T, Kumagai H, Morikawa Y, Wada Y, Sugiyama A, et al. (2000) A novel low-density lipoprotein receptor-related protein mediating cellular uptake of apolipoprotein E-enriched beta-VLDL in vitro. Biochemistry 39: 15817-15825.
33. Xie Z, Wu X, Zhuang C, Chen F, Wang Z, et al. (2009) [Protective effects of Ginkgo biloba extract on morphology and function of retinal ganglion cells after optic nerve transection in guinea pigs]. Zhong Xi Yi Jie He Xue Bao 7: 940-946.
34. Perdomo G, Henry Dong H (2009) Apolipoprotein D in lipid metabolism and its functional implication in atherosclerosis and aging. Aging (Albany NY) 1: 17-27.
35. Mahley RW, Innerarity TL, Rall SC, Weisgraber KH (1984) Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res 25: 1277-1294.
36. Steyrer E, Kostner GM (1988) Activation of lecithin-cholesterol acyltransferase by apolipoprotein D: comparison of proteoliposomes containing apolipoprotein D, A-I or C-I. Biochim Biophys Acta 958: 484-491.
37. Rassart E, Bedirian A, Do Carmo S, Guinard O, Sirois J, et al. (2000) Apolipoprotein D. Biochim Biophys Acta 1482: 185-198.
38. Blanco-Vaca F, Via DP, Yang CY, Massey JB, Pownall HJ (1992) Characterization of disulfide-linked heterodimers containing apolipoprotein D in human plasma lipoproteins. J Lipid Res 33: 1785-1796.
39. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, et al. (1996) Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271: 518-520.
40. Trigatti B, Rigotti A, Krieger M (2000) The role of the high-density lipoprotein receptor SR-BI in cholesterol metabolism. Curr Opin Lipidol 11: 123-131.
41. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, et al. (1997) A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc Natl Acad Sci U S A 94: 12610-12615.
42. Out R, Hoekstra M, Spijkers JA, Kruijt JK, van Eck M, et al. (2004) Scavenger receptor class B type I is solely responsible for the selective uptake of cholesteryl esters from HDL by the liver and the adrenals in mice. J Lipid Res 45: 2088-2095.
43. Trigatti B, Rayburn H, Viñals M, Braun A, Miettinen H, et al. (1999) Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A 96: 9322-9327.
44. Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73: 417-435.
45. Haigis MC, Guarente LP (2006) Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev 20: 2913-2921.
46. Liszt G, Ford E, Kurtev M, Guarente L (2005) Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J Biol Chem 280: 21313-21320.
47. Kanfi Y, Peshti V, Gil R, Naiman S, Nahum L, et al. (2010) SIRT6 protects against pathological damage caused by diet-induced obesity. Aging Cell 9: 162-173.
48. Beh CT, Cool L, Phillips J, Rine J (2001) Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics 157: 1117-1140.
49. Gill S, Chow R, Brown AJ (2008) Sterol regulators of cholesterol homeostasis and beyond: the oxysterol hypothesis revisited and revised. Prog Lipid Res 47: 391-404.
50. Langin D (2006) Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome. Pharmacol Res 53: 482-491.
51. Lafontan M, Berlan M (1995) Fat cell alpha 2-adrenoceptors: the regulation of fat cell function and lipolysis. Endocr Rev 16: 716-738.
52. Berlan M, Montastruc JL, Lafontan M (1992) Pharmacological prospects for alpha 2-adrenoceptor antagonist therapy. Trends Pharmacol Sci 13: 277-282.
53. Yang X, Lu X, Lombès M, Rha GB, Chi YI, et al. (2010) The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab 11: 194-205.
54. Achouri Y, Hegarty BD, Allanic D, Bécard D, Hainault I, et al. (2005) Long chain fatty acyl-CoA synthetase 5 expression is induced by insulin and glucose: involvement of sterol regulatory element-binding protein-1c. Biochimie 87: 1149-1155.
55. Li L (2006) Functions of Rat Acyl-CoA Synthetases in bacteria and mammalian cells: University of North Carolina.
56. Coleman RA, Lewin TM, Van Horn CG, Gonzalez-Baró MR (2002) Do longchain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J Nutr 132: 2123-2126.
57. Lewin TM, Kim JH, Granger DA, Vance JE, Coleman RA (2001) Acyl-CoA synthetase isoforms 1, 4, and 5 are present in different subcellular membranes in rat liver and can be inhibited independently. J Biol Chem 276: 24674-24679.
58. Kim JH, Lewin TM, Coleman RA (2001) Expression and characterization of recombinant rat Acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J Biol Chem 276: 24667-24673.
59. Igal RA, Wang P, Coleman RA (1997) Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid: evidence for functionally separate pools of acyl-CoA. Biochem J 324 (Pt 2): 529-534.
60. Varanasi U, Chu R, Huang Q, Castellon R, Yeldandi AV, et al. (1996) Identification of a peroxisome proliferator-responsive element upstream of the human peroxisomal fatty acyl coenzyme A oxidase gene. J Biol Chem 271: 2147-2155.
61. Mannaerts GP, Van Veldhoven PP, Casteels M (2000) Peroxisomal lipid degradation via beta- and alpha-oxidation in mammals. Cell Biochem Biophys 32 Spring: 73-87.
62. Bon GB (2008) [Adipose tissue: a multifunctional organ]. G Ital Cardiol (Rome) 9: 23S-28S.
63. Hausman DB, DiGirolamo M, Bartness TJ, Hausman GJ, Martin RJ (2001) The biology of white adipocyte proliferation. Obes Rev 2: 239-254.
64. Rosen ED, Hsu CH, Wang X, Sakai S, Freeman MW, et al. (2002) C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev 16: 22-26.
65. Miyaoka Y, Tanaka M, Naiki T, Miyajima A (2006) Oncostatin M inhibits adipogenesis through the RAS/ERK and STAT5 signaling pathways. J Biol Chem 281: 37913-37920.
66. White UA, Stephens JM (2010) Transcriptional factors that promote formation of white adipose tissue. Mol Cell Endocrinol 318: 10-14.
67. Nanbu-Wakao R, Morikawa Y, Matsumura I, Masuho Y, Muramatsu MA, et al. (2002) Stimulation of 3T3-L1 adipogenesis by signal transducer and activator of transcription 5. Mol Endocrinol 16: 1565-1576.
68. Schneider C, King RM, Philipson L (1988) Genes specifically expressed at growth arrest of mammalian cells. Cell 54: 787-793.
69. Shugart EC, Levenson AS, Constance CM, Umek RM (1995) Differential expression of gas and gadd genes at distinct growth arrest points during adipocyte development. Cell Growth Differ 6: 1541-1547.
70. Jing E, Gesta S, Kahn CR (2007) SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab 6: 105-114.
71. Claudio PP, Tonini T, Giordano A (2002) The retinoblastoma family: twins or distant cousins? Genome Biol 3: reviews3012.
72. Konishi M, Asaki T, Koike N, Miwa H, Miyake A, et al. (2006) Role of Fgf10 in cell proliferation in white adipose tissue. Mol Cell Endocrinol 249: 71-77.
73. Baxter RC, Twigg SM (2009) Actions of IGF binding proteins and related proteins in adipose tissue. Trends Endocrinol Metab 20: 499-505.
74. MacDougald OA, Lane MD (1995) Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem 64: 345-373.
75. Rehfeldt C, Renne U, Sawitzky M, Binder G, Hoeflich A (2010) Increased fat mass, decreased myofiber size, and a shift to glycolytic muscle metabolism in adolescent male transgenic mice overexpressing IGFBP-2. Am J Physiol Endocrinol Metab 299: E287-298.
76. Llagostera E, Carmona MC, Vicente M, Escorihuela RM, Kaliman P (2009) High-fat diet induced adiposity and insulin resistance in mice lacking the myotonic dystrophy protein kinase. FEBS Lett 583: 2121-2125.
77. Christiaens V, Lijnen HR (2010) Angiogenesis and development of adipose tissue. Mol Cell Endocrinol 318: 2-9.
78. Rupnick MA, Panigrahy D, Zhang CY, Dallabrida SM, Lowell BB, et al. (2002) Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci U S A 99: 10730-10735.
79. Hausman GJ, Richardson RL (2004) Adipose tissue angiogenesis. J Anim Sci 82: 925-934.
80. Garitaonandia I, Smith JL, Kupchak BR, Lyons TJ (2009) Adiponectin identified as an agonist for PAQR3/RKTG using a yeast-based assay system. J Recept Signal Transduct Res 29: 67-73.
81. Zhang Y, Jiang X, Qin X, Ye D, Yi Z, et al. (2010) RKTG inhibits angiogenesis by suppressing MAPK-mediated autocrine VEGF signaling and is downregulated in clear-cell renal cell carcinoma. Oncogene 29: 5404-5415.
82. Chen W, Li L, Zhu J, Liu J, Soria J, et al. (2004) Control of angiogenesis by inhibitor of phospholipase A2. Chin Med Sci J 19: 6-12.
83. Sirinian MI, Belleudi F, Campagna F, Ceridono M, Garofalo T, et al. (2005) Adaptor protein ARH is recruited to the plasma membrane by low density lipoprotein (LDL) binding and modulates endocytosis of the LDL/LDL receptor complex in hepatocytes. J Biol Chem 280: 38416-38423.
84. Takaishi K, Duplomb L, Wang MY, Li J, Unger RH (2004) Hepatic insig-1 or -2 overexpression reduces lipogenesis in obese Zucker diabetic fatty rats and in fasted/refed normal rats. Proc Natl Acad Sci U S A 101: 7106-7111.
85. LaFave LT, Augustin LB, Mariash CN (2006) S14: insights from knockout mice. Endocrinology 147: 4044-4047.
86. Magnuson MA, Nikodem VM (1983) Molecular cloning of a cDNA sequence for rat malic enzyme. Direct evidence for induction in vivo of rat liver malic enzyme mRNA by thyroid hormone. J Biol Chem 258: 12712-12717.
87. Wise EM, Ball EG (1964) Malic Enzyme and Lipogenesis. Proc Natl Acad Sci U S A 52: 1255-1263.
88. Bublitz C, Kennedy EP (1954) Synthesis of phosphatides in isolated mitochondria. III. The enzymatic phosphorylation of glycerol. J Biol Chem 211: 951-961.
89. Gachon F, Leuenberger N, Claudel T, Gos P, Jouffe C, et al. (2011) Prolineand acidic amino acid-rich basic leucine zipper proteins modulate peroxisome proliferator-activated receptor alpha (PPARalpha) activity. Proc Natl Acad Sci U S A 108: 4794-4799.
90. Pucci E, Chiovato L, Pinchera A (2000) Thyroid and lipid metabolism. Int J Obes Relat Metab Disord 24 Suppl 2: S109-112.
91. Bujalska IJ, Quinkler M, Tomlinson JW, Montague CT, Smith DM, et al. (2006) Expression profiling of 11beta-hydroxysteroid dehydrogenase type-1 and glucocorticoid-target genes in subcutaneous and omental human preadipocytes. J Mol Endocrinol 37: 327-340.
92. Nielsen TS, Kampmann U, Nielsen RR, Jessen N, Orskov L, et al. (2012) Reduced mRNA and protein expression of perilipin A and G0/G1 switch gene 2 (G0S2) in human adipose tissue in poorly controlled type 2 diabetes. J Clin Endocrinol Metab 97: E1348-1352.
93. Menéndez-Hurtado A, Vega-Núñez E, Santos A, Perez-Castillo A (1997) Regulation by thyroid hormone and retinoic acid of the CCAAT/enhancer binding protein alpha and beta genes during liver development. Biochem Biophys Res Commun 234: 605-610.
94. Sato Y, Nishio Y, Sekine O, Kodama K, Nagai Y, et al. (2007) Increased expression of CCAAT/enhancer binding protein-beta and -delta and monocyte chemoattractant protein-1 genes in aortas from hyperinsulinaemic rats. Diabetologia 50: 481-489.
95. Pereira RC, Durant D, Canalis E (2000) Transcriptional regulation of connective tissue growth factor by cortisol in osteoblasts. Am J Physiol Endocrinol Metab 279: E570-576.
96. Sharma P, Thakran S, Deng X, Elam MB, Park EA (2013) Nuclear corepressors mediate the repression of phospholipase A2 group IIa gene transcription by thyroid hormone. J Biol Chem 288: 16321-16333.
97. Narkewicz MR, Iynedjian PB, Ferre P, Girard J (1990) Insulin and triiodothyronine induce glucokinase mRNA in primary cultures of neonatal rat hepatocytes. Biochem J 271: 585-589.
98. Wang Z, Iwasaki Y, Zhao LF, Nishiyama M, Taguchi T, et al. (2009) Hormonal regulation of glycolytic enzyme gene and pyruvate dehydrogenase kinase/phosphatase gene transcription. Endocr J 56: 1019-1030.
99. Katsurada A, Iritani N, Fukuda H, Noguchi T, Tanaka T (1988) Transcriptional and posttranscriptional regulation of malic enzyme synthesis by insulin and triiodothyronine. Biochim Biophys Acta 950: 113-117.
100. Mariash CN, Jump DB, Oppenheimer JH (1984) T3 stimulates the synthesis of a specific mRNA in primary hepatocyte culture. Biochem Biophys Res Commun 123: 1122-1129.
101. Jump DB, Bell A, Lepar G, Hu D (1990) Insulin rapidly induces rat liver S14 gene transcription. Mol Endocrinol 4: 1655-1660.
102. Fernández-Alvarez A, Soledad Alvarez M, Cucarella C, Casado M (2010) Characterization of the human insulin-induced gene 2 (INSIG2) promoter: the role of Ets-binding motifs. J Biol Chem 285: 11765-11774.