Postnatal exposure to a high-carbohydrate diet interferes epigenetically with thyroid hormone receptor induction of the adult male rat skeletal muscle glucose transporter isoform 4 expression

Journal of Nutritional Biochemistry

Volumn 25, Issue 10, 2014, Pages 1066-1076

  Raychaudhuri, Nupur ^a,c   Thamotharan, Shanthie ^a   Srinivasan, Malathi ^b   Mahmood, Saleh ^b   Patel, Mulchand S ^b   Devaskar, Sherin U ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

DNA methylase; DNA methylation; High Carbohydrate programming; Histone code modifications; Histone deacetylase; Insulin resistance; Obesity

Indexed keywords

DNA FRAGMENT; DNA METHYLTRANSFERASE; GLUCOSE TRANSPORTER 4; HISTONE DEACETYLASE 4; LIOTHYRONINE; THYROID HORMONE RECEPTOR; THYROTROPIN; THYROXINE; CARBOHYDRATE DIET; CREBBP PROTEIN, RAT; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HDAC4 PROTEIN, RAT; HISTONE; HISTONE DEACETYLASE; MESSENGER RNA; SLC2A4 PROTEIN, RAT;

ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL MILK; CARBOHYDRATE DIET; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; GENE EXPRESSION; GLUCOSE TRANSPORT; HISTONE CODE; IN VIVO STUDY; INSULIN RESISTANCE; MALE; NONHUMAN; OBESITY; PERINATAL PERIOD; PROMOTER REGION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; THYROID HORMONE BLOOD LEVEL; THYROTROPIN BLOOD LEVEL; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; CELL CULTURE; CPG ISLAND; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; IMMUNOPRECIPITATION; METABOLISM; NEWBORN; POSTNATAL CARE;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CPG ISLANDS; CREB-BINDING PROTEIN; DIETARY CARBOHYDRATES; DNA METHYLATION; EPIGENESIS, GENETIC; GLUCOSE TRANSPORTER TYPE 4; HISTONE DEACETYLASES; HISTONES; IMMUNOPRECIPITATION; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; POSTNATAL CARE; PROMOTER REGIONS, GENETIC; RATS; RECEPTORS, THYROID HORMONE; RNA, MESSENGER; THYROXINE; TRIIODOTHYRONINE;

EID: 84926415917     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.05.011     Document Type: Article

References (54)

1. Garg M., Thamotharan M., Dai Y., Lagishetty V., Matveyenko A.V., Lee W.N., et al. Glucose intolerance and lipid metabolic adaptations in response to intrauterine and postnatal calorie restriction in male adult rats. Endocrinology 2013, 154:102-113.
2. Garg M., Thamotharan M., Dai Y., Thamotharan S., Shin B.C., Stout D., et al. Early postnatal caloric restriction protects adult male intrauterine growth-restricted offspring from obesity. Diabetes 2012, 61:1391-1398.
3. Srinivasan M., Katewa S.D., Palaniyappan A., Pandya J.D., Patel M.S. Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab 2006, 291:E792-E799.
4. Srinivasan M., Mitrani P., Sadhanandan G., Dodds C., Shbeir-ElDika S., Thamotharan S., et al. A high-carbohydrate diet in the immediate postnatal life of rats induces adaptations predisposing to adult-onset obesity. J Endocrinol 2008, 197:565-574.
5. O'Doherty R.M., Halseth A.E., Granner D.K., Bracy D.P., Wasserman D.H. Analysis of insulin-stimulated skeletal muscle glucose uptake in conscious rat using isotopic glucose analogs. Am J Physiol 1998, 274:E287-E296.
6. Dai Y., Thamotharan S., Garg M., Shin B.C., Devaskar S.U. Superimposition of postnatal calorie restriction protects the aging male intrauterine growth- restricted offspring from metabolic maladaptations. Endocrinology 2012, 153:4216-4226.
7. Raychaudhuri N., Raychaudhuri S., Thamotharan M., Devaskar S.U. Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J Biol Chem 2008, 283:13611-13626.
8. Thamotharan M., Shin B.C., Suddirikku D.T., Thamotharan S., Garg M., Devaskar S.U. GLUT4 expression and subcellular localization in the intrauterine growth-restricted adult rat female offspring. Am J Physiol Endocrinol Metab 2005, 288:E935-E947.
9. Wang C. The relationship between type 2 diabetes mellitus and related thyroid diseases. J Diabetes Res 2013, 390534.
10. Casla A., Rovira A., Wells J.A., Dohm G.L. Increased glucose transporter (GLUT4) protein expression in hyperthyroidism. Biochem Biophys Res Commun 1990, 171:182-188.
11. Weinstein S.P., O'Boyle E., Haber R.S. Thyroid hormone increases basal and insulin-stimulated glucose transport in skeletal muscle. The role of GLUT4 glucose transporter expression. Diabetes 1994, 43:1185-1189.
12. Richardson J.M., Pessin J.E. Identification of a skeletal muscle-specific regulatory domain in the rat GLUT4/muscle-fat gene. J Biol Chem 1993, 268:21021-21027.
13. Hiremagalur B.K., Vadlamudi S., Johanning G.L., Patel M.S. Long-term effects of feeding high carbohydrate diet in pre-weaning period by gastrostomy: a new rat model for obesity. Int J Obes Relat Metab Disord 1993, 17:495-502.
14. Patel M.S., Vadlamudi S., Johanning G.L. Artificial rearing of rat pups: implications for nutrition research. Annu Rev Nutr 1994, 14:21-40.
15. Mitrani P., Srinivasan M., Dodds C., Patel M.S. Role of the autonomic nervous system in the development of hyperinsulinemia by high-carbohydrate formula feeding to neonatal rats. Am J Physiol Endocrinol Metab 2007, 292:E1069-E1078.
16. Vadlamudi S., Hiremagalur B.K., Tao L., Kalhan S.C., Kalaria R.N., Kaung H.L., et al. Long-term effects on pancreatic function of feeding a HC formula to rats during the preweaning period. Am J Physiol 1993, 265:E565-E571.
17. Rajakumar A., Thamotharan S., Raychaudhuri N., Menon R.K., Devaskar S.U. Trans-activators regulating neuronal glucose transporter isoform-3 gene expression in mammalian neurons. J Biol Chem 2004, 279:26768-26779.
18. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
19. Brickner D.G., Cajigas I., Fondufe-Mittendorf Y., Ahmed S., Lee P.C., Widom J., et al. H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol 2007, 5:e81.
20. Ozanne S.E., Jensen C.B., Tingey K.J., Storgaard H., Madsbad S., Vaag A.A. Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 2005, 48:547-552.
21. Agote M., Goya L., Ramos S., Alvarez C., Gavete M.L., Pascual-Leone A.M., et al. Glucose uptake and glucose transporter proteins in skeletal muscle from undernourished rats. Am J Physiol Endocrinol Metab 2001, 281:E1101-E1109.
22. Santalucia T., Moreno H., Palacin M., Yacoub M.H., Brand N.J., Zorzano A. A novel functional co-operation between MyoD, MEF2 and TRalpha1 is sufficient for the induction of GLUT4 gene transcription. J Mol Biol 2001, 314:195-204.
23. Liu M.L., Olson A.L., Edgington N.P., Moye-Rowley W.S., Pessin J.E. Myocyte enhancer factor 2 (MEF2) binding site is essential for C2C12 myotube-specific expression of the rat GLUT4/muscle-adipose facilitative glucose transporter gene. J Biol Chem 1994, 269:28514-28521.
24. Thai M.V., Guruswamy S., Cao K.T., Pessin J.E., Olson A.L. Myocyte enhancer factor 2 (MEF2)-binding site is required for GLUT4 gene expression in transgenic mice. Regulation of MEF2 DNA binding activity in insulin-deficient diabetes. J Biol Chem 1998, 273:14285-14292.
25. Johnsen L., Kongsted A.H., Nielsen M.O. Prenatal undernutrition and postnatal overnutrition alter thyroid hormone axis function in sheep. J Endocrinol 2013, 216:389-402.
26. Suter M.A., Sangi-Haghpeykar H., Showalter L., Shope C., Hu M., Brown K., et al. Maternal high-fat diet modulates the fetal thyroid axis and thyroid gene expression in a nonhuman primate model. Mol Endocrinol 2012, 26:2071-2080.
27. Moreno M., de Lange P., Lombardi A., Silvestri E., Lanni A., Goglia F. Metabolic effects of thyroid hormone derivatives. Thyroid 2008, 18:239-253.
28. Schmitt T., Luqman W., McCool C., Lenz F., Ahmad U., Nolan S., et al. Unresponsiveness to exogenous TSH in obesity. Int J Obes 1977, 1:185-190.
29. Sultan K.R., Henkel B., Terlou M., Haagsman H.P. Quantification of hormone-induced atrophy of large myotubes from C2C12 and L6 cells: atrophy-inducible and atrophy-resistant C2C12 myotubes. Am J Physiol Cell Physiol 2006, 290(2):C650-C659.
30. Brent G.A. The molecular basis of thyroid hormone action. N Engl J Med 1994, 331:847-853.
31. Glass C.K., Holloway J.M. Regulation of gene expression by the thyroid hormone receptor. Biochim Biophys Acta 1990, 1032:157-176.
32. Desvergne B. How do thyroid hormone receptors bind to structurally diverse response elements?. Mol Cell Endocrinol 1994, 100:125-131.
33. Williams G.R., Bland R., Sheppard M.C. Retinoids modify regulation of endogenous gene expression by vitamin D3 and thyroid hormone in three osteosarcoma cell lines. Endocrinology 1995, 136:4304-4314.
34. Mangelsdorf D.J., Borgmeyer U., Heyman R.A., Zhou J.Y., Ong E.S., Oro A.E., et al. Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev 1992, 6:329-344.
35. Sugawara A., Yen P.M., Darling D.S., Chin W.W. Characterization and tissue expression of multiple triiodothyronine receptor-auxiliary proteins and their relationship to the retinoid X-receptors. Endocrinology 1993, 133:965-971.
36. Berrodin T.J., Marks M.S., Ozato K., Linney E., Lazar M.A. Heterodimerization among thyroid hormone receptor, retinoic acid receptor, retinoid X receptor, chicken ovalbumin upstream promoter transcription factor, and an endogenous liver protein. Mol Endocrinol 1992, 6:1468-1478.
37. Leid M., Kastner P., Lyons R., Nakshatri H., Saunders M., Zacharewski T., et al. Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell 1992, 68:377-395.
38. Torrance C.J., Usala S.J., Pessin J.E., Dohm G.L. Characterization of a low affinity thyroid hormone receptor binding site within the rat GLUT4 gene promoter. Endocrinology 1997, 138:1215-1223.
39. Thamotharan M., Garg M., Oak S., Rogers L.M., Pan G., Sangiorgi F., et al. Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 2007, 292:E1270-E1279.
40. Zambrano E., Martinez-Samayoa P.M., Bautista C.J., Deas M., Guillen L., Rodriguez-Gonzalez G.L., et al. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol 2005, 566:225-236.
41. Boloker J., Gertz S.J., Simmons R.A. Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 2002, 51:1499-1506.
42. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
43. Bernstein B.E., Meissner A., Lander E.S. The mammalian epigenome. Cell 2007, 128:669-681.
44. Devaskar S.U., Raychaudhuri S. Epigenetics - a science of heritable biological adaptation. Pediatr Res 2007, 61:1R-4R.
45. Fuks F., Hurd P.J., Deplus R., Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 2003, 31:2305-2312.
46. Dolinoy D.C., Das R., Weidman J.R., Jirtle R.L. Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr Res 2007, 61:30R-37R.
47. Roh T.Y., Cuddapah S., Zhao K. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 2005, 19:542-552.
48. Roh T.Y., Ngau W.C., Cui K., Landsman D., Zhao K. High-resolution genome-wide mapping of histone modifications. Nat Biotechnol 2004, 22:1013-1016.
49. Santos-Rosa H., Caldas C. Chromatin modifier enzymes, the histone code and cancer. Eur J Cancer 2005, 41:2381-2402.
50. Soutoglou E., Talianidis I. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 2002, 295:1901-1904.
51. Schneider R., Bannister A.J., Myers F.A., Thorne A.W., Crane-Robinson C., Kouzarides T. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 2004, 6:73-77.
52. Schubeler D., MacAlpine D.M., Scalzo D., Wirbelauer C., Kooperberg C., van Leeuwen F., et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 2004, 18:1263-1271.
53. Draker R., Ng M.K., Sarcinella E., Ignatchenko V., Kislinger T., Cheung P. A combination of H2A.Z and H4 acetylation recruits Brd2 to chromatin during transcriptional activation. PLoS Genet 2012, 8:e1003047.
54. Lu J., McKinsey T.A., Nicol R.L., Olson E.N. Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci U S A 2000, 97:4070-4075.