Thyroid hormone receptor alpha gene variants increase the risk of developing obesity and show gene-diet interactions

International Journal of Obesity

Volumn 37, Issue 11, 2013, Pages 1499-1505

  Fernandez Real J M ^a,b   Corella, D ^b,c   Goumidi, L ^d   Mercader, J M ^e   Valdes S ^f,g,h   Rojo Martinez G ^f,g   Ortega, F ^a,b   Martinez Larrad, M T ⁱ   Gomez Zumaquero J M ^f,g   Salas Salvado J ^b,j   Martinez Gonzalez M A ^k   Covas, M I ^b,l   Botas, P ^f,g   Delgado, E ^f,g   Cottel, D ^d   Ferrieres, J ^m   Amouyel, P ^d   Ricart, W ^a,b   Ros, E ^b,n   Meirhaeghe, A ^d   Serrano Rios, M ⁱ   Soriguer, F ^d   Estruch, R ^b,o   more..

^a GIRONA BIOMEDICAL RESEARCH INSTITUTE IDIBGI   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

^d UNIV LILLE   (France)

^e BARCELONA SUPERCOMPUTING CENTER   (Spain)

^f HOSPITAL REGIONAL UNIVERSITARIO DE MÁLAGA   (Spain)

^g INSTITUTO DE SALUD CARLOS III   (Spain)

^h HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

ⁱ HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^j UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^k UNIVERSITY OF NAVARRA   (Spain)

^l HOSPITAL DEL MAR   (Spain)

^m UNIVERSITÉ PAUL SABATIER   (France)

ⁿ HOSPITAL CLÍNIC   (Spain)

^o UNIVERSITY OF BARCELONA   (Spain)

more..

Author keywords

genetics; polymorphisms.; Thyroid hormone receptors

Indexed keywords

LEVOTHYROXINE; SATURATED FATTY ACID; THYROID HORMONE RECEPTOR ALPHA; TRIACYLGLYCEROL;

ADULT; AGED; ALLELE; ARTICLE; BODY MASS; CALORIC INTAKE; CARDIOVASCULAR RISK; COHORT ANALYSIS; CONTROLLED STUDY; DIET RESTRICTION; DIETARY INTAKE; DRUG DOSE INCREASE; DRUG DOSE REDUCTION; DRUG OVERDOSE; FAT INTAKE; FEMALE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOTE; HOMOZYGOTE; HORMONE RESISTANCE; HUMAN; HYPERTHYROIDISM; HYPOTHYROIDISM; MAJOR CLINICAL STUDY; MALE; OBESITY; PHYSICAL ACTIVITY; POPULATION; PRIORITY JOURNAL; RECEPTOR GENE; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; THYROID HORMONE RECEPTOR ALPHA GENE;

ADULT; BODY MASS INDEX; CARDIOVASCULAR DISEASES; CROSS-SECTIONAL STUDIES; DIETARY FATS; ENERGY INTAKE; FEMALE; FRANCE; GENETIC PREDISPOSITION TO DISEASE; HETEROZYGOTE; HUMANS; HYPOTHYROIDISM; INSULIN RESISTANCE; MALE; MIDDLE AGED; OBESITY; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK FACTORS; SPAIN; THYROID HORMONE RECEPTORS ALPHA;

EID: 84887848124     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2013.11     Document Type: Article

References (48)

1. Hu FB. Obesity epidemiology. Oxford Univ Press: New York, 2008.
2. Berrington de Gonzalez A, Hartge P, Cerhan JR, Flint AJ, Hannan L, MacInnis RJ et al. Body-mass index and mortality among 1.46 million white adults. N Engl J Med 2010; 363: 2211-2219.
3. McCarthy M. Genomics, type 2 diabetes, and obesity. N Engl J Med 2010; 363: 2339-2350.
4. O'Rahilly S. Human genetics illuminates the paths to metabolic disease. Nature 2009; 462: 307-314.
5. Maes HH, Neale MC, Eaves LJ. Genetic and environmental factors in relative body weight and human adiposity. Behav Genet 1997; 27: 325-351.
6. Speliotes EK, Willer CJ, Berndt SI, Speliotes EK, Willer CJ, Berndt SI et al. Association analyses of 249, 796 individuals reveal 18 new loci associated with body mass index. Nat Genet 2010; 42: 937-948.
7. Kokkoris P, Pi-Sunyer FX. Obesity and endocrine disease. Endocrinol Metab Clin North Am 2003; 32: 895-914.
8. Reinehr T. Obesity and thyroid function. Mol Cell Endocrinol 2010; 316: 165-171.
9. Biondi B. Thyroid and obesity: an intriguing relationship. J Clin Endocrinol Metab 2010; 95: 3614-3617.
10. Knudsen N, Laurberg P, Rasmussen LB, Bülow I, Perrild H, Ovesen L et al. Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population. J Clin Endocrinol Metab 2005; 90: 4019-4024.
11. Fox CS, Pencina MJ, D'Agostino RB, Murabito JM, Seely EW, Pearce EN et al. Relations of thyroid function to body weight: cross-sectional and longitudinal observations in a community-based sample. Arch Intern Med 2008; 168: 587-592.
12. Manji N, Boelaert K, Sheppard MC, Holder RL, Gough SC, Franklyn JA. Lack of association between serum TSH or free T4 and body mass index in euthyroid subjects. Clin Endocrinol 2006; 64: 125-128.
13. Jiang W, Miyamoto T, Kakizawa T, Sakuma T, Nishio S, Takeda T et al. Expression of thyroid hormone receptor alpha in 3T3-L1 adipocytes; triiodothyronine increases the expression of lipogenic enzyme and triglyceride accumulation. J Endocrinol 2004; 182: 295-302.
14. Ying H, Araki O, Furuya F, Kato Y, Cheng SY. Impaired adipogenesis caused by a mutated thyroid hormone alpha1 receptor. Mol Cell Biol 2007; 27: 2359-2371.
15. Alevizaki M, Saltiki K, Voidonikola P, Mantzou E, Papamichael C, Stamatelopoulos K. Free thyroxine is an independent predictor of subcutaneous fat in euthyroid individuals. Eur J Endocrinol 2009; 161: 459-465.
16. Forrest D, Sjoberg M, Vennstrom B. Contrasting developmental and tissue-specific expression of alpha and beta thyroid hormone receptor genes. EMBO J 1990; 9: 1519-1528.
17. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev 2005; 26: 704-728.
18. Wikström L, Johansson C, Saltó C, Barlow C, Campos Barros A, Baas F et al. Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. EMBO J 1998; 17: 455-461.
19. Cheng SY, Leonard JL, Davis PJ. Molecular aspects of thyroid hormone actions. Endocr Rev 2010; 31: 139-170.
20. Reyne Y, Nougues J, Cambon B, Viguerie-Bascands N, Casteilla L. Expression of c-erbA alpha, c-erbA beta and Rev-erbA alpha mRNA during the conversion of brown adipose tissue into white adipose tissue. Mol Cell Endocrinol 1996; 116: 59-65.
21. Weiss RE, Murata Y, Cua K, Hayashi Y, Seo H, Refetoff S. Thyroid hormone action on liver, heart, and energy expenditure in thyroid hormone receptor beta-deficient mice. Endocrinology 1998; 139: 4945-4952.
22. Lazar MA. Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 1993; 14: 184-193.
23. Lazar MA, Chin WW. Nuclear thyroid hormone receptors. J Clin Invest 1990; 86: 1777-1782.
24. Burman KD, Latham KR, Djuh YY, Smallridge RC, Tseng YC, Lukes YG et al. Solu-bilized nuclear thyroid hormone receptors in circulating human mononuclear cells. J Clin Endocrinol Metab 1980; 51: 106-116.
25. Reinehr T, Andler W. Thyroid hormones before and after weight loss in obesity. Arch Dis Child 2002; 87: 320-323.
26. Reinehr T, de Sousa G, Andler W. Hyperthyrotropinemia in obese children is reversible afterweight loss and is not related to lipids. J Clin Endocrinol Metab 2006; 91: 3088-3091.
27. Valdés S, Botas P, Delgado E, Alvarez F, Cadórniga FD. Population-based incidence of type 2 diabetes in northern Spain: the Asturias Study. Diabetes Care 2007; 30: 2258-2263.
28. Moreno-Navarrete JM, Ortega FJ, Bassols J, Castro A, Ricart W, Fernández-Real JM. Association of circulating lactoferrin concentration and 2 nonsynonymous LTF gene polymorphisms with dyslipidemia in men depends on glucose-tolerance status. Clin Chem 2008; 54: 301-309.
29. Martinez-Larrad MT, Fernandez-Perez C, Gonzalez-Sanchez JL, Gonzalez-Sanchez JL, López A, Fernández-Alvarez J et al. Prevalence of the metabolic syndrome (ATP-III criteria). Population-based study of rural and urban areas in the Spanish province of Segovia. Med Clin (Barc) 2005; 125: 481-486.
30. Soriguer F, Rojo-Martinez G, Almaraz MC, Esteva I, Ruiz de Adana MS, Morcillo S et al. Incidence of type 2 diabetes in southern Spain (Pizarra study). Eur J Clin Invest 2008; 38: 126-133.
31. The World Health Organization Monica Project. Ecological analysis of the association between mortality and major risk factors of cardiovascular disease. Int J Epidemiol 1994; 23: 505-516.
32. Estruch R, Mart́inez-González MA, Corella D, Salas-Salvadó J, Ruiz-Gutiérrez V, Covas MI et al. Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 2006; 145: 1-11.
33. Gonzalez JR, Armengol L, Sole X, Guinó E, Mercader JM, Estivill X et al. SNPassoc: an R package to perform whole genome association studies. Bioinformatics 2007; 23: 644-645.
34. Balding DJ. A tutorial on statistical methods for population association studies. Nat Rev Genet 2006; 7: 781-791.
35. Hastings ML, Wilson CM, Munroe SH. A purine-rich intronic element enhances alternative splicing of thyroid hormone receptor mRNA. RNA 2001; 7: 859-874.
36. Liu YY, Schultz JJ, Brent GA. A thyroid hormone receptor gene mutation (P398H) is associated with visceral adiposity and impaired catecholamine- stimulated lipo-lysis in mice. J Biol Chem 2003; 278: 38913-38920.
37. Sjogren M, Alkemade A, Mittag J, Nordström K, Katz A, Rozell B et al. Hyperme-tabolism in mice caused by the central action of an unliganded thyroid hormone receptor a1. EMBO J 2007; 26: 4535-4545.
38. Pelletier P, Gauthier K, Sideleva O, Samarut J, Silva JE. Mice lacking the thyroid hormone receptor-alpha gene spend more energy in thermogenesis, burn more fat, and are less sensitive to high-fat diet-induced obesity. Endocrinology 2008; 149: 6471-6486.
39. Dhillon H, Zigman JM, Ye C, Lee CE, McGovern RA, Tang V et al. Leptin directly activatesSF-1 neurons in the VMH and this action by leptin is required for normal body weight homeostasis. Neuron 2006; 49: 191-203.
40. Decherf S, Seugnet I, Kouidhi S, Lopez-Juarez A, Clerget-Froidevaux MS, Demeneix BA. Thyroid hormone exerts negative feedback on hypothalamic type 4 mela-nocortin receptor expression. Proc Natl Acad Sci USA 2010; 107: 4471-4476.
41. Coppola A, Liu ZW, Andrews ZB, Paradis E, Roy MC, Friedman JM et al. A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab 2007; 5: 21-33.
42. Villicev CM, Freitas FR, Aoki MS, Taffarel C, Scanlan TS, Moriscot AS et al. Thyroid hormone receptor beta-specific agonist GC-1 increases energy expenditure and prevents fat mass accumulation in rats. J Endocrinol 2007; 193: 21-29.
43. Mitchell CS, Savage DB, Dufour S, Schoenmakers N, Murgatroyd P, Befroy D et al. Resistance to thyroid hormone is associated with raised energy expenditure, muscle mitochondrial uncoupling, and hyperphagia. J Clin Invest 2010; 120: 1345-1354.
44. Suzuki T, Mochizuki K, Goda T. Localized expression of genes related to carbohydrate and lipid absorption along the crypt-villus axis of rat jejunum. Biochim Biophys Acta 2009; 1790: 1624-1635.
45. Mochizuki K, Yagi E, Sakaguchi N, Mochizuki H, Takabe S, Kuranuki S et al. The critical period for thyroid hormone responsiveness through thyroid hormone receptor isoform alpha in the postnatal small intestine. Biochim Biophys Acta 2007; 1770: 609-616.
46. Ladenson PW, Kristensen JD, Ridgway EC, Olsson AG, Carlsson B, Klein I et al. Use of the thyroid hormone analogue eprotirome in statin-treated dyslipidemia. N Engl J Med 2010; 362: 906-916.
47. Pearce EN. Hypothyroidism and dyslipidemia: modern concepts and approaches. Curr Cardiol Rep 2004; 6: 451-456.
48. Ortega FJ, Moreno-Navarrete JM, Ribas V, Esteve E, Rodriguez-Hermosa JI, Ruiz B et al. Subcutaneous fat shows higher thyroid hormone receptor-alpha1 gene expression than omental fat. Obesity (Silver Spring) 2009; 17: 2134-2141.