Decreased comfort food intake and allostatic load in adolescents carrying the A3669G variant of the glucocorticoid receptor gene

Appetite

Volumn 116, Issue , 2017, Pages 21-28

  Rodrigues, Danitsa Marcos ^a   Reis, Roberta Sena ^a   Dalle Molle, Roberta ^a   Machado, Tania Diniz ^a   Mucellini, Amanda Brondani ^a   Bortoluzzi, Andressa ^a   Toazza, Rudineia ^a   Pérez, Juliano Adams ^b   Salum, Giovanni Abrahão ^a   Agranonik, Marilyn ^c   Minuzzi, Luciano ^d   Levitan, Robert D ^g   Buchweitz, Augusto ^e   Franco, Alexandre Rosa ^e   Manfro, Gisele Gus ^a   Silveira, Patrícia Pelufo ^a,f  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c Statistics Information Center   (Brazil)

^d MCMASTER UNIVERSITY   (Canada)

^e PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^f MCGILL UNIVERSITY   (Canada)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

Comfort food; Feeding behaviour; Glucocorticoid receptor gene polymorphism; Insulin; Reward circuitry

Indexed keywords

GLUCOCORTICOID RECEPTOR; INSULIN; SUGAR;

ADOLESCENT; ADOLESCENT OBESITY; ALLELE; ALLOSTASIS; ANXIETY; ARTICLE; ASSOCIATION; BRAIN FUNCTION; COMFORT; ENERGY CONSUMPTION; FEMALE; FOLLOW UP; FOOD INTAKE; FOOD PREFERENCE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GENETIC VARIABILITY; GENOTYPE; HUMAN; IMAGE ANALYSIS; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; MAJOR CLINICAL STUDY; MALE; NUTRITIONAL ASSESSMENT; PALATABILITY; RECEPTOR SENSITIVITY; SINGLE NUCLEOTIDE POLYMORPHISM; SUGAR INTAKE; ADOLESCENT NUTRITION; BRAZIL; CALORIC INTAKE; CHILD; CHILD NUTRITION; COHORT ANALYSIS; GENETIC ASSOCIATION STUDY; GENETICS; INSULIN RESISTANCE; LONGITUDINAL STUDY; MENTAL STRESS; METABOLISM; PROSPECTIVE STUDY; PSYCHOLOGY;

ADOLESCENT; ADOLESCENT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ALLELES; ALLOSTASIS; ANXIETY; APPETITE REGULATION; BRAZIL; CHILD; CHILD NUTRITIONAL PHYSIOLOGICAL PHENOMENA; COHORT STUDIES; ENERGY INTAKE; FEMALE; FOOD PREFERENCES; GENETIC ASSOCIATION STUDIES; HUMANS; INSULIN RESISTANCE; LONGITUDINAL STUDIES; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSPECTIVE STUDIES; STRESS, PSYCHOLOGICAL;

EID: 85018789417     PISSN: 01956663     EISSN: 10958304     Source Type: Journal    
DOI: 10.1016/j.appet.2017.04.004     Document Type: Article

References (67)

1. Adam, T.C., Epel, E.S., Stress, eating and the reward system. Physiology & Behavior 91 (2007), 449–458.
2. American Psychological Association, Are teens adopting adults’ stress habits?. In. Washington, DC/USA, 2013 http://www.apa.org/news/press/releases/stress/2013/teen-stress.aspx.
3. Ashburner, J., Friston, K., Multimodal image coregistration and partitioning–a unified framework. Neuroimage 6 (1997), 209–217.
4. Ashburner, J., Friston, K.J., Unified segmentation. Neuroimage 26 (2005), 839–851.
5. Baik, J.H., Dopamine signaling in food addiction: Role of dopamine D2 receptors. BMB Reports 46 (2013), 519–526.
6. Berridge, K.C., Food reward: Brain substrates of wanting and liking. Neuroscience & Biobehavioral Reviews 20 (1996), 1–25.
7. Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., et al. The screen for Child anxiety related emotional disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry 36 (1997), 545–553.
8. Briassoulis, G., Damjanovic, S., Xekouki, P., Lefebvre, H., Stratakis, C.A., The glucocorticoid receptor and its expression in the anterior pituitary and the adrenal cortex: A source of variation in hypothalamic-pituitary-adrenal axis function; implications for pituitary and adrenal tumors. Endocrine Practice 17 (2011), 941–948.
9. Carlotti, A.P., Franco, P.B., Elias, L.L., Facincani, I., Costa, E.L., Foss, N., et al. Glucocorticoid receptors, in vitro steroid sensitivity, and cytokine secretion in idiopathic nephrotic syndrome. Kidney International 65 (2004), 403–408.
10. Charmandari, E., Kino, T., Chrousos syndrome: A seminal report, a phylogenetic enigma and the clinical implications of glucocorticoid signalling changes. European Journal of Clinical Investigation 40 (2010), 932–942.
11. Chriguer, R.S., Elias, L.L., da Silva, I.M. Jr., Vieira, J.G., Moreira, A.C., de Castro, M., Glucocorticoid sensitivity in young healthy individuals: In vitro and in vivo studies. The Journal of Clinical Endocrinology & Metabolism 90 (2005), 5978–5984.
12. Chriguer, R.S., Roselino, A.M., de Castro, M., Glucocorticoid sensitivity and proinflammatory cytokines pattern in pemphigus. Journal of Clinical Immunology 32 (2012), 786–793.
13. Dallman, M.F., Stress-induced obesity and the emotional nervous system. Trends in Endocrinology and Metabolism 21 (2010), 159–165.
14. Dallman, M.F., Pecoraro, N.C., la Fleur, S.E., Chronic stress and comfort foods: Self-medication and abdominal obesity. Brain, Behavior, and Immunity 19 (2005), 275–280.
15. De, A., Blotta, H.M., Mamoni, R.L., Louzada, P., Bertolo, M.B., Foss, N.T., et al. Effects of dexamethasone on lymphocyte proliferation and cytokine production in rheumatoid arthritis. The Journal of Rheumatology 29 (2002), 46–51.
16. Derijk, R.H., Schaaf, M.J., Turner, G., Datson, N.A., Vreugdenhil, E., Cidlowski, J., et al. A human glucocorticoid receptor gene variant that increases the stability of the glucocorticoid receptor beta-isoform mRNA is associated with rheumatoid arthritis. The Journal of Rheumatology 28 (2001), 2383–2388.
17. Epel, E., Lapidus, R., McEwen, B., Brownell, K., Stress may add bite to appetite in women: A laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology 26 (2001), 37–49.
18. Figlewicz, D.P., Benoit, S.C., Insulin, leptin, and food reward: Update 2008. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology 296 (2009), R9–R19.
19. Friston, K.J., Williams, S., Howard, R., Frackowiak, R.S., Turner, R., Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine 35 (1996), 346–355.
20. Greeno, C.G., Wing, R.R., Stress-induced eating. Psychological Bulletin 115 (1994), 444–464.
21. Hargrave, S.L., Jones, S., Davidson, T.L., The outward spiral: A vicious cycle model of obesity and cognitive dysfunction. Current Opinion in Behavioral Sciences 9 (2016), 40–46.
22. He, B., Cruz-Topete, D., Oakley, R.H., Xiao, X., Cidlowski, J.A., Human glucocorticoid receptor beta regulates gluconeogenesis and inflammation in mouse liver. Molecular and Cellular Biology 36 (2016), 714–730.
23. Henn, R.L., Fuchs, S.C., Moreira, L.B., Fuchs, F.D., Development and validation of a food frequency questionnaire (FFQ-Porto Alegre) for adolescent, adult and elderly populations from Southern Brazil. Cadernos de Saúde Pública 26 (2010), 2068–2079.
24. Hinds, T.D. Jr., Ramakrishnan, S., Cash, H.A., Stechschulte, L.A., Heinrich, G., Najjar, S.M., et al. Discovery of glucocorticoid receptor-beta in mice with a role in metabolism. Molecular Endocrinology 24 (2010), 1715–1727.
25. Hollenberg, S.M., Weinberger, C., Ong, E.S., Cerelli, G., Oro, A., Lebo, R., et al. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 318 (1985), 635–641.
26. Huizenga, N.A., Koper, J.W., De Lange, P., Pols, H.A., Stolk, R.P., Burger, H., et al. A polymorphism in the glucocorticoid receptor gene may be associated with and increased sensitivity to glucocorticoids in vivo. The Journal of Clinical Endocrinology & Metabolism 83 (1998), 144–151.
27. Huizenga, N.A., Koper, J.W., de Lange, P., Pols, H.A., Stolk, R.P., Grobbee, D.E., et al. Interperson variability but intraperson stability of baseline plasma cortisol concentrations, and its relation to feedback sensitivity of the hypothalamo-pituitary-adrenal axis to a low dose of dexamethasone in elderly individuals. The Journal of Clinical Endocrinology & Metabolism 83 (1998), 47–54.
28. Isolan, L., Salum, G.A., Osowski, A.T., Amaro, E., Manfro, G.G., Psychometric properties of the screen for Child anxiety related emotional disorders (SCARED) in brazilian children and adolescents. Journal of Anxiety Disorders 25 (2011), 741–748.
29. John, K., Marino, J.S., Sanchez, E.R., Hinds, T.D., The glucocorticoid receptor: Cause of or cure for obesity?. American Journal of Physiology. Endocrinology and Metabolism 310 (2016), E249–E257.
30. Kino, T., Manoli, I., Kelkar, S., Wang, Y., Su, Y.A., Chrousos, G.P., Glucocorticoid receptor (GR) β has intrinsic, GRα-independent transcriptional activity. Biochemical and Biophysical Research Communications 381 (2009), 671–675.
31. de Kloet, E.R., Hormones, brain and stress. Endocrine Regulations 37 (2003), 51–68.
32. Kumsta, R., Entringer, S., Koper, J.W., van Rossum, E.F., Hellhammer, D.H., Wüst, S., Sex specific associations between common glucocorticoid receptor gene variants and hypothalamus-pituitary-adrenal axis responses to psychosocial stress. Biological Psychiatry 62 (2007), 863–869.
33. Kurokawa, K., Tanahashi, T., Murata, A., Akaike, Y., Katsuura, S., Nishida, K., et al. Effects of chronic academic stress on mental state and expression of glucocorticoid receptor alpha and beta isoforms in healthy Japanese medical students. Stress 14 (2011), 431–438.
34. Lang, P., Bradley, M., Cuthbert, B., International affective picture system (IAPS): Affective ratings of pictures and instruction manual. In Technical Report A-8, 2008, University of Florida, National Institute of Mental Health. Center for the Study of Emotion and Attention, Gainesville, FL.
35. Marino, J.S., Stechschulte, L.A., Stec, D.E., Nestor-Kalinoski, A., Coleman, S., Hinds, T.D. Jr., Glucocorticoid receptor beta induces hepatic steatosis by augmenting inflammation and inhibition of the peroxisome proliferator-activated receptor (PPAR) alpha. The Journal of Biological Chemistry 291 (2016), 25776–25788.
36. Mikl, M., Marecek, R., Hlustík, P., Pavlicová, M., Drastich, A., Chlebus, P., et al. Effects of spatial smoothing on fMRI group inferences. Magnetic Resonance Imaging 26 (2008), 490–503.
37. Moraitis, A.G., Block, T., Nguyen, D., Belanoff, J.K., The role of glucocorticoid receptors in metabolic syndrome and psychiatric illness. The Journal of Steroid Biochemistry and Molecular Biology 165 (2017), 114–120.
38. Morley, J.E., Levine, A.S., Rowland, N.E., Minireview. Stress induced eating. Life Sciences 32 (1983), 2169–2182.
39. Muller, M.B., Zimmermann, S., Sillaber, I., Hagemeyer, T.P., Deussing, J.M., Timpl, P., et al. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nature Neuroscience 6 (2003), 1100–1107.
40. Ng, M., Fleming, T., Robinson, M., Thomson, B., Graetz, N., Margono, C., et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: A systematic analysis for the global burden of disease study 2013. Lancet 384 (2014), 766–781.
41. Oakley, R.H., Sar, M., Cidlowski, J.A., The human glucocorticoid receptor beta isoform. Expression, biochemical properties, and putative function. The Journal of Biological Chemistry 271 (1996), 9550–9559.
42. Oswald, L.M., Wong, D.F., McCaul, M., Zhou, Y., Kuwabara, H., Choi, L., et al. Relationships among ventral striatal dopamine release, cortisol secretion, and subjective responses to amphetamine. Neuropsychopharmacology 30 (2005), 821–832.
43. Page, K.A., Seo, D., Belfort-DeAguiar, R., Lacadie, C., Dzuira, J., Naik, S., et al. Circulating glucose levels modulate neural control of desire for high-calorie foods in humans. The Journal of Clinical Investigation 121 (2011), 4161–4169.
44. Panarelli, M., Holloway, C.D., Fraser, R., Connell, J.M., Ingram, M.C., Anderson, N.H., et al. Glucocorticoid receptor polymorphism, skin vasoconstriction, and other metabolic intermediate phenotypes in normal human subjects. The Journal of Clinical Endocrinology & Metabolism 83 (1998), 1846–1852.
45. Pecoraro, N., Dallman, M.F., Warne, J.P., Ginsberg, A.B., Laugero, K.D., la Fleur, S.E., et al. From malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants. Progress in Neurobiology 79 (2006), 247–340.
46. Pecoraro, N., Reyes, F., Gomez, F., Bhargava, A., Dallman, M.F., Chronic stress promotes palatable feeding, which reduces signs of stress: Feedforward and feedback effects of chronic stress. Endocrinology 145 (2004), 3754–3762.
47. Ramamoorthy, S., Cidlowski, J.A., Corticosteroids: Mechanisms of action in Health and disease. Rheumatic Disease Clinics of North America 42 (2016), 15–31 vii.
48. van Rossum, E.F., Koper, J.W., Huizenga, N.A., Uitterlinden, A.G., Janssen, J.A., Brinkmann, A.O., et al. A polymorphism in the glucocorticoid receptor gene, which decreases sensitivity to glucocorticoids in vivo, is associated with low insulin and cholesterol levels. Diabetes 51 (2002), 3128–3134.
49. Rovaris, D.L., Mota, N.R., de Azeredo, L.A., Cupertino, R.B., Bertuzzi, G.P., Polina, E.R., et al. MR and GR functional SNPs may modulate tobacco smoking susceptibility. Journal of Neural Transmission 120 (2013), 1499–1505.
50. Salum, G.A., Isolan, L.R., Bosa, V.L., Tocchetto, A.G., Teche, S.P., Schuch, I., et al. The multidimensional evaluation and treatment of anxiety in children and adolescents: Rationale, design, methods and preliminary findings. Revista Brasileira de Psiquiatria 33 (2011), 181–195.
51. Schaaf, M.J., Cidlowski, J.A., AUUUA motifs in the 3'UTR of human glucocorticoid receptor alpha and beta mRNA destabilize mRNA and decrease receptor protein expression. Steroids 67 (2002), 627–636.
52. Sinha, R., Chronic stress, drug use, and vulnerability to addiction. Annals of the New York Academy of Sciences 1141 (2008), 105–130.
53. Sladky, R., Friston, K.J., Trostl, J., Cunnington, R., Moser, E., Windischberger, C., Slice-timing effects and their correction in functional MRI. Neuroimage 58 (2011), 588–594.
54. Spijker, A.T., van Rossum, E.F., Hoencamp, E., DeRijk, R.H., Haffmans, J., Blom, M., et al. Functional polymorphism of the glucocorticoid receptor gene associates with mania and hypomania in bipolar disorder. Bipolar Disorders 11 (2009), 95–101.
55. Stechschulte, L.A., Wuescher, L., Marino, J.S., Hill, J.W., Eng, C., Hinds, T.D., Glucocorticoid receptor β stimulates Akt1 growth pathway by attenuation of PTEN*. The Journal of Biological Chemistry 289 (2014), 17885–17894.
56. Stratakis, C.A., Karl, M., Schulte, H.M., Chrousos, G.P., Glucocorticosteroid resistance in humans. Elucidation of the molecular mechanisms and implications for pathophysiology. Annals of the New York Academy of Sciences 746 (1994), 366–374 362-374; discussion.
57. van Strien, T., Roelofs, K., de Weerth, C., Cortisol reactivity and distress-induced emotional eating. Psychoneuroendocrinology 38 (2013), 677–684.
58. Syed, A.A., Irving, J.A., Redfern, C.P., Hall, A.G., Unwin, N.C., White, M., et al. Association of glucocorticoid receptor polymorphism A3669G in exon 9beta with reduced central adiposity in women. Obesity (Silver Spring) 14 (2006), 759–764.
59. Szczepankiewicz, A., Leszczynska-Rodziewicz, A., Pawlak, J., Rajewska-Rager, A., Dmitrzak-Weglarz, M., Wilkosc, M., et al. Glucocorticoid receptor polymorphism is associated with major depression and predominance of depression in the course of bipolar disorder. Journal of Affective Disorders 134 (2011), 138–144.
60. Trementino, L., Appolloni, G., Concettoni, C., Cardinaletti, M., Boscaro, M., Arnaldi, G., Association of glucocorticoid receptor polymorphism A3669G with decreased risk of developing diabetes in patients with Cushing's syndrome. European Journal of Endocrinology 166 (2012), 35–42.
61. Ulrich-Lai, Y.M., Self-medication with sucrose. Current Opinion in Behavioral Sciences 9 (2016), 78–83.
62. United States Department of Agriculture (USDA). (Date Accessed 2014). Standard reference, realese 26. In National Agricultural Library. https://ndb.nal.usda.gov/ndb/search/list.
63. Wand, G.S., Oswald, L.M., McCaul, M.E., Wong, D.F., Johnson, E., Zhou, Y., et al. Association of amphetamine-induced striatal dopamine release and cortisol responses to psychological stress. Neuropsychopharmacology 32 (2007), 2310–2320.
64. Warne, J.P., Shaping the stress response: Interplay of palatable food choices, glucocorticoids, insulin and abdominal obesity. Molecular and Cellular Endocrinology 300 (2009), 137–146.
65. World Health Organization, Global Health observatory data: Overweight and obesity. 2015 http://www.who.int/gho/ncd/risk_factors/overweight/en/.
66. Wust, S., Van Rossum, E.F., Federenko, I.S., Koper, J.W., Kumsta, R., Hellhammer, D.H., Common polymorphisms in the glucocorticoid receptor gene are associated with adrenocortical responses to psychosocial stress. The Journal of Clinical Endocrinology & Metabolism 89 (2004), 565–573.
67. Zhou, J., Cidlowski, J.A., The human glucocorticoid receptor: One gene, multiple proteins and diverse responses. Steroids 70 (2005), 407–417.