The weight gain response to stress during adulthood is conditioned by both sex and prenatal stress exposure

Psychoneuroendocrinology

Volumn 35, Issue 3, 2010, Pages 403-413

  García Cáceres, Cristina ^a   Diz Chaves, Yolanda ^b   Lagunas, Natalia ^b   Calmarza Font, Isabel ^b   Azcoitia, Iñigo ^c   Garcia Segura, Luis M ^b   Frago, Laura M ^a   Argente, Jesús ^a   Chowen, Julie A ^a  

^a HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

^b INSTITUTO CAJAL   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Corticosterone; Food intake; Glucose; Growth; Immobilization stress; Melatonin

Indexed keywords

CORTICOSTERONE; GHRELIN; MELATONIN;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CASTRATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENVIRONMENTAL EXPOSURE; FEMALE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HORMONE BLOOD LEVEL; MALE; NONHUMAN; PRENATAL STRESS; PRIORITY JOURNAL; PUBERTY; RAT; SENSITIVITY ANALYSIS; SEX DIFFERENCE; STRESS; WEANING; WEIGHT GAIN;

AGE FACTORS; ANIMALS; BLOOD GLUCOSE; CASTRATION; CORTICOSTERONE; EATING; FEMALE; HORMONES; MALE; MELATONIN; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; SEX FACTORS; SEXUAL MATURATION; STRESS, PSYCHOLOGICAL; WEIGHT GAIN;

EID: 77649273715     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2009.08.001     Document Type: Article

References (50)

1. Balthazar C.H., Ribeiro Oliveira A., Marubayashi U., dos Reis A.M., Coimbra C.C. Chronic treatment with bromocriptine modifies metabolic adjustment in response to restraint stress in rats. Auton. Autacoid Pharmacol. 2007, 27:123-127.
2. Bartolomucci A., Cabassi A., Govoni P., Ceresini G., Cero C., Berra D., Dadomo H., Franceschini P., Dell'Omo G., Parmigiani s., Palanza P. Metaolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress. PLoS One 2009, E4331.
3. Beiko J., Lander R., Hampson E., Boon F., Cain D.P. Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat. Behav. Brain Res. 2004, 151:239-253.
4. Bosch O.J., Krómer S.A., Neumann I.D. Prenatal stress: opposite effects on anxiety and hypothalamic expression of vasopressin and corticotrophin-releasing hormone in rats selectively bred for high and low anxiety. Eur. J. Neurosci. 2006, 23:541-551.
5. Bowman R.E., Maclusky N.J., Sarmiento Y., Frankfurt M., Gordon M., Luine V.N. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses and central neurotransmitters. Endocrinology 2004, 145:3778-3787.
6. Chowen J.A., Argente J., González-Parra S., García-Segura L.M. Differential effects of the neonatal and adult sex steroid environments on the organization and activation of hypothalamic growth hormone-releasing hormone and somatostatin neurons. Endocrinology 1993, 133:2792-2802.
7. Chung S., Son G.H., Park E., Lee K.H., Geum D., Kim K. Differential adaptive responses to chronic stress of maternally stressed male mice offspring. Endocrinology 2005, 146:3202-3210.
8. Clegg D.J., Brown L.M., Woods S.C., Benoit S.C. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 2006, 55:978-987.
9. Dallman M.F., la Fleur S.E., Pecoraro N.C., Gomez F., Houshyar H., Akana S.F. Minireview: glucocorticoids, food intake, abdominal obesity, and wealthy nations in 2004. Endocrinology 2004, 145:2633-2638.
10. Dallman M., Pecoraro N., la Fleur S. Chronic stress and comfort foods: self-medication and abdominal obesity. Brain Behav. Immun. 2005, 19:275-282.
11. Detanico B.C., Piato A.L., Freitas J.J., Lhullier F.L., Hidalgo M.P., Cuamo W., Elisabetsky E. Antidepressant-like effects of melatonin in the mouse chronic mild stress model. Eur. J. Pharmacol. 2009, 607:121-125.
12. Fernandez-Twinn D.S., Ozanne S.E. Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol. Behav. 2006, 88:234-243.
13. Fiqueiredo H.F., Ulrich-Lai Y.M., Choi D.C., Herman J.P. Estrogen potentiates adrenocortical responses to stress in female rats. Am. J. Physiol. Endocrinol. Metab. 2007, 292:E1173-E1182.
14. Goel N., Bale T.L. Organizational and activational effects of testosterone on masculinization of female physiology and behavioural stress responses. Endocrinology 2008, 149:6399-6405.
15. Goncharova N.D., Oganyan T.E., Taranov A.G. Functions of the hypothalamo-hypophyseal-adrenal system in aging in female monkeys. Neurosci. Behav. Physiol. 2000, 30:717-721.
16. Harris R.B., Bowen H.M., Mitchell T.D. Leptin resistance in mice is determined by gender and duration of exposure to high-fat diet. Physiol. Behav. 2003, 78:543-555.
17. Hong J., Subbins R.E., Smith R.R., Harvey A.E., Núñez N.P. Differential susceptibility to obesity between male, female and ovariectomized female mice. Nutr. J. 2009, 17:8-11.
18. Koehl M., Darnaudéry M., Dulluc J., Van Reeth O., le Moal M., Maccari S. Prenatal stress alters circadian activityof hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both genders. J. Neurobiol. 1999, 40:302-315.
19. Landt M., Gingerich R.L., Havel P.J., Mueller W.M., Schoner B., Hale J.E., Heiman M.L. Radioimmunoassay of rat leptin: sexual dimorphism reversed from humans. Clin. Chem. 1998, 44:565-570.
20. Lesage J., Del-Favero F., Leonhardt M., Louvart H., Maccari S., Vieau D., Darnaudery M. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behavior disturbances in the aged rat. J. Endocrinol. 2004, 181:291-296.
21. Levin B.E. Metabolic imprinting: critical impact of the perinatal environment and the regulation of energy homeostasis. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2006, 361:1107-1121.
22. Lynch H.J., Deng M.H. Pineal responses to stress. J. Neural. Transm. 1986, 21(Suppl.):461-473.
23. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A.R., Cinque C., Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 2003, 27:119-127.
24. Maccari S., Morley-Fletcher S. Effects of prenatal restrain stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 2007, 32:S10-S15.
25. Mattsson C., Olsson T. Estrogens and glucocorticoid hormones in adipose tissue metabolism. Curr. Med. Chem. 2007, 14:2918-2924.
26. Mayes J.S., Watson G.H. Direct effects of sex steroid hormones on adipose tissues and obesity. Obes. Rev. 2004, 5:197-216.
27. McCarthy M.M., Schwartz J.M., Wright C.L., Dean S.L. Mechanisms mediating oestradiol modulation of the developing brain. J. Neuroendocrinol. 2008, 20:777-783.
28. Menendez-Pelaez A., Reiter R.J., Guerrero J.M., Puig-Domingo M., Howes K.A. Sexual dimorphism in N-acetyltransferase activity, hydroxyindole-O-methyltransferase activity, and melatonin content in the Harderian gland of Syrian hamsters: changes following gonadectomy. Proc. Soc. Exp. Biol. Med. 1988, 187:287-291.
29. Mueller B.R., Bale T.L. Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity. Physiol. Behav. 2006, 88:605-614.
30. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 2008, 28:9055-9065.
31. Nathanielsz P.W. Animal models that elucidate basic principles of the developmental origins of adult diseases. ILAR J. 2006, 47:73-82.
32. Pankevich D.E., Bale T.L. Stress and sex influences on food-seeking behaviors. Obesity (Silver Spring) 2008, 16:1539-1544.
33. Patchev V.K., Almeida O.F. Gender specificity in the neural regulation of the response to stress: new leads from classical paradigms. Mol. Neurobiol. 1998, 16:63-77.
34. Patchev V.K., Hayashi S., Orikasa c., Almeida O.F. Ontogeny of gender-specific responsiveness to stress and glucocorticoids in the rat and its determination by the neonatal gonadal steroid environment. Stress 1999, 3:41-54.
35. Peters A., Schweiger U., Pellerin L., Hubold C., Oltmanns K.M., Conrad M., Schultes B., Born J., Fehm H.L. The selfish brain: competition for energy resources. Neurosci. Biobehav. Rev. 2004, 28:143-180.
36. Retana-Márquez S., Bonilla-Jaime H., Vázquez-Palacios G., Domínquez-Salazar E., Martínez-García R., Valázquez-Moctezuma J. Body weight gain and diurnal differences of corticosterone changes in response to acute and chronic stress in rats. Psychoneuroendocrinology 2003, 28:207-227.
37. Reznikov A.G., Nosenko N.D., Tarasenko L.V. Prenatal stress and glucocorticoid effects on the developing gender-related brain. J. Steroid Biochem. Mol. Biol. 1999, 69:109-115.
38. Roepke T.A. Oestrogen modulates hypothalamic control of energy homeostasis through multiple mechanisms. J. Neuroendocrinol. 2009, 21:141-150.
39. Rogers N.H., Perfield J.W., Strissel K.J., Obin M.S., Greenberg A.S. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 2009, 150:2161-2168.
40. Seckl J.R. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol. Cell. Endocrinol. 2001, 185:61-71.
41. Spencer S.J., Tilbrook A. Neonatal overfeeding alters adult anxiety and stress responsiveness. Psychoneuroendocrinology 2009, 34:1133-1143.
42. Tamashiro K.L., Terrillion C.E., Hyun J., Koenig J.I., Moran T.H. Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 2009, 58:1116-1125.
43. Tobe I., Ishida Y., Tanaka M., Endoh H., Fujioka T., Nakamura S. Effects of repeated maternal stress on FOS expression in the hypothalamic paraventricular nucleus of fetal rats. Neuroscience 2005, 134:387-395.
44. Torres S.J., Nowson C.A. Relationship between stress, eating behaviour, and obesity. Nutrition 2007, 23:887-894.
45. Vallée M., Mayo W., Maccari S., Le Moal M., Simon H. Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res. 1996, 12:287-292.
46. Vickers M.H., Gluckman P.D., Conveny A.H., Hofman P.L., Cutfield W.S., Gertler A., Breier B.H., Harris M. The effect of neonatal leptin treatment on postnatal weight gain in male rats is dependent on maternal nutritional status during pregnancy. Endocrinology 2008, 129:1906-1913.
47. Ward I.L., Weisz J. Maternal stress alters plasma testosterone in fetal males. Science 1980, 207:328-329.
48. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem. Res. 2007, 32:1730-1740.
49. Yoshihara T., Yawaka Y. Repeated immobilization stress in the early postnatal period increases stress response in adult rats. Physiol. Behav. 2008, 93:322-326.
50. Zuena A.R., Mairesse J., Casolini P., Cinque C., Alemà G.S., Morley-Fletcher S., Chiodi V., Spagnoli L.G., Gradini R., Catalani A., Nicoletti F., Maccari S. Prenatal restrain stress generates two distinct behavioural and neurochemical profiles in male and female rats. PloS One 2008, 5e2170:1-13.