Maternal high-fat diet alters anxiety behavior and glucocorticoid signaling in adolescent offspring

Neuroscience

Volumn 272, Issue , 2014, Pages 92-101

  Sasaki, A ^a   de Vega, W ^a   Sivanathan, S ^a   St Cyr, S ^a   McGowan, P ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anxiety behavior; Gene expression programming; Glucocorticoid receptor; Inflammatory; Maternal; Obesity

Indexed keywords

CORTICOSTEROID RECEPTOR; GLUCOCORTICOID; CORTICOSTERONE; GLUCOCORTICOID RECEPTOR;

ADOLESCENT; ADULT; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BEHAVIOR CHANGE; BLOOD LEVEL; BODY WEIGHT; BRAIN REGION; CONTROLLED STUDY; DISEASE ASSOCIATION; ELEVATED PLUS MAZE TEST; EXPERIMENTAL TEST; FEMALE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; HIPPOCAMPUS; INFLAMMATORY GENE; LIGHT DARK TRANSITION TEST; LIPID DIET; MATERNAL OBESITY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; TASK PERFORMANCE; ADVERSE EFFECTS; AGING; ANIMAL; ANXIETY; DRUG EFFECTS; ETIOLOGY; LONG EVANS RAT; MALE; METABOLISM; OBESITY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

AGING; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CORTICOSTERONE; DIET, HIGH-FAT; FEMALE; GLUCOCORTICOIDS; HIPPOCAMPUS; MALE; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS, LONG-EVANS; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION;

EID: 84900866155     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.04.012     Document Type: Article

References (56)

1. Almeida S.S., Tonkiss J., Galler J.R. Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav 1996, 60:675-680.
2. Arborelius L., Owens M.J., Plotsky P.M., Nemeroff C.B. The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 1999, 160:1-12.
3. Bersamin A., Luick B.R., King I.B., Stern J.S., Zidenberg-Cherr S. Westernizing diets influence fat intake, red blood cell fatty acid composition, and health in remote Alaskan Native communities in the center for Alaska Native health study. J Am Diet Assoc 2008, 108:266-273.
4. Bilbo S.D., Tsang V. Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 2010, 24:2104-2115.
5. Boksa P. Animal models of obstetric complications in relation to schizophrenia. Brain Res Rev 2004, 45:1-17.
6. Boney C.M., Verma A., Tucker R., Vohr B.R. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005, 115:e290-e296.
7. Bostic J.Q., Rubin D.H., Prince J., Schlozman S. Treatment of depression in children and adolescents. J Psychiatr Pract 2005, 11:141-154.
8. Brunton P.J. Resetting the dynamic range of hypothalamic-pituitary-adrenal axis stress responses through pregnancy. J Neuroendocrinol 2010, 22:1198-1213.
9. Cabanes A., de Assis S., Gustafsson J.A., Hilakivi-Clarke L. Maternal high n-6 polyunsaturated fatty acid intake during pregnancy increases voluntary alcohol intake and hypothalamic estrogen receptor alpha and beta levels among female offspring. Dev Neurosci 2000, 22:488-493.
10. Catalano P.M. Management of obesity in pregnancy. Obstet Gynecol 2007, 109:419-433.
11. Colorado R.A., Shumake J., Conejo N.M., Gonzalez-Pardo H., Gonzalez-Lima F. Effects of maternal separation, early handling, and standard facility rearing on orienting and impulsive behavior of adolescent rats. Behav Process 2006, 71:51-58.
12. De Souza C.T., Araujo E.P., Bordin S., Ashimine R., Zollner R.L., Boschero A.C., Saad M.J., Velloso L.A. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005, 146:4192-4199.
13. Desai R.A., Manley M., Desai M.M., Potenza M.N. Gender differences in the association between body mass index and psychopathology. CNS Spectr 2009, 14:372-383.
14. Dunn G.A., Bale T.L. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 2009, 150:4999-5009.
15. El-Haschimi K., Pierroz D.D., Hileman S.M., Bjorbaek C., Flier J.S. Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Investig 2000, 105:1827-1832.
16. Godfrey K.M., Gluckman P.D., Hanson M.A. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab 2010, 21:199-205.
17. Groeneweg F.L., Karst H., de Kloet E.R., Joels M. Rapid non-genomic effects of corticosteroids and their role in the central stress response. J Endocrinol 2011, 209:153-167.
18. Hilakivi-Clarke L., Cho E., Raygada M., Onojafe I., Clarke R., Lippman M.E. Early life affects the risk of developing breast cancer. Ann N Y Acad Sci 1995, 768:327-330.
19. Jacobson-Pick S., Richter-Levin G. Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav Brain Res 2010, 214:268-276.
20. Jacobson-Pick S., Audet M.-C., Nathoo N., Anisman H. Stressor experiences during the juvenile period increase stressor responsivity in adulthood: Transmission of stressor experiences. Behav Brain Res 2011, 216:365-374.
21. Kahn S.E., Hull R.L., Utzschneider K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006, 444:840-846.
22. Legendre A., Harris R.B. Exaggerated response to mild stress in rats fed high-fat diet. Am J Physiol Regul Integr Comp Physiol 2006, 291:R1288-R1294.
23. Llaneza D.C., Frye C.A. Progestogens and estrogen influence impulsive burying and avoidant freezing behavior of naturally cycling and ovariectomized rats. Pharmacol Biochem Behav 2009, 93:337-342.
24. Loram L.C., Sholar P.W., Taylor F.R., Wiesler J.L., Babb J.A., Strand K.A., Berkelhammer D., Day H.E., Maier S.F., Watkins L.R. Sex and estradiol influence glial pro-inflammatory responses to lipopolysaccharide in rats. Psychoneuroendocrinology 2012, 37:1688-1699.
25. Marx J. Unraveling the causes of diabetes. Science 2002, 296:686-689.
26. McCormick C.M., Green M.R. From the stressed adolescent to the anxious and depressed adult: investigations in rodent models. Neuroscience 2013, 249:242-257.
27. McCormick C.M., Smith C., Mathews I.Z. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 2008, 187:228-238.
28. McGowan P.O., Meaney M.J., Szyf M. Diet and the epigenetic (re)programming of phenotypic differences in behavior. Brain Res 2008, 1237:12-24.
29. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001, 24:1161-1192.
30. Munhoz C.D., Sorrells S.F., Caso J.R., Scavone C., Sapolsky R.M. Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner. J Neurosci 2010, 30:13690-13698.
31. Paxinos G., Watson C.R. The rat brain in stereotaxic coordinates 1997, Academic Press, San Diego.
32. Peleg-Raibstein D., Luca E., Wolfrum C. Maternal high-fat diet in mice programs emotional behavior in adulthood. Behav Brain Res 2012, 233:398-404.
33. Pine D.S., Cohen P., Gurley D., Brook J., Ma Y. The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Arch Gen Psychiatry 1998, 55:56-64.
34. Proulx K., Clavel S., Nault G., Richard D., Walker C.D. High neonatal leptin exposure enhances brain GR expression and feedback efficacy on the adrenocortical axis of developing rats. Endocrinology 2001, 142:4607-4616.
35. Purcell R.H., Sun B., Pass L.L., Power M.L., Moran T.H., Tamashiro K.L. Maternal stress and high-fat diet effect on maternal behavior, milk composition, and pup ingestive behavior. Physiol Behav 2011, 104:474-479.
36. Pyter L.M., Kelly S.D., Harrell C.S., Neigh G.N. Sex differences in the effects of adolescent stress on adult brain inflammatory markers in rats. Brain Behav Immun 2013, 30:88-94.
37. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 2002, 163:362-380.
38. Rofey D.L., Kolko R.P., Iosif A.M., Silk J.S., Bost J.E., Feng W., Szigethy E.M., Noll R.B., Ryan N.D., Dahl R.E. A longitudinal study of childhood depression and anxiety in relation to weight gain. Child Psychiatry Hum Dev 2009, 40:517-526.
39. Sasaki A., de Vega W.C., St-Cyr S., Pan P., McGowan P.O. Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience 2013, 240:1-12.
40. Smoak K.A., Cidlowski J.A. Mechanisms of glucocorticoid receptor signaling during inflammation. Mech Ageing Dev 2004, 125:697-706.
41. Sorrells S.F., Caso J.R., Munhoz C.D., Sapolsky R.M. The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 2009, 64:33-39.
42. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24:417-463.
43. Stein M.B., Fuetsch M., Muller N., Hofler M., Lieb R., Wittchen H.-U. Social anxiety disorder and the risk of depression: a prospective community study of adolescents and young adults. Arch Gen Psychiatry 2001, 58:251-256.
44. Sullivan E.L., Grayson B., Takahashi D., Robertson N., Maier A., Bethea C.L., Smith M.S., Coleman K., Grove K.L. Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring. J Neurosci 2010, 30:3826-3830.
45. 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.
46. Tannenbaum B.M., Brindley D.N., Tannenbaum G.S., Dallman M.F., McArthur M.D., Meaney M.J. High-fat feeding alters both basal and stress-induced hypothalamic-pituitary-adrenal activity in the rat. Am J Physiol 1997, 273:E1168-E1177.
47. Tirelli E., Laviola G., Adriani W. Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 2003, 27:163-178.
48. Van Gaal L.F., Mertens I.L., De Block C.E. Mechanisms linking obesity with cardiovascular disease. Nature 2006, 444:875-880.
49. Vazquez D.M. Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 1998, 23:663-700.
50. Walker C.D. Maternal touch and feed as critical regulators of behavioral and stress responses in the offspring. Dev Psychobiol 2010, 52:638-650.
51. Walker A.K., Nakamura T., Byrne R.J., Naicker S., Tynan R.J., Hunter M., Hodgson D.M. Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology 2009, 34:1515-1525.
52. Weiss R., Dziura J., Burgert T.S., Tamborlane W.V., Taksali S.E., Yeckel C.W., Allen K., Lopes M., Savoye M., Morrison J., Sherwin R.S., Caprio S. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 2004, 350:2362-2374.
53. Welberg L.A., Seckl J.R. Prenatal stress, glucocorticoids and the programming of the brain. J Endocrinol 2001, 13:113-128.
54. Whitaker R.C. Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics 2004, 114:e29-e36.
55. White C.L., Pistell P.J., Purpera M.N., Gupta S., Fernandez-Kim S.O., Hise T.L., Keller J.N., Ingram D.K., Morrison C.D., Bruce-Keller A.J. Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol Dis 2009, 35:3-13.
56. Zeidan M.A., Igoe S.A., Linnman C., Vitalo A., Levine J.B., Klibanski A., Goldstein J.M., Milad M.R. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol Psychiatry 2011, 70:920-927.