Maternal dietary fat determines metabolic profile and the magnitude of endocannabinoid inhibition of the stress response in neonatal rat offspring

Endocrinology

Volumn 151, Issue 4, 2010, Pages 1685-1694

  D'Asti, Esterina ^a   Long, Hong ^a   Tremblay Mercier, Jennifer ^b   Grajzer, Magdalena ^c   Cunnane, Stephen C ^b   Di Marzo, Vincenzo ^c   Walker, Claire Dominique ^a  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; ARACHIDONIC ACID; CORTICOSTERONE; ENDOCANNABINOID; FATTY ACID; INSULIN; LEPTIN; PHOSPHOLIPID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BREAST MILK; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; CORTICOTROPIN RELEASE; FAT INTAKE; FEMALE; GESTATIONAL AGE; HIPPOCAMPUS; HYPOTHALAMUS; INSULIN BLOOD LEVEL; LACTATION; LIPID DIET; MATERNAL NUTRITION; METABOLIC PARAMETERS; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; STRESS;

ADIPOSE TISSUE; ADRENOCORTICOTROPIC HORMONE; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, SUCKLING; BODY WEIGHT; BRAIN; BRAIN CHEMISTRY; CORTICOSTERONE; DIETARY FATS; ENDOCANNABINOIDS; FATTY ACIDS; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN; LACTATION; LEPTIN; PIPERIDINES; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PYRAZOLES; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; REGRESSION ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS, PHYSIOLOGICAL;

EID: 77950228903     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-1092     Document Type: Article

References (61)

1. Vieau D, Sebaai N, Léonhardt M, Dutriez-Casteloot I, Molendi-Coste O, Laborie C, Breton C, Deloof S, Lesage J 2007 HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 32:S16-S20
2. Walker CD 2005 Nutritional aspects modulating brain development and the responses to stress in early neonatal life. Prog Neuropsychopharmacol Biol Psychiatry 29:1249-1263
3. Amusquivar E, Rupérez FJ, Barbas C, Herrera E 2000 Low arachidonic acid rather than α-tocopherol is responsible for the delayed postnatal development in offspring of rats fed fish oil instead of olive oil during pregnancy and lactation. J Nutr 130:2855-2865
4. Innis SM 2007 Human milk: maternal dietary lipids and infant development. Proc Nutr Soc 66:397-404
5. Schiefermeier M, Yavin E 2002 n-3 Deficient and docosahexaenoic acid-enriched diets during critical periods of the developing prenatal rat brain. J Lipid Res 43:124-131
6. Tam O, Innis SM 2006 Dietary polyunsaturated fatty acids in gestation alter fetal cortical phospholipids, fatty acids and phosphatidylserine synthesis. Dev Neurosci 28:222-229
7. Innis SM 2003 Perinatal biochemistry and physiology of long-chain polyunsaturated fatty acids. J Pediat 143(4 Suppl): S1-S8
8. Yavin E, Brand A, Green P 2002 Docosahexaenoic acid abundance in the brain: a biodevice to combat oxidative stress. Nutr Neurosci 5:149-157
9. Innis SM, Friesen RW 2008 Essential n-3 fatty acids in pregnant women and early visual acuity maturation in term infants. Am J Clin Nutr 87:548-557
10. Uauy R, Hoffman DR, Peirano P, Birch DG, Birch EE 2001 Essential fatty acids in visual and brain development. Lipids 36:885-895
11. Chalon S, Vancassel S, Zimmer L, Guilloteau D, Durand G 2001 Polyunsaturated fatty acids and cerebral function: focus on monoaminergic neurotransmission. Lipids 36:937-944
12. Kodas E, Galineau L, Bodard S, Vancassel S, Guilloteau D, Besnard JC, Chalon S 2004 Serotoninergic neurotransmission is affected by n-3 polyunsaturated fatty acids in the rat. J Neurochem 89:695-702
13. Green P, Yavin E 1998 Mechanisms of docosahexaenoic acid accretion in the fetal brain. J Neurosci Res 52:129-136
14. Di Marzo V, Melck D, Bisogno T, De Petrocellis L 1998 Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci 21:521-528
15. Petrosino S, Ligresti A, Di Marzo V 2009 Endocannabinoid chemical biology: a tool for the development of novel therapies. Curr Opin Chem Biol 13:309-320
16. Watanabe S, Doshi M, Hamazaki T 2003 n-3 Polyunsaturated fatty acid (PUFA) deficiency elevates and n-3 PUFA enrichment reduces brain 2-arachidonoylglycerol level in mice. Prostaglandins Leukot Essent Fatty Acids 69:51-59
17. Berger A, Crozier G, Bisogno T, Cavaliere P, Innis S, Di Marzo V 2001 Anandamide and diet: inclusion of dietary arachidonate and docosahexaenoate leads to increased brain levels of the corresponding N-acylethanolamines in piglets. Proc Natl Acad Sci USA 98: 6402-6406
18. Di Marzo V 2008 Targeting the endocannabinoid system: to enhance or reduce? Nat Rev Drug Discov 7:438-455
19. Fernández-Ruiz J, Berrendero F, Hernández ML, Ramos JA 2000 The endogenous cannabinoid system and brain development. Trends Neurosci 23:14-20
20. Di S, Malcher-Lopes R, Halmos KC, Tasker JG 2003 Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 23:4850-4857
21. Malcher-Lopes R, Di S, Marcheselli VS, Weng FJ, Stuart CT, Bazan NG, Tasker JG 2006 Opposing crosstalk between leptin and glucocorticoids rapidly modulates synaptic excitation via endocannabinoid release. J Neurosci 26:6643-6650
22. Tasker JG, Di S, Malcher-Lopes R 2006 Rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 147: 5549-5556
23. Cota D, Steiner MA, Marsicano G, Cervino C, Herman JP, Grübler Y, Stalla J, Pasquali R, Lutz B, Stalla GK, Pagotto U 2007 Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary- adrenal axis function. Endocrinology 148: 1574-1581
24. Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ 2004 Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 145:5431-5438
25. Sapolsky RM, Meaney MJ 1986 Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396:64-76
26. Walker CD, Sapolsky RM, Meaney MJ, Vale WW, Rivier CL 1986 Increased pituitary sensitivity to glucocorticoid feedback during the stress nonresponsive period in the neonatal rat. Endocrinology 119: 1816-1821
27. Trottier G, Koski KG, Brun T, Toufexis DJ, Richard D, Walker CD 1998 Increased fat intake during lactation modifies hypothalamic-pituitary-adrenal responsiveness in developing rat pups: a possible role for leptin. Endocrinology 139:3704-3711
28. Heiman ML, Ahima RS, Craft LS, Schoner B, Stephens TW, Flier JS 1997 Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology 138:3859-3863
29. Huang Q, Rivest R, Richard D 1998 Effects of leptin on corticotropin-releasing factor (CRF) synthesis and CRF neuron activation in the paraventricular hypothalamic nucleus of obese (ob/ob) mice. Endocrinology 139:1524-1532
30. Bornstein SR, Uhlmann K, Haidan A, Ehrhart-Bornstein M, Scherbaum WA 1997 Evidence for a novel peripheral action of leptin as a metabolic signal to the adrenal gland: leptin inhibits cortisol release directly. Diabetes 46:1235-1238
31. Salzmann C, Otis M, Long H, Roberge C, Gallo-Payet N, Walker CD 2004 Inhibition of steroidogenic response to adrenocorticotropin by leptin: implications for the adrenal response to maternal separation in neonatal rats. Endocrinology 145:1810-1822
32. Walker CD, Salzmann C, Long H, Otis M, Roberge C, Gallo-Payet N 2004 Direct inhibitory effects of leptin on the neonatal adrenal and potential consequences for brain glucocorticoid feedback. Endocr Res 30:837-844
33. Hofer MA 1994 Early relationships as regulators of infant physiology and behavior. Acta Paediatr Suppl 397:9-18
34. Walker CD, Dallman MF 1993 Neonatal facilitation of stress-induced adrenocorticotropin secretion by prior stress: evidence for increased central drive to the pituitary. Endocrinology 132:1101-1107
35. Chambers AP, Koopmans HS, Pittman QJ, Sharkey KA 2006 AM 251 produces sustained reductions in food intake and body weight that are resistant to tolerance and conditioned taste aversion. Br J Pharmacol 147:109-116
36. Proulx K, Clavel S, Nault G, Richard D, Walker CD 2001 High neonatal leptin exposure enhances brain GR expression and feedback efficacy on the adrenocortical axis of developing rats. Endocrinology 142:4607-4616
37. Walker CD, Xu Z, Rochford J, Johnston CC 2008 Naturally occurring variations in maternal care modulate the effects of repeated neonatal pain on behavioral sensitivity to thermal pain in the adult offspring. Pain 140:167-176
38. García-Cáceres C, Lechuga-Sancho A, Argente J, Frago LM, Chowen JA 2008 Death of hypothalamic astrocytes in poorly controlled diabetic rats is associated with nuclear translocation of apoptosis inducing factor. J Neuroendocrinol 20:1348-1360
39. Folch J, Lees M, Sloane Stanley GH 1957 A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509
40. Juaneda P, Rocquelin G 1985 Rapid and convenient separation of phospholipids and non phosphorus lipids from rat heart using silica cartridges. Lipids 20:40-41
41. Morrison WR, Smith LM 1964 Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J Lipid Res 5:600-608
42. Di Marzo V, Goparaju SK, Wang L, Liu J, Bátkai S, Járai Z, Fezza F, Miura GI, Palmiter RD, Sugiura T, Kunos G 2001 Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410:822-825
43. -ΔΔCT method. Methods 25:402-408
44. Arachchige PG, Takahashi Y, Ide T 2006 Dietary sesamin and docosahexaenoic and eicosapentaenoic acids synergistically increase the gene expression of enzymes involved in hepatic peroxisomal fatty acid oxidation in rats. Metabolism 55:381-390
45. Wood PA 2006. How fat works. Cambridge, MA: Harvard University Press
46. Neschen S, Moore I, Regittnig W, Yu CL, Wang Y, Pypaert M, Petersen KF, Shulman GI 2002 Contrasting effects of fish oil and safflower oil on hepatic peroxisomal and tissue lipid content. Am J Physiol Endocrinol Metab 282:E395-E401
47. Cunnane SC, McAdoo RR, Horrobin DF 1986 n-3 Essential fatty acids decrease weight gain in genetically obese mice. Br J Nutr 56: 87-95
48. Batetta B, Griinari M, Carta G, Murru E, Ligresti A, Cordeddu L, Giordano E, Sanna F, Bisogno T, Uda S, Collu M, Bruheim I, Di Marzo V, Banni S 2009 Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats. J Nutr 139:1495-1501
49. Herrera E, Lasunción MA, Huerta L, Martín-Hidalgo A 2000 Plasma leptin levels in rat mother and offspring during pregnancy and lactation. Biol Neonate 78:315-320
50. Symonds ME, Mostyn A, Pearce S, Budge H, Stephenson T 2003 Endocrine and nutritional regulation of fetal adipose tissue development. Endocrinology 179:293-299
51. Zhang Y, Hufnagel C, Eiden S, Guo KY, Diaz PA, Leibel R, Schmidt I 2001 Mechanisms for LEPR-mediated regulation of leptin expression in brown and white adipocytes in rat pups. Physiol Genomics 4:189-199
52. Walker CD, Naef L, D'Asti E, Long H, Xu Z 2008c Maternal fat intake and offspring brain development: focus on the mesocorticolimbic dopaminergic system. In: Bridges R, ed. Neurobiology of the parental brain. New York: Academic Press; 293-300
53. Ilcol YO, Hizli ZB, Ozkan T 2006 Leptin concentration in breast milk and its relationship to duration of lactation and hormonal status. Int Breastfeed J 1:21
54. Sarel I, Widmaier EP 1995 Stimulation of steroidogenesis in cultured rat adrenocortical cells by unsaturated fatty acids. Am J Physiol 268(6 Pt 2): R1484-R1490
55. Jensen CL, Voigt RG, Prager TC, Zou YL, Fraley JK, Rozelle JC, Turcich MR, Llorente AM, Anderson RE, Heird WC 2005 Effects of maternal docosahexaenoic acid intake on visual function and neurodevelopment in breastfed term infants. Am J Clin Nutr 82: 125-132
56. Patel S, Hillard CJ 2008 Adaptations in endocannabinoid signaling in response to repeated homotypic stress: a novel mechanism for stress habituation. Eur J Neurosci 27:2821-2829
57. Jo YH, Chen YJ, Chua Jr SC, Talmage DA, Role LW 2005 Integration of endocannabinoid and leptin signaling in an appetite-related neural circuit. Neuron 48:1055-1066
58. Maccarrone M, Di Rienzo M, Finazzi-Agrò A, Rossi A 2003 Leptin activates the anandamide hydrolase promoter in human T lymphocytes through STAT3. J Biol Chem 278:13318-13324
59. Waleh NS, Cravatt BF, Apte-Deshpande A, Terao A, Kilduff TS 2002 Transcriptional regulation of the mouse fatty acid amide hydrolase gene. Gene 291:203-210
60. Monteleone P, Matias I, Martiadis V, De Petrocellis L, Maj M, Di Marzo V 2005 Blood levels of the endocannabinoid anandamide are increased in anorexia nervosa and in binge-eating disorder, but not in bulimia nervosa. Neuropsychopharmacology 30:1216-1221
61. Goodfriend TL, Ball DL, Raff H, Bruder ED, Gardner HW, Spiteller G 2002 Oxidized products of linoleic acid stimulate adrenal steroidogenesis. Endocr Res 28:325-330