Inhibition of steroidogenic response to adrenocorticotropin by leptin: Implications for the adrenal response to maternal separation in neonatal rats

Endocrinology

Volumn 145, Issue 4, 2004, Pages 1810-1822

  Salzmann, Camila ^a   Otis, Melissa ^a   Long, Hong ^b   Roberge, Claude ^a   Gallo Payet, Nicole ^a   Walker, Claire Dominique ^b,c  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ALDOSTERONE; BENZODIAZEPINE RECEPTOR; CORTICOSTERONE; CORTICOTROPIN; CYTOCHROME P450 C11B1; CYTOCHROME P450 ISOENZYME; LEPTIN; PERIPHERAL BENZODIAZEPINE RECEPTOR; STEROID HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; UNCLASSIFIED DRUG;

ADOLESCENT; ADRENAL CORTEX CELL; ADRENAL GLAND; ALDOSTERONE RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE RELEASE; FEMALE; HORMONAL REGULATION; HORMONE INHIBITION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN VITRO STUDY; IN VIVO STUDY; MATERNAL DEPRIVATION; MATERNAL NUTRITION; NEWBORN; NEWBORN PERIOD; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEROIDOGENESIS; STRESS;

EID: 1642423734     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2003-1514     Document Type: Article

References (65)

1. 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
2. Ahima RS, Prabakaran D, Flier JS 1998 Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest 101:1020-1027
3. Gomez L, Carrascosa A, Teste D, Potau N, Rique S, Ruiz-Cuevas P, Almar J 1999 Leptin values in placental cord blood of human newborns with normal intrauterine growth after 30-42 weeks of gestation. 51:10-14
4. Devaskar SU, Ollesch C, Rajakumar RA, Rajakumar PA 1997 Developmental changes in ob gene expression and circulating leptin peptide concentrations. Biochem Biophys Res Commun 238:44-47
5. Lonnerdal B, Havel PJ 2000 Serum leptin concentrations in infants: effects of diet, sex, and adiposity. Am J Clin Nutr 72:484-489
6. Bonnet M, Delavaud C, Laud K, Gourdou I, Leroux C, Djiane J, Chilliard Y 2002 Mammary leptin synthesis, milk leptin and their putative physiological roles. Reprod Nutr Dev 42:399-413
7. Casanueva FF, Dieguez C 1999 Neuroendocrine regulation and actions of leptin. Front Neuroendocrinol 20:317-363
8. Licinio J, Mantzoros C, Negrao AB, Cizza G, Wong ML, Bongiorno PB, Chrousos GP, Karp B, Allen C, Flier JS, Gold PW 1997 Human leptin levels are pulsatile and inversely related to pituitary-adrenal function. Nat Med 3:575-579
9. Nye EJ, Bornstein S, Grice JE, Tauchnitz R, Hockings GI, Strakosch CR, Jackson RV, Torpy DJ 2000 Interactions between the stimulated hypothalamic-pituitary-adrenal axis and leptin in humans. J Neuroendocrinol 12:141-145
10. 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
11. Morimoto I, Yamamoto S, Kai K, Fujihira T, Morita E, Eto S 2000 Centrally administered murine-leptin stimulates the hypothalamus-pituitary- adrenal axis through arginine-vasopressin. Neuroendocrinology 71:366-374
12. 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
13. 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
14. Pralong FP, Roduit R, Waeber G, Castillo E, Mosimann F, Thorens B, Gaillard RC 1998 Leptin inhibits directly glucocorticoid secretion by normal human and rat adrenal gland. Endocrinology 139:4264-4268
15. Malendowicz LK, Nussdorfer GG, Markowska A 1997 Effects of recombinant murine leptin on steroid secretion of dispersed rat adrenocortical cells. J Steroid Biochem Mol Biol 63:123-125
16. Cao GY, Considine RV, Lynn RB 1997 Leptin receptors in the adrenal medulla of the rat. Am J Physiol 273:E448-E452
17. Tena-Sempere M, Pinilla L, Gonzalez LC, Casanueva FF, Dieguez C, Aguilar E 2000 Homologous and heterologous down-regulation of leptin receptor messenger ribonucleic acid in rat adrenal gland. J Endocrinol 167:479-486
18. Glasow A, Haidan A, Hilbers U, Breidert M, Gillespie J, Scherbaum WA, Chrousos GP, Bornstein SR 1998 Expression of Ob receptor in normal human adrenals: differential regulation of adrenocortical and adrenomedullary function by leptin. J Clin Endocrinol Metab 83:4459-4466
19. Cherradi N, Capponi AM, Gaillard RC, Pralong FP 2001 Decreased expression of steroidogenic acute regulatory protein: a novel mechanism participating in the leptin-induced inhibition of glucocorticoid biosynthesis. Endocrinology 142:3302-3308
20. Fuxe K, Diaz R, Cintra A, Bhatnagar M, Tinner B, Gustafsson J-A, Ogren O, Agnati LF 1996 On the role of glucocorticoid receptors in brain plasticity. Cell Mol Neurobiol 16:239-258
21. Walker C-D, Anand KJS, Plotsky PM 2001 Ontogeny of the hypothalamus-pituitary adrenal axis and the stress response. In: McEwen BS, Goddman HM, eds. Handbook of physiology. Sect 7. Oxford: Oxford Press; 237
22. Sapolsky RM, Meaney MJ 1986 Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res Rev 11:64-76
23. Walker C.-D, Scribner KA, Cascio CS, Dallman MF 1991 The pituitary adrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion. Endocrinology 128:1385-1395
24. Yoshimura S, Sakamoto S, Kudo H, Sassa S, Kumai A, Okamoto R 2003 Sex-differences in adrenocortical responsiveness during development in rats. Steroids 68:439-445
25. Okimoto DK, Blaus A, Schmidt M, Gordon MK, Dent GW, Levine S 2002 Differential expression of c-fos and tyrosine hydroxylase mRNA in the adrenal gland of the infant rat: evidence for an adrenal hyporesponsive period. Endocrinology 143:1717-1725
26. Henning SJ, Genovese GM 1985 Postnatal development of cholesterol ester hydrolase activity in the rat adrenal. J Steroid Biochem 22:803-808
27. Arai M, Widmaier EP 1993 Steroidogenesis in isolated adrenocortical cells during development in rats. Mol Cell Endocrinol 92:91-97
28. Nagaya M, Arai M, Widmaier EP 1995 Ontogeny of immunoreactive and bioactive microsomol steroidogenic enzymes during adrenocortical development in rats. Mol Cell Endocrinol 114:27-34
29. Walker C-D 1995 Effects of chemical sympathectomy and maternal separation on neonatal adrenocortical stress responses and adrenal sensitivity to ACTH. Am J Physiol 268:R1281-R1288
30. Papadopoulos V 1998 Structure and function of the peripheral-type benzodiazepine receptor in steroidogenic cells. Proc Soc Exp Biol Med 217:130-142
31. Zilz A, Li H, Castello R, Papadopoulos V, Widmaier EP 1999 Developmental expression of the peripheral-type benzodiazepine receptor and the advent of steroidogenesis in rat adrenal glands. Endocrinology 140:859-864
32. Suchecki D, Nelson DY, Van Oers H, Levine S 1995 Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: effects of maternal deprivation. Psychoneuroendocrinology 20:169-182
33. Levine S, Huchton DM, Wiener SG, Rosenfeld P 1992 Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev Psychobiol 24:547-558
34. Levine S 2002 Regulation of the hypothalamic-pituitary-adrenal axis in the neonatal rat: the role of maternal behavior. Neurotox Res 4:557-564
35. Suchecki D, Rosenfeld P, Levine S 1993 Maternal regulation of the hypothalamic-pituitary-adrenal axis in the infant rat: the roles of feeding and stroking. Brain Res Dev Brain Res 75:185-192
36. West LA, Horvat RD, Roess DA, Barisas BG, Juengel JL, Niswender GD 2001 Steroidogenic acute regulatory protein and peripheral-type benzodiazepine receptor associate at the mitochondrial membrane. Endocrinology 142:502-505
37. Gallo-Payet N, Payet MD 1989 Excitation-secretion coupling: involvement of potassium channels in ACTH-stimulated rat adrenocortical cells. J Endocrinol 120:409-421
38. Salomon Y, Londos C, Rodbell M 1974 A highly sensitive adenylate cyclase assay. Anal Biochem 58:541-548
39. Côté M, Guillon G, Payet M, Gallo-Payet N 2001 Expression and regulation of adenylyl cyclase isoforms in the human adrenal gland. J Clin Endocrinol Metab 86:4495-4503
40. Proulx K, Clavel S, Nault G, Richard D, Walker C-D 2001 High neonatal leptin exposure enhances brain glucocorticoid receptor expression and feedback efficacy on the adrenocortical axis of developing rats. Endocrinology 142:4607-4616
41. mapk pathway and of intracellular calcium. Endocrinology 144:1486-1495
42. King SR, Liu Z, Soh J, Eimerl S, Orly J, Stocco DM 1999 Effects of disruption of the mitochondrial electrochemical gradient on steroidogenesis and the steroidogenic acute regulatory (StAR) protein. J Steroid Biochem Mol Biol 69:143-154
43. Amri H, Ogwuegbu SO, Boujrad N, Drieu K, Papadopoulos V 1996 In vivo regulation of peripheral-type benzodiazepine receptor and glucocorticoid synthesis by Ginkgo biloba extract EGb 761 and isolated ginkgolides. Endocrinology 137:5707-5718
44. Bustin SA 2002 Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29:23-39
45. Engeland WC, Wotus C, Rose JC 1998 Ontogeny of innervation of rat and ovine fetal adrenals. Endocr Res 24:889-898
46. Szucs N, Varga I, Jakab C, Patocs A, Glaz E, Toth M, Kiss R, Racz K 2001 Leptin inhibits cortisol and corticosterone secretion in pathologic human adrenocortical cells. Pituitary 4:71-77
47. Nowak KW, Pierzchala-Koziec K, Tortorella C, Nussdorfer GC, Malendowicz LK 2002 Effects of prolonged leptin infusion on rat pituitary-adrenocortical function. Int J. Mol Med 9:61-64
48. Oates M, Woodside B, Walker CD 2000 Chronic leptin administration in developing rats reduces stress responsiveness partly through changes in maternal behavior. Horm Behav 37:366-376
49. Stocco DM 2001 Tracking the role of a star in the sky of the new millennium. Mol Endocrinol 15:1245-1254
50. Cherradi N, Brandenburger Y, Capponi AM 1998 Mitochondrial regulation of mineralocorticoid biosynthesis by calcium and the StAR protein. Eur J Endocrinol 139:249-256
51. Raff H, Hong JJ, Oaks MK, Widmaier EP 2002 Adrenocortical responses to ACTH in neonatal rats: effect of hypoxia from birth on corticosterone, StAR, and PBR. Am J Physiol 284:R78-R85
52. Ariyoshi N, Kim YC, Artemenko I, Bhattacharyya KK, Jefcoate CR 1998 Characterization of the rat Star gene that encodes the predominant 3.5-kilobase pair mRNA. ACTH stimulation of adrenal steroids in vivo precedes elevation of Star mRNA and protein. J Biol Chem 273:7610-7619
53. Lehoux JG, Mathieu A, Lavigne P, Fleury A 2003 Adrenocorticotropin regulation of steroidogenic acute regulator protein. Microsc Res Tech 61:288-299
54. Ranganathan G, Phan D, Pokrovskaya ID, McEwen JE, Li C, Kern PA 2002 The translational regulation of lipoprotein lipase by epinephrine involves an RNA binding complex including the catalytic subunit of protein kinase A. J Biol Chem 277:43281-43287
55. Christenson LK, McAllister JM, Martin KO, Javitt NB, Osborne TF, Strauss III JF 1998 Oxysterol regulation of steroidogenic acute regulatory protein gene expression. Structural specificity and transcriptional and posttranscriptional actions. J Biol Chem 273:30729-30735
56. Sweeney G 2002 Leptin signalling. Cell Signalling 14:655-663
57. Marrero MB, Schleifer B, Paxton WG, Heerdt L, Berk BC, Delafontaine P, Bernstein KE 1995 Direct stimulation of Jak/STAT pathway by the angiotensin II AT1 receptor. Nature 375:247-250
58. Peters B, Clausmeyer S, Obermuller N, Woyth A, Kranzlin B, Gretz N, Peters J 1998 Specific regulation of StAR expression in the rat adrenal zona glomerulosa. An in situ hybridization study. J Histochem Cytochem 46:1215-1221
59. Lebrethon MC, Naville D, Begeot M, Saez JM 1994 Regulation of corticotropin receptor number and messenger RNA in cultured human adrenocortical cells by corticotropin and angiotensin II. J Clin Invest. 93:1828-1833
60. Tartaglia LA 1997 The leptin receptor. J Biol Chem 272:6093-6096
61. Hoggard N, Mercer JG, Rayner DV, Moar K, Trayhurn P, Williams LM 1997 Localization of leptin receptor mRNA splice variants in murine peripheral tissues by RT-PCR and in situ hybridization. Biochem Biophys Res Commun 232:383-387
62. Hileman SM, Pierroz DD, Masuzaki H, Bjorbaek C, El-Haschimi K, Banks WA, Flier JS 2002 Characterization of short isoforms of the leptin receptor in rat cerebral microvessels and of brain uptake of leptin in mouse models of obesity. Endocrinology 143:775-783
63. Murakami T, Yamashita T, Iida M, Kuwajima M, Shima K 1997 A short form of leptin receptor performs signal transduction. Biochem Biophys Res Commun 231:26-29
64. White DW, Tartaglia LA 1999 Evidence for ligand-independent homo-oligomerization of leptin receptor (OB-R) isoforms: a proposed mechanism permitting productive long-form signaling in the presence of excess short-form expression. J Cell Biochem 73:278-288
65. Walker C-D, Kudreikis K, Kerman B, Maternal food restriction as a model to reduce exposure to leptin in rat pups during a critical period of brain development. Program of the 31st Annual Meeting of the Society for Neuroscience, San Diego, CA, 2001, vol 27 (Abstract 635.7)