Programming neuroendocrine stress axis activity by exposure to glucocorticoids during postembryonic development of the frog, Xenopus laevis

Endocrinology

Volumn 149, Issue 11, 2008, Pages 5470-5481

  Hu, Fang ^a   Crespi, Erica J ^b   Denver, Robert J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b VASSAR COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY SIZE; CATCH UP GROWTH; CONTROLLED STUDY; DIET RESTRICTION; EMBRYO DEVELOPMENT; FEEDBACK SYSTEM; FOOD AVAILABILITY; HYPERPHAGIA; IMMUNOHISTOCHEMISTRY; METAMORPHOSIS; MOLECULAR MECHANICS; NEUROSECRETORY CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STRESS; TADPOLE; XENOPUS LAEVIS;

ANIMALS; BODY SIZE; BRAIN; CALORIC RESTRICTION; CORTICOSTERONE; EATING; GLUCOCORTICOIDS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LARVA; METAMORPHOSIS, BIOLOGICAL; NEUROSECRETORY SYSTEMS; PITUITARY GLAND; PITUITARY-ADRENAL SYSTEM; RECEPTORS, GLUCOCORTICOID; STRESS, PHYSIOLOGICAL; XENOPUS LAEVIS;

EID: 54349096794     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0767     Document Type: Article

References (95)

1. Phillips DIW 2004 Fetal programming of the neuroendocrine response to stress: links between low birth weight and the metabolic syndrome. Endocr Res 30:819-826
2. Ward AMV, Syddall HE, Wood PJ, Chrousos GP, Phillips DIW 2004 Fetal programming of the hypothalamic-pituitary-adrenal (HPA) axis: low birth weight and central HPA regulation. J Clin Endocrinol Metab 89:1227-1233
3. Barker DJP 2007 The origins of the developmental origins theory. J Intern Med 261:412-417
4. Gluckman PD, Hanson MA 2007 Developmental plasticity and human disease: research directions. J Intern Med 261:461-471
5. Welberg LAM, Seckl JR 2001 Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13:113-128
6. Matthews SG, Owen D, Kalabis G, Banjanin S, Setiawan EB, Dunn EA, Andrews MH 2004 Fetal glucocorticoid exposure and hypothalamo-pituitary- adrenal (HPA) function after birth. Endocr Res 30:827-836
7. Meaney MJ, Szyf M, Seckl JR 2007 Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 13:269-277
8. Yao M, Denver RJ 2007 Regulation of vertebrate corticotropin-releasing factor genes. Gen Comp Endocrinol 153:200-216
9. Yao M, Stenzel-Poore M, Denver RJ 2007 Structural and functional conservation of vertebrate corticotropin-releasing factor genes: evidence for a critical role for a conserved cyclic AMP response element. Endocrinology 148:2518-2531
10. Yao M, Schulkin J, Denver RJ 2008 Evolutionarily conserved glucocorticoid regulation of corticotropin-releasing factor expression. Endocrinology 149:2352-2360
11. Tasker JG, Di S, Malcher-Lopes R 2006 Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 147:5549-5556
12. Jacobson L, Sapolsky R 1991 The role of the hippocampus in feedback-regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118-134
13. Herman JP, Cullinan WE 1997 Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78-84
14. Matthews SG 2002 Early programming of the hypothalamo-pituitary- adrenal axis. Trends Endocrinol Metab 13:373-380
15. Herman JP, Ostrander MM, Mueller NK, Figueiredo H 2005 Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201-1213
16. Yao M, Hu F, Denver RJ 2008 Distribution and corticosteroid regulation of glucocorticoid receptor in the brain of Xenopus laevis. J Comp Neurol 508:967-982
17. Francis D, Diorio J, LaPlante P, Weaver S, Seckl JR, Meaney MJ 1996 The role of early environmental events in regulating neuroendocrine development: moms, pups, stress, and glucocorticoid receptors. Ann NY Acad Sci 794:136-152
18. O'Regan D, Welberg LL, Holmes MC, Seckl JR 2001 Glucocorticoid programming of pituitary-adrenal function: mechanisms and physiological consequences. Semin Neonatol 6:319-329
19. Seckl JR 2004 Prenatal glucocorticoids and long-term programming. Eur J Endocrinol 151:U49-U62
20. Henry C, Kabbaj M, Simon H, Lemoal M, Maccari S 1994 Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 6:341-345
21. McCormick CM, Smythe JW, Sharma S, Meaney MJ 1995 Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Dev Brain Res 84:55-61
22. Weinstock M 2001 Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427-451
23. Lesage J, Del-Favero F, Leonhardt M, Louvart H, Maccari S, Vieau D, Darnaudery M 2004 Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol 181:291-296
24. Barker DJ, Clark PM 1997 Fetal undernutrition and disease later in life. Rev Reprod 2:105-112
25. Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WPS 2001 Fetal programming of appetite and obesity. Mol Cell Endocrinol 185:73-79
26. Sapolsky RM 2003 Stress and plasticity in the limbic system. Neurochem Res 28:1735-1742
27. Welberg LAM, Seckl JR, Holmes MC 2001 Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 104:71-79
28. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Lemoal M 1995 Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15:110-116
29. Meaney MJ, Aitken DH, Vanberkel C, Bhatnagar S, Sapolsky RM 1988 Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239:766-768
30. Newman R 1992 Adaptive plasticity in amphibian metamorphosis. Bioscience 42:671-678
31. Denver RJ 1997 Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Horm Behav 31:169-179
32. Denver RJ, Boorse GC, Glennemeier KA 2002 Endocrinology of complex life cycles: amphibians. In: Pfaff D, Etgen A, Fahrbach S, Moss R, Rubin R, eds. Hormones, brain and behavior. San Diego: Academic Press, Inc.; 469-513
33. Semlitsch R, Scott D, Pechmann J 1988 Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184-192
34. Goater CP 1994 Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75:2264-2274
35. Denver RJ 1998 Hormonal correlates of environmentally induced metamorphosis in the Western spadefoot toad, Scaphiopus hammondii. Gen Comp Endocrinol 110:326-336
36. Denver RJ, Mirhadi N, Phillips M 1998 Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology 79:1859-1872
37. Beck CW, Congdon JD 1999 Effects of individual variation in age and size at metamorphosis on growth and survivorship of Southern toad (Bufo terrestris) metamorphs. Can J Zool 77:944-951
38. Van Buskirk J, Saxer G 2001 Delayed costs of an induced defense in tadpoles? Morphology, hopping, and development rate at metamorphosis. Evolution 55:821-829
39. Glennemeier KA, Denver RJ 2002 Developmental changes in interrenal responsiveness in anuran amphibians. Integr Comp Biol 42:565-573
40. Glennemeier KA, Denver RJ 2002 Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. J Exp Zool 292:32-40
41. Glennemeier KA, Denver RJ 2002 Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components. Gen Comp Endocrinol 127:16-25
42. Relyea RA, Hoverman JT 2003 The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596-604
43. Crespi EJ, Denver RJ 2005 Roles of stress hormones in food intake regulation in anuran amphibians throughout the life cycle. Comp Biochem Physiol A Mol Integr Physiol 141:381-390
44. Nieuwkoop PD, Faber J 1994 In: Normal table of Xenopus laevis (Daudin). New York: Garland Publishing Inc.
45. Kaufmann KW 1981 Fitting and using growth curves. Oecologia 49:293-299
46. Sinervo B, Adolph SC 1989 Thermal sensitivity of growth rate in hatchling Sceloporus lizards: environmental, behavioral and genetic aspects. Oecologia 78:411-419
47. Yao M, Westphal NJ, Denver RJ 2004 Distribution and acute stressor-induced activation of corticotrophin-releasing hormone neurones in the central nervous system of Xenopus laevis. J Neuroendocrinol 16:880-893
48. Licht P, McCreery BR, Barnes R, Pang R 1983 Seasonal and stress related changes in plasma gonadotropins, sex steroids, and corticosterone in the bull-frog, Rana catesbeiana. Gen Comp Endocrinol 50:124-145
49. Tuinhof R, Ubink R, Tanaka S, Atzori C, van Strien FJC, Roubos EW 1998 Distribution of pro-opiomelanocortin and its peptide end products in the brain and hypophysis of the aquatic toad, Xenopus laevis. Cell Tissue Res 292:251-265
50. Marin O, Smeets WJAJ, Gonzalez A 1998 Basal ganglia organization in amphibians: chemoarchitecture. J Comp Neurol 392:285-312
51. Krain LP, Denver RJ 2004 Developmental expression and hormonal regulation of glucocorticoid and thyroid hormone receptors during metamorphosis in Xenopus laevis. J Endocrinol 181:91-104
52. Kollros JJ, Thiesse ML 1988 Control of tectal cell number during larval development in Rana pipiens. J Comp Neurol 278:430-445
53. Denver RJ, Pavgi S, Shi YB 1997 Thyroid hormone-dependent gene expression program for Xenopus neural development. J Biol Chem 272:8179-8188
54. Denver RJ 1998 The molecular basis of thyroid hormone-dependent central nervous system remodeling during amphibian metamorphosis. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 119:219-228
55. Boorse GC, Denver RJ 2004 Expression and hypophysiotropic actions of corticotropin-releasing factor in Xenopus laevis. Gen Comp Endocrinol 137:272-282
56. Campantico E, Guastalla A, Patriarca E 1985 Identification by immunofluorescence of ACTH-producing cells in the pituitary gland of the tree frog Hyla arborea. Gen Comp Endocrinol 59:192-198
57. Vaudry H, Leboulenger F, Trochard MC, Vaillant R 1977 Changes in corticotropin producing cells in pituitary of Rana esculenta-L following inter-renalectomy and Metopirone treatment: immunohistochemical study. Gen Comp Endocrinol 32:78-88
58. Hayes T, Chan R, Licht P 1993 Interactions of temperature and steroids on larval growth, development and metamorphosis in a toad (Bufo boreas). J Exp Zool 266:206-215
59. Hayes TB 1995 Interdependence of corticosterone hormones and thyroid hormones in larval toads (Bufo boreas). 1. Thyroid hormone dependent and hormone-independent effects of corticosterone on growth and development. J Exp Zool 271:95-102
60. Wright ML, Cykowski LJ, Lundrigan L, Hemond KL, Kochan DM, Faszewski EE, Anuszewski CM 1994 Anterior-pituitary and adrenal-cortical hormones accelerate or inhibit tadpole hindlimb growth and development depending on stage of spontaneous development or thyroxine concentration in induced metamorphosis. J Exp Zool 270:175-188
61. Wilbur HM, Collins JP 1973 Ecological aspects of amphibian metamorphosis. Science 182:1305-1314
62. Boorse GC, Denver RJ 2002 Acceleration of Ambystoma tigrinum metamorphosis by corticotropin-releasing hormone. J Exp Zool 293:94-98
63. Newman RA 1988 Adaptive plasticity in development of Scaphiopus couchii tadpoles in desert ponds. Evolution 42:774-783
64. Denver RJ, Crespi EJ 2006 Stress hormones and human developmental plasticity: lessons from tadpoles. Neoreviews 7:183-188
65. Dallman MF, Akana SF, Levin N, Walker CD, Bradbury MJ, Suemaru S, Scribner KS 1994 Corticosteroids and the control of function in the hypothalamo-pituitary-adrenal (HPA) axis. Ann NY Acad Sci 746:22-32
66. Tataranni PA, Larson DE, Snitker S, Young JB, Flatt JP, Ravussin E 1996 Effects of glucocorticoids on energy metabolism and food intake in humans. Am J Physiol Endocrinol Metab 34:E317-E325
67. Crespi EJ, Vaudry H, Denver RJ 2004 Roles of corticotropin- releasing factor, neuropeptide Y and corticosterone in the regulation of food intake in Xenopus laevis. J Neuroendocrinol 16:279-288
68. Metcalfe NB, Monaghan P 2001 Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254-260
69. Fride E, Dan Y, Feldon J, Halevy G, Weinstock M 1986 Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol Behav 37:681-687
70. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG 2002 Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long Evans rats. Pharmacol Biochem Behav 73:131-140
71. Takahashi LK, Kalin NH 1991 Early developmental and temporal characteristics of stress induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Res 558:75-78
72. Koehl M, Darnaudery M, Dulluc J, Van Reeth O, Le Moal M, Maccari S 1999 Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 40:302-315
73. Shoener JA, Baig R, Page KC 2006 Prenatal exposure to dexamethasone alters hippocampal drive on hypothalamic-pituitary-adrenal axis activity in adult male rats. Am J Physiol Regul Integr Comp Physiol 290:R1366-R1373
74. Vallee M, Mayo W, Maccari S, LeMoal M, Simon H 1996 Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res 712:287-292
75. Tonon MC, Burlet A, Lauber M, Cuet P, Jegou S, Gouteux L, Ling N, Vaudry H 1985 Immunohistochemical localization and radioimmunoassay of corticotropin-releasing factor in the forebrain and hypophysis of the frog Rana ridibunda. Neuroendocrinology 40:109-119
76. Chung S, Son GH, Park SH, Park E, Lee KH, Geum D, Kim K 2005 Differential adaptive responses to chronic stress of maternally stressed male mice offspring. Endocrinology 146:3202-3210
77. Sapolsky RM, Meaney MJ, McEwen BS 1985 The development of the glucocorticoid receptor system in the rat limbic brain 3. Negative feedback regulation. Dev Brain Res 18:169-173
78. Levitt NS, Lindsay RS, Holmes MC, Seckl JR 1996 Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology 64:412-418
79. Francis DD, Diorio J, Plotsky PM, Meaney MJ 2002 Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840-7843
80. Theogaraj E, John CD, Christian HC, Morris JF, Smith SF, Buckingham JC 2005 Perinatal glucocorticoid treatment produces molecular, functional, and morphological changes in the anterior pituitary gland of the adult male rat. Endocrinology 146:4804-4813
81. Gomez F, Lahmame A, deKloet ER, Armario A 1996 Hypothalamic-pituitary-adrenal response to chronic stress in five inbred rat strains: differential responses are mainly located at the adrenocortical level. Neuroendocrinology 63:327-337
82. Herman JP, Adams D, Prewitt C 1995 Regulatory changes in neuroendocrine stress integrative circuitry produced by a variable stress paradigm. Neuroendocrinology 61:180-190
83. Makino S, Schulkin J, Smith MA, Pacak K, Palkovits M, Gold PW 1995 Regulation of corticotropin-releasing hormone receptor messenger ribonucleic acid in the rat brain and pituitary by glucocorticoids and stress. Endocrinology 136:4517-4525
84. Makino S, Smith MA, Gold PW 2002 Regulatory role of glucocorticoids and glucocorticoid receptor mRNA levels on tyrosine hydroxylase gene expression in the locus caeruleus during repeated immobilization stress. Brain Res 943:216-223
85. Nishimura K, Makino S, Tanaka Y, Kaneda T, Hashimoto K 2004 Altered expression of p53 mRNA in the brain and pituitary during repeated immobilization stress: negative correlation with glucocorticoid receptor mRNA levels. J Neuroendocrinol 16:84-91
86. Makino S, Smith MA, Gold PW 1995 Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (messenger RNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor messenger RNA levels. Endocrinology 136:3299-3309
87. Makino S, Hashimoto K, Gold PW 2002 Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol Biochem Behav 73:147-158
88. Deroo BJ, Rentsch C, Sampath S, Young J, DeFranco DB, Archer TK 2002 Proteasomal inhibition enhances glucocorticoid receptor transactivation and alters its subnuclear trafficking. Mol Cell Biol 22:4113-4123
89. Conway-Campbell BL, McKenna MA, Wiles CC, Atkinson HC, de Kloet ER, Lightman SL 2007 Proteasome-dependent down-regulation of activated nuclear hippocampal glucocorticoid receptors determines dynamic responses to corticosterone. Endocrinology 148:5470-5477
90. Seckl JR, Meaney MJ 2004 Glucocorticoid programming. Ann NY Acad Sci 1032:63-84
91. Feldman S, Weidenfeld J 1998 The excitatory effects of the amygdala on hypothalamo-pituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res Bull 45:389-393
92. Moreno N, Gonzalez A 2003 Hodological characterization of the medial amygdala in anuran amphibians. J Comp Neurol 466:389-408
93. Szyf M, Weaver ICG, Champagne FA, Diorio J, Meaney MJ 2005 Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 26:139-162
94. Weaver ICG, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, Szyf M 2005 Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25:11045-11054
95. Weaver ICG, D'Alessio AC, Brown SE, Hellstrom IC, Dymov S, Sharma S, Szyf M, Meaney MJ 2007 The transcription factor nerve growth factor-inducible protein A mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J Neurosci 27:1756-1768