Glucocorticoid receptor activation following elevated oocyte cortisol content is associated with zygote activation, early embryo cell division, and IGF system gene responses in rainbow trout

Journal of Endocrinology

Volumn 215, Issue 1, 2012, Pages 137-149

  Li, Mao ^a   Leatherland, John F ^a   Vijayan, Matt M ^b   King, WAllan ^a   Madan, Pavneesh ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MESSENGER RNA; MIFEPRISTONE; SOMATOMEDIN;

ARTICLE; CELL ACTIVATION; CELL COUNT; CELL DIVISION; EARLY EMBRYO CELL DIVISION; EMBRYO CELL; EPIGENETICS; FERTILIZATION; GAMETE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LONG TERM CARE; OOCYTE; PRIORITY JOURNAL; ZYGOTE;

ANIMALS; CELL DIVISION; CLEAVAGE STAGE, OVUM; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYDROCORTISONE; ONCORHYNCHUS MYKISS; OOCYTES; RECEPTORS, GLUCOCORTICOID; RECEPTORS, SOMATOMEDIN; SIGNAL TRANSDUCTION; SOMATOMEDINS; TIME FACTORS; UP-REGULATION; ZYGOTE;

EID: 84869233755     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0030     Document Type: Article

References (70)

1. Alderman SL, Mcguire A, Bernier NJ & Vijayan MM. 2012 Central and peripheral glucocorticoid receptors are involved in the plasma cortisol response to an acute stressor in rainbow trout. General and Comparative Endocrinology 176 79-85.
2. Aluru N, Jorgensen EH, Maule AG & Vijayan MM. 2004 PCB disruption of the hypothalamus-pituitary-interrenal axis involves brain glucocorticoid receptor downregulation in anadromous Arctic charr. American Journal of Physiology.Regulatory, Integrative and Comparative Physiology 287 R787-R793.
3. Aluru N, Leatherland JF & Vijayan MM. 2010 Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout. PLoS One 5 e10741.
4. Bahrekazemi M, Matinfar A, Soltani M, Abtahi B, Pusti I & Mohagheghi A. 2009 The relation between egg viability, selected aspects of egg and ovarian fluid composition and time of stripping in endangered Caspian brown trout (Salmo trutta caspius). Journal of Fisheries and Aquatic Science 4 306-315.
5. Barry TP, Malison JA, Held JA & Parrish JJ. 1995 Ontogeny of the cortisol stress response in larval rainbow trout. General and Comparative Endocrinology 97 57-65.
6. Bashirulla A, Cooperstock RL & Lipshitz HD. 2001 Spatial and temporal control of RNA stability. PNAS 98 7025-7028.
7. Bashirulla A, Halsell SR, Cooperstock RL, Kloc M, Karaiskakis A, Fisher WW, Fu W, Hamilton JK, Etkin LD & Lipshitz HD. 1999 Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO Journal 18 2610-2620.
8. Bury NR, Sturn A, Le Rouzic P, Lethimonier C, Ducouret B, Guiguen Y, Robinson-Rechavi MK, Laudet V, Rafestin-Oblin ME & Prunet P. 2003 Evidence for two distinct functional glucocorticoid receptors in teleost fish. Journal of Molecular Endocrinology 31 141-156.
9. Derfoul A, Perkings GL, Hall DJ & Tuan RS. 2006 Glucocorticoids promote chondrogenic differentiation of adult human mesenchymal stem cell by enhancing expression of cartilage extracellular matrix genes. Stem Cells 24 1487-1495.
10. Du J, Wang Y, Hunter R, Wei Y, Blumenthal R, Falke C, Khairova R, Zhou R, Yuan P, Machado-Vieira M et al. 2009 Dynamic regulation of mitochondrial function by glucocorticoids. PNAS 106 3543-3548.
11. Eriksen MS, Bakken M, Espmark A, Braastad BO & Salte R. 2006 Prespawning stress in farmed Atlantic salmon Salmo salar: maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations. Journal of Fish Biology 69 114-129.
12. Eriksen MS, Espmark A, Braastad BO, Salte R & Bakken M. 2007 Long-term effects of maternal cortisol exposure and mild hyperthermia during embryogeny on survival, growth and morphological anomalies in farmed Atlantic salmon Salmo salar offspring. Journal of Fish Biology 70 462-473.
13. Eriksen MS, Kittilsen FG, Mccormick S & Damsgård MI. 2011 Stressed mothers - troubled offspring: a study of behavioural maternal effects in farmed Salmo salar. Journal of Fish Biology 79 575-586.
14. Ferg M, Sanges R, Gehrig J, Kiss J, Bauer M, Lovas A, Szabo M, Yang L, Straehle U, Pankratz MJ, Olasz F, Stupka E & Muller F. 2007 The TATA-binding protein regulates maternal mRNA degradation and differential zygotic transcription in zebrafish. EMBO Journal 26 3945-3956.
15. Fitzsimons CP, Ahmed S, Wittevrongel CF, Schouten TG, Dijkmans TF, Scheenen WJ, Schaaf MJ, de Kloet ER & Vreugdenhil E. 2008 The microtubule-associated protein doublecortin-like regulates the transport of the glucocorticoid receptor in neuronal progenitor cells. Molecular Endocrinology 22 248-262.
16. Giraud GD, Louey S, Jonker S, Schultz J & Thomburg KL. 2006 Cortisol stimulates cell cycle activity in the cardiomyocyte of the sheep fetus. Endocrinology 147 3643-3649.
17. Gluckman PD, Hanson MA, Buklijas T, Low FM & Beedle AS. 2009 Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nature Reviews. Endocrinology 5 401-408.
18. Godfrey KM, Gluckman PD & Hanson MA. 2010 Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends in Endocrinology and Metabolism 21 199-205.
19. Gravel A & Vijayan MM. 2006 Salicylate disrupts interrenal steroidogenesis and brain glucocorticoid receptor expression in rainbow trout. Toxicological Sciences 93 41-49.
20. Hawkins MB & Thomas P. 2010 The unusual binding properties of the third distinct teleost estrogen receptor subtype ERba are accompanied by highly conserved amino acid changes in the ligand binding domain. Endocrinology 145 2968-2977.
21. Hayashi Y, Kobira H, Yamaguchi T, Shiraishi E, Yazawa T, Hirai T, Kamei Y & Kitano T. 2010 High temperature causes masculinization of genetically female medaka by elevation of cortisol. Molecular Reproduction and Development 77 679-686.
22. Heitzer MD, Wolf IM, Sanchez ER, Witchel SF & Defranco DB. 2007 Glucocorticoid receptor physiology. Reviews in Endocrine & Metabolic Disorders 8 321-330.
23. Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, Boileau P, Lillycrop K, Scharfmann R, Sheppard A et al. 2011 Child health, developmental plasticity, and epigenetic programming. Endocrine Reviews 32 159-224.
24. Huang WT, Yu HC, Hsu CC, Liao CF, Gong HY, Lin CJ, Wu JL &Weng CF. 2007 Steroid hormone (17b-estradiol and hydrocortisone) upregulate hepatocyte nuclear factor (HNF)-3b and insulin-like growth factors I and II expression in the gonads of tilapia (Oreochromis mossambicus) in vitro. Theriogenology 68 988-1002.
25. Lahnsteiner F. 2000 Morphological, physiological and biochemical parameters characterizing over-ripening of rainbow trout eggs. Fish Physiology and Biochemistry 23 107-118.
26. Leatherland JF. 2010 Endocrine and reproductive system, including their interaction with the immune system. In: Fish Diseases and Disorders. Volume 2, Non-Infectious Disorders, 2nd edn, pp 85-143. Eds JF Leatherland & PTK Woo. New York: CABI Publishing.
27. Leatherland JF, Ferris J & Li M. 2012 Comparison of the affect of stress on ovarian function, reproduction and neonatal outcomes in fish and mammals: possible mechanisms of action. In The Physiology of Stress. Eds SE Wendelaar Bonga, S Peter & B Peter. New York: Springer (In press).
28. Leatherland JF, LiM& Barkataki S. 2010 Stressors, glucocorticoids and ovarian function in teleosts. Journal of Fish Biology 76 86-111.
29. Leonhardt SA & Edwards DP. 2002 Mechanism of action of progesterone antagonists. Experimental Biology and Medicine 227 969-980
30. Lewis-Tuffin LJ, Jewell CM, Bienstock RJ, Collins JB & Cidlowski JA. 2007 Human glucocorticoid receptor b binds RU-486 and is transcriptionally active. Molecular and Cellular Biology 27 2266-2282.
31. Li M. 2011. The actions of cortisol on rainbowtrout (Oncorhynchus mykiss) early embryo developmental biology. PhD Dissertation. University of Guelph. Canada (http://search.proquest.com/docview/883529121/ PDF).
32. Li M, Bureau D, King WA & Leatherland JF. 2010 The actions of in ovo cortisol on egg fertility, embryo development and the expression of growthrelated genes in rainbow trout embryos, and the growth performance of juveniles. Molecular Reproduction and Development 77 922-931.
33. Li M & Leatherland JF. 2008 Temperature and ration level effect on rainbow trout embryo IGF system components and growth performance. General and Comparative Endocrinology 155 668-697.
34. Li M, Raine JC & Leatherland JF. 2007 Expression profiles of growth-related genes during the very early development of rainbow trout embryos reared at two incubation temperatures. General and Comparative Endocrinology 153 302-310.
35. Li M, Russell S, Lumsden JS & Leatherland JF. 2011 The influence of oocyte cortisol on the early ontogeny of intelectin and TLR-5, and changes in lysozyme activity in rainbow trout (Oncorhynchus mykiss) embryos. Comparative Biochemistry and Physiology 160B 159-165.
36. Madan P, Rose K & Watson AJ. 2007 Na/K-ATPase b1 subunit expression is required for blastocyst formation and normal assembly of trophectoderm tight junction associated proteins. Journal of Biological Chemistry 282 12127-12134.
37. Matthews SG & Phillips DIW. 2010 Transgenerational inheritance of the stress response: a new frontier in stress research. Endocrinology 151 7-13.
38. Mikami Y, Takahashi T, Kato S & Takagi M. 2008 Dexamethasone promotes DMP1 mRNA expression by inhibiting negative regulation of Runx2 in multipotential mesenchymal progenitor. Cell Biology International 32 239-246.
39. Milla S, Jalabert B, Rime H, Prunet P & Bobe J. 2006 Hydration of rainbow trout oocyte during meiotic maturation and in vitro regulation by 17,20b-dihydroxy-4-pregnen-3-one and cortisol. Journal of Experimental Biology 209 1147-1156.
40. Milla S, Wang N, Mandiki SNM & Kestemont P. 2009 Corticosteroids: friends or foes of teleost fish reproduction. Comparative Biochemistry and Physiology 153A 242-251.
41. Nesan D, Kamkar M, Burrows J, Scott IC, Marsden M & Vijayan MM. 2012 Glucocorticoid receptor signalling is essential for mesoderm formation and muscle development in zebrafish. Endocrinology 153 1288-1300
42. Pariante CM, Pearce BD, Pisell TL, Su C & Miller AH. 2001 The steroid receptor antagonist RU40555 and RU486 activate glucocorticoid receptor translocation and are not excreted by the steroid hormones transporter in L929 cells. Journal of Endocrinology 169 309-320.
43. Peeters BW, Ruigt GSF, Craighead M & Kitchener P. 2008 Differential effects of the new glucocorticoid receptor agonist ORG 34517 and RU486 (Mifepristone) on glucocorticoid receptor nuclear translocation in the AtT20 cell line. Annals of the New York Academy of Sciences 1148 536-541.
44. Pfaffl MW, Tichopad A, Prgomet C & Neuvians TP. 2004 Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnology Letters 26 509-515.
45. Phillips DIW. 2007 Programming of the stress response: a fundamental mechanism underlying the long-term effects of the fetal environment. Journal of Internal Medicine 261 453-460.
46. Phillips JE, Gersbach CA, Wojtowicz AM & Garci{dotless}́a AJ. 2006 Glucocorticoidinduced osteogenesis is negatively regulated by Runx2/Cbfa1 serine phosphorylation. Journal of Cell Science 119 581-591.
47. Pierce AL, Breves JP, Moriyama S, Hirano T & Grau EG. 2011 Differential regulation of igf1 and igf2 mRNA levels in tilapia hepatocytes: effects of insulin and cortisol on GH sensitivity. Journal of Endocrinology 211 201-210.
48. Raine JC, Cameron C, Vijayan MM, Lamarre J & Leatherland JF. 2004 The effect of elevated oocytes triiodothyronine content on development of rainbow trout embryos and the expression of mRNA encoding for thyroid hormone receptors. Journal of Fish Biology 65 206-226.
49. Reinecke M. 2010 Insulin-like growth factor and fish reproduction. Biology of Reproduction 82 656-661.
50. Sampath-Kumar R, Byers RE, Munro AD & Lam TJ. 1995 Profile of cortisol during the ontogeny of the Asian seabass, Lates calcarifer. Aquaculture 132 349-359.
51. Sathiyaa R & Vijayan MM. 2003 Autoregulation of glucocorticoid receptor by cortisol in rainbow trout hepatocytes. American Journal of Physiology. Cell Physiology 284 1508-1515.
52. Schlueter P, Peng G, Westerfield M & Duan C. 2007 Insulin-like growth factor signaling regulates zebrafish embryo growth and development by promoting cell survival and cell cycle progression. Cell Death and Differentiation 14 1095-1105.
53. Schreck CB. 2010 Stress and fish reproduction: the role of allostasis and hormoesis. General and Comparative Endocrinology 156 549-556.
54. Scott GR, Keir KR & Schulte PM. 2005 Effects of spironolactone and RU486 on gene expression and cell proliferation after freshwater transfer in the Euryhaline killifish. Journal of Comparative Physiology 175B 499-510.
55. Shiokawa K, Aso M, Kondo T, Uchiyama H, Kuroyanagi S, Takai JI, Takahashi S, Kajitani M, Kaito C, Sekimizu K et al. 2008 Gene expression in pre-MBT embryos and activation of maternally-inherited program of apoptosis to be executed at around MBTas a fail-safe mechanism in Xenopus early embryogenesis. Genetics 2 213-231.
56. Spiga F, Knight DM, Droste SK, Conway-Campbell B, Kershaw Y, Macsweeney CP, Thomson FJ, Craighead M, Peeters BWMM & Lightman SL. 2011 Differential effect of glucocorticoid receptor agonists on glucocorticoid receptor nuclear translocation and DNA binding. Journal of Psychopharmacology 25 211-221.
57. Stewart AA, Byron CR, Pondenis HC & Stewart MC. 2008 Effect of dexamethasone supplementation on chondrongenesis of equine mesenchymal stem cells. American Journal of Veterinary Research 69 1013-1021.
58. Tandros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smilbert CA & Lipshitz HD. 2007 SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Developmental Cell 12 143-155.
59. Tandros W, Houston SA, Bashirulla A, Cooperstock RL, Semotok JL, Reed BH & Lipshitz HD. 2003 Regulation of maternal transcript destabilization during egg activation in Drosophila. Genetics 164 989-1001.
60. Tandros W & Lipshitz HD. 2009 The maternal-to-zygotic transition: a play in two acts. Development 136 3033-3042.
61. Veillette PA, Serrano X, Garcia MM & Specker JL. 2007 Evidence for the onset of feedback regulation of cortisol in larval summer flounder. General and Comparative Endocrinology 154 105-110.
62. Veleiro AS, Alvarez LD, Eduardo SL & Burton G. 2010 Structure of the glucocorticoid receptor, a flexible protein that can adapt to different ligands. ChemMedChem 5 649-659.
63. Vijayan MM, Aluru N & Leatherland JF. 2010 Stress response and the role of cortisol. In: Fish Diseases and Disorders. Volume 2, Non-Infectious Disorders, 2nd edn, pp 182-201. Eds JF Leatherland & PTK Woo. New York: CABI Publishing.
64. Vijayan MM, Raptis S & Sathiuyaa R. 2003 Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. General and Comparative Endocrinology 132 256-263.
65. Vijayan MM, Reddy PK, Leatherland JF & Moon TW. 1994 The effects of cortisol on hepatocyte metabolism in rainbow trout: a study using the steroid analogue RU486. General and Comparative Endocrinology 96 75-84.
66. Vizzini A, Vazzana M, Cammarata M & Parrinello N. 2007 Peritoneal cavity phagocytes from the teleost sea bass express a glucocorticoid receptor (cloned and sequenced) involved in genomic modulation of the in vitro chemiluminescence response to zymogen. General and Comparative Endocrinology 150 114-123.
67. Wood AW, Duan C & Bern HA. 2005 Insulin-like growth factor signaling in fish. International Review of Cytology 243 215-285.
68. Yada T, Muto K, Azuma T, Hyodo S & Schreck CB. 2005 Cortisol stimulates growth hormone gene expression in rainbow trout leucocytes in vitro. General andComparative Endocrinology 142 248-255.
69. Yamaguchi T, Yoshinaga N, Yazawa T, Gen K & Kitano T. 2010 Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 151 3900-3908.
70. Zang S, Jonklaas J & Danielsen M. 2007 The glucocorticoid agonist activities of mifepristone (RU486) and progesterone are dependent on glucocorticoid receptor levels but not EC50 values. Steroids 72 600-608.