Role of glucocorticoid in developmental programming: evidence from zebrafish.

The vertebrate corticosteroid stress response is highly conserved and a key function is to restore homeostasis by mobilizing and reallocating energy stores. This process is primarily initiated by activation of the hypothalamus-pituitary-adrenal axis, leading to the release of corticosteroids into the circulation. In teleosts, cortisol is the primary corticosteroid that is released into the circulation in response to stress. This steroid activates corticosteroid receptors that are ligand-bound transcription factors, modulating downstream gene expression in target tissues. Recent research in zebrafish (Danio rerio) has identified novel roles for cortisol in early developmental processes, including organogenesis and mesoderm formation. As cortisol biosynthesis commences only around the time of hatch in teleosts, the early developmental events are orchestrated by cortisol that is maternally deposited prior to fertilization. This review will highlight the molecular events leading to the development of the corticosteroid stress axis, and the possible role of cortisol in the developmental programming of stress axis function. Use of zebrafish as a model may lead to significant insights into the conserved role of glucocorticoids during early development with potential implications in biomedical research, including fetal stress syndromes in humans.

[1]  K. Sloman Exposure of ova to cortisol pre-fertilisation affects subsequent behaviour and physiology of brown trout , 2010, Hormones and Behavior.

[2]  H. Delemarre-van de Waal,et al.  Glucocorticoids and lung development in the fetus and preterm infant , 2001, Pediatric pulmonology.

[3]  J. Cidlowski,et al.  Regulation of gene expression by glucocorticoids. , 1989, Annual review of physiology.

[4]  K. Cooper,et al.  Glucocorticoids alter craniofacial development and increase expression and activity of matrix metalloproteinases in developing zebrafish (Danio rerio). , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[5]  M. Barresi,et al.  Multiple roles for Hedgehog signaling in zebrafish pituitary development. , 2003, Developmental biology.

[6]  P. Fuller,et al.  Mineralocorticoid receptor binding, structure and function , 2004, Molecular and Cellular Endocrinology.

[7]  N. Youngson,et al.  Transgenerational epigenetic effects. , 2008, Annual review of genomics and human genetics.

[8]  D. Wheeler,et al.  Zebrafish dax1 is required for development of the interrenal organ, the adrenal cortex equivalent. , 2006, Molecular endocrinology.

[9]  J. Steffensen,et al.  Effects of maternal stress coping style on offspring characteristics in rainbow trout (Oncorhynchus mykiss) , 2011, Hormones and Behavior.

[10]  J. Wozney,et al.  Differential effects and glucocorticoid potentiation of bone morphogenetic protein action during rat osteoblast differentiation in vitro. , 1996, Endocrinology.

[11]  S. Levine Primary social relationships influence the development of the hypothalamic–pituitary–adrenal axis in the rat , 2001, Physiology & Behavior.

[12]  N. Bury,et al.  Evolution of the corticosteroid receptor signalling pathway in fish. , 2007, General and comparative endocrinology.

[13]  Z. Lele,et al.  The zebrafish as a model system in developmental, toxicological and transgenic research. , 1996, Biotechnology advances.

[14]  M. Vijayan,et al.  Hepatic transcriptome response to glucocorticoid receptor activation in rainbow trout. , 2007, Physiological genomics.

[15]  J. Grimm,et al.  Specification of hypothalamic neurons by dual regulation of the homeodomain protein Orthopedia , 2007, Development.

[16]  D. DeFranco,et al.  Glucocorticoid receptor physiology , 2007, Reviews in Endocrine and Metabolic Disorders.

[17]  S. Chapman,et al.  A three‐dimensional atlas of pituitary gland development in the zebrafish , 2005, The Journal of comparative neurology.

[18]  D. Bureau,et al.  The actions of in ovo cortisol on egg fertility, embryo development and the expression of growth‐related genes in rainbow trout embryos, and the growth performance of juveniles , 2010, Molecular reproduction and development.

[19]  M. Bakken,et al.  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 , 2007 .

[20]  V. Laudet,et al.  Unexpected Novel Relational Links Uncovered by Extensive Developmental Profiling of Nuclear Receptor Expression , 2007, PLoS genetics.

[21]  G. Chrousos,et al.  The role of stress in female reproduction and pregnancy: an update , 2010, Annals of the New York Academy of Sciences.

[22]  R. Peter,et al.  The hypothalamic-pituitary-interrenal axis and the control of food intake in teleost fish. , 2001, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[23]  D. Reeder,et al.  STRESS IN FREE-RANGING MAMMALS: INTEGRATING PHYSIOLOGY, ECOLOGY, AND NATURAL HISTORY , 2005 .

[24]  R. Pierce,et al.  Glucocorticoids upregulate tropoelastin expression during late stages of fetal lung development. , 1995, The American journal of physiology.

[25]  I. V. Nechaev,et al.  Dynamics of cortisol and the development of the glucocorticoid function in the early ontogenesis of Atlantic salmon Salmo salar , 2006, Journal of Ichthyology.

[26]  J. Komen,et al.  THE EFFECTS OF CHRONIC STRESS ON GROWTH IN FISH : A CRITICAL APPRAISAL , 1998 .

[27]  O. Vuolteenaho,et al.  Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. , 2002, Endocrinology.

[28]  J. Eisen,et al.  Headwaters of the zebrafish — emergence of a new model vertebrate , 2002, Nature Reviews Genetics.

[29]  J. Funder Glucocorticoid and mineralocorticoid receptors: biology and clinical relevance. , 1997, Annual review of medicine.

[30]  T. Dinan,et al.  Growth hormone secretion: the role of glucocorticoids. , 1994, Life sciences.

[31]  L. Hess Corticosteroid synthesis and metabolism in birds , 2002 .

[32]  P. Hwang,et al.  Role of cortisol in hypoosmoregulation in larvae of the tilapia (Oreochromis mossambicus). , 1993, General and comparative endocrinology.

[33]  C. Tsigos,et al.  Stress hormones: physiological stress and regulation of metabolism. , 2009, Current opinion in pharmacology.

[34]  A. Gutnick,et al.  Development of the zebrafish hypothalamus , 2011, Annals of the New York Academy of Sciences.

[35]  C. Foltzer-Jourdainne,et al.  Cytokine gene expression during postnatal small intestinal development: regulation by glucocorticoids , 2000, Gut.

[36]  F. Shanahan,et al.  The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia. , 2000, QJM : monthly journal of the Association of Physicians.

[37]  H. Spaink,et al.  The zebrafish as a model system for glucocorticoid receptor research. , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[38]  P. Czernichow,et al.  Dissecting the role of glucocorticoids on pancreas development. , 2004, Diabetes.

[39]  B. Walker Glucocorticoids and cardiovascular disease. , 2007, European journal of endocrinology.

[40]  J. Clobert,et al.  Increased pre‐natal maternal corticosterone promotes philopatry of offspring in common lizards Lacerta vivipara , 2000 .

[41]  D. Godfrey,et al.  GRKO mice express an aberrant dexamethasone-binding glucocorticoid receptor, but are profoundly glucocorticoid resistant , 2001, Molecular and Cellular Endocrinology.

[42]  S. Dunlop,et al.  Repeated prenatal corticosteroid administration delays astrocyte and capillary tight junction maturation in fetal sheep , 2001, International Journal of Developmental Neuroscience.

[43]  Douglas W DeSimone,et al.  The extracellular matrix in development and morphogenesis: a dynamic view. , 2010, Developmental biology.

[44]  H. Wada,et al.  Glucocorticoids: mediators of vertebrate ontogenetic transitions. , 2008, General and comparative endocrinology.

[45]  G. Chrousos,et al.  Glucocorticoid receptor beta, a potential endogenous inhibitor of glucocorticoid action in humans. , 1995, The Journal of clinical investigation.

[46]  E. R. Kloet,et al.  The postnatal development of the hypothalamic–pituitary–adrenal axis in the mouse , 2003, International Journal of Developmental Neuroscience.

[47]  T. Hirano,et al.  Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys olivaceus. , 1991, General and comparative endocrinology.

[48]  G. Litwack,et al.  Activation of the glucocorticoid-receptor complex. , 1982, Physiological reviews.

[49]  J. Fetcho,et al.  Using imaging and genetics in zebrafish to study developing spinal circuits in vivo , 2008, Developmental neurobiology.

[50]  S. Perry,et al.  Cortisol regulates Na+ uptake in zebrafish, Danio rerio, larvae via the glucocorticoid receptor , 2012, Molecular and Cellular Endocrinology.

[51]  G. Chrousos,et al.  Stressors, Stress, and Neuroendocrine Integration of the Adaptive Response: The 1997 Hans Selye Memorial Lecture , 1998, Annals of the New York Academy of Sciences.

[52]  H. S. Siegel Physiological Stress in Birds , 1980 .

[53]  M. Westerfield,et al.  pitx3 defines an equivalence domain for lens and anterior pituitary placode , 2005, Development.

[54]  B. Barton Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids1 , 2002, Integrative and comparative biology.

[55]  Karen M. Moritz,et al.  Glucocorticoid programming of adult disease , 2005, Cell and Tissue Research.

[56]  T. Lints,et al.  Cooperation of BMP7 and SHH in the Induction of Forebrain Ventral Midline Cells by Prechordal Mesoderm , 1997, Cell.

[57]  R. Shine,et al.  Can pregnant lizards adjust their offspring phenotypes to environmental conditions? , 1999, Oecologia.

[58]  H. Hsu,et al.  Parallel early development of zebrafish interrenal glands and pronephros: differential control by wt1 and ff1b , 2003, Development.

[59]  C. H. Summers,et al.  Glucocorticoid interaction with aggression in non-mammalian vertebrates: reciprocal action. , 2005, European journal of pharmacology.

[60]  G. Levkowitz,et al.  High resolution fate map of the zebrafish diencephalon , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[61]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[62]  H. Schwarz,et al.  Eya1 is required for lineage-specific differentiation, but not for cell survival in the zebrafish adenohypophysis. , 2006, Developmental biology.

[63]  M. Hammerschmidt,et al.  How to make a teleost adenohypophysis: Molecular pathways of pituitary development in zebrafish , 2009, Molecular and Cellular Endocrinology.

[64]  J. Cidlowski,et al.  The glucocorticoid receptor: coding a diversity of proteins and responses through a single gene. , 2002, Molecular endocrinology.

[65]  M. Hammerschmidt,et al.  Zebrafish in endocrine systems: recent advances and implications for human disease. , 2011, Annual review of physiology.

[66]  I. Dawid,et al.  Neuronal and neuroendocrine expression of lim3, a LIM class homeobox gene, is altered in mutant zebrafish with axial signaling defects. , 1997, Developmental biology.

[67]  G. Chrousos,et al.  The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. , 1992, JAMA.

[68]  T. J. Lam,et al.  Profile of cortisol during the ontogeny of the Asian seabass, Lates calcarifer , 1995 .

[69]  Dopaminergic neuronal cluster size is determined during early forebrain patterning , 2008, Development.

[70]  J. Seckl,et al.  Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour , 2001, Neuroscience.

[71]  C. Schreck,et al.  Ontogeny of the stress response in chinook salmon, Oncorhynchus tshawytscha* , 2001, Fish Physiology and Biochemistry.

[72]  J. B. Thomas,et al.  Physiological Causes and Consequences of Social Status in Salmonid Fish1 , 2005, Integrative and comparative biology.

[73]  C. Schreck,et al.  Effects of stress on fish reproduction, gamete quality, and progeny , 2001 .

[74]  W. Chan,et al.  Prox1 Is a Novel Coregulator of Ff1b and Is Involved in the Embryonic Development of the Zebra Fish Interrenal Primordium , 2003, Molecular and Cellular Biology.

[75]  I. Weaver Epigenetic effects of glucocorticoids. , 2009, Seminars in fetal & neonatal medicine.

[76]  F. Holsboer,et al.  Stress and the brain: from adaptation to disease , 2005, Nature Reviews Neuroscience.

[77]  J. López-Olmeda,et al.  Cortisol and finfish welfare , 2011, Fish Physiology and Biochemistry.

[78]  A. Schier,et al.  Zebrafish: genetic tools for studying vertebrate development. , 1994, Trends in genetics : TIG.

[79]  J. Funder,et al.  Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. , 1988, Science.

[80]  A. E. Fortunato,et al.  A peek inside the neurosecretory brain through Orthopedia lenses , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[81]  R. Ballard,et al.  Cytoplasmic receptor for glucocorticoids in lung of the human fetus and neonate. , 1974, The Journal of clinical investigation.

[82]  M. Wullimann,et al.  Anatomy of neurogenesis in the early zebrafish brain. , 2003, Brain research. Developmental brain research.

[83]  J. Cidlowski,et al.  The human glucocorticoid receptor: One gene, multiple proteins and diverse responses , 2005, Steroids.

[84]  Yan A. Su,et al.  Glucocorticoid receptor (GR) beta has intrinsic, GRalpha-independent transcriptional activity. , 2009, Biochemical and biophysical research communications.

[85]  D. Stainier,et al.  Bmp2 signaling regulates the hepatic versus pancreatic fate decision. , 2008, Developmental cell.

[86]  K. Godfrey,et al.  Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications , 2007, British Journal of Nutrition.

[87]  N. Greenberg Behavioral endocrinology of physiological stress in a lizard , 1990 .

[88]  K. Cooper,et al.  Matrix metalloproteinase-13 is required for zebra fish (Danio rerio) development and is a target for glucocorticoids. , 2007, Toxicological sciences : an official journal of the Society of Toxicology.

[89]  L. Rollins‐Smith Neuroendocrine-immune system interactions in amphibians , 2001, Immunologic research.

[90]  V. Rehan Antenatal steroids: Miracle drug for preemies , 1996, Indian journal of pediatrics.

[91]  C. Tsigos,et al.  Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. , 2002, Journal of psychosomatic research.

[92]  P. Prunet,et al.  Multiple corticosteroid receptors in fish: from old ideas to new concepts. , 2006, General and comparative endocrinology.

[93]  N. Ueno,et al.  Conservation of BMP signaling in zebrafish mesoderm patterning , 1997, Mechanisms of Development.

[94]  M. Wullimann,et al.  Atlas of Early Zebrafish Brain Development: A Tool for Molecular Neurogenetics , 2005 .

[95]  S. Harvey,et al.  Hormones and stress in birds: activation of the hypothalamo-pituitary-adrenal axis. , 1990, Progress in clinical and biological research.

[96]  H. Roehl,et al.  Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis , 2004, Development.

[97]  T. Pottinger,et al.  Stress Responsiveness Affects Dominant–Subordinate Relationships in Rainbow Trout , 2001, Hormones and Behavior.

[98]  C. Franceschi,et al.  The neuroimmunology of stress from invertebrates to man , 1996, Progress in Neurobiology.

[99]  C. H. Summers,et al.  Social Interaction Over Time, Implications for Stress Responsiveness1 , 2002, Integrative and comparative biology.

[100]  Evangelia Charmandari,et al.  Endocrinology of the stress response. , 2005, Annual review of physiology.

[101]  A. Look,et al.  Zebrafish as a model for myelopoiesis during embryogenesis. , 2005, Experimental hematology.

[102]  W. Vale,et al.  The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress , 2006, Dialogues in clinical neuroscience.

[103]  E. Borell,et al.  Stress, behaviour and reproductive performance in female cattle and pigs , 2007, Hormones and Behavior.

[104]  Stephen G. Matthews,et al.  Early programming of the hypothalamo–pituitary–adrenal axis , 2002, Trends in Endocrinology & Metabolism.

[105]  V. Korzh,et al.  New ways to admire zebrafish: progress in functional genomics research methodology. , 2005, BioTechniques.

[106]  Lynn B. Martin,et al.  STRESS HORMONES IN TROPICAL BIRDS: PATTERNS AND FUTURE DIRECTIONS , 2008 .

[107]  M. Suematsu,et al.  Development of functional zonation in the rat adrenal cortex. , 1999, Endocrinology.

[108]  A. Ward,et al.  Characterization of the zebrafish matrix metalloproteinase 9 gene and its developmental expression pattern. , 2007, Gene expression patterns : GEP.

[109]  G. Chrousos,et al.  The human glucocorticoid receptor: Molecular basis of biologic function , 2010, Steroids.

[110]  I. Clarke,et al.  Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. , 2000, Reviews of reproduction.

[111]  J. Wingfield,et al.  Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. , 2004, General and comparative endocrinology.

[112]  R. Jaffe,et al.  Development and function of the human fetal adrenal cortex: a key component in the feto-placental unit. , 2011, Endocrine reviews.

[113]  E. Donaldson,et al.  Stress induced elevation of plasma cortisol in adult female coho salmon (Oncorhynchus kisutch), is reflected in egg cortisol content, but does not appear to affect early development , 1997 .

[114]  C. Schreck,et al.  Stress and fish reproduction: the roles of allostasis and hormesis. , 2010, General and comparative endocrinology.

[115]  M. Tetsuka Actions of glucocorticoid and their regulatory mechanisms in the ovary , 2007 .

[116]  David A Padgett,et al.  How stress influences the immune response. , 2003, Trends in immunology.

[117]  I. Adcock,et al.  Glucocorticoid-regulated transcription factors. , 2001, Pulmonary pharmacology & therapeutics.

[118]  C. Suski,et al.  Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring , 2011, Proceedings of the Royal Society B: Biological Sciences.

[119]  A. Metz,et al.  Stress--mechanisms of immunosuppression. , 1991, Veterinary immunology and immunopathology.

[120]  L. Zon,et al.  Zebrafish: a model system for the study of human disease. , 2000, Current opinion in genetics & development.

[121]  P. Sangild,et al.  Developmental Regulation of the Porcine Exocrine Pancreas by Glucocorticoids , 1994, Journal of pediatric gastroenterology and nutrition.

[122]  J. Segar,et al.  Effects of cortisol on cardiac myocytes and on expression of cardiac genes in fetal sheep. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[123]  T. Porter,et al.  Ontogeny of the hypothalamo-pituitary-adrenocortical axis in the chicken embryo: a review. , 2004, Domestic animal endocrinology.

[124]  M. Moisan,et al.  Molecular genetics of hypothalamic–pituitary–adrenal axis activity and function , 2011, Annals of the New York Academy of Sciences.

[125]  M. Dubois,et al.  Ontogenesis of cells producing polypeptide hormones (ACTH, MSH, LPH, GH, Prolactin) in the fetal hypophysis of the rat: Influence of the hypothalamus , 1979, Cell and Tissue Research.

[126]  S. W. Wendelaar Bonga,et al.  Stress responsiveness of the pituitary-interrenal axis during early life stages of common carp (Cyprinus carpio). , 1998, The Journal of endocrinology.

[127]  M. Marsden,et al.  Glucocorticoid receptor signaling is essential for mesoderm formation and muscle development in zebrafish. , 2012, Endocrinology.

[128]  A. Meijer,et al.  Discovery of a functional glucocorticoid receptor beta-isoform in zebrafish. , 2008, Endocrinology.

[129]  K. Gilmour Mineralocorticoid receptors and hormones: fishing for answers. , 2005, Endocrinology.

[130]  M. Vijayan,et al.  Molecular programming of the corticosteroid stress axis during zebrafish development. , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[131]  J. Funder Mineralocorticoids, glucocorticoids, receptors and response elements. , 1993, Science.

[132]  J. Wingfield,et al.  Reproduction and Resistance to Stress: When and How , 2003, Journal of neuroendocrinology.

[133]  George P. Chrousos,et al.  Mechanisms of stress: A dynamic overview of hormonal and behavioral homeostasis , 1992, Neuroscience & Biobehavioral Reviews.

[134]  J. Leatherland,et al.  Stressors, glucocorticoids and ovarian function in teleosts. , 2010, Journal of fish biology.

[135]  M. Vijayan,et al.  Embryo exposure to elevated cortisol level leads to cardiac performance dysfunction in zebrafish , 2012, Molecular and Cellular Endocrinology.

[136]  M. Vijayan,et al.  Development of the corticosteroid stress axis and receptor expression in zebrafish. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[137]  B. Walderich,et al.  Genetic analysis of adenohypophysis formation in zebrafish. , 2004, Molecular endocrinology.

[138]  S. E. Bonga The stress response in fish , 1997 .

[139]  S. Hahner,et al.  Pituitary-interrenal interaction in zebrafish interrenal organ development. , 2007, Molecular endocrinology.

[140]  J. Malison,et al.  Ontogeny of the cortisol stress response in larval rainbow trout. , 1995, General and comparative endocrinology.

[141]  H. Segner Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption. , 2009, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[142]  P. Ballard,et al.  Ontogeny of tracheal fluid, pulmonary surfactant, and plasma corticoids in the fetal lamb. , 1975 .

[143]  R. Denver Endocrinology of Complex Life Cycles: Amphibians , 2002 .

[144]  S. Dunlop,et al.  Effect of corticosteroids on brain growth in fetal sheep. , 1999, Obstetrics and gynecology.

[145]  B. Walker,et al.  Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[146]  M. Dallman,et al.  Stress, Feedback and Facilitation in the Hypothalamo‐Pituitary‐Adrenal Axis , 1992, Journal of neuroendocrinology.

[147]  T. Lufkin,et al.  The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. , 2000, Developmental biology.

[148]  Ji Eun Lee,et al.  Canonical Wnt signaling through Lef1 is required for hypothalamic neurogenesis , 2006, Development.

[149]  A. Addink,et al.  The effects of cortisol administration on intermediary metabolism in teleost fish , 1991 .

[150]  G. Liggins,et al.  The role of cortisol in preparing the fetus for birth. , 1994, Reproduction, fertility, and development.

[151]  L. Tort,et al.  The Endocrine Response to Stress - A Comparative View , 2011 .

[152]  Gert Flik,et al.  Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish , 1999 .

[153]  A. Majumdar,et al.  Influence of glucocorticoids on prenatal development of the gut and pancreas in rats. , 1985, Scandinavian journal of gastroenterology.

[154]  N. W. Pankhurst,et al.  The endocrinology of stress in fish: an environmental perspective. , 2011, General and comparative endocrinology.

[155]  J. Eddy,et al.  Glucocorticoid dysregulation of natural killer cell function through epigenetic modification , 2011, Brain, Behavior, and Immunity.

[156]  M. McCormick BEHAVIORALLY INDUCED MATERNAL STRESS IN A FISH INFLUENCES PROGENY QUALITY BY A HORMONAL MECHANISM , 1998 .

[157]  M. McCormick Experimental test of the effect of maternal hormones on larval quality of a coral reef fish , 1999, Oecologia.

[158]  R. Denver Structural and Functional Evolution of Vertebrate Neuroendocrine Stress Systems , 2009, Annals of the New York Academy of Sciences.

[159]  S. Ekker,et al.  Effective targeted gene ‘knockdown’ in zebrafish , 2000, Nature Genetics.

[160]  S. Rhodes,et al.  Transcriptional control during mammalian anterior pituitary development. , 2003, Gene.

[161]  T. W. Moon,et al.  Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation , 1999, Reviews in Fish Biology and Fisheries.

[162]  C. Kimmel,et al.  Genetics and early development of zebrafish. , 1989, Trends in genetics : TIG.

[163]  J. Cidlowski,et al.  Mouse Glucocorticoid Receptor Phosphorylation Status Influences Multiple Functions of the Receptor Protein* , 1997, The Journal of Biological Chemistry.

[164]  Lance Va Stress in reptiles. , 1990 .

[165]  P. Schoonheim,et al.  The zebrafish as an in vivo model system for glucocorticoid resistance , 2010, Steroids.

[166]  Michael Papsdorf,et al.  Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses , 2008, Epigenetics.

[167]  M. Fishman,et al.  Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. , 1996, Development.

[168]  R. Boonstra EQUIPPED FOR LIFE: THE ADAPTIVE ROLE OF THE STRESS AXIS IN MALE MAMMALS , 2005 .

[169]  Stephen W. Wilson,et al.  Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by the conserved zinc finger protein Tof/Fezl. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[170]  H. Schwarz,et al.  The proneural gene ascl1a is required for endocrine differentiation and cell survival in the zebrafish adenohypophysis , 2006, Development.

[171]  L. Colombo,et al.  Expression analysis of steroid hormone receptor mRNAs during zebrafish embryogenesis. , 2010, General and comparative endocrinology.

[172]  A. Celeghin,et al.  The knockdown of maternal glucocorticoid receptor mRNA alters embryo development in zebrafish , 2011, Developmental dynamics : an official publication of the American Association of Anatomists.

[173]  C. Chai,et al.  Ff1b is required for the development of steroidogenic component of the zebrafish interrenal organ. , 2003, Developmental biology.

[174]  G. Stein,et al.  Glucocorticoids promote development of the osteoblast phenotype by selectively modulating expression of cell growth and differentiation associated genes , 1992, Journal of cellular biochemistry.

[175]  M. Vijayan,et al.  Stress transcriptomics in fish: a role for genomic cortisol signaling. , 2009, General and comparative endocrinology.

[176]  Yi-Wen Liu Interrenal Organogenesis in the Zebrafish Model , 2007, Organogenesis.

[177]  Wiebke Herzog,et al.  Pituitary corticotroph ontogeny and regulation in transgenic zebrafish. , 2003, Molecular endocrinology.

[178]  M. Langdown,et al.  Effects of prenatal glucocorticoid exposure on cardiac calreticulin and calsequestrin protein expression during early development and in adulthood. , 2003, The Biochemical journal.

[179]  L. Tort Stress and immune modulation in fish. , 2011, Developmental and comparative immunology.

[180]  N. Bernier,et al.  Ontogeny of the corticotropin-releasing factor system in zebrafish. , 2009, General and comparative endocrinology.

[181]  J. Herman,et al.  Differential expression of corticotropin-releasing hormone in developing mouse embryos and adult brain. , 1994, Endocrinology.

[182]  T. Baram,et al.  Ontogeny of corticotropin releasing hormone gene expression in rat hypothalamus — comparison with somatostatin , 1991, International Journal of Developmental Neuroscience.

[183]  P. Balm,et al.  Ontogeny of corticotropin-releasing factor and of hypothalamic-pituitary-interrenal axis responsiveness to stress in tilapia (Oreochromis mossambicus; Teleostei). , 2004, General and comparative endocrinology.

[184]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[185]  S. McCormick Endocrine Control of Osmoregulation in Teleost Fish1 , 2001 .

[186]  J. Malison,et al.  Ontogeny of the cortisol stress response in yellow perch (Perca flavescens) , 2002, Fish Physiology and Biochemistry.

[187]  J. Specker,et al.  Cortisol is necessary for seawater tolerance in larvae of a marine teleost the summer flounder. , 2007, General and comparative endocrinology.

[188]  P. Prunet,et al.  Functional Genomics of Stress Responses in Fish , 2008 .

[189]  ICV CRF and isolation stress differentially enhance plasma corticosterone concentrations in layer- and meat-type neonatal chicks. , 2005, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[190]  Z. Lele,et al.  Adenohypophysis formation in the zebrafish and its dependence on sonic hedgehog. , 2003, Developmental biology.

[191]  S. Mandiki,et al.  Corticosteroids: Friends or foes of teleost fish reproduction? , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[192]  M. Yasui,et al.  Glucocorticoids regulate the transcription of Na(+)-K(+)-ATPase genes in the infant rat kidney. , 1994, The American journal of physiology.

[193]  M. Hammerschmidt,et al.  Molecular genetics of pituitary development in zebrafish. , 2007, Seminars in cell & developmental biology.

[194]  Kaiping Yang,et al.  Placental 11 beta-hydroxysteroid dehydrogenase: barrier to maternal glucocorticoids. , 1997, Reviews of reproduction.

[195]  Peter Aleström,et al.  Zebrafish in functional genomics and aquatic biomedicine. , 2006, Trends in biotechnology.

[196]  A. Meyer,et al.  From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[197]  C. H. Summers,et al.  Stress coping style predicts aggression and social dominance in rainbow trout , 2004, Hormones and Behavior.

[198]  G. Chrousos The Hpa Axis and the Stress Response , 2000, Endocrine research.

[199]  Michael J Meaney,et al.  Epigenetics and the environmental regulation of the genome and its function. , 2010, Annual review of psychology.

[200]  R. Moots,et al.  Corticosteroids: do they damage the cardiovascular system? , 1994, Postgraduate medical journal.

[201]  M. Sarras,et al.  The expression of gelatinase A (MMP-2) is required for normal development of zebrafish embryos , 2003, Development Genes and Evolution.

[202]  O. Wolkowitz,et al.  Glucocorticoids. Mood, memory, and mechanisms. , 2009, Annals of the New York Academy of Sciences.

[203]  P. Prunet,et al.  Chapter 13 Xenobiotic impact on corticosteroid signaling , 2005 .

[204]  Stephen W. Wilson,et al.  Distinct and cooperative roles for Nodal and Hedgehog signals during hypothalamic development. , 2002, Development.

[205]  Gustavo Turecki,et al.  Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse , 2009, Nature Neuroscience.

[206]  J. Seckl Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms , 2001, Molecular and Cellular Endocrinology.

[207]  J. Cidlowski,et al.  Molecular mechanisms of glucocorticoid action and resistance , 2002, The Journal of Steroid Biochemistry and Molecular Biology.

[208]  W. Lamers,et al.  Mechanisms of glucocorticoid signalling. , 2004, Biochimica et biophysica acta.

[209]  J. Seckl,et al.  Prenatal Stress, Glucocorticoids and the Programming of the Brain , 2001, Journal of neuroendocrinology.

[210]  G. Nica,et al.  Zebrafish pit1 mutants lack three pituitary cell types and develop severe dwarfism. , 2004, Molecular endocrinology.

[211]  X. Nie,et al.  BMP signalling in craniofacial development. , 2006, The International journal of developmental biology.

[212]  R. Rasooly,et al.  Genetic and genomic tools for zebrafish research: The NIH zebrafish initiative , 2003, Developmental Dynamics.

[213]  C. Nüsslein-Volhard,et al.  Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. , 1997, Development.

[214]  W. Rutter,et al.  Glucocorticoids modulate the in vitro development of the embryonic rat pancreas , 1977, The Journal of cell biology.

[215]  G. Chrousos,et al.  Glucocorticoids and Their Actions: An Introduction , 2004, Annals of the New York Academy of Sciences.

[216]  N. Andreakis,et al.  Differential regulation of the zebrafish orthopedia1 gene during fate determination of diencephalic neurons , 2006, BMC Developmental Biology.

[217]  Q. Nie,et al.  Myocardin Expression Is Regulated by Nkx2.5, and Its Function Is Required for Cardiomyogenesis , 2003, Molecular and Cellular Biology.

[218]  G. Akusjärvi,et al.  Sensitive Periods for Glucocorticoids' Regulation of Na+,K+-ATPase mRNA in the Developing Lung and Kidney , 1993, Pediatric Research.

[219]  S. Potter,et al.  Multistep control of pituitary organogenesis. , 1997, Science.

[220]  I. Moore,et al.  Stress, reproduction, and adrenocortical modulation in amphibians and reptiles , 2003, Hormones and Behavior.

[221]  M. Bauer,et al.  Stress, glucocorticoids and ageing of the immune system , 2005, Stress.