Early-life perturbations in glucocorticoid activity impacts on the structure, function and molecular composition of the adult zebrafish (Danio rerio) heart

Molecular and Cellular Endocrinology

Volumn 414, Issue , 2015, Pages 120-131

  Wilson, K S ^a   Baily, J ^a   Tucker, C S ^a   Matrone, G ^a   Vass, S ^a   Moran, C ^a   Chapman, K E ^a   Mullins, J J ^a   Kenyon, C ^a   Hadoke, P W F ^a   Denvir, M A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Development; Echocardiography; Glucocorticoids; Heart; Zebrafish

Indexed keywords

DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE; IGF1 PROTEIN, ZEBRAFISH; SOMATOMEDIN; VENTRICULAR MYOSIN; ZEBRAFISH PROTEIN;

ADULT; ADULTHOOD; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL COMPOSITION; CONTROLLED STUDY; DOPPLER ECHOCARDIOGRAPHY; EMBRYO; EMBRYO (ANATOMY); EMBRYO DEVELOPMENT; GENE EXPRESSION; HEART; HEART FUNCTION; HEART MUSCLE CELL; HEART PERFORMANCE; HEART STRUCTURE; NONHUMAN; PRIORITY JOURNAL; ZEBRA FISH; ANIMAL; CARDIAC MUSCLE CELL; DRUG EFFECTS; EMBRYO CULTURE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART FUNCTION TEST; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; DEXAMETHASONE; EMBRYO CULTURE TECHNIQUES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOCORTICOIDS; HEART; HEART FUNCTION TESTS; MYOCYTES, CARDIAC; RECEPTORS, GLUCOCORTICOID; SOMATOMEDINS; VENTRICULAR MYOSINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84938766018     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.07.025     Document Type: Article

References (42)

1. Alsop D., Vijayan M.M. Development of the corticosteroid stress axis and receptor expression in the zebrafish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:711-719.
2. Aluru N., Vijayan M.M. Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen. Comp. Endocrinol. 2009, 164:142-150.
3. Benato F., Colletti E., Skobo T., Moro E., Colombo L., Argenton F., Dalla Valle L. Aliving biosensor model to dynamically trace glucocorticoid transcriptional activity during development and adult life in zebrafish. Mol. Cell Endocrinol. 2014, 392:60-72.
4. Burns C.G., MacRae C.A. Purification of hearts from zebrafish embryos. Biotechniques 2006, 40:278-281.
5. Chen Y.H., Pai C.W., Huang S.W., Chang S.N., Lin L.Y., Chiang F.T., Lin J.L., Hwang J.J., Tsai C.T. Inactivation of myosin binding protein C homolog in zebrafish as a model for human cardiac hypertrophy and diastolic dysfunction. J.Am. Heart Assoc. 2013, 2:e000231.
6. Cruz S.A., Lin C.H., Chao P.L., Hwang P.P. Glucocorticoid receptor, but not mineralocorticoid receptor, mediates cortisol regulation of epidermal ionocyte development and ion transport in zebrafish (Danio rerio). PLoS One 2013, 8:e77997.
7. Czubryt M.P., Olson E.N. Balancing contractility and energy production: the role of myocyte enhancer factor 2 (MEF2) in cardiac hypertrophy. Recent Prog. Horm. Res. 2004, 59:105-124.
8. De Marco R.J., Groneberg A.H., Yeh C.M., Castillo Ramirez L.A., Ryu S. Optogenetic elevation of endogenous glucocorticoid level in larval zebrafish. Front. Neural Circuits 2013, 7:e00082.
9. Fischer A.H., Jacobsen K.A., Zeller R. Hematoxylin and eosin staining of tissue and cell sections: Cold Spring Harb. Protoc 2008, 10.1101/pdb.prot4986.
10. Fowden A.L., Forhead A.J. Endocrine mechanisms of intrauterine programming. Reproduction 2004, 127:515-526.
11. Griffiths B.B., Schoonheim P.J., Ziv L., Voelker L., Baier H., Gahtan E. Azebrafish model of glucocorticoid resistance shows serotonergic modulation of the stress response. Front. Behav. Neurosci. 2012, 6:68.
12. Gupta V., Gemberling M., Karra R., Rosenfeld G.E., Evans T., Poss K.D. An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr. Biol. 2013, 23:1221-1227.
13. Hillegass J.M., Villano C.M., Cooper K.R., White L.A. Matrix metalloproteinase-13 is required for zebrafish (Danio rerio) development and is a target for glucocorticoids. Toxicol. Sci. 2007, 100:168-179.
14. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:254-310.
15. Kondo M. Bone morphogenetic proteins in the early development of zebrafish. FEBS J. 2007, 274:2960-2967.
16. Matrone G., Taylor J.M., Wilson K.S., Baily J., Love G.D., Girkin J.M., Mullins J.J., Tucker C.S., Denvir M.A. Laser-targeted ablation of the zebrafish embryonic ventricle: a novel model of cardiac injury and repair. Int. J. Cardiol. 2013, 168. 3913-3019.
17. Muto A., Taylor M.R., Suzawa M., Korenbrot J.I., Baier H. Glucocorticoid receptor activity regulates light adaptation in the zebrafish retina. Front. Neural Circuits 2013, 7:145.
18. Nesan D., Kamkar M., Burrows J., Scott I.C., Marsden M., Vijayan M.M. Glucocorticoid receptor signaling is essential for mesoderm formation and muscle development in zebrafish. Endocrinology 2012, 153:1288-1300.
19. Nesan D., Vijayan M.M. Embryo exposure to elevated cortisol level leads to cardiac performance dysfunction in zebrafish. Mol. Cell Endocrinol. 2012, 363:85-91.
20. Nesan D., Vijayan M.M. Role of glucocorticoid in developmental programming: evidence from zebrafish. Gen. Comp. Endocrinol. 2013, 181:35-44.
21. Nesan D., Vijayan M.M. The transcriptomics of glucocorticoid receptor signaling in developing zebrafish. PLoS One 2013, 8:e80726.
22. Nusslein-Volhard C., Dahm R. Zebrafish: a Practical Approach Book Description 2002, Oxford University Press, USA.
23. Nyirenda M.J., Lindsay R.S., Kenyon C.J., Burchell A., Seckl J.R. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J.Clin. Invest. 1998, 101:2174-2181.
24. Ohtani T., Mano T., Hikoso S., Sakata Y., Nishio M., Takeda Y., Otsu K., Miwa T., Masuyama T., Hori M., et al. Cardiac steroidogenesis and glucocorticoid in the development of cardiac hypertrophy during the progression to heart failure. J.Hypertens. 2009, 27:1074-1083.
25. Pikulkaew S., Benato F., Celeghin A., Zucal C., Skobo T., Colombo L., Dalla Valle L. The knockdown of maternal glucocorticoid receptor mRNA alters embryo development in zebrafish. Dev. Dyn. 2011, 240:874-889.
26. Quax R.A., Manenschijn L., Koper J.W., Hazes J.M., Lamberts S.W., van Rossum E.F., Feelders R.A. Glucocorticoid sensitivity in health and disease. Nat. Rev. Endocrinol. 2013, 9:670-686.
27. Ren R., Oakley R.H., Cruz-Topete D., Cidlowski J.A. Dual role for glucocorticoids in cardiomyocyte hypertrophy and apoptosis. Endocrinology 2012, 153:5346-5360.
28. Richardson R., Rog-Zielinska E., Thomson A., Moran C., Kenyon C., Gray G., Chapman K. Glucocorticoid receptor deficiency in cardiomyocytes causes pathological cardiac remodelling in mice: Presented at Society for Endocrinology BES 2013, Harrogate, UK,. Endocrine Abstracts 31 2013, OC4.1.
29. Rog-Zielinska E.A., Kenyon C.J., Holmes M.C., Chapman K.E. Maturational effects of glucocorticoids on fetal cardiomyocytes are direct and mediated by glucocorticoid receptor. Endocrinol. Abstr. 2012, 28:136.
30. Sabaliauskas N.A., Foutz C.A., Mest J.R., Budgeon L.R., Sidor A.T., Gershenson J.A., Joshi S.B., Cheng K.C. High-throughput zebrafish histology. Methods 2006, 39:246-254.
31. Sainte-Marie Y., Cat A.N.D., Perrier R., Mangin L., Soukaseum C., Peuchmaur M., Tronche F., Farman N., Escoubet B., Beritah J.-P., et al. Conditional glucocorticoid receptor expression in the heart induces atrio-ventricular block. FASEB J. 2007, 3133-3141.
32. Schoonheim P.J., Chatzopoulou A., Schaaf M.J.M. The zebrafish as an invivo model system for glucocorticoid resistance. Steroids 2010, 75:918-925.
33. Seckl J.R., Meaney M.J. Glucocorticoid programming. Ann. N. Y. Acad. Sci. 2004, 1032:63-84.
34. Speksnijder N., Christensen K.V., Didriksen M., De Kloet E.R., Datson N.A. Glucocorticoid receptor and myocyte enhancer factor 2 cooperate to regulate the expression of c-JUN in a neuronal context. J.Mol. Neurosci. 2012, 48:209-218.
35. Stellato C. Post-transcriptional and nongenomic effects of glucocorticoids. Proc. Am. Thorac. Soc. 2004, 1:255-263.
36. Schaff M.J.M., Champagne D., van Lannen I.H.C., van Wijk D.C.W.A., Meijer A.H., Meijer O.C., Spaink H.P., Richardson M.K. Discovery of a functional glucocorticoid receptor B-isoform in zebrafish. Endocrinology 2008, 149(4):1591-1599.
37. Tokarz J., Möller G., Hrabe de Angelis M., Adamski J. Zebrafish and steroids: what do we know and what do we need to know?. J.Steroid Biochem. Mol. Biol. 2013, 137:165-173.
38. Wada R., Muraoka N., Inagawa K., Yamakawa H., Miyamoto K., Sadahiro T., Umei T., Kaneda R., Suzuki T., Kamiya K., et al. Induction of human cardiomyocyte-like cells from fibroblasts by defined factors. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:12667-12672.
39. Walker B.R. Glucocorticoids and cardiovascular disease. Eur. J. Endocrinol. 2007, 157:545-559.
40. Wilson K.S., Matrone G., Livingstone D.E.W., Al-Dujaili E.A.S., Mullins J.J., Tucker C.S., Hadoke P.w.F., Kenyon C.J., Denvir M.A. Physiological roles of glucocorticoids during early embryonic development of the zebrafish (Danio rerio). J.Physiol. 2013, 591:6209-6220.
41. Wu H.H.T., Brennan C., Ashworth R. Ryanodine receptors, a family of intracellular calcium ion channels, are expressed throughoutearly vertebrate development. BMC Res. Notes 2011, 4:541-549.
42. Yu Z., Kong J., Pan B., Sun H., Lv T., Zhu J., Huang G., Tian J. Islet-1 may function as an assistant factor for histone acetylation and regulation of cardiac development-related transcription factor Mef2c expression. PLoS One 2013, 8:e77690.