Acute stress is detrimental to heart regeneration in zebrafish

Open Biology

Volumn 6, Issue 3, 2016, Pages

  Sallin, Pauline ^a   Jaźwińska, Anna ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Anxiolytic; Cortisol; Crowding; Infarction; Myocardium; Non mammalian model

Indexed keywords

HYDROCORTISONE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ANIMAL; CARDIAC MUSCLE CELL; CELL PROLIFERATION; CYTOLOGY; GENETICS; HEART; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REGENERATION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; CELL PROLIFERATION; HEART; HUMANS; HYDROCORTISONE; INSULIN-LIKE GROWTH FACTOR I; MYOCYTES, CARDIAC; RECEPTOR, IGF TYPE 1; REGENERATION; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85013046458     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.160012     Document Type: Article

References (65)

1. O'connor TM, O'Halloran DJ, Shanahan F. 2000 The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia. QJM 93, 323-333. (doi:10.1093/Qjmed/93.6.323)
2. Charmandari E, Tsigos C, Chrousos G. 2005 Endocrinology of the stress response. Annu. Rev. Physiol. 67, 259-284. (doi:10.1146/annurev.physiol.67.040403.120816)
3. Steenbergen PJ, Richardson MK, Champagne DL. 2011 The use of the zebrafish model in stress research. Prog Neuro-Psychopharmacol. Biol. Psychiatry 35, 1432-1451. (doi:10.1016/J.Pnpbp.2010.10.010)
4. Bonga SEW. 1997 The stress response in fish. Physiol. Rev. 77, 591-625.
5. Lohr H, Hammerschmidt M. 2011 Zebrafish in endocrine systems: recent advances and implications for human disease. Annu. Rev. Physiol. 73, 183-211. (doi:10.1146/annurev-physiol-012110-142320)
6. de Kloet ER, Joels M, Holsboer F. 2005 Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475. (doi:10.1038/nrn1683)
7. Chrousos GP. 2009 Stress and disorders of the stress system. Nat. Rev. Endocrinol. 5, 374-381. (doi:10.1038/nrendo.2009.106)
8. Nakano T, Afonso LO, Beckman BR, Iwama GK, Devlin RH. 2013 Acute physiological stress down-regulates mRNA expressions of growth-related genes in coho salmon. PLoS ONE 8, e71421. (doi:10.1371/journal.pone.0071421)
9. Barton BA. 2002 Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integr. Comp. Biol. 42, 517-525. (doi:10.1093/Icb/42.3.517)
10. Kikuchi K. 2014 Advances in understanding the mechanism of zebrafish heart regeneration. Stem Cell Res. 13, 542-555. (doi:10.1016/j.scr.2014.07.003)
11. Jazwinska A, Sallin P. 2016 Regeneration versus scarring in vertebrate appendages and heart. J. Pathol. 238, 233-246. (doi:10.1002/path.4644)
12. + cardiomyocytes. Nature 464, 601-605. (doi:10.1038/nature08804)
13. Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC. 2010 Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464, 606-609. (doi:10.1038/nature08899)
14. Sallin P, de Preux Charles AS, Duruz V, Pfefferli C, Jazwinska A. 2015 A dual epimorphic and compensatory mode of heart regeneration in zebrafish. Dev. Biol. 399, 27-40. (doi:10.1016/j.ydbio.2014.12.002)
15. Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG, Poss KD. 2006 A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619. (doi:10.1016/j.cell.2006.08.052)
16. Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G, Poss KD. 2011 Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell. 20, 397-404. (doi:10.1016/j.devcel.2011.01.010)
17. Chablais F, Jazwinska A. 2012 The regenerative capacity of the zebrafish heart is dependent on TGFbeta signaling. Development 139, 1921-1930. (doi:10.1242/dev.078543)
18. Huang Y, Harrison MR, Osorio A, Kim J, Baugh A, Duan CM, Sucov HM, Lien CL. 2013 Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS ONE 8, e67266. (doi:10.1371/journal.pone.0067266)
19. Mahmoud AI, et al. 2015 Nerves regulate cardiomyocyte proliferation and heart regeneration. Dev. Cell 34, 387-399. (doi:10.1016/j.devcel.2015.06.017)
20. Cachat J, et al. 2010 Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat. Protoc. 5, 1786-1799. (doi:10.1038/nprot.2010.140)
21. Ramsay JM, Feist GW, Varga ZM, Westerfield M, Kent ML, Schreck CB. 2006 Whole-body cortisol is an indicator of crowding stress in adult zebrafish, Danio rerio. Aquaculture 258, 565-574. (doi:10.1016/J.Aquaculture.2006.04.020)
22. Kadmiel M, Cidlowski JA. 2013 Glucocorticoid receptor signaling in health and disease. Trends Pharmacol. Sci. 34, 518-530. (doi:10.1016/j.tips.2013.07.003)
23. Czock D, Keller F, Rasche FM, Haussler U. 2005 Pharmacokinetics and pharmacodynamics of systemically administered glucocorticoids. Clin. Pharmacokinet. 44, 61-98. (doi:10.2165/00003088-200544010-00003)
24. Benato F, Colletti E, Skobo T, Moro E, Colombo L, Argenton F, Dalla Valle L. 2014 A living biosensor model to dynamically trace glucocorticoid transcriptional activity during development and adult life in zebrafish. Mol. Cell. Endocrinol. 392, 60-72. (doi:10.1016/j.mce.2014.04.015)
25. Chablais F, Veit J, Rainer G, Jazwinska A. 2011 The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev. Biol. 11, 21. (doi:10.1186/1471-213X-11-21)
26. Bazhan N, Zelena D. 2013 Food-intake regulation during stress by the hypothalamo-pituitary-adrenal axis. Brain Res. Bull. 95, 46-53. (doi:10.1016/j.brainresbull.2013.04.002)
27. Gupta V, Gemberling M, Karra R, Rosenfeld GE, Evans T, Poss KD. 2013 An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr. Biol. 23, 1221-1227. (doi:10.1016/j.cub.2013.05.028)
28. Jopling C, Boue S, Izpisua Belmonte JC. 2011 Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat. Rev. Mol. Cell Biol. 12, 79-89. (doi:10.1038/nrm3043)
29. Hans F, Dimitrov S. 2001 Histone H3 phosphorylation and cell division. Oncogene 20, 3021-3027. (doi:10.1038/sj.onc.1204326)
30. Wills AA, Holdway JE, Major RJ, Poss KD. 2008 Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 135, 183-192. (doi:10.1242/dev.010363)
31. Morley SC. 2012 The actin-bundling protein L-plastin: a critical regulator of immune cell function. Int. J. Cell Biol. 2012, 935173. (doi:10.1155/2012/935173)
32. Sarkar NN. 2002 Mifepristone: bioavailability, pharmacokinetics and use-effectiveness. Eur. J. Obstet. Gynecol. Reprod. Biol. 101, 113-120. (doi:10.1016/S0301-2115(01)00522-X)
33. Fleseriu M, Biller BM, Findling JW, Molitch ME, Schteingart DE, Gross C, Seismic Study Investigators. 2012 Mifepristone, a glucocorticoid receptor antagonist, produces clinical and metabolic benefits in patients with Cushing's syndrome. J. Clin. Endocrinol. Metab. 97, 2039-2049. (doi:10.1210/jc.2011-3350)
34. Peet M. 1988 The treatment of anxiety with beta-blocking drugs. Postgrad. Med. J. 64(Suppl. 2), 45-49.
35. Granville-Grossman KL, Turner P. 1966 The effect of propranolol on anxiety. Lancet 1, 788-790. (doi:10.1016/S0140-6736(66)91863-0)
36. Griffin CEIII, Kaye AM, Bueno FR, Kaye AD. 2013 Benzodiazepine pharmacology and central nervous system-mediated effects. Ochsner J. 13, 214-223.
37. Love MI, Huber W, Anders S. 2014 Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. (doi:10.1186/PREACCEPT-8897612761307401)
38. Hwa V, Oh Y, Rosenfeld RG. 1999 The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20, 761-787. (doi:10.1210/edrv.20.6.0382)
39. Chablais F, Jazwinska A. 2010 IGF signaling between blastema and wound epidermis is required for fin regeneration. Development 137, 871-879. (doi:10.1242/dev.043885)
40. Marques IJ, Leito JT, Spaink HP, Testerink J, Jaspers RT, Witte F, van den Berg S, Bagowski CP. 2008 Transcriptome analysis of the response to chronic constant hypoxia in zebrafish hearts. J. Comp. Physiol. B 178, 77-92. (doi:10.1007/s00360-007-0201-4)
41. Maxwell MA, Muscat GE. 2006 The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl. Recept. Signal. 4, e002. (doi:10.1621/nrs.04002)
42. Wang Z, Benoit G, Liu J, Prasad S, Aarnisalo P, Liu X, Xu H, Walker NP, Perlmann T. 2003 Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423, 555-560. (doi:10.1038/nature01645)
43. Scearce LM, Laz TM, Hazel TG, Lau LF, Taub R. 1993 RNR-1, a nuclear receptor in the NGFI-B/Nur77 family that is rapidly induced in regenerating liver. J. Biol. Chem. 268, 8855-8861.
44. Hu Y, Zhan Q, Liu HX, Chau T, Li Y, Yvonne Wan YJ. 2014 Accelerated partial hepatectomy-induced liver cell proliferation is associated with liver injury in Nur77 knockout mice. Am. J. Pathol. 184, 3272-3283. (doi:10.1016/j.ajpath.2014.08.002)
45. Sousounis K, Looso M, Maki N, Ivester CJ, Braun T, Tsonis PA. 2013 Transcriptome analysis of newt lens regeneration reveals distinct gradients in gene expression patterns. PLoS ONE 8, e61445. (doi:10.1371/journal.pone.0061445)
46. Rosenfeld RG et al. 1999 The insulin-like growth factor binding protein superfamily: new perspectives. Pediatrics 104, 1018-1020.
47. Duan C, Xu Q. 2005 Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen. Comp. Endocrinol. 142, 44-52. (doi:10.1016/j.ygcen.2004.12.022)
48. Mohan S, Baylink DJ. 2002 IGF-binding proteins are multifunctional and act via IGF-dependent and -independent mechanisms. J. Endocrinol. 175, 19-31. (doi:10.1677/joe.0.1750019)
49. Li P, Cavallero S, Gu Y, Chen TH, Hughes J, Hassan AB, Bruning JC, Pashmforoush M, Sucov HM. 2011 IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development. Development 138, 1795-1805. (doi:10.1242/dev.054338)
50. Godbout JP, Glaser R. 2006 Stress-induced immune dysregulation: implications for wound healing, infectious disease and cancer. J. Neuroimmune Pharmacol. 1, 421-427. (doi:10.1007/S11481-006-9036-0)
51. Kiecolt-Glaser JK, Marucha PT, Malarkey WB, Mercado AM, Glaser R. 1995 Slowing of wound healing by psychological stress. Lancet 346, 1194-1196. (doi:10.1016/S0140-6736(95)92899-5)
52. Ren RQ, Oakley RH, Cruz-Topete D, Cidlowski JA. 2012 Dual role for glucocorticoids in cardiomyocyte hypertrophy and apoptosis. Endocrinology 153, 5346-5360. (doi:10.1210/En.2012-1563)
53. De P, Roy SG, Kar D, Bandyopadhyay A. 2011 Excess of glucocorticoid induces myocardial remodeling and alteration of calcium signaling in cardiomyocytes. J. Endocrinol. 209, 105-114. (doi:10.1530/JOE-10-0431)
54. Girod JP, Brotman DJ. 2004 Does altered glucocorticoid homeostasis increase cardiovascular risk? Cardiovasc. Res. 64, 217-226. (doi:10.1016/J.Cardiores.2004.07.006)
55. Griebel G, Holmes A. 2013 50 years of hurdles and hope in anxiolytic drug discovery. Nat. Rev. Drug Discov. 12, 667-687. (doi:10.1038/nrd4075)
56. Rottbauer W et al.2002 Reptin and pontin antagonistically regulate heart growth in zebrafish embryos. Cell 111, 661-672. (doi:10.1016/S0092-8674(02)01112-1)
57. Chi NC et al. 2008 Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biol. 6, e109. (doi:10.1371/journal.pbio.0060109)
58. Motoike T, et al. 2000 Universal GFP reporter for the study of vascular development. Genesis 28, 75-81. (doi:10.1002/1526-968X(200010)28:2〈75::AID-GENE50〉3.0.CO;2-S)
59. Chablais F, Jazwinska A. 2012 Induction of myocardial infarction in adult zebrafish using cryoinjury. J. Vis. Exp. 62, e3666. (doi:10.3791/3666)
60. Eames SC, Philipson LH, Prince VE, Kinkel MD. 2010 Blood sugar measurement in zebrafish reveals dynamics of glucose homeostasis. Zebrafish 7, 205-213. (doi:10.1089/zeb.2009.0640)
61. Pedroso GL, Hammes TO, Escobar TD, Fracasso LB, Forgiarini LF, da Silveira TR. 2012 Blood collection for biochemical analysis in adult zebrafish. J. Vis. Exp. 63, e3865. (doi:10.3791/3865)
62. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013 TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36. (doi:10.1186/Gb-2013-14-4-R36)
63. Anders S, Huber W. 2010 Differential expression analysis for sequence count data. Genome Biol. 11, R106. (doi:10.1186/Gb-2010-11-10-R106)
64. Benjamini Y, Hochberg Y. 1995 Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Met. 57, 289-300.
65. Anders S, Pyl PT, Huber W. 2015 HTSeq: a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169. (doi:10.1093/bioinformatics/btu638)