Linking physiological and cellular responses to thermal stress: β-adrenergic blockade reduces the heat shock response in fish.

Nicole M Templeman, Sacha LeBlanc, Steve F Perry, Suzanne Currie
Author Information
  1. Nicole M Templeman: Department of Biology, Mount Allison University, 63B York Street, Sackville, NB, E4L 1G7, Canada.

Abstract

When faced with stress, animals use physiological and cellular strategies to preserve homeostasis. We were interested in how these high-level stress responses are integrated at the level of the whole animal. Here, we investigated the capacity of the physiological stress response, and specifically the β-adrenergic response, to affect the induction of the cellular heat shock proteins, HSPs, following a thermal stress in vivo. We predicted that blocking β-adrenergic stimulation during an acute heat stress in the whole animal would result in reduced levels of HSPs in red blood cells (RBCs) of rainbow trout compared to animals where adrenergic signaling remained intact. We first determined that a 1 h heat shock at 25 °C in trout acclimated to 13 °C resulted in RBC adrenergic stimulation as determined by a significant increase in cell swelling, a hallmark of the β-adrenergic response. A whole animal injection with the β2-adrenergic antagonist, ICI-118,551, successfully reduced this heat-induced RBC swelling. The acute heat shock caused a significant induction of HSP70 in RBCs of 13 °C-acclimated trout as well as a significant increase in plasma catecholamines. When heat-shocked fish were treated with ICI-118,551, we observed a significant attenuation of the HSP70 response. We conclude that circulating catecholamines influence the cellular heat shock response in rainbow trout RBCs, demonstrating physiological/hormonal control of the cellular stress response.

References

  1. Physiol Genomics. 2011 Jun 15;43(11):685-96 [PMID: 21467159]
  2. Am J Physiol Regul Integr Comp Physiol. 2012 Jan 1;302(1):R184-92 [PMID: 22031780]
  3. Comp Biochem Physiol B Biochem Mol Biol. 2001 Jun;129(2-3):679-85 [PMID: 11399505]
  4. J Exp Biol. 1975 Aug;63(1):207-17 [PMID: 1159362]
  5. Respir Physiol. 1989 Sep;77(3):365-77 [PMID: 2781171]
  6. Cell Stress Chaperones. 1996 Jun;1(2):139-47 [PMID: 9222599]
  7. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1998 Jul;120(1):1-27 [PMID: 9827012]
  8. Comp Biochem Physiol A Mol Integr Physiol. 2005 Feb;140(2):225-32 [PMID: 15748863]
  9. J Exp Biol. 1997;200(Pt 3):607-14 [PMID: 9318323]
  10. Gen Comp Endocrinol. 2001 Oct;124(1):97-105 [PMID: 11703075]
  11. J Exp Biol. 2011 May 15;214(Pt 10):1721-31 [PMID: 21525319]
  12. J Exp Biol. 1989 Nov;147:169-88 [PMID: 2614337]
  13. J Exp Zool. 1992 Aug 15;263(2):160-75 [PMID: 1323642]
  14. J Cell Physiol. 1994 Oct;161(1):169-77 [PMID: 7929603]
  15. Endocr Rev. 2000 Feb;21(1):55-89 [PMID: 10696570]
  16. Eur J Biochem. 2001 Dec;268(24):6465-72 [PMID: 11737201]
  17. Cell Stress Chaperones. 1999 Sep;4(3):199-204 [PMID: 10547069]
  18. Aquat Toxicol. 2009 Nov 27;95(3):195-202 [PMID: 19819565]
  19. Aquat Toxicol. 2007 May 15;82(3):145-62 [PMID: 17382413]
  20. J Exp Biol. 2006 Jul;209(Pt 14):2660-77 [PMID: 16809457]
  21. Am J Physiol Regul Integr Comp Physiol. 2003 Sep;285(3):R526-35 [PMID: 12775554]
  22. J Exp Biol. 2005 Jun;208(Pt 12):2217-25 [PMID: 15939765]
  23. Comp Biochem Physiol Part D Genomics Proteomics. 2006 Jun;1(2):238-52 [PMID: 20483255]
  24. Physiol Biochem Zool. 2008 Jul-Aug;81(4):414-25 [PMID: 18507532]
  25. J Cell Sci. 2001 Oct;114(Pt 19):3557-64 [PMID: 11682614]
  26. J Exp Biol. 2006 Aug;209(Pt 15):2961-70 [PMID: 16857880]
  27. J Neurochem. 2001 Feb;76(4):1142-52 [PMID: 11181834]
  28. J Exp Biol. 2006 Aug;209(Pt 15):2859-72 [PMID: 16857869]
  29. Am J Physiol. 1999 Apr;276(4):R990-6 [PMID: 10198376]
  30. J Clin Invest. 1993 Feb;91(2):465-73 [PMID: 8094399]
  31. J Exp Biol. 1976 Aug;65(1):131-45 [PMID: 993699]
  32. Proc Biol Sci. 2010 Mar 22;277(1683):905-13 [PMID: 19923129]
  33. J Biol Chem. 1991 Jun 25;266(18):11858-65 [PMID: 1646817]
  34. Fish Physiol Biochem. 1988 Jan;4(4):189-202 [PMID: 24226300]
  35. Am J Physiol Regul Integr Comp Physiol. 2002 Sep;283(3):R680-7 [PMID: 12185003]
  36. J Comp Physiol B. 2002 Apr;172(3):251-62 [PMID: 11919706]
  37. J Mol Neurosci. 1993 Fall;4(3):141-8 [PMID: 8292487]
  38. Am J Physiol Regul Integr Comp Physiol. 2011 Jun;300(6):R1373-83 [PMID: 21411771]
  39. Fish Physiol Biochem. 1993 Apr;10(6):485-90 [PMID: 24214448]
  40. Brain Res. 1996 Jul 15;727(1-2):145-52 [PMID: 8842392]
  41. J Exp Zool A Ecol Genet Physiol. 2012 Jun;317(5):303-10 [PMID: 25363579]
  42. Comp Biochem Physiol A Mol Integr Physiol. 2013 Jun;165(2):281-7 [PMID: 23507569]
  43. J Physiol. 1987 Jan;382:123-44 [PMID: 3040965]
  44. J Appl Physiol (1985). 2002 Jul;93(1):107-15 [PMID: 12070193]
  45. Physiol Rev. 1992 Apr;72(2):301-21 [PMID: 1557427]
  46. Cell Stress Chaperones. 2009 Nov;14(6):555-67 [PMID: 19280369]
  47. Annu Rev Physiol. 1999;61:243-82 [PMID: 10099689]
  48. J Exp Biol. 1996;199(Pt 9):2105-18 [PMID: 9320017]

MeSH Term

Acclimatization
Adrenergic beta-Antagonists
Analysis of Variance
Animals
Blotting, Western
Catecholamines
Erythrocyte Count
Erythrocytes
Heat-Shock Proteins
Heat-Shock Response
Hematocrit
Homeostasis
Hot Temperature
Oncorhynchus mykiss
Propanolamines
Stress, Physiological

Chemicals

Adrenergic beta-Antagonists
Catecholamines
Heat-Shock Proteins
Propanolamines
ICI 118551

Word Cloud

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