Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1983 Jul;80(14):4513–4517. doi: 10.1073/pnas.80.14.4513

Psychological stress activates phosphorylase in the heart of the conscious pig without increasing heart rate and blood pressure.

J E Skinner, S D Beder, M L Entman
PMCID: PMC384069  PMID: 6410394

Abstract

The present study uses a technique that enables the collection of multiple freeze-biopsy samples from the myocardium of the conscious pig (i.e., through a thoracic window). This technique enables sequential analysis of the metabolic state of the myocardium during different behavioral conditions. The results demonstrate that with daily adaptations to an unfamiliar environment (i.e., stress reduction), the phosphorylase activation ratio (phosphorylase a/total phosphorylase) in the quiescent pig declines steadily from approximately 80% to 30% (r = -0.91, P less than 0.01). This decline occurs with both the mean resting heart rate and left ventricular blood pressure remaining constant. The decline is seen within individual subjects during the whole adaptation sequence as well as between subjects whose samples were taken either early or late in the adaptation series. The dissociation of hemodynamic functional and metabolic activation in the unadapted, psychologically stressed pig may be associated with the occurrence of increased vulnerability of the ischemic heart to ventricular fibrillation, a phenomenon previously observed under the same behavioral conditions.

Full text

PDF
4513

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baust W., Bohnert B. The regulation of heart rate during sleep. Exp Brain Res. 1969;7(2):169–180. doi: 10.1007/BF00235442. [DOI] [PubMed] [Google Scholar]
  2. Blukoo-Allotey J. A., Vincent N. H., Ellis S. Interactions of acetylcholine and epinephrine on contractility, glycogen and phosphorylase activity of isolated mammalian hearts. J Pharmacol Exp Ther. 1969 Nov;170(1):27–36. [PubMed] [Google Scholar]
  3. CORNBLATH M., RANDLE P. J., PARMEGGIANI A., MORGAN H. E. Regulation of glycogenolysis in muscle. Effects of glucagon and anoxia on lactate production, glycogen content, and phosphorylase activity in the perfused isolated rat heart. J Biol Chem. 1963 May;238:1592–1597. [PubMed] [Google Scholar]
  4. Corley K. C., Shiel F. O., Mauck H. P., Greenhoot J. Electrocardiographic and cardiac morphological changes associated with environmental stress in squirrel monkeys. Psychosom Med. 1973 Jul-Aug;35(4):361–364. doi: 10.1097/00006842-197307000-00010. [DOI] [PubMed] [Google Scholar]
  5. Cottington E. M., Matthews K. A., Talbott E., Kuller L. H. Environmental events preceding sudden death in women. Psychosom Med. 1980 Nov;42(6):567–574. doi: 10.1097/00006842-198011000-00005. [DOI] [PubMed] [Google Scholar]
  6. DRUMMOND G. I., DUNCAN L., FRIESEN A. J. SOME PROPERTIES OF CARDIAC PHOSPHORYLASE B KINASE. J Biol Chem. 1965 Jul;240:2778–2785. [PubMed] [Google Scholar]
  7. Dobson J. G., Jr, Mayer S. E. Mechanisms of activation of cardiac glycogen phosphorylase in ischemia and anoxia. Circ Res. 1973 Oct;33(4):412–420. doi: 10.1161/01.res.33.4.412. [DOI] [PubMed] [Google Scholar]
  8. Entam M. L., Kanike K., Goldstein M. A., Nelson T. E., Bornet E. P., Futch T. W., Schwartz A. Association of gylcogenolysis with cardiac sarcoplasmic reticulum. J Biol Chem. 1976 May 25;251(10):3140–3146. [PubMed] [Google Scholar]
  9. Exton J. H., Assimacopoulos-Jeannet F. D., Blackmore P. F., Cherrington A. D., Chan T. M. Mechanisms of catecholamine actions on liver carbohydrate metabolism. Adv Cyclic Nucleotide Res. 1978;9:441–452. [PubMed] [Google Scholar]
  10. Furberg C., Romo M., Linko E., Siltanen P., Tibblin G., Wilhelmsen L. Sudden coronary death in Scandinavia. A report from Scandinavian coronary heart disease registers. Acta Med Scand. 1977;201(6):553–557. [PubMed] [Google Scholar]
  11. Garber A. J., Birnbaumer L., Bornet E. P., Thompson W. J., Entman M. L. Skeletal muscle protein and amino acid metabolism in hereditary mouse muscular dystrophy. The role of disordered cyclic nucleotide metabolism in the accelerated alanine and glutamine formation and release. J Biol Chem. 1980 Sep 10;255(17):8325–8333. [PubMed] [Google Scholar]
  12. Jenkins C. D. Recent evidence supporting psychologic and social risk factors for coronary disease. N Engl J Med. 1976 May 6;294(19):1033–1038. doi: 10.1056/NEJM197605062941904. [DOI] [PubMed] [Google Scholar]
  13. Johansson G., Jonsson L., Lannek N., Blomgren L., Lindberg P., Poupa O. Severe stress-cardiopathy in pigs. Am Heart J. 1974 Apr;87(4):451–457. doi: 10.1016/0002-8703(74)90170-7. [DOI] [PubMed] [Google Scholar]
  14. LUMB G., SINGLETARY H. Blood supply to cardiac conduction tissue in pig and man. Surg Forum. 1961;12:218–220. [PubMed] [Google Scholar]
  15. LaRaia P. J., Sonnenblick E. H. Autonomic control of cardiac C-AMP. Circ Res. 1971 Mar;28(3):377–384. doi: 10.1161/01.res.28.3.377. [DOI] [PubMed] [Google Scholar]
  16. Lee T. P., Kuo J. F., Greengard P. Role of muscarinic cholinergic receptors in regulation of guanosine 3':5'-cyclic monophosphate content in mammalian brain, heart muscle, and intestinal smooth muscle. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3287–3291. doi: 10.1073/pnas.69.11.3287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lown B., Verrier R. L. Neural activity and ventricular fibrillation. N Engl J Med. 1976 May 20;294(21):1165–1170. doi: 10.1056/NEJM197605202942107. [DOI] [PubMed] [Google Scholar]
  18. MURAD F., CHI Y. M., RALL T. W., SUTHERLAND E. W. Adenyl cyclase. III. The effect of catecholamines and choline esters on the formation of adenosine 3',5'-phosphate by preparations from cardiac muscle and liver. J Biol Chem. 1962 Apr;237:1233–1238. [PubMed] [Google Scholar]
  19. Matta R. J., Lawler J. E., Lown B. Ventricular electrical instability in the conscious dog: effects of psychologic stress and beta adrenergic blockade. Am J Cardiol. 1976 Nov 4;38(5):594–598. doi: 10.1016/s0002-9149(76)80008-2. [DOI] [PubMed] [Google Scholar]
  20. Mayer S. E., Williams B. J., Smith J. M. Adrenergic mechanisms in cardiac glycogen metabolism. Ann N Y Acad Sci. 1967 Feb 10;139(3):686–702. doi: 10.1111/j.1749-6632.1967.tb41238.x. [DOI] [PubMed] [Google Scholar]
  21. Namm D. H., Mayer S. E. Effects of epinephrine on cardiac cyclic 3',5'-AMP, phosphorylase kinase, and phosphorylase. Mol Pharmacol. 1968 Jan;4(1):61–69. [PubMed] [Google Scholar]
  22. Namm D. H., Mayer S. E., Maltbie M. The role of potassium and calcium ions in the effect of epinephrine on cardiac cyclic adenosine 3',5'-monophosphate, phosphorylase kinase, and phosphorylase. Mol Pharmacol. 1968 Sep;4(5):522–530. [PubMed] [Google Scholar]
  23. Parkes C. M., Benjamin B., Fitzgerald R. G. Broken heart: a statistical study of increased mortality among widowers. Br Med J. 1969 Mar 22;1(5646):740–743. doi: 10.1136/bmj.1.5646.740. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rahe R. H., Bennett L., Romo M., Siltanen P., Arthur R. J. Subjects' recent life changes and coronary heart disease in Finland. Am J Psychiatry. 1973 Nov;130(11):1222–1226. doi: 10.1176/ajp.130.11.1222. [DOI] [PubMed] [Google Scholar]
  25. Rahe R. H., Lind E. Psychosocial factors and sudden cardiac death: a pilot study. J Psychosom Res. 1971 Mar;15(1):19–24. doi: 10.1016/0022-3999(71)90069-9. [DOI] [PubMed] [Google Scholar]
  26. Rees W. D., Lutkins S. G. Mortality of bereavement. Br Med J. 1967 Oct 7;4(5570):13–16. doi: 10.1136/bmj.4.5570.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reich P., DeSilva R. A., Lown B., Murawski B. J. Acute psychological disturbances preceding life-threatening ventricular arrhythmias. JAMA. 1981 Jul 17;246(3):233–235. [PubMed] [Google Scholar]
  28. Rissanen V., Romo M., Siltanen P. Premonitory symptoms and stress factors preceding sudden death from ischaemic heart disease. Acta Med Scand. 1978;204(5):389–396. doi: 10.1111/j.0954-6820.1978.tb08460.x. [DOI] [PubMed] [Google Scholar]
  29. Robison G. A., Butcher R. W., Oye I., Morgan H. E., Sutherland E. W. The effect of epinephrine on adenosine 3', 5'-phosphate levels in the isolated perfused rat heart. Mol Pharmacol. 1965 Sep;1(2):168–177. [PubMed] [Google Scholar]
  30. Robison G. A., Butcher R. W., Sutherland E. W. Adenyl cyclase as an adrenergic receptor. Ann N Y Acad Sci. 1967 Feb 10;139(3):703–723. doi: 10.1111/j.1749-6632.1967.tb41239.x. [DOI] [PubMed] [Google Scholar]
  31. Skinner J. E., Lie J. T., Entman M. L. Modification of ventricular fibrillation latency following coronary artery occlusion in the conscious pig. Circulation. 1975 Apr;51(4):656–667. doi: 10.1161/01.cir.51.4.656. [DOI] [PubMed] [Google Scholar]
  32. Skinner J. E., Mohr D. N., Kellaway P. Sleep-stage regulation of ventricular arrhythmias in the unanesthetized pig. Circ Res. 1975 Sep;37(3):342–349. doi: 10.1161/01.res.37.3.342. [DOI] [PubMed] [Google Scholar]
  33. Skinner J. E., Reed J. C. Blockade of frontocortical-brain stem pathway prevents ventricular fibrillation of ischemic heart. Am J Physiol. 1981 Feb;240(2):H156–H163. doi: 10.1152/ajpheart.1981.240.2.H156. [DOI] [PubMed] [Google Scholar]
  34. Skinner J. E., Reed J. C., Welch K. M., Nell J. H. Cutaneous shock produces correlated shifts in slow potential amplitude and cyclic 3',5'-adenosine monophosphate level in the parietal cortex of the conscious rat. J Neurochem. 1978 Apr;30(4):699–704. doi: 10.1111/j.1471-4159.1978.tb10774.x. [DOI] [PubMed] [Google Scholar]
  35. Skinner J. E., Welch K. M., Reed J. C., Nell J. H. Psychological stress reduces cyclic 3',5'-adenosine monophosphate levels in the cerebral cortex of conscious rats, as determined by a new cryogenic method of rapid tissue fixation. J Neurochem. 1978 Apr;30(4):691–698. doi: 10.1111/j.1471-4159.1978.tb10773.x. [DOI] [PubMed] [Google Scholar]
  36. Skinner J. E., Yingling C. D. Regulation of slow potential shifts in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. Electroencephalogr Clin Neurophysiol. 1976 Mar;40(3):288–296. doi: 10.1016/0013-4694(76)90152-8. [DOI] [PubMed] [Google Scholar]
  37. Walsh D. A., Perkins J. P., Brosom C. O., Ho E. S., Kreb E. G. Catlysis of the phosphrylaseinase actition reaction. J Biol Chem. 1971 Apr 10;246(7):1968–1976. [PubMed] [Google Scholar]
  38. Watanabe A. M., McConnaughey M. M., Strawbridge R. A., Fleming J. W., Jones L. R., Besch H. R., Jr Muscarinic cholinergic receptor modulation of beta-adrenergic receptor affinity for catecholamines. J Biol Chem. 1978 Jul 25;253(14):4833–4836. [PubMed] [Google Scholar]
  39. Wolf S. Neural mechanisms in sudden cardiac death. Trans Am Clin Climatol Assoc. 1968;79:158–176. [PMC free article] [PubMed] [Google Scholar]
  40. Wollenberger A., Krause E. G., Heier G. Stimulation of 3',5'-cyclic AMP formation in dog myocardium following arrest of blood flow. Biochem Biophys Res Commun. 1969 Aug 15;36(4):664–670. doi: 10.1016/0006-291x(69)90357-x. [DOI] [PubMed] [Google Scholar]
  41. Yingling C. D., Skinner J. E. Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami. Electroencephalogr Clin Neurophysiol. 1976 Nov;41(5):476–482. doi: 10.1016/0013-4694(76)90059-6. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES