Heart rate contributes to the vascular effects of chronic mental stress: Effects on endothelial function and ischemic brain injury in mice

Stroke

Volumn 42, Issue 6, 2011, Pages 1742-1749

  Custodis, Florian ^a   Gertz, Karen ^b   Balkaya, Mustafa ^b   Prinz, Vincent ^b   Mathar, Ilka ^c   Stamm, Christoph ^a   Kronenberg, Golo ^b   Kazakov, Andrey ^a   Freichel, Marc ^c   Böhm, Michael ^a   Endres, Matthias ^b   Laufs, Ulrich ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

endothelial dysfunction; focal brain ischemia; heart rate reduction; mental stress

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; IVABRADINE; LIPID HYDROPEROXIDE; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BRAIN CAPILLARY; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN TISSUE; CHRONIC MENTAL STRESS; CHRONIC STRESS; CONTROLLED STUDY; DENSITY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE EXPRESSION; HEART RATE VARIABILITY; MALE; MENTAL STRESS; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; UPREGULATION; VASCULAR RING;

ANIMALS; BENZAZEPINES; BLOOD PRESSURE; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; ENDOTHELIUM, VASCULAR; HEART RATE; INFARCTION, MIDDLE CEREBRAL ARTERY; LIPID PEROXIDATION; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; RANDOM ALLOCATION; STRESS, PSYCHOLOGICAL;

EID: 79958267032     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.110.598607     Document Type: Article

References (48)

1. Rosengren A, Hawken S, Ounpuu S, Sliwa K, Zubaid M, Almahmeed WA, et al. Association of psychosocial risk factors with risk of acute myocardial infarction in 11119 cases and 13648 controls from 52 countries (the INTERHEART study): Case-control study. Lancet. 2004;364:953-962. (Pubitemid 39208456)
2. May M, McCarron P, Stansfeld S, Ben-Shlomo Y, Gallacher J, Yarnell J, Davey Smith G, Elwood P, Ebrahim S. Does psychological distress predict the risk of ischemic stroke and transient ischemic attack? The Caerphilly Study. Stroke. 2002;33:7-12. (Pubitemid 34052175)
3. Salaycik KJ, Kelly-Hayes M, Beiser A, Nguyen AH, Brady SM, Kase CS, Wolf PA. Depressive symptoms and risk of stroke: the Framingham Study. Stroke. 2007;38:16-21. (Pubitemid 46035600)
4. Surtees PG, Wainwright NW, Luben RN, Wareham NJ, Bingham SA, Khaw KT. Psychological distress, major depressive disorder, and risk of stroke. Neurology. 2008;70:788-794.
5. Angerer P, Siebert U, Kothny W, Mühlbauer D, Mudra H, von Schacky C. Impact of social support, cynical hostility and anger expression on progression of coronary atherosclerosis. J Am Coll Cardiol. 2000;36:1781-1788.
6. Knox SS, Adelman A, Ellison RC, Arnett DK, Siegmund K, Weidner G, Province MA. Hostility, social support, and carotid artery atherosclerosis in the National Heart, Lung, and Blood Institute Family Heart Study. Am J Cardiol. 2000;86:1086-1089.
7. Ghiadoni L, Donald AE, Cropley M, Mullen MJ, Oakley G, Taylor M, O'Connor G, Betteridge J, Klein N, Steptoe A, Deanfield JE. Mental stress induces transient endothelial dysfunction in humans. Circulation. 2000;102:2473-2478.
8. von Känel R, Hepp U, Traber R, Kraemer B, Mica L, Keel M, Mausbach BT, Schnyder U. Measures of endothelial dysfunction in plasma of patients with posttraumatic stress disorder. Psychiatry Res. 2008;158:363-373.
9. Carter JR, Kupiers NT, Ray CA. Neurovascular responses to mental stress. J Physiol. 2005;564:321-327. (Pubitemid 40552748)
10. Hayashi N, Someya N, Maruyama T, Hirooka Y, Endo MY, Fukuba Y. Vascular responses to fear-induced stress in humans. Physiol Behav. 2009;98:441-446.
11. Fox K, Borer JS, Camm AJ, Danchin N, Ferrari R, Lopez Sendon JL, et al. Resting heart rate in cardiovascular disease. J Am Coll Cardiol. 2007;50:823-830. (Pubitemid 47277500)
12. Gardiner SM, Kemp PA, March JE, Bennett T. Acute and chronic cardiac and regional haemodynamic effects of the novel bradycardic agent, S16257, in conscious rats. Br J Pharmacol. 1995;115:579-586.
13. Bois P, Bescond J, Renaudon B, Lenfant J. Mode of action of bradycardic agent, S 16257, on ionic currents of rabbit sinoatrial node cells. Br J Pharmacol. 1996;118:1051-1057. (Pubitemid 26261281)
14. Custodis F, Baumhäkel M, Schlimmer N, List F, Gensch C, Böhm M, Laufs U. Heart rate reduction by ivabradine reduces oxidative stress, improves endothelial function, and prevents atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2008;117:2377-2387. (Pubitemid 351653554)
15. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P. Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology. 2004;29:2007-2017. (Pubitemid 39486552)
16. Mills PA, Huetteman DA, Brockway BP, Zwiers LM, Gelsema AJ, Schwartz RS, Kramer K. A new method for measurement of blood pressure, heart rate, and activity in the mouse by radiotelemetry. J Appl Physiol. 2000;88:1537-1544. (Pubitemid 30336898)
17. Custodis F, Eberl M, Kilter H, Böhm M, Laufs U. Association of RhoGDIalpha with Rac1 GTPase mediates free radical production during myocardial hypertrophy. Cardiovasc Res. 2006;71:342-351.
18. Maack C, Kartes T, Kilter H, Schäfers HJ, Nickenig G, Böhm M, Laufs U. Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment. Circulation. 2003;108:1567-1574. (Pubitemid 37187782)
19. Müller P, Kazakov A, Semenov A, Böhm M, Laufs U. Pressure-induced cardiac overload induces upregulation of endothelial and myocardial progenitor cells. Cardiovasc Res. 2008;77:151-159. (Pubitemid 351195160)
20. Prinz V, Laufs U, Gertz K, Kronenberg G, Balkaya M, Leithner C, Lindauer U, Endres M. Intravenous rosuvastatin for acute stroke treatment: an animal study. Stroke. 2008;39:433-438. (Pubitemid 351619468)
21. Endres M, Laufs U, Huang Z, Nakamura T, Huang P, Moskowitz MA, Liao JK. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 1998;95:8880-8885. (Pubitemid 28350583)
22. Gertz K, Priller J, Kronenberg G, Fink KB, Winter B, Schröck H, Ji S, Milosevic M, Harms C, Böhm M, Dirnagl U, Laufs U, Endres M. Physical activity improves long-term stroke outcome via endothelial nitric oxide synthase-dependent augmentation of neovascularization and cerebral blood flow. Circ Res. 2006;99:1132-1140. (Pubitemid 44729938)
23. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol. 2003;91:7A-11A. (Pubitemid 36351457)
24. Landmesser U, Hornig B, Drexler H. Endothelial function: a critical determinant in atherosclerosis? Circulation. 2004;109:II27-II33. (Pubitemid 38724153)
25. Wassmann S, Stumpf M, Strehlow K, Schmid A, Schieffer B, Böhm M, Nickenig G. Interleukin-6 induces oxidative stress and endothelial dysfunction by overexpression of the angiotensin II type 1 receptor. Circ Res. 2004;94:534-541. (Pubitemid 38326289)
26. Ejchel-Cohen TF, Wood GE, Wang JF, Barlow K, Nobrega JN, S McEwen B, Trevor Young L. Chronic restraint stress decreases the expression of glutathione S-transferase pi2 in the mouse hippocampus. Brain Res. 2006;1090:156-162. (Pubitemid 43817937)
27. Liu Y, Yang N, Zuo P. Cdna microarray analysis of gene expression in the cerebral cortex and hippocampus of balb/c mice subjected to chronic mild stress. Cell Mol Neurobiol. 2010:30:1035-1047.
28. Li JM, Mogi M, Iwanami J, Min LJ, Tsukuda K, Sakata A, Fujita T, Iwai M, Horiuchi M. Temporary pretreatment with the angiotensin II type 1 receptor blocker, valsartan, prevents ischemic brain damage through an increase in capillary density. Stroke. 2008;39:2029-2036.
29. Williams JK, Kaplan JR, Manuck SB. Effects of psychosocial stress on endothelium-mediated dilation of atherosclerotic arteries in cynomolgus monkeys. J Clin Invest. 1993;92:1819-1823. (Pubitemid 23304548)
30. Skantze HB, Kaplan J, Pettersson K, Manuck S, Blomqvist N, Kyes R, Williams K, Bondjers G. Psychosocial stress causes endothelial injury in cynomolgus monkeys via beta1-adrenoceptor activation. Atherosclerosis. 1998;136:153-161. (Pubitemid 28341453)
31. Dimsdale JE. Psychological stress and cardiovascular disease. J Am Coll Cardiol. 2008;51:1237-1246. (Pubitemid 351400899)
32. DiFrancesco D, Camm JA. Heart rate lowering by specific and selective I(f) current inhibition with ivabradine: a new therapeutic perspective in cardiovascular disease. Drugs. 2004;64:1757-1765. (Pubitemid 39215187)
33. Thorin E, Thorin-Trescases N. Vascular endothelial ageing, heartbeat after heartbeat. Cardiovasc Res. 2009;84:24-32.
34. Baumhäkel M, Custodis F, Schlimmer N, Laufs U, Böhm M. Heart rate reduction with ivabradine improves erectile dysfunction in parallel to decrease in atherosclerotic plaque load in apoe-knockout mice. Atherosclerosis. 2010;212:55-62.
35. Drouin A, Gendron ME, Thorin E, Gillis MA, Mahlberg-Gaudin F, Tardif JC. Chronic heart rate reduction by ivabradine prevents endothelial dysfunction in dyslipidaemic mice. Br J Pharmacol. 2008;154:749-757. (Pubitemid 351821579)
36. Heusch G. Pleiotropic action(s) of the bradycardic agent ivabradine: cardiovascular protection beyond heart rate reduction. Br J Pharmacol. 2008;155:970-971.
37. Yasunari K, Matsui T, Maeda K, Nakamura M, Watanabe T, Kiriike N. Anxiety-induced plasma norepinephrine augmentation increases reactive oxygen species formation by monocytes in essential hypertension. Am J Hypertens. 2006;19:573-578. (Pubitemid 44218677)
38. Hovatta I, Tennant RS, Helton R, Marr RA, Singer O, Redwine JM, Ellison JA, Schadt EE, Verma IM, Lockhart DJ, Barlow C. Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature. 2005;438:662-666. (Pubitemid 41740575)
39. Vanhoutte PM. How we learned to say NO. Arterioscler Thromb Vasc Biol. 2009;29:1156-1160.
40. Aguilera G, Kiss A, Luo X, Akbasak BS. The renin angiotensin system and the stress response. Ann N Y Acad Sci. 1995;771:173-186. (Pubitemid 26077405)
41. Wassmann S, Czech T, van Eickels M, Fleming I, Böhm M, Nickenig G. Inhibition of diet-induced atherosclerosis and endothelial dysfunction in apolipoprotein E/angiotensin II type 1a receptor double-knockout mice. Circulation. 2004;110:3062-3067. (Pubitemid 39491999)
42. Fontella FU, Siqueira IR, Vasconcellos AP, Tabajara AS, Netto CA, Dalmaz C. Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem Res. 2005;30:105-111. (Pubitemid 40254210)
43. Lucca G, Comim CM, Valvassori SS, Réus GZ, Vuolo F, Petronilho F, Dal-Pizzol F, Gavioli EC, Quevedo J. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int. 2009;54:358-362.
44. Larson SL, Owens PL, Ford D, Eaton W. Depressive disorder, dysthymia, and risk of stroke: Thirteen-year follow-up from the Baltimore epidemiologic catchment area study. Stroke. 2001;32:1979-1983. (Pubitemid 32878509)
45. Gump BB, Matthews KA, Eberly LE, Chang YF, MRFIT Research Group. Depressive symptoms and mortality in men: results from the multiple risk factor intervention trial. Stroke. 2005;36:98-102. (Pubitemid 40054182)
46. Jonas BS, Mussolino ME. Symptoms of depression as a prospective risk factor for stroke. Psychosom Med. 2000;62:463-471. (Pubitemid 30604788)
47. Rozanski A, Blumenthal JA, Kaplan J. Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation. 1999;99:2192-2217. (Pubitemid 29196806)
48. Laufs U, Endres M, Stagliano N, Amin-Hanjani S, Chui DS, Yang SX, Simoncini T, Yamada M, Rabkin E, Allen PG, Huang PL, Böhm M, Schoen FJ, Moskowitz MA, Liao JK. Neuroprotection mediated by changes in the endothelial actin cytoskeleton. J Clin Invest. 2000;106:15-24. (Pubitemid 30437236)