Adenosine inhibits norepinephrine release in the postischemic rat heart: The mechanism of neuronal stunning

Christof Burgdorf, Doreen Richardt, Thomas Kurz, Melchior Seyfarth, Deepak Jain, Hugo A. Katus, Gert Richardt*

*Corresponding author for this work
28 Citations (Scopus)

Abstract

Objective: Numerous studies support the concept of impaired postischemic sympathetic neurotransmission in the heart. We hypothesized that postischemic neuronal dysfunction (neuronal stunning) is caused by a transient suppression of exocytotic norepinephrine (NE) release from sympathetic nerve terminals. Furthermore, we assessed the role of presynaptic adenosine-receptors and α2-adrenoceptors in neuronal stunning. Methods and results: Exocytotic NE release was induced by two electrical field stimulations (S1 and S2) in isolated perfused rat hearts. S1 was performed under baseline conditions and S2 either during or following intervention. Results are expressed as mean S2/S1 ratios ± S.E.M. Stepwise increase of global ischemic periods (10, 20, and 30 min) induced a progressive suppression of NE release in the postischemic hearts, which was reversible during reperfusion. Both the degree and duration of NE suppression was dependent on the extent of the preceding ischemic period. Following 10-min ischemia complete recovery of NE release was achieved after 5-min reperfusion (1.07 ± 0.12), whereas 5-min reperfusion did not restore NE release after 30 min (0.36 ± 0.07) of ischemia. The adenosine-receptor antagonists 8-phenyltheophylline (8-PT; non-selective) and 8-cyclopentyl-1,3-dipropylxanthine (DPCPX; adenosine A1-receptor subtype selective) significantly increased NE release after 30-min ischemia and 5-min reperfusion (0.78 ± 0.06 and 0.64 ± 0.07), while in the same experimental protocol blockade of α2-adrenoceptors by yohimbine failed to restore the postischemic release (0.24 ± 0.06). In non-ischemic hearts the adenosine analogue R(-)N6-(2-phenylisopropyl)adenosine (R-PIA) resulted in a marked suppression of NE release (0.61 ± 0.07). The inhibitory effect of R-PIA and 2-chloro-N6-cyclopentyladenosine (CCPA; adenosine A1-receptor subtype selective agonist) persisted 5 min after cessation of R-PIA (0.62 ± 0.05) and CCPA (0.58 ± 0.04). Activation of α2-adrenoceptors by 5-bromo-N-(4,5-dihydro-1H-imidazol-2-yl)-6-quinoxalinamine (UK 14,304) also caused a reduction of NE release (0.50 ± 0.02), but the release increased to control levels 5 min after cessation of UK 14,304 (0.90 ± 0.06). Conclusions: The results establish the phenomenon of neuronal stunning in terms of a postischemic suppression of exocytotic NE release and provide evidence that neuronal stunning is mediated by endogenous adenosine through activation of presynaptic adenosine A1-receptors.

Original languageEnglish
JournalCardiovascular Research
Volume49
Issue number4
Pages (from-to)713-720
Number of pages8
ISSN0008-6363
DOIs
Publication statusPublished - 2001

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