Original Article
Ischemic preconditioning prevents ischemia-induced beta-adrenergic
receptor sequestration
Kousaku Iwatsubo
a
, Yoshiyuki Toya
a
, Takayuki Fujita
a
, Toshiaki Ebina
a
, Carsten Schwencke
b
,
Susumu Minamisawa
a
, Satoshi Umemura
a
,Yoshihiro Ishikawa
a,b,
*
a
Departments of Physiology and Medicine, Yokohama City University School of Medicine, Yokohama 236-0004, Japan
b
Departments of Medicine (Cardiology) and Cell Biology and Molecular Medicine, Cardiovascular Research Institute, New Jersey Medical School,
University of Medicine and Dentistry of New Jersey, 185 South Orange Avenue, Newark, NJ 07103, USA
Received 3 December 2002; received in revised form 16 April 2003; accepted 25 April 2003
Abstract
Preconditioning enables endogenous protection to repeated myocardial ischemia. However, the effect of preconditioning on beta1
adrenergic receptor (AR) signal remains controversial. We have recently developed receptor assay system using whole cells, in which
overexpressed cell surface beta ARs can be readily quantitated without disrupting the cell. Using this technique, we examined the effects of
chemical/metabolic ischemia on the beta1AR sequestration and adenylyl cyclase activity. Isoproterenol treatment, but not forskolin treatment,
of HEK293T cells overexpressing beta1 ARs led to a rapid decrease (within 2 hours) in the number of the cell surface receptor, which was
negated in the presence of concanavalin A. Similarly, treatment of cells with potassium cyanide and 2-deoxy-D-glucose (chemical/metabolic
ischemia) induced similar receptor sequestration. When isoproterenol was superimposed on chemical/metabolic ischemia, the degree of
sequestration became greater. However, when cells were pre-exposed to potassium cyanide on the preceding day (chemical preconditioning),
the sequestration induced by either isoproterenol or chemical/metabolic ischemia was attenuated. Adenylyl cyclase catalytic activity as
assessed by stimulation with forskolin was decreased by chemical/metabolic ischemia but fully recovered after 24 hours, suggesting that
chemical/metabolic ischemia treatment did not alter cell viability. Putting together, chemical/metabolic ischemia induced beta1 AR
sequestration in a similar manner to isoproterenol. In addition, preconditioning prevented the beta1 AR sequestration induced by both
isoproterenol and chemical/metabolic ischemia. Pre-conditioning may play a role in preserving the cell surface beta ARs by inhibiting the
sequestration that is usually induced by an ischemic event or beta adrenergic stimulation.
© 2003 Published by Elsevier Ltd.
Keywords: Beta-adrenergic receptor; Myocardial ischemia; Ischemic preconditioning; Receptor downregulation; Receptor desensitization; Receptor seques-
tration; Adenylyl cyclase
1. Introduction
Ischemic preconditioning indicates increased cardiopro-
tection against myocardial ischemia following a brief period
of ischemia. Recently, several studies have revealed that
there are indeed two phases in ischemic preconditioning; an
early phase that develops within minutes and lasts for 2–3 h
and a late phase that occurs 12–24 h after ischemia lasting for
3–4 d [1]. Several investigators reported the alterations in the
early phase ischemic preconditioning included the changes
of beta-adrenergic receptor (AR) density and adenylyl cy-
clase catalytic activity. However, the alterations in the late
phase preconditioning and their relationship as to beta-
adrenergic signaling has remained poorly characterized and
controversial [2–8].
Beta1-ARs, like other G-protein-coupled receptors, un-
dergo rapid agonist-promoted sequestration [9,10]. Receptor
sequestration is the event that follows agonist binding to the
receptor, leading to the translocation of receptors from the
plasma membrane to the cytoplasm. Several investigators
reported that the alteration of the number of beta-ARs and
adenylyl cyclase catalytic activity in the late phase after
myocardial ischemia. Mukherjee et al. reported that the num-
ber of beta-ARs increased after 1 h ligation of canine coro-
nary artery [2]. Their results have been supported by several
other studies thereafter [3,4]. However, there have been sub-
* Corresponding author. Tel.: +1-973-972-8925; fax: +1-973-972-8929.
E-mail address: ishikayo@umdnj.edu (Y. Ishikawa).
Journal of Molecular and Cellular Cardiology 35 (2003) 923–929
www.elsevier.com/locate/yjmcc
© 2003 Published by Elsevier Ltd.
DOI: 10.1016/S0022-2828(03)00173-1