European Journal of Pharmacology, 192 (1991) 371-375
© 1991 Elsevier Science Publishers B.V. (Biomedical Division) 0014-2999/91/$03.50
ADONIS 0014299991001221
371
EJP 51671
Pharmacological characterization of [D-Ala2,LeuS,Ser 6]enkephalin (DALES):
antinociceptive actions at the 6non.complexed-Opioid receptor
Antonia Mattia, Todd Vanderah, Henry I. Mosbcrg 1, John R. Omnaas 1, Wayne D. Bowen 2
and Frank Porrcca
Department of Pharmacology, University of Arizona Health Sciences Center, Tucson, A Z 85724, U.S.A., I College of Pharmacy, University of Michigan,
Ann Arbor, M1 48109, U.S.A. and e Section of Biochemistry, Division of Biology and Medicine, Brown University, Providence, RI 02912, U.S.A.
Received 30 July 1990, revised MS received 12 October 1990, accepted 23 October 1990
Substantial evidence has been accumulated which suggests that opioid 8 receptors may be distinguished on the basis of their
involvement in the modulation (i.e., increase or decrease in potency) of/x-mediated antinociception. On this basis, it has been
hypothesized that some opioid 8 receptors exist within a functional complex with /L receptors (8~omplexe d (8c~) receptors) while
other 8 sites do not (8....... plex,d (Sncx) receptors). Recent work with [D-Ala2,LeuS,Cys6]enkephalin (DALCE) has demonstrated
that this compound produces initial antinociceptive actions, does not modulate morphine antinociception and appears to bind
irreversibly to the 8no x site, presumably by means of thiol-disulfide exchange between the receptor and the cysteine sulfhydryl
group. To determine if a structural basis exists for actions at the hypothesized 8n~ x receptor, in the present study we report the
synthesis and pharmacological characterization of [D-Ala2,LeuS,Ser6]enkephalin (DALES), a close structural analogue of DALCE.
If a structural basis for action at the 8no x site exists, then DALES would be predicted to produce antinociception, fail to modulate
morphine antinociception and, since it lacks the free sulfhydryl group present in DALCE, fail to exhibit irreversible antagonistic
actions; these predictions were supported. Additionally, pretreatment with DALCE at -24 h, but not with DALES, blocked
DALES-induced antinociception. These observations in vivo support the concept of a structural basis for activity at the
hypothesized 8nCx site and suggest that DALES, like DALCE, may be a useful probe for pharmacological characterization of
putative 8 receptor subtypes.
Opioid antinociception; 8-Opioid receptors; /~-Opioid receptors; Enkephalins;
DALES ([D-Ala2,LeuS,Ser6]enkephalin); (Intracerebroventricular)
1. Introduction
The multiplicity of opioid receptors has been well
accepted since the initial suggestion of multiple opioid
receptors by Martin et al. (1976). While uncertainty still
exists as to the specific physiological functions of opioid
receptors, pharmacological evidence has accumulated
which strongly implicate 3, as well as /~, receptors in
supraspinal antinociception in the mouse (Heyman et
al., 1987; Heyman et al., 1988). Additionally, data have
also been accumulated which indicate that in some
cases, opioid bt and ~ receptors may be involved in
functional interactions in vitro (e.g., Rothman and
Westfall, 1982) and in vivo (Heyman et al., 1989a,b;
Jiang et al., 1990a,b; and see Holaday et al., 1985 for
review).
Early observations demonstrated that the proposed
endogenous ligands for the opioid 8 receptor, [LeuS]en-
Correspondence to: F. Porreca, Department of Pharmacology, College
of Medicine, University of Arizona, Tucson, AZ 85724, U.S.A.
kephalin and [MetS]enkephalin, respectively produced
an increase and decrease in morphine antinociceptive
potency (Vaught and Takemori, 1979; Lee et al., 1980).
These observations have been confirmed with other
synthetic ~ ligands in vivo (Heyman et al., 1989a,b) as
well as with radioligand binding techniques in vitro
(Rothman et al., 1988) and have supported the sugges-
tion that endogenous opioids may function in a modula-
tory capacity for ~t-mediated analgesia (Barrett and
Vaught, 1982). The hypothesis of functional or physical
interactions between/~ and 8 opioid receptors has been
extended to suggest that some opioid 8 receptors may
exist within a /~-8 complex (i.e., ~complexed (~cx) recep-
tors) while other 8 receptors do not (i.e., 8....... plexea
(Sncx) receptors) (Rothman et al., 1988).
Substantial data in vivo are consistent with such a
hypothesis. In this regard, doses of 8 agonists such as
[D-Pen2,D-PenS]enkephalin (DPDPE) or [D-Ala 2,
MetS]enkephalinamide (DAMA) which do not produce
antinociceptive actions alone, respectively increase and
decrease the antinociceptive potency of intracerebro-
ventricular (i.c.v.) morphine in mice (Heyman et al.,