Species- or isozyme-selective enzyme inhibitors. 8. Synthesis of disubstituted two-substrate condensation products as inhibitors of rat adenylate kinases

Journal of Medicinal Chemistry
1982.0

Abstract

Syntheses are described of 5'(R)- and 5'(S)-C-Me-ATP, 5'(R)- and 5'(S)-C-n-Pr-ATP, and the phosphonate isostere of ATP with a C(5')-CH2-P system. Determinations of KM (ATP)/Ki for competitive inhibition showed that two of the five compounds inhibited rat muscle adenylate kinase (AK-M) 8-9.5 times more effectively than AK II (present in poorly differentiated rat hepatoma tissue) and that two other compounds inhibited AK II at least 2-fold more effectively than AK-M, further indicating that monosubstituted substrate derivatives are potentially useful probes in the design of isozyme-selective inhibitors. P1-[8-(Ethylthio)adenosine-5']-P5-(adenosine-5') pentaphosphate (8SEt-Ap5A) is a potent dual substrate site inhibitor of the rat AK isozymes with selectivity for AK II. Three derivatives of 8-SEt-Ap5A were synthesized: P1-[8-(ethylthio)adenosine-5']-P5-[5'(R)-C-methyladenosine-5'] pentaphosphate (I), its 5'(R)-C-n-Pr analogue (II), and di(8-SEt)-Ap5A (III). Unsymmetrical pentaphosphates, such as I and II, are shown to be readily accessible via reaction of a derivative of ATP γ-piperidinate with an ADP derivative. Conversion of 8-SEt-ATP to 8-(ethylthio)adenosine 5'-trimetaphosphate, followed by reaction of the latter in situ with added piperidine, gave 8-SEt-ATP γ-piperidinate quantitatively. Except in the interaction of III with AK-M, I-III acted as two-site competitive inhibitors of AK-M and AK II with Ki < KM of AMP or ATP. Inhibitory potencies [KM (ATP)/Ki] of I-III with the two isozymes varied over more than a 95-fold range, and inhibitory potencies for AK-M relative to those of AK II varied more than 61-fold. III was an effective inhibitor of AK II (KM/Ki = 8 and 14 with AMP and ATP, respectively) and exhibited at least 4 times more selectivity for AK II [relative inhibitory potency, AK II/AK-M, >22] than 8-SEt-Ap5A. Evidence, summarized previously, suggests that selective inhibitors of fetal-type isozymes of key metabolic enzymes could, if available, be potentially useful in the design of new types of antineoplastic agents. Studies of approaches that might have utility in the design of isozyme-selective inhibitors showed that such inhibitors were frequently produced when a single short (1 to 3 atoms) substituent was introduced at various atoms in turn of a substrate of the target enzyme. This result was obtained with each of three enzymic substrates studied. The selective inhibitors so obtained were usually of weak or moderate potency, however. In the case of one target enzyme, adenylate kinase (AK), it proved possible to maintain the selectivity while enhancing potency 1000-fold by elaborating a monosubstituted substrate derivative into a monosubstituted two-substrate condensation product that appears to bind simultaneously to two adjoining substrate sites. In the present study, two-substrate condensation products bearing a substituent at each substrate moiety were synthesized in order to further explore the potential of dual-site inhibitors for isozyme selectivity and with the hope of progressing further toward a potent and specific inhibitor of the isozyme AK II that predominates in poorly differentiated rat hepatoma tissue. AK catalyzes the equilibrium ATP + AMP ⇌ 2ADP and possesses nonidentical binding sites for AMP and ATP. The previous studies revealed that 8-SEt-Ap5A acts as a potent two-site inhibitor and inhibits AK II (Ki = 0.07 μM) more effectively than the rat muscle isozyme AK-M (Ki = 3.25 μM). 8-SEt-ATP inhibits AK II more effectively than AK-M, and it was concluded from this and other lines of evidence that the selectivity of 8-SEt-Ap5A originates from interactions of its 8-(ethylthio)adenosine moiety at the ATP binding sites. In the present work, single substituents have been attached to the unsubstituted adenosine moiety of 8-SEt-Ap5A in attempts to increase the selectivity for inhibition of AK II by decreasing affinity for the AMP site of AK-M by a larger factor than affinity for the AMP site of AK II. In preceding studies, a series of AMP derivatives monosubstituted at a variety of positions had been evaluated kinetically as inhibitors of the isozymes; for no compound could definitive evidence be obtained that inhibitory potency [KM (AMP)/Ki for competitive inhibition] with AK II exceeded that with AK-M. The compound in the series most likely to possess that property was 5'(R)-C-n-Pr-AMP: this was a weak competitive inhibitor of AK II with KM (AMP)/Ki = 0.025 and a weak noncompetitive inhibitor of AK-M with KM (AMP)/Ki < 0.1, though of undetermined magnitude. 5'(R)-C-Me-AMP resembled its n-propyl homologue in its inhibitory properties toward the two isozymes; in addition, it was a substrate of AK II but, under the same conditions, was not a substrate of AK-M. Hence, despite the incompletely defined relative inhibitory potencies of the 5'-(R)-C-alkyl-AMP derivatives toward the two isozymes, it was decided to determine the effect on isozyme-selective inhibition of introducing these substituents into 8-SEt-Ap5A. The effect of introducing a second 8-SEt group into 8-SEt-Ap5A was also investigated. This report describes the syntheses of P1-[8-(ethylthio)adenosine-5']-P5-[5'(R)-C-methyladenosine-5'] pentaphosphate (4a), its 5'-(R)-C-n-propyl homologue 4b, and P1,P5-bis[8-(ethylthio)adenosine-5'] pentaphosphate [di(8-SEt)-Ap5A], together with kinetic analyses of their inhibitor properties. In addition, in order to extend our studies of the tendency of ATP derivatives to exhibit isozyme-selective inhibitory effects with AK isozymes, the corresponding 5'(R)-alkyl-ATP derivatives and their 5'(S) epimers and a phosphonate isostere of ATP (5) were synthesized, and their substrate and inhibitor properties with AK II and AK-M were evaluated.

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