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Why the International Olympic Committee Convened Cyclic activation of endplate acetylcholine receptors Tapan K. Nayaka and Anthony Auerbacha,1 aDepartment of Physiology and Biophysics, State University of New York at Buffalo, Buffalo, NY 14214 Edited by Richard W. Aldrich, The University of Texas at Austin, Austin, TX, and approved September 20, 2017 (received for review June 21, 2017) Agonists turn on receptors because they have a higher affinity for On rare occasions, WT AChRs activate without a bound agonist active versus resting conformations of the protein. Activation can (10, 11). Many mutations throughout the protein increase sub- occur by either of two pathways that connect to form a cycle: stantially the frequency of constitutive openings (12), including some Agonists bind to resting receptors that then become active, or that occur naturally to cause disease (13). Hence, a second possible resting receptors activate and then bind agonists. We used muta- activation sequence is that an unliganded receptor switches on and A tions to construct endplate acetylcholine receptors (AChRs) having the agonist then binds (C ↔ O ↔ O). The equilibrium constants of “ ” only one functional neurotransmitter-binding site and single-channel the two steps of this gate-bind path are E0 (gating without any electrophysiology to measure independently binding constants for agonists) and 1/Jd (dissociation constant for binding to O). The four different agonists, to both resting and active conformations of agonist-independent, unliganded gating equilibrium constant E0 has each site. For all agonists and sites, the total free energy change in been measured for both fetal and adult AChRs (14, 15). each pathway was the same, confirming the activation cycle without These two agonist-activation pathways can be connected to external energy. Other results show that (i) there is no cooperativity form a cycle that, without external energy, must obey the prin- ciple of microscopic reversibility (MR; the total energy change between sites; (ii) agonist association is slower than diffusion for a complete transit around a cycle is zero). A secondary goal in resting receptors but nearly diffusional in active receptors; iii was to measure independently all of the rate constants in the ( ) whereas resting affinity is determined mainly by agonist associ- cycle to ascertain whether or not MR is satisfied in AChRs. If so, ation, active affinity is determined mainly by agonist dissociation; and “ ” iv the coupling constant, which is the factor by which an agonist ( ) at each site and for all agonists, receptor activation approxi- increases the gating equilibrium constant over the basal level mately doubles the agonist-binding free energy. We discuss a two- (E1/E0), will be equal to the equilibrium dissociation constant step mechanism for binding that involves diffusion and a local ratio (Kd/Jd)(SI Appendix, Eq. S1). conformational change (“catch”) that is modulated by receptor ac- Several observations are relevant regarding the mechanism of tivation. The results suggest that binding to a resting site and the agonist binding to adult AChRs. An equilibrium dissociation con- switch to high affinity are both integral parts of a single allosteric stant is the off/on rate constant ratio. The Kd values for agonists of transition. We hypothesize that catch ensures proper signal recog- similar size and charge differ substantially, mainly because of dif- nition in complex chemical environments and that binding site com- ferences in the association rate constant (kon) (16). Further, for all paction is a determinant of both resting and active affinity. agonists, kon is slower than expected from diffusion, and for some, it is temperature-dependent (17). These results suggest that the for- allosteric activation | ion channel | agonist binding | nicotinic mation of the low-affinity AC complex requires both diffusion to the target and a local conformational change of the binding site “ ” cetylcholine receptors (AChRs) are allosteric signaling ( catch ). An inference is that in binding to C, the agonist first forms an ultra-low-affinity “encounter complex” (18, 19) that then converts Aproteins that produce transient membrane currents by A switching globally between a resting C (closed-channel) confor- (via catch) to C. The encounter complex is too short-lived to be detected as a discrete shut interval in electrophysiology experiments. mation and an active O (open-channel) conformation. Agonists are small molecules that bind to AChRs with higher affinity to O versus C. When a resting neuromuscular AChR activates with Significance bound agonists, the newfound ligand-binding energy lowers the energy barrier between C and O and stabilizes the O conformation The binding of agonists to receptors is an essential event in cell so as to increase the activation rate and activation probability signaling. We propose a general mechanism for agonist bind- above their basal levels. ing based on a model allosteric protein, the neuromuscular Neuromuscular AChRs (∼300 kDa) have two α1 subunits and acetylcholine receptor. Binding constants were measured for one each of β, δ, and either e (adult-type) or γ (fetal-type), with different agonists, to both resting and active individual target two neurotransmitter-binding sites located at α–e/γ and α–δ sites. The results confirm a cyclic activation mechanism. Agonist subunit interfaces. The rate and equilibrium constants for bind- binding requires diffusion and a local conformational change, ing to the resting C conformation have been measured for many with receptor activation accelerating the latter so that associ- agonists in wild-type (WT) adult and fetal AChRs (1–4), but only ation becomes nearly diffusion-limited. At each site, receptor a few studies have addressed binding to the active O confor- activation approximately doubles the agonist-binding energy. mation (5, 6). Our primary goal was to compare agonist binding These results indicate that binding (“affinity”) and activation to C versus O at each kind of binding site. (“efficacy”), long considered to be independent processes, are Activation of receptors by agonists can be described by a re- linked obligatorily. We speculate that cyclic activation and action cycle (7–9). In this scheme (Fig. 1), C and O represent coupling between activation and binding are fundamental as- stable end states (energy wells) and the arrows represent un- pects of receptor operation. stable transition states (energy barriers). For a receptor with only one functional binding site, there are two activation pathways Author contributions: T.K.N. and A.A. designed research; T.K.N. performed research; that connect the unliganded resting state C with liganded active T.K.N. contributed new reagents/analytic tools; T.K.N. analyzed data; A.A. wrote the state AO (where the superscripted A is the agonist). The usual paper; and T.K.N. contributed to writing and critical assessment of the manuscript. sequence in WT receptors is that the agonist binds and the re- The authors declare no conflict of interest. ceptor then activates (C ↔ AC ↔ AO). The equilibrium constants This article is a PNAS Direct Submission. of this “bind-gate” path are 1/Kd (dissociation constant for Published under the PNAS license. 1 binding to C) and E1 (gating with one bound agonist). The free To whom correspondence should be addressed. Email: [email protected]. A energy difference, C to O, is the sum of the energy differences This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. for each step in the pathway. 1073/pnas.1711228114/-/DCSupplemental. 11914–11919 | PNAS | November 7, 2017 | vol. 114 | no. 45 www.pnas.org/cgi/doi/10.1073/pnas.1711228114 Downloaded by guest on September 23, 2021 is “closing.” Likewise, “binding” is a complete passage between A A A unliganded and ligand-bound conformations (e.g., C and AC) that C C includes sojourns in the encounter complex. Forward binding is “association,” and backward binding is “dissociation.”“Affinity” is bind the inverse of an equilibrium dissociation constant. C K A α–e. We start by describing rate and equilibrium constants of the d A A C bind-gate pathway (C ↔ C ↔ O) at the adult AChR α–e site gate activated by the partial agonist carbamylcholine (CCh) (Fig. 2A and SI Appendix, Table S1). In these experiments, the α–δ site was disabled by the mutation δP123R so that only α–e was Eo E1 functional. Because these receptors were activated by CCh at A A A only one site, we added background mutations (SI Appendix, O O Table S8) to increase the unliganded gating equilibrium constant CCh SI Appendix gate E0, to put E1 into a suitable range for analysis ( , Eq. S1). The background mutations had no effect on agonist binding (21) (SI Appendix, Fig. S10). A CCh O J O E1 was measured using 20 mM [CCh] to ensure that the d occupancy probability of the resting α–e site was >0.99. After ac- bind counting for a short-lived desensitized state and correcting for the effects of the background mutations and depolarization (which was Fig. 1. Activation pathways. Each receptor has two agonist-binding sites. A applied to reduce fast channel block by the agonist), we estimate CCh = − (superscript), agonist; C, resting state (low-affinity, closed-channel); O, active that E1 0.0026 at the standard condition ( 100 mV). We WT −7 state (high-affinity, open-channel). Vertical steps are gating, and others are know from experiments that E0 in adult AChRs is 7.6 × 10 (14), binding. On the front face, the activation cycle for one binding site shows two pathways connecting C with AO: bind-gate (red) and gate-bind (blue). Kd and Jd, resting and active equilibrium dissociation constants; E0 and E1, unliganded and monoliganded gating equilibrium constants. Without ex- A B ternal energy, E1/E0 = Kd/Jd, where each ratio is the coupling constant. In AChRs, the apparent Kd value is mainly determined by catch rather than by diffusion (SI Appendix,Eq.S6).
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