Master equation approach to protein folding

The dynamics of two 12-monomer heteropolymers on the square lattice is studied exactly within the master equation approach. The time evolution of the occupancy of the native state is determined. At low temperatures, the median folding time follows the Arrhenius law and is governed by the longest...

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Veröffentlicht in:Condensed Matter Physics
Datum:1999
Hauptverfasser: Cieplak, M., Henkel, M., Banavar, J.R.
Sprache:English
Veröffentlicht: Інститут фізики конденсованих систем НАН України 1999
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Zitieren:Master equation approach to protein folding / M. Cieplak, M. Henkel, J.R. Banavar // Condensed Matter Physics. — 1999. — Т. 2, № 2(18). — С. 369-378. — Бібліогр.: 17 назв. — англ.

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Digital Library of Periodicals of National Academy of Sciences of Ukraine
id nasplib_isofts_kiev_ua-123456789-120399
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spelling Cieplak, M.
Henkel, M.
Banavar, J.R.
2017-06-12T06:53:00Z
2017-06-12T06:53:00Z
1999
Master equation approach to protein folding / M. Cieplak, M. Henkel, J.R. Banavar // Condensed Matter Physics. — 1999. — Т. 2, № 2(18). — С. 369-378. — Бібліогр.: 17 назв. — англ.
1607-324X
DOI:10.5488/CMP.2.2.369
PACS: 87.15.By, 87.10.+e
https://nasplib.isofts.kiev.ua/handle/123456789/120399
The dynamics of two 12-monomer heteropolymers on the square lattice is studied exactly within the master equation approach. The time evolution of the occupancy of the native state is determined. At low temperatures, the median folding time follows the Arrhenius law and is governed by the longest relaxation time. For both good and bad folders, significant kinetic traps appear in the folding funnel and the kinetics of the two kinds of folders are quite similar. What distinguishes between the good and bad folders are the differences in their thermodynamic stabilities.
За допомогою методу керуючого рівняння точно проаналізована динаміка двох 12-мономерних гетерополімерів на квадратній гратці. Визначена часова еволюція зайнятості нативного стану. При низьких температурах середній час скручування підлягає закону Ареніуса і визначається найдовшим часом релаксації. Для білків, що добре скручуються, з’являються суттєві кінетичні пастки у наборі послідовних конформацій, у той час як для білків, що погано скручуються, пастки присутні також і в ділянках, що не відповідають нативній конформації.
We thank Jan Karbowski for collaboration and T. X. Hoang for discussions. This work was supported by KBN (Grant No. 2P03B-025-13), Polonium, CNRS-UMR 7556, NASA, and the Applied Research Laboratory at Penn State.
en
Інститут фізики конденсованих систем НАН України
Condensed Matter Physics
Master equation approach to protein folding
Метод керуючого рівняння у явищі скручування білків
published earlier
institution Digital Library of Periodicals of National Academy of Sciences of Ukraine
collection DSpace DC
title Master equation approach to protein folding
spellingShingle Master equation approach to protein folding
Cieplak, M.
Henkel, M.
Banavar, J.R.
title_short Master equation approach to protein folding
title_full Master equation approach to protein folding
title_fullStr Master equation approach to protein folding
title_full_unstemmed Master equation approach to protein folding
title_sort master equation approach to protein folding
author Cieplak, M.
Henkel, M.
Banavar, J.R.
author_facet Cieplak, M.
Henkel, M.
Banavar, J.R.
publishDate 1999
language English
container_title Condensed Matter Physics
publisher Інститут фізики конденсованих систем НАН України
title_alt Метод керуючого рівняння у явищі скручування білків
description The dynamics of two 12-monomer heteropolymers on the square lattice is studied exactly within the master equation approach. The time evolution of the occupancy of the native state is determined. At low temperatures, the median folding time follows the Arrhenius law and is governed by the longest relaxation time. For both good and bad folders, significant kinetic traps appear in the folding funnel and the kinetics of the two kinds of folders are quite similar. What distinguishes between the good and bad folders are the differences in their thermodynamic stabilities. За допомогою методу керуючого рівняння точно проаналізована динаміка двох 12-мономерних гетерополімерів на квадратній гратці. Визначена часова еволюція зайнятості нативного стану. При низьких температурах середній час скручування підлягає закону Ареніуса і визначається найдовшим часом релаксації. Для білків, що добре скручуються, з’являються суттєві кінетичні пастки у наборі послідовних конформацій, у той час як для білків, що погано скручуються, пастки присутні також і в ділянках, що не відповідають нативній конформації.
issn 1607-324X
url https://nasplib.isofts.kiev.ua/handle/123456789/120399
citation_txt Master equation approach to protein folding / M. Cieplak, M. Henkel, J.R. Banavar // Condensed Matter Physics. — 1999. — Т. 2, № 2(18). — С. 369-378. — Бібліогр.: 17 назв. — англ.
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AT henkelm metodkeruûčogorívnânnâuâviŝískručuvannâbílkív
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fulltext Condensed Matter Physics, 1999, Vol. 2, No 2(18), pp. 369–378 Master equation approach to protein folding M.Cieplak 1 , M.Henkel 2 , J.R.Banavar 3 1 Institute of Physics, Polish Academy of Sciences, and College of Sciences, 02-668 Warsaw, Poland 2 Laboratoire de Physique des Matériaux, Université Henri Poincaré Nancy I, F-54506 Vandœuvre, France 3 Department of Physics and Center for Materials Physics, 104 Davey Laboratory, The Pennsylvania State University, University Park, PA 16802 Received June 25, 1998 The dynamics of two 12-monomer heteropolymers on the square lattice is studied exactly within the master equation approach. The time evolution of the occupancy of the native state is determined. At low temperatures, the median folding time follows the Arrhenius law and is governed by the longest relaxation time. For both good and bad folders, significant kinetic traps appear in the folding funnel and the kinetics of the two kinds of folders are quite similar. What distinguishes between the good and bad folders are the differences in their thermodynamic stabilities. Key words: protein folding, kinetic equations PACS: 87.15.By, 87.10.+e 1. Introduction A denatured protein folds into a compact native state in a time of the order of a millisecond after the physiological conditions are restored [1]. This process is reversible and the native state is believed to coincide with the ground state of the system. Studies of simplified lattice models of proteins have provided many insights into the dynamics of the folding process [2]. The crucial feature that makes lattice models useful is the possibility of enumerating the complete set of conformations and determining which of them is the ground state. This can be accomplished provided the length of the heteropolymer, N , is small. Such studies have elucidated the role of thermodynamic stability [2,3], stability against mutations [4] and the existence of a linkage between the rapid folding and the stability of the native state [3]. The key concept that has been introduced to explain the rapid folding occurring in natural proteins is that of the folding funnel [5,6] – a set of conformations that are c© M.Cieplak, M.Henkel, J.R.Banavar 369 M.Cieplak, M.Henkel, J.R.Banavar smoothly connected to the native state, as indicated schematically at the top of figure 1. It is expected that for random sequences of aminoacids there exist competing basins of attraction which would otherwise trap the system away from the native state. This corresponds schematically to what is shown at the bottom of figure 1. It isn’t easy to identify the states belonging to the funnel because of an enormous number of conformations present even for a small N as well as because the problem is a dynamical one. Possible approaches include the monitoring of frequencies of passages between various states in Monte Carlo trajectories [6] or the mapping of states into underlying valleys of effective states [7,8]. Figure 1. A schematic representation of the phase space properties of good (top) and bad (bottom) folders. The vertical axis cor- responds to energy and the horizontal axis to a “coordinate” in the phase space. Essentially all approaches to the studies of the folding dynamics are restricted to Monte Carlo simula- tions that start from a few randomly chosen initial conformations [9]. The only exception is an approach due to Chan and Dill [10] in which an enu- meration of transition rates between classes of conformations which have the same number of contacts and are a given number of kinetic steps away from the native state. Recently, we presented an exact method to study the dynamics of short model proteins [11] which was based on the master equation [13]. We have specifically considered two N=12 sequences, called A and B, which are placed on a square lattice. The dynamics of these sequences can be studied exactly because the se- quences can acquire only N=15037 conformations. The two sequences have the same set of contact energies Bij but their assignment to various monomers i and j is different with the result that A is a good folder and B is a bad folder. The basic finding of [10] is that the qualitative picture corresponding to figure 1 is absolutely correct. By identifying kinetic trap states responsible for the slowest dynamical processes in the system we could demonstrate that the traps for sequence A are within the folding funnel whereas for sequence B the relevant traps form a valley which competes with the native valley similar to the bottom of figure 1. In the current paper we provide a deeper characterization and comparisons of the two sequences and elucidate the nature of the trap states. The sequences that we study are described by the Hamiltonian H = ∑ ij Bij∆ij , (1) 370 Master equation approach to protein folding Figure 2. Top: The native conformation and its energy for sequence A. The enlarged circle shows the first monomer. Main: Dy- namical data for the folding. The solid line marked by tfold gives the median folding time derived from 1000 Monte Carlo trajec- tories. The solid line τ1 is the longest re- laxation time. The broken line t 1 2 with the black circles gives the time for P0(t) to reach 1 2P0 from the uniformly random initial state. The dotted line tA is a fit of the Monte Car- lo data to the Arrhenius law with δE=2.76. The arrow at the top indicates the value of the folding transition temperature. where ∆ij indicates the contact in- teraction Bij assigned to monomers which are geometrical nearest neigh- bours on the lattice but are not neighbours along the sequence. In such arrangements ∆ij is equal to 1, otherwise it is 0. The values of the 25 couplings are chosen as Gaussian numbers which are centred around -1 to provide an overall attraction, as detailed in [10]. The ground state of sequence A is maximally compact and it fills the 3×4 lattice, as shown at the top of figure 2. For sequence B, the ground state, shown at the top of figure 3, is doubly degener- ate. Both of the ground states are compact. However they are not max- imally compact. They differ merely by a placement of one end monomer and therefore they were considered as an effective single native state. We have found that the dynam- ics of A and B are superficially sim- ilar: for both, the median folding time, tfold, and the longest relaxation time, τ1 diverge at low T according to an Arrhenius law. The temper- ature Tmin at which folding to the native state proceeds the fastest is about the same for both sequences. It is the location of the folding transition temperature, T f , with respect to Tmin which distinguishes between sequences A and B. Tf is defined as the temperature at which the equilibrium value of the probability to occupy the native state, P0, crosses 1 2 and is a measure of thermodynamic stability. For bad folders, T f is well below Tmin and thus a substantial occupation probability for the native state is found only in a temperature range in which the dynamics are glassy. For sequence A, the values of T f and Tmin are 0.71 and 1.0±0.1, respectively, while for sequence B, the corresponding values are 0.01 and 1.1 ± 0.1. Thus the two sequences are dynamically similar but the equilibrium properties differ dramatically. 371 M.Cieplak, M.Henkel, J.R.Banavar 2. Methods Figure 3. Same as figure 2, but for sequence B. For the curve tA, δE=3.55. There are two native conformations with the same energy. We study our sequences through an analysis of the master equation and then compare the results to those obtained by the Monte Carlo approach. The master equation does not deal with a specific trajectory but with an ensemble of trajectories and it reads ∂Pα ∂t = ∑ β 6=α [ w(β → α)Pβ (2) −w(α → β)Pα ] , where Pα = Pα(t) is the probabil- ity of finding the sequence in con- formation α at time t. The quantity wαβ = w(β → α) is the transition rate from conformation β to confor- mation α. Of course, writing a mas- ter equation relies on the assumption that a Markov chain description ad- equately describes protein kinetics. In particular, memory effects are assumed to be negligible. The actual derivation of a master equation remains a formidable problem in itself [12]. One may bring this into a matrix form by letting ~P = (P1, . . . , PN ) and mαβ = −wαβ 6 0, α 6= β; , mαα = ∑ β 6=α wβα . (3) The master equation then takes the form of an imaginary-time Schrödinger equation [13,14] ∂t ~P = −M̂ ~P , (4) where the mαβ are the matrix elements of M̂ . The time-dependence state vector ~P (t) at time t = nτ0 can be obtained by applying n times the recursion ~P ((n + 1)τ0) = (1− τ0M̂)~P (nτ0) to ~Pin, where τ0 is a microscopic time associated with a single move and ~Pin is some initial probability distribution. On the other hand, the spectrum of relaxation times τλ = 1/(Re Mλ) > 0 follows directly from the eigenvalues Mλ of M̂ . The transition rates wαβ are designed so that a stationary solution of the master equation corresponds to equilibrium with the Hamiltonian given by equation (1). This can be accomplished provided the detailed balance condition wαβP eq β = wβαP eq α (5) 372 Master equation approach to protein folding is satisfied. Here, P eq α ∼ e−Eα/T is a stationary solution of the master equation and Eα is the energy of the sequence in conformation α. Equation (5) is satisfied by any wαβ = fαβ exp [−(Eα − Eβ)/2T ] provided only that fαβ = fβα. Here, we choose wαβ = w (1) αβ + w (2) αβ , where w (σ) αβ = 2 τ0 Rσ cosh [(Eα − Eβ) /T ] (6) with R1+R2 = 1. Here, σ = 1 and 2 refer to the single- and double-monomer moves respectively. It is understood that w (σ) αβ = 0 if there is no move of type σ linking β with α. The choice (6) guarantees that transition rates are finite and bounded for all temperatures. Similar to [3], we focus on R1 = 0.2 and take the single and two-monomer (crankshaft) moves as in [10]. Because of the detailed balance condition, the eigenvalues Eα are not calculated by diagonalizing M̂ directly, but by diagonalizing an auxiliary matrix K̂ with ele- ments kαβ = vβ vα mαβ = kβα , (7) where vα = e−Eα/2T . The master equation can be then rewritten as ∂t ~Q = −K̂ ~Q , (8) where K̂ is real symmetric and Qα = Pα/vα. This equation is then diagonalized using the standard symmetric Lanczos algorithm without reorthogonalization, as described in [15,16] and then the eigenmodes of M̂ are determined. In particular, since K̂ and M̂ are related by a similarity transformation, all eigenmodes Mλ are real. The eigenvector corresponding to Mλ = 0, i.e. to the infinite relaxation time, de- termines the equilibrium occupancies of the conformations. This eigenvector needs to be normalized to satisfy its probabilistic interpretation. The longest finite relaxation time τ1 = 1/M1 is found from the smallest non-zero eigenvalue M1. Our Monte Carlo simulations were done in a way that satisfies the detailed balance conditions and were devised along the lines described in [10]. For poly- mers, getting these conditions satisfied is not trivial because each conformation has its own number, K, of allowed moves that the conformation can make. Thus the propensities to make a move in a unit time vary from conformation to conforma- tion and the effective “activities” of the conformations need to be matched. This can be accomplished by first determining the maximum value of K, Kmax. For the 12-monomer chain on the square lattice, Kmax is equal to 14. We associate a single time unit with the conformations in which K=Kmax. This means that each move allowed is attempted always with probability 1/Kmax. For a conformation with K allowed moves, the probability to attempt any move is then K/Kmax and the proba- bility not to carry out any attempt is 1 − K/Kmax. The attempted moves are then accepted or rejected as in the standard Metropolis procedure. The probability of a single monomer move (an end flip or a switch in a pair of bonds that make the 90◦ angle) is additionally reduced by the factor of 0.2 and an allowed double monomer 373 M.Cieplak, M.Henkel, J.R.Banavar crankshaft move by 0.8. The time is then measured in terms of the total number of the Monte Carlo attempts divided by Kmax. This scheme not only establishes the detailed balance conditions but it also uses less CPU compared to a process in which moves are attempted regardless of their being allowed or not allowed. 3. Results Figure 4 shows the 4 longest finite relaxation times for sequence A as a function of temperature. It is seen that they are all roughly proportional to each other and they all appear to diverge at T=0, albeit with different energy barriers. The longest relaxation time follows the Arrhenius law, τ1 ∼ eδE1/T with δE1 of about 4.1. The Monte Carlo derived median folding time also follows the Arrhenius law at low tem- peratures but with δE = 2.76± 0.06. The overall Arrhenius-like behaviour suggests that the physics of folding at low T ’s is dominated by processes that establish equi- librium. Their longest time scale is then set by τ1. At temperatures above Tmin, tfold no longer follows τ1. Here, the physics of folding is dominated by the statistics of rare events: the system establishes equilibrium rapidly and then folding is reached by a search in equilibrium. The search becomes more and more random when T becomes larger and larger. For sequence B, similar results are obtained but the Arrhenius barrier in tfold is 3.55± 0.06, whereas δE1 = 4.0±0.06. Figures 2 and 3 show fits to the Arrhenius law for sequences A and B respectively. Figure 4. The four longest relaxation times versus T for sequence A. The very longest, τ1, is drawn by a solid line whereas the re- maining three – by the dotted lines. The value of Tf is indicated by an arrow and the Monte Carlo data on tfold are repeated from figure 2 for a comparison. We now focus on the time evo- lution of the probability, P0(t), to occupy the native state, where t de- notes time. This probability depends on the initial conditions. The solid lines in figure 5 show the evolution of P0(t) when in the initial state all conformations have equal probabil- ity of 1/N to be occupied. The main figure is for sequence A and the time evolution is shown for three temper- atures: 1.2, 0.9 and 0.6. The data for the lowest of these temperatures are also compared with the Monte Carlo evolution. The Monte Car- lo data, obtained by starting from random conformation, agree with the exact evolution. The time scales at which the equilibrium saturation values of P0 are reached are of order τ1. The top portion of figure 5 shows P0(t) for sequence B. It is seen that the saturation levels are significantly 374 Master equation approach to protein folding lower for B than for A at the same temperatures. This reflects a significantly lower value of Tf for B. We also observe, by looking at figures 2 and 3 that the median folding time at low temperatures appears to coincide with the time needed for P 0(t) to reach half of its equilibrium value. Figure 5. Probability of occupation of the native state, P0(t), of sequence A, for three values of the temperatures, indicated on the right. P0(∞) agrees with the equilibrium value. The solid lines correspond to the uni- formly random initial condition and the dot- ted lines correspond to an initial placement of the system in the trap state. The squares correspond to Monte Carlo results, based on 200 random starting conformations. The top figure shows P0(t) for sequence B. The ini- tial condition is that of uniform randomness. The y-axis scale is indicated on the right. The dotted line in figure 5 cor- responds to the initial state being the kinetic “trap” conformation [17] which is the strongest obstacle in reaching equilibrium. If the system starts in the trap state, it will still reach the final equilibrium in a time scale set by τ1 but at shorter times the occupancy of the native state is significantly smaller compared to the start from a totally random state. In general, it is not easy to de- termine which conformation forms the most potent trap. One may at- tempt to determine it by monitor- ing the occupation of the local en- ergy minima in a Monte Carlo pro- cess performed at very low tempera- tures. This approach has been suc- cessfully applied in [8]. Here, the trap state is determined in an ex- act way by studying the eigenvector corresponding to the longest relax- ation time and by identifying the lo- cal energy minima which contribute the most to this eigenvector at low T . The largest weight is associated with the native state. Usually, the second largest weight corresponds to the most relevant trap. This happens provided the second largest occupancy is in a local energy minimum state. A non-minimum state, immediately preceding the native state kinetically, may also possess a significant occupancy but it does not constitute a trap. Thus the search for the most relevant trap goes after non-native local energy minima which have the biggest occupancy. In the limit of T → 0, weights associated with all other local energy minima states become small. We now focus on the interpretation of the trap states to demonstrate the qual- itative validity of figure 1. We place the system in the trap state and ask what is the best trajectory which leads from the trap state to the native state. The best trajectory is defined to be one in which the highest energy state is lower than the highest energy state on all other trajectories. 375 M.Cieplak, M.Henkel, J.R.Banavar Figure 6. The best trajectory linking the trap state of sequence A (shown at the top left) and the native state. The energies in- volved are shown below each conformation. The biggest single step and global energy expenses are indicated at the bottom. Figure 7. As in figure 6 but for sequence B. Figure 6 shows the trap state (of energy -8.9627) for sequence A and the best corresponding trajec- tory that connects it to the native state. The trajectory reaches the na- tive state in 8 steps and it elevates in energy by 4.5323, relative to the the energy of the trap state, after ac- complishing the second step. Thus it takes only two uphill steps to enable a flow to the native state. The first of these steps breaks two contacts and it costs 2.8823 in energy. Thus this biggest single step energy cost is what determines the value of the en- ergy barrier in the Arrhenius law for tfold, as derived through the Monte Carlo technique. On the other hand, δE1, that determines τ1, appears to be governed by the energy costs to make the initial two-step climb to the point of the highest elevation. In a Monte Carlo process, two consec- utive climbs up are not very likely at low T ’s and can be missed. How- ever, the exactly derived longest re- laxation time indicates the true na- ture of the barrier. The kinetics of sequence B is quite similar to that of sequence A. Thus what distinguishes the two sequences are their thermodynamic stabilities as measured by Tf . Figure 7 shows the steps of the best tra- jectory from the the most important trap state for sequence B (of energy – 8.4431) to the native state. The trap state is almost identical in shape to the two native conformations: it is only the positioning of the middle portion of the conformation that is not quite right. And yet it takes 10 steps, like in figure 6, to accomplish the transi- tion between the trap and native states. The overall barrier that is climbed is equal to 4.4 which is close to the Arrhenius barrier δE1 in τ1 of 4.0. The biggest single step 376 Master equation approach to protein folding energy cost of 2.7478 on the trajectory is, however, further away from δE in tfold of about 3.6. The important observation is that for the bad folder B the most relevant trap conformation is still in the folding funnel of the native state. The presence of other low lying valleys that compete with the native valley does not really affect the trapping effects in the native funnel. Instead it generates low stability of the native state through a substantial equilibrium probability of being in some other valleys. Even though our exact results have been obtained in a toy model of only 12 monomers, it is expected that the essential physics of protein folding and the dis- tinction between the good and bad folders are as illustrated here. Tools to study larger and off-lattice systems in this spirit remain to be developed. We thank Jan Karbowski for collaboration and T. X. Hoang for discussions. 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Метод керуючого рівняння у явищі скручування білків М.Цєпляк 1 , М.Генкел 2 , Дж.Р.Беневер 3 1 Інститут фізики Польської Академії Наук та Коледж природничих наук, 02–668 Варшава, Польща 2 Лабораторія фізики матеріалів, Університет Генрі Пуанкаре Нансі I, F–54506 Вандоувр, Франція 3 Факультет фізики і Центр фізики матеріалів, лабораторія Дейвей 104, університет штату Пенсильванія, Юнівесіті Пак, PA 16802, США Отримано 25 червня 1998 р. За допомогою методу керуючого рівняння точно проаналізована ди- наміка двох 12-мономерних гетерополімерів на квадратній гратці. Визначена часова еволюція зайнятості нативного стану. При низь- ких температурах середній час скручування підлягає закону Ареніу- са і визначається найдовшим часом релаксації. Для білків, що до- бре скручуються, з’являються суттєві кінетичні пастки у наборі послі- довних конформацій, у той час як для білків, що погано скручуються, пастки присутні також і в ділянках, що не відповідають нативній кон- формації. Ключові слова: скручування білків, кінетичні рівняння PACS: 87.15.By, 87.10.+e 378