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Title: The Role of Proton Transport in Gating Current in a Voltage Gated Ion Channel, as Shown by Quantum Calculations

Abstract

Over two-thirds of a century ago, Hodgkin and Huxley proposed the existence of voltage gated ion channels (VGICs) to carry Na+ and K+ ions across the cell membrane to create the nerve impulse, in response to depolarization of the membrane. The channels have multiple physiological roles, and play a central role in a wide variety of diseases when they malfunction. The first channel structure was found by MacKinnon and coworkers in 1998. Subsequently, the structure of a number of VGICs was determined in the open (ion conducting) state. This type of channel consists of four voltage sensing domains (VSDs), each formed from four transmembrane (TM) segments, plus a pore domain through which ions move. Understanding the gating mechanism (how the channel opens and closes) requires structures. One TM segment (S4) has an arginine in every third position, with one such segment per domain. It is usually assumed that these arginines are all ionized, and in the resting state are held toward the intracellular side of the membrane by voltage across the membrane. They are assumed to move outward (extracellular direction) when released by depolarization of this voltage, producing a capacitive gating current and opening the channel. We suggest alternate interpretationsmore » of the evidence that led to these models. Measured gating current is the total charge displacement of all atoms in the VSD; we propose that the prime, but not sole, contributor is proton motion, not displacement of the charges on the arginines of S4. It is known that the VSD can conduct protons. Quantum calculations on the Kv1.2 potassium channel VSD show how; the key is the amphoteric nature of the arginine side chain, which allows it to transfer a proton. This appears to be the first time the arginine side chain has had its amphoteric character considered. We have calculated one such proton transfer in detail: this proton starts from a tyrosine that can ionize, transferring to the NE of the third arginine on S4; that arginine’s NH then transfers a proton to a glutamate. The backbone remains static. A mutation predicted to affect the proton transfer has been qualitatively confirmed experimentally, from the change in the gating current-voltage curve. The total charge displacement in going from a normal closed potential of -70 mV across the membrane to 0 mV (open), is calculated to be approximately consistent with measured values, although the error limits on the calculation require caution in interpretation.« less

Authors:
 [1];  [1]
  1. City College of New York, NY (United States). Dept. of Chemistry and Biochemistry
Publication Date:
Research Org.:
City College of New York, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1483356
Grant/Contract Number:  
SC0012704
Resource Type:
Accepted Manuscript
Journal Name:
Sensors
Additional Journal Information:
Journal Volume: 18; Journal Issue: 9; Journal ID: ISSN 1424-8220
Publisher:
MDPI AG
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; ion channel; gating; gating current; proton transport; quantum calculations on proteins

Citation Formats

Kariev, Alisher M., and Green, Michael E. The Role of Proton Transport in Gating Current in a Voltage Gated Ion Channel, as Shown by Quantum Calculations. United States: N. p., 2018. Web. doi:10.3390/s18093143.
Kariev, Alisher M., & Green, Michael E. The Role of Proton Transport in Gating Current in a Voltage Gated Ion Channel, as Shown by Quantum Calculations. United States. doi:10.3390/s18093143.
Kariev, Alisher M., and Green, Michael E. Tue . "The Role of Proton Transport in Gating Current in a Voltage Gated Ion Channel, as Shown by Quantum Calculations". United States. doi:10.3390/s18093143. https://www.osti.gov/servlets/purl/1483356.
@article{osti_1483356,
title = {The Role of Proton Transport in Gating Current in a Voltage Gated Ion Channel, as Shown by Quantum Calculations},
author = {Kariev, Alisher M. and Green, Michael E.},
abstractNote = {Over two-thirds of a century ago, Hodgkin and Huxley proposed the existence of voltage gated ion channels (VGICs) to carry Na+ and K+ ions across the cell membrane to create the nerve impulse, in response to depolarization of the membrane. The channels have multiple physiological roles, and play a central role in a wide variety of diseases when they malfunction. The first channel structure was found by MacKinnon and coworkers in 1998. Subsequently, the structure of a number of VGICs was determined in the open (ion conducting) state. This type of channel consists of four voltage sensing domains (VSDs), each formed from four transmembrane (TM) segments, plus a pore domain through which ions move. Understanding the gating mechanism (how the channel opens and closes) requires structures. One TM segment (S4) has an arginine in every third position, with one such segment per domain. It is usually assumed that these arginines are all ionized, and in the resting state are held toward the intracellular side of the membrane by voltage across the membrane. They are assumed to move outward (extracellular direction) when released by depolarization of this voltage, producing a capacitive gating current and opening the channel. We suggest alternate interpretations of the evidence that led to these models. Measured gating current is the total charge displacement of all atoms in the VSD; we propose that the prime, but not sole, contributor is proton motion, not displacement of the charges on the arginines of S4. It is known that the VSD can conduct protons. Quantum calculations on the Kv1.2 potassium channel VSD show how; the key is the amphoteric nature of the arginine side chain, which allows it to transfer a proton. This appears to be the first time the arginine side chain has had its amphoteric character considered. We have calculated one such proton transfer in detail: this proton starts from a tyrosine that can ionize, transferring to the NE of the third arginine on S4; that arginine’s NH then transfers a proton to a glutamate. The backbone remains static. A mutation predicted to affect the proton transfer has been qualitatively confirmed experimentally, from the change in the gating current-voltage curve. The total charge displacement in going from a normal closed potential of -70 mV across the membrane to 0 mV (open), is calculated to be approximately consistent with measured values, although the error limits on the calculation require caution in interpretation.},
doi = {10.3390/s18093143},
journal = {Sensors},
number = 9,
volume = 18,
place = {United States},
year = {2018},
month = {9}
}

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C.; Wikstrom, M.; Hummer, G.</span> </li> <li> Proceedings of the National Academy of Sciences, Vol. 106, Issue 33</li> <li> <span class="text-muted related-url">DOI: <a href="https://doi.org/10.1073/pnas.0903938106" class="text-muted" target="_blank" rel="noopener noreferrer">10.1073/pnas.0903938106<span class="fa fa-external-link" aria-hidden="true"></span></a></span> </li> </ul> <hr/> </div> <div> <h2 class="title" style="margin-bottom:0;" data-apporder=""> <a href="https://doi.org/10.1016/j.jtbi.2004.10.021" target="_blank" rel="noopener noreferrer" class="name">A possible role for phosphate in complexing the arginines of S4 in voltage gated channels<span class="fa fa-external-link" aria-hidden="true"></span></a> <small class="text-muted" style="text-transform:uppercase; font-size:0.75rem;"><br/> <span class="type">journal</span>, <span class="date" data-date="2005-04-01">April 2005</span></small> </h2> <ul class="small references-list" style="list-style-type:none; margin-top: 0.5em; padding-left: 0; line-height:1.8em;"> <li> <span style="color:#5C7B2D;"> Green, Michael E.</span> </li> <li> Journal of Theoretical Biology, Vol. 233, Issue 3</li> <li> <span class="text-muted related-url">DOI: <a href="https://doi.org/10.1016/j.jtbi.2004.10.021" class="text-muted" target="_blank" rel="noopener noreferrer">10.1016/j.jtbi.2004.10.021<span class="fa fa-external-link" aria-hidden="true"></span></a></span> </li> </ul> <hr/> </div> <div> <h2 class="title" style="margin-bottom:0;" data-apporder=""> <a href="https://doi.org/10.1021/la500560w" target="_blank" rel="noopener noreferrer" class="name">Direct Evidence of Conformational Changes Associated with Voltage Gating in a Voltage Sensor Protein by Time-Resolved X-ray/Neutron Interferometry<span class="fa fa-external-link" aria-hidden="true"></span></a> <small class="text-muted" style="text-transform:uppercase; font-size:0.75rem;"><br/> <span class="type">journal</span>, <span class="date" data-date="2014-04-16">April 2014</span></small> </h2> <ul class="small references-list" style="list-style-type:none; margin-top: 0.5em; padding-left: 0; line-height:1.8em;"> <li> <span style="color:#5C7B2D;"> Tronin, Andrey Y.; Nordgren, C. Erik; Strzalka, Joseph W.</span> </li> <li> Langmuir, Vol. 30, Issue 16</li> <li> <span class="text-muted related-url">DOI: <a href="https://doi.org/10.1021/la500560w" class="text-muted" target="_blank" rel="noopener noreferrer">10.1021/la500560w<span class="fa fa-external-link" aria-hidden="true"></span></a></span> </li> </ul> <hr/> </div> <div> <h2 class="title" style="margin-bottom:0;" data-apporder=""> <a href="https://doi.org/10.3791/54127" target="_blank" rel="noopener noreferrer" class="name">Site Directed Spin Labeling and EPR Spectroscopic Studies of Pentameric Ligand-Gated Ion Channels<span class="fa fa-external-link" aria-hidden="true"></span></a> <small class="text-muted" style="text-transform:uppercase; font-size:0.75rem;"><br/> <span class="type">journal</span>, <span class="date" data-date="2016-01-01">January 2016</span></small> </h2> <ul class="small references-list" style="list-style-type:none; margin-top: 0.5em; padding-left: 0; line-height:1.8em;"> <li> <span style="color:#5C7B2D;"> Basak, Sandip; Chatterjee, Soumili; Chakrapani, Sudha</span> </li> <li> Journal of Visualized Experiments, Issue 113</li> <li> <span class="text-muted related-url">DOI: <a href="https://doi.org/10.3791/54127" class="text-muted" target="_blank" rel="noopener noreferrer">10.3791/54127<span class="fa fa-external-link" aria-hidden="true"></span></a></span> </li> </ul> <hr/> </div> </div> <div class="pagination-container small"> <a class="pure-button prev page" href="#" rel="prev"><span class="fa fa-angle-left"></span></a><ul class="pagination d-inline-block" style="padding-left:.2em;"></ul><a class="pure-button next page" href="#" rel="next"><span class="fa fa-angle-right"></span></a> </div> </div> </div> <div class="col-sm-3 order-sm-3"> <ul class="nav nav-stacked"> <li class="active"><a href="" class="reference-type-filter tab-nav" data-tab="biblio-references" data-filter="type" data-pattern="*"><span class="fa fa-angle-right"></span> All References</a></li> <li class="small" style="margin-left:.75em; 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float:none;">[ × clear filter / sort ]</a> </div> </form> </div> </div> </div> </section> <section id="biblio-related" class="tab-content tab-content-sec " data-tab="biblio"> <div class="row"> <div class="col-sm-9 order-sm-9"> <section id="biblio-similar" class="tab-content tab-content-sec active" data-tab="related"> <div class="padding"> <p class="lead text-muted" style="font-size: 18px; margin-top:0px;">Similar Records in DOE PAGES and OSTI.GOV collections:</p> <aside> <ul class="item-list" itemscope itemtype="http://schema.org/ItemList" style="padding-left:0; list-style-type: none;"> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="0" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/pages/biblio/1628371-caution-required-interpretation-mutations-voltage-sensing-domain-voltage-gated-channels-evidence-gating-mechanisms" itemprop="url">Caution Is Required in Interpretation of Mutations in the Voltage Sensing Domain of Voltage Gated Channels as Evidence for Gating Mechanisms</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Kariev, Alisher</span> ; <span class="author">Green, Michael</span> <span class="text-muted pubdata"> - International Journal of Molecular Sciences (Online)</span> </span> </div> <div class="abstract">The gating mechanism of voltage sensitive ion channels is generally considered to be the motion of the S4 transmembrane segment of the voltage sensing domains (VSD). The primary supporting evidence came from R→C mutations on the S4 transmembrane segment of the VSD, followed by reaction with a methanethiosulfonate (MTS) reagent. The cys side chain is –SH (reactive form –S<sup>-</sup>); the arginine side chain is much larger, leaving space big enough to accommodate the MTS sulfonate head group. The cavity created by the mutation has space for up to seven more water molecules than were present in wild type, which could<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> be displaced irreversibly by the MTS reagent. Our quantum calculations show there is major reorientation of three aromatic residues that face into the cavity in response to proton displacement within the VSD. Two phenylalanines reorient sufficiently to shield/unshield the cysteine from the intracellular and extracellular ends, depending on the proton positions, and a tyrosine forms a hydrogen bond to the cysteine sulfur with its side chain –OH. These could produce the results of the experiments that have been interpreted as evidence for physical motion of the S4 segment, without physical motion of the S4 backbone. The computations strongly suggest that the interpretation of cysteine substitution reaction experiments be re-examined in the light of these considerations. OPEN</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <span class="fa fa-book text-muted" aria-hidden="true"></span> Cited by 3<div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink">DOI: <a class="misc doi-link " href="https://doi.org/10.3390/ijms16011627" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1628371" data-product-type="Journal Article" data-product-subtype="AM" >10.3390/ijms16011627</a></span></li> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc fulltext-link " href="/pages/servlets/purl/1628371" title="Link to document media" target="_blank" rel="noopener" data-ostiid="1628371" data-product-type="Journal Article" data-product-subtype="AM" >Full Text Available</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="1" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/biblio/1564813-molecular-dynamics-investigation-current-kv1-voltage-sensor-domains" itemprop="url">Molecular Dynamics Investigation of the ω-Current in the Kv1.2 Voltage Sensor Domains</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Khalili-Araghi, Fatemeh</span> ; <span class="author">Tajkhorshid, Emad</span> ; <span class="author">Roux, Benoît</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - Biophysical Journal</span> </span> </div> <div class="abstract">Voltage sensor domains (VSD) are transmembrane proteins that respond to changes in membrane voltage and modulate the activity of ion channels, enzymes, or in the case of proton channels allow permeation of protons across the cell membrane. VSDs consist of four transmembrane segments, S1–S4, forming an antiparallel helical bundle. The S4 segment contains several positively charged residues, mainly arginines, located at every third position along the helix. In the voltage-gated Shaker K<sup>+</sup> channel, the mutation of the first arginine of S4 to a smaller uncharged amino acid allows permeation of cations through the VSD. These currents, known as ω-currents, pass<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> through the VSD and are distinct from K<sup>+</sup> currents passing through the main ion conduction pore. Here we report molecular dynamics simulations of the ω-current in the resting-state conformation for Kv1.2 and for four of its mutants. The four tested mutants exhibit various degrees of conductivity for K<sup>+</sup> and Cl<sup>-</sup> ions, with a slight selectivity for K<sup>+</sup> over Cl<sup>-</sup>. Analysis of the ion permeation pathway, in the case of a highly conductive mutant, reveals a negatively charged constriction region near the center of the membrane that might act as a selectivity filter to prevent permeation of anions through the pore. The residues R1 in S4 and E1 in S2 are located at the narrowest region of the ω-pore for the resting state conformation of the VSD, in agreement with experiments showing that the largest increase in current is produced by the double mutation E1D and R1S.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink">DOI: <a class="misc doi-link " href="https://doi.org/10.1016/j.bpj.2011.10.057" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1564813" data-product-type="Journal Article" data-product-subtype="AC" >10.1016/j.bpj.2011.10.057</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="2" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/biblio/1564674-calculation-gating-charge-kv1-voltage-activated-potassium-channel" itemprop="url">Calculation of the Gating Charge for the Kv1.2 Voltage-Activated Potassium Channel</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Khalili-Araghi, Fatemeh</span> ; <span class="author">Jogini, Vishwanath</span> ; <span class="author">Yarov-Yarovoy, Vladimir</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - Biophysical Journal</span> </span> </div> <div class="abstract">The atomic models of the Kv1.2 potassium channel in the active and resting state, originally presented elsewhere, are here refined using molecular dynamics simulations in an explicit membrane-solvent environment. With a minor adjustment of the orientation of the first arginine along the S4 segment, the total gating charge of the channel determined from >0.5 μs of molecular dynamics simulation is ~12–12.7 e, in good accord with experimental estimates for the Shaker potassium channel, indicating that the final models offer a realistic depiction of voltage-gating. In the resting state of Kv1.2, the S4 segment in the voltage-sensing domain (VSD) spontaneously converts<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> into a 3<sub>10</sub> helix over a stretch of 10 residues. The 3<sub>10</sub> helical conformation orients the gating arginines on S4 toward a water-filled crevice within the VSD and allows salt-bridge interactions with negatively charged residues along S2 and S3. Free energy calculations of the fractional transmembrane potential, acting upon key charged residues of the VSD, reveals that the applied field varies rapidly over a narrow region of 10–15 Å corresponding to the outer leaflet of the bilayer. The focused field allows the transfer of a large gating charge without translocation of S4 across the membrane.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink">DOI: <a class="misc doi-link " href="https://doi.org/10.1016/j.bpj.2010.02.056" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1564674" data-product-type="Journal Article" data-product-subtype="AC" >10.1016/j.bpj.2010.02.056</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="3" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/biblio/1001551-consequences-phosphate-arginine-complexes-voltage-gated-ion-channels" itemprop="url">Consequences of Phosphate-Arginine Complexes in Voltage-Gated Ion Channels</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Green, Michael E</span> <span class="text-muted pubdata"> - Channels, 2(6):395-400</span> </span> </div> <div class="abstract">There are two reasons for suspecting that phosphate complexes of arginine make it very difficult to derive gating charge in voltage gated potassium (and presumably sodium) channels from the motion of charged arginines. For one thing, the arginines should be complexed with phosphate, thereby neutralizing the charge, at least partially. Second, Li et al.(1) have shown that there is a large energy penalty for putting a charged arginine into a membrane. on channel gating current is generally attributed to S4 motion, in that the S4 segment of the voltage sensing domain (VSD) of these channels contains arginines, some of which<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> are not (or at least not obviously) salt bridged, or otherwise charge compensated. There is, however, good reason to expect that there should be a complex of these arginines with phosphate, very probably from lipid headgroups. This has consequences for gating current; the complexed arginines, if they moved, would carry too much of the membrane along. This leads to the suggestion that an alternative to S4 physical motion, H+ transport, should be considered as a possible resolution of the apparent paradox. The consequences for a gating model that was proposed in our earlier work are discussed; there is one major difference in the model in the present form (a conformational change), but the proton cascade as gating current and the role of water in the closed state are reinforced.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink">DOI: <a class="misc doi-link " href="https://doi.org/10.4161/chan.2.6.7097" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1001551" data-product-type="Journal Article" data-product-subtype="AC" >10.4161/chan.2.6.7097</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="4" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/biblio/263056-direct-physical-measure-conformational-rearrangement-underlying-potassium-channel-gating" itemprop="url">Direct physical measure of conformational rearrangement underlying potassium channel gating</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Mannuzzu, L M</span> ; <span class="author">Moronne, M M</span> ; <span class="author">Isacoff, E Y</span> <span class="text-muted pubdata"> - Science</span> </span> </div> <div class="abstract">In response to membrane depolarization, voltage-grated ion channels undergo a structural rearrangement that moves charges or diapoles in the membrane electric field and opens the channel-conducting pathway. By combination of site-specific fluorescent labeling of the Shaker potassium channel protein with voltage clamping, this gating conformational charge was measured in real time. Curing channel activation, a stretch of at least seven amino acids of the putative transmembrane segment S4 moved from a buried postions into the extracellular environment. This movement correlated with the displacement of the gating charge, providing physical evidence in support of the hypothesis that S4 is the voltage<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> sensor of voltage-gated ion channels. 24 refs., 4 figs.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink">DOI: <a class="misc doi-link " href="https://doi.org/10.1126/science.271.5246.213" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="263056" data-product-type="Journal Article" data-product-subtype="AC" >10.1126/science.271.5246.213</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> </ul> </aside> </div> </section> </div> <div class="col-sm-3 order-sm-3"> <ul class="nav nav-stacked"> <li class="active"><a class="tab-nav disabled" data-tab="related" style="color: #636c72 !important; opacity: 1;"><span class="fa fa-angle-right"></span> Similar Records</a></li> </ul> </div> </div> </section> </div></div> </div> </div> </section> <footer class="" style="background-color:#f9f9f9; /* padding-top: 0.5rem; */"> <div class="footer-minor"> <div class="container"> <hr class="footer-separator" /> <div class="text-center" style="margin-top:1.25rem;"> <div class="pure-menu pure-menu-horizontal"> <ul class="pure-menu-list" id="footer-org-menu"> <li class="pure-menu-item"> <a href="https://energy.gov" target="_blank" rel="noopener noreferrer"> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAP///wAAACH5BAEAAAAALAAAAAABAAEAAAICRAEAOw==" class="sprite sprite-footer-us-doe-min" alt="U.S. Department of Energy" /> </a> </li> <li class="pure-menu-item"> <a href="https://www.energy.gov/science/office-science" target="_blank" rel="noopener noreferrer"> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAP///wAAACH5BAEAAAAALAAAAAABAAEAAAICRAEAOw==" class="sprite sprite-footer-office-of-science-min" alt="Office of Science" /> </a> </li> <li class="pure-menu-item"> <a href="/"> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAP///wAAACH5BAEAAAAALAAAAAABAAEAAAICRAEAOw==" class="sprite sprite-footer-osti-min" alt="Office of Scientific and Technical Information" /> </a> </li> </ul> </div> </div> <div class="text-center small" style="margin-top:0.5em;margin-bottom:2.0rem;"> <div class="pure-menu pure-menu-horizontal"> <ul class="pure-menu-list"> <li class="pure-menu-item"><a href="/disclaim" class="pure-menu-link"><span class="fa fa-institution"></span> Website Policies <span class="hidden-xs">/ Important Links</span></a></li> <li class="pure-menu-item"><a href="/pages/contact" class="pure-menu-link"><span class="fa fa-comments-o"></span> Contact Us</a></li> <li class="d-block d-md-none"></li> <li class="pure-menu-item"><a href="https://www.facebook.com/ostigov" target="_blank" rel="noopener noreferrer" class="pure-menu-link social"><span class="fa fa-facebook" style=""></span></a></li> <li class="pure-menu-item"><a href="https://twitter.com/OSTIgov" target="_blank" rel="noopener noreferrer" class="pure-menu-link social"><span class="fa fa-twitter" style=""></span></a></li> <li class="pure-menu-item"><a href="https://www.youtube.com/user/ostigov" target="_blank" rel="noopener noreferrer" class="pure-menu-link social"><span class="fa fa-youtube-play" style=""></span></a></li> </ul> </div> </div> </div> </div> </footer> <link href="/pages/css/pages.fonts.200912.1307.css" rel="stylesheet"> <script src="/pages/js/pages.200912.1307.js"></script><noscript></noscript> <script defer src="/pages/js/pages.biblio.200912.1307.js"></script><noscript></noscript> <script defer src="/pages/js/lity.js"></script><noscript></noscript> <script async type="text/javascript" src="/pages/js/Universal-Federated-Analytics-Min.js?agency=DOE" id="_fed_an_ua_tag"></script><noscript></noscript> </body> <!-- DOE PAGES v.200912.1307 --> </html>