Biopolymers

VOLUME 99 NUMBER 3 MARCH 2013

PDB40: The Protein Data Bank Celebrates its 40th Birthday Guest Editors: Stephen K. Burley and Kenneth J. Breslauer
View this journal online at wileyonlinelibrary.com

Editor-in-chief:
Gary D. Glick University of Michigan, Ann Arbor, Michigan USA Executive Editor: Kenneth J. Breslauer Rutgers University, Piscataway, New Jersey, USA Associate Editors: Jean Baum Rutgers University, Piscataway, New Jersey USA Stephen Blacklow Harvard University Boston, Massachusetts, USA C. Allen Bush University of Maryland Baltimore, Maryland USA David A. Case Rutgers University, Piscataway, New Jersey, USA Robert Glaeser University of California Berkeley Berkeley, California USA

J. A. McCammon University of California, San Diego La Jolla, California USA Joel Schneider Department of Chemistry and Biochemistry, University of Delaware, Newark, DE USA Eric J. Toone Duke University Durham, North Carolina USA Nils G. Walter University of Michigan Ann Arbor, Michigan USA David E. Wemmer University of California, Berkeley Berkeley, California USA Alfred Wittinghofer Max Planck Institute Dortmund, Germany Sarah A. Woodson Johns Hopkins University Baltimore, Maryland, USA

Biopolymers Advisory Board

Ettorre Benedetti Naples, Italy David N. Beratan Durham, NC, USA Helen M. Berman Piscataway, NJ, USA David L. Beveridge Middletown, CT, USA David Bocian Riverside, CA, USA Philip E. Bourne La Jolla, CA, USA Axel T. Brunger Stanford, CA, USA Charles M. Deber Toronto, ONT, Canada Peter Dervan Pasadena, CA, USA Ken A. Dill San Francisco, CA, USA David Draper Baltimore, MD, USA H. Jane Dyson La Jolla, CA, USA Elliot L. Elson St. Louis, MO, USA Carol A. Fierke Ann Arbor, MI, USA Maxim D. FrankKamenetskii Boston, MA, USA Ernesto Freire Baltimore, MD, USA Michael K. Gilson Rockville, MD, USA Roger Goody Dortmund, Germany

Christian Griesinger Gttingen, Germany Helmut Grubmller Gttingen, Germany Michael H. Hecht Princeton, NJ, USA Volkhard Helms Saarbrcken, Germany Dan Herschlag Palo Alto, CA, USA Barbara Imperiali Cambridge, MA, USA Thomas M. Jovin Gttingen, Germany Robert Kaptein Utrecht, The Netherlands Isabella Karle Washington, DC, USA Timothy Keiderling Chicago, IL, USA Stephen Kent Chicago, IL, USA Horst Kessler Garching, Germany Sung-Ho Kim Berkeley, CA, USA Toru Kitagawa Osaka, Japan Yuji Kobayashi Osaka, Japan Eric T. Kool Stanford, CA, USA Irwin D. Kuntz San Francisco, CA, USA Joseph Lakowicz Baltimore, MD, USA Jrg Langowski Heidelberg, Germany

David M. J. Lilley Dundee, United Kingdom John L. Markley Madison, WI, USA Dale F. Mierke Providence, RI, USA Luis Moroder Martinsried, Germany Fred Naider Staten Island, NY, USA Terrence G. Oas Durham, NC, USA Wilma K. Olson New Brunswick, NJ, USA Stanley J. Opella La Jolla, CA, USA Dinshaw J. Patel New York, NY, USA Evaristo Peggion Padova, Italy B. Monte Pettitt Houston, TX, USA M. Thomas Record, Jr. Madison, WI, USA Alex Rich Cambridge, MA, USA Benoit Roux Chicago, IL, USA John A. Schellman Eugene, OR, USA Harold A. Scheraga Ithaca, NY, USA Nadrian C. Seeman New York, NY, USA Lawerence Shapiro New York, NY, USA Molly S. Shoichet Toronto, ONT, Canada John D. Simon Durham, NC, USA

Giulietta Smulevich Florence, Italy Nancy C. Stellwagen Iowa City, IA, USA Bjorn Torger Stokke Trondheim, Norway Junichi Takagi Osaka, Japan Mitsuo Tasumi Saitama, Japan Ignacio Tinoco, Jr. Berkeley, CA, USA David Tirrell Pasadena, CA, USA Olke C. Uhlenbeck Evanston, IL, USA Peter H. von Hippel Eugene, OR, USA Rebecca Wade Heidelberg, Germany Jamie Williamson La Jolla, CA, USA Peter Wolynes La Jolla, CA, USA Kurt Wthrich Zurich, Switzerland Founding Editors: Elkan Blout Harvard Medical School Boston, Massachusetts, USA Murray Goodman, University of California, San Diego La Jolla, California, USA Ephraim (Katchalski) Katzir The Weizmann Institute of Science Rehovot, Israel

Aims and Scope: BIOPOLYMERS publishes original research papers and review articles in the general area of macromolecular structure and function, as well as biologically relevant model systems. Manuscripts should report on studies that examine biological macromolecules (naturally occurring and designed), their interactions, reactions, and macromolecular assemblies at structural, chemical, and physical levels. The Journal strives to publish high-impact papers that will significantly enhance our understanding of the chemistry and/or the biology of the systems under investigation. Reports describing techniques that could be applied to the study of biological macromolecules will be considered for publication only if they will have broad utility to the biochemical and biophysical research community. For more information, please visit wileyonlinelibrary.com/biopolymers. BIOPOLYMERS (ISSN 0006-3525) is published 18 times per year by Wiley Subscription Services, Inc., a Wiley Company, 111 River Street, Hoboken, NJ 07030. US mailing agent: Mercury Media Processing, LLC 1634 East Elizabeth Ave, Linden NJ 07036 USA. Periodical postage paid at Rahway, NJ. Copyright 2013 Wiley Periodicals, Inc. All rights reserved. No part of this publication may be reproduced, stored or transmitted in any form or by any means without the prior permission in writing from the copyright holder. Authorization to photocopy items for internal and personal use is granted by the copyright holder for libraries and other users registered with their local Reproduction Rights Organisation (RRO), e.g. Copyright Clearance Center (CCC), 222 Rosewood Drive, Danvers, MA 01923, USA (www.copyright.com), provided the appropriate fee is paid directly to the RRO. This consent does not extend to other kinds of copying such as copying for general distribution, for advertising or promotional purposes, for creating new collective works or for resale. Special requests should be addressed to: permissionsuk@wiley.com. Disclaimer: The Publisher and Editors cannot be held responsible for errors or any consequences arising from the use of information contained in this journal; the views and opinions expressed do not necessarily reflect those of the Publisher and Editors, neither does the publication of advertisements constitute any endorsement by the Publisher and Editors of the products advertised. Postmaster: Send all address changes to BIOPOLYMERS, Journal Customer Services, John Wiley & Sons Inc., 350 Main St., Malden, MA 02148-5020. Information for subscribers: BIOPOLYMERS is published in 18 issues per year. Institutional subscription prices for 2013 are: Online: US$12,181 (US), US$12,181

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1 This paper meets the requirements of ANSI/NISO Z39.48-1992

(Permanence of Paper).

TableofContents
iv 165
Research Highlights

Editorial
PDB40: The Protein Data Bank Celebrates its 40th Birthday S. K. Burley Published online 15 November 2012

Articles
Cover Illustration:
Some examples of the diversity and complexity of the structures found in the Protein Data Bank are shown. Top row: beta-adrenergic GPCR from 2rh1;1 middle row: hemoglobin from 2dhb,2 potassium channel from 1bl8,3 Paramecium bursaria Chlorella virus type 1 from 1m4x;4 bottom row: photosynthetic reaction center from 1prc,5 cAMP-dependent Protein Kinase (PKA) from 3tnp,6 nuclear pore complex from EMD-1097,7 and ribosome from 3pio.8 1. Cherezov, V.; Rosenbaum, D. M.; Hanson, M. A.; Rasmussen, S. G.; Thian, F. S.; Kobilka, T. S.; Choi, H. J.; Kuhn, P.; Weis, W. I.; Kobilka, B. K.; Stevens, R. C. Science 2007, 318, 12581265. 2. Bolton, W.; Perutz, M. F. Nature 1970, 228, 551552. 3. Doyle, D. A.; Morais Cabral, J.; Pfuetzner, R. A.; Kuo, A.; Gulbis, J. M.; Cohen, S. L.; Chait, B. T.; MacKinnon, R. Science 1998, 280, 6977. 4. Nandhagopal, N.; Simpson, A. A.; Gurnon, J. R.; Yan, X.; Baker, T. S.; Graves, M. V.; Van Etten, J. L.; Rossmann, M. G. Proc Natl Acad Sci USA 2002, 99, 1475814763. 5. Deisenhofer, J.; Epp, O.; Sinning, I.; Michel, H. J Mol Biol 1995, 246, 429457. 6. Zhang, P.; Smith-Nguyen, E. V.; Keshwani, M. M.; Deal, M. S.; Kornev, A. P.; Taylor, S. S. Science 2012, 335, 712716. 7. Beck, M.; Forster, F.; Ecke, M.; Plitzko, J. M.; Melchior, F.; Gerisch, G.; Baumeister, W.; Medalia, O. Science 2004, 306, 13871390. 8. Belousoff, M. J.; Shapira, T.; Bashan, A.; Zimmerman, E.; Rozenberg, H.; Arakawa, K.; Kinashi, H.; Yonath, A. Proc Natl Acad Sci USA 2011, 108, 27172722.

170 183 189 196 203 218

Invited Review: Studying and Polishing the PDB's Macromolecules J. S. Richardson and D. C. Richardson Published online 22 June 2012 Invited Review: Abstracting Knowledge from the Protein Data Bank N. Furnham, R. A. Laskowski, and J. M. Thornton Published online 22 June 2012 The Impact of Influenza Hemagglutinin Fusion Peptide Length and Viral Subtype on Its Structure and Dynamics J. L. Lorieau, J. M. Louis, and A. Bax Published online 7 June 2012 Invited Review: Sweet EntanglementsProtein:Glycan Interactions in Two HIV-Inactivating Lectin Families L. M. I. Koharudin and A. M. Gronenborn Published online 22 June 2012 Review: A Primer in Macromolecular Linguistics D. B. Searls Published online 7 June 2012 Mini Review: The Future of the Protein Data Bank H. M. Berman, G. J. Kleywegt, H. Nakamura, and J. L. Markley Published online 25 July 2012

Biopolymers and Peptide Science are now publishing Preprints online within 5 days of acceptance*! Preprints are peer-reviewed articles that are published online in EarlyView T before copyediting and author correction. Preprint articles are citable by DOI. The final copyedited, author-corrected, paginated version is available shortly thereafter within 12 weeks of first submission.
*Upon receipt of all necessary materials (figure files, signed Copyright Transfer Agreement, etc. from authors).