Table Of ContentNuclear Magnetic Resonance of
Paramagnetic Macromolecules
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Series C: Mathematical and Physical Sciences-Vol. 457
Nuclear Magnetic Resonance of
Paramagnetic Macromolecules
edited by
Gerd N. La Mar
Department of Chemistry,
University of California,
Davis, California, U.S.A.
Springer-Science+Business Media, B.V.
Proceedings of the NATO Advanced Research Workshop on
Nuclear Magnetic Resonance of Paramagnetic Macromolecules
Sintra, Portugal
June 4-8, 1994
A C.I.P. Catalogue record for this book is available from the Library of Congress.
ISBN 978-90-481-4522-5 ISBN 978-94-015-8573-6 (eBook)
DOI 10.1007/978-94-015-8573-6
Printed on acid-free paper
All Rights Reserved
© 1995 Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 1995
Softcover reprint of the hardcover 1st edition 1995
No part of the material protected by this copyright notice may be reproduced or
utilized in any form or by any means, electronic or mechanical, including photo
copying, recording or by any information storage and retrieval system, without written
permission from the copyright owner.
This book contains the proceedings of a NATO Advanced Research Workshop held within the programme
of activities of the NATO Special Programme on Supramolecular Chemistry as part of the activities of the
NATO Science Committee.
Other books previously published as a result of the activities of the Special Programme are:
WIPFF, G. (Ed.), Computational Approaches in Supramolecular Chemistry. (ASIC 426) 1994.
ISBN 0-7923-2767-5
FLEISCHAKER, G.R., COLONNA, S. and LUISI, P.L. (Eds.), Self-Production of Supramolecular
Structures. From Synthetic Structures to Models of Minimal Living Systems. (ASIC 446) 1994.
ISBN 0-7923-3163-X
FABBRIZZI, L., POGGI, A. (Eds.), Transition Metals in Supramolecular Chemistry. (ASIC 448) 1994.
ISBN 0-7923-3196-6
BECHER, J., SCHAUMBURG, K. (Eds.), Molecular Engineering for Advanced Materials. (ASIC 456)
1995. ISBN 0-7923-3347-0
TABLE OF CONTENTS
Participants xi
Contributors xvu
New Approaches to NMR of Paramagnetic Molecules
Claudio Luchinat and Mario Piccioli 1
The Hyperfine Coupling
Ivano Bertini and Paula Turano 29
Assignment Strategies and Structure Determination in
Cyanide-Inhibited Heme Peroxidases
Gerd N. La Mar, Zhigang Chen and Jeffrey S. de Ropp 55
Homology Modeling of Horseradish Peroxidase
Andrew T. Smith, Ping Du and Gilda H. Loew 75
NMR Studies of Paramagnetic Systems to Characterise Small
Molecule:Protein and Protein:Protein Interactions
G. R. Moore, M. C. Cox, D. Crowe, M. J. Osborne,
A. G. Mauk and M. T. Wilson 95
Recombinant Perdeuterated Protein as an Efficient Method for
Making Unambiguous Heme Proton Resonance Assignments:
Cyanide-Ligated Glycera Dibranchiata Monomer Methemoglobin
Component IV as an Example
Steve L. Alam, David P. Dutton and James D. Satterlee 123
Redox and Spin-State Control of the Activity of a Diheme
Cytochrome c Peroxidase - Spectroscopic Studies
Susana Prazeres, Isabel Moura, Raymond Gilmour, Graham Pettigrew,
Natarajan Ravi and Boi Hanh Huynh 141
Metalloprotein-Endor-Spectroscopy: Structure Determination
of the Prosthetic Site froin Randomly Oriented Specimen and
Correlations with NMR-Spectroscopy
J. Hiittermann, G. P. Dages, H. Reinhard and G. Schmidt 165
NMR Studies of Nonheme Iron Proteins
Zhigang Wang and Lawrence Que, Jr. 193
Cobalt Substituted Proteins
A. Donaire, J. Salgado, H. R. Jimenez and J. M. Moratal 213
vii
Vlll
Paramagnetic Lanthanide(III) Ions as NMR Probes for
Biomolecular Structure and Function
Li-June Ming 245
Chemical Functions of Single and Double NH---S Hydrogen
Bond in Iron-Sulfur Metalloproteins; Model Ligands with
Cys-Containing Peptide and Simple Acylaminobenzenethiolate
Akira Nakamura and Norikazu Ueyama 265
3D Structure of HiPIPs in Solution Through NMR and
Molecular Dynamics Studies
Lucia Banci and Roberta Pierattelli 281
Multinuclear Magnetic Resonance and Mutagenesis Studies of
Structure-Function Relationships in [2Fe-2S] Ferredoxins
Young Kee Chae, Bin Xia, Hong Cheng, Byung-Ha Oh,
Lars Skjeldal, William M. Westler and John L. Markley 297
lD and 2D Proton NMR Studies on [3Fe-4S] and [4Fe-4S]
Ferredoxins Isolated from Desulfovibrio gigas
Anjos L. Macedo and Jose J. G. Moura 319
Isotropic Proton Hyperfine Coupling in High Potential
[Fe4S4]+3 Models
L. Noodleman, J. -L Chen, D. A. Case, C. Giori, G. Rius,
J. -M. Mouesca and B. Lamotte 339
Spin Dependent Electron Delocalization, Vibronic and
Antiferromagnetic Couplings in Iron-Sulfur Clusters
G. Blondin, E. L. Bominaar, J. -J. Girerd and S. A. Borshch 369
Index 387
PREFACE
The NATO Advanced Research Workshop, "Nuclear Magnetic Resonance of
Paramagnetic Macromolecules", took place at the Hotel Tivoli, Sintra, Portugal on June
4-8, 1994. The contents of this monograph represent the lectures at this Workshop.
The unique and valuable information content of the NMR spectra of paramagnetic
macromolecules has been recognized since the initial report on the spectrum of
cytochrome c (A. Kowalsky (1965) Biochemistry, 4, 2382). However, the road to
developing the methods for first detecting, then assigning the resonances of active site
residues, and lastly interpreting the hyperfine shifts and relaxation in terms of molecular
and electronic structure, has been a long and tortuous one. Nevertheless, the past decade
has witnessed not only a strong resurgence in the interest in NMR of paramagnetic
macromolecules, but also remarkable progress in the experimental methodology and
understanding of the origins of the paramagnetically influenced spectral parameters.
Hence the broad and in-depth potential of NMR studies on paramagnetic macromolecules
has been clearly established.
This workshop was organized to assess the current status of NMR studies of
paramagnetic macromolecules with respect to the scope and limitations of the needed
experimental approaches, the interpretive bases of the hyperfine shifts and relaxation for
defining both molecular and electronic structure, and the range of systems which can be
studied. The subject matter of the lectures, moreover, was not restricted to NMR
studies, but included key contributions on the theoretical framework for interpreting
NMR spectral parameters of spin-coupled chromophores, and computational approaches
for modeling solution structure of macromolecules with paramagnetic centers.
Two classes of systems have played a key role in the development of the field of
NMR in paramagnetic macromolecules, heme proteins and iron-sulfur proteins. The
unique role played by these two systems is due, in part, to their diverse function,
structure and genetic origin, but largely because they contain well-defined chromophores,
each of which can be studied in detail outside the protein matrix. These systems
constitute the most successfully studied macromolecules, and a major portion (first eight
and last six) of the seventeen contributions deal with heme and/or iron-sulfur proteins.
The middle three chapters survey the progress on, and significant promise of, more
difficult systems which do not possess a chromophore, but nevertheless have yielded
remarkable insight into their structure in spite of the complexities.
The Director is grateful to the members of the Organizing Committee, Ivana
Bertini, Bernard Lamotte, Geoffrey R. Moore and Isabel Moura, for their contributions in
planning the program, to Anjos L. Macedo for making all local arrangements in Sintra,
and to Kendra L. Tanner for valuable and expert assistance in both organizing the
Workshop and completing this monograph. Most importantly, the Director and
Organizing Committee are indebted to the Scientific and Environmental Affairs Division
of NATO, and to Alain Jubier, Director of the Supramolecular Chemistry Program, for
the generous financial support of the Advanced Research Workshop.
Gerd N. La Mar, Director
August 20, 1994
ix
PARTICIPANTS
Lucia BANCI • University of Florence, Via G. Caponi 7,1-50121 Florence, Italy
Nursen BAYRAKTAR • Marmara Research Center, Research Institute for Basic
Sciences, Department of Chemistry, P.O. Box 21,41470 Gebze, Turkey
Moshe BELINSKII• School of Chemistry, Tel Aviv University, Ramat-Aviv 69 976,
P.O. Box 39040, Tel-Aviv, Israel
lvano BERTINI • Professor of Inorganic Chemistry, University of Florence, Via G.
Caponi 7, 1-50121 Florence, Italy
Sergei BORSHCH • IRC, CNRS, 69626 Villeurbanne Cedex, France
Catherine BOUGAULT • Centre d'Etudes Nucleaires de Grenoble DRFMC SESAM
SCPM, CEA, 17 rue des Martyrs, 38054 Grenoble Cedex 9, France
Michael CAFFREY • Institut de Biologie Structurale, CNRS CEA, 41, Avenue des
Martyrs, 38027 Grenoble Cedex 1 France
Jorge CALDEIRA • Universidade Nova de Lisboa, Departamento de Quimica,
Faculdade de Ciencias e Tecnologia, 2825 Monte de Caparica, Portugal
Gerard W. CANTERS • Department of Chemistry, Gorlaeus Laboratory, Leid en
University, P.O. Box 9502, 2300 RA Leiden, The Netherlands
Carla M. CARNEIRO • Instituto de Tecnologia Quimica e Biol6gica, Universidade
Nova de Lisboa, Rua da Quinta Grande 6, Apartado 127, 2780 Oeiras, Portugal
David A. CASE • Scripps Research Institute, Department of Molecular Biology, 10666
N. Torrey Pines Road, La Jolla, CA 92037 USA
Kimber CLARK • University of California, Department of Chemistry, Davis, CA
95616 USA
Christina COSTA • Universidade Nova de Lisboa, Departamento de Quimica,
Faculdade de Ciencias e Tecnologia, 2825 Monte de Caparica, Portugal
Helena S. COSTA • Instituto de Tecnologia Quimica e Biol6gica, Universidade Nova
de LisboaL, Rua da Quinta Grande, 6, Apartado 127, P-2780 Oeiras, Portugal
Isabel B. COUTINHO • Instituto de Tecnologia Quimica e Biol6gica, Universidade
Nova de Lisboa, Rua da Quinta Grande, 6, Apartado 127, P-2780 Oeiras,
Portugal
Sharon DAVY • University of East Anglia, School of Chemical Sciences, Norwich
NR4 7TJ, England
Xl
