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Methods in
Molecular Biology 1929

Claus W. Heizmann Editor

Calcium-Binding
Proteins of
the EF-Hand
Superfamily
From Basics to Medical Applications
METHODS IN MOLECULAR BIOLOGY

Series Editor
John M. Walker
School of Life and Medical Sciences
University of Hertfordshire
Hatfield, Hertfordshire, AL10 9AB, UK

For further volumes:

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 Calcium-Binding Proteins
of the EF-Hand Superfamily

From Basics to Medical Applications

Edited by

Claus W. Heizmann
Division of Clinical Chemistry and Biochemistry, Department of Pediatrics,
University of Zürich, Zürich, Switzerland
Editor
Claus W. Heizmann
Division of Clinical Chemistry
and Biochemistry
Department of Pediatrics
University of Zürich
Zürich, Switzerland

ISSN 1064-3745 ISSN 1940-6029 (electronic)

Methods in Molecular Biology
ISBN 978-1-4939-9029-0 ISBN 978-1-4939-9030-6 (eBook)
https://doi.org/10.1007/978-1-4939-9030-6
Library of Congress Control Number: 2018967209

© Springer Science+Business Media, LLC, part of Springer Nature 2019

This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is
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The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to
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The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Cover Illustration: The cover image is taken from Kozlyuk et al. (Chapter 18), and it represents the binding of calcium to
the S100A12 protein

This Humana Press imprint is published by the registered company Springer Science+Business Media, LLC, part of
Springer Nature.
The registered company address is: 233 Spring Street, New York, NY 10013, U.S.A.
Preface

A major direction in medical research leading to clinical applications targets the regulation of
intracellular calcium and the various human diseases associated with an altered homeostasis of
this global messenger. After entering the cell, Ca2+ is reversibly complexed to Ca2+-binding
proteins of the EF-hand superfamily which decipher the information carried by Ca2+ and pass
it on to various targets, receptors, and channels. Many proteins of this family are of
major clinical importance in cardiomyopathy, inflammation, allergy, brain disorders, and
cancer as predictive biomarkers in modern laboratory medicine and as novel therapeutic
drug targets.
One example is the measurement of troponin, the first intracellular Ca2+-sensor protein
to be discovered, is nowadays the “gold standard” in the diagnosis of patients with acute
coronary syndrome. Parvalbumins were the first Ca2+-binding proteins to have their amino
sequence and atomic 3D structure resolved, are selective markers of neurons in the CNS,
and are also known to be the major allergens in fish. In addition, parvalbumin gene transfer
in an animal model was able to correct diastolic heart failure. Mutations in calmodulin were
identified in individuals affected by severe cardiac arrhythmias suggesting that this protein
could be a therapeutic target for some cardiac disorders. Inhibition of calcineurin by
cyclosporine A or FK506 has been proven to be beneficial in preventing rejection of
allogeneic organ transplants, and members of the penta-EF-hand (PEF) protein family
(calpains, sorcin, or ALGs) are of clinical relevance in cardiovascular diseases and oncology.
S100 proteins constitute the largest subgroup within the EF-hand protein family with
intracellular and extracellular, cytokine-like functions. Some members are routinely analyzed
in practical laboratory medicine, e.g., S100B is an established biomarker for malignant
melanoma and traumatic brain injury, S100A4 is known to be an angiogenic factor inducing
tumor progression and metastasis, and S100A8/A9 is involved in inflammatory and auto-
immune diseases and several types of cancer. Drug discovery efforts exploiting the identifi-
cation of selective Ca2+-binding protein inhibitors are underway for specific
pharmacological interventions and personalized treatments.
Individual chapters provide step-by-step protocols for studying the many facets of Ca2+-
signaling and Ca2+-binding with background information on the principle and application
of these techniques. This volume also contains a few chapters with more general reviews on
the clinical importance of this protein family.
Part I includes data mining to explore calmodulin bibliography, modern technologies
such as deep two-photon and high-resolution imaging, molecular MR imaging methods,
measurement of contractility and calcium release in cardiac spheroids, simultaneous record-
ings of subcellular Ca2+-signals from the cytosol and sarco/endoplasmic reticulum, and
designing Ca2+-binding proteins for molecular MR imaging.
Part II includes the expression and purification of calmodulin, calpain, plastins, MICU2,
ALG-2, calumenin GCAPs, swiprosin/EFhd2, Ca2+-binding proteins from parasitic worms,
and S100 proteins for structural studies (NMR- and X-ray crystallography), other biophysi-
cal applications, metal-binding studies, as well as interactions with target proteins and small
molecule inhibitors. Other chapters provide detailed protocols of gene transfers of Ca2+-
binding proteins to cardiomyocytes, dissecting the role of calcineurin by using Cre-loxP
inducible mouse models, analysis of S100 in DNA damage repair, Fluorine-18 labeling of

v
vi Preface

S100 proteins for positron emission tomography, and tryptophan scanning mutagenesis of
EF-hand motifs.
Part III includes the analysis of Ca2+-binding proteins as important diagnostic and
prognostic biomarkers in laboratory medicine. This includes high-sensitive troponin assays
in the clinical diagnosis of patients with acute coronary syndrome, measurements of S100B
as biomarker for head injury and melanoma, S100A7 in psoriasis, S100A8/A9 in myocardial
infarction, and S100A12 in fecal samples of children and adults.
All chapters include an introduction to their respective topics, a comprehensive list of
the required materials, step-by-step and readily reproducible laboratory protocols, and key
tips on troubleshooting to avoid known pitfalls. These methods and techniques are generally
applicable to many other areas of basic and applied medical research and laboratory
medicine.
This volume is a collection of chapters written by leading experts in the field containing
state-of-the-art, lab-based methods and easy-to-follow protocols for daily use, making it
interesting for basic and medical researchers, cell and molecular biologists, clinicians, clinical
chemists, and the diagnostic industry.
I am very grateful to all the contributors for the opportunity to make this volume
possible, to my daughter Melanie Heizmann for her expert secretarial assistance, and to my
wife Erika Heizmann for her patience and understanding during the process of editing
this book.

Zürich, Switzerland Claus W. Heizmann

About the Editor

CLAUS W. HEIZMANN Professor em. of Clinical Biochemistry at

the University of Zürich, Switzerland. He received his
Diploma in Chemistry from the University of Basel,
Switzerland, and his PhD degree in 1970 from the
University of Konstanz, Germany. Subsequently, he was
trained as a postdoctoral fellow at the University Hospital,
Basel, in the laboratory of Dr. Edmond Fischer at the
Department of Biochemistry at the University of
Washington, Seattle, at the Department of Cell Biology at
the Federal Institute of Technology (ETH), Zürich, and was
an independent researcher at the Institute of Pharmacology
and Biochemistry at the University of Zürich. From 1989 to
2007 he was Director of the Division of Clinical Chemistry
and Biochemistry at the Department of Pediatrics, University
of Zürich. He was visiting professor at the Mie University, Tsu,
Japan, and general secretary of the Swiss Society for Clinical
Chemistry (SGKC). His research focuses on “the Structures
and Functions of the Ca2+-Binding Proteins of the EF-Hand
Superfamily and their Targets in Health and Disease.” He was
a co-founding, board, and honorary member of the European
Calcium Society (ECS) and its first president. He is co-editor
of the special issues on calcium published in Biochimica et
Biophysica Acta-Molecular Cell Research, the author of more
than 400 scientific publications, and editor of several books
including Calcium-Binding Proteins and RAGE: From
Structural Basics to Clinical Applications (Vol 963, 2013)
and Calcium-Binding Proteins of the EF-Hand Superfamily:
From Basics to Medical Applications (Vol 1929, 2019).

vii
Contents

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v
About the Editor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii
Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiii

PART I DATA ANALYSIS AND MODERN TECHNOLOGIES TO STUDY

CALCIUM-BINDING AND SIGNALING IN CELLS

1 Using Data Mining to Explore Calmodulin Bibliography . . . . . . . . . . . . . . . . . . . . 3

Jacques Haiech and Marie-Claude Kilhoffer
2 Deep Two-Photon Imaging In Vivo with a Red-Shifted
Calcium Indicator. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
Antje Birkner and Arthur Konnerth
3 High-Resolution Calcium Imaging Method for Local Calcium Signaling . . . . . . 27
Björn-Philipp Diercks, René Werner, Daniel Schetelig, Insa M. A. Wolf,
and Andreas H. Guse
4 Measurement of Contractility and Calcium Release in Cardiac Spheroids . . . . . . 41
Christian Zuppinger
5 Simultaneous Recording of Subcellular Ca2+ Signals from the Cytosol
and Sarco/Endoplasmic Reticulum: Compartmentalized Dye Loading,
Imaging, and Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
Ernst Niggli and Miguel Fernandez-Tenorio
6 The Use of Complementary Luminescent and Fluorescent Techniques
for Imaging Ca2+ Signaling Events During the Early Development
of Zebrafish (Danio rerio) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
Sarah E. Webb and Andrew L. Miller
7 Cellular Ca2+-Responding Nanoluciferase Reporter Gene System
Directed by Tandemly Repeated Pseudo-palindromic NFAT-Response
Elements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
Wei Zhang, Terunao Takahara, Takuya Achiha, Hideki Shibata,
and Masatoshi Maki
8 Designing Calcium-Binding Proteins for Molecular MR Imaging . . . . . . . . . . . . . 111
Mani Salarian, Shenghui Xue, Oluwatosin Y. Ibhagui,
and Jenny J. Yang
9 Coordination to Divalent Cations by Calcium-Binding Proteins . . . . . . . . . . . . . . 127
Masayuki Nara, Hisayuki Morii, and Masaru Tanokura
10 Chaperoning Against Amyloid Aggregation: Monitoring
In Vitro and In Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
Ravichandran Vignesh and Gopala Krishna Aradhyam

ix
x Contents

PART II THE SUPERFAMILY OF CALCIUM-BINDING PROTEINS

CHARACTERIZED BY THE EF-HAND STRUCTURAL MOTIF

11 Ca2+-Binding Proteins of the EF-Hand Superfamily: Diagnostic

and Prognostic Biomarkers and Novel Therapeutic Targets . . . . . . . . . . . . . . . . . . 157
Claus W. Heizmann
12 Gene Transfer of Calcium-Binding Proteins into Adult Cardiac Myocytes. . . . . . 187
Brian R. Thompson, Houda Cohen, Addeli Bez Batti Angulski,
and Joseph M. Metzger
13 Expression and Purification of Calmodulin for NMR and Other
Biophysical Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207
Benjamin M. M. Grant, Christopher B. Marshall, and Mitsuhiko Ikura
14 The Use of Cre/loxP Inducible Mouse Models to Dissect the
Specific Roles of Calcineurin Signaling in Myeloid Cells . . . . . . . . . . . . . . . . . . . . . 223
Teresa Zelante and Jan Frič
15 Calpain Purification Through Calpastatin and Calcium: Strategy
and Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233
Hung Huy Nguyen, Peter Tompa, and Kris Pauwels
16 Characterization of the EF-Hand Calcium-Binding Domains
of Human Plastins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245
Oleg Khassan, Katharine V. Jensen, Andrew G. Woodman,
Hans J. Vogel, and Hiroaki Ishida
17 Expression and Characterization of MICU2, a Ca2+ Sensor Protein . . . . . . . . . . . 261
Wenping Wu, Jimin Zheng, and Zongchao Jia
18 S100 Proteins in the Innate Immune Response to Pathogens . . . . . . . . . . . . . . . . 275
Natalia Kozlyuk, Andrew J. Monteith, Velia Garcia,
and Steven M. Damo, Eric P. Skaar, and Walter J. Chazin
19 Targeting S100 Calcium-Binding Proteins with Small Molecule Inhibitors. . . . . 291
Paul T. Wilder, Kristen M. Varney, and David J. Weber
20 Monitoring Interactions Between S100B and the Dopamine D2
Receptor Using NMR Spectroscopy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311
Yuning Wang, Roya Tadayon, and Gary S. Shaw
21 Isolation and Characterization of S100 Protein-Protein Complexes . . . . . . . . . . . 325
Bence Kiss, Péter Ecsédi, Márton Simon, and Lászl
o Nyitray
22 The Multifaceted S100A4 Protein in Cancer and Inflammation. . . . . . . . . . . . . . . 339
Noona Ambartsumian, Jörg Klingelhöfer, and Mariam Grigorian
23 Interaction of S100A6 with Target Proteins In Vitro and in Living Cells . . . . . . 367
Kyohei Sakane, Fuminori Yamaguchi, Mitsumasa Tsuchiya,
and Rina Kondo, Naoki Kanayama, Masaki Magari,
and Naoya Hatano, Ryoji Kobayashi, and Hiroshi Tokumitsu
24 Preparation of the Oxidized and Reduced Forms of Psoriasin (S100A7) . . . . . . . 379
Lisa S. Cunden and Elizabeth M. Nolan
25 Preparation and Iron Redox Speciation Study of the Fe(II)-Binding
Antimicrobial Protein Calprotectin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397
Rose C. Hadley and Elizabeth M. Nolan
 Contents xi

26 Structural Analysis of S100A8 Complex with Zinc and Calcium:

A General Protocol for the Study of S100 Proteins in the Presence
of Divalent Cations by X-Ray Crystallography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417
Laure Yatime
27 Analysis of Ca2+-Dependent Weibel–Palade Body Tethering
by Live Cell TIRF Microscopy: Involvement
of a Munc13-4/S100A10/Annexin A2 Complex . . . . . . . . . . . . . . . . . . . . . . . . . . . 437
Nina Criado Santos, Tarek Chehab, Anna Holthenrich,
and Volker Gerke
28 Analysis of S100A11 in DNA Damage Repair . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 447
Franziska Foertsch and Christian Melle
29 Fluorine-18 Labeling of S100 Proteins for Small Animal Positron
Emission Tomography. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 461
Markus Laube, Torsten Kniess, Christin Neuber, Cathleen Haase-Kohn,
and Jens Pietzsch
30 Reviewing the Crystal Structure of S100Z and Other Members
of the S100 Family: Implications in Calcium-Regulated Quaternary
Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487
Vito Calderone, Marco Fragai, and Claudio Luchinat
31 High Sensitive Quantitative Binding Assays Using a Nanoluciferase-Fused
Probe for Analysis of ALG-2-Interacting Proteins. . . . . . . . . . . . . . . . . . . . . . . . . . . 501
Wei Zhang, Rina Matsuo, Terunao Takahara, Hideki Shibata,
and Masatoshi Maki
32 Calcium-Induced Protein Folding in Calumenin and Calmodulin. . . . . . . . . . . . . 517
Marco Mazzorana and Thomas Lykke-Møller Sørensen
33 Measuring Calumenin Impact on ER-Calcium Depletion Using
Transient Calumenin Overexpression and Silencing . . . . . . . . . . . . . . . . . . . . . . . . . 539
Réginald Philippe and Olivier Mignen
34 Secretagogin Purification and Quality Control Strategies for Biophysical
and Cell Biological Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 551
Anand Kumar Sharma, Radhika Khandelwal, and Yogendra Sharma
35 Tryptophan Scanning Mutagenesis of EF-Hand Motifs . . . . . . . . . . . . . . . . . . . . . . 567
Uday Kiran, Michael R. Kreutz, Yogendra Sharma, and Asima
Chakraborty
36 Mapping Calcium-Sensitive Regions in GCAPs by Site-Specific
Fluorescence Labelling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 583
Karl-Wilhelm Koch and Jens Christoffers
37 Quantification of Human Swiprosin-1/EFhd2 Expression on Protein
and RNA Level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 595
Barbara G. Fürnrohr and Dirk Mielenz
38 Three-Dimensional Reconstruction Imaging Method to Study
the Function of EFHD2 in Invadopodia Formation. . . . . . . . . . . . . . . . . . . . . . . . . 607
Yun Hyun Huh, Yu Ra Yeo, and Woo Keun Song
39 Characterization of Calcium-Binding Proteins from Parasitic Worms . . . . . . . . . . 615
Charlotte M. Thomas and David J. Timson
xii Contents

PART III BIOMARKERS, DIAGNOSTICS AND LABORATORY MEDICINE

40 High-Sensitivity Troponin Assays in Clinical Diagnostics of Acute

Coronary Syndrome. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 645
Danielle Hof and Arnoldvon Eckardstein
41 Targeted Mass Spectrometry of S100 Proteins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 663
Juan Martı́nez-Aguilar and Mark P. Molloy
42 Clinical Use of the Calcium-Binding S100B Protein, a Biomarker
for Head Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 679
Ramona Astrand and Johan Undén
43 Serum S100B Levels in Melanoma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 691
Anna Lisa Frauchiger, Reinhard Dummer, and Joanna Mangana
44 The Ca2+-Binding S100B Protein: An Important Diagnostic
and Prognostic Neurobiomarker in Pediatric Laboratory Medicine. . . . . . . . . . . . 701
Diego Gazzolo, Francesca Pluchinotta, Giuseppe Lapergola,
and Simone Franchini
45 S100A7 in Psoriasis: Immunodetection and Activation by CRISPR
technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 729
Mariagrazia Granata, Evangelia Skarmoutsou, Maria Clorinda
Mazzarino, and Fabio D’Amico
46 S100A8/A9 in Myocardial Infarction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 739
Gopalkrishna Sreejit, Sunil Kiran Nooti, Baskaran Athmanathan,
and Prabhakara Reddy Nagareddy
47 Enzyme-Linked Immunosorbent Assay to Measure S100A12
in Fecal Samples of Children and Adults . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 755
Steven T. Leach and Andrew S. Day
48 S100 Proteins as Biomarkers in Risk Estimations for Malignant
Transformation in Oral Lesions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 763
Rainer Probstmeier, Dominik Kraus, Matthias Wenghoefer,
and Jochen Winter

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 773
Contributors

TAKUYA ACHIHA  Department of Applied Molecular Biosciences, Graduate School of

Bioagricultural Sciences, Nagoya University, Nagoya, Japan
NOONA AMBARTSUMIAN  Faculty of Health, Department of Neuroscience, Copenhagen
University, Copenhagen, Denmark
ADDELI BEZ BATTI ANGULSKI  Department of Integrative Biology and Physiology, University
of Minnesota Medical School, Minneapolis, MN, USA
GOPALA KRISHNA ARADHYAM  Signal Transduction Laboratory, Department of
Biotechnology, Bhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology
Madras, Chennai, India
RAMONA ASTRAND  Department of Neurosurgery, Rigshospitalet, Copenhagen University
Hospital, Copenhagen, Denmark
BASKARAN ATHMANATHAN  Department of Pathology, University of Alabama, Birmingham,
AL, USA
ANTJE BIRKNER  Institute of Neuroscience, Technical University of Munich, Munich,
Germany; Munich Cluster for Systems Neurology (SyNergy) and Center for Integrated
Protein Sciences (CIPSM), Munich, Germany
VITO CALDERONE  CERM, University of Florence, Sesto Fiorentino, Florence, Italy;
Department of Chemistry Ugo Schiff, University of Florence, Sesto Fiorentino, Florence,
Italy
ASIMA CHAKRABORTY  CSIR-Centre for Cellular and Molecular Biology (CCMB),
Hyderabad, India
WALTER J. CHAZIN  Department of Biochemistry, Vanderbilt University, Nashville, TN,
USA; Center for Structural Biology, Vanderbilt University, Nashville, TN, USA;
Department of Chemistry, Vanderbilt University, Nashville, TN, USA
TAREK CHEHAB  Centre for Molecular Biology of Inflammation, Institute of Medical
Biochemistry, University of Münster, Münster, Germany
JENS CHRISTOFFERS  Organic Chemistry, Faculty V, Institut für Chemie, University of
Oldenburg, Oldenburg, Germany
HOUDA COHEN  Department of Integrative Biology and Physiology, University of Minnesota
Medical School, Minneapolis, MN, USA
NINA CRIADO SANTOS  Centre for Molecular Biology of Inflammation, Institute of Medical
Biochemistry, University of Münster, Münster, Germany; Department of Cell Physiology
and Metabolism, University of Geneva, Geneva, Switzerland
LISA S. CUNDEN  Department of Chemistry, Massachusetts Institute of Technology,
Cambridge, MA, USA
FABIO D’AMICO  Department of Biomedical and Biotechnological Sciences, University of
Catania, Catania, Italy
STEVEN M. DAMO  Department of Biochemistry, Vanderbilt University, Nashville, TN,
USA; Center for Structural Biology, Vanderbilt University, Nashville, TN, USA;
Department of Life and Physical Sciences, Fisk University, Nashville, TN, USA
ANDREW S. DAY  School of Women’s and Children’s Health, University of New South Wales
Medicine, Sydney, Australia; Department of Pediatrics, University of Otago
(Christchurch), Christchurch, New Zealand

xiii
xiv Contributors

BJÖRN-PHILIPP DIERCKS  The Calcium Signalling Group, Department of Biochemistry and

Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Hamburg,
Germany
REINHARD DUMMER  Department of Dermatology, University Hospital Zurich, Zurich,
Switzerland
PÉTER ECSÉDI  Department of Biochemistry, ELTE Eötvös Loránd University, Budapest,
Hungary
MIGUEL FERNANDEZ-TENORIO  Department of Physiology, University of Bern, Bern,
Switzerland
FRANZISKA FOERTSCH  Biomolecular Photonics Group, Jena University Hospital, Jena,
Germany
MARCO FRAGAI  CERM, University of Florence, Sesto Fiorentino, Florence, Italy;
Department of Chemistry Ugo Schiff, University of Florence, Sesto Fiorentino, Florence,
Italy
SIMONE FRANCHINI  Neonatal Intensive Care Unit, Department of Pediatrics, University of
Chieti, Chieti, Italy
ANNA LISA FRAUCHIGER  Department of Dermatology, University Hospital Zurich, Zurich,
Switzerland
JAN FRIČ  Center for Translational Medicine, International Clinical Research Center, St.
Anne’s University Hospital Brno, Brno, Czechia
BARBARA G. FÜRNROHR  Division of Molecular Immunology, Department of Internal
Medicine III, Nikolaus-Fiebiger-Center, University of Erlangen-Nürnberg, Erlangen,
Germany
VELIA GARCIA  Center for Structural Biology, Vanderbilt University, Nashville, TN, USA;
Department of Chemistry, Vanderbilt University, Nashville, TN, USA
DIEGO GAZZOLO  Neonatal Intensive Care Unit, Department of Pediatrics, University of
Chieti, Chieti, Italy; Neonatal Intensive Care Unit, Department of Maternal, Fetal and
Neonatal Medicine, C. Arrigo Children’s Hospital, Alessandria, Italy
VOLKER GERKE  Centre for Molecular Biology of Inflammation, Institute of Medical
Biochemistry, University of Münster, Münster, Germany
MARIAGRAZIA GRANATA  Department of Biomedical and Biotechnological Sciences, University
of Catania, Catania, Italy
BENJAMIN M. M. GRANT  Department of Medical Biophysics, University of Toronto, Toronto,
ON, Canada; Princess Margaret Cancer Centre, University Health Network, Toronto,
ON, Canada
MARIAM GRIGORIAN  Faculty of Health, Department of Neuroscience, Copenhagen
University, Copenhagen, Denmark
ANDREAS H. GUSE  The Calcium Signalling Group, Department of Biochemistry and
Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Hamburg,
Germany
CATHLEEN HAASE-KOHN  Department of Radiopharmaceutical and Chemical Biology,
Helmholtz-Zentrum Dresden-Rossendorf, Institute of Radiopharmaceutical Cancer
Research, Dresden, Germany
ROSE C. HADLEY  Department of Chemistry, Massachusetts Institute of Technology,
Cambridge, MA, USA
JACQUES HAIECH  CNRS UMR7242 BSC, ESBS, Illkirch Cedex, France
NAOYA HATANO  Applied Cell Biology, Graduate School of Interdisciplinary Science and
Engineering in Health Systems, Okayama University, Kita-ku, Okayama, Japan
 Contributors xv

CLAUS W. HEIZMANN  Department of Pediatrics, Division of Clinical Chemistry and

Biochemistry, University of Zürich, Zürich, Switzerland
DANIELLE HOF  Unilabs, Dübendorf, Dübendorf, Switzerland
ANNA HOLTHENRICH  Centre for Molecular Biology of Inflammation, Institute of Medical
Biochemistry, University of Münster, Münster, Germany
YUN HYUN HUH  Cell Logistics and Silver Health Research Center, School of Life Sciences,
Gwangju Institute of Science and Technology, Gwangju, Republic of Korea
OLUWATOSIN Y. IBHAGUI  Department of Chemistry, Center for Diagnostics and
Therapeutics, Georgia State University, Atlanta, GA, USA
MITSUHIKO IKURA  Department of Medical Biophysics, University of Toronto, Toronto, ON,
Canada; Princess Margaret Cancer Centre, University Health Network, Toronto, ON,
Canada
HIROAKI ISHIDA  Biochemistry Research Group, Department of Biological Sciences,
University of Calgary, Calgary, AB, Canada
KATHARINE V. JENSEN  Biochemistry Research Group, Department of Biological Sciences,
University of Calgary, Calgary, AB, Canada
ZONGCHAO JIA  Department of Biochemical and Molecular Science, Queen University,
Kingston, ON, Canada
NAOKI KANAYAMA  Applied Cell Biology, Graduate School of Interdisciplinary Science and
Engineering in Health Systems, Okayama University, Kita-ku, Okayama, Japan
RADHIKA KHANDELWAL  CSIR-Centre for Cellular and Molecular Biology, Hyderabad,
India; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India
OLEG KHASSAN  Biochemistry Research Group, Department of Biological Sciences, University
of Calgary, Calgary, AB, Canada
MARIE-CLAUDE KILHOFFER  CNRS UMR7242 BSC, ESBS, Illkirch Cedex, France
UDAY KIRAN  CSIR-Centre for Cellular and Molecular Biology (CCMB), Hyderabad,
India; Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India
BENCE KISS  Department of Biochemistry, ELTE Eötvös Loránd University, Budapest,
Hungary
JÖRG KLINGELHÖFER  Faculty of Health, Department of Neuroscience, Copenhagen
University, Copenhagen, Denmark
TORSTEN KNIESS  Department of GMP Radiopharmaceuticals Production, Helmholtz-
Zentrum Dresden-Rossendorf, Institute of Radiopharmaceutical Cancer Research,
Dresden, Germany
RYOJI KOBAYASHI  Sakuragi Psychiatric Hospital, Mima, Tokushima, Japan
KARL-WILHELM KOCH  Biochemistry Group, Department of Neuroscience, Faculty VI,
University of Oldenburg, Oldenburg, Germany
RINA KONDO  Applied Cell Biology, Graduate School of Interdisciplinary Science and
Engineering in Health Systems, Okayama University, Kita-ku, Okayama, Japan
ARTHUR KONNERTH  Institute of Neuroscience, Technical University of Munich, Munich,
Germany; Munich Cluster for Systems Neurology (SyNergy) and Center for Integrated
Protein Sciences (CIPSM), Munich, Germany
NATALIA KOZLYUK  Department of Biochemistry, Vanderbilt University, Nashville, TN,
USA; Center for Structural Biology, Vanderbilt University, Nashville, TN, USA
DOMINIK KRAUS  Department of Prosthodontics, Preclinical Education, and Material
Sciences, University of Bonn, Bonn, Germany
MICHAEL R. KREUTZ  RG Neuroplasticity, Leibniz Institute for Neurobiology, Magdeburg,
Germany; Leibniz Group ‘Dendritic Organelles and Synaptic Function’, University
xvi Contributors

Medical Center Hamburg-Eppendorf, Center for Molecular Neurobiology, ZMNH,

Hamburg, Germany
GIUSEPPE LAPERGOLA  Neonatal Intensive Care Unit, Department of Pediatrics, University
of Chieti, Chieti, Italy
MARKUS LAUBE  Department of Radiopharmaceutical and Chemical Biology, Helmholtz-
Zentrum Dresden-Rossendorf, Institute of Radiopharmaceutical Cancer Research,
Dresden, Germany
STEVEN T. LEACH  School of Women’s and Children’s Health, University of New South Wales
Medicine, Sydney, Australia
CLAUDIO LUCHINAT  CERM, University of Florence, Sesto Fiorentino, Florence, Italy;
Department of Chemistry Ugo Schiff, University of Florence, Sesto Fiorentino, Florence,
Italy
MASAKI MAGARI  Applied Cell Biology, Graduate School of Interdisciplinary Science and
Engineering in Health Systems, Okayama University, Kita-ku, Okayama, Japan
MASATOSHI MAKI  Department of Applied Molecular Biosciences, Graduate School of
Bioagricultural Sciences, Nagoya University, Nagoya, Japan
JOANNA MANGANA  Department of Dermatology, University Hospital Zurich, Zurich,
Switzerland
CHRISTOPHER B. MARSHALL  Princess Margaret Cancer Centre, University Health Network,
Toronto, ON, Canada
JUAN MARTÍNEZ-AGUILAR  Red de Apoyo a la Investigaci
on, Universidad Nacional
Aut
onoma de México, INCMNSZ, Mexico City, Mexico
RINA MATSUO  Department of Applied Molecular Biosciences, Graduate School of
Bioagricultural Sciences, Nagoya University, Nagoya, Japan
MARIA CLORINDA MAZZARINO  Department of Biomedical and Biotechnological Sciences,
University of Catania, Catania, Italy
MARCO MAZZORANA  Diamond Light Source, Harwell Science and Innovation Campus,
Didcot, UK
CHRISTIAN MELLE  Biomolecular Photonics Group, Jena University Hospital, Jena, Germany
JOSEPH M. METZGER  Department of Integrative Biology and Physiology, University of
Minnesota Medical School, Minneapolis, MN, USA
DIRK MIELENZ  Division of Molecular immunology, Department of Internal Medicine III,
Nikolaus-Fiebiger-Center, University of Erlangen-Nürnberg, Erlangen, Germany
OLIVIER MIGNEN  Laboratoire Canalopathies & Signalisation Calcique, INSERM U1227,
Université de Bretagne Occidentale (UBO), Brest, France
ANDREW L. MILLER  Division of Life Science and State Key Laboratory of Molecular
Neuroscience, HKUST, Clear Water Bay, Hong Kong, People’s Republic of China
MARK P. MOLLOY  Bowel Cancer and Biomarker Research, Kolling Institute, Royal North
Shore Hospital, The University of Sydney, St. Leonards, Australia
ANDREW J. MONTEITH  Department of Pathology, Microbiology, and Immunology,
Vanderbilt University Medical Center, Nashville, TN, USA
HISAYUKI MORII  Department of Chemistry, College of Liberal Arts and Sciences, Tokyo
Medical and Dental University, Chiba, Japan
PRABHAKARA REDDY NAGAREDDY  Department of Pathology, University of Alabama,
Birmingham, AL, USA
MASAYUKI NARA  Department of Chemistry, College of Liberal Arts and Sciences, Tokyo
Medical and Dental University, Chiba, Japan
 Contributors xvii

CHRISTIN NEUBER  Department of Radiopharmaceutical and Chemical Biology, Helmholtz-

Zentrum Dresden-Rossendorf, Institute of Radiopharmaceutical Cancer Research,
Dresden, Germany
HUNG HUY NGUYEN  VIB-VUB Centre for Structural Biology (VIB CSB), Vlaams Instituut
voor Biotechnologie (VIB), Brussels, Belgium; Structural Biology Brussels (SBB),
Department of Biotechnology (DBIT), Vrije Universiteit Brussel (VUB), Brussels, Belgium
ERNST NIGGLI  Department of Physiology, University of Bern, Bern, Switzerland
ELIZABETH M. NOLAN  Department of Chemistry, Massachusetts Institute of Technology,
Cambridge, MA, USA
SUNIL KIRAN NOOTI  Department of Pathology, University of Alabama, Birmingham, AL,
USA
LÁSZLÓ NYITRAY  Department of Biochemistry, ELTE Eötvös Loránd University, Budapest,
Hungary
KRIS PAUWELS  VIB-VUB Centre for Structural Biology (VIB CSB), Vlaams Instituut voor
Biotechnologie (VIB), Brussels, Belgium; Structural Biology Brussels (SBB), Department of
Biotechnology (DBIT), Vrije Universiteit Brussel (VUB), Brussels, Belgium
RÉGINALD PHILIPPE  Institut National de la Santé et de la Recherche Médicale, U1151,
Paris, France
JENS PIETZSCH  Department of Radiopharmaceutical and Chemical Biology, Helmholtz-
Zentrum Dresden-Rossendorf, Institute of Radiopharmaceutical Cancer Research,
Dresden, Germany; Faculty of Chemistry and Food Chemistry, Technische Universit€ at
Dresden, Dresden, Germany
FRANCESCA PLUCHINOTTA  Department of Pediatric Cardiac Surgery, IRCCS San Donato
Milanese Hospital, Milan, Italy
RAINER PROBSTMEIER  Neuro- and Tumor Cell Biology Group, Department of Nuclear
Medicine, University Hospital Bonn, University of Bonn, Bonn, Germany
KYOHEI SAKANE  Applied Cell Biology, Graduate School of Interdisciplinary Science and
Engineering in Health Systems, Okayama University, Kita-ku, Okayama, Japan
MANI SALARIAN  Department of Chemistry, Center for Diagnostics and Therapeutics,
Georgia State University, Atlanta, GA, USA
DANIEL SCHETELIG  Department of Computational Neuroscience, University Medical
Center Hamburg-Eppendorf, Hamburg, Germany
ANAND KUMAR SHARMA  CSIR-Centre for Cellular and Molecular Biology, Hyderabad,
India
YOGENDRA SHARMA  CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India;
Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India
GARY S. SHAW  Department of Biochemistry, The University of Western Ontario, London,
ON, Canada
HIDEKI SHIBATA  Department of Applied Molecular Biosciences, Graduate School of
Bioagricultural Sciences, Nagoya University, Nagoya, Japan
MÁRTON SIMON  Department of Biochemistry, ELTE Eötvös Loránd University, Budapest,
Hungary
ERIC P. SKAAR  Department of Pathology, Microbiology, and Immunology, Vanderbilt
University Medical Center, Nashville, TN, USA
EVANGELIA SKARMOUTSOU  Department of Biomedical and Biotechnological Sciences,
University of Catania, Catania, Italy
WOO KEUN SONG  Cell Logistics and Silver Health Research Center, School of Life Sciences,
Gwangju Institute of Science and Technology, Gwangju, Republic of Korea
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