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TGF-β Signaling Methods and Protocols
Book in Methods in molecular biology (Clifton, N.J.) · June 2015
DOI: 10.1007/978-1-4939-2966-5
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Methods in
Molecular Biology 1344
Xin-Hua Feng
Pinglong Xu
Xia Lin Editors
TGF-β
Signaling
Methods and Protocols
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:
http://www.springer.com/series/7651
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qwwwwwww
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TGF-β Signaling
Methods and Protocols
Edited by
Xin-Hua Feng
Life Sciences Institute and Innovation Center for Cell Signaling Network,
Zhejiang University, Hangzhou, Zhejiang Province, China; Departments of Surgery,
and Molecular & Cellular Biology, Baylor College of Medicine, Houston, Texas, USA
Pinglong Xu
Life Sciences Institute, Zhejiang University, Hangzhou, Zhejiang Proviince, China
Xia Lin
Department of Surgery, Baylor College of Medicine, Houston, USA
xupl@zju.edu.cn
Editors
Xin-Hua Feng
Life Sciences Institute and Innovation
Center for Cell Signaling Network
Zhejiang University, Hangzhou
Zhejiang Province, China
Pinglong Xu
Life Sciences Institute
Zhejiang University
Hangzhou, Zhejiang Proviince, China
Xia Lin
Department of Surgery
Baylor College of Medicine
Houston, USA
Departments of Surgery
and Molecular & Cellular Biology
Baylor College of Medicine
Houston, Texas, USA
ISSN 1064-3745
ISSN 1940-6029 (electronic)
Methods in Molecular Biology
ISBN 978-1-4939-2965-8
ISBN 978-1-4939-2966-5 (eBook)
DOI 10.1007/978-1-4939-2966-5
Library of Congress Control Number: 2015951954
Springer New York Heidelberg Dordrecht London
© Springer Science+Business Media New York 2016
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is
concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction
on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation,
computer software, or by similar or dissimilar methodology now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not
imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and
regulations and therefore free for general use.
The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to
be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty,
express or implied, with respect to the material contained herein or for any errors or omissions that may have been made.
Printed on acid-free paper
Humana Press is a brand of Springer
Springer Science+Business Media LLC New York is part of Springer Science+Business Media (www.springer.com)
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Preface
Cells that respond to environmental cues through the complex and dynamic network of
signaling pathways maintain a critical balance between cellular proliferation, differentiation,
and death. Since the original discovery of TGF-β about more than 30 years ago, the molecule only represents a prototype of a large family that consists of at least 33 members encoded
by the human genome. The TGF-β superfamily members are secreted proteins, including
TGF-β, activins, bone morphogenetic proteins, growth/differentiation factors, and
Müllerian inhibiting substance, and can regulate many developmental processes in a range of
organisms from worms to humans. At cellular level, they control a wide range of cellular
functions such as proliferation, death, differentiation, and other functions in many cell types.
Dysfunctions of the TGF-β family members often result in the pathogenesis of cancer, autoimmune diseases, diabetes, heart disease, hereditary hemorrhagic telangiectasia, Marfan syndrome, Vascular Ehlers-Danlos syndrome, Loeys–Dietz syndrome, and neurodegenerative
diseases. The characterization of the TGF-β family underscores its importance in physiological and pathophysiological functions.
The research on TGF-β biology, including its regulation, signaling, and physiological
functions, has developed rapidly into a large field with thousands of publications per year.
In the last 20 years, the components of the canonical signaling pathways—the TGF-β receptors and downstream intracellular effectors Smad proteins—have been identified, and the
concept for context-dependent TGF-β actions has been well established. Many conventional methodologies or state-of-the-art technologies have been employed to elucidate how
the TGF-β pathways are regulated and what functions they have in the context from single
cells to complexed tissues to the whole organism. The rapidly evolving nature of TGF-β
signaling research also necessitates a continuous updating of methods used. TGF-β
Signaling: Methods and Protocols brings together a comprehensive collection of methods
and techniques in TGF-β signaling research that are scientifically grounded within the cancer and development fields. Thus, this volume grows out of the necessity that a comprehensive method book covering biochemical, molecular, and biological description of TGF-β
ligands, receptors, and intracellular events is needed for researchers who are already in the
TGF-β field and for those who wish to enter the field.
This volume provides the reader with up-to-date information in this continuing evolving field and attempts to take the reader into the exciting realm of TGF-β from the basic
principles to the practical applications. All the chapters are provided by leading researchers
in the TGF-β field. The first chapter by Budi and Derynck gives a basic introduction of
TGF-β receptor signaling at the cell surface. Subsequent chapters are generally concerned
with methods and techniques for the investigation of TGF-β signaling mechanism including receptors, intracellular kinases, microRNA, epigenetic regulation, post-translational
regulations, non-Smad pathway; the physiological implications including those in
epithelial-mesenchymal transition, endothelial cells, adipogenesis, Th differentiation, stem
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Preface
cell, bone remodeling, ovary, zebrafish development, and frog animal capping; and the
methodologies including metastasis imaging, 3D morphogenesis, membrane receptor
quantification, conditional knockout, bone remodeling, kinase and phosphatase assays,
BiFC interaction assays, and genome-wide siRNA screen.
This book would not be possible were it not for all the contributors who devoted their
precious time and considerable energy to bring this volume into reality and provide such
clear and detailed accounts of their experimental protocols and useful hints. We are greatly
indebted to them for their excellent contributions and for their patience in dealing with the
editors. I also wish to thank Dr. P.J. Higgins and their overall help and patience in keeping
the book on track. We hope this volume will prove valuable to all researchers, rookie or
veteran, in the TGF-β signaling field and serve as a useful reference for many years to come.
Hangzhou, China and Houston, TX, USA
Hangzhou, China
Houston, TX, USA
xupl@zju.edu.cn
Xin-Hua Feng
Pinglong Xu
Xia Lin
Contents
Preface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
v
ix
1 Regulation of TGF-β Receptors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Erine H. Budi, Jian Xu, and Rik Derynck
2 Determining TGF-β Receptor Levels in the Cell Membrane . . . . . . . . . . . . . .
Long Zhang, Fangfang Zhou, Maarten van Dinther, and Peter ten Dijke
3 Posttranslational Modifications of TGF-β Receptors . . . . . . . . . . . . . . . . . . . .
Xiaohua Yan and Ye-Guang Chen
4 Production, Isolation, and Structural Analysis of Ligands
and Receptors of the TGF-β Superfamily. . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Tao Huang and Andrew P. Hinck
5 Phosphorylation of Smads by Intracellular Kinases. . . . . . . . . . . . . . . . . . . . . .
Fang Liu and Isao Matsuura
6 Analysis of Smad Phosphatase Activity In Vitro . . . . . . . . . . . . . . . . . . . . . . . .
Tao Shen, Lan Qin, and Xia Lin
7 Three-dimensional Mammary Epithelial Cell Morphogenesis Model
for Analysis of TGFß Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Juliet Rashidian and Kunxin Luo
8 TGF-β Signaling in Stem Cell Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Wenlin Li, Wanguo Wei, and Sheng Ding
9 Analysis of Epithelial–Mesenchymal Transition Induced
by Transforming Growth Factor β . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Ulrich Valcourt, Jonathon Carthy, Yukari Okita, Lindsay Alcaraz,
Mitsuyasu Kato, Sylvie Thuault, Laurent Bartholin, and Aristidis Moustakas
10 In Vitro Th Differentiation Protocol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Takashi Sekiya and Akihiko Yoshimura
11 Interrogating TGF-β Function and Regulation in Endothelial Cells. . . . . . . . .
J.A. Maring, L.A. van Meeteren, M.J. Goumans, and Peter ten Dijke
12 Isolation and Manipulation of Adipogenic Cells to Assess TGF-β
Superfamily Functions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Maria Namwanje, Juan C. Bournat, and Chester W. Brown
13 Imaging TGFβ Signaling in Mouse Models of Cancer Metastasis . . . . . . . . . . .
Yibin Kang
14 Generation and Characterization of Smad7 Conditional Knockout Mice . . . . .
Yi Pan and Yan Chen
15 Monitoring Smad Activity In Vivo Using the Xenopus Model System . . . . . . .
Marco Montagner, Graziano Martello, and Stefano Piccolo
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49
63
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111
121
137
147
183
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219
233
245
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Contents
16 Animal Cap Assay for TGF-β Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Chenbei Chang
17 Detection of Smad Signaling in Zebrafish Embryos . . . . . . . . . . . . . . . . . . . . .
Xingfeng Liu, Qiang Wang, and Anming Meng
18 Role of TGF-β Signaling in Coupling Bone Remodeling . . . . . . . . . . . . . . . . .
Janet L. Crane, Lingling Xian, and Xu Cao
19 Studying the Functions of TGF-β Signaling in the Ovary. . . . . . . . . . . . . . . . .
Chao Yu, Jian-Jie Zhou, and Heng-Yu Fan
20 Quantitative Real-Time PCR Analysis of MicroRNAs and Their
Precursors Regulated by TGF-β Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Hara Kang and Akiko Hata
21 TGF-β-Regulated MicroRNAs and Their Function in Cancer Biology . . . . . . .
Pengyuan Yang, Yun Zhang, Geoffrey J. Markowitz, Xing Guo,
and Xiao-Fan Wang
22 Epigenomic Regulation of Smad1 Signaling During Cellular
Senescence Induced by Ras Activation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Atsushi Kaneda, Aya Nonaka, Takanori Fujita, Ryota Yamanaka,
Mai Fujimoto, Kohei Miyazono, and Hiroyuki Aburatani
23 The Role of Ubiquitination to Determine Non-Smad
Signaling Responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Shyam Kumar Gudey and Marene Landström
24 Genome-Wide RNAi Screening to Dissect the TGF-β Signal
Transduction Pathway. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Xiaochu Chen and Lan Xu
25 Measuring TGF-β Ligand Dynamics in Culture Medium . . . . . . . . . . . . . . . . .
Zipei Feng, Zhike Zi, and Xuedong Liu
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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301
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325
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355
365
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391
Contributors
HIROYUKI ABURATANI • Genome Science Division, Research Center for Advanced Science
and Technology (RCAST), The University of Tokyo, Tokyo, Japan
LINDSAY ALCARAZ • Inserm U1052, Centre de Recherche en Cancérologie de Lyon, Lyon, France;
CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon, France;
Université de Lyon, Lyon, France; Université Lyon 1, Lyon, France; Centre Léon Bérard,
Lyon, France
LAURENT BARTHOLIN • Inserm U1052, Centre de Recherche en Cancérologie de Lyon,
Lyon, France; CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon, Lyon,
France; Université de Lyon, Lyon, France; Université Lyon 1, Lyon, France;
Centre Léon Bérard, Lyon, France
JUAN C. BOURNAT • Department of Pediatrics, Baylor College of Medicine,
Houston, TX, USA
CHESTER W. BROWN • Department of Molecular and Human Genetics, Baylor College
of Medicine, Houston, TX, USA; Department of Pediatrics, Baylor College of Medicine,
Houston, TX, USA; Texas Children’s Hospital, Houston, TX, USA
ERINE H. BUDI • Department of Cell and Tissue Biology, Broad Center, University
of California, San Francisco, CA, USA
XU CAO • Department of Orthopaedic Surgery, Johns Hopkins University School
of Medicine, Baltimore, MD, USA
JONATHON CARTHY • Ludwig Institute for Cancer Research, Science for Life Laboratory,
Uppsala University, Uppsala, Sweden
CHENBEI CHANG • Department of Cell, Developmental and Integrative Biology, University
of Alabama at Birmingham, Birmingham, AL, USA
XIAOCHU CHEN • Program in Molecular Medicine, University of Massachusetts Medical
School, Worcester, MA, USA
YAN CHEN • Key Laboratory of Nutrition and Metabolism, Institute for Nutritional Sciences,
Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
YE-GUANG CHEN • State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life
Sciences, School of Life Sciences, Tsinghua University, Beijing, China
JANET L. CRANE • Department of Orthopaedic Surgery, Johns Hopkins University School
of Medicine, Baltimore, MD, USA; Department of Pediatrics, Johns Hopkins University
School of Medicine, Baltimore, MD, USA
RIK DERYNCK • Department of Cell and Tissue Biology, Eli and Edythe Broad Center
of Regeneration Medicine and Stem Cell Research, Programs in Cell Biology,
and Developmental and Stem Cell Biology, University of California,
San Francisco, CA, USA
PETER TEN DIJKE • Department of Molecular Cell Biology, Cancer Genomics Centre
Netherlands, Centre for Biomedical Genetics, Leiden University Medical Center, Leiden,
The Netherlands
SHENG DING • Department of Pharmaceutical Chemistry, Gladstone Institute
of Cardiovascular Disease, University of California, San Francisco, CA, USA
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Contributors
MAARTEN VAN DINTHER • Department of Molecular Cell Biology, Leiden University Medical
Center, Leiden, The Netherlands
HENG-YU FAN • Life Sciences Institute and Innovation Center for Cell Signaling Network,
Zhejiang University, Hangzhou, China
ZIPEI FENG • Department of Chemistry and Biochemistry, University of Colorado Boulder,
Boulder, CO, USA; Otto-Warburg Laboratory, Max Planck Institute for Molecular Genetics,
Berlin, Germany
MAI FUJIMOTO • Genome Science Division, Research Center for Advanced Science
and Technology (RCAST), The University of Tokyo, Tokyo, Japan; Department of
Molecular Oncology, Graduate School of Medicine, Chiba University, Chiba, Japan
TAKANORI FUJITA • Genome Science Division, Research Center for Advanced Science
and Technology (RCAST), The University of Tokyo, Tokyo, Japan
M.J. GOUMANS • Department of Molecular Cell Biology, Cancer Genomics Centre
Netherlands, Centre for Biomedical Genetics, Leiden University Medical Center, Leiden,
The Netherlands
SHYAM KUMAR GUDEY • Department of Medical Biosciences, Umeå University, Umeå, Sweden
XING GUO • Department of Pharmacology and Cancer Biology, Duke University Medical
Center, Durham, NC, USA
AKIKO HATA • Cardiovascular Research Institute, University of California, San Francisco,
CA, USA
ANDREW P. HINCK • Department of Structural Biology, University of Pittsburgh, Pittsburgh,
PA, USA
TAO HUANG • Protein Chemistry, Novo Nordisk Research Center China, Beijing, China
ATSUSHI KANEDA • Genome Science Division, Research Center for Advanced Science
and Technology (RCAST), The University of Tokyo, Tokyo, Japan; Department of
Molecular Oncology, Graduate School of Medicine, Chiba University, Chiba, Japan;
CREST, Japan Science and Technology Agency, Saitama, Japan
YIBIN KANG • Lewis Thomas Laboratory 255, Department of Molecular Biology, Princeton
University, Princeton, NJ, USA
HARA KANG • Division of Life Sciences, College of Life Sciences and Bioengineering, Incheon
National University, Incheon, Republic of Korea; Cardiovascular Research Institute,
University of California, San Francisco, CA, USA
MITSUYASU KATO • Department of Experimental Pathology, Graduate School
of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
MARENE LANDSTRÖM • Department of Medical Biosciences, Umeå University, Umeå, Sweden
WENLIN LI • Department of Cell Biology, Second Military Medical University, Shanghai,
China
XIA LIN • Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston,
TX, USA
XUEDONG LIU • Department of Chemistry and Biochemistry, University of Colorado Boulder,
Boulder, CO, USA
FANG LIU • Center for Advanced Biotechnology and Medicine, Rutgers, The State University of
New Jersey, Piscataway, NJ, USA; Susan Lehman Cullman Laboratory for Cancer Research,
Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers, The State
University of New Jersey, Piscataway, NJ, USA; Rutgers Cancer Institute of New Jersey,
Rutgers, The State University of New Jersey, New Brunswick, NJ, USA
xupl@zju.edu.cn
Contributors
xi
XINGFENG LIU • State-key Laboratory of Biomembrane and Membrane Engineering,
Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University,
Beijing, China
KUNXIN LUO, PH.D. • Department of Molecular and Cell Biology (MCB),
University of California, Berkeley, CA, USA
J.A. MARING • Department of Molecular Cell Biology, Cancer Genomics Centre
Netherlands, Centre for Biomedical Genetics, Leiden University Medical Center, Leiden,
The Netherlands
GEOFFREY J. MARKOWITZ • Department of Pharmacology and Cancer Biology, Duke
University Medical Center, Duke University, Durham, NC, USA
GRAZIANO MARTELLO • Department of Molecular Medicine, University of Padua School
of Medicine, Padua, Italy
ISAO MATSUURA • Division of Molecular Genomics and Medicine, National Health Research
Institutes, Zhunan Town, Miaoli County, Taiwan
L.A. VAN MEETEREN • Department of Molecular Cell Biology, Cancer Genomics Centre
Netherlands, Centre for Biomedical Genetics, Leiden University Medical Center, Leiden,
The Netherlands
ANMING MENG • State-key Laboratory of Biomembrane and Membrane Engineering,
Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University,
Beijing, China; Institute of Zoology, Chinese Academy of Sciences, Beijing, China
KOHEI MIYAZONO • Department of Molecular Pathology, Graduate School of Medicine,
The University of Tokyo, Tokyo, Japan
MARCO MONTAGNER • Department of Molecular Medicine, University of Padua School
of Medicine, Padua, Italy
ARISTIDIS MOUSTAKAS • Ludwig Institute for Cancer Research, Science for Life Laboratory,
Uppsala University, Uppsala, Sweden; Department of Medical Biochemistry and Microbiology,
Science for Life Laboratory, Uppsala University, Uppsala, Sweden
MARIA NAMWANJE • Department of Molecular and Human Genetics, Baylor College
of Medicine, Houston, TX, USA
AYA NONAKA • Genome Science Division, Research Center for Advanced Science
and Technology (RCAST), The University of Tokyo, Tokyo, Japan
YUKARI OKITA • Ludwig Institute for Cancer Research, Science for Life Laboratory,
Uppsala University, Uppsala, Sweden; Department of Experimental Pathology,
Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba,
Ibaraki, Japan
YI PAN • Key Laboratory of Nutrition and Metabolism, Institute for Nutritional Sciences,
Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
STEFANO PICCOLO • Department of Molecular Medicine, University of Padua School
of Medicine, Padua, Italy
LAN QIN • Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston,
TX, USA
JULIET RASHIDIAN • Department of Molecular and Cell Biology (MCB), University
of California, Berkeley, CA, USA
TAKASHI SEKIYA • Department of Microbiology and Immunology, Keio University School
of Medicine, Tokyo, Japan
TAO SHEN • Department of Molecular and Cellular Biology, Baylor College of Medicine,
Houston, TX, USA; Michael E. DeBakey Department of Surgery, Baylor College
of Medicine, Houston, TX, USA
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Contributors
SYLVIE THUAULT • Faculty of Pharmacy, INSERM UMR 911 CRO2, Marseille, France
ULRICH VALCOURT • Inserm U1052, Centre de Recherche en Cancérologie de Lyon,
Lyon, France; ; CNRS UMR 5286, Centre de Recherche en Cancérologie de Lyon,
France; Université de Lyon, Lyon, France; Université Lyon 1, Lyon, France;
Centre Léon Bérard, Lyon, France
QIANG WANG • Institute of Zoology, Chinese Academy of Sciences, Beijing, China
XIAO-FAN WANG • Department of Pharmacology and Cancer Biology, Duke University
Medical Center, Durham, NC, USA
WANGUO WEI • Stem Cell and Regenerative Medicine Center, Chinese Academy of Science,
Shanghai Advanced Research Institute, Shanghai, China
LINGLING XIAN • Department of Orthopaedic Surgery, Johns Hopkins University School
of Medicine, Baltimore, MD, USA
JIAN XU • Center for Craniofacial Molecular Biology, Ostrow School of Dentistry of USC,
University of Southern California, Los Angeles, CA, USA
LAN XU • Blueprint Medicines, Cambridge, MA, USA
PINGLONG XU • Life Sciences Institute and Innovation Center for Cell Signaling Network,
Zhejiang University, Hangzhou, China
RYOTA YAMANAKA • Genome Science Division, Research Center for Advanced Science
and Technology (RCAST), The University of Tokyo, Tokyo, Japan
XIAOHUA YAN • State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life
Sciences, School of Life Sciences, Tsinghua University, Beijing, China
PENGYUAN YANG • CAS Key Laboratory of Infection and Immunity, Institute of Biophysics,
Chinese Academy of Sciences, Beijing, China
AKIHIKO YOSHIMURA • Department of Microbiology and Immunology, Keio University
School of Medicine, Tokyo, Japan
CHAO YU • Life Sciences Institute and Innovation Center for Cell Signaling Network,
Zhejiang University, Hangzhou, China
LONG ZHANG • Life Sciences Institute and Innovation Center for Cell Signaling Network,
Zhejiang University, Hangzhou, China
YUN ZHANG • Department of Pharmacology and Cancer Biology, Duke University Medical
Center, Durham, NC, USA
FANGFANG ZHOU • Institutes of Biology and Medical Sciences, Soochow University,
Suzhou, China
JIAN-JIE ZHOU • Life Sciences Institute and Innovation Center for Cell Signaling Network,
Zhejiang University, Hangzhou, China
ZHIKE ZI • Otto-Warburg Laboratory, Max Planck Institute for Molecular Genetics, Berlin,
Germany
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