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Human Stem Cell Toxicology

 View Online

Issues in Toxicology

Series Editors:
Professor Diana Anderson, University of Bradford, UK
Dr Michael D. Waters, Michael Waters Consulting, N. Carolina, USA
Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP001

Dr Timothy C. Marrs, Edentox Associates, Kent, UK

Advisor to the Board:

Professor Alok Dhawan, CSIR-Indian Institute of Toxicology Research,
Lucknow, India

Titles in the Series:

1: Hair in Toxicology: An Important Bio-Monitor
2: Male-mediated Developmental Toxicity
3: Cytochrome P450: Role in the Metabolism and Toxicity of Drugs and
other Xenobiotics
4: Bile Acids: Toxicology and Bioactivity
5: The Comet Assay in Toxicology
6: Silver in Healthcare
7: In Silico Toxicology: Principles and Applications
8: Environmental Cardiology
9: Biomarkers and Human Biomonitoring, Volume 1: Ongoing Programs
and Exposures
10: Biomarkers and Human Biomonitoring, Volume 2: Selected Biomarkers
of Current Interest
11: Hormone-Disruptive Chemical Contaminants in Food
12: Mammalian Toxicology of Insecticides
13: The Cellular Response to the Genotoxic Insult: The Question of
Threshold for Genotoxic Carcinogens
14: Toxicological Effects of Veterinary Medicinal Products in Humans:
Volume 1
15: Toxicological Effects of Veterinary Medicinal Products in Humans:
Volume 2
16: Aging and Vulnerability to Environmental Chemicals: Age-related
Disorders and their Origins in Environmental Exposures
17: Chemical Toxicity Prediction: Category Formation and Read-Across
18: The Carcinogenicity of Metals: Human Risk Through Occupational and
Environmental Exposure
19: Reducing, Refining and Replacing the Use of Animals in Toxicity Testing
20: Advances in Dermatological Sciences
21: Metabolic Profiling: Disease and Xenobiotics
22: Manganese in Health and Disease
23: Toxicology, Survival and Health Hazards of Combustion Products
24: Masked Mycotoxins in Food: Formation, Occurrence and Toxicological
Relevance
 View Online

25: Aerobiology: The Toxicology of Airborne Pathogens and Toxins

26: Chemical Warfare Toxicology, Volume 1: Fundamental Aspects
27: Chemical Warfare Toxicology, Volume 2: Management of Poisoning
28: Toxicogenomics in Predictive Carcinogenicity
29: Human Stem Cell Toxicology
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How to obtain future titles on publication:

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 View Online

Human Stem Cell Toxicology

Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP001

Edited by

James L. Sherley
Asymmetrex, LLC, Boston, MA, USA
Email: [email protected]
Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP001 View Online

Issues in Toxicology No. 29

Print ISBN: 978-1-78262-421-9

PDF eISBN: 978-1-78262-678-7
EPUB eISBN: 978-1-78262-873-6
ISSN: 1757-7179

A catalogue record for this book is available from the British Library

r The Royal Society of Chemistry 2016

All rights reserved

Apart from fair dealing for the purposes of research for non-commercial purposes or for
private study, criticism or review, as permitted under the Copyright, Designs and Patents
Act 1988 and the Copyright and Related Rights Regulations 2003, this publication may not
be reproduced, stored or transmitted, in any form or by any means, without the prior
permission in writing of The Royal Society of Chemistry or the copyright owner, or in the
case of reproduction in accordance with the terms of licences issued by the Copyright
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appropriate Reproduction Rights Organization outside the UK. Enquiries concerning
reproduction outside the terms stated here should be sent to The Royal Society of
Chemistry at the address printed on this page.

The RSC is not responsible for individual opinions expressed in this work.

The authors have sought to locate owners of all reproduced material not in their own
possession and trust that no copyrights have been inadvertently infringed.

Published by The Royal Society of Chemistry,

Thomas Graham House, Science Park, Milton Road,
Cambridge CB4 0WF, UK

Registered Charity Number 207890

For further information see our web site at www.rsc.org

Printed in the United Kingdom by CPI Group (UK) Ltd, Croydon, CR0 4YY, UK
Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP007

Contents

Chapter 1 Addressing Challenges to Progress in Human Stem Cell

Toxicology Concepts and Practice 1
James L. Sherley

1.1 Filling in the Stem Cell Gap in Human Toxicology 1

1.2 Historical Impact of the Hierarchical, Anatomical,
Sub-disciplinary Structure of Toxicological Sciences 2
1.3 Human Stem Cell Toxicology as a Stem Cell Exact
Science 3
1.4 Health and Medical Applications for Human Stem
Cell Toxicological Sciences 5
1.5 Introducing the Future Diverse Impacts of Human
Stem Cell Toxicology 6
Acknowledgements 7
References 7

Chapter 2 Alternative Methods in Haematopoietic Stem Cell

Toxicology 9
Navneet Kumar Yadav, Pooja Shukla and R. K. Singh

2.1 Introduction 9
2.2 Haematopoietic Stem Cell Toxicity or
Hematotoxicity 11
2.2.1 Sources of Haematopoietic Stem Cell Toxicity 12
2.2.2 Importance of Studying Haematopoietic
Stem Cell Toxicity 13

Issues in Toxicology No. 29

Human Stem Cell Toxicology
Edited by James L. Sherley
r The Royal Society of Chemistry 2016
Published by the Royal Society of Chemistry, www.rsc.org

vii
 View Online

viii Contents

2.2.3Haematopoietic Stem Cell Toxicity in Drug

Development 14
2.3 Colonogenic Assays as Predictors of Haematopoietic
Stem Cell Toxicity 14
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2.3.1 CFU-GM Colonogenic Assay 15

2.3.2 CFU-Mk Colonogenic Assay 16
2.3.3 BFU-E Colonogenic Assay 18
2.3.4 Lymphoid Lineage Based Colonogenic
Assays 18
2.4 Conclusions 21
Acknowledgements 22
References 22

Chapter 3 High-throughput Screening of Toxic Chemicals on Neural

Stem Cells 31
Kurt Farrell, Pranav Joshi, Alexander Roth, Chandrasekhar
Kothapalli and Moo-Yeal Lee

3.1 Neural Stem Cells 31

3.2 Toxic Chemicals in the Environment 32
3.3 Mechanisms of Neural Stem Cell Toxicity 33
3.3.1 Ion Channel Blocking 34
3.3.2 Drug Metabolism Effects 37
3.3.3 Oxidative Stress 40
3.3.4 DNA/RNA Denaturation 42
3.3.5 Membrane Compromise 42
3.3.6 Other Mechanisms of
Neurotoxicity 43
3.4 NSC Differentiation 43
3.5 Conventional In vitro Assays for Toxicity Screening
against Neural Stem Cells 45
3.5.1 Well Plate Assays 45
3.5.2 Cellular Microarray Assays 47
3.5.3 Microfluidic Assays 49
3.5.4 Other Assays 51
3.6 Challenges of Conventional In vitro Approaches
in Neurotoxicity Screening 51
3.7 Conclusions and Future Directions 52
Acknowledgements 53
References 53
 View Online

Contents ix

Chapter 4 The Role of Catecholamines in Stem Cell Mobilisation 64

Brı́d M. Ryan and Oscar Vidal

4.1 Introduction 64
4.2 Catecholamines 64
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4.3 Catecholamines and Stem Cell Mobilisation 67

4.3.1 Endothelial Progenitor Cells 70
4.3.2 Mesenchymal Stem Cells 71
4.3.3 Catecholamines and Stem Cell Biology 72
4.4 Consequences of Catecholamine-modulating
Agents for Stem Cell Toxicity 73
4.4.1 Other Considerations 78
4.5 Concluding Comments 80
References 81

Chapter 5 Toxicological Risk Assessment – Proposed Assay Platform

Using Stem and Progenitor Cell Differentiation in
Response to Environmental Toxicants 94
John W. Ludlow, Alexander Kinev, Michael VanKanegan,
Ben Buehrer, Nick Trotta and Joydeep Basu

5.1 Introduction 94
5.1.1 Toxicity 95
5.1.2 Environmental Toxicology 95
5.1.3 Predictive Toxicology 95
5.1.4 Automated High Content Imaging and
High Throughput, or High Content,
Screening 96
5.1.5 Risk Assessment 97
5.1.6 Components of Risk Assessment 97
5.2 Environmental Toxicological Risk Assessment
Employing an Assay Platform That Uses Stem and
Progenitor Cell Differentiation 98
5.2.1 Endothelial Colony Forming Cells (ECFCs) 99
5.2.2 ECFCs are Sensitive to Low-dose Ionizing
Radiation (LDIR) 100
5.2.3 Individual ECFC Cultures Exhibit
Donor-related LDIR Responses 100
5.2.4 The Profiling of Intracellular Signal
Transduction Pathways Provides an Insight
into the Mechanism of LDIR Toxicity 101
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x Contents

5.3 Current State of ECF Platform Development 102

5.3.1 Impedance-based Analysis of ECFC Viability
after Exposure to Environmental Toxicants 102
5.3.2 ECFCs Exhibit Lot-to-lot Variability in
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Toxicant Response 105

5.3.3 Development of a Novel ROS Assay Using
ECFCs 105
5.3.4 Density-dependent ROS Levels in Cultured
ECFCs 106
5.3.5 Signal Transduction Assays in Toxicant-
treated ECFCs 108
5.4 Bioanalytical Method Validation 110
5.4.1 Development of a Quantitative High
Content Imaging (QHCA) Platform Using
ECFCs 112
5.4.2 Optimize Culture Conditions for
High-throughput Screening 112
5.4.3 Initiate Translation of Assay to 384-Well
Plates 113
5.4.4 Incorporation of Automation to Increase
Throughput 114
5.4.5 Validation of the ECFC QHCA 114
5.4.6 Determining the Z 0 factor of the Cell Death
Assays Using Positive and Negative Controls 115
5.4.7 Assessing Sources of Assay Variability
Including Manual Pipetting, Plating and
Edge Effects 116
5.4.8 Determining Day-to-day Variability of EC50
for Each Assay 116
5.4.9 Determining Significant Biological
Replicate Power 117
5.4.10 Perform the High-throughput Assay Using
Compounds from the ToxCastt Phase I
Library 117
5.4.11 Incorporation of the Toxicant-induced
ECFC Differentiation Assays into the QHCA
Screen 118
5.4.12 Establish a Repository of ECFCs from
Various Donors 120
5.5 Final Thoughts 121
References 121
 View Online

Contents xi

Chapter 6 Current Developments in the Use of Human Stem Cell

Derived Cardiomyocytes to Examine Drug-induced
Cardiotoxicity 124
Varun Ahuja, Sharad Sharma and Raj Kamboj
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6.1 Introduction 124

6.2 Constraints Due to Species Differences 125
6.3 Stem Cells and iPSC-CMs 127
6.4 Limitations with Stem Cells 128
6.5 Stem Cells in Cardiovascular Safety
Pharmacology 129
6.6 Disease Models Based on iPSC-CMs 135
6.7 Generation of iPSC-CMs – Considerations on
Differentiation, Maturity, Heterogeneity and
Purification Protocols 137
6.7.1 Differentiation 137
6.7.2 Maturity 138
6.7.3 Heterogeneity 138
6.7.4 Purification 138
6.8 Use of iPSC-CMs in Phenotypic Assays 139
6.9 Assay Technologies Incorporating iPSC-CMs
and hESC-CMs 140
6.9.1 Manual Patch Clamp 140
6.9.2 Automated Patch Clamp 142
6.9.3 MEA (Microelectrode Array) 142
6.10 CiPA: Comprehensive In vitro Proarrhythmia
Assay 144
6.11 Conclusion 146
References 147

Chapter 7 Pesticides and Hematopoietic Stem Cells 160

Sujata Law and Malay Chaklader

7.1 Pesticide Toxicity-induced Disorders of

Hematopoietic System 160
7.1.1 Hematopoietic System and Hematotoxic
Pesticides 160
7.1.2 Pesticide-induced Aplastic Anemia: A Rare
but Severe Hematopathology due to Stem
Cell Failure 162
7.1.3 Assessment of Hematotoxicity 166
 View Online

xii Contents

7.2 Pesticide Toxicity on Hematopoietic Stem Cells and

their Microenvironment 167
7.2.1 Oxidative Stress Induction 167
7.2.2 Apoptosis Induction 167
Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP007

7.2.3 Alteration of Developmental Signaling

Pathways 168
7.3 Experimental Medicine Against Pesticide
Toxicity-induced Hematopoietic Failure 170
7.4 Future Direction 171
References 171

Chapter 8 Epigenetic Impact of Stem Cell Toxicants 178

Anup Kumar Singh, Akhilesh Singh, Rakesh Kumar Arya,
Navneet Kumar Yadav and Dipak Datta

8.1 Introduction 178

8.2 Epigenetic Regulation of Stem Cells 181
8.3 Stem Cell Toxicants as Modulators of Epigenetic
Programming 182
8.3.1 Heavy Metals 183
8.3.2 Pharmaceuticals 185
8.4 Conclusion 187
Acknowledgements 187
References 187

Chapter 9 Metakaryotic Cancer Stem Cells are Constitutively

Resistant to X-Rays and Chemotherapeutic Agents, but
Sensitive to Many Common Drugs 196
Elena V. Gostjeva, Vera V. Koledova, Liyuan Bai, Kailin C.
Duan, Tushar Kamath, Meghan Nelson, Parul Agnihotri,
Deborah J. Moshinski, Li Ping Wu, Lawrence Zukerberg,
Daniel C. Chung, Susan Tsai, Douglas B. Evans, Aoy
Tomita-Mitchell, Michael Mitchell and William G. Thilly

9.1 Introduction 197

9.1.1 Introduction to Metakaryotic Biology 197
9.2 Materials and Methods 200
9.2.1 Methods for Studies of Metakaryotic Cancer
Stem Cells In vivo and In vitro 200
9.3 Results 204
9.3.1 Observations in Tumors after Radiation
Therapy and Chemotherapy 204
9.3.2 Observations in Cell Cultures 206
 View Online

Contents xiii

9.4 Discussion 233

9.4.1 Stem Cells in Human Tumors and Tumor-
derived Cell Lines are Amitotic,
Metakaryotic Cells 233
Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP007

9.4.2 Assays that Recognize and Measure the

Toxicity of Radiation and Chemicals
to Metakaryotic Stem Cells 235
9.4.3 Growth and Development of Turnover Units
in HT-29 Cultures 235
9.4.4 Metakaryotic Stem Cells are Resistant to
Doses of X-Rays and Drug Classes
Commonly in Use for Cancer
Chemotherapy 237
9.4.5 Metakaryotic Stem Cells are Sensitive to
Many Drugs in Common Use:
Verapamil, Metformin, NSAIDS
and Antibiotics 237
9.4.6 Hypotheses about Metakaryocidal
Mechanisms, e.g. Inhibition
of Mitochondrial Function 239
9.4.7 Other Potential Targets for Metakaryocides:
Genome Replication and Segregation 241
9.4.8 Translation into Clinical Practice 242
9.4.9 Potential Use of Metakaryocides in
Prevention of Cancers and Other Clonal
Diseases 244
9.4.10 Other Considerations 244
Acknowledgements 246
References 246

Chapter 10 Distributed Stem Cell Kinetotoxicity: A New Concept to

Account for the Human Carcinogenicity of Non-genotoxic
Environmental Toxicants 250
Krishnanchali Panchalingam, Minsoo Noh, Yang Hoon Huh
and James L. Sherley

10.1 Introduction 250

10.2 Results and Discussion 253
10.2.1 Development of a High-throughput Cell
Kinetics Assay for Kinetotoxicity 253
10.2.2 Use of High-throughput Screening to
Detect Benzene and Hydroquinone as
Kinetotoxic Agents 256
 View Online

xiv Contents

10.2.3Confirmation Studies for Benzene and

Hydroquinone Kinetotoxicity 262
10.2.4 Validation of Benzene and Hydroquinone
Kinetotoxicity with DSCs 265
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10.2.5 Use of Microarray Analyses to Discover a

Potential Molecular Biomarker for
Kinetotoxicity 268
10.3 Conclusions and Closing Thoughts 270
10.3.1 Kinetotoxicity, An Extended Concept in
Human Stem Cell Toxicology for
Carcinogens 270
10.3.2 Development of a High-throughput Screen
for Kinetotoxic Agents 271
10.3.3 Mechanisms of Kinetotoxicity by Benzene
and Hydroquinone 272
10.3.4 The DSC Specification Problem in Human
Stem Cell Toxicology 273
10.3.5 Looking Forward 274
10.4 Materials and Methods 275
10.4.1 Cells 275
10.4.2 Chemicals 275
10.4.3 Development of the High-throughput
Microplate Assay for Kinetotoxicity 276
10.4.4 Assays for Self-renewal Kinetics Pattern
Determination 276
10.4.5 Microarray Analyses 276
Acknowledgements 276
References 277

Chapter 11 Cancer Stem Cells as Therapeutic Targets 280

Shinji Tanaka

11.1 Introduction 280

11.2 CSC Markers and Therapeutic Targets 282
11.3 Signal Transduction in CSCs and Targeted
Agents 283
11.4 Asymmetric Cell Divisions: The Dilemma of
Studies on CSCs 284
11.5 Asymmetric Cell Divisions: Visualization of
CSCs and Toxicology 286
 View Online

Contents xv

11.6 Asymmetric Cell Divisions; Potential Therapeutics

Targeting CSCs 289
11.7 Closing Remarks 291
Acknowledgements 291
Published on 09 August 2016 on http://pubs.rsc.org | doi:10.1039/9781782626787-FP007

References 291

Subject Index 295

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