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A reference induced pluripotent stem cell line for large-scale collaborative studies

Caroline B. Pantazis, Andrian Yang, Erika Lara, Justin A. McDonough, Cornelis Blauwendraat, Lirong Peng, Hideyuki Oguro, Jizhong Zou, David Sebesta, Gretchen Pratt, Erin Cross, Jeffrey Blockwick, Philip Buxton, Lauren Kinner-Bibeau, Constance Medura, Christopher Tompkins, Stephen Hughes, Marianita Santiana, Faraz Faghri, Mike A. Nalls, Daniel Vitale, Yue A. Qi, Daniel M. Ramos, Kailyn M. Anderson, Julia Stadler, Priyanka Narayan, Jason Papademetriou, Luke Reilly, Matthew P. Nelson, Sanya Aggarwal, Leah U. Rosen, Peter Kirwan, Venkat Pisupati, Steven L. Coon, Sonja W. Scholz, Elena Coccia, Lily Sarrafha, Tim Ahfeldt, Salome Funes, Daryl A. Bosco, Melinda S. Beccari, Don W. Cleveland, Maria Clara Zanellati, Richa Basundra, Mohanish Deshmukh, Sarah Cohen, Zachary S. Nevin, Madeline Matia, Jonas Van Lent, Vincent Timmerman, Bruce R. Conklin, Dan Dou, Erika L.F. Holzbaur, Emmy Li, Indigo V.L. Rose, View ORCID ProfileMartin Kampmann, Theresa Priebe, Miriam Öttl, Jian Dong, Rik van der Kant, Lena Erlebach, Marc Welzer, Deborah Kronenberg-Versteeg, Dad Abu-Bonsrah, Clare L. Parish, View ORCID ProfileMalavika Raman, Laurin Heinrich, Birgitt Schüle, Carles Calatayud Aristoy, Patrik Verstreken, Aaron Held, Brian J. Wainger, Guochang Lyu, Ernest Arenas, Ana-Caroline Raulin, Guojun Bu, Dennis Crusius, Dominik Paquet, Rebecca M.C. Gabriele, Selina Wray, Katherine Johnson Chase, Ke Zhang, John C. Marioni, William C. Skarnes, View ORCID ProfileMark R. Cookson, View ORCID ProfileMichael E. Ward, View ORCID ProfileFlorian T. Merkle
doi: https://doi.org/10.1101/2021.12.15.472643
Caroline B. Pantazis
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Andrian Yang
2European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK
3Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, UK
4Metabolic Research Laboratories and Medical Research Council Metabolic Diseases Unit, Wellcome Trust - Medical Research Council Institute of Metabolic Science, University of Cambridge, Cambridge CB2 0QQ, UK
5Wellcome Trust - Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK
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Erika Lara
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Justin A. McDonough
6The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA
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Cornelis Blauwendraat
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
7Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA
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Lirong Peng
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
8Data Tecnica International LLC, Glen Echo, MD, USA
9Integrated Research Facility, National Institute of Allergy and Infectious Diseases, National Institute of Health, Frederick, MD, USA
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Hideyuki Oguro
6The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA
10Department of Cell Biology, University of Connecticut Health Center, Farmington, CT, USA
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Jizhong Zou
11iPS Cell Core Facility, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD, USA
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David Sebesta
12KromaTiD Inc., Longmont, CO, USA
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Gretchen Pratt
12KromaTiD Inc., Longmont, CO, USA
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Erin Cross
12KromaTiD Inc., Longmont, CO, USA
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Jeffrey Blockwick
12KromaTiD Inc., Longmont, CO, USA
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Philip Buxton
12KromaTiD Inc., Longmont, CO, USA
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Lauren Kinner-Bibeau
12KromaTiD Inc., Longmont, CO, USA
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Constance Medura
12KromaTiD Inc., Longmont, CO, USA
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Christopher Tompkins
12KromaTiD Inc., Longmont, CO, USA
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Stephen Hughes
12KromaTiD Inc., Longmont, CO, USA
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Marianita Santiana
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Faraz Faghri
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
7Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA
8Data Tecnica International LLC, Glen Echo, MD, USA
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Mike A. Nalls
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
7Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA
8Data Tecnica International LLC, Glen Echo, MD, USA
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Daniel Vitale
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
7Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA
8Data Tecnica International LLC, Glen Echo, MD, USA
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Yue A. Qi
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Daniel M. Ramos
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Kailyn M. Anderson
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Julia Stadler
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Priyanka Narayan
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
13Genetics and Biochemistry Branch, NIDDK, National Institutes of Health, Bethesda, MD 20814, USA
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Jason Papademetriou
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Luke Reilly
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Matthew P. Nelson
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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Sanya Aggarwal
4Metabolic Research Laboratories and Medical Research Council Metabolic Diseases Unit, Wellcome Trust - Medical Research Council Institute of Metabolic Science, University of Cambridge, Cambridge CB2 0QQ, UK
5Wellcome Trust - Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK
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Leah U. Rosen
2European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK
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Peter Kirwan
4Metabolic Research Laboratories and Medical Research Council Metabolic Diseases Unit, Wellcome Trust - Medical Research Council Institute of Metabolic Science, University of Cambridge, Cambridge CB2 0QQ, UK
5Wellcome Trust - Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK
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Venkat Pisupati
5Wellcome Trust - Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK
14John van Geest Centre for Brain Repair, University of Cambridge, Cambridge CB2 0PY, UK
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Steven L. Coon
15Molecular Genomics Core, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA
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Sonja W. Scholz
16Neurodegenerative Diseases Research Unit, National Institute of Neurological Disorders and Stroke, Bethesda, MD, USA
17Department of Neurology, Johns Hopkins University, Baltimore, MD 21287, USA
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Elena Coccia
18Nash Family Department of Neuroscience at Mount Sinai, New York, NY, USA; Departments of Neurology and Cell, Developmental and Regenerative Biology at Mount Sinai, New York, NY, USA; Ronald M. Loeb Center for Alzheimer’s Disease at Mount Sinai, New York, NY, USA; Friedman Brain Institute at Mount Sinai, New York, NY, USA; Black Family Stem Cell Institute at Mount Sinai, New York, NY, USA
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Lily Sarrafha
18Nash Family Department of Neuroscience at Mount Sinai, New York, NY, USA; Departments of Neurology and Cell, Developmental and Regenerative Biology at Mount Sinai, New York, NY, USA; Ronald M. Loeb Center for Alzheimer’s Disease at Mount Sinai, New York, NY, USA; Friedman Brain Institute at Mount Sinai, New York, NY, USA; Black Family Stem Cell Institute at Mount Sinai, New York, NY, USA
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Tim Ahfeldt
18Nash Family Department of Neuroscience at Mount Sinai, New York, NY, USA; Departments of Neurology and Cell, Developmental and Regenerative Biology at Mount Sinai, New York, NY, USA; Ronald M. Loeb Center for Alzheimer’s Disease at Mount Sinai, New York, NY, USA; Friedman Brain Institute at Mount Sinai, New York, NY, USA; Black Family Stem Cell Institute at Mount Sinai, New York, NY, USA
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Salome Funes
19Department of Neurology, UMass Chan Medical School, Worcester, MA, USA
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Daryl A. Bosco
19Department of Neurology, UMass Chan Medical School, Worcester, MA, USA
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Melinda S. Beccari
20Department of Cellular and Molecular Medicine, University of California at San Diego, La Jolla, CA, USA; Ludwig Institute for Cancer Research, University of California at San Diego, La Jolla, CA, USA
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Don W. Cleveland
20Department of Cellular and Molecular Medicine, University of California at San Diego, La Jolla, CA, USA; Ludwig Institute for Cancer Research, University of California at San Diego, La Jolla, CA, USA
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Maria Clara Zanellati
21Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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Richa Basundra
21Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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Mohanish Deshmukh
21Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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Sarah Cohen
21Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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Zachary S. Nevin
22Gladstone Institutes, San Francisco, CA, USA
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Madeline Matia
22Gladstone Institutes, San Francisco, CA, USA
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Jonas Van Lent
23Peripheral Neuropathy Research Group, Department of Biomedical Sciences, University of Antwerp, Antwerp, 2610, Belgium
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Vincent Timmerman
23Peripheral Neuropathy Research Group, Department of Biomedical Sciences, University of Antwerp, Antwerp, 2610, Belgium
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Bruce R. Conklin
22Gladstone Institutes, San Francisco, CA, USA
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Dan Dou
24Department of Physiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
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Erika L.F. Holzbaur
24Department of Physiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
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Emmy Li
25Institute for Neurodegenerative Diseases, University of California, San Francisco, San Francisco, CA, USA; Chan Zuckerberg Biohub, San Francisco, CA, USA; Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA
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Indigo V.L. Rose
25Institute for Neurodegenerative Diseases, University of California, San Francisco, San Francisco, CA, USA; Chan Zuckerberg Biohub, San Francisco, CA, USA; Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA
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Martin Kampmann
25Institute for Neurodegenerative Diseases, University of California, San Francisco, San Francisco, CA, USA; Chan Zuckerberg Biohub, San Francisco, CA, USA; Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA, USA
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Theresa Priebe
26Department of Functional Genomics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam de Boelelaan 1087, 1081 HV Amsterdam, the Netherlands
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Miriam Öttl
26Department of Functional Genomics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam de Boelelaan 1087, 1081 HV Amsterdam, the Netherlands
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Jian Dong
26Department of Functional Genomics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam de Boelelaan 1087, 1081 HV Amsterdam, the Netherlands
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Rik van der Kant
26Department of Functional Genomics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam de Boelelaan 1087, 1081 HV Amsterdam, the Netherlands
27Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Amsterdam UMC, Amsterdam, Netherlands
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Lena Erlebach
28Department of Cellular Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany
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Marc Welzer
28Department of Cellular Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany
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Deborah Kronenberg-Versteeg
28Department of Cellular Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany; German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany
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Dad Abu-Bonsrah
29Florey Institute of Neuroscience and Mental Health, Parkville, VIC 3052, Australia
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Clare L. Parish
29Florey Institute of Neuroscience and Mental Health, Parkville, VIC 3052, Australia
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Malavika Raman
30Department of Developmental Molecular and Chemical Biology, Tufts University School of Medicine, Boston, MA, USA
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Laurin Heinrich
31Department of Pathology, Stanford University School of Medicine, Stanford, California, USA
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Birgitt Schüle
31Department of Pathology, Stanford University School of Medicine, Stanford, California, USA
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Carles Calatayud Aristoy
32VIB-KU Leuven Center for Brain & Disease Research, 3000 Leuven, Belgium; KU Leuven, Department of Neurosciences, Leuven Brain Institute, Mission Lucidity, Leuven, Belgium
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Patrik Verstreken
32VIB-KU Leuven Center for Brain & Disease Research, 3000 Leuven, Belgium; KU Leuven, Department of Neurosciences, Leuven Brain Institute, Mission Lucidity, Leuven, Belgium
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Aaron Held
33Department of Neurology, Sean M. Healey & AMG Center for ALS, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
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Brian J. Wainger
34Department of Neurology, Sean M. Healey & AMG Center for ALS, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA; Department of Anesthesiology, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA; Harvard Stem Cell Institute, Cambridge, MA, USA; Broad Institute of Harvard University and MIT, Cambridge, MA, USA
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Guochang Lyu
35Division of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
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Ernest Arenas
35Division of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden
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Ana-Caroline Raulin
36Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA
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Guojun Bu
36Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA
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Dennis Crusius
37Institute for Stroke and Dementia Research, University Hospital Munich, Ludwig-Maximilians-Universität München, 81377 Munich, Germany
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Dominik Paquet
37Institute for Stroke and Dementia Research, University Hospital Munich, Ludwig-Maximilians-Universität München, 81377 Munich, Germany
38Munich Cluster for Systems Neurology (SyNergy), 81377 Munich, Germany
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Rebecca M.C. Gabriele
39Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, London, WC1N 3BG, UK
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Selina Wray
39Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, London, WC1N 3BG, UK
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Katherine Johnson Chase
36Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA
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Ke Zhang
36Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA
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John C. Marioni
2European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK
3Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, UK
40Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, UK
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William C. Skarnes
6The Jackson Laboratory for Genomic Medicine, Farmington, CT, USA
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  • For correspondence: fm436@medschl.cam.ac.uk bill.skarnes@jax.org cookson@mail.nih.gov michael.ward4@nih.gov
Mark R. Cookson
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
7Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA
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  • For correspondence: fm436@medschl.cam.ac.uk bill.skarnes@jax.org cookson@mail.nih.gov michael.ward4@nih.gov
Michael E. Ward
1Center for Alzheimer’s and Related Dementias, National Institutes of Health, Bethesda, MD, USA
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  • ORCID record for Michael E. Ward
  • For correspondence: fm436@medschl.cam.ac.uk bill.skarnes@jax.org cookson@mail.nih.gov michael.ward4@nih.gov
Florian T. Merkle
4Metabolic Research Laboratories and Medical Research Council Metabolic Diseases Unit, Wellcome Trust - Medical Research Council Institute of Metabolic Science, University of Cambridge, Cambridge CB2 0QQ, UK
5Wellcome Trust - Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK
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  • ORCID record for Florian T. Merkle
  • For correspondence: fm436@medschl.cam.ac.uk bill.skarnes@jax.org cookson@mail.nih.gov michael.ward4@nih.gov
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Abstract

Human induced pluripotent stem cells (iPSCs) are a powerful tool for studying development and disease. However, different iPSC lines show considerable phenotypic variation. The lack of common well-characterised cell lines that are used widely frustrates efforts to integrate data across research groups or replicate key findings. Inspired by model organism communities who addressed this issue by establishing a limited number of widely accepted strains, we characterised candidate iPSC lines in unprecedented detail to select a well-performing line to underpin collaborative studies. Specifically, we characterised the morphology, growth rates, and single-cell transcriptomes of iPSC lines in the pluripotent state and assessed their genomic integrity using karyotyping, DNA microarrays, whole genome sequencing, and functional assays for p53 activity. We further tested their ability to be edited by CRISPR/Cas9 and used single-cell RNA sequencing to compare the efficiency with which they could be differentiated into multiple lineages. We found that there was significant variability in the performance of lines across the tested assays that enabled the rational selection of a lead line, KOLF2.1J, which is a gene-corrected derivative of a publicly available line from the Human Induced Pluripotent Stem Cells Initiative (HipSci) resource. We are now using this line in an initiative from the NIH Center for Alzheimer’s and Related Dementias to derive hundreds of gene-edited and functionalized sub-clones to be distributed widely throughout the research community along with associated datasets, with the aim of promoting the standardisation required for large-scale collaborative science in the stem cell field.

Summary The authors of this collaborative science study describe a deep characterisation of widely available human induced pluripotent stem cell (hiPSC) lines to rationally select a line that performs well in multiple experimental approaches. Analysis of transcriptional patterns in the pluripotent state, whole genome sequencing, genomic stability after highly efficient CRISPR-mediated gene editing, integrity of the p53 pathway, and differentiation efficiency towards multiple lineages identified KOLF2.1J as an all-around well-performing cell line. The widespread distribution and use of this line makes it an attractive cell line for comparative and collaborative efforts in the stem cell field.

Highlights

  • Deep genotyping and phenotyping reveal KOLF2.1J as an all-around well-performing cell line that is readily distributed and could serve as common reference line

  • Despite rare copy-neutral loss of heterozygosity (CN-LOH) events, iPSC lines retain genomic fidelity after CRISPR/Cas9-based gene editing

  • Our multifactorial pipeline serves as a blueprint for future efforts to identify other lead iPSC lines

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Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵^ denotes co-first authorship

  • https://github.com/NIH-CARD/INDI-README/tree/main/INDI-genetics

  • https://fair.addi.ad-datainitiative.org/#/data/datasets/a_reference_induced_pluripotent_stem_cell_line_for_large_scale_collaborative_studies

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Posted February 07, 2022.
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A reference induced pluripotent stem cell line for large-scale collaborative studies
Caroline B. Pantazis, Andrian Yang, Erika Lara, Justin A. McDonough, Cornelis Blauwendraat, Lirong Peng, Hideyuki Oguro, Jizhong Zou, David Sebesta, Gretchen Pratt, Erin Cross, Jeffrey Blockwick, Philip Buxton, Lauren Kinner-Bibeau, Constance Medura, Christopher Tompkins, Stephen Hughes, Marianita Santiana, Faraz Faghri, Mike A. Nalls, Daniel Vitale, Yue A. Qi, Daniel M. Ramos, Kailyn M. Anderson, Julia Stadler, Priyanka Narayan, Jason Papademetriou, Luke Reilly, Matthew P. Nelson, Sanya Aggarwal, Leah U. Rosen, Peter Kirwan, Venkat Pisupati, Steven L. Coon, Sonja W. Scholz, Elena Coccia, Lily Sarrafha, Tim Ahfeldt, Salome Funes, Daryl A. Bosco, Melinda S. Beccari, Don W. Cleveland, Maria Clara Zanellati, Richa Basundra, Mohanish Deshmukh, Sarah Cohen, Zachary S. Nevin, Madeline Matia, Jonas Van Lent, Vincent Timmerman, Bruce R. Conklin, Dan Dou, Erika L.F. Holzbaur, Emmy Li, Indigo V.L. Rose, Martin Kampmann, Theresa Priebe, Miriam Öttl, Jian Dong, Rik van der Kant, Lena Erlebach, Marc Welzer, Deborah Kronenberg-Versteeg, Dad Abu-Bonsrah, Clare L. Parish, Malavika Raman, Laurin Heinrich, Birgitt Schüle, Carles Calatayud Aristoy, Patrik Verstreken, Aaron Held, Brian J. Wainger, Guochang Lyu, Ernest Arenas, Ana-Caroline Raulin, Guojun Bu, Dennis Crusius, Dominik Paquet, Rebecca M.C. Gabriele, Selina Wray, Katherine Johnson Chase, Ke Zhang, John C. Marioni, William C. Skarnes, Mark R. Cookson, Michael E. Ward, Florian T. Merkle
bioRxiv 2021.12.15.472643; doi: https://doi.org/10.1101/2021.12.15.472643
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A reference induced pluripotent stem cell line for large-scale collaborative studies
Caroline B. Pantazis, Andrian Yang, Erika Lara, Justin A. McDonough, Cornelis Blauwendraat, Lirong Peng, Hideyuki Oguro, Jizhong Zou, David Sebesta, Gretchen Pratt, Erin Cross, Jeffrey Blockwick, Philip Buxton, Lauren Kinner-Bibeau, Constance Medura, Christopher Tompkins, Stephen Hughes, Marianita Santiana, Faraz Faghri, Mike A. Nalls, Daniel Vitale, Yue A. Qi, Daniel M. Ramos, Kailyn M. Anderson, Julia Stadler, Priyanka Narayan, Jason Papademetriou, Luke Reilly, Matthew P. Nelson, Sanya Aggarwal, Leah U. Rosen, Peter Kirwan, Venkat Pisupati, Steven L. Coon, Sonja W. Scholz, Elena Coccia, Lily Sarrafha, Tim Ahfeldt, Salome Funes, Daryl A. Bosco, Melinda S. Beccari, Don W. Cleveland, Maria Clara Zanellati, Richa Basundra, Mohanish Deshmukh, Sarah Cohen, Zachary S. Nevin, Madeline Matia, Jonas Van Lent, Vincent Timmerman, Bruce R. Conklin, Dan Dou, Erika L.F. Holzbaur, Emmy Li, Indigo V.L. Rose, Martin Kampmann, Theresa Priebe, Miriam Öttl, Jian Dong, Rik van der Kant, Lena Erlebach, Marc Welzer, Deborah Kronenberg-Versteeg, Dad Abu-Bonsrah, Clare L. Parish, Malavika Raman, Laurin Heinrich, Birgitt Schüle, Carles Calatayud Aristoy, Patrik Verstreken, Aaron Held, Brian J. Wainger, Guochang Lyu, Ernest Arenas, Ana-Caroline Raulin, Guojun Bu, Dennis Crusius, Dominik Paquet, Rebecca M.C. Gabriele, Selina Wray, Katherine Johnson Chase, Ke Zhang, John C. Marioni, William C. Skarnes, Mark R. Cookson, Michael E. Ward, Florian T. Merkle
bioRxiv 2021.12.15.472643; doi: https://doi.org/10.1101/2021.12.15.472643

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