Recurrent Variations in DNA Methylation in Human Pluripotent Stem Cells and Their Differentiated Derivatives
Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 s...
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| Published in | Cell stem cell Vol. 10; no. 5; pp. 620 - 634 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Cambridge, MA
Elsevier Inc
04.05.2012
Cell Press |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1934-5909 1875-9777 1875-9777 |
| DOI | 10.1016/j.stem.2012.02.013 |
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| Abstract | Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 somatic samples, we identified hPSC-specific epigenetic and transcriptional aberrations in genes subject to X chromosome inactivation (XCI) and genomic imprinting, which were not corrected during directed differentiation. We also found that specific tissue types were distinguished by unique patterns of DNA hypomethylation, which were recapitulated by DNA demethylation during in vitro directed differentiation. Our results suggest that verification of baseline epigenetic status is critical for hPSC-based disease models in which the observed phenotype depends on proper XCI or imprinting and that tissue-specific DNA methylation patterns can be accurately modeled during directed differentiation of hPSCs, even in the presence of variations in XCI or imprinting.
► Global analysis of DNA methylation differences between somatic and pluripotent cells ► Tissue-specific DNA demethylation occurs during differentiation ► X chromosome inactivation is unstable in pluripotent cells over time in culture ► Aberrations in X inactivation and imprinting are maintained during differentiation |
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| AbstractList | Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 somatic samples, we identified hPSC-specific epigenetic and transcriptional aberrations in genes subject to X chromosome inactivation (XCI) and genomic imprinting, which were not corrected during directed differentiation. We also found that specific tissue types were distinguished by unique patterns of DNA hypomethylation, which were recapitulated by DNA demethylation during in vitro directed differentiation. Our results suggest that verification of baseline epigenetic status is critical for hPSC-based disease models in which the observed phenotype depends on proper XCI or imprinting and that tissue-specific DNA methylation patterns can be accurately modeled during directed differentiation of hPSCs, even in the presence of variations in XCI or imprinting. Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 somatic samples, we identified hPSC-specific epigenetic and transcriptional aberrations in genes subject to X chromosome inactivation (XCI) and genomic imprinting, which were not corrected during directed differentiation. We also found that specific tissue types were distinguished by unique patterns of DNA hypomethylation, which were recapitulated by DNA demethylation during in vitro directed differentiation. Our results suggest that verification of baseline epigenetic status is critical for hPSC-based disease models in which the observed phenotype depends on proper XCI or imprinting, and that tissue-specific DNA methylation patterns can be accurately modeled during directed differentiation of hPSCs, even in the presence of variations in XCI or imprinting. Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 somatic samples, we identified hPSC-specific epigenetic and transcriptional aberrations in genes subject to X chromosome inactivation (XCI) and genomic imprinting, which were not corrected during directed differentiation. We also found that specific tissue types were distinguished by unique patterns of DNA hypomethylation, which were recapitulated by DNA demethylation during in vitro directed differentiation. Our results suggest that verification of baseline epigenetic status is critical for hPSC-based disease models in which the observed phenotype depends on proper XCI or imprinting and that tissue-specific DNA methylation patterns can be accurately modeled during directed differentiation of hPSCs, even in the presence of variations in XCI or imprinting. ► Global analysis of DNA methylation differences between somatic and pluripotent cells ► Tissue-specific DNA demethylation occurs during differentiation ► X chromosome inactivation is unstable in pluripotent cells over time in culture ► Aberrations in X inactivation and imprinting are maintained during differentiation Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 somatic samples, we identified hPSC-specific epigenetic and transcriptional aberrations in genes subject to X chromosome inactivation (XCI) and genomic imprinting, which were not corrected during directed differentiation. We also found that specific tissue types were distinguished by unique patterns of DNA hypomethylation, which were recapitulated by DNA demethylation during in vitro directed differentiation. Our results suggest that verification of baseline epigenetic status is critical for hPSC-based disease models in which the observed phenotype depends on proper XCI or imprinting and that tissue-specific DNA methylation patterns can be accurately modeled during directed differentiation of hPSCs, even in the presence of variations in XCI or imprinting.Human pluripotent stem cells (hPSCs) are potential sources of cells for modeling disease and development, drug discovery, and regenerative medicine. However, it is important to identify factors that may impact the utility of hPSCs for these applications. In an unbiased analysis of 205 hPSC and 130 somatic samples, we identified hPSC-specific epigenetic and transcriptional aberrations in genes subject to X chromosome inactivation (XCI) and genomic imprinting, which were not corrected during directed differentiation. We also found that specific tissue types were distinguished by unique patterns of DNA hypomethylation, which were recapitulated by DNA demethylation during in vitro directed differentiation. Our results suggest that verification of baseline epigenetic status is critical for hPSC-based disease models in which the observed phenotype depends on proper XCI or imprinting and that tissue-specific DNA methylation patterns can be accurately modeled during directed differentiation of hPSCs, even in the presence of variations in XCI or imprinting. |
| Author | Garitaonandia, Ibon Schmidt, Uli Müller, Franz-Josef Altun, Gulsah Nazor, Kristopher L. D'Lima, Darryl D. Laurent, Louise C. Slavin, Ileana Tran, Ha Keirstead, Hans S. Olee, Tsaiwei Loring, Jeanne F. Semechkin, Ruslan Park, Hyun Sook Parast, Mana M. Wang, Yu-Chieh Laslett, Andrew L. Harness, Julie V. Fakunle, Eyitayo Galat, Vasiliy Dumevska, Biljana Lynch, Candace Lee, Sunray Boscolo, Francesca S. |
| AuthorAffiliation | 8 Developmental Biology Program, iPS and Human Stem Cell Core Facility, Children’s Memorial Research Center, Northwestern University, Feinberg School of Medicine, Chicago, Illinois 10 Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria 3168, Australia 3 Center for Psychiatry, ZIP-Kiel, University Hospital Schleswig Holstein, Niemannsweg 147, D-24105 Kiel, Germany 5 International Stem Cell Corporation, Carlsbad, California 92008, USA 9 Commonwealth Scientific and Industrial Research Organisation (CSIRO), Division of Materials Science & Engineering Clayton, Victoria3168, Australia 2 Reeve-Irvine Research Center, Sue and Bill Gross Stem Cell Research Center, Department of Anatomy and Neurobiology, School of Medicine, University of California at Irvine, Irvine, California 92697, USA 6 Shiley Center for Orthopaedic Research & Education, Scripps Clinic, La Jolla, California 92037, USA 7 University of California, San Diego, Department of Pathology, 200 West Arbor Dr |
| AuthorAffiliation_xml | – name: 1 Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037, USA – name: 9 Commonwealth Scientific and Industrial Research Organisation (CSIRO), Division of Materials Science & Engineering Clayton, Victoria3168, Australia – name: 4 Laboratory of Stem Cell Niche, CEFO Co. Inc, 46-21 Susong-dong, Jongno-gu, Seoul 110-140, South Korea – name: 8 Developmental Biology Program, iPS and Human Stem Cell Core Facility, Children’s Memorial Research Center, Northwestern University, Feinberg School of Medicine, Chicago, Illinois – name: 6 Shiley Center for Orthopaedic Research & Education, Scripps Clinic, La Jolla, California 92037, USA – name: 3 Center for Psychiatry, ZIP-Kiel, University Hospital Schleswig Holstein, Niemannsweg 147, D-24105 Kiel, Germany – name: 7 University of California, San Diego, Department of Pathology, 200 West Arbor Drive, San Diego, California 92035, USA – name: 12 MCTT, Gongneungdong, Nowon-gu, Seoul 139-743, South Korea – name: 2 Reeve-Irvine Research Center, Sue and Bill Gross Stem Cell Research Center, Department of Anatomy and Neurobiology, School of Medicine, University of California at Irvine, Irvine, California 92697, USA – name: 13 University of California, San Diego, Department of Reproductive Medicine, 200 West Arbor Drive, San Diego, California 92035, USA – name: 5 International Stem Cell Corporation, Carlsbad, California 92008, USA – name: 10 Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria 3168, Australia – name: 11 Stem Cell Laboratory, Genea, Sydney, New South Wales 2000, Australia |
| Author_xml | – sequence: 1 givenname: Kristopher L. surname: Nazor fullname: Nazor, Kristopher L. organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 2 givenname: Gulsah surname: Altun fullname: Altun, Gulsah organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 3 givenname: Candace surname: Lynch fullname: Lynch, Candace organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 4 givenname: Ha surname: Tran fullname: Tran, Ha organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 5 givenname: Julie V. surname: Harness fullname: Harness, Julie V. organization: Reeve-Irvine Research Center, Sue and Bill Gross Stem Cell Research Center, Department of Anatomy and Neurobiology, Department of Neurological Surgery, School of Medicine, University of California at Irvine, Irvine, CA 92697, USA – sequence: 6 givenname: Ileana surname: Slavin fullname: Slavin, Ileana organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 7 givenname: Ibon surname: Garitaonandia fullname: Garitaonandia, Ibon organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 8 givenname: Franz-Josef surname: Müller fullname: Müller, Franz-Josef organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 9 givenname: Yu-Chieh surname: Wang fullname: Wang, Yu-Chieh organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 10 givenname: Francesca S. surname: Boscolo fullname: Boscolo, Francesca S. organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 11 givenname: Eyitayo surname: Fakunle fullname: Fakunle, Eyitayo organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 12 givenname: Biljana surname: Dumevska fullname: Dumevska, Biljana organization: Stem Cell Laboratory, Genea, Sydney, New South Wales 2000, Australia – sequence: 13 givenname: Sunray surname: Lee fullname: Lee, Sunray organization: Laboratory of Stem Cell Niche, CEFO Co. Inc., 46-21 Susong-dong, Jongno-gu, Seoul 110-140, South Korea – sequence: 14 givenname: Hyun Sook surname: Park fullname: Park, Hyun Sook organization: MCTT, Gongneungdong, Nowon-gu, Seoul 139-743, South Korea – sequence: 15 givenname: Tsaiwei surname: Olee fullname: Olee, Tsaiwei organization: Shiley Center for Orthopaedic Research & Education, Scripps Clinic, La Jolla, CA 92037, USA – sequence: 16 givenname: Darryl D. surname: D'Lima fullname: D'Lima, Darryl D. organization: Shiley Center for Orthopaedic Research & Education, Scripps Clinic, La Jolla, CA 92037, USA – sequence: 17 givenname: Ruslan surname: Semechkin fullname: Semechkin, Ruslan organization: International Stem Cell Corporation, Carlsbad, CA 92008, USA – sequence: 18 givenname: Mana M. surname: Parast fullname: Parast, Mana M. organization: Department of Pathology, University of California, San Diego, 200 West Arbor Drive, San Diego, CA 92035, USA – sequence: 19 givenname: Vasiliy surname: Galat fullname: Galat, Vasiliy organization: Developmental Biology Program, iPS and Human Stem Cell Core Facility, Children's Memorial Research Center, Northwestern University, Feinberg School of Medicine, Chicago, IL 60614, USA – sequence: 20 givenname: Andrew L. surname: Laslett fullname: Laslett, Andrew L. organization: Commonwealth Scientific and Industrial Research Organisation (CSIRO), Division of Materials Science & Engineering, Clayton, Victoria 3168, Australia – sequence: 21 givenname: Uli surname: Schmidt fullname: Schmidt, Uli organization: Stem Cell Laboratory, Genea, Sydney, New South Wales 2000, Australia – sequence: 22 givenname: Hans S. surname: Keirstead fullname: Keirstead, Hans S. organization: Reeve-Irvine Research Center, Sue and Bill Gross Stem Cell Research Center, Department of Anatomy and Neurobiology, Department of Neurological Surgery, School of Medicine, University of California at Irvine, Irvine, CA 92697, USA – sequence: 23 givenname: Jeanne F. surname: Loring fullname: Loring, Jeanne F. organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 24 givenname: Louise C. surname: Laurent fullname: Laurent, Louise C. email: llaurent@ucsd.edu organization: Center for Regenerative Medicine, Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25913723$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/22560082$$D View this record in MEDLINE/PubMed |
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| Keywords | Human Genetic variability Recurrent Methylation Pluripotent cell Stem cell |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: International Stem Cell Corp., Carlsbad, California, 92008, USA These authors contributed equally to this work. Current address: Life Technologies, Foster City, California, 94404, USA |
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| SubjectTerms | Biological and medical sciences Cell Differentiation Cell differentiation, maturation, development, hematopoiesis Cell physiology Cells, Cultured Chromosome Aberrations Chromosomes, Human, X disease models DNA DNA Methylation drugs Fundamental and applied biological sciences. Psychology genes Genetic Variation Genomic Imprinting Humans medicine Molecular and cellular biology Organ Specificity phenotype Pluripotent Stem Cells - physiology Recurrence Stem Cell Niche stem cells transcription (genetics) X chromosome X Chromosome Inactivation |
| Title | Recurrent Variations in DNA Methylation in Human Pluripotent Stem Cells and Their Differentiated Derivatives |
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