Transient naive reprogramming corrects hiPS cells functionally and epigenetically.

Humans Cellular Reprogramming Chromatin / genetics DNA Demethylation DNA Methylation DNA Transposable Elements Epigenesis, Genetic Induced Pluripotent Stem Cells / cytology Human Embryonic Stem Cells / cytology Lamin Type B

Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Aug 2023
Historique:
received: 04 06 2021
accepted: 11 07 2023
medline: 25 8 2023
pubmed: 17 8 2023
entrez: 16 8 2023
Statut: ppublish

Résumé

Cells undergo a major epigenome reconfiguration when reprogrammed to human induced pluripotent stem cells (hiPS cells). However, the epigenomes of hiPS cells and human embryonic stem (hES) cells differ significantly, which affects hiPS cell function

Identifiants

DOI: 10.1038/s41586-023-06424-7 PMID: 37587336 PMC: PMC10447250
pubmed: 37587336
doi: 10.1038/s41586-023-06424-7
pii: 10.1038/s41586-023-06424-7
pmc: PMC10447250
doi:

Substances chimiques

Chromatin 0
DNA Transposable Elements 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

863-872

Informations de copyright

© 2023. The Author(s).

Références

Kim, K. et al. Epigenetic memory in induced pluripotent stem cells. Nature 467, 285–290 (2010).
pubmed: 20644535 pmcid: 3150836 doi: 10.1038/nature09342
Polo, J. M. et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 28, 848–855 (2010).
pubmed: 20644536 pmcid: 3148605 doi: 10.1038/nbt.1667
Kim, K. et al. Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat. Biotechnol. 29, 1117–1119 (2011).
pubmed: 22119740 pmcid: 3357310 doi: 10.1038/nbt.2052
Lister, R. et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68–73 (2011).
pubmed: 21289626 pmcid: 3100360 doi: 10.1038/nature09798
Ohi, Y. et al. Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat. Cell Biol. 13, 541–549 (2011).
pubmed: 21499256 pmcid: 3987913 doi: 10.1038/ncb2239
Ruiz, S. et al. Identification of a specific reprogramming-associated epigenetic signature in human induced pluripotent stem cells. Proc. Natl Acad. Sci. USA 109, 16196–16201 (2012).
pubmed: 22991473 pmcid: 3479609 doi: 10.1073/pnas.1202352109
Bar-Nur, O., Russ, H. A., Efrat, S. & Benvenisty, N. Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell 9, 17–23 (2011).
pubmed: 21726830 doi: 10.1016/j.stem.2011.06.007
Panopoulos, A. D. et al. Aberrant DNA methylation in human iPSCs associates with MYC-binding motifs in a clone-specific manner independent of genetics. Cell Stem Cell 20, 505–517.e6 (2017).
pubmed: 28388429 pmcid: 5444384 doi: 10.1016/j.stem.2017.03.010
Yamanaka, S. & Blau, H. M. Nuclear reprogramming to a pluripotent state by three approaches. Nature 465, 704–712 (2010).
pubmed: 20535199 pmcid: 2901154 doi: 10.1038/nature09229
Guenther, M. G. et al. Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 7, 249–257 (2010).
pubmed: 20682450 pmcid: 3010384 doi: 10.1016/j.stem.2010.06.015
Choi, J. et al. A comparison of genetically matched cell lines reveals the equivalence of human iPSCs and ESCs. Nat. Biotechnol. 33, 1173–1181 (2015).
pubmed: 26501951 pmcid: 4847940 doi: 10.1038/nbt.3388
Tapia, N. & Schöler, H. R. Molecular obstacles to clinical translation of iPSCs. Cell Stem Cell 19, 298–309 (2016).
pubmed: 27452174 doi: 10.1016/j.stem.2016.06.017
Ma, H. et al. Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature 511, 177–183 (2014).
pubmed: 25008523 pmcid: 4898064 doi: 10.1038/nature13551
Cacchiarelli, D. et al. Integrative analyses of human reprogramming reveal dynamic nature of induced pluripotency. Cell 162, 412–424 (2015).
pubmed: 26186193 pmcid: 4511597 doi: 10.1016/j.cell.2015.06.016
Xing, Q. R. et al. Diversification of reprogramming trajectories revealed by parallel single-cell transcriptome and chromatin accessibility sequencing. Sci. Adv. 6, eaba1190 (2020).
pubmed: 32917699 pmcid: 7486102 doi: 10.1126/sciadv.aba1190
Liu, X. et al. Comprehensive characterization of distinct states of human naive pluripotency generated by reprogramming. Nat. Methods 14, 1055–1062 (2017).
pubmed: 28945704 doi: 10.1038/nmeth.4436
Giulitti, S. et al. Direct generation of human naive induced pluripotent stem cells from somatic cells in microfluidics. Nat. Cell Biol. 21, 275–286 (2019).
pubmed: 30598530 doi: 10.1038/s41556-018-0254-5
Wang, Y. et al. Unique molecular events during reprogramming of human somatic cells to induced pluripotent stem cells (iPSCs) at naïve state.eLife 7, e29518 (2018).
pubmed: 29381138 pmcid: 5807049 doi: 10.7554/eLife.29518
Guo, G. et al. Naive pluripotent stem cells derived directly from isolated cells of the human inner cell mass. Stem Cell Rep. 6, 437–446 (2016).
doi: 10.1016/j.stemcr.2016.02.005
Theunissen, T. W. et al. Molecular criteria for defining the naive human pluripotent state. Cell Stem Cell 19, 502–515 (2016).
pubmed: 27424783 pmcid: 5065525 doi: 10.1016/j.stem.2016.06.011
Pastor, W. A. et al. Naive human pluripotent cells feature a methylation landscape devoid of blastocyst or germline memory. Cell Stem Cell 18, 323–329 (2016).
pubmed: 26853856 pmcid: 4779431 doi: 10.1016/j.stem.2016.01.019
Liu, X. et al. Reprogramming roadmap reveals route to human induced trophoblast stem cells. Nature 586, 101–107 (2020).
pubmed: 32939092 doi: 10.1038/s41586-020-2734-6
Knaupp, A. S. et al. Transient and permanent reconfiguration of chromatin and transcription factor occupancy drive reprogramming. Cell Stem Cell 21, 834–845.e6 (2017).
pubmed: 29220667 doi: 10.1016/j.stem.2017.11.007
Roost, M. S. et al. DNA methylation and transcriptional trajectories during human development and reprogramming of isogenic pluripotent stem cells. Nat. Commun. 8, 908 (2017).
pubmed: 29030611 pmcid: 5640655 doi: 10.1038/s41467-017-01077-3
Bar, S., Schachter, M., Eldar-Geva, T. & Benvenisty, N. Large-scale analysis of loss of imprinting in human pluripotent stem cells. Cell Rep. 19, 957–968 (2017).
pubmed: 28467909 doi: 10.1016/j.celrep.2017.04.020
Court, F. et al. Genome-wide parent-of-origin DNA methylation analysis reveals the intricacies of human imprinting and suggests a germline methylation-independent mechanism of establishment. Genome Res. 24, 554–569 (2014).
pubmed: 24402520 pmcid: 3975056 doi: 10.1101/gr.164913.113
Lee, H. J., Hore, T. A. & Reik, W. Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 14, 710–719 (2014).
pubmed: 24905162 pmcid: 4051243 doi: 10.1016/j.stem.2014.05.008
van Steensel, B. & Belmont, A. S. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169, 780–791 (2017).
pubmed: 28525751 pmcid: 5532494 doi: 10.1016/j.cell.2017.04.022
Soufi, A., Donahue, G. & Zaret, K. S. Facilitators and impediments of the pluripotency reprogramming factors’ initial engagement with the genome. Cell 151, 994–1004 (2012).
pubmed: 23159369 pmcid: 3508134 doi: 10.1016/j.cell.2012.09.045
Godoy, P. et al. Assessment of stem cell differentiation based on genome-wide expression profiles. Phil. Trans. R. Soc. B 373, 20170221 (2018).
pubmed: 29786556 pmcid: 5974444 doi: 10.1098/rstb.2017.0221
Ortmann, D. et al. Naive pluripotent stem cells exhibit phenotypic variability that is driven by genetic variation. Cell Stem Cell 27, 470–481.e6 (2020).
pubmed: 32795399 pmcid: 7487768 doi: 10.1016/j.stem.2020.07.019
Skelly, D. A. et al. Mapping the effects of genetic variation on chromatin state and gene expression reveals loci that control ground state pluripotency. Cell Stem Cell 27, 459–469.e8 (2020).
pubmed: 32795400 pmcid: 7484384 doi: 10.1016/j.stem.2020.07.005
Pontis, J. et al. Hominoid-specific transposable elements and KZFPs facilitate human embryonic genome activation and control transcription in naive human ESCs. Cell Stem Cell 24, 724–735.e5 (2019).
pubmed: 31006620 pmcid: 6509360 doi: 10.1016/j.stem.2019.03.012
Guo, G. et al. Epigenetic resetting of human pluripotency. Development 144, 2748–2763 (2017).
pubmed: 28765214 pmcid: 5560041 doi: 10.1242/dev.146811
Greenberg, M. V. C. & Bourc’his, D. The diverse roles of DNA methylation in mammalian development and disease. Nat. Rev. Mol. Cell Biol. 20, 590–607 (2019).
pubmed: 31399642 doi: 10.1038/s41580-019-0159-6
Friedli, M. et al. Loss of transcriptional control over endogenous retroelements during reprogramming to pluripotency. Genome Res. 24, 1251–1259 (2014).
pubmed: 24879558 pmcid: 4120079 doi: 10.1101/gr.172809.114
Ohnuki, M. et al. Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential. Proc. Natl Acad. Sci. USA 111, 12426–12431 (2014).
pubmed: 25097266 pmcid: 4151758 doi: 10.1073/pnas.1413299111
Müller, F.-J. et al. A bioinformatic assay for pluripotency in human cells. Nat. Methods 8, 315–317 (2011).
pubmed: 21378979 pmcid: 3265323 doi: 10.1038/nmeth.1580
Koyanagi-Aoi, M. et al. Differentiation-defective phenotypes revealed by large-scale analyses of human pluripotent stem cells. Proc. Natl Acad. Sci. USA 110, 20569–20574 (2013).
pubmed: 24259714 pmcid: 3870695 doi: 10.1073/pnas.1319061110
Poleshko, A. et al. Genome–nuclear lamina interactions regulate cardiac stem cell lineage restriction. Cell 171, 573–587.e14 (2017).
pubmed: 29033129 pmcid: 5683101 doi: 10.1016/j.cell.2017.09.018
Wang, C. et al. Reprogramming of H3K9me3-dependent heterochromatin during mammalian embryo development. Nat. Cell Biol. 20, 620–631 (2018).
pubmed: 29686265 doi: 10.1038/s41556-018-0093-4
Guo, H. et al. The DNA methylation landscape of human early embryos. Nature 511, 606–610 (2014).
pubmed: 25079557 doi: 10.1038/nature13544
Salvador-Palomeque, C. et al. Dynamic methylation of an L1 transduction family during reprogramming and neurodifferentiation. Mol. Cell. Biol. 39, e00499–18 (2019).
pubmed: 30692270 pmcid: 6425141 doi: 10.1128/MCB.00499-18
Kyttälä, A. et al. Genetic variability overrides the impact of parental cell type and determines iPSC differentiation potential. Stem Cell Rep. 6, 200–212 (2016).
doi: 10.1016/j.stemcr.2015.12.009
Rouhani, F. et al. Genetic background drives transcriptional variation in human induced pluripotent stem cells. PLoS Genet. 10, e1004432 (2014).
pubmed: 24901476 pmcid: 4046971 doi: 10.1371/journal.pgen.1004432
Matoba, S. et al. Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159, 884–895 (2014).
pubmed: 25417163 pmcid: 4243038 doi: 10.1016/j.cell.2014.09.055
Fishilevich, S. et al. GeneHancer: genome-wide integration of enhancers and target genes in GeneCards. Database 2017, bax028 (2017).
pubmed: 28605766 pmcid: 5467550 doi: 10.1093/database/bax028
Polo, J., Liu, X. & Nefzger, C. Establishment and maintenance of human naive pluripotent stem cells by primed to naive conversion and reprogramming of fibroblasts. Protoc. Exch. https://doi.org/10.1038/protex.2017.099 (2017).
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Ewing, A. D. et al. Nanopore sequencing enables comprehensive transposable element epigenomic profiling. Mol. Cell 80, 915–928.e5 (2020).
pubmed: 33186547 doi: 10.1016/j.molcel.2020.10.024
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033
Efron, B. The 1977 RIETZ lecture. Ann. Stat. 7, 1–26 (1979).
Butcher, L. M. et al. Non-CG DNA methylation is a biomarker for assessing endodermal differentiation capacity in pluripotent stem cells. Nat. Commun. 7, 10458 (2016).
pubmed: 26822956 pmcid: 4740175 doi: 10.1038/ncomms10458
Hannan, N. R. F., Segeritz, C.-P., Touboul, T. & Vallier, L. Production of hepatocyte-like cells from human pluripotent stem cells. Nat. Protoc. 8, 430–437 (2013).
pubmed: 23424751 pmcid: 3673228 doi: 10.1038/nprot.2012.153
Vargas-Landin, D. B., Pflüger, J. & Lister, R. Generation of whole genome bisulfite sequencing libraries for comprehensive DNA methylome analysis. Methods Mol. Biol. 1767, 291–298 (2018).
pubmed: 29524142 doi: 10.1007/978-1-4939-7774-1_16
Chen, P.-Y., Cokus, S. J. & Pellegrini, M. BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 11, 203 (2010).
pubmed: 20416082 pmcid: 2871274 doi: 10.1186/1471-2105-11-203
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
pubmed: 19261174 pmcid: 2690996 doi: 10.1186/gb-2009-10-3-r25
Tarasov, A., Vilella, A. J., Cuppen, E., Nijman, I. J. & Prins, P. Sambamba: fast processing of NGS alignment formats. Bioinformatics 31, 2032–2034 (2015).
pubmed: 25697820 pmcid: 4765878 doi: 10.1093/bioinformatics/btv098
Guo, W. et al. CGmapTools improves the precision of heterozygous SNV calls and supports allele-specific methylation detection and visualization in bisulfite-sequencing data. Bioinformatics 34, 381–387 (2018).
pubmed: 28968643 doi: 10.1093/bioinformatics/btx595
Korthauer, K., Chakraborty, S., Benjamini, Y. & Irizarry, R. A. Detection and accurate false discovery rate control of differentially methylated regions from whole genome bisulfite sequencing. Biostatistics 20, 367–383 (2019).
pubmed: 29481604 doi: 10.1093/biostatistics/kxy007
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
pubmed: 30423086 pmcid: 6129281 doi: 10.1093/bioinformatics/bty560
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142 pmcid: 4655817 doi: 10.1038/nmeth.3317
Jin, Y., Tam, O. H., Paniagua, E. & Hammell, M. TEtranscripts: a package for including transposable elements in differential expression analysis of RNA-seq datasets. Bioinformatics 31, 3593–3599 (2015).
pubmed: 26206304 pmcid: 4757950 doi: 10.1093/bioinformatics/btv422
Kumar, L. & E Futschik, M. Mfuzz: a software package for soft clustering of microarray data. Bioinformation 2, 5–7 (2007).
pubmed: 18084642 pmcid: 2139991 doi: 10.6026/97320630002005
Reimand, J., Kull, M., Peterson, H., Hansen, J. & Vilo, J. g:Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res. 35, W193–W200 (2007).
pubmed: 17478515 pmcid: 1933153 doi: 10.1093/nar/gkm226
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
pubmed: 20513432 pmcid: 2898526 doi: 10.1016/j.molcel.2010.05.004
McCole, R. B., Erceg, J., Saylor, W. & Wu, C.-T. Ultraconserved elements occupy specific arenas of three-dimensional mammalian genome organization. Cell Rep. 24, 479–488 (2018).
pubmed: 29996107 pmcid: 6363003 doi: 10.1016/j.celrep.2018.06.031
Burger, L., Gaidatzis, D., Schübeler, D. & Stadler, M. B. Identification of active regulatory regions from DNA methylation data. Nucleic Acids Res. 41, e155 (2013).
pubmed: 23828043 pmcid: 3763559 doi: 10.1093/nar/gkt599
Dekker, J. et al. The 4D nucleome project. Nature 549, 219–226 (2017).
pubmed: 28905911 pmcid: 5617335 doi: 10.1038/nature23884
Reiff, S. B. et al. The 4D Nucleome Data Portal as a resource for searching and visualizing curated nucleomics data. Nat. Commun. 13, 2365 (2022).
pubmed: 35501320 pmcid: 9061818 doi: 10.1038/s41467-022-29697-4
ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74 (2012).
doi: 10.1038/nature11247
Schultz, M. D. et al. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature 523, 212–216 (2015).
pubmed: 26030523 pmcid: 4499021 doi: 10.1038/nature14465

Auteurs

Sam Buckberry (S)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.
Telethon Kids Institute, Perth, Western Australia, Australia.
John Curtin School of Medical Research, College of Health and Medicine, Australian National University, Canberra, Australian Capital Territory, Australia.
ORCID: 0000-0003-2388-6046

Xiaodong Liu (X)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.
School of Life Sciences, Westlake University, Hangzhou, China.
Research Center for Industries of the Future, Westlake University, Hangzhou, China.
Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, China.
Westlake Institute for Advanced Study, Hangzhou, China.
ORCID: 0000-0002-9315-3406

Daniel Poppe (D)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.
ORCID: 0000-0002-6674-8420

Jia Ping Tan (JP)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.

Guizhi Sun (G)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.

Joseph Chen (J)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.

Trung Viet Nguyen (TV)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.

Alex de Mendoza (A)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.
School of Biological and Behavioural Sciences, Queen Mary University of London, London, UK.
ORCID: 0000-0002-6441-6529

Jahnvi Pflueger (J)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.

Thomas Frazer (T)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.

Dulce B Vargas-Landín (DB)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia.
ORCID: 0000-0002-4773-9406

Jacob M Paynter (JM)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.

Nathan Smits (N)

Mater Research Institute, University of Queensland, Brisbane, Queensland, Australia.
ORCID: 0000-0002-0156-5076

Ning Liu (N)

South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

John F Ouyang (JF)

Program in Cardiovascular and Metabolic Disorders, Duke-National University of Singapore Medical School, Singapore, Singapore.
ORCID: 0000-0002-1239-1577

Fernando J Rossello (FJ)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.
Murdoch Children's Research Institute, Melbourne, Victoria, Australia.

Hun S Chy (HS)

Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.
Biomedical Manufacturing, Commonwealth Scientific and Industrial Research Organisation, Melbourne, Victoria, Australia.

Owen J L Rackham (OJL)

Program in Cardiovascular and Metabolic Disorders, Duke-National University of Singapore Medical School, Singapore, Singapore.
School of Biological Sciences, University of Southampton, Southampton, UK.
ORCID: 0000-0002-4390-0872

Andrew L Laslett (AL)

Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia.
Biomedical Manufacturing, Commonwealth Scientific and Industrial Research Organisation, Melbourne, Victoria, Australia.

James Breen (J)

John Curtin School of Medical Research, College of Health and Medicine, Australian National University, Canberra, Australian Capital Territory, Australia.
South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia.

Geoffrey J Faulkner (GJ)

Mater Research Institute, University of Queensland, Brisbane, Queensland, Australia.
Queensland Brain Institute, University of Queensland, Brisbane, Queensland, Australia.
ORCID: 0000-0001-5769-4494

Christian M Nefzger (CM)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia.
Institute for Molecular Bioscience, University of Queensland, Brisbane, Queensland, Australia.
ORCID: 0000-0003-4631-5633

Jose M Polo (JM)

Department of Anatomy and Developmental Biology, Monash University, Melbourne, Victoria, Australia. jose.polo@monash.edu.
Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Melbourne, Victoria, Australia. jose.polo@monash.edu.
Australian Regenerative Medicine Institute, Monash University, Melbourne, Victoria, Australia. jose.polo@monash.edu.
Adelaide Centre for Epigenetics, School of Biomedicine, Faculty of Health and Medical Sciences, The University of Adelaide, Adelaide, South Australia, Australia. jose.polo@monash.edu.
The South Australian Immunogenomics Cancer Institute, Faculty of Health and Medical Sciences, The University of Adelaide, Adelaide, South Australia, Australia. jose.polo@monash.edu.
ORCID: 0000-0002-2531-778X

Ryan Lister (R)

Harry Perkins Institute of Medical Research, QEII Medical Centre and Centre for Medical Research, The University of Western Australia, Perth, Western Australia, Australia. ryan.lister@uwa.edu.au.
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia. ryan.lister@uwa.edu.au.
ORCID: 0000-0001-6637-7239

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Phénomènes génétiques › Reprogrammation cellulaire › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Structures de chromosome › Chromatine › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Métabolisme › Désalkylation › Déméthylation › Déméthylation de l'ADN › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Phénomènes génétiques › Méthylation de l'ADN › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Séquences répétées dispersées › Éléments transposables d'ADN › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Épigenèse génétique › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Cellules › Cellules souches › Cellules souches pluripotentes › Cellules souches pluripotentes induites › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Cellules › Cellules souches › Cellules souches pluripotentes › Cellules souches embryonnaires › Cellules souches embryonnaires humaines › Transient naive reprogramming corrects hiPS...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines nucléaires › Protéines associées à la matrice nucléaire › Lamines › Lamine B › Transient naive reprogramming corrects hiPS...