Parallel derivation of isogenic human primed and naive induced pluripotent stem cells

Stéphanie Kilens; DImitri Meistermann; DIego Moreno; Caroline Chariau; Anne Gaignerie; Arnaud Reignier; Yohann Lelièvre; Miguel Casanova; Céline Vallot; Steven Nedellec; Léa Flippe; Julie Firmin; Juan Song; Eric Charpentier; Jenna Lammers; Audrey Donnart; Nadège Marec; Wallid Deb; Audrey Bihouée; Cédric Le Caignec; Claire Pecqueur; Richard Redon; Paul Barrière; Jérémie Bourdon; Vincent Pasque; Magali Soumillon; Tarjei S. Mikkelsen; Claire Rougeulle; Thomas Fréour; Laurent David; Laurent Abel; Andres Alcover; Kalla Astrom; Philippe Bousso; Pierre Bruhns; Ana Cumano; Darragh Duffy; Caroline Demangel; Ludovic Deriano; James DI Santo; Françoise Dromer; Gérard Eberl; Jost Enninga; Jacques Fellay; Antonio Freitas; Odile Gelpi; Ivo Gomperts-Boneca; Serge Hercberg; Olivier Lantz; Claude Leclerc; Hugo Mouquet; Etienne Patin; Sandra Pellegrini; Stanislas Pol; Lars Rogge; Anavaj Sakuntabhai; Olivier Schwartz; Benno Schwikowski; Spencer Shorte; Vassili Soumelis; Frédéric Tangy; Eric Tartour; Antoine Toubert; Marie Noëlle Ungeheuer; Lluis Quintana-Murci; Matthew L. Albert

doi:10.1038/s41467-017-02107-w

Parallel derivation of isogenic human primed and naive induced pluripotent stem cells

Stéphanie Kilens
, DImitri Meistermann
, DIego Moreno
, Caroline Chariau
, Anne Gaignerie
, Arnaud Reignier
, Yohann Lelièvre
, Miguel Casanova
, Céline Vallot
, Steven Nedellec
, Léa Flippe
, Julie Firmin
, Juan Song
, Eric Charpentier
, Jenna Lammers
, Audrey Donnart
, Nadège Marec
, Wallid Deb
, Audrey Bihouée
, Cédric Le Caignec

Claire Pecqueur, Richard Redon, Paul Barrière, Jérémie Bourdon, Vincent Pasque, Magali Soumillon, Tarjei S. Mikkelsen, Claire Rougeulle, Thomas Fréour, Laurent David, Laurent Abel, Andres Alcover, Kalla Astrom, Philippe Bousso, Pierre Bruhns, Ana Cumano, Darragh Duffy, Caroline Demangel, Ludovic Deriano, James DI Santo, Françoise Dromer, Gérard Eberl, Jost Enninga, Jacques Fellay, Antonio Freitas, Odile Gelpi, Ivo Gomperts-Boneca, Serge Hercberg, Olivier Lantz, Claude Leclerc, Hugo Mouquet, Etienne Patin, Sandra Pellegrini, Stanislas Pol, Lars Rogge, Anavaj Sakuntabhai, Olivier Schwartz, Benno Schwikowski, Spencer Shorte, Vassili Soumelis, Frédéric Tangy, Eric Tartour, Antoine Toubert, Marie Noëlle Ungeheuer, Lluis Quintana-Murci, Matthew L. Albert

Université de Nantes
Centre Hospitalier Universitaire
LabEx IGO 'Immunotherapy
Oncology
UMR CNRS 6597
INSERM UMS 016
IPSC Core Facility
Service de Biologie de la Reproduction
Paris Descartes University
INSERM UMS 016
Department of Development and Regeneration
KU Leuven-University of Leuven
CNRS UMR6291 Université de Nantes L'institut du Thorax
Bone Sarcoma and Remodeling of Calcified Tissue
Université de Nantes
Harvard University
Berkeley Lights Inc.
Department of Molecular Biology
Harvard Stem Cell Institute
10x Genomics
INSERM U1163
Department of Immunology
Institut Pasteur, Paris
Department of Clinical Pathology and Cytology
Karolinska University Hospital
Dynamics of Immune Responses Unit
Unit for Lymphopoiesis
Institut Pasteur
Center for Translational Research
Immunobiology of Infection Unit
Immunity and Cancer Unit
Department of Immunology
Functional Genetics of Infectious Diseases Unit
Innate Immunity Unit
U1223
Institut Pasteur
Centre national de la recherche scientifique
Unité Microenvironment and Immunity
Department of Cell Biology and Infection
Global Health Institute
ENAC-IIC-GEL
Unité de Biologie des Populations Lymphocytaires
Unité Biologie et Génétique de la Paroi Bactérienne
Sorbonne Paris Cité
Université Paris 13
Laboratoire D'Immunologie Clinique
INSERM U869
Unité de Régulation Immunitaire et Vaccinologie
Center of Bioinformatics Biostatistics
Unit of Cytokine Signaling
Département D'hépatologie
Pôle Gérontologie
Immunoregulation Unit
Virus and Immunity Unit
INSERM U932
Unité de Génomique Virale et Vaccination
Department of Immunology
Pôle de Biologie
Laboratory of Human Evolutionary Genetics

Research output: Contribution to journal › Article › peer-review

108 Citations (Scopus)

Abstract

Induced pluripotent stem cells (iPSCs) have considerably impacted human developmental biology and regenerative medicine, notably because they circumvent the use of cells of embryonic origin and offer the potential to generate patient-specific pluripotent stem cells. However, conventional reprogramming protocols produce developmentally advanced, or primed, human iPSCs (hiPSCs), restricting their use to post-implantation human development modeling. Hence, there is a need for hiPSCs resembling preimplantation naive epiblast. Here, we develop a method to generate naive hiPSCs directly from somatic cells, using OKMS overexpression and specific culture conditions, further enabling parallel generation of their isogenic primed counterparts. We benchmark naive hiPSCs against human preimplantation epiblast and reveal remarkable concordance in their transcriptome, dependency on mitochondrial respiration and X-chromosome status. Collectively, our results are essential for the understanding of pluripotency regulation throughout preimplantation development and generate new opportunities for disease modeling and regenerative medicine.

Original language	English
Article number	360
Journal	Nature Communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02107-w
Publication status	Published - 1 Dec 2018
Externally published	Yes

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This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

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10.1038/s41467-017-02107-w

Cite this

Kilens, S., Meistermann, DI., Moreno, DI., Chariau, C., Gaignerie, A., Reignier, A., Lelièvre, Y., Casanova, M., Vallot, C., Nedellec, S., Flippe, L., Firmin, J., Song, J., Charpentier, E., Lammers, J., Donnart, A., Marec, N., Deb, W., Bihouée, A., ... Albert, M. L. (2018). Parallel derivation of isogenic human primed and naive induced pluripotent stem cells. Nature Communications , 9(1), Article 360. https://doi.org/10.1038/s41467-017-02107-w

@article{c0cdb766dd9049e88b3453a4a5335183,

title = "Parallel derivation of isogenic human primed and naive induced pluripotent stem cells",

abstract = "Induced pluripotent stem cells (iPSCs) have considerably impacted human developmental biology and regenerative medicine, notably because they circumvent the use of cells of embryonic origin and offer the potential to generate patient-specific pluripotent stem cells. However, conventional reprogramming protocols produce developmentally advanced, or primed, human iPSCs (hiPSCs), restricting their use to post-implantation human development modeling. Hence, there is a need for hiPSCs resembling preimplantation naive epiblast. Here, we develop a method to generate naive hiPSCs directly from somatic cells, using OKMS overexpression and specific culture conditions, further enabling parallel generation of their isogenic primed counterparts. We benchmark naive hiPSCs against human preimplantation epiblast and reveal remarkable concordance in their transcriptome, dependency on mitochondrial respiration and X-chromosome status. Collectively, our results are essential for the understanding of pluripotency regulation throughout preimplantation development and generate new opportunities for disease modeling and regenerative medicine.",

author = "St{\'e}phanie Kilens and DImitri Meistermann and DIego Moreno and Caroline Chariau and Anne Gaignerie and Arnaud Reignier and Yohann Leli{\`e}vre and Miguel Casanova and C{\'e}line Vallot and Steven Nedellec and L{\'e}a Flippe and Julie Firmin and Juan Song and Eric Charpentier and Jenna Lammers and Audrey Donnart and Nad{\`e}ge Marec and Wallid Deb and Audrey Bihou{\'e}e and \{Le Caignec\}, C{\'e}dric and Claire Pecqueur and Richard Redon and Paul Barri{\`e}re and J{\'e}r{\'e}mie Bourdon and Vincent Pasque and Magali Soumillon and Mikkelsen, \{Tarjei S.\} and Claire Rougeulle and Thomas Fr{\'e}our and Laurent David and Laurent Abel and Andres Alcover and Kalla Astrom and Philippe Bousso and Pierre Bruhns and Ana Cumano and Darragh Duffy and Caroline Demangel and Ludovic Deriano and \{DI Santo\}, James and Fran{\c c}oise Dromer and G{\'e}rard Eberl and Jost Enninga and Jacques Fellay and Antonio Freitas and Odile Gelpi and Ivo Gomperts-Boneca and Serge Hercberg and Olivier Lantz and Claude Leclerc and Hugo Mouquet and Etienne Patin and Sandra Pellegrini and Stanislas Pol and Lars Rogge and Anavaj Sakuntabhai and Olivier Schwartz and Benno Schwikowski and Spencer Shorte and Vassili Soumelis and Fr{\'e}d{\'e}ric Tangy and Eric Tartour and Antoine Toubert and Ungeheuer, \{Marie No{\"e}lle\} and Lluis Quintana-Murci and Albert, \{Matthew L.\}",

note = "Publisher Copyright: {\textcopyright} 2018 The Author(s).",

year = "2018",

month = dec,

day = "1",

doi = "10.1038/s41467-017-02107-w",

language = "English",

volume = "9",

journal = "Nature Communications ",

issn = "2041-1723",

number = "1",

}

Kilens, S, Meistermann, DI, Moreno, DI, Chariau, C, Gaignerie, A, Reignier, A, Lelièvre, Y, Casanova, M, Vallot, C, Nedellec, S, Flippe, L, Firmin, J, Song, J, Charpentier, E, Lammers, J, Donnart, A, Marec, N, Deb, W, Bihouée, A, Le Caignec, C, Pecqueur, C, Redon, R, Barrière, P, Bourdon, J, Pasque, V, Soumillon, M, Mikkelsen, TS, Rougeulle, C, Fréour, T, David, L, Abel, L, Alcover, A, Astrom, K, Bousso, P, Bruhns, P, Cumano, A, Duffy, D, Demangel, C, Deriano, L, DI Santo, J, Dromer, F, Eberl, G, Enninga, J, Fellay, J, Freitas, A, Gelpi, O, Gomperts-Boneca, I, Hercberg, S, Lantz, O, Leclerc, C, Mouquet, H, Patin, E, Pellegrini, S, Pol, S, Rogge, L, Sakuntabhai, A, Schwartz, O, Schwikowski, B, Shorte, S, Soumelis, V, Tangy, F, Tartour, E, Toubert, A, Ungeheuer, MN, Quintana-Murci, L & Albert, ML 2018, 'Parallel derivation of isogenic human primed and naive induced pluripotent stem cells', Nature Communications , vol. 9, no. 1, 360. https://doi.org/10.1038/s41467-017-02107-w

TY - JOUR

T1 - Parallel derivation of isogenic human primed and naive induced pluripotent stem cells

AU - Kilens, Stéphanie

AU - Meistermann, DImitri

AU - Moreno, DIego

AU - Chariau, Caroline

AU - Gaignerie, Anne

AU - Reignier, Arnaud

AU - Lelièvre, Yohann

AU - Casanova, Miguel

AU - Vallot, Céline

AU - Nedellec, Steven

AU - Flippe, Léa

AU - Firmin, Julie

AU - Song, Juan

AU - Charpentier, Eric

AU - Lammers, Jenna

AU - Donnart, Audrey

AU - Marec, Nadège

AU - Deb, Wallid

AU - Bihouée, Audrey

AU - Le Caignec, Cédric

AU - Pecqueur, Claire

AU - Redon, Richard

AU - Barrière, Paul

AU - Bourdon, Jérémie

AU - Pasque, Vincent

AU - Soumillon, Magali

AU - Mikkelsen, Tarjei S.

AU - Rougeulle, Claire

AU - Fréour, Thomas

AU - David, Laurent

AU - Abel, Laurent

AU - Alcover, Andres

AU - Astrom, Kalla

AU - Bousso, Philippe

AU - Bruhns, Pierre

AU - Cumano, Ana

AU - Duffy, Darragh

AU - Demangel, Caroline

AU - Deriano, Ludovic

AU - DI Santo, James

AU - Dromer, Françoise

AU - Eberl, Gérard

AU - Enninga, Jost

AU - Fellay, Jacques

AU - Freitas, Antonio

AU - Gelpi, Odile

AU - Gomperts-Boneca, Ivo

AU - Hercberg, Serge

AU - Lantz, Olivier

AU - Leclerc, Claude

AU - Mouquet, Hugo

AU - Patin, Etienne

AU - Pellegrini, Sandra

AU - Pol, Stanislas

AU - Rogge, Lars

AU - Sakuntabhai, Anavaj

AU - Schwartz, Olivier

AU - Schwikowski, Benno

AU - Shorte, Spencer

AU - Soumelis, Vassili

AU - Tangy, Frédéric

AU - Tartour, Eric

AU - Toubert, Antoine

AU - Ungeheuer, Marie Noëlle

AU - Quintana-Murci, Lluis

AU - Albert, Matthew L.

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Induced pluripotent stem cells (iPSCs) have considerably impacted human developmental biology and regenerative medicine, notably because they circumvent the use of cells of embryonic origin and offer the potential to generate patient-specific pluripotent stem cells. However, conventional reprogramming protocols produce developmentally advanced, or primed, human iPSCs (hiPSCs), restricting their use to post-implantation human development modeling. Hence, there is a need for hiPSCs resembling preimplantation naive epiblast. Here, we develop a method to generate naive hiPSCs directly from somatic cells, using OKMS overexpression and specific culture conditions, further enabling parallel generation of their isogenic primed counterparts. We benchmark naive hiPSCs against human preimplantation epiblast and reveal remarkable concordance in their transcriptome, dependency on mitochondrial respiration and X-chromosome status. Collectively, our results are essential for the understanding of pluripotency regulation throughout preimplantation development and generate new opportunities for disease modeling and regenerative medicine.

AB - Induced pluripotent stem cells (iPSCs) have considerably impacted human developmental biology and regenerative medicine, notably because they circumvent the use of cells of embryonic origin and offer the potential to generate patient-specific pluripotent stem cells. However, conventional reprogramming protocols produce developmentally advanced, or primed, human iPSCs (hiPSCs), restricting their use to post-implantation human development modeling. Hence, there is a need for hiPSCs resembling preimplantation naive epiblast. Here, we develop a method to generate naive hiPSCs directly from somatic cells, using OKMS overexpression and specific culture conditions, further enabling parallel generation of their isogenic primed counterparts. We benchmark naive hiPSCs against human preimplantation epiblast and reveal remarkable concordance in their transcriptome, dependency on mitochondrial respiration and X-chromosome status. Collectively, our results are essential for the understanding of pluripotency regulation throughout preimplantation development and generate new opportunities for disease modeling and regenerative medicine.

U2 - 10.1038/s41467-017-02107-w

DO - 10.1038/s41467-017-02107-w

M3 - Article

C2 - 29367672

AN - SCOPUS:85041034731

SN - 2041-1723

VL - 9

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 360

ER -

Parallel derivation of isogenic human primed and naive induced pluripotent stem cells

Abstract

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