Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids

Ary Marsee; Floris J.M. Roos; Monique M.A. Verstegen; Floris Roos; Monique Verstegen; Hans Clevers; Ludovic Vallier; Takanori Takebe; Meritxell Huch; Weng Chuan Peng; Stuart Forbes; Frédéric Lemaigre; Eelco de Koning; Helmuth Gehart; Luc van der Laan; Bart Spee; Sylvia Boj; Pedro Baptista; Kerstin Schneeberger; Carol Soroka; Markus Heim; Sandro Nuciforo; Kenneth Zaret; Yoshimasa Saito; Matthias Lutolf; Vincenzo Cardinale; Ben Simons; Sven van IJzendoorn; Akihide Kamiya; Hiromi Chikada; Shuyong Wang; Seon Ju Mun; Myung Jin Son; Tamer Tevfik Onder; James Boyer; Toshiro Sato; Nikitas Georgakopoulos; Andre Meneses; Laura Broutier; Luke Boulter; Dominic Grün; Jan IJzermans; Benedetta Artegiani; Ruben van Boxtel; Ewart Kuijk; Guido Carpino; Gary Peltz; Jesus Banales; Nancy Man; Sabine Fuchs

doi:10.1016/j.stem.2021.04.005

Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids

Ary Marsee
, Floris J.M. Roos
, Monique M.A. Verstegen
, Floris Roos
, Monique Verstegen
, Hans Clevers
, Ludovic Vallier
, Takanori Takebe
, Meritxell Huch
, Weng Chuan Peng
, Stuart Forbes
, Frédéric Lemaigre
, Eelco de Koning
, Helmuth Gehart
, Luc van der Laan
, Bart Spee^*
, Sylvia Boj
, Pedro Baptista
, Kerstin Schneeberger
, Carol Soroka

Markus Heim, Sandro Nuciforo, Kenneth Zaret, Yoshimasa Saito, Matthias Lutolf, Vincenzo Cardinale, Ben Simons, Sven van IJzendoorn, Akihide Kamiya, Hiromi Chikada, Shuyong Wang, Seon Ju Mun, Myung Jin Son, Tamer Tevfik Onder, James Boyer, Toshiro Sato, Nikitas Georgakopoulos, Andre Meneses, Laura Broutier, Luke Boulter, Dominic Grün, Jan IJzermans, Benedetta Artegiani, Ruben van Boxtel, Ewart Kuijk, Guido Carpino, Gary Peltz, Jesus Banales, Nancy Man, Sabine Fuchs,

^*Corresponding author for this work

Research output: Contribution to journal › Review article › peer-review

21 Citations (Scopus)

Abstract

Hepatic, pancreatic, and biliary (HPB) organoids are powerful tools for studying development, disease, and regeneration. As organoid research expands, the need for clear definitions and nomenclature describing these systems also grows. To facilitate scientific communication and consistent interpretation, we revisit the concept of an organoid and introduce an intuitive classification system and nomenclature for describing these 3D structures through the consensus of experts in the field. To promote the standardization and validation of HPB organoids, we propose guidelines for establishing, characterizing, and benchmarking future systems. Finally, we address some of the major challenges to the clinical application of organoids.

Original language	English
Pages (from-to)	816-832
Number of pages	17
Journal	Cell stem cell
Volume	28
Issue number	5
DOIs	https://doi.org/10.1016/j.stem.2021.04.005
Publication status	Published - 6 May 2021

Keywords

bile duct
Delphi method
epithelial organoid
gallbladder
HPB
liver
multi-organ organoid
multi-tissue organoid
pancreas
tumor organoid

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10.1016/j.stem.2021.04.005

1-s2.0-S1934590921001624-mainFinal published version, 2.36 MBLicence: Taverne

Cite this

Marsee, A., Roos, F. J. M., Verstegen, M. M. A., Roos, F., Verstegen, M., Clevers, H., Vallier, L., Takebe, T., Huch, M., Peng, W. C., Forbes, S., Lemaigre, F., de Koning, E., Gehart, H., van der Laan, L., Spee, B., Boj, S., Baptista, P., Schneeberger, K., ... ETH Zurich (2021). Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids. Cell stem cell, 28(5), 816-832. https://doi.org/10.1016/j.stem.2021.04.005

@article{341705ba047744098b2d5181939f925e,

title = "Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids",

abstract = "Hepatic, pancreatic, and biliary (HPB) organoids are powerful tools for studying development, disease, and regeneration. As organoid research expands, the need for clear definitions and nomenclature describing these systems also grows. To facilitate scientific communication and consistent interpretation, we revisit the concept of an organoid and introduce an intuitive classification system and nomenclature for describing these 3D structures through the consensus of experts in the field. To promote the standardization and validation of HPB organoids, we propose guidelines for establishing, characterizing, and benchmarking future systems. Finally, we address some of the major challenges to the clinical application of organoids.",

keywords = "bile duct, Delphi method, epithelial organoid, gallbladder, HPB, liver, multi-organ organoid, multi-tissue organoid, pancreas, tumor organoid",

author = "Ary Marsee and Roos, \{Floris J.M.\} and Verstegen, \{Monique M.A.\} and Floris Roos and Monique Verstegen and Hans Clevers and Ludovic Vallier and Takanori Takebe and Meritxell Huch and Peng, \{Weng Chuan\} and Stuart Forbes and Fr{\'e}d{\'e}ric Lemaigre and \{de Koning\}, Eelco and Helmuth Gehart and \{van der Laan\}, Luc and Bart Spee and Sylvia Boj and Pedro Baptista and Kerstin Schneeberger and Carol Soroka and Markus Heim and Sandro Nuciforo and Kenneth Zaret and Yoshimasa Saito and Matthias Lutolf and Vincenzo Cardinale and Ben Simons and \{van IJzendoorn\}, Sven and Akihide Kamiya and Hiromi Chikada and Shuyong Wang and Mun, \{Seon Ju\} and Son, \{Myung Jin\} and Onder, \{Tamer Tevfik\} and James Boyer and Toshiro Sato and Nikitas Georgakopoulos and Andre Meneses and Laura Broutier and Luke Boulter and Dominic Gr{\"u}n and Jan IJzermans and Benedetta Artegiani and \{van Boxtel\}, Ruben and Ewart Kuijk and Guido Carpino and Gary Peltz and Jesus Banales and Nancy Man and Sabine Fuchs",

note = "Funding Information: The L.J.W.v.d.L. lab is supported by the MLDS-Diagnostiek grant D16-26 of the Dutch Gastroenterology \& Hepatology Fund (MLDS) and the Medical Delta Regenerative Medicine 4D program. The B.S. lab is supported by the European Union{\textquoteright}s Horizon 2020 research and innovation program under grant agreement no. 874586 . The L.V. lab is funded by the ERC advanced grant New-Chol, the Cambridge University Hospitals National Institute for Health Research Biomedical Research Centre, and the core support grant from the Wellcome and Medical Research Council Cambridge Stem Cell Institute. The M.H. lab is funded by a Lise Meitner Excellence Program award from the Max Planck Society. For a detailed breakdown of the additional affiliations, locations, and roles of each HPB Organoid Consortium member, see Table S1 . Funding Information: The L.J.W.v.d.L. lab is supported by the MLDS-Diagnostiek grant D16-26 of the Dutch Gastroenterology \& Hepatology Fund (MLDS) and the Medical Delta Regenerative Medicine 4D program. The B.S. lab is supported by the European Union's Horizon 2020 research and innovation program under grant agreement no. 874586. The L.V. lab is funded by the ERC advanced grant New-Chol, the Cambridge University Hospitals National Institute for Health Research Biomedical Research Centre, and the core support grant from the Wellcome and Medical Research Council Cambridge Stem Cell Institute. The M.H. lab is funded by a Lise Meitner Excellence Program award from the Max Planck Society. For a detailed breakdown of the additional affiliations, locations, and roles of each HPB Organoid Consortium member, see Table S1. A.M. and F.J.M.R. drafted the manuscript, designed the questionnaires, and contacted all experts from the HPB organoid consortium. A.M. F.J.M.R. M.M.A.V. H.G. E.d.K. F.L. S.J.F. W.C.P. M.H. T.T. L.V. H.C. L.J.W.v.d.L. and B.S. discussed questionnaire results and provided recommendations. All authors discussed the results and contributed to the final manuscript. H.G. M.H. T.T. L.V. and H.C. are inventors on several patents related to organoid technology. Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",

year = "2021",

month = may,

day = "6",

doi = "10.1016/j.stem.2021.04.005",

language = "English",

volume = "28",

pages = "816--832",

journal = "Cell stem cell",

issn = "1934-5909",

publisher = "Cell Press",

number = "5",

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Marsee, A, Roos, FJM, Verstegen, MMA, Roos, F, Verstegen, M, Clevers, H, Vallier, L, Takebe, T, Huch, M, Peng, WC, Forbes, S, Lemaigre, F, de Koning, E, Gehart, H, van der Laan, L, Spee, B, Boj, S, Baptista, P, Schneeberger, K, Soroka, C, Heim, M, Nuciforo, S, Zaret, K, Saito, Y, Lutolf, M, Cardinale, V, Simons, B, van IJzendoorn, S, Kamiya, A, Chikada, H, Wang, S, Mun, SJ, Son, MJ, Onder, TT, Boyer, J, Sato, T, Georgakopoulos, N, Meneses, A, Broutier, L, Boulter, L, Grün, D, IJzermans, J, Artegiani, B, van Boxtel, R, Kuijk, E, Carpino, G, Peltz, G, Banales, J, Man, N, Fuchs, S & ETH Zurich 2021, 'Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids', Cell stem cell, vol. 28, no. 5, pp. 816-832. https://doi.org/10.1016/j.stem.2021.04.005

TY - JOUR

T1 - Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids

AU - Marsee, Ary

AU - Roos, Floris J.M.

AU - Verstegen, Monique M.A.

AU - Roos, Floris

AU - Verstegen, Monique

AU - Clevers, Hans

AU - Vallier, Ludovic

AU - Takebe, Takanori

AU - Huch, Meritxell

AU - Peng, Weng Chuan

AU - Forbes, Stuart

AU - Lemaigre, Frédéric

AU - de Koning, Eelco

AU - Gehart, Helmuth

AU - van der Laan, Luc

AU - Spee, Bart

AU - Boj, Sylvia

AU - Baptista, Pedro

AU - Schneeberger, Kerstin

AU - Soroka, Carol

AU - Heim, Markus

AU - Nuciforo, Sandro

AU - Zaret, Kenneth

AU - Saito, Yoshimasa

AU - Lutolf, Matthias

AU - Cardinale, Vincenzo

AU - Simons, Ben

AU - van IJzendoorn, Sven

AU - Kamiya, Akihide

AU - Chikada, Hiromi

AU - Wang, Shuyong

AU - Mun, Seon Ju

AU - Son, Myung Jin

AU - Onder, Tamer Tevfik

AU - Boyer, James

AU - Sato, Toshiro

AU - Georgakopoulos, Nikitas

AU - Meneses, Andre

AU - Broutier, Laura

AU - Boulter, Luke

AU - Grün, Dominic

AU - IJzermans, Jan

AU - Artegiani, Benedetta

AU - van Boxtel, Ruben

AU - Kuijk, Ewart

AU - Carpino, Guido

AU - Peltz, Gary

AU - Banales, Jesus

AU - Man, Nancy

AU - Fuchs, Sabine

N1 - Funding Information: The L.J.W.v.d.L. lab is supported by the MLDS-Diagnostiek grant D16-26 of the Dutch Gastroenterology & Hepatology Fund (MLDS) and the Medical Delta Regenerative Medicine 4D program. The B.S. lab is supported by the European Union’s Horizon 2020 research and innovation program under grant agreement no. 874586 . The L.V. lab is funded by the ERC advanced grant New-Chol, the Cambridge University Hospitals National Institute for Health Research Biomedical Research Centre, and the core support grant from the Wellcome and Medical Research Council Cambridge Stem Cell Institute. The M.H. lab is funded by a Lise Meitner Excellence Program award from the Max Planck Society. For a detailed breakdown of the additional affiliations, locations, and roles of each HPB Organoid Consortium member, see Table S1 . Funding Information: The L.J.W.v.d.L. lab is supported by the MLDS-Diagnostiek grant D16-26 of the Dutch Gastroenterology & Hepatology Fund (MLDS) and the Medical Delta Regenerative Medicine 4D program. The B.S. lab is supported by the European Union's Horizon 2020 research and innovation program under grant agreement no. 874586. The L.V. lab is funded by the ERC advanced grant New-Chol, the Cambridge University Hospitals National Institute for Health Research Biomedical Research Centre, and the core support grant from the Wellcome and Medical Research Council Cambridge Stem Cell Institute. The M.H. lab is funded by a Lise Meitner Excellence Program award from the Max Planck Society. For a detailed breakdown of the additional affiliations, locations, and roles of each HPB Organoid Consortium member, see Table S1. A.M. and F.J.M.R. drafted the manuscript, designed the questionnaires, and contacted all experts from the HPB organoid consortium. A.M. F.J.M.R. M.M.A.V. H.G. E.d.K. F.L. S.J.F. W.C.P. M.H. T.T. L.V. H.C. L.J.W.v.d.L. and B.S. discussed questionnaire results and provided recommendations. All authors discussed the results and contributed to the final manuscript. H.G. M.H. T.T. L.V. and H.C. are inventors on several patents related to organoid technology. Publisher Copyright: © 2021 Elsevier Inc.

PY - 2021/5/6

Y1 - 2021/5/6

N2 - Hepatic, pancreatic, and biliary (HPB) organoids are powerful tools for studying development, disease, and regeneration. As organoid research expands, the need for clear definitions and nomenclature describing these systems also grows. To facilitate scientific communication and consistent interpretation, we revisit the concept of an organoid and introduce an intuitive classification system and nomenclature for describing these 3D structures through the consensus of experts in the field. To promote the standardization and validation of HPB organoids, we propose guidelines for establishing, characterizing, and benchmarking future systems. Finally, we address some of the major challenges to the clinical application of organoids.

AB - Hepatic, pancreatic, and biliary (HPB) organoids are powerful tools for studying development, disease, and regeneration. As organoid research expands, the need for clear definitions and nomenclature describing these systems also grows. To facilitate scientific communication and consistent interpretation, we revisit the concept of an organoid and introduce an intuitive classification system and nomenclature for describing these 3D structures through the consensus of experts in the field. To promote the standardization and validation of HPB organoids, we propose guidelines for establishing, characterizing, and benchmarking future systems. Finally, we address some of the major challenges to the clinical application of organoids.

KW - bile duct

KW - Delphi method

KW - epithelial organoid

KW - gallbladder

KW - HPB

KW - liver

KW - multi-organ organoid

KW - multi-tissue organoid

KW - pancreas

KW - tumor organoid

UR - https://www.scopus.com/pages/publications/85105055143

U2 - 10.1016/j.stem.2021.04.005

DO - 10.1016/j.stem.2021.04.005

M3 - Review article

AN - SCOPUS:85105055143

SN - 1934-5909

VL - 28

SP - 816

EP - 832

JO - Cell stem cell

JF - Cell stem cell

IS - 5

ER -

Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids

Abstract

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