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Two decades of embryonic stem cells : a historical overview

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Abstract
STUDY QUESTION How did the field of stem cell research develop in the years following the derivation of the first human embryonic stem cell (hESC) line? SUMMARY ANSWER Supported by the increasing number of clinical trials to date, significant technological advances in the past two decades have brought us ever closer to clinical therapies derived from pluripotent cells. WHAT IS KNOWN ALREADY Since their discovery 20 years ago, the use of human pluripotent stem cells has progressed tremendously from bench to bedside. Here, we provide a concise review of the main keystones of this journey and focus on ongoing clinical trials, while indicating the most relevant future research directions. STUDY DESIGN, SIZE, DURATION This is a historical narrative, including relevant publications in the field of pluripotent stem cells (PSC) derivation and differentiation, recounted both through scholarly research of published evidence and interviews of six pioneers who participated in some of the most relevant discoveries in the field. PARTICIPANTS/MATERIALS, SETTING, METHODS The authors all contributed by researching the literature and agreed upon body of works. Portions of the interviews of the field pioneers have been integrated into the review and have also been included in full for advanced reader interest. MAIN RESULTS AND THE ROLE OF CHANCE The stem cell field is ever expanding. We find that in the 20 years since the derivation of the first hESC lines, several relevant developments have shaped the pluripotent cell field, from the discovery of different states of pluripotency, the derivation of induced PSC, the refinement of differentiation protocols with several clinical trials underway, as well as the recent development of organoids. The challenge for the years to come will be to validate and refine PSCs for clinical use, from the production of highly defined cell populations in clinical grade conditions to the possibility of creating replacement organoids for functional, if not anatomical, function restoration. LIMITATIONS, REASONS FOR CAUTION This is a non-systematic review of current literature. Some references may have escaped the experts’ analysis due to the exceedingly diverse nature of the field. As the field of regenerative medicine is rapidly advancing, some of the most recent developments may have not been captured entirely. WIDER IMPLICATIONS OF THE FINDINGS The multi-disciplinary nature and tremendous potential of the stem cell field has important implications for basic as well as translational research. Recounting these activities will serve to provide an in-depth overview of the field, fostering a further understanding of human stem cell and developmental biology. The comprehensive overview of clinical trials and expert opinions included in this narrative may serve as a valuable scientific resource, supporting future efforts in translational approaches. STUDY FUNDING/COMPETING INTEREST(S) ESHRE provided funding for the authors’ on-site meeting and discussion during the preparation of this manuscript. S.M.C.S.L. is funded by the European Research Council Consolidator (ERC-CoG-725722-OVOGROWTH). M.P. is supported by the Special Research Fund, Bijzonder Onderzoeksfonds (BOF01D08114). M.G. is supported by the Methusalem grant of Vrije Universiteit Brussel, in the name of Prof. Karen Sermon and by Innovation by Science and Technology in Flanders (IWT, Project Number: 150042). A.V. and B.A. are supported by the Plataforma de Proteomica, Genotipado y Líneas Celulares (PT1770019/0015) (PRB3), Instituto de Salud Carlos III. Research grant to B.H. by the Research Foundation—Flanders (FWO) (FWO.KAN.2016.0005.01 and FWO.Project G051516N). There are no conflicts of interest to declare. TRIAL REGISTRATION NUMBER Not applicable. ESHRE Pages are not externally peer reviewed. This article has been approved by the Executive Committee of ESHRE.
Keywords
pluripotency, human embryonic stem cell (hESC), human-induced pluripotent stem cells (hiPSC), regenerative medicine, differentiation, clinical trials

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MLA
Eguizabal, Cristina, et al. “Two Decades of Embryonic Stem Cells : A Historical Overview.” HUMAN REPRODUCTION OPEN, no. 1, 2019, pp. 1–17, doi:10.1093/hropen/hoy024.
APA
Eguizabal, C., Aran, B., Chuva de Sousa Lopes, S. M., Geens, M., Heindryckx, B., Panula, S., … Veiga, A. (2019). Two decades of embryonic stem cells : a historical overview. HUMAN REPRODUCTION OPEN, (1), 1–17. https://doi.org/10.1093/hropen/hoy024
Chicago author-date
Eguizabal, Cristina, Begoña Aran, Susana Marina Chuva de Sousa Lopes, M. Geens, Björn Heindryckx, S. Panula, Mina Popovic, Rita Vassena, and Anna Veiga. 2019. “Two Decades of Embryonic Stem Cells : A Historical Overview.” HUMAN REPRODUCTION OPEN, no. 1: 1–17. https://doi.org/10.1093/hropen/hoy024.
Chicago author-date (all authors)
Eguizabal, Cristina, Begoña Aran, Susana Marina Chuva de Sousa Lopes, M. Geens, Björn Heindryckx, S. Panula, Mina Popovic, Rita Vassena, and Anna Veiga. 2019. “Two Decades of Embryonic Stem Cells : A Historical Overview.” HUMAN REPRODUCTION OPEN (1): 1–17. doi:10.1093/hropen/hoy024.
Vancouver
1.
Eguizabal C, Aran B, Chuva de Sousa Lopes SM, Geens M, Heindryckx B, Panula S, et al. Two decades of embryonic stem cells : a historical overview. HUMAN REPRODUCTION OPEN. 2019;(1):1–17.
IEEE
[1]
C. Eguizabal et al., “Two decades of embryonic stem cells : a historical overview,” HUMAN REPRODUCTION OPEN, no. 1, pp. 1–17, 2019.
@article{8679404,
  abstract     = {STUDY QUESTION
How did the field of stem cell research develop in the years following the derivation of the first human embryonic stem cell (hESC) line?

SUMMARY ANSWER
Supported by the increasing number of clinical trials to date, significant technological advances in the past two decades have brought us ever closer to clinical therapies derived from pluripotent cells.

WHAT IS KNOWN ALREADY
Since their discovery 20 years ago, the use of human pluripotent stem cells has progressed tremendously from bench to bedside. Here, we provide a concise review of the main keystones of this journey and focus on ongoing clinical trials, while indicating the most relevant future research directions.

STUDY DESIGN, SIZE, DURATION
This is a historical narrative, including relevant publications in the field of pluripotent stem cells (PSC) derivation and differentiation, recounted both through scholarly research of published evidence and interviews of six pioneers who participated in some of the most relevant discoveries in the field.

PARTICIPANTS/MATERIALS, SETTING, METHODS
The authors all contributed by researching the literature and agreed upon body of works. Portions of the interviews of the field pioneers have been integrated into the review and have also been included in full for advanced reader interest.

MAIN RESULTS AND THE ROLE OF CHANCE
The stem cell field is ever expanding. We find that in the 20 years since the derivation of the first hESC lines, several relevant developments have shaped the pluripotent cell field, from the discovery of different states of pluripotency, the derivation of induced PSC, the refinement of differentiation protocols with several clinical trials underway, as well as the recent development of organoids. The challenge for the years to come will be to validate and refine PSCs for clinical use, from the production of highly defined cell populations in clinical grade conditions to the possibility of creating replacement organoids for functional, if not anatomical, function restoration.

LIMITATIONS, REASONS FOR CAUTION
This is a non-systematic review of current literature. Some references may have escaped the experts’ analysis due to the exceedingly diverse nature of the field. As the field of regenerative medicine is rapidly advancing, some of the most recent developments may have not been captured entirely.

WIDER IMPLICATIONS OF THE FINDINGS
The multi-disciplinary nature and tremendous potential of the stem cell field has important implications for basic as well as translational research. Recounting these activities will serve to provide an in-depth overview of the field, fostering a further understanding of human stem cell and developmental biology. The comprehensive overview of clinical trials and expert opinions included in this narrative may serve as a valuable scientific resource, supporting future efforts in translational approaches.

STUDY FUNDING/COMPETING INTEREST(S)
ESHRE provided funding for the authors’ on-site meeting and discussion during the preparation of this manuscript. S.M.C.S.L. is funded by the European Research Council Consolidator (ERC-CoG-725722-OVOGROWTH). M.P. is supported by the Special Research Fund, Bijzonder Onderzoeksfonds (BOF01D08114). M.G. is supported by the Methusalem grant of Vrije Universiteit Brussel, in the name of Prof. Karen Sermon and by Innovation by Science and Technology in Flanders (IWT, Project Number: 150042). A.V. and B.A. are supported by the Plataforma de Proteomica, Genotipado y Líneas Celulares (PT1770019/0015) (PRB3), Instituto de Salud Carlos III. Research grant to B.H. by the Research Foundation—Flanders (FWO) (FWO.KAN.2016.0005.01 and FWO.Project G051516N). There are no conflicts of interest to declare.

TRIAL REGISTRATION NUMBER
Not applicable.

ESHRE Pages are not externally peer reviewed. This article has been approved by the Executive Committee of ESHRE.},
  author       = {Eguizabal, Cristina and Aran, Begoña and Chuva de Sousa Lopes, Susana Marina and Geens, M. and Heindryckx, Björn and Panula, S. and Popovic, Mina and Vassena, Rita and Veiga, Anna},
  issn         = {2399-3529},
  journal      = {HUMAN REPRODUCTION OPEN},
  keywords     = {pluripotency,human embryonic stem cell (hESC),human-induced pluripotent stem cells (hiPSC),regenerative medicine,differentiation,clinical trials},
  language     = {eng},
  number       = {1},
  pages        = {1--17},
  title        = {Two decades of embryonic stem cells : a historical overview},
  url          = {http://dx.doi.org/10.1093/hropen/hoy024},
  year         = {2019},
}

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