Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

Chloé Mayère; Violaine Regard; Aitana Perea-Gomez; Corey Bunce; Yasmine Neirijnck; Cyril Djari; Natividad Bellido-Carreras; Pauline Sararols; Richard Reeves; Simon Greenaway; Michelle Simon; Pam Siggers; Diana Condrea; Françoise Kühne; Ivana Gantar; Furong Tang; Isabelle Stévant; Laura Batti; Norbert B. Ghyselinck; Dagmar Wilhelm; Andy Greenfield; Blanche Capel; Marie Christine Chaboissier; Serge Nef

doi:10.1126/sciadv.abm0972

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

Chloé Mayère
, Violaine Regard
, Aitana Perea-Gomez
, Corey Bunce
, Yasmine Neirijnck
, Cyril Djari
, Natividad Bellido-Carreras
, Pauline Sararols
, Richard Reeves
, Simon Greenaway
, Michelle Simon
, Pam Siggers
, Diana Condrea
, Françoise Kühne
, Ivana Gantar
, Furong Tang
, Isabelle Stévant
, Laura Batti
, Norbert B. Ghyselinck
, Dagmar Wilhelm

Andy Greenfield, Blanche Capel, Marie Christine Chaboissier, Serge Nef

University of Geneva
Université Côte d'Azur
Duke University
Medical Research Council
Université de Strasbourg
Wyss Center for Bio and Neuroengineering
University of Melbourne

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

56 Scopus citations

Abstract

Gonadal sex determination represents a unique model for studying cell fate decisions. However, a complete understanding of the different cell lineages forming the developing testis and ovary remains elusive. Here, we investigated the origin, specification, and subsequent sex-specific differentiation of a previously uncharacterized population of supporting-like cells (SLCs) in the developing mouse gonads. The SLC lineage is closely related to the coelomic epithelium and specified as early as E10.5, making it the first somatic lineage to be specified in the bipotential gonad. SLC progenitors are localized within the genital ridge at the interface with the mesonephros and initially coexpress Wnt4 and Sox9. SLCs become sexually dimorphic around E12.5, progressively acquire a more Sertoli- or pregranulosa-like identity and contribute to the formation of the rete testis and rete ovarii. Last, we found that WNT4 is a crucial regulator of the SLC lineage and is required for normal development of the rete testis.

Original language	English
Article number	eabm0972
Journal	Science advances
Volume	8
Issue number	21
DOIs	https://doi.org/10.1126/sciadv.abm0972
State	Published - 27 May 2022
Externally published	Yes

Bibliographical note

Publisher Copyright:
Copyright © 2022 The Authors, some rights reserved.

Funding

Swiss National Science Foundation grant 31003A_173070 (S.N.), Swiss National Science Foundation grant 310030_200316 (S.N.), Département de l'Instruction Publique of the State of Geneva (S.N.), Agence Nationale de la Recherche grant ANR-19-CE14-0022-01 SexDiff (M.-C.C.), UK Medical Research Council grant MC_U142684167 (A.G.), National Institutes of Health grant 1R01HD090050 (B.C. and C.B.), and National Institutes of Health grant R37HD039963 (B.C.). N.B.G. and C.D. were supported by grants from Agence Nationale de la Recherche (ANR-16-CE14-0017 and ANR-20-CE14-0022).

Funders	Funder number
Département de l'Instruction Publique of the State of Geneva
National Institutes of Health	ANR-20-CE14-0022, ANR-16-CE14-0017, 1R01HD090050
National Institute of Child Health and Human Development	R01HD039963
Medical Research Council	MC_U142684167
Agence Nationale de la Recherche	ANR-19-CE14-0022-01
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	310030_200316, 31003A_173070

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10.1126/sciadv.abm0972

Cite this

Mayère, C., Regard, V., Perea-Gomez, A., Bunce, C., Neirijnck, Y., Djari, C., Bellido-Carreras, N., Sararols, P., Reeves, R., Greenaway, S., Simon, M., Siggers, P., Condrea, D., Kühne, F., Gantar, I., Tang, F., Stévant, I., Batti, L., Ghyselinck, N. B., ... Nef, S. (2022). Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad. Science advances, 8(21), Article eabm0972. https://doi.org/10.1126/sciadv.abm0972

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title = "Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad",

abstract = "Gonadal sex determination represents a unique model for studying cell fate decisions. However, a complete understanding of the different cell lineages forming the developing testis and ovary remains elusive. Here, we investigated the origin, specification, and subsequent sex-specific differentiation of a previously uncharacterized population of supporting-like cells (SLCs) in the developing mouse gonads. The SLC lineage is closely related to the coelomic epithelium and specified as early as E10.5, making it the first somatic lineage to be specified in the bipotential gonad. SLC progenitors are localized within the genital ridge at the interface with the mesonephros and initially coexpress Wnt4 and Sox9. SLCs become sexually dimorphic around E12.5, progressively acquire a more Sertoli- or pregranulosa-like identity and contribute to the formation of the rete testis and rete ovarii. Last, we found that WNT4 is a crucial regulator of the SLC lineage and is required for normal development of the rete testis.",

author = "Chlo{\'e} May{\`e}re and Violaine Regard and Aitana Perea-Gomez and Corey Bunce and Yasmine Neirijnck and Cyril Djari and Natividad Bellido-Carreras and Pauline Sararols and Richard Reeves and Simon Greenaway and Michelle Simon and Pam Siggers and Diana Condrea and Fran{\c c}oise K{\"u}hne and Ivana Gantar and Furong Tang and Isabelle St{\'e}vant and Laura Batti and Ghyselinck, \{Norbert B.\} and Dagmar Wilhelm and Andy Greenfield and Blanche Capel and Chaboissier, \{Marie Christine\} and Serge Nef",

note = "Publisher Copyright: Copyright {\textcopyright} 2022 The Authors, some rights reserved.",

year = "2022",

month = may,

day = "27",

doi = "10.1126/sciadv.abm0972",

language = "אנגלית",

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Mayère, C, Regard, V, Perea-Gomez, A, Bunce, C, Neirijnck, Y, Djari, C, Bellido-Carreras, N, Sararols, P, Reeves, R, Greenaway, S, Simon, M, Siggers, P, Condrea, D, Kühne, F, Gantar, I, Tang, F, Stévant, I, Batti, L, Ghyselinck, NB, Wilhelm, D, Greenfield, A, Capel, B, Chaboissier, MC & Nef, S 2022, 'Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad', Science advances, vol. 8, no. 21, eabm0972. https://doi.org/10.1126/sciadv.abm0972

TY - JOUR

T1 - Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

AU - Mayère, Chloé

AU - Regard, Violaine

AU - Perea-Gomez, Aitana

AU - Bunce, Corey

AU - Neirijnck, Yasmine

AU - Djari, Cyril

AU - Bellido-Carreras, Natividad

AU - Sararols, Pauline

AU - Reeves, Richard

AU - Greenaway, Simon

AU - Simon, Michelle

AU - Siggers, Pam

AU - Condrea, Diana

AU - Kühne, Françoise

AU - Gantar, Ivana

AU - Tang, Furong

AU - Stévant, Isabelle

AU - Batti, Laura

AU - Ghyselinck, Norbert B.

AU - Wilhelm, Dagmar

AU - Greenfield, Andy

AU - Capel, Blanche

AU - Chaboissier, Marie Christine

AU - Nef, Serge

PY - 2022/5/27

Y1 - 2022/5/27

N2 - Gonadal sex determination represents a unique model for studying cell fate decisions. However, a complete understanding of the different cell lineages forming the developing testis and ovary remains elusive. Here, we investigated the origin, specification, and subsequent sex-specific differentiation of a previously uncharacterized population of supporting-like cells (SLCs) in the developing mouse gonads. The SLC lineage is closely related to the coelomic epithelium and specified as early as E10.5, making it the first somatic lineage to be specified in the bipotential gonad. SLC progenitors are localized within the genital ridge at the interface with the mesonephros and initially coexpress Wnt4 and Sox9. SLCs become sexually dimorphic around E12.5, progressively acquire a more Sertoli- or pregranulosa-like identity and contribute to the formation of the rete testis and rete ovarii. Last, we found that WNT4 is a crucial regulator of the SLC lineage and is required for normal development of the rete testis.

AB - Gonadal sex determination represents a unique model for studying cell fate decisions. However, a complete understanding of the different cell lineages forming the developing testis and ovary remains elusive. Here, we investigated the origin, specification, and subsequent sex-specific differentiation of a previously uncharacterized population of supporting-like cells (SLCs) in the developing mouse gonads. The SLC lineage is closely related to the coelomic epithelium and specified as early as E10.5, making it the first somatic lineage to be specified in the bipotential gonad. SLC progenitors are localized within the genital ridge at the interface with the mesonephros and initially coexpress Wnt4 and Sox9. SLCs become sexually dimorphic around E12.5, progressively acquire a more Sertoli- or pregranulosa-like identity and contribute to the formation of the rete testis and rete ovarii. Last, we found that WNT4 is a crucial regulator of the SLC lineage and is required for normal development of the rete testis.

UR - https://www.scopus.com/pages/publications/85130804331

U2 - 10.1126/sciadv.abm0972

DO - 10.1126/sciadv.abm0972

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C2 - 35613264

AN - SCOPUS:85130804331

SN - 2375-2548

VL - 8

JO - Science advances

JF - Science advances

IS - 21

M1 - eabm0972

ER -

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

Abstract

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