Protein expression reveals a molecular sexual identity of avian primordial germ cells at pre-gonadal stages.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
28 09 2021
Historique:
received: 26 02 2021
accepted: 06 09 2021
entrez: 29 9 2021
pubmed: 30 9 2021
medline: 29 12 2021
Statut: epublish

Résumé

In poultry, in vitro propagated primordial germ cells (PGCs) represent an important tool for the cryopreservation of avian genetic resources. However, several studies have highlighted sexual differences exhibited by PGCs during in vitro propagation, which may compromise their reproductive capacities. To understand this phenomenon, we compared the proteome of pregonadal migratory male (ZZ) and female (ZW) chicken PGCs propagated in vitro by quantitative proteomic analysis using a GeLC-MS/MS strategy. Many proteins were found to be differentially abundant in chicken male and female PGCs indicating their early sexual identity. Many of the proteins more highly expressed in male PGCs were encoded by genes localised to the Z sex chromosome. This suggests that the known lack of dosage compensation of the transcription of Z-linked genes between sexes persists at the protein level in PGCs, and that this may be a key factor of their autonomous sex differentiation. We also found that globally, protein differences do not closely correlate with transcript differences indicating a selective translational mechanism in PGCs. Male and female PGC expressed protein sets were associated with differential biological processes and contained proteins known to be biologically relevant for male and female germ cell development, respectively. We also discovered that female PGCs have a higher capacity to uptake proteins from the cell culture medium than male PGCs. This study presents the first evidence of an early predetermined sex specific cell fate of chicken PGCs and their sexual molecular specificities which will enable the development of more precise sex-specific in vitro culture conditions for the preservation of avian genetic resources.

Identifiants

pubmed: 34584135
doi: 10.1038/s41598-021-98454-2
pii: 10.1038/s41598-021-98454-2
pmc: PMC8478952
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

19236

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/D/20320000
Pays : United Kingdom

Informations de copyright

© 2021. The Author(s).

Références

J Biol Chem. 2009 May 29;284(22):15246-54
pubmed: 19349277
PLoS One. 2010 Nov 29;5(11):e15518
pubmed: 21124737
Stem Cell Reports. 2014 Nov 11;3(5):892-904
pubmed: 25418731
J Cell Biol. 2003 Nov 24;163(4):801-12
pubmed: 14623865
FEBS Lett. 2018 Jun;592(12):2108-2125
pubmed: 29723415
Gynecol Oncol. 2013 Oct;131(1):182-90
pubmed: 23911878
Mol Cell Proteomics. 2007 May;6(5):798-811
pubmed: 17289661
Biol Reprod. 2014 Jan 23;90(1):15
pubmed: 24337317
J Biol Chem. 2015 Jun 19;290(25):15662-15669
pubmed: 25911097
Dev Growth Differ. 2013 Jan;55(1):20-40
pubmed: 23294359
Dev Biol. 2009 Jan 1;325(1):33-42
pubmed: 18926813
J Biol Chem. 2013 Jun 21;288(25):18271-82
pubmed: 23653357
Science. 1992 Jan 24;255(5043):467-70
pubmed: 1734525
Cell Rep. 2019 Jul 30;28(5):1268-1281.e6
pubmed: 31365869
PLoS Genet. 2011 Apr;7(4):e1002030
pubmed: 21490958
Neurosci Lett. 2017 Mar 16;643:32-37
pubmed: 28188849
Dev Biol. 2009 Aug 1;332(1):142-55
pubmed: 19464282
Int J Mol Sci. 2020 Jan 25;21(3):
pubmed: 31991812
Stem Cells Dev. 2012 Sep 1;21(13):2343-9
pubmed: 22296229
Endocrinology. 2017 Nov 1;158(11):4000-4016
pubmed: 28938460
Cell Mol Life Sci. 2018 Nov;75(21):3877-3894
pubmed: 29872871
Evolution. 2001 Jan;55(1):190-7
pubmed: 11263738
Mol Biol Evol. 2015 Oct;32(10):2716-25
pubmed: 26108680
Genome Biol. 2013 Mar 25;14(3):R26
pubmed: 23531366
Elife. 2013 Nov 05;2:e00924
pubmed: 24192035
Mol Biol Cell. 2013 Jun;24(12):1863-71
pubmed: 23615451
Biol Open. 2014 May 08;3(6):475-85
pubmed: 24812355
PLoS One. 2012;7(3):e33558
pubmed: 22448252
Nat Cell Biol. 2005 May;7(5):510-6
pubmed: 15852002
Nucleic Acids Res. 2016 Jan 4;44(D1):D7-19
pubmed: 26615191
Front Cell Dev Biol. 2019 Mar 28;7:35
pubmed: 30984757
Biochem Biophys Res Commun. 2018 Jun 22;501(2):440-447
pubmed: 29738775
PLoS Genet. 2014 Jun 26;10(6):e1004444
pubmed: 24967676
Wiley Interdiscip Rev Syst Biol Med. 2009 Sep-Oct;1(2):228-236
pubmed: 20016762
Protein Cell. 2011 Sep;2(9):755-63
pubmed: 21976065
Mamm Genome. 2017 Aug;28(7-8):315-323
pubmed: 28612238
Int J Mol Sci. 2019 Oct 10;20(20):
pubmed: 31658625
Proc Natl Acad Sci U S A. 2013 Aug 6;110(32):E3017-26
pubmed: 23884650
Biol Reprod. 2007 Oct;77(4):697-706
pubmed: 17615405
Sci Rep. 2016 Feb 02;6:20193
pubmed: 26830971
Stem Cell Reports. 2015 Dec 8;5(6):1171-1182
pubmed: 26677769
Nature. 2006 Jun 8;441(7094):766-9
pubmed: 16760981
Hum Mol Genet. 2016 Apr 1;25(7):1392-405
pubmed: 26908624
J Reprod Dev. 2013;59(3):252-7
pubmed: 23386102
Nat Cell Biol. 2012 Feb 29;14(3):224-30
pubmed: 22373868
Nucleic Acids Res. 2020 Jan 8;48(D1):D682-D688
pubmed: 31691826
Development. 2015 May 1;142(9):1616-27
pubmed: 25922525
Mol Reprod Dev. 2007 Jan;74(1):68-75
pubmed: 16941668
Int J Mol Sci. 2013 May 29;14(6):11424-37
pubmed: 23759991
Mol Cell Proteomics. 2014 Jul;13(7):1644-58
pubmed: 24797263
Front Cell Neurosci. 2016 Jan 11;9:506
pubmed: 26793058
Proc Natl Acad Sci U S A. 2005 Oct 18;102(42):15093-8
pubmed: 16214886
Development. 2017 Nov 15;144(22):4148-4158
pubmed: 28993400
Cell Rep. 2016 Mar 22;14(11):2587-98
pubmed: 26972001
FEBS Lett. 2011 Mar 9;585(5):791-6
pubmed: 21310149
Semin Cell Dev Biol. 2014 Aug;32:22-9
pubmed: 24769255
Nat Rev Mol Cell Biol. 2005 Feb;6(2):112-26
pubmed: 15687999
Theriogenology. 2015 Sep 15;84(5):732-42.e1-2
pubmed: 26037665
Curr Osteoporos Rep. 2019 Jun;17(3):138-146
pubmed: 30982184
Biol Reprod. 2017 Mar 1;96(3):686-693
pubmed: 28339605
Asian J Androl. 2015 May-Jun;17(3):360-6
pubmed: 25578929
Genetics. 1993 Oct;135(2):489-505
pubmed: 8244010
BioData Min. 2019 Aug 6;12:16
pubmed: 31406507
Neuroscientist. 2018 Feb;24(1):54-72
pubmed: 28459188
J Cell Sci. 2020 Jan 23;133(2):
pubmed: 31974276
Dev Dyn. 2004 Dec;231(4):859-70
pubmed: 15517586
Poult Sci. 2007 Mar;86(3):555-64
pubmed: 17297169
Mol Cell. 2009 Dec 11;36(5):794-804
pubmed: 20005843
Biochemistry. 2009 Mar 24;48(11):2538-49
pubmed: 19182904
J Cell Sci. 2013 Jan 1;126(Pt 1):117-27
pubmed: 23077176
Poult Sci. 2016 Aug 1;95(8):1905-11
pubmed: 27099306
Front Endocrinol (Lausanne). 2021 Jan 29;11:620013
pubmed: 33584548
Nature. 2009 Aug 13;460(7257):909-13
pubmed: 19578360
Cell Death Dis. 2015 Jul 16;6:e1818
pubmed: 26181199
Nature. 2010 Mar 11;464(7286):237-242
pubmed: 20220842
Biochim Biophys Acta Gene Regul Mech. 2017 Mar;1860(3):299-315
pubmed: 28095296
BMC Biol. 2007 Sep 20;5:40
pubmed: 17883843
J Cell Biol. 2017 Aug 9;216(10):3017-3028
pubmed: 28794128
PLoS One. 2016 Sep 14;11(9):e0162897
pubmed: 27627652
Asian J Androl. 2019 Jul-Aug;21(4):345-350
pubmed: 30198493
Sci Rep. 2016 Jun 13;6:27974
pubmed: 27294500
Mol Reprod Dev. 2003 Aug;65(4):420-8
pubmed: 12840815
Annu Rev Anim Biosci. 2020 Feb 15;8:47-69
pubmed: 31525067
Br Poult Sci. 2001 Mar;42(1):134-8
pubmed: 11337963
Curr Top Microbiol Immunol. 2004;286:45-79
pubmed: 15645710
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
Sci Rep. 2017 Apr 12;7:46135
pubmed: 28401892
Proc Natl Acad Sci U S A. 2019 Oct 15;116(42):20930-20937
pubmed: 31575742

Auteurs

Laura Soler (L)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.
Toxalim (Research Centre in Food Toxicology), INRAE, Université de Toulouse, ENVT, INP-Purpan, UPS, 31027, Toulouse, France.

Sabine Alves (S)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Aurélien Brionne (A)

INRAE, Université de Tours, BOA, 37380, Nouzilly, France.

Aurore Jacques (A)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Vanessa Guérin (V)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Maeva Cherif-Feildel (M)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Lucie Combes-Soia (L)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.
INRAE, CHU de Tours, Université de Tours, PRC, PIXANIM, 37380, Nouzilly, France.

Sophie Fouchécourt (S)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Aurore Thélie (A)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Elisabeth Blesbois (E)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.

Michael J McGrew (MJ)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK.

Valérie Labas (V)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France.
INRAE, CHU de Tours, Université de Tours, PRC, PIXANIM, 37380, Nouzilly, France.

Marina S Govoroun (MS)

INRAE, CNRS, Université de Tours, IFCE, PRC, 37380, Nouzilly, France. marina.govoroun@inrae.fr.

Articles similaires

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
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH