Molecular basis of egg coat cross-linking sheds light on ZP1-associated female infertility.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
12 07 2019
Historique:
received: 09 07 2018
accepted: 11 06 2019
entrez: 14 7 2019
pubmed: 14 7 2019
medline: 28 10 2019
Statut: epublish

Résumé

Mammalian fertilisation begins when sperm interacts with the egg zona pellucida (ZP), whose ZP1 subunit is important for fertility by covalently cross-linking ZP filaments into a three-dimensional matrix. Like ZP4, a structurally-related component absent in the mouse, ZP1 is predicted to contain an N-terminal ZP-N domain of unknown function. Here we report a characterisation of ZP1 proteins carrying mutations from infertile patients, which suggests that, in human, filament cross-linking by ZP1 is crucial to form a stable ZP. We map the function of ZP1 to its ZP-N1 domain and determine crystal structures of ZP-N1 homodimers from a chicken homolog of ZP1. These reveal that ZP filament cross-linking is highly plastic and can be modulated by ZP1 fucosylation and, potentially, zinc sparks. Moreover, we show that ZP4 ZP-N1 forms non-covalent homodimers in chicken but not in human. Together, these data identify human ZP1 cross-links as a promising target for non-hormonal contraception.

Identifiants

pubmed: 31300655
doi: 10.1038/s41467-019-10931-5
pii: 10.1038/s41467-019-10931-5
pmc: PMC6626044
doi:

Substances chimiques

Recombinant Proteins 0
ZP1 protein, human 0
ZP4 protein, human 0
Zona Pellucida Glycoproteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3086

Subventions

Organisme : Vetenskapsrådet (Swedish Research Council)
ID : 2016-03999
Pays : International
Organisme : European Molecular Biology Organization (EMBO)
ID : YIP 2009-1931
Pays : International
Organisme : EC | EC Seventh Framework Programm | FP7 Ideas: European Research Council (FP7-IDEAS-ERC - Specific Programme: "Ideas" Implementing the Seventh Framework Programme of the European Community for Research, Technological Development and Demonstration Activities (2007 to 2013))
ID : 260759
Pays : International

Références

Bioinformatics. 2012 Dec 1;28(23):3150-2
pubmed: 23060610
DNA Seq. 1994;4(6):361-93
pubmed: 7841460
Electrophoresis. 1999 Dec;20(18):3551-67
pubmed: 10612281
Biol Reprod. 2007 Jan;76(1):9-18
pubmed: 17005939
Hum Reprod. 2010 Jul;25(7):1643-56
pubmed: 20504872
Nat Cell Biol. 2002 Jun;4(6):457-61
pubmed: 12021773
Integr Biol (Camb). 2017 Feb 20;9(2):135-144
pubmed: 28102396
J Mol Biol. 2007 Sep 21;372(3):774-97
pubmed: 17681537
Curr Top Dev Biol. 2018;130:275-305
pubmed: 29853180
Development. 2001 Apr;128(7):1119-26
pubmed: 11245577
J Cell Biol. 2012 Jun 25;197(7):897-905
pubmed: 22734000
Acta Crystallogr D Biol Crystallogr. 2009 Jun;65(Pt 6):582-601
pubmed: 19465773
Hum Reprod. 2008 Jun;23(6):1385-93
pubmed: 18332087
Biochim Biophys Acta. 1999 Oct 28;1447(2-3):303-6
pubmed: 10542331
Nature. 2008 Dec 4;456(7222):653-7
pubmed: 19052627
J Cell Biol. 2014 Jun 23;205(6):801-9
pubmed: 24934154
ACS Chem Biol. 2011 Jul 15;6(7):716-23
pubmed: 21526836
Dev Biol. 1988 Aug;128(2):376-85
pubmed: 3396765
Science. 2010 Jul 9;329(5988):216-9
pubmed: 20616279
Curr Top Dev Biol. 2018;130:413-442
pubmed: 29853186
Nat Struct Mol Biol. 2015 Nov;22(11):833-4
pubmed: 26581513
J Mol Biol. 1985 Jan 20;181(2):253-64
pubmed: 3845123
Cell. 2017 Jun 15;169(7):1315-1326.e17
pubmed: 28622512
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
J Assist Reprod Genet. 2019 Apr;36(4):741-747
pubmed: 30778819
J Synchrotron Radiat. 2006 May;13(Pt 3):227-38
pubmed: 16645249
J Struct Biol. 2016 Apr;194(1):1-7
pubmed: 26850170
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
FEBS Open Bio. 2015 May 27;5:454-65
pubmed: 26106520
Histol Histopathol. 1998 Jan;13(1):293-300
pubmed: 9476659
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W327-31
pubmed: 15215404
Fertil Steril. 2017 Jun;107(6):1364-1369
pubmed: 28577617
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W382-8
pubmed: 15980494
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W522-5
pubmed: 17488841
Proc Natl Acad Sci U S A. 2016 Feb 9;113(6):1552-7
pubmed: 26811476
Hum Mutat. 2019 Nov;40(11):2001-2006
pubmed: 31292994
J Biol Chem. 2000 Sep 15;275(37):28866-72
pubmed: 10979984
Biol Reprod. 1996 May;54(5):1032-7
pubmed: 8722623
Biol Reprod. 2014 Nov;91(5):107
pubmed: 25253730
Trends Biochem Sci. 1997 Dec;22(12):488-90
pubmed: 9433130
N Engl J Med. 2014 Mar 27;370(13):1220-6
pubmed: 24670168
Development. 1999 Sep;126(17):3847-55
pubmed: 10433913
Nucleic Acids Res. 2018 Jan 4;46(D1):D493-D496
pubmed: 29040681
Protein Sci. 1993 Apr;2(4):669-70
pubmed: 8518738
Mol Cell Biol. 2006 Nov;26(21):7991-8
pubmed: 17047254
Biochem Biophys Res Commun. 2007 Dec 21;364(3):682-8
pubmed: 17964539
Curr Top Dev Biol. 2018;130:379-411
pubmed: 29853184
Biochem J. 2004 Nov 15;384(Pt 1):191-9
pubmed: 15264999
J Biol Chem. 2003 Sep 5;278(36):34189-202
pubmed: 12799386
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Sci Rep. 2016 Apr 26;6:24737
pubmed: 27113677
Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41
pubmed: 11517324
Proc Natl Acad Sci U S A. 1996 May 28;93(11):5431-6
pubmed: 8643592
Dev Biol. 1980 Apr;76(1):185-202
pubmed: 7380091
Science. 2011 Sep 23;333(6050):1761-4
pubmed: 21852454
Acta Crystallogr D Biol Crystallogr. 2012 Apr;68(Pt 4):352-67
pubmed: 22505256
Cell. 1980 Jul;20(3):873-82
pubmed: 7418009
Biol Reprod. 2001 Mar;64(3):822-30
pubmed: 11207197
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
Reproduction. 2012 Dec;144(6):649-60
pubmed: 23028122
Reproduction. 2011 Mar;141(3):313-9
pubmed: 21173071
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32
pubmed: 20124692
Hum Reprod. 1995 Sep;10(9):2467-71
pubmed: 8530692
Hum Reprod. 2005 May;20(5):1148-52
pubmed: 15760956
Development. 1996 Sep;122(9):2903-10
pubmed: 8787763
Cell. 2010 Oct 29;143(3):404-15
pubmed: 20970175
Nucleic Acids Res. 2011 Jan;39(Database issue):D38-51
pubmed: 21097890
FEBS Lett. 1992 Apr 6;300(3):237-40
pubmed: 1313375
Development. 1995 Jul;121(7):1947-56
pubmed: 7635043
J Chem Theory Comput. 2011 Oct 11;7(10):3162-3180
pubmed: 22125473
Curr Top Dev Biol. 2018;130:307-329
pubmed: 29853181
Biol Reprod. 1981 Dec;25(5):997-1008
pubmed: 7326313
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W473-6
pubmed: 17584791
Trends Dev Biol. 2014;8:65-76
pubmed: 26504367
J Cell Biol. 1993 Dec;123(6 Pt 1):1431-40
pubmed: 8253842
J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674
pubmed: 19461840
Bioinformatics. 2007 Aug 1;23(15):1871-4
pubmed: 17510169
Biol Reprod. 2002 Feb;66(2):407-14
pubmed: 11804956
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W5-9
pubmed: 18440982
Nat Methods. 2017 Jan;14(1):71-73
pubmed: 27819658
Hum Reprod. 2004 Jul;19(7):1580-6
pubmed: 15142998
J Biol Chem. 2000 Mar 17;275(11):7731-42
pubmed: 10713085

Auteurs

Kaoru Nishimura (K)

Department of Biosciences and Nutrition and Center for Innovative Medicine, Karolinska Institutet, Huddinge, SE-141 83, Sweden.

Elisa Dioguardi (E)

Department of Biosciences and Nutrition and Center for Innovative Medicine, Karolinska Institutet, Huddinge, SE-141 83, Sweden.

Shunsuke Nishio (S)

Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan.
Department of Biosciences and Nutrition and Center for Innovative Medicine, Karolinska Institutet, Huddinge, SE-141 83, Sweden.

Alessandra Villa (A)

Department of Biosciences and Nutrition and Center for Innovative Medicine, Karolinska Institutet, Huddinge, SE-141 83, Sweden.

Ling Han (L)

Department of Biosciences and Nutrition and Center for Innovative Medicine, Karolinska Institutet, Huddinge, SE-141 83, Sweden.

Tsukasa Matsuda (T)

Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan.

Luca Jovine (L)

Department of Biosciences and Nutrition and Center for Innovative Medicine, Karolinska Institutet, Huddinge, SE-141 83, Sweden. luca.jovine@ki.se.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

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

Classifications MeSH