Placenta-specific 1 regulates oocyte meiosis and fertilization through furin
Placenta-specific 1 (Plac1) has been found to be essential for placentation, and abnormal Plac1 expression and distribution is highly correlated with preeclampsia and implantation failure; however, its function in mammalian oocytes has not been elucidated. Here, we report that Plac1 was more promine...
Saved in:
Published in | The FASEB journal Vol. 32; no. 10; p. 5483 |
---|---|
Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
01.10.2018
|
Subjects | |
Online Access | Get more information |
Cover
Loading…
Abstract | Placenta-specific 1 (Plac1) has been found to be essential for placentation, and abnormal Plac1 expression and distribution is highly correlated with preeclampsia and implantation failure; however, its function in mammalian oocytes has not been elucidated. Here, we report that Plac1 was more prominent in mouse oocytes and enriched at the membrane region throughout meiosis. On the one hand, Plac1 knockdown severely disrupted microvillus organization; however, on the other hand, Plac1 significantly decreased oocyte maturation and increased aneuploidy, consequently disrupting normal fertilization. On the basis of immunoprecipitate matrix-assisted laser desorption/ionization, we established a working model, then verified and suggested that, at the germinal vesicle stage, Plac1 enriches the membrane to activate furin, and active furin subsequently activates IGF-1 receptor to maintain regular microvillus organization. Upon meiosis onset, active furin/IGF-1 receptor relocates into the cytoplasm to activate (phosphorylate) Akt to promote meiosis. In summary, our finding suggests that Plac1, a protein that is crucial for placentation, is also essential for oocyte meiosis and fertilization.-Shi, L.-Y., Ma, Y., Zhu, G.-Y., Liu, J.-W., Zhou, C.-X., Chen, L.-J., Wang, Y., Li, R.-C., Yang, Z.-X., Zhang, D. Placenta-specific 1 regulates oocyte meiosis and fertilization through furin. |
---|---|
AbstractList | Placenta-specific 1 (Plac1) has been found to be essential for placentation, and abnormal Plac1 expression and distribution is highly correlated with preeclampsia and implantation failure; however, its function in mammalian oocytes has not been elucidated. Here, we report that Plac1 was more prominent in mouse oocytes and enriched at the membrane region throughout meiosis. On the one hand, Plac1 knockdown severely disrupted microvillus organization; however, on the other hand, Plac1 significantly decreased oocyte maturation and increased aneuploidy, consequently disrupting normal fertilization. On the basis of immunoprecipitate matrix-assisted laser desorption/ionization, we established a working model, then verified and suggested that, at the germinal vesicle stage, Plac1 enriches the membrane to activate furin, and active furin subsequently activates IGF-1 receptor to maintain regular microvillus organization. Upon meiosis onset, active furin/IGF-1 receptor relocates into the cytoplasm to activate (phosphorylate) Akt to promote meiosis. In summary, our finding suggests that Plac1, a protein that is crucial for placentation, is also essential for oocyte meiosis and fertilization.-Shi, L.-Y., Ma, Y., Zhu, G.-Y., Liu, J.-W., Zhou, C.-X., Chen, L.-J., Wang, Y., Li, R.-C., Yang, Z.-X., Zhang, D. Placenta-specific 1 regulates oocyte meiosis and fertilization through furin. |
Author | Ma, Yang Liu, Jin-Wei Wang, Yang Zhang, Dong Li, Rui-Chao Shi, Li-Ya Zhou, Chun-Xiang Yang, Zhi-Xia Chen, Liang-Jian Zhu, Gang-Yi |
Author_xml | – sequence: 1 givenname: Li-Ya surname: Shi fullname: Shi, Li-Ya organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China – sequence: 2 givenname: Yang surname: Ma fullname: Ma, Yang organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China – sequence: 3 givenname: Gang-Yi surname: Zhu fullname: Zhu, Gang-Yi organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China – sequence: 4 givenname: Jin-Wei surname: Liu fullname: Liu, Jin-Wei organization: Department of Gynecology, Zhejiang Provincial People's Hospital, Hangzhou, China – sequence: 5 givenname: Chun-Xiang surname: Zhou fullname: Zhou, Chun-Xiang organization: Prenatal Diagnosis Center of Jiangsu Province, Affiliated Drum Tower Hospital, Nanjing University Medical School, Nanjing, China – sequence: 6 givenname: Liang-Jian surname: Chen fullname: Chen, Liang-Jian organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China – sequence: 7 givenname: Yang surname: Wang fullname: Wang, Yang organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China – sequence: 8 givenname: Rui-Chao surname: Li fullname: Li, Rui-Chao organization: Liuzhou Worker's Hospital, Liuzhou, China – sequence: 9 givenname: Zhi-Xia surname: Yang fullname: Yang, Zhi-Xia organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China – sequence: 10 givenname: Dong surname: Zhang fullname: Zhang, Dong organization: State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29723063$$D View this record in MEDLINE/PubMed |
BookMark | eNo1j09LwzAcQIMo7o9ePUq-QOcviU2bowydQkEpeh5J-suW0TYjSQ_z0ztQT-_2eG9BLscwIiF3DFYMlHxwhxUHVgEoztv2gsxZKaCQtYQZWaR0AAAGTF6TGVcVFyDFnDQfvbY4Zl2kI1rvvKWMRtxNvc6YaAj2lJEO6EPyieqxow5j9r3_1tmHkeZ9DNNuT90U_XhDrpzuE97-cUm-Xp4_169F8755Wz81hRW1agupS-ZKqawwympw4FDUzqKqHkUFxnJRd1UnlTISGcdzcyXw_FUyWRs0JV-S-1_vcTIDdttj9IOOp-3_Fv8BpxVPnQ |
CitedBy_id | crossref_primary_10_1038_s41538_024_00261_2 crossref_primary_10_1111_cpr_12769 crossref_primary_10_3390_ijms23095175 crossref_primary_10_1002_iub_2514 crossref_primary_10_1111_cpr_12825 crossref_primary_10_1096_fj_202002128RR crossref_primary_10_1016_j_cbd_2021_100925 crossref_primary_10_1007_s43032_024_01467_1 crossref_primary_10_1002_jcb_29839 crossref_primary_10_1038_s41418_021_00861_5 crossref_primary_10_1080_01443615_2019_1674263 crossref_primary_10_1016_j_yexcr_2022_113135 crossref_primary_10_1016_j_theriogenology_2021_11_006 crossref_primary_10_1016_j_reprotox_2020_08_008 crossref_primary_10_3389_fvets_2023_1250551 |
ContentType | Journal Article |
DBID | CGR CUY CVF ECM EIF NPM |
DOI | 10.1096/fj.201700922RR |
DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed |
DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) |
DatabaseTitleList | MEDLINE |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
DeliveryMethod | no_fulltext_linktorsrc |
Discipline | Biology |
EISSN | 1530-6860 |
ExternalDocumentID | 29723063 |
Genre | Research Support, Non-U.S. Gov't Journal Article |
GroupedDBID | --- -DZ -~X .55 0R~ 0VX 123 18M 1OB 1OC 29H 2WC 33P 34G 39C 3O- 4.4 53G 5GY 5RE 85S AAHHS AANLZ ABCUV ABDNZ ABEFU ABJNI ABOCM ACCFJ ACCZN ACGFS ACIWK ACNCT ACPOU ACPRK ACXQS ACYGS ADKYN ADZMN AEEZP AEIGN AENEX AEQDE AEUYR AFFNX AFFPM AFRAH AGCDD AHBTC AI. AITYG AIURR AIWBW AIZAD AJBDE ALMA_UNASSIGNED_HOLDINGS ALUQN AMYDB BFHJK BIYOS C1A CGR CS3 CUY CVF DCZOG DU5 D~5 E3Z EBS ECM EIF EJD F20 F5P F9R FRP H13 HGLYW HZ~ H~9 J5H L7B LATKE LEEKS MEWTI MVM NEJ NPM O9- OHT OVD Q-A RHF RHI RJQFR ROL SAMSI SJN SUPJJ TEORI TFA TR2 TWZ VH1 W8F WH7 WHG WOQ WXSBR X7M XJT XOL XSW Y6R YBU YCJ YHG YKV YNH YSK Z0Y ZCA ZE2 ZGI ZXP ~KM |
ID | FETCH-LOGICAL-c389R-6a51f569c3b9ca0f0fe38fce974370bc238d7d699b6e12e10173e1705168beb52 |
IngestDate | Sat Sep 28 08:37:30 EDT 2024 |
IsDoiOpenAccess | false |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 10 |
Keywords | Plac1 microvillus Akt IGF1R |
Language | English |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c389R-6a51f569c3b9ca0f0fe38fce974370bc238d7d699b6e12e10173e1705168beb52 |
OpenAccessLink | https://doi.org/10.1096/fj.201700922rr |
PMID | 29723063 |
ParticipantIDs | pubmed_primary_29723063 |
PublicationCentury | 2000 |
PublicationDate | 2018-10-00 |
PublicationDateYYYYMMDD | 2018-10-01 |
PublicationDate_xml | – month: 10 year: 2018 text: 2018-10-00 |
PublicationDecade | 2010 |
PublicationPlace | United States |
PublicationPlace_xml | – name: United States |
PublicationTitle | The FASEB journal |
PublicationTitleAlternate | FASEB J |
PublicationYear | 2018 |
SSID | ssj0001016 |
Score | 2.4227254 |
Snippet | Placenta-specific 1 (Plac1) has been found to be essential for placentation, and abnormal Plac1 expression and distribution is highly correlated with... |
SourceID | pubmed |
SourceType | Index Database |
StartPage | 5483 |
SubjectTerms | Animals Enzyme Activation - physiology Female Fertilization - physiology Furin - genetics Furin - metabolism Meiosis - physiology Mice Mice, Inbred ICR Oocytes - cytology Oocytes - metabolism Pregnancy Proteins - genetics Pregnancy Proteins - metabolism Protein Transport - physiology Proto-Oncogene Proteins c-akt - genetics Proto-Oncogene Proteins c-akt - metabolism Receptor, IGF Type 1 - genetics Receptor, IGF Type 1 - metabolism |
Title | Placenta-specific 1 regulates oocyte meiosis and fertilization through furin |
URI | https://www.ncbi.nlm.nih.gov/pubmed/29723063 |
Volume | 32 |
hasFullText | |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3fT9swELZgCImXifFzgyE_7K0yJHHiJI8dAiFE0VRAo08odi5SEE2rqX3o_vrd2UnaMqYBL1F1bqLI9-V8d7r7jrFvEIEJcvwAozzORBiHWiRGSpHLyADxb_kedSP3rtXFXXh5H93P63Rtd8lEH5vfL_aVvEerKEO9UpfsGzTbPhQF-Bv1i1fUMF5fpeMflAOvJpmgfkmq-en4nV9uuDxxyY7MbAKdIZQjYh2hDHlBVdRPdetlO6OnoIz7opdK2Dnv3px97yy-hiVydM3UpRi05rxn3c9BVh-BNgk9tel2FIlB2UivSiu9LCvxE8rFbIOftHVreFg0FhLjzcQNAWhM6DxFOW3LVJ1BxIBIvmipMXSi7X2k6rqYmJ-Cfn_xj7jT46HVW0CD0Twl_7_6jDm7WVplq3FC1u-aMjn1KU1Zi5bEU50svwhRRNc3Pws3rNtxu8k-1vEC7zrlf2IrUG2xdTdBdLbNrv6CAPd5CwHuIMBrCHCEAF-CAK8hwC0Edtjd-dnt6YWoB2QIg35mX6gs8otIpUbq1GRe4RUgk8IAxogy9rRBdyyPc5WmWoEfAFlfCcSf5KtEg46CXfahGlWwz7iUWRB4EGmZqBAwCjdhrCDO_VQbLy3kZ7bntuFh7FhQHpoN-vLPlQO2MYfQIVsr8LODr-jDTfSRVcYfnd1Edg |
link.rule.ids | 786 |
linkProvider | National Library of Medicine |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Placenta-specific+1+regulates+oocyte+meiosis+and+fertilization+through+furin&rft.jtitle=The+FASEB+journal&rft.au=Shi%2C+Li-Ya&rft.au=Ma%2C+Yang&rft.au=Zhu%2C+Gang-Yi&rft.au=Liu%2C+Jin-Wei&rft.date=2018-10-01&rft.eissn=1530-6860&rft.volume=32&rft.issue=10&rft.spage=5483&rft_id=info:doi/10.1096%2Ffj.201700922RR&rft_id=info%3Apmid%2F29723063&rft_id=info%3Apmid%2F29723063&rft.externalDocID=29723063 |