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Embryo biosensing by uterine natural killer cells determines endometrial fate decisions at implantation

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Kong, Chow-Seng, Ordoñez, Alexandra Almansa, Turner, Sarah, Tremaine, Tina, Muter, Joanne, Lucas, Emma S., Salisbury, Emma, Vassena, Rita, Tiscornia, Gustavo, Fouladi-Nashta, Ali, Hartshorne, Geraldine M., Brosens, Jan J. and Brighton, Paul (2021) Embryo biosensing by uterine natural killer cells determines endometrial fate decisions at implantation. The FASEB Journal, 35 (4). e21336. doi:10.1096/fj.202002217R ISSN 0892-6638.

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Official URL: https://doi.org/10.1096/fj.202002217R

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Abstract

Decidualizing endometrial stromal cells (EnSC) critically determine the maternal response to an implanting conceptus, triggering either menstruation-like disposal of low-fitness embryos or creating an environment that promotes further development. However, the mechanism that couples maternal recognition of low-quality embryos to tissue breakdown remains poorly understood. Recently, we demonstrated that successful transition of the cycling endometrium to a pregnancy state requires selective elimination of pro-inflammatory senescent decidual cells by activated uterine natural killer (uNK) cells. Here we report that uNK cells express CD44, the canonical hyaluronan (HA) receptor, and demonstrate that high-molecular weight HA (HMWHA) inhibits uNK cell-mediated killing of senescent decidual cells. By contrast, low-molecular weight HA (LMWHA) did not attenuate uNK cell activity in co-culture experiments. Killing of senescent decidual cells by uNK cells was also inhibited upon exposure to medium conditioned by IVF embryos that failed to implant, but not successful embryos. Embryo-mediated inhibition of uNK cell activity was reversed by recombinant hyaluronidase 2 (HYAL2), which hydrolyses HMWHA. We further report a correlation between the levels of HYAL2 secretion by human blastocysts, morphological scores, and implantation potential. Taken together, the data suggest a pivotal role for uNK cells in embryo biosensing and endometrial fate decisions at implantation.

Item Type: Journal Article
Subjects: Q Science > QR Microbiology
R Medicine > RG Gynecology and obstetrics
Divisions: Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences > Cell & Developmental Biology
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): Killer cells, Aging
Journal or Publication Title: The FASEB Journal
Publisher: Federation of American Societies for Experimental Biology
ISSN: 0892-6638
Official Date: April 2021
Dates:
DateEvent
April 2021Published
22 March 2021Available
17 December 2020Accepted
Volume: 35
Number: 4
Article Number: e21336
DOI: 10.1096/fj.202002217R
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Restricted or Subscription Access
Date of first compliant deposit: 22 December 2020
Date of first compliant Open Access: 23 March 2021
Funder: Tommy’s National Miscarriage Research Centre, Wellcome Trust, WPH Charitable Trust , UHCW NHS Trust, Secretary for Universities and Research of the Ministry of Economy and Knowledge of the Government of Catalonia, Torres Quevedo Program of the Spanish Ministry of Science and Innovation, Clinica Eugin intramural funding
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
UNSPECIFIEDTommy'shttp://dx.doi.org/10.13039/501100009324
212233/Z/18/ZWellcome Trusthttp://dx.doi.org/10.13039/100010269
UNSPECIFIEDWPH Charitable Trusthttp://dx.doi.org/10.13039/100012362
UNSPECIFIEDNHS TrustUNSPECIFIED
UNSPECIFIEDUniversity Hospital Coventry and Warwickshire (UHCW) NHS Trusthttps://www.uhcw.nhs.uk/
GENCAT 2018 DI 103Generalitat de Catalunyahttp://dx.doi.org/10.13039/501100002809
Torres Quevedo ProgramMinisterio de Ciencia e Innovaciónhttp://dx.doi.org/10.13039/501100004837
UNSPECIFIEDClinica Eugin intramuralUNSPECIFIED
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