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Molecular Mechanism of Mouse Uterine Smooth Muscle Regulation on Embryo Implantation

Cao, Rui ; Yang, Zhen Shan LU orcid ; Hu, Sui Li ; Liang, Shi Jin ; Zhang, Shu Miao ; Zhu, Song Qi ; Lu, Lin ; Long, Cheng Hong ; Yao, Si Tong and Ma, Yong Jiang , et al. (2022) In International Journal of Molecular Sciences 23(20).
Abstract

Myometrium plays critical roles in multiple processes such as embryo spacing through peristalsis during mouse implantation, indicating vital roles of smooth muscle in the successful establishment and quality of implantation. Actin, a key element of cytoskeleton structure, plays an important role in the movement and contraction of smooth muscle cells (SMCs). However, the function of peri-implantation uterine smooth muscle and the regulation mechanism of muscle tension are still unclear. This study focused on the molecular mechanism of actin assembly regulation on implantation in smooth muscle. Phalloidin is a highly selective bicyclic peptide used for staining actin filaments (also known as F-actin). Phalloidin staining showed that... (More)

Myometrium plays critical roles in multiple processes such as embryo spacing through peristalsis during mouse implantation, indicating vital roles of smooth muscle in the successful establishment and quality of implantation. Actin, a key element of cytoskeleton structure, plays an important role in the movement and contraction of smooth muscle cells (SMCs). However, the function of peri-implantation uterine smooth muscle and the regulation mechanism of muscle tension are still unclear. This study focused on the molecular mechanism of actin assembly regulation on implantation in smooth muscle. Phalloidin is a highly selective bicyclic peptide used for staining actin filaments (also known as F-actin). Phalloidin staining showed that F-actin gradually weakened in the CD-1 mouse myometrium from day 1 to day 4 of early pregnancy. More than 3 mice were studied for each group. Jasplakinolide (Jasp) used to inhibit F-actin depolymerization promotes F-actin polymerization in SMCs during implantation window and consequently compromises embryo implantation quality. Transcriptome analysis following Jasp treatment in mouse uterine SMCs reveals significant molecular changes associated with actin assembly. Tagln is involved in the regulation of the cell cytoskeleton and promotes the polymerization of G-actin to F-actin. Our results show that Tagln expression is gradually reduced in mouse uterine myometrium from day 1 to 4 of pregnancy. Furthermore, progesterone inhibits the expression of Tagln through the progesterone receptor. Using siRNA to knock down Tagln in day 3 SMCs, we found that phalloidin staining is decreased, which confirms the critical role of Tagln in F-actin polymerization. In conclusion, our data suggested that decreases in actin assembly in uterine smooth muscle during early pregnancy is critical to optimal embryo implantation. Tagln, a key molecule involved in actin assembly, regulates embryo implantation by controlling F-actin aggregation before implantation, suggesting moderate uterine contractility is conducive to embryo implantation. This study provides new insights into how the mouse uterus increases its flexibility to accommodate implanting embryos in the early stage of pregnancy.

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publishing date
type
Contribution to journal
publication status
published
keywords
actin, implantation, SMCs, Tagln, uterus
in
International Journal of Molecular Sciences
volume
23
issue
20
article number
12494
publisher
MDPI AG
external identifiers
  • scopus:85140715867
  • pmid:36293350
ISSN
1661-6596
DOI
10.3390/ijms232012494
language
English
LU publication?
no
additional info
Funding Information: This study was supported by Natural Science Foundation of Guangdong Province (2019A1515010954 and 2021A1515012089). Publisher Copyright: © 2022 by the authors.
id
09a1556e-1bbf-469d-b9ec-2f99515ae1d1
date added to LUP
2024-02-28 14:57:11
date last changed
2024-06-08 17:40:24
@article{09a1556e-1bbf-469d-b9ec-2f99515ae1d1,
  abstract     = {{<p>Myometrium plays critical roles in multiple processes such as embryo spacing through peristalsis during mouse implantation, indicating vital roles of smooth muscle in the successful establishment and quality of implantation. Actin, a key element of cytoskeleton structure, plays an important role in the movement and contraction of smooth muscle cells (SMCs). However, the function of peri-implantation uterine smooth muscle and the regulation mechanism of muscle tension are still unclear. This study focused on the molecular mechanism of actin assembly regulation on implantation in smooth muscle. Phalloidin is a highly selective bicyclic peptide used for staining actin filaments (also known as F-actin). Phalloidin staining showed that F-actin gradually weakened in the CD-1 mouse myometrium from day 1 to day 4 of early pregnancy. More than 3 mice were studied for each group. Jasplakinolide (Jasp) used to inhibit F-actin depolymerization promotes F-actin polymerization in SMCs during implantation window and consequently compromises embryo implantation quality. Transcriptome analysis following Jasp treatment in mouse uterine SMCs reveals significant molecular changes associated with actin assembly. Tagln is involved in the regulation of the cell cytoskeleton and promotes the polymerization of G-actin to F-actin. Our results show that Tagln expression is gradually reduced in mouse uterine myometrium from day 1 to 4 of pregnancy. Furthermore, progesterone inhibits the expression of Tagln through the progesterone receptor. Using siRNA to knock down Tagln in day 3 SMCs, we found that phalloidin staining is decreased, which confirms the critical role of Tagln in F-actin polymerization. In conclusion, our data suggested that decreases in actin assembly in uterine smooth muscle during early pregnancy is critical to optimal embryo implantation. Tagln, a key molecule involved in actin assembly, regulates embryo implantation by controlling F-actin aggregation before implantation, suggesting moderate uterine contractility is conducive to embryo implantation. This study provides new insights into how the mouse uterus increases its flexibility to accommodate implanting embryos in the early stage of pregnancy.</p>}},
  author       = {{Cao, Rui and Yang, Zhen Shan and Hu, Sui Li and Liang, Shi Jin and Zhang, Shu Miao and Zhu, Song Qi and Lu, Lin and Long, Cheng Hong and Yao, Si Tong and Ma, Yong Jiang and Liang, Xiao Huan}},
  issn         = {{1661-6596}},
  keywords     = {{actin; implantation; SMCs; Tagln; uterus}},
  language     = {{eng}},
  number       = {{20}},
  publisher    = {{MDPI AG}},
  series       = {{International Journal of Molecular Sciences}},
  title        = {{Molecular Mechanism of Mouse Uterine Smooth Muscle Regulation on Embryo Implantation}},
  url          = {{http://dx.doi.org/10.3390/ijms232012494}},
  doi          = {{10.3390/ijms232012494}},
  volume       = {{23}},
  year         = {{2022}},
}