Neutrophil infiltration leads to fetal growth restriction by impairing the placental vasculature in DENV-infected pregnant mice.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 09 11 2022
revised: 22 06 2023
accepted: 18 07 2023
medline: 18 9 2023
pubmed: 7 8 2023
entrez: 6 8 2023
Statut: ppublish

Résumé

Dengue virus (DENV) infection during pregnancy increases the risk of adverse fetal outcomes, which has become a new clinical challenge. However, the underlying mechanism remains unknown. The effect of DENV-2 infection on fetuses was investigated using pregnant interferon α/β receptor-deficient (Ifnar1 Fetal growth restriction observed in DENV-2 infection was mainly caused by the destruction of the placental vasculature rather than direct damage from the virus in our mouse model. After infection, neutrophil infiltration into the placenta disrupts the expression profile of matrix metalloproteinases, which leads to placental dysvascularization and insufficiency. Notably, similar histopathological changes were observed in the placentas from DENV-infected puerperae. Neutrophils play key roles in placental histopathological damage during DENV infection, which indicates that interfering with aberrant neutrophil infiltration into the placenta may be an important therapeutic target for adverse pregnancy outcomes in DENV infection. The National Key Research and Development Plans of China (2021YFC2300200-02 to J.A., 2019YFC0121905 to Q.Z.C.), the National Natural Science Foundation of China (NSFC) (U1902210 and 81972979 to J. A., 81902048 to Z. Y. S., and 82172266 to P.G.W.), and the Support Project of High-level Teachers in Beijing Municipal Universities in the Period of 13th Five-year Plan, China (IDHT20190510 to J. A.).

Sections du résumé

BACKGROUND BACKGROUND
Dengue virus (DENV) infection during pregnancy increases the risk of adverse fetal outcomes, which has become a new clinical challenge. However, the underlying mechanism remains unknown.
METHODS METHODS
The effect of DENV-2 infection on fetuses was investigated using pregnant interferon α/β receptor-deficient (Ifnar1
FINDINGS RESULTS
Fetal growth restriction observed in DENV-2 infection was mainly caused by the destruction of the placental vasculature rather than direct damage from the virus in our mouse model. After infection, neutrophil infiltration into the placenta disrupts the expression profile of matrix metalloproteinases, which leads to placental dysvascularization and insufficiency. Notably, similar histopathological changes were observed in the placentas from DENV-infected puerperae.
INTERPRETATION CONCLUSIONS
Neutrophils play key roles in placental histopathological damage during DENV infection, which indicates that interfering with aberrant neutrophil infiltration into the placenta may be an important therapeutic target for adverse pregnancy outcomes in DENV infection.
FUNDING BACKGROUND
The National Key Research and Development Plans of China (2021YFC2300200-02 to J.A., 2019YFC0121905 to Q.Z.C.), the National Natural Science Foundation of China (NSFC) (U1902210 and 81972979 to J. A., 81902048 to Z. Y. S., and 82172266 to P.G.W.), and the Support Project of High-level Teachers in Beijing Municipal Universities in the Period of 13th Five-year Plan, China (IDHT20190510 to J. A.).

Identifiants

pubmed: 37544202
pii: S2352-3964(23)00304-3
doi: 10.1016/j.ebiom.2023.104739
pmc: PMC10432184
pii:
doi:

Substances chimiques

Cytokines 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104739

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.

Auteurs

Yingying Zhang (Y)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China; Department of Blood Transfusion, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Ziyang Sheng (Z)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China. Electronic address: shengzy@ccmu.edu.cn.

Qiaozhu Chen (Q)

Department of Ob&Gyn, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, China.

Anni Zhou (A)

Beijing Key Laboratory for Precancerous Lesion of Digestive Disease, Department of Gastroenterology, National Clinical Research Center for Digestive Disease, Beijing Digestive Disease Center, Beijing Friendship Hospital, Capital Medical University, Beijing, China.

Jiaying Cao (J)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Feiyang Xue (F)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Yanzhen Ye (Y)

Department of Obstetrics and Gynecology, People's Hospital of Nanhai District, Foshan City, 528200, Guangdong, China.

Na Wu (N)

Laboratory Animal Center, Capital Medical University, Beijing, 100069, China.

Na Gao (N)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Dongying Fan (D)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Libo Liu (L)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Yuetong Li (Y)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Peigang Wang (P)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.

Li Liang (L)

Guangzhou Eighth People's Hospital, Guangzhou Medical University, Guangzhou, China.

Deshan Zhou (D)

Department of Histology and Embryology, School of Basic Medical Sciences, Capital Medical University, Beijing, China.

Fuchun Zhang (F)

Guangzhou Eighth People's Hospital, Guangzhou Medical University, Guangzhou, China.

Fang Li (F)

Department of Ob&Gyn, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, China; Guangzhou Eighth People's Hospital, Guangzhou Medical University, Guangzhou, China. Electronic address: gz8hlf@126.com.

Jing An (J)

Department of Microbiology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China. Electronic address: anjing@ccmu.edu.cn.

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