Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV

Highly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) is a mutant strain of the classic porcine reproductive and respiratory syndrome virus (PRRSV) characterized by high morbidity and mortality rates. Epidemiological analysis revealed a natural mutation and stable inherita...

Full description

Saved in:
Bibliographic Details
Main Authors: Xianchang Zhu, Yang Xia, Qian Lei, Yu Gan, Shenghai Jiang, Lian Huang, Qihu Wen, Wei Fu, Bo Zhang, Yi Zhang, Shanshan Xie, Jida Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1587634/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850082780403204096
author Xianchang Zhu
Yang Xia
Qian Lei
Yu Gan
Shenghai Jiang
Lian Huang
Qihu Wen
Wei Fu
Bo Zhang
Yi Zhang
Shanshan Xie
Jida Li
Jida Li
author_facet Xianchang Zhu
Yang Xia
Qian Lei
Yu Gan
Shenghai Jiang
Lian Huang
Qihu Wen
Wei Fu
Bo Zhang
Yi Zhang
Shanshan Xie
Jida Li
Jida Li
author_sort Xianchang Zhu
collection DOAJ
description Highly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) is a mutant strain of the classic porcine reproductive and respiratory syndrome virus (PRRSV) characterized by high morbidity and mortality rates. Epidemiological analysis revealed a natural mutation and stable inheritance of amino acid 46 (41-PGKKNKK-47 mutated to 41-PGKKNRK-47) in the nuclear localization signal or sequence (NLS) region of the N protein of HP-PRRSV. In this study, we showed that the nucleoplasmic shuttling of the HP-PRRSV N protein was associated with a higher efficiency of viral replication than that of the classical PRRSV. The nuclear transporter receptors KPNB1, KPNA1, KPNA2, KPNA6, and KPNA7 were involved in the nuclear import of the N protein. Additionally, the mRNA expression levels of KPNB1 and KPNA1 differed between the two strains after infecting the Marc-145 cells with these strains. The viral replication efficiency also decreased when expression levels of KPNA1 and/or KPNB1 were lowered. Finally, protein binding simulation and kinetic assay showed that the mutation of key amino acid 46 in the NLS region altered the binding mode and kinetics of the N proteins to KPNA1 and KPNB1. This study elucidates, for the first time, the reasons for the enhanced nucleoplasmic shuttling and replication efficiency of HP-PRRSV from the perspective of protein entry into the nucleus. It also provides a foundational reference for the prevention and control of PRRSV.
format Article
id doaj-art-c3311fc5c7874447b7f0b4cd8c5652cd
institution DOAJ
issn 1664-302X
language English
publishDate 2025-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj-art-c3311fc5c7874447b7f0b4cd8c5652cd2025-08-20T02:44:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-07-011610.3389/fmicb.2025.15876341587634Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSVXianchang Zhu0Yang Xia1Qian Lei2Yu Gan3Shenghai Jiang4Lian Huang5Qihu Wen6Wei Fu7Bo Zhang8Yi Zhang9Shanshan Xie10Jida Li11Jida Li12Institute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaSouthwest Guizhou Vocational and Technical College for Nationalities, Xingyi, Guizhou, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaDepartment of Preventive Health Care, Yunan District People's Hospital, Yunfu, Guangdong, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaCollege of Basic Medicine, Zunyi Medical University, Zunyi, Guizhou, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaCollege of Veterinary Medicine, Henan Agricultural University, Zhengzhou, Henan, ChinaInstitute of Zoonosis, College of Public Health, Zunyi Medical University, Zunyi, Guizhou, ChinaKey Laboratory of Maternal & Child Health and Exposure Science of Guizhou Higher Education Institutes, Zunyi, Guizhou, ChinaHighly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) is a mutant strain of the classic porcine reproductive and respiratory syndrome virus (PRRSV) characterized by high morbidity and mortality rates. Epidemiological analysis revealed a natural mutation and stable inheritance of amino acid 46 (41-PGKKNKK-47 mutated to 41-PGKKNRK-47) in the nuclear localization signal or sequence (NLS) region of the N protein of HP-PRRSV. In this study, we showed that the nucleoplasmic shuttling of the HP-PRRSV N protein was associated with a higher efficiency of viral replication than that of the classical PRRSV. The nuclear transporter receptors KPNB1, KPNA1, KPNA2, KPNA6, and KPNA7 were involved in the nuclear import of the N protein. Additionally, the mRNA expression levels of KPNB1 and KPNA1 differed between the two strains after infecting the Marc-145 cells with these strains. The viral replication efficiency also decreased when expression levels of KPNA1 and/or KPNB1 were lowered. Finally, protein binding simulation and kinetic assay showed that the mutation of key amino acid 46 in the NLS region altered the binding mode and kinetics of the N proteins to KPNA1 and KPNB1. This study elucidates, for the first time, the reasons for the enhanced nucleoplasmic shuttling and replication efficiency of HP-PRRSV from the perspective of protein entry into the nucleus. It also provides a foundational reference for the prevention and control of PRRSV.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1587634/fullPRRSVnucleocapsid proteinNLSNTRnuclear-mass shuttle
spellingShingle Xianchang Zhu
Yang Xia
Qian Lei
Yu Gan
Shenghai Jiang
Lian Huang
Qihu Wen
Wei Fu
Bo Zhang
Yi Zhang
Shanshan Xie
Jida Li
Jida Li
Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV
Frontiers in Microbiology
PRRSV
nucleocapsid protein
NLS
NTR
nuclear-mass shuttle
title Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV
title_full Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV
title_fullStr Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV
title_full_unstemmed Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV
title_short Natural mutations in key NLS amino acids regulate nucleoplasmic shuttling and replication efficiency in PRRSV
title_sort natural mutations in key nls amino acids regulate nucleoplasmic shuttling and replication efficiency in prrsv
topic PRRSV
nucleocapsid protein
NLS
NTR
nuclear-mass shuttle
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1587634/full
work_keys_str_mv AT xianchangzhu naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT yangxia naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT qianlei naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT yugan naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT shenghaijiang naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT lianhuang naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT qihuwen naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT weifu naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT bozhang naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT yizhang naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT shanshanxie naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT jidali naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv
AT jidali naturalmutationsinkeynlsaminoacidsregulatenucleoplasmicshuttlingandreplicationefficiencyinprrsv