دورية أكاديمية

Nectin1 is a pivotal host factor involved in attachment and entry of red-spotted grouper nervous necrosis virus in the early stages of the viral life cycle.

التفاصيل البيبلوغرافية
العنوان: Nectin1 is a pivotal host factor involved in attachment and entry of red-spotted grouper nervous necrosis virus in the early stages of the viral life cycle.
المؤلفون: Zhang Z; Laboratory of Pathology and Immunology of Aquatic Animals, Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China., Xing J; Laboratory of Pathology and Immunology of Aquatic Animals, Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China.; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China., Tang X; Laboratory of Pathology and Immunology of Aquatic Animals, Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China.; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China., Sheng X; Laboratory of Pathology and Immunology of Aquatic Animals, Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China.; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China., Chi H; Laboratory of Pathology and Immunology of Aquatic Animals, Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China.; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China., Zhan W; Laboratory of Pathology and Immunology of Aquatic Animals, Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, China.; Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.
المصدر: Journal of virology [J Virol] 2024 Sep 17; Vol. 98 (9), pp. e0090124. Date of Electronic Publication: 2024 Aug 28.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: American Society For Microbiology Country of Publication: United States NLM ID: 0113724 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1098-5514 (Electronic) Linking ISSN: 0022538X NLM ISO Abbreviation: J Virol Subsets: MEDLINE
أسماء مطبوعة: Publication: Washington Dc : American Society For Microbiology
Original Publication: Baltimore, American Society for Microbiology.
مواضيع طبية MeSH: Nectins*/metabolism , Nodaviridae*/physiology , Virus Internalization* , Fish Diseases*/virology , Fish Diseases*/metabolism , RNA Virus Infections*/virology , RNA Virus Infections*/metabolism , RNA Virus Infections*/veterinary, Animals ; Virus Replication ; Virus Attachment ; Capsid Proteins/metabolism ; Capsid Proteins/genetics ; Brain/virology ; Brain/metabolism ; Virion/metabolism ; Cell Line
مستخلص: Nervous necrosis virus (NNV) is a highly neurotropic virus that poses a persistent threat to the survival of multiple fish species. However, its inimitable neuropathogenesis remains largely elusive. To rummage potential partners germane to the nervous system, we investigated the interaction between red-spotted grouper NNV (RGNNV) and grouper brain by immunoprecipitation coupled with mass spectrometry and discerned Nectin1 as a novel host factor subtly involved in viral early invasion events. Nectin1 was abundant in neural tissues and implicated in the inception of tunnel nanotubes triggered by RGNNV. Its overexpression not only dramatically potentiated the replication dynamics of RGNNV in susceptible cells, but also empowered non-sensitive cells to expeditiously capture free virions within 2 min. This potency was impervious to low temperatures but was dose-dependently suppressed by soluble protein or specific antibody of Nectin1 ectodomain, indicating Nectin1 as an attachment receptor for RGNNV. Mechanistically, efficient hijacking of virions by Nectin1 strictly depended on intricate linkages to different modules of viral capsid protein, especially the direct binding between the IgC1 loop and P-domain. More strikingly, despite abortive proliferation in Nectin1-reconstructed CHSE-214 cells, a non-sensitive cell, RGNNV could gain access to the intracellular compartment by capitalizing on Nectin1, thereby inducing canonical cytoplasmic vacuolation. Altogether, our findings delineate a candidate entrance for RGNNV infiltration into the nervous system, which may shed unprecedented insights into the exploration and elucidation of RGNNV pathogenesis.IMPORTANCENervous necrosis virus (NNV) is one of the most virulent pathogens in the aquaculture industry, which inflicts catastrophic damage to ecology, environment, and economy annually around the world. Nevertheless, its idiosyncratic invasion and latency mechanisms pose enormous hardships to epidemic prevention and control. In this study, deploying grouper brain as a natural screening library, a single-transmembrane glycoprotein, Nectin1, was first identified as an emergent functional receptor for red-spotted grouper NNV (RGNNV) that widely allocated in nervous tissues and directly interacted with viral capsid protein through distinct Ig-like loops to bridge virus-host crosstalk, apprehend free virions, and concomitantly propel viral entry. Our findings illuminate the critical role of Nectin1 in RGNNV attachment and entry and provide a potential target for future clinical intervention strategies in the therapeutic race against RGNNV.
Competing Interests: The authors declare no conflict of interest.
References: Cell Mol Life Sci. 2015 Feb;72(4):645-58. (PMID: 25326769)
J Gen Virol. 2005 Oct;86(Pt 10):2807-2816. (PMID: 16186236)
Front Microbiol. 2020 Apr 30;11:790. (PMID: 32425913)
J Virol. 2003 May;77(9):5324-32. (PMID: 12692234)
Nucleic Acids Res. 2018 Jan 4;46(D1):D493-D496. (PMID: 29040681)
J Fish Dis. 2009 May;32(5):421-31. (PMID: 19392682)
Sci Rep. 2017 Jan 06;7:40360. (PMID: 28059146)
Nucleic Acids Res. 1997 Dec 15;25(24):4876-82. (PMID: 9396791)
J Fish Dis. 2004 Jul;27(7):385-99. (PMID: 15228608)
Viruses. 2018 Jun 28;10(7):. (PMID: 29958408)
J Fish Dis. 2017 Nov;40(11):1489-1496. (PMID: 28449248)
Annu Rev Microbiol. 2013;67:355-74. (PMID: 24024635)
Sci Adv. 2022 Jul 22;8(29):eabo0171. (PMID: 35857849)
PLoS Pathog. 2011 Sep;7(9):e1002277. (PMID: 21980294)
Int J Biol Macromol. 2022 Oct 1;218:654-664. (PMID: 35878672)
Pathogens. 2020 Feb 09;9(2):. (PMID: 32050492)
Nat Struct Mol Biol. 2012 Sep;19(9):906-15. (PMID: 22902367)
J Virol. 2023 Apr 27;97(4):e0021023. (PMID: 36975780)
Curr Eye Res. 2004 Oct-Nov;29(4-5):303-9. (PMID: 15590476)
Gene. 1995 Apr 3;155(2):261-5. (PMID: 7721102)
J Fish Dis. 2007 Jul;30(7):419-26. (PMID: 17584439)
J Virol. 2021 Sep 27;95(20):e0119521. (PMID: 34379506)
J Gen Virol. 2005 Sep;86(Pt 9):2553-2561. (PMID: 16099914)
Viruses. 2015 Jun 02;7(6):2794-815. (PMID: 26043381)
J Gen Virol. 1999 Nov;80 ( Pt 11):3019-3022. (PMID: 10580064)
J Virol. 2012 Apr;86(8):4468-76. (PMID: 22345445)
J Virol. 2015 Jan;89(1):61-70. (PMID: 25320288)
Front Vet Sci. 2019 Feb 27;6:53. (PMID: 30873421)
Viruses. 2018 Nov 02;10(11):. (PMID: 30400213)
Vet Res. 2018 Sep 5;49(1):86. (PMID: 30185222)
J Virol. 2014 Dec;88(23):13678-88. (PMID: 25231300)
Fish Shellfish Immunol. 2016 Jun;53:35-49. (PMID: 26997200)
J Virol. 2022 Dec 21;96(24):e0144622. (PMID: 36472440)
Viruses. 2020 Sep 04;12(9):. (PMID: 32899810)
Appl Immunohistochem Mol Morphol. 2006 Sep;14(3):341-7. (PMID: 16932027)
J Virol. 2022 Mar 23;96(6):e0011322. (PMID: 35107370)
Front Microbiol. 2022 Feb 28;13:830699. (PMID: 35295302)
Appl Environ Microbiol. 1997 Apr;63(4):1633-6. (PMID: 9097459)
Science. 2001 May 11;292(5519):1102-5. (PMID: 11352064)
Fish Shellfish Immunol. 2022 Mar;122:426-436. (PMID: 35183740)
Vet Res. 2017 Feb 8;48(1):8. (PMID: 28179028)
Virulence. 2024 Dec;15(1):2301244. (PMID: 38230744)
PLoS Pathog. 2015 Oct 22;11(10):e1005203. (PMID: 26491970)
J Virol. 2021 Oct 27;95(22):e0122721. (PMID: 34468169)
J Fish Dis. 2004 Oct;27(10):591-601. (PMID: 15482424)
J Virol. 2003 Mar;77(5):3307-11. (PMID: 12584355)
Sci China Life Sci. 2024 Apr;67(4):733-744. (PMID: 38388846)
J Fish Dis. 2017 May;40(5):717-742. (PMID: 27633881)
mBio. 2021 Mar 30;12(2):. (PMID: 33785615)
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W252-8. (PMID: 24782522)
Arch Virol. 2022 Oct;167(10):1961-1975. (PMID: 35752988)
Fish Shellfish Immunol. 2019 Oct;93:720-725. (PMID: 31404634)
PLoS Pathog. 2017 May 19;13(5):e1006314. (PMID: 28542478)
Virology. 1992 Mar;187(1):368-71. (PMID: 1736540)
Methods. 2001 Dec;25(4):402-8. (PMID: 11846609)
Vet Microbiol. 2023 Apr;279:109672. (PMID: 36774841)
PLoS Pathog. 2020 Jul 8;16(7):e1008668. (PMID: 32639977)
J Gen Virol. 2015 Jun;96(Pt 6):1287-1296. (PMID: 25626678)
Arch Virol. 2007;152(12):2217-24. (PMID: 17891330)
Science. 1998 Jun 5;280(5369):1618-20. (PMID: 9616127)
Dev Dyn. 2009 Jan;238(1):43-55. (PMID: 19097185)
J Virol. 2020 Mar 31;94(8):. (PMID: 32024778)
Sci Adv. 2020 May 13;6(20):eaba5147. (PMID: 32426511)
EMBO J. 2021 Apr 15;40(8):e105789. (PMID: 33646572)
Neuron. 2016 Dec 7;92(5):949-958. (PMID: 27930910)
J Biol Chem. 2002 Jul 26;277(30):27006-13. (PMID: 12011057)
Virology. 2009 Mar 15;385(2):444-54. (PMID: 19136133)
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W320-4. (PMID: 24753421)
Virulence. 2021 Dec;12(1):968-980. (PMID: 33724154)
PLoS Pathog. 2021 Jun 29;17(6):e1009665. (PMID: 34185811)
Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17916-20. (PMID: 19805039)
معلومات مُعتمدة: 2023YFD2400701, 2023YFD2400702, 2018YFD0900503 MOST | National Key Research and Development Program of China (NKPs); 32173005 MOST | National Natural Science Foundation of China (NSFC)
فهرسة مساهمة: Keywords: Nectin1; attachment; entry; red-spotted grouper nervous necrosis virus; virus-host interaction
المشرفين على المادة: 0 (Nectins)
0 (Capsid Proteins)
تواريخ الأحداث: Date Created: 20240828 Date Completed: 20240917 Latest Revision: 20240919
رمز التحديث: 20240919
مُعرف محوري في PubMed: PMC11406929
DOI: 10.1128/jvi.00901-24
PMID: 39194240
قاعدة البيانات: MEDLINE
الوصف
تدمد:1098-5514
DOI:10.1128/jvi.00901-24