دورية أكاديمية
Interaction between host G3BP and viral nucleocapsid protein regulates SARS-CoV-2 replication and pathogenicity.
العنوان: | Interaction between host G3BP and viral nucleocapsid protein regulates SARS-CoV-2 replication and pathogenicity. |
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المؤلفون: | Yang Z; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA; Integrated Biomedical Sciences Program, University of Tennessee Health Science Center, Memphis, TN, USA., Johnson BA; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA; Institute for Human Infection and Immunity, University of Texas Medical Branch, Galveston, TX, USA; Center for Tropical Diseases, University of Texas Medical Branch, Galveston, TX, USA., Meliopoulos VA; Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN, USA., Ju X; School of Medicine, Tsinghua University, Beijing, China., Zhang P; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA., Hughes MP; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA., Wu J; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA; Integrated Biomedical Sciences Program, University of Tennessee Health Science Center, Memphis, TN, USA., Koreski KP; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA., Clary JE; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA., Chang TC; Center for Applied Bioinformatics, St. Jude Children's Research Hospital, Memphis, TN, USA., Wu G; Center for Applied Bioinformatics, St. Jude Children's Research Hospital, Memphis, TN, USA., Hixon J; Faze Medicines, Cambridge, MA, USA., Duffner J; Faze Medicines, Cambridge, MA, USA., Wong K; Faze Medicines, Cambridge, MA, USA., Lemieux R; Faze Medicines, Cambridge, MA, USA., Lokugamage KG; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA., Alvarado RE; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA., Crocquet-Valdes PA; Department of Pathology, University of Texas Medical Branch, Galveston, TX, USA., Walker DH; Department of Pathology, University of Texas Medical Branch, Galveston, TX, USA., Plante KS; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA; World Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical Branch, Galveston, TX, USA., Plante JA; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA; World Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical Branch, Galveston, TX, USA., Weaver SC; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA; Institute for Human Infection and Immunity, University of Texas Medical Branch, Galveston, TX, USA; World Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical Branch, Galveston, TX, USA., Kim HJ; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA., Meyers R; Faze Medicines, Cambridge, MA, USA., Schultz-Cherry S; Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN, USA., Ding Q; School of Medicine, Tsinghua University, Beijing, China., Menachery VD; Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA; World Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical Branch, Galveston, TX, USA. Electronic address: vimenach@utmb.edu., Taylor JP; Department of Cell and Molecular Biology, St. Jude Children's Research Hospital, Memphis, TN, USA; Howard Hughes Medical Institute, Chevy Chase, MD, USA. Electronic address: jpaul.taylor@stjude.org. |
المصدر: | Cell reports [Cell Rep] 2024 Mar 26; Vol. 43 (3), pp. 113965. Date of Electronic Publication: 2024 Mar 15. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Cell Press Country of Publication: United States NLM ID: 101573691 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2211-1247 (Electronic) NLM ISO Abbreviation: Cell Rep Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: [Cambridge, MA] : Cell Press, c 2012- |
مواضيع طبية MeSH: | SARS-CoV-2*/genetics , COVID-19*, Humans ; DNA Helicases/metabolism ; RNA Helicases/metabolism ; RNA Recognition Motif Proteins/metabolism ; Poly-ADP-Ribose Binding Proteins/metabolism ; Virulence ; RNA, Guide, CRISPR-Cas Systems ; Nucleocapsid Proteins ; Virus Replication ; RNA, Viral/genetics |
مستخلص: | G3BP1/2 are paralogous proteins that promote stress granule formation in response to cellular stresses, including viral infection. The nucleocapsid (N) protein of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) inhibits stress granule assembly and interacts with G3BP1/2 via an ITFG motif, including residue F17, in the N protein. Prior studies examining the impact of the G3PB1-N interaction on SARS-CoV-2 replication have produced inconsistent findings, and the role of this interaction in pathogenesis is unknown. Here, we use structural and biochemical analyses to define the residues required for G3BP1-N interaction and structure-guided mutagenesis to selectively disrupt this interaction. We find that N-F17A mutation causes highly specific loss of interaction with G3BP1/2. SARS-CoV-2 N-F17A fails to inhibit stress granule assembly in cells, has decreased viral replication, and causes decreased pathology in vivo. Further mechanistic studies indicate that the N-F17-mediated G3BP1-N interaction promotes infection by limiting sequestration of viral genomic RNA (gRNA) into stress granules. Competing Interests: Declaration of interests J.P.T. is a consultant for Nido Biosciences. V.D.M. has filed a patent on the reverse genetic system and reporter SARS-CoV-2. (Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.) |
التعليقات: | Update of: bioRxiv. 2023 Jun 30;:. (PMID: 37425880) |
References: | Front Cell Dev Biol. 2021 Feb 11;9:625711. (PMID: 33644063) iScience. 2022 Jan 21;25(1):103562. (PMID: 34901782) J Biol Chem. 2022 Mar;298(3):101677. (PMID: 35131265) Lancet Glob Health. 2022 Jul;10(7):e961-e969. (PMID: 35597249) FEBS J. 2022 Jul;289(13):3813-3825. (PMID: 34665939) Curr Protoc Immunol. 2020 Dec;131(1):e116. (PMID: 33215858) BMJ. 2022 Mar 9;376:e069761. (PMID: 35264324) PLoS Pathog. 2022 Jun 21;18(6):e1010627. (PMID: 35728038) Elife. 2022 Jan 20;11:. (PMID: 35049501) Mol Cell. 2017 Nov 16;68(4):808-820.e5. (PMID: 29129640) Nat Protoc. 2021 Mar;16(3):1761-1784. (PMID: 33514944) PLoS One. 2021 Nov 11;16(11):e0259165. (PMID: 34762662) Cell Discov. 2021 May 25;7(1):38. (PMID: 34035218) Proc Natl Acad Sci U S A. 2022 Nov;119(44):e2207975119. (PMID: 36279435) PLoS One. 2013 Nov 18;8(11):e79546. (PMID: 24260247) Open Biol. 2016 Jul;6(7):. (PMID: 27383630) mBio. 2014 May 20;5(3):e01174-14. (PMID: 24846384) Elife. 2019 Aug 12;8:. (PMID: 31403400) Cell Host Microbe. 2012 Jul 19;12(1):71-85. (PMID: 22817989) Nucleic Acids Res. 2015 Jan;43(Database issue):D447-52. (PMID: 25352553) Cell. 2020 May 14;181(4):914-921.e10. (PMID: 32330414) PLoS One. 2010 Jan 15;5(1):e8729. (PMID: 20090954) Cell Death Dis. 2019 Dec 11;10(12):946. (PMID: 31827077) J Virol. 2014 May;88(10):5888-93. (PMID: 24623412) Viruses. 2014 Aug 07;6(8):2991-3018. (PMID: 25105276) Sci Bull (Beijing). 2021 Jun 30;66(12):1194-1204. (PMID: 33495715) Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2184-95. (PMID: 15572771) Nat Commun. 2021 Aug 25;12(1):5120. (PMID: 34433827) China CDC Wkly. 2021 Dec 3;3(49):1049-1051. (PMID: 34934514) Annu Rev Virol. 2014 Nov;1(1):147-70. (PMID: 26958719) J Virol. 2021 Apr 12;95(9):. (PMID: 33568512) Clin Infect Dis. 2020 Dec 3;71(9):2428-2446. (PMID: 32215622) PLoS Pathog. 2021 Mar 12;17(3):e1009439. (PMID: 33711082) Acta Pharm Sin B. 2020 Jul;10(7):1228-1238. (PMID: 32363136) Biochem Biophys Res Commun. 2015 Nov 6;467(1):53-7. (PMID: 26410532) Open Biol. 2023 May;13(5):220369. (PMID: 37161291) Cell Host Microbe. 2014 Oct 8;16(4):462-72. (PMID: 25299332) PLoS Biol. 2021 Oct 11;19(10):e3001425. (PMID: 34634033) J Mol Biol. 2022 May 15;434(9):167516. (PMID: 35240128) Mol Biol Cell. 2012 Dec;23(24):4701-12. (PMID: 23087212) PLoS Pathog. 2022 Dec 19;18(12):e1011041. (PMID: 36534661) Signal Transduct Target Ther. 2022 Sep 7;7(1):312. (PMID: 36071039) J Virol. 2019 May 1;93(10):. (PMID: 30867299) Saudi Med J. 2023 Apr;44(4):427. (PMID: 37062542) Antiviral Res. 2021 Jun;190:105064. (PMID: 33781803) J Virol. 2019 Jan 4;93(2):. (PMID: 30404792) J Virol. 2016 Jun 24;90(14):6489-6501. (PMID: 27147742) Protein Sci. 2020 Sep;29(9):1890-1901. (PMID: 32654247) J Virol. 2012 Oct;86(19):10873-9. (PMID: 22837213) Mol Syst Biol. 2021 Nov;17(11):e10396. (PMID: 34709727) Med. 2021 Jan 15;2(1):99-112.e7. (PMID: 32838362) Nature. 2020 Jul;583(7818):834-838. (PMID: 32408338) J Virol. 2004 Nov;78(22):12683-8. (PMID: 15507657) Mol Cell. 2023 Apr 6;83(7):1180-1196.e8. (PMID: 37028415) Cell Host Microbe. 2007 Nov 15;2(5):295-305. (PMID: 18005751) Antiviral Res. 2014 Mar;103:39-50. (PMID: 24418573) mBio. 2013 Apr 30;4(3):e00165-13. (PMID: 23631916) EMBO J. 2021 Sep 1;40(17):e107776. (PMID: 34232536) Bioinformatics. 2018 Dec 1;34(23):4121-4123. (PMID: 29790939) Proc Natl Acad Sci U S A. 2020 Jul 14;117(28):16587-16595. (PMID: 32571934) Cell. 2015 Sep 24;163(1):123-33. (PMID: 26406374) Nature. 2021 Jun;594(7862):246-252. (PMID: 33845483) Mol Biomed. 2020;1(1):2. (PMID: 34765991) Cell Host Microbe. 2020 May 13;27(5):841-848.e3. (PMID: 32289263) Protein Eng. 2001 Dec;14(12):993-1000. (PMID: 11809930) Signal Transduct Target Ther. 2022 Jan 24;7(1):22. (PMID: 35075101) J Virol. 2013 Sep;87(17):9511-22. (PMID: 23785203) Emerg Infect Dis. 2020 Jun;26(6):1266-1273. (PMID: 32160149) Nat Biotechnol. 2023 Jan;41(1):128-139. (PMID: 36217030) Nat Methods. 2022 Apr;19(4):392-394. (PMID: 35396468) Nat Microbiol. 2021 Jul;6(7):821-823. (PMID: 34108654) J Virol. 2015 Apr;89(8):4457-69. (PMID: 25653451) Nat Commun. 2021 Nov 19;12(1):6761. (PMID: 34799561) J Cell Biol. 2016 Mar 28;212(7):845-60. (PMID: 27022092) J Virol. 2019 May 29;93(12):. (PMID: 30944179) Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32. (PMID: 15572765) Front Microbiol. 2022 Aug 23;13:997539. (PMID: 36081788) EMBO J. 2020 Oct 15;39(20):e105938. (PMID: 32914439) J Virol. 2017 Jul 27;91(16):. (PMID: 28592527) J Proteome Res. 2022 Feb 4;21(2):459-469. (PMID: 34982558) Lancet. 2022 Apr 2;399(10332):1303-1312. (PMID: 35305296) Proc Natl Acad Sci U S A. 2021 Feb 9;118(6):. (PMID: 33547245) Sci Adv. 2024 Feb 2;10(5):eadk8152. (PMID: 38295168) Lancet Reg Health Eur. 2023 Feb;25:100556. (PMID: 36530491) Life Sci Alliance. 2022 Jan 7;5(4):. (PMID: 34996842) Viruses. 2020 Sep 04;12(9):. (PMID: 32899736) Signal Transduct Target Ther. 2021 Sep 1;6(1):331. (PMID: 34471099) Front Chem. 2021 Jan 12;8:624765. (PMID: 33511102) PLoS One. 2013 Dec 04;8(12):e80947. (PMID: 24324649) Nature. 2020 Sep;585(7826):588-590. (PMID: 32698190) J Virol. 2022 Jun 22;96(12):e0041222. (PMID: 35652658) PLoS Pathog. 2020 Dec 2;16(12):e1009100. (PMID: 33264373) J Virol. 2010 Feb;84(4):2169-75. (PMID: 19955314) Nat Protoc. 2013 Nov;8(11):2281-2308. (PMID: 24157548) Neuron. 2017 Aug 16;95(4):808-816.e9. (PMID: 28817800) PLoS Pathog. 2016 Feb 10;12(2):e1005444. (PMID: 26862753) Mol Aspects Med. 2023 Jun;91:101151. (PMID: 36371228) J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674. (PMID: 19461840) J Proteome Res. 2010 Oct 1;9(10):5133-41. (PMID: 20698585) Cell. 2020 Apr 16;181(2):271-280.e8. (PMID: 32142651) Vet Microbiol. 2019 Sep;236:108392. (PMID: 31500725) Mol Biol Cell. 2005 Aug;16(8):3753-63. (PMID: 15930128) Acta Crystallogr D Struct Biol. 2018 Feb 1;74(Pt 2):85-97. (PMID: 29533234) Nature. 2020 Jul;583(7816):459-468. (PMID: 32353859) Cell Discov. 2021 Aug 17;7(1):69. (PMID: 34400613) Cell. 2020 Apr 16;181(2):325-345.e28. (PMID: 32302571) Nat Commun. 2021 Mar 29;12(1):1936. (PMID: 33782395) |
معلومات مُعتمدة: | R21 AI145400 United States AI NIAID NIH HHS; U19 AI171413 United States AI NIAID NIH HHS; 75N93021C00016 United States AI NIAID NIH HHS; R35 NS097974 United States NS NINDS NIH HHS; R24 AI120942 United States AI NIAID NIH HHS |
فهرسة مساهمة: | Keywords: CP: Microbiology; G3BP; NTF2L domain; SARS-CoV-2 replication and pathogenesis; host-pathogen interaction; nucleocapsid protein; stress granule; vRNA sequestration |
المشرفين على المادة: | EC 3.6.4.- (DNA Helicases) EC 3.6.4.13 (RNA Helicases) 0 (RNA Recognition Motif Proteins) 0 (Poly-ADP-Ribose Binding Proteins) 0 (RNA, Guide, CRISPR-Cas Systems) 0 (Nucleocapsid Proteins) 0 (RNA, Viral) EC 3.6.4.12 (G3BP1 protein, human) |
تواريخ الأحداث: | Date Created: 20240316 Date Completed: 20240401 Latest Revision: 20240427 |
رمز التحديث: | 20240427 |
مُعرف محوري في PubMed: | PMC11044841 |
DOI: | 10.1016/j.celrep.2024.113965 |
PMID: | 38492217 |
قاعدة البيانات: | MEDLINE |
تدمد: | 2211-1247 |
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DOI: | 10.1016/j.celrep.2024.113965 |