Viral envelope proteins fused to multiple distinct fluorescent reporters to probe receptor binding.
GFP
SARS‐CoV‐2
attachment protein
hemagglutinin
influenza a virus
multivalency
receptor‐binding
Journal
Protein science : a publication of the Protein Society
ISSN: 1469-896X
Titre abrégé: Protein Sci
Pays: United States
ID NLM: 9211750
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
revised:
04
03
2024
received:
25
10
2023
accepted:
13
03
2024
medline:
27
3
2024
pubmed:
27
3
2024
entrez:
27
3
2024
Statut:
ppublish
Résumé
Enveloped viruses carry one or multiple proteins with receptor-binding functionalities. Functional receptors can be glycans, proteinaceous, or both; therefore, recombinant protein approaches are instrumental in attaining new insights regarding viral envelope protein receptor-binding properties. Visualizing and measuring receptor binding typically entails antibody detection or direct labeling, whereas direct fluorescent fusions are attractive tools in molecular biology. Here, we report a suite of distinct fluorescent fusions, both N- and C-terminal, for influenza A virus hemagglutinins and SARS-CoV-2 spike RBD. The proteins contained three or six fluorescent protein barrels and were applied directly to cells to assess receptor binding properties.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4974Subventions
Organisme : NWO Rubicon Grant
ID : 45219118
Organisme : European Commission
ID : 802780
Informations de copyright
© 2024 The Authors. Protein Science published by Wiley Periodicals LLC on behalf of The Protein Society.
Références
Bacia K, Kim SA, Schwille P. Fluorescence cross‐correlation spectroscopy in living cells. Nat Methods. 2006;3(2):83–89.
Banfield DK. Mechanisms of protein retention in the Golgi. Cold Spring Harb Perspect Biol. 2011;3(8):a005264.
Bastiaens PI, Squire A. Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol. 1999;9(2):48–52.
Bindels DS, Haarbosch L, van Weeren L, Postma M, Wiese KE, Mastop M, et al. mScarlet: a bright monomeric red fluorescent protein for cellular imaging. Nat Methods. 2017;14(1):53–56.
Bouwman KM, Tomris I, Turner HL, van der Woude R, Shamorkina TM, Bosman GP, et al. Multimerization‐ and glycosylation‐dependent receptor binding of SARS‐CoV‐2 spike proteins. PLoS Pathogen. 2021;17(2):e1009282.
Broszeit F, Tzarum N, Zhu X, Nemanichvili N, Eggink D, Leenders T, et al. N‐glycolylneuraminic acid as a receptor for influenza a viruses. Cell Rep. 2019;27(11):3284–3294 e6.
Broszeit F, van Beek RJ, Unione L, Bestebroer TM, Chapla D, Yang JY, et al. Glycan remodeled erythrocytes facilitate antigenic characterization of recent A/H3N2 influenza viruses. Nat Commun. 2021;12(1):5449.
Byrd‐Leotis L, Gao C, Jia N, Mehta AY, Trost J, Cummings SF, et al. Antigenic pressure on H3N2 influenza virus drift strains imposes constraints on binding to sialylated receptors but not phosphorylated glycans. J Virol. 2019;93(22):e01178‐19.
Byrd‐Leotis L, Jia N, Matsumoto Y, Lu D, Kawaoka Y, Steinhauer DA, et al. Sialylated and sulfated N‐Glycans in MDCK and engineered MDCK cells for influenza virus studies. Sci Rep. 2022;12(1):12757.
Canales A, Sastre J, Orduña JM, Spruit CM, Pérez‐Castells J, Domínguez G, et al. Revealing the specificity of human H1 influenza A viruses to complex N‐glycans. JACS Au. 2023;3(3):868–878.
Chang DK, Cheng SF, Kantchev EAB, Lin CH, Liu YT. Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex. BMC Biol. 2008;6:2.
Chen SX, Osipovich AB, Ustione A, Potter LA, Hipkens S, Gangula R, et al. Quantification of factors influencing fluorescent protein expression using RMCE to generate an allelic series in the ROSA26 locus in mice. Dis Model Mech. 2011;4(4):537–547.
Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev. 2010;90(3):1103–1163.
Costantini LM, Fossati M, Francolini M, Snapp EL. Assessing the tendency of fluorescent proteins to oligomerize under physiologic conditions. Traffic. 2012;13(5):643–649.
Cranfill PJ, Sell BR, Baird MA, Allen JR, Lavagnino Z, de Gruiter HM, et al. Quantitative assessment of fluorescent proteins. Nat Methods. 2016;13(7):557–562.
Cummings RD. The repertoire of glycan determinants in the human glycome. Mol Biosyst. 2009;5(10):1087–1104.
de Vries RP, de Vries E, Bosch BJ, de Groot RJ, Rottier PJM, de Haan CAM. The influenza A virus hemagglutinin glycosylation state affects receptor‐binding specificity. Virology. 2010;403(1):17–25.
Deliolanis NC, Kasmieh R, Wurdinger T, Tannous BA, Shah K, Ntziachristos V. Performance of the red‐shifted fluorescent proteins in deep‐tissue molecular imaging applications. J Biomed Opt. 2008;13(4):44008.
Ekiert DC, Bhabha G, Elsliger MA, Friesen RHE, Jongeneelen M, Throsby M, et al. Antibody recognition of a highly conserved influenza virus epitope. Science. 2009;324(5924):246–251.
Ekiert DC, Friesen RHE, Bhabha G, Kwaks T, Jongeneelen M, Yu W, et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science. 2011;333(6044):843–850.
Everest H, Stevenson‐Leggett P, Bailey D, Bickerton E, Keep S. Known cellular and receptor interactions of animal and human coronaviruses: a review. Viruses. 2022;14(2):351.
Fraser BJ, Beldar S, Seitova A, Hutchinson A, Mannar D, Li Y, et al. Structure and activity of human TMPRSS2 protease implicated in SARS‐CoV‐2 activation. Nat Chem Biol. 2022;18(9):963–971.
Gambaryan A, Yamnikova S, Lvov D, Tuzikov A, Chinarev A, Pazynina G, et al. Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology. 2005;334(2):276–283.
Goedhart J, von Stetten D, Noirclerc‐Savoye M, Lelimousin M, Joosen L, Hink MA, et al. Structure‐guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun. 2012;3:751.
Gulati S, Smith DF, Cummings RD, Couch RB, Griesemer SB, St. George K, et al. Human H3N2 influenza viruses isolated from 1968 to 2012 show varying preference for receptor substructures with No apparent consequences for disease or spread. PLoS One. 2013;8(6):e66325.
Hanson MR, Kohler RH. GFP imaging: methodology and application to investigate cellular compartmentation in plants. J Exp Bot. 2001;52(356):529–539.
Heesters BA, van Megesen K, Tomris I, de Vries RP, Magri G, Spits H. Characterization of human FDCs reveals regulation of T cells and antigen presentation to B cells. J Exp Med. 2021;218(10):e20210790.
Hovmoller S, Zhou T. Why are both ends of the polypeptide chain on the outside of proteins? Proteins. 2004;55(2):219–222.
Hua S, Saunders M, Dimapasoc LM, Jeong SH, Kim BJ, Kim S, et al. Differentiation of cancer cell origin and molecular subtype by plasma membrane N‐glycan profiling. J Proteome Res. 2014;13(2):961–968.
Ji Y, White YJB, Hadden JA, Grant OC, Woods RJ. New insights into influenza a specificity: an evolution of paradigms. Curr Opin Struct Biol. 2017;44:219–231.
Joyce MG, Wheatley AK, Thomas PV, Chuang GY, Soto C, Bailer RT, et al. Vaccine‐induced antibodies that neutralize group 1 and group 2 influenza a viruses. Cell. 2016;166(3):609–623.
Katayama H, Yamamoto A, Mizushima N, Yoshimori T, Miyawaki A. GFP‐like proteins stably accumulate in lysosomes. Cell Struct Funct. 2008;33(1):1–12.
Katz BZ, Krylov D, Aota SI, Olive M, Vinson C, Yamada KM. Green fluorescent protein labeling of cytoskeletal structures – novel targeting approach based on leucine zippers. Biotechniques. 1998;25(2):298.
Kermani AA. Applications of fluorescent protein tagging in structural studies of membrane proteins. FEBS J. 2024.
Kleeman B, Olsson A, Newkold T, Kofron M, DeLay M, Hildeman D, et al. A guide to choosing fluorescent protein combinations for flow cytometric analysis based on spectral overlap. Cytometry A. 2018;93(5):556–562.
Kneen M, Farinas J, Li Y, Verkman AS. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys J. 1998;74(3):1591–1599.
Kremers GJ, Gilbert SG, Cranfill PJ, Davidson MW, Piston DW. Fluorescent proteins at a glance. J Cell Sci. 2011;124(Pt 2):157–160.
Lander GC, Stagg SM, Voss NR, Cheng A, Fellmann D, Pulokas J, et al. Appion: an integrated, database‐driven pipeline to facilitate EM image processing. J Struct Biol. 2009;166(1):95–102.
Li F. Receptor recognition mechanisms of coronaviruses: a decade of structural studies. J Virol. 2015;89(4):1954–1964.
Li ZM, Fan ZL, Wang XY, Wang TY. Factors affecting the expression of recombinant protein and improvement strategies in Chinese hamster ovary cells. Front Bioeng Biotechnol. 2022;10:880155.
Liao HY, Hsu CH, Wang SC, Liang CH, Yen HY, Su CY, et al. Differential receptor binding affinities of influenza hemagglutinins on glycan arrays. J Am Chem Soc. 2010;132(42):14849–14856.
Liu L, Chopra P, Li X, Bouwman KM, Tompkins SM, Wolfert MA, et al. Heparan sulfate proteoglycans as attachment factor for SARS‐CoV‐2. ACS Cent Sci. 2021;7(6):1009–1018.
Nemanichvili N, Berends AJ, Tomris I, Barnard KN, Parrish CR, Gröne A, et al. Influenza D binding properties vary amongst the two major virus clades and wildlife species. Vet Microbiol. 2022;264:109298.
Nemanichvili N, Tomris I, Turner HL, McBride R, Grant OC, van der Woude R, et al. Fluorescent trimeric hemagglutinins reveal multivalent receptor binding properties. J Mol Biol. 2019;431(4):842–856.
Nguyen L, McCord KA, Bui DT, Bouwman KM, Kitova EN, Elaish M, et al. Sialic acid‐containing glycolipids mediate binding and viral entry of SARS‐CoV‐2. Nat Chem Biol. 2022;18(1):81–90.
O'Donnell EA, Ernst DN, Hingorani R. Multiparameter flow cytometry: advances in high resolution analysis. Immune Netw. 2013;13(2):43–54.
Ogando NS, Dalebout TJ, Zevenhoven‐Dobbe JC, Limpens RWAL, van der Meer Y, Caly L, et al. SARS‐coronavirus‐2 replication in Vero E6 cells: replication kinetics, rapid adaptation and cytopathology. J Gen Virol. 2020;101(9):925–940.
Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS. Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol. 2006;24(1):79–88.
Peng W, Bouwman KM, McBride R, Grant OC, Woods RJ, Verheije MH, et al. Enhanced human‐type receptor binding by ferret‐transmissible H5N1 with a K193T mutation. J Virol. 2018;92(10):e02016–e02017.
Peng W, de Vries RP, Grant OC, Thompson AJ, McBride R, Tsogtbaatar B, et al. Recent H3N2 viruses have evolved specificity for extended, branched human‐type receptors, conferring potential for increased avidity. Cell Host Microbe. 2017;21(1):23–34.
Potter CS, Chu H, Frey B, Green C, Kisseberth N, Madden TJ, et al. Leginon: a system for fully automated acquisition of 1000 electron micrographs a day. Ultramicroscopy. 1999;77(3):153–161.
Qing E, Hantak M, Perlman S, Gallagher T. Distinct roles for sialoside and protein receptors in coronavirus infection. MBio. 2020;11(1):e02764‐19.
Rana MS, Wang X, Banerjee A. An improved strategy for fluorescent tagging of membrane proteins for overexpression and purification in mammalian cells. Biochemistry. 2018;57(49):6741–6751.
Scheres SH. Semi‐automated selection of cryo‐EM particles in RELION‐1.3. J Struct Biol. 2015;189(2):114–122.
Sekar RB, Periasamy A. Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations. J Cell Biol. 2003;160(5):629–633.
Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, et al. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods. 2008;5(6):545–551.
Shen Y, Chen Y, Wu J, Shaner NC, Campbell RE. Engineering of mCherry variants with long stokes shift, red‐shifted fluorescence, and low cytotoxicity. PLoS One. 2017;12(2):e0171257.
Snapp E. Design and use of fluorescent fusion proteins in cell biology. Curr Protoc Cell Biol. 2005;Chapter 21:21 4 1–21 4 13.
Spruit CM, Sweet IR, Maliepaard JCL, Bestebroer T, Lexmond P, Qiu B, et al. Contemporary human H3N2 influenza a viruses require a low threshold of suitable glycan receptors for efficient infection. Glycobiology. 2023;33:784–800.
Srinivasan A, Viswanathan K, Raman R, Chandrasekaran A, Raguram S, Tumpey TM, et al. Quantitative biochemical rationale for differences in transmissibility of 1918 pandemic influenza A viruses. Proc Natl Acad Sci U S A. 2008;105(8):2800–2805.
Stepanenko OV, Stepanenko OV, Kuznetsova IM, Verkhusha VV, Turoverov KK. Beta‐barrel scaffold of fluorescent proteins: folding, stability and role in chromophore formation. Int Rev Cell Mol Biol. 2013;302:221–278.
Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, et al. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol. 2006;355(5):1143–1155.
Subach OM, Cranfill PJ, Davidson MW, Verkhusha VV. An enhanced monomeric blue fluorescent protein with the high chemical stability of the chromophore. PLoS One. 2011;6(12):e28674.
Takada K, Kawakami C, Fan S, Chiba S, Zhong G, Gu C, et al. A humanized MDCK cell line for the efficient isolation and propagation of human influenza viruses. Nat Microbiol. 2019;4(8):1268–1273.
Tharakaraman K, Subramanian V, Cain D, Sasisekharan V, Sasisekharan R. Broadly neutralizing influenza hemagglutinin stem‐specific antibody CR8020 targets residues that are prone to escape due to host selection pressure. Cell Host Microbe. 2014;15(5):644–651.
Thorn K. Genetically encoded fluorescent tags. Mol Biol Cell. 2017;28(7):848–857.
Tomris I, Unione L, Nguyen L, Zaree P, Bouwman KM, Liu L, et al. SARS‐CoV‐2 spike N‐terminal domain engages 9‐O‐acetylated alpha2‐8‐linked sialic acids. ACS Chem Biol. 2023;18(5):1180–1191.
Tsai HC, Lehman CW, Lin CC, Tsai SW, Chen CM. Functional evaluation for adequacy of MDCK‐lineage cells in influenza research. BMC Res Notes. 2019;12(1):101.
Tsien RY. The green fluorescent protein. Annu Rev Biochem. 1998;67:509–544.
van der Woude R, Turner HL, Tomris I, Bouwman KM, Ward AB, de Vries RP. Drivers of recombinant soluble influenza A virus hemagglutinin and neuraminidase expression in mammalian cells. Protein Sci. 2020;29(9):1975–1982.
Voss NR, Yoshioka CK, Radermacher M, Potter CS, Carragher B. DoGPicker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J Struct Biol. 2009;166(2):205–213.
Walls AC, Park YJ, Tortorici MA, Wall A, McGuire AT, Veesler D. Structure, function, and antigenicity of the SARS‐CoV‐2 spike glycoprotein. Cell. 2020;181(2):281–292 e6.
Wang L, Jackson WC, Steinbach PA, Tsien RY. Evolution of new nonantibody proteins via iterative somatic hypermutation. Proc Natl Acad Sci U S A. 2004;101(48):16745–16749.
Wang Q, Zhang Y, Wu L, Niu S, Song C, Zhang Z, et al. Structural and functional basis of SARS‐CoV‐2 entry by using human ACE2. Cell. 2020;181(4):894–904 e9.
Wannier TM, Gillespie SK, Hutchins N, McIsaac R, Wu SY, Shen Y, et al. Monomerization of far‐red fluorescent proteins. Proc Natl Acad Sci U S A. 2018;115(48):E11294–E11301.
Wu NC, Wilson IA. Influenza hemagglutinin structures and antibody recognition. Cold Spring Harb Perspect Med. 2020;10(8):a038778.