Novel coronavirus-like particles targeting cells lining the respiratory tract

PLoS ONE

Volumn 13, Issue 9, 2018, Pages

  Naskalska, Antonina ^a   Dabrowska, Agnieszka ^a   Nowak, Paulina ^a   Szczepanski, Artur ^a   Jasik, Krzysztof ^b   Milewska, Aleksandra ^a   Ochman, Marek ^b   Zeglen, Slawomir ^b   Rajfur, Zenon ^a   Pyrc, Krzysztof ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b MEDICAL UNIVERSITY OF SILESIA   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BACULOVIRUS VECTOR; BETA SECRETASE 2; NANOPARTICLE; PROTEIN ACE2; UNCLASSIFIED DRUG; VIRAL PROTEIN; ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE; VIRUS LIKE PARTICLE VACCINE;

AIRWAY EPITHELIUM CELL; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CELL TRANSPORT; CHROMATOGRAPHY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CORONAVIRUS NL63; HUMAN TISSUE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; VIRAL TROPISM; VIRUS LIKE AGENT; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG DELIVERY SYSTEM; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES; RESPIRATORY MUCOSA; RHESUS MONKEY; SPODOPTERA;

ANIMALS; CELL LINE; CORONAVIRUS NL63, HUMAN; DRUG DELIVERY SYSTEMS; HUMANS; MACACA MULATTA; NANOPARTICLES; PEPTIDYL-DIPEPTIDASE A; RESPIRATORY MUCOSA; SPODOPTERA; VACCINES, VIRUS-LIKE PARTICLE;

EID: 85053030815     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0203489     Document Type: Article

References (69)

1. Kushnir N, Streatfield SJ, Yusibov V. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine. 2012; 31(1):58–83. https://doi.org/10.1016/j.vaccine.2012.10.083 PMID: 23142589.
2. Zeltins A. Construction and characterization of virus-like particles: a review. Mol Biotechnol. 2013; 53 (1):92–107. https://doi.org/10.1007/s12033-012-9598-4 PMID: 23001867.
3. Naskalska A, Pyrć K. Virus Like Particles as Immunogens and Universal Nanocarriers. Pol J Microbiol. 2015; 64(1):3–13. PMID: 26094310.
4. Mortola E, Roy P. Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Lett. 2004; 576(1–2):174–8. https://doi.org/10.1016/j.febslet.2004.09.009PMID: 15474033.
5. Hsieh PK, Chang SC, Huang CC, Lee TT, Hsiao CW, Kou YH, et al. Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent. J Virol. 2005; 79(22):13848–55. https://doi.org/10.1128/JVI.79.22.13848-13855.2005 PMID: 16254320.
6. Siu YL, Teoh KT, Lo J, Chan CM, Kien F, Escriou N, et al. The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles. J Virol. 2008; 82(22):11318–30. Epub 2008/08/27. https://doi.org/10.1128/JVI.01052-08 PMID: 18753196.
7. Ho Y, Lin PH, Liu CY, Lee SP, Chao YC. Assembly of human severe acute respiratory syndrome coronavirus-like particles. Biochem Biophys Res Commun. 2004; 318(4):833–8. https://doi.org/10.1016/j.bbrc.2004.04.111 PMID: 15147946.
8. Nakauchi M, Kariwa H, Kon Y, Yoshii K, Maeda A, Takashima I. Analysis of severe acute respiratory syndrome coronavirus structural proteins in virus-like particle assembly. Microbiol Immunol. 2008; 52 (12):625–30. https://doi.org/10.1111/j.1348-0421.2008.00079.x PMID: 19120977.
9. Vennema H, Godeke GJ, Rossen JW, Voorhout WF, Horzinek MC, Opstelten DJ, et al. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 1996; 15(8):2020–8. PMID: 8617249.
10. de Haan CA, Kuo L, Masters PS, Vennema H, Rottier PJ. Coronavirus particle assembly: primary structure requirements of the membrane protein. J Virol. 1998; 72(8):6838–50. PMID: 9658133.
11. Narayanan K, Maeda A, Maeda J, Makino S. Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J Virol. 2000; 74(17):8127–34. PMID: 10933723.
12. Arndt AL, Larson BJ, Hogue BG. A conserved domain in the coronavirus membrane protein tail is important for virus assembly. J Virol. 2010; 84(21):11418–28. Epub 2010/08/18. https://doi.org/10.1128/JVI. 01131-10 PMID: 20719948.
13. Boscarino JA, Logan HL, Lacny JJ, Gallagher TM. Envelope protein palmitoylations are crucial for murine coronavirus assembly. J Virol. 2008; 82(6):2989–99. Epub 2008/01/09. https://doi.org/10.1128/JVI.01906-07 PMID: 18184706.
14. Corse E, Machamer CE. Infectious bronchitis virus E protein is targeted to the Golgi complex and directs release of virus-like particles. J Virol. 2000; 74(9):4319–26. PMID: 10756047.
15. Baudoux P, Carrat C, Besnardeau L, Charley B, Laude H. Coronavirus pseudoparticles formed with recombinant M and E proteins induce alpha interferon synthesis by leukocytes. J Virol. 1998; 72 (11):8636–43. PMID: 9765403.
16. Gelhaus S, Thaa B, Eschke K, Veit M, Schwegmann-Weßels C. Palmitoylation of the Alphacoronavirus TGEV spike protein S is essential for incorporation into virus-like particles but dispensable for S-M interaction. Virology. 2014; 464–465:397–405. Epub 2014/08/09. https://doi.org/10.1016/j.virol.2014.07.035PMID: 25113909.
17. Wang C, Yan F, Zheng X, Wang H, Jin H, Zhao Y, et al. Porcine epidemic diarrhea virus virus-like particles produced in insect cells induce specific immune responses in mice. Virus Genes. 2017. Epub 2017/03/29. https://doi.org/10.1007/s11262-017-1450-2 PMID: 28357676.
18. Tseng YT, Chang CH, Wang SM, Huang KJ, Wang CT. Identifying SARS-CoV membrane protein amino acid residues linked to virus-like particle assembly. PLoS One. 2013; 8(5):e64013. https://doi.org/10.1371/journal.pone.0064013 PMID: 23700447.
19. Thorp EB, Boscarino JA, Logan HL, Goletz JT, Gallagher TM. Palmitoylations on murine coronavirus spike proteins are essential for virion assembly and infectivity. J Virol. 2006; 80(3):1280–9. https://doi.org/10.1128/JVI.80.3.1280-1289.2006 PMID: 16415005.
20. Liu G, Lv L, Yin L, Li X, Luo D, Liu K, et al. Assembly and immunogenicity of coronavirus-like particles carrying infectious bronchitis virus M and S proteins. Vaccine. 2013; 31(47):5524–30. https://doi.org/10.1016/j.vaccine.2013.09.024 PMID: 24099870.
21. Xu PW, Wu X, Wang HN, Ma BC, Ding MD, Yang X. Assembly and immunogenicity of baculovirus-derived infectious bronchitis virus-like particles carrying membrane, envelope and the recombinant spike proteins. Biotechnol Lett. 2016; 38(2):299–304. Epub 2015/10/13. https://doi.org/10.1007/ s10529-015-1973-3 PMID: 26463372.
22. Lu B, Huang Y, Huang L, Li B, Zheng Z, Chen Z, et al. Effect of mucosal and systemic immunization with virus-like particles of severe acute respiratory syndrome coronavirus in mice. Immunology. 2010; 130(2):254–61. Epub 2010/04/06. https://doi.org/10.1111/j.1365-2567.2010.03231.x PMID: 20406307.
23. Lu X, Chen Y, Bai B, Hu H, Tao L, Yang J, et al. Immune responses against severe acute respiratory syndrome coronavirus induced by virus-like particles in mice. Immunology. 2007; 122(4):496–502. Epub 2007/08/03. https://doi.org/10.1111/j.1365-2567.2007.02676.x PMID: 17680799.
24. Lander GC, Baudoux AC, Azam F, Potter CS, Carragher B, Johnson JE. Capsomer dynamics and stabilization in the T = 12 marine bacteriophage SIO-2 and its procapsid studied by CryoEM. Structure. 2012; 20(3):498–503. https://doi.org/10.1016/j.str.2012.01.007 PMID: 22405008.
25. Wang C, Zheng X, Gai W, Zhao Y, Wang H, Feng N, et al. MERS-CoV virus-like particles produced in insect cells induce specific humoural and cellular imminity in rhesus macaques. Oncotarget. 2017; 8 (8):12686–94. https://doi.org/10.18632/oncotarget.8475 PMID: 27050368.
26. van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, et al. Identification of a new human coronavirus. Nat Med. 2004; 10(4):368–73. Epub 2004/03/21. https://doi.org/10.1038/ nm1024 PMID: 15034574.
27. Pyrc K, Jebbink MF, Berkhout B, van der Hoek L. Genome structure and transcriptional regulation of human coronavirus NL63. Virol J. 2004; 1:7. https://doi.org/10.1186/1743-422X-1-7 PMID: 15548333.
28. Müller MA, van der Hoek L, Voss D, Bader O, Lehmann D, Schulz AR, et al. Human coronavirus NL63 open reading frame 3 encodes a virion-incorporated N-glycosylated membrane protein. Virol J. 2010; 7:6. Epub 2010/01/15. https://doi.org/10.1186/1743-422X-7-6 PMID: 20078868.
29. Neuman BW, Kiss G, Kunding AH, Bhella D, Baksh MF, Connelly S, et al. A structural analysis of M protein in coronavirus assembly and morphology. J Struct Biol. 2011; 174(1):11–22. Epub 2010/12/03. https://doi.org/10.1016/j.jsb.2010.11.021 PMID: 21130884.
30. Ruch TR, Machamer CE. The coronavirus E protein: assembly and beyond. Viruses. 2012; 4(3):363–82. Epub 2012/03/08. https://doi.org/10.3390/v4030363 PMID: 22590676.
31. Ye Y, Hogue BG. Role of the coronavirus E viroporin protein transmembrane domain in virus assembly. J Virol. 2007; 81(7):3597–607. Epub 2007/01/17. https://doi.org/10.1128/JVI.01472-06 PMID: 17229680.
32. Zheng Q, Deng Y, Liu J, van der Hoek L, Berkhout B, Lu M. Core structure of S2 from the human coronavirus NL63 spike glycoprotein. Biochemistry. 2006; 45(51):15205–15. Epub 2006/12/01. https://doi.org/10.1021/bi061686w PMID: 17176042.
33. Gallagher TM, Buchmeier MJ. Coronavirus spike proteins in viral entry and pathogenesis. Virology. 2001; 279(2):371–4. https://doi.org/10.1006/viro.2000.0757 PMID: 11162792.
34. Hofmann H, Pyrc K, van der Hoek L, Geier M, Berkhout B, Pohlmann S. Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry. Proc Natl Acad Sci U S A. 2005; 102(22):7988–93. https://doi.org/10.1073/pnas.0409465102 PMID: 15897467.
35. Milewska A, Ciejka J, Kaminski K, Karewicz A, Bielska D, Zeglen S, et al. Novel polymeric inhibitors of HCoV-NL63. Antiviral Res. 2013; 97(2):112–21. Epub 2012/11/29. https://doi.org/10.1016/j.antiviral.2012.11.006 PMID: 23201315.
36. Lai ZW, Hanchapola I, Steer DL, Smith AI. Angiotensin-converting enzyme 2 ectodomain shedding cleavage-site identification: determinants and constraints. Biochemistry. 2011; 50(23):5182–94. Epub 2011/05/20. https://doi.org/10.1021/bi200525y PMID: 21563828.
37. Lambert DW, Yarski M, Warner FJ, Thornhill P, Parkin ET, Smith AI, et al. Tumor necrosis factor-alpha convertase (ADAM17) mediates regulated ectodomain shedding of the severe-acute respiratory syndrome-coronavirus (SARS-CoV) receptor, angiotensin-converting enzyme-2 (ACE2). J Biol Chem. 2005; 280(34):30113–9. Epub 2005/06/27. https://doi.org/10.1074/jbc.M505111200 PMID: 15983030.
38. Fernandes F, Teixeira AP, Carinhas N, Carrondo MJ, Alves PM. Insect cells as a production platform of complex virus-like particles. Expert Rev Vaccines. 2013; 12(2):225–36. https://doi.org/10.1586/erv.12. 153 PMID: 23414412.
39. Liu F, Wu X, Li L, Liu Z, Wang Z. Use of baculovirus expression system for generation of virus-like particles: successes and challenges. Protein Expr Purif. 2013; 90(2):104–16. https://doi.org/10.1016/j.pep.2013.05.009 PMID: 23742819.
40. Cavanagh D. Coronavirus IBV glycopolypeptides: size of their polypeptide moieties and nature of their oligosaccharides. J Gen Virol. 1983; 64(Pt 5):1187–91. https://doi.org/10.1099/0022-1317-64-5-1187PMID: 6302214.
41. Niemann H, Geyer R, Klenk HD, Linder D, Stirm S, Wirth M. The carbohydrates of mouse hepatitis virus (MHV) A59: structures of the O-glycosidically linked oligosaccharides of glycoprotein E1. EMBO J. 1984; 3(3):665–70. PMID: 6325180.
42. Lapps W, Hogue BG, Brian DA. Deduced amino acid sequence and potential O-glycosylation sites for the bovine coronavirus matrix protein. Adv Exp Med Biol. 1987; 218:123–9. PMID: 3434434.
43. Hogue BG, Nayak DP. Expression of the porcine transmissible gastroenteritis coronavirus M protein. Adv Exp Med Biol. 1990; 276:121–6. PMID: 1966402.
44. Mounir S, Talbot PJ. Sequence analysis of the membrane protein gene of human coronavirus OC43 and evidence for O-glycosylation. J Gen Virol. 1992; 73 (Pt 10):2731–6. https://doi.org/10.1099/0022-1317-73-10-2731 PMID: 1402806.
45. Hu Y, Wen J, Tang L, Zhang H, Zhang X, Li Y, et al. The M protein of SARS-CoV: basic structural and immunological properties. Genomics Proteomics Bioinformatics. 2003; 1(2):118–30. https://doi.org/10.1016/S1672-0229(03)01016-7 PMID: 15626342.
46. Jouvenne P, Richardson CD, Schreiber SS, Lai MM, Talbot PJ. Sequence analysis of the membrane protein gene of human coronavirus 229E. Virology. 1990; 174(2):608–12. PMID: 2305554.
47. Burden CS, Jin J, Podgornik A, Bracewell DG. A monolith purification process for virus-like particles from yeast homogenate. J Chromatogr B Analyt Technol Biomed Life Sci. 2012; 880(1):82–9. https://doi.org/10.1016/j.jchromb.2011.10.044 PMID: 22134039.
48. Zaveckas M, Snipaitis S, Pesliakas H, Nainys J, Gedvilaite A. Purification of recombinant virus-like particles of porcine circovirus type 2 capsid protein using ion-exchange monolith chromatography. J Chromatogr B Analyt Technol Biomed Life Sci. 2015; 991:21–8. Epub 2015/04/09. https://doi.org/10.1016/j.jchromb.2015.04.004 PMID: 25910233.
49. Urbas L, Jarc BL, Barut M, Zochowska M, Chroboczek J, Pihlar B, et al. Purification of recombinant ade-novirus type 3 dodecahedric virus-like particles for biomedical applications using short monolithic columns. J Chromatogr A. 2011; 1218(17):2451–9. Epub 2011/01/19. https://doi.org/10.1016/j.chroma. 2011.01.032 PMID: 21295784.
50. Milewska A, Zarebski M, Nowak P, Stozek K, Potempa J, Pyrc K. Human coronavirus NL63 utilizes heparan sulfate proteoglycans for attachment to target cells. J Virol. 2014; 88(22):13221–30. https://doi.org/10.1128/JVI.02078-14 PMID: 25187545.
51. Huang Y, Yang ZY, Kong WP, Nabel GJ. Generation of synthetic severe acute respiratory syndrome coronavirus pseudoparticles: implications for assembly and vaccine production. J Virol. 2004; 78 (22):12557–65. https://doi.org/10.1128/JVI.78.22.12557-12565.2004 PMID: 15507643.
52. Lee YN, Chen LK, Ma HC, Yang HH, Li HP, Lo SY. Thermal aggregation of SARS-CoV membrane protein. J Virol Methods. 2005; 129(2):152–61. https://doi.org/10.1016/j.jviromet.2005.05.022 PMID: 16023741.
53. Ujike M, Taguchi F. Incorporation of spike and membrane glycoproteins into coronavirus virions. Viruses. 2015; 7(4):1700–25. Epub 2015/04/03. https://doi.org/10.3390/v7041700 PMID: 25855243.
54. Corse E, Machamer CE. The cytoplasmic tails of infectious bronchitis virus E and M proteins mediate their interaction. Virology. 2003; 312(1):25–34. PMID: 12890618.
55. de Haan CA, Vennema H, Rottier PJ. Assembly of the coronavirus envelope: homotypic interactions between the M proteins. J Virol. 2000; 74(11):4967–78. PMID: 10799570.
56. Kuo L, Koetzner CA, Masters PS. A key role for the carboxy-terminal tail of the murine coronavirus nucleocapsid protein in coordination of genome packaging. Virology. 2016; 494:100–7. Epub 2016/04/ 19. https://doi.org/10.1016/j.virol.2016.04.009 PMID: 27105451.
57. Chen SC, Lo SY, Ma HC, Li HC. Expression and membrane integration of SARS-CoV E protein and its interaction with M protein. Virus Genes. 2009; 38(3):365–71. Epub 2009/03/19. https://doi.org/10.1007/ s11262-009-0341-6 PMID: 19322648.
58. Hsieh YC, Li HC, Chen SC, Lo SY. Interactions between M protein and other structural proteins of severe, acute respiratory syndrome-associated coronavirus. J Biomed Sci. 2008; 15(6):707–17. Epub 2008/09/16. https://doi.org/10.1007/s11373-008-9278-3 PMID: 18792806.
59. Risco C, Antón IM, Suñé C, Pedregosa AM, Martín-Alonso JM, Parra F, et al. Membrane protein molecules of transmissible gastroenteritis coronavirus also expose the carboxy-terminal region on the external surface of the virion. J Virol. 1995; 69(9):5269–77. PMID: 7636969.
60. Steppert P, Burgstaller D, Klausberger M, Tover A, Berger E, Jungbauer A. Quantification and characterization of virus-like particles by size-exclusion chromatography and nanoparticle tracking analysis. J Chromatogr A. 2017; 1487:89–99. Epub 2017/01/04. https://doi.org/10.1016/j.chroma.2016.12.085PMID: 28110946.
61. Ladd Effio C, Oelmeier SA, Hubbuch J. High-throughput characterization of virus-like particles by interlaced size-exclusion chromatography. Vaccine. 2016; 34(10):1259–67. Epub 2016/02/01. https://doi.org/10.1016/j.vaccine.2016.01.035 PMID: 26845741.
62. Szurgot I, Jedynak M, Podsiadla-Bialoskorska M, Piwowarski J, Szolajska E, Chroboczek J. Adenovirus Dodecahedron, a VLP, Can be Purified by Size Exclusion Chromatography Instead of Time-Consuming Sucrose Density Gradient Centrifugation. Mol Biotechnol. 2015; 57(6):565–73. https://doi.org/10.1007/ s12033-015-9850-9 PMID: 25711740.
63. Du P, Sun S, Dong J, Zhi X, Chang Y, Teng Z, et al. Purification of foot-and-mouth disease virus by heparin as ligand for certain strains. J Chromatogr B Analyt Technol Biomed Life Sci. 2017; 1049–1050:16–23. Epub 2016/12/26. https://doi.org/10.1016/j.jchromb.2016.12.033 PMID: 28260627.
64. Liu J, Moon YA. Simple Purification of Adeno-Associated Virus-DJ for Liver-Specific Gene Expression. Yonsei Med J. 2016; 57(3):790–4. https://doi.org/10.3349/ymj.2016.57.3.790 PMID: 26996583.
65. Kim HJ, Lim SJ, Kwag HL. The choice of resin-bound ligand affects the structure and immunogenicity of column-purified human papillomavirus type 16 virus-like particles. PLoS One. 2012; 7(4):e35893. Epub 2012/04/26. https://doi.org/10.1371/journal.pone.0035893 PMID: 22563414.
66. Nasimuzzaman M, Lynn D, van der Loo JC, Malik P. Purification of baculovirus vectors using heparin affinity chromatography. Mol Ther Methods Clin Dev. 2016; 3:16071. Epub 2016/12/07. https://doi.org/10.1038/mtm.2016.71 PMID: 27933303.
67. Yu YT, Chien SC, Chen IY, Lai CT, Tsay YG, Chang SC, et al. Surface vimentin is critical for the cell entry of SARS-CoV. Journal of biomedical science. 2016; 23:14. https://doi.org/10.1186/s12929-016-0234-7 PMID: 26801988.
68. Fender P, Schoehn G, Foucaud-Gamen J, Gout E, Garcel A, Drouet E, et al. Adenovirus dodecahedron allows large multimeric protein transduction in human cells. J Virol. 2003; 77(8):4960–4. https://doi.org/10.1128/JVI.77.8.4960-4964.2003 PMID: 12663801.
69. Bosch BJ, de Haan CA, Rottier PJ. Coronavirus spike glycoprotein, extended at the carboxy terminus with green fluorescent protein, is assembly competent. J Virol. 2004; 78(14):7369–78. https://doi.org/10.1128/JVI.78.14.7369-7378.2004 PMID: 15220410.