Endogenous capsid-forming protein ARC for self-assembling nanoparticle vaccines.
ARC
Immunostimulant
Protein nanoparticles
Self-assembly
Vaccines
Journal
Journal of nanobiotechnology
ISSN: 1477-3155
Titre abrégé: J Nanobiotechnology
Pays: England
ID NLM: 101152208
Informations de publication
Date de publication:
27 Aug 2024
27 Aug 2024
Historique:
received:
13
05
2024
accepted:
13
08
2024
medline:
28
8
2024
pubmed:
28
8
2024
entrez:
27
8
2024
Statut:
epublish
Résumé
The application of nanoscale scaffolds has become a promising strategy in vaccine design, with protein-based nanoparticles offering desirable avenues for the biocompatible and efficient delivery of antigens. Here, we presented a novel endogenous capsid-forming protein, activated-regulated cytoskeleton-associated protein (ARC), which could be engineered through the plug-and-play strategy (SpyCatcher3/SpyTag3) for multivalent display of antigens. Combined with the self-assembly capacity and flexible modularity of ARC, ARC-based vaccines elicited robust immune responses against Mpox or SARS-CoV-2, comparable to those induced by ferritin-based vaccines. Additionally, ARC-based nanoparticles functioned as immunostimulants, efficiently stimulating dendritic cells and facilitating germinal center responses. Even without adjuvants, ARC-based vaccines generated protective immune responses in a lethal challenge model. Hence, this study showed the feasibility of ARC as a novel protein-based nanocarrier for multivalent surface display of pathogenic antigens and demonstrated the potential of exploiting recombinant mammalian retrovirus-like protein as a delivery vehicle for bioactive molecules.
Identifiants
pubmed: 39192264
doi: 10.1186/s12951-024-02767-z
pii: 10.1186/s12951-024-02767-z
doi:
Substances chimiques
COVID-19 Vaccines
0
Capsid Proteins
0
Cytoskeletal Proteins
0
activity regulated cytoskeletal-associated protein
0
Nanovaccines
0
Nerve Tissue Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
513Subventions
Organisme : Beijing Nova Program of Science and Technology
ID : 20220484127
Organisme : National Natural Science Foundation of China
ID : 82171818
Informations de copyright
© 2024. The Author(s).
Références
Smith DM, Simon JK, Baker JR Jr. Applications of nanotechnology for immunology. Nat Rev Immunol. 2013;13(8):592–605.
pubmed: 23883969
pmcid: 7097370
doi: 10.1038/nri3488
Keikha R, Daliri K, Jebali A. The Use of Nanobiotechnology in Immunology and Vaccination. Vaccines (Basel). 2021;9(2).
Mobeen H, Safdar M, Fatima A, Afzal S, Zaman H, Mehdi Z. Emerging applications of nanotechnology in context to immunology: a comprehensive review. Front Bioeng Biotechnol. 2022;10:1024871.
pubmed: 36619389
pmcid: 9815620
doi: 10.3389/fbioe.2022.1024871
Sanchez-Villamil JI, Tapia D, Torres AG. Development of a gold nanoparticle vaccine against Enterohemorrhagic Escherichia coli O157:H7. mBio. 2019;10(4).
Dykman LA. Gold nanoparticles for preparation of antibodies and vaccines against infectious diseases. Expert Rev Vaccines. 2020;19(5):465–77.
pubmed: 32306785
doi: 10.1080/14760584.2020.1758070
Nguyen TL, Choi Y, Kim J. Mesoporous Silica as a versatile platform for Cancer Immunotherapy. Adv Mater. 2019;31(34):e1803953.
pubmed: 30417454
doi: 10.1002/adma.201803953
Wu X, Farooq MA, Li T, Geng T, Kutoka PT, Wang B. Cationic chitosan-modified silica nanoparticles for oral delivery of protein vaccine. J Biomed Mater Res A. 2021;109(11):2111–9.
pubmed: 33871158
doi: 10.1002/jbm.a.37198
Khan MS, Baskoy SA, Yang C, Hong J, Chae J, Ha H, et al. Lipid-based colloidal nanoparticles for applications in targeted vaccine delivery. Nanoscale Adv. 2023;5(7):1853–69.
pubmed: 36998671
pmcid: 10044484
doi: 10.1039/D2NA00795A
Nguyen B, Tolia NH. Protein-based antigen presentation platforms for nanoparticle vaccines. NPJ Vaccines. 2021;6(1):70.
pubmed: 33986287
pmcid: 8119681
doi: 10.1038/s41541-021-00330-7
Tapia D, Reyes-Sandoval A, Sanchez-Villamil JI. Protein-based Nanoparticle Vaccine approaches against Infectious diseases. Arch Med Res. 2023;54(3):168–75.
pubmed: 36894463
doi: 10.1016/j.arcmed.2023.02.003
Nguyen QD, Kikuchi K, Maity B, Ueno T. The versatile manipulations of self-assembled proteins in Vaccine Design. Int J Mol Sci. 2021;22(4).
Morales-Hernández S, Ugidos-Damboriena N, López-Sagaseta J. Self-assembling protein nanoparticles in the design of vaccines: 2022 update. Vaccines (Basel). 2022;10(9).
Nooraei S, Bahrulolum H, Hoseini ZS, Katalani C, Hajizade A, Easton AJ, et al. Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J Nanobiotechnol. 2021;19(1):59.
doi: 10.1186/s12951-021-00806-7
Schiller JT, Lowy DR. Understanding and learning from the success of prophylactic human papillomavirus vaccines. Nat Rev Microbiol. 2012;10(10):681–92.
pubmed: 22961341
pmcid: 6309166
doi: 10.1038/nrmicro2872
Peron JM, Larrue H, Izopet J, Buti M. The pressing need for a global HEV vaccine. J Hepatol. 2023;79(3):876–80.
pubmed: 37003442
doi: 10.1016/j.jhep.2023.03.024
Song N, Zhang J, Zhai J, Hong J, Yuan C, Liang M. Ferritin: a multifunctional nanoplatform for Biological Detection, Imaging diagnosis, and Drug Delivery. Acc Chem Res. 2021;54(17):3313–25.
pubmed: 34415728
doi: 10.1021/acs.accounts.1c00267
Kim BR, Yoon JW, Choi H, Kim D, Kang S, Kim JH. Application of periostin peptide-decorated self-assembled protein cage nanoparticles for therapeutic angiogenesis. BMB Rep. 2022;55(4):175–80.
pubmed: 34814976
pmcid: 9058470
doi: 10.5483/BMBRep.2022.55.4.137
Jones JA, Giessen TW. Advances in encapsulin nanocompartment biology and engineering. Biotechnol Bioeng. 2021;118(1):491–505.
pubmed: 32918485
doi: 10.1002/bit.27564
Tan TK, Rijal P, Rahikainen R, Keeble AH, Schimanski L, Hussain S, et al. A COVID-19 vaccine candidate using SpyCatcher multimerization of the SARS-CoV-2 spike protein receptor-binding domain induces potent neutralising antibody responses. Nat Commun. 2021;12(1):542.
pubmed: 33483491
pmcid: 7822889
doi: 10.1038/s41467-020-20654-7
Obata J, Kawakami N, Tsutsumi A, Nasu E, Miyamoto K, Kikkawa M, et al. Icosahedral 60-meric porous structure of designed supramolecular protein nanoparticle TIP60. Chem Commun (Camb). 2021;57(79):10226–9.
pubmed: 34523636
doi: 10.1039/D1CC03114G
Lu Y, Chan W, Ko BY, VanLang CC, Swartz JR. Assessing sequence plasticity of a virus-like nanoparticle by evolution toward a versatile scaffold for vaccines and drug delivery. Proc Natl Acad Sci U S A. 2015;112(40):12360–5.
pubmed: 26392546
pmcid: 4603490
doi: 10.1073/pnas.1510533112
Zhang J, Yang J, Li Q, Peng R, Fan S, Yi H, et al. Cell activating Thermostable Self-Assembly Nanoscaffold tailored for Cellular Immunity Antigen Delivery. Adv Sci (Weinh). 2023;10(26):e2303049.
pubmed: 37395451
doi: 10.1002/advs.202303049
Segel M, Lash B, Song J, Ladha A, Liu CC, Jin X, et al. Mammalian retrovirus-like protein PEG10 packages its own mRNA and can be pseudotyped for mRNA delivery. Science. 2021;373(6557):882–9.
pubmed: 34413232
pmcid: 8431961
doi: 10.1126/science.abg6155
Zhang W, Wu J, Ward MD, Yang S, Chuang YA, Xiao M, et al. Structural basis of arc binding to synaptic proteins: implications for cognitive disease. Neuron. 2015;86(2):490–500.
pubmed: 25864631
pmcid: 4409568
doi: 10.1016/j.neuron.2015.03.030
Sibarov DA, Tsytsarev V, Volnova A, Vaganova AN, Alves J, Rojas L, et al. Arc protein, a remnant of ancient retrovirus, forms virus-like particles, which are abundantly generated by neurons during epileptic seizures, and affects epileptic susceptibility in rodent models. Front Neurol. 2023;14:1201104.
pubmed: 37483450
pmcid: 10361770
doi: 10.3389/fneur.2023.1201104
Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV, McCormick J, et al. The neuronal Gene Arc encodes a repurposed retrotransposon gag protein that mediates intercellular RNA transfer. Cell. 2018;172(1–2):275–e28818.
pubmed: 29328916
pmcid: 5884693
doi: 10.1016/j.cell.2017.12.024
Eriksen MS, Nikolaienko O, Hallin EI, Grødem S, Bustad HJ, Flydal MI, et al. Arc self-association and formation of virus-like capsids are mediated by an N-terminal helical coil motif. Febs j. 2021;288(9):2930–55.
pubmed: 33175445
doi: 10.1111/febs.15618
Hallin EI, Eriksen MS, Baryshnikov S, Nikolaienko O, Grødem S, Hosokawa T, et al. Structure of monomeric full-length ARC sheds light on molecular flexibility, protein interactions, and functional modalities. J Neurochem. 2018;147(3):323–43.
pubmed: 30028513
doi: 10.1111/jnc.14556
Mao L, Chen Z, Wang Y, Chen C. Design and application of nanoparticles as vaccine adjuvants against human corona virus infection. J Inorg Biochem. 2021;219:111454.
pubmed: 33878530
pmcid: 8007196
doi: 10.1016/j.jinorgbio.2021.111454
Volckmar J, Knop L, Hirsch T, Frentzel S, Erck C, van Ham M et al. Chemical Conjugation of a purified DEC-205-Directed antibody with full-length protein for Targeting Mouse dendritic cells in Vitro and in vivo. J Vis Exp. 2021;(168).
Wang C, Lakshmipriya T, Gopinath SCB. Amine-Aldehyde Chemical conjugation on a potassium hydroxide-treated polystyrene ELISA surface for nanosensing an HIV-p24 Antigen. Nanoscale Res Lett. 2019;14(1):21.
pubmed: 30644016
pmcid: 6331347
doi: 10.1186/s11671-018-2848-z
Caldeira JC, Perrine M, Pericle F, Cavallo F. Virus-like particles as an immunogenic platform for Cancer vaccines. Viruses. 2020;12(5).
Sun XB, Cao JW, Wang JK, Lin HZ, Gao DY, Qian GY, et al. SpyTag/SpyCatcher molecular cyclization confers protein stability and resilience to aggregation. N Biotechnol. 2019;49:28–36.
pubmed: 30572026
doi: 10.1016/j.nbt.2018.12.003
Kellmann SJ, Hentrich C, Putyrski M, Hanuschka H, Cavada M, Knappik A, et al. SpyDisplay: a versatile phage display selection system using SpyTag/SpyCatcher technology. MAbs. 2023;15(1):2177978.
pubmed: 36803166
pmcid: 9980448
doi: 10.1080/19420862.2023.2177978
Lu L, Duong VT, Shalash AO, Skwarczynski M, Toth I. Chemical conjugation strategies for the development of protein-based subunit nanovaccines. Vaccines (Basel). 2021;9(6).
Lichtenstein M, Zabit S, Hauser N, Farouz S, Melloul O, Hirbawi J et al. TAT for Enzyme/Protein delivery to restore or destroy cell activity in Human diseases. Life (Basel). 2021;11(9).
Wu B, Li M, Li K, Hong W, Lv Q, Li Y, et al. Cell penetrating peptide TAT-functionalized liposomes for efficient ophthalmic delivery of flurbiprofen: penetration and its underlying mechanism, retention, anti-inflammation and biocompatibility. Int J Pharm. 2021;598:120405.
pubmed: 33647409
doi: 10.1016/j.ijpharm.2021.120405
Gao Z, He X, Chen G, Fang Y, Meng Z, Tian H et al. The viral protein poly(A) polymerase Catalytic Subunit interacts with guanylate-binding proteins 2 to antagonize the antiviral ability of Targeting Ectromelia Virus. Int J Mol Sci. 2023;24(21).
Butkovich N, Tucker JA, Ramirez A, Li E, Meli VS, Nelson EL, et al. Nanoparticle vaccines can be designed to induce pDC support of mDCs for increased antigen display. Biomater Sci. 2023;11(2):596–610.
pubmed: 36476811
pmcid: 10775882
doi: 10.1039/D2BM01132H
Heath WR, Kato Y, Steiner TM, Caminschi I. Antigen presentation by dendritic cells for B cell activation. Curr Opin Immunol. 2019;58:44–52.
pubmed: 31071588
doi: 10.1016/j.coi.2019.04.003
Reddy ST, van der Vlies AJ, Simeoni E, Angeli V, Randolph GJ, O’Neil CP, et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat Biotechnol. 2007;25(10):1159–64.
pubmed: 17873867
doi: 10.1038/nbt1332
Zhang YN, Lazarovits J, Poon W, Ouyang B, Nguyen LNM, Kingston BR, et al. Nanoparticle size influences Antigen Retention and Presentation in Lymph Node Follicles for Humoral Immunity. Nano Lett. 2019;19(10):7226–35.
pubmed: 31508968
doi: 10.1021/acs.nanolett.9b02834
Ma X, Zou F, Yu F, Li R, Yuan Y, Zhang Y, et al. Nanoparticle vaccines based on the receptor binding domain (RBD) and Heptad repeat (HR) of SARS-CoV-2 Elicit Robust Protective Immune responses. Immunity. 2020;53(6):1315–e13309.
pubmed: 33275896
pmcid: 7687490
doi: 10.1016/j.immuni.2020.11.015
Tai W, Chai B, Feng S, Zhuang X, Ma J, Pang M, et al. Development of a ferritin-based nanoparticle vaccine against the SARS-CoV-2 Omicron variant. Signal Transduct Target Ther. 2022;7(1):173.
pubmed: 35650183
pmcid: 9157036
doi: 10.1038/s41392-022-01041-8
Rodrigues MQ, Alves PM, Roldão A. Functionalizing ferritin nanoparticles for Vaccine Development. Pharmaceutics. 2021;13(10).
Weidenbacher PA, Sanyal M, Friedland N, Tang S, Arunachalam PS, Hu M, et al. A ferritin-based COVID-19 nanoparticle vaccine that elicits robust, durable, broad-spectrum neutralizing antisera in non-human primates. Nat Commun. 2023;14(1):2149.
pubmed: 37069151
pmcid: 10110616
doi: 10.1038/s41467-023-37417-9
Kato Y, Abbott RK, Freeman BL, Haupt S, Groschel B, Silva M, et al. Multifaceted effects of Antigen Valency on B Cell response composition and differentiation in vivo. Immunity. 2020;53(3):548–e5638.
pubmed: 32857950
pmcid: 7451196
doi: 10.1016/j.immuni.2020.08.001
Ols S, Lenart K, Arcoverde Cerveira R, Miranda MC, Brunette N, Kochmann J et al. Multivalent antigen display on nanoparticle immunogens increases B cell clonotype diversity and neutralization breadth to pneumoviruses. Immunity. 482023;56(10):2425–2441.e14.
Oropallo MA, Cerutti A. Germinal center reaction: antigen affinity and presentation explain it all. Trends Immunol. 2014;35(7):287–9.
pubmed: 24934509
pmcid: 4174395
doi: 10.1016/j.it.2014.06.001
Myrum C, Baumann A, Bustad HJ, Flydal MI, Mariaule V, Alvira S, et al. Arc is a flexible modular protein capable of reversible self-oligomerization. Biochem J. 2015;468(1):145–58.
pubmed: 25748042
doi: 10.1042/BJ20141446
Cottee MA, Letham SC, Young GR, Stoye JP, Taylor IA. Structure of Drosophila melanogaster ARC1 reveals a repurposed molecule with characteristics of retroviral gag. Sci Adv. 2020;6(1):eaay6354.
pubmed: 31911950
pmcid: 6938703
doi: 10.1126/sciadv.aay6354
Purdy JG, Flanagan JM, Ropson IJ, Rennoll-Bankert KE, Craven RC. Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J Virol. 2008;82(12):5951–61.
pubmed: 18400856
pmcid: 2395126
doi: 10.1128/JVI.00214-08
Byers CE, Barylko B, Ross JA, Southworth DR, James NG, t Taylor CA, et al. Enhancement of dynamin polymerization and GTPase activity by Arc/Arg3.1. Biochim Biophys Acta. 2015;1850(6):1310–8.
pubmed: 25783003
pmcid: 4398645
doi: 10.1016/j.bbagen.2015.03.002
Irvine DJ, Read BJ. Shaping humoral immunity to vaccines through antigen-displaying nanoparticles. Curr Opin Immunol. 2020;65:1–6.
pubmed: 32200132
pmcid: 7501207
doi: 10.1016/j.coi.2020.01.007
Irvine DJ, Swartz MA, Szeto GL. Engineering synthetic vaccines using cues from natural immunity. Nat Mater. 2013;12(11):978–90.
pubmed: 24150416
pmcid: 3928825
doi: 10.1038/nmat3775
Zheng P, Yang Y, Fu Y, He J, Hu Y, Zheng X, et al. Engineered Norovirus-Derived nanoparticles as a Plug-and-play Cancer Vaccine platform. ACS Nano. 2023;17(4):3412–29.
pubmed: 36779845
doi: 10.1021/acsnano.2c08840
Ji M, Xie XX, Liu DQ, Yu XL, Zhang Y, Zhang LX, et al. Hepatitis B core VLP-based mis-disordered tau vaccine elicits strong immune response and alleviates cognitive deficits and neuropathology progression in Tau.P301S mouse model of Alzheimer’s disease and frontotemporal dementia. Alzheimers Res Ther. 2018;10(1):55.
pubmed: 29914543
pmcid: 6006857
doi: 10.1186/s13195-018-0378-7
Ji M, Xie XX, Liu DQ, Lu S, Zhang LX, Huang YR, Liu RT. Engineered Hepatitis B core virus-like particle carrier for precise and personalized Alzheimer’s disease vaccine preparation via fixed-point coupling. Appl Mater Today. 2020;100575:19.
Lee BR, Ko HK, Ryu JH, Ahn KY, Lee YH, Oh SJ, et al. Engineered Human Ferritin nanoparticles for Direct Delivery of Tumor antigens to Lymph Node and Cancer Immunotherapy. Sci Rep. 2016;6:35182.
pubmed: 27725782
pmcid: 5057094
doi: 10.1038/srep35182
Jeon IS, Yoo JD, Gurung S, Kim M, Lee C, Park EJ, et al. Anticancer nanocage platforms for combined immunotherapy designed to harness immune checkpoints and deliver anticancer drugs. Biomaterials. 2021;270:120685.
pubmed: 33524811
doi: 10.1016/j.biomaterials.2021.120685
Cheng X, Fan K, Wang L, Ying X, Sanders AJ, Guo T, et al. TfR1 binding with H-ferritin nanocarrier achieves prognostic diagnosis and enhances the therapeutic efficacy in clinical gastric cancer. Cell Death Dis. 2020;11(2):92.
pubmed: 32024821
pmcid: 7002446
doi: 10.1038/s41419-020-2272-z
Zhang Q, Chen J, Shen J, Chen S, Liang K, Wang H, et al. Inlaying Radiosensitizer onto the Polypeptide Shell of Drug-Loaded Ferritin for Imaging and Combinational Chemo-Radiotherapy. Theranostics. 2019;9(10):2779–90.
pubmed: 31244922
pmcid: 6568179
doi: 10.7150/thno.33472