Immunogenic Properties of MVs Containing Structural Hantaviral Proteins: An Original Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells
2.2. Animals
2.3. PUUV Peptides
2.4. Flow Cytometry
2.5. Recombinant Lentivirus
2.6. Transduction
2.7. MVs Production
2.8. Transmission Electron Microscopy (TEM)
2.9. Protein Concentration Analysis
2.10. Multiplex Analysis
2.11. Cell Treatment with MVs
2.12. Western Blot
2.13. Immunofluorescence Assay (IFA)
2.14. Enzyme-Linked Immunosorbent Assay (ELISA)
2.15. ELISpot Assay
2.16. Statistical Analysis
3. Results
3.1. Immunophenotype of mMSCs
3.2. TEM Analysis of MVs Size and Structure
3.3. Western Blot Analysis of MVs
3.4. Cytokines Released by Genetically Modified mMSCs
3.5. Analysis of Cytokines in Cargo of Genetically Modified mMSCs
3.6. Analysis of PUUV N and Gn/Gc Proteins Expression in A549 Cells Treated with MVs
3.7. Serum Anti-PUUV Antibodies
3.8. Cytotoxic T-Cell Activation
3.9. Serum Cytokine Analysis
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fulhorst, C.F.; Koster, F.T.; Enría, D.A.; Peters, C.J. CHAPTER 71—Hantavirus Infections. In Tropical Infectious Diseases: Principles, Pathogens and Practice, 3rd ed.; Guerrant, R.L., Walker, D.H., Weller, P.F., Eds.; W.B. Saunders: Edinburgh, UK, 2011; pp. 470–480. [Google Scholar] [CrossRef]
- Tkachenko, E.A.; Ishmukhametov, A.A.; Dzagurova, T.K.; Bernshtein, A.D.; Morozov, V.G.; Siniugina, A.A.; Kurashova, S.S.; Balkina, A.S.; Tkachenko, P.E.; Kruger, D.H.; et al. Hemorrhagic Fever with Renal Syndrome, Russia. Emerg. Infect. Dis. 2019, 25, 2325–2328. [Google Scholar] [CrossRef]
- Garanina, E.; Martynova, E.; Davidyuk, Y.; Kabwe, E.; Ivanov, K.; Titova, A.; Markelova, M.; Zhuravleva, M.; Cherepnev, G.; Shakirova, V.G.; et al. Cytokine Storm Combined with Humoral Immune Response Defect in Fatal Hemorrhagic Fever with Renal Syndrome Case, Tatarstan, Russia. Viruses 2019, 11, 601. [Google Scholar] [CrossRef] [Green Version]
- Khismatullina, N.A.; Karimov, M.M.; Khaertynov, K.S.; Shuralev, E.A.; Morzunov, S.P.; Khaertynova, I.M.; Ivanov, A.A.; Milova, I.V.; Khakimzyanova, M.B.; Sayfullina, G.; et al. Epidemiological dynamics of nephropathia epidemica in the Republic of Tatarstan, Russia, during the period of 1997–2013. Epidemiol. Infect. 2016, 144, 618–626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Federal Service for Surveillance on Consumer Rights Protection and Human Welfare. On the State of Sanitary and Epidemiological Well-Being of the Population in the Russian Federation in 2020. 2021. Available online: https://www.rospotrebnadzor.ru/upload/iblock/5fa/gd-seb_02.06-_s-podpisyu_.pdf (accessed on 12 December 2021).
- Shakirova, V.; Martynova, E.; Saubanova, A.; Khaertynova, I.; Khaybullina, S.; Garanina, E. Analysis of markers of renal damage in patients with hantaan hemorrhagic fever. Pract. Med. 2019, 17, 97–102. [Google Scholar] [CrossRef]
- Podkopay, A.V.; Kruglov, E.E.; Myakisheva, Y.V.; Segodina, A.V.; Lomakin, D.N.; Redkozubov, A.A.; Gavrilov, I.N. Clinical, laboratory and epidemiological features of hemorrhagic fever with renal syndrome in pacients from organized collectives in the Middle Volga region, Astrakhan. Med. J. 2021, 16, 47–56. Available online: https://cyberleninka.ru/article/n/klinicheskie-laboratornye-i-epidemiologicheskie-sobennosti-techeniya-gemorragicheskoy-lihoradki-s-pochechnym-sindromom-u-patsientov (accessed on 12 December 2021).
- Liu, R.; Ma, H.; Shu, J.; Zhang, Q.; Han, M.; Liu, Z.; Jin, X.; Zhang, F.; Wu, X. Vaccines and Therapeutics Against Hantaviruses. Front. Microbiol. 2020, 10, 2989. [Google Scholar] [CrossRef] [Green Version]
- Dheerasekara, K.; Sumathipala, S.; Muthugala, R. Hantavirus Infections—Treatment and Prevention. Curr. Treat. Options Infect. Dis. 2020, 12, 410–421. [Google Scholar] [CrossRef]
- Davidyuk, Y.N.; Kabwe, E.; Shakirova, V.G.; Martynova, E.V.; Ismagilova, R.K.; Khaertynova, I.M.; Khaiboullina, S.F.; Rizvanov, A.A.; Morzunov, S.P. Characterization of the Puumala orthohantavirus Strains in the Northwestern Region of the Republic of Tatarstan in Relation to the Clinical Manifestations in Hemorrhagic Fever With Renal Syndrome Patients. Front. Pharmacol. 2019, 10, 10. [Google Scholar] [CrossRef]
- Guardado-Calvo, P.; Rey, F.A. The Envelope Proteins of the Bunyavirales. Adv. Virus Res. 2017, 98, 83–118. [Google Scholar] [CrossRef]
- Mir, M.A. Hantaviruses. Clin. Lab. Med. 2010, 30, 67–91. [Google Scholar] [CrossRef]
- Laenen, L.; Vergote, V.; Calisher, C.H.; Klempa, B.; Klingström, J.; Kuhn, J.H.; Maes, P. Hantaviridae: Current Classification and Future Perspectives. Viruses 2019, 11, 788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, D.B.; Zhang, J.P.; Cheng, L.F.; Zhang, G.W.; Li, Y.; Li, Z.C.; Lu, Z.H.; Zhang, Z.X.; Lu, Y.C.; Zheng, L.H.; et al. Hantavirus Gc induces long-term immune protection via LAMP-targeting DNA vaccine strategy. Antivir. Res. 2018, 150, 174–182. [Google Scholar] [CrossRef]
- Slough, M.M.; Chandran, K.; Jangra, R.K. Two Point Mutations in Old World Hantavirus Glycoproteins Afford the Generation of Highly Infectious Recombinant Vesicular Stomatitis Virus Vectors. mBio 2019, 10, e02372–e02381. [Google Scholar] [CrossRef] [PubMed]
- Whitt, M.A. Generation of VSV pseudotypes using recombinant ΔG-VSV for studies on virus entry, identification of entry inhibitors, and immune responses to vaccines. J. Virol. Methods 2010, 169, 365–374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geldmacher, A.; Skrastina, D.; Borisova, G.; Petrovskis, I.; Krüger, D.H.; Pumpens, P.; Ulrich, R. A hantavirus nucleocapsid protein segment exposed on hepatitis B virus core particles is highly immunogenic in mice when applied without adjuvants or in the presence of pre-existing anti-core antibodies. Vaccine 2005, 23, 3973–3983. [Google Scholar] [CrossRef]
- Ying, Q.; Ma, T.; Cheng, L.; Zhang, X.; Truax, A.D.; Ma, R.; Liu, Z.; Lei, Y.; Zhang, L.; Ye, W.; et al. Construction and immunological characterization of CD40L or GM-CSF incorporated Hantaan virus like particle. Oncotarget 2016, 7, 63488–63503. [Google Scholar] [CrossRef]
- Dong, Y.; Ma, T.; Zhang, X.; Ying, Q.; Han, M.; Zhang, M.; Yang, R.; Li, Y.; Wang, F.; Liu, R.; et al. Incorporation of CD40 ligand or granulocyte-macrophage colony stimulating factor into Hantaan virus (HTNV) virus-like particles significantly enhances the long-term immunity potency against HTNV infection. J. Med. Microbiol. 2019, 68, 480–492. [Google Scholar] [CrossRef] [PubMed]
- Geldmacher, A.; Skrastina, D.; Petrovskis, I.; Borisova, G.; Berriman, J.A.; Roseman, A.M.; Crowther, R.A.; Fischer, J.; Musema, S.; Gelderblom, H.R.; et al. An amino-terminal segment of hantavirus nucleocapsid protein presented on hepatitis B virus core particles induces a strong and highly cross-reactive antibody response in mice. Virology 2004, 323, 108–119. [Google Scholar] [CrossRef]
- Schmaljohn, C.S.; Chu, Y.K.; Schmaljohn, A.L.; Dalrymple, J.M. Antigenic subunits of Hantaan virus expressed by baculovirus and vaccinia virus recombinants. J. Virol. 1990, 64, 3162–3170. [Google Scholar] [CrossRef] [Green Version]
- Lundkvist, A.; Kallio-Kokko, H.; Sjölander, K.B.; Lankinen, H.; Niklasson, B.; Vaheri, A.; Vapalahti, O. Characterization of Puumala virus nucleocapsid protein: Identification of B-cell epitopes and domains involved in protective immunity. Virology 1996, 216, 397–406. [Google Scholar] [CrossRef] [Green Version]
- Maes, P.; Clement, J.; Cauwe, B.; Bonnet, V.; Keyaerts, E.; Robert, A.; Van Ranst, M. Truncated recombinant puumala virus nucleocapsid proteins protect mice against challenge in vivo. Viral Immunol. 2008, 21, 49–60. [Google Scholar] [CrossRef] [Green Version]
- Cho, H.W.; Howard, C.R.; Lee, H.W. Review of an inactivated vaccine against hantaviruses. Intervirology 2002, 45, 328–333. [Google Scholar] [CrossRef]
- Sohn, Y.M.; Rho, H.O.; Park, M.S.; Kim, J.S.; Summers, P.L. Primary humoral immune responses to formalin inactivated hemorrhagic fever with renal syndrome vaccine (Hantavax): Consideration of active immunization in South Korea. Yonsei Med. J. 2001, 42, 278–284. [Google Scholar] [CrossRef]
- .Cho, H.-W.; Howard, C.R. Antibody responses in humans to an inactivated hantavirus vaccine (Hantavax®). Vaccine 1999, 17, 2569–2575. [Google Scholar] [CrossRef]
- Schmaljohn, C. Vaccines for hantaviruses. Vaccine 2009, 27 (Suppl. S4), D61–D64. [Google Scholar] [CrossRef] [PubMed]
- Sinyugina, A.; Dzagurova, T.; Ishmukhametov, A.; Balovneva, M.; Kurashova, S.; Korotina, N.; Egorova, M.; Tkachenko, E. Pre-Clinical Studies of Inactivated Polivalent Vaccine Against Hemorrhagic Fever with Renal Syndrome. Epidemiol. Vaccinal Prev. 2019, 18, 52–58. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Zeng, H.; Wang, Y.; Zhang, Y.; Cheng, L.; Zhang, F.; Lei, Y.; Jin, B.; Ma, Y.; Chen, L. The assessment of Hantaan virus-specific antibody responses after the immunization program for hemorrhagic fever with renal syndrome in northwest China. Hum. Vaccines Immunother. 2017, 13, 802–807. [Google Scholar] [CrossRef] [Green Version]
- Xiao, D.; Wu, K.; Tan, X.; Yan, T.; Li, H.; Yan, Y. The impact of the vaccination program for hemorrhagic fever with renal syndrome in Hu County, China. Vaccine 2014, 32, 740–745. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Zhou, B.Y.; Wei, J.; Xu, Y.; Dong, J.H.; Guan, L.Y.; Ma, P.; Yu, P.B.; Wang, J.J. Persistence of immune responses to vaccine against haemorrhagic fever with renal syndrome in healthy adults aged 16-60 years: Results from an open-label2-year follow-up study. Infect. Dis. 2018, 50, 21–26. [Google Scholar] [CrossRef]
- Yi, Y.; Park, H.; Jung, J. Effectiveness of inactivated hantavirus vaccine on the disease severity of hemorrhagic fever with renal syndrome. Kidney Res. Clin. Pract. 2018, 37, 366–372. [Google Scholar] [CrossRef] [Green Version]
- Dzagurova, T.K.; Siniugina, A.A.; Ishmukhametov, A.A.; Egorova, M.S.; Kurashova, S.S.; Balovneva, M.V.; Deviatkin, A.A.; Tkachenko, P.E.; Leonovich, O.A.; Tkachenko, E.A. Pre-Clinical Studies of Inactivated Polyvalent HFRS Vaccine. Front. Cell Infect. Microbiol. 2020, 10, 545372. [Google Scholar] [CrossRef]
- Abdulla, F.; Nain, Z.; Hossain, M.M.; Syed, S.B.; Khan, M.S.A.; Adhikari, U.K. A comprehensive screening of the whole proteome of hantavirus and designing a multi-epitope subunit vaccine for cross-protection against hantavirus: Structural vaccinology and immunoinformatics study. Microb. Pathog. 2021, 150, 104705. [Google Scholar] [CrossRef] [PubMed]
- Ma, Y.; Tang, K.; Zhang, Y.; Zhang, C.; Zhang, Y.; Jin, B.; Ma, Y. Design and synthesis of HLA-A*02-restricted Hantaan virus multiple-antigenic peptide for CD8+ T cells. Virol. J. 2020, 17, 15. [Google Scholar] [CrossRef] [PubMed]
- Schmaljohn, C.S.; Spik, K.W.; Hooper, J.W. DNA vaccines for HFRS: Laboratory and clinical studies. Virus Res. 2014, 187, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Hooper, J.W.; Kamrud, K.I.; Elgh, F.; Custer, D.; Schmaljohn, C.S. DNA vaccination with hantavirus M segment elicits neutralizing antibodies and protects against seoul virus infection. Virology 1999, 255, 269–278. [Google Scholar] [CrossRef] [PubMed]
- Kwilas, S.; Kishimori, J.M.; Josleyn, M.; Jerke, K.; Ballantyne, J.; Royals, M.; Hooper, J.W. A hantavirus pulmonary syndrome (HPS) DNA vaccine delivered using a spring-powered jet injector elicits a potent neutralizing antibody response in rabbits and nonhuman primates. Curr. Gene Ther. 2014, 14, 200–210. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Y.; Wei, J.; Zhou, B.Y.; Xu, Y.; Dong, J.H.; Guan, L.Y.; Ma, P.; Yu, P.B.; Wang, J.J. Long-term persistence of anti-hantavirus antibodies in sera of patients undergoing hemorrhagic fever with renal syndrome and subjects vaccinated against the disease. Infect. Dis. 2016, 48, 262–266. [Google Scholar] [CrossRef] [PubMed]
- Morozov, V.; Ishmukhametov, A.; Dzagurova, T.; Tkachenko, E. Clinical manifestations of hemorrhagic fever with renal syndrome in Russia. Med. Counc. 2017, 5, 156–161. [Google Scholar] [CrossRef]
- Valdivieso, F.; Vial, P.; Ferres, M.; Ye, C.; Goade, D.; Cuiza, A.; Hjelle, B. Neutralizing antibodies in survivors of Sin Nombre and Andes hantavirus infection. Emerg. Infect. Dis. 2006, 12, 166–168. [Google Scholar] [CrossRef]
- Hörling, J.; Lundkvist, A.; Huggins, J.W.; Niklasson, B. Antibodies to Puumala virus in humans determined by neutralization test. J. Virol. Methods 1992, 39, 139–147. [Google Scholar] [CrossRef]
- Alexeyev, O.; Elgh, F.; Zhestkov, A.; Wadell, G.; Juto, P. Hantaan and Puumala virus antibodies in blood donors in Samara, an HFRS-endemic region in European Russia. Lancet 1996, 347, 1483. [Google Scholar] [CrossRef]
- Xiong, H.R.; Li, Q.; Chen, W.; Liu, D.Y.; Ling, J.X.; Liu, J.; Liu, Y.J.; Zhang, Y.; Yang, Z.Q. Specific humoral reaction of hemorrhagic fever with renal syndrome (HFRS) patients in China to recombinant nucleocapsid proteins from European hantaviruses. Eur. J. Clin. Microbiol. Infect. Dis. 2011, 30, 645–651. [Google Scholar] [CrossRef]
- Miettinen, M.H.; Makela, S.M.; Ala-Houhala, I.O.; Huhtala, H.S.; Koobi, T.; Vaheri, A.I.; Pasternack, A.I.; Porsti, I.H.; Mustonen, J.T. Tubular proteinuria and glomerular filtration 6 years after puumala hantavirus-induced acute interstitial nephritis. Nephron Clin. Pract. 2009, 112, c115–c120. [Google Scholar] [CrossRef]
- Pimenov, L.T.; Dudarev, M.V.; Vasil’ev, M. Arterial hypertension, its metabolic aspects and kidney function in patients after hemorrhagic fever with renal syndrome. Terapevticheskii Arkhiv 2003, 75, 28–31. [Google Scholar]
- Shkair, L.; Garanina, E.E.; Stott, R.J.; Foster, T.L.; Rizvanov, A.A.; Khaiboullina, S.F. Membrane Microvesicles as Potential Vaccine Candidates. Int. J. Mol. Sci. 2021, 22, 1142. [Google Scholar] [CrossRef]
- Zani-Ruttenstock, E.; Antounians, L.; Khalaj, K.; Figueira, R.L.; Zani, A. The Role of Exosomes in the Treatment, Prevention, Diagnosis, and Pathogenesis of COVID-19. Eur. J. Pediatr. Surg. 2021, 31, 326–334. [Google Scholar] [CrossRef]
- Pap, E.; Pállinger, É.; Pásztói, M.; Falus, A. Highlights of a new type of intercellular communication: Microvesicle-based information transfer. Inflamm. Res. 2009, 58, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Algarni, A.; Greenman, J.; Madden, L.A. Procoagulant tumor microvesicles attach to endothelial cells on biochips under microfluidic flow. Biomicrofluidics 2019, 13, 064124. [Google Scholar] [CrossRef]
- Ratajczak, M.Z.; Ratajczak, J. Extracellular microvesicles/exosomes: Discovery, disbelief, acceptance, and the future? Leukemia 2020, 34, 3126–3135. [Google Scholar] [CrossRef] [PubMed]
- Stahl, P.D.; Raposo, G. Extracellular Vesicles: Exosomes and Microvesicles, Integrators of Homeostasis. Physiology 2019, 34, 169–177. [Google Scholar] [CrossRef] [PubMed]
- Armstrong, J.P.K.; Stevens, M.M. Strategic design of extracellular vesicle drug delivery systems. Adv. Drug Deliv. Rev. 2018, 130, 12–16. [Google Scholar] [CrossRef]
- Armstrong, J.P.K.; Holme, M.N.; Stevens, M.M. Re-Engineering Extracellular Vesicles as Smart Nanoscale Therapeutics. ACS Nano 2017, 11, 69–83. [Google Scholar] [CrossRef] [Green Version]
- Mehanny, M.; Koch, M.; Lehr, C.M.; Fuhrmann, G. Streptococcal Extracellular Membrane Vesicles Are Rapidly Internalized by Immune Cells and Alter Their Cytokine Release. Front. Immunol. 2020, 11, 80. [Google Scholar] [CrossRef] [PubMed]
- Gerritzen, M.J.H.; Martens, D.E.; Wijffels, R.H.; van der Pol, L.; Stork, M. Bioengineering bacterial outer membrane vesicles as vaccine platform. Biotechnol. Adv. 2017, 35, 565–574. [Google Scholar] [CrossRef] [PubMed]
- O’Dwyer Clíona, A.; Reddin, K.; Martin, D.; Stephen, C.T.; Gorringe, R.A.; Hudson, J.M.; Brodeur, R.B.; Langford, R.P.; Kroll, J.S. Expression of Heterologous Antigens in Commensal Neisseria spp.: Preservation of Conformational Epitopes with Vaccine Potential. Infect. Immun. 2004, 72, 6511–6518. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rappazzo, C.G.; Watkins, H.C.; Guarino, C.M.; Chau, A.; Lopez, J.L.; DeLisa, M.P.; Leifer, C.A.; Whittaker, G.R.; Putnam, D. Recombinant M2e outer membrane vesicle vaccines protect against lethal influenza A challenge in BALB/c mice. Vaccine 2016, 34, 1252–1258. [Google Scholar] [CrossRef] [Green Version]
- Carvalho, A.L.; Miquel-Clopés, A.; Wegmann, U.; Jones, E.; Stentz, R.; Telatin, A.; Walker, N.J.; Butcher, W.A.; Brown, P.J.; Holmes, S.; et al. Use of bioengineered human commensal gut bacteria-derived microvesicles for mucosal plague vaccine delivery and immunization. Clin. Exp. Immunol. 2019, 196, 287–304. [Google Scholar] [CrossRef] [Green Version]
- Bishop, A.L.; Tarique, A.A.; Patimalla, B.; Calderwood, S.B.; Qadri, F.; Camilli, A. Immunization of Mice With Vibrio cholerae Outer-Membrane Vesicles Protects Against Hyperinfectious Challenge and Blocks Transmission. J. Infect. Dis. 2012, 205, 412–421. [Google Scholar] [CrossRef] [Green Version]
- Sung, J.H.; Yang, H.M.; Park, J.B.; Choi, G.S.; Joh, J.W.; Kwon, C.H.; Chun, J.M.; Lee, S.K.; Kim, S.J. Isolation and characterization of mouse mesenchymal stem cells. Transplant. Proc. 2008, 40, 2649–2654. [Google Scholar] [CrossRef]
- Gomzikova, M.O.; Aimaletdinov, A.M.; Bondar, O.V.; Starostina, I.G.; Gorshkova, N.V.; Neustroeva, O.A.; Kletukhina, S.K.; Kurbangaleeva, S.V.; Vorobev, V.V.; Garanina, E.E.; et al. Immunosuppressive properties of cytochalasin B-induced membrane vesicles of mesenchymal stem cells: Comparing with extracellular vesicles derived from mesenchymal stem cells. Sci. Rep. 2020, 10, 10740. [Google Scholar] [CrossRef]
- Gomzikova, M.O.; Kletukhina, S.K.; Kurbangaleeva, S.V.; Neustroeva, O.A.; Vasileva, O.S.; Garanina, E.E.; Khaiboullina, S.F.; Rizvanov, A.A. Mesenchymal Stem Cell Derived Biocompatible Membrane Vesicles Demonstrate Immunomodulatory Activity Inhibiting Activation and Proliferation of Human Mononuclear Cells. Pharmaceutics 2020, 12, 577. [Google Scholar] [CrossRef]
- Takahashi, A.; Nakajima, H.; Uchida, K.; Takeura, N.; Honjoh, K.; Watanabe, S.; Kitade, M.; Kokubo, Y.; Johnson, W.E.B.; Matsumine, A. Comparison of Mesenchymal Stromal Cells Isolated from Murine Adipose Tissue and Bone Marrow in the Treatment of Spinal Cord Injury. Cell Transplant. 2018, 27, 1126–1139. [Google Scholar] [CrossRef] [Green Version]
- Pick, H.; Schmid, E.L.; Tairi, A.P.; Ilegems, E.; Hovius, R.; Vogel, H. Investigating cellular signaling reactions in single attoliter vesicles. J. Am. Chem. Soc. 2005, 127, 2908–2912. [Google Scholar] [CrossRef] [PubMed]
- Gomzikova, M.O.; Zhuravleva, M.N.; Miftakhova, R.R.; Arkhipova, S.S.; Evtugin, V.G.; Khaiboullina, S.F.; Kiyasov, A.P.; Persson, J.L.; Mongan, N.P.; Pestell, R.G.; et al. Cytochalasin B-induced membrane vesicles convey angiogenic activity of parental cells. Oncotarget 2017, 8, 70496–70507. [Google Scholar] [CrossRef] [PubMed]
- Panagioti, E.; Klenerman, P.; Lee, L.N.; van der Burg, S.H.; Arens, R. Features of Effective T Cell-Inducing Vaccines against Chronic Viral Infections. Front. Immunol. 2018, 9, 276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bertoletti, A.; Le Bert, N.; Qui, M.; Tan, A.T. SARS-CoV-2-specific T cells in infection and vaccination. Cell. Mol. Immunol. 2021, 18, 2307–2312. [Google Scholar] [CrossRef] [PubMed]
- Klingström, J.; Smed-Sörensen, A.; Maleki, K.T.; Solà-Riera, C.; Ahlm, C.; Björkström, N.K.; Ljunggren, H.G. Innate and adaptive immune responses against human Puumala virus infection: Immunopathogenesis and suggestions for novel treatment strategies for severe hantavirus-associated syndromes. J. Intern. Med. 2019, 285, 510–523. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, X.; Peng, H.; Tian, Z. Innate lymphoid cell memory. Cell. Mol. Immunol. 2019, 16, 423–429. [Google Scholar] [CrossRef]
- Brillantes, M.; Beaulieu, A.M. Memory and Memory-Like NK Cell Responses to Microbial Pathogens. Front. Cell. Infect. Microbiol. 2020, 10, 102. [Google Scholar] [CrossRef]
- Arango Duque, G.; Descoteaux, A. Macrophage Cytokines: Involvement in Immunity and Infectious Diseases. Front. Immunol. 2014, 5, 491. [Google Scholar] [CrossRef] [Green Version]
- Acharya, D.; Li, X.R.; Heineman, R.E.-S.; Harrison, R.E. Complement Receptor-Mediated Phagocytosis Induces Proinflammatory Cytokine Production in Murine Macrophages. Front. Immunol. 2020, 10, 10. [Google Scholar] [CrossRef] [PubMed]
- Ratthé, C.; Ennaciri, J.; Garcês Gonçalves, D.M.; Chiasson, S.; Girard, D. Interleukin (IL)-4 Induces Leukocyte Infiltration In Vivo by an Indirect Mechanism. Mediat. Inflamm. 2009, 2009, 193970. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fagundes, D.L.G.; França, E.L.; Morceli, G.; Rudge, M.V.C.; Calderon, I.d.M.P.; Honorio-França, A.C. The Role of Cytokines in the Functional Activity of Phagocytes in Blood and Colostrum of Diabetic Mothers. Clin. Dev. Immunol. 2013, 2013, 590190. [Google Scholar] [CrossRef] [PubMed]
- Jonsson, C.B.; Figueiredo, L.T.M.; Vapalahti, O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 2010, 23, 412–441. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bi, X.; Yi, S.; Zhang, A.; Zhao, Z.; Liu, Y.; Zhang, C.; Ye, Z. Epidemiology of hemorrhagic fever with renal syndrome in Tai’an area. Sci. Rep. 2021, 11, 11596. [Google Scholar] [CrossRef]
- He, X.; Wang, S.; Huang, X.; Wang, X. Changes in age distribution of hemorrhagic fever with renal syndrome: An implication of China’s expanded program of immunization. BMC Public Health 2013, 13, 394. [Google Scholar] [CrossRef] [Green Version]
- Liang, W.; Gu, X.; Li, X.; Zhang, K.; Wu, K.; Pang, M.; Dong, J.; Merrill, H.; Hu, T.; Liu, K.; et al. Mapping the epidemic changes and risks of hemorrhagic fever with renal syndrome in Shaanxi Province, China, 2005–2016. Sci. Rep. 2018, 8, 1–10. [Google Scholar] [CrossRef] [Green Version]
- She, K.; Li, C.; Qi, C.; Liu, T.; Jia, Y.; Zhu, Y.; Liu, L.; Wang, Z.; Zhang, Y.; Li, X. Epidemiological Characteristics and Regional Risk Prediction of Hemorrhagic Fever with Renal Syndrome in Shandong Province, China. Int. J. Environ. Res. Public Health 2021, 18, 8495. [Google Scholar] [CrossRef]
- Mofijur, M.; Fattah, I.M.R.; Alam, M.A.; Islam, A.B.M.S.; Ong, H.C.; Rahman, S.M.A.; Najafi, G.; Ahmed, S.F.; Uddin, M.A.; Mahlia, T.M.I. Impact of COVID-19 on the social, economic, environmental and energy domains: Lessons learnt from a global pandemic. Sustain. Prod. Consum. 2021, 26, 343–359. [Google Scholar] [CrossRef]
- Jiang, H.; Du, H.; Wang, L.M.; Wang, P.Z.; Bai, X.F. Hemorrhagic Fever with Renal Syndrome: Pathogenesis and Clinical Picture. Front. Cell. Infect. Microbiol. 2016, 6, 1. [Google Scholar] [CrossRef] [Green Version]
- Price, N.L.; Goyette-Desjardins, G.; Nothaft, H.; Valguarnera, E.; Szymanski, C.M.; Segura, M.; Feldman, M.F. Glycoengineered Outer Membrane Vesicles: A Novel Platform for Bacterial Vaccines. Sci. Rep. 2016, 6, 24931. [Google Scholar] [CrossRef]
- Sedaghat, M.; Siadat, S.D.; Mirabzadeh, E.; Keramati, M.; Vaziri, F.; Shafiei, M.; Shahcheraghi, F. Evaluation of antibody responses to outer membrane vesicles (OMVs) and killed whole cell of Vibrio cholerae O1 El Tor in immunized mice. Iran J. Microbiol. 2019, 11, 212–219. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Yu, J.; Kadungure, T.; Beyene, J.; Zhang, H.; Lu, Q. ARMMs as a versatile platform for intracellular delivery of macromolecules. Nat. Commun. 2018, 9, 960. [Google Scholar] [CrossRef] [PubMed]
- Fuhrmann, G.; Chandrawati, R. Engineering Extracellular Vesicles with the Tools of Enzyme Prodrug Therapy. Adv. Mater. 2018, 30, e1706616. [Google Scholar] [CrossRef]
- Pieragostino, D.; Lanuti, P.; Cicalini, I.; Cufaro, M.C.; Ciccocioppo, F.; Ronci, M.; Simeone, P.; Onofrj, M.; van der Pol, E.; Fontana, A.; et al. Proteomics characterization of extracellular vesicles sorted by flow cytometry reveals a disease-specific molecular cross-talk from cerebrospinal fluid and tears in multiple sclerosis. J. Proteom. 2019, 204, 103403. [Google Scholar] [CrossRef] [PubMed]
- Saint-Pol, J.; Gosselet, F. Targeting and Crossing the Blood-Brain Barrier with Extracellular Vesicles. Cells 2020, 9, 851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ito, S.; Nakamura, J.; Fukuta, M.; Ura, T.; Teshigawara, T.; Fukushima, J.; Mizuki, N.; Okuda, K.; Shimada, M. Prophylactic and therapeutic vaccine against Pseudomonas aeruginosa keratitis using bacterial membrane vesicles. Vaccine 2021, 39, 3152–3160. [Google Scholar] [CrossRef] [PubMed]
- Kimura, A.; Toneatto, D.; Kleinschmidt, A.; Wang, H.; Dull, P. Immunogenicity and Safety of a Multicomponent Meningococcal Serogroup B Vaccine and a Quadrivalent Meningococcal CRM 197 Conjugate Vaccine against Serogroups A, C, W-135, and Y in Adults Who Are at Increased Risk for Occupational Exposure to Meningococcal Isolates. Clin. Vaccine Immunol. 2011, 18, 483–486. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirayama, S.; Nakao, R. Intranasal Vaccine Study Using Porphyromonas gingivalis Membrane Vesicles: Isolation Method and Application to a Mouse Model. Methods Mol. Biol. 2021, 2210, 157–166. [Google Scholar] [CrossRef]
- Watkins, H.C.; Rappazzo, C.G.; Higgins, J.S.; Sun, X.; Brock, N.; Chau, A.; Misra, A.; Cannizzo, J.P.B.; King, M.R.; Maines, T.R.; et al. Safe Recombinant Outer Membrane Vesicles that Display M2e Elicit Heterologous Influenza Protection. Mol. Ther. 2017, 25, 989–1002. [Google Scholar] [CrossRef] [Green Version]
- Ma, Y.; Tang, K.; Zhang, Y.; Zhang, C.; Cheng, L.; Zhang, F.; Zhuang, R.; Jin, B.; Zhang, Y. Protective CD8+ T-cell response against Hantaan virus infection induced by immunization with designed linear multi-epitope peptides in HLA-A2.1/Kb transgenic mice. Virol. J. 2020, 17, 146. [Google Scholar] [CrossRef] [PubMed]
- Rowland-Jones, S.; Dong, T.; Krausa, P.; Sutton, J.; Newell, H.; Ariyoshi, K.; Gotch, F.; Sabally, S.; Corrah, T.; Kimani, J.; et al. The role of cytotoxic T-cells in HIV infection. Dev. Biol. Stand. 1998, 92, 209–214. [Google Scholar] [PubMed]
- Ito, H.; Seishima, M. Regulation of the Induction and Function of Cytotoxic T Lymphocytes by Natural Killer T Cell. J. Biomed. Biotechnol. 2010, 2010, 641757. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Epps, H.L.; Terajima, M.; Mustonen, J.; Arstila, T.P.; Corey, E.A.; Vaheri, A.; Ennis, F.A. Long-lived memory T lymphocyte responses after hantavirus infection. J. Exp. Med. 2002, 196, 579–588. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tuuminen, T.; Kekäläinen, E.; Mäkelä, S.; Ala-Houhala, I.; Ennis, F.A.; Hedman, K.; Mustonen, J.; Vaheri, A.; Arstila, T.P. Human CD8+ T Cell Memory Generation in Puumala Hantavirus Infection Occurs after the Acute Phase and Is Associated with Boosting of EBV-Specific CD8+ Memory T Cells. J. Immunol. 2007, 179, 1988. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rose-John, S.; Winthrop, K.; Calabrese, L. The role of IL-6 in host defence against infections: Immunobiology and clinical implications. Nat. Rev. Rheumatol. 2017, 13, 399–409. [Google Scholar] [CrossRef] [PubMed]
- Repeke, C.E.; Garlet, T.P.; Francisconi, C.F.; Broll, D.; Trombone, A.P.F.; Garlet, G.P. CCL3. In Encyclopedia of Signaling Molecules; Choi, S., Ed.; Springer: New York, NY, USA, 2016; pp. 1–7. [Google Scholar] [CrossRef]
- Marques, R.E.; Guabiraba, R.; Russo, R.C.; Teixeira, M.M. Targeting CCL5 in inflammation. Expert Opin. Targets 2013, 17, 1439–1460. [Google Scholar] [CrossRef] [PubMed]
- Gschwandtner, M.; Derler, R.; Midwood, K.S. More Than Just Attractive: How CCL2 Influences Myeloid Cell Behavior Beyond Chemotaxis. Front. Immunol. 2019, 10, 2759. [Google Scholar] [CrossRef] [Green Version]
- Kindstedt, E.; Holm, C.K.; Sulniute, R.; Martinez-Carrasco, I.; Lundmark, R.; Lundberg, P. CCL11, a novel mediator of inflammatory bone resorption. Sci. Rep. 2017, 7, 5334. [Google Scholar] [CrossRef] [Green Version]
- Khaiboullina, S.F.; Rizvanov, A.A.; Lombardi, V.C.; Morzunov, S.P.; Reis, H.J.; Palotás, A.; St Jeor, S. Andes-virus-induced cytokine storm is partially suppressed by ribavirin. Antivir. Ther. 2013, 18, 575–584. [Google Scholar] [CrossRef] [Green Version]
- Parameswaran, N.; Patial, S. Tumor necrosis factor-α signaling in macrophages. Crit. Rev. Eukaryot. Gene Expr. 2010, 20, 87–103. [Google Scholar] [CrossRef]
- Jose, P.J.; Griffiths-Johnson, D.A.; Collins, P.D.; Walsh, D.T.; Moqbel, R.; Totty, N.F.; Truong, O.; Hsuan, J.J.; Williams, T.J. Eotaxin: A potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J. Exp. Med. 1994, 179, 881–887. [Google Scholar] [CrossRef] [Green Version]
- Wolpe, S.D.; Davatelis, G.; Sherry, B.; Beutler, B.; Hesse, D.G.; Nguyen, H.T.; Moldawer, L.L.; Nathan, C.F.; Lowry, S.F.; Cerami, A. Macrophages secrete a novel heparin-binding protein with inflammatory and neutrophil chemokinetic properties. J. Exp. Med. 1988, 167, 570–581. [Google Scholar] [CrossRef]
- Kitaura, M.; Nakajima, T.; Imai, T.; Harada, S.; Combadiere, C.; Tiffany, H.L.; Murphy, P.M.; Yoshie, O. Molecular cloning of human eotaxin, an eosinophil-selective CC chemokine, and identification of a specific eosinophil eotaxin receptor, CC chemokine receptor 3. J. Biol. Chem. 1996, 271, 7725–7730. [Google Scholar] [CrossRef] [Green Version]
- Francis, J.N.; Lloyd, C.M.; Sabroe, I.; Durham, S.R.; Till, S.J. T lymphocytes expressing CCR3 are increased in allergic rhinitis compared with non-allergic controls and following allergen immunotherapy. Allergy 2007, 62, 59–65. [Google Scholar] [CrossRef] [Green Version]
- Conroy, D.M.; Williams, T.J. Eotaxin and the attraction of eosinophils to the asthmatic lung. Respir. Res. 2001, 2, 150–156. [Google Scholar] [CrossRef] [Green Version]
- Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25, 677–686. [Google Scholar] [CrossRef]
- Olszewski, M.A.; Huffnagle, G.B.; McDonald, R.A.; Lindell, D.M.; Moore, B.B.; Cook, D.N.; Toews, G.B. The role of macrophage inflammatory protein-1 alpha/CCL3 in regulation of T cell-mediated immunity to Cryptococcus neoformans infection. J. Immunol. 2000, 165, 6429–6436. [Google Scholar] [CrossRef]
- Fischmeister, G.; Kurz, M.; Haas, O.A.; Micksche, M.; Buchinger, P.; Printz, D.; Ressmann, G.; Stroebel, T.; Peters, C.; Fritsch, G.; et al. G-CSF versus GM-CSF for stimulation of peripheral blood progenitor cells (PBPC) and leukocytes in healthy volunteers: Comparison of efficacy and tolerability. Ann. Hematol. 1999, 78, 117–123. [Google Scholar] [CrossRef] [PubMed]
- Castellani, S.; D’Oria, S.; Diana, A.; Polizzi, A.M.; Di Gioia, S.; Mariggiò, M.A.; Guerra, L.; Favia, M.; Vinella, A.; Leonetti, G.; et al. G-CSF and GM-CSF Modify Neutrophil Functions at Concentrations found in Cystic Fibrosis. Sci. Rep. 2019, 9, 12937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carr, R.; Modi, N.; Doré, C. G-CSF and GM-CSF for treating or preventing neonatal infections. Cochrane Database Syst. Rev. 2003, 2003, CD003066. [Google Scholar] [CrossRef] [PubMed]
- Gibaldi, D.; Vilar-Pereira, G.; Pereira, I.R.; Silva, A.A.; Barrios, L.C.; Ramos, I.P.; dos Santos, H.A.M.; Gazzinelli, R.; Lannes-Vieira, J. CCL3/Macrophage Inflammatory Protein-1α Is Dually Involved in Parasite Persistence and Induction of a TNF- and IFNγ-Enriched Inflammatory Milieu in Trypanosoma cruzi-Induced Chronic Cardiomyopathy. Front. Immunol. 2020, 11, 11. [Google Scholar] [CrossRef] [PubMed]
- Lotz, M.; Jirik, F.; Kabouridis, P.; Tsoukas, C.; Hirano, T.; Kishimoto, T.; Carson, D.A. B cell stimulating factor 2/interleukin 6 is a costimulant for human thymocytes and T lymphocytes. J. Exp. Med. 1988, 167, 1253–1258. [Google Scholar] [CrossRef]
- Ayroldi, E.; Zollo, O.; Cannarile, L.; D’Adamio, F.; Grohmann, U.; Delfino, D.V.; Riccardi, C. Interleukin-6 (IL-6) prevents activation-induced cell death: IL-2-independent inhibition of Fas/fasL expression and cell death. Blood 1998, 92, 4212–4219. [Google Scholar] [CrossRef]
- Rincón, M.; Anguita, J.; Nakamura, T.; Fikrig, E.; Flavell, R.A. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 1997, 185, 461–469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diehl, S.; Anguita, J.; Hoffmeyer, A.; Zapton, T.; Ihle, J.N.; Fikrig, E.; Rincón, M. Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 2000, 13, 805–815. [Google Scholar] [CrossRef] [Green Version]
- Bradley, L.M.; Dalton, D.K.; Croft, M. A direct role for IFN-gamma in regulation of Th1 cell development. J. Immunol. 1996, 157, 1350. [Google Scholar]
- Mehta, H.M.; Malandra, M.; Corey, S.J. G-CSF and GM-CSF in Neutropenia. J. Immunol. 2015, 195, 1341–1349. [Google Scholar] [CrossRef] [PubMed]
- Huleihel, M.; Douvdevani, A.; Segal, S.; Apte, R.N. Different regulatory levels are involved in the generation of hemopoietic cytokines (CSFs and IL-6) in fibroblasts stimulated by inflammatory products. Cytokine 1993, 5, 47–56. [Google Scholar] [CrossRef]
- Pitrak, D.L. Effects of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor on the bactericidal functions of neutrophils. Curr. Opin. Hematol. 1997, 4, 183–190. [Google Scholar] [CrossRef]
Peptides | Sequence (aa) | Position (aa) |
---|---|---|
PUUV N-25 | EKECPFIKPEVKPGT | 241–255 |
PUUV N-29 | HVADIDKLIDYAASG | 281–295 |
PUUV N-43 | EIKVKEISNQEPLKI | 424–438 |
PUUV M-26 | FQGYYICLVGSSSEP | 51–65 |
PUUV M-44 | KFVCQRVDMDITVYC | 431–445 |
PUUV M-82 | YTRKACIQLGTEQTC | 811–825 |
Lentiviruses | Protein Expressed |
---|---|
LV-PUUV-S | PUUV N |
LV-PUUV-M | PUUV Gn/Gc |
LV-Katushka2S | Red fluorescent protein (Katushka2S) |
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Shkair, L.; Garanina, E.E.; Martynova, E.V.; Kolesnikova, A.I.; Arkhipova, S.S.; Titova, A.A.; Rizvanov, A.A.; Khaiboullina, S.F. Immunogenic Properties of MVs Containing Structural Hantaviral Proteins: An Original Study. Pharmaceutics 2022, 14, 93. https://doi.org/10.3390/pharmaceutics14010093
Shkair L, Garanina EE, Martynova EV, Kolesnikova AI, Arkhipova SS, Titova AA, Rizvanov AA, Khaiboullina SF. Immunogenic Properties of MVs Containing Structural Hantaviral Proteins: An Original Study. Pharmaceutics. 2022; 14(1):93. https://doi.org/10.3390/pharmaceutics14010093
Chicago/Turabian StyleShkair, Layaly, Ekaterina Evgenevna Garanina, Ekaterina Vladimirovna Martynova, Alena Igorevna Kolesnikova, Svetlana Sergeevna Arkhipova, Angelina Andreevna Titova, Albert Anatolevich Rizvanov, and Svetlana Francevna Khaiboullina. 2022. "Immunogenic Properties of MVs Containing Structural Hantaviral Proteins: An Original Study" Pharmaceutics 14, no. 1: 93. https://doi.org/10.3390/pharmaceutics14010093
APA StyleShkair, L., Garanina, E. E., Martynova, E. V., Kolesnikova, A. I., Arkhipova, S. S., Titova, A. A., Rizvanov, A. A., & Khaiboullina, S. F. (2022). Immunogenic Properties of MVs Containing Structural Hantaviral Proteins: An Original Study. Pharmaceutics, 14(1), 93. https://doi.org/10.3390/pharmaceutics14010093