A highly attenuated vaccinia virus strain LC16m8-based vaccine for severe fever with thrombocytopenia syndrome

Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both...

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Published inPLoS pathogens Vol. 17; no. 2; p. e1008859
Main Authors Yoshikawa, Tomoki, Taniguchi, Satoshi, Kato, Hirofumi, Iwata-Yoshikawa, Naoko, Tani, Hideki, Kurosu, Takeshi, Fujii, Hikaru, Omura, Natsumi, Shibamura, Miho, Watanabe, Shumpei, Egawa, Kazutaka, Inagaki, Takuya, Sugimoto, Satoko, Phanthanawiboon, Supranee, Harada, Shizuko, Yamada, Souichi, Fukushi, Shuetsu, Morikawa, Shigeru, Nagata, Noriyo, Shimojima, Masayuki, Saijo, Masayuki
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2021
Public Library of Science (PLoS)
Subjects
Animal models
Antibodies
Antibody response
Biology and Life Sciences
Complications
Conjunctivitis
Deoxyribonucleic acid
DNA
DNA vaccines
Eczema
Encephalitis
Encephalopathy
Experiments
Fetuses
Fever
Gene expression
Genomes
Glycoproteins
GPC gene
Immunogenicity
Mammalian cells
Mammals
Medicine and Health Sciences
Microscopy
Polyclonal antibodies
Proteins
Research and Analysis Methods
RNA polymerase
Side effects
Skin diseases
Smallpox
Stomatitis
Strains (organisms)
Thrombocytopenia
Vaccines
Viruses
Japan
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Abstract Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both humoral and cellular immunity. We applied a highly attenuated but still immunogenic vaccinia virus strain LC16m8 (m8) as a recombinant vaccine for SFTS. Recombinant m8s expressing SFTSV nucleoprotein (m8-N), envelope glycoprotein precursor (m8-GPC), and both N and GPC (m8-N+GPC) in the infected cells were generated. Both m8-GPC- and m8-N+GPC-infected cells were confirmed to produce SFTSV-like-particles (VLP) in vitro , and the N was incorporated in the VLP produced by the infection of cells with m8-N+GPC. Specific antibodies to SFTSV were induced in mice inoculated with each of the recombinant m8s, and the mice were fully protected from lethal challenge with SFTSV at both 10 3 TCID 50 and 10 5 TCID 50 . In mice that had been immunized with vaccinia virus strain Lister in advance of m8-based SFTSV vaccine inoculation, protective immunity against the SFTSV challenge was also conferred. The pathological analysis revealed that mice immunized with m8-GPC or m8-N+GPC did not show any histopathological changes without any viral antigen-positive cells, whereas the control mice showed focal necrosis with inflammatory infiltration with SFTSV antigen-positive cells in tissues after SFTSV challenge. The passive serum transfer experiments revealed that sera collected from mice inoculated with m8-GPC or m8-N+GPC but not with m8-N conferred protective immunity against lethal SFTSV challenge in naïve mice. On the other hand, the depletion of CD8-positive cells in vivo did not abrogate the protective immunity conferred by m8-based SFTSV vaccines. Based on these results, the recombinant m8-GPC and m8-N+GPC were considered promising vaccine candidates for SFTS.
AbstractList [...]the development of an effective vaccine for SFTS is urgently needed. [...]far, it has been reported that a live recombinant vesicular stomatitis virus or a DNA vaccine expressing the SFTSV glycoproteins (GPs) originated from SFTSV GPC gene-elicited protective immunity against SFTSV in lethal mouse or ferret models [16, 17]. Vaccinia virus (VAC) was used as the smallpox vaccine, and smallpox vaccines produced by using a variety of VAC strains were used during the global smallpox eradication program led by the World Health Organization. Since smallpox eradication was declared in 1980, VAC has been used as a recombinant vaccine vector with an expectation of immunogenicity [18, 19]. [...]since the VAC strains used as the vaccine vector in the beginning of the eradication campaign were mainly so-called second-generation smallpox vaccines that were associated with severe side effects, such as encephalitis, encephalopathy, conjunctivitis, progressive vaccinia, eczema vaccinatum and generalized fetal VAC infections [18, 20, 21], the application of VAC has not been popular. [...]MVA can infect mammalian cells but cannot replicate well in most mammalian cells [21]. m8 is licensed for use in healthy people in Japan, and approximately 100,000 people have been vaccinated with m8 thus far, with antibody response comparable to the first generation vaccine [25] and without experiencing severe postvaccine complications [25, 26].
Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both humoral and cellular immunity. We applied a highly attenuated but still immunogenic vaccinia virus strain LC16m8 (m8) as a recombinant vaccine for SFTS. Recombinant m8s expressing SFTSV nucleoprotein (m8-N), envelope glycoprotein precursor (m8-GPC), and both N and GPC (m8-N+GPC) in the infected cells were generated. Both m8-GPC- and m8-N+GPC-infected cells were confirmed to produce SFTSV-like-particles (VLP) in vitro , and the N was incorporated in the VLP produced by the infection of cells with m8-N+GPC. Specific antibodies to SFTSV were induced in mice inoculated with each of the recombinant m8s, and the mice were fully protected from lethal challenge with SFTSV at both 10 3 TCID 50 and 10 5 TCID 50 . In mice that had been immunized with vaccinia virus strain Lister in advance of m8-based SFTSV vaccine inoculation, protective immunity against the SFTSV challenge was also conferred. The pathological analysis revealed that mice immunized with m8-GPC or m8-N+GPC did not show any histopathological changes without any viral antigen-positive cells, whereas the control mice showed focal necrosis with inflammatory infiltration with SFTSV antigen-positive cells in tissues after SFTSV challenge. The passive serum transfer experiments revealed that sera collected from mice inoculated with m8-GPC or m8-N+GPC but not with m8-N conferred protective immunity against lethal SFTSV challenge in naïve mice. On the other hand, the depletion of CD8-positive cells in vivo did not abrogate the protective immunity conferred by m8-based SFTSV vaccines. Based on these results, the recombinant m8-GPC and m8-N+GPC were considered promising vaccine candidates for SFTS.
[...]the development of an effective vaccine for SFTS is urgently needed. [...]far, it has been reported that a live recombinant vesicular stomatitis virus or a DNA vaccine expressing the SFTSV glycoproteins (GPs) originated from SFTSV GPC gene-elicited protective immunity against SFTSV in lethal mouse or ferret models [16, 17]. Vaccinia virus (VAC) was used as the smallpox vaccine, and smallpox vaccines produced by using a variety of VAC strains were used during the global smallpox eradication program led by the World Health Organization. Since smallpox eradication was declared in 1980, VAC has been used as a recombinant vaccine vector with an expectation of immunogenicity [18, 19]. [...]since the VAC strains used as the vaccine vector in the beginning of the eradication campaign were mainly so-called second-generation smallpox vaccines that were associated with severe side effects, such as encephalitis, encephalopathy, conjunctivitis, progressive vaccinia, eczema vaccinatum and generalized fetal VAC infections [18, 20, 21], the application of VAC has not been popular. [...]MVA can infect mammalian cells but cannot replicate well in most mammalian cells [21]. m8 is licensed for use in healthy people in Japan, and approximately 100,000 people have been vaccinated with m8 thus far, with antibody response comparable to the first generation vaccine [25] and without experiencing severe postvaccine complications [25, 26].
Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both humoral and cellular immunity. We applied a highly attenuated but still immunogenic vaccinia virus strain LC16m8 (m8) as a recombinant vaccine for SFTS. Recombinant m8s expressing SFTSV nucleoprotein (m8-N), envelope glycoprotein precursor (m8-GPC), and both N and GPC (m8-N+GPC) in the infected cells were generated. Both m8-GPC- and m8-N+GPC-infected cells were confirmed to produce SFTSV-like-particles (VLP) in vitro , and the N was incorporated in the VLP produced by the infection of cells with m8-N+GPC. Specific antibodies to SFTSV were induced in mice inoculated with each of the recombinant m8s, and the mice were fully protected from lethal challenge with SFTSV at both 10 3 TCID 50 and 10 5 TCID 50 . In mice that had been immunized with vaccinia virus strain Lister in advance of m8-based SFTSV vaccine inoculation, protective immunity against the SFTSV challenge was also conferred. The pathological analysis revealed that mice immunized with m8-GPC or m8-N+GPC did not show any histopathological changes without any viral antigen-positive cells, whereas the control mice showed focal necrosis with inflammatory infiltration with SFTSV antigen-positive cells in tissues after SFTSV challenge. The passive serum transfer experiments revealed that sera collected from mice inoculated with m8-GPC or m8-N+GPC but not with m8-N conferred protective immunity against lethal SFTSV challenge in naïve mice. On the other hand, the depletion of CD8-positive cells in vivo did not abrogate the protective immunity conferred by m8-based SFTSV vaccines. Based on these results, the recombinant m8-GPC and m8-N+GPC were considered promising vaccine candidates for SFTS. Severe fever with thrombocytopenia syndrome (SFTS) is an emerging viral hemorrhagic fever with a high case-fatality rate (approximately 5% to >40%). Indigenous SFTS has been reported in China, Japan, South Korea, and Vietnam. Thus, the development of an effective vaccine for SFTS is urgently needed. Vaccinia virus (VAC) was previously used as a vaccine for smallpox. Unfortunately, after these strains, the so-called second generation of VAC used during the eradication campaign was associated with severe adverse events, and the third generation of VAC strains such as LC16m8 (m8) and modified vaccinia Ankara (MVA) was established. m8 is confirmed to be highly attenuated while still maintaining immunogenicity. m8 is licensed for use in healthy people in Japan. At the present time, approximately 100,000 people have undergone vaccination with m8 without experiencing any severe postvaccine complications. At present, third-generation VAC strains are attractive for a recombinant vaccine vector, especially for viral hemorrhagic infectious diseases, such as Ebola virus disease, Lassa fever, Crimean-Congo hemorrhagic fever, and SFTS. We investigated the practicality of an m8-based recombinant vaccine for SFTS as well as other promising recombinant VAC-based vaccines for viral hemorrhagic infectious diseases.
Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both humoral and cellular immunity. We applied a highly attenuated but still immunogenic vaccinia virus strain LC16m8 (m8) as a recombinant vaccine for SFTS. Recombinant m8s expressing SFTSV nucleoprotein (m8-N), envelope glycoprotein precursor (m8-GPC), and both N and GPC (m8-N+GPC) in the infected cells were generated. Both m8-GPC- and m8-N+GPC-infected cells were confirmed to produce SFTSV-like-particles (VLP) in vitro, and the N was incorporated in the VLP produced by the infection of cells with m8-N+GPC. Specific antibodies to SFTSV were induced in mice inoculated with each of the recombinant m8s, and the mice were fully protected from lethal challenge with SFTSV at both 103 TCID50 and 105 TCID50. In mice that had been immunized with vaccinia virus strain Lister in advance of m8-based SFTSV vaccine inoculation, protective immunity against the SFTSV challenge was also conferred. The pathological analysis revealed that mice immunized with m8-GPC or m8-N+GPC did not show any histopathological changes without any viral antigen-positive cells, whereas the control mice showed focal necrosis with inflammatory infiltration with SFTSV antigen-positive cells in tissues after SFTSV challenge. The passive serum transfer experiments revealed that sera collected from mice inoculated with m8-GPC or m8-N+GPC but not with m8-N conferred protective immunity against lethal SFTSV challenge in naïve mice. On the other hand, the depletion of CD8-positive cells in vivo did not abrogate the protective immunity conferred by m8-based SFTSV vaccines. Based on these results, the recombinant m8-GPC and m8-N+GPC were considered promising vaccine candidates for SFTS.
Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both humoral and cellular immunity. We applied a highly attenuated but still immunogenic vaccinia virus strain LC16m8 (m8) as a recombinant vaccine for SFTS. Recombinant m8s expressing SFTSV nucleoprotein (m8-N), envelope glycoprotein precursor (m8-GPC), and both N and GPC (m8-N+GPC) in the infected cells were generated. Both m8-GPC- and m8-N+GPC-infected cells were confirmed to produce SFTSV-like-particles (VLP) in vitro, and the N was incorporated in the VLP produced by the infection of cells with m8-N+GPC. Specific antibodies to SFTSV were induced in mice inoculated with each of the recombinant m8s, and the mice were fully protected from lethal challenge with SFTSV at both 103 TCID50 and 105 TCID50. In mice that had been immunized with vaccinia virus strain Lister in advance of m8-based SFTSV vaccine inoculation, protective immunity against the SFTSV challenge was also conferred. The pathological analysis revealed that mice immunized with m8-GPC or m8-N+GPC did not show any histopathological changes without any viral antigen-positive cells, whereas the control mice showed focal necrosis with inflammatory infiltration with SFTSV antigen-positive cells in tissues after SFTSV challenge. The passive serum transfer experiments revealed that sera collected from mice inoculated with m8-GPC or m8-N+GPC but not with m8-N conferred protective immunity against lethal SFTSV challenge in naïve mice. On the other hand, the depletion of CD8-positive cells in vivo did not abrogate the protective immunity conferred by m8-based SFTSV vaccines. Based on these results, the recombinant m8-GPC and m8-N+GPC were considered promising vaccine candidates for SFTS.Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious disease with a high case-fatality rate. One of the best strategies for preventing SFTS is to develop a vaccine, which is expected to induce both humoral and cellular immunity. We applied a highly attenuated but still immunogenic vaccinia virus strain LC16m8 (m8) as a recombinant vaccine for SFTS. Recombinant m8s expressing SFTSV nucleoprotein (m8-N), envelope glycoprotein precursor (m8-GPC), and both N and GPC (m8-N+GPC) in the infected cells were generated. Both m8-GPC- and m8-N+GPC-infected cells were confirmed to produce SFTSV-like-particles (VLP) in vitro, and the N was incorporated in the VLP produced by the infection of cells with m8-N+GPC. Specific antibodies to SFTSV were induced in mice inoculated with each of the recombinant m8s, and the mice were fully protected from lethal challenge with SFTSV at both 103 TCID50 and 105 TCID50. In mice that had been immunized with vaccinia virus strain Lister in advance of m8-based SFTSV vaccine inoculation, protective immunity against the SFTSV challenge was also conferred. The pathological analysis revealed that mice immunized with m8-GPC or m8-N+GPC did not show any histopathological changes without any viral antigen-positive cells, whereas the control mice showed focal necrosis with inflammatory infiltration with SFTSV antigen-positive cells in tissues after SFTSV challenge. The passive serum transfer experiments revealed that sera collected from mice inoculated with m8-GPC or m8-N+GPC but not with m8-N conferred protective immunity against lethal SFTSV challenge in naïve mice. On the other hand, the depletion of CD8-positive cells in vivo did not abrogate the protective immunity conferred by m8-based SFTSV vaccines. Based on these results, the recombinant m8-GPC and m8-N+GPC were considered promising vaccine candidates for SFTS.
Author Omura, Natsumi
Taniguchi, Satoshi
Harada, Shizuko
Shimojima, Masayuki
Kato, Hirofumi
Saijo, Masayuki
Inagaki, Takuya
Watanabe, Shumpei
Egawa, Kazutaka
Yamada, Souichi
Nagata, Noriyo
Shibamura, Miho
Kurosu, Takeshi
Fujii, Hikaru
Morikawa, Shigeru
Iwata-Yoshikawa, Naoko
Phanthanawiboon, Supranee
Sugimoto, Satoko
Fukushi, Shuetsu
Tani, Hideki
Yoshikawa, Tomoki
AuthorAffiliation 2 Department of Pathology, National Institute of Infectious Diseases, Musashimurayama-shi, Tokyo, Japan
4 Department of Microbiology, Faculty of Veterinary Medicine, Okayama University of Science, Imabari-shi, Ehime, Japan
University of Texas Medical Branch / Galveston National Laboratory, UNITED STATES
1 Department of Virology 1, National Institute of Infectious Diseases, Musashimurayama-shi, Tokyo, Japan
3 Department of Virology, Toyama Institute of Health, Imizu-shi, Toyama, Japan
AuthorAffiliation_xml – name: University of Texas Medical Branch / Galveston National Laboratory, UNITED STATES
– name: 4 Department of Microbiology, Faculty of Veterinary Medicine, Okayama University of Science, Imabari-shi, Ehime, Japan
– name: 1 Department of Virology 1, National Institute of Infectious Diseases, Musashimurayama-shi, Tokyo, Japan
– name: 3 Department of Virology, Toyama Institute of Health, Imizu-shi, Toyama, Japan
– name: 2 Department of Pathology, National Institute of Infectious Diseases, Musashimurayama-shi, Tokyo, Japan
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  givenname: Masayuki
  surname: Saijo
  fullname: Saijo, Masayuki
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33534867$$D View this record in MEDLINE/PubMed
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2021 Yoshikawa et al 2021 Yoshikawa et al
Copyright_xml – notice: 2021 Yoshikawa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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– volume: 8
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  article-title: A Single dose of modified vaccinia Ankara expressing ebola virus like particles protects nonhuman primates from lethal ebola virus challenge
  publication-title: Sci Rep
  doi: 10.1038/s41598-017-19041-y
– volume: 72
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  article-title: Efficacy of individual measles virus structural proteins in the protection of rats from measles encephalitis
  publication-title: J Gen Virol
  doi: 10.1099/0022-1317-72-10-2491
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Snippet Severe fever with thrombocytopenia syndrome (SFTS) caused by a species Dabie bandavirus (formerly SFTS virus [SFTSV]) is an emerging hemorrhagic infectious...
[...]the development of an effective vaccine for SFTS is urgently needed. [...]far, it has been reported that a live recombinant vesicular stomatitis virus or...
[...]the development of an effective vaccine for SFTS is urgently needed. [...]far, it has been reported that a live recombinant vesicular stomatitis virus or...
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StartPage e1008859
SubjectTerms Animal models
Antibodies
Antibody response
Biology and Life Sciences
Complications
Conjunctivitis
Deoxyribonucleic acid
DNA
DNA vaccines
Eczema
Encephalitis
Encephalopathy
Experiments
Fetuses
Fever
Gene expression
Genomes
Glycoproteins
GPC gene
Immunogenicity
Mammalian cells
Mammals
Medicine and Health Sciences
Microscopy
Polyclonal antibodies
Proteins
Research and Analysis Methods
RNA polymerase
Side effects
Skin diseases
Smallpox
Stomatitis
Strains (organisms)
Thrombocytopenia
Vaccines
Viruses
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Title A highly attenuated vaccinia virus strain LC16m8-based vaccine for severe fever with thrombocytopenia syndrome
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http://dx.doi.org/10.1371/journal.ppat.1008859
Volume 17
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