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. 2019 Aug 2;10:1781. doi: 10.3389/fmicb.2019.01781

TABLE 2.

Potential vaccine candidates against Middle East respiratory syndrome-coronavirus.

Vaccine type Vector and antigen Administration route Results References
Viral-vector rAd5 encoding S1 protein IM Immunization with rAd5 constructs expressing CD40-targeted S1 fusion protein (rAd5-S1/F/CD40L) offered complete protection to hDPP4 transgenic mice against MERS-CoV challenge and prevented pulmonary perivascular hemorrhage. Hashem et al., 2019
rAd5 or rAd41 encoding S protein IM or IG IG administration of rAd5-S or rAd41-S elicited antigen-specific IgG and neutralizing antibody in serum, but T-cell responses were not detected. A single IM injection of Ad5-S or Ad41-S induced systemic humoral response in addition to the functional antigen-specific T-cell responses in the spleen and pulmonary lymphocytes of the mice, which persisted for several months. Guo et al., 2015
rAd5 encoding S protein or S1 IM and later boosted with IN Immunized mice demonstrated antibody responses against spike protein, which neutralized MERS-CoV in vitro. Stronger neutralizing antibody responses were observed in the mice vaccinated with the vector encoding the shorter S1 protein than the full-length S protein. Kim et al., 2014
ChAdOx1 encoding S protein* IM or IN Single dose intranasal or intramuscular immunization protected transgenic BALB/c mice against lethal virus challenge. Immunogenicity and efficacy were comparable between immunization routes. Munster et al., 2017
ChAdOx1 encoding S protein* IM Single dose immunization with ChAdOx1 MERS vaccine with tPA induced 5 logs of neutralizing antibodies in BALB/c mice. Alharbi et al., 2017
MVA encoding S protein IM Immunization with MVA MERS vaccine containing tPA regulated by F11 promoter induced 4.7 logs of neutralizing antibodies in BALB/c mice. Alharbi et al., 2017
MVA encoding S protein∗∗ IM or SC Both immunization routes induced neutralizing antibodies and CD8+ T-cell responses in mice. Vaccinated mice were protected against MERS-CoV challenge infection after transduction with the hDPP4 receptor. Volz et al., 2015
MVA encoding S protein∗∗ IM Neutralizing antibody responses were induced in immunized mice. Song et al., 2013
MVA encoding the N-protein IM or IP CD8+ T-cell response was elicited in the immunized mice in both immunization routes. Veit et al., 2018
NDV encoding S protein IM Recombinant NDV expressing MERS-CoV S protein induced neutralizing antibodies in BALB/c mice and Bactrian camels. Liu et al., 2017
Viral-vector and nanoparticle rAd5 and MERS-CoV S nanoparticle IM Heterologous prime-boost vaccination with rAd5-S protein and alum-adjuvanted recombinant S protein induced both Th1 and Th2 immune responses in SPF BALB/c mice. Jung et al., 2018
DNA DNA encoding S protein∗∗∗ IM followed by EP The DNA vaccine was immunogenic in mice, camels and rhesus macaques. When the immunized macaques were challenged with MERS-CoV, characteristic clinical symptoms including pneumonia were reduced. Muthumani et al., 2015
DNA encoding S or S1 protein IM DNA encoding S1 protein elicited stronger antibody and cellular immune responses in mice than that encoding the S protein. Both DNAs encoding S1 and S proteins induced neutralizing antibodies that cross-reacted with MERS-CoV strains of human and camel origins. Al-Amri et al., 2017
DNA encoding S1 protein IM Immunization with DNA encoding S1 protein and passive transfer of immune sera from the vaccinated mice protected hDPP4-transduced-mice from MERS-CoV infection. Chi et al., 2017
Subunit MERS-CoV S1 protein SC Adjuvanted (MF59) MERS-CoV S1 protein protected hDPP4 transgenic mice against lethal MERS-CoV challenge, where the protection correlated well with the neutralizing antibody titer. Wang et al., 2017c
MERS-CoV S1 protein IM Immunization with adjuvanated (Advax HCXL adjuvant and Sigma Adjuvant System) S1 protein reduced and delayed virus shedding in the upper respiratory tract of dromedary camels and provided complete protection in alpaca against MERS-CoV challenge. Adney et al., 2019
MERS-CoV S protein trimer on Fd IM Recombinant prefusion trimeric MERS-CoV S protein induced high titer of neutralizing antibodies in BALB/cJ mice. Pallesen et al., 2017
RBD trimer on Fd SC or IM Adjuvanted (alum) RBD-Fd induced neutralizing antibodies in BALB/c mice and protected (83%) hDPP4 transgenic mice against lethal MERS-CoV challenge. Tai et al., 2016
RBD fused to Fc SC Adjuvanted RBD-Fc induced high titer of neutralizing antibodies in BALB/c mice and New Zealand white rabbits. Ma et al., 2014b
RBD fused to Fc SC Mice immunized with the vaccine and Montanide ISA 51 adjuvant produced neutralizing antibodies which inhibited binding of the RBD to DPP4 receptor, neutralizing MERS-CoV infection. Du et al., 2013
RBD fused to Fc IN or SC Mice vaccinated with both immunization routes in the presence of adjuvants (Montanide ISA 51 adjuvant for SC and Poly(I:C) for IN) elicited systemic humoral immune responses. Stronger systemic cellular immune responses and local mucosal immune responses were observed in mice immunized via IN route. Ma et al., 2014a
RBD fused to Fc IM hCD26/DPP4 transgenic mice immunized with the vaccine in the presence of adjuvant, AddaVax elicited neutralizing antibodies and were protected against MERS-CoV infection. Nyon et al., 2018
RBD fused to Fc SC Mice immunized with the vaccine alone produced detectable neutralizing antibodies and cellular immune responses. Immunogenicity of the vaccine improved when the adjuvants such as Freund’s adjuvant, alum, monophosphoryl lipid A, Montanide ISA51 or MF59 was included in the formulation. MF59 was demonstrated to be superior in enhancing the vaccine immunogenicity and protection against viral challenge. Zhang et al., 2016
Recombinant RBD IM or SC When the subunit vaccine was administered together with combination of alum and CpG ODN, optimized RBD-specific humoral and cellular immunity were elicted. Robust RBD-specific antibody and T-cell responses were induced in mice immunized with the vaccine in combination with IFA and CpG ODN, but low level of neutralizing antibodies were induced. Lan et al., 2014
Recombinant RBD IM Rhesus macaques immunized with the subunit vaccine and alum adjuvant produced neutralizing antibodies and experienced mitigated clinical symptoms when challenged with MERS-CoV. Lan et al., 2015
rNTD of S protein IM Immunization with rNTD of MERS-CoV S protein adjuvanted with alum induced neutralizing antibodies and reduced the respiratory tract pathology of BALB/c mice challenged with MERS-CoV. Jiaming et al., 2017
VLPs MERS-CoV VLPs IM Co-administration of the VLPs-based vaccine and alum activated RBD specific humoral and cellular immune responses in rhesus macaques. Wang et al., 2017b
S protein nanoparticles IM S protein produced in the baculovirus insect cells expression system assembled into nanoparticles of approximately 25 nm. Mice immunized with these nanoparticles in the presence of alum produced high titer of neutralizing antibody. Coleman et al., 2014
S protein nanoparticles IM The vaccine together with Matrix M1 adjuvant activated S protein specific humoral immune responses, and protected hDPP4 transduced mice against viral challenge. Coleman et al., 2017
CPV VLP displaying RBD IM Immunization of the mice with the chimeric VLPs displaying RBD in the presence of adjuvants [alum or Poly(I:C)] elicited neutralizing antibody responses as well as cellular immune responses. Wang et al., 2017a
Influenza A VLP displaying S protein IM Immunization of the mice with the chimeric VLPs displaying RBD in the presence of a combination of adjuvants (alum and CpG ODN) elicited neutralizing antibody responses. Lan et al., 2018
Nanoparticle Ferritin displaying RBD IM Immunization with chaperna-mediated ferritin nanoparticle displaying MERS-CoV RBD adjuvanted with MF59 induced RBD-specific antibodies in BALB/c mice which inhibited RBD binding to hDPP4 receptor protein. Kim et al., 2018
Inactivated whole -virus MERS-CoV IM Mice immunized with the inactivated vaccine in the presence of a combination of adjuvants (alum and CpG ODN) elicited neutralizing activity but not cell-mediated immunity. This vaccine also protected hDPP4 transduced mice against MERS-CoV challenge. Deng et al., 2018
MERS-CoV IM Gamma radiation-inactivated MERS-CoV induced neutralizing antibodies and reduced viral load in hDPP4 transgenic mice but may cause hypersensitivity-type lung immunopathologic reaction upon MERS-CoV challenge. Agrawal et al., 2016
Chimeric RABV displaying S1 protein IM The inactivated vaccine induced high titer of neutralizing antibodies in mice, and protected hDPP4-transduced-mice against MERS-CoV infection. Wirblich et al., 2017
Live-attenuated MERS-CoV mutant - The mutant was produced by deleting the E gene of the MERS-CoV. This mutant lacked infectivity but was single-cycle replicative. Almazan et al., 2013
MERS-CoV mutant IN Attenuated MERS-CoV through mutation of NSP16 (D130A) protected CRISPR-Cas9- targeted 288–330+/+ C57BL/6 mice from mouse-adapted MERS-CoV challenge. Menachery et al., 2017
MV expressing full-length or truncated, soluble variant of S protein IP The recombinant MV was replication competent. Immunization of the type I interferon receptor-deficient (IFNAR–/–) CD46Ge mice with the recombinant MV induced both MV and S protein specific neutralizing antibodies as well as cellular immune responses. The recombinant MV protected hDPP4-transduced-mice against viral challenge. Malczyk et al., 2015
MV expressing N protein IP Recombinant MV expressing MERS-CoV N protein induced N-specific T cell responses in IFNAR–/–-CD46Ge mice. Bodmer et al., 2018
Recombinant VSV expressing S protein IN or IM Recombinant VSV was produced by replacing the glycoprotein of VSV with the S protein of MERS-CoV. The recombinant virus induced neutralizing antibodies and T cell responses in rhesus macaques after a single intramuscular or intranasal immunization dose. Liu et al., 2018

MERS-CoV, Middle East respiratory syndrome-coronavirus; rAd5, recombinant human adenovirus type-5; rAd41, recombinant human adenovirus type-41; MVA, modified vaccinia virus Ankara; ChAdOx1, chimpanzee adenovirus, Oxford University #1; NDV, Newcastle disease virus; MV, measles virus; CPV, canine parvovirus; RABV, rabies virus; VLP, virus-like particle; NSP, non-structural protein; S protein, spike protein; S1 protein, spike protein receptor binding subunit; RBD, receptor-binding domain in S1; N protein, nucleocapsid protein; rNTD, recombinant N-terminal domain; Fd, foldon trimerization motif; Fc, Fc region of human IgG; tPA, leader sequence of the human tissue plasminogen activator gene; IFNAR–/–-CD46Ge mice, genetically modified mice deficient of type I IFN receptor and transgenically expressing human CD46; SPF, specific-pathogen-free; IM, intramuscular; IN, intranasal; IP, intraperitoneal; SC, subcutaneous; IG, intragastric; EP, electroporation. Vectors and antigens marked with “*” have entered phase I clinical trial (*MERS001; ∗∗MVA-MERS-S; ∗∗∗GLS-5300).