Receptor-binding domain of MERS-CoV with optimal immunogen dosage and immunization interval protects human transgenic mice from MERS-CoV infection

References

• Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012; 367:1814-20; PMID:23075143; https://doi.org/10.1056/NEJMoa1211721; http://www.ncbi.nlm.nih.gov/pubmed/23075143
   PubMed Web of Science ®Google Scholar
• Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V, Epstein JH, Alhakeem R, Durosinloun A, Al Asmari M, Islam A, et al. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 2013; 19:1819-23; PMID:24206838; https://doi.org/10.3201/eid1911.131172; http://www.ncbi.nlm.nih.gov/pubmed/24206838
   PubMed Web of Science ®Google Scholar
• Madani TA, Azhar EI, Hashem AM. Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med 2014; 371:1360; PMID:25271614; http://www.ncbi.nlm.nih.gov/pubmed/25271614
   PubMed Web of Science ®Google Scholar
• Briese T, Mishra N, Jain K, Zalmout IS, Jabado OJ, Karesh WB, Daszak P, Mohammed OB, Alagaili AN, Lipkin WI. Middle East respiratory syndrome coronavirus quasispecies that include homologues of human isolates revealed through whole-genome analysis and virus cultured from dromedary camels in Saudi Arabia. Mbio 2014; 5:e01146-14; PMID:24781747; https://doi.org/10.1128/mBio.01146-14
   PubMed Web of Science ®Google Scholar
• Azhar EI, Hashem AM, El-Kafrawy SA, Sohrab SS, Aburizaiza AS, Farraj SA, Hassan AM, Al-Saeed MS, Jamjoom GA, Madani TA. Detection of the Middle East respiratory syndrome coronavirus genome in an air sample originating from a camel barn owned by an infected patient. Mbio 2014; 5:e01450-14; PMID:25053787; https://doi.org/10.1128/mBio.01450-14; http://www.ncbi.nlm.nih.gov/pubmed/25053787
   PubMed Web of Science ®Google Scholar
• Yang Y, Du L, Liu C, Wang L, Ma C, Tang J, Baric RS, Jiang S, Li F. Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc Natl Acad Sci U S A 2014; 111:12516-21; PMID:25114257; https://doi.org/10.1073/pnas.1405889111
   PubMed Web of Science ®Google Scholar
• Wang Q, Qi J, Yuan Y, Xuan Y, Han P, Wan Y, Ji W, Li Y, Wu Y, Wang J, et al. Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 2014; 16:328-37; PMID:25211075; https://doi.org/10.1016/j.chom.2014.08.009; http://www.ncbi.nlm.nih.gov/pubmed/25211075
   PubMed Web of Science ®Google Scholar
• Omrani AS, Matin MA, Haddad Q, Al-Nakhli D, Memish ZA, Albarrak AM. A family cluster of Middle East respiratory syndrome coronavirus infections related to a likely unrecognized asymptomatic or mild case. Int J Infect Dis 2013; 17:e668-72; PMID:23916548; https://doi.org/10.1016/j.ijid.2013.07.001; http://www.ncbi.nlm.nih.gov/pubmed/23916548
   PubMed Web of Science ®Google Scholar
• Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA, Cummings DA, Alabdullatif ZN, Assad M, Almulhim A, Makhdoom H, et al. Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med 2013; 369:407-16; PMID:23782161; https://doi.org/10.1056/NEJMoa1306742; http://www.ncbi.nlm.nih.gov/pubmed/23782161
   PubMed Web of Science ®Google Scholar
• Memish ZA, Zumla AI, Al-Hakeem RF, Al-Rabeeah AA, Stephens GM. Family cluster of Middle East respiratory syndrome coronavirus infections. N Engl J Med 2013; 368:2487-94; PMID:23718156; https://doi.org/10.1056/NEJMoa1303729; http://www.ncbi.nlm.nih.gov/pubmed/23718156
   PubMed Web of Science ®Google Scholar
• Abroug F, Slim A, Ouanes-Besbes L, Hadj Kacem MA, Dachraoui F, Ouanes I, Lu X, Tao Y, Paden C, Caidi H, et al. Family cluster of Middle East respiratory syndrome coronavirus infections, Tunisia. Emerg Infect Dis 2014; 20:1527-30; PMID:25148113; https://doi.org/10.3201/eid2009.140378; http://www.ncbi.nlm.nih.gov/pubmed/25148113
   PubMed Web of Science ®Google Scholar
• Park SH, Kim YS, Jung Y, Choi SY, Cho NH, Jeong HW, Heo JY, Yoon JH, Lee J, Cheon S, et al. Outbreaks of Middle East respiratory syndrome in two hospitals initiated by a single patient in daejeon, South Korea. Infect Chemother 2016; 48:99-107; PMID:27433380; https://doi.org/10.3947/ic.2016.48.2.99; http://www.ncbi.nlm.nih.gov/pubmed/27433380
   PubMed Web of Science ®Google Scholar
• Gao J, Lu G, Qi J, Li Y, Wu Y, Deng Y, Geng H, Li H, Wang Q, Xiao H, et al. Structure of the fusion core and inhibition of fusion by a heptad repeat peptide derived from the S protein of Middle East respiratory syndrome coronavirus. J Virol 2013; 87:13134-40; PMID:24067982; https://doi.org/10.1128/JVI.02433-13; http://www.ncbi.nlm.nih.gov/pubmed/24067982
   PubMed Web of Science ®Google Scholar
• Lu L, Liu Q, Zhu Y, Chan KH, Qin L, Li Y, Wang Q, Chan JF, Du L, Yu F, et al. Structure-based discovery of Middle East respiratory syndrome coronavirus fusion inhibitor. Nat Commun 2014; 5:3067; PMID:24473083; http://www.ncbi.nlm.nih.gov/pubmed/24473083
   PubMed Web of Science ®Google Scholar
• Li F. Receptor recognition mechanisms of coronaviruses: a decade of structural studies. J Virol 2015; 89:1954-64; PMID:25428871; https://doi.org/10.1128/JVI.02615-14
   PubMed Web of Science ®Google Scholar
• Lu G, Hu Y, Wang Q, Qi J, Gao F, Li Y, Zhang Y, Zhang W, Yuan Y, Bao J, et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 2013; 500:227-31; PMID:23831647; https://doi.org/10.1038/nature12328
   PubMed Web of Science ®Google Scholar
• Wang N, Shi X, Jiang L, Zhang S, Wang D, Tong P, Guo D, Fu L, Cui Y, Liu X, et al. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res 2013; 23:986-93; PMID:23835475; https://doi.org/10.1038/cr.2013.92; http://www.ncbi.nlm.nih.gov/pubmed/23835475
   PubMed Web of Science ®Google Scholar
• Du L, Kou Z, Ma C, Tao X, Wang L, Zhao G, Chen Y, Yu F, Tseng CT, Zhou Y, et al. A truncated receptor-binding domain of MERS-CoV spike protein potently inhibits MERS-CoV infection and induces strong neutralizing antibody responses: implication for developing therapeutics and vaccines. PloS One 2013; 8:e81587; PMID:24324708; https://doi.org/10.1371/journal.pone.0081587; http://www.ncbi.nlm.nih.gov/pubmed/24324708
   PubMed Web of Science ®Google Scholar
• Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 2013; 495:251-4; PMID:23486063; https://doi.org/10.1038/nature12005
   PubMed Web of Science ®Google Scholar
• Ma C, Li Y, Wang L, Zhao G, Tao X, Tseng CT, Zhou Y, Du L, Jiang S. Intranasal vaccination with recombinant receptor-binding domain of MERS-CoV spike protein induces much stronger local mucosal immune responses than subcutaneous immunization: Implication for designing novel mucosal MERS vaccines. Vaccine 2014; 32:2100-8; PMID:24560617; https://doi.org/10.1016/j.vaccine.2014.02.004
   PubMed Web of Science ®Google Scholar
• Zhang N, Jiang S, Du L. Current advancements and potential strategies in the development of MERS-CoV vaccines. Expert Rev Vaccines 2014; 13:761-74; PMID:24766432; https://doi.org/10.1586/14760584.2014.912134; http://www.ncbi.nlm.nih.gov/pubmed/24766432
   PubMed Web of Science ®Google Scholar
• Tang J, Zhang N, Tao X, Zhao G, Guo Y, Tseng CT, Jiang S, Du L, Zhou Y. Optimization of antigen dose for a receptor-binding domain-based subunit vaccine against MERS coronavirus. Hum Vaccin Immunother 2015; 11:1244-50; PMID:25874632; https://doi.org/10.1080/21645515.2015.1021527; http://www.ncbi.nlm.nih.gov/pubmed/25874632
   PubMed Web of Science ®Google Scholar
• Mou H, Raj VS, van Kuppeveld FJ, Rottier PJ, Haagmans BL, Bosch BJ. The receptor binding domain of the new Middle East respiratory syndrome coronavirus maps to a 231-residue region in the spike protein that efficiently elicits neutralizing antibodies. J Virol 2013; 87:9379-83; PMID:23785207; https://doi.org/10.1128/JVI.01277-13
   PubMed Web of Science ®Google Scholar
• Ma C, Wang L, Tao X, Zhang N, Yang Y, Tseng CT, Li F, Zhou Y, Jiang S, Du L. Searching for an ideal vaccine candidate among different MERS coronavirus receptor-binding fragments–the importance of immunofocusing in subunit vaccine design. Vaccine 2014; 32:6170-6; PMID:25240756; https://doi.org/10.1016/j.vaccine.2014.08.086
   PubMed Web of Science ®Google Scholar
• Zhang N, Channappanavar R, Ma C, Wang L, Tang J, Garron T, Tao X, Tasneem S, Lu L, Tseng CT, et al. Identification of an ideal adjuvant for receptor-binding domain-based subunit vaccines against Middle East respiratory syndrome coronavirus. Cell Mol Immunol 2016; 13:180-90; PMID:25640653; https://doi.org/10.1038/cmi.2015.03; http://www.ncbi.nlm.nih.gov/pubmed/25640653
   PubMed Web of Science ®Google Scholar
• Tai W, Wang Y, Fett CA, Zhao G, Li F, Perlman S, Jiang S, Zhou Y, L D. Recombinant receptor-binding domains of multiple MERS-coronaviruses induce cross-neutralizing antibodies against divergent human and camel MERS-coronaviruses and antibody-escape mutants. J Virol 2016; 91:pii: e01651-16; https://doi.org/10.1128/JVI.01651-16
   Web of Science ®Google Scholar
• Tai W, Zhao G, Sun S, Guo Y, Wang Y, Tao X, Tseng CK, Li F, Jiang S, Du L, et al. A recombinant receptor-binding domain of MERS-CoV in trimeric form protects human dipeptidyl peptidase 4 (hDPP4) transgenic mice from MERS-CoV infection. Virology 2016; 499:375-82; PMID:27750111; https://doi.org/10.1016/j.virol.2016.10.005
   PubMed Web of Science ®Google Scholar
• Zhao G, Jiang Y, Qiu H, Gao T, Zeng Y, Guo Y, Yu H, Li J, Kou Z, Du L, et al. Multi-organ damage in human dipeptidyl peptidase 4 transgenic mice infected with Middle East respiratory syndrome-coronavirus. PloS One 2015; 10:e0145561; PMID:26701103; https://doi.org/10.1371/journal.pone.0145561
   PubMed Web of Science ®Google Scholar
• Tao X, Garron T, Agrawal AS, Algaissi A, Peng BH, Wakamiya M, Chan TS, Lu L, Du L, Jiang S, et al. Characterization and demonstration of the value of a lethal mouse model of Middle East respiratory syndrome coronavirus infection and disease. J Virol 2015; 90:57-67; PMID:26446606; https://doi.org/10.1128/JVI.02009-15
   PubMed Web of Science ®Google Scholar
• Du L, Tai W, Yang Y, Zhao G, Zhu Q, Sun S, Liu C, Tao X, Tseng CK, Perlman S, et al. Introduction of neutralizing immunogenicity index to the rational design of MERS coronavirus subunit vaccines. Nat Commun 2016; 7:13473
   PubMed Web of Science ®Google Scholar
• Levin Y, Kochba E, Shukarev G, Rusch S, Herrera-Taracena G, van Damme P. A phase 1, open-label, randomized study to compare the immunogenicity and safety of different administration routes and doses of virosomal influenza vaccine in elderly. Vaccine 2016; 34:5262-72; PMID:27667332; https://doi.org/10.1016/j.vaccine.2016.09.008
   PubMed Web of Science ®Google Scholar
• Gasparini R, Schioppa F, Lattanzi M, Barone M, Casula D, Pellegrini M, Veitch K, Gaitatzis N. Impact of prior or concomitant seasonal influenza vaccination on MF59-adjuvanted H1N1v vaccine (Focetria) in adult and elderly subjects. Int J Clin Pract 2010; 64:432-8; PMID:20039974; https://doi.org/10.1111/j.1742-1241.2009.02309.x
   PubMed Web of Science ®Google Scholar
• Black S. Safety and effectiveness of MF-59 adjuvanted influenza vaccines in children and adults. Vaccine 2015; 8:062
   Google Scholar
• Lee S, Nguyen MT. Recent advances of vaccine adjuvants for infectious diseases. Immune Netw 2015; 15:51-7; PMID:25922593; https://doi.org/10.4110/in.2015.15.2.51
   PubMed Web of Science ®Google Scholar
• O'Hagan DT, Ott GS, Nest GV, Rappuoli R, Giudice GD. The history of MF59(R) adjuvant: a phoenix that arose from the ashes. Expert Rev Vaccines 2013; 12:13-30; PMID:23256736; https://doi.org/10.1586/erv.12.140
   PubMed Web of Science ®Google Scholar
• Fouda GG, Cunningham CK, McFarland EJ, Borkowsky W, Muresan P, Pollara J, Song LY, Liebl BE, Whitaker K, Shen X, et al. Infant HIV type 1 gp120 vaccination elicits robust and durable anti-V1V2 immunoglobulin G responses and only rare envelope-specific immunoglobulin A responses. J Infect Dis 2015; 211:508-17; PMID:25170104; https://doi.org/10.1093/infdis/jiu444
   PubMed Web of Science ®Google Scholar
• Riley S, Wu JT, Leung GM. Optimizing the dose of pre-pandemic influenza vaccines to reduce the infection attack rate. PLoS Med 2007; 4:e218; PMID:17579511; https://doi.org/10.1371/journal.pmed.0040218; http://www.ncbi.nlm.nih.gov/pubmed/17579511
   PubMed Web of Science ®Google Scholar
• Zhao G, Du L, Ma C, Li Y, Li L, Poon VK, Wang L, Yu F, Zheng BJ, Jiang S, et al. A safe and convenient pseudovirus-based inhibition assay to detect neutralizing antibodies and screen for viral entry inhibitors against the novel human coronavirus MERS-CoV. Virol J 2013; 10:266; PMID:23978242; https://doi.org/10.1186/1743-422X-10-266; http://www.ncbi.nlm.nih.gov/pubmed/23978242
   PubMed Web of Science ®Google Scholar
• Du L, He Y, Wang Y, Zhang H, Ma S, Wong CK, Wu SH, Ng F, Huang JD, Yuen KY, et al. Recombinant adeno-associated virus expressing the receptor-binding domain of severe acute respiratory syndrome coronavirus S protein elicits neutralizing antibodies: Implication for developing SARS vaccines. Virology 2006; 353:6-16; PMID:16793110; https://doi.org/10.1016/j.virol.2006.03.049; http://www.ncbi.nlm.nih.gov/pubmed/16793110
   PubMed Web of Science ®Google Scholar
• Cao Z, Liu L, Du L, Zhang C, Jiang S, Li T, He Y. Potent and persistent antibody responses against the receptor-binding domain of SARS-CoV spike protein in recovered patients. Virol J 2010; 7:299; PMID:21047436; https://doi.org/10.1186/1743-422X-7-299; http://www.ncbi.nlm.nih.gov/pubmed/21047436
   PubMed Web of Science ®Google Scholar
• Sui J, Deming M, Rockx B, Liddington RC, Zhu QK, Baric RS, Marasco WA. Effects of human anti-spike protein receptor binding domain antibodies on severe acute respiratory syndrome coronavirus neutralization escape and fitness. J Virol 2014; 88:13769-80; PMID:25231316; https://doi.org/10.1128/JVI.02232-14; http://www.ncbi.nlm.nih.gov/pubmed/25231316
   PubMed Web of Science ®Google Scholar
• Levine L, Edsall G. Tetanus toxoid: what determines reaction proneness? J Infect Dis 1981; 144:376; PMID:7288216; https://doi.org/10.1093/infdis/144.4.376
   PubMed Web of Science ®Google Scholar
• Edsall G, Elliott MW, Peebles TC, Eldred MC. Excessive use of tetanus toxoid boosters. JAMA 1967; 202:111-3; PMID:6071998; https://doi.org/10.1001/jama.202.1.111
   PubMed Web of Science ®Google Scholar
• Visciano ML, Tagliamonte M, Tornesello ML, Buonaguro FM, Buonaguro L. Effects of adjuvants on IgG subclasses elicited by virus-like particles. J Transl Med 2012; 10:1479-5876; https://doi.org/10.1186/1479-5876-10-4
   Web of Science ®Google Scholar
• Schulte S, Sukhova GK, Libby P. Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis. Am J Pathol 2008; 172:1500-8; PMID:18467709; https://doi.org/10.2353/ajpath.2008.070776
   PubMed Web of Science ®Google Scholar
• Crank MC, Gordon IJ, Yamshchikov GV, Sitar S, Hu Z, Enama ME, Holman LA, Bailer RT, Pearce MB, Koup RA, et al. Phase 1 study of pandemic H1 DNA vaccine in healthy adults. PloS One 2015; 10:e0123969; PMID:25884189; https://doi.org/10.1371/journal.pone.0123969; http://www.ncbi.nlm.nih.gov/pubmed/25884189
   PubMed Web of Science ®Google Scholar
• Meyer RG, Britten CM, Siepmann U, Petzold B, Sagban TA, Lehr HA, Weigle B, Schmitz M, Mateo L, Schmidt B, et al. A phase I vaccination study with tyrosinase in patients with stage II melanoma using recombinant modified vaccinia virus Ankara (MVA-hTyr). Cancer Immunol Immunother 2005; 54:453-67; PMID:15627214; https://doi.org/10.1007/s00262-004-0616-7
   PubMed Web of Science ®Google Scholar
• Haagmans BL, van den Brand JM, Raj VS, Volz A, Wohlsein P, Smits SL, Schipper D, Bestebroer TM, Okba N, Fux R, et al. An orthopoxvirus-based vaccine reduces virus excretion after MERS-CoV infection in dromedary camels. Science 2016; 351:77-81; PMID:26678878; https://doi.org/10.1126/science.aad1283
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, He Y, Guo Y, Zheng BJ, Jiang S, Zhou Y. Receptor-binding domain of SARS-CoV spike protein induces long-term protective immunity in an animal model. Vaccine 2007; 25:2832-8; PMID:17092615; https://doi.org/10.1016/j.vaccine.2006.10.031
   PubMed Web of Science ®Google Scholar
• Du L, He Y, Zhou Y, Liu S, Zheng BJ, Jiang S. The spike protein of SARS-CoV–a target for vaccine and therapeutic development. Nat Rev Microbiol 2009; 7:226-36; PMID:19198616; https://doi.org/10.1038/nrmicro2090
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, Sun S, Zhang X, Zhou X, Guo Y, Li Y, Zhou Y, Jiang S. A critical HA1 neutralizing domain of H5N1 influenza in an optimal conformation induces strong cross-protection. PloS One 2013; 8:e53568; PMID:23320093; https://doi.org/10.1371/journal.pone.0053568; http://www.ncbi.nlm.nih.gov/pubmed/23320093
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, Zhang X, Liu Z, Yu H, Zheng BJ, Zhou Y, Jiang S. Development of a safe and convenient neutralization assay for rapid screening of influenza HA-specific neutralizing monoclonal antibodies. Biochem Biophys Res Commun 2010; 397:580-5; PMID:20617558; https://doi.org/10.1016/j.bbrc.2010.05.161; http://www.ncbi.nlm.nih.gov/pubmed/20617558
   PubMed Web of Science ®Google Scholar
• Liu C, Tang J, Ma Y, Liang X, Yang Y, Peng G, Qi Q, Jiang S, Li J, Du L, et al. Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J Virol 2015; 89:6121-5; PMID:25787280; https://doi.org/10.1128/JVI.00430-15
   PubMed Web of Science ®Google Scholar
• Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58:621-81; PMID:16968952; https://doi.org/10.1124/pr.58.3.10; http://www.ncbi.nlm.nih.gov/pubmed/16968952
   PubMed Web of Science ®Google Scholar