Single-dose intranasal administration with mDEF201 (adenovirus vectored mouse interferon-alpha) confers protection from mortality in a lethal SARS-CoV BALB/c mouse model

Antiviral Research

Volumn 89, Issue 1, 2011, Pages 75-82

  Kumaki, Yohichi ^a   Ennis, Jane ^b   Rahbar, Ramtin ^b   Turner, Jeffrey D ^b   Wandersee, Miles K ^a   Smith, Aaron J ^a   Bailey, Kevin W ^a   Vest, Zachary G ^a   Madsen, Jason R ^a   Li, Joseph K K ^a   Barnard, Dale L ^a  

^a UTAH STATE UNIVERSITY   (United States)

^b Defyrus Inc   (Canada)

Author keywords

Interferon; MDEF201; Prophylaxis; SARS; Treatment

Indexed keywords

ADENOVIRUS VECTOR; ADENOVIRUS VECTORED MOUSE INTERFERON ALPHA; ALPHA INTERFERON; CARBOXYMETHYLCELLULOSE POLYCYTIDYLIC POLYINOSINIC ACID POLYLYSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; BODY WEIGHT; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; INFECTION PREVENTION; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SEVERE ACUTE RESPIRATORY SYNDROME;ED MOUSE INTERFERON ALPHA; SINGLE DRUG DOSE;

ADENOVIRIDAE; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIVIRAL AGENTS; BIOLOGICAL PRODUCTS; BODY WEIGHT; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; FEMALE; GENETIC VECTORS; HUMANS; INTERFERON-ALPHA; MICE; MICE, INBRED BALB C; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SURVIVAL ANALYSIS; VERO CELLS;

ADENOVIRIDAE; MUS; SARS CORONAVIRUS;

EID: 78650964144     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2010.11.007     Document Type: Article

References (51)

1. Ahlquist P. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science 2002, 296:1270-1273.
2. Anand K., Ziebuhr J., Wadhwani P., Mesters J.R., Hilgenfeld R. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 2003, 300:1763-1767.
3. Barnard D.L., Kumaki Y. Development in the search for the small-molecule inhibitors for treatment of severe acute respiratory syndrome coronavirus. Antiviral Research: Strategies in Antiviral Drug Discovery 2009, 209-222. ASM Press, Washington, DC. R.L. LaFemina (Ed.).
4. Barnard D.L., Day C.W., Bailey K., Heiner M., Montgomery R., Lauridsen L., Chan P.K., Sidwell R.W. Evaluation of immunomodulators, interferons and known in vitro SARS-coV inhibitors for inhibition of SARS-coV replication in BALB/c mice. Antivir. Chem. Chemother. 2006, 17:275-284.
5. Bell S.J., Fam C.M., Chlipala E.A., Carlson S.J., Lee J.I., Rosendahl M.S., Doherty D.H., Cox G.N. Enhanced circulating half-life and antitumor activity of a site-specific pegylated interferon-alpha protein therapeutic. Bioconjug. Chem. 2008, 19:299-305.
6. Blatt L.M., Davis J.M., Klein S.B., Taylor M.W. The biologic activity and molecular characterization of a novel synthetic interferon-alpha species, consensus interferon. J. Interferon Cytokine Res. 1996, 16:489-499.
7. Bosch B.J., Martina B.E., Van Der Zee R., Lepault J., Haijema B.J., Versluis C., Heck A.J., De Groot R., Osterhaus A.D., Rottier P.J. Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. U.S.A 2004, 101:8455-8460.
8. Brassard D.L., Grace M.J., Bordens R.W. Interferon-alpha as an immunotherapeutic protein. J. Leukoc. Biol. 2002, 71:565-581.
9. Chang Z., Babiuk L.A., Hu J. Therapeutic and prophylactic potential of small interfering RNAs against severe acute respiratory syndrome: progress to date. BioDrugs 2007, 21(1):9-15.
10. Chen J., Subbarao K. The immunobiology of SARS. Annu. Rev. Immunol. 2007, 25:443-472.
11. Chen F., Chan K.H., Jiang Y., Kao R.Y., Lu H.T., Fan K.W., Cheng V.C., Tsui W.H., Hung I.F., Lee T.S., Guan Y., Peiris J.S., Yuen K.Y. In vitro susceptibility of 10 clinical isolates of SARS coronavirus to selected antiviral compounds. J. Clin. Virol. 2004, 31(1):69-75.
12. Cinatl J., Morgenstern B., Bauer G., Chandra P., Rabenau H., Doerr H.W. Treatment of SARS with human interferons. Lancet 2003, 362:293-294.
13. Croyle M.A., Patel A., Tran K.N., Gray M., Zhang Y., Strong J.E., Feldmann H., Kobinger G.P. Nasal delivery of an adenovirus-based vaccine bypasses pre-existing immunity to the vaccine carrier and improves the immune response in mice. PLoS One 2008, 3:e3548.
14. Dahl H., Linde A., Strannegard O. In vitro inhibition of SARS virus replication by human interferons. Scand. J. Infect. Dis. 2004, 36(11-12):829-831.
15. Day C.W., Baric R., Cai S.X., Frieman M., Kumaki Y., Morrey J.D., Smee D.F., Barnard D.L. A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. Virology 2009, 395:210-222.
16. Drosten C., Gunther S., Preiser W., van der Werf S., Brodt H.R., Becker S., Rabenau H., Panning M., Kolesnikova L., Fouchier R.A., Berger A., Burguiere A.M., Cinatl J., Eickmann M., Escriou N., Grywna K., Kramme S., Manuguerra J.C., Muller S., Rickerts V., Sturmer M., Vieth S., Klenk H.D., Osterhaus A.D., Schmitz H., Doerr H.W. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003, 348:1967-1976.
17. Frantz S. Safety concerns raised over RNA interference. Nat. Rev. Drug. Discov. 2006, 5:528-529.
18. Gibson I. Antisense DNA and RNA strategies: new approaches to therapy. J. R. Coll. Physicians Lond. 1994, 28:507-511.
19. Groneberg D.A., Witt C., Wagner U., Chung K.F., Fischer A. Fundamentals of pulmonary drug delivery. Respir. Med. 2003, 97:382-387.
20. Groneberg D.A., Fischer A., Chung K.F., Daniel H. Molecular mechanisms of pulmonary peptidomimetic drug and peptide transport. Am. J. Respir. Cell Mol. Biol. 2004, 30:251-260.
21. Haagmans B.L., Kuiken T., Martina B.E., Fouchier R.A., Rimmelzwaan G.F., van Amerongen G., van Riel D., de Jong T., Itamura S., Chan K.H., Tashiro M., Osterhaus A.D. Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat. Med. 2004, 10:290-293.
22. Ho T.Y., Wu S.L., Chen J.C., Wei Y.C., Cheng S.E., Chang Y.H., Liu H.J., Hsiang C.Y. Design and biological activities of novel inhibitory peptides for SARS-CoV spike protein and angiotensin-converting enzyme 2 interaction. Antiviral Res. 2006, 69:70-76.
23. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:7034.
24. Johnson-Saliba M., Jans D.A. Gene therapy: optimising DNA delivery to the nucleus. Curr. Drug Targets 2001, 2:371-399.
25. Judge A.D., Sood V., Shaw J.R., Fang D., McClintock K., MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 2005, 23:457-462.
26. Kamitani W., Huang C., Narayanan K., Lokugamage K.G., Makino S. A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat. Struct. Mol. Biol. 2009, 16:1134-1140.
27. Katze M.G., Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., Penaranda S., Bankamp B., Maher K., Chen M.H., Tong S., Tamin A., Lowe L., Frace M., DeRisi J.L., Chen Q., Wang D., Erdman D.D., Peret T.C., Burns C., Ksiazek T.G., Rollin P.E., Sanchez A., Liffick S., Holloway B., Limor J., McCaustland K., Olsen-Rasmussen M., Fouchier R., Gunther S., Osterhaus A.D., Drosten C., Pallansch M.A., Anderson L.J., Bellini W.J. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 2003, 300:1394-1399.
28. Kopecky-Bromberg S.A., Martinez-Sobrido L., Frieman M., Baric R.A., Palese P. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J. Virol. 2007, 81:548-557.
29. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., Dowell S.F., Ling A.E., Humphrey C.D., Shieh W.J., Guarner J., Paddock C.D., Rota P., Fields B., DeRisi J., Yang J.Y., Cox N., Hughes J.M., LeDuc J.W., Bellini W.J., Anderson L.J. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 2003, 348:1953-1966.
30. Kumaki Y., Day C.W., Wandersee M.K., Schow B.P., Madsen J.S., Grant D., Roth J.P., Smee D.F., Blatt L.M., Barnard D.L. Interferon alfacon 1 inhibits SARS-CoV infection in human bronchial epithelial Calu-3 cells. Biochem. Biophys. Res. Commun. 2008, 371:110-113.
31. Kumaki Y., Day C.W., Bailey K.W., Wandersee M.K., Wong M.H., Madsen J.R., Madsen J.S., Nelson N.M., Hoopes J.D., Woolcott J.D., McLean T.Z., Blatt L.M., Salazar A.M., Smee D.F., Barnard D.L. Induction of interferon-gamma-inducible protein 10 by SARS-CoV infection, interferon alfacon 1 and interferon inducer in human bronchial epithelial Calu-3 cells and BALB/c mice. Antivir. Chem. Chemother. 2010, 20:169-177.
32. Kuri T., Zhang X., Habjan M., Martinez-Sobrido L., Garcia-Sastre A., Yuan Z., Weber F. Interferon priming enables cells to partially overturn the SARS coronavirus-induced block in innate immune activation. J. Gen. Virol. 2009, 2686-2694.
33. Leonard J.N., Schaffer D.V. Antiviral RNAi therapy: emerging approaches for hitting a moving target. Gene Ther. 2006, 13:532-540.
34. Lin R., Heylbroeck C., Pitha P.M., Hiscott J. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 1998, 18:2986-2996.
35. Loutfy M.R., Blatt L.M., Siminovitch K.A., Ward S., Wolff B., Lho H., Pham D.H., Deif H., LaMere E.A., Chang M., Kain K.C., Farcas G.A., Ferguson P., Latchford M., Levy G., Dennis J.W., Lai E.K., Fish E.N. Interferon alfacon-1 plus corticosteroids in severe acute respiratory syndrome: a preliminary study. JAMA 2003, 290:3222-3228.
36. Lu X., Pan J., Tao J., Guo D. SARS-CoV nucleocapsid protein antagonizes IFN-beta response by targeting initial step of IFN-beta induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes 2009, (Epub date: 2010/10/27). 10.1007/s11262-010-0544-x.
37. Paragas J., Blatt L.M., Hartmann C., Huggins J.W., Endy T.P. Interferon alfacon1 is an inhibitor of SARS-corona virus in cell-based models. Antiviral Res. 2005, 66:99-102.
38. Peiris J.S., Lai S.T., Poon L.L., Guan Y., Yam L.Y., Lim W., Nicholls J., Yee W.K., Yan W.W., Cheung M.T., Cheng V.C., Chan K.H., Tsang D.N., Yung R.W., Ng T.K., Yuen K.Y. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 2003, 361:1319-1325.
39. Roberts A., Deming D., Paddock C.D., Cheng A., Yount B., Vogel L., Herman B.D., Sheahan T., Heise M., Genrich G.L., Zaki S.R., Baric R., Subbarao K. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog. 2007, 3(1):e5.
40. Rockx B., Baas T., Zornetzer G.A., Haagmans B., Sheahan T., Frieman M., Dyer M.D., Teal T.H., Proll S., van den Brand J., Baric R. Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection. J. Virol. 2009, 83:7062-7074.
41. Sidwell R.W., Bailey K.W., Wong M.H., Huffman J.H. In vitro and in vivo sensitivity of a non-mouse-adapted influenza A (Beijing) virus infection to amantadine and ribavirin. Chemotherapy 1995, 41:455-461.
42. Smits S.L., de Lang A., van den Brand J.M.A., Leijten L.M., van Ijcken W.F., Eijkemans M.J.C., van Amerongen G., Kuiken T., Andeweg A.C., Osterhaus A.D.M.E., Haagmans B.L. Exacerbated innate host response to SARS-CoV in aged non-human primates. PLoS Pathog. 2010, 6:e1000756.
43. Spiegel M., Pichlmair A., Martinez-Sobrido L., Cros J., Garcia-Sastre A., Haller O., Weber F. Inhibition of Beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3. J. Virol. 2005, 79:2079-2086.
44. Ströher U., DiCaro A., Li Y., Strong J.E., Aoki F., Plummer F., Jones S.M., Feldmann H. Severe acute respiratory syndrome-related coronavirus is inhibited by interferon-α. J. Infect. Dis. 2004, 189:1164-1167.
45. Subbarao K., McAuliffe J., Vogel L., Fahle G., Fischer S., Tatti K., Packard M., Shieh W.J., Zaki S., Murphy B. Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. J. Virol. 2004, 78:3572-3577.
46. Sui J., Li W., Murakami A., Tamin A., Matthews L.J., Wong S.K., Moore M.J., Tallarico A.S., Olurinde M., Choe H., Anderson L.J., Bellini W.J., Farzan M., Marasco W.A. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc. Natl. Acad. Sci. U.S.A 2004, 101:2536-2541.
47. Tan E.L., Ooi E.E., Lin C.Y., Tan H.C., Ling A.E., Lim B., Stanton L.W. Inhibition of SARS coronavirus infection in vitro with clinically approved antiviral drugs. Emerg. Infect. Dis. 2004, 10:581-586.
48. Weaver E.A., Barry M.A. Effects of shielding adenoviral vectors with polyethylene glycol on vector-specific and vaccine-mediated immune responses. Hum. Gene Ther. 2008, 19:1369-1382.
49. Wu J.Q., Barabe N.D., Huang Y.M., Rayner G.A., Christopher M.E., Schmaltz F.L. Pre- and post-exposure protection against Western equine encephalitis virus after single inoculation with adenovirus vector expressing interferon alpha. Virology 2007, 369:206-213.
50. Yang H., Yang M., Ding Y., Liu Y., Lou Z., Zhou Z., Sun L., Mo L., Ye S., Pang H., Gao G.F., Anand K., Bartlam M., Hilgenfeld R., Rao Z. The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc. Natl. Acad. Sci. U.S.A 2003, 100:13190-13195.
51. Zheng B., He M.L., Wong K.L., Lum C.T., Poon L.L., Peng Y., Guan Y., Lin M.C., Kung H.F. Potent inhibition of SARS-associated coronavirus (SCOV) infection and replication by type I interferons (IFN-alpha/beta) but not by type II interferon (IFN-gamma). J. Interferon Cytokine Res. 2004, 24:388-390.