Expression of interferon gamma by a recombinant rabies virus strongly attenuates the pathogenicity of the virus via induction of type I interferon

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 312-322

  Barkhouse, Darryll A ^a,b   Garcia, Samantha A ^a,b   Bongiorno, Emily K ^a,b   Lebrun, Aurore ^a,b   Faber, Milosz ^a   Hooper, D Craig ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; NEUTRALIZING ANTIBODY; INTERFERON; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PATHOGENICITY; RABIES VIRUS; RHABDOVIRIDAE; T LYMPHOCYTE; VIRUS ENTRY; VIRUS GENOME; VIRUS REPLICATION; ANIMAL; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; RABIES; SECRETION (PROCESS); SURVIVAL;

ANIMALIA; MURINAE; MUS; RABIES VIRUS;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; INTERFERON TYPE I; INTERFERON-GAMMA; MICE; MICE, KNOCKOUT; RABIES; RABIES VIRUS; RECOMBINANT PROTEINS; SURVIVAL ANALYSIS;

EID: 84919458578     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01572-14     Document Type: Article

References (52)

1. Holloway BP, Obijeski JF. 1980. Rabies virus-induced RNA synthesis in BHK21 cells. J Gen Virol 49:181-195. http://dx.doi.org/10.1099/0022-1317-49-1-181.
2. Tordo N, Poch O, Ermine A, Keith G, Rougeon F. 1988. Completion of the rabies virus genome sequence determination: highly conserved domains among the L (polymerase) proteins of unsegmented negativestrand RNA viruses. Virology 165:565-576. http://dx.doi.org/10.1016/0042-6822(88)90600-9.
3. Knobel DL, Cleaveland S, Coleman PG, Fèvre EM, Meltzer MI, Miranda MEG, Shaw A, Zinsstag J, Meslin F-X. 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 83:360-368.
4. Hattwick MAW. 1972. Recovery from rabies: a case report. Ann Intern Med 76:931. http://dx.doi.org/10.7326/0003-4819-76-6-931.
5. Willoughby RE, Jr, Tieves KS, Hoffman GM, Ghanayem NS, Amlie-Lefond CM, Schwabe MJ, Chusid MJ, Rupprecht CE. 2005. Survival after treatment of rabies with induction of coma. N Engl J Med 352:2508-2514. http://dx.doi.org/10.1056/NEJMoa050382.
6. Phares TW, Kean RB, Mikheeva T, Hooper DC. 2006. Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system. J Immunol 176: 7666-7675. http://dx.doi.org/10.4049/jimmunol.176.12.7666.
7. Wang ZW, Sarmento L, Wang Y, Li X-Q, Dhingra V, Tseggai T, Jiang B, Fu ZF. 2005. Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol 79:12554-12565. http://dx.doi.org/10.1128/JVI.79.19.12554-12565.2005.
8. Roy A, Hooper DC. 2007. Lethal silver-haired bat rabies virus infection can be prevented by opening the blood-brain barrier. J Virol 81:7993-7998. http://dx.doi.org/10.1128/JVI.00710-07.
9. Jackson AC. 2011. Therapy of human rabies. Adv Virus Res 79:365-375. http://dx.doi.org/10.1016/B978-0-12-387040-7.00017-2.
10. Roy A, Phares TW, Koprowski H, Hooper DC. 2007. Failure to open the blood-brain barrier and deliver immune effectors to central nervous system tissues leads to the lethal outcome of silver-haired bat rabies virus infection. J Virol 81:1110-1118. http://dx.doi.org/10.1128/JVI.01964-06.
11. Baer GM, Shaddock JH, Williams LW. 1975. Prolonging morbidity in rabid dogs by intrathecal injection of attenuated rabies vaccine. Infect Immun 12:98-103.
12. Faber M, Li J, Kean RB, Hooper DC, Alugupalli KR, Dietzschold B. 2009. Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc Natl Acad Sci USA 106:11300-11305. http://dx.doi.org/10.1073/pnas.0905640106.
13. Warrell MJ, White NJ, Looareesuwan S, Phillips RE, Suntharasamai P, Chanthavanich P, Riganti M, Fisher-Hoch SP, Nicholson KG, Manatsathit S. 1989. Failure of interferon alfa and tribavirin in rabies encephalitis. BMJ 299:830-833. http://dx.doi.org/10.1136/bmj.299.6703.830.
14. Wheelock EF. 1965. Interferon-like virus-inhibitor induced in human leukocytes by phytohemagglutinin. Science 149:310-311. http://dx.doi.org/10.1126/science.149.3681.310.
15. Schroder K, Hertzog PJ, Ravasi T, Hume DA. 2004. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75:163-189. http://dx.doi.org/10.1189/jlb.0603252.
16. Der SD, Zhou A, Williams BR, Silverman RH. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 95:15623-15628. http://dx.doi.org/10.1073/pnas.95.26.15623.
17. Matsumoto M, Tanaka N, Harada H, Kimura T, Yokochi T, Kitagawa M, Schindler C, Taniguchi T. 1999. Activation of the transcription factor ISGF3 by interferon-gamma. Biol Chem 380:699-703.
18. Improta T, Pine R, Pfeffer LM. 1992. Interferon-gamma potentiates the antiviral activity and the expression of interferon-stimulated genes induced by interferon-alpha in U937 cells. J Interferon Res 12:87-94. http://dx.doi.org/10.1089/jir.1992.12.87.
19. Levy DE, Lew DJ, Decker T, Kessler DS, Darnell JE, Jr. 1990. Synergistic interaction between interferon-alpha and interferon-gamma through induced synthesis of one subunit of the transcription factor ISGF3. EMBO J 9:1105-1111.
20. Giavedoni L, Ahmad S, Jones L, Yilma T. 1997. Expression of gamma interferon by simian immunodeficiency virus increases attenuation and reduces postchallenge virus load in vaccinated rhesus macaques. J Virol 71:866-872.
21. Haq K, Elawadli I, Parvizi P, Mallick AI, Behboudi S, Sharif S. 2011. Interferon-γ influences immunity elicited by vaccines against very virulent Marek's disease virus. Antiviral Res 90:218-226. http://dx.doi.org/10.1016/j.antiviral.2011.04.001.
22. Mata-Espinosa DA, Mendoza-Rodríguez V, Aguilar-León D, Rosales R, López-Casillas F, Hernández-Pando R. 2008. Therapeutic effect of recombinant adenovirus encoding interferon-gamma in a murine model of progressive pulmonary tuberculosis. Mol Ther 16:1065-1072. http://dx.doi.org/10.1038/mt.2008.69.
23. Marciano BE, Wesley R, De Carlo ES, Anderson VL, Barnhart LA, Darnell D, Malech HL, Gallin JI, Holland SM. 2004. Long-term interferon-gamma therapy for patients with chronic granulomatous disease. Clin Infect Dis 39:692-699. http://dx.doi.org/10.1086/422993.
24. Prescrire International. 2006. Interferon gamma-1b: new indication. Severe malignant osteopetrosis: too many unknowns. Prescrire Int 15:179-180.
25. Yasukawa K, Saito S, Kubo T, Shibasaki Y, Yamaoka K, Hachimura H, Kuyama T, Amimoto A, Kumata T, Kitahara Y, Takenaka M, Matsumura H, Uno T, Uchino T, Takehara K, Nishida K, Kadoya M, Sato M, Kato K, Matsumoto K, Saito S, Shimoda T. 2010. Low-dose recombinant canine interferon-γ for treatment of canine atopic dermatitis: an open randomized comparative trial of two doses. Vet Dermatol 21:42-49. http://dx.doi.org/10.1111/j.1365-3164.2009.00764.x.
26. Phares TW, Fabis MJ, Brimer CM, Kean RB, Hooper DC. 2007. A peroxynitrite-dependent pathway is responsible for blood-brain barrier permeability changes during a central nervous system inflammatory response: TNF-alpha is neither necessary nor sufficient. J Immunol 178: 7334-7343. http://dx.doi.org/10.4049/jimmunol.178.11.7334.
27. Chai Q, He WQ, Zhou M, Lu H, Fu ZF. 2014. Enhancement of bloodbrain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol 88:4698-4710. http://dx.doi.org/10.1128/JVI.03149-13.
28. Müller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
29. Macpherson I, Stoker M. 1962. Polyoma transformation of hamster cell clones-an investigation of genetic factors affecting cell competence. Virology 16:147-151.
30. Conzelmann KK, Cox JH, Schneider LG, Thiel HJ. 1990. Molecular cloning and complete nucleotide sequence of the attenuated rabies virus SAD B19. Virology 175:485-499.
31. Schnell MJ, Mebatsion T, Conzelmann KK. 1994. Infectious rabies viruses from cloned cDNA. EMBO J 13:4195-4203.
32. Pulmanausahakul R, Faber M, Morimoto K, Spitsin S, Weihe E, Hooper DC, Schnell MJ, Dietzschold B. 2001. Overexpression of cytochrome c by a recombinant rabies virus attenuates pathogenicity and enhances antiviral immunity. J Virol 75:10800-10807. http://dx.doi.org/10.1128/JVI.75.22.10800-10807.2001.
33. Faber M, Bette M, Preuss MAR, Pulmanausahakul R, Rehnelt J, Schnell MJ, Dietzschold B, Weihe E. 2005. Overexpression of tumor necrosis factor alpha by a recombinant rabies virus attenuates replication in neurons and prevents lethal infection in mice. J Virol 79:15405-15416. http://dx.doi.org/10.1128/JVI.79.24.15405-15416.2005.
34. World Health Organization. 1996. Laboratory techniques in rabies, 4th ed. World Health Organization, Geneva, Switzerland.
35. Kuang Y, Lackay SN, Zhao L, Fu ZF. 2009. Role of chemokines in the enhancement of BBB permeability and inflammatory infiltration after rabies virus infection. Virus Res 144:18-26. http://dx.doi.org/10.1016/j.virusres.2009.03.014.
36. Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B. 1998. Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol 72:3711-3719.
37. Dietzschold B, Kao M, Zheng YM, Chen ZY, Maul G, Fu ZF, Rupprecht CE, Koprowski H. 1992. Delineation of putative mechanisms involved in antibody-mediated clearance of rabies virus from the central nervous system. Proc Natl Acad Sci USA 89:7252-7256.
38. Platanias LC. 2005. Mechanisms of type-I-and type-II-interferonmediated signalling. Nat Rev Immunol 5:375-386. http://dx.doi.org/10.1038/nri1604.
39. Lodmell DL, Wiedbrauk DL, Ewalt LC. 1989. Interferon induced within the central nervous system during infection is inconsequential as a mechanism responsible for murine resistance to street rabies virus. J Gen Virol 70:473-478.
40. Marcovistz R, Galabru J, Tsiang H, Hovanessian AG. 1986. Neutralization of interferon produced early during rabies virus infection in mice. J Gen Virol 67:387-390.
41. Fabis MJ, Phares TW, Kean RB, Koprowski H, Hooper DC. 2008. Blood-brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity. Proc Natl Acad Sci USA 105:15511-15516. http://dx.doi.org/10.1073/pnas.0807656105.
42. Roy A, Hooper DC. 2008. Immune evasion by rabies viruses through the maintenance of blood-brain barrier integrity. J Neurovirol 14:401-411. http://dx.doi.org/10.1080/13550280802235924.
43. Talaat KR, Luke CJ, Khurana S, Manischewitz J, King LR, McMahon BA, Karron RA, Lewis KDC, Qin J, Follmann DA, Golding H, Neuzil KM, Subbarao K. 2014. A live attenuated influenza A(H5N1) vaccine induces long-term immunity in the absence of a primary antibody response. J Infect Dis 209:1860-1869. http://dx.doi.org/10.1093/infdis/jiu123.
44. Irwin DJ, Wunner WH, Ertl HC, Jackson AC. 1999. Basis of rabies virus neurovirulence in mice: expression of major histocompatibility complex class I and class II mRNAs. J Neurovirol 5:485-494.
45. Griffin DE. 2010. Recovery from viral encephalomyelitis: immunemediated noncytolytic virus clearance from neurons. Immunol Res 47: 123-133. http://dx.doi.org/10.1007/s12026-009-8143-4.
46. Patterson CE, Lawrence DMP, Echols LA, Rall GF. 2002. Immunemediated protection from measles virus-induced central nervous system disease is noncytolytic and gamma interferon dependent. J Virol 76:4497-4506. http://dx.doi.org/10.1128/JVI.76.9.4497-4506.2002.
47. Chopy D, Pothlichet J, Lafage M, Megret F, Fiette L, Si-Tahar M, Lafon M. 2011. Ambivalent role of the innate immune response in rabies virus pathogenesis. J Virol 85:6657-6668. http://dx.doi.org/10.1128/JVI.00302-11.
48. Chopy D, Detje CN, Lafage M, Kalinke U, Lafon M. 2011. The type I interferon response bridles rabies virus infection and reduces pathogenicity. J Neurovirol 17:353-367. http://dx.doi.org/10.1007/s13365-011-0041-6.
49. Faul EJ, Wanjalla CN, McGettigan JP, Schnell MJ. 2008. Interferon-β expressed by a rabies virus-based HIV-1 vaccine vector serves as a molecular adjuvant and decreases pathogenicity. Virology 382:226-238. http://dx.doi.org/10.1016/j.virol.2008.09.019.
50. Brzózka K, Finke S, Conzelmann K-K. 2005. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J Virol 79:7673-7681. http://dx.doi.org/10.1128/JVI.79.12.7673-7681.2005.
51. Masatani T, Ito N, Ito Y, Nakagawa K, Abe M, Yamaoka S, Okadera K, Sugiyama M. 2013. Importance of rabies virus nucleoprotein in viral evasion of interferon response in the brain. Microbiol Immunol 57:511-517. http://dx.doi.org/10.1111/1348-0421.12058.
52. Rieder M, Brzozka K, Pfaller CK, Cox JH, Stitz L, Conzelmann K-K. 2011. Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J Virol 85:842-852. http://dx.doi.org/10.1128/JVI.01427-10.