Overcoming innate host resistance to vaccination: Employing a genetically distinct strain of murine cytomegalovirus avoids vector-mediated resistance to virally vectored immunocontraception

Vaccine

Volumn 27, Issue 38, 2009, Pages 5226-5232

  Nikolovski, Sonia ^a,c   Lloyd, Megan L ^a,c   Harvey, Nicole ^a,c   Hardy, Christopher M ^b,c   Shellam, Geoffrey R ^a,c   Redwood, Alec J ^a,c  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b CSIRO   (Australia)

^c UNIVERSITY OF CANBERRA   (Australia)

Author keywords

Cmv1; Immunocontraception; Innate immunity; Ly49H; m157; Vaccine vector; Zona pellucida

Indexed keywords

PROTEIN; UNCLASSIFIED DRUG; VIRUS VECTOR; ZONA PELLUCIDA 3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; EMBRYO; FEMALE; FEMALE FERTILITY; FEMALE STERILIZATION; GENETIC ENGINEERING; HISTOCOMPATIBILITY; HOST RESISTANCE; IMMUNOCONTRACEPTION; IMMUNOGENETICS; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VACCINATION; VIRUS STRAIN;

ANIMALS; CONTRACEPTION, IMMUNOLOGIC; EGG PROTEINS; FEMALE; IMMUNITY, INNATE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUROMEGALOVIRUS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; RECEPTORS, CELL SURFACE; STERILIZATION, REPRODUCTIVE; VACCINES, CONTRACEPTIVE;

EID: 67749129350     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.06.064     Document Type: Article

References (53)

1. Fayer-Hosken R.A., Grobler D., Van Altena J.J., Bertschinger H.J., and Kirkpatrick J.F. Immunocontraception of African elephants. Nature 407 6801 (2000) 149
2. Kirkpatrick J.F., Liu I.M., Turner Jr. J.W., Naugle R., and Keiper R. Long-term effects of porcine zonae pellucidae immunocontraception on ovarian function in feral horses (Equus caballus). J Reprod Fertil 94 2 (1992) 437-444
3. Turner Jr. J.W., Liu I.K., Flanagan D.R., Bynum K.S., and Rutberg A.T. Porcine zona pellucida (PZP) immunocontraception of wild horses (Equus caballus) in Nevada: a 10 year study. Reprod Suppl 60 (2002) 177-186
4. Miller L.A., Johns B.E., and Killian G.J. Immunocontraception of white-tailed deer using native and recombinant zona pellucida vaccines. Anim Reprod Sci 63 3-4 (2000) 187-195
5. Fayrer-Hosken R. Controlling animal populations using anti-fertility vaccines. Reprod Domest Anim 43 July (Suppl. 2) (2008) 179-185
6. Shellam G.R. The potential of murine cytomegalovirus as a viral vector for immunocontraception. Reprod Fert Dev 6 3 (1994) 401-409
7. Lloyd M.L., Shellam G.R., Papadimitriou J.M., and Lawson M.A. Immunocontraception is induced in BALB/c mice inoculated with murine cytomegalovirus expressing mouse zona pellucida 3. Biol Reprod 68 6 (2003) 2024-2032
8. Lloyd M.L., Nikolovski S., Lawson M.A., and Shellam G.R. Innate antiviral resistance influences the efficacy of a recombinant murine cytomegalovirus immunocontraceptive vaccine. Vaccine 25 4 (2007) 679-690
9. Redwood A.J., Messerle M., Harvey N.L., Hardy C.M., Koszinowski U.H., Lawson M.A., et al. Use of a murine cytomegalovirus, K181-derived, bacterial artificial chromosome as a vaccine vector for immunocontraception. J Virol 79 5 (2005) 2998-3008
10. Redwood A.J., Harvey N.L., Lloyd M.L., Lawson M.A., Hardy C.M., and Shellam G.R. Viral vectored immunocontraception: screening of multiple fertility antigens using murine cytomegalovirus as a vaccine vector. Vaccine 25 (2007) 698-708
11. Jackson R.J., Maguire D.J., Hinds L.A., and Ramshaw I.A. Infertility in mice induced by a recombinant ectromelia virus expressing mouse zona pellucida glycoprotein 3. Biol Reprod 58 1 (1998) 152-159
12. Redwood A.J., Smith L.M., Lloyd M., Hinds L.A., Hardy C.M., and Shellam G.R. Prospects for virally vectored immunocontraception in the control of wild house mice (Mus domesticus). Wildlife Res 34 7 (2007) 530-539
13. O'Leary S., Lloyd M.L., Shellam G.R., and Robertson S.A. Immunization with recombinant murine cytomegalovirus expressing murine zona pellucida 3 causes permanent infertility in BALB/c mice due to follicle depletion and ovulation failure. Biol Reprod 79 5 (2008) 849-860
14. Grundy J.E., Mackenzie J.S., and Stanley N.F. Influence of H-2 and non-H-2 genes on resistance to murine cytomegalovirus infection. Infect Immun 32 1 (1981) 277-286
15. Allan J.E., and Shellam G.R. Genetic control of murine cytomegalovirus infection: virus titres in resistant and susceptible strains of mice. Arch Virol 81 1-2 (1984) 139-150
16. Scalzo A.A., Fitzgerald N.A., Simmons A., La Vista A.B., and Shellam G.R. Cmv-1, a genetic locus that controls murine cytomegalovirus replication in the spleen. J Exp Med 171 5 (1990) 1469-1483
17. Rodriguez M., Sabastian P., Clark P., and Brown M.G. Cmv1-independent antiviral role of NK cells revealed in murine cytomegalovirus-infected New Zealand white mice. J Immunol 173 10 (2004) 6312-6318
18. Desrosiers M.P., Kielczewska A., Loredo-Osti J.C., Adam S.G., Makrigiannis A.P., Lemieux S., et al. Epistasis between mouse Klra and major histocompatibility complex class I loci is associated with a new mechanism of natural killer cell-mediated innate resistance to cytomegalovirus infection. Nat Genet 37 6 (2005) 593-599
19. Adam S.G., Caraux A., Fodil-Cornu N., Loredo-Osti J.C., Lesjean-Pottier S., Jaubert J., et al. Cmv4, a new locus linked to the NK cell gene complex, controls innate resistance to cytomegalovirus in wild-derived mice. J Immunol 176 9 (2006) 5478-5485
20. Scalzo A.A., Fitzgerald N.A., Wallace C.R., Gibbons A.E., Smart Y.C., Burton R.C., et al. The effect of the Cmv-1 resistance gene, which is linked to the natural killer cell gene complex, is mediated by natural killer cells. J Immunol 149 2 (1992) 581-589
21. Brown M.G., Dokun A.O., Heusel J.W., Smith H.R., Beckman D.L., Blattenberger E.A., et al. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292 5518 (2001) 934-937
22. Arase H., Mocarski E.S., Campbell A.E., Hill A.B., and Lanier L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296 5571 (2002) 1323-1326
23. Smith H.R., Heusel J.W., Mehta I.K., Kim S., Dorner B.G., Naidenko O.V., et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci USA 99 13 (2002) 8826-8831
24. Smith L.M., Shellam G.R., and Redwood A.J. Genes of murine cytomegalovirus exist as a number of distinct genotypes. Virology 352 2 (2006) 450-465
25. Corbett A.J., Forbes C.A., Moro D., and Scalzo A.A. Extensive sequence variation exists among isolates of murine cytomegalovirus within members of the m02 family of genes. J Gen Virol 88 Pt 3 (2007) 758-769
26. Smith L.M., McWhorter A.R., Masters L., Shellam G.R., and Redwood A.J. Laboratory strains of murine cytomegalovirus are genetically similar to but phenotypically distinct from wild strains of virus. J Virol 82 13 (2008) 6689-6696
27. Booth T.W., Scalzo A.A., Carrello C., Lyons P.A., Farrell H.E., Singleton G.R., et al. Molecular and biological characterization of new strains of murine cytomegalovirus isolated from wild mice. Arch Virol 132 1-2 (1993) 209-220
28. Voigt V., Forbes C.A., Tonkin J.N., Degli-Esposti M.A., Smith H.R., Yokoyama W.M., et al. Murine cytomegalovirus m157 mutation and variation leads to immune evasion of natural killer cells. Proc Natl Acad Sci USA 100 23 (2003) 13483-13488
29. Scalzo A.A., Manzur M., Forbes C.A., Brown M.G., and Shellam G.R. NK gene complex haplotype variability and host resistance alleles to murine cytomegalovirus in wild mouse populations. Immunol Cell Biol 83 2 (2005) 144-149
30. Scalzo A.A., Brown M.G., Chu D.T., Heusel J.W., Yokoyama W.M., and Forbes C.A. Development of intra-natural killer complex (NKC) recombinant and congenic mouse strains for mapping and functional analysis of NK cell regulatory loci. Immunogenetics 49 3 (1999) 238-241
31. Daniels K.A., Devora G., Lai W.C., O'Donnell C.L., Bennett M., and Welsh R.M. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med 194 1 (2001) 29-44
32. Lee S.H., Girard S., Macina D., Busa M., Zafer A., Belouchi A., et al. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genet 28 1 (2001) 42-45
33. Xu J., Dallas P.B., Lyons P.A., Shellam G.R., and Scalzo A.A. Identification of the glycoprotein H gene of murine cytomegalovirus. J Gen Virol 73 Pt 7 (1992) 1849-1854
34. Gorman S., Lloyd M., Smith L.M., McWhorter A.R., Lawson M.A., Redwood A.J., et al. Prior infection with murine cytomegalovirus (MCMV) limits the immunocontraceptive effects of an MCMV vector expressing the mouse zona-pellucida-3 protein. Vaccine 26 31 (2008) 3860-3869
35. Mercer J.A., Marks J.R., and Spector D.H. Molecular cloning and restriction endonuclease mapping of the murine cytomegalovirus genome (Smith Strain). Virology 129 1 (1983) 94-106
36. East I.J., Gulyas B.J., and Dean J. Monoclonal antibodies to the major protein of the murine zona pellucida: effects on fertilization and early development. Dev Biol 109 (1985) 268-273
37. Andrews D.M., Andoniou C.E., Fleming P., Smyth M.J., and Degli-Esposti M.A. The early kinetics of cytomegalovirus-specific CD8+ T cell responses are not affected by antigen load or the absence of perforin or IFN-{gamma}. J Virol (2008)
38. Su H.C., Nguyen K.B., Salazar-Mather T.P., Ruzek M.C., Dalod M.Y., and Biron C.A. NK cell functions restrain T cell responses during viral infections. Eur J Immunol 31 10 (2001) 3048-3055
39. Robbins S.H., Bessou G., Cornillon A., Zucchini N., Rupp B., Ruzsics Z., et al. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Path 3 8 (2007) 24
40. Bancroft G.J., Shellam G.R., and Chalmer J.E. Genetic influences on the augmentation of natural killer (NK) cells during murine cytomegalovirus infection: correlation with patterns of resistance. J Immunol 126 3 (1981) 988-994
41. Grundy J.E., and Melief C.J. Effect of Nu/Nu gene on genetically determined resistance to murine cytomegalovirus. J Gen Virol 61 Pt l (1982) 133-136
42. Kielczewska A., Pyzik M., Sun T., Krmpotic A., Lodoen M.B., Munks M.W., et al. Ly49P recognition of cytomegalovirus-infected cells expressing H2-Dk and CMV-encoded m04 correlates with the NK cell antiviral response. J Exp Med (2009) Epub ahead of print
43. Kleijnen M.F., Huppa J.B., Lucin P., Mukherjee S., Farrell H., Campbell A.E., et al. A mouse cytomegalovirus glycoprotein, gp34, forms a complex with folded class I MHC molecules in the ER which is not retained but is transported to the cell surface. EMBO J 16 4 (1997) 685-694
44. Kavanagh D.G., Gold M.C., Wagner M., Koszinowski U.H., and Hill A.B. The multiple immune-evasion genes of murine cytomegalovirus are not redundant: m4 and m152 inhibit antigen presentation in a complementary and cooperative fashion. J Exp Med 194 7 (2001) 967-977
45. Holtappels R., Gillert-Marien D., Thomas D., Podlech J., Deegen P., Herter S., et al. Cytomegalovirus encodes a positive regulator of antigen presentation. J Virol 80 15 (2006) 7613-7624
46. Wagner M., Gutermann A., Podlech J., Reddehase M.J., and Koszinowski U.H. Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J Exp Med 196 6 (2002) 805-816
47. Chalmer J.E., Mackenzie J.S., and Stanley N.F. Resistance to murine cytomegalovirus linked to the major histocompatibility complex of the mouse. J Gen Virol 37 1 (1977) 107-114
48. Cottingham M.G., van Maurik A., Zago M., Newton A.T., Anderson R.J., Howard M.K., et al. Different levels of immunogenicity of two strains of Fowlpox virus as recombinant vaccine vectors eliciting T-cell responses in heterologous prime-boost vaccination strategies. Clin Vaccine Immunol 13 7 (2006) 747-757
49. Anderson R.J., Hannan C.M., Gilbert S.C., Laidlaw S.M., Sheu E.G., Korten S., et al. Enhanced CD8+ T cell immune responses and protection elicited against Plasmodium berghei malaria by prime boost immunization regimens using a novel attenuated fowlpox virus. J Immunol 172 5 (2004) 3094-3100
50. Ramirez J.C., Gherardi M.M., and Esteban M. Biology of attenuated modified vaccinia virus Ankara recombinant vector in mice: virus fate and activation of B- and T-cell immune responses in comparison with the Western Reserve strain and advantages as a vaccine. J Virol 74 2 (2000) 923-933
51. Vogels R., Zuijdgeest D., van Rijnsoever R., Hartkoorn E., Damen I., de Bethune M.P., et al. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J Virol 77 15 (2003) 8263-8271
52. Roy S., Zhi Y., Kobinger G.P., Figueredo J., Calcedo R., Miller J.R., et al. Generation of an adenoviral vaccine vector based on simian adenovirus 21. J Gen Virol 87 Pt 9 (2006) 2477-2485
53. Farina S.F., Gao G.P., Xiang Z.Q., Rux J.J., Burnett R.M., Alvira M.R., et al. Replication-defective vector based on a chimpanzee adenovirus. J Virol 75 23 (2001) 11603-11613