Myxoma virus Serp2 is a weak inhibitor of granzyme B and interleukin- 1β-converting enzyme in vitro and unlike CrmA cannot block apoptosis in cowpox virus-infected cells

Journal of Virology

Volumn 73, Issue 8, 1999, Pages 6394-6404

  Turner, Peter C ^a   Sancho, M Carmen ^a,c   Thoennes, S R ^a   Caputo, A ^b   Bleackley, R C ^b   Moyer, Richard W ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GRANZYME B; INTERLEUKIN 1BETA CONVERTING ENZYME;

APOPTOSIS; ARTICLE; COMPLEX FORMATION; COVALENT BOND; COWPOX VIRUS; CROSS LINKING; ENZYME ACTIVITY; ENZYME INHIBITION; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POXVIRUS; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS VIRULENCE;

EID: 0032811049     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.8.6394-6404.1999     Document Type: Article

References (58)

1. Alcami, A., and G. L. Smith. 1995. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J. Virol. 69:4633-4639.
2. Ali, A. N., P. C. Turner, M. A. Brooks, and R. W. Moyer. 1994. The SPI-1 gene of rabbitpox virus determines host range and is required for hemorrhagic pock formation. Virology 202:305-314.
3. Alnemri, E. S., D. J. Livingston, D. W. Nicholson, G. Salvesen, N. A. Thornberry, W. W. Wong, and J. Yuan. 1996. Human ICE/ced-3 protease nomenclature. Cell 87:171.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Expression of proteins in mammalian cells using vaccinia viral vectors. In Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
5. Barry, M., S. Hnatiuk, K. Mossman, S. F. Lee, L. Boshkov, and G. McFadden. 1997. The myxoma virus M-T4 gene encodes a novel RDEL-containing protein that is retained within the endoplasmic reticulum and is important for the productive infection of lymphocytes. Virology 239:360-377.
6. Bieth, J. G. 1995. Theoretical and practical aspects of proteinase inhibition kinetics. Methods Enzymol. 248:59-84.
7. Bird, C. H., V. R. Sutton, J. Sun, C. E. Hirst, A. Novak, S. Kumar, J. A. Trapani, and P. I. Bird. 1998. Selective regulation of apoptosis: the cytotoxic lymphocyte serpin proteinase inhibitor 9 protects against granzyme B-mediated apoptosis without perturbing the Fas cell death pathway. Mol. Cell. Biol. 18:6387-6398.
8. Bump, N. J., M. Hackett, M. Hugunin, S. Seshagiri, K. Brady, P. Chen, C. Ferenz, S. Franklin, T. Ghayur, P. Li, P. Licari, J. Mankovitch, L. Shi, A. H. Greenberg, L. K. Miller, and W. W. Wong. 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269:1885-1888.
9. Chakrabarti, S., J. R. Sisler, and B. Moss. 1997. Compact, synthetic, vaccinia virus early/late promoter for protein expression. BioTechniques 23:1094-1097.
10. Cohen, G. M. 1997. Caspases: the executioners of apoptosis. Biochem. J. 324:1-16.
11. Coligan, J., B. Dunn, H. Ploegh, D. Spelcher, and P. Wingfield. 1998. In Current protocols in protein science. John Wiley & Sons, New York, N.Y.
12. Fathi, Z., P. Sridhar, R. F. Pacha, and R. C. Condit. 1986. Efficient targeted insertion of an unselected marker into the vaccinia virus genome. Virology 155:97-105.
13. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
14. Graham, K. A., A. S. Lalani, J. L. Macen, T. L. Ness, M. Barry, L.-Y. Liu, A. Lucas, I. Clark-Lewis, R. W. Moyer, and G. McFadden. 1997. The T1/35kDa family of poxvirus secreted proteins bind chemokines and modulate leukocyte influx into virus infected tissues. Virology 229:12-24.
15. r 38.5 and 40K, intracellular polypeptides that do not affect virus virulence in a murine intranasal model. Virology 206:136-147.
16. Komiyama, T., L. Quan, S. Snipas, C. A. Ray, D. J. Pickup, and G. Salvesen. 1994. In vitro expression of serpins, p. 305-312. In J. W. Crabb (ed.). Techniques in protein chemistry V. Academic Press, Inc., San Diego, Calif.
17. Komiyama, T., C. A. Ray, D. J. Pickup, A. D. Howard, N. A. Thornberry, E. P. Peterson, and G. Salvesen. 1994. Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J. Biol. Chem. 269:19331-19337.
18. Lalani, A. S., K. Graham, K. Mossman, K. Rajarathnam, I. Clark-Lewis, D. Kelvin, and G. McFadden. 1997. The purified myxoma virus gamma interferon receptor homolog M-T7 interacts with the heparin-binding domains of chemokines. J. Virol. 71:4356-4363.
19. Lucas, A., L.-Y. Liu, J. Macen, P. Nash, E. Dai, M. Stewart, K. Graham, W. Etches, L. Boshkov, P. N. Nation, D. Humen, M. L. Hobman, and G. McFadden. 1996. Virus-encoded serine proteinase-inhibitor SERP-1 inhibits atherosclerotic plaque development after balloon angioplasty. Circulation 94:2890-2900.
20. Macen, J., A. Takahashi, K. B. Moon, R. Nathaniel, P. C. Turner, and R. W. Moyer. 1998. Activation of caspases in pig kidney cells infected with wildtype and crmA/SPI-2 mutants of cowpox and rabbitpox viruses. J. Virol. 72:3524-3533.
21. Macen, J. L., R. S. Garner, P. Y. Musy, M. A. Brooks, P. C. Turner, R. W. Moyer, G. McFadden, and R. C. Bleackley. 1996. Differential inhibition of the Fas and granule-mediated cytolysis pathways by the orthopoxvirus cytokine response modifier A/SPI-2 and SPI-1 protein. Proc. Natl. Acad. Sci. USA 93:9108-9113.
22. Macen, J. L., C. Upton, N. Nation, and G. McFadden. 1993. SERP1, a serine proteinase inhibitor encoded by myxoma virus, is a secreted glycoprotein that interferes with inflammation. Virology 195:348-363.
23. Maksymowych, W. P., N. Nation, P. Nash, J. Macen, A. Lucas, G. McFadden, and A. S. Russell. 1996. Amelioration of antigen induced arthritis in rabbits treated with a secreted viral serine proteinase inhibitor. J. Rheumatol. 23: 878-882.
24. Massung, R. F., V. Jayarama, and R. W. Moyer. 1993. DNA sequence analysis of conserved and unique regions of swinepox virus: identification of genetic elements supporting phenotypic observations including a novel G protein-coupled receptor homologue. Virology 197:511-528.
25. McFadden, G., and M. Barry. 1998. How poxviruses oppose apoptosis. Semin. Virol. 8:429-442.
26. McFadden, G. 1994. Poxviruses: rabbit, hare, squirrel, and swinepox, p. 1153. In R. G. Webster and A. Granoff (ed.), Encyclopedia of virology. Academic Press, Inc., London, England.
27. McFadden, G., K. Graham, K. Ellison, M. Barry, J. Macen, M. Schreiber, K. Mossman, P. Nash, A. Lalani, and H. Everett. 1995. Interruption of cytokine networks by poxviruses: lessons from myxoma virus. J. Leukoc. Biol. 57:731-738.
28. Messud-Petit, F., J. Gelfi, M. Delverdier, M. F. Amardeilh, R. Py, G. Sutter, and S. Bertagnoli. 1998. Serp2, an inhibitor of the interleukin-1β-converting enzyme, is critical in the pathobiology of myxoma virus. J. Virol. 72:7830-7839.
29. Moss, B. 1996. Poxviridae: the viruses and their replication, p. 2637-2672. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology. Raven Press, New York, N.Y.
30. Moss, B., O. Elroy Stein, T. Mizukami, W. A. Alexander, and T. R. Fuerst. 1990. Product review. New mammalian expression vectors. Nature 348:91-92.
31. Mossman, K., C. Upton, R. M. Buller, and G. McFadden. 1995. Species specificity of ectromelia virus and vaccinia virus interferon-gamma binding proteins. Virology 208:762-769.
32. Mossman, K., C. Upton, and G. McFadden. 1995. The myxoma virus-soluble interferon-gamma receptor homolog, M-T7, inhibits interferon-gamma in a species-specific manner. J. Biol. Chem. 270:3031-3038.
33. Musy, P. Y. Unpublished data.
34. Odake, S., C. M. Kam, L. Narasimhan, M. Poe, J. T. Blake, O. Krahenbuhl, J. Tschopp, and J. C. Powers. 1991. Human and murine cytotoxic T lymphocyte serine proteases: subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins. Biochemistry 30:2217-2227.
35. Palumbo, G. J., D. J. Pickup, T. N. Fredrickson, L. J. McIntyre, and R. M. Buller. 1989. Inhibition of an inflammatory response is mediated by a 38-kDa protein of cowpox virus. Virology 172:262-273.
36. Petit, F., S. Bertagnoli, J. Gelfi, F. Fassy, C. Boucraut-Baralon, and A. Milon. 1996. Characterization of a myxoma virus-encoded serpin-like protein with activity against interleukin-1β-converting enzyme. J. Virol. 70: 5860-5866.
37. Pickup, D. J. 1994. Poxviral modifiers of cytokine responses to infection. Infect. Agents Dis. 3:116-127.
38. Pickup, D. J., B. S. Ink, W. Hu, C. A. Ray, and W. K. Joklik. 1986. Hemorrhage in lesions caused by cowpox virus is induced by a viral protein that is related to plasma protein inhibitors of serine proteases. Proc. Natl. Acad. Sci. USA 83:7698-7702.
39. Potempa, J., E. Korzus, and J. Travis. 1994. The serpin superfamily of proteinase inhibitors: structure, function, and regulation. J. Biol. Chem. 269:15957-15960.
40. Quan, L. T., A. Caputo, R. C. Bleackley, D. J. Pickup, and G. S. Salvesen. 1995. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J. Biol. Chem. 270:10377-10379.
41. Ray, C. A., R. A. Black, S. R. Kronheim, T. A. Greenstreet, P. R. Sleath, G. S. Salvesen, and D. J. Pickup. 1992. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 69:597-604.
42. Ray, C. A., and D. J. Pickup. 1996. The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene. Virology 217:384-391.
43. Smith, G. L. 1996. Virus proteins that bind cytokines, chemokines or interferons. Curr. Opin. Immunol. 8:467-471.
44. Srinivasula, S. M., M. Ahmad, T. Fernandes-Alnemri, G. Litwack, and E. S. Alnemri. 1996. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc. Natl. Acad. Sci. USA 93:14486-14491.
45. Sun, J., C. H. Bird, V. Sutton, L. McDonald, P. B. Coughlin, J. T. De, J. A. Trapanl, and P. I. Bird. 1996. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J. Biol. Chem. 271:27802-27809.
46. Takahashi, A., H. Hirata, S. Yonehara, Y. Imai, K.-K. Lee, R. W. Moyer, P. C. Turner, P. W. Mesner, T. Okazaki, H. Sawai, S. Kishi, K. Yamamoto, M. Okuma, and M. Sasada. 1997. Affinity labeling displays the stepwise activation of ICE-related proteases by Fas, staurosporine, and CrmA-sensitive caspase-8. Oncogene 14:2741-2752.
47. Takahashi, A., P. Y. Musy, L. M. Martins, G. G. Poirier, R. W. Moyer, and W. C. Earnshaw. 1996. CrmA/SPI-2 inhibition of an endogenous ICE-related protease responsible for lamin A cleavage and apoptotic nuclear fragmentation. J. Biol. Chem. 271:32487-32490.
48. Tewari, M., W. G. Telford, R. A. Miller, and V. M. Dixit. 1995. CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J. Biol. Chem. 270:22705-22708.
49. Thompson, J. P., P. C. Turner, A. N. Ali, B. C. Crenshaw, and R. W. Moyer. 1993. The effects of serpin gene mutations on the distinctive pathobiology of cowpox and rabbitpox virus following intranasal inoculation of BALB/c mice. Virology 197:328-338.
50. Thornbeny, N. A. 1994. Interleukin-1 beta converting enzyme. Methods Enzymol. 244:615-631.
51. Thornbeny, N. A., H. G. Bull, J. R. Calaycay, K. T. Chapman, A. D. Howard, M. J. Kostura, D. K. Miller, S. M. Molineaux, J. R. Weidner, J. Aunins, et al. 1992. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356:768-774.
52. Thornbeny, N. A., and Y. Lazebnik. 1998. Caspases: enemies within. Science 281:1312-1316.
53. Turner, P. C. 1997. Analysis of interactions between proteinases and serpins expressed in vitro using the TNT T7 Quick system. Promega Notes 60:11-13.
54. Turner, P. C., P. Y. Musy, and R. W. Moyer. 1995. Poxvirus serpins, p. 67-88. In G. McFadden (ed.), Viroceptors, virokines and related immune modulators encoded by DNA viruses. R. G. Landes Co., Austin, Tex.
55. Turner, P. C., D. C. Young, J. B. Flanegan, and R. W. Moyer. 1989. Interference with vaccinia virus growth caused by insertion of the coding sequence for poliovirus protease 2A. Virology 173:509-521.
56. Upton, C., J. L. Macen, D. S. Wishart, and G. McFadden. 1990. Myxoma virus and malignant rabbit fibroma virus encode a serpin-like protein important for virus virulence. Virology 179:618-631.
57. Xue, D., and R. Horvitz. 1995. Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377:248-251.
58. Zhou, Q., S. Snipas, K. Orth, M. Muzio, V. M. Dixit, and G. S. Salvesen. 1997. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem. 272:7797-7800.