Abstract
This review considers properties of secreted cysteine proteinases of protozoa, bacteria, and viruses and presents information on the contemporary taxonomy of cysteine proteinases. Literature data on the structure and physicochemical and enzymatic properties of these enzymes are reviewed. High interest in cysteine proteinases is explained by the discovery of these enzymes mostly in pathogenic organisms. The role of the proteinases in pathogenesis of several severe diseases of human and animals is discussed.
Key words: cysteine proteinases, properties, protozoa, bacteria, viruses
Abbreviations
- DTT
dithiothreitol
- FMDV
foot-and-mouth disease virus
- RDRP
RNA-dependent RNA polymerase
- TLCK
tosyl-L-lysine chloromethyl ketone
- TPCK
tosyl-L-phenylalanine chloromethyl ketone
Footnotes
Original Russian Text © G. N. Rudenskaya, D. V. Pupov, 2008, published in Biokhimiya, 2008, Vol. 73, No. 1, pp. 3–17.
References
- 1.Rosenthal P. J., McKerrow J. H., Aikawa M., Nagasawa H., Leech J. H. J. Clin. Invest. 1988;82:1560–1566. doi: 10.1172/JCI113766. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Shenai B. R., Sijwali P. S., Singh A., Rosenthal P. J. J. Biol. Chem. 2000;275:29000–29010. doi: 10.1074/jbc.M004459200. [DOI] [PubMed] [Google Scholar]
- 3.Rosenthal P. J., Nelson R. G. Mol. Biochem. Parasitol. 1992;51:143–152. doi: 10.1016/0166-6851(92)90209-3. [DOI] [PubMed] [Google Scholar]
- 4.Hanspal M. Biochim. Biophys. Acta. 2000;1493:242–245. doi: 10.1016/s0167-4781(00)00159-7. [DOI] [PubMed] [Google Scholar]
- 5.Sijwali P. S., Shenai B. R., Gut J., Singh A., Rosenthal P. J. Biochem. J. 2001;360:481–489. doi: 10.1042/0264-6021:3600481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Na B. K., Shenai B. R., Sijwali P. S., Choe Y., Pandey K. C., Singh A., Craik C. S., Rosenthal P. J. Biochem. J. 2004;378:529–538. doi: 10.1042/BJ20031487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Tannich E., Scholze H., Nickel R., Horstmann R. D. J. biol. Chem. 1991;266:4798–4803. [PubMed] [Google Scholar]
- 8.Scholze H., Schulte W. Biomed. Biochim. Acta. 1988;47:115–123. [PubMed] [Google Scholar]
- 9.Luaces A. L., Barrett A. J. Biochem. J. 1988;250:903–909. doi: 10.1042/bj2500903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Li E., Yang W. G., Zhang T., Stanley S. L., Jr. Infect. Immun. 1995;63:4150–4153. doi: 10.1128/iai.63.10.4150-4153.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Jacobs T., Bruchhaus I., Dandekar T., Tannich E., Leippe M. Mol. Microbiol. 1998;27:269–276. doi: 10.1046/j.1365-2958.1998.00662.x. [DOI] [PubMed] [Google Scholar]
- 12.Keene W. E., Petitt M. G., Allen S., McKerrow J. H. J. Exp. Med. 1986;163:536–549. doi: 10.1084/jem.163.3.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Spinella S., Levavasseur E., Petek F., Rigothier M. C. Eur. J. Biochem. 1999;266:170–180. doi: 10.1046/j.1432-1327.1999.00841.x. [DOI] [PubMed] [Google Scholar]
- 14.Bruchhaus I., Jacobs T., Leippe M., Tannich E. Mol. Microbiol. 1996;22:255–263. doi: 10.1046/j.1365-2958.1996.00111.x. [DOI] [PubMed] [Google Scholar]
- 15.Willhoeft U., Hamann L., Tannich E. Infect. Immun. 1999;67:5925–5929. doi: 10.1128/iai.67.11.5925-5929.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Que X., Reed S. L. Clin. Microbiol. Rev. 2000;13:196–206. doi: 10.1128/CMR.13.2.196-206.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Serveau C., Lalmanach G., Juliano M. A., Scharfstein J., Juliano L., Gauthier F. Biochem. J. 1996;313:951–956. doi: 10.1042/bj3130951. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Gillmor S. A., Craik C. S., Fletterick R. J. Protein Sci. 1997;6:1603–1611. doi: 10.1002/pro.5560060801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Turk B., Stoka V., Turk V., Johansson G., Cazzulo J. J., Bjork I. FEBS Lett. 1996;391:109–112. doi: 10.1016/0014-5793(96)00611-4. [DOI] [PubMed] [Google Scholar]
- 20.Stoka V., Nycander M., Lenarcic B., Labriola C., Cazzulo J. J., Bjork I., Turk V. FEBS Lett. 1995;370:101–104. doi: 10.1016/0014-5793(95)00798-E. [DOI] [PubMed] [Google Scholar]
- 21.Martinez J., Campetella O., Frasch A. C., Cazzulo J. J. Immunol. Lett. 1993;35:191–196. doi: 10.1016/0165-2478(93)90090-O. [DOI] [PubMed] [Google Scholar]
- 22.McGrath M. E., Eakin A. E., Engel J. C., McKerrow J. H., Craik C. S., Fletterick R. J. J. Mol. Biol. 1995;247:251–259. doi: 10.1006/jmbi.1994.0137. [DOI] [PubMed] [Google Scholar]
- 23.Yokoyama-Yasunaka J. K., Pral E. M., Oliveira O. C., Jr., Alfieri S. C., Stolf A. M. Acta Trop. 1994;57:307–315. doi: 10.1016/0001-706X(94)90076-0. [DOI] [PubMed] [Google Scholar]
- 24.Cazzulo J. J., Stoka V., Turk V. Biol. Chem. 1997;378:1–10. doi: 10.1515/bchm.1997.378.1.1. [DOI] [PubMed] [Google Scholar]
- 25.Robertson C. D., Coombs G. H. Mol. Biochem. Parasitol. 1990;42:269–276. doi: 10.1016/0166-6851(90)90170-Q. [DOI] [PubMed] [Google Scholar]
- 26.Souza A. E., Waugh S., Coombs G. H., Mottram J. C. FEBS Lett. 1992;311:124–127. doi: 10.1016/0014-5793(92)81382-V. [DOI] [PubMed] [Google Scholar]
- 27.Mottram J. C., Souza A. E., Hutchison J. E., Carter R., Frame M. J., Coombs G. H. Proc. Natl. Acad. Sci. USA. 1996;93:6008–6013. doi: 10.1073/pnas.93.12.6008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Mallinson D. J., Lockwood B. C., Coombs G. H., North M. J. Microbiology. 1994;140:2725–2735. doi: 10.1099/00221287-140-10-2725. [DOI] [PubMed] [Google Scholar]
- 29.Mallinson D. J., Livingstone J., Appleton K. M., Lees S. J., Coombs G. H., North M. J. Microbiology. 1995;141:3077–3085. doi: 10.1099/13500872-141-12-3077. [DOI] [PubMed] [Google Scholar]
- 30.Parenti D. M. J. Infect. Dis. 1989;160:1076–1080. doi: 10.1093/infdis/160.6.1076. [DOI] [PubMed] [Google Scholar]
- 31.Williams A. G., Coombs G. H. Int. J. Parasitol. 1995;25:771–778. doi: 10.1016/0020-7519(94)00201-X. [DOI] [PubMed] [Google Scholar]
- 32.Arroyo R., Alderete J. F. Infect. Immun. 1989;57:2991–2997. doi: 10.1128/iai.57.10.2991-2997.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Provenzano D., Alderete J. F. Infect. Immun. 1995;63:3388–3395. doi: 10.1128/iai.63.9.3388-3395.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Potempa J., Dubin A., Korzus G., Travis J. J. Biol. Chem. 1988;263:2664–2667. [PubMed] [Google Scholar]
- 35.Rzychon M., Sabat A., Kosowska K., Potempa J., Dubin A. Mol. Microbiol. 2003;49:1051–1066. doi: 10.1046/j.1365-2958.2003.03613.x. [DOI] [PubMed] [Google Scholar]
- 36.Filipek R., Rzychon M., Oleksy A., Gruca M., Dubin A., Potempa J., Bochtler M. J. Biol. Chem. 2003;278:40959–40966. doi: 10.1074/jbc.M302926200. [DOI] [PubMed] [Google Scholar]
- 37.Kembhavi A. A., Buttle D. J., Rauber P., Barrett A. J. FEBS Lett. 1991;283:277–280. doi: 10.1016/0014-5793(91)80607-5. [DOI] [PubMed] [Google Scholar]
- 38.Gilles A. M., Imhoff J. M., Keil B. J. Biol. Chem. 1979;254:1462–1468. [PubMed] [Google Scholar]
- 39.Ullmann D., Jakubke H. D. Eur. J. Biochem. 1994;223:865–872. doi: 10.1111/j.1432-1033.1994.tb19063.x. [DOI] [PubMed] [Google Scholar]
- 40.Dargatz H., Diefenthal T., Witte V., Reipen G., von Wettstein D. Mol. Gen. Genet. 1993;240:140–145. doi: 10.1007/BF00276893. [DOI] [PubMed] [Google Scholar]
- 41.Witte V., Wolf N., Dargatz H. Curr. Microbiol. 1996;33:281–286. doi: 10.1007/s002849900114. [DOI] [PubMed] [Google Scholar]
- 42.Porter W. H., Cunningham L. W., Mitchell W. M. J. Biol. Chem. 1971;246:7675–7682. [PubMed] [Google Scholar]
- 43.Siffert O., Emod I., Keil B. FEBS Lett. 1976;66:114–119. doi: 10.1016/0014-5793(76)80598-4. [DOI] [PubMed] [Google Scholar]
- 44.Gusman H., Grogan J., Kagan H. M., Troxler R. F., Oppenheim F. G. FEBS Lett. 2001;489:97–100. doi: 10.1016/S0014-5793(01)02077-4. [DOI] [PubMed] [Google Scholar]
- 45.Potempa J., Sroka A., Imamura T., Travis J. Curr. Protein Pept. Sci. 2003;4:397–407. doi: 10.2174/1389203033487036. [DOI] [PubMed] [Google Scholar]
- 46.Potempa J., Travis J. Acta Biochim. Pol. 1996;43:455–465. [PubMed] [Google Scholar]
- 47.Kadowaki T., Yoneda M., Okamoto K., Maeda K., Yamamoto K. J. Biol. Chem. 1994;269:21371–21378. [PubMed] [Google Scholar]
- 48.Pike R. N., Potempa J., McGraw W., Coetzer T. H., Travis J. J. Bacteriol. 1996;178:2876–2882. doi: 10.1128/jb.178.10.2876-2882.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Potempa J., Mikolajczyk-Pawlinska J., Brassell D., Nelson D., Thogersen I. B., Enghild J. J., Travis J. J. Biol. Chem. 1998;273:21648–21657. doi: 10.1074/jbc.273.34.21648. [DOI] [PubMed] [Google Scholar]
- 50.Pavloff N., Pemberton P. A., Potempa J., Chen W. C., Pike R. N., Prochazka V., Kiefer M. C., Travis J., Barr P. J. J. Biol. Chem. 1997;272:1595–1600. doi: 10.1074/jbc.272.3.1595. [DOI] [PubMed] [Google Scholar]
- 51.Eichinger A., Beisel H. G., Jacob U., Huber R., Medrano F. J., Banbula A., Potempa J., Travis J., Bode W. EMBO J. 1999;18:5453–5462. doi: 10.1093/emboj/18.20.5453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Imamura T., Banbula A., Pereira P. J., Travis J., Potempa J. J. Biol. Chem. 2001;276:18984–18991. doi: 10.1074/jbc.M006760200. [DOI] [PubMed] [Google Scholar]
- 53.Wingrove J. A., DiScipio R. G., Chen Z., Potempa J., Travis J., Hugli T. E. J. Biol. Chem. 1992;267:18902–18907. [PubMed] [Google Scholar]
- 54.Nelson D., Potempa J., Kordula T., Travis J. J. Biol. Chem. 1999;274:12245–12251. doi: 10.1074/jbc.274.18.12245. [DOI] [PubMed] [Google Scholar]
- 55.Gerwin B. I., Stein W. H., Moore S. J. Biol. Chem. 1966;241:3331–3339. [PubMed] [Google Scholar]
- 56.Liu T. Y., Elliott S. D. Nature. 1965;206:33–34. doi: 10.1038/206033a0. [DOI] [PubMed] [Google Scholar]
- 57.Kagawa T. F., Cooney J. C., Baker H. M., McSweeney S., Liu M., Gubba S., Musser J. M., Baker E. N. Proc. Natl. Acad. Sci. USA. 2000;97:2235–2240. doi: 10.1073/pnas.040549997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Lukomski S., Montgomery C. A., Rurangirwa J., Geske R. S., Barrish J. P., Adams G. J., Musser J. M. Infect. Immun. 1999;67:1779–1788. doi: 10.1128/iai.67.4.1779-1788.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Kapur V., Topouzis S., Majesky M. W., Li L. L., Hamrick M. R., Hamill R. J., Patti J. M., Musser J. M. Microb. Pathog. 1993;15:327–346. doi: 10.1006/mpat.1993.1083. [DOI] [PubMed] [Google Scholar]
- 60.Collin M., Olsen A. Infect. Immun. 2001;69:7187–7189. doi: 10.1128/IAI.69.11.7187-7189.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Kapur V., Majesky M. W., Li L. L., Black R. A., Musser J. M. Proc. Natl. Acad. Sci. USA. 1993;90:7676–7680. doi: 10.1073/pnas.90.16.7676. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Li F., Browning G. F., Studdert M. J., Crabb B. S. Proc. Natl. Acad. Sci. USA. 1996;93:990–995. doi: 10.1073/pnas.93.3.990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.Roberts P. J., Belsham G. J. Virology. 1995;213:140–146. doi: 10.1006/viro.1995.1554. [DOI] [PubMed] [Google Scholar]
- 64.Guarne A., Kirchweger R., Verdaguer N., Liebig H. D., Blaas D., Skern T., Fita I. Protein Sci. 1996;5:1931–1933. doi: 10.1002/pro.5560050921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Medina M., Domingo E., Brangwyn J. K., Belsham G. J. Virology. 1993;194:355–359. doi: 10.1006/viro.1993.1267. [DOI] [PubMed] [Google Scholar]
- 66.Piccone M. E., Rieder E., Mason P. W., Grubman M. J. J. Virol. 1995;69:5376–5382. doi: 10.1128/jvi.69.9.5376-5382.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 67.Brown C. C., Piccone M. E., Mason P. W., McKenna T. S., Grubman M. J. J. Virol. 1996;70:5638–5641. doi: 10.1128/jvi.70.8.5638-5641.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68.Bredenbeek P. J., Pachuk C. J., Noten A. F., Charite J., Luytjes W., Weiss S. R., Spaan W. J. Nucleic Acids Res. 1990;18:1825–1832. doi: 10.1093/nar/18.7.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69.Gorbalenya A. E., Koonin E. V., Lai M. M. FEBS Lett. 1991;288:201–205. doi: 10.1016/0014-5793(91)81034-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70.Bonilla P. J., Hughes S. A., Pinon J. D., Weiss S. R. Virology. 1995;209:489–497. doi: 10.1006/viro.1995.1281. [DOI] [PubMed] [Google Scholar]
- 71.Kim J. C., Spence R. A., Currier P. F., Lu X., Denison M. R. Virology. 1995;208:1–8. doi: 10.1006/viro.1995.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72.Den Boon J. A., Faaberg K. S., Meulenberg J. J., Wassenaar A. L., Plagemann P. G., Gorbalenya A. E., Snijder E. J. J. Virol. 1995;69:4500–4505. doi: 10.1128/jvi.69.7.4500-4505.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 73.De Groot R. J., Hardy W. R., Shirako Y., Strauss J. H. EMBO J. 1990;9:2631–2638. doi: 10.1002/j.1460-2075.1990.tb07445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74.Hardy W. R., Strauss J. H. J. Virol. 1989;63:4653–4664. doi: 10.1128/jvi.63.11.4653-4664.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75.Strauss E. G., de Groot R. J., Levinson R., Strauss J. H. Virology. 1992;191:932–940. doi: 10.1016/0042-6822(92)90268-T. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76.Lemm J. A., Rumenapf T., Strauss E. G., Strauss J. H., Rice C. M. EMBO J. 1994;13:2925–2934. doi: 10.1002/j.1460-2075.1994.tb06587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77.Shirako Y., Strauss J. H. J. Virol. 1994;68:1874–1885. doi: 10.1128/jvi.68.3.1874-1885.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Hanecak R., Semler B. L., Ariga H., Anderson C. W., Wimmer E. Cell. 1984;37:1063–1073. doi: 10.1016/0092-8674(84)90441-0. [DOI] [PubMed] [Google Scholar]
- 79.Brenner S. Nature. 1988;334:528–530. doi: 10.1038/334528a0. [DOI] [PubMed] [Google Scholar]
- 80.Ypma-Wong M. F., Filman D. J., Hogle J. M., Semler B. L. J. Biol. Chem. 1988;263:17846–17856. [PubMed] [Google Scholar]
- 81.Clark M. E., Hammerle T., Wimmer E., Dasgupta A. EMBO J. 1991;10:2941–2947. doi: 10.1002/j.1460-2075.1991.tb07844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82.Clark M. E., Lieberman P. M., Berk A. J., Dasgupta A. Mol. Cell. Biol. 1993;13:1232–1237. doi: 10.1128/mcb.13.2.1232. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 83.Joachims M., Harris K. S., Etchison D. Virology. 1995;211:451–461. doi: 10.1006/viro.1995.1427. [DOI] [PubMed] [Google Scholar]
- 84.Tesar M., Marquardt O. Virology. 1990;174:364–374. doi: 10.1016/0042-6822(90)90090-E. [DOI] [PubMed] [Google Scholar]
- 85.Andino R., Rieckhof G. E., Achacoso P. L., Baltimore D. EMBO J. 1993;12:3587–3598. doi: 10.1002/j.1460-2075.1993.tb06032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 86.Krausslich H. G., Nicklin M. J., Toyoda H., Etchison D., Wimmer E. J. Virol. 1987;61:2711–2718. doi: 10.1128/jvi.61.9.2711-2718.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 87.Bazan J. F., Fletterick R. J. Proc. Natl. Acad. Sci. USA. 1988;85:7872–7876. doi: 10.1073/pnas.85.21.7872. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 88.Sommergruber W., Ahorn H., Zophel A., Maurer-Fogy I., Fessl F., Schnorrenberg G., Liebig H. D., Blaas D., Kuechler E., Skern T. J. Biol. Chem. 1992;267:22639–22644. [PubMed] [Google Scholar]
- 89.Sommergruber W., Ahorn H., Klump H., Seipelt J., Zoephel A., Fessl F., Krystek E., Blaas D., Kuechler E., Liebig H. D., et al. Virology. 1994;198:741–745. doi: 10.1006/viro.1994.1089. [DOI] [PubMed] [Google Scholar]