Biotechnologia Acta

...

  • Increase font size
  • Default font size
  • Decrease font size
Home Archive 2013 № 6 PROTEIN INHIBITORS SYNTHESISED BY MICROORGANISMS O. V. Matseliukh, L. D. Varbanets
Print PDF

ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)

Biotechnologia Acta
v. 6, No. 6, 2013

"Biotechnologia Acta" v. 6, no 6, 2013
doi: 10.15407/biotech6.06.009
Р. 9-28, Bibliography 92, Russian.
Universal Decimal classification: 577.112:579.22

PROTEIN INHIBITORS SYNTHESISED BY MICROORGANISMS

O. V. Matseliukh, L. D. Varbanets

Zabolotny Institute of Microbiology and Virology of National Academy of Sciences of Ukraine, Kyiv

In a review the literature data on protein inhibitors of peptidases synthesised by different types of microorganisms are systematized. It is shown that at the present time on the basis of amino acid sequence homology protein inhibitors are grouped into 77 families, 29 of which include inhibitors of microorganisms. The mechanism of inhibition of peptidases by proteins may be related to their catalytic mechanism of action or include unrelated blocking of the active site or its surroundings. The structural elements of the protein inhibitors are responsible for binding to the peptidases, mostly include the N- or C-terminal sequences, the unprotected polypeptide loops (chains), which are acting independently or in combination with other elements. The basic properties, structural features and, where it is established, the functions of the protein inhibitors of peptidases are considered. Since some of these proteins effectively inhibit such peptidases as subtilisin, chymotrypsin, pancreatic elastase, their practical use in the treatment of diseases such as emphysema, arthritis, pancreatitis, thrombosis, hypertension, muscular dystrophy, cancer. It is suggested that the role of a bacterial homologue of Escherichia coli alphaacroglobulin, which is a periplasmic protein, is to protect the periplasmic space from the action of bacteria own proteases. Based on the specific properties of alpha-2-macroglobulin to bind endopeptidases active molecules, they are used in biotechnology to isolate endopeptidases from crude biological preparations and titration of its active centers. Some free–living bacteria are able to synthesize protein inhibitors to protect from the effects of its own enzymes, while the presence of these proteins in pathogens may play a certain role both in the infectious process and in the protection of the host proteases.

Key words: microorganisms, protein inhibitors of proteases.

© Palladin Institute of Biochemistry of National Academy of Sciences of Ukraine, 2008

  • References
    • 1. De Filippis V., Colombo G., Russo I. Probing the hirudin–thrombin interaction by incorporation of noncoded amino acids and molecular dynamics simulation. Biochemistry. 2002, V. 41, P. 13556–13569.
      http://dx.doi.org/10.1021/bi0203482

      2. Lomas D. A., Lourbakos A., Cumming S. A., Belorgey D. Hypersensitive mousetraps, alpha1-antitrypsin deficiency and dementia. Biochem. Soc. Trans. 2002, V. 30, P. 89–92.
      http://dx.doi.org/10.1042/bst0300089

      3. Bitoun E., Chavanas S., Irvine A.D. Netherton syndrome: disease expression and spectrum of SPINK5 mutations in 21 families. J. Invest. Dermatol. 2002, V. 118, P. 352–361.
      http://dx.doi.org/10.1046/j.1523-1747.2002.01603.x

      4. Ritchie B. C. Protease inhibitors in the treatment of hereditary angioedema. Transfus. Apheresis. Sci. 2003, V. 29, P. 259–267.
      http://dx.doi.org/10.1016/j.transci.2003.08.004

      5. Lehesjoki A. E. Molecular background of progressive myoclonus epilepsy. EMBO J. 2003, V. 22, P. 3473–3478.
      http://dx.doi.org/10.1093/emboj/cdg338

      6. Krol J., Kopitz C., Kirschenhofer A. Inhibition of intraperitoneal tumor growth of human ovarian cancer cells by bi- and trifunctional inhibitors of tumor–associated proteolytic systems. Biol. Chem. 2003, V. 384, P. 1097–1102.
      http://dx.doi.org/10.1515/bc.2003.122

      7. McKay T. R., Bell S., Tenev T. Procaspase 3 expression in ovarian carcinoma cells increases survivin transcription which can be countered with a domi­nant–negative mutant, survivin T34A; a combination gene therapy strategy. Onco­gene. 2003, V. 22, P. 3539–3547.
      http://dx.doi.org/10.1038/sj.onc.1206417

      8. Samac D. A., Smigocki A. C. Expression of oryzacystatin I and II in alfalfa increases resistance to the root–lesion nematode. Phytopathology. 2003, V. 93, P. 799–804.
      http://dx.doi.org/10.1094/PHYTO.2003.93.7.799

      9. Telang M., Srinivasan A., Patankar A. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry. 2003, V. 63, P. 643–652.
      http://dx.doi.org/10.1016/S0031-9422(03)00239-5

      10. Laskowski M. J., Kato I. Protein inhibitors of proteinases. Annu. Rev. Biochem. 1980, V. 49, P. 593–626.
      http://dx.doi.org/10.1146/annurev.bi.49.070180.003113

      11. Rawlings N. D., Barrett A. J., Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucl. Acids Res. 2012, V. 40, P. D343–D350.
      http://dx.doi.org/10.1093/nar/gkr987

      12. Otlewski J., Jelen F., Zakrzewska M., Oleksy A. The many faces of protease–protein inhibitor interaction. EMBO J. 2005, V. 24, P. 1303–1310.
      http://dx.doi.org/10.1038/sj.emboj.7600611

      13. Rzychon M., Filipek R., Sabat A. Staphostatins resemble lipocalins, not cystatins in fold. Prot. Sci. 2003, V. 12, P. 2252–2256.
      http://dx.doi.org/10.1110/ps.03247703

      14. Callus B.A., Vaux D. L. Caspase inhibitors: viral, cellular and chemical. Cell Death Differ. 2007, 14(1), 73–78.
      http://dx.doi.org/10.1038/sj.cdd.4402034

      15. Rzychon M., Chmiel D., Stec-Niemczyk J. Modes of inhibition of cysteine proteas. Acta Biochim. Pol. 2004, 51(4), 861–873.

      16. Kantyka T., Rawlings N. D., Potempaa J. Prokaryote–derived protein inhibitors of peptidases: a sketchy occurrence and mostly unknown function. Biochimie. 2010, 92(11), 1644–1656.
      http://dx.doi.org/10.1016/j.biochi.2010.06.004

      17. Shiga T., Wajima Z., Inoue T., Sakamoto A. Aprotinin in major orthopedic surgery: a systematic review of randomized controlled trials. Anesth. Analg. 2005, 101(6), 1602–1607.
      http://dx.doi.org/10.1213/01.ANE.0000180767.50529.45

      18. Hunt L. T., Dayhoff M. O. A surprising new protein superfamily containing ovalbumin, antithrombin-III, and alpha 1-proteinase inhibitor. Biochem. Biophys. Res. Commun. 1980, V. 95, P. 864–871.
      http://dx.doi.org/10.1016/0006-291X(80)90867-0

      19. Carrell R., Travis J. Alpha1-antitrypsin and the serpins: variation and countervariation. Trends Biochem. Sci. 1985, V. 10, P. 20–24.
      http://dx.doi.org/10.1016/0968-0004(85)90011-8

      20. Irving J. A., Pike R. N., Lesk A. M., Whisstock J. C. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res. 2000, V. 12, P. 1845–1864.
      http://dx.doi.org/10.1101/gr.GR-1478R

      21. Roberts T. H., Hejgaard J., Saunders N. F. Serpins in unicellular Eukarya, Archaea and Bacteria: sequence analysis and evolution. J. Mol. Evol. 2004, 59(4), 437–447.
      http://dx.doi.org/10.1007/s00239-004-2635-6

      22. Irving J. A., Steenbakkers P. J., Lesk A. M. Serpins in prokaryotes. Mol. Biol. Evol. 2002, 19(11), 1881–1890.
      http://dx.doi.org/10.1093/oxfordjournals.molbev.a004012

      23. Kang S., Barak Y., Lamed R. The functional repertoire of prokaryote cellulosomes includes the serpin superfamily of serine proteinase inhibitors. Mol. Microbiol. 2006, 60(6), 1344–1354.
      http://dx.doi.org/10.1111/j.1365-2958.2006.05182.x

      24. Fulton K. F., Buckle A. M., Cabrita L. D. The high resolution crystal structure of a native thermostable serpin reveals the complex mechanism underpinning the stressed to relaxed transition. J. Biol. Chem. 2005, V. 280, P. 8435–8442.
      http://dx.doi.org/10.1074/jbc.M410206200

      25. Irving J. A., Cabrita L. D., Rossjohn J., Pike R. N. The 1.5 A crystal structure of a prokaryote serpin: controlling conformational change in a heated environment. Structure. 2003, V. 11, P. 387–26.397.

      26. Cabrita L. D., Irving J. A., Pearce M. C. Aeropin from the extremophile Pyrobaculum aerophilum bypasses the serpin misfolding trap. J. Biol. Chem. 2007, 282(37), 26802–26809.
      http://dx.doi.org/10.1074/jbc.M705020200

      27. Khan M. S., Singh P., Azhar A. Serpin inhibition mechanism: a delicate balance between native metastable state and polymerization. J. Amino Acids. 2011, V. 2011, Avaiable at.: http://www.hindawi.com/ journals/jaa/2011/606797/.

      28. Li Y., Hu Z., Jordan F., Inouye M. Functional analysis of the propeptide of subtilisin E as an intramolecular chaperone for protein folding. Refolding and inhibitory abilities of propeptide mutants. J. Biol. Chem. 1995, V. 270, P. 25127–25132.
      http://dx.doi.org/10.1074/jbc.270.42.25127

      29. Kojima S., Minagawa T., Miura K. The propeptide of subtilisin BPN’ as a temporary inhibitor and effect of an amino acid replacement on its inhibitory activity. FEBS Lett. 1997, V. 411, P. 128–132.
      http://dx.doi.org/10.1016/S0014-5793(97)00678-9

      30. Gallagher T., Gilliland G., Wang L., Bryan P. The prosegment–subtilisin BPN’ complex: crystal structure of a specific «foldase». Structure. 1995, V. 3, P. 907–914.
      http://dx.doi.org/10.1016/S0969-2126(01)00225-8

      31. Maier K., Muller H., Tesch R. Primary structure of yeast proteinase B inhibitor 2. J. Biol. Chem. 1979, V. 254, P. 12555–12561.

      32. Kanaori K., Kamei K., Taniguchi M. Solution structure of marinostatin, a natural ester-linked protein protease inhibitor. Biochemistry. 2005, V. 44, P. 2462–2468.
      http://dx.doi.org/10.1021/bi048034x

      33. Taniguchi M., Kamei K., Kanaori K. Relationship between temporary inhibition and structure of disulfide–linkage analogs of marinostatin, a natural ester-linked protein protease inhibitor. J. Pept. Res. 2005, V. 66, P. 49–58.
      http://dx.doi.org/10.1111/j.1399-3011.2005.00271.x

      34. Imada C. Enzyme inhibitors of marine microbial origin with pharmaceutical importance. Mar. Biotechnol. (NY). 2004, V. 6, P. 193–198.
      http://dx.doi.org/10.1007/s10126-003-0027-3

      35. Eggers C. T., Wang S. X., Fletterick R. J., Craik C. S. The role of ecotin dimerization in protease inhibition. J. Mol. Biol. 2001, V. 308, P. 975–991.
      http://dx.doi.org/10.1006/jmbi.2001.4754

      36. McGrath M. E., Gillmor S. A., Fletterick R. J. Ecotin: lessons on survival in a protease–filled world. Prot. Sci. 1995,  4(2), 141–148.
      http://dx.doi.org/10.1002/pro.5560040201

      37. Yang S. Q., Wang C. I., Gillmor S. A. Ecotin: a serine protease inhibitor with two distinct and interacting binding sites. J. Mol. Biol. 1998, 279(4), 945–957.
      http://dx.doi.org/10.1006/jmbi.1998.1748

      38. Jin L., Pandey P., Babine R. E., Gorga J. C. Crystal structures of the FXIa catalytic domain in complex with ecotin mutants reveal substrate–like interactions. J. Biol. Chem. 2005, V. 280, P. 4704–4712.
      http://dx.doi.org/10.1074/jbc.M411309200

      39. Sathler P. C., Craik C. S., Takeuchi T. Engineering ecotin for identifying proteins with a trypsin fold. Appl. Biochem. Biotechnol. 2010, V. 160, P. 2355–2365.
      http://dx.doi.org/10.1007/s12010-009-8711-z

      40. Stoop A. A., Craik C. S. Engineering of a macromolecular scaffold to develop specific protease inhibitors. Nat. Biotechnol. 2003, V. 21, P. 1063–1068.
      http://dx.doi.org/10.1038/nbt860

      41. Stoop A. A., Joshi R. V., Eggers C. T., Craik C. S. Analysis of an engineered plasma kallikrein inhibitor and its effect on contact activation. Biol. Chem. 2010, V. 391, P. 425–433.
      http://dx.doi.org/10.1515/bc.2010.047

      42. Chung C. H., Ives H. E., Almeda S., Gold­berg A. L. Purification from Escherichia coli of a periplasmic protein that is a potent inhibitor of pancreatic proteases. J. Biol. Chem. 1983, V. 258, P. 11032–11038.

      43. Eggers C. T., Murray I. A., Delmar V. A. The periplasmic serine protease inhibitor ecotin protects bacteria against neutrophil elastase. Biochem J. 2004, V. 379, P. 107–118
      http://dx.doi.org/10.1042/bj20031790

      44. Murao S., Sato S. S-SI, a new alkaline protease inhibitor from Streptomyces albogriseolus S–3253. Agric. Biol. Chem. 1972, V. 36, P. 160–163.
      http://dx.doi.org/10.1271/bbb1961.36.160

      45. Taguchi S., Kojima S., Terabe M. Molecular phylogenetic characterization of Strepto­myces protease inhibitor family. J. Mol. Evol. 1997, 44(5), P. 542–551.
      http://dx.doi.org/10.1007/PL00006178

      46. Taguchi S., Yamada S., Kojima S., Momose H. An endogenous target protease, SAM-P26, of Streptomyces protease inhibitor (SSI): primary structure, enzymatic characterization, and its interaction with SSI. J. Biochem. 1998, V. 124, P. 804–810.
      http://dx.doi.org/10.1093/oxfordjournals.jbchem.a022183

      47. Kumazaki T., Kajiwara K., Kojima S. Interaction of Streptomyces subtilisin inhibitor (SSI) with Streptomyces griseus metallo-endopeptidase II (SGMP II). J. Biochem. 1993, V. 114, P. 570–575.

      48. Hiraga K., Suzuki T., Oda K. A novel double-headed proteinaceous inhibitor for metalloproteinase and serine proteinase. J. Biol. Chem. 2000, V. 275, P. 25173–25179.
      http://dx.doi.org/10.1074/jbc.M002623200

      49. Hirono S., Akagawa H., Mitsui Y., Iitaka Y. Crystal structure at 2.6 A resolution of the complex of subtilisin BPN’ with streptomyces subtilisin inhibitor. J. Mol. Biol. 1984, V. 178, P. 389–414.
      http://dx.doi.org/10.1016/0022-2836(84)90150-5

      50. Taguchi S., Odaka A., Watanabe Y., Momose H. Molecular characterization of a gene encoding extracellular serine protease isolated from a subtilisin inhibitor-deficient mutant of Streptomyces albogriseolus S-3253. Appl. Environ. Microbiol. 1995, V. 61, P. 180–186.

      51. Taguchi S., Suzuki M., Kojima S. Streptomyces serine protease (SAM-P20): recombinant production, characterization, and interaction with endogenous protease inhibitor. J. Bacteriol. 1995, V. 177, P. 6638–6643.

      52. Kato J. Y., Hirano S., Ohnishi Y., Horinouchi S. The Streptomyces subtilisin inhibitor (SSI) gene in Streptomyces coelicolor A3(2). Biosci. Biotechnol. Biochem. 2005, V. 69, P. 1624–1629.
      http://dx.doi.org/10.1271/bbb.69.1624

      53. Schmidt S., Adolf F., Fuchsbauer H. L. The transglutaminase activating metalloprotease inhibitor from Streptomyces mobaraensis is a glutamine and lysine donor substrate of the intrinsic transglutaminase. FEBS Lett. 2008, V. 582, P. 3132–3138.
      http://dx.doi.org/10.1016/j.febslet.2008.07.049

      54. Zhang D., Wang M., Du G. Surfactant protein of the Streptomyces subtilisin inhibitor family inhibits transglutaminase activation in Streptomyces hygroscopicus. J. Agric. Food Chem. 2008, V. 56, P. 3403–3408.
      http://dx.doi.org/10.1021/jf703567t

      55. Zhang D., Wang M., Wu J. Two different proteases from Streptomyces hygroscopicus are involved in transglutaminase activation. J. Agric. Food Chem. 2008, V. 56, P. 10261–10264.
      http://dx.doi.org/10.1021/jf8008519

      56. Lenarcic B., Ritonja A., Strukelj B. Equistatin, a new inhibitor of cysteine proteinases from Actinia equina, is structurally related to thyroglobulin type-1 domain. J. Biol. Chem. 1997, V. 272, P. 13899–13903.

      57. Mihelic M., Turk D. Two decades of thyroglobulin type-1 domain research. Biol. Chem. 2007, V. 388, P. 1123–1130.
      http://dx.doi.org/10.1515/BC.2007.155

      58. Ghigo E., Pretat L., Desnues B. Intracellular life of Coxiella burnetii in macrophages. Ann. NY Acad. Sci. 2009, V. 1166, P. 55–66.
      http://dx.doi.org/10.1111/j.1749-6632.2009.04515.x

      59. Saheki T., Matsuda Y., Holzer H. Purification and characterization of macromolecular inhibitors of proteinase A from yeast. Eur. J. Biochem. 1974, V. 47, P. 325–332.

      60. Phylip L. H., Lees W. E., Brownsey B. G. The potency and specificity of the interaction between the IA3 inhibitor and its target aspartic proteinase from Saccharomyces cerevisiae. J. Biol. Chem. 2001, V. 276, P. 2023–2030.
      http://dx.doi.org/10.1074/jbc.M008520200

      61. Green T. B., Ganesh O., Perry K. IA3, an aspartic proteinase inhibitor from Saccharo­myces cerevisiae, is intrinsically unstructured in solution. Biochemistry. 2004, V. 43, P. 4071–4081.
      http://dx.doi.org/10.1021/bi034823n

      62. Li M., Phylip L. H., Lees W. E. The aspartic proteinase from Saccharomyces cerevisiae folds its own inhibitor into a helix. Nat. Struct. Biol. 2000, V. 7, P. 113–117.
      http://dx.doi.org/10.1038/72378

      63. Oda K., Koyama T., Murao S. Purification and properties of a proteinaceous metallo-proteinase inhibitor from Streptomyces nigrescens TK–23. Biochim. Biophys. Acta. 1979, V. 571, P. 147–156.

      64. Murai H., Hara S., Ikenaka T. Amino acid sequence of Streptomyces metallo-proteinase inhibitor from Streptomyces nigrescens TK–23. J. Biochem. 1985, V. 97, P. 173–180.

      65. Ohno A., Tate S., Seeram S.S. NMR structure of the Streptomyces metalloproteinase inhibitor, SMPI, isolated from Streptomyces nigrescens TK–23: another example of an ancestral beta gamma-crystallin precursor structure. J. Mol. Biol. 1998, V. 282, P. 421–433.
      http://dx.doi.org/10.1016/0005-2744(79)90235-3

      66. Seeram S. S., Hiraga K., Oda K. Resynthesis of reactive site peptide bond and temporary inhibition of Streptomyces metalloproteinase inhibitor. J. Biochem. 1997,  V. 122, P. 788–794.
      http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021824

      67. Hiraga K., Seeram S. S., Tate S. Mutational analysis of the reactive site loop of Streptomyces metalloproteinase inhibitor, SMPI. J. Biochem. 1999, 125(1), 202–209.
      http://dx.doi.org/10.1093/oxfordjournals.jbchem.a022260

      68. Letoffe S., Delepelaire P., Wandersman C. Characterization of a protein inhibitor of extracellular proteases produced by Erwinia chrysanthemi. Mol. Microbiol. 1989, V. 3, P. 79–86.
      http://dx.doi.org/10.1111/j.1365-2958.1989.tb00106.x

      69. Feltzer R. E., Trent J. O., Gray R. D. Alkaline proteinase inhibitor of Pseudomonas aeruginosa: a mutational and molecular dynamics study of the role of N-terminal residues in the inhibition of Pseudomonas alkaline proteinase. J. Biol. Chem. 2003, V. 278, P. 25952–25957.
      http://dx.doi.org/10.1074/jbc.M212691200

      70. Arumugam S., Gray R. D., Lane A. N. NMR structure note: alkaline proteinase inhibitor APRin from Pseudomonas aeruginosa. J. Biomol. NMR. 2008, 40(3), 213–217.
      http://dx.doi.org/10.1007/s10858-008-9218-6

      71. Hege T., Feltzer R. E., Gray R. D., Baumann U. Crystal structure of a complex between Pseudomonas aeruginosa alkaline protease and its cognate inhibitor: inhibition by a zinc-NH2 coordinative bond . J. Biol. Chem. 2001, V. 276, P. 35087–35092.
      http://dx.doi.org/10.1074/jbc.M104020200

      72. Gray R. D., Trent J. O. Contribution of a single-turn alpha-helix to the conformational stability and activity of the alkaline proteinase inhibitor of Pseudomonas aeruginosa. Biochemistry. 2005, V. 44, P. 2469–2477.
      http://dx.doi.org/10.1021/bi048287q

      73. Barrett A. J., Starkey P. M. The interaction of alpha2-macroglobulin with proteinases. Characteristics and specificity of the reaction, and a hypothesis concerning its molecular mechanism. Biochem. J. 1973, V. 133, P. 709–724.
      http://dx.doi.org/10.1042/bj1330709

      74. Kolodziej S. J., Wagenknecht T., Strickland D. K., Stoops J. K. The three-dimensional structure of the human alpha 2-macroglobulin dimer reveals its structural organization in the tetrameric native and chymotrypsin alpha 2-macroglobulin complexes. J. Biol. Chem. 2002, V. 277, P. 28031–28037.
      http://dx.doi.org/10.1074/jbc.M202714200

      75. Armstrong P. B., Melchior R., Quigley J. P. Humoral immunity in long–lived arthropods. J. Insect. Physiol. 1996, V. 42, P. 53–64.
      http://dx.doi.org/10.1016/0022-1910(95)00082-8

      76. Little T. J., Colbourne J. K., Crease T. J. Molecular evolution of Daphnia immunity genes: polymorphism in a gram-negative binding protein gene and an alpha-2-macroglobulin gene. J. Mol. Evol. 2004, V. 59, P. 498–506.
      http://dx.doi.org/10.1007/s00239-004-2641-8

      77. Budd A., Blandin S., Levashina E. A., Gibson T. J. Bacterial alpha2-macroglobulins: colonization factors acquired by horizontal gene transfer from the metazoan genome?  Genome Biol. 2004, V. 5, Article R38.
      http://dx.doi.org/10.1186/gb-2004-5-6-r38

      78. Doan N., Gettins P. G. alpha-Macroglobulins are present in some gram-negative bacteria: characterization of the alpha2-macroglobulin from Escherichia coli. J. Biol. Chem. 2008. V. 283, P. 28747–28756.
      http://dx.doi.org/10.1074/jbc.M803127200

      79. Slot L. A., Hendil K. B. alpha-2-Macroglobulin used to isolate intracellular endopeptidases from mammalian cells in culture. Biochem. J. 1988, V. 255, P. 437–443.
      http://dx.doi.org/10.1042/bj2550437

      80. Osada T., Ookata K., Athauda S. B.. The active site titration of proteinases by using alpha2-macroglobulin and high-performance liquid chromatography. Anal. Biochem. 1992, V. 207, P. 76–79.
      http://dx.doi.org/10.1016/0003-2697(92)90503-Y

      81. Sanderson S. J., Westrop G. D., Scharfstein J. Functional conservation of a natural cysteine peptidase inhibitor in protozoan and bacterial pathogens. FEBS Lett. 2003, V. 542, P. 12–16.
      http://dx.doi.org/10.1016/S0014-5793(03)00327-2

      82. Ljunggren A., Redzynia I., Alvarez-Fernandez M. Crystal structure of the parasite protease inhibitor chagasin in complex with a host target cysteine protease. J. Mol. Biol. 2007, V. 371, P. 137–153.
      http://dx.doi.org/10.1016/j.jmb.2007.05.005

      83. Monteiro A. C., Abrahamson M., Lima A. P. Identification, characterization and localization of chagasin, a tight–binding cysteine protease inhibitor in Trypanosoma cruzi. J. Cell Sci. 2001, V. 114, P. 3933–3942.

      84. Riekenberg S., Witjes B., Saric M. Identification of EhICP1, a chagasin-like cysteine protease inhibitor of Entamoeba histolytica. FEBS Lett. 2005, V. 579, P. 1573–1578.
      http://dx.doi.org/10.1016/j.febslet.2005.01.067

      85. Kang J. M., Ju H. L., Yu J. R. Cryptostatin, a chagasin-family cysteine protease inhibitor of Cryptosporidium parvum. Parasitology. 2012, 139(8), 1029–1037.
      http://dx.doi.org/10.1017/S0031182012000297

      86. Matern H., Hoffmann M., Holzer H. Isolation and characterization of the carboxypeptidase Y inhibitor from yeast. Proc. Natl. Acad. Sci. USA. 1974, V. 71, P. 4874–4878.
      http://dx.doi.org/10.1073/pnas.71.12.4874

      87. Mima J., Hayashida M., Fujii T. Structure of the carboxypeptidase Y inhibitor IC in complex with the cognate proteinase reveals a novel mode of the proteinase–protein inhibitor interaction. J. Mol. Biol. 2005, 346(5), 1323–1334.
      http://dx.doi.org/10.1016/j.jmb.2004.12.051

      88. Dubin G., Wladyka B., Stec-Niemczyk J. The staphostatin family of cysteine protease inhibitors in the genus Staphylococcus as an example of parallel evolution of protease and inhibitor specificity. Biol. Chem. 2007, V. 388, P. 227–235.
      http://dx.doi.org/10.1515/BC.2007.025

      89. Filipek R., Potempa J., Bochtler M. A comparison of staphostatin B with standard mechanism serine protease inhibitors. J. Biol. Chem. 2005, V. 280, P. 14669–14674.
      http://dx.doi.org/10.1074/jbc.M411792200

      90. Kagawa T. F., O’Toole P. W., Cooney J. C. SpeB-Spi: a novel protease–inhibitor pair from Streptococcus pyogenes. Mol. Microbiol. 2005, V. 57, P. 650–666.
      http://dx.doi.org/10.1111/j.1365-2958.2005.04708.x

      91. Kagawa T. F., Cooney J. C., Baker H. M. Crystal structure of the zymogen form of the group A Streptococcus virulence factor SpeB: an integrin-binding cysteine protease. Proc. Natl. Acad. Sci. USA. 2000, V. 97, P. 2235–2240.
      http://dx.doi.org/10.1073/pnas.040549997

      92. Okumura Y., Ogawa K., Uchiya K. Biological properties of elastase inhibitor, AFLEI from Aspergillus flavus. Nippon. Ishinkin. Gakkai. Zasshi. 2008, V. 49, P. 87–93.
      http://dx.doi.org/10.3314/jjmm.49.87


 

Additional menu

Site search

Site navigation

Home Archive 2013 № 6 PROTEIN INHIBITORS SYNTHESISED BY MICROORGANISMS O. V. Matseliukh, L. D. Varbanets

Invitation to cooperation

Dear colleagues, we invite you to publish your articles in our journal.
© Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine, 2008.
All rights are reserved. Complete or partial reprint of the journal is possible only with the written permission of the publisher.
E-mail
for information: biotech@biochem.kiev.ua.