High-level production and purification of clostripain expressed in a virulence-attenuated strain of Clostridium perfringens

Protein Expression and Purification

Volumn 76, Issue 1, 2011, Pages 83-89

  Tanaka, Hiroaki ^a,b   Nariya, Hirofumi ^a   Suzuki, Motoo ^a   Houchi, Hitoshi ^b   Tamai, Eiji ^c   Miyata, Shigeru ^a   Okabe, Akinobu ^a  

^a KAGAWA UNIVERSITY   (Japan)

^b KAGAWA UNIVERSITY HOSPITAL   (Japan)

^c MATSUYAMA UNIVERSITY   (Japan)

Author keywords

Arginyl endopeptidase; Clostridium histolyticum; Clostridium perfringens; Clostripain; Cystein protease; Expression

Indexed keywords

CLOSTRIPAIN; CYSTEINE PROTEINASE; RECOMBINANT PROTEIN;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CLOSTRIDIUM PERFRINGENS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PATHOGENICITY; VIRULENCE;

AMINO ACID SEQUENCE; CHROMATOGRAPHY, AFFINITY; CLOSTRIDIUM PERFRINGENS; CYSTEINE ENDOPEPTIDASES; RECOMBINANT PROTEINS; VIRULENCE;

CLOSTRIDIUM HISTOLYTICUM; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM PERFRINGENS STR. 13;

EID: 78650169460     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2010.10.002     Document Type: Article

References (43)

1. J.M. Chen, N.D. Rawlings, R.A. Stevens, and A.J. Barrett Identification of the active site of legumain links it to caspases, clostripain and gingipains in a new clan of cysteine endopeptidases FEBS Lett. 441 1998 361 365 (Pubitemid 29065315)
2. A.J. Barrett, and N.D. Rawlings Evolutionary lines of cysteine peptidases Biol. Chem. 382 2001 727 733 (Pubitemid 32631709)
3. J. Potempa, A. Sroka, T. Imamura, and J. Travis Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes Curr. Protein Pept. Sci. 4 2003 397 407 (Pubitemid 37455910)
4. I. Cambra, F.J. Garcia, and M. Martinez Clan CD of cysteine peptidases as an example of evolutionary divergences in related protein families across plant clades Gene 449 2010 59 69
5. A.M. Gilles, A. De Wolf, and B. Keil Amino-acid sequences of the active-site sulfhydryl peptide and other thiol peptides from the cysteine proteinase alpha-clostripain Eur. J. Biochem. 130 1983 473 479
6. H. Dargatz, T. Diefenthal, V. Witte, G. Reipen, and D. von Wettstein The heterodimeric protease clostripain from Clostridium histolyticum is encoded by a single gene Mol. Gen. Genet. 240 1993 140 145 (Pubitemid 23205605)
7. D. Ullmann, and F. Bordusa Clostripain A.J. Barrett, N.D. Rawlings, J.F. Woessner, Handbook of Proteolytic Enzymes second ed. 2004 Elsevier Academic Press London 1317 1319
8. W.M. Mitchell Hydrolysis at arginylproline in polypeptides by clostridiopeptidase B Science 162 1968 374 375
9. R. Günther, A. Stein, and F. Bordusa Investigations on the enzyme specificity of clostripain: a new efficient biocatalyst for the synthesis of peptide isosteres J. Org. Chem. 65 2000 1672 1679 (Pubitemid 30161307)
10. N. Wehofsky, S. Thust, J. Burmeiste, S. Klussmann, and F. Bordusa All-d-polypeptides: novel targets for semisynthesis Angew. Chem., Int. Ed. Engl. 42 2003 677 679 (Pubitemid 36253873)
11. C.K. Kim, S.Y. Lee, O.J. Kwon, S.M. Lee, S.Y. Nah, and S.M. Jeong Secretory expression of active clostripain in Escherichia coli J. Biotechnol. 131 2007 346 352 (Pubitemid 47362431)
12. D. Liu, H. Sun, L. Zhang, S. Li, and Z. Qin High-level expression of milk-derived antihypertensive peptide in Escherichia coli and its bioactivity J. Agric. Food Chem. 55 2007 5109 5112 (Pubitemid 47056064)
13. C.J. Park, J.H. Lee, S.S. Hong, H.S. Lee, and S.C. Kim High-level expression of the angiotensin-converting-enzyme-inhibiting peptide, as tandem multimers in Escherichia coli Appl. Microbiol. Biotechnol. 50 1998 71 76 (Pubitemid 28372378)
14. J. Meiwes, W. Müller, S. Grabley, and M. Schudok Clostripain: production and use for peptide synthesis Biomed. Biochim. Acta 50 1991 S80 83
15. F. Bordusa Nonconventional amide bond formation catalysis: programming enzyme specificity with substrate mimetics Braz. J. Med. Biol. Res. 33 2000 469 485
16. B. Yoo, and K. Kirshenbaum Protease-mediated ligation of abiotic oligomers J. Am. Chem. Soc. 127 2005 17132 17133 (Pubitemid 41791002)
17. K. Guzik, M. Bzowska, J. Smagur, O. Krupa, M. Sieprawska, J. Travis, and J. Potempa A new insight into phagocytosis of apoptotic cells: proteolytic enzymes divert the recognition and clearance of polymorphonuclear leukocytes by macrophages Cell Death Differ. 14 2007 171 182 (Pubitemid 44911904)
18. K. Guzik, and J. Potempa Friendly fire against neutrophils: proteolytic enzymes confuse the recognition of apoptotic cells by macrophages Biochimie 90 2008 405 415 (Pubitemid 351172574)
19. B. Antonioli, I. Fermo, S. Cainarca, S. Marzorati, R. Nano, M. Baldissera, A. Bachi, R. Paroni, C. Ricordi, and F. Bertuzzi Characterization of collagenase blend enzymes for human islet transplantation Transplantation 84 2007 1568 1575
20. F. Hesse, H. Burtscher, F. Popp, and D. Ambrosius Recombinant enzymes for islet isolation: purification of a collagenase from Clostridium histolyticum and cloning/expression of the gene Transplant. Proc. 27 1995 3287
21. H. Wang, C.A. Van Blitterswijk, M. Bertrand-De Haas, A.H. Schuurman, and E.N. Lamme Improved enzymatic isolation of fibroblasts for the creation of autologous skin substitutes In Vitro Cell Dev. Biol. Anim. 40 2004 268 277 (Pubitemid 40315823)
22. E. Tamai, S. Miyata, H. Tanaka, H. Nariya, M. Suzuki, O. Matsushita, N. Hatano, and A. Okabe High-level expression of his-tagged clostridial collagenase in Clostridium perfringens Appl. Microbiol. Biotechnol. 80 2008 627 635
23. S. Manabe, H. Nariya, S. Miyata, H. Tanaka, J. Minami, M. Suzuki, Y. Taniguchi, and A. Okabe Purification and characterization of a clostripain-like protease from a recombinant Clostridium perfringens culture Microbiology 156 2010 561 569
24. D. O'gorman, T. Kin, S. Imes, R. Pawlick, P. Senior, and A.M. Shapiro Comparison of human islet isolation outcomes using a new mammalian tissue-free enzyme versus collagenase NB-1 Transplantation 90 2010 255 259
25. J. Jóźwiak, T. Grzela, E. Jankowska-Steifer, A. Komar, S. Moskalewski, and G. Martirosian Lethal factor of Clostridium histolyticum kills cells by apoptosis FEMS Immunol. Med. Microbiol. 49 2007 296 303
26. S. Moskalewski, K.R. Sochañska, and T. Wiwatowski The presence of a factor toxic to pancreatic beta cells in some collagenase preparations Bull. Acad. Pol. Sci. Biol. 22 1973 127 130
27. W.M. Mitchell, and W.F. Harrington Clostripain Methods Enzymol. 19 1970 635 642
28. V. Witte, N. Wolf, T. Diefenthal, G. Reipen, and H. Dargatz Heterologous expression of the clostripain gene from Clostridium histolyticum in Escherichia coli and Bacillus subtilis: maturation of the clostripain precursor is coupled with self-activation Microbiology 140 1994 1175 1182 (Pubitemid 24157868)
29. V. Witte, N. Wolf, and H. Dargatz Clostripain linker deletion variants yield active enzyme in Escherichia coli: a possible function of the linker peptide as intramolecular inhibitor of clostripain automaturation Curr. Microbiol. 33 1996 281 286 (Pubitemid 26357306)
30. A. Takamizawa, S. Miyata, O. Matsushita, M. Kaji, Y. Taniguchi, E. Tamai, S. Shimamoto, and A. Okabe High-level expression of clostridial sialidase using a ferredoxin gene promoter-based plasmid Protein Expr. Purif. 36 2004 70 75 (Pubitemid 38836766)
31. H. Tanaka, E. Tamai, S. Miyata, Y. Taniguchi, H. Nariya, N. Hatano, H. Houchi, and A. Okabe Construction and characterization of a clostripain-like protease-deficient mutant of Clostridium perfringens as a strain for clostridial gene expression Appl. Microbiol. Biotechnol. 77 2008 1063 1071 (Pubitemid 350264445)
32. H. Nariya, S. Miyata, M. Suzuki, and A. Okabe Development of a method for couterselectable in-frame deletion and its application to construction of a less virulent strain of Clostridium perfringens Appl. Environ. Microbiol. 2010
33. C. Matsushita, O. Matsushita, M. Koyama, and A. Okabe A Clostridium perfringens vector for the selection of the promoters Plasmid 31 1994 317 319 (Pubitemid 24184092)
34. M. Kaji, O. Matsushita, E. Tamai, S. Miyata, Y. Taniguchi, S. Shimamoto, S. Katayama, S. Morita, and A. Okabe A novel type of DNA curvature present in a Clostridium perfringens ferredoxin gene: characterization and role in gene expression Microbiology 149 2003 3083 3091 (Pubitemid 37441991)
35. S. Chohnan, K. Shiraki, K. Yokota, M. Ohshima, N. Kuroiwa, K. Ahmed, T. Masaki, and F. Sakiyama A second lysine-specific serine protease from Lysobacter sp. strain IB-9374 J. Bacteriol. 186 2004 5093 5100 (Pubitemid 38970836)
36. O. Matsushita, K. Yoshihara, S. Katayama, J. Minami, and A. Okabe Purification and characterization of Clostridium perfringens 120-kDa collagenase and nucleotide sequence of the corresponding gene J. Bacteriol. 176 1994 149 156 (Pubitemid 24014934)
37. O. Matsushita, C.M. Jung, J. Minami, S. Katayama, N. Nishi, and A. Okabe A study of the collagen-binding domain of a 116-kDa Clostridium histolyticum collagenase J. Biol. Chem. 273 1998 3643 3648 (Pubitemid 28109790)
38. S. Miyata, O. Matsushita, J. Minami, S. Katayama, S. Shimamoto, and A. Okabe Cleavage of a C-terminal peptide is essential for heptamerization of Clostridium perfringens -toxin in the synaptosomal membrane J. Biol. Chem. 276 2001 13778 13783
39. N.E. Labrou, and D.J. Rigden The structure-function relationship in the clostripain family of peptidases Eur. J. Biochem. 271 2004 983 992 (Pubitemid 38299652)
40. T. Shimizu, K. Shima, K. Yoshino, K. Yonezawa, T. Shimizu, and H. Hayashi Proteome and transcriptome analysis of the virulence genes regulated by the VirR/VirS system in Clostridium perfringens J. Bacteriol. 184 2002 2587 2594 (Pubitemid 34457024)
41. J. Potempa, J. Mikolajczyk-Pawlinska, D. Brassell, D. Nelson, I.B. Thøgersen, J.J. Enghild, and J. Travis Comparative properties of two cysteine proteinases (gingipains R), the products of two related but individual genes of Porphyromonas gingivalis J. Biol. Chem. 273 1998 21648 21657 (Pubitemid 28405337)
42. L.B. Silva, A.P. Reis, E.J. Pereira, M.G. Oliveira, and R.N. Guedes Altered cysteine proteinase activity in insecticide-resistant strains of the maize weevil: purification and characterization Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 157 2010 80 87
43. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254