Applied and Environmental Soil Science
Volume 2010 (2010), Article ID 294258, 13 pages
http://dx.doi.org/10.1155/2010/294258
Review Article
Earthworm Protease
Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, 15 Da Tun Road, Chaoyang District, Beijing 100101, China
Received 1 August 2009; Accepted 30 October 2009
Academic Editor: Natchimuthu Karmegam
Copyright © 2010 Rong Pan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- L. Frédéricq, “La digestion des matières albuminoides chez quelques invertébrés,” Archives de Zoologie Expérimentale et Générale, vol. 7, p. 391, 1878. View at Google Scholar
- D. Keilin, “On the pharyngeal or salivary gland of the earthworm,” Quarterly Journal of Microscopical Science, vol. 65, pp. 33–61, 1920. View at Google Scholar
- H. Mihara, H. Sumi, and K. Akazawa, “Fibrinolytic enzyme extracted from the earthworm,” Thrombosis and Haemostasis, vol. 50, p. 258, 1983. View at Google Scholar
- H. Mihara, H. Sumi, T. Yoneta et al., “A novel fibrinolytic enzyme extracted from the earthworm, Lumbricus rubellus,” Japanese Journal of Physiology, vol. 41, no. 3, pp. 461–472, 1991. View at Google Scholar · View at Scopus
- P. Wu and R. Fan, “An effective and rapid thromblytic agent e-TPA,” Acta Biophysica Sinica, vol. 87, 1986. View at Google Scholar
- J. S. Yang and B. G. Ru, “Purification and characterization of an SDS-activated fibrinolytic enzyme from Eisenia fetida,” Comparative Biochemistry and Physiology Part B, vol. 118, no. 3, pp. 623–631, 1997. View at Publisher · View at Google Scholar · View at Scopus
- J. S. Yang, L. Y. Li, and B. G. Ru, “Degradation of N-acetyl-L-tyrosine ethyl ester (ATEE) by a plasminogen activator from Eisenia fetida (e-PA),” Chinese Journal of Biochemistry & Molecular Biology, vol. 14, pp. 417–421, 1998. View at Google Scholar
- J. S. Yang, L. Y. Li, and B. G. Ru, “Degradation of benzoyl-L-arginine ethyl ester (BAEE) by a plasminogen activator from Eisenia fetida (e-PA),” Chinese Journal of Biochemistry & Molecular Biology, vol. 14, pp. 412–416, 1998. View at Google Scholar
- J. S. Yang, L. Y. Li, and B. G. Ru, “Characterization of a plasminogen activator from Eisenia fetida,” Chinese Journal of Biochemistry & Molecular Biology, vol. 14, pp. 164–169, 1998. View at Google Scholar
- J. S. Yang, L. Y. Li, and B. G. Ru, “Purification of a plasminogen activator from Eisenia fetida,” Chinese Journal of Biochemistry & Molecular Biology, vol. 14, pp. 156–163, 1998. View at Google Scholar
- J. S. Yang, Y. Q. Guo, and B. G. Ru, “The enzymology properties and the CD spectra of the active centers of the small subunit of a plasminogen activator from Eisenia fetida (e-PA),” Chinese Journal of Biochemistry & Molecular Biology, vol. 14, pp. 721–725, 1998. View at Google Scholar
- Y. Tang, J. Zhang, L. Gui et al., “Crystallization and preliminary X-ray analysis of earthworm fibrinolytic enzyme component A from Eisenia fetida,” Acta Crystallographica D, vol. 56, no. 12, pp. 1659–1661, 2000. View at Publisher · View at Google Scholar · View at Scopus
- Y. Tang, D. Liang, T. Jiang, J. Zhang, L. Gui, and W. Chang, “Crystal structure of earthworm fibrinolytic enzyme component A: revealing the structural determinants of its dual fibrinolytic activity,” Journal of Molecular Biology, vol. 321, no. 1, pp. 57–68, 2002. View at Publisher · View at Google Scholar · View at Scopus
- M. Popović, T. M. Hrženjak, T. Babić, J. Kos, and M. Grdiša, “Effect of earthworm (G-90) extracton formation and lysis of clots originated from venous blood of dogs with cardiopathies and with malignant tumors,” Pathology and Oncology Research, vol. 7, no. 3, pp. 197–202, 2001. View at Publisher · View at Google Scholar · View at Scopus
- M. Popović, T. M. Hrženjak, M. Grdiša, and S. Vuković, “Adhesins of immunoglobulin-like superfamily from earthworm Eisenia fetida,” General Pharmacology, vol. 30, pp. 795–780, 1998. View at Google Scholar
- T. M. Hrženjak, M. Popović, and L. Tiška-Rudman, “Fibrinolytic activity of earthworms extract (G-90) on lysis of fibrin clots originated from the venous blood of patients with malignant tumors,” Pathology & Oncology Research, vol. 4, no. 3, pp. 206–211, 1998. View at Google Scholar · View at Scopus
- T. M. Hrženjak, M. Popović, T. Božić, M. Grdiša, D. Kobrehel, and L. Tiška-Rudman, “Fibrinolytic and anticoagulative activities from the earthworm Eisenia foetida,” Comparative Biochemistry and Physiology Part B, vol. 119, no. 4, pp. 825–832, 1998. View at Publisher · View at Google Scholar · View at Scopus
- T. Hrženjak, M. Hrženjak, V. Kasuba, P. Efenberger-Marinculić, and S. Levanat, “A new source of biologically active compounds-earthworm tissue (Eisenia foetida, Lumbricus rubelus),” Comparative Biochemistry and Physiology Part A, vol. 102, no. 3, pp. 441–447, 1992. View at Publisher · View at Google Scholar · View at Scopus
- M. Grdiša, M. Popović, and T. Hrženjak, “Glycolipoprotein extract (G-90) from earthworm Eisenia foetida exerts some antioxidative activity,” Comparative Biochemistry and Physiology Part A, vol. 128, no. 4, pp. 821–825, 2001. View at Publisher · View at Google Scholar · View at Scopus
- J. E. Satchell, “Lumbricidae,” in Soil Biology, A. Burges and F. Raw, Eds., pp. 259–322, Academic Press, New York, NY, USA, 1967. View at Google Scholar
- Y. Lu, R. Jin, Y. Wu, and X. Mang, “The purification and characterization of fibinolytic enzymes from Amynthas dancatala,” Chinese Journal of Biochemistry & Molecular Biology, vol. 4, pp. 166–172, 1988. View at Google Scholar
- Y. C. Zhou, H. Zhu, and Y. C. Chen, “The isolation and purification of earthworm fibrinolytic protease from Eisenia fetida,” Acta Biochimica et Biophysica Sinica, vol. 20, pp. 35–42, 1988. View at Google Scholar
- N. Nakajima, H. Mihara, and H. Sumi, “Characterization of potent fibrinolytic enzymes in earthworm, Lumbricus rubellus,” Bioscience, Biotechnology & Biochemistry, vol. 57, no. 10, pp. 1726–1730, 1993. View at Google Scholar · View at Scopus
- J. Zhou, R. Fan, C. Wu, and R.-Q. He, “Assay of lumbrokinase with a chromophoric substrate,” Protein and Peptide Letters, vol. 4, no. 6, pp. 409–414, 1997. View at Google Scholar · View at Scopus
- N. Nakajima, M. Sugimoto, S. Tsuboi, H. Tsuji, and K. Ishihara, “An isozyme of earthworm serine proteases acts on hydrolysis of triacylglycerol,” Bioscience, Biotechnology & Biochemistry, vol. 69, no. 10, pp. 2009–2011, 2005. View at Publisher · View at Google Scholar · View at Scopus
- J. X. Wu, X. Y. Zhao, R. Pan, and R. Q. He, “Glycosylated trypsin-like proteases from earthworm Eisenia fetida,” International Journal of Biological Macromolecules, vol. 40, pp. 399–406, 2007. View at Google Scholar
- M. Ueda, K. Noda, M. Nakazawa et al., “A novel anti-plant viral protein from coelomic fluid of the earthworm Eisenia foetida: purification, characterization and its identification as a serine protease,” Comparative Biochemistry and Physiology Part B, vol. 151, no. 4, pp. 381–385, 2008. View at Publisher · View at Google Scholar · View at Scopus
- Y. Xu, G. Liang, Z. Sun et al., “Cloning and expression of the novel gene-PV242 of earthworm fibrinolytic enzyme,” Progress in Biochemistry and Biophysics, vol. 29, pp. 610–614, 2002. View at Google Scholar
- C. K. Lee, J. S. Shin, B. S. Kim, I. H. Cho, Y. S. Kim, and E. B. Lee, “Antithrombotic effects by oral administration of novel proteinase fraction from earthworm Eisenia andrei on venous thrombosis model in rats,” Archives of Pharmacal Research, vol. 30, pp. 475–480, 2007. View at Google Scholar
- J. Zhao, R. Xiao, J. He et al., “In situ localization and substrate specificity of earthworm protease-II and protease-III-1 from Eisenia fetida,” International Journal of Biological Macromolecules, vol. 40, no. 2, pp. 67–75, 2007. View at Publisher · View at Google Scholar · View at Scopus
- H. Sumi, N. Nakajima, and H. Mihara, “A very stable and potent fibrinolytic enzyme found in earthworm Lumbricus rubellus autolysate,” Comparative Biochemistry and Physiology Part B, vol. 106, pp. 763–766, 1993. View at Google Scholar
- A. Tage and M. Sten, “The fibrin plate method for estimating fibrinolytic activity,” Archives of Biochemistry and Biophysics, vol. 40, no. 2, pp. 346–351, 1952. View at Google Scholar · View at Scopus
- J. Zhou, K. Jiang, R. He, and Y. Han, “Assays of therombin, hirudin and lumbrokinase with light scattering in the solution of fibirinogen,” Acta Biophysica Sinica, vol. 14, pp. 531–535, 1997. View at Google Scholar
- J. Zhao, R. Pan, J. He, Y. Liu, D. F. Li, and R. Q. He, “Eisenia fetida protease-III-1 functions in both fibrinolysis and fibrogenesis,” Journal of Biomedicine and Biotechnology, vol. 2007, Article ID 97654, 10 pages, 2007. View at Publisher · View at Google Scholar
- S. Mao, Z. Yan, and S. Chen, “Purification and kinetic characteristics of fibrinolytic enzymes from earthworm,” Journal of Wenzhou Medical College, vol. 30, pp. 277–278, 2000. View at Google Scholar
- J. Zhao, L. Li, C. Wu, and R.-Q. He, “Hydrolysis of fibrinogen and plasminogen by immobilized earthworm fibrinolytic enzyme II from Eisenia fetida,” International Journal of Biological Macromolecules, vol. 32, pp. 165–171, 2003. View at Google Scholar
- A. J. Barret and P. M. Starkey, “The interaction of 2-Macroglobulln with proteinases,” Biochemical Journal, vol. 133, pp. 709–724, 1973. View at Google Scholar
- P. E. H. Jensen and L. Sottrup-Je, “Primary structure of human 2-Macroglobulin,” Journal of Biological Chemistry, vol. 261, pp. 15863–15869, 1986. View at Google Scholar
- C. Wu, L. Li, J. Zhao, Q. Fan, W. X. Tian, and R. Q. He, “Effect of 2M on earthworm fibrinolytic enzyme III-1 from Lumbricus rubellus,” International Journal of Biological Macromolecules, vol. 31, pp. 71–77, 2002. View at Google Scholar
- GenBank database, accession number, BAB40768.1.
- GenBank database, accession number, BAB40767.1.
- GenBank database, accession number, AAM73677.1.
- Protein Data Bank, accession number, 1YM0A.
- GenBank database, accession number, ABG68022.
- GenBank database, accession number, ABD76397.
- GenBank database, accession number, ABG68023.
- GenBank database, accession number, ABB19359.
- L. H. Takahashi, R. Radhakrishnan, R. E. Rosenfield Jr., E. F. Meyer Jr., and D. A. Trainor, “Crystal structure of the covalent complex formed by a peptidyl..,..-difluoro-..-keto amide with porcine pancreatic elastase at 1.78.ANG. resolution,” Journal of the American Chemical Society, vol. 111, pp. 3368–3374, 1989. View at Google Scholar
- A.-Z. Wei, I. Mayra, and W. Bode, “The refined 2.3 Å crystal structure of human leukocyte elastase in a complex with a valine chloromethyl ketone inhibitor,” Federation of the Societies of Biochemistry and Molecular Biology Letter, vol. 234, no. 2, pp. 367–373, 1988. View at Publisher · View at Google Scholar · View at Scopus
- M. Marquart, J. Walter, J. Deisenhofer, W. Bode, and R. Huber, “The geometry of the reactive site and of the peptide groups in trypsin, trypsinogen and its complexes with inhibitors,” Acta Crystallographica B, vol. 39, pp. 480–490, 1983. View at Google Scholar
- A. Mac Sweeney, G. Birrane, M. A. Walsh, T. O'Connell, J. P. G. Malthouse, and T. M. Higgins, “Crystal structure of deta-chymotrypsin bound to a peptidyl chloromethyl ketone inhibitor,” Acta Crystallographica D, vol. 56, pp. 280–286, 2000. View at Google Scholar
- G. Spraggon, C. Phillips, U. K. Nowak et al., “The crystal structure of the catalytic domain of human urokinase-type plasminogen activator,” Structure, vol. 3, no. 7, pp. 681–691, 1995. View at Google Scholar · View at Scopus
- L. Doriano, B. Margit, H. Robert et al., “The 2.3 Å crystal structure of the catalytic domain of recombinant two-chain human t-type plasminogen activator,” Journal of Molecular Biology, vol. 258, pp. 117–135, 1996. View at Google Scholar
- X. Wang, X. Lin, A. L. Jeffrey, J. Tang, and X. C. Zhang, “Crystal structure of the catalytic domain of human plasmin complexed with streptokinase,” Science, vol. 281, no. 5383, pp. 1662–1668, 1998. View at Publisher · View at Google Scholar · View at Scopus
- M. Sugimoto and N. Nakajima, “Molecular cloning, sequencing, and expression of cDNA encoding serine protease with fibrinolytic activity from earthworm,” Bioscience, Biotechnology and Biochemistry, vol. 65, no. 7, pp. 1575–1580, 2001. View at Publisher · View at Google Scholar · View at Scopus
- F. Wang, C. Wang, M. Li et al., “Crystal structure of earthworm fibrinolytic enzyme component B: a novel, glycosylated two-chained trypsin,” Journal of Molecular Biology, vol. 348, no. 3, pp. 671–685, 2005. View at Google Scholar · View at Scopus
- F. Wang, C. Wang, M. Li, L. Gui, J. Zhang, and W. Chang, “Crystallization and preliminary crystallographic analysis of earthworm fibrinolytic enzyme component B from Eisenia fetida,” Acta Crystallographica D, vol. 60, no. 5, pp. 933–935, 2004. View at Publisher · View at Google Scholar · View at Scopus
- N. Nakajima, M. Sugimoto, K. Ishihara, K. Nakamura, and H. Hamada, “Further characterization of earthworm serine proteases: cleavage specificity against peptide substrates and on autolysis,” Bioscience, Biotechnology and Biochemistry, vol. 63, no. 11, pp. 2031–2033, 1999. View at Google Scholar · View at Scopus
- E. Bovill, R. Tracy, T. Hayes, R. Jenny, F. Bhushan, and K. Mann, “Evidence that meizothrombin is an intermediate product in the clotting of whole blood,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 15, no. 6, pp. 754–758, 1995. View at Google Scholar · View at Scopus
- A. B. Barua, “Intestinal absorption of epoxy--carotenes by humans,” Biochemical Journal, vol. 339, no. 2, pp. 359–362, 1999. View at Publisher · View at Google Scholar · View at Scopus
- Q. Fan, C. Wu, L. Li et al., “Some features of intestinal absorption of intact fibrinolytic enzyme III-1 from Lumbricus rubellus,” Biochimica et Biophysica Acta, vol. 1526, no. 3, pp. 286–292, 2001. View at Publisher · View at Google Scholar · View at Scopus
- M. Green and P. M. Loewenstein, “Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein,” Cell, vol. 55, no. 6, pp. 1179–1188, 1988. View at Google Scholar · View at Scopus
- M. Verstraete, “Third-generation thrombolytic drugs,” American Journal of Medicine, vol. 109, no. 1, pp. 52–58, 2000. View at Publisher · View at Google Scholar · View at Scopus
- J. Zhao and D. Li, “Research progress on anticoagulant protein molucular,” Microbiology, vol. 29, pp. 102–107, 2002. View at Google Scholar
- S. Kasai, H. Arimura, M. Nishida, and T. Suyama, “Proteolytic cleavage of single-chain pro-urokinase induces conformational change which follows activation of the zymogen and reduction of its high affinity for fibrin,” Journal of Biological Chemistry, vol. 260, pp. 12367–12376, 1985. View at Google Scholar
- E. L. Madison, G. S. Coombs, and D. R. Corey, “Substrate specificity of tissue type plasminogen activator,” Journal of Biological Chemistry, vol. 270, no. 13, pp. 7558–7562, 1995. View at Publisher · View at Google Scholar · View at Scopus
- J. S. Kim, J. K. Kang, H. C. Chang et al., “The thrombolytic effect of lumbrokinase is not as potent as urokinase in a rabbit cerebral embolism model,” Journal of Korean Medical Science, vol. 8, no. 2, pp. 117–120, 1993. View at Google Scholar · View at Scopus
- Y. Cong, Y. Liu, and J. C. Chen, “Advance in lumbrokinase,” Chinese Journal of Biochemical Pharmaceutics, vol. 21, pp. 159–162, 2000. View at Google Scholar
- N. Nakajima, M. Sugimoto, and K. Ishihara, “Stable earthworm serine proteases: application of the protease function and usefulness of the earthworm autolysate,” Journal of Bioscience and Bioengineering, vol. 90, no. 2, pp. 174–179, 2000. View at Publisher · View at Google Scholar · View at Scopus
- L. Jin, H. Jin, G. Zhang, and G. Xu, “Changes in coagulation and tissue plasminogen activator after the treatment of cerebral infarction with lumbrokinase,” Clinical Hemorheology and Microcirculation, vol. 23, no. 2–4, pp. 213–218, 2000. View at Google Scholar · View at Scopus
- F. Zhang and K. W. Wang, “The inhibition of hep-2 cells using earthworm extract (912),” Journal of the Fourth Military Medical University, vol. 8, p. 224, 1987. View at Google Scholar
- X. Zeng, B. Zhang, X. Mai et al., “The effects of extraction from earthworm on various tumour cells in vitro,” Journal of Shanxi Medical University, vol. 18, pp. 81–83, 1995. View at Google Scholar
- K. Wang, S. Zhang, Y. Li, Q. Tian, and G. Zhi, “Antltumorigenic effect of an extract of rarthworm on S_(180) and H_(22) cells in mice,” Journal of the Fourth Military Medical University, vol. 7, pp. 85–88, 1986. View at Google Scholar
- W. Zhang, L. Li, and H. Mao, “The clinical observation of lymphoma and lung cancer treated with chemical drugs and 912,” Chinese Journal of Clinical Oncology, vol. 18, pp. 181–182, 1991. View at Google Scholar
- S.-Z. Zhang, Q. Tian, K.-W. Wang, and D.-M. Xu, “Radio enhancement effect of radiotherapy combined with earthworm capsule in the treatment of esophagus and lung carcinoma,” Journal of the Fourth Military Medical University, vol. 13, pp. 165–168, 1992. View at Google Scholar
- J. B. Xie, Z. Q. Guo, N. Weng, H. T. Wang, G. Q. Jiang, and B. G. Ru, “Purification, identification and partial characterization of an apoptosis-related serine protease from earthworm,” Progress in Biochemistry and Biophysics, vol. 30, no. 3, pp. 453–460, 2003. View at Google Scholar · View at Scopus
- H. Chen, S. Takahashi, M. Imamura et al., “Earthworm fibrinolytic enzyme: anti-tumor activity on human hepatoma cells in vitro and in vivo,” Chinese Medical Journal, vol. 120, no. 10, pp. 898–904, 2007. View at Google Scholar · View at Scopus
- G. H. Ryu, S. Park, M. Kim, D. K. Han, Y. H. Kim, and B. Min, “Antithrombogenicity of lumbrokinase-immobilized polyurethane,” Journal of Biomedical Materials Research, vol. 28, no. 9, pp. 1069–1077, 1994. View at Google Scholar · View at Scopus
- Y. Park, E. Ryu, H. Kim et al., “Characterization of antithrombotic activity of lumbrokinase-immobilized polyurethane valves in the total artificial heart,” Artificial Organs, vol. 23, no. 2, pp. 210–214, 1999. View at Publisher · View at Google Scholar · View at Scopus
- G. H. Ryu, D. K. Han, S. Park, M. Kim, Y. H. Kim, and B. Min, “Surface characteristics and properties of lumbrokinase-immobilized polyurethane,” Journal of Biomedical Materials Research, vol. 29, pp. 403–409, 1995. View at Google Scholar
- G. H. Ryu, S. Park, D. K. Han, Y. H. Kim, and B. Min, “Antithrombotic activity of a lumbrokinase immobilized polyurethane surface,” Asaio Journal, vol. 39, no. 3, pp. 314–318, 1993. View at Publisher · View at Google Scholar · View at Scopus
- H. L. Sun, J. D. Jiao, Z. W. Pan, D. L. Dong, and B. F. Yang, “The cardioprotective effect and mechanism of lumbrokinase,” Yao Xue Xue Bao, vol. 41, no. 3, pp. 247–251, 2006. View at Google Scholar · View at Scopus
- M. Kasim, A. A. Kiat, M. S. Rohman, Y. Hanifah, and H. Kiat, “Improved myocardial perfusion in stable angina pectoris by oral lumbrokinase: a pilot study,” Journal of Alternative and Complementary Medicine, vol. 15, no. 5, pp. 539–544, 2009. View at Publisher · View at Google Scholar · View at Scopus
- H. Ji, L. Wang, H. Bi et al., “Mechanisms of lumbrokinase in protection of cerebral ischemia,” European Journal of Pharmacology, vol. 590, pp. 281–289, 2008. View at Google Scholar
- D. Collen, “On the regulation and control of fibrinolysis,” Thrombosis and Haemostasis, vol. 43, no. 2, pp. 77–89, 1980. View at Google Scholar
- M. B. Cheng, J. C. Wang, Y. H. Li et al., “Characterization of water-in-oil microemulsion for oral delivery of earthworm fibrinolytic enzyme,” Journal of Controlled Release, vol. 129, no. 1, pp. 41–48, 2008. View at Publisher · View at Google Scholar · View at Scopus
- Y. H. Li, M. Zhang, J. C. Wang, S. Zhang, J. R. Liu, and Q. Zhang, “Effects of absorption enhancers on intestinal absorption of lumbrokinase,” Yao Xue Xue Bao, vol. 41, pp. 939–944, 2006. View at Google Scholar
- X. Y. Zhao, T. Y. Jing, X. Y. Jiang, M. X. Duan, and C. X. Zheng, “Antigenicity of components constituting earthworm fibrinolytic enzyme,” Chinese Journal of Biochemistry & Molecular Biology, vol. 18, pp. 209–212, 2002. View at Google Scholar
- N. Nakajima, K. Ishihara, M. Sugimoto, T. Nakahara, and H. Tsuji, “Further stabilization of earthworm serine protease by chemical modification and immobilization,” Bioscience, Biotechnology and Biochemistry, vol. 66, no. 12, pp. 2739–2742, 2002. View at Google Scholar · View at Scopus
- N. Nakajima, K. Ishihara, M. Sugimoto, H. Sumi, K. Mikuni, and H. Hamada, “Chemical modification of earthworm fibrinolytic enzyme with human serum albumin fragment and characterization of the protease as a therapeutic enzyme,” Bioscience, Biotechnology and Biochemistry, vol. 60, no. 2, pp. 293–300, 1996. View at Google Scholar · View at Scopus