Collagenolytic Enzymes and their Applications in Biomedicine

Author(s): Anatoly B. Shekhter*, Anastasia V. Balakireva, Natalia V. Kuznetsova, Marina N. Vukolova, Petr F. Litvitsky, Andrey A. Zamyatnin Jr.

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 3 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

Nowadays, enzymatic therapy is a very promising line of treatment for many different diseases. There is a group of disorders and conditions, caused by fibrotic and scar processes and associated with the excessive accumulation of collagen that needs to be catabolized to normalize the connective tissue content. The human body normally synthesizes special extracellular enzymes, matrix metalloproteases (MMPs) by itself. These enzymes can cleave components of extracellular matrix (ECM) and different types of collagen and thus maintain the balance of the connective tissue components. MMPs are multifunctional enzymes and are involved in a variety of organism processes. However, under pathological conditions, the function of MMPs is not sufficient, and these enzymes fail to deal with disease. Thus, medical intervention is required. Enzymatic therapy is a very effective way of treating such collagen-associated conditions. It involves the application of exogenous collagenolytic enzymes that catabolize excessive collagen at the affected site and lead to the successful elimination of disease. Such collagenolytic enzymes are synthesized by many organisms: bacteria, animals (especially marine organisms), plants and fungi. The most studied and commercially available are collagenases from Clostridium histolyticum and from the pancreas of the crab Paralithodes camtschatica, due to their ability to effectively hydrolyse human collagen without affecting other tissues, and their wide pH ranges of collagenolytic activity. In the present review, we summarize not only the data concerning existing collagenase-based medications and their applications in different collagen-related diseases and conditions, but we also propose collagenases from different sources for their potential application in enzymatic therapy.

Keywords: Collagen, collagenase, Clostridium histolyticum, Paralithodes camtschatica, MMPs, collagen-related disorders, collagenolytic enzymes.

[1]
Santos-Laso, A.; Munoz-Garrido, P.; Felipe-Agirre, M.; Bujanda, L.; Banales, J.M.; Perugorria, M.J. New advances in the molecular mechanisms driving biliary fibrosis and emerging molecular targets. Curr. Drug Targets, 2017, 18(8), 908-920.
[2]
Tundis, R.; Loizzo, M.R.; Bonesi, M.; Menichini, F. Potential role of natural compounds against skin aging. Curr. Med. Chem., 2015, 22(12), 1515-1538.
[3]
Shoulders, M.D.; Raines, R.T. Collagen structure and stability. Annu. Rev. Biochem., 2009, 78, 929-958.
[4]
Gordon, M.K.; Hahn, R.A. Collagens. Cell Tissue Res., 2010, 339(1), 247-257.
[5]
Nagase, H.; Visse, R.; Murphy, G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res., 2006, 69(3), 562-573.
[6]
Lauer-Fields, J.L.; Juska, D.; Fields, G.B. Matrix metalloproteinases and collagen catabolism. Biopolymers, 2002, 66(1), 19-32.
[7]
Overall, C.M.; López-Otín, C. Strategies for MMP inhibition in cancer: Innovations for the post trial era. Nat. Rev. Cancer, 2002, 2(9), 657-672.
[8]
Maradni, A.; Khoshnevisan, A.; Mousavi, S.H.; Emamirazavi, S.H.; Noruzijavidan, A. Role of matrix metalloproteinases (MMPs) and MMP inhibitors on intracranial aneurysms: A review article. Med. J. Islam. Repub. Iran, 2013, 27(4), 249-254.
[9]
Stolow, M.A.; Bauzon, D.D.; Li, J.; Sedgwick, T.; Liang, V.C.; Sang, Q.A.; Shi, Y.B. Identification and characterization of a novel collagenase in Xenopus laevis: possible roles during frog development. Mol. Biol. Cell, 1996, 7(10), 1471-1483.
[10]
Yu, Q.; Stamenkovic, I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev., 2000, 14(2), 163-176.
[11]
McQuibban, G.A.; Gong, J.H.; Tam, E.M.; McCulloch, C.A.; Clark-Lewis, I.; Overall, C.M. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science, 2000, 289(5482), 1202-1206.
[12]
Fernandez-Patron, C.; Radomski, M.W.; Davidge, S.T. Vascular matrix metalloproteinase-2 cleaves big endothelin-1 yielding a novel vasoconstrictor. Circ. Res., 1999, 85(10), 906-911.
[13]
Visse, R.; Nagase, H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: Structure, function, and biochemistry. Circ. Res., 2003, 92(8), 827-839.
[14]
Manzetti, S.; McCulloch, D.R.; Herington, A.C.; van der Spoel, D. Modeling of enzyme-substrate complexes for the metalloproteases MMP-3, ADAM-9 and ADAM-10. J. Comput. Aided Mol. Des., 2003, 17(9), 551-565.
[15]
Liu, Y.; Zhao, Y.; Lu, C.; Fu, M.; Dou, T.; Tan, X. Signatures of positive selection at hemopexin (PEX) domain of matrix metalloproteinase-9 (MMP-9) gene. J. Biosci., 2015, 40(5), 885-890.
[16]
Cheng, S.; Tada, M.; Hida, Y.; Asano, T.; Kuramae, T.; Takemoto, N.; Hamada, J.; Miyamoto, M.; Hirano, S.; Kondo, S.; Moriuchi, T. High MMP-1 mRNA expression is a risk factor for disease-free and overall survivals in patients with invasive breast carcinoma. J. Surg. Res., 2008, 146(1), 104-109.
[17]
Inoue, K.; Mikuni-Takagaki, Y.; Oikawa, K.; Itoh, T.; Inada, M.; Noguchi, T.; Park, J.S.; Onodera, T.; Krane, S.M.; Noda, M.; Itohara, S. A crucial role for matrix metalloproteinase 2 in osteocytic canalicular formation and bone metabolism. J. Biol. Chem., 2006, 281(44), 33814-33824.
[18]
Mehner, C.; Hockla, A.; Miller, E.; Ran, S.; Radisky, D.C.; Radisky, E.S. Tumor cell-produced matrix metalloproteinase 9 (MMP-9) drives malignant progression and metastasis of basal-like triple negative breast cancer. Oncotarget, 2014, 5(9), 2736-2749.
[19]
Pei, D.; Majmudar, G.; Weiss, S.J. Hydrolytic inactivation of a breast carcinoma cell-derived serpin by human stromelysin-3. J. Biol. Chem., 1994, 269(41), 25849-25855.
[20]
Luo, D.; Mari, B.; Stoll, I.; Anglard, P. Alternative splicing and promoter usage generates an intracellular stromelysin 3 isoform directly translated as an active matrix metalloproteinase. J. Biol. Chem., 2002, 277(28), 25527-25536.
[21]
Keles, D.; Arslan, B.; Terzi, C.; Tekmen, I.; Dursun, E.; Altungoz, O.; Oktay, G. Expression and activity levels of matrix metalloproteinase-7 and in situ localization of caseinolytic activity in colorectal cancer. Clin. Biochem., 2014, 47(13-14), 1265-1271.
[22]
Guan, P.P.; Yu, X.; Guo, J.J.; Wang, Y.; Wang, T.; Li, J.Y.; Konstantopoulos, K.; Wang, Z.Y.; Wang, P. By activating matrix metalloproteinase-7, shear stress promotes chondrosarcoma cell motility, invasion and lung colonization. Oncotarget, 2015, 6(11), 9140-9159.
[23]
Apte, S.S.; Fukai, N.; Beier, D.R.; Olsen, B.R. The matrix metalloproteinase-14 (MMP-14) gene is structurally distinct from other MMP genes and is co-expressed with the TIMP-2 gene during mouse embryogenesis. J. Biol. Chem., 1997, 272(41), 25511-25517.
[24]
Zigrino, P.; Ayachi, O.; Schild, A.; Kaltenberg, J.; Zamek, J.; Nischt, R.; Koch, M.; Mauch, C. Loss of epidermal MMP-14 expression interferes with angiogenesis but not with reepithelialization. Eur. J. Cell Biol., 2012, 91(10), 748-756.
[25]
Sekine-Aizawa, Y.; Hama, E.; Watanabe, K.; Tsubuki, S.; Kanai-Azuma, M.; Kanai, Y.; Arai, H.; Aizawa, H.; Iwata, N.; Saido, T.C. Matrix metalloproteinase (MMP) system in brain: identification and characterization of brain-specific MMP highly expressed in cerebellum. Eur. J. Neurosci., 2001, 13(5), 935-948.
[26]
Velasco, G.; Cal, S.; Merlos-Suárez, A.; Ferrando, A.A.; Alvarez, S.; Nakano, A.; Arribas, J.; López-Otín, C. Human MT6-matrix metalloproteinase: Identification, progelatinase A activation, and expression in brain tumors. Cancer Res., 2000, 60(4), 877-882.
[27]
Lamort, A.S.; Gravier, R.; Laffitte, A.; Juliano, L.; Zani, M.L.; Moreau, T. New insights into the substrate specificity of macrophage elastase MMP-12. Biol. Chem., 2016, 397(5), 469-484.
[28]
Cervinková, M.; Horák, P.; Kanchev, I.; Matěj, R.; Fanta, J.; Sequens, R.; Kašpárek, P.; Sarnová, L.; Turečková, J.; Sedláček, R. Differential expression and processing of matrix metalloproteinase 19 marks progression of gastrointestinal diseases. Folia Biol. (Praha), 2014, 60(3), 113-122.
[29]
Yu, G.; Kovkarova-Naumovski, E.; Jara, P.; Parwani, A.; Kass, D.; Ruiz, V.; Lopez-Otín, C.; Rosas, I.O.; Gibson, K.F.; Cabrera, S.; Ramírez, R.; Yousem, S.A.; Richards, T.J.; Chensny, L.J.; Selman, M.; Kaminski, N.; Pardo, A. Matrix metalloproteinase-19 is a key regulator of lung fibrosis in mice and humans. Am. J. Respir. Crit. Care Med., 2012, 186(8), 752-762.
[30]
Koli, K.; Saxena, G.; Ogbureke, K.U. Expression of matrix metalloproteinase (MMP)-20 and potential interaction with dentin sialophosphoprotein (DSPP) in human major salivary glands. J. Histochem. Cytochem., 2015, 63(7), 524-533.
[31]
Rodgers, U.R.; Kevorkian, L.; Surridge, A.K.; Waters, J.G.; Swingler, T.E.; Culley, K.; Illman, S.; Lohi, J.; Parker, A.E.; Clark, I.M. Expression and function of matrix metallopro-teinase (MMP)-28. Matrix Biol., 2009, 28(5), 263-272.
[32]
Chen, H.; Fok, K.L.; Yu, S.; Jiang, J.; Chen, Z.; Gui, Y.; Cai, Z.; Chan, H.C. CD147 is required for matrix metalloproteinases-2 production and germ cell migration during spermatogenesis. Mol. Hum. Reprod., 2011, 17(7), 405-414.
[33]
Ramón de Fata, F.; Ferruelo, A.; Andrés, G.; Gimbernat, H.; Sánchez-Chapado, M.; Angulo, J.C. The role of matrix metalloproteinase MMP-9 and TIMP-2 tissue inhibitor of metalloproteinases as serum markers of bladder cancer. Actas Urol. Esp., 2013, 37(8), 480-488.
[34]
Higashikata, T.; Yamagishi, M.; Sasaki, H.; Minatoya, K.; Ogino, H.; Ishibashi-Ueda, H.; Hao, H.; Nagaya, N.; Tomoike, H.; Sakamoto, A. Application of real-time RT-PCR to quantifying gene expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human abdominal aortic aneurysm. Atherosclerosis, 2004, 177(2), 353-360.
[35]
Ala-aho, R.; Kähäri, V.M. Collagenases in cancer. Biochimie, 2005, 87(3-4), 273-286.
[36]
Shuman Moss, L.A.; Jensen-Taubman, S.; Stetler-Stevenson, W.G. Matrix metalloproteinases: changing roles in tumor progression and metastasis. Am. J. Pathol., 2012, 181(6), 1895-1899.
[37]
Mohseni, S.; Moghadam, T.T.; Dabirmanesh, B.; Khajeh, K. Expression, purification, refolding and in vitro recovery of active full length recombinant human gelatinase MMP-9 in Escherichia coli. Protein Expr. Purif., 2016, 126, 42-48.
[38]
Rasch, M.G.; Lund, I.K.; Illemann, M.; Høyer-Hansen, G.; Gårdsvoll, H. Purification and characterization of recombinant full-length and protease domain of murine MMP-9 expressed in Drosophila S2 cells. Protein Expr. Purif., 2010, 72(1), 87-94.
[39]
Muta, Y.; Yasui, N.; Matsumiya, Y.; Kubo, M.; Inouye, K. Expression in Escherichia coli, refolding, and purification of the recombinant mature form of human matrix metalloproteinase 7 (MMP-7). Biosci. Biotechnol. Biochem., 2010, 74(12), 2515-2517.
[40]
Fields, G.B. Interstitial collagen catabolism. J. Biol. Chem., 2013, 288(13), 8785-8793.
[41]
Crowley, J.T.; Strle, K.; Drouin, E.E.; Pianta, A.; Arvikar, S.L.; Wang, Q.; Costello, C.E.; Steere, A.C. Matrix metalloproteinase-10 is a target of T and B cell responses that correlate with synovial pathology in patients with antibiotic-refractory Lyme arthritis. J. Autoimmun., 2016, 69, 24-37.
[42]
Paye, A.; Truong, A.; Yip, C.; Cimino, J.; Blacher, S.; Munaut, C.; Cataldo, D.; Foidart, J.M.; Maquoi, E.; Collignon, J.; Delvenne, P.; Jerusalem, G.; Noel, A.; Sounni, N.E. EGFR activation and signaling in cancer cells are enhanced by the membrane-bound metalloprotease MT4-MMP. Cancer Res., 2014, 74(23), 6758-6770.
[43]
Sedlacek, R.; Mauch, S.; Kolb, B.; Schätzlein, C.; Eibel, H.; Peter, H.H.; Schmitt, J.; Krawinkel, U. Matrix metalloproteinase MMP-19 (RASI-1) is expressed on the surface of activated peripheral blood mononuclear cells and is detected as an autoantigen in rheumatoid arthritis. Immunobiology, 1998, 198(4), 408-423.
[44]
Tamagno, G.; Vigolo, S.; Olivieri, M.; Martini, C.; De Carlo, E. From the rat to the beta cell: A fast and effective technique of separation of Langerhans islets and direct purification of pancreatic beta cells. Endocr. Res., 2014, 39(1), 18-21.
[45]
Kegel, V.; Deharde, D.; Pfeiffer, E.; Zeilinger, K.; Seehofer, D.; Damm, G. Protocol for isolation of primary human hepatocytes and corresponding major populations of non-parenchymal liver cells. J. Vis. Exp., 2016, (109), e53069.
[46]
Kuivaniemi, H.; Tromp, G.; Prockop, D.J. Mutations in collagen genes: causes of rare and some common diseases in humans. FASEB J., 1991, 5(7), 2052-2060.
[47]
Shi, L.; Ramsay, S.; Ermis, R.; Carson, D. pH in the bacteria-contaminated wound and its impact on Clostridium histo-lyticum collagenase activity: Implications for the use of collagenase wound debridement agents. J. Wound Ostomy Continence Nurs., 2011, 38(5), 514-521.
[48]
Bond, M.D.; Van Wart, H.E. Characterization of the individual collagenases from Clostridium histolyticum. Biochemistry, 1984, 23(13), 3085-3091.
[49]
Glyantsev, S.; Adamyan, A.; Sakharov, Y. Crab collagenase in wound debridement. J. Wound Care, 1997, 6(1), 13-16.
[50]
MacLennan, J.D.; Mandl, I.; Howes, E.L. Bacterial digestion of collagen. J. Clin. Invest., 1953, 32(12), 1317-1322.
[51]
Thomas, A.; Bayat, A. The emerging role of Clostridium histolyticum collagenase in the treatment of Dupuytren disease. Ther. Clin. Risk Manag., 2010, 6, 557-572.
[52]
Watanabe, K. Collagenolytic proteases from bacteria. Appl. Microbiol. Biotechnol., 2004, 63(5), 520-526.
[53]
Klimova, O.A.; Borukhov, S.I.; Solovyeva, N.I.; Balaevskaya, T.O. Strongin AYa, The isolation and properties of collagenolytic proteases from crab hepatopancreas. Biochem. Biophys. Res. Commun., 1990, 166(3), 1411-1420.
[54]
Sakharov, I.Y.; Litvin, F.E. Stability of serine collagenolytic protease A from hepatopancreas of crab Paralithodes camtschatica. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1990, 97(3), 407-410.
[55]
Sakharov, I.Y.; Litvin, F.E.; Artyukov, A.A. Purification and characterization of two serine collagenolytic proteases from crab Paralithodes camtschatica. Comp. Biochem. Physiol. Biochem. Mol. Biol., 1994, 108(4), 561-568.
[56]
Sakharov, I.Y.; Litvin, F.E.; Mitkevitch, O.V.; Samokhin, G.P.; Bespalova, Z.D. Substrate specificity of collagenolytic proteases from the king crab Paralithodes camtschatica. Comp. Biochem. Physiol. Biochem. Mol. Biol., 1994, 107(3), 411-417.
[57]
Grant, G.A.; Henderson, K.O.; Eisen, A.Z.; Bradshaw, R.A. Amino acid sequence of a collagenolytic protease from the hepatopancreas of the fiddler crab, Uca pugilator. Biochemistry, 1980, 19(20), 4653-4659.
[58]
Welgus, H.G.; Grant, G.A. Degradation of collagen substrates by a trypsin-like serine protease from the fiddler crab Uca pugilator. Biochemistry, 1983, 22(9), 2228-2233.
[59]
Duarte, A.S.; Pereira, A.O.; Cabrita, A.M.; Moir, A.J.; Pires, E.M.; Barros, M.M. The characterisation of the collagenolytic activity of cardosin a demonstrates its potential application for extracellular matrix degradative processes. Curr. Drug Discov. Technol., 2005, 2(1), 37-44.
[60]
Pereira, A.O.; Cartucho, D.J.; Duarte, A.S.; Gil, M.H.; Cabrita, A.M.; Patrício, J.A.; Barros, M.M. Immobilisation of cardosin A in chitosan sponges as a novel implant for drug delivery. Curr. Drug Discov. Technol., 2005, 2(4), 231-238.
[61]
Corvo, I.; Cancela, M.; Cappetta, M.; Pi-Denis, N.; Tort, J.F.; Roche, L. The major cathepsin L secreted by the invasive juvenile Fasciola hepatica prefers proline in the S2 subsite and can cleave collagen. Mol. Biochem. Parasitol., 2009, 167(1), 41-47.
[62]
Hamdy, H.S. Extracellular collagenase from Rhizoctonia solani: Production, purification and characterization. Indian J. Biotechnol., 2008, 7, 333-340.
[63]
Savvateeva, L.V.; Gorokhovets, N.V.; Makarov, V.A.; Serebryakova, M.V.; Solovyev, A.G.; Morozov, S.Y.; Reddy, V.P.; Zernii, E.Y.; Zamyatnin, A.A., Jr; Aliev, G. Glutenase and collagenase activities of wheat cysteine protease Triticain-α: feasibility for enzymatic therapy assays. Int. J. Biochem. Cell Biol., 2015, 62, 115-124.
[64]
Gorokhovets, N.V.; Makarov, V.A.; Petushkova, A.I.; Prokopets, O.S.; Rubtsov, M.A.; Savvateeva, L.V.; Zernii, E.Y.; Zamyatnin, A.A., Jr Rational design of recombinant papain-like cysteine protease: Optimal domain structure and expression conditions for wheat-derived enzyme triticain-α. Int. J. Mol. Sci., 2017, 18(7), E1395.
[65]
Kim, M.; Hamilton, S.E.; Guddat, L.W.; Overall, C.M. Plant collagenase: unique collagenolytic activity of cysteine proteases from ginger. Biochim. Biophys. Acta, 2007, 1770(12), 1627-1635.
[66]
Taga, Y.; Kusubata, M.; Ogawa-Goto, K.; Hattori, S. Efficient absorption of x-hydroxyproline (hyp)-gly after oral administration of a novel gelatin hydrolysate prepared using ginger protease. J. Agric. Food Chem., 2016, 64(14), 2962-2970.
[67]
Souchet, N.; Laplante, S. Recovery and characterization of a serine collagenolytic extract from snow crab (Chionoecetes opilio) by-products. Appl. Biochem. Biotechnol., 2011, 163(6), 765-779.
[68]
Papisova, A.I.; Javadov, A.; Rudenskaya, Y.A.; Balandina, G.N.; Zhantiev, R.D.; Korsunovskaia, O.S.; Dunaevsky, Y.E.; Rudenskaya, G.N. Novel cathepsin L-like protease from dermestid beetle Dermestes frischii maggot. Biochimie, 2011, 93(2), 141-148.
[69]
Kristjánsson, M.M.; Guthmundsdóttir, S.; Fox, J.W.; Bjarnason, J.B. Characterization of a collagenolytic serine proteinase from the Atlantic cod (Gadus morhua). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1995, 110(4), 707-717.
[70]
Lima, C.A.; Marques, D.A.; Barros Neto, B.; Lima Filho, J.L.; Carneiro-da-Cunha, M.G.; Porto, A.L. Fermentation medium for collagenase production by Penicillium aurantiogriseum URM4622. Biotechnol. Prog., 2011, 27(5), 1470-1477.
[71]
Bogacheva, A.M.; Rudenskaya, G.N.; Dunaevsky, Y.E.; Chestuhina, G.G.; Golovkin, B.N. New subtilisin-like collagenase from leaves of common plantain. Biochimie, 2001, 83(6), 481-486.
[72]
Bracho, G.E.; Haard, N.F. Identification of two matrix metal-loproteinases in the skeletal muscle of Pacific rockfish (Se-bastes sp.). J. Food Biochem., 1995, 19(4), 299-319.
[73]
Uesugi, Y.; Arima, J.; Usuki, H.; Iwabuchi, M.; Hatanaka, T. Two bacterial collagenolytic serine proteases have different topological specificities. Biochim. Biophys. Acta, 2008, 1784(4), 716-726.
[74]
Luan, X.; Chen, J.; Zhang, X.H.; Li, Y.; Hu, G. Expression and characterization of a metalloprotease from a Vibrio parahaemolyticus isolate. Can. J. Microbiol., 2007, 53(10), 1168-1173.
[75]
Miyoshi, S.; Nakazawa, H.; Kawata, K.; Tomochika, K.; Tobe, K.; Shinoda, S. Characterization of the hemorrhagic reaction caused by Vibrio vulnificus metalloprotease, a member of the thermolysin family. Infect. Immun., 1998, 66(10), 4851-4855.
[76]
Olutiola, P.O.N.; Growth, R.I. sporulation and production of maltase and proteolytic enzymes in Aspergillus aculeatus. Trans. Br. Mycol. Soc., 1982, 78(1), 105-113.
[77]
Zhu, W.S.; Wojdyla, K.; Donlon, K.; Thomas, P.A.; Eberle, H.I. Extracellular proteases of Aspergillus flavus. Fungal keratitis, proteases, and pathogenesis. Diagn. Microbiol. Infect. Dis., 1990, 13(6), 491-497.
[78]
Suphatharaprateep, W.; Cheirsilp, B.; Jongjareonrak, A. Production and properties of two collagenases from bacteria and their application for collagen extraction. N. Biotechnol., 2011, 28(6), 649-655.
[79]
Wu, Q.; Li, C.; Li, C.; Chen, H.; Shuliang, L. Purification and characterization of a novel collagenase from Bacillus pumilus Col-J. Appl. Biochem. Biotechnol., 2010, 160(1), 129-139.
[80]
Roy, P.; Colas, B.; Durand, P. Purification, kinetical and molecular characterizations of a serine collagenolytic protease from greenshore crag (Carcinus maenas) digestive gland. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1996, 115(1), 87-95.
[81]
Matsushita, O.; Yoshihara, K.; Katayama, S.; Minami, J.; Okabe, A. Purification and characterization of Clostridium perfringens 120-kilodalton collagenase and nucleotide sequence of the corresponding gene. J. Bacteriol., 1994, 176(1), 149-156.
[82]
Iida, Y.; Nakagawa, T.; Nagayama, F. Properties of collagenolytic proteinase in Japanese spiny lobster and horsehair crab hepatopancreas. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1991, 98(2-3), 403-410.
[83]
Takahashi, S.; Seifter, S. An Enzyme with collagenolytic activity from dog pancreatic juice. Isr. J. Chem., 1974, 12(1‐2), 557-571.
[84]
Lecroisey, A.; Boulard, C.; Keil, B. Chemical and enzymatic characterization of the collagenase from the insect Hypoderma lineatum. Eur. J. Biochem., 1979, 101(2), 385-393.
[85]
Lecroisey, A.; Keil, B. Specificity of the collagenase from the insect Hypoderma lineatum. Eur. J. Biochem., 1985, 152(1), 123-130.
[86]
Burgos-Hernández, A.; Farias, S.I.; Torres-Arreola, W.; Ezquerra-Brauer, J.M. In vitro studies of the effects of afla-toxin B 1 and fumonisin B 1 on trypsin-like and collagenase-like activity from the hepatopancreas of white shrimp (Litopenaeus vannamei). Aquaculture, 2005, 250(1), 399-410.
[87]
Kim, S-K.; Park, P-J.; Kim, J-B.; Shahidi, F. Purification and characterization of a collagenolytic protease from the filefish, Novoden modestrus. J. Biochem. Mol. Biol., 2002, 35(2), 165-171.
[88]
Aoki, H.; Ahsan, M.N.; Matsuo, K.; Hagiwara, T.; Watabe, S. Purification and characterization of collagenolytic proteases from the hepatopancreas of northern shrimp (Pandalus eous). J. Agric. Food Chem., 2003, 51(3), 777-783.
[89]
Yoshinaka, R.; Sato, M.; Yamashita, M.; Itoko, M.; Ikeda, S. Specificity of the collagenolytic serine proteinase from the pancreas of the catfish (Parasilurus asotus). Comp. Biochem. Physiol. B, 1987, 88(2), 557-561.
[90]
Tsai, I.H.; Lu, P.J.; Chuang, J.L. The midgut chymotrypsins of shrimps (Penaeus monodon, Penaeus japonicus and Penaeus penicillatus). Biochim. Biophys. Acta, 1991, 1080(1), 59-67.
[91]
Kato, T.; Takahashi, N.; Kuramitsu, H.K. Sequence analysis and characterization of the Porphyromonas gingivalis prtC gene, which expresses a novel collagenase activity. J. Bacteriol., 1992, 174(12), 3889-3895.
[92]
Teruel, S.; Simpson, B. Characterization of the collagenolytic enzyme fraction from winter flounder (Pseudopleuronectes americanus). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1995, 112(1), 131-136.
[93]
Alexander, M.E.; Dresden, M.H. Collagenolytic enzymes from the starfish, Pycnopodia helianthoides. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1980, 67(4), 505-509.
[94]
Jeffrey, J.J.; Gross, J. Collagenase from rat uterus. Isolation and partial characterization. Biochemistry, 1970, 9(2), 268-273.
[95]
Tokoro, Y.; Eisen, A.Z.; Jeffrey, J.J. Characterization of a collagenase from rat skin. Biochim. Biophys. Acta, 1972, 258(1), 289-302.
[96]
Park, P.J.; Lee, S.H.; Byun, H.G.; Kim, S.H.; Kim, S.K. Purification and characterization of a collagenase from the mackerel, Scomber japonicus. J. Biochem. Mol. Biol., 2002, 35(6), 576-582.
[97]
Sivakumar, P.; Sampath, P.; Chandrakasan, G. Collagenolyt-ic metalloprotease (gelatinase) from the hepatopancreas of the marine crab, Scylla serrata. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1999, 123(3), 273-279.
[98]
Yoshinaka, R.; Sato, M.; Ikeda, S. Studies on collagenase in fish, 2: Some properties of a collagenase from the pyloric caeca of Seriola quinqueradiata. Nippon Suisan Gakkaishi, 42(4), 455-463.
[99]
Yoshinaka, R.; Sato, M.; Ikeda, S. Studies on collagenase in fish, 3: Purification and properties of a collagenase from the pyloric caeca of yellow-tail. Nihon-suisan-gakkai-shi, 1977, 43(10), 1195-1201.
[100]
Juarez, Z.E.; Stinson, M.W. An extracellular protease of Streptococcus gordonii hydrolyzes type IV collagen and collagen analogues. Infect. Immun., 1999, 67(1), 271-278.
[101]
Jain, R.; Jain, P.C. Production and partial characterization of collagenase of Streptomyces exfoliatus CFS 1068 using poultry feather. Indian J. Exp. Biol., 2010, 48(2), 174-178.
[102]
Byun, H.G.; Park, P.J.; Sung, N.I.; Kim, S.K. Purification and characterization of a serine proteinase from the tuna pyloric caeca. J. Food Biochem., 2002, 26(6), 479-494.
[103]
Sorsa, T.; Ding, Y.L.; Ingman, T.; Salo, T.; Westerlund, U.; Haapasalo, M.; Tschesche, H.; Konttinen, Y.T. Cellular source, activation and inhibition of dental plaque collagenase. J. Clin. Periodontol., 1995, 22(9), 709-717.
[104]
Barrett, A.J.A. Aspartic and Metallo Peptidases.Handbook of Proteolytic Enzymes, 2nd ed; , 2004, p. 1.
[105]
Gross, J.; Nagai, Y. Specific degradation of the collagen molecule by tadpole collagenolytic enzyme. Proc. Natl. Acad. Sci. USA, 1965, 54(4), 1197-1204.
[106]
Ramundo, J.; Gray, M. Collagenase for enzymatic debridement: A systematic review. J. Wound Ostomy Continence Nurs., 2009, 36(6)(Suppl.), S4-S11.
[107]
Waycaster, C.; Milne, C.T. Clinical and economic benefit of enzymatic debridement of pressure ulcers compared to autolytic debridement with a hydrogel dressing. J. Med. Econ., 2013, 16(7), 976-986.
[108]
Motley, T.A.; Lange, D.L.; Dickerson, J.E., Jr; Slade, H.B. Clinical outcomes associated with serial sharp debridement of diabetic foot ulcers with and without clostridial collagenase ointment. Wounds, 2014, 26(3), 57-64.
[109]
Hoppe, I.C.; Granick, M.S. Debridement of chronic wounds: A qualitative systematic review of randomized controlled trials. Clin. Plast. Surg., 2012, 39(3), 221-228.
[110]
Duarte, A.S.; Correia, A.; Esteves, A.C. Bacterial collagenases - A review. Crit. Rev. Microbiol., 2016, 42(1), 106-126.
[111]
Tallis, A.; Motley, T.A.; Wunderlich, R.P.; Dickerson, J.E., Jr; Waycaster, C.; Slade, H.B. Collagenase Diabetic Foot Ulcer Study, G. Clinical and economic assessment of diabetic foot ulcer debridement with collagenase: results of a random-ized controlled study. Clin. Ther., 2013, 35(11), 1805-1820.
[112]
McCallon, S.K.; Weir, D.; Lantis, J.C., II Optimizing wound bed preparation with collagenase enzymatic debridement. J. Am. Coll. Clin. Wound Spec., 2015, 6(1-2), 14-23.
[113]
Sheets, A.R.; Demidova-Rice, T.N.; Shi, L.; Ronfard, V.; Grover, K.V.; Herman, I.M. Identification and characterization of novel matrix-derived bioactive peptides: A role for collagenase from santyl® ointment in post-debridement wound healing? PLoS One, 2016, 11(7), e0159598.
[114]
Rudenskaya, G.; Isaev, V.; Shmoylov, A.; Karabasova, M.; Shvets, S.; Miroshnikov, A.; Brusov, A. Preparation of pro-teolytic enzymes from Kamchatka crab Paralithodes camchat-ica hepatopancreas and their application. Appl. Biochem. Biotechnol., 2000, 88(1-3), 175-183.
[115]
Shmoilov, A.M.; Rudenskaya, G.N.; Isaev, V.A.; Baydakov, A.V.; Zhantiev, R.D.; Korsunovskaya, O.S.; Ageeva, L.V.; Starikova, N.V. A comparative study of collagenase complex and new homogeneous collagenase preparations for scar treatment. J. Drug Deliv. Sci. Technol., 2006, 16(4), 285-292.
[116]
Sandakhchiev, L.S.; Stavskii, E.A.; Zinov’ey, V.V.; Nazarov, V.P.; Renau, I.V.; Satrikhina, T.N.; Katkova, L.R.; Krinitsin, L.A.; Markovich, N.A.; Kolesnikova, L.V. Effect of ointment containing king crab collagenase on infected wound. Bull. Exp. Biol. Med., 1997, 124(4), 992-995.
[117]
Manosroi, A.; Chankhampan, C.; Pattamapun, K.; Manosroi, W.; Manosroi, J. Antioxidant and gelatinolytic activities of papain from papaya latex and bromelain from pineapple fruits. Chiang Mai J.Sci., 2014, 41(3), 635-648.
[118]
Guzman, A.V.; Stein De Guzman, M.G. The enzymatic debridement of suppurations, necrotic lesions and burns with papain. J. Int. Coll. Surg., 1953, 20(6), 695-702.
[119]
Langer, V.; Bhandari, P.S.; Rajagopalan, S.; Mukherjee, M.K. Enzymatic debridement of large burn wounds with papain-urea: Is it safe? Med. J. Armed Forces India, 2013, 69(2), 144-150.
[120]
Levine, N.; Seifter, E.; Connerton, C.; Levenson, S.M. Debridement of experimental skin burns of pigs with bromelain, a pineapple-stem enzyme. Plast. Reconstr. Surg., 1973, 52(4), 413-424.
[121]
Rosenberg, L.; Shoham, Y.; Krieger, Y.; Rubin, G.; Sander, F.; Koller, J.; David, K.; Egosi, D.; Ahuja, R.; Singer, A.J. Minimally invasive burn care: A review of seven clinical studies of rapid and selective debridement using a bromelain-based debriding enzyme (Nexobrid®). Ann. Burns Fire Disasters, 2015, 28(4), 264-274.
[122]
Klasen, H.J. A review on the nonoperative removal of necrotic tissue from burn wounds. Burns, 2000, 26(3), 207-222.
[123]
Rob, C.; Singer, A. “Debricin”: A new agent for wound debridement. BMJ, 1959, 2(5159), 1069-1071.
[124]
Kadioglu, A.; Boyuk, A.; Salabas, E. Re: Clinical Efficacy of Collagenase Clostridium histolyticum in the Treatment of Peyronie’s Disease by Subgroups: Results from Two Large, Double-blind, Randomized, Placebo-controlled, Phase III Studies. Eur. Urol., 2015, 68(5), 908-909.
[125]
Dhillon, S. Collagenase Clostridium Histolyticum: A Review in Peyronie’s Disease. Drugs, 2015, 75(12), 1405-1412.
[126]
Gelbard, M.K.; Chagan, L.; Tursi, J.P. Collagenase Clostridium histolyticum for the treatment of Peyronie’s Disease: The development of this novel pharmacologic approach. J. Sex. Med., 2015, 12(6), 1481-1489.
[127]
Alwaal, A.; Hussein, A.A.; Zaid, U.B.; Lue, T.F. Management of Peyronie’s disease after collagenase (Xiaflex:®). Curr. Drug Targets, 2015, 16(5), 484-494.
[128]
Watt, A.J.H.V.R. Collagenase clostridium histolyticum: A novel nonoperative treatment for Dupuytren’s disease. Int. J. Clin. Rheumatol., 2011, 6(2), 123-133.
[129]
Warwick, D.; Arandes-Renú, J.M.; Pajardi, G.; Witthaut, J.; Hurst, L.C. Collagenase Clostridium histolyticum: Emerging practice patterns and treatment advances. J. Plast. Surg. Hand Surg., 2016, 50(5), 251-261.
[130]
Rubin, G.; Rinott, M.; Wolovelsky, A.; Rosenberg, L.; Shoham, Y.; Rozen, N. A new bromelain-based enzyme for the release of Dupuytren’s contracture: Dupuytren’s enzymatic bromelain-based release. Bone Joint Res., 2016, 5(5), 175-177.
[131]
Sangkum, P.; Yafi, F.A.; Kim, H.; Bouljihad, M.; Ranjan, M.; Datta, A.; Mandava, S.H.; Sikka, S.C.; Abdel-Mageed, A.B.; Moparty, K.; Hellstrom, W.J. Collagenase Clostridium histolyticum (Xiaflex) for the treatment of urethral stricture disease in a rat model of urethral fibrosis. Urology, 2015, 86(3), e641-e646.
[132]
Kang, N.; Sivakumar, B.; Sanders, R.; Nduka, C.; Gault, D. Intra-lesional injections of collagenase are ineffective in the treatment of keloid and hypertrophic scars. J. Plast. Reconstr. Aesthet. Surg., 2006, 59(7), 693-699.
[133]
Bae-Harboe, Y.S.; Harboe-Schmidt, J.E.; Graber, E.; Gilchrest, B.A. Collagenase followed by compression for the treatment of earlobe keloids. Dermatol. Surg., 2014, 40(5), 519-524.
[134]
Paramonov, B.A. Turkovskii, II; Bondarev, S.V. [Application of enzymes for treatment of patients with hypertrophic cicatrices] Vestn. Khir. Im. I I Grek., 2007, 166(4), 84-85.
[135]
Lebedev, O.I. [Regulation of reparative processes in glaucoma surgery by collalysin]. Vestn. Oftalmol., 1989, 105(3), 4-6.
[136]
Cakir, M.; Tekin, A.; Kucukkartallar, T.; Yılmaz, H.; Belviranlı, M.; Kartal, A. Effectiveness of collagenase in preventing postoperative intra-abdominal adhesions. Int. J. Surg., 2013, 11(6), 487-491.
[137]
Aysan, E.; Bektas, H.; Ersoz, F.; Behzat, K. Role of single-dose clostridiopeptidase A collagenase in peritoneal adhesions. European surgical research. Eur. Surg. Res., 2011, 47(3), 130-134.
[138]
Zhang, D.; Zhang, Y.; Wang, Z.; Zhang, X.; Sheng, M. Target radiofrequency combined with collagenase chemonucleolysis in the treatment of lumbar intervertebral disc herniation. Int. J. Clin. Exp. Med., 2015, 8(1), 526-532.
[139]
Simmons, J.W.; Nordby, E.J.; Hadjipavlou, A.G. Chemonucleolysis: The state of the art. Eur. Spine J., 2001, 10(3), 192-202.
[140]
Johnson, K.; Zhu, S.; Tremblay, M.S.; Payette, J.N.; Wang, J.; Bouchez, L.C.; Meeusen, S.; Althage, A.; Cho, C.Y.; Wu, X.; Schultz, P.G. A stem cell-based approach to cartilage repair. Science, 2012, 336(6082), 717-721.
[141]
Bertassoni, L.E.; Marshall, G.W. Papain-gel degrades intact nonmineralized type I collagen fibrils. Scanning, 2009, 31(6), 253-258.
[142]
Dayem, R.N.; Tameesh, M.A. A new concept in hybridization: Bromelain enzyme for deproteinizing dentin before application of adhesive system. Contemp. Clin. Dent., 2013, 4(4), 421-426.
[143]
Chernyakov, A.R.S. Method for producing a combined preparation exhibiting collagenase activity., 2009.
[144]
Cazander, G.; Pritchard, D.I.; Nigam, Y.; Jung, W.; Nibbering, P.H. Multiple actions of Lucilia sericata larvae in hard-to-heal wounds: larval secretions contain molecules that accelerate wound healing, reduce chronic inflammation and inhibit bacterial infection. BioEssays, 2013, 35(12), 1083-1092.
[145]
Chambers, L.; Woodrow, S.; Brown, A.P.; Harris, P.D.; Phillips, D.; Hall, M.; Church, J.C.; Pritchard, D.I. Degradation of extracellular matrix components by defined proteinases from the greenbottle larva Lucilia sericata used for the clinical debridement of non-healing wounds. Br. J. Dermatol., 2003, 148(1), 14-23.
[146]
Li, Z.J.; Kim, S.M. The application of the starfish hatching enzyme for the improvement of scar and keloid based on the fibroblast-populated collagen lattice. Appl. Biochem. Biotechnol., 2014, 173(4), 989-1002.
[147]
Turkiewicz, M.; Galas, E.; Kalinowska, H. Collagenolytic serine proteinase from Euphausia superba Dana (Antarctic krill). Comp. Biochem. Physiol. B, 1991, 99(2), 359-371.
[148]
Mekkes, J.R.; Le Poole, I.C.; Das, P.K.; Bos, J.D.; Westerhof, W. Efficient debridement of necrotic wounds using proteolytic enzymes derived from Antarctic krill: a double-blind, placebo-controlled study in a standardized animal wound model. Wound Repair Regen., 1998, 6(1), 50-57.
[149]
Westerhof, W.; van Ginkel, C.J.; Cohen, E.B.; Mekkes, J.R. Prospective randomized study comparing the debriding effect of krill enzymes and a non-enzymatic treatment in venous leg ulcers. Dermatologica, 1990, 181(4), 293-297.
[150]
Lee, S-G.; Koh, H-Y.; Lee, H-K.; Yim, J-H. Possible roles of Antarctic krill proteases for skin regeneration. Ocean Polar Res., 2008, 30(4), 467-472.
[151]
Rajesh, R.; Shivaprasad, H.V.; Gowda, C.D.R.; Nataraju, A.; Dhananjaya, B.L.; Vishwanath, B.S. Comparative study on plant latex proteases and their involvement in hemostasis: A special emphasis on clot inducing and dissolving properties. Planta Med., 2007, 73(10), 1061-1067.
[152]
Yariswamy, M.; Shivaprasad, H.V.; Joshi, V.; Nanjaraj Urs, A.N.; Nataraju, A.; Vishwanath, B.S. Topical application of serine proteases from Wrightia tinctoria R. Br. (Apocyanaceae) latex augments healing of experimentally induced excision wound in mice. J. Ethnopharmacol., 2013, 149(1), 377-383.
[153]
Kemparaju, K.; Manasagangothri, M. Biochemical characterization of protease isoforms in cucumber sap extract. Int. J. Pharm. Phytopharmacol. Res, 2014, 4(2), 77-83.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 3
Year: 2019
Page: [487 - 505]
Pages: 19
DOI: 10.2174/0929867324666171006124236
Price: $58

Article Metrics

PDF: 29
HTML: 3
EPUB: 1
PRC: 1