Collagenase from smooth weakfish: extraction, partial purification, characterization and collagen specificity test for industrial application
DOI:
https://doi.org/10.20950/1678-2305.2017v43n1p52Keywords:
byproducts, collagenolytic protease, Cynoscion leiarchus, smooth weakfish, wastesAbstract
Fish processing residues are rich sources of biomolecules with industrial potential, such as enzymes with collagenolytic properties applied in the pharmaceutical, textile and leather sectors. Here, collagenolytic serine proteases were partially purified from the waste (viscera) of smooth weakfish Cynoscion leiarchus and characterized for the purpose of obtaining a value-added product from fisheries resources. The higher activity of the enzyme (72.5 U mL-1) was verified in optimal temperature and pH of 55°C and 8.0 respectively. The enzyme was stable in wide ranges of temperature (25í 60°C) and pH (6.5 to 11.5). The ions Ca2+ and Mg2+ increased the protease activity, whilst Pb2+, Al3+ and Cu2+ had an inhibitory effect, as observed in the presence of Benzamidine and TLCK (inhibitors of serine proteases). Hydrolysis was detected after 48 hours, when the enzyme and bovine collagen type I were incubated together. Thus, digestive viscera of C. leiarchus is suggested as an alternative source of enzymes capable of cleaving type I collagen, with similar biochemical properties to those of bacterial collagenases commonly employed in industrial processes, reducing costs, adding value to the fisheries product and minimizing the environmental impact caused by its waste.
References
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elastolytic and keratinolytic proteases in peptidelimited cultures of two Bacillus cereus strains
isolated from wool. Journal of Applied Microbiology,107(1): 226 í 234.
BEZERRA, R.S.; BUARQUE, D.S.; AMARAL, I.P.G.;CASTRO, P.F.; ESPÓSITO, T.S.; CARVALHO JR,
L.B. 2006 Propriedades e aplicações biotecnológicas das proteases de vísceras de peixes. In: CYRINO,J.E.P.; URBINATI, E.C. AquaCiência 2004 Tópicos Especiais em Biologia Aquática e Aquicultura. Artpoint Produção Gráfica, Campinas. p. 261 í 275.
BAEHAKI, A.; SUHARTONO, M.T.; SUKARNO; SYAH, D.; SITANGGANG, A.B., SETYAHADI,
S.; MEINHARDT, F. 2012 Purification and characterization of collagenase from Bacillus
licheniformis F11.4. African Journal of Microbiology Research, 6(10): 2373í 2379.
BYUN, H.G.; PARK, P.J.; SUNG, N.J.; KIM, S.K. 2002 Purification and characterization of a serine
proteinase from the tuna pyloric caeca. Journal of Food Biochemistry, 26(6): 479í 494.
CHUNG, H.J.; UITTO, J. 2010 Type VII Collagen: the anchoring fibril protein at fault in dystrophic
epidermolysis bullosa. Dermatologic Clinics, 28(1):93í 105.
MINISTÉRIO DA PESCA E AQUICULTURA (MPA). Boletim estatístico da pesca e aquicultura Brasil
2011. Disponível em: < http://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/
estatistica/est_2011_bol__bra.pdf> Acesso: 10 dez.2013.
DABOOR, S.M.; BUDGE, S.M.; GHALY, A.E.; BROOKS,M.S.; DAVE, D. 2010 Extraction and Purification
of Collagenase Enzymes: A Critical Review.American Journal of Biochemistry and Biotechnology,
6(4): 239-263.
DABOOR, S.M.; BUDGE, S.M.; GHALY, A.E.; BROOKS,M.S.; DAVE, D. 2012 Isolation and activation of
collagenase from fish processing waste. Advances in Bioscience and Biotechnology, 3: 191í 203.
FAO í Food and Agriculture Organization. 2013 World Bank 2013 Fish to 2030: prospects for fisheries and aquaculture. In: Agriculture and environmental services discussion paper; no. 3. World Bank Group, FAO, Washington DC. 102 p.
FAO í Food and Agriculture Organization. 2012 FAO yearbook 2014 Fishery and Aquaculture Statistics.FAO, Rome. 76 p.
FERREIRA, A.M.; GENTILE, P.; CHIONO, V.;CIARDELLI, G. 2012 Collagen for bone tissue
regeneration. Acta Biomaterialia, 8(9): 3191í 3200.
FRANí"¡A, R.C.P.; ASSIS, C.R.D.; SANTOS, J.F.; TORQUATO, R.J.S.; TANAKA, A.S.; HIRATA,
I.Y.; ASSIS, D.M.; JULIANO, M.A.; CAVALLI, R.O.; CARVALHO JR, L.B.; BEZERRA, R.S. 2016
Bovine pancreatic trypsin inhibitor immobilized onto sepharose as a new strategy to purify a
thermostable alkaline peptidase from cobia (Rachycentron canadum) processing waste.
Comparative Biochemistry and Physiology - Part B,1033-1034: 210-217.
HAYET, B.K.; RYM, N.; ALI, B.; SOFIANE, G.;MONCEF, N. 2011 Low molecular weight serine
protease from the viscera of sardinelle (Sardinella aurita) with collagenolytic activity: Purification
and characterization. Food Chemistry, 124: 788í 794.
HERNANDEZ-HERRERO, M.M.; DUFLOS, G.; MALLE, P.; BOUQUELET, S. 2003 Collagenase
activity and protein hydrolysis as related to spoilage of iced cod (Gadus morhua). Food Research
International, 36(2): 141í 147.
J A Y A T H I L A K A N , K . ; S U L T A N A , K . ;RADHAKRISHNA, K.; BAWA, A.S. 2012 Utilization of byproducts and waste materials from meat, poultry and fish processing industries:
a review. Journal of Food Science and Technology, 49(3): 278í 293.
KANTH, S.V.; VENBA, R.; MADHAN, B.;CHANDRABABU, N.K.; SADULLA, S. 2008 Studies on the influence of bacterial collagenase in leather dyeing. Dyes Pigments 76(2): 338-347.
KIM, S.K.; MENDS, E. 2006 Bioactive compounds from marine processing byprodcts í A review. Food Research International, 39(4): 383í 393.
KIM, S. K.; PARK, P. J.; KIM, J.B.; SHAHIDI, F. 2002 Purification and characterization of a collagenolytic protease from the filefish, Novoden modestrus. Journal of biochemistry and molecular biology, 35(2):165-171.
KLOMKLAO, S. 2008 Digestive proteinases from marine organisms and their applications. Songklanakarin Journal of Science and Technology, 30(1): 37í 48.
KRISTJÁNSSON, M. M.; GUDMUNDSDÓTTIR S.; FOX, J. W.; BJARNASON, J. B. 1995 Characterization of collagenolytic serine proreinase from the Atlantic cod (Gadus morhua). Comparative Biochemistry and Physiology - Part B, 110(4): 707í 717.
LIMA, C.A.; FREITAS JUNIOR, A.C.V.; LIMA FILHO, J.L.; CONVERTI, A.; MARQUES, D.A.V.;
CARNEIRO-DA-CUNHA, M.G.; PORTO, A.L.F. 2013 Two-phase partitioning and partial
characterization of a colagenase from Penicillium aurantiogriseum URM4622: Application to collagen hydrolysis. Biochemical Engineering Journal, 75:64í 71.
MAKAREEVA, E.; LEIKIN, S. 2014. Collagen structure, folding and function. In: SHAPIRO, J.R.; BYERS,
P.H.; GLORIEUX, F.H.; SPONSELLER, P.D. Osteogenesis imperfecta: a translational approach
to Brittle Bone Disease. Elsevier, New York. p. 7-83.
MOORE, S.; STEIN, W. 1954 A modified ninhydrin reagent for the photometric determination of
amino acids and related compounds. The Journal of Biological Chemistry, 211(2): 907í 913.
MUKHERJEE, J.; WEBSTER, N.; LLEWELLYN, L.E. 2009 Purification and Characterization of a
Collagenolytic Enzyme from a Pathogen of the Great Barrier Reef Sponge, Rhopaloeides odorabile. PLoS ONE, 4(9): 1í 5.
MURADO, M.A.; GONZÁLEZ, M.P.; VÁZQUEZ, J.A. 2009 Recovery of proteolytic and collagenolytic
activities from viscera by-products of Rayfish (Raja clavata). Mar Drugs, 7(4): 803í 815.
MYLLYHARJU, J.; KIVIRIKKO, K.I. 2004 Collagens, modifying enzymes and their mutations in
humans, flies and worms. Trends in Genetics, 20(1):33í 43.
OLIVEIRA, V.M.; ASSIS, C. R. D.; COSTA, H. M. S.;SILVA, R. P. F.; SANTOS, J. F.; CARVALHO JR,
L. B.; BEZERRA, R. S. 2017a Aluminium sulfate exposure: A set of effects on hydrolases from brain,
muscle and digestive tract of juvenile Nile tilapia (Oreochromis niloticus). Comparative Biochemistry and Physiology - Part C, 191: 101-108.
OLIVEIRA, V.M., CARNEIRO CUNHA, M.N.; ASSIS, C.R.D.; NASCIMENTO, T.P.; HERCULANO, P.N.; CAVALCANTI, M.T.H.; PORTO, A.L. 2017b Colagenases de pescado e suas aplicações industriais. Pubvet, 11(3): 243-255.
PARK, J.P.; LEE, S.H.; BYUN, H.G.; KIM, S.H.; KIM, S.K. 2002 Purification and characterization of a
collagenase from the mackerel, Scomber japonicus. Journal of biochemistry and molecular iology, 35(6): 576í 582.
ROY, P.; BERNARD, C.; PATRICK, D. 1996 Purification, kinetical and molecular characterizations of a
serine collagenolytic protease from green shore Crab (Carcinus maenas) digestive gland. Comparative Biochemistry and Physiology - Part B, 115: 87í 95.
SARAN, S.; MAHAJAN, R.V.; KAUSHIK, R.; ISAR, J.; SAXENA, R. 2013 Enzyme mediated beam house
operations of leather industry: a needed step towards greener technology. Journal of Cleaner
Production, 54: 315-322.
SMITH, P.K.; KROHN, R.I.; HERMANSON, G.T.;MALLIA, A.K.; GARTNER, F.H.; PROVENZANO,
M.D.; FUJIMOTO, E.K.; GOEKE, N.M.; OLSON, B.J.; KLENK, D.C. 1985 Measurement of protein
using bicinchoninic acid. Analytical Biochemistry,150(1): 76í 85.
SIMPSON, B.K. 2000 Digestive proteinases from marine animals. In: HAARD, N.F.; SIMPSON, B.K. Seafood Enzymes: Utilization and Influence on Postharvest Seafood Quality. Marcel Dekker, New York. p. 531-540.
Sí–DERHí"žLL, C.; MARENHOLZ, I.; KERSCHER, T.;RíÅ“SCHENDORF, F.; ESPARZA-GORDILLO, J.;
WORM, M.; GRUBER, C.; MAYR, G.; ALBRECHT,M.; ROHDE, K.; SCHULZ, H.; WAHN, U.; HUBNER, N.; LEE, Y.A. 2007 Variants in a novel epidermal collagen gene (COL29A1) are associated with atopic dermatitis. PLOS Biology, 5(9): 1952-1961.
SOUZA, A.A.G.; AMARAL, I.P.G.; ESPÍRITO SANTO, A.R.; CARVALHO JR, L.B., BEZERRA, R.S. 2007
Trypsin-like enzyme from intestine and pyloric caeca of spotted goatfish (Pseudupeneus maculatus).Food Chemistry, 100(4): 1429í 1434.
SOVIK, S.L.; RUSTAD, T. 2006 Effect of season and fishing ground on the activity of cathepsin B and
collagenase in by-products from cod species. LWTFood Science and Technology, 39(1): 43í 53.
SOUCHET, N.; LAPLANTE, S. 2011 Recovery and Characterization of a serine collagenolytic extract
from Snow Crab (Chionoecetes opilio) by-products.Applied Biochemistry and Biotechnology, 163(6):765í 779.
SUPHATHARAPRATEEP, W.; CHEIRSILP, B.;JONGJAREONRAK, A. 2011 Production and properties of two collagenases from bacteria and their application for collagen extraction. New Biotechnology, 28(6): 649í 655.
TERUEL, S.R.L.T. 1997 Purification and characterizationof collagenases from the skeletal muscle of winter flounder (Pseudopleuronectes americanus), Quebec, Canada. Montreal. 204f. (Doctor of Phylosophy Thesis. McGill University) Disponível em: http://digitool.library.mcgill.ca/R/?func=dbin-jumpfull&object_id=34467&local_base=GEN01-MCG02 Acesso em: 20 jan. 2016.
TERUEL, S.R.L., SIMPSON, B.K. 1995 Characterization of the collagenolytic enzyme fraction from
winter flounder (Pseudopleuronectes americanus). Comparative Biochemistry and Physiology - Part B,112(1): 131-136.
TURKIEWICZ, M.; GALAS, E.; KALINOWSKA, H. 1991 Collagenolytic serine proteinase from Euphausia superba dana (Antarctic Krill). Comparative Biochemistry and Physiology - Part B, 99(2): 359í 371.
WU, G.P.; CHEN, S.H.; LIU, G.M.; YOSHIDA,A.; ZHANG, L.J.; SU, W.J.; CAO, M.J. 2010a Purification and characterization of a collagenolytic serine proteinase from the skeletal muscle of red sea bream (Pagrus major). Comparative Biochemistry and Physiology - Part B, 155(3): 281í 287.
WU, Q.; LI, C.; LI, C.; CHEN, H.; SHULIANG, L. 2010b Purification and characterization of a novel
collagenase from Bacillus pumilus Col-J. Applied Biochemistry and Biotechnology, 160(1): 129í 139.
YOSHINAKA, R.; SATO, M.; IKEDA, S. 1978 Distribution of collagenase in the digestive of some teleost. Bulletin of the Japanese Society for the Science of Fish,44: 26 í 267.
elastolytic and keratinolytic proteases in peptidelimited cultures of two Bacillus cereus strains
isolated from wool. Journal of Applied Microbiology,107(1): 226 í 234.
BEZERRA, R.S.; BUARQUE, D.S.; AMARAL, I.P.G.;CASTRO, P.F.; ESPÓSITO, T.S.; CARVALHO JR,
L.B. 2006 Propriedades e aplicações biotecnológicas das proteases de vísceras de peixes. In: CYRINO,J.E.P.; URBINATI, E.C. AquaCiência 2004 Tópicos Especiais em Biologia Aquática e Aquicultura. Artpoint Produção Gráfica, Campinas. p. 261 í 275.
BAEHAKI, A.; SUHARTONO, M.T.; SUKARNO; SYAH, D.; SITANGGANG, A.B., SETYAHADI,
S.; MEINHARDT, F. 2012 Purification and characterization of collagenase from Bacillus
licheniformis F11.4. African Journal of Microbiology Research, 6(10): 2373í 2379.
BYUN, H.G.; PARK, P.J.; SUNG, N.J.; KIM, S.K. 2002 Purification and characterization of a serine
proteinase from the tuna pyloric caeca. Journal of Food Biochemistry, 26(6): 479í 494.
CHUNG, H.J.; UITTO, J. 2010 Type VII Collagen: the anchoring fibril protein at fault in dystrophic
epidermolysis bullosa. Dermatologic Clinics, 28(1):93í 105.
MINISTÉRIO DA PESCA E AQUICULTURA (MPA). Boletim estatístico da pesca e aquicultura Brasil
2011. Disponível em: < http://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/
estatistica/est_2011_bol__bra.pdf> Acesso: 10 dez.2013.
DABOOR, S.M.; BUDGE, S.M.; GHALY, A.E.; BROOKS,M.S.; DAVE, D. 2010 Extraction and Purification
of Collagenase Enzymes: A Critical Review.American Journal of Biochemistry and Biotechnology,
6(4): 239-263.
DABOOR, S.M.; BUDGE, S.M.; GHALY, A.E.; BROOKS,M.S.; DAVE, D. 2012 Isolation and activation of
collagenase from fish processing waste. Advances in Bioscience and Biotechnology, 3: 191í 203.
FAO í Food and Agriculture Organization. 2013 World Bank 2013 Fish to 2030: prospects for fisheries and aquaculture. In: Agriculture and environmental services discussion paper; no. 3. World Bank Group, FAO, Washington DC. 102 p.
FAO í Food and Agriculture Organization. 2012 FAO yearbook 2014 Fishery and Aquaculture Statistics.FAO, Rome. 76 p.
FERREIRA, A.M.; GENTILE, P.; CHIONO, V.;CIARDELLI, G. 2012 Collagen for bone tissue
regeneration. Acta Biomaterialia, 8(9): 3191í 3200.
FRANí"¡A, R.C.P.; ASSIS, C.R.D.; SANTOS, J.F.; TORQUATO, R.J.S.; TANAKA, A.S.; HIRATA,
I.Y.; ASSIS, D.M.; JULIANO, M.A.; CAVALLI, R.O.; CARVALHO JR, L.B.; BEZERRA, R.S. 2016
Bovine pancreatic trypsin inhibitor immobilized onto sepharose as a new strategy to purify a
thermostable alkaline peptidase from cobia (Rachycentron canadum) processing waste.
Comparative Biochemistry and Physiology - Part B,1033-1034: 210-217.
HAYET, B.K.; RYM, N.; ALI, B.; SOFIANE, G.;MONCEF, N. 2011 Low molecular weight serine
protease from the viscera of sardinelle (Sardinella aurita) with collagenolytic activity: Purification
and characterization. Food Chemistry, 124: 788í 794.
HERNANDEZ-HERRERO, M.M.; DUFLOS, G.; MALLE, P.; BOUQUELET, S. 2003 Collagenase
activity and protein hydrolysis as related to spoilage of iced cod (Gadus morhua). Food Research
International, 36(2): 141í 147.
J A Y A T H I L A K A N , K . ; S U L T A N A , K . ;RADHAKRISHNA, K.; BAWA, A.S. 2012 Utilization of byproducts and waste materials from meat, poultry and fish processing industries:
a review. Journal of Food Science and Technology, 49(3): 278í 293.
KANTH, S.V.; VENBA, R.; MADHAN, B.;CHANDRABABU, N.K.; SADULLA, S. 2008 Studies on the influence of bacterial collagenase in leather dyeing. Dyes Pigments 76(2): 338-347.
KIM, S.K.; MENDS, E. 2006 Bioactive compounds from marine processing byprodcts í A review. Food Research International, 39(4): 383í 393.
KIM, S. K.; PARK, P. J.; KIM, J.B.; SHAHIDI, F. 2002 Purification and characterization of a collagenolytic protease from the filefish, Novoden modestrus. Journal of biochemistry and molecular biology, 35(2):165-171.
KLOMKLAO, S. 2008 Digestive proteinases from marine organisms and their applications. Songklanakarin Journal of Science and Technology, 30(1): 37í 48.
KRISTJÁNSSON, M. M.; GUDMUNDSDÓTTIR S.; FOX, J. W.; BJARNASON, J. B. 1995 Characterization of collagenolytic serine proreinase from the Atlantic cod (Gadus morhua). Comparative Biochemistry and Physiology - Part B, 110(4): 707í 717.
LIMA, C.A.; FREITAS JUNIOR, A.C.V.; LIMA FILHO, J.L.; CONVERTI, A.; MARQUES, D.A.V.;
CARNEIRO-DA-CUNHA, M.G.; PORTO, A.L.F. 2013 Two-phase partitioning and partial
characterization of a colagenase from Penicillium aurantiogriseum URM4622: Application to collagen hydrolysis. Biochemical Engineering Journal, 75:64í 71.
MAKAREEVA, E.; LEIKIN, S. 2014. Collagen structure, folding and function. In: SHAPIRO, J.R.; BYERS,
P.H.; GLORIEUX, F.H.; SPONSELLER, P.D. Osteogenesis imperfecta: a translational approach
to Brittle Bone Disease. Elsevier, New York. p. 7-83.
MOORE, S.; STEIN, W. 1954 A modified ninhydrin reagent for the photometric determination of
amino acids and related compounds. The Journal of Biological Chemistry, 211(2): 907í 913.
MUKHERJEE, J.; WEBSTER, N.; LLEWELLYN, L.E. 2009 Purification and Characterization of a
Collagenolytic Enzyme from a Pathogen of the Great Barrier Reef Sponge, Rhopaloeides odorabile. PLoS ONE, 4(9): 1í 5.
MURADO, M.A.; GONZÁLEZ, M.P.; VÁZQUEZ, J.A. 2009 Recovery of proteolytic and collagenolytic
activities from viscera by-products of Rayfish (Raja clavata). Mar Drugs, 7(4): 803í 815.
MYLLYHARJU, J.; KIVIRIKKO, K.I. 2004 Collagens, modifying enzymes and their mutations in
humans, flies and worms. Trends in Genetics, 20(1):33í 43.
OLIVEIRA, V.M.; ASSIS, C. R. D.; COSTA, H. M. S.;SILVA, R. P. F.; SANTOS, J. F.; CARVALHO JR,
L. B.; BEZERRA, R. S. 2017a Aluminium sulfate exposure: A set of effects on hydrolases from brain,
muscle and digestive tract of juvenile Nile tilapia (Oreochromis niloticus). Comparative Biochemistry and Physiology - Part C, 191: 101-108.
OLIVEIRA, V.M., CARNEIRO CUNHA, M.N.; ASSIS, C.R.D.; NASCIMENTO, T.P.; HERCULANO, P.N.; CAVALCANTI, M.T.H.; PORTO, A.L. 2017b Colagenases de pescado e suas aplicações industriais. Pubvet, 11(3): 243-255.
PARK, J.P.; LEE, S.H.; BYUN, H.G.; KIM, S.H.; KIM, S.K. 2002 Purification and characterization of a
collagenase from the mackerel, Scomber japonicus. Journal of biochemistry and molecular iology, 35(6): 576í 582.
ROY, P.; BERNARD, C.; PATRICK, D. 1996 Purification, kinetical and molecular characterizations of a
serine collagenolytic protease from green shore Crab (Carcinus maenas) digestive gland. Comparative Biochemistry and Physiology - Part B, 115: 87í 95.
SARAN, S.; MAHAJAN, R.V.; KAUSHIK, R.; ISAR, J.; SAXENA, R. 2013 Enzyme mediated beam house
operations of leather industry: a needed step towards greener technology. Journal of Cleaner
Production, 54: 315-322.
SMITH, P.K.; KROHN, R.I.; HERMANSON, G.T.;MALLIA, A.K.; GARTNER, F.H.; PROVENZANO,
M.D.; FUJIMOTO, E.K.; GOEKE, N.M.; OLSON, B.J.; KLENK, D.C. 1985 Measurement of protein
using bicinchoninic acid. Analytical Biochemistry,150(1): 76í 85.
SIMPSON, B.K. 2000 Digestive proteinases from marine animals. In: HAARD, N.F.; SIMPSON, B.K. Seafood Enzymes: Utilization and Influence on Postharvest Seafood Quality. Marcel Dekker, New York. p. 531-540.
Sí–DERHí"žLL, C.; MARENHOLZ, I.; KERSCHER, T.;RíÅ“SCHENDORF, F.; ESPARZA-GORDILLO, J.;
WORM, M.; GRUBER, C.; MAYR, G.; ALBRECHT,M.; ROHDE, K.; SCHULZ, H.; WAHN, U.; HUBNER, N.; LEE, Y.A. 2007 Variants in a novel epidermal collagen gene (COL29A1) are associated with atopic dermatitis. PLOS Biology, 5(9): 1952-1961.
SOUZA, A.A.G.; AMARAL, I.P.G.; ESPÍRITO SANTO, A.R.; CARVALHO JR, L.B., BEZERRA, R.S. 2007
Trypsin-like enzyme from intestine and pyloric caeca of spotted goatfish (Pseudupeneus maculatus).Food Chemistry, 100(4): 1429í 1434.
SOVIK, S.L.; RUSTAD, T. 2006 Effect of season and fishing ground on the activity of cathepsin B and
collagenase in by-products from cod species. LWTFood Science and Technology, 39(1): 43í 53.
SOUCHET, N.; LAPLANTE, S. 2011 Recovery and Characterization of a serine collagenolytic extract
from Snow Crab (Chionoecetes opilio) by-products.Applied Biochemistry and Biotechnology, 163(6):765í 779.
SUPHATHARAPRATEEP, W.; CHEIRSILP, B.;JONGJAREONRAK, A. 2011 Production and properties of two collagenases from bacteria and their application for collagen extraction. New Biotechnology, 28(6): 649í 655.
TERUEL, S.R.L.T. 1997 Purification and characterizationof collagenases from the skeletal muscle of winter flounder (Pseudopleuronectes americanus), Quebec, Canada. Montreal. 204f. (Doctor of Phylosophy Thesis. McGill University) Disponível em: http://digitool.library.mcgill.ca/R/?func=dbin-jumpfull&object_id=34467&local_base=GEN01-MCG02 Acesso em: 20 jan. 2016.
TERUEL, S.R.L., SIMPSON, B.K. 1995 Characterization of the collagenolytic enzyme fraction from
winter flounder (Pseudopleuronectes americanus). Comparative Biochemistry and Physiology - Part B,112(1): 131-136.
TURKIEWICZ, M.; GALAS, E.; KALINOWSKA, H. 1991 Collagenolytic serine proteinase from Euphausia superba dana (Antarctic Krill). Comparative Biochemistry and Physiology - Part B, 99(2): 359í 371.
WU, G.P.; CHEN, S.H.; LIU, G.M.; YOSHIDA,A.; ZHANG, L.J.; SU, W.J.; CAO, M.J. 2010a Purification and characterization of a collagenolytic serine proteinase from the skeletal muscle of red sea bream (Pagrus major). Comparative Biochemistry and Physiology - Part B, 155(3): 281í 287.
WU, Q.; LI, C.; LI, C.; CHEN, H.; SHULIANG, L. 2010b Purification and characterization of a novel
collagenase from Bacillus pumilus Col-J. Applied Biochemistry and Biotechnology, 160(1): 129í 139.
YOSHINAKA, R.; SATO, M.; IKEDA, S. 1978 Distribution of collagenase in the digestive of some teleost. Bulletin of the Japanese Society for the Science of Fish,44: 26 í 267.
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2017-03-21
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