Collagenolytic enzymes produced by fungi: a systematic review

Wanderley, Maria Carolina de Albuquerque; Duarte, José Manoel Wanderley; Lima, José Luiz de; Lima, Carolina de Albuquerque; Teixeira, José António Couto; Porto, Ana Lúcia Figueiredo

doi:10.1016/j.bjm.2016.08.001

Maria Carolina de Albuquerque Wanderley

Universidade Federal de Pernambuco (UFPE), Laboratório de Imunopatologia Keizo Asami (LIKA), Recife, PE, Brasil

José Manoel Wanderley Duarte Neto

Universidade Federal de Pernambuco (UFPE), Laboratório de Imunopatologia Keizo Asami (LIKA), Recife, PE, Brasil

José Luiz de Lima Filho

Universidade Federal de Pernambuco (UFPE), Laboratório de Imunopatologia Keizo Asami (LIKA), Recife, PE, Brasil

Carolina de Albuquerque Lima

Universidade de Pernambuco (UPE), Faculdade de Ciências, Educação e Tecnologia de Garanhuns, Garanhuns, PE, Brasil

José António Couto Teixeira

Universidade do Minho (UMinho), Centro de Engenharia Biológica, Braga, Portugal

Ana Lúcia Figueiredo Porto ^**Corresponding author at: Department of Morphology and Animal Physiology, Federal Rural University of Pernambuco, Av. Dom Manoel de Medeiros, s/n, 52171-900 Recife, PE, Brazil. E-mail: analuporto@yahoo.com.br (A.L. Porto).

Universidade Federal Rural de Pernambuco (UFRPE), Departamento de Morfologia e Fisiologia Animal, Recife, PE, Brasil

*Corresponding author at: Department of Morphology and Animal Physiology, Federal Rural University of Pernambuco, Av. Dom Manoel de Medeiros, s/n, 52171-900 Recife, PE, Brazil. E-mail: analuporto@yahoo.com.br (A.L. Porto).

Associate Editor: Adalberto Pessoa Jr

Conflicts of interest

The authors declare no conflicts of interest.

Criteria for determining the scores	Pointing
	2	1	0
(A) Production	Specific for collagenase, with controlled variables	Specific for collagenase, with uncontrolled variables	No specific for collagenase
(B) Characterization	Complete	Partial	Absent
(C) Microorganism		Non-pathogenic	Pathogenic
(D) Collagenolytic activity method	Azocoll or OrangeCollagen	Others	Absent
(E) Purification	Complete	Partial	Absent
(F) Substrate		Collagenase (specific)	Non-Specific

Authors	(A)	(B)	(C)	(D)	(E)	(F)	Total
Hurion et al. (1977)⁴¹41 Hurion N, Fromentin H, Keil B. Proteolytic enzymes of Entomophthora coronata. Characterization of a collagenase. Comp Biochem Physiol. 1977;56:259-264.	1	0	0	2	2	0	4
Hurion et al. (1979)⁴²42 Hurion N, Fromentin H, Keil B. Specificity of the collagenolytic enzyme from the fungus Entomophthora coronata: comparison with the bacterial collagenase from Achromobacter iophagus. Arch Biochem Biophys. 1979;192(2):438-445.	1	0	0	2	2	0	4
Olutiola and Nwaogwugwu (1982)⁴³43 Olutiola PO, Nwaogwugwu RI. Growth, sporulation and production of maltase and proteolytic enzymes in Aspergillus aculeatus. Trans Br Mycol Soc. 1982;78(1):105-113.	0	2	1	0	0	0	4
Dean and Domnas (1983)⁴⁴44 Dean DD, Domnas AJ. The extracellular proteolytic enzymes of the mosquito-parasitizing fungus Lagenidium giganteum. Exp Mycol. 1983;7(1):31-39.	0	2	1	1	1	0	6
Zhu et al. (1990)⁴⁵45 Zhu WS, Wojdyla K, Donlon K, Thomas PA, Eberle HI. Extracellular proteases of Aspergillus flavus. Fungal keratitis, proteases, and pathogenesis. Diagn Microbiol Infect Dis. 1990;13:491-497.	0	0	0	0	0	0	0
Tomee et al. (1994)⁴⁶46 Tomee JF, Kauffman HF, Klimp AH, de Monchy JG, Köeter GH, Dubois a E. Immunologic significance of a collagen-derived culture filtrate containing proteolytic activity in Aspergillus-related diseases. J Allergy Clin Immunol. 1994;93(4):768-778.	1	0	0	0	0	0	3
Ibrahim-Granet et al. (1996)⁴⁷47 Ibrahim-Granet O, Hernandez FH, Chevrier G, Dupont B. Expression of PZ-peptidases by cultures of several pathogenic fungi. Purification and characterization of a collagenase from Trichophyton schoenleinii. J Med Vet Mycol. 1996;34(2):83-90.	0	1	0	2	2	0	4
Ok and Hashinaga (1996)⁴⁸48 Ok T, Hashinaga F. Detection and production of extracellular collagenolytic enzyme from Zygosaccharomyces rouxii. J Gen Appl Microbiol. 1996;42:517-523.	2	1	1	1	1	1	7
Benito et al. (2002)⁴⁹49 Benito MJ, Rodríguez M, Núñez F, Miguel a, Bermúdez ME, Córdoba JJ. Purification and characterization of an extracellular protease from Penicillium chrysogenum Pg222 active against meat proteins purification and characterization of an extracellular protease from Penicillium chrysogenum Pg222 active against meat proteins. 2002;68(7):5–10.	0	2	1	2	2	0	7
Minglian et al. (2004)⁵⁰50 Minglian Z, Minghe M, Keqin Z. Characterization of a neutral serine protease and its full-length cDNA from the nematode-trapping fungus Arthrobotrys oligospora. Mycologia. 2004;96(1):16-22.	1	2	1	2	2	0	8
Yang et al. (2005)⁵¹51 Yang J, Huang X, Tian B, Wang M, Niu Q, Zhang K. Isolation and characterization of a serine protease from the nematophagous fungus. Lecanicillium psalliotae, displaying nematicidal activity. Biotechnol Lett. 2005;27(15):1123-1128.	1	2	1	1	1	0	6
Wang et al. (2006)⁵²52 Wang M, Yang J, Zhang K-Q. Characterization of an extracellular protease and its cDNA from the nematode-trapping fungus Monacrosporium microscaphoides. Can J Microbiol. 2006;52(2):130-139.	1	2	1	2	2	0	7
Mahmoud et al. (2007)⁵³53 Mahmoud Y-G, Abu El-Souod SM, El-Shourbagy SM, El-Badry ASM. Characterisation and inhibition effect of cetrimide on collagenase produced byAspergillus flavus, isolated from mycotic ulcers. Ann Microbiol. 2007;57(1):109-113.	2	1	0	2	2	0	6
Viani et al. (2007)⁵⁴54 Viani FC, Cazares Viani PR, Gutierrez Rivera IN, da Silva ÉG, Paula CR, Gambale W. Actividad proteolítica extracelular y análisis molecular de cepas de Microsporum canis aisladas de gatos con y sin sintomatología. Rev Iberoam Micol. 2007;24(1):19-23.	1	0	1	0	0	0	3
Hamdy (2008)⁵⁵55 Hamdy HS. Extracellular collagenase from Rhizoctonia solani: production, purification and characterization. Indian J Biotechnol. 2008;7(July):333-340.	2	2	1	2	2	0	8
Lopes et al. (2008)⁵⁶56 Lopes BGB, Santos LSD, Bezerra CDCF, et al. A 25-kDa serine peptidase with keratinolytic activity secreted by Coccidioides immitis. Mycopathologia. 2008;166(1):35-40.	0	1	0	0	0	0	1
Voltan et al. (2008)⁵⁷57 Voltan AR, Donofrio F, Miranda ET, Moraes RA, Mendes-Giannini MJS. Induction and secretion of elastinolytic and proteolytic activity in cultures of Paracoccidioides brasiliensis. Rev Ciências Farm Básica e Apl. 2008;29(1):97-106.	1	0	0	1	1	0	4
Lima et al. (2011a)²⁴24 Lima CA, Filho JLL, Neto BB, Converti A, Carneiro da Cunha MG, Porto ALF. Production and characterization of a collagenolytic serine proteinase by Penicillium aurantiogriseum URM 4622: a factorial study. Biotechnol Bioprocess Eng. 2011;16(3):549-560.	2	2	1	1	1	1	9
Lima et al. (2011b)⁵⁸58 Lima CA, Viana Marques DA, Neto BB, Lima Filho JL, Carneiro-da-Cunha MG, Porto ALF. Fermentation medium for collagenase production by Penicillium aurantiogriseum URM4622. Biotechnol Prog. 2011;27(5):1470-1477.	2	0	1	0	0	0	5
de Siqueira et al. (2014)⁵⁹59 de Siqueira ACR, da Rosa NG, Motta CMS, Cabral H. Peptidase with keratinolytic activity secreted by Aspergillus terreus during solid-state fermentation. Braz Arch Biol Technol. 2014;57(4):514-522.	0	2	1	1	1	0	6
Sharkova et al. (2015)²⁶26 Sharkova TS, Kurakov AV, Osmolovskiy AA, et al. Screening of producers of proteinases with fibrinolytic and collagenolytic activities among micromycetes. Microbiology. 2015;84(3):359-364.	0	0	1	0	0	0	3

Purif.	Enzyme nature	Enzyme sequence	Substrate	Specific activity	Inhibitors	pH and temper.	Isoelectric point
Chromatography	Gelatinolytic	X	BAE (trypsin-like), Elastin, Synthetic Peptides	0.088 nkat/mg	X	X	X
Ultrafiltration, Sephadex G-25 column	Gelatinolytic	X	Casein, Elastin, Synthetic Peptides	X	EDTA, DFP, TLCK, TPCK	X	X
Ammonium sulfate	Collagenolytic	X	Casein, Elastin, Collagen, Gelatin, p-nitrophenol caprylate	3.6 U/mg	Ca²⁺, Na⁺, EDTA, 2,4-DNP	pH 7, 35º	X
X	Collagenolytic	X	BAPA, TAME	X	PMSF, TPCK, IAA2-mercaptoethanol, cysteine HCl, Zn, Ca, Mg, EDTA, Ca, Mg	pH 8.4, 60º	X
(NH₄)₂SO₄ Ammonium Sulfate, Sephadex G25, Biogel A	Collagenolytic	X	Azocasein, Type I Collagen, Elastin	X	EDTA, fenantrolin, PA, PMSF, elastina, NEM	X	X
Cation exchange chromatography	Collagenolytic	X	Casein, Elastin, Orange Collagen	0.39 U/mg	X	X	X
GF, Orange 3, Yellow 1, HA, TSK	Collagenolytic	VFLGREPKPDAFY	Synthetic Peptides, Collagen	X	Fenantrolina, EDTA,	X	X
X	Collagenolytic	X	Synthetic Collagen, Peptides	70.4 U/mg	X	pH 8.2	X
Ammonium sulfate and cation exchange chromatography	X	AEQTDSTWGL	Casein, BSA, Skimmed milk, Gelatin, Collagen, Denatured Collagen, Nematode cuticle	0.37 U/mg	PMSF, EDTA, Pepstatin A, Leupeptin, Aprotinins	pH 10, 55º	X
Ammonium sulfate, Q Sepharose FF, Sephacryl S-100	Gellatonolytic	X	Casein, Gelatin, Nematode cuticle, Azocoll	1.12 U/mg	PMSF e SSI	pH 6-8, 45º	4.9
Ultrafiltration, HITrap SP FF, HiPrep phenyl FF	Gellatonolytic	AITQQQGAPW	Casein, BSA, Gelatin, Collagen, Nematode cuticle	48 U/mg	Leupeptin, Aprotinin, EDTA, Pepstatin A, PMSF	pH 10, 70º	X
Source 15Q, Phenyl Superose	Gellatonolytic	AEQLDSTWGL	Casein, BSA, Skimmed milk, Gelatin, Hydrolyzed Collagen	X	PMSF	pH 9, 60º	6.8
Ammonium Sulfate, Sephadex G-25 e DEAE-cellulose	Collagenolytic	X	X	92.17 U/mg	Cetrimide	X	X
X	Gelatinolytic	X	Keratin, Elastase, Synthetic Peptide	X	X	X	X
Ammonium sulfate, DEAE-cellulose, Sephadex G150	Collagenolytic	X	Collagen, Casein, elastin	18,064.7x10³ U/mg	EDTA, Iodoacetate, Sodium arsenate, arsenito, Cysteine	pH 5, 40º	X
X	X	X	Casein, Gelatin, Keratin, Albumin, Hemoglobin	X	PMSF	X	X
X	Collagenolytic	X	Casein, Elastase. Azocoll	X	PMSF, EDTA, Phenanthroline	X	X
X	Collagenolytic	X	Azocoll, Type I collagen, Gelatin, Azocasein	319 U/mg	PMSF, iodoacetic acid, EDTA e Pepstatin A	pH 9, 37º	X
X	Collagenolytic	X	X	X	X	X	X
X	Collagenolytic	X	Casein, Keratin	X	PMSF, EDTA, IAA	pH 6.5, 55º	X
X	Collagenolytic	X	Plasmin, Plasminogen, Azocoll	X	X	X	X
Purif.	Molecular weight (kDa)	Col. activ.	Col. activ. method.	Culture conditions	Culture medium	Microorg.	Authors
Chromatography	23-40	X	Synthetic peptide	pH 5.6, 30º C, without agitation, 15 days	Casamino acids, Dextrose, CaCl2, YE and Berthelot solution	E. coronata	Hurion et al. (1977)⁴¹41 Hurion N, Fromentin H, Keil B. Proteolytic enzymes of Entomophthora coronata. Characterization of a collagenase. Comp Biochem Physiol. 1977;56:259-264.
Ultrafiltration, Sephadex G-25 column	X	X	Synthetic peptide	pH 5.6, 30º C, without, 15 days	Casamino acids, Dextrose, CaCl2, YE and Berthelot solution	E. coronata	Hurion et al. (1979)⁴²42 Hurion N, Fromentin H, Keil B. Specificity of the collagenolytic enzyme from the fungus Entomophthora coronata: comparison with the bacterial collagenase from Achromobacter iophagus. Arch Biochem Biophys. 1979;192(2):438-445.
Ammonium sulfate	X	X	Achilles tendon bovine	7 days, 30 ºC	Glucose, salts, l-cysteine, tryptone, biotin, thiamine	A. aculeatus	Olutiola and Nwaogwugwu (1982)⁴³43 Olutiola PO, Nwaogwugwu RI. Growth, sporulation and production of maltase and proteolytic enzymes in Aspergillus aculeatus. Trans Br Mycol Soc. 1982;78(1):105-113.
X	X	8 U/mL	Azocoll	Gyrotory shaker (20-24 ºC), sob luzes fluorescents	Peptone, yeast extract and glucose (PYG) broth	L. giganteum	Dean and Domnas (1983)⁴⁴44 Dean DD, Domnas AJ. The extracellular proteolytic enzymes of the mosquito-parasitizing fungus Lagenidium giganteum. Exp Mycol. 1983;7(1):31-39.
(NH₄)₂SO₄ Ammonium Sulfate, Sephadex G25, Biogel A	X	X	SDS-PAGE	2 weeks, T.A.	M9 (without NH₄Cl) + collagen	A. flavus	Zhu et al. (1990)⁴⁵45 Zhu WS, Wojdyla K, Donlon K, Thomas PA, Eberle HI. Extracellular proteases of Aspergillus flavus. Fungal keratitis, proteases, and pathogenesis. Diagn Microbiol Infect Dis. 1990;13:491-497.
Cation exchange chromatography	32	X	Orange collagen e Synthetic Peptide	5 days, 37 ºC, 150 rpm	Yeast carbon base + collagen type I	Aspergillus	Tomee et al. (1994)⁴⁶46 Tomee JF, Kauffman HF, Klimp AH, de Monchy JG, Köeter GH, Dubois a E. Immunologic significance of a collagen-derived culture filtrate containing proteolytic activity in Aspergillus-related diseases. J Allergy Clin Immunol. 1994;93(4):768-778.
GF, Orange 3, Yellow 1, HA, TSK	82	X	Rat native type I collagen	25 ºC, pH 6, 7 days	Sabouraud	T. schoenleinii	Ibrahim-Granet et al. (1996)⁴⁷47 Ibrahim-Granet O, Hernandez FH, Chevrier G, Dupont B. Expression of PZ-peptidases by cultures of several pathogenic fungi. Purification and characterization of a collagenase from Trichophyton schoenleinii. J Med Vet Mycol. 1996;34(2):83-90.
X	X	70.4 U/mL	Ninhydrin	pH 7, 25 ºC, 50 h, with agitation	YPG	Z. rouxii	Ok and Hashinaga (1996)⁴⁸48 Ok T, Hashinaga F. Detection and production of extracellular collagenolytic enzyme from Zygosaccharomyces rouxii. J Gen Appl Microbiol. 1996;42:517-523.
Ammonium sulfate and cation exchange chromatography	35	1% and 2%	Azocoll	26 ºC, 200 rpm, 7 days	LMZ	P. chrysogenum	Benito et al. (2002)⁴⁹49 Benito MJ, Rodríguez M, Núñez F, Miguel a, Bermúdez ME, Córdoba JJ. Purification and characterization of an extracellular protease from Penicillium chrysogenum Pg222 active against meat proteins purification and characterization of an extracellular protease from Penicillium chrysogenum Pg222 active against meat proteins. 2002;68(7):5–10.
Ammonium sulfate, Q Sepharose FF, Sephacryl S-100	38	0.0134 U/mL/m	Azocoll	25-18 ºC, 6 days,150-200 rpm pH 6.5	LMZ - with gelatin	A. oligospora	Minglian et al. (2004)⁵⁰50 Minglian Z, Minghe M, Keqin Z. Characterization of a neutral serine protease and its full-length cDNA from the nematode-trapping fungus Arthrobotrys oligospora. Mycologia. 2004;96(1):16-22.
Ultrafiltration, HITrap SP FF, HiPrep phenyl FF	32	14%	Non described	26 ºC, 100 rpm, 6 days	Glucose, gelatin and salts	L. psalliotae	Yang et al. (2005)⁵¹51 Yang J, Huang X, Tian B, Wang M, Niu Q, Zhang K. Isolation and characterization of a serine protease from the nematophagous fungus. Lecanicillium psalliotae, displaying nematicidal activity. Biotechnol Lett. 2005;27(15):1123-1128.
Source 15Q, Phenyl Superose	39 kDa	Collagen 15.9%, Denatured Collagen 48.1%,	Folin	6 days, 26 ºC, 200 rpm	Protease inducing - with gelatin	M. microscaphoides	Wang et al. (2006)⁵²52 Wang M, Yang J, Zhang K-Q. Characterization of an extracellular protease and its cDNA from the nematode-trapping fungus Monacrosporium microscaphoides. Can J Microbiol. 2006;52(2):130-139.
Ammonium Sulfate, Sephadex G-25 e DEAE-cellulose	72-92 kDa	82.95 U/mL	Ninhydrin	6 days, 37 ºC	Gelatin, glucose, yeast extract, and native bovine collagen	A. flavus	Mahmoud et al. (2007)⁵³53 Mahmoud Y-G, Abu El-Souod SM, El-Shourbagy SM, El-Badry ASM. Characterisation and inhibition effect of cetrimide on collagenase produced byAspergillus flavus, isolated from mycotic ulcers. Ann Microbiol. 2007;57(1):109-113.
X	X	1 Unit of collagenase	Synthetic peptide	14 days	Medium with type I collagen	M. canis	Viani et al. (2007)⁵⁴54 Viani FC, Cazares Viani PR, Gutierrez Rivera IN, da Silva ÉG, Paula CR, Gambale W. Actividad proteolítica extracelular y análisis molecular de cepas de Microsporum canis aisladas de gatos con y sin sintomatología. Rev Iberoam Micol. 2007;24(1):19-23.
Ammonium sulfate, DEAE-cellulose, Sephadex G150	66 kDa	212.33 U/mL	Ninhydrin	108 h, 175 rpm, pH 5.5, 30 ºC	Sabouraud-glucose-collagen	R. solani	Hamdy (2008)⁵⁵55 Hamdy HS. Extracellular collagenase from Rhizoctonia solani: production, purification and characterization. Indian J Biotechnol. 2008;7(July):333-340.
X	25 kDa	X	Zymogram	pH 5.5, 9 days, T.A.	Czapek	C. immitis	Lopes et al. (2008)⁵⁶56 Lopes BGB, Santos LSD, Bezerra CDCF, et al. A 25-kDa serine peptidase with keratinolytic activity secreted by Coccidioides immitis. Mycopathologia. 2008;166(1):35-40.
X	20-200 kDa	1.2 U/mL	Azocoll	150 rpm, 35 ºC, for 7, 14, 21 e 28 days	Yeast carbon base + collagen + vitamin solution; neopeptoneBHI + elastin	P. brasiliensis	Voltan et al. (2008)⁵⁷57 Voltan AR, Donofrio F, Miranda ET, Moraes RA, Mendes-Giannini MJS. Induction and secretion of elastinolytic and proteolytic activity in cultures of Paracoccidioides brasiliensis. Rev Ciências Farm Básica e Apl. 2008;29(1):97-106.
X	X	164 U/mL	Azocoll	0.75% gelatin, 200 rpm, pH 8.0 and 28 ºC	Soybean flour, glucose and mineral solution	P. aurantiogriseum	Lima et al. (2011a)²⁴24 Lima CA, Filho JLL, Neto BB, Converti A, Carneiro da Cunha MG, Porto ALF. Production and characterization of a collagenolytic serine proteinase by Penicillium aurantiogriseum URM 4622: a factorial study. Biotechnol Bioprocess Eng. 2011;16(3):549-560.
X	X	231 U/mL	Azocoll	pH 7.0, 24 ºC, 24 h	Soybean flour, Glucose and mineral solution	P. aurantiogriseum	Lima et al. (2011b)⁵⁸58 Lima CA, Viana Marques DA, Neto BB, Lima Filho JL, Carneiro-da-Cunha MG, Porto ALF. Fermentation medium for collagenase production by Penicillium aurantiogriseum URM4622. Biotechnol Prog. 2011;27(5):1470-1477.
X	X	0.165 OD/mL	Azocoll	2.0 × 10⁵ espores, 72 h, 30 ºC, 75% humidity	Solid medium of wheat bran	A. terreus	de Siqueira et al. (2014)⁵⁹59 de Siqueira ACR, da Rosa NG, Motta CMS, Cabral H. Peptidase with keratinolytic activity secreted by Aspergillus terreus during solid-state fermentation. Braz Arch Biol Technol. 2014;57(4):514-522.
X	X	113.2 and 332 × 10^-3 U/mL	Azocoll	200 rpm, 28 ºC, 4 days	Several	Micromycetes	Sharkova et al. (2015)²⁶26 Sharkova TS, Kurakov AV, Osmolovskiy AA, et al. Screening of producers of proteinases with fibrinolytic and collagenolytic activities among micromycetes. Microbiology. 2015;84(3):359-364.

[1] *Corresponding author at: Department of Morphology and Animal Physiology, Federal Rural University of Pernambuco, Av. Dom Manoel de Medeiros, s/n, 52171-900 Recife, PE, Brazil. E-mail: analuporto@yahoo.com.br (A.L. Porto).

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Collagenolytic enzymes produced by fungi: a systematic review

Abstract