Cultivation conditions and biochemical characterization of the proteolytic enzymes with fibrinolytic action obtained from mushrooms in the last ten years

Authors

DOI:

https://doi.org/10.33448/rsd-v11i14.36652

Keywords:

Fibrinolytic Proteases; Mushroom; Thrombolytic Therapy; Fibrin.

Abstract

Fibrinolytic enzymes are proteases that are capable of degrading the fibrin mesh present in blood clots and can be obtained through fungal extracts. Thus, the objective of this paper was to seek out and compare all the information regarding the production and biochemical characterization of fibrinolytic enzymes of mushroom species published in papers in the last ten years. The research was carried out in eight national and international electronic databases using the terms: “fungal enzymes”, “fibrinolytic Proteases”, “thrombosis” and “mushrooms”. The results obtained were analyzed according to each step. In the first stage, the titles and abstracts of all papers were analyzed independently; in the second stage, all papers were read and those that did not meet the inclusion criteria were excluded. Then, the remaining papers were reviewed and the data were tabulated and compared. As a result, it was found that enzymes with fibrinolytic action were obtained from eight species of mushrooms in the period of this research: P. sajor-cashew, P. ferulae, P. ostreatus, L. shimeji, A. polytricha, H. erinaceum, C. comatus and C. militaris. The enzymes were identified as protease SPPs, metalloproteases, serine proteases and serine metalloproteases. The methods used to evaluate fibrinolytic activity were the fibrin plate method and/or the formation of artificial thrombus through thrombin and fibrinogen. The molecular mass of these enzymes ranged from ~18 to 66 kDa and, for the biochemical characterization of the extracts, the pH ranged from 4.0 to 9.5 and the optimum temperature from 25 to 70 ºC. Via the review, it was observed that few articles were published on the subject in question, which made it necessary to carry out more studies to discover the biotechnological properties of mushrooms and define their applications in the most diverse sectors of industries, not only in commercial species of mushrooms, but also in native species.

References

Acosta, G. A., Fonseca, M. I., Fariña, J. I., & Zapata, P. D. (2022). Exploring Agaricomycetes from the Paranaense rainforest (Misiones, Argentina) as an unconventional source of fibrinolytic enzymes. Mycologia. 114(2):242-253.10.1080/00275514.2022.2035148

Aguilar, J. G., & Sato, H. H. (2018). Microbial proteases: Production and application in obtaining protein hydrolysates. Food Research International, 103, 253-262.

Ali, A. M. M., et al. (2022). Production of fibrinolytic enzymes during food production. In: Current Developments in Biotechnology and Bioengineering, p. 157-187. https://doi.org/10.1016/B978-0-12-823506-5.00018-7

Ali, A. M., & Bavisetty, S. C. B. (2020). Purification, physicochemical properties, and statistical optimization of fibrinolytic enzymes especially from fermented foods: a comprehensive review. International Journal of Biological Macromolecules, v. 163, p. 1498-1517.

Ali, S. M., Ling, T. C., Sekaran, M., Y. S. T., Jegadeesh, R., & Vikineswary, S. (2014). Recovery and partial purification of fibrinolytic enzymes of Auricularia polytricha (Mont.) Sacc by an aqueous two-phase system. Separation and Purification Technology, 122 359–366. http://dx.doi.org/10.1016/j.seppur.2013.11.016

Altaf, F., Wu, S., & Kasim, V. (2021). Role of Fibrinolytic Enzymes in Anti-Thrombosis Therapy. Front Mol Biosci, 8:680397. 10.3389/fmolb.2021.680397.

Ângelo, R. S. (2010). Enzimas hidrolíticas. In: Esposito, E., Azevedo, J. L. (Org.). Fungos: uma introdução à biologia, bioquímica e biotecnologia. Caxias do Sul: Educs, (2ª edição).

Anna, D., Protopopova, R. I., Litvinov, D. K., Galanakis, C., Nagaswami, N. A., Barinov, A. R., Mukhitov, Dmitry, V. K., & John. W. W. (2017). Morphometric characterization of fibrinogen’s αC regions and their role in fibrin self-assembly and molecular organization. Nanoscale. 10.1039/c7nr04413e

Astrup, T., & Mullertz, S. (1952). The fibrin platemethod for estimating of fibrinolyticactivity. Arch Biochem Biophys; 40: 346–51p. http://dx.doi.org/10.1016/0003-9861(52)90121-5

Bajaj, B. K., Singh, S., Khullar, M., Singh, K., & Bhardwaj, S. (2014). Optimization of fibrinolytic protease production from Bacillus subtilis I-2 using agro-residues. Braz Arch Biol Technol 57:653–662. https://doi.org/10.1590/S1516-8913201402132

Banerjee, G., & Ray, A. K. (2017). Impact of microbial proteases on biotechnological industries. Biotechnology and Genetic Engineering Reviews, 33(2), 119-143.

Barbosa, E. E. P., Pimenta, L., Brito, A. K. P., Martim, S. R., & Teixeira, M. F. S. (2020). Cultivo de cogumelo comestível em resíduos lignocelulósicos de floresta tropical para produção de proteases / Mushroom cultivation edible in lignocellulosic residues from rainforest for protease production. Brazilian Journal of Development, 6(11), 92475–92485. https://doi.org/10.34117/bjdv6n11-598

Benmrad, O., M., Mechri, S., Zaraî, J. N., et al. (2019). Purification and biochemical characterization of a novel thermostable protease from the oyster mushroom Pleurotus sajor-caju strain CTM10057 with industrial interest. BMC Biotechnol 19, 43. https://doi.org/10.1186/s12896-019-0536-4

Bezerra, V. H. S., Cardoso, S. L., Fonseca-Bazzo, Y., Silveira, D., Magalhães, P. O., & Souza, P. M. (2021). Protease Produced by Endophytic Fungi: A Systematic Review. Molecules, 26 (22):7062. Published 2021 Nov 22.10.3390/molecules26227062

Brito, A. K. P., Pimenta, L., Barbosa, E. E. P., Batista, S. C. P., Coelho, M. P. S. L. V., Castillo, T. A., Martim, S. R., & Teixeira, M. F. S. (2021). Evaluation of tropical forest substrates for cultivation and production of proteases by Pleurotus djamor. Research, Society and Development, 10(3), e31810313385. https://doi.org/10.33448/rsd-v10i3.13385

Buba, J. C. (2018). Produção de protease com atividade fibrinolítica por cultivo submerso de Mucor subtilissimus em biorreator. Universidade de São Paulo. http://www.teses.usp.br/teses/disponiveis/3/3137/tde28022018-133041/pt-br.php

Cardoso, K. B. B., Nascimento, M. C., Batista, A. C., Oliveira, V. M., Nascimento, T. P., Batista, J. M. S., Costa, R. M. P. B., Pastrana, L., & Porto, A. L. F. (2022). Systematic analysis on the obtaining of fibrinolytic fungi enzymes. Research, Society and Development, 11(2), e13611225449, 2022. 10.33448/rsd-v11i2.25449.

Cho, I. H., Choi, E. S., Lim, H. G., & Lee, H. H. (2004). Purification and characterization of six fibrinolytic serine-proteases from earthworm Lumbricus rubellus. J Biochem Mol Biol, 37 (2):199-205.10.5483/bmbrep.2004.37.2.199.

Choi, B. S., Sapkota, K., Choi, J. H., Shin, C. H., Kim, S., & Kim, S. J. (2013). Herinase: a novel bi-functional fibrinolytic protease from the monkey head mushroom, Hericium erinaceum. Appl Biochem Biotechnol, Jun; 170 (3):609-22. 10.1007/s12010-013-0206-2. Epub 2013 Apr 7. PMID: 23564433.

Choi, J. H., Kim, D. W., Kim, S., & Kim, S. J. (2016). Purification and partial characterization of a fibrinolytic enzyme from the fruiting body of the medicinal and edible mushroom Pleurotus ferulae. Prep Biochem Biotechnol, Jul 3;47(6):539-546. 10.1080/10826068.2016.1181083.

Coelho, M., Figueiredo, A. S. F., Martim, S. R. M., & Teixeira, M. F. S. T. (2022). Ciclo de produção de cogumelos comestíveis cultivados em resíduos lignocelulósicos da fruticultura Amazônica: um estudo de caso. Concilium, 284–294. https://doi.org/10.53660/CLM-116-138

Das, G., & Prasad, M. P. (2010). Isolation, purification & mass production of protease enzyme from Bacillus subtilis. International Research Journals of Microbiology, 1(2), 026-031, April.

Erez, E., Fass, D., & Bibi, E. (2009). How intramembrane proteases bury hydrolytic reactions in the membrane. Nature, 459 (7245):371-378.10.1038/nature08146

Fasim, A., More, V. S., & More, Sunil, S. (2021). Large-scale production of enzymes for biotechnology uses. Current Opinion in Biotechnology, v. 69, p. 68-76. https://doi.org/10.1016/j.copbio.2020.12.002.

Feijoo-Siota, L., and& Villa, T. G. (2011). Native and Biotechnologically Engineered Plant Proteases with Industrial Applications. Food Bioprocess Technol, 4:1066–1088., 4(6), 1066-1088, 2011. 10.1007/s11947-010-0431-4

Ferreira, C. N., Sousa, M. O., Dusse, L. M. S., & Carvalho, M. G. (2010). O novo modelo da cascata de coagulação baseado nas superfícies celulares e suas implicações. Rev Bras Hematol Hemoter, 32(5), 416-421. https://doi.org/10.1590/S1516-84842010000500016

Flute, P. T. (1964). Haemorrhage and fibrinolysis. Proceedings of the Royal Society of Medicine, 57(7), 603–606.

Fonseca, T. R. B. (2013). Pleurotus ostreatoroseus DPUA 1720: Avaliação do Crescimento, Produção de Basidioma e Determinação da Atividade Proteolítica em Resíduos Agroindustriais. Universidade Federal do Amazonas.

Galo, L. A., & Colombo, M. F. (2009). Espectrofotometria de longo caminho óptico em espectrofotômetro de duplo-feixe convencional: uma alternativa simples para investigações de amostras com densidade óptica muito baixa. Química Nova, 32 (2), 488-492. https://doi.org/10.1590/S0100-40422009000200036

Katrolia, P., Liu, X., Zhao, Y., Kopparapu, N. K., & Zheng, X. (2020). Gene cloning, expression and homology modeling of first fibrinolytic enzyme from mushroom (Cordyceps militaris). Int J Biol Macromol, 146:897-906. 10.1016/j.ijbiomac.2019.09.212

Kollman, J. M., Pandi, L., Sawaya, M. R., Riley, M., & Doolittle, R. F. (2009). Crystal structure of human fibrinogen. Biochemistry, 48(18):3877-3886.10.1021/bi802205g

Li, G., Liu, X., Cong, S., Deng, Y., & Zheng, X. (2021). A novel serine protease with anticoagulant and fibrinolytic activities from the fruiting bodies of mushroom Agrocybe aegerita. Int J Biol Macromol, 168:631-639. 10.1016/j.ijbiomac.2020.11.118

Liu, X. L., Zheng, X. Q., Qian, P. Z., Kopparapu, N. K., Deng, Y. P., Nonaka, M., & Harada, N. (2014). Purification and characterization of a novel fibrinolytic enzyme from culture supernatant of Pleurotus ostreatus. J Microbiol Biotechnol, Feb 28;24(2):245-53. 10.4014/jmb.1307.07063.

Liu, X. L., Zheng, X. Q., & Zhang, J. K. (2012). Production of a Fibrinolytic Enzyme from Coprinus comatus YY-20. Applied Mechanics and Materials, Vols. 138–139, pp. 1195–1201. https://doi.org/10.4028/www.scientific.net/amm.138-139.1195

Machado, A. R. G., Teixeira, M. F. S., Kirsch, L. S. M., Campelo, C. L., & Oliveira, I. M. A. (2016). Nutritional value and proteases of Lentinus citrinus produced by solid state fermentation of lignocellulosic waste from tropical region. Saudi Journal of Biological Sciences, 23(5): 621-627. DOI: https://doi.org/10.1016/j.sjbs.2015.07.002

Mander, P., Cho, S. S., Simkhada, J. R., Choi, Y. H., & Yoo, J. C. (2011). A low molecular weight chymotrypsin-like novel fibrinolytic enzyme from Streptomyces sp. CS624. Process Biochemistry, v. 46, p. 1449–1455. https://doi.org/10.1016/j.procbio.2011.03.016

Mine, Y., Wong, A. H. K., & Jinag, B. (2005). Fibrinolytic enzymes in Asian traditional fermented foods. Food Research International, 38:243–250. https://doi.org/10.1016/j.foodres.2004.04.008

Moon, S. M., Kim, J. S., Kim, H. J., Choi, M. S., Park, B. R., Kim, S. G., Ahn, H., Chun, H. S., Shin, Y. K., Kim, J. J., Kim, D. K., Lee, S. Y., Seo, Y. W., Kim, Y. H., & Kim, C. S. (2014). Purification and characterization of a novel fibrinolytic α chymotrypsin like serine metalloprotease from the edible mushroom, Lyophyllum shimeji. J Biosci Bioeng, May;117(5):544-50. 10.1016/j.jbiosc.2013.10.019.

Naeem, M., Manzoor, S., Abid, M. U. H., Tareen, M. B. K., Asad, M., Mushtaq, S., Ehsan, N., Amna, D., Xu, B., & Hazafa, A. (2022). Fungal Proteases as Emerging Biocatalysts to Meet the Current Challenges and Recent Developments in Biomedical Therapies: An Updated Review. J. Fungi, 8, 109. https://doi.org/10.3390/jof8020109

Pechik, I., Yakovlev, S., Mosesson, M. W., Gilliland, G. L., & Medved, L. (2006). Structural basis for sequential cleavage of fibrinopeptides upon fibrin assembly. Biochemistry, Mar 21;45 (11):3588-97. 10.1021/bi0525369. PMID: 16533041; PMCID: PMC2531209.

Pimenta, L., Barbosa, E. E. P., Brito, A. K. P. de, Martim, S. R., & Teixeira, M. F. S. (2021). Processo eco-amigável para selecionar substrato Lignocelulósico para produção de peptidases ácidas / Eco-friendly process to select Lignocellulosic substrate for the production of acid peptidases. Brazilian Journal of Development, 7(1), 3469–3479. https://doi.org/10.34117/bjdv7n1-234

Ruiz, M. A., Greco, O. T., Braile, D. M. (2009). Fator de impacto: importância e influência no meio editorial, acadêmico e científico. Rev Bras Cir Cardiovasc. 24(3): 273-278. https://doi.org/10.1590/S0102-76382009000400004

Shafee, T. (2014). Evolvability of a Viral Protease: Experimental Evolution of Catalysis, Robustness and Specificity. University of Cambridge: Cambridge, UK.

Sharma, C., Osmolovskiy, A., & Singh, R. (2021). Microbial Fibrinolytic Enzymes as Anti-Thrombotics: Production, Characterisation and Prodigious Biopharmaceutical Applications. Pharmaceutics. 2021;13 (11):1880. Published Nov 5.10.3390/pharmaceutics13111880

Sharma, M., & Bajaj, B. K. (2017). Optimization of bioprocess variables for production of a thermostable and wide range pH stable carboxymethyl cellulase from Bacillus subtilis MS 54 under solid state fermentation. Environ Prog Sustain Energy. doi:10.1002/ep.12557

Souza, H. Q., et al. (2008). Seleção de Basidiomycetes da Amazônia para produção de enzimas de interesse biotecnológico. Ciência e Tecnologia de Alimentos, v. 28, pg. 116-124, Campinas, SP.

Strehl, L. (2005). O fator de impacto do ISI e a avaliação da produção científica: aspectos conceituais e metodológicos. Ci. Inf., Brasília, 34(1), 19-27. https://wp.scielo.org/wp-content/uploads/STREHL-L..pdf

Wang, J., Wu, C., Chen, Y., Chen, C., Hu, S., & Chang, S. (2014). Antihyperglycemic activity of exopolysaccharide produced by mushroom Pleurotus ferulae with submerged liquid culture on streptozotocin-induced diabetic rats. Journal of Food and Nutrition Research, 2(7), 419-424.

Weisel, J. W., & Litvinov, R. I. (2017). Fibrin Formation, Structure and Properties. Subcell Biochem, 82: 405–456. 10.1007/978-3-319-49674-0_13

Wu, S., et al. (2021). Biocatalysis: enzymatic synthesis for industrial applications. Angew. Chem. Int. Ed., 60,88–119. https://doi.org/10.1002/anie.202006648

Downloads

Published

05/11/2022

How to Cite

SANTANA, R. da S.; FARIAS, V. G. de; SEVALHO, E. de S. .; CANDIDO, K.; CARPIO, K. C. R. .; GOMES, W. R. .; CARVALHO, R. P. . Cultivation conditions and biochemical characterization of the proteolytic enzymes with fibrinolytic action obtained from mushrooms in the last ten years . Research, Society and Development, [S. l.], v. 11, n. 14, p. e530111436652, 2022. DOI: 10.33448/rsd-v11i14.36652. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/36652. Acesso em: 14 nov. 2024.

Issue

Section

Review Article