Research Article
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Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa

Year 2021, Volume: 25 Issue: 2, 601 - 609, 15.04.2021
https://doi.org/10.16984/saufenbilder.853961

Abstract

Azurin which has attracted much attention as potential anticancer agent in recent years is a bacterial secondary metabolite. This copper-containing redox protein secreted by Pseudomonas aeruginosa has capability of preferentially entering into many human cancer cells and inducing apoptosis. In this study, whey which is the considerable by-product of the casein or cheese manufacture was used as azurin production medium by P. aeruginosa. Also, effects of copper (II) sulphate (CuSO4) and potassium nitrate (KNO3) on the azurin production were determined. At the end of the studies, optimum azurin expression level was reached during the incubation of 18 hours. The best CuSO4 concentration was 2.5 mg/L while the best KNO3 concentration was 45 mg/L according to Western blot analysis. This process can be used to obtain high levels of azurin using P. aeruginosa in whey medium. Also, using whey for azurin production can reduce many processing industrial whey waste management problems.

Thanks

The author would like to acknowledge East Anatolia High Technology Application and Research Center (DAYTAM, Erzurum, Turkey) and Prof. Dr. Bülent Çetin for providing P. aeruginosa ATCC9027.

References

  • A.R. Awan, W.M. Shaw, T. Ellis, ''Biosynthesis of therapeutic natural products using synthetic biology'', Advanced Drug Delivery Reviews, vol. 105, Part A, pp. 96–106, 2016.
  • S.B. Singh, Confronting the challenges of discovery of novel antibacterial agents, Bioorganic & Medicinal Chemistry Letters, vol. 24, no. 6, pp. 3683¬-3689, 2014.
  • D.J. Newman, G.M. Cragg, Natural products as sources of new drugs over the last 25 years, Journal of Natural Products, vol. 70, pp. 461¬-477, 2007.
  • B. Ruiz, A. Chávez, A. Forero, Y. García-Huante, A. Romero, M. Snchez, D. Rocha, B. Snchez, R. Rodríguez-Sanoja, S. Sánchez, E. Langley, Production of microbial secondary metabolites: Regulation by the carbon source, Critical Reviews in Microbiology, vol. 36, no. 2, pp. 146-167, 2010.
  • G.M. Cragg, D.J. Newman, Natural products: A continuing source of novel drug leads, Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1830, no. 6, pp. 3670-3695, 2013.
  • F. Huang, Q. Shu, Z. Qin, J. Tian, Z. Su, Y. Huang, M. Gao, Anticancer Actions of Azurin and Its Derived Peptide p28, The Protein Journal, vol. 39, no.2 pp. 182-189, 2020.
  • S. Biswas, P. Kumari, P.M. Lakhani, B. Ghosh, Recent advances in polymeric micelles for anti-cancer drug delivery, European Journal of Pharmaceutical Sciences, vol. 83, pp. 184-202, 2016.
  • N. Bernardes, R. Seruca, a M. Chakrabarty, a M. Fialho, Microbial-based therapy of cancer: current progress and future prospects, Bioengineered Bugs. vol. 1, no. 3, pp. 178-190, 2010.
  • A. Sharma, N. Kumari, E. Menghani, Bioactive Secondary Metabolites: an Overview, International Journal of Scientific & Engineering Research, vol. 5, no. 4, pp. 1395-1407, 2014.
  • T. Chatzisideri, G. Leonidis, V. Sarli, Cancer-targeted delivery systems based on peptides, Future Medicinal Chemistry, vol. 10, no. 18, pp. 2201-2226, 2018.
  • R. Soudy, N. Byeon, Y. Raghuwanshi, S. Ahmed, A. Lavasanifar, K. Kaur, Engineered Peptides for Applications in Cancer-Targeted Drug Delivery and Tumor Detection, Mini-Reviews Medicinal Chemistry, vol. 17, no. 18, pp.1696-1712, 2016.
  • M. Sánchez, F.J. Aranda, M.J. Espuny, A. Marqués, J.A. Teruel, Á. Manresa, A. Ortiz, Aggregation behaviour of a dirhamnolipid biosurfactant secreted by Pseudomonas aeruginosa in aqueous media, Journal of Colloid and Interface Science, vol. 307, no. 1, pp.246-253, 2007.
  • A.M. Chakrabarty, N. Bernardes, A.M. Fialho, Bacterial proteins and peptides in cancer therapy: Today and tomorrow, Bioengineered, vol. 5 pp. 234-242, 2014.
  • A. Fialho, T. Das Gupta, A. Chakrabarty, Designing Promiscuous Drugs? Look at What Nature Made!, Letters in Drug Design & Discovery, vol. 4, no. 1, pp.40-43, 2007.
  • D. Raucher, J.S. Ryu, Cell-penetrating peptides: Strategies for anticancer treatment, Trends in Molecular Medicine, vol. 21, no. 9, pp.560-570, 2015.
  • Y. Zhang, Y. Zhang, L. Xia, X. Zhang, X. Ding, F. Yan, F. Wu, Escherichia coli Nissle 1917 targets and restrains mouse B16 melanoma and 4T1 breast tumors through expression of azurin protein, Applied Environmental Microbiology, vol. 78, no. 271, pp.7603-7610, 2012.
  • P. Ghasemi-Dehkordi, A. Doosti, M.S. Jami, The concurrent effects of azurin and Mammaglobin-A genes in inhibition of breast cancer progression and immune system stimulation in cancerous BALB/c mice, 3 Biotechnology, vol. 9, no. 27, pp.1-15, 2019.
  • P.M.R. Guimarães, J.A. Teixeira, L. Domingues, Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorisation of cheese whey, Biotechnology Advances, vol. 28, no. 3, pp.375-384, 2010.
  • M.I. González Siso, The biotechnological utilization of cheese whey: A review, Bioresource Technology, vol. 57, no. 1, pp.1-11, 1996.
  • A.R. Prazeres, F. Carvalho, J. Rivas, Cheese whey management: A review, Journal of Environmental Management, vol. 110, pp.48-68, 2012.
  • M. Pescuma, G.F. de Valdez, F. Mozzi, Whey-derived valuable products obtained by microbial fermentation, Applied Microbiology and Biotechnology, vol. 99, pp.6183-6196, 2015.
  • M.P. Ryan, G. Walsh, The biotechnological potential of whey, Reviews in Environmental Science and Bio/Technology, vol. 15, no. 3, pp.479-498, 2016.
  • F. V Kosikowski, V. V Mistry, Cheese and Fermented Milk Foods, Cheese Fermented Milk Foods, 1997.
  • G.W. Smithers, Whey and whey proteins-From “gutter-to-gold,” International Dairy Journal, vol. 18, no. 7, pp.695-704, 2008.
  • S. Ramachandran, M. Singh, M. Mandal, Purification of Azurin from Pseudomonas aeuroginosa, in: Chromatogr. - Most Versatile Method, Analytical Chemistry, 2012.
  • M. Bradford, A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Analytical Biochemistry, vol. 72, pp.248-254, 1976.
  • T. Yamada, M. Goto, V. Punj, O. Zaborina, M.L. Chen, K. Kimbara, D. Majumdar, E. Cunningham, T.K. Das Gupta, A.M. Chakrabarty, Bacterial redox protein azurin, tumor suppressor protein p53, and regression of cancer , Proceedings of the National Academy of Science, vol. 99, pp.14098-14103, 2002.
  • V. Punj, S. Bhattacharyya, D. Saint-Dic, C. Vasu, E.A. Cunningham, J. Graves, T. Yamada, Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer, Oncogene, vol. 23, no. 13, pp.2367-2378, 2004.
  • J.H. Choi, M.H. Lee, Y.J. Cho, B.S., Park, S. Kim, G.C. Kim, The bacterial protein Azurin enhances sensitivity of oral squamous carcinoma cells to anticancer drugs, Yonsei Medical Journal, vol. 52, 773-78, 2011.
  • M. Goto, T. Yamada, K. Kimbara, J. Horner, M. Newcomb, T.K. Das Gupta, A.M. Chakrabarty, Induction of apoptosis in macrophages by Pseudomonas aeruginosa azurin: Tumour-suppressor protein p53 and reactive oxygen species, but not redox activity, as critical elements in cytotoxicity, Molecular Microbiology, vol. 47, no. 2, pp.549-559, 2003.
  • I. Pozdnyakova, J. Guidry, P. Wittung-Stafshede, Copper stabilizes azurin by decreasing the unfolding rate, Archieves of Biochemistry and Biophysics, vol. 390, no. 1, pp.146-148, 2001.
  • R. Knowles, Denitrification, Microbiology Reviews, vol. 46, no. 1, pp.43-70, 1982.
  • Y. Han, T. Wang, G. Chen, Q. Pu, Q. Liu, Y. Zhang, L. Xu, M. Wu, H. Liang, A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition, PLoS Pathogens, vol. 15, no. 12, pp.1-25, 2019.
  • E. Vijgenboom, J.E. Busch, G.W. Canters, In vivo studies disprove an obligatory role of azurin in denitrification in Pseudomonas aeruginosa and show that azu expression is under control of RpoS and ANR, Microbiology. vol. 143, no. 9, pp.2853-2863, 1997.
  • I. W. Sutherland, The Production of Azurin and Similar Proteins, Archiv für Mikrobiologie, vol. 54, pp.350-357, 1966.
Year 2021, Volume: 25 Issue: 2, 601 - 609, 15.04.2021
https://doi.org/10.16984/saufenbilder.853961

Abstract

References

  • A.R. Awan, W.M. Shaw, T. Ellis, ''Biosynthesis of therapeutic natural products using synthetic biology'', Advanced Drug Delivery Reviews, vol. 105, Part A, pp. 96–106, 2016.
  • S.B. Singh, Confronting the challenges of discovery of novel antibacterial agents, Bioorganic & Medicinal Chemistry Letters, vol. 24, no. 6, pp. 3683¬-3689, 2014.
  • D.J. Newman, G.M. Cragg, Natural products as sources of new drugs over the last 25 years, Journal of Natural Products, vol. 70, pp. 461¬-477, 2007.
  • B. Ruiz, A. Chávez, A. Forero, Y. García-Huante, A. Romero, M. Snchez, D. Rocha, B. Snchez, R. Rodríguez-Sanoja, S. Sánchez, E. Langley, Production of microbial secondary metabolites: Regulation by the carbon source, Critical Reviews in Microbiology, vol. 36, no. 2, pp. 146-167, 2010.
  • G.M. Cragg, D.J. Newman, Natural products: A continuing source of novel drug leads, Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1830, no. 6, pp. 3670-3695, 2013.
  • F. Huang, Q. Shu, Z. Qin, J. Tian, Z. Su, Y. Huang, M. Gao, Anticancer Actions of Azurin and Its Derived Peptide p28, The Protein Journal, vol. 39, no.2 pp. 182-189, 2020.
  • S. Biswas, P. Kumari, P.M. Lakhani, B. Ghosh, Recent advances in polymeric micelles for anti-cancer drug delivery, European Journal of Pharmaceutical Sciences, vol. 83, pp. 184-202, 2016.
  • N. Bernardes, R. Seruca, a M. Chakrabarty, a M. Fialho, Microbial-based therapy of cancer: current progress and future prospects, Bioengineered Bugs. vol. 1, no. 3, pp. 178-190, 2010.
  • A. Sharma, N. Kumari, E. Menghani, Bioactive Secondary Metabolites: an Overview, International Journal of Scientific & Engineering Research, vol. 5, no. 4, pp. 1395-1407, 2014.
  • T. Chatzisideri, G. Leonidis, V. Sarli, Cancer-targeted delivery systems based on peptides, Future Medicinal Chemistry, vol. 10, no. 18, pp. 2201-2226, 2018.
  • R. Soudy, N. Byeon, Y. Raghuwanshi, S. Ahmed, A. Lavasanifar, K. Kaur, Engineered Peptides for Applications in Cancer-Targeted Drug Delivery and Tumor Detection, Mini-Reviews Medicinal Chemistry, vol. 17, no. 18, pp.1696-1712, 2016.
  • M. Sánchez, F.J. Aranda, M.J. Espuny, A. Marqués, J.A. Teruel, Á. Manresa, A. Ortiz, Aggregation behaviour of a dirhamnolipid biosurfactant secreted by Pseudomonas aeruginosa in aqueous media, Journal of Colloid and Interface Science, vol. 307, no. 1, pp.246-253, 2007.
  • A.M. Chakrabarty, N. Bernardes, A.M. Fialho, Bacterial proteins and peptides in cancer therapy: Today and tomorrow, Bioengineered, vol. 5 pp. 234-242, 2014.
  • A. Fialho, T. Das Gupta, A. Chakrabarty, Designing Promiscuous Drugs? Look at What Nature Made!, Letters in Drug Design & Discovery, vol. 4, no. 1, pp.40-43, 2007.
  • D. Raucher, J.S. Ryu, Cell-penetrating peptides: Strategies for anticancer treatment, Trends in Molecular Medicine, vol. 21, no. 9, pp.560-570, 2015.
  • Y. Zhang, Y. Zhang, L. Xia, X. Zhang, X. Ding, F. Yan, F. Wu, Escherichia coli Nissle 1917 targets and restrains mouse B16 melanoma and 4T1 breast tumors through expression of azurin protein, Applied Environmental Microbiology, vol. 78, no. 271, pp.7603-7610, 2012.
  • P. Ghasemi-Dehkordi, A. Doosti, M.S. Jami, The concurrent effects of azurin and Mammaglobin-A genes in inhibition of breast cancer progression and immune system stimulation in cancerous BALB/c mice, 3 Biotechnology, vol. 9, no. 27, pp.1-15, 2019.
  • P.M.R. Guimarães, J.A. Teixeira, L. Domingues, Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorisation of cheese whey, Biotechnology Advances, vol. 28, no. 3, pp.375-384, 2010.
  • M.I. González Siso, The biotechnological utilization of cheese whey: A review, Bioresource Technology, vol. 57, no. 1, pp.1-11, 1996.
  • A.R. Prazeres, F. Carvalho, J. Rivas, Cheese whey management: A review, Journal of Environmental Management, vol. 110, pp.48-68, 2012.
  • M. Pescuma, G.F. de Valdez, F. Mozzi, Whey-derived valuable products obtained by microbial fermentation, Applied Microbiology and Biotechnology, vol. 99, pp.6183-6196, 2015.
  • M.P. Ryan, G. Walsh, The biotechnological potential of whey, Reviews in Environmental Science and Bio/Technology, vol. 15, no. 3, pp.479-498, 2016.
  • F. V Kosikowski, V. V Mistry, Cheese and Fermented Milk Foods, Cheese Fermented Milk Foods, 1997.
  • G.W. Smithers, Whey and whey proteins-From “gutter-to-gold,” International Dairy Journal, vol. 18, no. 7, pp.695-704, 2008.
  • S. Ramachandran, M. Singh, M. Mandal, Purification of Azurin from Pseudomonas aeuroginosa, in: Chromatogr. - Most Versatile Method, Analytical Chemistry, 2012.
  • M. Bradford, A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Analytical Biochemistry, vol. 72, pp.248-254, 1976.
  • T. Yamada, M. Goto, V. Punj, O. Zaborina, M.L. Chen, K. Kimbara, D. Majumdar, E. Cunningham, T.K. Das Gupta, A.M. Chakrabarty, Bacterial redox protein azurin, tumor suppressor protein p53, and regression of cancer , Proceedings of the National Academy of Science, vol. 99, pp.14098-14103, 2002.
  • V. Punj, S. Bhattacharyya, D. Saint-Dic, C. Vasu, E.A. Cunningham, J. Graves, T. Yamada, Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer, Oncogene, vol. 23, no. 13, pp.2367-2378, 2004.
  • J.H. Choi, M.H. Lee, Y.J. Cho, B.S., Park, S. Kim, G.C. Kim, The bacterial protein Azurin enhances sensitivity of oral squamous carcinoma cells to anticancer drugs, Yonsei Medical Journal, vol. 52, 773-78, 2011.
  • M. Goto, T. Yamada, K. Kimbara, J. Horner, M. Newcomb, T.K. Das Gupta, A.M. Chakrabarty, Induction of apoptosis in macrophages by Pseudomonas aeruginosa azurin: Tumour-suppressor protein p53 and reactive oxygen species, but not redox activity, as critical elements in cytotoxicity, Molecular Microbiology, vol. 47, no. 2, pp.549-559, 2003.
  • I. Pozdnyakova, J. Guidry, P. Wittung-Stafshede, Copper stabilizes azurin by decreasing the unfolding rate, Archieves of Biochemistry and Biophysics, vol. 390, no. 1, pp.146-148, 2001.
  • R. Knowles, Denitrification, Microbiology Reviews, vol. 46, no. 1, pp.43-70, 1982.
  • Y. Han, T. Wang, G. Chen, Q. Pu, Q. Liu, Y. Zhang, L. Xu, M. Wu, H. Liang, A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition, PLoS Pathogens, vol. 15, no. 12, pp.1-25, 2019.
  • E. Vijgenboom, J.E. Busch, G.W. Canters, In vivo studies disprove an obligatory role of azurin in denitrification in Pseudomonas aeruginosa and show that azu expression is under control of RpoS and ANR, Microbiology. vol. 143, no. 9, pp.2853-2863, 1997.
  • I. W. Sutherland, The Production of Azurin and Similar Proteins, Archiv für Mikrobiologie, vol. 54, pp.350-357, 1966.
There are 35 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Yağmur Ünver 0000-0003-1497-081X

Publication Date April 15, 2021
Submission Date January 12, 2021
Acceptance Date March 23, 2021
Published in Issue Year 2021 Volume: 25 Issue: 2

Cite

APA Ünver, Y. (2021). Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa. Sakarya University Journal of Science, 25(2), 601-609. https://doi.org/10.16984/saufenbilder.853961
AMA Ünver Y. Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa. SAUJS. April 2021;25(2):601-609. doi:10.16984/saufenbilder.853961
Chicago Ünver, Yağmur. “Utilization of Cheese Whey for Production of Azurin by Pseudomonas Aeruginosa”. Sakarya University Journal of Science 25, no. 2 (April 2021): 601-9. https://doi.org/10.16984/saufenbilder.853961.
EndNote Ünver Y (April 1, 2021) Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa. Sakarya University Journal of Science 25 2 601–609.
IEEE Y. Ünver, “Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa”, SAUJS, vol. 25, no. 2, pp. 601–609, 2021, doi: 10.16984/saufenbilder.853961.
ISNAD Ünver, Yağmur. “Utilization of Cheese Whey for Production of Azurin by Pseudomonas Aeruginosa”. Sakarya University Journal of Science 25/2 (April 2021), 601-609. https://doi.org/10.16984/saufenbilder.853961.
JAMA Ünver Y. Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa. SAUJS. 2021;25:601–609.
MLA Ünver, Yağmur. “Utilization of Cheese Whey for Production of Azurin by Pseudomonas Aeruginosa”. Sakarya University Journal of Science, vol. 25, no. 2, 2021, pp. 601-9, doi:10.16984/saufenbilder.853961.
Vancouver Ünver Y. Utilization of Cheese Whey for Production of Azurin by Pseudomonas aeruginosa. SAUJS. 2021;25(2):601-9.