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Year 2020, Volume: 24 Issue: 6, 812 - 820, 27.06.2025

Engin Koçak , Ceren Özkul , Gülce Taşkor Önel , Emirhan Nemutlu , Sedef Kir Meral Sağıroğlu

https://doi.org/10.35333/jrp.2020.240

Abstract

References

  • [1] Munita JM, Arias CA. Mechanisms of Antibiotic Resistance. Microbiol Spectr. 2016; 4(2): 201-208. [CrossRef]
  • [2] Hassan KS, Al-Riyami D. Infective Endocarditis of the Aortic Valve caused by Pseudomonas aeruginosa and Treated Medically in a Patient on Haemodialysis. Sultan Qaboos Univ Med J. 2012; 12(1): 120-123. [CrossRef]
  • [3] Lu CW, Hao JL, Liu XF, Liang LL, Zhou DD. Pseudomonas aeruginosa endophthalmitis caused by accidental iatrogenic ocular injury with a hypodermic needle. J Int Med Res. 2017; 45(2): 882-885. [CrossRef]
  • [4] Lister, PD, Wolter, DJ, Hanson ND. Antibacterial-Resistant Pseudomonas aeruginosa: Clinical Impact and Complex Regulation of Chromosomally Encoded Resistance Mechanisms. Clin Microbiol Rev. 2009; 22(4): 582-610. [CrossRef]
  • [5] Gasser G, Ott I, Metzler-Nolte N. Organometallic anticancer compounds. J Med Chem. 2011; 54(1): 3-25. [CrossRef]
  • [6] Forti KM, Bernard F, Santiago-Collazo G, Garcia W, Vera JL, Meléndez E. Para-Substituted Functionalised Ferrocene Esters with Novel Antibacterial Properties. J Clin Diagn Res. 2018; 12(2): 1-4. [CrossRef]
  • [7] Albada B, Metzler-Nolte N. Highly Potent Antibacterial Organometallic Peptide Conjugates. Acc Chem Res. 2017; 50(10): 2510-2518. [CrossRef]
  • [8] Patra M, Gasser G, Metzler-Nolte N. Small organometallic compounds as antibacterial agents. Dalton Trans. 2012; 41(21): 6350-6358. [CrossRef]
  • [9] Janka V, Žatko D, Ladislav V, Pál P, Janka P, Gabriela M. Some ferrocenyl chalcones as useful candidates for cancer treatment. In Vitro Cell Dev Biol Anim. 2015; 51(9): 964-974. [CrossRef]
  • [10] Wu C, Ye H, Bai W, Li Q, Guo D, Lv G. New potential anticancer agent of carborane derivatives: selective cellular interaction and activity of ferrocene-substituted dithio-o-carborane conjugates. Bioconjug Chem. 2011; 22(1): 16-25. [CrossRef]
  • [11] Ferle-Vidović A, Poljak-Blazi M, Rapić V, Skare D. Ferrocenes (F168, F169) and fero-sorbitol-citrate (FSC): potential anticancer drugs. Cancer Biother Radiopharm. 2000; 15(6): 617-624. [CrossRef]
  • [12] López-Cabrera Y, Castillo-García EL, Altamirano-Espino JA, Pérez-Capistran T, Farfán-García ED, Trujillo-Ferrara JG. Profile of three boron-containing compounds on the body weight, metabolism and inflammatory markers of diabetic rats. J Trace Elem Med Biol. 2018; 50: 424-429. [CrossRef]
  • [13] Ryu JH, Lee GJ, Shih YV, Kim TI, Varghese S. Phenylboronic acid-polymers for biomedical applications. Curr Med Chem. 2018; 37(26): 6797-6816. [CrossRef]
  • [14] Wang W, Liao L, Zhang X, Lei F, Zhang Y, Liu G. An Intelligent Nanoscale Insulin Delivery System. Molecules. 2018; 23(11); 2933-2945. [CrossRef]
  • [15] Windsor IW, Palte MJ, Lukesh JC, Gold B, Forest KT, Raines RT. Sub-picomolar Inhibition of HIV-1 Protease with a Boronic Acid. J Am Chem Soc. 2018; 140(43): 14015-14018. [CrossRef]
  • [16] Zhou J, Stapleton P, Haider S, Healy J. Boronic acid inhibitors of the class A β-lactamase KPC-2. Bioorg Med Chem. 2018; 26(11): 2921-2927. [CrossRef]
  • [17] Kiener, PA, Waley SG. Reversible Inhibitors of Penicillinases. Biochemical Journal. 1978; 169(1): 197-204. [CrossRef]
  • [18] Beesley T, Gascoyne N, Knotthunziker V, Petursson S, Waley SG, Jaurin B, Grundstrom T. The Inhibition of Class-C Beta-Lactamases by Boronic Acids. Biochemical Journal. 1983; 209(1): 229-233. [CrossRef]
  • [19] Patel TS, Pogue JM, Mills JP, Kaye KS. Meropenem-vaborbactam: a new weapon in the war against infections due to resistant Gram-negative bacteria. Future Microbiol. 2018; 13(1): 971-983. [CrossRef]
  • [20] Wu G, Cheon E. Meropenem-vaborbactam for the treatment of complicated urinary tract infections including acute pyelonephritis. Expert Opin Pharmacother. 2018; 19(13): 1495-1502. [CrossRef]
  • [21] Hishida T, Han YW, Shibata T, Kubota Y, Ishino Y, Iwasaki H, et al. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 2004; 18(15): 1886-1897. [CrossRef]
  • [22] Shereda RD, Bernstein DA, Keck JL. A central role for SSB in Escherichia coli RecQ DNA helicase function. J Biol Chem. 2007; 282(26): 19247-19258. [CrossRef]
  • [23] Farra A, Islam S, Strålfors A, Sörberg M, Wretlind B. Role of outer membrane protein OprD and penicillin-binding proteins in resistance of Pseudomonas aeruginosa to imipenem and meropenem. Int J Antimicrob Agents. 2008; 31(5): 427-433. [CrossRef]
  • [24] Fusté E, López-Jiménez L, Segura C, Gainza E, Vinuesa T, Viñas M. Carbapenem-resistance mechanisms of multidrug-resistant Pseudomonas aeruginosa. J Med Microbiol. 2013; 62(9): 1317-1325. [CrossRef]
  • [25] Santiviago CA, Fuentes JA, Bueno SM, Trombert AN, Hildago AA, Socias LT. The Salmonella enterica sv. Typhimurium smvA, yddG and ompD (porin) genes are required for the efficient efflux of methyl viologen. Mol Microbiol. 2002; 46(3): 687-698. [CrossRef]
  • [26] Pilonieta MC, Erickson KD, Ernst RK, Detweiler CS. A protein important for antimicrobial peptide resistance, YdeI/OmdA, is in the periplasm and interacts with OmpD/NmpC. J Bacteriol. 2009; 191(23): 7243-7252. [CrossRef]
  • [27] Donovan GT, Norton JP, Bower JM, Mulvey MA. Adenylate cyclase and the cyclic AMP receptor protein modulate stress resistance and virulence capacity of uropathogenic Escherichia coli. Infect Immun. 2013; 81(1): 249-258. [CrossRef]
  • [28] Roberts J, Park JS. Mfd, the bacterial transcription repair coupling factor: translocation, repair and termination. Curr Opin Microbiol. 2004; 7(2): 120-125. [CrossRef]
  • [29] Marsden AE, King JM, Spies MA, Kim OK, Yahr TL. Inhibition of Pseudomonas aeruginosa ExsA DNA-Binding Activity by N-Hydroxybenzimidazoles. Antimicrob Agents Chemother. 2016; 60(2): 766-776. [CrossRef]
  • [30] Lakkis C, Fleiszig SM. Resistance of Pseudomonas aeruginosa isolates to hydrogel contact lens disinfection correlates with cytotoxic activity. J Clin Microbiol. 2001; 39(4): 1477-1486. [CrossRef]
  • [31] Windgassen TA, Wessel SR, Bhattacharyya B, Keck JL. Mechanisms of bacterial DNA replication restart. Nucleic Acids Res. 2018; 46(2): 504-519. [CrossRef]
  • [32] Van Eijk E, Wittekoek B, Kuijper EJ, Smits WK. DNA replication proteins as potential targets for antimicrobials in drug-resistant bacterial pathogens. J Antimicrob Chemother. 2017; 72(5): 1275-1284. [CrossRef]
  • [33] Huang YH, Huang CC, Chen CC, Yang KJ, Huang CY. Inhibition of Staphylococcus aureus PriA Helicase by Flavonol Kaempferol. Protein J. 2015; 34(3): 169-172. [CrossRef]
  • [34] Ozkan E, Nemutlu E, Beksac MS, Kir S. GC-MS analysis of seven metabolites for the screening of pregnant women with Down Syndrome fetuses. J Pharmaceut Biomed. 2020; 188: 113427. [CrossRef]
  • [35] Moffatt BA, Ashihara H. Purine and pyrimidine nucleotide synthesis and metabolism. Arabidopsis Book. 2002: 1(18); 1-20. [CrossRef]
  • [36] Samant S, Lee H, Ghassemi M, Chen J, Cook JL, Mankin AS. Nucleotide biosynthesis is critical for growth of bacteria in human blood. PLoS Pathog. 2008; 4(2): 1-10. [CrossRef]
  • [37] Quéméneur L, Gerland LM, Flacher M, Ffrench M, Revillard JP, Genestier L. Differential control of cell cycle, proliferation, and survival of primary T lymphocytes by purine and pyrimidine nucleotides. J Immunol. 2003; 170(10): 4986-4995. [CrossRef]
  • [38] Yao J, Rock CO. Bacterial fatty acid metabolism in modern antibiotic discovery. Biochim Biophys Acta Mol Cell Biol Lipids. 2017; 1862(11): 1300-1309. [CrossRef]
  • [39] Heung LJ, Luberto C, Del Poeta M. Role of sphingolipids in microbial pathogenesis. Infect Immun. 2006; 74(1): 28- 39. [CrossRef]
  • [40] Johnson L, Mulcahy H, Kanevets U, Shi Y, Lewenza S. Surface-localized spermidine protects the Pseudomonas aeruginosa outer membrane from antibiotic treatment and oxidative stress. J Bacteriol. 2012; 194(4): 813-826. [CrossRef]
  • [41] CLSI. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard -Tenth Edition.CLSI document M07-A10. Wayne, PA: Clinical and Laboratory Standards Institute. 2008.
  • [42] Corte L, Tiecco M, Roscini L, De Vincenzi S, Colabella C, Germani R. FTIR Metabolomic Fingerprint Reveals Different Modes of Action Exerted by Structural Variants of N-Alkyltropinium Bromide Surfactants on Escherichia coli and Listeria innocua Cells. Plos One. 2015; 10(1): 1-10. [CrossRef]
  • [43] Kocak E, Altinoz S. Evaluation of regular UPLC/MS system for experimental and clinical proteomics. J Res Pharm. 2020; 24(4): 582-592. [CrossRef]
  • [44] Eylem C C, Yilmaz M, Derkus B, Nemutlu E, Camci C, Yilmaz B, Turkoglu M A, Aytac B, Ozyurt N, Emregul, E Untargeted multi-omic analysis of colorectal cancer-specific exosomes reveals joint pathways of colorectal cancer in both clinical samples and cell culture. Cancer Letters. 2020; 469: 186-194. [CrossRef]
  • [45] Kocak E, Ozkul C. Metabolic response of Escherichia coli to subinhibitory concentration of ofloxacin. J Res Pharm. 2020; 24(4): 593-601. [CrossRef]

Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach

Year 2020, Volume: 24 Issue: 6, 812 - 820, 27.06.2025

Engin Koçak , Ceren Özkul , Gülce Taşkor Önel , Emirhan Nemutlu , Sedef Kir Meral Sağıroğlu

https://doi.org/10.35333/jrp.2020.240

Abstract

Antibiotic resistance is one of the most serious global problems around the world. Pseudomonas aeruginosa is gram-negative bacteria and plays important role in local and systemic infections. In our work, we tried to understand mode of antimicrobial action of ferroccene- boronic acid over Pseudomonas aeruginosa via metabolomics and proteomics analysis. In proteomics analysis, we found that ferrocene-boronic acid effects various antimicrobial targets like ATP-dependent DNA helicase RecQ, Transcription-repair-coupling factor and Primasome assembly protein PriA. In metabolomics analysis, the ferrocene-boronic acid induced various metabolites involved in pyrimidine metabolism, lipid and fatty acid metabolism. Moreover, various polyamines like spermine and spermidine, which are very important for antibiotic resistance, pathogenesis and bacterial biofilm formation were decreased by ferroceneboronic acid. We believe that our results will contribute further studies regarding organometallic compounds in microbiology filelds.

Keywords

Metabolomics proteomics boronic acid Pseudomonas aeruginosa

References

  • [1] Munita JM, Arias CA. Mechanisms of Antibiotic Resistance. Microbiol Spectr. 2016; 4(2): 201-208. [CrossRef]
  • [2] Hassan KS, Al-Riyami D. Infective Endocarditis of the Aortic Valve caused by Pseudomonas aeruginosa and Treated Medically in a Patient on Haemodialysis. Sultan Qaboos Univ Med J. 2012; 12(1): 120-123. [CrossRef]
  • [3] Lu CW, Hao JL, Liu XF, Liang LL, Zhou DD. Pseudomonas aeruginosa endophthalmitis caused by accidental iatrogenic ocular injury with a hypodermic needle. J Int Med Res. 2017; 45(2): 882-885. [CrossRef]
  • [4] Lister, PD, Wolter, DJ, Hanson ND. Antibacterial-Resistant Pseudomonas aeruginosa: Clinical Impact and Complex Regulation of Chromosomally Encoded Resistance Mechanisms. Clin Microbiol Rev. 2009; 22(4): 582-610. [CrossRef]
  • [5] Gasser G, Ott I, Metzler-Nolte N. Organometallic anticancer compounds. J Med Chem. 2011; 54(1): 3-25. [CrossRef]
  • [6] Forti KM, Bernard F, Santiago-Collazo G, Garcia W, Vera JL, Meléndez E. Para-Substituted Functionalised Ferrocene Esters with Novel Antibacterial Properties. J Clin Diagn Res. 2018; 12(2): 1-4. [CrossRef]
  • [7] Albada B, Metzler-Nolte N. Highly Potent Antibacterial Organometallic Peptide Conjugates. Acc Chem Res. 2017; 50(10): 2510-2518. [CrossRef]
  • [8] Patra M, Gasser G, Metzler-Nolte N. Small organometallic compounds as antibacterial agents. Dalton Trans. 2012; 41(21): 6350-6358. [CrossRef]
  • [9] Janka V, Žatko D, Ladislav V, Pál P, Janka P, Gabriela M. Some ferrocenyl chalcones as useful candidates for cancer treatment. In Vitro Cell Dev Biol Anim. 2015; 51(9): 964-974. [CrossRef]
  • [10] Wu C, Ye H, Bai W, Li Q, Guo D, Lv G. New potential anticancer agent of carborane derivatives: selective cellular interaction and activity of ferrocene-substituted dithio-o-carborane conjugates. Bioconjug Chem. 2011; 22(1): 16-25. [CrossRef]
  • [11] Ferle-Vidović A, Poljak-Blazi M, Rapić V, Skare D. Ferrocenes (F168, F169) and fero-sorbitol-citrate (FSC): potential anticancer drugs. Cancer Biother Radiopharm. 2000; 15(6): 617-624. [CrossRef]
  • [12] López-Cabrera Y, Castillo-García EL, Altamirano-Espino JA, Pérez-Capistran T, Farfán-García ED, Trujillo-Ferrara JG. Profile of three boron-containing compounds on the body weight, metabolism and inflammatory markers of diabetic rats. J Trace Elem Med Biol. 2018; 50: 424-429. [CrossRef]
  • [13] Ryu JH, Lee GJ, Shih YV, Kim TI, Varghese S. Phenylboronic acid-polymers for biomedical applications. Curr Med Chem. 2018; 37(26): 6797-6816. [CrossRef]
  • [14] Wang W, Liao L, Zhang X, Lei F, Zhang Y, Liu G. An Intelligent Nanoscale Insulin Delivery System. Molecules. 2018; 23(11); 2933-2945. [CrossRef]
  • [15] Windsor IW, Palte MJ, Lukesh JC, Gold B, Forest KT, Raines RT. Sub-picomolar Inhibition of HIV-1 Protease with a Boronic Acid. J Am Chem Soc. 2018; 140(43): 14015-14018. [CrossRef]
  • [16] Zhou J, Stapleton P, Haider S, Healy J. Boronic acid inhibitors of the class A β-lactamase KPC-2. Bioorg Med Chem. 2018; 26(11): 2921-2927. [CrossRef]
  • [17] Kiener, PA, Waley SG. Reversible Inhibitors of Penicillinases. Biochemical Journal. 1978; 169(1): 197-204. [CrossRef]
  • [18] Beesley T, Gascoyne N, Knotthunziker V, Petursson S, Waley SG, Jaurin B, Grundstrom T. The Inhibition of Class-C Beta-Lactamases by Boronic Acids. Biochemical Journal. 1983; 209(1): 229-233. [CrossRef]
  • [19] Patel TS, Pogue JM, Mills JP, Kaye KS. Meropenem-vaborbactam: a new weapon in the war against infections due to resistant Gram-negative bacteria. Future Microbiol. 2018; 13(1): 971-983. [CrossRef]
  • [20] Wu G, Cheon E. Meropenem-vaborbactam for the treatment of complicated urinary tract infections including acute pyelonephritis. Expert Opin Pharmacother. 2018; 19(13): 1495-1502. [CrossRef]
  • [21] Hishida T, Han YW, Shibata T, Kubota Y, Ishino Y, Iwasaki H, et al. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 2004; 18(15): 1886-1897. [CrossRef]
  • [22] Shereda RD, Bernstein DA, Keck JL. A central role for SSB in Escherichia coli RecQ DNA helicase function. J Biol Chem. 2007; 282(26): 19247-19258. [CrossRef]
  • [23] Farra A, Islam S, Strålfors A, Sörberg M, Wretlind B. Role of outer membrane protein OprD and penicillin-binding proteins in resistance of Pseudomonas aeruginosa to imipenem and meropenem. Int J Antimicrob Agents. 2008; 31(5): 427-433. [CrossRef]
  • [24] Fusté E, López-Jiménez L, Segura C, Gainza E, Vinuesa T, Viñas M. Carbapenem-resistance mechanisms of multidrug-resistant Pseudomonas aeruginosa. J Med Microbiol. 2013; 62(9): 1317-1325. [CrossRef]
  • [25] Santiviago CA, Fuentes JA, Bueno SM, Trombert AN, Hildago AA, Socias LT. The Salmonella enterica sv. Typhimurium smvA, yddG and ompD (porin) genes are required for the efficient efflux of methyl viologen. Mol Microbiol. 2002; 46(3): 687-698. [CrossRef]
  • [26] Pilonieta MC, Erickson KD, Ernst RK, Detweiler CS. A protein important for antimicrobial peptide resistance, YdeI/OmdA, is in the periplasm and interacts with OmpD/NmpC. J Bacteriol. 2009; 191(23): 7243-7252. [CrossRef]
  • [27] Donovan GT, Norton JP, Bower JM, Mulvey MA. Adenylate cyclase and the cyclic AMP receptor protein modulate stress resistance and virulence capacity of uropathogenic Escherichia coli. Infect Immun. 2013; 81(1): 249-258. [CrossRef]
  • [28] Roberts J, Park JS. Mfd, the bacterial transcription repair coupling factor: translocation, repair and termination. Curr Opin Microbiol. 2004; 7(2): 120-125. [CrossRef]
  • [29] Marsden AE, King JM, Spies MA, Kim OK, Yahr TL. Inhibition of Pseudomonas aeruginosa ExsA DNA-Binding Activity by N-Hydroxybenzimidazoles. Antimicrob Agents Chemother. 2016; 60(2): 766-776. [CrossRef]
  • [30] Lakkis C, Fleiszig SM. Resistance of Pseudomonas aeruginosa isolates to hydrogel contact lens disinfection correlates with cytotoxic activity. J Clin Microbiol. 2001; 39(4): 1477-1486. [CrossRef]
  • [31] Windgassen TA, Wessel SR, Bhattacharyya B, Keck JL. Mechanisms of bacterial DNA replication restart. Nucleic Acids Res. 2018; 46(2): 504-519. [CrossRef]
  • [32] Van Eijk E, Wittekoek B, Kuijper EJ, Smits WK. DNA replication proteins as potential targets for antimicrobials in drug-resistant bacterial pathogens. J Antimicrob Chemother. 2017; 72(5): 1275-1284. [CrossRef]
  • [33] Huang YH, Huang CC, Chen CC, Yang KJ, Huang CY. Inhibition of Staphylococcus aureus PriA Helicase by Flavonol Kaempferol. Protein J. 2015; 34(3): 169-172. [CrossRef]
  • [34] Ozkan E, Nemutlu E, Beksac MS, Kir S. GC-MS analysis of seven metabolites for the screening of pregnant women with Down Syndrome fetuses. J Pharmaceut Biomed. 2020; 188: 113427. [CrossRef]
  • [35] Moffatt BA, Ashihara H. Purine and pyrimidine nucleotide synthesis and metabolism. Arabidopsis Book. 2002: 1(18); 1-20. [CrossRef]
  • [36] Samant S, Lee H, Ghassemi M, Chen J, Cook JL, Mankin AS. Nucleotide biosynthesis is critical for growth of bacteria in human blood. PLoS Pathog. 2008; 4(2): 1-10. [CrossRef]
  • [37] Quéméneur L, Gerland LM, Flacher M, Ffrench M, Revillard JP, Genestier L. Differential control of cell cycle, proliferation, and survival of primary T lymphocytes by purine and pyrimidine nucleotides. J Immunol. 2003; 170(10): 4986-4995. [CrossRef]
  • [38] Yao J, Rock CO. Bacterial fatty acid metabolism in modern antibiotic discovery. Biochim Biophys Acta Mol Cell Biol Lipids. 2017; 1862(11): 1300-1309. [CrossRef]
  • [39] Heung LJ, Luberto C, Del Poeta M. Role of sphingolipids in microbial pathogenesis. Infect Immun. 2006; 74(1): 28- 39. [CrossRef]
  • [40] Johnson L, Mulcahy H, Kanevets U, Shi Y, Lewenza S. Surface-localized spermidine protects the Pseudomonas aeruginosa outer membrane from antibiotic treatment and oxidative stress. J Bacteriol. 2012; 194(4): 813-826. [CrossRef]
  • [41] CLSI. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard -Tenth Edition.CLSI document M07-A10. Wayne, PA: Clinical and Laboratory Standards Institute. 2008.
  • [42] Corte L, Tiecco M, Roscini L, De Vincenzi S, Colabella C, Germani R. FTIR Metabolomic Fingerprint Reveals Different Modes of Action Exerted by Structural Variants of N-Alkyltropinium Bromide Surfactants on Escherichia coli and Listeria innocua Cells. Plos One. 2015; 10(1): 1-10. [CrossRef]
  • [43] Kocak E, Altinoz S. Evaluation of regular UPLC/MS system for experimental and clinical proteomics. J Res Pharm. 2020; 24(4): 582-592. [CrossRef]
  • [44] Eylem C C, Yilmaz M, Derkus B, Nemutlu E, Camci C, Yilmaz B, Turkoglu M A, Aytac B, Ozyurt N, Emregul, E Untargeted multi-omic analysis of colorectal cancer-specific exosomes reveals joint pathways of colorectal cancer in both clinical samples and cell culture. Cancer Letters. 2020; 469: 186-194. [CrossRef]
  • [45] Kocak E, Ozkul C. Metabolic response of Escherichia coli to subinhibitory concentration of ofloxacin. J Res Pharm. 2020; 24(4): 593-601. [CrossRef]
There are 45 citations in total.

Details

Primary Language English
Subjects Pharmaceutical Chemistry
Journal Section Articles
Authors

Engin Koçak

Ceren Özkul

Gülce Taşkor Önel

Emirhan Nemutlu

Sedef Kir

Meral Sağıroğlu

Publication Date June 27, 2025
Published in Issue Year 2020 Volume: 24 Issue: 6

Cite

APA Koçak, E., Özkul, C., Taşkor Önel, G., Nemutlu, E., et al. (2025). Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach. Journal of Research in Pharmacy, 24(6), 812-820. https://doi.org/10.35333/jrp.2020.240
AMA Koçak E, Özkul C, Taşkor Önel G, Nemutlu E, Kir S, Sağıroğlu M. Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach. J. Res. Pharm. June 2025;24(6):812-820. doi:10.35333/jrp.2020.240
Chicago Koçak, Engin, Ceren Özkul, Gülce Taşkor Önel, Emirhan Nemutlu, Sedef Kir, and Meral Sağıroğlu. “Screening the Antimicrobial Effect of Ferrocene-Boronic Acid on Pseudomonas Aeruginosa Using Proteomics and Metabolomics Approach”. Journal of Research in Pharmacy 24, no. 6 (June 2025): 812-20. https://doi.org/10.35333/jrp.2020.240.
EndNote Koçak E, Özkul C, Taşkor Önel G, Nemutlu E, Kir S, Sağıroğlu M (June 1, 2025) Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach. Journal of Research in Pharmacy 24 6 812–820.
IEEE E. Koçak, C. Özkul, G. Taşkor Önel, E. Nemutlu, S. Kir, and M. Sağıroğlu, “Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach”, J. Res. Pharm., vol. 24, no. 6, pp. 812–820, 2025, doi: 10.35333/jrp.2020.240.
ISNAD Koçak, Engin et al. “Screening the Antimicrobial Effect of Ferrocene-Boronic Acid on Pseudomonas Aeruginosa Using Proteomics and Metabolomics Approach”. Journal of Research in Pharmacy 24/6 (June 2025), 812-820. https://doi.org/10.35333/jrp.2020.240.
JAMA Koçak E, Özkul C, Taşkor Önel G, Nemutlu E, Kir S, Sağıroğlu M. Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach. J. Res. Pharm. 2025;24:812–820.
MLA Koçak, Engin et al. “Screening the Antimicrobial Effect of Ferrocene-Boronic Acid on Pseudomonas Aeruginosa Using Proteomics and Metabolomics Approach”. Journal of Research in Pharmacy, vol. 24, no. 6, 2025, pp. 812-20, doi:10.35333/jrp.2020.240.
Vancouver Koçak E, Özkul C, Taşkor Önel G, Nemutlu E, Kir S, Sağıroğlu M. Screening the antimicrobial effect of ferrocene-boronic acid on Pseudomonas aeruginosa using proteomics and metabolomics approach. J. Res. Pharm. 2025;24(6):812-20.