Chemistry, Biosynthesis and Pharmacology of Streptonigrin: An Old Molecule with Future Prospects for New Drug Design, Development and Therapy

References

• Donohoe TJ, Jones CR, Kornahrens AF, et al. Total synthesis of the antitumor antibiotic (±)-streptonigrin: first-and second-generation routes for de novo pyridine formation using ring-closing metathesis. J Org Chem. 2013;78(24):12338–12350. doi:10.1021/jo402388f
   PubMed Web of Science ®Google Scholar
• Chiu -Y-YH, Lipscomb WN. Molecular and crystal structure of streptonigrin. J Am Chem Soc. 1975;97(9):2525–2530. doi:10.1021/ja00842a033
   PubMed Web of Science ®Google Scholar
• Boger DL. Diels–alder reactions of heterocyclic azadienes: development of a strategy for the total synthesis of streptonigrin, lavendamycin, and synthetic quinoline-5, 8-quinones. In: Strategies and Tactics in Organic Synthesis. Vol. 2. Elsevier; 1989.
   Google Scholar
• Dreyton CJ, Anderson ED, Subramanian V, Boger DL, Thompson PR. Insights into the mechanism of streptonigrin-induced protein arginine deiminase inactivation. Bioorg Med Chem. 2014;22(4):1362–1369. doi:10.1016/j.bmc.2013.12.064
   PubMed Web of Science ®Google Scholar
• Wizeman JW, Mohan R. Expression of peptidylarginine deiminase 4 in an alkali injury model of retinal gliosis. Biochem Biophys Res Commun. 2017;487(1):134–139. doi:10.1016/j.bbrc.2017.04.031
   PubMed Web of Science ®Google Scholar
• Ham A, Rabadi M, Kim M, et al. Peptidyl arginine deiminase-4 activation exacerbates kidney ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2014;307(9):F1052–F1062. doi:10.1152/ajprenal.00243.2014
   PubMed Web of Science ®Google Scholar
• Rabadi M, Kim M, D’Agati V, Lee HT. Peptidyl arginine deiminase-4-deficient mice are protected against kidney and liver injury after renal ischemia and reperfusion. Am J Physiol Renal Physiol. 2016;311(2):F437–F449. doi:10.1152/ajprenal.00254.2016
   PubMed Web of Science ®Google Scholar
• Chen DB, Gao HW, Peng C, et al. Quinones as preventive agents in Alzheimer’s diseases: focus on NLRP3 inflammasomes. J Pharm Pharmacol. 2020;72(11):1481–1490. doi:10.1111/jphp.13332
   PubMed Web of Science ®Google Scholar
• Dahlem Junior MA, Nguema Edzang RW, Catto AL, Raimundo J-M. Quinones as an efficient molecular scaffold in the antibacterial/antifungal or antitumoral arsenal. Int J Mol Sci. 2022;23(22):14108. doi:10.3390/ijms232214108
   PubMed Web of Science ®Google Scholar
• Nilufer B, Hatice Y, Amac TF, et al. Synthesis, computational study, and evaluation of in vitro antimicrobial, antibiofilm, and anticancer activities of new sulfanyl aminonaphthoquinone derivatives. Lett Drug Des Discov. 2017;14(6). doi:10.2174/157018081406170606155530
   Web of Science ®Google Scholar
• Lee HW, Choi H, Nam SJ, Fenical W, Kim H. Potent inhibition of monoamine oxidase B by a piloquinone from marine-derived streptomyces sp. CNQ-027. J Microbiol Biotechnol. 2017;27:785–790. doi:10.4014/jmb.1612.12025
   PubMed Web of Science ®Google Scholar
• Alfadhli A, Mack A, Harper L, Berk S, Ritchie C, Barklis E. Analysis of quinolinequinone reactivity, cytotoxicity, and anti-HIV-1 properties. Bioorg Med Chem. 2016;24(21):5618–5625. doi:10.1016/j.bmc.2016.09.028
   PubMed Web of Science ®Google Scholar
• Patel OPS, Beteck RM, Legoabe LJ. Antimalarial application of quinones: a recent update. Eur J Med Chem. 2021;210:113084. doi:10.1016/j.ejmech.2020.113084
   PubMed Web of Science ®Google Scholar
• Benites J, Valderrama JA, Ramos M, Muccioli GG, Buc Calderon P. Targeting Akt as strategy to kill cancer cells using 3-substituted 5-anilinobenzo[c]isoxazolequinones: a preliminary study. Biomed Pharmacother. 2018;97:778–783. doi:10.1016/j.biopha.2017.10.108
   PubMed Web of Science ®Google Scholar
• Lee HW, Ryu HW, Kang MG, Park D, Oh SR, Kim H. Selective inhibition of monoamine oxidase A by purpurin, an anthraquinone. Bioorg Med Chem Lett. 2017;27(5):1136–1140. doi:10.1016/j.bmcl.2017.01.085
   PubMed Web of Science ®Google Scholar
• Pingaew R, Prachayasittikul V, Worachartcheewan A, et al. Novel 1,4-naphthoquinone-based sulfonamides: synthesis, QSAR, anticancer and antimalarial studies. Eur J Med Chem. 2015;103:446–459. doi:10.1016/j.ejmech.2015.09.001
   PubMed Web of Science ®Google Scholar
• Yildirim H, Bayrak N, Tuyun AF, Kara EM, Celik BO, Gupta GK. 2,3-disubstituted-1,4-naphthoquinones containing an arylamine with trifluoromethyl group: synthesis, biological evaluation, and computational study. RSC Adv. 2017;7:25753–25764. doi:10.1039/C7RA00868F
   Web of Science ®Google Scholar
• Xu F, Kong D, He X, et al. Characterization of streptonigrin biosynthesis reveals a cryptic carboxyl methylation and an unusual oxidative cleavage of a N–C bond. J Am Chem Soc. 2013;135(5):1739–1748. doi:10.1021/ja3069243
   PubMed Web of Science ®Google Scholar
• Lee S-H, Lee W-K, Kim N, et al. Renal cell carcinoma is abrogated by p53 stabilization through transglutaminase 2 inhibition. Cancers. 2018;10(11):455. doi:10.3390/cancers10110455
   PubMed Web of Science ®Google Scholar
• Sztiller-Sikorska M, Koprowska K, Majchrzak K, Hartman M, Czyz M. Natural compounds’ activity against cancer stem-like or fast-cycling melanoma cells. PLoS One. 2014;9(3):e90783. doi:10.1371/journal.pone.0090783
   PubMed Web of Science ®Google Scholar
• Ambaye N, Chen C-H, Khanna S, Li Y-J, Chen Y. Streptonigrin inhibits SENP1 and reduces the protein level of hypoxia-inducible factor 1α (HIF1α) in cells. Biochemistry. 2018;57(11):1807–1813. doi:10.1021/acs.biochem.7b00947
   PubMed Web of Science ®Google Scholar
• Nayak A, Müller S. SUMO-specific proteases/isopeptidases: sENPs and beyond. Genome Biol. 2014;15(7):1–7. doi:10.1186/s13059-014-0422-2
   Web of Science ®Google Scholar
• Wang Q, Xia N, Li T, et al. SUMO-specific protease 1 promotes prostate cancer progression and metastasis. Oncogene. 2013;32(19):2493–2498. doi:10.1038/onc.2012.250
   PubMed Web of Science ®Google Scholar
• Cheng J, Kang X, Zhang S, Yeh ET. SUMO-specific protease 1 is essential for stabilization of HIF1α during hypoxia. Cell. 2007;131(3):584–595. doi:10.1016/j.cell.2007.08.045
   PubMed Web of Science ®Google Scholar
• Park S, Chun S. Streptonigrin inhibits β-Catenin/Tcf signaling and shows cytotoxicity in β-catenin-activated cells. Biochimica et Biophysica Acta. 2011;1810(12):1340–1345. doi:10.1016/j.bbagen.2011.06.023
   PubMed Web of Science ®Google Scholar
• Loyola AC, Dao K, Shang R, et al. Streptonigrin at low concentration promotes heterochromatin formation. Sci Rep. 2020;10(1):1–11. doi:10.1038/s41598-020-60469-6
   PubMed Web of Science ®Google Scholar
• Mahfuz AB, Iqbal MN, Opazo FS, Zubair-Bin-Mahfuj A. Characterization of ribonucleotide reductases of emerging pathogens Elizabethkingia anophelis and Elizabethkingia meningoseptica and streptonigrin as their inhibitor: a computational study. J Biomol Struct Dyn. 2021;40:1–13.
   Web of Science ®Google Scholar
• Sankari S, O’Brian MR. Synthetic lethality of the bfr and mbfA genes reveals a functional relationship between iron storage and iron export in managing stress responses in Bradyrhizobium japonicum. PLoS One. 2016;11(6):e0157250. doi:10.1371/journal.pone.0157250
   PubMed Web of Science ®Google Scholar
• Bhubhanil S, Chamsing J, Sittipo P, Chaoprasid P, Sukchawalit R, Mongkolsuk S. Roles of Agrobacterium tumefaciens membrane-bound ferritin (MbfA) in iron transport and resistance to iron under acidic conditions. Microbiology. 2014;160(5):863–871. doi:10.1099/mic.0.076802-0
   PubMedGoogle Scholar
• Herlt A, Rickards R, Wu J-P. The structure of streptonigrone, and a comment on the biosynthesis of the streptonigrin antibiotics. J Antibiot. 1985;38(4):516–518. doi:10.7164/antibiotics.38.516
   PubMed Web of Science ®Google Scholar
• Crepps SC, Fields EE, Galan D, Corbett JP, Von Hasseln ER, Spatafora GA. The SloR metalloregulator is involved in the Streptococcus mutans oxidative stress response. Mol Oral Microbiol. 2016;31(6):526–539. doi:10.1111/omi.12147
   PubMed Web of Science ®Google Scholar
• Knuckley B, Jones JE, Bachovchin DA, et al. A fluopol-ABPP HTS assay to identify PAD inhibitors. Chem Commun. 2010;46(38):7175–7177. doi:10.1039/c0cc02634d
   PubMed Web of Science ®Google Scholar
• Raup-Konsavage WM, Wang Y, Wang WW, Feliers D, Ruan H, Reeves WB. Neutrophil peptidyl arginine deiminase-4 has a pivotal role in ischemia/reperfusion-induced acute kidney injury. Kidney Int. 2018;93(2):365–374. doi:10.1016/j.kint.2017.08.014
   PubMed Web of Science ®Google Scholar
• Luo Y, Arita K, Bhatia M, et al. Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry. 2006;45(39):11727–11736. doi:10.1021/bi061180d
   PubMed Web of Science ®Google Scholar
• Anderberg PI, Luck IJ, Harding MM. Assignment of the 13C and 15N NMR spectra of the antitumour antibiotic streptonigrin. Magn Reson Chem. 2002;40(4):313–315. doi:10.1002/mrc.997
   Web of Science ®Google Scholar
• Kametani T, Ogasawara K, Shio M, Kozuka A. Streptonigrin and related compounds. VI. The NMR spectra of 4-(2, 3, 4-trimethoxyphenyl)-2, 3-dimethylpyridine derivatives. (Studies on the syntheses of heterocyclic compounds. CLXX). Yakugaku zassh. 1967;87(3):260–265. doi:10.1248/yakushi1947.87.3_260
   PubMedGoogle Scholar
• Rao KV, Rock CP. Streptonigrin and related compounds. 6. Synthesis and activity of some quinoxaline analogues. J Heterocycl Chem. 1996;33(2):447–458. doi:10.1002/jhet.5570330238
   Web of Science ®Google Scholar
• Auger I, Charpin C, Balandraud N, Martin M, Roudier J. Autoantibodies to PAD4 and BRAF in rheumatoid arthritis. Autoimmun Rev. 2012;11(11):801–803. doi:10.1016/j.autrev.2012.02.009
   PubMed Web of Science ®Google Scholar
• Wang X, Xu F, Huang T, Deng Z, Lin S. A novel streptonigrin type alkaloid from the Streptomyces flocculus CGMCC 4.1223 mutant Δ stnA/Q2. Nat Prod Res. 2022;36(13):3337–3345. doi:10.1080/14786419.2020.1856840
   PubMed Web of Science ®Google Scholar
• Bayrak N, Ciftci HI, Yildiz M, et al. ‘Structure based design, synthesis, and evaluation of anti-CML activity of the quinolinequinones as LY83583 analogs’. Chem Biol Interact. 2021;345:109555. doi:10.1016/j.cbi.2021.109555
   PubMed Web of Science ®Google Scholar
• Ciftci HI, Bayrak N, Mahmut Y, et al. Design, synthesis and investigation of the mechanism of action underlying anti-leukemic effects of the quinolinequinones as LY83583 analogs. Bioorg Chem. 2021;114:105160. doi:10.1016/j.bioorg.2021.105160
   PubMed Web of Science ®Google Scholar
• Mataraci-Kara E, Bayrak N, Yildiz M, Yildirim H, Ozbek-Celik B, Tuyun AF. Discovery and structure-activity relationships of the quinolinequinones: promising antimicrobial agents and mode of action evaluation. Drug Dev Res. 2022;83:628–636. doi:10.1002/ddr.21893
   PubMed Web of Science ®Google Scholar
• Mataraci-Kara E, Bayrak N, Yildiz M, Yildirim H, TuYuN AF. Active quinolinequinones against methicillin-resistant staphylococcus spp. Chem Biodivers. 2022;19:e202100616. doi:10.1002/cbdv.202100616
   PubMed Web of Science ®Google Scholar
• Yildirim H, Bayrak N, Yildiz M, et al. Highly active small aminated quinolinequinones against drug-resistant Staphylococcus aureus and Candida albicans. Molecules. 2022;27(9):2923. doi:10.3390/molecules27092923
   PubMed Web of Science ®Google Scholar
• Yildiz M, Bayrak N, Yildirim H, et al. Discovery of quinolinequinones with N-phenylpiperazine by conversion of hydroxyquinoline as a new class of antimicrobial agents targeting resistant pathogenic microorganisms. Bioorg Chem. 2022;128:106045. doi:10.1016/j.bioorg.2022.106045
   PubMed Web of Science ®Google Scholar
• Yildirim H, Bayrak N, Yildiz M, et al. Aminated quinolinequinones as privileged scaffolds for antibacterial agents: synthesis, in vitro evaluation, and putative mode of action. ACS Omega. 2022;7(46):41915–41928. doi:10.1021/acsomega.2c03193
   PubMedGoogle Scholar
• Attia MF, Anton N, Wallyn J, Omran Z, Vandamme TF. An overview of active and passive targeting strategies to improve the nanocarriers efficiency to tumour sites. J Pharm Pharmacol. 2019;71(8):1185–1198. doi:10.1111/jphp.13098
   PubMed Web of Science ®Google Scholar
• Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv Drug Deliv Rev. 2011;63(3):131–135. doi:10.1016/j.addr.2010.03.011
   PubMed Web of Science ®Google Scholar
• Osaki F, Kanamori T, Sando S, Sera T, Aoyama Y. A quantum dot conjugated sugar ball and its cellular uptake. On the size effects of endocytosis in the subviral region. J Am Chem Soc. 2004;126(21):6520–6521. doi:10.1021/ja048792a
   PubMed Web of Science ®Google Scholar
• Rowinsky EK, Rizzo J, Ochoa L, et al. A Phase I and pharmacokinetic study of pegylated camptothecin as a 1-hour infusion every 3 weeks in patients with advanced solid malignancies. J Clin Oncol. 2003;21(1):148–157. doi:10.1200/JCO.2003.03.143
   PubMed Web of Science ®Google Scholar
• Yoo HS, Park TG. Folate receptor targeted biodegradable polymeric doxorubicin micelles. J Control Release. 2004;96(2):273–283. doi:10.1016/j.jconrel.2004.02.003
   PubMed Web of Science ®Google Scholar
• Kobayashi H, Watanabe R, Choyke PL. Improving conventional enhanced permeability and retention (EPR) effects; what is the appropriate target? Theranostics. 2014;4(1):81. doi:10.7150/thno.7193
   Web of Science ®Google Scholar
• Noble GT, Stefanick JF, Ashley JD, Kiziltepe T, Bilgicer B. Ligand-targeted liposome design: challenges and fundamental considerations. Trends Biotechnol. 2014;32(1):32–45. doi:10.1016/j.tibtech.2013.09.007
   PubMed Web of Science ®Google Scholar
• Liu Y, Ran R, Chen J, et al. Paclitaxel loaded liposomes decorated with a multifunctional tandem peptide for glioma targeting. Biomaterials. 2014;35(17):4835–4847. doi:10.1016/j.biomaterials.2014.02.031
   PubMed Web of Science ®Google Scholar
• Choudhury H, Sisinthy SP, Gorain B, Kesharwani P. History and introduction of dendrimers. In: Dendrimer-Based Nanotherapeutics. Elsevier; 2021.
   Google Scholar
• Graf N, Bielenberg DR, Kolishetti N, et al. αVβ3 integrin-targeted PLGA-PEG nanoparticles for enhanced anti-tumor efficacy of a Pt (IV) prodrug. ACS Nano. 2012;6(5):4530–4539. doi:10.1021/nn301148e
   PubMed Web of Science ®Google Scholar
• Lasa-Saracibar B, Estella-Hermoso de Mendoza A, Guada M, Dios-Vieitez C, Blanco-Prieto MJ. Lipid nanoparticles for cancer therapy: state of the art and future prospects. Expert Opin Drug Deliv. 2012;9(10):1245–1261. doi:10.1517/17425247.2012.717928
   PubMed Web of Science ®Google Scholar
• Watermann A, Brieger J. Mesoporous silica nanoparticles as drug delivery vehicles in cancer. Nanomaterials. 2017;7(7):189. doi:10.3390/nano7070189
   Web of Science ®Google Scholar
• Holmannova D, Borsky P, Svadlakova T, Borska L, Fiala Z. Carbon nanoparticles and their biomedical applications. Appl Sci. 2022;12(15):7865. doi:10.3390/app12157865
   Google Scholar
• Humphrey E, Dietrich F. Clinical experience with the methyl ester of streptonigrin (Ncs-45384). Cancer Chemother Rep. 1963;33:21–26.
   PubMedGoogle Scholar
• Isshiki K, Sawa T, Miura K, et al. A new antitumor antibiotic: demethylstreptonigrin. J Antibiot. 1986;39(7):1013–1015. doi:10.7164/antibiotics.39.1013
   PubMed Web of Science ®Google Scholar
• Inouye Y, Okada H, Roy SK, et al. Biological properties of streptonigrin derivatives I. antimicrobial and cytocidal activities. J Antibiot. 1985;38(10):1429–1432. doi:10.7164/antibiotics.38.1429
   PubMed Web of Science ®Google Scholar