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Current Protein & Peptide Science

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ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

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Mini-Review Article

Compelling Cyclic Peptide Scaffolds for Antitubercular Action: An Account (2011-21) of the Natural Source

Author(s): Arnab Chowdhury and Anupam Bandyopadhyay*

Volume 23, Issue 12, 2022

Published on: 27 October, 2022

Page: [823 - 836] Pages: 14

DOI: 10.2174/1389203723666220930111259

Price: $65

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Abstract

Natural cyclic peptide scaffolds are indispensable in medicinal chemistry, chemical biology, and drug discovery platforms due to their chemical diversity, structural integrity, proteolytic stability and biocompatibility. Historically, their isolation and profound understanding of target engagement have been identified as lead pharmacophore discovery. Natural cyclic peptides are the largest class of pharmacologically active scaffold, in which most show activity against drug-resistant Mycobacterium tuberculosis (Mtb). Nevertheless, eight recently discovered cyclic peptide scaffolds exhibit promising antitubercular activity among numerous naturally occurring antitubercular peptides, and they are amenable scaffolds to drug development. We examined their biological origin, scaffolds, isolations, chemical synthesis, and reasons for biological actions against Mtb. Understanding these peptide scaffold details will further allow synthetic and medicinal chemists to develop novel peptide therapeutics against tuberculosis-infected deadly diseases. This review emphasizes these cyclic peptides' in vitro and in vivo activity profiles, including their structural and chemical features.

Keywords: Natural cyclic peptide, Peptide metabolites, Antitubercular, Peptide synthesis and characterization, In vitro and vivo activity, Peptide scaffolds

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[1]
Blunt, J.W.; Copp, B.R.; Keyzers, R.A.; Munro, M.H.G.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep., 2013, 30(2), 237-323.
[http://dx.doi.org/10.1039/C2NP20112G] [PMID: 23263727]
[2]
Demain, A.L.; Fang, A. The natural functions of secondary metabolites. Adv. Biochem. Eng. Biotechnol., 2000, 69, 1-39.
[http://dx.doi.org/10.1007/3-540-44964-7_1] [PMID: 11036689]
[3]
Newman, D.J.; Cragg, G.M. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J. Nat. Prod., 2012, 75(3), 311-335.
[http://dx.doi.org/10.1021/np200906s] [PMID: 22316239]
[4]
Abdalla, M.; McGaw, L. Natural cyclic peptides as an attractive modality for therapeutics: A mini review. Molecules, 2018, 23(8), 2080.
[http://dx.doi.org/10.3390/molecules23082080] [PMID: 30127265]
[5]
Fang, W.Y.; Dahiya, R.; Qin, H.L.; Mourya, R.; Maharaj, S. Natural proline-rich cyclopolypeptides from marine organisms: Chemistry, synthetic methodologies and biological status. Mar. Drugs, 2016, 14(11), 194.
[http://dx.doi.org/10.3390/md14110194] [PMID: 27792168]
[6]
Mi, Y.; Zhang, J.; He, S.; Yan, X. New peptides isolated from marine cyanobacteria, an overview over the past decade. Mar. Drugs, 2017, 15(5), 132.
[http://dx.doi.org/10.3390/md15050132] [PMID: 28475149]
[7]
Thorstholm, L.; Craik, D.J. Discovery and applications of naturally occurring cyclic peptides. Drug Discov. Today. Technol., 2012, 9(1), e13-e21.
[http://dx.doi.org/10.1016/j.ddtec.2011.07.005] [PMID: 24064240]
[8]
Ajith, T.A.; Janardhanan, K.K. Antidiabetic properties of medicinal mushrooms with special reference to phellinus species: A review. Nat. Prod. J., 2021, 11(2), 120-126.
[http://dx.doi.org/10.2174/2210315510666200124124540]
[9]
Jiménez, C. Marine natural products in medicinal chemistry. ACS Med. Chem. Lett., 2018, 9(10), 959-961.
[http://dx.doi.org/10.1021/acsmedchemlett.8b00368] [PMID: 30344898]
[10]
Lee, A.C.L.; Harris, J.L.; Khanna, K.K.; Hong, J.H. A comprehensive review on current advances in peptide drug development and design. Int. J. Mol. Sci., 2019, 20(10), 2383.
[http://dx.doi.org/10.3390/ijms20102383] [PMID: 31091705]
[11]
Ramakrishnan, C.; Paul, P.K.C.; Ramnarayan, K. Cyclic peptides-Small and big and their conformational aspects. J. Biosci., 1985, 8(1-2), 239-251.
[http://dx.doi.org/10.1007/BF02703979]
[12]
Cascales, L.; Craik, D.J. Naturally occurring circular proteins: Distribution, biosynthesis and evolution. Org. Biomol. Chem., 2010, 8(22), 5035-5047.
[http://dx.doi.org/10.1039/c0ob00139b] [PMID: 20835453]
[13]
Tan, N.H.; Zhou, J. Plant Cyclopeptides. Chem. Rev., 2006, 106(3), 840-895.
[http://dx.doi.org/10.1021/cr040699h] [PMID: 16522011]
[14]
Guharoy, M.; Chakrabarti, P. Secondary structure based analysis and classification of biological interfaces: identification of binding motifs in protein-protein interactions. Bioinformatics, 2007, 23(15), 1909-1918.
[http://dx.doi.org/10.1093/bioinformatics/btm274] [PMID: 17510165]
[15]
Adusumalli, S.R.; Yudin, A.K.; Rai, V. Cyclic peptides. Nat. Lact. Lact. Synth. Occur. Biol. Act., 2013, 321-369.
[http://dx.doi.org/10.1002/9783527666911.ch8]
[16]
Jin, K. Developing cyclic peptide-based drug candidates: An overview. Future Med. Chem., 2020, 12(19), 1687-1690.
[http://dx.doi.org/10.4155/fmc-2020-0171] [PMID: 32972246]
[17]
Cheung, R.; Ng, T.; Wong, J. Marine peptides. Mar. Drugs, 2015, 13(7), 4006-4043.
[http://dx.doi.org/10.3390/md13074006] [PMID: 26132844]
[18]
Joo, S.H. Cyclic peptides as therapeutic agents and biochemical tools. Biomol. Ther. (Seoul), 2012, 20(1), 19-26.
[http://dx.doi.org/10.4062/biomolther.2012.20.1.019] [PMID: 24116270]
[19]
Jing, X.; Jin, K. A gold mine for drug discovery: Strategies to develop cyclic peptides into therapies. Med. Res. Rev., 2020, 40(2), 753-810.
[http://dx.doi.org/10.1002/med.21639] [PMID: 31599007]
[20]
Fu, H.; Lewnard, J.A.; Frost, I.; Laxminarayan, R.; Arinaminpathy, N. Modelling the global burden of drug-resistant tuberculosis averta-ble by a post-exposure vaccine. Nat. Commun., 2021, 12(1), 1-9.
[http://dx.doi.org/10.1038/s41467-020-20731-x]
[21]
Rajagopalan, S.; Yoshikawa, T.T. Tuberculosis. Pathy’sPrinc. Pract. Geriatr. Med. , Fifth Ed; , 2012, 2, pp. 1413-1423.
[http://dx.doi.org/10.1002/9781119952930.ch115]
[22]
Education, H. Search for N E W drugs. Pharm. Chem. J., 2000, 34(1), 11-18.
[23]
Mukai, A.; Fukai, T.; Hoshino, Y.; Yazawa, K.; Harada, K.; Mikami, Y. Nocardithiocin, a novel thiopeptide antibiotic, produced by patho-genic Nocardia pseudobrasiliensis IFM 0757. J. Antibiot. (Tokyo), 2009, 62(11), 613-619.
[http://dx.doi.org/10.1038/ja.2009.90] [PMID: 19745839]
[24]
Haritakun, R.; Sappan, M.; Suvannakad, R.; Tasanathai, K.; Isaka, M. An antimycobacterial cyclodepsipeptide from the entomopathogenic fungus Ophiocordyceps communis BCC 16475. J. Nat. Prod., 2010, 73(1), 75-78.
[http://dx.doi.org/10.1021/np900520b] [PMID: 20028029]
[25]
Isaka, M.; Berkaew, P.; Intereya, K.; Komwijit, S.; Sathitkunanon, T. Antiplasmodial and antiviral cyclohexadepsipeptides from the endo-phytic fungus Pullularia sp. BCC 8613. Tetrahedron, 2007, 63(29), 6855-6860.
[http://dx.doi.org/10.1016/j.tet.2007.04.062]
[26]
Huang, X.; Roemer, E.; Sattler, I.; Moellmann, U.; Christner, A.; Grabley, S. Lydiamycins A-D: Cyclodepsipetides with antimycobacterial properties. Angew. Chem. Int. Ed., 2006, 45(19), 3067-3072.
[http://dx.doi.org/10.1002/anie.200503381] [PMID: 16619323]
[27]
Okunade, A.; Elvin-Lewis, M.P.F.; Lewis, W.H. Natural antimycobacterial metabolites: Current status. Phytochemistry, 2004, 65(8), 1017-1032.
[http://dx.doi.org/10.1016/j.phytochem.2004.02.013] [PMID: 15110681]
[28]
Copp, B.R.; Pearce, A.N. Natural product growth inhibitors of Mycobacterium tuberculosis. Nat. Prod. Rep., 2007, 24(2), 278-297.
[http://dx.doi.org/10.1039/B513520F] [PMID: 17389998]
[29]
Gao, W.; Kim, J.Y.; Chen, S.N.; Cho, S.H.; Choi, J.; Jaki, B.U.; Jin, Y.Y.; Lankin, D.C.; Lee, J.E.; Lee, S.Y.; McAlpine, J.B.; Napolitano, J.G.; Franzblau, S.G.; Suh, J.W.; Pauli, G.F. Discovery and characterization of the tuberculosis drug lead ecumicin. Org. Lett., 2014, 16(23), 6044-6047.
[http://dx.doi.org/10.1021/ol5026603] [PMID: 25409285]
[30]
Hawkins, P.M.E.; Giltrap, A.M.; Nagalingam, G.; Britton, W.J.; Payne, R.J. Total synthesis of ecumicin. Org. Lett., 2018, 20(4), 1019-1022.
[http://dx.doi.org/10.1021/acs.orglett.7b03967] [PMID: 29412668]
[31]
Ling, L.L.; Schneider, T.; Peoples, A.J.; Spoering, A.L.; Engels, I.; Conlon, B.P.; Mueller, A.; Schäberle, T.F.; Hughes, D.E.; Epstein, S.; Jones, M.; Lazarides, L.; Steadman, V.A.; Cohen, D.R.; Felix, C.R.; Fetterman, K.A.; Millett, W.P.; Nitti, A.G.; Zullo, A.M.; Chen, C.; Lew-is, K. A new antibiotic kills pathogens without detectable resistance. Nature, 2015, 517(7535), 455-459.
[http://dx.doi.org/10.1038/nature14098] [PMID: 25561178]
[32]
Nichols, D.; Cahoon, N.; Trakhtenberg, E.M.; Pham, L.; Mehta, A.; Belanger, A.; Kanigan, T.; Lewis, K.; Epstein, S.S. Use of ichip for high-throughput in situ cultivation of “uncultivable” microbial species. Appl. Environ. Microbiol., 2010, 76(8), 2445-2450.
[http://dx.doi.org/10.1128/AEM.01754-09] [PMID: 20173072]
[33]
Kollef, M.H. Limitations of vancomycin in the management of resistant staphylococcal infections. Clin. Infect. Dis., 2007, 45(Suppl. 3), S191-S195.
[http://dx.doi.org/10.1086/519470] [PMID: 17712746]
[34]
Jin, K.; Sam, I.H.; Po, K.H.L.; Lin, D.; Ghazvini Zadeh, E.H.; Chen, S.; Yuan, Y.; Li, X. Total synthesis of teixobactin. Nat. Commun., 2016, 7(1), 12394.
[http://dx.doi.org/10.1038/ncomms12394] [PMID: 27484680]
[35]
Craig, W.; Chen, J.; Richardson, D.; Thorpe, R.; Yuan, Y. A highly stereoselective and scalable synthesis of L -allo-Enduracididine. Org. Lett., 2015, 17(18), 4620-4623.
[http://dx.doi.org/10.1021/acs.orglett.5b02362] [PMID: 26356680]
[36]
Sun, C.; Liu, Z.; Zhu, X.; Fan, Z.; Huang, X.; Wu, Q.; Zheng, X.; Qin, X.; Zhang, T.; Zhang, H.; Ju, J.; Ma, J. Antitubercular Ilamycins from Marine-Derived Streptomyces atratus SCSIO ZH16 Δ ilaR. J. Nat. Prod., 2020, 83(5), 1646-1657.
[http://dx.doi.org/10.1021/acs.jnatprod.0c00151] [PMID: 32324401]
[37]
Ma, J.; Huang, H.; Xie, Y.; Liu, Z.; Zhao, J.; Zhang, C.; Jia, Y.; Zhang, Y.; Zhang, H.; Zhang, T.; Ju, J. Biosynthesis of ilamycins featuring unusual building blocks and engineered production of enhanced anti-tuberculosis agents. Nat. Commun., 2017, 8(1), 391.
[http://dx.doi.org/10.1038/s41467-017-00419-5] [PMID: 28855504]
[38]
Zhou, W.; Fang, H.; Wu, Q.; Wang, X.; Liu, R.; Li, F.; Xiao, J.; Yuan, L.; Zhou, Z.; Ma, J.; Wang, L.; Zhao, W.; You, H.; Ju, J.; Feng, J.; Chen, C. Ilamycin E, a natural product of marine actinomycete, inhibits triple-negative breast cancer partially through ER stress-CHOP-Bcl-2. Int. J. Biol. Sci., 2019, 15(8), 1723-1732.
[http://dx.doi.org/10.7150/ijbs.35284] [PMID: 31360114]
[39]
Xie, Q.; Yang, Z.; Huang, X.; Zhang, Z.; Li, J.; Ju, J.; Zhang, H.; Ma, J.; Ilamycin, C. Ilamycin C induces apoptosis and inhibits migration and invasion in triple-negative breast cancer by suppressing IL-6/STAT3 pathway. J. Hematol. Oncol., 2019, 12(1), 60.
[http://dx.doi.org/10.1186/s13045-019-0744-3] [PMID: 31186039]
[40]
Cheng, Y.; Tang, S.; Guo, Y.; Ye, T. Total synthesis of anti-tuberculosis natural products Ilamycins E 1 and F. Org. Lett., 2018, 20(19), 6166-6169.
[http://dx.doi.org/10.1021/acs.orglett.8b02643] [PMID: 30252492]
[41]
Ardá, A.; Soengas, R. G.; Nieto, M. I.; Jiménez, C.; Rodríguez, J. Synthesis of ( - ) -Dysithiazolamide. 2008.
[42]
Um, S.; Choi, T.J.; Kim, H.; Kim, B.Y.; Kim, S.H.; Lee, S.K.; Oh, K.B.; Shin, J.; Oh, D.C. Ohmyungsamycins A and B: Cytotoxic and an-timicrobial cyclic peptides produced by Streptomyces sp. from a volcanic island. J. Org. Chem., 2013, 78(24), 12321-12329.
[http://dx.doi.org/10.1021/jo401974g] [PMID: 24266328]
[43]
Hur, J.; Jang, J.; Sim, J.; Son, W.S.; Ahn, H.C.; Kim, T.S.; Shin, Y.H.; Lim, C.; Lee, S.; An, H.; Kim, S.H.; Oh, D.C.; Jo, E.K.; Jang, J.; Lee, J.; Suh, Y.G. Conformation-enabled total syntheses of ohmyungsamycins A and B and structural revision of ohmyungsamycin B. Angew. Chem. Int. Ed., 2018, 57(12), 3069-3073.
[http://dx.doi.org/10.1002/anie.201711286] [PMID: 29380472]
[44]
Kim, T.S.; Shin, Y.H.; Lee, H.M.; Kim, J.K.; Choe, J.H.; Jang, J.C.; Um, S.; Jin, H.S.; Komatsu, M.; Cha, G.H.; Chae, H.J.; Oh, D.C.; Jo, E.K. Ohmyungsamycins promote antimicrobial responses through autophagy activation via AMP-activated protein kinase pathway. Sci. Rep., 2017, 7(1), 3431.
[http://dx.doi.org/10.1038/s41598-017-03477-3] [PMID: 28611371]
[45]
Hawkins, P.M.E.; Tran, W.; Nagalingam, G.; Cheung, C.Y.; Giltrap, A.M.; Cook, G.M.; Britton, W.J.; Payne, R.J. Total synthesis and anti-mycobacterial activity of ohmyungsamycin a, deoxyecumicin, and ecumicin. Chemistry, 2020, 26(66), 15200-15205.
[http://dx.doi.org/10.1002/chem.202002408] [PMID: 32567168]
[46]
Maksimov, M.O.; Pan, J.; Link, A.J. Lasso Peptides: Structure; Function, Biosynthesis, and Engineering, 2012, pp. 996-1006.
[http://dx.doi.org/10.1039/c2np20070h]
[47]
Gao, W.; Kim, J.Y.; Anderson, J.R.; Akopian, T.; Hong, S.; Jin, Y.Y.; Kandror, O.; Kim, J.W.; Lee, I.A.; Lee, S.Y.; McAlpine, J.B.; Mulu-geta, S.; Sunoqrot, S.; Wang, Y.; Yang, S.H.; Yoon, T.M.; Goldberg, A.L.; Pauli, G.F.; Suh, J.W.; Franzblau, S.G.; Cho, S. The cyclic pep-tide ecumicin targeting ClpC1 is active against Mycobacterium tuberculosis in vivo. Antimicrob. Agents Chemother., 2015, 59(2), 880-889.
[http://dx.doi.org/10.1128/AAC.04054-14] [PMID: 25421483]
[48]
Lear, S.; Munshi, T.; Hudson, A.S.; Hatton, C.; Clardy, J.; Mosely, J.A.; Bull, T.J.; Sit, C.S.; Cobb, S.L. Total chemical synthesis of lassomycin and lassomycin amide. Org. Biomol. Chem., 2016, 4534-4541.
[http://dx.doi.org/10.1039/C6OB00631K]
[49]
Harris, P.W.R.; Cook, E.G.M.; Leung, D.I.K.H. An efficient chemical synthesis of lassomycin enabled by an on-resin lactamisation-off-resin methanolysis strategy and preparation of chemical variants. Austr. J. Chem., 2017, 70(2), 172-183.
[50]
Daletos, G.; Kalscheuer, R.; Koliwer-brandl, H.; Hartmann, R.; Voogd, N.J. De; Wray, V.; Lin, W.; Proksch, P. Callyaerins from the marine sponge Callyspongia aerizusa: Cyclic peptides with antitubercular activity. J. Nat. Prod., 2015, 78(8), 1910-1925.
[http://dx.doi.org/10.1021/acs.jnatprod.5b00266]
[51]
Ibrahim, S.R.M.; Min, C.C.; Teuscher, F.; Ebel, R.; Kakoschke, C.; Lin, W.; Wray, V.; Edrada-Ebel, R.; Proksch, P.; Val, R. Callyaerins A-F and H, new cytotoxic cyclic peptides from the Indonesian marine sponge Callyspongia aerizusa. Bioorg. Med. Chem., 2010, 18(14), 4947-4956.
[http://dx.doi.org/10.1016/j.bmc.2010.06.012] [PMID: 20599387]
[52]
Type, I. Callyaerin G, a new cytotoxic cyclic peptide from the marine sponge Callyspongia aerizusa. ARKIVOC, 2008, 12, 164.
[53]
Zhang, S.; De Leon Rodriguez, L.M.; Leung, I.K.H.; Cook, G.M.; Harris, P.W.R.; Brimble, M.A. Total Synthesis and conformational study of callyaerin A: Anti-tubercular cyclic peptide bearing a rare rigidifying (Z)-2,3- Diaminoacrylamide Moiety. Angew. Chem. Int. Ed., 2018, 57(14), 3631-3635.
[http://dx.doi.org/10.1002/anie.201712792] [PMID: 29345033]
[54]
Liu, Q.; Liu, Z.; Sun, C.; Shao, M.; Ma, J.; Wei, X.; Zhang, T.; Li, W.; Ju, J. Discovery and biosynthesis of atrovimycin, an antitubercular and antifungal cyclodepsipeptide featuring vicinal-dihydroxylated cinnamic acyl chain. Org. Lett., 2019, 21(8), 2634-2638.
[http://dx.doi.org/10.1021/acs.orglett.9b00618] [PMID: 30958008]
[55]
Khalil, Z.G.; Salim, A.A.; Lacey, E.; Blumenthal, A.; Capon, R.J. Wollamides: Antimycobacterial cyclic hexapeptides from an Australian soil Streptomyces. Org. Lett., 2014, 16(19), 5120-5123.
[http://dx.doi.org/10.1021/ol502472c] [PMID: 25229313]
[56]
Asfaw, H.; Laqua, K.; Walkowska, A.M.; Cunningham, F.; Martinez-Martinez, M.S.; Cuevas-Zurita, J.C.; Ballell-Pages, L.; Imming, P. Design, synthesis and structure-activity relationship study of wollamide B; a new potential anti TB agent. PLoS One, 2017, 12(4), e0176088.
[http://dx.doi.org/10.1371/journal.pone.0176088] [PMID: 28423019]
[57]
Tsutsumi, L.S.; Tan, G.T.; Sun, D. Solid-phase synthesis of cyclic hexapeptides wollamides A, B and desotamide B. Tetrahedron Lett., 2017, 58(27), 2675-2680.
[http://dx.doi.org/10.1016/j.tetlet.2017.05.084] [PMID: 29129945]
[58]
Asfaw, H.; Wetzlar, T.; Martinez-Martinez, M.S.; Imming, P. An efficient synthetic route for preparation of antimycobacterial wollamides and evaluation of their in vitro and in vivo efficacy. Bioorg. Med. Chem. Lett., 2018, 28(17), 2899-2905.
[http://dx.doi.org/10.1016/j.bmcl.2018.07.021] [PMID: 30031620]
[59]
Tsutsumi, L.S.; Elmore, J.M.; Dang, U.T.; Wallace, M.J.; Marreddy, R.; Lee, R.B.; Tan, G.T.; Hurdle, J.G.; Lee, R.E.; Sun, D. Solid-phase synthesis and antibacterial activity of cyclohexapeptide wollamide B analogs. ACS Comb. Sci., 2018, 20(3), 172-185.
[http://dx.doi.org/10.1021/acscombsci.7b00189] [PMID: 29431987]
[60]
Zhang, S.; Kavianinia, I.; Brimble, M.A. Naturally occurring antitubercular cyclic peptides. Tetrahedron Lett., 2019, 60(50), 151339.
[http://dx.doi.org/10.1016/j.tetlet.2019.151339]

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