doi: 10.15389/agrobiology.2019.2.199eng
UDC: 619+61]:615.28
Acknowledgements:
Supported financially by Russian Science Foundation (Agreement No. 15-16-00019)
PRODUCTION OF AVERMECTINS: BIOTECHNOLOGIES
AND ORGANIC SYNTHESIS (review)
M.Kh. Dzhafarov, F.I. Vasilevich, M.N. Mirzaev
Skryabin Moscow State Academy of Veterinary Medicine and Biotechnology, 23, ul. Akademika K.I. Skryabina, Moscow, 109472 Russia, e-mail mxd123@mail.ru (✉ corresponding author), niacid@yandex.ru;rector@mgavm.ru
ORCID:
Dzhafarov M.Kh. orcid.org/0000-0001-6170-4165
Mirzaev M.N. orcid.org/0000-0002-7093-1711
Vasilevich F.I. orcid.org/0000-0003-0786-5317
Received November 22, 2018
The proposed review analyzes the results of research on various aspects of improving the technology of obtaining avermectins, the 16-membered macrocyclic lactones which have a wide spectrum of antiparasitic action with a high therapeutic index and harmlessness for mammals (W.C. Campbell, 2012). According to published data, the unique ability of avermectins to suppress the development of insects, nematodes and ticks is associated with the ability to block the transmission of nerve impulses in the neuromuscular synapse. The essence of this mechanism of action, leading to paralysis and death of parasites, is to stimulate the release of chlorine ions, depolarization of the cell membrane and pathological disorders of its functions (A.J. Wolstenholme et al., 2016). Of the known 8 components (A1a, A1b, A2a, A2b, B1a, B1b, B2a and B2b) of the avermectin complex produced by the microorganism Streptomyces avermitilis, the avermectin B1 is the most active against parasite pathogens (S. Omura, 2002; W.C. Campbell, 2012). Therefore, the main studies on the production of avermectins are associated with the selection of highly productive strains which predominantly synthesize avermectins B1 (S.S. Ki et al., 2005; H. Gao et al., 2010; W. Liu et al., 2015; L. Meng et al., 2016), and the preparation of semi-synthetic analogs of avermectins B1 with improved physicochemical and pharmacological properties (J. Vercruysse et al., 2001; A. Awasthi et al., 2012). Attempts to develop a technology for the complete chemical synthesis of avermectins have not yet yielded significant results due to the low yield of the target product and the complexity of the synthesis scheme (S. Yamashita et al., 2016). Considerable attention has been paid to the biochemical aspects of the diversity of 16-membered macrocyclic lactones and their producers, as well as to semisynthetic analogues, and prospects for searching for new highly efficient and environmentally friendly semisynthetic analogues of avermectin B1 have been defined. Main streams of researches on genetics, biochemistry and physiology of the producer of avermectins, ways of regulated culture of S. avermitilis strains and biosynthesis of required components of avermectin complex are discussed (S. Kitani et al., 2009; J. Guo et al., 2018). The data on the problem of emerging resistance in some species of parasites to long-used avermectin-containing drugs are analyzed. This phenomenon is shown to have a multifactor nature, including mutation of genes determining GluCl subunits and increased P-glycoprotein expression (J.H. Gill et al, 1998; R.K.Prichard, 2007; F.D. Guerrero et al., 2012; P.C. Pohl et al., 2014; P. Godoy et al, 2016). For the successful control of nematodes, insects and mites of agricultural, sanitary and medical importance, it seems appropriate to create drugs based on natural avermectins and their new semi-synthetic derivatives, for example, 5-O-succinylavermectin B1 and C2017 compounds.
Keywords: avermectins, milbemycins, nemadectins, doramectin, abamectin, moxidectin, ivermectin, moxidectin, milbemycin oxime, 5-O-succinylavermectin B1, compound C2017, avermectin oximes, Streptomyces avermitilis, organic synthesis, antiparasitic drugs, nematicides, insectoacaricides.
REFERENCES
- Macrolide antibiotics. Chemistry, biology and practice. 2nd ed. S. Omura (ed.). Elsevier Science, NY, 2002.
- Campbell W.C. History of avermectin and ivermectin, with notes on the history of other macrocyclic lactone antiparasitic agents. Curr. Pharm. Biotechnol., 2012, 13(6): 853-865 CrossRef
- Omura S. Ivermectin: 25 years and still going strong. Int. J. Antimicrob. Agents, 2008, 31(2): 91-98 CrossRef
- Crump A., Omura S. Ivermectin, ‘Wonder drug’ from Japan: the human use perspective. Proc. Jpn. Acad., Ser. B, 2011, 87(2): 13-28 CrossRef
- Goodman and Gilman’s the pharmacological basis of therapeutics. 13th ed. L. Brunton, R. Hilal-Dandan, B.C. Knollman (eds.). McGraw Hill Medical, NY, 2018.
- Safiullin R.T. Rossiiskii veterinarnyi zhurnal, 2006, 2: 6-8 (in Russ.).
- Dolzhenko T.V. Agrokhimiya, 2017, 4: 34-40 (in Russ.).
- Kitani S., Miyamoto K.T., Takamatsu S., Herawati E., Iguchi H., Nishitomi K., Uchida M., Nagamitsu T., Omura S., Ikeda H., Nihira T. Avenolide, a Streptomyces hormone controlling antibiotic production in Streptomyces avermitilis. Proc. Natl. Acad. Sci. USA, 2011, 108: 16410-16415 CrossRef
- Corey E.J., Czako B., Kurti L. Molecules and medicine. Wiley-VCH Verlag, Weinheim, 2007.
- Macrocyclic lactones in antiparasitic therapy. J. Vercruysse, R.S. Rew (eds.). Wallingford, CABI Publishing, NY, 2002.
- Lynagh T., Lynch J.W. Molecular mechanisms of Cys-loop ion channel receptor modulation by ivermectin. Front. Mol. Neurosci., 2012, 5: 60 CrossRef
- Chen I.S., Kubo Y. Ivermectin and its target molecules: shared and unique modulation mechanisms of ion channels and receptors by ivermectin. J. Physiol., 2018, 596(10): 1833-1845 CrossRef
- Chen I.S., Tateyama M., Fukata Y., Uesugi M., Kubo Y. Ivermectin activates GIRK channels in a PIP2-dependent, Gβγ-independent manner and an amino acid residue at the slide helix governs the activation. J. Physiol., 2017, 595(17): 5895-5912 CrossRef
- Hashimoto H., Messerli S.M., Sudo T., Maruta H. Ivermectin inactivates the kinase PAK1 and blocks the PAK1-dependent growth of human ovarian cancer and NF2 tumor cell lines. Drug Discov. Ther., 2009, 3(6): 243-246.
- Gallardo F., Mariamé B., Gence R., Tilkin-Mariamé A.F. Macrocyclic lactones inhibit nasopharyngeal carcinoma cells proliferation through PAK1 inhibition and reduce in vivo tumor growth. Drug Des. Devel. Ther., 2018, 12: 2805-2814 CrossRef
- Melotti A., Mas C., Kuciak M., Lorente-Trigos A., Borges I., Altaba A.R. The river blindness drug Ivermectin and related macrocyclic lactones inhibit WNT-TCF pathway responses in human cancer. EMBO Molecular Medicine, 2014, 6(10): 1263-1278 CrossRef
- Drinyaev V.A., Mosin V.A., Kruglyak E.B., Novik T.S., Sterlina T.S., Ermakova N.V., Kublik L.N., Levitman M.Kh., Shaposhnikova V.V., Korystov Y.N. Antitumor effect of avermectins. Eur. J. Pharmacol., 2004, 501(1-3): 19-23 CrossRef
- Kwon Y.J., Petrie K., Leibovitch B.A., Zeng L., Mezei M., Howell L., Gil V., Christova R., Bansal N., Yang S., Sharma R., Ariztia E.V., Frankum J., Brough R., Sbirkov Y., Ashworth A., Lord C.J., Zelent A., Farias E., Zhou M.M., Waxman S. Selective inhibition of SIN3 corepressor with avermectins as a novel therapeutic strategy in triple-negative breast cancer. Mol. Cancer Ther., 2015, 14(8): 1824-1836 CrossRef
- Juarez M., Schcolnik-Cabrera A., Dueñas-Gonzalez A. The multitargeted drug ivermectin: from an antiparasitic agent to a repositioned cancer drug. Am. J. Cancer. Res., 2018, 8(2): 317-331 (https://www.ncbi.nlm.nih.gov/pubmed/29511601).
- Mastrangelo E., Pezzullo M., De Burghgraeve T., Kaptein S., Pastorino B., Dallmeier K., de Lamballerie X., Neyts J., Hanson A. M., Frick D.N., Bolognesi M., Milani M. Ivermectin is a potent inhibitor of flavivirus replication specifically targeting NS3 helicase activity: new prospects for an old drug. J. Antimicrob. Chemother., 2012, 67(8): 1884-1894 CrossRef
- Kobylinski K.C., Foy B.D., Richardson J.H. Ivermectin inhibits the sporogony of Plasmodium falciparum in Anopheles gambiae. Malaria Journal, 2012, 11: 381 CrossRef
- Lim L.E., Vilchèze C., Ng C., Jacobs W.R. Jr., Ramón-García S., Thompson C.J. Anthelmintic avermectins kill M. tuberculosis, including multidrug resistant clinical strains. Antimicrob. Agents Chemother., 2013, 57(2): 1040-1046 CrossRef
- Khoja S., Huynh N., Warnecke A.M.P., Asatryan L., Jakowec M.W., Davies D.L. Preclinical evaluation of avermectins as novel therapeutic agents for alcohol use disorders. Psychopharmacology (Berl.), 2018, 235(6): 1697-1709 CrossRef
- Zabala A., Vazquez-Villoldo N., Rissiek B., Gejo J., Martin A., Palomino A., Perez-Samartín A., Pulagam K.R., Lukowiak M., Capetillo-Zarate E., Llop J., Magnus T., Koch-Nolte F., Rassendren F., Matute C., Domercq M. P2X4 receptor controls microglia activation and favors remyelination in autoimmune encephalitis EMBO Mol. Med., 2018, 10(8): e8743 CrossRef
- Di Virgilio F., Sarti A.C. Microglia P2X4 receptors as pharmacological targets for demyelinating diseases. EMBO Mol. Med., 2018, 10(8): e9369 CrossRef
- Davies D.L., Bortolato M., Finn D.A., Ramaker M.J., Barak S., Ron D., Liang J., Olsen R.W. Recent advances in the discovery and preclinical testing of novel compounds for the prevention and/or treatment of alcohol use disorders. Alcohol Clin. Exp. Res., 2013, 37(1): 8-15 CrossRef
- Pasqualetto G., Brancale A., Young M.T. The Molecular determinants of small-molecule ligand binding at P2X receptors. Front. Pharmacol., 2018, 9: 58 CrossRef
- Van Voorhis W.C. Profile of William C. Campbell, Satoshi Omura, and Youyou Tu, 2015 Nobel Laureates in Physiology or Medicine. Proc. Natl. Acad. Sci. USA, 2015, 112(52): 15773-15776 CrossRef
- Wang S.-Y., Bo Y.-H., Zhou X., Chen J.H., Li W.J., Liang J.P., Xiao G.Q., Wang Y.C., Liu J., Hu W., Jiang B.L. Significance of heavy-ion beam irradiation-induced avermectin B1a production by engineered Streptomyces avermitilis. BioMed. Research. Int., 2017, 2017: 5373262 CrossRef
- Awasthi A., Razzak M., Al-Kassas R., Harvey J., Garg S. An overview on chemical derivatization and stability aspects of selected avermectin derivatives. Chem. Pharm. Bull., 2012, 60(8): 931-944 CrossRef
- Cummings M., Breitling R., Takano E. Steps towards the synthetic biology of polyketide biosynthesis. FEMS Microbiol. Lett., 2014, 351: 116-125 CrossRef
- Zhuo Y., Zhang T., Wang Q., Cruz-Morales P., Zhang B., Liu M., Barona-Gómez F., Zhang L. Synthetic biology of avermectin for production improvement and structure diversification. Biotechnol. J., 2014, 9(3): 316-325 CrossRef
- Thuan N.H., Pandey R.P., Sohng J.K. Recent advances in biochemistry and biotechnological synthesis of avermectins and their derivatives. Appl. Microbiol. Biotechnol., 2014, 98(18): 7747-7759 CrossRef
- Alper H.S., Avalos J.L. Metabolic pathway engineering. Synth. Syst. Biotechnol., 2018, 3(1): 1-2 CrossRef
- Brady P.B., Oda S., Yamamoto H. Stereodivergent approach to the avermectins based on “Super Silyl” directed aldol reactions. Org. Lett., 2014, 16(15): 3864-3867 CrossRef
- Hirama M. Total synthesis and related studies of large, strained, and bioactive natural products. Proc. Jpn. Acad. Ser. B. Phys. Biol. Sci., 2016, 92(8): 290-329 CrossRef
- Yamashita S., Hayashi D., Nakano A., Hayashi Y., Hirama M. Total synthesis of avermectin B1a revisited. J. Antibiot. (Tokyo), 2016, 69(1): 31-50 CrossRef
- Pitterna T., Cassayre J. Hüter O.F., Jung P.M., Maienfisch P., Kessabi F.M., Quaranta L., Tobler H. New ventures in the chemistry of avermectins. Bioorg. Med. Chem., 2009, 17(12): 4085-4095 CrossRef
- Bennett C.S., Galan M.C. Methods for 2-deoxyglycoside synthesis. Chem. Rev., 2018, 118(17): 7931-7985 CrossRef
- Kim S.B., Goodfellow M. Streptomyces avermitilis sp. nov., nom. rev., a taxonomic home for the avermectin-producing streptomycetes. Int. J. Syst. Evol. Microbiol., 2002, 52(Pt 6): 2011-2014 CrossRef
- Wu L., Sun Q., Sugawara H., Yang S., Zhou Y., McCluskey K., Vasilenko A., Suzuki K., Ohkuma M., Lee Y., Robert V., Ingsriswang S., Guissart F., Philippe D., Ma J. Global catalogue of microorganisms (gcm): a comprehensive database and information retrieval, analysis, and visualization system for microbial resources. BMC Genomics, 2013, 14: 933 CrossRef
- Chermenskii D.N., Adanin V.A., Drinyaev V.A., Kovalev V.N., Golovleva L.A. Prikladnaya biokhimiya i mikrobiologiya, 1991, 6: 838-844 (in Russ.).
- Drinyaev V.A., Sterlina T.S., Berezkina N.E., Mosin V.A., Kruglyak E.B., Esipov S.E., Kobrin M.B., Yurkiv V.A. Biotekhnologiya, 1993, 11-12: 21-25 (in Russ.).
- Ki S.S., Jeong Y.-S., Kim P.-H., Chun G.-T. Effects of dissolved oxygen level on avermectin B1a production by Streptomyces avermitilis in computer-controlled bioreactor cultures. J. Microbiol. Biotechnol., 2006, 16(11): 1690-1698.
- Gao H. Liu M., Zhou X., Liu J., Zhuo Y., Gou Z., Xu B., Zhang W., Liu X., Luo A., Zheng C., Chen X., Zhang L. Identification of avermectin-high-producing strains by high throughput screening methods. Appl. Microbiol. Biotechnol., 2010, 85(4): 219-1225 CrossRef
- Chen J., Liu M., Liu X., Miao J., Fu C., Gao H., Müller R., Zhang Q., Zhang L. Interrogation of Streptomyces avermitilis for efficient production of avermectins. Synth. Syst. Biotechnol., 2016, 1(1): 7-16 CrossRef
- Meng L., Xiong Z., Chu J., Wang Y. Enhanced production of avermectin by deletion of type III polyketide synthases biosynthetic cluster rpp in Streptomyces avermitilis. Lett. Appl. Microbiol., 2016, 63(5): 384-390 CrossRef
- Drinyaev V.A., Sterlina T.S., Berezkina N.E., Mosin V.A., Kruglyak E.B., Zinov'ev O.A., Yurkiv V.A. Biotekhnologiya, 1994, 12: 16-18 (in Russ.).
- Drinyaev V.A., Sterlina T.e., Berezkina N.E., Mosin V.A., Kruglyak E.B., Zinov'ev O.A., Yurkiv V.A. Biotekhnologiya, 1994, 4: 17-20 (in Russ.).
- Belyavskaya L.A., Kozyritskaya V.E., Valagurova E.V., Iutinskaya G.A. Mikrobiologicheskii zhurnal, 2012, 74(3): 10-15 (in Russ.).
- Adamovich O.T., Kolomiets E.I. Materialy Mezhdunarodnoi nauchno-prakticheskoi konferentsii «Perspektivy i problemy razvitiya biotekhnologii v ramkakh edinogo ekonomicheskogo prostranstva stran sodruzhestva, 25-28 maya 2005 g. Minsk—Naroch'» [Proc. Int. Conf. «Prospects and challenges of biotechnologies within common economic space of Commonwealth countries, May 25-28, 2005 Minsk-Naroch»]. Minsk, 2005: 6-7 (in Russ.).
- Biliavska L., Kozyrits’ka V., Valaghurova H., Iutynska G. Effect of pyruvate and valine on avermectin bіosintesis in Streptomyces avermitilis UCM As-2179. Mikrobiologicheskii zhurnal, 2007, 69(4): 10-17 (in Russ.).
- Mirzaev M.N., Sherstnev V.V., Buyantogtokh Ch. Biotekhnologiya, 2004, 3: 75-77 (in Russ.).
- Kodym A., Afza R. Physical and chemical mutagenesis. Methods Mol. Biol., 2003, 236: 189-204 CrossRef
- Wang L.Y., Huang Z.L., Li G., Zhao H.X., Xing X.H., Sun W.T., Li H.P., Gou Z.X., Bao C.Y. Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma. J. Appl. Microbiol., 2010, 108(3): 851-858 CrossRef
- Savchenkov S.N., Mirzaev M.N., Devrishov D.A. Biotekhnologiya, 1997, 3: 35-38 (in Russ.).
- Ikeda H., Kotaki H., Tanaka H., Omura S. Involvent of glucose catabolism in avermectin production by Streptomyces avermitilis. Antimicrob. Agents Chemother., 1988, 32(2): 282-284.
- Cao P., Hu D., Zhang J., Zhang B., Gao Q. Enhanced avermectin production by rational feeding strategies based on comparative metabolomics. Wei Sheng Wu Xue Bao, 2017, 57(2): 281-292.
- Tian P., Cao P., Hu D., Wang D., Zhang J., Wang L., Zhu Y., Gao Q. Comparative metabolomics reveals the mechanism of avermectin production enhancement by S-adenosylmethionine. J. Ind. Microbiol. Biotechnol., 2017, 44(4-5): 595-604 CrossRef
- Schulman M.D., Valentino D., Streicher S., Ruby C. Streptomyces avermitilis mutants defective in methylation of avermectins. Antimicrob. Agents Chemother., 1987, 31(5): 744-749 CrossRef
- Yin P., Li Y.Y., Zhou J., Wang Y.H., Zhang S.L., Ye B.C., Ge W.F., Xia Y.L. Direct proteomic mapping of Streptomyces avermitilis wild and industrial strain and insights into avermectin production. J. Proteomics, 2013, 79: 1-12 CrossRef
- Mironov V.A., Sergeeva A.B., Voronkova V.V., Danilenko V.N. Antibiotiki i khimioterapiya, 1997, 42(3): 31-36 (in Russ.).
- Mironov V.A., Sergeeva A.V., Gavrilina A.V., Danilenko V.N. Prikladnaya biokhimiya i mikrobiologiya, 2003, 2: 208-212 (in Russ.).
- Yoon Y.J., Kim E.-S., Hwang Y.-S., Choi C.-Y. Avermectin biochemical and molecular basis of its biosynthesis and regulation. Appl. Microbiol. Biotechnol., 2004, 63(6): 626-634 CrossRef
- Davydova E.M., Drinyaev V.A., Kruglyak E.B., Kantere V.M. Biotekhnologiya, 2000, 6: 66-74 (in Russ.).
- Ikeda H., Ishikawa J., Hanamoto A., Shinose M., Kikuchi H., Shiba T., Sakaki Y., Hattori M., Omura S. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol., 2003, 21(5): 526-531 CrossRef
- Ikeda H., Kazuo S.Y., Omura S. Genome mining of the Streptomyces avermitilis genome and development of genome-minimized hosts for heterologous expression of biosynthetic gene clusters. J. Ind. Microbiol. Biotechnol., 2014, 41(2): 233-250 CrossRef
- Fischbach M.A., Walsh C.T. Assembly-line enzymology for polyketide and nonribosomal Peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev., 2006, 106(8): 3468-3496 CrossRef
- Dutta S., Whicher J.R., Hansen D.A., Hale W.A., Chemler J.A., Congdon G.R., Narayan A.R., Håkansson K., Sherman D.H., Smith J.L., Skiniotis G. Structure of a modular polyketide synthase. Nature, 2014, 510(7506): 512-517 CrossRef
- Kwan D.H., Schulz F. The stereochemistry of complex polyketide biosynthesis by modular polyketide synthases. Molecules, 2011, 16(7): 6092-6115 CrossRef
- Bayly C.L., Yadav V.G. Towards precision engineering of canonical polyketide synthase domains: recent advances and future prospects. Molecules, 2017, 22(2): 235 CrossRef
- Zhang W., Liu J. Recent advances in understanding and engineering polyketide synthesis. F1000Research, 2016, 5(F1000 Faculty Rev): 208 CrossRef
- Yuzawa S., Backman T.W.H., Keasling J.D., Katz L. Synthetic biology of polyketide synthases. J. Ind. Microbiol. Biotechnol., 2018, 45(7): 621-633 CrossRef
- Smith J.L., Skiniotis G., Sherman D.H. Architecture of the polyketide synthase module: surprises from electron cryo-microscopy. Curr. Opin. Struct. Biol., 2015, (31): 9-19 CrossRef
- Klaus M., Grininger M. Engineering strategies for rational polyketide synthase design. Nat. Prod. Rep., 2018, 35(10): 1070-1081 CrossRef
- Wang F., Wang Y., Ji J., Zhou Z., Yu J., Zhu H., Su Z., Zhang L., Zheng J. Structural and functional analysis of the loading acyltransferase from avermectin modular polyketide synthase. ACS Chem. Biol., 2015, 10(4): 1017-1025 CrossRef
- Sun P., Zhao Q., Yu F, Zhang H., Wu Z., Wang Y., Wang Y., Zhang Q., Liu W. Spiroketal formation and modification in avermectin biosynthesis involves a dual activity of AveC. J. Am. Chem. Soc., 2013, 135(4): 1540-1548 CrossRef
- Tang M.C., Zou Y., Watanabe K., Walsh C.T., Tang Y. Oxidative cyclization in natural product biosynthesis. Chem. Rev., 2017, 117(8): 5226-5333 CrossRef
- Kim M.S., Cho W.J., Song M.C., Park S.W., Kim K., Kim E., Lee N., Nam S.J., Oh K.H., Yoon Y.J. Engineered biosynthesis of milbemycins in the avermectin high‑producing strain Streptomyces avermitilis. Microbial Cell Factories, 2017, 16: 9 CrossRef
- Nonaka K., Tsukiyama T., Okamoto Y., Sato K., Kumasaka C., Yammoto T., Maruyama F., Yoshikawa H. New milbemycins from Streptomyces hygroscopicus subsp. aureolacrimosus: fermentation, isolation and structure elucidation. J. Antibiot. (Tokyo), 2000, 53(7): 694-704.
- He H., Ye L., Li C., Wang H., Guo X., Wang X., Zhang Y., Xiang W. SbbR/SbbA, an important ArpA/AfsA-like system, regulates milbemycin production in Streptomyces bingchenggensis. Front. Microbiol., 2018, 9: 1064 CrossRef
- van Wezel G.P., McDowall K.J. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat. Prod. Rep., 2011, 28(7): 1311-1333 CrossRef
- Sun D., Wang Q., Chen Z., Li J., Wen Y. An Alternative Factor, s8, controls avermectin production and multiple stress responses in Streptomyces avermitilis. Front. Microbiol., 2017, 8: 736 CrossRef
- McCormick J.R., Flärdh K. Signals and regulators that govern Streptomyces development. FEMS Microbiol. Rev., 2012, 36(1): 206-231 CrossRef
- Kitani S., Ikeda H., Sakamoto T., Noguchi S., Nihira T. Characterization of a regulatory gene, aveR, for the biosynthesis of avermectin in Streptomyces avermitilis. Appl. Microbiol. Biotechnol., 2009, 82(6): 1089-1096 CrossRef
- Guo J., Zhao J., Li L., Chen Z., Wen Y., Li J. The pathway-specific regulator AveR from Streptomyces avermitilis positively regulates avermectin production while it negatively affects oligomycin biosynthesis. Mol. Genet. Genomics, 2010, 283(2): 123-133 CrossRef
- Liu W., Zhang Q., Guo J., Chen Z., Li J., Wen Y. Increasing avermectin production in Streptomyces avermitilis by manipulating the expression of a novel TetR-family regulator and its target gene product. Appl. Environ. Microbiol., 2015, 81(15): 5157-5173 CrossRef
- Guo J., Zhang X., Lu X., Liu W., Chen Z., Li J., Deng L., Wen Y. SAV4189, a MarR-family regulator in Streptomyces avermitilis, activates avermectin biosynthesis. Front. Microbiol., 2018, 9: 1358 CrossRef
- Sun Y., Zhou X., Liu J., Bao K., Zhang G., Tu G., Kieser T., Deng Z. Streptomyces nanchangensis, a producer of the insecticidal polyether antibiotic nanchangmycin and the antiparasitic macrolide meilingmycin, contains multiple polyketide gene clusters. Microbiology, 2002, 148(Pt 2): 361-371 CrossRef
- Yang L.Y., Wang J.D., Zhang J., Xue C.Y., Zhang H., Wang X.J., Xiang W.S. New nemadectin congeners with acaricidal and nematocidal activity from Streptomyces microflavus neau3 Y-3. Bioorg. Med. Chem. Lett., 2013, 23(20): 5710-5713 CrossRef
- Gao C., Wang Y., Chen Y., He B., Zhang R., Xu M., Huang R. Two new avermectin derivatives from the Beibu Gulf gorgonian Anthogorgia caerulea. Chem. Biodivers., 2014, 11(5): 812-818 CrossRef
- Wong F.T., Khosla C. Combinatorial biosynthesis of polyketides – a perspective. Curr. Opin. Chem. Biol., 2012, 16(1-2): 117-123 CrossRef
- Cane D.E. Nature as organic chemist. J. Antibiot. (Tokyo), 2016, 69(7): 473-485 CrossRef
- Blakemore D.C., Castro L., Churcher I., Rees D.C., Thomas A.W., Wilson D.M., Wood A. Organic synthesis provides opportunities to transform drug discovery. Nat. Chem., 2018, 10(4): 383-394 CrossRef
- Zhang J., Yan Y.J., An J., Huang S.X., Wang X.J., Xiang W.S. Designed biosynthesis of 25-methyl and 25-ethyl ivermectin with enhanced insecticidal activity by domain swap of avermectin polyketide synthase. Microbial Cell Factories, 2015, 14: 152 CrossRef
- Zhao X., Wang Y., Wang S., Chen Z., Wen Y., Song Y. Construction of a doramectin producer mutant from an avermectin-overproducing industrial strain of Streptomyces avermitilis. Can. J. Microbiol., 2009, 55(12): 1355-1363 CrossRef
- Deng Q., Zhou L, Luo M., Deng Z., Zhao C. Heterologous expression of avermectins biosynthetic gene cluster by construction of a bacterial artificial chromosome library of the producers. Synth. Syst. Biotechnol., 2017, 2(1): 59-64 CrossRef
- Wang X.J., Zhang J., Wang J.D., Huang S.X., Chen Y.H., Liu C.X., Xiang W.S. Four new doramectin congeners with acaricidal and insecticidal activity from Streptomyces avermitilis NEAU1069. Chem. Biodivers., 2011, 8(11): 2117-2125 CrossRef
- Wang J.B., Pan H.X., Tang G.L. Production of doramectin by rational engineering of the avermectin biosynthetic pathway. Bioorg. Med. Chem. Lett., 2011, 21(11): 3320-3323 CrossRef
- Wolstenholme A.J., Maclean M.J., Coates R., McCoy C.J., Reaves B.J. How do the macrocyclic lactones kill filarial nematode larvae? Invert. Neurosci., 2016, 16(3): 7 CrossRef
- Prichard R., Ménez C., Lespine A. Moxidectin and the avermectins: consanguinity but not identity. Int. J. Parasitol. Drugs Drug Resist., 2012, 2: 134-153 CrossRef
- Mounsey K.E., Walton S.F., Innes A., Cash-Deans S., McCarthy J. In vitro efficacy of moxidectin versus ivermectin against Sarcoptes scabiei. Antimicrob. Agents Chemother., 2017, 61(8): e00381-17 CrossRef
- Raymond V., Sattelle D.B. Novel animal-health drug targets from ligand-gated chloride channels. Nat. Rev. Drug Discov., 2002, 1(6): 427-436 CrossRef
- Wolstenholme A.J., Rogers A.T. Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology, 2005, 131 Suppl: S85-95 CrossRef
- Estrada-Mondragon A., Lynch J.W. Functional characterization of ivermectin binding sites in α1β2γ2L GABA(A) receptors. Front. Mol. Neurosci., 2015, 8: 55 CrossRef
- Wolstenholme A.J. Glutamate-gated chloride channels. J. Biol. Chem., 2012, 287(48): 40232-40238 CrossRef
- Degani-Katzav N., Gortler R., Weissman M., Paas Y. Mutational analysis at intersubunit interfaces of an anionic glutamate receptor reveals a key interaction important for channel gating by ivermectin. Front. Mol. Neurosci., 2017, 10: 92 CrossRef
- Stokes L., Layhadi J.A., Bibic L., Dhuna K., Fountain S.J. P2X4 receptor function in the nervous system and current breakthroughs in pharmacology. Front. Pharmacol., 2017, 8: Article 291 CrossRef
- Godoy P., Che H., Beech R.N., Prichard R.K. Characterisation of P-glycoprotein-9.1 in Haemonchus contortus. Parasites & Vectors, 2016, 9: 52 CrossRef
- Mealey K.L., Bentjen S.A., Gay J.M., Cantor G.H. Ivermectin sensitivity in collies is associated with a deletion mutation of the mdr1 gene. Pharmacogenetics, 2001, 11(8): 727-733 CrossRef
- Xin-Jun Z., Wen-Cai L., Ya-Ning F., Lin H. High γ-aminobutyric acid content, a novel component associated with resistance to abamectin in Tetranychus cinnabarinus (Boisduval). J. Insect. Physiol., 2010, 56(12): 1895-1900 CrossRef
- Chen L.-P., Wang P., Sun Y.-J., Wu Y.-J. Direct interaction of avermectin with epidermal growth factor receptor mediates the penetration resistance in Drosophila larvae. Open Biol., 2016, 6(4): 150231 CrossRef
- Driggers E.M., Hale S.P., Lee J., Terrett N.K. The exploration of macrocycles for drug discovery — an underexploited structural class. Nat. Rev. Drug Discov., 2008, 7(7): 608-624 CrossRef
- Wessjohann L.A., Ruijter E., Garcia-Rivera D., Brandt W. What can a chemist learn from nature’s macrocycles? — A brief conceptual view. Mol. Divers., 2005, 9(1-3): 171-186 CrossRef
- Yudin A.K. Macrocycles: lessons from the distant past, recent developments, and future directions. Chem. Sci., 2015, 6(1): 30-49 CrossRef
- Fisher M.H. Recent advances in avermectin research. Pure App. Chem., 1990, 62(7): 1231-1240 CrossRef
- Dzhafarov M.Kh. Evolution in chemotherapy of human and animal helminthiases (review). Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2013, 4: 26-44 CrossRef
- Chernoburova E.I., Danchenko K.V., Shchetinina M.A., Zharov A.A., Kolobov A.V., Dzhafarov M.Kh., Vasilevich F.I., Zavarzin I.V. Synthesis of 5,4-di-O-succinoylavermectin B1. Russ. Chem. Bull., 2016, 65(12): 2952-2955 CrossRef
- Chernoburova E.I., Polyukhova E.S., Shchetinina M.A., Kolobov A.V., Dzhafarov M.Kh., Vasilevich F.I., Zavarzin I.V. Synthesis of esters of bile acids and avermectin B. Russ. Chem. Bull., 2016, 65(12): 2956-2964 CrossRef
- Chernoburova E.I., Lishchuk V.A., Ovchinnikov K.L., Kolobov A.V., Dzhafarov M.Kh., Vasilevich F.I., Zavarzin I.V. Reaction of 5-O-succinoylavermectin B1 with alkylating agents. Russ. Chem. Bull., 2016, 65(12): 2965-2969 CrossRef
- Blinnikov A.N., Chernoburova E.I., Kolotyrkina N.G. Shchetinina M.A., Lishchuk V.A., Ovchinnikov K.L., Kolobov A.V., Dzhafarov M.Kh., Vasilevich F.I., Zavarzin I.V. Synthesis of ivermectin-4″,5-diyl[bis(N-methylcarbamate)]. Russ. Chem. Bull., 2018, 67(5): 833-835 CrossRef
- Shchetinina M.A., Chernoburova E.I., Kolotyrkina N.G., Dzhafarov M.Kh., Vasilevich F.I., Zavarzin I.V. Synthesis of sodium 5-sulfate-ivermectin and disodium 4,5-disulfate-ivermectin. Russ. Chem. Bull., 2018, 67(5): 836-839 CrossRef
- Zeng X., Tian X., Hong X., Yu Y., Deng Z., Zhao C. Patent CN 103833811 A. Abamectin derivative and preparation method thereof. Appl. 2014. Publ. 2014.
- Li Y., Qin Y., Liu S., Xing R., Yu H., Li K., Li P. Preparation, characterization, and insecticidal activity of avermectin-grafted-carboxymethyl chitosan. Biomed. Res. Int., 2016, 2016: 9805675 CrossRef
- Del Rosso D. Vestnik dermatologii i venerologii, 2016, 2: 21-31 CrossRef (in Russ.).
- Dzhafarov M.Kh., Shemyakova S.A., Mirzaev M.N., Esaulova N.V., Vasilevich F.I. Meditsinskaya parazitologiya i parazitarnye bolezni, 2017, 3: 25-28 (in Russ.).
- Dzhafarov M.Kh., Mirzaeva K.M., Vasilevich F.I., Mirzaev M.N., Mel'nitskaya T.I. Metodicheskie polozheniya po primeneniyu preparata Gemaks (Sumektin) pri strongilyatozakh zheludochno-kishechnogo trakta ovets [Guidelines for the use of drug Gemax (Sumectin) to control strongylotosis of the gastrointestinal tract of sheep]. Moscow, 2018 (in Russ.).
- Mirzaeva K.M., Zemtsova L.K., Mirzaev M.N., Dzhafarov M.Kh., Mel'nitskaya T.I., Yusufov Yu.A. Veterinariya, zootekhniya i biotekhnologiya, 2017, 2: 16-21 (in Russ.).
- Zemtsova L.K., Mirzaev M.N., Dzhafarov M.Kh., Mirzaeva K.M. Veterinariya, zootekhniya i biotekhnologiya, 2017, 3: 73-78 (in Russ.).