Insights into the biosynthesis of duramycin

Applied and Environmental Microbiology

Volumn 83, Issue 3, 2017, Pages

  Huo, Liujie ^a   Ökesli, Ayşe ^a   Zhao, Ming ^b   van der Donk, Wilfred A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Antibiotic; Antiviral agents; Biosynthesis; Duramycin; Phosphatidylethanolamine

Indexed keywords

ANTIBIOTICS; ANTIVIRAL AGENTS; BINDING ENERGY; BIOCHEMISTRY; BIOSYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION; MACHINERY; MAMMALS; PEPTIDES;

ANTIMICROBIAL PEPTIDE; BINDING AFFINITIES; BIOLOGICAL TARGETS; BIOSYNTHETIC GENE CLUSTER; DURAMYCIN; HETEROLOGOUS EXPRESSION; PHOSPHATIDYLETHANOLAMINE; SUBSTRATE RECOGNITION;

AMINO ACIDS;

AMINO ACID; ANTIBIOTICS; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOACTIVITY; CELLS AND CELL COMPONENTS; CHEMICAL BINDING; DRUG; GENOME; LIPID; MACHINERY; MAMMAL; PEPTIDE; PROBE;

ESCHERICHIA COLI; MAMMALIA; STREPTOMYCES CINNAMONEUS;

BACTERIAL PROTEIN; BACTERIOCIN; DURAMYCIN C; LANCOVUTIDE; PEPTIDE;

BACTERIAL GENOME; BIOSYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; STREPTOMYCES; TRANSGENIC ORGANISM;

BACTERIAL PROTEINS; BACTERIOCINS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; ORGANISMS, GENETICALLY MODIFIED; PEPTIDES; STREPTOMYCES;

EID: 85010187567     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02698-16     Document Type: Article

References (47)

1. Chatterjee C, Paul M, Xie L, van der Donk WA. 2005. Biosynthesis and mode of action of lantibiotics. Chem Rev 105:633-684. https://doi.org/10.1021/cr030105v
2. Willey JM, van der Donk WA. 2007. Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61:477-501. https://doi.org/10.1146/annurev.micro.61.080706.093501
3. Bierbaum G, Sahl HG. 2009. Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 10:2-18. https://doi.org/10.2174/138920109787048616
4. Cotter PD, Hill C, Ross RP. 2005. Bacterial lantibiotics: strategies to improve therapeutic potential. Curr Protein Pept Sci 6:61-75. https://doi.org/10.2174/1389203053027584
5. Kondo S, Sezaki M, Shimura M, Sato K, Hara T. 1964. Leucopeptin, a new peptide antibiotic. J Antibiot 17:262-263
6. Widdick DA, Dodd HM, Barraille P, White J, Stein TH, Chater KF, Gasson MJ, Bibb MJ. 2003. Cloning and engineering of the cinnamycin biosynthetic gene cluster from Streptomyces cinnamoneus cinnamoneus DSM 40005 Proc Natl Acad Sci U S A 100:4316-4321. https://doi.org/10.1073/pnas.0230516100
7. Wakamiya T, Fukase K, Naruse N, Konishi M, Shiba T. 1988. Lanthiopep-tin, a new peptide effective against herpes simplex virus: structural determination and comparison with Ro 09-0198, an immunopotentiating peptide. Tetrahedron Lett 29:4771-4772. https://doi.org/10.1016/S0040-4039(00)80604-8
8. Fredenhagen A, Fendrich G, Marki F, Marki W, Gruner J, Raschdorf F, Peter HH. 1990. Duramycins B and C, two new lanthionine containing antibiotics as inhibitors of phospholipase A2. Structural revision of duramycin and cinnamycin. J Antibiot 43:1403-1412
9. Hayashi F, Nagashima K, Terui Y, Kawamura Y, Matsumoto K, Itazaki H. 1990. The structure of PA48009: the revised structure of duramycin. J Antibiot 43:1421-1430. https://doi.org/10.7164/antibiotics.43.1421
10. Kessler H, Steuernagel S, Will M, Jung G, Kellner R, Gillessen D, Kamiyama T. 1988. The structure of the polycyclic nonadecapeptide Ro 09-0198. Helv Chim Acta 71:1924-1929. https://doi.org/10.1002/hlca.19880710811
11. Kodani S, Komaki H, Ishimura S, Hemmi H, Ohnishi-Kameyama M. 2016. Isolation and structure determination of a new lantibiotic cinnamycin B from Actinomadura atramentaria based on genome mining. J Ind Microbiol Biotechnol 43:1159-1165. https://doi.org/10.1007/s10295-016-1788-9
12. Lindenfelser LA, Pridham TG, Shotwell OL, Stodola FH. 1957. Antibiotics against plant disease. IV. Activity of duramycin against selected microorganisms. Antibiot Annu 5:241-247
13. Märki F, Hanni E, Fredenhagen A, van Oostrum J. 1991. Mode of action of the lanthionine-containing peptide antibiotics duramycin, duramycin B and C, and cinnamycin as indirect inhibitors of phospholipase A2. Biochem Pharmacol 42:2027-2035. https://doi.org/10.1016/0006-2952(91)90604-4
14. Zimmermann N, Freund S, Fredenhagen A, Jung G. 1993. Solution structures of the lantibiotics duramycin B and C Eur J Biochem 216: 419-428
15. Seelig J. 2004. Thermodynamics of lipid-peptide interactions. Biochim Biophys Acta 1666:40-50. https://doi.org/10.1016/j.bbamem.2004.08 .004
16. Hosoda K, Ohya M, Kohno T, Maeda T, Endo S, Wakamatsu K. 1996. Structure determination of an immunopotentiator peptide, cinnamycin, complexed with lysophosphatidylethanolamine by 1H-NMR. J Biochem 119:226-230. https://doi.org/10.1093/oxfordjournals.jbchem.a021226
17. Oliynyk I, Varelogianni G, Roomans GM, Johannesson M. 2010. Effect of duramycin on chloride transport and intracellular calcium concentration in cystic fibrosis and non-cystic fibrosis epithelia. APMIS 118:982-990. https://doi.org/10.1111/j.1600-0463.2010.02680.x
18. Grasemann H, Stehling F, Brunar H, Widmann R, Laliberte TW, Molina L, Doring G, Ratjen F. 2007. Inhalation of Moli1901 in patients with cystic fibrosis. Chest 131:1461-1466. https://doi.org/10.1378/chest.06-2085
19. Jones AM, Helm JM. 2009. Emerging treatments in cystic fibrosis. Drugs 69:1903-1910. https://doi.org/10.2165/11318500-000000000-00000
20. Richard AS, Zhang A, Park SJ, Farzan M, Zong M, Choe H. 2015. Virionassociated phosphatidylethanolamine promotes TIM1-mediated infection by Ebola, dengue, and West Nile viruses. Proc Natl Acad Sci U S A 112:14682-14687. https://doi.org/10.1073/pnas.1508095112
21. Rouser G, Yamamoto A, Kritchevsky G. 1971. Cellular membranes. Structure and regulation of lipid class composition species differences, changes with age, and variations in some pathological states. Arch Intern Med 127:1105-1121
22. Spector AA, Yorek MA. 1985. Membrane lipid composition and cellular function. J Lipid Res 26:1015-1035
23. Zhao M. 2011. Lantibiotics as probes for phosphatidylethanolamine. Amino Acids 41:1071-1079. https://doi.org/10.1007/s00726-009-0386-9
24. Zhao M, Li Z, Bugenhagen S. 2008. 99mTc-labeled duramycin as a novel phosphatidylethanolamine-binding molecular probe. J Nucl Med 49: 1345-1352. https://doi.org/10.2967/jnumed.107.048603
25. Ökesli A, Cooper LE, Fogle EJ, van der Donk WA. 2011. Nine posttranslational modifications during the biosynthesis of cinnamycin. J Am Chem Soc 133:13753-13760. https://doi.org/10.1021/ja205783f
26. Håvarstein LS, Diep DB, Nes IF. 1995. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol 16:229-240. https://doi.org/10.1111/j.1365-2958.1995.tb02295.x
27. Carlos JL, Paetzel M, Brubaker G, Karla A, Ashwell CM, Lively MO, Cao G, Bullinger P, Dalbey RE. 2000. The role of the membrane-spanning domain of type I signal peptidases in substrate cleavage site selection. J Biol Chem 275:38813-38822. https://doi.org/10.1074/jbc.M007093200
28. Caetano T, Krawczyk JM, Mosker E, Süssmuth RD, Mendo S. 2011. Heterologous expression, biosynthesis, and mutagenesis of type II lantibiotics from Bacillus licheniformis in Escherichia coli. Chem Biol 18: 90-100. https://doi.org/10.1016/j.chembiol.2010.11.010
29. Nagao J, Harada Y, Shioya K, Aso Y, Zendo T, Nakayama J, Sonomoto K. 2005. Lanthionine introduction into nukacin ISK-1 prepeptide by coexpression with modification enzyme NukM in Escherichia coli. Biochem Biophys Res Commun 336:507-513. https://doi.org/10.1016/j.bbrc.2005.08.125
30. Shi Y, Yang X, Garg N, van der Donk WA. 2011. Production of lantipeptides in Escherichia coli. J Am Chem Soc 133:2338-2341. https://doi.org/10.1021/ja109044r
31. Garg N, Tang W, Goto Y, Nair SK, van der Donk WA. 2012. Lantibiotics from Geobacillus thermodenitrificans. Proc Natl Acad Sci U S A 109: 5241-5246. https://doi.org/10.1073/pnas.1116815109
32. Tang W, van der Donk WA. 2013. The sequence of the enterococcal cytolysin imparts unusual lanthionine stereochemistry. Nat Chem Biol 9:157-159. https://doi.org/10.1038/nchembio.1162
33. Lin Y, Teng K, Huan L, Zhong J. 2011. Dissection of the bridging pattern of bovicin HJ50, a lantibiotic containing a characteristic disulfide bridge. Microbiol Res 166:146-154. https://doi.org/10.1016/j.micres.2010.05.001
34. Wang J, Ma H, Ge X, Zhang J, Teng K, Sun Z, Zhong J. 2014. Bovicin HJ50-like lantibiotics, a novel subgroup of lantibiotics featured by an indispensable disulfide bridge. PLoS One 9:e97121. https://doi.org/10.1371/journal.pone.0097121
35. Gomi T, Fujioka M. 1982. Inactivation of rat-liver S-adenosylhomocysteinase by iodoacetamide. Biochemistry 21:4171-4176. https://doi.org/10.1021/bi00260a039
36. Velásquez JE, Zhang X, van der Donk WA. 2011. Biosynthesis of the antimicrobial peptide epilancin 15X and its unusual N-terminal lactate moiety. Chem Biol 18:857-867. https://doi.org/10.1016/j.chembiol .2011.05.007
37. Zhao X, van der Donk WA. 2016. Structural characterization and bioactivity analysis of the two-component lantibiotic Flv system from a ruminant bacterium. Cell Chem Biol 23:246-256. https://doi.org/10.1016/j.chembiol.2015.11.014
38. Bindman NA, van der Donk WA. 2013. A general method for fluorescent labeling of the N-termini of lanthipeptides and its application to visualize their cellular localization. J Am Chem Soc 135:10362-10371. https://doi.org/10.1021/ja4010706
39. Majchrzykiewicz JA, Lubelski J, Moll GN, Kuipers A, Bijlsma JJ, Kuipers OP, Rink R. 2010. Production of a class II two-component lantibiotic of Streptococcus pneumoniae using the class I nisin synthetic machinery and leader sequence. Antimicrob Agents Chemother 54:1498-1505. https://doi.org/10.1128/AAC.00883-09
40. Shi Y, Bueno A, van der Donk WA. 2012. Heterologous production of the lantibiotic Ala(0)actagardine in Escherichia coli. Chem Commun (Cambridge) 48:10966-10968. https://doi.org/10.1039/c2cc36336d
41. Rink R, Arkema-Meter A, Baudoin I, Post E, Kuipers A, Nelemans SA, Akanbi MH, Moll GN. 2010. To protect peptide pharmaceuticals against peptidases. J Pharmacol Toxicol Methods 61:210-218. https://doi.org/10.1016/j.vascn.2010.02.010
42. Machaidze G, Seelig J. 2003. Specific binding of cinnamycin (Ro 09-0198) to phosphatidylethanolamine. Comparison between micellar and membrane environments. Biochemistry 42:12570-12576
43. Iwamoto K, Hayakawa T, Murate M, Makino A, Ito K, Fujisawa T, Kobayashi T. 2007. Curvature-dependent recognition of ethanolamine phospholipids by duramycin and cinnamycin. Biophys J 93:1608-1619. https://doi.org/10.1529/biophysj.106.101584
44. Stenflo J, Holme E, Lindstedt S, Chandramouli N, Huang LH, Tam JP, Merrifield RB. 1989. Hydroxylation of aspartic acid in domains homologous to the epidermal growth factor precursor is catalyzed by a 2-oxoglutarate-dependent dioxygenase. Proc Natl Acad Sci U S A 86: 444-447. https://doi.org/10.1073/pnas.86.2.444
45. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, III, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343-345. https://doi.org/10.1038/nmeth.1318
46. Li B, Cooper LE, van der Donk WA. 2009. In vitro studies of lantibiotic biosynthesis. Methods Enzymol 458:533-558. https://doi.org/10.1016/S0076-6879(09)04821-6
47. O'Rourke S, Widdick D, Bibb M. 2016. A novel mechanism of immunity controls the onset of cinnamycin biosynthesis in Streptomyces cinnamoneus DSM 40646. J Ind Microbiol Biotechnol https://doi.org/10.1007/s10295-016-1869-9