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Nucleoside Natural Product Antibiotics Targetting Microbial Cell Wall Biosynthesis

Chapter
Part of the Topics in Medicinal Chemistry book series (TMC, volume 26)

Abstract

The nucleoside antibiotics are a group of natural product antibiotics with activity against Gram-negative bacteria that are based upon the nucleoside uridine, which were first identified in the 1970s, and for which new members have been recently discovered. The nucleoside antibacterials primarily target translocase MraY on the bacterial peptidoglycan biosynthetic pathway, and a second group of nucleoside antifungal natural products target chitin synthase involved in fungal cell wall synthesis. This chapter reviews the structures and structure–activity studies in each group of antibiotics, describes studies on the biosynthesis of each class, and discusses prospects for the development of novel bioactive nucleosides via chemical synthesis and engineered biosynthesis.

Keywords

A-500359A Caprazamycin Capuramycin Chitin synthase Liposidomycin MraY Muraymycin Mureidomycin Napsamycin Nikkomycin Nucleoside antibiotics Pacidamycin Polyoxin Sansanmycin Tunicamycin 

References

  1. 1.
    Fernandes P (2006) Antibacterial discovery and development – the failure of success. Nat Biotechnol 24:1497–1503. doi: 10.1038/nbt1206-1497CrossRefPubMedGoogle Scholar
  2. 2.
    Kimura K, Bugg TDH (2003) Recent advances in antimicrobial nucleoside antibiotics targeting cell wall biosynthesis. Nat Prod Rep 20:252–273. doi: 10.1039/B202149HCrossRefPubMedGoogle Scholar
  3. 3.
    Winn M, Goss RJM, Kimura K, Bugg TDH (2010) Antimicrobial nucleoside antibiotics targeting cell wall assembly: recent advances in structure-function studies and nucleoside biosynthesis. Nat Prod Rep 27:279–304. doi: 10.1039/b816215hCrossRefPubMedGoogle Scholar
  4. 4.
    Wiegmann D, Koppermann S, Wirth M, Niro G, Leyerer K, Ducho C (2016) Muraymycin nucleoside-peptide antibiotics: uridine-derived natural products as lead structures for the development of novel antibacterial agents. Beilstein J Org Chem 12:769–795. doi: 10.3762/bjoc.12.77CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Serpi M, Ferrari V, Pertusati F (2016) Nucleoside derived antibiotics to fight microbial drug resistance: new utilities for an established class of drugs. J Med Chem 59:10343–10382. doi: 10.1021/acs.jmedchem.6b00325CrossRefPubMedGoogle Scholar
  6. 6.
    Ichikawa S (2016) Function-oriented synthesis: how to design simplified analogues of antibacterial nucleoside natural products? Chem Rec 16:1106–1115. doi: 10.1002/tcr.201500247CrossRefPubMedGoogle Scholar
  7. 7.
    Takatsuki A, Arima K, Tamura G (1971) Tunicamycin, a new antibiotic. I. Isolation and characterization of tunicamycin. J Antibiot 24:215–223. doi: 10.7164/antibiotics.24.215CrossRefPubMedGoogle Scholar
  8. 8.
    Heifetz A, Keenan RW, Elbein AD (1979) Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry 18:2186–2192. doi: 10.1021/bi00578a008CrossRefPubMedGoogle Scholar
  9. 9.
    Isono K, Uramoto M, Kusakabe H, Kimura K, Isaki K, Nelson CC, McCloskey JA (1985) Liposidomycins: novel nucleoside antibiotics which inhibit bacterial peptidoglycan synthesis. J Antibiot 38:1617–1621. doi: 10.7164/antibiotics.38.1617CrossRefPubMedGoogle Scholar
  10. 10.
    Isono F, Inukai M, Takahashi S, Haneishi T, Kinoshita T, Kuwano H (1989) Mureidomycins A-D, novel peptidylnucleoside antibiotics with spheroplast forming activity. II. Structural elucidation. J Antibiot 42:667–673. doi: 10.7164/antibiotics.42.667CrossRefPubMedGoogle Scholar
  11. 11.
    Isono F, Inukai M (1991) Mureidomycin A, a new inhibitor of bacterial peptidoglycan synthesis. Antimicrob Agents Chemother 35:234–236. doi: 10.1128/AAC.35.2.234CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Inukai M, Isono F, Takatsuki A (1993) Selective inhibition of the bacterial translocase reaction in peptidoglycan synthesis by mureidomycins. Antimicrob Agents Chemother 37:980–983. doi: 10.1128/AAC.37.5.980CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Bouhss A, Trunkfield AE, Bugg TDH, Mengin-Lecreulx D (2008) The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 32:208–233. doi: 10.1111/j.1574-6976.2007.00089.xCrossRefPubMedGoogle Scholar
  14. 14.
    Liu Y, Breukink E (2016) The membrane steps of bacterial cell wall synthesis as antibiotic targets. Antibiotics (Basel) 5:28. doi: 10.3390/antibiotics5030028CrossRefGoogle Scholar
  15. 15.
    Koppermann S, Ducho C (2016) Natural products at work: structural insights into inhibition of the bacterial membrane protein MraY. Angew Chem Int Ed Engl 55:11722–11724. doi: 10.1002/anie.201606396CrossRefPubMedGoogle Scholar
  16. 16.
    Bouhss A, Mengin-Lecreulx D, Le Beller D, Van Heijenoort J (1999) Topological analysis of the MraY protein catalysing the first membrane step of peptidoglycan synthesis. Mol Microbiol 34:576–585. doi: 10.1046/j.1365-2958.1999.01623.xCrossRefPubMedGoogle Scholar
  17. 17.
    Brandish PE, Burnham MK, Lonsdale JT, Southgate R, Inukai M, Bugg TDH (1996) Slow binding inhibition of phospho-N-acetylmuramyl-pentapeptide-translocase (Escherichia coli) by mureidomycin A. J Biol Chem 271:7609–7614. doi: 10.1074/jbc.271.13.7609CrossRefPubMedGoogle Scholar
  18. 18.
    Bouhss A, Crouvoisier M, Blanot D, Mengin-Lecreulx D (2004) Purification and characterization of the bacterial MraY translocase catalyzing the first membrane step of peptidoglycan biosynthesis. J Biol Chem 279:29974–29980. doi: 10.1074/jbc.M314165200CrossRefPubMedGoogle Scholar
  19. 19.
    Liu Y, Rodrigues JP, Bonvin AM, Zaal EA, Berkers CR, Heger M, Gawarecka K, Swiezewska E, Breukink E, Egmond MR (2016) New insight into the catalytic mechanism of bacterial MraY from enzyme kinetics and docking studies. J Biol Chem 291:15057–15068. doi: 10.1074/jbc.M116.717884CrossRefPubMedGoogle Scholar
  20. 20.
    Al-Dabbagh B, Olatunji S, Crouvoisier M, El Ghachi M, Blanot D, Mengin-Lecreulx D, Bouhss A (2016) Catalytic mechanism of MraY and WecA, two paralogues of the polyprenyl-phosphate N-acetylhexosamine 1-phosphate transferase superfamily. Biochimie 127:249–257. doi: 10.1016/j.biochi.2016.06.005CrossRefPubMedGoogle Scholar
  21. 21.
    Lloyd AJ, Brandish PE, Gilbey AM, Bugg TDH (2004) Phospho-N-acetyl-muramyl-pentapeptide translocase from Escherichia coli: catalytic role of conserved aspartic acid residues. J Bacteriol 186:1747–1757. doi: 10.1128/JB.186.6.1747-1757.2004CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Chung BC, Zhao J, Gillespie RA, Kwon DY, Guan Z, Hong J, Zhou P, Lee SY (2013) Crystal structure of MraY, an essential membrane enzyme for bacterial cell wall synthesis. Science 341:1012–1016. doi: 10.1126/science.1236501CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Brandish PE, Kimura KI, Inukai M, Southgate R, Lonsdale JT, Bugg TDH (1996) Modes of action of tunicamycin, liposidomycin B, and mureidomycin A: inhibition of phospho-N-acetylmuramyl-pentapeptide translocase from Escherichia coli. Antimicrob Agents Chemother 40:1640–1644PubMedPubMedCentralGoogle Scholar
  24. 24.
    Wyszynski FJ, Hesketh AR, Bibb MJ, Davis BG (2010) Dissecting tunicamycin biosynthesis by genome mining: cloning and heterologous expression of a minimal gene cluster. Chem Sci 1:581–589. doi: 10.1039/C0SC00325ECrossRefGoogle Scholar
  25. 25.
    Wyszynski FJ, Lee SS, Yabe T, Wang H, Gomez-Escribano JP, Bibb MJ, Lee SJ, Davies GJ, Davis BG (2012) Biosynthesis of the tunicamycin antibiotics proceeds via unique exo-glycal intermediates. Nat Chem 4:539–546. doi: 10.1038/nchem.1351CrossRefPubMedGoogle Scholar
  26. 26.
    Inukai M, Isono F, Takahashi S, Enokita R, Sakaida Y, Haneishi T (1989) Mureidomycins A-D, novel peptidylnucleoside antibiotics with spheroplast forming activity. I. Taxonomy, fermentation, isolation and physico-chemical properties. J Antibiot 42:662–666. doi: 10.7164/antibiotics.42.662CrossRefPubMedGoogle Scholar
  27. 27.
    Isono F, Katayama T, Inukai M, Haneishi T (1989) Mureidomycins A–D, novel peptidylnucleoside antibiotics with spheroplast forming activity. III. Biological properties. J Antibiot 42:674–679. doi: 10.7164/antibiotics.42.674CrossRefPubMedGoogle Scholar
  28. 28.
    Karwowski JP, Jackson M, Theriault RJ, Chen RH, Barlow GJ, Maus ML (1989) Pacidamycins, a novel series of antibiotics with anti-Pseudomonas aeruginosa activity. I. Taxonomy of the producing organism and fermentation. J Antibiot 42:506–511. doi: 10.7164/antibiotics.42.506CrossRefPubMedGoogle Scholar
  29. 29.
    Chen RH, Buko AM, Whittern DN, McAlpine JB (1989) Pacidamycins, a novel series of antibiotics with anti-Pseudomonas aeruginosa activity. II. Isolation and structural elucidation. J Antibiot 42:512–520. doi: 10.7164/antibiotics.42.512CrossRefPubMedGoogle Scholar
  30. 30.
    Fernandes PB, Swanson RN, Hardy DJ, Hanson CW, Coen L, Rasmussen RR, Chen RH (1989) Pacidamycins, a novel series of antibiotics with anti-Pseudomonas aeruginosa activity. III. Microbiologic profile. J Antibiot 42:521–526. doi: 10.7164/antibiotics.42.521CrossRefPubMedGoogle Scholar
  31. 31.
    Isono F, Sakaida Y, Takahashi S, Kinoshita T, Nakamura T, Inukai M (1993) Mureidomycins E and F, minor components of mureidomycins. J Antibiot 46:1203–1207. doi: 10.7164/antibiotics.46.1203CrossRefPubMedGoogle Scholar
  32. 32.
    Chatterjee S, Nadkarni SR, Vijayakumar EKS, Patel MV, Gangul BN, Fehlhaber H-W, Vertesy L (1994) Napsamycins, new Pseudomonas active antibiotics of the mureidomycin family from Streptomyces sp. HIL Y-82, 11372. J Antibiot 47:595–598. doi: 10.7164/antibiotics.47.595CrossRefPubMedGoogle Scholar
  33. 33.
    Xie Y, Chen R, Si S, Sun CH, Xu HZ (2007) A new nucleosidyl-peptide antibiotic, sansanmycin. J Antibiot 60:158–161. doi: 10.1038/ja.2007.16CrossRefPubMedGoogle Scholar
  34. 34.
    Xie Y, Xu HZ, Si S, Sun CH, Chen R (2008) Sansanmycins B and C, new components of sansanmycins. J Antibiot 61:237–240. doi: 10.1038/ja.2008.34CrossRefPubMedGoogle Scholar
  35. 35.
    Gentle CA, Bugg TDH (1999) Role of the enamide linkage of nucleoside antibiotic mureidomycin A: synthesis and reactivity of enamide-containing analogues. J Chem Soc Perkin Trans 1:1279–1286. doi: 10.1039/A901279FCrossRefGoogle Scholar
  36. 36.
    Gentle CA, Harrison SA, Inukai M, Bugg TDH (1999) Structure-function studies on nucleoside antibiotic mureidomycin A: synthesis of 5’-functionalised uridine models. J Chem Soc Perkin Trans 1:1287–1294. doi: 10.1039/A901287GCrossRefGoogle Scholar
  37. 37.
    Howard NI, Bugg TDH (2003) Synthesis and activity of 5’-uridinyl dipeptide analogues mimicking the amino terminal peptide chain of nucleoside antibiotic mureidomycin A. Bioorg Med Chem 11:3083–3099. doi: 10.1016/S0968-0896(03)00270-0CrossRefPubMedGoogle Scholar
  38. 38.
    Boojamra CG, Lemoine RC, Lee JC, Léger R, Stein KA, Vernier NG, Magon A, Lomovskaya O, Martin PK, Chamberland S, Lee MD, Hecker SJ, Lee VJ (2001) Stereochemical elucidation and total synthesis of dihydropacidamycin D, a semisynthetic pacidamycin. J Am Chem Soc 123:870–874. doi: 10.1021/ja003292cCrossRefPubMedGoogle Scholar
  39. 39.
    Boojamra CG, Lemoine RC, Blais J, Vernier NG, Stein KA, Magon A, Chamberland S, Hecker SJ, Lee VJ (2003) Synthetic dihydropacidamycin antibiotics: a modified spectrum of activity for the pacidamycin class. Bioorg Med Chem Lett 13:3305–3309. doi: 10.1016/S0960-894X(03)00682-6CrossRefPubMedGoogle Scholar
  40. 40.
    Okamoto K, Sakagami M, Feng F, Togame H, Takemoto H, Ichikawa S, Matsuda A (2011) Total synthesis of pacidamycin D by Cu(I)-catalyzed oxy enamide formation. Org Lett 13:5240–5243. doi: 10.1021/ol202124bCrossRefPubMedGoogle Scholar
  41. 41.
    Okamoto K, Sakagami M, Feng F, Takahashi F, Uotani K, Togame H, Takemoto H, Ichikawa S, Matsuda A (2012) Synthesis of pacidamycin analogues via an Ugi-multicomponent reaction. Bioorg Med Chem Lett 22:4810–4815. doi: 10.1016/j.bmcl.2012.05.050CrossRefPubMedGoogle Scholar
  42. 42.
    Rackham EJ, Grüschow S, Ragab AE, Dickens S, Goss RJM (2010) Pacidamycin biosynthesis: identification and heterologous expression of the first uridyl peptide antibiotic gene cluster. ChemBioChem 11:1700–1709. doi: 10.1002/cbic.201000200CrossRefPubMedGoogle Scholar
  43. 43.
    Zhang W, Ostash B, Walsh CT (2010) Identification of the biosynthetic gene cluster for the pacidamycin group of peptidyl nucleoside antibiotics. Proc Natl Acad Sci U S A 107:16828–16833. doi: 10.1073/pnas.1011557107CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Zhang W, Ames BD, Walsh CT (2011) Identification of phenylalanine 3-hydroxylase for meta-tyrosine biosynthesis. Biochemistry 50:5401–5403. doi: 10.1021/bi200733cCrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Lam W-H, Rychli K, Bugg TDH (2008) Identification of a novel β-replacement reaction in the biosynthesis of 2,3-diaminobutyric acid in peptidylnucleoside mureidomycin A. Org Biomol Chem 6:1912–1917. doi: 10.1039/b802585aCrossRefPubMedGoogle Scholar
  46. 46.
    Ragab AE, Grüschow S, Tromans DR, Goss RJM (2011) Biogenesis of the unique 4’,5’-dehydronucleoside of the uridyl peptide antibiotic pacidamycin. J Am Chem Soc 133:15288–15291. doi: 10.1021/ja206163jCrossRefPubMedGoogle Scholar
  47. 47.
    Zhang W, Ntai I, Kelleher NL, Walsh CT (2011) tRNA-dependent peptide bond formation by the transferase PacB in biosynthesis of the pacidamycin group of pentapeptidyl nucleoside antibiotics. Proc Natl Acad Sci U S A 108:12249–12253. doi: 10.1073/pnas.1109539108CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Zhang W, Ntai I, Bolla ML, Malcolmson SJ, Kahne D, Kelleher NL, Walsh CT (2011) Nine enzymes are required for assembly of the pacidamycin group of peptidyl nucleoside antibiotics. J Am Chem Soc 133:5240–5243. doi: 10.1021/ja2011109CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Grüschow S, Rackham EJ, Goss RJM (2011) Diversity in natural product families is governed by more than enzyme promiscuity alone: establishing control of the pacidamycin portfolio. Chem Sci 2:2182–2186. doi: 10.1039/C1SC00378JCrossRefGoogle Scholar
  50. 50.
    Deb Roy A, Grüschow S, Cairns N, Goss RJM (2010) Gene expression enabling synthetic diversification of natural products: chemogenetic generation of pacidamycin analogs. J Am Chem Soc 132:12243–12245. doi: 10.1021/ja1060406CrossRefPubMedGoogle Scholar
  51. 51.
    Shi Y, Jiang Z, Lei X, Zhang N, Cai Q, Li Q, Wang L, Si S, Xie Y, Hong B (2016) Improving the N-terminal diversity of sansanmycin through mutasynthesis. Microb Cell Fact 15:77. doi: 10.1186/s12934-016-0471-1CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Ubukata M, Isono K, Kimura K, Nelson CC, McCloskey JA (1988) The structure of liposidomycin B, an inhibitor of bacterial peptidoglycan synthesis. J Am Chem Soc 110:4416–4417. doi: 10.1021/ja00221a052CrossRefGoogle Scholar
  53. 53.
    Igarashi M, Nakagawa N, Doi N, Hattori S, Naganawa H, Hamada M (2003) Caprazamycin B, a novel anti-tuberculosis antibiotic, from Streptomyces sp. J Antibiot 56:580–583. doi: 10.7164/antibiotics.56.580CrossRefPubMedGoogle Scholar
  54. 54.
    Igarashi M, Takahashi Y, Shitara T, Nakamura H, Naganawa H, Miyake T, Akamatsu Y (2005) Caprazamycins, novel lipo-nucleoside antibiotics, from Streptomyces sp. II. Structure elucidation of caprazamycins. J Antibiot 58:327–337. doi: 10.1038/ja.2005.41CrossRefPubMedGoogle Scholar
  55. 55.
    Dini C, Collette P, Drochon N, Guillot JC, Lemoine G, Mauvais P, Aszodi J (2000) Synthesis of the nucleoside moiety of liposidomycins: elucidation of the pharmacophore of this family of MraY inhibitors. Bioorg Med Chem Lett 10:1839–1843CrossRefGoogle Scholar
  56. 56.
    Dini C, Drochon N, Feteanu S, Guillot JC, Peixoto C, Aszodi J (2001) Synthesis of analogues of the O-β-D-ribofuranosyl nucleoside moiety of liposidomycins. Part 1: contribution of the amino group and the uracil moiety upon the inhibition of MraY. Bioorg Med Chem Lett 11:529–531CrossRefGoogle Scholar
  57. 57.
    Dini C, Didier-Laurent S, Drochon N, Feteanu S, Guillot JC, Monti F, Uridat E, Zhang J, Aszodi J (2002) Synthesis of sub-micromolar inhibitors of MraY by exploring the region originally occupied by the diazepanone ring in the liposidomycin structure. Bioorg Med Chem Lett 12:1209–1213CrossRefGoogle Scholar
  58. 58.
    Fer MJ, Bouhss A, Patrão M, Le Corre L, Pietrancosta N, Amoroso A, Joris B, Mengin-Lecreulx D, Calvet-Vitale S, Gravier-Pelletier C (2015) 5’-Methylene-triazole-substituted-aminoribosyl uridines as MraY inhibitors: synthesis, biological evaluation and molecular modeling. Org Biomol Chem 13:7193–7222. doi: 10.1039/c5ob00707kCrossRefPubMedGoogle Scholar
  59. 59.
    Ichikawa S, Yamaguchi M, Hsuan LS, Kato Y, Matsuda A (2015) Carbacaprazamycins: chemically stable analogues of the caprazamycin nucleoside antibiotics. ACS Infect Dis 1:151–156. doi: 10.1021/id5000376CrossRefPubMedGoogle Scholar
  60. 60.
    Ishizaki Y, Hayashi C, Inoue K, Igarashi M, Takahashi Y, Pujari V, Crick DC, Brennan PJ, Nomoto A (2013) Inhibition of the first step in synthesis of the mycobacterial cell wall core, catalyzed by the GlcNAc-1-phosphate transferase WecA, by the novel caprazamycin derivative CPZEN-45. J Biol Chem 288:30309–30319. doi: 10.1074/jbc.M113.492173CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Kaysser L, Lutsch L, Siebenberg S, Wemakor E, Kammerer B, Gust B (2009) Identification and manipulation of the caprazamycin gene cluster lead to new simplified liponucleoside antibiotics and give insights into the biosynthetic pathway. J Biol Chem 284:14987–14996. doi: 10.1074/jbc.M901258200CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Kaysser L, Wemakor E, Siebenberg S, Salas JA, Sohng JK, Kammerer B, Gust B (2010) Formation and attachment of the deoxysugar moiety and assembly of the gene cluster for caprazamycin biosynthesis. Appl Environ Microbiol 76:4008–4018. doi: 10.1128/AEM.02740-09CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Yang Z, Chi X, Funabashi M, Baba S, Nonaka K, Pahari P, Unrine J, Jacobsen JM, Elliott GI, Rohr J, Van Lanen SG (2011) Characterization of LipL as a non-heme, Fe(II)-dependent α-ketoglutarate:UMP dioxygenase that generates uridine-5’-aldehyde during A-90289 biosynthesis. J Biol Chem 286:7885–7892. doi: 10.1074/jbc.M110.203562CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Barnard-Britson S, Chi X, Nonaka K, Spork AP, Tibrewal N, Goswami A, Pahari P, Ducho C, Rohr J, Van Lanen SG (2012) Amalgamation of nucleosides and amino acids in antibiotic biosynthesis: discovery of an L-threonine:uridine-5’-aldehyde transaldolase. J Am Chem Soc 134:18514–18517. doi: 10.1021/ja308185qCrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Chi X, Pahari P, Nonaka K, Van Lanen SG (2011) Biosynthetic origin and mechanism of formation of the aminoribosyl moiety of peptidyl nucleoside antibiotics. J Am Chem Soc 133:14452–14459. doi: 10.1021/ja206304kCrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    McDonald LA, Barbieri LR, Carter GT, Lenoy E, Lotvin J, Petersen PJ, Siegel MM, Singh G, Williamson RT (2002) Structures of the muraymycins, novel peptidoglycan biosynthesis inhibitors. J Am Chem Soc 124:10260–10261. doi: 10.1021/ja017748hCrossRefPubMedGoogle Scholar
  67. 67.
    Tanino T, Ichikawa S, Al-Dabbagh B, Bouhss A, Oyama H, Matsuda A (2010) Synthesis and biological evaluation of muraymycin analogues active against anti-drug-resistant bacteria. ACS Med Chem Lett 1:258–262. doi: 10.1021/ml100057zCrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Tanino T, Al-Dabbagh B, Mengin-Lecreulx D, Bouhss A, Oyama H, Ichikawa S, Matsuda A (2011) Mechanistic analysis of muraymycin analogues: a guide to the design of MraY inhibitors. J Med Chem 54:8421–8439. doi: 10.1021/jm200906rCrossRefPubMedGoogle Scholar
  69. 69.
    Takeoka Y, Tanino T, Sekiguchi M, Yonezawa S, Sakagami M, Takahashi F, Togame H, Tanaka Y, Takemoto H, Ichikawa S, Matsuda A (2014) Expansion of antibacterial spectrum of muraymycins toward Pseudomonas aeruginosa. ACS Med Chem Lett 5:556–560. doi: 10.1021/ml5000096CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Spork AP, Büschleb M, Ries O, Wiegmann D, Boettcher S, Mihalyi A, Bugg TDH, Ducho C (2014) Lead structures for new antibacterials: stereocontrolled synthesis of a bioactive muraymycin analogue. Chemistry 20:15292–15297. doi: 10.1002/chem.201404775CrossRefPubMedGoogle Scholar
  71. 71.
    Ries O, Carnarius C, Steinem C, Ducho C (2015) Membrane-interacting properties of the functionalised fatty acid moiety of muraymycin antibiotics. Med Chem Commun 6:879–886. doi: 10.1039/C4MD00526KCrossRefGoogle Scholar
  72. 72.
    Mitachi K, Aleiwi BA, Schneider CM, Siricilla S, Kurosu M (2016) Stereocontrolled total synthesis of muraymycin D1 having a dual mode of action against Mycobacterium tuberculosis. J Am Chem Soc 138:12975–12980. doi: 10.1021/jacs.6b07395CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Cheng L, Chen W, Zhai L, Xu D, Huang T, Lin S, Zhou X, Deng Z (2011) Identification of the gene cluster involved in muraymycin biosynthesis from Streptomyces sp. NRRL 30471. Mol Biosyst 7:920–927. doi: 10.1039/c0mb00237bCrossRefPubMedGoogle Scholar
  74. 74.
    Rodolis MT, Mihalyi A, Ducho C, Eitel K, Gust B, Goss RJM, Bugg TDH (2014) Mechanism of action of the uridyl peptide antibiotics: an unexpected link to a protein-protein interaction site in translocase MraY. Chem Commun 50:13023–13025. doi: 10.1039/c4cc06516fCrossRefGoogle Scholar
  75. 75.
    Rodolis MT, Mihalyi A, O’Reilly A, Slikas J, Roper DI, Hancock REW, Bugg TDH (2014) Identification of a novel inhibition site in translocase MraY based upon the site of interaction with lysis protein E from bacteriophage ΦX174. ChemBioChem 15:1300–1308. doi: 10.1002/cbic.201402064CrossRefPubMedGoogle Scholar
  76. 76.
    Yamaguchi H, Sato S, Yoshida S, Takada K, Itoh M, Seto H, Otake N (1986) Capuramycin, a new nucleoside antibiotic. Taxonomy, fermentation, isolation and characterization. J Antibiot 39:1047–1053. doi: 10.7164/antibiotics.39.1047CrossRefPubMedGoogle Scholar
  77. 77.
    Seto H, Otake N, Sato S, Yamaguchi H, Takada K, Itoh M, Lu HSM, Clardy J (1988) The structure of a new nucleoside antibiotic, capuramycin. Tetrahedron Lett 29:2343–2346. doi: 10.1016/S0040-4039(00)86055-4CrossRefGoogle Scholar
  78. 78.
    Muramatsu Y, Muramatsu A, Ohnuki T, Ishii MM, Kizuka M, Enokita R, Tsutsumi S, Arai M, Ogawa Y, Suzuki T, Takatsu T, Inukai M (2003) Studies on novel bacterial translocase I inhibitors, A-500359s. I. Taxonomy, fermentation, isolation, physico-chemical properties and structure elucidation of A-500359 A, C, D and G. J Antibiot 56:243–252. doi: 10.7164/antibiotics.56.243CrossRefPubMedGoogle Scholar
  79. 79.
    Muramatsu Y, Ishii MM, Inukai M (2003) Studies on novel bacterial translocase I inhibitors, A-500359s. II. Biological activities of A-500359 A, C, D and G. J Antibiot 56:253–258. doi: 10.7164/antibiotics.56.253CrossRefPubMedGoogle Scholar
  80. 80.
    Muramatsu Y, Miyakoshi S, Ogawa Y, Ohnuki T, Ishii MM, Arai M, Takatsu T, Inukai M (2003) Studies on novel bacterial translocase I inhibitors, A-500359s. III. Deaminocaprolactam derivatives of capuramycin: A-500359 E, F, H; M-1 and M-2. J Antibiot 56:259–267. doi: 10.7164/antibiotics.56.259CrossRefPubMedGoogle Scholar
  81. 81.
    Hotoda H, Furukawa M, Daigo M, Murayama K, Kaneko M, Muramatsu Y, Ishii MM, Miyakoshi S, Takatsu T, Inukai M, Kakuta M, Abe T, Harasaki T, Fukuoka T, Utsui Y, Ohya S (2003) Synthesis and antimycobacterial activity of capuramycin analogues. Part 1: substitution of the azepan-2-one moiety of capuramycin. Bioorg Med Chem Lett 13:2829–2832. doi: 10.1016/S0960-894X(03)00596-1CrossRefPubMedGoogle Scholar
  82. 82.
    Hotoda H, Daigo M, Furukawa M, Murayama K, Hasegawa CA, Kaneko M, Muramatsu Y, Ishii MM, Miyakoshi S, Takatsu T, Inukai M, Kakuta M, Abe T, Fukuoka T, Utsui Y, Ohya S (2003) Synthesis and antimycobacterial activity of capuramycin analogues. Part 2: acylated derivatives of capuramycin-related compounds. Bioorg Med Chem Lett 13:2833–2836. doi: 10.1016/S0960-894X(03)00597-3CrossRefPubMedGoogle Scholar
  83. 83.
    Funabashi M, Yang Z, Nonaka K, Hosobuchi M, Fujita Y, Shibata T, Chi X, Van Lanen SG (2010) An ATP-independent strategy for amide bond formation in antibiotic biosynthesis. Nat Chem Biol 6:581–586. doi: 10.1038/nchembio.393CrossRefPubMedGoogle Scholar
  84. 84.
    Cai W, Goswami A, Yang Z, Liu X, Green KD, Barnard-Britson S, Baba S, Funabashi M, Nonaka K, Sunkara M, Morris AJ, Spork AP, Ducho C, Garneau-Tsodikova S, Thorson JS, Van Lanen SG (2015) The biosynthesis of capuramycin-type antibiotics: identification of the A-102395 biosynthetic gene cluster, mechanism of self-resistance, and formation of uridine-5’-carboxamide. J Biol Chem 290:13710–13724. doi: 10.1074/jbc.M115.646414CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Liu X, Jin Y, Cai W, Green KD, Goswami A, Garneau-Tsodikova S, Nonaka K, Baba S, Funabashi M, Yang Z, Van Lanen SG (2016) A biocatalytic approach to capuramycin analogues by exploiting a substrate permissive N-transacylase CapW. Org Biomol Chem 14:3956–3962. doi: 10.1039/c6ob00381hCrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Lehrer J, Vigeant KA, Tatar LD, Valvano MA (2007) Functional characterization and membrane topology of Escherichia coli WecA, a sugar-phosphate transferase initiating the biosynthesis of enterobacterial common antigen and O-antigen lipopolysaccharide. J Bacteriol 189:2618–2628. doi: 10.1128/JB.01905-06CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Soldo B, Lazarevic V, Karamata D (2002) tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168a. Microbiology 148:2079–2087. doi: 10.1099/00221287-148-7-2079CrossRefPubMedGoogle Scholar
  88. 88.
    Farha MA, Leung A, Sewell EW, D’Elia MA, Allison SE, Ejim L, Pereira PM, Pinho MG, Wright GD, Brown ED (2013) Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to β-lactams. ACS Chem Biol 8:226–233. doi: 10.1021/cb300413mCrossRefPubMedGoogle Scholar
  89. 89.
    Farha MA, Koteva K, Gale RT, Sewell EW, Wright GD, Brown ED (2014) Designing analogs of tirisclopidine, a wall teichoic acid inhibitor, to avoid formation of its oxidative metabolites. Bioorg Med Chem Lett 24:905–910. doi: 10.1016/j.bmcl.2013.12.069CrossRefPubMedGoogle Scholar
  90. 90.
    Glover KJ, Weerapana E, Chen MM, Imperiali B (2006) Direct biochemical evidence for the utilization of UDP-bacillosamine by PglC, an essential glycosyl-1-phosphate transferase in the Campylobacter jejuni N-linked glycosylation pathway. Biochemistry 45:5343–5350. doi: 10.1021/bi0602056CrossRefPubMedGoogle Scholar
  91. 91.
    Walvoort MTC, Lukose V, Imperiali B (2016) A modular approach to phosphoglycosyltransferase inhibitors inspired by nucleoside antibiotics. Chemistry 22:3856–3864. doi: 10.1002/chem.201503986CrossRefPubMedGoogle Scholar
  92. 92.
    Zhang D, Miller MJ (1999) Polyoxins and nikkomycins: progress in synthetic and biological studies. Curr Pharm Des 5:73–99PubMedGoogle Scholar
  93. 93.
    Isono K, Nagatsu J, Kawashima Y, Suzuki S (1965) Studies on polyoxins, antifungal antibiotics. Part I. Isolation and characterization of polyoxins A and B. Agric Biol Chem 29:848–854. doi: 10.1271/bbb1961.29.848CrossRefGoogle Scholar
  94. 94.
    Dähn U, Hagenmaier H, Höhne H, König WA, Wolf G, Zähner H (1976) Stoffwechselprodukte von mikroorganismen. 154. Mitteilung. Nikkomycin, ein neuer hemmstoff der chitinsynthese bei pilzen. Arch Microbiol 107:143–160CrossRefGoogle Scholar
  95. 95.
    Zhang D, Miller MJ (1998) Total synthesis of (±)-carbocyclic polyoxin C and its α-epimer. J Org Chem 63:755–759. doi: 10.1021/jo971711rCrossRefPubMedGoogle Scholar
  96. 96.
    Li F, Brogan JB, Gage JL, Zhang D, Miller MJ (2004) Chemoenzymatic synthesis and synthetic application of enantiopure aminocyclopentenols: total synthesis of carbocyclic (+)-uracil polyoxin C and its α-epimer. J Org Chem 69:4538–4540. doi: 10.1021/jo0496796CrossRefPubMedGoogle Scholar
  97. 97.
    Stauffer CS, Bhaket P, Fothergill AW, Rinaldi MG, Datta A (2007) Total synthesis and antifungal activity of a carbohydrate ring-expanded pyranosyl nucleoside analogue of nikkomycin B. J Org Chem 72:9991–9997. doi: 10.1021/jo701814bCrossRefPubMedGoogle Scholar
  98. 98.
    Bormann C, Möhrle V, Bruntner C (1996) Cloning and heterologous expression of the entire set of structural genes for nikkomycin synthesis from Streptomyces tendae Tü901 in Streptomyces lividans. J Bacteriol 178:1216–1218CrossRefGoogle Scholar
  99. 99.
    Bruckner RC, Zhao G, Venci D, Jorns MS (2004) Nikkomycin biosynthesis: formation of a 4-electron oxidation product during turnover of NikD with its physiological substrate. Biochemistry 43:9160–9167. doi: 10.1021/bi0493618CrossRefPubMedGoogle Scholar
  100. 100.
    Ling H, Wang G, Tian Y, Liu G, Tan H (2007) SanM catalyzes the formation of 4-pyridyl-2-oxo-4-hydroxyisovalerate in nikkomycin biosynthesis by interacting with SanN. Biochem Biophys Res Commun 361:196–201. doi: 10.1016/j.bbrc.2007.07.016CrossRefPubMedGoogle Scholar
  101. 101.
    Jia L, Tian Y, Tan H (2007) SanT, a bidomain protein, is essential for nikkomycin biosynthesis of Streptomyces ansochromogenes. Biochem Biophys Res Commun 362:1031–1036. doi: 10.1016/j.bbrc.2007.08.114CrossRefPubMedGoogle Scholar
  102. 102.
    Chen W, Huang T, He X, Meng Q, You D, Bai L, Li J, Wu M, Li R, Xie Z, Zhou H, Zhou X, Tan H, Deng Z (2009) Characterization of the polyoxin biosynthetic gene cluster from Streptomyces cacaoi and engineered production of polyoxin H. J Biol Chem 284:10627–10638. doi: 10.1074/jbc.M807534200CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Bugg TDH, Rodolis MT, Mihalyi A, Jamshidi S (2016) Inhibition of phospho-MurNAc-pentapeptide translocase (MraY) by nucleoside natural product antibiotics, bacteriophage ∏X174 lysis protein E, and cationic antibacterial peptides. Bioorg Med Chem 24:6340–6347. doi: 10.1016/j.bmc.2016.03.018CrossRefPubMedGoogle Scholar
  104. 104.
    Chen KT, Chen PT, Lin CK, Huang LY, Hu CM, Chang YF, Hsu HT, Cheng TJ, Wu YT, Cheng WC (2016) Structural investigation of Park’s nucleotide on bacterial translocase MraY: discovery of unexpected MraY inhibitors. Sci Rep 6:31579. doi: 10.1038/srep31579CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Wohnig S, Spork AP, Koppermann S, Mieskes G, Gisch N, Jahn R, Ducho C (2016) Total synthesis of dansylated Park’s nucleotide for high-throughput MraY assays. Chemistry 22:17813–17819. doi: 10.1002/chem.201604279CrossRefPubMedGoogle Scholar
  106. 106.
    Chung BC, Mashalidis EH, Tanino T, Kim M, Matsuda A, Hong J, Ichikawa S, Lee SY (2016) Structural insights into inhibition of lipid I production in bacterial cell wall synthesis. Nature 533:557–560. doi: 10.1038/nature17636CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Zhang MM, Wang Y, Ang EL, Zhao H (2016) Engineering microbial hosts for production of bacterial natural products. Nat Prod Rep 33:963–987. doi: 10.1039/c6np00017gCrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325:1089–1093. doi: 10.1126/science.1176667CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Wencewicz TA (2016) New antibiotics from nature’s chemical inventory. Bioorg Med Chem 24:6227–6252. doi: 10.1016/j.bmc.2016.09.014CrossRefPubMedGoogle Scholar
  110. 110.
    Moloney MG (2016) Natural products as a source for novel antibiotics. Trends Pharmacol Sci 37:689–701. doi: 10.1016/j.tips.2016.05.001CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of ChemistryUniversity of WarwickCoventryUK

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