Thiazole/oxazole-modified microcins: Complex natural products from ribosomal templates

Current Opinion in Chemical Biology

Volumn 15, Issue 3, 2011, Pages 369-378

  Melby, Joel O ^a   Nard, Nathan J ^a,b   Mitchell, Douglas A ^a  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL WARFARE AGENT; CYSTEINE; MICROCIN B17; NATURAL PRODUCT; OXAZOLE; SERINE; STREPTOLYSIN S; THIAZOLE; THIAZOLE OXAZOLE MODIFIED MICROCIN DERIVATIVE; THREONINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BIOSYNTHESIS; CHEMICAL STRUCTURE; COMBINATORIAL LIBRARY; CYANOBACTERIUM; GENE CLUSTER; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; PROTEIN PROCESSING; REVIEW; RIBOSOME; SYMBIOSIS;

BACTERIA; BACTERIOCINS; BIOLOGICAL PRODUCTS; OXAZOLES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RIBOSOMES; THIAZOLES;

EID: 79957973597     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.02.027     Document Type: Review

References (70)

1. Velasquez J.E., van der Donk W.A. Genome mining for ribosomally synthesized natural products. Curr Opin Chem Biol 2010.
2. Bagley M.C., Dale J.W., Merritt E.A., Xiong A. Thiopeptide antibiotics. Chem Rev 2005, 105:685-714.
3. Salvatella X., Caba J.M., Albericio F., Giralt E. Solution structure of the antitumor candidate trunkamide A by 2D NMR and restrained simulated annealing methods. J Org Chem 2003, 68:211-215.
4. Vizan J.L., Hernandez-Chico C., del Castillo I., Moreno F. The peptide antibiotic microcin B17 induces double-strand cleavage of DNA mediated by E. coli DNA gyrase. EMBO J 1991, 10:467-476.
5. Igarashi Y., Kan Y., Fujii K., Fujita T., Harada K., Naoki H., Tabata H., Onaka H., Furumai T. Goadsporin, a chemical substance which promotes secondary metabolism and morphogenesis in streptomycetes. II. Structure determination. J Antibiot (Tokyo) 2001, 54:1045-1053.
6. Pelludat C., Rakin A., Jacobi C.A., Schubert S., Heesemann J. The yersiniabactin biosynthetic gene cluster of Yersinia enterocolitica: organization and siderophore-dependent regulation. J Bacteriol 1998, 180:538-546.
7. Ho D.D., Neumann A.U., Perelson A.S., Chen W., Leonard J.M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 1995, 373:123-126.
8. Li Y.M., Milne J.C., Madison L.L., Kolter R., Walsh C.T. From peptide precursors to oxazole and thiazole-containing peptide antibiotics: microcin B17 synthase. Science 1996, 274:1188-1193.
9. Fischbach M.A., Walsh C.T. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem Rev 2006, 106:3468-3496.
10. Schneider T.L., Shen B., Walsh C.T. Oxidase domains in epothilone and bleomycin biosynthesis: thiazoline to thiazole oxidation during chain elongation. Biochemistry 2003, 42:9722-9730.
11. Milne J.C., Eliot A.C., Kelleher N.L., Walsh C.T. ATP/GTP hydrolysis is required for oxazole and thiazole biosynthesis in the peptide antibiotic microcin B17. Biochemistry 1998, 37:13250-13261.
12. Milne J.C., Roy R.S., Eliot A.C., Kelleher N.L., Wokhlu A., Nickels B., Walsh C.T. Cofactor requirements and reconstitution of microcin B17 synthetase: a multienzyme complex that catalyzes the formation of oxazoles and thiazoles in the antibiotic microcin B17. Biochemistry 1999, 38:4768-4781.
13. Oman T.J., van der Donk W.A. Follow the leader: the use of leader peptides to guide natural product biosynthesis. Nat Chem Biol 2010, 6:9-18.
14. Schmidt E.W. Trading molecules and tracking targets in symbiotic interactions. Nat Chem Biol 2008, 4:466-473.
15. Haft D.H., Basu M.K., Mitchell D.A. Expansion of ribosomally produced natural products: a nitrile hydratase- and Nif11-related precursor family. BMC Biol 2010, 8:70.
16. Mitchell D.A., Lee S.W., Pence M.A., Markley A.L., Limm J.D., Nizet V., Dixon J.E. Structural and functional dissection of the heterocyclic peptide cytotoxin streptolysin S. J Biol Chem 2009, 284:13004-13012.
17. Donia M.S., Hathaway B.J., Sudek S., Haygood M.G., Rosovitz M.J., Ravel J., Schmidt E.W. Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians. Nat Chem Biol 2006, 2:729-735.
18. Weissman K.J., Leadlay P.F. Combinatorial biosynthesis of reduced polyketides. Nat Rev Microbiol 2005, 3:925-936.
19. Arndt H.D., Schoof S., Lu J.Y. Thiopeptide antibiotic biosynthesis. Angew Chem Int Ed Engl 2009, 48:6770-6773.
20. Li C., Kelly W.L. Recent advances in thiopeptide antibiotic biosynthesis. Nat Prod Rep 2010, 27:153-164.
21. Houssen W.E., Jaspars M. Azole-based cyclic peptides from the sea squirt lissoclinum patella: old scaffolds, new avenues. Chembiochem 2010, 11:1803-1815.
22. Severinov K., Semenova E., Kazakov A., Kazakov T., Gelfand M.S. Low-molecular-weight post-translationally modified microcins. Mol Microbiol 2007, 65:1380-1394.
23. Jones A.C., Gu L., Sorrels C.M., Sherman D.H., Gerwick W.H. New tricks from ancient algae: natural products biosynthesis in marine cyanobacteria. Curr Opin Chem Biol 2009, 13:216-223.
24. McIntosh J.A., Donia M.S., Schmidt E.W. Ribosomal peptide natural products: bridging the ribosomal and nonribosomal worlds. Nat Prod Rep 2009, 26:537-559.
25. Nolan E.M., Walsh C.T. How nature morphs peptide scaffolds into antibiotics. Chembiochem 2009, 10:34-53.
26. Sivonen K., Leikoski N., Fewer D.P., Jokela J. Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol 2010, 86:1213-1225.
27. Walsh C.T., Acker M.G., Bowers A.A. Thiazolyl peptide antibiotic biosynthesis: a cascade of post-translational modifications on ribosomal nascent proteins. J Biol Chem 2010, 285:27525-27531.
28. Kelleher N.L., Belshaw P.J., Walsh C.T. Regioselectivity and chemoselectivity analysis of oxazole and thiazole ring formation by the peptide-heterocyclizing microcin B17 synthetase using high-resolution MS/MS. J Am Chem Soc 1998, 120:9716-9717.
29. Sinha Roy R., Belshaw P.J., Walsh C.T. Mutational analysis of posttranslational heterocycle biosynthesis in the gyrase inhibitor microcin B17: distance dependence from propeptide and tolerance for substitution in a GSCG cyclizable sequence. Biochemistry 1998, 37:4125-4136.
30. Belshaw P.J., Roy R.S., Kelleher N.L., Walsh C.T. Kinetics and regioselectivity of peptide-to-heterocycle conversions by microcin B17 synthetase. Chem Biol 1998, 5:373-384.
31. Kelleher N.L., Hendrickson C.L., Walsh C.T. Posttranslational heterocyclization of cysteine and serine residues in the antibiotic microcin B17: distributivity and directionality. Biochemistry 1999, 38:15623-15630.
32. Donia M.S., Ravel J., Schmidt E.W. A global assembly line for cyanobactins. Nat Chem Biol 2008, 4:341-343.
33. Donia M.S., Schmidt E.W. Cyanobactins-ubiquitous cyanobacterial ribosomal peptide metabolites. Comprehensive Natural Products II 2010, Elsevier Ltd. L. Mander, H.-W. Liu (Eds.).
34. Schmidt E.W., Nelson J.T., Rasko D.A., Sudek S., Eisen J.A., Haygood M.G., Ravel J. Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci U S A 2005, 102:7315-7320.
35. Ziemert N., Ishida K., Quillardet P., Bouchier C., Hertweck C., de Marsac N.T., Dittmann E. Microcyclamide biosynthesis in two strains of Microcystis aeruginosa: from structure to genes and vice versa. Appl Environ Microbiol 2008, 74:1791-1797.
36. Sudek S., Haygood M.G., Youssef D.T.A., Schmidt E.W. Structure of trichamide, a cyclic peptide from the bloom-forming cyanobacterium Trichodesmium erythraeum, predicted from the genome sequence. Appl Environ Microbiol 2006, 72:4382-4387.
37. Leikoski N., Fewer D.P., Sivonen K. Widespread occurrence and lateral transfer of the cyanobactin biosynthesis gene cluster in cyanobacteria. Appl Environ Microbiol 2009, 75:853-857.
38. Lee J., McIntosh J., Hathaway B.J., Schmidt E.W. Using marine natural products to discover a protease that catalyzes peptide macrocyclization of diverse substrates. J Am Chem Soc 2009, 131:2122.
39. McIntosh J.A., Donia M.S., Schmidt E.W. Insights into heterocyclization from two highly similar enzymes. J Am Chem Soc 2010, 132:4089-4091.
40. McIntosh J.A., Schmidt E.W. Marine molecular machines: heterocyclization in cyanobactin biosynthesis. Chembiochem 2010, 11:1413-1421.
41. McIntosh J.A., Robertson C.R., Agarwal V., Nair S.K., Bulaj G.W., Schmidt E.W. Circular logic: nonribosomal peptide-like macrocyclization with a ribosomal peptide catalyst. J Am Chem Soc 2010, 132:15499-15501.
42. Lee S.W., Mitchell D.A., Markley A.L., Hensler M.E., Gonzalez D., Wohlrab A., Dorrestein P.C., Nizet V., Dixon J.E. Discovery of a widely distributed toxin biosynthetic gene cluster. Proc Natl Acad Sci U S A 2008, 105:5879-5884.
43. Betschel S.D., Borgia S.M., Barg N.L., Low D.E., De Azavedo J.C. Reduced virulence of group A streptococcal Tn916 mutants that do not produce streptolysin S. Infect Immun 1998, 66:1671-1679.
44. Nizet V., Beall B., Bast D.J., Datta V., Kilburn L., Low D.E., De Azavedo J.C. Genetic locus for streptolysin S production by group A streptococcus. Infect Immun 2000, 68:4245-4254.
45. Gonzalez D.J., Lee S.W., Hensler M.E., Markley A.L., Dahesh S., Mitchell D.A., Bandeira N., Nizet V., Dixon J.E., Dorrestein P.C. Clostridiolysin S, a post-translationally modified biotoxin from Clostridium botulinum. J Biol Chem 2010, 285:28220-28228.
46. Cotter P.D., Draper L.A., Lawton E.M., Daly K.M., Groeger D.S., Casey P.G., Ross R.P., Hill C. Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog 2008, 4:e1000144.
47. Roy R.S., Kim S., Baleja J.D., Walsh C.T. Role of the microcin B17 propeptide in substrate recognition: solution structure and mutational analysis of McbA1-26. Chem Biol 1998, 5:217-228.
48. Su T.L. Micrococcin, an antibacterial substance formed by a strain of Micrococcus. Br J Exp Pathol 1948, 29:473-481.
49. Mocek U., Zeng Z.P., Ohagan D., Zhou P., Fan L.D.G., Beale J.M., Floss H.G. Biosynthesis of the modified peptide antibiotic thiostrepton in Streptomyces azureus and Streptomyces laurentii. J Am Chem Soc 1993, 115:7992-8001.
50. Kelly W.L., Pan L., Li C. Thiostrepton biosynthesis: prototype for a new family of bacteriocins. J Am Chem Soc 2009, 131:4327-4334.
51. Liao R., Duan L., Lei C., Pan H., Ding Y., Zhang Q., Chen D., Shen B., Yu Y., Liu W. Thiopeptide biosynthesis featuring ribosomally synthesized precursor peptides and conserved posttranslational modifications. Chem Biol 2009, 16:141-147.
52. Morris R.P., Leeds J.A., Naegeli H.U., Oberer L., Memmert K., Weber E., LaMarche M.J., Parker C.N., Burrer N., Esterow S., et al. Ribosomally synthesized thiopeptide antibiotics targeting elongation factor Tu. J Am Chem Soc 2009, 131:5946-5955.
53. Wieland Brown L.C., Acker M.G., Clardy J., Walsh C.T., Fischbach M.A. Thirteen posttranslational modifications convert a 14-residue peptide into the antibiotic thiocillin. Proc Natl Acad Sci U S A 2009, 106:2549-2553.
54. Yu Y., Duan L., Zhang Q., Liao R., Ding Y., Pan H., Wendt-Pienkowski E., Tang G., Shen B., Liu W. Nosiheptide biosynthesis featuring a unique indole side ring formation on the characteristic thiopeptide framework. ACS Chem Biol 2009, 4:855-864.
55. Wei M., Deng J., Wang S., Liu N., Chen Y. A simple reverse genetics approach to elucidating the biosynthetic pathway of nocathiacin. Biotechnol Lett 2011, 33:585-591.
56. Ding Y., Yu Y., Pan H., Guo H., Li Y., Liu W. Moving posttranslational modifications forward to biosynthesize the glycosylated thiopeptide nocathiacin I in Nocardia sp. ATCC202099. Mol Biosyst 2010, 6:1180-1185.
57. Engelhardt K., Degnes K.F., Zotchev S.B. Isolation and characterization of the biosynthetic gene cluster for thiopeptide antibiotic TP-1161. Appl Environ Microbiol 2010, 76:4969-4976.
58. Wang J., Yu Y., Tang K., Liu W., He X., Huang X., Deng Z. Identification and analysis of the biosynthetic gene cluster encoding the thiopeptide antibiotic cyclothiazomycin in Streptomyces hygroscopicus 10-22. Appl Environ Microbiol 2010, 76:2335-2344.
59. Bycroft B.W., Gowland M.S. Structures of highly modified peptide antibiotics micrococcin P1 and P2. J Chem Soc-Chem Commun 1978, 256-258.
60. Bowers A.A., Walsh C.T., Acker M.G. Genetic interception and structural characterization of thiopeptide cyclization precursors from Bacillus cereus. J Am Chem Soc 2010, 132:12182-12184.
61. Yu Y., Guo H., Zhang Q., Duan L., Ding Y., Liao R., Lei C., Shen B., Liu W. NosA catalyzing carboxyl-terminal amide formation in nosiheptide maturation via an enamine dealkylation on the serine-extended precursor peptide. J Am Chem Soc 2010.
62. Li C., Zhang F., Kelly W.L. Heterologous production of thiostrepton A and biosynthetic engineering of thiostrepton analogs. Mol Biosyst 2010.
63. Acker M.G., Bowers A.A., Walsh C.T. Generation of thiocillin variants by prepeptide gene replacement and in vivo processing by Bacillus cereus. J Am Chem Soc 2009, 131:17563-17565.
64. Bowers A.A., Acker M.G., Koglin A., Walsh C.T. Manipulation of thiocillin variants by prepeptide gene replacement: structure, conformation, and activity of heterocycle substitution mutants. J Am Chem Soc 2010, 132:7519-7527.
65. Li B., Sher D., Kelly L., Shi Y., Huang K., Knerr P.J., Joewono I., Rusch D., Chisholm S.W., van der Donk W.A. Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria. Proc Natl Acad Sci U S A 2010, 107:10430-10435.
66. Scholz R., Molohon K.J., Nachtigall J., Vater J., Markley A.L., Sussmuth R.D., Mitchell D.A., Borriss R. Plantazolicin, a novel microcin B17/streptolysin S-like natural product from Bacillus amyloliquefaciens FZB42. J Bacteriol 2011, 193:215-224.
67. Onaka H., Nakaho M., Hayashi K., Igarashi Y., Furumai T. Cloning and characterization of the goadsporin biosynthetic gene cluster from Streptomyces sp. TP-A0584. Microbiology 2005, 151:3923-3933.
68. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
69. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res 2004, 14:1188-1190.
70. Cock P.J., Antao T., Chang J.T., Chapman B.A., Cox C.J., Dalke A., Friedberg I., Hamelryck T., Kauff F., Wilczynski B., et al. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 2009, 25:1422-1423.