The posttranslational modification cascade to the thiopeptide berninamycin generates linear forms and altered macrocyclic scaffolds

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 21, 2013, Pages 8483-8488

  Malcolmson, Steven J ^a   Young, Travis S ^a   Ruby, J Graham ^b,c   Skewes Cox, Peter ^b,c,d   Walsh, Christopher T ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Heterologous expression; Linear precursors; Prepeptide gene replacement

Indexed keywords

BERNINAMYCIN; MACROCYCLIC COMPOUND; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; GENE STRUCTURE; HETEROLOGOUS EXPRESSION; HYDROLYSIS; HYDROXYLATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; STREPTOMYCES; STREPTOMYCES BERNENSIS; STREPTOMYCES LIVIDANS; STREPTOMYCES VENEZUELAE;

HETEROLOGOUS EXPRESSION; LINEAR PRECURSORS; PREPEPTIDE GENE REPLACEMENT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; MACROCYCLIC COMPOUNDS; MOLECULAR SEQUENCE DATA; PEPTIDES; PEPTIDES, CYCLIC; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; STREPTOMYCES LIVIDANS; THIAZOLES;

EID: 84878120464     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307111110     Document Type: Article

References (38)

1. Bagley MC, Dale JW, Merritt EA, Xiong X (2005) Thiopeptide antibiotics. Chem Rev 105(2): 685-714.
2. Arndt H-D, Schoof S, Lu J-Y (2009) Thiopeptide antibiotic biosynthesis. Angew Chem Int Ed Engl 48(37): 6770-6773.
3. Li C, Kelly WL (2010) Recent advances in thiopeptide antibiotic biosynthesis. Nat Prod Rep 27(2): 153-164.
4. Walsh CT, Acker MG, Bowers AA (2010) Thiazolyl peptide antibiotic biosynthesis: A cascade of post-translational modifications on ribosomal nascent proteins. J Biol Chem 285(36): 27525-27531.
5. Walsh CT, Malcolmson SJ, Young TS (2012) Three ring posttranslational circuses: Insertion of oxazoles, thiazoles, and pyridines into protein-derived frameworks. ACS Chem Biol 7(3): 429-442.
6. Arnison PG, et al. (2013) Ribosomally synthesized and post-translationally modified peptide natural products: Overview and recommendations for a universal nomenclature. Nat Prod Rep 30(1): 108-160.
7. Zhang Q, Liu W (2013) Biosynthesis of thiopeptide antibiotics and their pathway engineering. Nat Prod Rep 30(2): 218-226.
8. Dunbar KL, Mitchell DA (2013) Revealing Nature's synthetic potential through the study of ribosomal natural product biosynthesis. ACS Chem Biol 8(3): 473-487.
9. Cameron DM, Thompson J, March PE, Dahlberg AE (2002) Initiation factor IF2, thiostrepton and micrococcin prevent the binding of elongation factor G to the Escherichia coli ribosome. J Mol Biol 319(1): 27-35.
10. Harms JM, et al. (2008) Translational regulation via L11: Molecular switches on the ribosome turned on and off by thiostrepton and micrococcin. Mol Cell 30(1): 26-38.
11. Mikolajka A, et al. (2011) Differential effects of thiopeptide and orthosomycin antibiotics on translational GTPases. Chem Biol 18(5): 589-600.
12. Heffron SE, Jurnak F (2000) Structure of an EF-Tu complex with a thiazolyl peptide antibiotic determined at 2.35 A resolution: Atomic basis for GE2270A inhibition of EF-Tu. Biochemistry 39(1): 37-45.
13. Parmeggiani A, et al. (2006) Structural basis of the action of pulvomycin and GE2270 A on elongation factor Tu. Biochemistry 45(22): 6846-6857.
14. Morris RP, et al. (2009) Ribosomally synthesized thiopeptide antibiotics targeting elongation factor Tu. J Am Chem Soc 131(16): 5946-5955.
15. LaMarche MJ, et al. (2012) Antibiotic optimization and chemical structure stabilization of thiomuracin A. J Med Chem 55(15): 6934-6941.
16. Bowers AA, Walsh CT, Acker MG (2010) Genetic interception and structural characterization of thiopeptide cyclization precursors from Bacillus cereus. J Am Chem Soc 132(35): 12182-12184.
17. Young TS, Walsh CT (2011) Identification of the thiazolyl peptide GE37468 gene cluster from Streptomyces ATCC 55365 and heterologous expression in Streptomyces lividans. Proc Natl Acad Sci USA 108(32): 13053-13058.
18. Young TS, Dorrestein PC, Walsh CT (2012) Codon randomization for rapid exploration of chemical space in thiopeptide antibiotic variants. Chem Biol 19(12): 1600-1610.
19. Egawa Y, Umino K, Tamura Y, Shimizu M, Kaneko K (1969) Sulfomycins, a series of new sulfur-containing antibiotics. I. Isolation, purification and properties. J Antibiot (Tokyo) 22(1): 12-17.
20. Ohyama S, Wada Y, Hasumi K (2002) Antibiotic A10255 (thioplabin) enhances fibrin binding and activation of plasminogen. J Antibiot (Tokyo) 55(1): 83-91.
21. Engelhardt K, et al. (2010) Production of a new thiopeptide antibiotic, TP-1161, by a marine Nocardiopsis species. Appl Environ Microbiol 76(15): 4969-4976.
22. Engelhardt K, Degnes KF, Zotchev SB (2010) Isolation and characterization of the gene cluster for biosynthesis of the thiopeptide antibiotic TP-1161. Appl Environ Microbiol 76(21): 7093-7101.
23. Abe H, Kushida K, Shiobara Y, Kodama M (1988) The structures of sulfomycin I and berninamycin A. Tetrahedron Lett 29: 1401-1404.
24. Lau RCM, Rinehart KL (1994) Berninamycins B, C, and D, minor metabolites from Streptomyces bernensis. J Antibiot (Tokyo) 47(12): 1466-1472.
25. Lau RCM, Rinehart KL (1995) Biosynthesis of berninamycin: Incorporation of 13C-labeled amino acids. J Am Chem Soc 117: 7606-7610.
26. Reusser F (1969) Mode of action of berninamycin. An inhibitor of protein biosynthesis. Biochemistry 8(8): 3303-3308.
27. Thompson J, Cundliffe E, Stark MJR (1982) The mode of action of berninamycin and mechanism of resistance in the producing organism, Streptomyces bernensis. J Gen Microbiol 128(4): 875-884.
28. Wieland Brown LC, Acker MG, Clardy J, Walsh CT, Fischbach MA (2009) Thirteen posttranslational modifications convert a 14-residue peptide into the antibiotic thiocillin. Proc Natl Acad Sci USA 106(8): 2549-2553.
29. Kelly WL, Pan L, Li C (2009) Thiostrepton biosynthesis: Prototype for a new family of bacteriocins. J Am Chem Soc 131(12): 4327-4334.
30. Liao R, et al. (2009) Thiopeptide biosynthesis featuring ribosomally synthesized precursor peptides and conserved posttranslational modifications. Chem Biol 16(2): 141-147.
31. Wang J, et al. (2010) Identification and analysis of the biosynthetic gene cluster encoding the thiopeptide antibiotic cyclothiazomycin in Streptomyces hygroscopicus 10-22. Appl Environ Microbiol 76(7): 2335-2344.
32. Oman TJ, van der Donk WA (2010) Follow the leader: The use of leader peptides to guide natural product biosynthesis. Nat Chem Biol 6(1): 9-18.
33. Yu Y, et al. (2010) NosA catalyzing carboxyl-terminal amide formation in nosiheptide maturation via an enamine dealkylation on the serine-extended precursor peptide. J Am Chem Soc 132(46): 16324-16326.
34. Cundliffe E (1978) Mechanism of resistance to thiostrepton in the producing-organism Streptomyces azureus. Nature 272(5656): 792-795.
35. Cundliffe E, Thompson J (1979) Ribose methylation and resistance to thiostrepton. Nature 278(5707): 859-861.
36. Acker MG, Bowers AA, Walsh CT (2009) Generation of thiocillin variants by prepeptide gene replacement and in vivo processing by Bacillus cereus. J Am Chem Soc 131(48): 17563-17565.
37. Bowers AA, Acker MG, Koglin A, Walsh CT (2010) Manipulation of thiocillin variants by prepeptide gene replacement: Structure, conformation, and activity of heterocycle substitution mutants. J Am Chem Soc 132(21): 7519-7527.
38. Kieser T, Bibb MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces Genetics (John Innes Foundation, Norwich, UK).