Lasso Peptides: An Intriguing Class of Bacterial Natural Products

Accounts of Chemical Research

Volumn 48, Issue 7, 2015, Pages 1909-1919

  Hegemann, Julian D ^a   Zimmermann, Marcel ^a   Xie, Xiulan ^a   Marahiel, Mohamed A ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PRODUCT; PEPTIDE;

BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM;

BACTERIA; BIOLOGICAL PRODUCTS; MODELS, MOLECULAR; PEPTIDES;

EID: 84937459511     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.5b00156     Document Type: Article

References (58)

1. Weber, W.; Fischli, W.; Hochuli, E.; Kupfer, E.; Weibel, E. K. Anantin - a peptide antagonist of the atrial natriuretic factor (ANF). I. Producing organism, fermentation, isolation and biological activity J. Antibiot. 1991, 44, 164-171
2. Salomon, R. A.; Farias, R. N. Microcin 25, a novel antimicrobial peptide produced by Escherichia coli J. Bacteriol. 1992, 174, 7428-7435
3. Morishita, Y.; Chiba, S.; Tsukuda, E.; Tanaka, T.; Ogawa, T.; Yamasaki, M.; Yoshida, M.; Kawamoto, I.; Matsuda, Y. RES-701-1, a novel and selective endothelin type B receptor antagonist produced by Streptomyces sp. RE-701. I. Characterization of producing strain, fermentation, isolation, physico-chemical and biological properties J. Antibiot. 1994, 47, 269-275
4. Ogawa, T.; Ochiai, K.; Tanaka, T.; Tsukuda, E.; Chiba, S.; Yano, K.; Yamasaki, M.; Yoshida, M.; Matsuda, Y. RES-701-2, -3 and -4, novel and selective endothelin type B receptor antagonists produced by Streptomyces sp. I. Taxonomy of producing strains, fermentation, isolation, and biochemical properties J. Antibiot. 1995, 48, 1213-1220
5. Frechet, D.; Guitton, J. D.; Herman, F.; Faucher, D.; Helynck, G.; Monegier du Sorbier, B.; Ridoux, J. P.; James-Surcouf, E.; Vuilhorgne, M. Solution structure of RP 71955, a new 21 amino acid tricyclic peptide active against HIV-1 virus Biochemistry 1994, 33, 42-50
6. Potterat, O.; Stephan, H.; Metzger, J. W.; Gnau, V.; Zähner, H.; Jung, G. Aborycin-a tryciclic 21-peptide antibiotic isolated from Streptomyces griseoflavus Liebigs Ann. Chem. 1994, 7, 741-743
7. Chokekijchai, S.; Kojima, E.; Anderson, S.; Nomizu, M.; Tanaka, M.; Machida, M.; Date, T.; Toyota, K.; Ishida, S.; Watanabe, K.; Yoshioka, H.; Roller, P. P.; Murakami, K.; Mitsuya, H. NP-06: A novel anti-human immunodeficiency virus polypeptide produced by a Streptomyces species Antimicrob. Agents Chemother. 1995, 39, 2345-2347
8. Tsunakawa, M.; Hu, S. L.; Hoshino, Y.; Detlefson, D. J.; Hill, S. E.; Furumai, T.; White, R. J.; Nishio, M.; Kawano, K.; Yamamoto, S.; Fukagawa, Y.; Oki, T. Siamycins I and II, new anti-HIV peptides: I. Fermentation, isolation, biological activity and initial characterization J. Antibiot. 1995, 48, 433-434
9. Yano, K.; Toki, S.; Nakanishi, S.; Ochiai, K.; Ando, K.; Yoshida, M.; Matsuda, Y.; Yamasaki, M. MS-271, a novel inhibitor of calmodulin-activated myosin light chain kinase from Streptomyces sp. - I. Isolation, structural determination and biological properties of MS-271 Bioorg. Med. Chem. 1996, 4, 115-120
10. Kimura, K.; Kanou, F.; Takahashi, H.; Esumi, Y.; Uramoto, M.; Yoshihama, M. Propeptin, a new inhibitor of prolyl endopeptidase produced by Microbispora. I. Fermentation, isolation and biological properties J. Antibiot. 1997, 50, 373-378
11. Delgado, M. A.; Rintoul, M. R.; Farias, R. N.; Salomon, R. A. Escherichia coli RNA polymerase is the target of the cyclopeptide antibiotic microcin J25 J. Bacteriol. 2001, 183, 4543-4550
12. Potterat, O.; Wagner, K.; Gemmecker, G.; Mack, J.; Puder, C.; Vettermann, R.; Streicher, R. BI-32169, a bicyclic 19-peptide with strong glucagon receptor antagonist activity from Streptomyces sp J. Nat. Prod. 2004, 67, 1528-1531
13. Iwatsuki, M.; Tomoda, H.; Uchida, R.; Gouda, H.; Hirono, S.; Omura, S. Lariatins, antimycobacterial peptides produced by Rhodococcus sp. K01-B0171, have a lasso structure J. Am. Chem. Soc. 2006, 128, 7486-7491
14. Knappe, T. A.; Linne, U.; Zirah, S.; Rebuffat, S.; Xie, X.; Marahiel, M. A. Isolation and structural characterization of capistruin, a lasso peptide predicted from the genome sequence of Burkholderia thailandensis E264 J. Am. Chem. Soc. 2008, 130, 11446-11454
15. Knappe, T. A.; Manzenrieder, F.; Mas-Moruno, C.; Linne, U.; Sasse, F.; Kessler, H.; Xie, X.; Marahiel, M. A. Introducing lasso peptides as molecular scaffolds for drug design: engineering of an integrin antagonist Angew. Chem., Int. Ed. 2011, 50, 8714-8717
16. Um, S.; Kim, Y. J.; Kwon, H.; Wen, H.; Kim, S. H.; Kwon, H. C.; Park, S.; Shin, J.; Oh, D. C. Sungsanpin, a lasso peptide from a deep-sea streptomycete J. Nat. Prod. 2013, 76, 873-879
17. Gavrish, E.; Sit, C. S.; Cao, S.; Kandror, O.; Spoering, A.; Peoples, A.; Ling, L.; Fetterman, A.; Hughes, D.; Bissell, A.; Torrey, H.; Akopian, T.; Mueller, A.; Epstein, S.; Goldberg, A.; Clardy, J.; Lewis, K. Lassomycin, a ribosomally synthesized cyclic peptide, kills mycobacterium tuberculosis by targeting the ATP-dependent protease ClpC1P1P2 Chem. Biol. 2014, 21, 509-518
18. Hegemann, J. D.; De Simone, M.; Zimmermann, M.; Knappe, T. A.; Xie, X.; Di Leva, F. S.; Marinelli, L.; Novellino, E.; Zahler, S.; Kessler, H.; Marahiel, M. A. Rational improvement of the affinity and selectivity of integrin binding of grafted lasso peptides J. Med. Chem. 2014, 57, 5829-5834
19. Metelev, M.; Tietz, J. I.; Melby, J. O.; Blair, P. M.; Zhu, L.; Livnat, I.; Severinov, K.; Mitchell, D. A. Structure, bioactivity, and resistance mechanism of streptomonomicin, an unusual lasso peptide from an understudied halophilic actinomycete Chem. Biol. 2015, 22, 241-250
20. Maksimov, M. O.; Pan, S. J.; Link, A. J. Lasso peptides: Structure, function, biosynthesis, and engineering Nat. Prod. Rep. 2012, 29, 996-1006
21. Maksimov, M. O.; Link, A. J. Prospecting genomes for lasso peptides J. Ind. Microbiol. Biotechnol. 2014, 41, 333-344
22. Hegemann, J. D.; Zimmermann, M.; Xie, X.; Marahiel, M. A. Caulosegnins I-III: a highly diverse group of lasso peptides derived from a single biosynthetic gene cluster J. Am. Chem. Soc. 2013, 135, 210-222
23. Knappe, T. A.; Linne, U.; Xie, X.; Marahiel, M. A. The glucagon receptor antagonist BI-32169 constitutes a new class of lasso peptides FEBS Lett. 2010, 584, 785-789
24. Helynck, G.; Dubertret, C.; Mayaux, J. F.; Leboul, J. Isolation of RP 71955, a new anti-HIV-1 peptide secondary metabolite J. Antibiot. 1993, 46, 1756-1757
25. Kersten, R. D.; Yang, Y. L.; Xu, Y.; Cimermancic, P.; Nam, S. J.; Fenical, W.; Fischbach, M. A.; Moore, B. S.; Dorrestein, P. C. A mass spectrometry-guided genome mining approach for natural product peptidogenomics Nat. Chem. Biol. 2011, 7, 794-802
26. Maksimov, M. O.; Pelczer, I.; Link, A. J. Precursor-centric genome-mining approach for lasso peptide discovery Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 15223-15228
27. Hegemann, J. D.; Zimmermann, M.; Zhu, S.; Klug, D.; Marahiel, M. A. Lasso peptides from proteobacteria: Genome mining employing heterologous expression and mass spectrometry Biopolymers 2013, 100, 527-542
28. Maksimov, M. O.; Link, A. J. Discovery and characterization of an isopeptidase that linearizes lasso peptides J. Am. Chem. Soc. 2013, 135, 12038-12047
29. Zimmermann, M.; Hegemann, J. D.; Xie, X.; Marahiel, M. A. The astexin-1 lasso peptides: Biosynthesis, stability, and structural studies Chem. Biol. 2013, 20, 558-569
30. Hegemann, J. D.; Zimmermann, M.; Zhu, S.; Steuber, H.; Harms, K.; Xie, X.; Marahiel, M. A. Xanthomonins I-III: A New Class of Lasso Peptides with a Seven-Residue Macrolactam Ring Angew. Chem., Int. Ed. 2014, 53, 2230-2234
31. Zimmermann, M.; Hegemann, J. D.; Xie, X.; Marahiel, M. A. Characterization of caulonodin lasso peptides revealed unprecedented N-terminal residues and a precursor motif essential for peptide maturation Chem. Sci. 2014, 5, 4032-4043
32. Vincent, P. A.; Delgado, M. A.; Farias, R. N.; Salomon, R. A. Inhibition of Salmonella enterica serovars by microcin J25 FEMS Microbiol. Lett. 2004, 236, 103-107
33. Bellomio, A.; Vincent, P. A.; de Arcuri, B. F.; Farias, R. N.; Morero, R. D. Microcin J25 has dual and independent mechanisms of action in Escherichia coli: RNA polymerase inhibition and increased superoxide production J. Bacteriol. 2007, 189, 4180-4186
34. Solbiati, J. O.; Ciaccio, M.; Farias, R. N.; Gonzalez-Pastor, J. E.; Moreno, F.; Salomon, R. A. Sequence analysis of the four plasmid genes required to produce the circular peptide antibiotic microcin J25 J. Bacteriol. 1999, 181, 2659-2662
35. Inokoshi, J.; Matsuhama, M.; Miyake, M.; Ikeda, H.; Tomoda, H. Molecular cloning of the gene cluster for lariatin biosynthesis of Rhodococcus jostii K01-B0171 Appl. Microbiol. Biotechnol. 2012, 95, 451-460
36. Constantine, K. L.; Friedrichs, M. S.; Detlefsen, D.; Nishio, M.; Tsunakawa, M.; Furumai, T.; Ohkuma, H.; Oki, T.; Hill, S.; Bruccoleri, R. E.; Lin, P.-F.; Mueller, L. High-resolution solution structure of siamycin II: Novel amphipathic character of a 21-residue peptide that inhibits HIV fusion J. Biomol. NMR 1995, 5, 271-286
37. Detlefsen, D. J.; Hill, S. E.; Volk, K. J.; Klohr, S. E.; Tsunakawa, M.; Furumai, T.; Lin, P. F.; Nishio, M.; Kawano, K.; Oki, T.; Lee, M. S. Siamycins I and II, new anti-HIV-1 peptides: II. Sequence analysis and structure determination of siamycin I J. Antibiot. 1995, 48, 1515-1517
38. Katahira, R.; Shibata, K.; Yamasaki, M.; Matsuda, Y.; Yoshida, M. Solution structure of endothelin B receptor selective antagonist RES-701-1 determined by 1H NMR spectroscopy Bioorg. Med. Chem. 1995, 3, 1273-1280
39. Bayro, M. J.; Mukhopadhyay, J.; Swapna, G. V.; Huang, J. Y.; Ma, L. C.; Sineva, E.; Dawson, P. E.; Montelione, G. T.; Ebright, R. H. Structure of antibacterial peptide microcin J25: A 21-residue lariat protoknot J. Am. Chem. Soc. 2003, 125, 12382-12383
40. Rosengren, K. J.; Clark, R. J.; Daly, N. L.; Goransson, U.; Jones, A.; Craik, D. J. Microcin J25 has a threaded sidechain-to-backbone ring structure and not a head-to-tail cyclized backbone J. Am. Chem. Soc. 2003, 125, 12464-12474
41. Wilson, K. A.; Kalkum, M.; Ottesen, J.; Yuzenkova, J.; Chait, B. T.; Landick, R.; Muir, T.; Severinov, K.; Darst, S. A. Structure of microcin J25, a peptide inhibitor of bacterial RNA polymerase, is a lassoed tail J. Am. Chem. Soc. 2003, 125, 12475-12483
42. Nar, H.; Schmid, A.; Puder, C.; Potterat, O. High-resolution crystal structure of a lasso peptide ChemMedChem 2010, 5, 1689-1692
43. Kuznedelov, K.; Semenova, E.; Knappe, T. A.; Mukhamedyarov, D.; Srivastava, A.; Chatterjee, S.; Ebright, R. H.; Marahiel, M. A.; Severinov, K. The antibacterial threaded-lasso peptide capistruin inhibits bacterial RNA polymerase J. Mol. Biol. 2011, 412, 842-848
44. Chiuchiolo, M. J.; Delgado, M. A.; Farias, R. N.; Salomon, R. A. Growth-phase-dependent expression of the cyclopeptide antibiotic microcin J25 J. Bacteriol. 2001, 183, 1755-1764
45. Choudhury, H. G.; Tong, Z.; Mathavan, I.; Li, Y.; Iwata, S.; Zirah, S.; Rebuffat, S.; van Veen, H. W.; Beis, K. Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 9145-9150
46. Yuzenkova, J.; Delgado, M.; Nechaev, S.; Savalia, D.; Epshtein, V.; Artsimovitch, I.; Mooney, R. A.; Landick, R.; Farias, R. N.; Salomon, R.; Severinov, K. Mutations of bacterial RNA polymerase leading to resistance to microcin j25 J. Biol. Chem. 2002, 277, 50867-50875
47. Adelman, K.; Yuzenkova, J.; La Porta, A.; Zenkin, N.; Lee, J.; Lis, J. T.; Borukhov, S.; Wang, M. D.; Severinov, K. Molecular mechanism of transcription inhibition by peptide antibiotic microcin J25 Mol. Cell 2004, 14, 753-762
48. Mathavan, I.; Zirah, S.; Mehmood, S.; Choudhury, H. G.; Goulard, C.; Li, Y.; Robinson, C. V.; Rebuffat, S.; Beis, K. Structural basis for hijacking siderophore receptors by antimicrobial lasso peptides Nat. Chem. Biol. 2014, 10, 340-342
49. Yan, K. P.; Li, Y.; Zirah, S.; Goulard, C.; Knappe, T. A.; Marahiel, M. A.; Rebuffat, S. Dissecting the maturation steps of the lasso peptide microcin J25 in vitro ChemBioChem 2012, 13, 1046-1052
50. Knappe, T. A.; Linne, U.; Robbel, L.; Marahiel, M. A. Insights into the biosynthesis and stability of the lasso peptide capistruin Chem. Biol. 2009, 16, 1290-1298
51. Cheung, W. L.; Pan, S. J.; Link, A. J. Much of the microcin J25 leader peptide is dispensable J. Am. Chem. Soc. 2010, 132, 2514-2515
52. Pan, S. J.; Rajniak, J.; Maksimov, M. O.; Link, A. J. The role of a conserved threonine residue in the leader peptide of lasso peptide precursors Chem. Commun. 2012, 48, 1880-1882
53. Pavlova, O.; Mukhopadhyay, J.; Sineva, E.; Ebright, R. H.; Severinov, K. Systematic structure-activity analysis of microcin J25 J. Biol. Chem. 2008, 283, 25589-25595
54. Dasgupta, S.; Wu, J. Formation of [2]rotaxanes by encircling [20], [21] and [22]crown ethers onto the dibenzylammonium dumbbell Chem. Sci. 2012, 3, 425-432
55. Dasgupta, S.; Huang, K.-W.; Wu, J. Trifluoromethyl acting as stopper in [2]rotaxane Chem. Commun. 2012, 48, 4821-4823
56. Rosengren, K. J.; Blond, A.; Afonso, C.; Tabet, J. C.; Rebuffat, S.; Craik, D. J. Structure of thermolysin cleaved microcin J25: Extreme stability of a two-chain antimicrobial peptide devoid of covalent links Biochemistry 2004, 43, 4696-4702
57. Xie, X.; Marahiel, M. A. NMR as an effective tool for the structure determination of lasso peptides ChemBioChem 2012, 13, 621-625
58. Jeanne Dit Fouque, K.; Afonso, C.; Zirah, S.; Hegemann, J. D.; Zimmermann, M.; Marahiel, M. A.; Rebuffat, S.; Lavanant, H. Ion mobility-mass spectrometry of lasso peptides: signature of a rotaxane topology Anal. Chem. 2015, 87, 1166-1172