Citation: Yuanjun Han, Suze Ma, Qi Zhang. Substrate specificity and reaction directionality of a three-residue cyclophane forming enzyme PauB[J]. Chinese Chemical Letters, ;2023, 34(1): 107589. doi: 10.1016/j.cclet.2022.06.012 shu

Substrate specificity and reaction directionality of a three-residue cyclophane forming enzyme PauB

Department of Chemistry, Fudan University, Shanghai 200433, China

qizhang@sioc.ac.cn

Received Date: 17 April 2022
Revised Date: 2 June 2022
Accepted Date: 5 June 2022
Available Online: 10 June 2022

Figures(5)

Three-residue cyclophane-forming enzymes (3-CyFEs) are a group of radical S-adenosylmethionine (SAM) enzymes involved in the biosynthesis of ribosomally synthesized and posttranslationally modified peptides (RiPPs). 3-CyFE catalyzes the crosslinking between an aromatic residue (Ω1) and a non-aromatic residue (X3) in a Ω1-X2-X3 motif to produce a cyclophane ring, a key step in the biosynthesis of the RiPP natural product triceptide. In this study, we perform a genome-wide search for the Xye-type triceptides, showing these RiPPs are likely class-specific and only present in gamma-proteobacteria. The 3-CyFE PauB from Photorhabdus australis exhibits a relaxed substrate specificity on the X3 position, but glycine in this position is not suitable for cyclophane formation. We also reconstituted the activity of PauB in vitro, showing it produces the N-terminal cyclophane firstly, and then the C-terminal ring, whereas the middle cyclophane is produced in the last step.
- Cyclophane,
- Biosynthesis,
- Radical SAM,
- Enzyme catalysis,
- Peptide,
- Natural product
1. [1]
  P.G. Arnison, M.J. Bibb, G. Bierbaum, et al., Nat. Prod. Rep. 30 (2013) 108-160. doi: 10.1039/C2NP20085F
2. [2]
  M. Montalbán-López, T.A. Scott, S. Ramesh, et al., Nat. Prod. Rep. 38 (2021) 130-239. doi: 10.1039/d0np00027b
3. [3]
  R. Zallot, N. Oberg, J.A. Gerlt, Biochemistry 58 (2019) 4169-4182. doi: 10.1021/acs.biochem.9b00735
4. [4]
  N. Oberg, T.W. Precord, D.A. Mitchell, J.A. Gerlt, ACS Bio Med Chem. Au 2 (2022) 22-35. doi: 10.1021/acsbiomedchemau.1c00048
5. [5]
  D.H. Haft, M.K. Basu, J. Bacteriol. 193 (2011) 2745-2755. doi: 10.1128/JB.00040-11
6. [6]
  N. Mahanta, G.A. Hudson, D.A. Mitchell, Biochemistry 56 (2017) 5229-5244. doi: 10.1021/acs.biochem.7b00771
7. [7]
  A. Benjdia, C. Balty, O. Berteau, Front. Chem. 5 (2017) 87. doi: 10.3389/fchem.2017.00087
8. [8]
  K.A. Clark, L.B. Bushin, M.R. Seyedsayamdost, ACS Bio Med Chem Au 2 (2022) 328–339. doi: 10.1021/acsbiomedchemau.2c00004
9. [9]
  A. Mendauletova, A. Kostenko, Y. Lien, J. Latham, ACS Bio Med Chem Au 2 (2022) 53-59. doi: 10.1021/acsbiomedchemau.1c00045
10. [10]
  T. Mo, X. Ji, W. Yuan, et al., Angew. Chem. Int. Ed. 58 (2019) 18793-18797. doi: 10.1002/anie.201908490
11. [11]
  L.B. Bushin, B.C. Covington, B.E. Rued, M.J. Federle, M.R. Seyedsayamdost, J. Am. Chem. Soc. 142 (2020) 16265–16275. doi: 10.1021/jacs.0c05546
12. [12]
  S. Chiumento, C. Roblin, S. Kieffer-Jaquinod, et al., Sci. Adv. 5 (2019) eaaw9969. doi: 10.1126/sciadv.aaw9969
13. [13]
  C. Balty, A. Guillot, L. Fradale, et al., J. Biol. Chem. 294 (2019) 14512-14525. doi: 10.1074/jbc.ra119.009416
14. [14]
  C. Roblin, S. Chiumento, O. Bornet, et al., Proc. Natl. Acad. Sci. USA. 117 (2020) 19168-19177. doi: 10.1073/pnas.2004045117
15. [15]
  G.A. Hudson, B.J. Burkhart, A.J. DiCaprio, et al., J. Am. Chem. Soc. 141 (2019) 8228-8238. doi: 10.1021/jacs.9b01519
16. [16]
  Y. Chen, Y. Yang, X. Ji, et al., J. Biotechnol. (2020) e2000136.
17. [17]
  A. Caruso, L.B. Bushin, K.A. Clark, R.J. Martinie, M.R. Seyedsayamdost, J. Am. Chem. Soc. 141 (2019) 990-997. doi: 10.1021/jacs.8b11060
18. [18]
  K.R. Schramma, L.B. Bushin, M.R. Seyedsayamdost, Nat. Chem. 7 (2015) 431-437. doi: 10.1038/nchem.2237
19. [19]
  K.A. Clark, L.B. Bushin, M.R. Seyedsayamdost, J. Am. Chem. Soc. 141 (2019) 10610-10615. doi: 10.1021/jacs.9b05151
20. [20]
  A. Caruso, R.J. Martinie, L.B. Bushin, M.R. Seyedsayamdost, J. Am. Chem. Soc. 141 (2019) 16610-16614. doi: 10.1021/jacs.9b09210
21. [21]
  Y. Imai, K.J. Meyer, A. Iinishi, et al., Nature 576 (2019) 459-464. doi: 10.1038/s41586-019-1791-1
22. [22]
  S. Groß, F. Panter, D. Pogorevc, et al., Chem. Sci. 12 (2021) 11882-11893. doi: 10.1039/d1sc02725e
23. [23]
  S. Guo, S. Wang, S. Ma, et al., Nat. Commun. 13 (2022) 2361. doi: 10.1038/s41467-022-30084-2
24. [24]
  A. Kostenko, Y. Lien, A. Mendauletova, et al., J. Biol. Chem. 298 (2022) 101881. doi: 10.1016/j.jbc.2022.101881
25. [25]
  H.J. Sofia, G. Chen, B.G. Hetzler, J.F. Reyes-Spindola, N.E. Miller, Nucleic Acid. Res. 29 (2001) 1097-1106. doi: 10.1093/nar/29.5.1097
26. [26]
  W.E. Broderick, B.M. Hoffman, J.B. Broderick, Acc. Chem. Res. 51 (2018) 2611-2619. doi: 10.1021/acs.accounts.8b00356
27. [27]
  T.Q.N. Nguyen, Y.W. Tooh, R. Sugiyama, et al., Nat. Chem. 12 (2020) 1042–1053. doi: 10.1038/s41557-020-0519-z
28. [28]
  S. Ma, H. Chen, H. Li, et al., Angew. Chem. Int. Ed. 60 (2021) 19957-19964. doi: 10.1002/anie.202107192
29. [29]
  S.C. Bobeica, S.H. Dong, L. Huo, et al., eLife 8 (2019) e42305. doi: 10.7554/eLife.42305
30. [30]
  T.J. Oman, W.A. van der Donk, Nat. Chem. Biol. 6 (2010) 9-18. doi: 10.1038/nchembio.286
31. [31]
  J.A. Gerlt, J.T. Bouvier, D.B. Davidson, et al., Biochim. Biophys. Acta 1854 (2015) 1019-1037. doi: 10.1016/j.bbapap.2015.04.015
32. [32]
  J.I. Tietz, C.J. Schwalen, P.S. Patel, et al., Nat. Chem. Biol. 13 (2017) 470-478. doi: 10.1038/nchembio.2319
33. [33]
  M. Lv, X. Ji, J. Zhao, et al., J. Am. Chem. Soc. 138 (2016) 6427-6435. doi: 10.1021/jacs.6b02221
34. [34]
  Y. Zhong, X. Ji, Chin. J. Chem. 38 (2020) 218-219. doi: 10.1002/cjoc.201900480
35. [35]
  Y. Zhong, X. Ji, Q. Zhang, Chin. J. Chem. 38 (2020) 39-42. doi: 10.1002/cjoc.201900399
36. [36]
  Y. Yin, X. Ji, Q. Zhang, Chin. J. Chem. 39 (2021) 2417-2421. doi: 10.1002/cjoc.202100304
37. [37]
  W. Ji, X. Ji, Q. Zhang, et al., Angew. Chem. Int. Ed. 59 (2020) 8880-8884. doi: 10.1002/anie.202000812
38. [38]
  T.A. Grell, P.J. Goldman, C.L. Drennan, J. Biol. Chem. 290 (2015) 3964-3971. doi: 10.1074/jbc.R114.581249
39. [39]
  N.D. Lanz, S.J. Booker, Biochim. Biophys. Acta 1853 (2015) 1316-1334. doi: 10.1016/j.bbamcr.2015.01.002
40. [40]
  M.W. Ruszczycky, S.H. Choi, H.W. Liu, J. Am. Chem. Soc. 132 (2010) 2359-2369. doi: 10.1021/ja909451a
41. [41]
  X. Ji, T. Mo, W.Q. Liu, et al., Angew. Chem. Int. Ed. 58 (2019) 6235-6238. doi: 10.1002/anie.201814708
42. [42]
  J. Cheng, W. Ji, S. Ma, et al., Angew. Chem. Int. Ed. 60 (2021) 7570-7575. doi: 10.1002/anie.202015177
43. [43]
  J. Cheng, W. Ding, Q. Zhang, Chin. J. Chem. 40 (2022) 1053-1058. doi: 10.1002/cjoc.202200032
44. [44]
  J. Zhao, W. Ji, X. Ji, Q. Zhang, Chin. J. Chem. 38 (2020) 959-962. doi: 10.1002/cjoc.202000119
45. [45]
  R. Wu, W. Ding, Q. Zhang, Chin. J. Chem. 38 (2020) 959–962. doi: 10.1002/cjoc.202000119
46. [46]
  H. Lee, W.A. van der Donk, Annu. Rev. Biochem. 91 (2022) 269–294. doi: 10.1146/annurev-biochem-032620-104956
1. [1]
  Fenglin Jiang , Anan Liu , Qian Wei , Youcai Hu . Editing function of type Ⅱ thioesterases in the biosynthesis of fungal polyketides. Chinese Chemical Letters, 2024, 35(10): 109504-. doi: 10.1016/j.cclet.2024.109504
2. [2]
  Liliang Chu , Xiaoyan Zhang , Jianing Li , Xuelei Deng , Miao Wu , Ya Cheng , Weiping Zhu , Xuhong Qian , Yunpeng Bai . Continuous-flow synthesis of polysubstituted γ-butyrolactones via enzymatic cascade catalysis. Chinese Chemical Letters, 2024, 35(4): 108896-. doi: 10.1016/j.cclet.2023.108896
3. [3]
  Jianhui Yin , Wenjing Huang , Changyong Guo , Chao Liu , Fei Gao , Honggang Hu . Tryptophan-specific peptide modification through metal-free photoinduced N-H alkylation employing N-aryl glycines. Chinese Chemical Letters, 2024, 35(6): 109244-. doi: 10.1016/j.cclet.2023.109244
4. [4]
  Fang-Yuan Chen , Wen-Chao Geng , Kang Cai , Dong-Sheng Guo . Molecular recognition of cyclophanes in water. Chinese Chemical Letters, 2024, 35(5): 109161-. doi: 10.1016/j.cclet.2023.109161
5. [5]
  Kunya Wang , Bingyu Liu , Daojiang Yan , Jian Bai , Haibo Yu , Youcai Hu . Full biosynthetic pathway of pyrrolobenzoxazines. Chinese Chemical Letters, 2025, 36(1): 109811-. doi: 10.1016/j.cclet.2024.109811
6. [6]
  Weiyu Chen , Zenghui Li , Chenguang Zhao , Lisha Zha , Junfeng Shi , Dan Yuan . Enzyme-modulate conformational changes in amphiphile peptide for selectively cell delivery. Chinese Chemical Letters, 2024, 35(12): 109628-. doi: 10.1016/j.cclet.2024.109628
7. [7]
  Peng Chen , Lijuan Liang , Yufei Zhu , Zhimin Xing , Zhenhua Jia , Teck-Peng Loh . Strategies for constructing seven-membered rings: Applications in natural product synthesis. Chinese Chemical Letters, 2024, 35(6): 109229-. doi: 10.1016/j.cclet.2023.109229
8. [8]
  Zihan Lin , Wanzhen Lin , Fa-Jie Chen . Electrochemical Modifications of Native Peptides. University Chemistry, 2025, 40(3): 318-327. doi: 10.12461/PKU.DXHX202406089
9. [9]
  Yixuan Zhu , Qingtong Wang , Jin Li , Lin Chen , Junlong Zhao . Blog of Oxytocin. University Chemistry, 2024, 39(9): 134-140. doi: 10.12461/PKU.DXHX202310090
10. [10]
  Yanwei Duan , Qing Yang . Molecular targets and their application examples for interrupting chitin biosynthesis. Chinese Chemical Letters, 2025, 36(4): 109905-. doi: 10.1016/j.cclet.2024.109905
11. [11]
  Xiaofang Luo , Ye Wu , Xiaokun Zhang , Min Tang , Feiye Ju , Zuodong Qin , Gregory J Duns , Wei-Dong Zhang , Jiang-Jiang Qin , Xin Luan . Peptide-based strategies for overcoming multidrug-resistance in cancer therapy. Chinese Chemical Letters, 2025, 36(1): 109724-. doi: 10.1016/j.cclet.2024.109724
12. [12]
  Rui Wang , He Qi , Haijiao Zheng , Qiong Jia . Light/pH dual-responsive magnetic metal-organic frameworks composites for phosphorylated peptide enrichment. Chinese Chemical Letters, 2024, 35(7): 109215-. doi: 10.1016/j.cclet.2023.109215
13. [13]
  Cheng-Yan Wu , Yi-Nan Gao , Zi-Han Zhang , Rui Liu , Quan Tang , Zhong-Lin Lu . Enhancing self-assembly efficiency of macrocyclic compound into nanotubes by introducing double peptide linkages. Chinese Chemical Letters, 2024, 35(11): 109649-. doi: 10.1016/j.cclet.2024.109649
14. [14]
  Chuanfeng Fan , Jian Gao , Yingkai Gao , Xintong Yang , Gaoning Li , Xiaochun Wang , Fei Li , Jin Zhou , Haifeng Yu , Yi Huang , Jin Chen , Yingying Shan , Li Chen . A non-peptide-based chymotrypsin-targeted long-wavelength emission fluorescent probe with large Stokes shift and its application in bioimaging. Chinese Chemical Letters, 2024, 35(10): 109838-. doi: 10.1016/j.cclet.2024.109838
15. [15]
  Zhengzhong Zhu , Shaojun Hu , Zhi Liu , Lipeng Zhou , Chongbin Tian , Qingfu Sun . A cationic radical lanthanide organic tetrahedron with remarkable coordination enhanced radical stability. Chinese Chemical Letters, 2025, 36(2): 109641-. doi: 10.1016/j.cclet.2024.109641
16. [16]
  Conghui Wang , Lei Xu , Zhenhua Jia , Teck-Peng Loh . Recent applications of macrocycles in supramolecular catalysis. Chinese Chemical Letters, 2024, 35(4): 109075-. doi: 10.1016/j.cclet.2023.109075
17. [17]
  Wei Chen , Pieter Cnudde . A minireview to ketene chemistry in zeolite catalysis. Chinese Journal of Structural Chemistry, 2024, 43(11): 100412-100412. doi: 10.1016/j.cjsc.2024.100412
18. [18]
  Lin Zhang , Chaoran Li , Thongthai Witoon , Xingda An , Le He . Nano-thermometry in photothermal catalysis. Chinese Journal of Structural Chemistry, 2025, 44(4): 100456-100456. doi: 10.1016/j.cjsc.2024.100456
19. [19]
  Chuang LIU , Lichao SUN , Qingfeng ZHANG . Chiral inorganic nanocatalysts for electrochemical and enzyme-mimicked biosensing. Chinese Journal of Inorganic Chemistry, 2025, 41(1): 59-78. doi: 10.11862/CJIC.20240406
20. [20]
  Yu Mao , Yilin Liu , Xiaochen Wang , Shengyang Ni , Yi Pan , Yi Wang . Acylfluorination of enynes via phosphine and silver catalysis. Chinese Chemical Letters, 2024, 35(8): 109443-. doi: 10.1016/j.cclet.2023.109443

Get Citation

PDF

XML

Metrics

PDF Downloads(7)
Abstract views(735)
HTML views(91)

通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142