journal article·2024-07Open access

Four Parallel Pathways in T4 Ligase‐Catalyzed Repair of Nicked DNA with Diverse Bending Angles

Na Li, Jianbing Ma, Hang Fu, Zhiwei Yang, Chunhua Xu, Haihong Li, Yimin Zhao, Yizhen Zhao, Shuyu Chen, Lu Gou, Xinghua Zhang, Shengli Zhang, Ming Li, Ximiao Hou, Lei Zhang, Ying Lu

Advanced Science· Volume 11· Issue 25

Abstract

Abstract The structural diversity of biological macromolecules in different environments contributes complexity to enzymological processes vital for cellular functions. Fluorescence resonance energy transfer and electron microscopy are used to investigate the enzymatic reaction of T4 DNA ligase catalyzing the ligation of nicked DNA. The data show that both the ligase–AMP complex and the ligase–AMP–DNA complex can have four conformations. This finding suggests the parallel occurrence of four ligation reaction pathways, each characterized by specific conformations of the ligase–AMP complex that persist in the ligase–AMP–DNA complex. Notably, these complexes have DNA bending angles of ≈0°, 20°, 60°, or 100°. The mechanism of parallel reactions challenges the conventional notion of simple sequential reaction steps occurring among multiple conformations. The results provide insights into the dynamic conformational changes and the versatile attributes of T4 DNA ligase and suggest that the parallel multiple reaction pathways may correspond to diverse T4 DNA ligase functions. This mechanism may potentially have evolved as an adaptive strategy across evolutionary history to navigate complex environments.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: DNA and Nucleic Acid Chemistry · Advanced biosensing and bioanalysis techniques · DNA Repair Mechanisms

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

MOE Key Laboratory for Nonequilibrium Synthesis and Modulation of Condensed Matter School of Physics Xi'an Jiaotong University Xi'an 710049 China

Beijing National Laboratory for Condensed Matter Physics Institute of Physics Chinese Academy of Sciences Beijing 100190 China

University of Chinese Academy of Sciences Beijing 100049 China

Wenzhou Institute University of Chinese Academy of Sciences Wenzhou Zhejiang 325011 China

College of Life Sciences Northwest A&F University Yangling 712100 China

Hubei Key Laboratory of Cell Homeostasis College of Life Sciences Wuhan University Wuhan 430072 China

Songshan Lake Materials Laboratory Dongguan Guangdong 523808 China

Funding

National Natural Science Foundation of China · China Postdoctoral Science Foundation · National Key Research and Development Program of China

References (65)

Show source-provided references
1. 10.1126/science.116937510.1126/science.1169375 ↗
2. 10.1021/acs.chemrev.1c0086910.1021/acs.chemrev.1c00869 ↗
3. 10.1039/D1SM00470K10.1039/D1SM00470K ↗
4. 10.1021/acs.biochem.8b0100410.1021/acs.biochem.8b01004 ↗
5. 10.1021/jacs.5b0170510.1021/jacs.5b01705 ↗
6. 10.1038/s41570-023-00495-w10.1038/s41570-023-00495-w ↗
7. 10.1021/ar500390e10.1021/ar500390e ↗
8. 10.1021/acs.chemrev.5b0059010.1021/acs.chemrev.5b00590 ↗
9. 10.1093/nar/gkaa30710.1093/nar/gkaa307 ↗
10. 10.1016/S0092-8674(00)81260-X10.1016/S0092-8674(00)81260-X ↗
11. 10.1016/S1097-2765(00)00115-510.1016/S1097-2765(00)00115-5 ↗
12. 10.1021/cr040498d10.1021/cr040498d ↗
13. 10.1016/j.molcel.2006.08.01510.1016/j.molcel.2006.08.015 ↗
14. 10.1038/s41467-019-08296-w10.1038/s41467-019-08296-w ↗
15. 10.1016/S0969-2126(96)00070-610.1016/S0969-2126(96)00070-6 ↗
16. 10.1038/s41467-018-05024-810.1038/s41467-018-05024-8 ↗
17. 10.1038/nature0308210.1038/nature03082 ↗
18. 10.1093/nar/gky77610.1093/nar/gky776 ↗
19. 10.1016/j.cell.2020.12.03410.1016/j.cell.2020.12.034 ↗
20. 10.1016/j.cell.2016.05.04010.1016/j.cell.2016.05.040 ↗
21. 10.1038/nsmb.346310.1038/nsmb.3463 ↗
22. Brünger A. T. · Nat. Struct. Biol. · 1997 · 4 · 862
23. 10.1126/science.aan113310.1126/science.aan1133 ↗
24. 10.7554/eLife.6041610.7554/eLife.60416 ↗
25. 10.1016/j.cell.2018.10.04510.1016/j.cell.2018.10.045 ↗
26. 10.1016/j.molcel.2018.02.02610.1016/j.molcel.2018.02.026 ↗
27. 10.1126/science.aat771610.1126/science.aat7716 ↗
28. 10.1371/journal.pcbi.100921510.1371/journal.pcbi.1009215 ↗
29. 10.1016/j.sbi.2020.05.00610.1016/j.sbi.2020.05.006 ↗
30. 10.1038/s41586-019-1029-210.1038/s41586-019-1029-2 ↗
31. 10.1038/nmeth.120810.1038/nmeth.1208 ↗
32. 10.1038/nature0492810.1038/nature04928 ↗
33. 10.1103/PhysRevLett.119.13810210.1103/PhysRevLett.119.138102 ↗
34. 10.1126/science.114413010.1126/science.1144130 ↗
35. 10.1038/nature0862710.1038/nature08627 ↗
36. 10.1093/nar/gkaa05710.1093/nar/gkaa057 ↗
37. 10.1038/ncomms1108310.1038/ncomms11083 ↗
38. 10.1093/nar/gkz59610.1093/nar/gkz596 ↗
39. 10.1093/emboj/19.5.111910.1093/emboj/19.5.1119 ↗
40. 10.1016/S1097-2765(03)00187-410.1016/S1097-2765(03)00187-4 ↗
41. 10.1016/j.molcel.2007.02.02610.1016/j.molcel.2007.02.026 ↗
42. 10.1016/j.sbi.2007.12.00810.1016/j.sbi.2007.12.008 ↗
43. 10.1002/bies.20080021010.1002/bies.200800210 ↗
44. 10.1021/jacs.8b1083610.1021/jacs.8b10836 ↗
45. 10.1021/acs.biochem.2c0017810.1021/acs.biochem.2c00178 ↗
46. 10.1016/0378-1119(83)90069-010.1016/0378-1119(83)90069-0 ↗
47. 10.1039/D1SC07115G10.1039/D1SC07115G ↗
48. 10.1073/pnas.170113211410.1073/pnas.1701132114 ↗
49. 10.1038/nature0404910.1038/nature04049 ↗
50. 10.1016/j.jsb.2012.09.00610.1016/j.jsb.2012.09.006 ↗
51. 10.7554/eLife.4216610.7554/eLife.42166 ↗
52. 10.1016/j.jsb.2015.11.00310.1016/j.jsb.2015.11.003 ↗
53. 10.1073/pnas.131444911010.1073/pnas.1314449110 ↗
54. 10.1016/j.jmb.2003.07.01310.1016/j.jmb.2003.07.013 ↗
55. a)D. S.BIOVIA Discovery Studio Visualizer https://discover.3ds.com/discovery‐studio‐visualizer‐download (accessed: 2019).
56. 10.1110/ps.07334490810.1110/ps.073344908 ↗
57. 10.1016/j.softx.2015.06.00110.1016/j.softx.2015.06.001 ↗
58. 10.1038/nmeth.406710.1038/nmeth.4067 ↗
59. 10.1021/ci300363c10.1021/ci300363c ↗
60. 10.1021/ci300364910.1021/ci3003649 ↗
61. 10.1021/jacs.9b1050510.1021/jacs.9b10505 ↗
62. 10.1039/D0RA09059J10.1039/D0RA09059J ↗
63. 10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.0.CO;2-M10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.0.CO;2-M ↗
64. 10.1002/jcc.2008410.1002/jcc.20084 ↗
65. 10.1038/nmeth.208910.1038/nmeth.2089 ↗