journal article·2020-02-25

Nanopore Passport Control for Substrate-Specific Translocation

Devika Vikraman, Remya Satheesan, K. Santhosh Kumar, Kozhinjampara R. Mahendran

ACS Nano· Volume 14· Issue 2
Publisher page

Abstract

Membrane protein pores have demonstrated applications in nanobiotechnology and single-molecule chemistry for effective detection of biomolecules. Here, we define the molecular basis of carbohydrate polymers translocation through a substrate-specific bacterial nanopore, CymA, which has a 15-residue N terminus segment inside the pore, restricting its diameter. Using single-channel recordings, we determined the kinetics of cationic cyclic oligosaccharide binding and elucidated the translocation mechanism across the pore in real-time. The cationic cyclic hexasaccharide binds to the densely packed negatively charged residues at the extracellular side of the pore with high affinity, facilitating its entry into the pore driven by the applied voltage. Further, the dissociation rate constant increased with increasing voltages, indicating unidirectional translocation toward the pore exit. Specifically, a larger cationic cyclic octasaccharide rapidly blocked the pore more effectively, resulting in the complete closure of the pore with increasing voltage, implying only strong binding. Further, we show that uncharged oligosaccharides exclusively bind to the extracellular side of the pore and the electroosmotic flow most likely drives their translocation. We propose that CymA favors selective translocation of cyclic hexasaccharide and linear maltooligosaccharides due to an asymmetrical charge pattern and the N terminus that regulates the substrate transport. We suggest that this substrate-specific nanopore with sophisticated geometry will be useful for complex biopolymer characterization.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Nanopore and Nanochannel Transport Studies · Microfluidic and Bio-sensing Technologies · Microfluidic and Capillary Electrophoresis Applications

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

Affiliations

Membrane Biology Laboratory, Interdisciplinary Research Program, Rajiv Gandhi Centre for Biotechnology, Thiruvananthapuram 695014, India

Manipal Academy of Higher Education, Manipal, Karnataka, 576104, India

Funding

Council of Scientific and Industrial Research · Science and Engineering Research Board · Department of Biotechnology , Ministry of Science and Technology

References (57)

Show source-provided references
1. 10.1128/MMBR.67.4.593-656.200310.1128/MMBR.67.4.593-656.2003 ↗
2. 10.1038/nrmicro199410.1038/nrmicro1994 ↗
3. 10.1073/pnas.071156110510.1073/pnas.0711561105 ↗
4. 10.1016/S0006-3495(02)75442-810.1016/S0006-3495(02)75442-8 ↗
5. 10.1074/jbc.M30543420010.1074/jbc.M305434200 ↗
6. 10.1038/nsb0198-3710.1038/nsb0198-37 ↗
7. 10.1038/s41467-017-02523-y10.1038/s41467-017-02523-y ↗
8. 10.1073/pnas.142483511210.1073/pnas.1424835112 ↗
9. 10.1021/acsnano.6b0861310.1021/acsnano.6b08613 ↗
10. 10.1073/pnas.160271611310.1073/pnas.1602716113 ↗
11. 10.1016/S0167-7799(00)01426-810.1016/S0167-7799(00)01426-8 ↗
12. 10.1073/pnas.93.24.1377010.1073/pnas.93.24.13770 ↗
13. 10.1038/3509303810.1038/35093038 ↗
14. 10.1529/biophysj.104.05740610.1529/biophysj.104.057406 ↗
15. 10.1038/nnano.2009.1210.1038/nnano.2009.12 ↗
16. 10.1016/j.cbpa.2016.08.00510.1016/j.cbpa.2016.08.005 ↗
17. 10.1016/j.bbamem.2015.09.02310.1016/j.bbamem.2015.09.023 ↗
18. 10.1038/nbt.342310.1038/nbt.3423 ↗
19. 10.1016/j.copbio.2010.05.00210.1016/j.copbio.2010.05.002 ↗
20. 10.1073/pnas.080751410610.1073/pnas.0807514106 ↗
21. 10.1038/s41587-019-0096-010.1038/s41587-019-0096-0 ↗
22. 10.1039/C4CC07919A10.1039/C4CC07919A ↗
23. 10.1186/s13059-016-1103-010.1186/s13059-016-1103-0 ↗
24. 10.1038/nbt.431610.1038/nbt.4316 ↗
25. 10.1038/nnano.2016.26710.1038/nnano.2016.267 ↗
26. 10.1002/smll.20180119210.1002/smll.201801192 ↗
27. 10.1088/0957-4484/26/7/07400410.1088/0957-4484/26/7/074004 ↗
28. 10.1038/s41565-018-0236-610.1038/s41565-018-0236-6 ↗
29. 10.1038/nnano.2017.9910.1038/nnano.2017.99 ↗
30. 10.1038/s41467-017-00423-910.1038/s41467-017-00423-9 ↗
31. 10.1038/s41467-019-08761-610.1038/s41467-019-08761-6 ↗
32. 10.1016/j.copbio.2017.11.00610.1016/j.copbio.2017.11.006 ↗
33. 10.1103/PhysRevLett.85.305710.1103/PhysRevLett.85.3057 ↗
34. 10.1073/pnas.080829610510.1073/pnas.0808296105 ↗
35. 10.1021/acsnano.6b0315910.1021/acsnano.6b03159 ↗
36. 10.1038/nnano.2016.6610.1038/nnano.2016.66 ↗
37. 10.1038/s41467-018-03418-210.1038/s41467-018-03418-2 ↗
38. 10.1021/jacs.8b1197010.1021/jacs.8b11970 ↗
39. 10.1021/acsnano.7b0698010.1021/acsnano.7b06980 ↗
40. 10.1021/acssensors.7b0068010.1021/acssensors.7b00680 ↗
41. 10.1038/nnano.2011.8810.1038/nnano.2011.88 ↗
42. 10.1098/rsif.2011.022210.1098/rsif.2011.0222 ↗
43. 10.1016/S0006-3495(03)74527-510.1016/S0006-3495(03)74527-5 ↗
44. 10.1016/j.bpj.2015.12.02710.1016/j.bpj.2015.12.027 ↗
45. Sen K. · J. Biol. Chem. · 1988 · 263 · 118210.1016/S0021-9258(19)57283-0 ↗
46. 10.1021/acsinfecdis.8b0010810.1021/acsinfecdis.8b00108 ↗
47. 10.1039/C6NR06936C10.1039/C6NR06936C ↗
48. 10.1038/nchem.169510.1038/nchem.1695 ↗
49. 10.1074/jbc.274.35.2515910.1074/jbc.274.35.25159 ↗
50. 10.1002/anie.20140040010.1002/anie.201400400 ↗
51. 10.1021/acsnano.8b0926610.1021/acsnano.8b09266 ↗
52. 10.1038/s41565-018-0139-610.1038/s41565-018-0139-6 ↗
53. 10.1021/ja405339810.1021/ja4053398 ↗
54. 10.1021/acs.nanolett.5b0196010.1021/acs.nanolett.5b01960 ↗
55. 10.1021/acsnano.5b0209610.1021/acsnano.5b02096 ↗
56. 10.1021/acsnano.7b0121210.1021/acsnano.7b01212 ↗
57. 10.1038/nprot.2015.00310.1038/nprot.2015.003 ↗