Effect of Copper(II) Ion Binding by Porin P1 Precursor Fragments from Fusobacterium nucleatum on DNA Degradation
Abstract
:1. Introduction
2. Results and Discussion
2.1. Coordination of Cu(II) Ions at Various pH
2.2. Oxidative Properties
3. Materials and Methods
3.1. Materials
3.2. Mass Spectrometry
3.3. Potentiometric Measurements
3.4. Spectroscopic Studies
3.5. Theoretical Studies
3.6. DNA Cleavage and Reactive Oxygen Species Detection
3.7. ROS Generation Measurements
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- World Health Organization. Cancer Statistics Reports. Available online: https://www.who.int/news-room/fact-sheets/detail/cancer (accessed on 20 November 2020).
- Giovannucci, E. Modifiable risk factors for colon cancer. Gastroenterol. Clin. N. Am. 2002, 31, 925–943. [Google Scholar] [CrossRef]
- Brennan, C.A.; Garrett, W.S. Gut Microbiota, Inflammation, and Colorectal Cancer. Annu. Rev. Microbiol. 2016, 70, 395–411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Savage, D.C. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 1977, 31, 107–133. [Google Scholar] [CrossRef]
- Sears, C.L.; Garrett, W.S. Microbes, microbiota, and colon cancer. Cell Host Microbe 2014, 15, 317–328. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kostic, A.D.; Chun, E.; Robertson, L.; Glickman, J.N.; Gallini, C.A.; Michaud, M.; Clancy, T.E.; Chung, D.C.; Lochhead, P.; Hold, G.L.; et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013, 14, 207–215. [Google Scholar] [CrossRef] [Green Version]
- Rubinstein, M.R.; Wang, X.; Liu, W.; Hao, Y.; Cai, G.; Han, Y.W. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 2013, 14, 195–206. [Google Scholar] [CrossRef] [Green Version]
- Hwang, I.M.; Sun, L.M.; Lin, C.L.; Lee, C.F.; Kao, C.H. Periodontal disease with treatment reduces subsequent cancer risks. QJM 2014, 107, 805–812. [Google Scholar] [CrossRef]
- Rubinstein, M.R.; Baik, J.E.; Lagana, S.M.; Han, R.P.; Raab, W.J.; Sahoo, D.; Dalerba, P.; Wang, T.C.; Han, Y.W. promotes colorectal cancer by inducing Wnt/β-catenin modulator Annexin A1. EMBO Rep. 2019, 20. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Peng, Y.; Yu, J.; Chen, T.; Wu, Y.; Shi, L.; Li, Q.; Wu, J.; Fu, X. Invasive Fusobacterium nucleatum activates beta-catenin signaling in colorectal cancer via a TLR4/P-PAK1 cascade. Oncotarget 2017, 8, 31802–31814. [Google Scholar] [CrossRef]
- Ganesan, K.; Guo, S.; Fayyaz, S.; Zhang, G.; Xu, B. Targeting Programmed. Cancers 2019, 11, 1592. [Google Scholar] [CrossRef] [Green Version]
- Brennan, C.A.; Garrett, W.S. Fusobacterium nucleatum—Symbiont, opportunist and oncobacterium. Nat. Rev. Microbiol. 2019, 17, 156–166. [Google Scholar] [CrossRef]
- Toussi, D.N.; Liu, X.; Massari, P. The FomA porin from Fusobacterium nucleatum is a Toll-like receptor 2 agonist with immune adjuvant activity. Clin. Vaccine Immunol. 2012, 19, 1093–1101. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.; Weng, W.; Peng, J.; Hong, L.; Yang, L.; Toiyama, Y.; Gao, R.; Liu, M.; Yin, M.; Pan, C.; et al. Fusobacterium nucleatum Increases Proliferation of Colorectal Cancer Cells and Tumor Development in Mice by Activating Toll-Like Receptor 4 Signaling to Nuclear Factor-κB, and Up-regulating Expression of MicroRNA-21. Gastroenterology 2017, 152, 851–866.e824. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ziech, D.; Franco, R.; Pappa, A.; Panayiotidis, M.I. Reactive oxygen species (ROS)-induced genetic and epigenetic alterations in human carcinogenesis. Mutat. Res. 2011, 711, 167–173. [Google Scholar] [CrossRef] [PubMed]
- Bhattacharjee, A.; Chakraborty, K.; Shukla, A. Cellular copper homeostasis: Current concepts on its interplay with glutathione homeostasis and its implication in physiology and human diseases. Metallomics 2017, 9, 1376–1388. [Google Scholar] [CrossRef] [PubMed]
- Relling, D.P.; Esberg, L.B.; Johnson, W.T.; Murphy, E.J.; Carlson, E.C.; Lukaski, H.C.; Saari, J.T.; Ren, J. Dietary interaction of high fat and marginal copper deficiency on cardiac contractile function. Obesity 2007, 15, 1242–1257. [Google Scholar] [CrossRef]
- Lorincz, M.T. Wilson disease and related copper disorders. Handb. Clin. Neurol. 2018, 147, 279–292. [Google Scholar] [CrossRef]
- Waldron, K.J.; Robinson, N.J. How do bacterial cells ensure that metalloproteins get the correct metal? Nat. Rev. Microbiol. 2009, 7, 25–35. [Google Scholar] [CrossRef] [PubMed]
- Hodgkinson, V.; Petris, M.J. Copper homeostasis at the host-pathogen interface. J. Biol. Chem. 2012, 287, 13549–13555. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giachino, A.; Waldron, K.J. Copper tolerance in bacteria requires the activation of multiple accessory pathways. Mol. Microbiol. 2020, 114, 377–390. [Google Scholar] [CrossRef]
- Porcheron, G.; Garénaux, A.; Proulx, J.; Sabri, M.; Dozois, C.M. Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: Correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front. Cell Infect. Microbiol. 2013, 3, 90. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, Z.; Jacobsen, F.E.; Giedroc, D.P. Coordination chemistry of bacterial metal transport and sensing. Chem. Rev. 2009, 109, 4644–4681. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andreini, C.; Banci, L.; Bertini, I.; Rosato, A. Zinc through the three domains of life. J. Proteome Res. 2006, 5, 3173–3178. [Google Scholar] [CrossRef]
- Kapatral, V.; Anderson, I.; Ivanova, N.; Reznik, G.; Los, T.; Lykidis, A.; Bhattacharyya, A.; Bartman, A.; Gardner, W.; Grechkin, G.; et al. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 2002, 184, 2005–2018. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- National Center for Biotechnology Information. Outer Membrane Protein P1 Precursor [Fusobacterium nucleatum subsp. nucleatum ATCC 25586]. Available online: https://www.ncbi.nlm.nih.gov/protein/AAL95199.1 (accessed on 18 October 2021).
- Sigel, H.; Martin, R.B. Coordinating properties of the amide bond. Stability and structure of metal ion complexes of peptides and related ligands. Chem. Rev. 1982, 82, 385–426. [Google Scholar] [CrossRef]
- Peisach, J.; Blumberg, W.E. Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch. Biochem. Biophys. 1974, 165, 691–708. [Google Scholar] [CrossRef]
- Galey, J.-F.; Galey, B.D.-L.R.; Lebkiri, A.; Pettit, L.D.; Pyburn, S.I.; Kozlowski, H. Specific interactions of the β-carboxylate group of the aspartic acid residue in oligopeptides containing one, two or three such residues with copper(II) ions. A potentiometric and spectroscopic study. J. Chem. Soc. Dalton Trans. 1991, 2281–2287. [Google Scholar] [CrossRef]
- Daniele, P.G.; Prenesti, E.; Ostacoli, G. Ultraviolet-circular dichroism spectra for structural analysis of copper(II) complexes with aliphatic and aromatic ligands in aqueous solution. J. Chem. Soc. Dalton Trans. 1996, 3269–3275. [Google Scholar] [CrossRef]
- Bellotti, D.; Sinigaglia, A.; Guerrini, R.; Marzola, E.; Rowińska-Żyrek, M.; Remelli, M. The N-terminal domain of Helicobacter pylori’s Hpn protein: The role of multiple histidine residues. J. Inorg. Biochem. 2021, 214, 111304. [Google Scholar] [CrossRef]
- Bellotti, D.; Toniolo, M.; Dudek, D.; Mikołajczyk, A.; Guerrini, R.; Matera-Witkiewicz, A.; Remelli, M.; Rowińska-Żyrek, M. Bioinorganic chemistry of calcitermin—The picklock of its antimicrobial activity. Dalton Trans. 2019, 48, 13740–13752. [Google Scholar] [CrossRef] [PubMed]
- Travaglia, A.; Arena, G.; Fattorusso, R.; Isernia, C.; La Mendola, D.; Malgieri, G.; Nicoletti, V.G.; Rizzarelli, E. The inorganic perspective of nerve growth factor: Interactions of Cu2+ and Zn2+ with the N-terminus fragment of nerve growth factor encompassing the recognition domain of the TrkA receptor. Chemistry 2011, 17, 3726–3738. [Google Scholar] [CrossRef] [PubMed]
- Grasso, G.; Magrì, A.; Bellia, F.; Pietropaolo, A.; La Mendola, D.; Rizzarelli, E. The copper(II) and zinc(II) coordination mode of HExxH and HxxEH motif in small peptides: The role of carboxylate location and hydrogen bonding network. J. Inorg. Biochem. 2014, 130, 92–102. [Google Scholar] [CrossRef] [PubMed]
- Kowalik-Jankowska, T.; Ruta-Dolejsz, M.; Wiśniewska, K.; Łankiewicz, L.; Kozłowski, H. Copper(II) complexation by human and mouse fragments (11-16) of β-amyloid peptide. J. Chem. Soc. Dalton Trans. 2000, 4511–4519. [Google Scholar] [CrossRef]
- Jezowska-Bojczuk, M.; Várnagy, K.; Sóvágó, I.; Pietrzyński, G.; Dyba, M.; Kubica, Z.; Rzeszotarska, B.; Smełka, L.; Kozłowski, H. Co-ordination of copper(II) ions by prolyl-α,β-dehydroamino acids: Comparative studies and general considerations. J. Chem. Soc. Dalton Trans. 1996, 15, 3265–3268. [Google Scholar] [CrossRef]
- Tsangaris, J.M.; Martin, R.B. Visible circular dichroism of copper(II) complexes of amino acids and peptides. J. Am. Chem. Soc. 1970, 92, 4255–4260. [Google Scholar] [CrossRef]
- Stokowa-Sołtys, K.; Kasprowicz, A.; Wrzesiński, J.; Ciesiołka, J.; Gaggelli, N.; Gaggelli, E.; Valensin, G.; Jeżowska-Bojczuk, M. Impact of Cu2+ ions on the structure of colistin and cell-free system nucleic acid degradation. J. Inorg. Biochem. 2015, 151, 67–74. [Google Scholar] [CrossRef]
- Kowalik-Jankowska, T.; Ruta, M.; Wiśniewska, K.; Łankiewicz, L. Coordination abilities of the 1-16 and 1-28 fragments of β-amyloid peptide towards copper(II) ions: A combined potentiometric and spectroscopic study. J. Inorg. Biochem. 2003, 95, 270–282. [Google Scholar] [CrossRef]
- Zoroddu, M.; Kowalik-Jankowska, T.; Kozlowski, H.; Salnikow, K.; Costa, M. Ni(II) and Cu(II) binding with a 14-aminoacid sequence of Cap43 protein, TRSRSHTSEGTRSR. J. Inorg. Biochem. 2001, 84, 47–54. [Google Scholar] [CrossRef]
- Yang, A.S.; Gunner, M.R.; Sampogna, R.; Sharp, K.; Honig, B. On the calculation of pKas in proteins. Proteins 1993, 15, 252–265. [Google Scholar] [CrossRef]
- Szczepanik, W.; Mlynarz, P.; Stefanowicz, P.; Kucharczyk-Klaminska, M.; D’Amelio, N.; Olbert-Majkut, A.; Staszewska, A.; Ratajska, M.; Szewczuk, Z.; Jezowska-Bojczuk, M. Structural studies of Cu(II) binding to the novel peptidyl derivative of quinoxaline: N-(3-(2,3-di(pyridin-2-yl)quinoxalin-6-yl)alanyl)glycine. Polyhedron 2011, 30, 9–15. [Google Scholar] [CrossRef]
- Stokowa-Sołtys, K.; Dzyhovskyi, V.; Wieczorek, R.; Jeżowska-Bojczuk, M. Coordination pattern and reactivity of two model peptides from porin protein P1. J. Inorg. Biochem. 2021, 215, 111332. [Google Scholar] [CrossRef] [PubMed]
- Wilmes, A.; Crean, D.; Aydin, S.; Pfaller, W.; Jennings, P.; Leonard, M.O. Identification and dissection of the Nrf2 mediated oxidative stress pathway in human renal proximal tubule toxicity. Toxicol. In Vitro 2011, 25, 613–622. [Google Scholar] [CrossRef]
- Breslow, R.; Anslyn, E.; Huang, D. Ribonuclease mimics. Tetrahedron 1991, 47, 2365–2376. [Google Scholar] [CrossRef]
- Young, M.; Chin, J. Dinuclear copper(II) complex that hydrolyzes RNA. J. Am. Chem. Soc. 1995, 117, 10577–10578. [Google Scholar] [CrossRef]
- Rammo, J.; Hettich, R.; Roigk, A.; Schneider, H. Catalysis of DNA cleavage by lanthanide complexes with nucleophilic or intercalating ligands and their kinetic characterization. Chem. Commun. 1996, 105–107. [Google Scholar] [CrossRef]
- Alla, N.R.; Nicholson, A.W. Evidence for a dual functional role of a conserved histidine in RNA·DNA heteroduplex cleavage by human RNase H1. FEBS J. 2012, 279, 4492–4500. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, Y.; Chen, X.; Sun, M.; Wan, R.; Zhu, C.; Li, Y.; Zhao, Y. DNA cleavage function of seryl-histidine dipeptide and its application. Amino Acids 2008, 35, 251–256. [Google Scholar] [CrossRef] [PubMed]
- Gans, P.; Sabatini, A.; Vacca, A. Superquad—An improved general program for computation of formation-constants from potentiometric data. J. Chem. Soc. Dalton Trans. 1985, 1195–1200. [Google Scholar] [CrossRef]
- Gans, P.; Sabatini, A.; Vacca, A. Investigation of equilibria in solution. Determination of equilibrium constants with the HYPERQUAD suite of programs. Talanta 1996, 43, 1739–1753. [Google Scholar] [CrossRef]
- Mielke, Z.; Latajka, Z.; Olbert-Majkut, A.; Wieczorek, R. Matrix infrared spectra and ab initio calculations of the nitrous acid compelxes with nitrogen monoxide. J. Phys. Chem. A 2000, 104, 3764–3769. [Google Scholar] [CrossRef]
- Wieczorek, R.; Latajka, Z.; Lundell, J. Quantum chemical study of the bimolecular complex of HONO. J. Phys. Chem. A 1999, 103, 6234–6239. [Google Scholar] [CrossRef]
- Olszewski, T.K.; Wojaczyńska, E.; Wieczorek, R.; Bąkowicz, J. α-Hydroxyphosphonic acid derivatives of 2-azanorbornane: Synthesis, DFT calculations, and crystal structure analysis. Tetrahedron-Asymmetry 2015, 26, 601–607. [Google Scholar] [CrossRef]
- Salvador, P.; Wieczorek, R.; Dannenberg, J.J. Direct calculation oftranshydrogen-bond 13C-15N 3-bond J-couplings in entire polyalanine α-helices. A density functional theory study. J. Phys. Chem. B 2007, 111, 2398–2403. [Google Scholar] [CrossRef]
- Rudowska, M.; Wieczorek, R.; Kluczyk, A.; Stefanowicz, P.; Szewczuk, Z. Gas-phase fragmentation of oligoproline peptide ions lacking easily mobilizable protons. J. Am. Soc. Mass Spectrom. 2013, 24, 846–856. [Google Scholar] [CrossRef] [Green Version]
- Gumienna-Kontecka, E.; Berthon, G.; Fritsky, I.O.; Wieczorek, R.; Latajka, Z.; Kozłowski, H. 2-(Hydroxyimino)propanohydroxamic acid, a new effective ligand for aluminium. J. Chem. Soc. Dalton Trans. 2000, 4201–4208. [Google Scholar] [CrossRef]
- Pontecchiani, F.; Simonovsky, E.; Wieczorek, R.; Barbosa, N.; Rowinska-Zyrek, M.; Potocki, S.; Remelli, M.; Miller, Y.; Kozlowski, H. The unusual binding mechanism of Cu(II) ions to the poly-histidyl domain of a peptide found in the venom of an African viper. Dalton Trans. 2014, 43, 16680–16689. [Google Scholar] [CrossRef] [PubMed]
- Cammi, R. Molecular Response Functions for the Polarizable Continuum Model: Physical Basis and Quantum Mechanical Formalism, 1st ed.; Springer International Publishing: Berlin/Heidelberg, Germany, 2013. [Google Scholar]
- Frisch, M.J.; Trucks, G.W.; Schlegel, H.B.; Scuseria, G.E.; Robb, M.A.; Cheeseman, J.R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G.A. (Eds.) Gaussian 09, Revision E.01; Gaussian, Inc.: Wallingford, CT, USA, 2009. [Google Scholar]
- Chai, J.D.; Head-Gordon, M. Long-range corrected hybrid density functionals with damped atom-atom dispersion corrections. Phys. Chem. Chem. Phys. 2008, 10, 6615–6620. [Google Scholar] [CrossRef] [Green Version]
- World Health Organization. Cancer. 2019. Available online: https://www.who.int/health-topics/cancer#tab=tab_1 (accessed on 19 April 2019).
- Bullman, S.; Pedamallu, C.; Sicinska, E.; Clancy, T.; Ogino, S.; Tabernero, J.; Fuchs, C.; Hahn, W.; Nuciforo, P.; Meyerson, M. Fusobacterium and co-occurring microbes in primary and metastatic colorectal cancer. Cancer Res. 2018, 78. [Google Scholar] [CrossRef]
- Bhatt, A.; Redinbo, M.; Bultman, S. The Role of the Microbiome in Cancer Development and Therapy. CA Cancer J. Clin. 2017, 67, 327–344. [Google Scholar] [CrossRef] [Green Version]
- Lesiów, M.K.; Komarnicka, U.K.; Stokowa-Sołtys, K.; Rolka, K.; Łęgowska, A.; Ptaszyńska, N.; Wieczorek, R.; Kyzioł, A.; Jeżowska-Bojczuk, M. Relationship between copper(ii) complexes with FomA adhesin fragments of F. nucleatum and colorectal cancer. Coordination pattern and ability to promote ROS production. Dalton Trans. 2018, 47, 5445–5458. [Google Scholar] [CrossRef]
- Kędziora, A.; Lesiów, M.K.; Krupa, K.; Korzeniowska-Kowal, A.; Adamski, R.; Komarnicka, U.K.; Stokowa-Sołtys, K.; Bugla-Płoskońska, G.; Jeżowska-Bojczuk, M. Protocol of proceedings with. Future Microbiol. 2020, 15, 259–271. [Google Scholar] [CrossRef] [PubMed]
Species | Potentiometry | UV-Vis | CD | EPR | ||||
---|---|---|---|---|---|---|---|---|
Logβ a | pKa b | Λ | Ε | Λ | Δε | A‖ | g‖ | |
[nm] | [M−1 cm−1] | [nm] | [M−1 cm−1] | [G] | ||||
Ac-AKGHEHQLE-NH2 (L1) | ||||||||
CuH2L1 | 21.01(2) | 6.13 | 255 sh | 39,870 | 231 | −2.59 | 143 | 2.335 |
700 | 40 | 255 | +0.83 | |||||
CuHL1 | 14.88(2) | 6.56 | - | - | - | - | 167 | 2.300 |
CuL1 | 8.32(2) | 7.43 | 255 sh 600 | 49,210 97 | 221 248 292 sh 337 505 645 | −6.66 +6.06 +2.55 −1.24 +0.43 −0.19 | 185 | 2.264 |
CuH-1L1 | 0.89(1) | 9.88 | 255 sh 540 | 62,300 170 | 221 249 292 sh 337 400 510 644 | −6.75 +7.79 +2.93 −1.80 +0.18 +0.45 −0.29 | 190 | 2.197 |
CuH-2L1 | −8.99(2) | - | 255 sh 540 | 62,349 170 | 221 249 292 sh 337 400 510 644 | −6.75 +7.79 +2.93 −1.80 +0.18 +0.45 −0.29 | 193 | 2.188 |
Ac-FGEHEHGRD-NH2 (L2) | ||||||||
CuH2L2 | 21.47(1) | 5.61 | 250 sh 707 | 25,200 38 | 238 250 sh | −7.26 −2.34 | 141 | 2.338 |
CuHL2 | 15.86(2) | 6.65 | 250 sh 610 | 48,400 98 | 237 250 sh 650 | −9.23 −4.90 +0.56 | 165 | 2.295 |
CuL2 | 9.21(2) | 7.15 | 250 sh 575 | 48,620 106 | 235 250 sh 325 635 | −14.71 −4.90 −1.23 +0.63 | 180 | 2.215 |
CuH-1L2 | 2.06(3) | 9.11 | 255 sh 540 | 61,450 114 | 230 260 290 340 590 640 | −14.80 +4.80 +2.63 −2.43 +0.50 −0.21 | 190 | 2.199 |
CuH-2L2 | −7.05(2) | 10.39 | 260 sh 540 | 70,140 178 | 230 250 280 315 610 690 | −14.80 +2.53 +2.54 −2.50 +1.50 −1.11 | 190 | 2.199 |
CuH-3L2 | −17.44(4) | - | 260 sh 540 | 70,140 178 | 230 250 280 315 610 690 | −14.80 +2.53 +2.54 −2.50 +1.50 −1.11 | 198 | 2.193 |
CuH2L | CuHL | CuL | CuH-1L | |
---|---|---|---|---|
Ac-AKGHEHQLE-NH2 (L1) | ||||
H6 (N1) | 1.862 | 1.941 | 1.992 | 1.994 |
H4 (N2) | 1.919 | 1.888 | 2.013 | |
E9 (amide N3) | 2.074 | 2.011 | ||
L8 (amide N4) | 2.353 | |||
E9 O1 | 1.777 | 2.043 | 2.554 | 2.033 |
E9 O2 | 2.047 | |||
Ac-FGEHEHGRD-NH2 (L2) | ||||
H4 (N1) | 1.829 | 1.829 | 1.833 | 1.910 |
H6 (N2) | 1.851 | 2.210 | 1.828 | |
H4 (amide N3) | 1.872 | 1.839 | ||
H6 (amide N4) | 1.919 | |||
H6 (carbonyl O) | 1.834 | 1.887 | 1.912 | |
E3 O1 | 1.910 | 1.836 |
Residue | H..PA [Å] | PD-H..PA [deg] | Fragment |
---|---|---|---|
CuH2L1 | |||
Ac..H4 | 1.718 | 159.8 | O..H*-N* |
Ac..E5 | 1.905 | 161.9 | O..H*-N* |
E5..K2 | 2.100 | 150.3 | O..H-N (alpha helix) |
G3..E5 | 1.906 | 154.5 | N-H..O* |
CuHL1 | |||
Q7..E9 | 1.904 | 170.2 | N*-H*..O* |
E5..K2 | 1.833 | 162.6 | O..H-N (alpha helix) |
K2..G3 | 1.913 | 155.2 | O*..H-N |
L8..E5 | 1.968 | 160.1 | O..H-N (alpha helix) |
CuL1 | |||
E5..K2 | 1.885 | 162.2 | O..H-N (alpha helix) |
K2..G3 | 1.980 | 168.3 | O*..H-N |
CuH-1L1 | |||
K2..G3 | 1.914 | 169.4 | O*..H-N |
K2..H4 | 1.850 | 154.6 | O*..H-N |
Residue | H..PA [Å] | PD-H..PA [deg] | Fragment |
---|---|---|---|
CuH2L2 | |||
D9..H6 | 1.984 | 151.7 | O*..H*-N* |
D9..NH2 (C-terminus) | 1.866 | 166.4 | O*..H-N |
R8..R8 | 1.837 | 165.9 | N*-H*..O |
R8..E3 | 1.831 | 167.4 | N*-H*..O |
R8..Ac | 1.884 | 151.9 | N*-H*..O |
E3..G7 | 1.930 | 166.9 | O*..H-N |
E3..R8 | 1.792 | 175.5 | O*..H-N |
CuHL2 | |||
D9..NH2 (C-terminus) | 1.832 | 153.8 | O*..H-N |
R8..R8 | 1.856 | 158.3 | N*-H*..O |
R8..Ac | 1.891 | 150.6 | N*-H*..O |
R8..E3 | 2.267 | 165.6 | N*-H*..O |
H6..F1 | 1.936 | 162.9 | N*-H*..O |
H6..E5 | 1.873 | 158.3 | N-H..O* |
CuL2 | |||
D9..NH2 (C-terminus) | 1.828 | 153.7 | O*..H-N |
R8..D9 | 1.848 | 153.7 | N*-H*..O |
R8..H6 | 1.765 | 168.8 | N*-H*..O |
E5..R8 | 2.061 | 172.3 | O..H-N (3-10 helix) |
G7..E5 | 1.718 | 167.4 | N-H..O* |
F1..E3 | 1.851 | 1.665 | O..H-N (3-10 helix) |
CuH-1L2 | |||
D9..NH2 (C-terminus) | 1.813 | 111.2 | O*..H-N |
R8..D9 | 1.771 | 160.6 | N*-H*..O |
R8..E5 | 1.963 | 162.7 | N*-H*..O |
E5..G7 | 1.722 | 165.4 | O*..H-N |
E5..R8 | 1.901 | 162.3 | O*..H-N |
H4..E3 | 1.780 | 152.9 | N-H..O* |
F1..H4 | 1.803 | 159.5 | O..H-N (alpha helix) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Stokowa-Sołtys, K.; Wojtkowiak, K.; Dzyhovskyi, V.; Wieczorek, R. Effect of Copper(II) Ion Binding by Porin P1 Precursor Fragments from Fusobacterium nucleatum on DNA Degradation. Int. J. Mol. Sci. 2021, 22, 12541. https://doi.org/10.3390/ijms222212541
Stokowa-Sołtys K, Wojtkowiak K, Dzyhovskyi V, Wieczorek R. Effect of Copper(II) Ion Binding by Porin P1 Precursor Fragments from Fusobacterium nucleatum on DNA Degradation. International Journal of Molecular Sciences. 2021; 22(22):12541. https://doi.org/10.3390/ijms222212541
Chicago/Turabian StyleStokowa-Sołtys, Kamila, Kamil Wojtkowiak, Valentyn Dzyhovskyi, and Robert Wieczorek. 2021. "Effect of Copper(II) Ion Binding by Porin P1 Precursor Fragments from Fusobacterium nucleatum on DNA Degradation" International Journal of Molecular Sciences 22, no. 22: 12541. https://doi.org/10.3390/ijms222212541
APA StyleStokowa-Sołtys, K., Wojtkowiak, K., Dzyhovskyi, V., & Wieczorek, R. (2021). Effect of Copper(II) Ion Binding by Porin P1 Precursor Fragments from Fusobacterium nucleatum on DNA Degradation. International Journal of Molecular Sciences, 22(22), 12541. https://doi.org/10.3390/ijms222212541