Insights into the Binding Sites of Organometallic Ruthenium Anticancer Compounds on Peptides Using Ultra-High Resolution Mass Spectrometry
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- 作者：Rebecca H. Wills (1)
Abraha Habtemariam (1)
Andrea F. Lopez-Clavijo (1)
Mark P. Barrow (1)
Peter J. Sadler (1)
Peter B. O’Connor (1) - 关键词：Ruthenium ; Anticancer compounds ; FTICR mass spectrometry
- 刊名：Journal of The American Society for Mass Spectrometry
- 出版年：2014
- 出版时间：April 2014
- 年：2014
- 卷：25
- 期：4
- 页码：662-672
- 全文大小：841 KB
- 参考文献：1. Ang, W.H., Dyson, P.J.: Classical and non-classical ruthenium-based anticancer drugs: towards targeted chemotherapy. Eur. J. Inorg. Chem.
2. Ivanov, A.I., Christodoulou, J., Parkinson, J.A., Barnham, K.J., Tucker, A., Woodrow, J., Sadler, P.J.: Cisplatin binding sites on human albumin. J. Biol. Chem.
3. Zhao, T., King, F.L.: A mass spectrometric comparison of the interactions of cisplatin and transplatin with myoglobin. J. Inorg. Biochem.
4. Gibson, D., Costello, C.E.: A mass spectral study of the binding of the anticancer drug cisplatin to ubiquitin. Eur. Mass Spectrom.
5. Moreno-Gordaliza, E., Canas, B., Palacios, M.A., Gomez-Gomez, M.M.: Top-down mass spectrometric approach for the full characterization of insulin-cisplatin adducts. Anal. Chem.
6. Allardyce, C.S., Dyson, P.J., Coffey, J., Johnson, N.: Determination of drug binding sites to proteins by electrospray ionization mass spectrometry: the interaction of cisplatin with transferrin. Rapid Commun. Mass Spectrom.
7. Khalaila, I., Allardyce, C.S., Verma, C.S., Dyson, P.J.: A mass spectrometric and molecular modelling study of cisplatin binding to transferrin. Chem. BioChem.
8. Li, H.L., Zhao, Y., Phillips, H.I.A., Qi, Y.L., Lin, T.Y., Sadler, P.J., O’Connor, P.B.: Mass spectrometry evidence for cisplatin as a protein cross-linking reagent. Anal. Chem.
9. Li, H., Lin, T.-Y., Van Orden, S.L., Zhao, Y., Barrow, M.P., Pizarro, A.M., Qi, Y., Sadler, P.J., O’Connor, P.B.: Use of top-down and bottom-up Fourier transform ion cyclotron resonance mass spectrometry for mapping calmodulin sites modified by platinum anticancer drugs. Anal. Chem.
10. Rademaker-Lakhai, J.M., van den Bongard, D., Pluim, D., Beijnen, J.H., Schellens, J.H.M.: A phase I and pharmacological study with imidazolium-trans-DMSO-imidazole-tetrachlororuthenate, a novel ruthenium anticancer agent. Clin. Cancer Res.
11. Alessio, E., Mestroni, G., Bergamo, A., Sava, G.: Ruthenium antimetastatic agents. Curr. Top. Med. Chem.
12. Jakupec, M.A., Galanski, M., Arion, V.B., Hartinger, C.G., Keppler, B.K.: Antitumor metal compounds: more than theme and variations. Dalton Trans.
13. Groessl, M., Tsybin, Y.: O., Hartinger, C.G., Keppler, B.K., Dyson, P.J.: Ruthenium versus platinum: interactions of anticancer metallodrugs with duplex oligonucleotides characterized by electrospray ionization mass spectrometry. J. Biol. Inorg. Chem.
14. Kratz, F., Hartmann, M., Keppler, B., Messori, L.: The binding-properties of 2 anticancer ruthenium(III) complexes to apotransferrin. J. Biol. Chem.
15. Yan, Y.K., Melchart, M., Habtemariam, A., Sadler, P.J.: Organometallic chemistry, biology, and medicine: ruthenium arene anticancer complexes. Chem. Commun.
16. Bugarcic, T., Habtemariam, A., Deeth, R.J., Fabbiani, F.P.A., Parsons, S., Sadler, P.J.: Ruthenium(II) arene anticancer complexes with redox-active diamine ligands. Inorg. Chem.
17. Aird, R.E., Cummings, J., Ritchie, A.A., Muir, M., Morris, R.E., Chen, H., Sadler, P.J., Jodrell, D.I.: In vitro and in vivo activity and cross resistance profiles of novel ruthenium (II) organometallic arene complexes in human ovarian cancer. Br. J. Cancer
18. Morris, R.E., Aird, R.E., Murdoch, P.D., Chen, H.M., Cummings, J., Hughes, N.D., Parsons, S., Parkin, A., Boyd, G., Jodrell, D.I., Sadler, P.J.: Inhibition of cancer cell growth by ruthenium(II) arene complexes. J. Med. Chem.
19. Habtemariam, A., Melchart, M., Fernandez, R., Parsons, S., Oswald, I.D.H., Parkin, A., Fabbiani, F.P.A., Davidson, J.E., Dawson, A., Aird, R.E., Jodrell, D.I., Sadler, P.J.: Structure–activity relationships for cytotoxic ruthenium(II) arene complexes containing N, N-, N, O-, and O,O-chelating ligands. J. Med. Chem.
20. Comisarow, M.B., Marshall, A.G.: Fourier transform ion cyclotron resonance spectroscopy. Chem. Phys. Lett.
21. Wang, F.Y., Bella, J., Parkinson, J.A., Sadler, P.J.: Competitive reactions of a ruthenium arene anticancer complex with histidine, cytochrome / c, and an oligonucleotide. J. Biol. Inorg. Chem.
22. Jennings, K.R.: Collision-induced decompositions of aromatic molecular ions. Int. J. Mass Spectrom. Ion Phys.
23. Senko, M.W., Speir, J.P., McLafferty, F.W.: Collisional activation of large multiply charged ions using fourier transform mass spectrometry. Anal. Chem.
24. Zubarev, R.A., Kelleher, N.L., McLafferty, F.W.: Electron capture dissociation of multiply charged protein cations. A nonergodic process. J. Am. Chem. Soc.
25. Zubarev, R.A., Kruger, N.A., Fridriksson, E.K., Lewis, M.A., Horn, D.M., Carpenter, B.K., McLafferty, F.W.: Electron capture dissociation of gaseous multiply-charged proteins is favored at disulfide bonds and other sites of high hydrogen atom affinity. J. Am. Chem. Soc.
26. McLafferty, F.W., Horn, D.M., Breuker, K., Ge, Y., Lewis, M.A., Cerda, B., Zubarev, R.A., Carpenter, B.K.: Electron capture dissociation of gaseous multiply charged ions by Fourier-transform ion cyclotron resonance. J. Am. Soc. Mass Spectrom.
27. Syrstad, E.A., Turecek, F.: Toward a general mechanism of electron capture dissociation. J. Am. Soc. Mass Spectrom.
28. Simons, J.: Mechanisms for S–S and N–C(alpha) bond cleavage in peptide ECD and ETD mass spectrometry. Chem. Phys. Lett.
29. Iavarone, A.T., Paech, K., Williams, E.R.: Effects of charge state and cationizing agent on the electron capture dissociation of a peptide. Anal. Chem.
30. Fung, Y.M.E., Liu, H.C., Chan, T.W.D.: Electron capture dissociation of peptides metalated with alkaline-earth metal ions. J. Am. Soc. Mass Spectrom.
31. Kleinnijenhuis, A.J., Mihalca, R., Heeren, R.M.A., Heck, A.J.R.: Atypical behavior in the electron capture induced dissociation of biologically relevant transition metal ion complexes of the peptide hormone oxytocin. Int. J. Mass Spectrom.
32. Liu, H.C., Hakansson, K.: Divalent metal ion–peptide interactions probed by electron capture dissociation of trications. J. Am. Soc. Mass Spectrom.
33. Kaczorowska, M.A., Hotze, A.C.G., Hannon, M.J., Cooper, H.J.: Electron capture dissociation mass spectrometry of metallo-supramolecular complexes. J. Am. Soc. Mass Spectrom.
34. Turecek, F., Jones, J.W., Holm, A.I.S., Panja, S., Nielsen, S.B., Hvelplund, P.: Transition metals as electron traps. I. Structures, energetics, electron capture, and electron-transfer-induced dissociations of ternary copper-peptide complexes in the gas phase. J. Mass Spectrom.
35. Turecek, F., Holm, A.I.S., Panja, S., Nielsen, S.B., Hvelplund, P.: Transition metals as electron traps. II. Structures, energetics, and electron transfer dissociations of ternary Co, Ni, and Zn-peptide complexes in the gas phase. J. Mass Spectrom
36. Chen, X.F., Chan, W.Y.K., Wong, P.S., Yeung, H.S., Chan, T.W.D.: Formation of peptide radical cations (M(+center dot)) in electron capture dissociation of peptides adducted with group IIB metal ions. J. Am. Soc. Mass Spectrom.
37. Williams, J.P., Brown, J.M., Campuzano, I., Sadler, P.J.: Identifying drug metallation sites on peptides using electron transfer dissociation (ETD), collision induced dissociation (CID), and ion mobility-mass spectrometry (IM-MS). Chem. Commun.
38. McNae, I.W., Fishburne, K., Habtemariam, A., Hunter, T.M., Melchart, M., Wang, F.Y., Walkinshaw, M.D., Sadler, P.J.: Half-sandwich arene ruthenium(II)-enzyme complex. Chem. Commun.
39. Piccioli, F., Sabatini, S., Messori, L., Orioli, P., Hartinger, C.G., Keppler, B.K.: A comparative study of adduct formation between the anticancer ruthenium(III) compound HInd / trans-[RuCl4(Ind)2] and serum proteins. J. Inorg. Biochem.
40. Hartinger, C.G., Casini, A., Duhot, C., Tsybin, Y.O., Messori, L., Dyson, P.J.: Stability of an organometallic ruthenium-ubiquitin adduct in the presence of glutathione: relevance to antitumor activity. J. Inorg. Biochem.
41. Casini, A., Gabbiani, C., Michelucci, E., Pieraccini, G., Moneti, G., Dyson, P.J., Messori, L.: Exploring metallodrug–protein interactions by mass spectrometry: comparisons between platinum coordination complexes and an organometallic ruthenium compound. J. Biol. Inorg. Chem.
42. Casini, A., Karotki, A., Gabbiani, C., Rugi, F., Vasak, M., Messori, L., Dyson, P.J.: Reactivity of an antimetastatic organometallic ruthenium compound with metallothionein-2: relevance to the mechanism of action. Metallomics
43. Hu, W.B., Luo, Q., Ma, X.Y., Wu, K., Liu, J.A., Chen, Y., Xiong, S.X., Wang, J.P., Sadler, P.J., Wang, F.Y.: Arene control over thiolate to sulfinate oxidation in albumin by organometallic ruthenium anticancer complexes. Chem. Eur. J.
44. Meier, S.M., Hanif, M., Kandioller, W., Keppler, B.K., Hartinger, C.G.: Biomolecule binding versus anticancer activity: reactions of Ru(arene) (thio)pyr-(id)one compounds with amino acids and proteins. J. Inorg. Biochem.
45. Casini, A., Mastrobuoni, G., Ang, W.H., Gabbiani, C., Pieraccini, G., Moneti, G., Dyson, P.J., Messori, L.: ESI-MS characterization of protein adducts of anticancer ruthenium(II)-arene PTA (RAPTA) complexes. Chem. Med. Chem.
46. Chatterjee, S., Kundu, S., Bhattacharyya, A., Hartinger, C., Dyson, P.: The ruthenium(II)–arene compound RAPTA-C induces apoptosis in EAC cells through mitochondrial and p53–JNK pathways. J. Biol. Inorg. Chem.
47. Wu, B., Ong, M.S., Groessl, M., Adhireksan, Z., Hartinger, C.G., Dyson, P.J., Davey, C.A.: A ruthenium antimetastasis agent forms specific histone protein adducts in the nucleosome core. Chem. Eur. J.
48. Wang, Y., Vivekananda, S., Men, L., Zhang, Q.: Fragmentation of protonated ions of peptides containing cysteine, cysteine sulfinic acid, and cysteine sulfonic acid. J. Am. Soc. Mass Spectrom.
49. Claiborne, A., Yeh, J.I., Mallett, T.C., Luba, J., Crane, E.J., Charrier, V., Parsonage, D.: Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry
50. Chang, Y.-C., Huang, C.-N., Lin, C.-H., Chang, H.-C., Wu, C.-C.: Mapping protein cysteine sulfonic acid modifications with specific enrichment and mass spectrometry: An integrated approach to explore the cysteine oxidation. Proteomics
51. Winterbourn, C.C., Hampton, M.B.: Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med.
52. Caravatti, P., Allemann, M.: The ‘infinity cell- a new trapped-ion cell with radiofrequency covered trapping electrodes for Fourier transform ion cyclotron resonance mass spectrometry. Org. Mass Spectrom.
53. Williams, J.P., Lough, J.A., Campuzano, I., Richardson, K., Sadler, P.J.: Use of ion mobility mass spectrometry and a collision cross-section algorithm to study an organometallic ruthenium anticancer complex and its adducts with a DNA oligonucleotide. Rapid Commun. Mass Spectrom.
54. Hu, P., Loo, J.A.: Gas-phase coordination properties of Zn2+, Cu2+, Ni2+, and Co2+ with histidine-containing peptides. J. Am. Chem. Soc.
55. Loo, J.A., Hu, P., Smith, R.D.: Interaction of angiotensin peptides and zinc metal ions probed by electrospray ionization mass spectrometry. J. Am. Soc. Mass Spectrom.
56. Zubarev, R.A., Horn, D.M., Fridriksson, E.K., Kelleher, N.L., Kruger, N.A., Lewis, M.A., Carpenter, B.K., McLafferty, F.W.: Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem.
57. Leymarie, N., Costello, C.E., O’Connor, P.B.: Electron capture dissociation initiates a free radical reaction cascade. J. Am. Chem. Soc.
58. Belyayev, M.A., Cournoyer, J.J., Lin, C., O’Connor, P.B.: The effect of radical trap moieties on electron capture dissociation spectra of Substance P. J. Am. Soc. Mass Spectrom.
59. Hong, J., Miao, Y., Miao, R., Yang, G., Tang, H., Guo, Z., Zhu, L.: Binding sites of [Ru(bpy)2(H2O)2](BF4)2 with sulfur- and histidine-containing peptides studied by electrospray ionization mass spectrometry and tandem mass spectrometry. J. Mass Spectrom.
60. Schmidbaur, H., Classen, H.G., Helbig, J.: Aspartic and glutamic acid as ligands to alkali and alkaline-earth metals: structural chemistry as related to magnesium therapy. Angew. Chem. Int. Ed. Engl.
61. Sajadi, S.: Metal ion-binding properties of L-glutamic acid and L-aspartic acid, a comparative investigation. Nat. Sci. - 作者单位：Rebecca H. Wills (1)
Abraha Habtemariam (1)
Andrea F. Lopez-Clavijo (1)
Mark P. Barrow (1)
Peter J. Sadler (1)
Peter B. O’Connor (1)
1. Department of Chemistry, University of Warwick, Coventry, CV4 7AL, UK - ISSN：1879-1123
文摘
The binding sites of two ruthenium(II) organometallic complexes of the form [(η6-arene)Ru(N,N)Cl]+, where arene/N,N = biphenyl (bip)/bipyridine (bipy) for complex AH076, and biphenyl (bip)/o-phenylenediamine (o-pda) for complex AH078, on the peptides angiotensin and bombesin have been investigated using Fourier transform ion cyclotron resonance (FTICR) mass spectrometry. Fragmentation was performed using collisionally activated dissociation (CAD), with, in some cases, additional data being provided by electron capture dissociation (ECD). The primary binding sites were identified as methionine and histidine, with further coordination to phenylalanine, potentially through a π-stacking interaction, which has been observed here for the first time. This initial peptide study was expanded to investigate protein binding through reaction with insulin, on which the binding sites proposed are histidine, glutamic acid, and tyrosine. Further reaction of the ruthenium complexes with the oxidized B chain of insulin, in which two cysteine residues are oxidized to cysteine sulfonic acid (Cys-SO3H), and glutathione, which had been oxidized with hydrogen peroxide to convert the cysteine to cysteine sulfonic acid, provided further support for histidine and glutamic acid binding, respectively. Fig. a ?/div>