RGD labeled Ru(II) polypyridyl conjugates for platelet integrin αiIb3 recognition and as reporters of integrin conformation

Bioconjugate Chemistry

Volumn 25, Issue 5, 2014, Pages 928-944

  Adamson, Kellie ^a   Dolan, Ciaran ^a   Moran, Niamh ^b   Forster, Robert J ^a   Keyes, Tia E ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; DISSOCIATION; LUMINESCENCE; MANGANESE COMPOUNDS; PEPTIDES; RUTHENIUM COMPOUNDS;

ARG GLY ASPS; CONFORMATIONAL CHANGE; DITHIOTHREITOL; INTEGRIN ACTIVATION; INTEGRIN CONFORMATION; INTEGRINS; PHENANTHROLINES; PLATELET INTEGRIN; RGD PEPTIDE; ROTATIONAL CORRELATION TIME;

PROBES;

ARGINYLGLYCYLASPARTIC ACID; DITHIOTHREITOL; INTEGRIN; MANGANESE; RUTHENIUM ARGINYLGLYCYLASPARTIC ACID CONJUGATE; RUTHENIUM COMPLEX; UNCLASSIFIED DRUG; ARGINYL-GLYCYL-ASPARTIC ACID; FIBRINOGEN RECEPTOR; OLIGOPEPTIDE; ORGANOMETALLIC COMPOUND; POLYMER; PYRIDINE DERIVATIVE; RUTHENIUM;

ANISOTROPY; ARTICLE; CELLULAR DISTRIBUTION; CHO CELL LINE; CONFORMATIONAL TRANSITION; DISSOCIATION CONSTANT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; LUMINESCENCE; MOLECULAR PROBE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; QUANTUM YIELD; ANIMAL; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CRICETULUS; HUMAN; METABOLISM; SYNTHESIS;

ANIMALS; ANISOTROPY; CELL MEMBRANE; CHO CELLS; CRICETULUS; DITHIOTHREITOL; HUMANS; MANGANESE; MOLECULAR STRUCTURE; OLIGOPEPTIDES; ORGANOMETALLIC COMPOUNDS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; POLYMERS; PROTEIN CONFORMATION; PYRIDINES; RUTHENIUM;

EID: 84900988535     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc5000737     Document Type: Article

References (89)

1. Bennett, J. S., Berger, B. W., and Billings, P. C. (2009) J. Thromb. Haemost. 7, 200-205
2. Yan, B., Hu, D. D., Knowles, S. K., and Smith, J. W. (2000) Probing chemical and conformational differences in the resting and active conformers of platelet integrin alpha (IIb) beta (3) J. Biol. Chem. 275, 7249-7260
3. Zhu, J., Luo, B. H., Xiao, T., Zhang, C., Nishida, N., and Springer, T. A. (2008) Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces Mol. Cells 32, 849-861
4. Humphries, M. J. (2000) Integrin structure Biochem. Soc. Trans. 28, 311-339
5. Luo, B.-H., Carmen, C., and Springer, T. (2007) Structural basis of integrin regulation and signalling Annu. Rev. Immunol. 25, 619-647
6. Campbell, I. D. and Humphries, M. J. (2011) Integrin structure, activation, and interactions CSH Perspectives 4, 1-14
7. Fuss, C., Palmaz, J. C., and Sprague, E. A. (2001) Fibrinogen structure, function, and surface interactions Journal of Vascular and Interventional Radiology 12, 677-682
8. Mosesson, M. W. (2005) Fibrinogen and fibrin structure and functions J. Thromb. Haemost. 3, 1894-1904
9. Bambace, N. M. and Holmes, C. E. (2011) The platelet contribution to cancer progression J. Thromb. Haemost. 9, 237-249
10. Ma, Y. Q., Qin, J., and Plow, E. F. (2007) Platelet integrin alpha(IIb)beta(3): activation mechanisms J. Thromb. Haemost. 5, 1345-1352
11. Litvinov, R. I., Nagaswami, C., Vilaire, G., Shuman, H., Bennett, J. S., and Weisal, J. W. (2004) Functional and structural correlations of individual aIIbb3 molecules Blood 104, 3979-3985
12. Tiwari, S., Askari, J. A., Humphries, M. J., and Bulleid, N. J. (2011) Divalent cations regulate the folding and activation status of integrins during their intracellular trafficking J. Cell Sci. 124, 1672-1680
13. Yan, B. and Smith, J. W. (2001) Mechanism of integrin activation by disulfide bond reduction Biochemistry 40, 8861-8867
14. Hantgan, R. R., Rocco, M., Nagaswami, C., and Weisal, J. W. (2001) Binding of a fibrinogen mimetic stabilizes integrin aIIbb3′s open conformation Protein Sci. 10, 1614-1626
15. Takagi, J., Petre, B. M., Walz, T., and Springer, T. (2002) Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling Cell 110, 599-611
16. Hantgan, R. R., Stahle, M. C., Connor, J. H., Horita, D. A., Rocco, M., McLane, M., Yakovlev, S., and Medve, L. (2006) Integrin αIIbo3: ligand interactions are linked to binding-site remodelling Protein Sci. 15, 1893-1905
17. Hantgan, R. R., Stahle, M. C., Connor, J. H., Connor, R. F., and Mousa, S. A. (2006) αIIbo3 priming and clustering by orally active and intravenous integrin antagonists J. Thromb. Haemost. 5, 542-550
18. Gonzalez-Rodriguez, J., Acuna, A. U., Alvarez, M. V., and Jovin, T. M. (1994) Rotational mobility of the fibrinogen receptor glycoprotein IIb/IIIa or integrin.alpha.IIb.beta.3 in the plasma membrane of human platelets Biochemistry 33, 266-274
19. Ye, Y. and Chen, X. (2011) Integrin targeting for tumor optical imaging Theranostics 1, 102-126
20. Bartholomä, M. D. (2012) Recent developments in the design of bifunctional chelators for metal-based radiopharmaceuticals used in Positron Emission Tomography Inorg. Chim. Acta 389, 36-51
21. Gaertner, F. C., Kessler, H., Wester, H. J., Schwaiger, M., and Beer, A. J. (2012) Radiolabelled RGD peptides for imaging and therapy Eur. J. Nucl. Med. Mol. Imaging 39, 126-138
22. Kuil, J., Velders, A. H., and van Leeuwen, F. W. B. (2010) Multimodal tumor-targeting peptides functionalized with both a radio- and a fluorescent label Bioconjugate Chem. 10, 1709-1719
23. Wang, W., Wu, Q., Pasuelo, M., McMurray, J. S., and Li, C. (2005) Probing for integrin αvo3 binding of RGD peptides using fluorescence polarization Bioconjugate Chem. 16, 729-734
24. Zhou, Y., Chakrabortv, S., and Liu, S. (2011) Radiolabeled cyclic RGD peptides as radiotracers for imaging tumors and thrombosis by SPECT Theranostics 1, 58-82
25. Calvete, J. J., Schafer, W., Mann, K., Henschen, A., and Gonzalez-Rodriguez, J. (1992) Localization of the cross-linking sites of RGD and KQAGDV peptides to the isolated fibrinogen receptor, the human platelet integrin glycoprotein IIb/IIIa. Influence of peptide length Eur. J. Biochem. 206, 759-765
26. Kurtz, L., Kao, L., Newman, D., Kurtz, I., and Zhu, Q. (2012) Integrin αIIbo3 inside-out activation J. Biol. Chem. 287, 23255-23265
27. 6transition metal complexes in fluorescence cell imaging Chem. Commun. 46, 186-202
28. Li, L., Szmacinski, H., and Lakowicz, J. R. (1997) Synthesis and luminescence spectral characterizationof long-lifetime lipid metal-ligand probes Anal. Biochem. 244, 80-85
29. Piszczek, G. (2006) Luminescent metal-ligand complexes as probes of macromolecular interactions and biopolymer dynamics Biochem. Biophys. 453, 54-62
30. Zhang, J., Qi, H., Li, Y., Yang, J., Gao, Q., and Zhang, C. (2008) Electrogenerated chemiluminescence DNA biosensor based on hairpin DNA probe labeled with ruthenium complex Anal. Chem. 80, 2888-2894
31. Gill, M. R. and Thomas, J. A. (2012) Ruthenium(II) polypyridyl complexes and DNA-from structural probes to cellular imaging and therapeutics Chem. Soc. Rev. 41, 3179-3192
32. Slim, M. and Sleiman, H. F. (2004) Ruthenium(II)-phenanthroline-biotin complexes: synthesis and luminescence enhancement upon binding to avidin Bioconjugate Chem. 15, 949-953
33. Zsmacinski, H., Terpetschnig, E., and Lakowicz, J. R. (1996) Synthesis and evaluation of Ru-complexes as anisotropy probes for protein hydrodynamics and immunoassays of high-molecular-weight antigens Biophys. Chem. 62, 109-120
34. McConnell, A. J., Lim, M. H., Olmon, E. D., Song, H., Dervan, E. E., and Barton, J. K. (2012) Luminescent properties of ruthenium(II) complexes with sterically expansive ligands bound to DNA defects Inorg. Chem. 51, 12511-12520
35. Song, H., Kaiser, J. T., and Barton, J. K. (2012) Crystal structure of delta-[Ru(bpy)2(dppz)]2+ bound to mismatched DNA reveals side-by-side metalloinsertion and intercalation Nat. Chem. 4, 615-620
36. Puckett, C. A. and Barton, J. K. (2010) Targeting a ruthenium complex to the nucleus with short peptides Bioorg. Med. Chem. 18, 3564-3569
37. Bruijnincx, P. C. A. and Sadler, P. J. (2008) New trends for metal complexes with anticancer activity Curr. Opin. Chem. Biol. 12, 197-206
38. Meier, S. M., Novak, M., Kandioller, W., Jakupec, M. A., Arion, V. B., Metzler-Nolte, N., Keppler, B. K., and Hartinger, C. G. (2013) Identification of the structural determinants for anticancer activity of a ruthenium arene peptide conjugate Chemistry 19, 9297-9307
39. Corral, E., Hotze, A. C., den Dulk, H., Leczkowska, A., Rodger, A., Hannon, M. J., and Reekijk, J. (2009) Ruthenium polypyridyl complexes and their modes of interaction with DNA: Is there a correlation between these interactions and the antitumor activity of the compounds? J. Biol. Inorg. Chem. 14, 439-448
40. DeGraff, B. A. and Demas, J. N. (1994) Direct measurement of rotational correlation times of luminescent ruthenium(II) molecular probes by differential polarized phase fluorimetry J. Phys. Chem. 98, 12478-12480
41. Ruggi, A., van Leeuwan, F. W. B., and Velders, A. H. (2011) Interaction of dioxygen with the electronic excited state of Ir(III) and Ru(II) complexes: Principles and biomedical applications Coord. Chem. Rev. 255, 2542-2554
42. Davies, C. L., Dux, E. L., and Duhme-Klair, A.-K. (2009) Supramolecular interactions between functional metal complexes and proteins Dalton Trans. 10141-10154
43. Lo, K. W., Lee, T. K. M., Lau, J. S. Y., Poon, W. L., and Cheng, S. H. (2008) Luminescent biological probes derived from ruthenium(II) estradiol polypyridine complexes Inorg. Chem. 47, 200-208
44. Lo, K. W., Choi, A. W., and Law, W. H. (2012) Applications of luminescent inorganic and organometallic transition metal complexes as biomolecular and cellular probes Dalton Trans. 41, 6021-6047
45. Muldoon, J., Ashcroft, A. E., and Wilson, A. J. (2010) Selective protein-surface sensing using ruthenium(II) tris(bipyridine) complexes Chem.-Eur. J. 16, 100-103
46. Vergara, A., Krauss, I. R., Montesarchio, D., Paduano, L., and Merlino, A. (2013) Investigating the ruthenium metalation of proteins: X-ray structure and raman microspectroscopy of the complex between RNase A and AziRu Inorg. Chem. 52, 10714-10716
47. Li, F., Feterl, M., Warner, J. M., Day, A. I., Keene, F. R., and Collins, J. G. (2013) Protein binding by dinuclear polypyridyl ruthenium(II) complexes and the effect of cucurbit[10]uril encapsulation† Dalton Trans. 42, 8868-8877
48. Karidi, K., Ypsilantis, K., Papakyriakou, A., and Garoufis, A. (2013) Synthesis and characterization of ruthenium(II)-oligopyridine-peptide conjugates. Interactions of the diasteromeres - and -[Ru(bpy)2(4-COY-4′- Mebpy)]Cl2 (Y = Gly-Lys1-Lys2CONH2, Lys1-Gly-Lys2CONH2, Lys1-Lys2-GlyCONH2) with the oligonucleotide d(5′-CGCGAATTCGCG-3′)2 J. Inorg. Biochem. 127, 13-23
49. Blackmore, L., Moriarty, R., Dolan, C., Adamson, K., Forster, R. J., Devocelle, M., and Keyes, T. K. (2013) Peptide directed transmembrane transport and nuclear localization of Ru(II) polypyridyl complexes in mammalian cells Chem. Commun. 49, 2658-2660
50. Puckett, C. A. and Barton, J. K. (2010) Targeting a ruthenium complex to the nucleus with short peptides Bioorg. Med. Chem. 18, 3564-3569
51. Fischer, M. J. (2010) Amine coupling through EDC/NHS: A practical approach Methods Mol. Biol. 627, 55-73
52. Hermanson, G. T. (2008) Modification of amines with NHS-aldehydes (SFB and SFPA) in Bioconjugate Techniques, pp 1233, Elsevier.
53. Dolan, C., Moriarty, R., Lestini, E., Devocelle, M., Forster, R. J., and Keyes, T. E. (2013) Cell uptake and cytotoxicity of a novel cyclometalated iridium(III) complex and its octaarginine peptide conjugate J. Inorg. Biochem. 119, 65-74
54. Ruggi, A., van Leeuwan, F. W. B., and Velders, A. H. (2011) Interaction of dioxygen with the electronic excited state of Ir(III) and Ru(II) complexes: Principles and biomedical applications Coord. Chem. Rev. 255, 2542-2554
55. Kirchhofer, D., Gailit, J., Ruoslahti, E., Grzesiak, J., and Pierschbacher, M. D. (1990) Cation dependant changes in the binding specificty of the platelet receptor GPIIb/IIIa J. Biol. Chem. 265, 18525-18530
56. Hsu, C.-C., Chuang, W.-J., Chang, C.-H., Tseng, Y.-L., Peng, H.-C., and Huang, T.-F. (2011) Improvements in endotoxemic syndromes using a disintegrin, rhodostomin, through integrin avb3-dependent pathway J. Thromb. Haemost. 9, 593-602
57. Szmacinski, H., Castellano, F. N., Terpetschnig, E., Dattelbaum, J. D., Lakowicz, J. R., and Meyer, G. J. (1998) Long-lifetime Ru II complexes for the measurement of high molecular weight protein hydrodynamics Biochim. Biophys. Acta 1383, 151-159
58. Hantgan, R. R., Paumi, C., Rocco, M., and Weisel, J. W. (1999) Effects of ligand-mimetic peptides Arg-Gly-Asp-X (X Phe, Trp, Ser) on αIIbo3 integrin conformation and oligomerization Biochemistry 38, 14461-14474
59. Hantgan, R. R., Lyles, D. S., Mallett, T. C., Rocco, M., Nagaswami, C., and Weisel, J. (2003) Ligand binding promotes the entropy-driven oligomerization of integrin αIIbo3 J. Biol. Chem. 278, 3417-3426
60. Hantgan, R. R., Rocco, M., Nagaswami, C., and Weisal, J. W. (2001) Binding of a fibrinogen mimetic stabilizes integrin αIIbo3′s open conformation Protein Sci. 10, 1614-1626
61. Schror, K. and Weber, A.-A. (2003) Comparative pharmacology of GP IIb/IIIa antagonists J. Thromb. Thrombolys. 15, 71-80
62. 2+-dependent binding of a synthetic Arg-Gly-Asp (RGD) peptide to a single site on the purified platelet glycoprotein IIb-IIIa complex J. Biol. Chem. 264, 13102-13108
63. Pfaff, M., Tangemann, K., Muller, B., Gurrath, M., Muller, G., Kessler, H., Timple, R., and Engel, J. (1994) Selective recognition of cyclic RGD peptides of NMR defined conformation by αIIbo3, αVo3, and α5ol Integrins J. Biol. Chem. 269, 20293-20238
64. Litvinov, R. I., Nagaswami, C., Vilaire, G., Shuman, H., Bennett, J. S., and Weisal, J. W. (2004) Functional and structural correlations of individual αIIbo3 molecules Blood 104, 3979-3985
65. Xiong, J. P., Stehle, T., Diefenbach, B., Zhang, R., Dunker, R., Scott, D. L., Joachimiak, A., Goodman, S. L., and Arnaout, M. A. (2001) Crystal structure of the extracellular segment of integrin alpha Vbeta3 Science 294, 339-345
66. Xiong, J. P., Stehle, T., Zhang, R., Joachimiak, A., Frech, A., Goodman, S. L., and Arnaout, M. A. (2002) Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand Science 296, 151-155
67. Gailit, J. and Ruoslahti, E. (1988) Regulation of the fibronectin receptor affinity by divalent cations J. Biol. Chem. 263, 12927-12932
68. Hautanen, A., Gailit, J., Mann, D. M., and Ruoslahti, E. (1989) Effects of modifications of the RGD sequence and its context on recognition by the fibronectin receptor* J. Biol. Chem. 264, 1437-1442
69. Litvinov, R. I., Mekler, A., Shuman, H., Bennett, J. S., Barsegov, V., and Weisel, J. W. (2012) Resolving two-dimensional kinetics of the integrin IIb 3-fibrinogen interactions using binding-unbinding correlation spectroscopy J. Biol. Chem. 287, 35275-35285
70. Takagi, J., Petre, B. M., Walz, T., and Springer, T. (2002) Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling Cell 110, 599-611
71. Xiong, J. P., Stehle, T., Goodman, S. L., and Arnaout, M. A. (2003) Integrins, cations and ligands: making the connection J. Thromb. Haemost. 1, 1642-1654
72. 3 receptor on resting and activated human platelets Biochemistry 301, 429-436
73. Bednar, R. A., Lee Gaul, S., Hamill, T. G., Egbertson, M. S., Shafer, J. A., Hartman, G. A., Gould, R. J., and Bednar, B. (1998) Identification of low molecular weight gp iib/iiia antagonists that bind preferentially to activated platelets J. Pharmocol. Exp. Ther. 285, 1317-1326
74. 3* J. Biol. Chem. 274, 4633-4639
75. Sanchez-Cortes, J. and Mrksich, M. (2009) The platelet integrin aIIbb3 binds to the RGD and AGD motifs in fibrinogen Chem. Biol. 16, 990-1000
76. Kamata, T., Ambo, H., Puzon-McLaughlin, W., Tieu, K. K., Handa, M., Ikeda, Y., and Takada, Y. (2004) Critical cysteine residues for regulation of integrin alphaIIbbeta3 are clustered in the epidermal growth factor domains of the beta3 subunit Biochem. J. 378, 1079-1082
77. ONeill, S., Robinson, A., Deering, A., Ryan, M., Fitzgerald, D. J., and Moran, N. (2000) The platelet integrin αIIbo3 has an endogenous thiol isomerase activity* J. Biol. Chem. 275, 36984-36990
78. Kamata, T., Handa, M., Sato, Y., Ikeda, Y., and Aiso, S. (2005) Membrane-proximal α/o stalk interactions differentially regulate integrin activation* J. Biol. Chem. 280, 24775-24783
79. Leane, D., Walsh, G., Moran, N., Forster, R. J., Kenny, D., ONeill, S., and Keyes, T. E. (2007) Activation induced conformational changes within the platelet integrin aIIbb3 using surface enhanced raman spectroscopy Biochemistry 46, 6429-6436
80. Garrigues, H. J., Rubinchikova, Y. R., DiPersio, C. M., and Rose, T. M. (2008) Integrin αVo3 binds to the RGD motif of glycoprotein B of Kaposis aarcoma-associated herpesvirus and functions as an RGD-dependent entry receptor J. Virol. 82, 1570-1580
81. Schwarz, M., Meade, G., Stoll, P., Ylanne, J., Bassler, N., Chen, Y. C., Hagemeyer, C. E., Ahrens, I., Moran, N., Kenny, D., Fitzgerald, D., Bode, C., and Peter, K. (2006) Conformation-specific blockade of the integrin GPIIb/IIIa a novel antiplatelet strategy that selectively targets activated platelets Mol. Med. 99, 25-33
82. Xiao, T., Takagi, J., Coller, B. S., Wang, J. H., and Springer, T. A. (2004) Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics Nature 432, 59-67
83. Bella, J. and Humphries, M. J. (2005) Cα- H···O=C hydrogen bonds contribute to the specificity of RGD cell-adhesion interactions. BMC Struct. Biol. 5.
84. Pellegrin, Y., Forster, R. J., and Keyes, T. E. (2009) PH dependant photophysics and role of medium on photoinduced electron transfer between ruthenium polypyridyl complex and anthraquinone Inorg. Chim. Acta 362, 1715-1722
85. Sullivan, B. P., Salmon, D. J., and Meyer, T. J. (1978) Mixed phosphine 2,2′-bipyridine complexes of ruthenium, pp 3334-3341, Vol 17.
86. Goldstein, B. M., Barton, J. K., and Berman, H. M. (1986) Crystal and molecular structure of a chiral-specific DNA-binding agent: tris(4,7-diphenyl-1, 10-phenanthroline)ruthenium(II) Inorg. Chem. 25, 842-847
87. Cosgrave, L., Devocelle, M., Forster, R. J., and Keyes, T. E. (2010) Multimodal cell imaging by ruthenium polypyridyl labelled cell penetrating peptides Chem. Commun. 46, 103-105
88. Williams, A. T. R., Winfield, S. A., and Miller, J. N. (1983) Relative fluorescence quantum yields using a computer controlled luminescence spectrometer Analyst 108, 1067
89. Pederson, S. E., Lurtz, M. M., and Papineni, R. V. L. (2010) Ligand binding methods for analysis of ion channel structure and function, in Essential Ion Methods (Conn, M. P., Ed.) pp 249, Baker and Taylor.