Target-directed catalytic metallodrugs

Brazilian Journal of Medical and Biological Research

Volumn 46, Issue 6, 2013, Pages 465-485

  Joyner, J C ^a,b,c   Cowan, J A ^a,b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b MetalloPharm LLC ^*  (United States)

^c MetalloPharm LLC   (United States)

Author keywords

Angiotensin converting enzyme; Artificial nuclease; Artificial protease; Catalytic metallodrug; Hiv; Ribonuclease mimic

Indexed keywords

DEOXYRIBONUCLEASE; DIPEPTIDYL CARBOXYPEPTIDASE; LISINOPRIL; MESSENGER RNA; METAL CHELATE; METAL DERIVATIVE; REACTIVE OXYGEN METABOLITE;

ARTICLE; BINDING AFFINITY; CATALYST; CHEMICAL MODIFICATION; DISSOCIATION CONSTANT; DRUG MEGADOSE; DRUG STABILITY; DRUG TARGETING; ELECTRON TRANSPORT; HEART FAILURE; HUMAN; HYPERTENSION; IC 50; LIMIT OF DETECTION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; OXIDATION REDUCTION POTENTIAL; RNA CLEAVAGE; STOICHIOMETRY;

BIOLOGICAL AVAILABILITY; CATALYSIS; COORDINATION COMPLEXES; GENES, ENV; HUMANS; MOLECULAR TARGETED THERAPY; OXIDATION-REDUCTION; PEPTIDE HYDROLASES; PEPTIDYL-DIPEPTIDASE A; REACTIVE OXYGEN SPECIES;

EID: 84880342071     PISSN: 0100879X     EISSN: 1414431X     Source Type: Journal    
DOI: 10.1590/1414-431X20133086     Document Type: Article

References (84)

1. Hocharoen L, Cowan JA. Metallotherapeutics: novel strategies in drug design. Chemistry 2009; 15: 8670-8676, doi: 10.1002/chem.200900821.
2. Cowan JA. Catalytic metallodrugs. Pure Appl Chem 2008; 80: 1799-1810, doi: 10.1351/pac200880081799.
3. Bradford S, Cowan JA. Catalytic metallodrugs targeting HCV IRES RNA. Chem Commun 2012; 48: 3118-3120, doi: 10.1039/c2cc17377h.
4. Joyner JC, Keuper KD, Cowan JA. DNA nuclease activity of Rev-coupled transition metal chelates. Dalton Trans 2012; 41: 6567-6578, doi: 10.1039/c2dt00026a.
5. Gokhale NH, Cowan JA. Metallopeptide-promoted inactivation of angiotensin-converting enzyme and endothelinconverting enzyme 1: Toward dual-action therapeutics. J Biol Inorg Chem 2006; 11: 937-947, doi: 10.1007/s00775006-0145-2.
6. Gokhale NH, Bradford S, Cowan JA. Catalytic inactivation of human carbonic anhydrase I by a metallopeptide-sulfonamide conjugate is mediated by oxidation of active site residues. J Am Chem Soc 2008; 130: 2388-2389, doi: 10.1021/ja0778038.
7. Lee J, Udugamasooriya DG, Lim HS, Kodadek T. Potent and selective photo-inactivation of proteins with peptoidruthenium conjugates. Nat Chem Biol 2010; 6: 258-260, doi: 10.1038/nchembio.333.
8. Gallagher J, Zelenko O, Walts AD, Sigman DS. Protease activity of 1,10-phenanthroline-copper(I). Targeted scission of the catalytic site of carbonic anhydrase. Biochemistry 1998; 37: 2096-2104, doi: 10.1021/bi971565j.
9. Suh J, Yoo SH, Kim MG, Jeong K, Ahn JY, Kim MS, et al. Cleavage agents for soluble oligomers of amyloid beta peptides. Angew Chem Int Ed Engl 2007; 46: 7064-7067, doi: 10.1002/anie.200702399.
10. Kim MG, Kim MS, Lee SD, Suh J. Peptide-cleaving catalyst selective for melanin-concentrating hormone: Oxidative decarboxylation of N-terminal aspartate catalyzed by Co(III)cyclen. J Biol Inorg Chem 2006; 11: 867-875, doi: 10.1007/s00775-006-0139-0.
11. Suh J, Chei WS. Metal complexes as artificial proteases: toward catalytic drugs. Curr Opin Chem Biol 2008; 12: 207-213, doi: 10.1016/j.cbpa.2008.01.028.
12. Jeong K, Chung WY, Kye YS, Kim D. Cu(II) cyclen cleavage agent for human islet amyloid peptide. Bioorg Med Chem 2010; 18: 2598-2601, doi: 10.1016/j.bmc.2010.02.045.
13. Chei WS, Ju H, Suh J. New chelating ligands for Co(III) based peptide-cleaving catalysts selective for pathogenic proteins of amyloidoses. J Biol Inorg Chem 2011; 16: 511-519, doi: 10.1007/s00775-010-0750-y.
14. Suh J, Chei WS, Lee TY, Kim MG, Yoo SH, Jeong K, et al. Cleavage agents for soluble oligomers of human islet amyloid polypeptide. J Biol Inorg Chem 2008; 13: 693-701, doi: 10.1007/s00775-008-0354-y.
15. Meggers E. Targeting proteins with metal complexes. Chem Commun 2009; 1001-1010, doi: 10.1039/b813568a.
16. Brown KC, Yang SH, Kodadek T. Highly specific oxidative cross-linking of proteins mediated by a nickel-peptide complex. Biochemistry 1995; 34: 4733-4739, doi: 10.1021/ bi00014a030.
17. Joyner JC, Hocharoen L, Cowan JA. Targeted catalytic inactivation of angiotensin converting enzyme by lisinoprilcoupled transition-metal chelates. J Am Chem Soc 2012; 134: 3396-3410, doi: 10.1021/ja208791f.
18. Joyner JC, Cowan JA. Targeted cleavage of HIV RRE RNA by Rev-coupled transition metal chelates. J Am Chem Soc 2011; 133: 9912-9922, doi: 10.1021/ja203057z.
19. Joyner JC, Reichfield J, Cowan JA. Factors influencing the DNA nuclease activity of iron, cobalt, nickel, and copper chelates. J Am Chem Soc 2011; 133: 15613-15626, doi: 10.1021/ja2052599.
20. Bradford S, Kawarasaki Y, Cowan JA. Copper.Lys-Gly-HisLys mediated cleavage of tRNA(Phe): studies of reaction mechanism and cleavage specificity. J Inorg Biochem 2009; 103: 871-875, doi: 10.1016/j.jinorgbio.2009.03.003.
21. Jin Y, Cowan JA. DNA cleavage by copper-ATCUN complexes. Factors influencing cleavage mechanism and linearization of dsDNA. J Am Chem Soc 2005; 127: 8408-8415, doi: 10.1021/ja0503985.
22. Jin Y, Cowan JA. Targeted cleavage of HIV rev response element RNA by metallopeptide complexes. J Am Chem Soc 2006; 128: 410-411, doi: 10.1021/ja055272m.
23. Jin Y, Cowan JA. Cellular activity of Rev response element RNA targeting metallopeptides. J Biol Inorg Chem 2007; 12: 637-644, doi: 10.1007/s00775-007-0221-2.
24. Jin Y, Lewis MA, Gokhale NH, Long EC, Cowan JA. Influence of stereochemistry and redox potentials on the singleand double-strand DNA cleavage efficiency of Cu(II) and Ni(II) Lys-Gly-His-derived ATCUN metallopeptides. J Am Chem Soc 2007; 129: 8353-8361, doi: 10.1021/ ja0705083.
25. Sigman DS. Chemical nucleases. Biochemistry 1990; 29: 9097-9105, doi: 10.1021/bi00491a001.
26. Sigman DS, Bruice T, Mazumder A, Sutton CL. Targeted chemical nucleases. Acc Chem Res 1993; 26: 98-104, doi: 10.1021/ar00027a004.
27. Joyner JC, Hodnick WF, Cowan AS, Tamuly D, Boyd R, Cowan JA. Antimicrobial metallopeptides with broad nuclease and ribonuclease activity. Chem Commun 2013; 49: 2118-2120, doi: 10.1039/c3cc38977d.
28. Fitzsimons MP, Barton JK. Design of a synthetic nuclease: DNA hydrolysis by a zinc-binding peptide pethered to a rhodium intercalator. J Am Chem Soc 1997; 119: 3379-3380, doi: 10.1021/ja9633981.
29. Jeung CS, Kim CH, Min K, Suh SW, Suh J. Hydrolysis of plasmid DNA catalyzed by Co(III) complex of cyclen attached to polystyrene. Bioorg Med Chem Lett 2001; 11: 2401-2404, doi: 10.1016/S0960-894X(01)00439-5.
30. Matsumura K, Komiyama M. Enormously fast RNA hydrolysis by lanthanide(III) ions under physiological conditions: eminent candidates for novel tools of biotechnology. J Biochem 1997; 122: 387-394, doi: 10.1093/oxfordjournals.jbchem.a021765.
31. Pei D, Corey DR, Schultz PG. Site-specific cleavage of duplex DNA by a semisynthetic nuclease via triple-helix formation. Proc Natl Acad Sci U S A 1990; 87: 9858-9862, doi: 10.1073/pnas.87.24.9858.
32. Pei D, Schultz PG. Artificial nucleases. In: Linn SM (Editor), Nucleases. New York: Cold Spring Harbor Laboratory Press; 1993. p 317-340.
33. Joyce LE, Aguirre JD, Angeles-Boza AM, Chouai A, Fu PK, Dunbar KR, et al. Photophysical properties, DNA photocleavage, and photocytotoxicity of a series of dppn dirhodium(II,II) complexes. Inorg Chem 2010; 49: 5371-5376, doi: 10.1021/ic100588d.
34. Sun Y, Joyce LE, Dickson NM, Turro C. DNA photocleavage by an osmium(II) complex in the PDT window. Chem Commun 2010; 46: 6759-6761, doi: 10.1039/c0cc02571b.
35. Magda D, Wright M, Crofts S, Lin A, Sessler JL. Metal complex conjugates of antisense DNA which display ribozyme-like activity. J Am Chem Soc 1997; 6947-6948, doi: 10.1021/ja9711223.
36. Boulikas T, Vougiouka M. Cisplatin and platinum drugs at the molecular level. (Review). Oncol Rep 2003; 10: 1663-1682.
37. Go RS, Adjei AA. Review of the comparative pharmacology and clinical activity of cisplatin and carboplatin. J Clin Oncol 1999; 17: 409-422.
38. Crook TR, Souhami RL, McLean AE. Cytotoxicity, DNA cross-linking, and single strand breaks induced by activated cyclophosphamide and acrolein in human leukemia cells. Cancer Res 1986; 46: 5029-5034.
39. Mattes WB, Hartley JA, Kohn KW. DNA sequence selectivity of guanine-N7 alkylation by nitrogen mustards. Nucleic Acids Res 1986; 14: 2971-2987, doi: 10.1093/nar/14.7.2971.
40. Boger DL, Garbaccio RM. Shape-dependent catalysis: insights into the source of catalysis for the CC-1065 and duocarmycin DNA alkylation reaction. Ac Chem Res 1999; 32: 1043-1052, doi: 10.1021/ar9800946.
41. Minoshima M, Bando T, Shinohara K, Sugiyama H. Molecular design of sequence specific DNA alkylating agents. Nucleic Acids Symp Ser 2009; 69-70, doi: 10.1093/nass/nrp035.
42. Graf E, Mahoney JR, Bryant RG, Eaton JW. Iron-catalyzed hydroxyl radical formation. Stringent requirement for free iron coordination site. J Biol Chem 1984; 259: 3620-3624.
43. Inoue S, Kawanishi S. Hydroxyl radical production and human DNA damage induced by ferric nitrilotriacetate and hydrogen peroxide. Cancer Res 1987; 47: 6522-6527.
44. Oberley LW, Buettner GR. The production of hydroxyl radical by bleomycin and iron(II). FEBS Lett 1979; 97: 47-49, doi: 10.1016/0014-5793(79)80049-6.
45. Pou S, Bhan A, Bhadti VS, Wu SY, Hosmane RS, Rosen GM. The use of fluorophore-containing spin traps as potential probes to localize free radicals in cells with fluorescence imaging methods. FASEB J 1995; 9: 1085-1090.
46. Samuni A, Goldstein S, Russo A, Mitchell JB, Krishna MC, Neta P. Kinetics and mechanism of hydroxyl radical and OH-adduct radical reactions with nitroxides and with their hydroxylamines. J Am Chem Soc 2002; 124: 8719-8724, doi: 10.1021/ja017587h.
47. Matko J, Ohki K, Edidin M. Luminescence quenching by nitroxide spin labels in aqueous solution: studies on the mechanism of quenching. Biochemistry 1992; 31: 703-711, doi: 10.1021/bi00118a010.
48. Yu F, Xu D, Lei R, Li N, Li K. Free-radical scavenging capacity using the fenton reaction with rhodamine B as the spectrophotometric indicator. J Agric Food Chem 2008; 56: 730-735, doi: 10.1021/jf072383r.
49. Azab HA, Banci L, Borsari M, Luchinat C, Sola M, Viezzoli MS. Redox chemistry of superoxide dismutase. Cyclic voltammetry of wild-type enzymes and mutants on functionally relevant residues. Inorg Chem 1992; 31: 4649-4655, doi: 10.1021/ic00048a037.
50. Barrette WC Jr, Sawyer DT, Fee JA, Asada K. Potentiometric titrations and oxidation reduction potentials of several iron superoxide dismutases. Biochemistry 1983; 22: 624-627, doi: 10.1021/bi00272a015.
51. Finnen D, Pinkerton A, Dunham WR, Sands RH, Funk MO. Structures and spectroscopic characteristics of iron(III) diethylenetriaminepentaacetic acid complexes. A non-heme iron(III) complex with relevance to the iron environment in lipoxygenases. Inorg Chem 1990; 30: 3960-3964, doi: 10.1021/ ic00020a034.
52. 4DOTA): Structural overview and analyses on structure-stability relationships. Coordin Chem Rev 2009; 253: 1906-1925, doi: 10.1016/j.ccr.2009.03.013.
53. Lacourciere KA, Stivers JT, Marino JP. Mechanism of neomycin and Rev peptide binding to the Rev responsive element of HIV-1 as determined by fluorescence and NMR spectroscopy. Biochemistry 2000; 39: 5630-5641, doi: 10.1021/bi992932p.
54. Luedtke NW, Tor Y. Fluorescence-based methods for evaluating the RNA affinity and specificity of HIV-1 RevRRE inhibitors. Biopolymers 2003; 70: 103-119, doi: 10.1002/bip.10428.
55. Battiste JL, Mao H, Rao NS, Tan R, Muhandiram DR, Kay LE, et al. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science 1996; 273: 1547-1551, doi: 10.1126/science.273.5281.1547.
56. Joyner JC, Keuper KD, Cowan JA. Analysis of RNA cleavage by MALDI-TOF mass spectrometry. Nucleic Acids Res 2013; 41: e2, doi: 10.1093/nar/gks811.
57. Joyner JC, Keuper KD, Cowan JA. Kinetics and mechanisms of oxidative cleavage of HIV RRE RNA by Rev-coupled transition metal-chelates. Chem Sci 2013; 4: 1707-1718, doi: 10.1039/c3sc22135k.
58. Pogozelski WK, Tullius TD. Oxidative Strand Scission of Nucleic Acids: Routes Initiated by Hydrogen Abstraction from the Sugar Moiety. Chem Rev 1998; 98: 1089-1108, doi: 10.1021/cr960437i.
59. Sreedhara A, Freed JD, Cowan JA. Efficient inorganic deoxyribonucleases. Greater than 50-million-fold rate enhancement in enzyme-like DNA cleavage. J Am Chem Soc 2000; 122: 8814-8824, doi: 10.1021/ja994411v.
60. Cowan JA. Inorganic biochemistry. An introduction. New York: Wiley-VCH; 1997.
61. Reedijk J. Mechanistic studies of Pt and Ru compounds with antitumor properties. Med Inorg Chem 2005; 80-109.
62. Liu HK, Sadler PJ. Metal complexes as DNA intercalators. Acc Chem Res 2011; 44: 349-359, doi: 10.1021/ar100140e.
63. Wheate NJ, Brodie CR, Collins JG, Kemp S, Aldrich-Wright JR. DNA intercalators in cancer therapy: organic and inorganic drugs and their spectroscopic tools of analysis. Mini Rev Med Chem 2007; 7: 627-648, doi: 10.2174/ 138955707780859413.
64. Baum C, von Kalle C, Staal FJ, Li Z, Fehse B, Schmidt M, et al. Chance or necessity? Insertional mutagenesis in gene therapy and its consequences. Mol Ther 2004; 9: 5-13, doi: 10.1016/j.ymthe.2003.10.013.
65. Hacein-Bey-Abina S, von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003; 302: 415-419, doi: 10.1126/ science.1088547.
66. Brown NJ, Vaughan DE. Angiotensin-converting enzyme inhibitors. Circulation 1998; 97: 1411-1420, doi: 10.1161/01.CIR.97.14.1411.
67. Deddish PA, Marcic B, Jackman HL, Wang HZ, Skidgel RA, Erdos EG. N-domain-specific substrate and C-domain inhibitors of angiotensin-converting enzyme: angiotensin (1-7) and keto-ACE. Hypertension 1998; 31: 912-917, doi: 10.1161/01.HYP.31.4.912.
68. Chappell MC, Pirro NT, Sykes A, Ferrario CM. Metabolism of angiotensin-(1-7) by angiotensin-converting enzyme. Hypertension 1998; 31: 362-367, doi: 10.1161/01.HYP. 31.1.362.
69. Georgiadis D, Beau F, Czarny B, Cotton J, Yiotakis A, Dive V. Roles of the two active sites of somatic angiotensinconverting enzyme in the cleavage of angiotensin I and bradykinin: insights from selective inhibitors. Circ Res 2003; 93: 148-154, doi: 10.1161/01.RES.0000081593.33848.FC.
70. Lonn EM, Yusuf S, Jha P, Montague TJ, Teo KK, Benedict CR, et al. Emerging role of angiotensin-converting enzyme inhibitors in cardiac and vascular protection. Circulation 1994; 90: 2056-2069, doi: 10.1161/01.CIR.90.4.2056.
71. Bernstein KE, Welsh SL, Inman JK. A deeply recessed active site in angiotensin-converting enzyme is indicated from the binding characteristics of biotin-spacer-inhibitor reagents. Biochem Biophys Res Commun 1990; 167: 310-316, doi: 10.1016/0006-291X(90)91766-L.
72. Corradi HR, Schwager SL, Nchinda AT, Sturrock ED, Acharya KR. Crystal structure of the N domain of human somatic angiotensin I-converting enzyme provides a structural basis for domain-specific inhibitor design. J Mol Biol 2006; 357: 964-974, doi: 10.1016/j.jmb.2006.01.048.
73. Ehlers MR, Riordan JF. Angiotensin-converting enzyme: zincand inhibitor-binding stoichiometries of the somatic and testis isozymes. Biochemistry 1991; 30: 7118-7126, doi: 10.1021/bi00243a012.
74. Michaud A, Williams TA, Chauvet MT, Corvol P. Substrate dependence of angiotensin I-converting enzyme inhibition: captopril displays a partial selectivity for inhibition of Nacetyl-seryl-aspartyl-lysyl-proline hydrolysis compared with that of angiotensin I. Mol Pharmacol 1997; 51: 1070-1076.
75. Natesh R, Schwager SL, Sturrock ED, Acharya KR. Crystal structure of the human angiotensin-converting enzymelisinopril complex. Nature 2003; 421: 551-554, doi: 10.1038/ nature01370.
76. Amici A, Levine RL, Tsai L, Stadtman ER. Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions. J Biol Chem 1989; 264: 3341-3346.
77. Stadtman ER. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 1993; 62: 797-821, doi: 10.1146/annurev.bi.62.070193.004053.
78. Bradshaw RA, Peters T Jr. The amino acid sequence of peptide (1-24) of rat and human serum albumins. J Biol Chem 1969; 244: 5582-5589.
79. Camerman N, Camerman A, Sarkar B. Molecular design to mimic the copper (II) transport site of human albumin. Can J Chem 1976.
80. Lau SJ, Sarkar B. Ternary coordination complex between human serum albumin, copper (II), and L-histidine. J Biol Chem 1971; 246: 5938-5943.
81. Lau SJ, Kruck TP, Sarkar B. A peptide molecule mimicking the copper(II) transport site of human serum albumin. A comparative study between the synthetic site and albumin. J Biol Chem 1974; 249: 5878-5884.
82. Cabras T, Patamia M, Melino S, Inzitari R, Messana I, Castagnola M, et al. Pro-oxidant activity of histatin 5 related Cu(II)-model peptide probed by mass spectrometry. Biochem Biophys Res Commun 2007; 358: 277-284, doi: 10.1016/j.bbrc.2007.04.121.
83. Grogan J, McKnight CJ, Troxler RF, Oppenheim FG. Zinc and copper bind to unique sites of histatin 5. FEBS Lett 2001; 491: 76-80, doi: 10.1016/S0014-5793(01)02157-3.
84. Harford C, Sarkar B. Neuromedin C binds Cu(II) and Ni(II) via the ATCUN motif: implications for the CNS and cancer growth. Biochem Biophys Res Commun 1995; 209: 877-882, doi: 10.1006/bbrc.1995.1580.