Unusual Structural Features in the Adduct of Dirhodium Tetraacetate with Lysozyme

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2021 Feb 5

PMID 33540880

Citations 7

Authors

Domenico Loreto

Giarita Ferraro

Antonello Merlino

Affiliations

Soon will be listed here.

Abstract

The structures of the adducts formed upon reaction of the cytotoxic paddlewheel dirhodium complex [Rh(μ-OCCH)] with the model protein hen egg white lysozyme (HEWL) under different experimental conditions are reported. Results indicate that [Rh(μ-OCCH)] extensively reacts with HEWL:it in part breaks down, at variance with what happens in reactions with other proteins. A Rh center coordinates the side chains of Arg14 and His15. Dimeric Rh-Rh units with Rh-Rh distances between 2.3 and 2.5 Å are bound to the side chains of Asp18, Asp101, Asn93, and Lys96, while a dirhodium unit with a Rh-Rh distance of 3.2-3.4 Å binds the C-terminal carboxylate and the side chain of Lys13 at the interface between two symmetry-related molecules. An additional monometallic fragment binds the side chain of Lys33. These data, which are supported by replicated structural determinations, shed light on the reactivity of dirhodium tetracarboxylates with proteins, providing useful information for the design of new Rh-containing biomaterials with an array of potential applications in the field of catalysis or of medicinal chemistry and valuable insight into the mechanism of action of these potential anticancer agents.

Citing Articles

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Cross-Linked Crystals of Dirhodium Tetraacetate/RNase A Adduct Can Be Used as Heterogeneous Catalysts.

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PMID: 37144589 PMC: 10189731. DOI: 10.1021/acs.inorgchem.3c00852.

Effect of Equatorial Ligand Substitution on the Reactivity with Proteins of Paddlewheel Diruthenium Complexes: Structural Studies.

Teran A, Ferraro G, Sanchez-Pelaez A, Herrero S, Merlino A Inorg Chem. 2023; 62(2):670-674.

PMID: 36597851 PMC: 9846696. DOI: 10.1021/acs.inorgchem.2c04103.

Multiple and Variable Binding of Pharmacologically Active Bis(maltolato)oxidovanadium(IV) to Lysozyme.

Ferraro G, Paolillo M, Sciortino G, Garribba E, Merlino A Inorg Chem. 2022; 61(41):16458-16467.

PMID: 36205235 PMC: 9579999. DOI: 10.1021/acs.inorgchem.2c02690.

Unexpected Imidazole Coordination to the Dirhodium Center in a Protein Environment: Insights from X-ray Crystallography and Quantum Chemistry.

Loreto D, Fasulo F, Munoz-Garcia A, Pavone M, Merlino A Inorg Chem. 2022; 61(22):8402-8405.

PMID: 35609175 PMC: 9175176. DOI: 10.1021/acs.inorgchem.2c01370.

References

Trynda L, Pruchnik F . Interaction of tetra-mu-acetatodirhodium(II) with human serum albumin. J Inorg Biochem. 1995; 58(1):69-77. DOI: 10.1016/0162-0134(94)00040-h. View

Erck A, Rainen L, Whileyman J, Chang I, Kimball A, Bear J . Studies of rhodium(II) carboxylates as potential antitumor agents. Proc Soc Exp Biol Med. 1974; 145(4):1278-83. DOI: 10.3181/00379727-145-37996. View

Ueno T . Porous protein crystals as reaction vessels. Chemistry. 2013; 19(28):9096-102. DOI: 10.1002/chem.201300250. View

Yang H, Swartz A, Park H, Srivastava P, Ellis-Guardiola K, Upp D . Evolving artificial metalloenzymes via random mutagenesis. Nat Chem. 2018; 10(3):318-324. PMC: 5891097. DOI: 10.1038/nchem.2927. View

Tanley S, Schreurs A, Kroon-Batenburg L, Meredith J, Prendergast R, Walsh D . Structural studies of the effect that dimethyl sulfoxide (DMSO) has on cisplatin and carboplatin binding to histidine in a protein. Acta Crystallogr D Biol Crystallogr. 2012; 68(Pt 5):601-12. DOI: 10.1107/S0907444912006907. View

Russo Krauss I, Ferraro G, Pica A, Marquez J, Helliwell J, Merlino A . Principles and methods used to grow and optimize crystals of protein-metallodrug adducts, to determine metal binding sites and to assign metal ligands. Metallomics. 2017; 9(11):1534-1547. DOI: 10.1039/c7mt00219j. View

Liu W, Kuang Y, Wang Z, Zhu J, Wang Y . Dirhodium(II)-catalyzed [3 + 2] cycloaddition of -arylaminocyclopropane with alkyne derivatives. Beilstein J Org Chem. 2019; 15:542-550. PMC: 6404392. DOI: 10.3762/bjoc.15.48. View

Zaykov A, Ball Z . A general synthesis of dirhodium metallopeptides as MDM2 ligands. Chem Commun (Camb). 2011; 47(39):10927-9. DOI: 10.1039/c1cc13169a. View

Messori L, Marzo T, Sanches R, Hanif-Ur-Rehman , de Oliveira Silva D, Merlino A . Unusual structural features in the lysozyme derivative of the tetrakis(acetato)chloridodiruthenium(II,III) complex. Angew Chem Int Ed Engl. 2014; 53(24):6172-5. DOI: 10.1002/anie.201403337. View

10.

Tabe H, Fujita K, Abe S, Tsujimoto M, Kuchimaru T, Kizaka-Kondoh S . Preparation of a cross-linked porous protein crystal containing Ru carbonyl complexes as a CO-releasing extracellular scaffold. Inorg Chem. 2014; 54(1):215-20. DOI: 10.1021/ic502159x. View

11.

Kataoka Y, Yano N, Handa M, Kawamoto T . Intrinsic hydrogen evolution capability and a theoretically supported reaction mechanism of a paddlewheel-type dirhodium complex. Dalton Trans. 2019; 48(21):7302-7312. DOI: 10.1039/c8dt05035j. View

12.

Santos M, Seixas J, Coelho A, Mukhopadhyay A, Reis P, Romao M . New insights into the chemistry of fac-[Ru(CO)₃]²⁺ fragments in biologically relevant conditions: the CO releasing activity of [Ru(CO)₃Cl₂(1,3-thiazole)], and the X-ray crystal structure of its adduct with lysozyme. J Inorg Biochem. 2012; 117:285-91. DOI: 10.1016/j.jinorgbio.2012.06.018. View

13.

Messori L, Scaletti F, Massai L, Cinellu M, Gabbiani C, Vergara A . The mode of action of anticancer gold-based drugs: a structural perspective. Chem Commun (Camb). 2013; 49(86):10100-2. DOI: 10.1039/c3cc46400h. View

14.

Reibscheid E, ZYNGIER S, Maria D, Mistrone R, Sinisterra R, Couto L . Antitumor effects of rhodium (II) complexes on mice bearing Ehrlich tumors. Braz J Med Biol Res. 1994; 27(1):91-4. View

15.

Panzner M, Bilinovich S, Youngs W, Leeper T . Silver metallation of hen egg white lysozyme: X-ray crystal structure and NMR studies. Chem Commun (Camb). 2011; 47(46):12479-81. PMC: 3677188. DOI: 10.1039/c1cc15908a. View

16.

Howard R, Spring T, Bear J . The interaction of rhodium(II) carboxylates with enzymes. Cancer Res. 1976; 36(12):4402-5. View

17.

Santos-Silva T, Mukhopadhyay A, Seixas J, Bernardes G, Romao C, Romao M . CORM-3 reactivity toward proteins: the crystal structure of a Ru(II) dicarbonyl-lysozyme complex. J Am Chem Soc. 2011; 133(5):1192-5. DOI: 10.1021/ja108820s. View

18.

Murshudov G, Vagin A, Dodson E . Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997; 53(Pt 3):240-55. DOI: 10.1107/S0907444996012255. View

19.

Brink A, Helliwell J . Formation of a highly dense tetra-rhenium cluster in a protein crystal and its implications in medical imaging. IUCrJ. 2019; 6(Pt 4):695-702. PMC: 6608631. DOI: 10.1107/S2052252519006651. View

20.

Otwinowski Z, Minor W . Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997; 276:307-26. DOI: 10.1016/S0076-6879(97)76066-X. View