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Pt(IV) Prodrugs with Nsaids As Axial Ligands

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Pt(IV) Prodrugs with Nsaids As Axial Ligands International Journal of Molecular Sciences Review Pt(IV) Prodrugs with NSAIDs as Axial Ligands Daniil Spector 1,2,* , Olga Krasnovskaya 1,2,* , Kirill Pavlov 2 , Alexander Erofeev 1,2, Peter Gorelkin 1,2 , Elena Beloglazkina 2 and Alexander Majouga 1,2,3 1 Department of Materials Science of Semiconductors and Dielectrics, National University of Science and Technology (MISIS), Leninskiy Prospect 4, 101000 Moscow, Russia; [email protected] (A.E.); [email protected] (P.G.); [email protected] (A.M.) 2 Chemistry Department, Lomonosov Moscow State University, Leninskie Gory 1,3, 119991 Moscow, Russia; [email protected] (K.P.); [email protected] (E.B.) 3 Mendeleev University of Chemical Technology of Russia, Miusskaya Ploshchad’ 9, 125047 Moscow, Russia * Correspondence: [email protected] (D.S.); [email protected] (O.K.) Abstract: A chemo-anti-inflammatory strategy is of interest for the treatment of aggressive cancers. The platinum (IV) prodrug with non-steroidal anti-inflammatory drugs (NSAIDs) as axial ligands is designed to efficiently enter tumor cells due to high lipophilicity and release the cytotoxic metabolite and NSAID intracellularly, thereby reducing side effects and increasing the therapeutic efficacy of platinum chemotherapy. Over the last 7 years, a number of publications have been devoted to the design of such Pt(IV) prodrugs in combination with anti-inflammatory chemotherapy, with high therapeutic efficacy in vitro and In vivo. In this review, we summarize the studies devoted to the development of Pt(IV) prodrugs with NSAIDs as axial ligands, the study of the mechanism of their cytotoxic action and anti-inflammatory activity, the structure–activity ratio, and therapeutic efficacy. Keywords: platinum; prodrugs; NSAIDs Citation: Spector, D.; Krasnovskaya, O.; Pavlov, K.; Erofeev, A.; Gorelkin, P.; Beloglazkina, E.; Majouga, A. Pt(IV) Prodrugs with NSAIDs as 1. Introduction Axial Ligands. Int. J. Mol. Sci. 2021, Platinum-containing antineoplastic agents are effective anticancer drugs that are used 22, 3817. https://doi.org/10.3390/ in 50% of all chemotherapy regimens in clinical practice [1]. Three FDA-approved platinum- ijms22083817 containing anticancer drugs have been applied around the world for decades: cisplatin, carboplatin, and oxaliplatin [2]. Also, a second generation drug, nedaplatin, is approved Academic Editor: Nicola Margiotta in Japan for the treatment of lung, esophageal, and head and neck cancers; lobaplatin is approved in China for the treatment of inoperable metastatic breast cancer and small- Received: 12 March 2021 cell lung cancer [3]; and heptaplatin is approved in Korea for the treatment of stomach Accepted: 31 March 2021 Published: 7 April 2021 cancer [4]. Pt(II) coordination compounds easily undergo non-selective ligand substitution on the Publisher’s Note: MDPI stays neutral way to the tumor site, while approximately 90% of the administered cisplatin is deactivated with regard to jurisdictional claims in in the bloodstream due to irreversible binding to albumin and other plasma proteins, with published maps and institutional affil- only 1% (or less) binding with the intended target (nuclear DNA) [5]. Protein binding to iations. cisplatin leads to the formation of toxic metabolites that cause serious side effects such as kidney damage, nerve damage, and hearing loss [6]. Cisplatin was also reported to cause severe delayed emesis after 24 hours of administration [7]. The second-generation platinum anticancer drugs, carboplatin and oxaliplatin, are less toxic than cisplatin but show no improvement in potency or selectivity [8,9]. Various strategies have been suggested to Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. improve the efficiency of platinum drugs [10]. One of the approaches to overcome these and This article is an open access article the other well-known disadvantages of Pt(II)-based drugs, such as low bioavailability and distributed under the terms and rapidly emerging resistance, is to use Pt(IV) complexes as prodrugs. Pt(IV) have a low-spin conditions of the Creative Commons octahedral d6 geometry and have the potential to overcome the disadvantages associated Attribution (CC BY) license (https:// with platinum-containing chemotherapeutic agents [11]. The oxidation state of Pt(IV) creativecommons.org/licenses/by/ provides an increased inertness of the coordination compounds compared to the Pt(II) 4.0/). complexes, and the conjugation of additional ligands in the axial position allows for both Int. J. Mol. Sci. 2021, 22, 3817. https://doi.org/10.3390/ijms22083817 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 28 The oxidation state of Pt(IV) provides an increased inertness of the coordination com- pounds compared to the Pt(II) complexes, and the conjugation of additional ligands in the axial position allows for both adjusting the lipophilicity and increasing the selectivity of the coordination compounds to tumor cells [12]. Chronic inflammation is an important therapeutic target in both the treatment of ma- lignant neoplasms and drug development [13]. Various isoforms of cyclooxygenase Int. J. Mol. Sci. 2021, 22, 3817 2 of 27 (COX), such as COX-1 and COX-2, are markers of chronic inflammation, catalyzing the rate-limiting stage of prostaglandin formation, which plays a key role in the formation of the immune responseadjusting [14]. Since the lipophilicity COX-2 and and increasingprostaglandin-2 the selectivity are ofinvolved the coordination in the compoundsinflam- to matory response, thetumor suppression cells [12]. of apoptosis, and the formation of drug resistance, the inhibition of COX-2 can Chronicreduce inflammationinflammation is anand, important as a result, therapeutic reduce target the rate in both of metastasis the treatment of of malignant neoplasmsmalignant [15]. neoplasmsDrug resistance and drug is developmentalso associated [13]. with Various epithelial–mesenchy- isoforms of cyclooxygenase mal transition (EMT),(COX), which such is as the COX-1 transdifferentiation and COX-2, are markers of epithelial of chronic inflammation, cells into motile catalyzing mes- the rate- limiting stage of prostaglandin formation, which plays a key role in the formation of the enchymal cells [16].immune EMT-activated response [14 cells]. Since release COX-2 matrix and prostaglandin-2 metalloproteinases are involved (MMPs); in the inflammatory the increased expressionresponse, of MMPs the suppressioncontributes of to apoptosis, the development and the formation of malignant of drug resistance, neoplasms the inhibi- [17]. In addition, EMTtion transition of COX-2 can is reduceaccompan inflammationied by the and, overexpression as a result, reduce of the COX-2, rate of metastasiswhich of can lead to immunemalignant evasion neoplasmsand tumor [15 drug]. Drug resistance resistance is [18]. also associated with epithelial–mesenchymal transition (EMT), which is the transdifferentiation of epithelial cells into motile mesenchy- Non-steroidal malanti-inflammatory cells [16]. EMT-activated drugs cells (NSA releaseIDs) matrix are metalloproteinasescapable of inhibiting (MMPs); various the increased isoforms of cyclooxygenase,expression which of MMPs makes contributes them toa thepromising development addition of malignant to existing neoplasms chemo- [17]. In therapy regimens, bothaddition, in view EMT transitionof their anti-inflammatory is accompanied by the and overexpression analgesic of effects, COX-2, whichbut also can lead their ability to reduceto immune the rate evasion of metastas and tumoris drugand resistancemount an [18 ].immune response [19]. The development of Pt(IV) prodrugsNon-steroidal with anti-inflammatory COX inhibitors drugs in the (NSAIDs) axial position are capable is of a inhibitingpromising various isoforms of cyclooxygenase, which makes them a promising addition to existing chemother- therapeutic approachapy due regimens, to the both fact in that view the of their Pt(IV) anti-inflammatory prodrug’s ability and analgesic to bind effects, COX-2 but will also their increase the selectivityability of to prodrugs reduce the rateforof tumor metastasis cells and in mount comparison an immune with response classical [19]. ThePt(II) develop- drugs. Also, an increasement ofin Pt(IV) the lipophilicity prodrugs with COXof the inhibitors Pt(IV) in prodrug the axial positioncompared is a promising to the initial therapeutic Pt(II) drugs significantlyapproach increases due to the drug fact intracellular that the Pt(IV) prodrug’saccumulation, ability tothereby bind COX-2 increasing will increase its the selectivity of prodrugs for tumor cells in comparison with classical Pt(II) drugs. Also, effectiveness and reducingan increase side in the effects lipophilicity due to of a the decrease Pt(IV) prodrug in the comparedeffective todose. the initial Thus, Pt(II) the drugs design and synthesissignificantly of Pt(IV) increasesprodrugs drug modified intracellular with accumulation, NSAID moieties thereby increasingwill make its it effectiveness pos- sible to obtain effectiveand reducing drugs with side effects increased due to selectivity a decrease infor the tumor effective cells, dose. higher Thus, theefficacy design and compared to classicalsynthesis platinum-containing of Pt(IV) prodrugs modifieddrugs, as with well NSAID as an moieties additional will make anti-inflamma- it possible to obtain effective drugs with increased selectivity for tumor cells, higher efficacy compared to tory effect that provides
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