Strategies for the Design of HIV-1 Non-Nucleoside Reverse Transcriptase Inhibitors: Lessons from the Development of Seven Representative Paradigms

Journal of Medicinal Chemistry
2012.0

Abstract

According to the latest data released by Joint United Nations Programme on HIV/AIDS (UNAIDS) and World Health Organization (WHO), there are 2.6 million people newly infected with human immunodeficiency virus type 1 (HIV-1) in 2009 compared to 2.5 million people newly infected in 2007.1 Therefore, acquired immune deficiency syndrome (AIDS) caused by HIV-1 is still a prevalent disease. The most efficient and standard treatment regimen for HIV-1 infection, namely, as highly active antiretroviral therapy (HAART), commonly involves two nucleoside reverse transcriptase inhibitors (NRTIs) and a ritonavir-boosted protease inhibitor (PI) or a non-nucleoside reverse transcriptase inhibitor (NNRTI). As a key component of HAART, NNRTIs present higher specificity and lower toxicity than NRTIs and PIs.2,3Currently, five NNRTIs have been approved by U.S. Food and Drug Administration (U.S. FDA) for the clinical treatment of AIDS, i.e., nevirapine, delavirdine, efavirenz, etravirine, and rilpivirine (Figure 1). However, for the first-generation NNRTIs(nevirapine, delavirdine, and efavirenz), the rapid emergency of drug resistance (such as L100I, K103N, Y181C, Y188L, V106A, G190A, L100I/K103N, and K103N/Y181C mutations) dramatically reduced their potency, thus compromising the patient's clinical compliance. Alternatively, the second-generation NNRTI (etravirine and rilpivirine) possesses a high genetic barrier to resist various clinically relevant mutations, attributing to its structurally intrinsic flexibility, and readily adapted conformations to adjust to the NNRTI binding pocket (NNIBP) rearrangements caused by drug-resistant mutants.4 Nonetheless, in 2009, clinical cases with Stevens−Johnson syndrome, hypersensitivity reactions, or other adverse effects were found in postmarketing surveillance reports.5 In addition, more drug resistance occurred when patients failed therapy with rilpivirine compared to efavirenz.6 Therefore, there is still an urgent need for novel NNRTIs possessing high potency while overcoming drug resistance, lesser toxicity, good patient adherence, and better pharmacokinetic properties.NNRTIs are targeted at a hydrophobic binding site (namely, NNIBP), which is located at a short distance of 10 Å from the catalytic site.7 The NNIBP has high flexibility, as it does not exist until binding with NNRTI, the formation of which is related to torsional rotations of the flexible side chains of some important amino acids.8,9 In addition, mutations can be observed frequently in and around the NNIBP.9 Although the threedimensional structure of HIV reverse transcriptase (RT) has been elucidated, the inherent flexibility and mutability of NNIBP still limit the structure-based NNRTI design. Currently, with the continued efforts in the development of computational tools and increased structural information on the RT, coordinated multidisciplinary efforts involving medicinal chemistry (bioisosterism, molecular hybridization, scaffold hopping, and fragment-based drug discovery), structural biology (crystallography), and computational chemistry (molecular modeling) have proven to be powerful strategies for handling the flexibility and mutability of the NNIBP for identifying new generation of NNRTIs.As a result of coordinated multidisciplinary efforts, great achievements have been made in the discovery of new generation of NNRTIs. In past 5 years, seven NNRTI representatives have been marketed or are undergoing clinical trials, i.e., etravirine, rilpivirine (Figure 1), 1 (UK-453061),10 2 (RDEA806),11 3 (IDX-899),12 4 (MK-4965),13 and a discontinued drug candidate 5 (BILR 355)14 (Figure 2). Their development processes are representative and full of revelations. In this review, we will successively describe (1) the pharmacophoric similarities15 of NNRTIs and elaborate a typical pharmacophore model, (2) the convoluted development processes of seven representative candidates and drugs of NNRTIs, (3) the common structural characteristics of seven NNRTIs, and (4) the fragment-based drug discovery, with implications of halogenated aryls and nitrile groups.

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