Background: Maraviroc (MVC) binds to a hydrophobic cavity within the trans-membrane helices of CCR5, and induces conformational alterations in the extra-cellular loops (ECLs) rendering CCR5 unrecognizable by HIV-1. HIV-1 can develop resistance to MVC by acquiring the ability to utilize the MVC-bound conformation of CCR5. Here, we compared the functional properties of two patient-derived MVC-resistant HIV-1 envelopes (Envs) with their parental sensitive Envs in order to elucidate the molecular mechanisms involved in development of resistance.
Materials and methods: Four HIV-1 Envs were isolated from patients 17 and 24 before the initiation of MVC (17-Sens and 24-Sens) and after virological failure (17-Res and 24-Res). The resistance phenotypes were determined in NP2-CD4/CCR5 cells and PBMCs by measuring the maximum percent inhibition (MPI). The 293-Affinofile assay was used to determine the ability of the resistant Envs to utilize MVC-bound CCR5. The mechanism of CCR5 engagement by resistant Envs was determined using entry assays in cells expressing alternative CCR5 mutants, and neutralization/inhibition assays.
Results: The resistant Envs displayed broad and divergent levels of resistance to MVC, with MPIs as high as 90% for 17-Res Env and as low as 0-12% for 24-Res Env. The magnitude of resistance was associated with the ability of the Envs to utilize the inhibitor-bound CCR5. Despite having highly divergent resistant phenotypes, and lack of common Env resistance mutations, both the resistant Envs acquired a critical dependence on the CCR5 N-terminus and charged histidine residues in the CCR5 ECLs to escape MVC. Increased dependence on the CCR5 N-terminus rendered the resistant Envs susceptible to inhibition by a sulfated peptide mimic of the CCR5 N-terminus.
Conclusion: A common molecular pathway of altered CCR5 engagement appears to be a common mechanism of HIV-1 escape from MVC, regardless of the level of resistance and the underlying resistance mutations. This altered pathway suggests a new avenue for blocking HIV-1 entry by CCR5 N-terminus sulfopeptidomimetic drugs.