Article

Proprotein Convertase Subtilisin/Kexin 9 (PCSK9) Inhibition in Patients With or at High Risk of Coronary Heart Disease

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Abstract

Proprotein convertase subtilisin/kexin 9 (PCSK9) is an enzyme that binds and inactivates the low-density lipoprotein (LDL) receptor onhepatocytes, leading to higher levels of serum LDL cholesterol (LDL-C). Individuals with ‘loss of function’ mutations in the PCSK9 gene havelower LDL-C levels and are at decreased risk of coronary heart disease. In light of this, inhibition of PCSK9 activity has become a target forreducing LDL-C levels, with approaches including monoclonal antibodies, antisense oligonucleotides, and RNA interference technology. Twomonoclonal antibodies to PCSK9, alirocumab and evolocumab, have recently been FDA approved. Although large-scale clinical trials to assesscardiovascular outcomes are awaited, reductions in LDL-C levels have been demonstrated, with no increase in muscle-related adverse effects.In addition to these monoclonal antibody approaches, inclisiran – a molecule that inhibits PCSK9 synthesis by RNA interference – is currentlyunder development. Phase 1 and 2 studies indicate an LDL-C-lowering effect comparable to that of monoclonal antibodies, with effectspersisting to as long as 180 days. Phase 3 studies are planned investigating dose administration two to three times per year. The aim of this report is to summarize the role of PCSK9 inhibition in the lowering of LDL-C. Approaches to PCSK9 inhibition are discussed, and an up-todate insight into current developments in the field is provided.

Disclosure: SP has no conflicts of interest to declare. TMB receives research funding from Amgen Inc. and is the site principal investigator for a clinical trial funded by Omthera Pharmaceuticals and AstraZeneca.

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Correspondence Details:Todd M Brown, MD, MSPH, UAB Division of Cardiovascular Disease, LHRB 313, 1720 Second Avenue South, Birmingham, AL, 35294, USA. E: tmbrown@uab.edu

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Proprotein convertases are proteolytic enzymes that activate proteins by post-translational alterations in protein structure. Proprotein convertase subtilisin/kexin 9 (PCSK9) is a proprotein convertase that binds and inactivates the low-density lipoprotein (LDL) receptor on the surface of hepatocytes resulting in higher levels of serum LDL cholesterol (LDL-C).1 Over-expression of PCSK9 leads to a decrease in LDL receptor-mediated LDL-C endocytosis and, therefore, increases circulating levels of LDL-C.1 Under-expression of PCSK9 leads to an increase in LDL receptormediated LDL-C uptake and clearance in hepatocytes, lowing serum LDL-C.1 Mendelian studies have provided evidence of the effect of PCSK9 activity on LDL-C levels and ultimately cardiovascular disease. Individuals with ‘gain-of-function’ mutations in PCSK9 have higher LDL-C levels, representing an autosomal dominant form of hypercholesterolemia.2,3 Conversely, individuals with ‘loss-of-function’ mutations in PCSK9 have lower LDL-C levels and lower coronary heart disease (CHD) risk.4

Developments in the understanding of PCSK9 function and its affect on LDL-C have led to the rapid development of therapies targeted at reducing PCSK9 activity. Interference with the activity of PCSK9 by multiple post-translational mechanisms including monoclonal antibodies, antisense oligonucleotides, or RNA interference technology has become a promising target for LDL-C reduction. In 2015, alirocumab and evolocumab, two subcutaneously administered monoclonal antibodies to PCSK9, were approved for use by the US Food and Drug Administration.5,6 These agents have been associated with a 40–70 % reduction in LDL-C in individuals with familial hypercholesterolemia and/or atherosclerotic disease when used as monotherapy in individuals intolerant to statins or in addition to statins and/or ezetimibe.7–17 Importantly, there has not been an increase in muscle-related adverse effects, and medication adherence has been as good as with other lipid-lowering agents.7–17 In addition to reductions in LDL-C, one agent, evolocumab, has been associated with coronary plaque regression. In the Global Assessment of Plaque Regression with a PCSK9 Antibody as Measured by Intravascular Ultrasound (GLAGOV) randomized clinical trial, evolocumab 420 mg administered monthly in addition to statin therapy was associated with a greater reduction in percent atheroma volume (PAV) as measured by intravascular ultrasonography as compared to those on statins alone (PAV difference -1.0 %; 95 % CI [-1.8 % to -0.64 %].18

Although large scale clinical trials powered to assess cardiovascular outcomes have yet to be published, one meta-analysis of 10,159 individuals who participated in 24 phase 2 or 3 clinical trials has demonstrated reductions in major adverse cardiovascular events with the use of alirocumab and evolocumab.19 Statistically significant reductions in all-cause mortality (OR 0.45; 95 % CI [0.23–0.86]) and myocardial infarction (OR 0.49; 95 % CI [0.26–0.93]) were seen with a trend toward a significant reduction in cardiovascular mortality (OR 0.50; 95 % CI [0.23–1.10]).19 Serum creatinine kinase levels were lower in the PCSK9 group, and serious adverse events did not increase with administration of PCSK9 antibodies.19

In addition to monoclonal antibodies directed against PCSK9, agents using RNA interference technology to lower PCSK9 are currently being studied. Small interfering RNA (siRNA) molecules are taken up by hepatocytes and directly bind to the RNA-induced silencing complex (RISC), part of the cells natural machinery.20 Once the siRNA is loaded onto the RISC, the RISC cleaves messenger RNA encoding PCSK9 thereby preventing its translation into protein. Inclisiran is a long-acting, subcutaneously administered synthetic siRNA currently under development.20 In a phase 1 clinical trial, inclisiran was associated with a similar degree of LDL-C reduction to that observed with PCSK9 antibodies; however, the duration of effect persisted for at least 180 days, demonstrating the potential for administration only once every 3–6 months.21 Importantly, there were no treatment discontinuations because of adverse events or serious adverse events noted.21 Phase 2 clinical trials are currently ongoing, and pre-specified interim analyses of these data have revealed >50 % reductions in LDL-C at 6 months with a 300 mg dose of inclisiran. Subsequent phase 3 trials are planned using the 300 mg dose of inclisiran administered two to three times per year.22

Although the majority of clinical data surrounding the potential cardiovascular benefits of PCSK9 inhibition have been acquired in individuals with familial hypercholesterolemia and/or high risk CHD who were stable, there is increasing interest in the role of PCSK9 inhibition in plaque stabilization in the acute coronary syndrome (ACS) setting. PCSK9 levels are increased in individuals following ACS, and higher levels of PCSK9 are associated with higher rates of recurrent ACS and death. Potential beneficial effects of PCSK9 inhibition in ACS include reductions in oxidized LDL, inflammatory cells and platelets, and lipoprotein(a) levels.23

Data from large scale clinical trials powered to assess the effect of monoclonal antibodies to PCSK9 on cardiovascular risk are expected to be presented at the 2017 American College of Cardiology (ACC) Annual Scientific Sessions. The results of these studies should provide more definitive data on the role of these agents in individuals with or at high risk of CHD. Until then, clinicians must rely on the limited clinical data currently available when selecting the appropriate patients for this therapy. Some guidance has been provided by the ACC in a recent expert consensus statement on the use of non-statin cholesterol lowering medications.24 Based on this statement, high-risk patients who fail to achieve at least a 50 % reduction in LDL-C or an absolute LDL-C level of <70–100 mg/dL could be considered for PCSK9 inhibition.24

PCSK9 inhibition is a new and exciting mechanism for LDL-C lowering in patients with or at high risk of CHD. Although definitive data on cardiovascular outcomes is thus far lacking, there are good data that the monoclonal antibodies to PCSK9 substantially lower LDL-C and result in regression of coronary atherosclerosis. Preliminary data suggest that they may also significantly reduce cardiovascular events. These agents seem to be well tolerated and not associated with significant adverse events. At present, it remains unclear what the magnitude of cardiovascular risk reduction will be with these agents and what, if any, long term consequences there are to very low LDL-C levels. However, should these agents prove to be safe and effective therapies, they will have a substantial role in the treatment of patients with and at high risk of CHD.

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