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    Features

    Drug Discovery Technology Trends

    Combining native mass spectrometry with fragment-based drug discovery in medicinal chemistry

    Drug Discovery Technology Trends
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    Sally-Ann Poulsen, Professor of Chemical Biology, Griffith Institute for Drug Discovery (GRIDD), Griffith University09.16.19
    For decades, high throughput screening (HTS) has been the go-to technique for early-stage drug discovery. This method enables researchers to rapidly identify large numbers of active compounds which could potentially influence a particular biological pathway of interest, and therefore progress through the lead discovery and target validation pipeline.

    Advanced laboratories are now using robotics for automated screening, to increase the overall speed of drug discovery. One such laboratory at the Griffith Institute for Drug Discovery (GRIDD), Griffith University, Brisbane, uses HTS robotics for both phenotypic screening—where the drug target is unknown —and target-based screening—where the protein of interest is known and the user is attempting to affect how it behaves, either by inhibiting or activating it. Another key research focus at GRIDD is the use of mass spectrometry (MS) in drug discovery, to observe small molecule protein interactions to identify better small molecules as starting points for drug discovery. This article highlights how our group has used MS together with fragment-based drug discovery (FBDD) as a powerful tool for discovering drug leads.

    Fragment based drug discovery
    Fragment-based screening (FBS) is now a widely applied method for the discovery of lead molecules in fragment-based drug discovery (FBDD) and complements HTS as one of the most popular method for screening molecules, however requiring significantly fewer compounds for screening. FBDD first identifies very small molecules (fragments), which are approximately half the size of standard drugs, and these fragments are expanded or linked together to generate drug leads.

    Bringing mass spectrometry to drug discovery
    At GRIDD, we have recently invested in Magnetic Resonance Mass Spectrometry (MRMS), formerly known as Fourier Transform Mass Spectrometry (FTMS), which has significantly improved fragment screening capabilities. The upper size limit of proteins that we can study in their native state has increased from 50 to 150 kilodaltons (kDa), and a high proportion of proteins in that size gap are of interest for drug discovery and are now accessible with this advanced technology.

    The extreme resolution of the MRMS instrument provides an extra layer of confidence in screening for weak interactions of fragments. The accurate identification of the binding and molecule mass for fragments is very important as a starting point in drug discovery. By combining MRMS technology with quadrupole time-of-flight (QTOF) MS, another filter of obtaining fragment binding data and ruling out ineffective compounds quickly, fragment screening is also achievable. The team then takes those compounds with binding potential over to the MRMS machine for higher resolution analysis.

    An additional benefit of the MRMS system is its minimal false positive results. Other techniques suffer from producing high false positives, because they are dealing with fragments at higher concentrations, which can aggregate and behave irregularly. When using MRMS, the fragment is at the same concentration as the protein, so false hits are less likely to occur. This is a big advantage, because if there are 1000 compounds screening in the library, only 200-300 might be filtered if there are a high number of false positives, rather than 10-30 true hits. The MRMS method avoids wasting valuable time on compounds that will not advance to drug discovery.

    Lowering attrition with FBDD
    It is becoming increasingly challenging to progress new drugs through the drug development process, and the rate of acceptance is declining. Investment by the pharmaceutical industry in small molecules to progress them to phase I, II and III clinical trials, before failing late in the process, is referred to as attrition, which is extremely costly. The drive to reduce attrition rates has drawn more attention to FBDD.

    The difference between fragment and traditional HTS is the molecular size. A fragment (or small molecule) is typically under 200 daltons (Da) in molecular weight, whereas a HTS compound is between 400-500 Da. The ability of a fragment to interact with a protein is less than a HTS compound and the binding affinity is weaker, but if an interaction occurs it indicates a perfect fit. This means that molecules resulting from FBDD workflows are likely to progress further in the clinical trial process and towards Food and Drug Administration (FDA) approval, or more likely to exit early and limit the investment knock, therefore lowering attrition rates.

    Combining fragment screening technologies
    Fragment screening has been a successful approach for FBDD researchers as there have been three approved drugs from the process, Vemurafenib (also known as Zelboraf), Venetoclax and Kisqali (LEE011, (ribociclib), with many more in phase I, II and III clinical trials.1 It is proving an area of great and growing interest for the pharmaceutical industry and in academic research. FBDD is, however, contingent on the development of analytical methods such as MS to be able to identify the weak binding fragments. As such, researchers at GRIDD are optimizing their workflows and combining techniques together with collaborators in order to give the best chance of accelerating drug discovery. Techniques for FBDD, in addition to MS, include Surface Plasmon Resonance (SPR), X‑ray Crystallography, Nuclear Magnetic Resonance (NMR) and Isothermal Titration Calorimetry (ITC). Each method has advantages and disadvantages but there is a need for multiple (orthogonal) methods, in order to be confident that a hit is a true hit.

    The group at GRIDD has combined native state MS with two proven and popular fragment screening methods, SPR and X-ray crystallography, in a fragment screening campaign against human carbonic anhydrase II (CA II).2 CA II is an enzyme which catalyzes the hydration of carbon dioxide, and defects are associated with diseases such as osteopetrosis (or “stone bone”) and renal tubular acidosis.3 The research recognized native state MS as a rapid, sensitive, high throughput, and label-free method to directly investigate protein−ligand interactions. However, there were few studies using this approach as a screening method to identify relevant protein−fragment interactions in FBDD. The results showed the first fragment screening analysis of electrospray ionization (ESI)-MS and NanoESI-MS using a high resolution Fourier-transform ion cyclotron resonance (FTICR) instrument (Bruker solariX XR 12.0T MRMS) in parallel with SPR as shown in Figure 1 and Table 1.


    Figure 1


    Table 1. Correlation of screening results for fragment hit chemotypes with surface plasmon resonance (SPR), electrospray ionization-mass spectrometry (ESI-MS), NanoESI-MS, and X-ray crystallography (green tick = hit, red cross = not a hit, n/a fragment not tested. aDose-response experiment performed at 25 degrees Celsius with a 5-point fragment concentration series range. bnano MS hit with ratio of unbound CA II:fragment bound CA II peak intensities in brackets.

    MS has a wide range of advantages over the other techniques, partly due to its speed and minimal sample requirement. For these reasons, GRIDD uses MS at the front end of the fragment screening cascade of methods, acting as a pre-filtering tool. Compounds for screening could start at, for example, 1000 for MS, and be brought down to 50 for the subsequent techniques, or MS could be used standalone in the workflow.

    Quantitative native MS
    The group at GRIDD has recently identified a new zinc binder fragment, in collaboration with the Commonwealth Scientific and Industrial Research Organization (CSIRO),4 which is a potent inhibitor of CA II. SPR and native ESI-MS identified compound 10, which has an affinity and ligand efficiency approaching that of sulfonamides, a well-known class of zinc binder for CA II.

    The group determined the crystal structure of compound 10 bound to CA II, confirming the binding pose of the new fragment to CA II, which included a primary interaction with the zinc and two hydrogen bonds with the protein, therefore explaining the high affinity as seen in Figure 2.


    Figure 2

    The study used a series of 18 analogues of compound 10 to assess the structure-activity relationship (SAR) using both SPR and MS. The group was able to obtain quantitative MS data by holding protein concentration constant (at 14.5 µM) and varying the fragment concentration from 0.5 – 120 µM. Plotting the percentage of protein bound and curve-fitting revealed dissociation constants remarkably similar to those determined using SPR. Nine of the new fragments showed at least some activity, although none were significantly more potent than compound 10. Crystal soaking experiments led to seven new structures, with all fragments binding in a similar manner as compound 10.

    The future of FBDD
    Collaboration with industry is a key focus for many academic research institutions, as there is a growing interest from the pharmaceutical sector in FBDD to aid drug discovery. Such industry-academia relationships, as well as the advances in analytical technology such as MRMS have made it possible to discover otherwise overlooked drug leads. 

    References
    1. Singh M, Tam B and Akabayov B. (2018) NMR-Fragment Based Virtual Screening: A Brief Overview, Molecules,  23, 233.
    2. Woods L, Dolezal O, Ren B, Ryan J, Peat T, Poulsen S. (2016) Native State Mass Spectrometry, Surface Plasmon Resonance, and X‑ray Crystallography Correlate Strongly as a Fragment Screening Combination, Journal for Medical Chemistry, 59, 5, 2192-2204
    3. Roth DE, Venta PJ, Tashian RE, and Sly WS. (1992) Molecular basis of human carbonic anhydrase II deficiency, Proc Natl Acad Sci USA, 89(5): 1804–1808.
    4. Chrysanthopoulos P, Mujumdar P, Woods L, Dolezal O, Ren B, Peat T and Poulsen S. (2017) Identification of a New Zinc Binding Chemotype by Fragment Screening, Journal for Medical Chemistry, 60, 7333−7349.

    Professor Sally-Ann Poulsen, Professor of Chemical Biology at Griffith Institute for Drug Discovery (GRIDD), Griffith University, introduced MRMS (FTMS) use for the study of protein-ligand complexes to Australia, and was one of the first researchers worldwide, and the first in Australia, to utilize native state mass spectrometry to screen fragments by the direct observation of protein-ligand complexes.      
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