Dieter Bromme

Professor

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Graduate Student Supervision

Doctoral Student Supervision

Dissertations completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest dissertations.

Structural insights into inhibitory mechanisms of cathepsin K (2019)

Cathepsin K (CatK) is a lysosomal cysteine protease highly expressed in osteoclasts and is responsible for the degradation of bone. Implication of CatK in various musculoskeletal disorders including osteoporosis highlights CatK as an important target for drug development. This thesis aims to identify and characterize different classes of CatK inhibitors, which target the active site and collagenolytically relevant ectosteric sites using X-ray crystallography combined with mutational and kinetic studies.In chapter 2, odanacatib, a specific CatK inhibitor recently abandoned in clinical trials due to adverse side effects, was investigated for its selectivity for mouse CatK over the human counterpart. Structural, mutagenic, and kinetic studies identified two structural features in the mouse enzyme which determines odanacatib’s selectivity. Replacement of these features from the human counterpart was able to restore inhibitory activity in the mouse enzyme. In chapters 3 and 4, composite docking and high throughput fluorescence polarization (FP) assay methods were developed to identify novel ectosteric inhibitors of CatK by targeting the protein oligomerization site required for collagen degradation. Screening of the NCI Database (280,000 compounds) using three distinct molecular modeling methods identified nine active compounds. The best compound had an IC50 value around 300 nM in cell-based resorption assays. Over 5,000 compounds were also screened using a developed FP assay and nine collagenase inhibitors were identified. Three of these compounds were active in subsequent cell-based assays.In chapter 5, NSC-13345, the structure of a putative allosteric inhibitor of CatK described in literature was determined in complex with the enzyme using X-ray crystallography. Previous characterization was performed using an inactive variant and the allosteric site affected by the presence of an extra loop. Structural determination with the fully processed enzyme identified three binding sites. One site located above the active site may explain its substrate selective inhibition. In addition, the crystal structure of T-06, a potent collagenase inhibitor of CatK, in complex with CatK was determined and provided insight into its ectosteric inhibition. These findings suggest that NSC-13345 and T-06 function as a substrate selective ectosteric inhibitors for CatK.

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Structural requirements for the elastolytic and collagenolytic activities of cathespins and the identification of exosite inhibitors (2013)

It has become increasingly transparent that substrate recognition and degradation of extracellular matrix proteins such as elastin and collagen by proteases require more than the binding to small areas around the scissile bond of the target protein. Important surface structures on proteases, known as exosites or the formation of protease complexes are likely required for the correct positioning and modification of the substrate. This thesis embarks on the identification of such exosites in lysosomal cysteine cathepsins and their involvement in protein unfolding that are required for their elastolytic and collagenolytic activities. In chapter 2, two exosites were identified in cathepsin V that are crucial for the degradation of insoluble elastin. Both exosites are distant from the active site of the protease. Replacement of both exosites completely abolished the elastolytic activity without affecting the general proteolytic efficacy of cathepsin V. Although the exact mechanism of contribution of these exosites to elastolysis is yet to be elucidated, the finding that the double exosite variant failed to bind to insoluble elastin implies that these exosites are involved in substrate recognition.In chapter 3, the involvement of exosites and the effect of protease oligomerization on the collagenase activity of cathepsin K was studied. Two mechanistic models including a cathepsin K/GAG tetramer and a dimer were proposed based on available crystal structures. Both models, although displaying different modes of GAG binding, share a number of important amino acid residues in their protein-protein interactions. Mutational, biochemical, and structural analysis revealed various mechanistic aspects of substrate specificity towards soluble and insoluble collagens, respectively.In chapter 4, a library of 1280 known drug derivatives was screened using a fluorometric polarization assay to identify potential exosite inhibitors that prevent the formation of active cathepsin K/GAG complexes. Two groups of compounds were identified: 1) polyanionic and 2) polyaromatic compounds, whose IC₅₀ values for the inhibition of soluble tropocollagen degradation were between 10 – 186 µM. Exosite inhibitors might have the advantage of overcoming the off-site effects of active site-directed inhibitors presently in development.

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Master's Student Supervision

Theses completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest theses.

Investigating the in vitro and in vivo anti-resorptive effects of herbal-and TCM-based extracts on Cathepsin K activity (2021)

Osteoporosis is a chronic skeletal disease primarily affecting post-menopausal women and men over the age of 50. Current pharmacological interventions, such as bisphosphonates (BP) and denosumab, target the bone resorption process and have limitations in efficacy due to the disruption of important bone remodeling mechanisms and thus reducing bone formation and quality. Cathepsin K (CatK) is the major enzyme that is responsible for the breakdown of type I collagen in the bone matrix, therefore inhibitors of CatK have been a new approach to the treatment of osteoporosis without decreasing bone formation. Several active site CatK inhibitors such as odanacatib (ODN) have shown high efficacy in clinical trials, but were not approved due to risks of adverse effects. Adverse effects were postulated to be due to inhibition of CatK normal physiological as well as pathophysiological functions such as its part in the catabolism of essential growth hormones. Exosite inhibitors extracted from red sage plants, such as tanshinone IIA sulfonic sodium (T06) and dihydrotanshinone-1 (DHT-1) have so far shown a potent anti-resorptive effect while demonstrating an increased specificity in targeting the disease-related collagenase activity of CatK. These inhibitors are able to bind at a site on CatK to prevent collagenase activity while leaving other enzymatic activities unaltered. The major aim of my thesis will be to elucidate the in vitro and in vivo efficacy of herbal-based CatK inhibitors in the treatment of osteoporosis. The in vitro and in vivo efficacy of a pan-tanshinone-containing extracts of Salvia Milthorizoa (SM) , and a formulation used in Traditional Chinese medicine where SM is part of a multi-herbal combination (XLGB Pills), which will be compared against a standard-of-care bisphosphonate through the analysis of bone microstructural as well as CatK activity subsequent to these treatments.

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Characterization of glycosaminoglycan interaction sites and exosite inhibitors of cathespin K (2014)

Cysteine cathepsins belong to the papain-like family and are critically involved in the pathogenesis of various diseases, such as osteoporosis and cardiovascular diseases. These disorders are associated with failures in the degradation of extracellular matrix proteins, collagens and elastins. Based on enzymatic and structural studies, the active site mechanism has been well elucidated and many active site inhibitors have been identified, especially inhibitors for cathepsin K. Cathepsin K is primarily expressed in osteoclasts and the enzyme is responsible for most of the bone resorption, and thus an important pharmaceutical target for the treatment of osteoporosis. However, as cathepsin K is expressed not only in osteoclasts but also has functions outside the skeletal system, active site inhibitors may lead to severe side effects when used for treatment. In cathepsins, there are certain binding sites that are distinct from the active site, termed exosites, which have been defined as important for the degradation of extracellular matrix proteins. The hypothesis is that exosites could block the degradation of matrix proteins but would not interfere with other biological functions of the target protease such as cathepsin K. My thesis is focused on the characterization of these exosites and the identification of selective exosite inhibitors.In Project 1, protein-GAG interaction sites were studied for their involvement in the collagenase activity. According to the X-ray structures of cathepsin K -chondroitin sulfate (CS) complex, two mechanistic models were built: cathepsin K/CS tetramer and dimer. The hypothesis is that the cathepsin K/CS dimer complex solubilizes collagen fibers into tropocollagen and the cathepsin K/CS tetramer complex further degrades tropocollagen into peptides. The objective is to elucidate the mechanism of cathepsin K/CS complex-mediated collagen degradation by generating GAG binding sites mutants. In project 2, potential exosite inhibitors of cathepsin K were identified by drug screening assays. Compounds which have been reported to be effective in osteoporosis animal models were studied. The hypothesis is that exosite inhibitors for cathepsins specifically inhibit the degradation of collagen but not that of other biological substrates. The objective is to determine IC50 values of the compounds for the inhibition of the degradation of collagen.

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Investigation of the collagenolytic activity of Cathepsin K complexes by site-directed mutagenesis (2013)

Cathepsin K (catK) is a lysosomal cysteine protease predominantly expressed in osteoclasts. It is the most potent collagenase and elastase in human and involved in a variety of physiological functions including bone degradation, wound healing, maturation of hormones, and a range of important proteolytic activities required for normal cellular function. The main organic constituent of bone, type I collagen, has a highly organized and tightly packed structure and is resistant to proteolysis by most proteases. CatK is the only human protease that efficiently cleaves triple helical collagen, leading to the complete degradation of bone organic matter. This enzyme is the main protease expressed by osteoclasts and is responsible for bone degradation during bone resorption. In recent years, it has been shown that catK forms a complex with bone associated glycosaminoglycans (GAGs) to gain this collagenase activity. However, precise mechanism remains unclear. Due to the major role in bone resorption, catK has been a pharmaceutical target for osteoporosis treatment. Several catK inhibitors have been developed, yet adverse side effects remain a concern. A major issue of the active site inhibitors is its interference to other functions of this enzyme. Gaining the insight of mechanical details of collagenolytic activity of catK can lead to substrate-targeting specific inhibitors that can treat osteoporosis with minimum side effects. There are two catK-GAG complex models based on x-ray crystallography developed in our laboratory; the dimer and the tetramer models.In this study, mutant proteases were made to assess the role of specific protein interaction sites in these proposed models. Mutation at one residue in particular, N99, exhibited 40~50% reduction of degradation activity toward soluble and insoluble collagen without affecting regular proteolytic activity. The atomic force microscopy analysis revealed that the complex formation, observed in the wild type enzyme, was compromised in this mutant protease. This indicates that N99 contributes to the protein interaction necessary for the collagenolytic catK complex formation. Additionally, two mutant proteases showed facilitated collagenase activity against insoluble fibers. These finding contribute to gain better understanding of catK’s collagenolytic activity and will lead development of exosite inhibitors to treat osteoporosis in the future.

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Characterization of Elastolytic Cathepsins in Macrophages (2012)

Atherosclerosis is characterized by a thickening of the arterial wall and loss of its elasticity. The elasticity of the arterial wall is impaired when the extracellular matrix undergoes extensive proteolytic remodeling. Cathepsins are papain-like cysteine proteases that are known to have elastolytic/fibrinolytic activities. They are highly expressed in macrophages present in plaque areas of diseased blood vessels and are thought to contribute to the tissue remodeling. Using cathepsin deficient macrophages and various protease inhibitors, the elastolytic activities of cathepsins B, K, L, and S were quantitatively determined. Up to 60% of the total elastase activity of macrophages was attributed to cathepsin activities. Deficiencies in single cathepsins appeared to be compensated by other cathepsins. The capability and potency of cathepsins B, K, L, and V to hydrolyze fibrin was also determined.The exact quantification of individual cathepsin activities with the help of inhibitors or enzyme deficiencies in biological samples is difficult due to compensatory effects. Thus, specific substrates could be a viable alternative. Commercially available cathepsin activity assay kits that exploit fluorogenic peptidyl substrates are widely used to measure individual cathepsin activities in biological samples. However, substrates marketed as cathepsin K, L and S specific were found to be only marginally specific or completely non-specific, and were hydrolyzed by various other cathepsins. Furthermore, the presence of highly potent endogenous inhibitors in biological samples and the lack of specificity of the substrates skew the measurements towards cathepsin B which is relatively resistant to endogenous inhibitors. Thus, data obtained using commercial substrate kits are to be interpreted with great caution.

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Antipain and its analogues, natural product inhibitors of cathepsin K isolated from streptomyces (2011)

In human bone, 90% of organic bone matrix is composed of type 1 collagen. Cathepsin K is a cysteine protease involved in osteoclast mediated bone absorption and has been identified as a major drug target for the treatment of osteoporosis. Numerous potent inhibitors of cathepsin K have already been identified from natural sources including epoxide inhibitors such as E-64 isolated from the fungi Aspergillus japonicus as well as various peptide aldehydes such as Leupeptin and alpha-MAPI purified from Streptomyces. 350 soil and lichen-associated bacterial strains collected in the rain forests of British Columbia were screened and 22 samples were identified containing significant cathepsin K inhibitory activity. From those active samples, L-91-3 was selected as one of the most potent samples for further characterization of their cathepsin inhibitor content. Three Antipain-related peptide inhibitors were identified from L-91-3 strain of Streptomyces.Antipain (Ki 41nM +/- 37nM) and Vince 2 (cyclized P1 derivative Ki 295nM +/- 123nM) were isolated by traditional purification and subsequent NMR and Mass Spectrometry analysis. The cyclized compound, Vince 2 (phenylalanyl-ureido-arginyl-valinyl- cycloarginal), lacked the aldehyde function and resulted in a lower binding affinity towards cathepsin K. Using Cathepsin K as bait for active site directed inhibitors a third compound, named Lichostatinal was identified by x-ray crystallography where recombinant human cathepsin K was co-crystallized with the semi-crude fermentation broth resulting in 2.0 Å resolution crystal structure. Lichostatinal is a peptide-based aldehyde with the amino acid composition (agmatinyl-ureido-serine-valinyl-arginal). The P1-P4 substrate residues of Lichostatinal interact with the non primed S1-S4 subsites of cathepsin K.

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Novel peptide-derived cathepsin K inhibitors from Streptomyces (2011)

Human cathepsin K is a cysteine protease that is a member of the papainsuperfamily. It is selectively expressed in osteoclasts where it is involved in collagen typeI degradation during bone resorption. As such, cathepsin K represents a potential drugtarget for the treatment of metabolic bone diseases such as osteoporosis.In the search for novel inhibitors of cathepsin K, several Streptomyces strainshave been screened. The strain designated IS2-4 was observed to secrete inhibitors ofcathepsin K into its growth media. A bioassay-guided purification of the inhibitoryactivity resulted in the isolation of five compounds, 6-10. Although appearing to bederivatives of the known microbial cysteine protease inhibitor leupeptin, compounds 6-10are structurally novel. Compounds 6 and 9 inhibited cathepsin K in a concentrationdependent manner with Ki values of 44 and 64 μM, respectively.In addition, a 2.1 Å resolution crystal structure of cathepsin K in complex with 6was determined. The structure revealed that compound 6 has been cleaved by cathepsin Kinto acetyl-leucyl-leucine and a pyridotriazine fragment, with the former interacting withthe S1’ and S2’ subsites and the latter binding in the S2 subsite. These results suggest aunique mechanism for the inhibition of cathepsin K. Moreover, since cathepsin Knormally prefers leucine residues at S2, the preferential binding of the pyridotriazinefragment of 6 over the acetyl-leucyl-leucine fragment at S2 is unusual as well.

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