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Research Overview Research in my laboratory uses a multi-disciplinary, collaborative and structurally-oriented approach to address key problems in biology and medicine. At the molecular level, we study the structure and dynamics of proteins and their complexes with other proteins, nucleic acids and small molecule ligands. My independent career began as a biomolecular NMR spectroscopist, but has evolved to a point where I could be categorized as a structural biochemist. At the technical level, we now make use of many structural and biophysical techniques, including calorimetry, fluorescence spectroscopy, X-ray crystallography, X-ray/neutron scattering, cryo electron microscopy and computation. These studies are integrated with in vitro and cell-based biochemistry, in our own lab and by numerous collaborators at our institution, around the country and across the world. The following sections outline our three research programs. The Structural Basis for Function of DNA Processing Machinery One of the great scientific challenges today is to understand how proteins act together to perform the major processes in a cell such as DNA replication, all of which involve a sequence of multiple biochemical steps. Much of our work has revolved around human Replication Protein A (RPA), the major eukaryotic single-strand DNA (ssDNA) binding protein, which is essential for most DNA transactions in all cells. RPA is structurally very complex with three subunits containing eight different domains. It functions by constantly adjusting its binding of ssDNA and other proteins through structural changes within its domains as well as by altering the organization of its domains.Our work has helped delineate the way in which RPA helps to orchestrate the intricate dance of proteins that is required to replicate DNA, respond when DNA is damaged, and repair the damage. Important insights have been obtained by identifying, and structurally characterizing, the interactions of RPA with specific proteins required for each of these processes. Recently, we have focused on the rearrangements in the global architecture of RPA, the mechanisms of binding and unbinding DNA, and how the binding of protein partners alter the landscape. As we have progressed, there has been an increasing need to determine structures of RPA binding partners. Current efforts center on human DNA primase, XPA and XPC. Together, these studies are laying the foundation to determine how mutations in the DNA processing proteins cause defects that lead to cancer and other diseases. Moreover, we are well invested into exploring translation of this knowledge into potential therapeutics by using fragment-based inhibitor discovery targeted to suppressing RPA-mediated recruitment of proteins to sites of DNA damage. Structure and Function of U-box E3 Ubiquitin Ligases. Covalent attachment of ubiquitin to a target protein serves as a cellular signal. For example, poly-ubiquitination of a target typically signals for degradation in the proteasome. Defects in this process are associated with cancer, for example a target can become overabundant if it is not degraded at a sufficient rate. The process of attaching ubquitin to a substrate protein involves a dynamic multi-protein machine comprised of E1, E2 and E3 enzymes. Our laboratory was the first to experimentally determine the structure of the U-box class of E3 ligases. Our studies of U-box proteins have focused on the mechanism of activation of the E2~ubiquitin conjugates, understanding how target proteins are recognized, and what factors control the type of ubiquitin chain attached. We are also investigating how the U-box E3 CHIP differentially regulates targets in the cell stress response. Ca2+ Signal Transduction by EF-hand Proteins Change in levels of calcium inside a cell is a common means for regulating biochemical signaling cascades and stimulating biomechanical actions. EF-hand calcium binding proteins play a central role in virtually every aspect of calcium signaling. Consequently, studies of their response to the binding of calcium and activation of targets are keys to understanding how this ion influences so many aspects of health and disease. I have worked in this field for nearly 30 years, starting as a postdoctoral fellow. Currently we have two active research programs.
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