Theoretical Study of Metalloenzymes

An essential element in bioenergetics is proton pumping, in which protons are driven from one side of the membrane to the other, coupled with light-induced excitation (e.g. bacteriorhodopsin) or redox coupled processes involving transition metal ions (e.g. cytochrome c oxidase). The resulting concentration gradient is employed by other energy consuming processes such as ATP synthesis, as in the ATP synthase above. Therefore, proton pumps can be thought as the "power engines" of living systems. Due to their importance in bioenergetics, proton pumps have attracted much attention both experimentally and theoretically. Although concepts such as "proton wires" are well accepted and characterized in a number of systems, more issues such as the coupling between electron transfer, chemistry at redox sites and proton translocation are still under active research and debate. Computational studies beyond classical MD should be able to provide useful insights into the working mechanisms of those complicated systems.

Our long-term goal is to understand the detailed mechanism of cytochrome c oxidase (ccO), one of the most important proton pumps that has been studied extensively. X-ray and mutagenesis studies have revealed two channels that facilitate proton translocation within the protein and are believed to be important in different stages of the catalytic cycle. However, the precise relationship between proton pumping and the reactions at the redox site is not understood and different mechanisms have been proposed. For example, the classical paradigm suggests that all four protons are pumped after the initial reduction of the binuclear center and the binding of O2. This mechanism was recently challenged by Michel, who proposed, based on the re-evaluation of available experimental data and the principle of electroneutrality, that one proton is pumped before O2 binding. Also the proton acceptors in several proposed intermediates are not known, and it is not clear whether protons associated with them are "chemical" (for O2 reduction) or "physical" (for pumping). The precise role of the copper ion in the proton pumping process is also not well established. Careful computational work on the energetics of proposed pathways and dynamics of ccO will be of great value in complementing experimental investigations on these mechanistic issues.

The role of transition metals in neuroscience have not been recognized until fair recently, mainly driven by the explosive number of publications pointing to their importance in the regulation of radicals that are associated with many neurological diseases. Therefore, it is of great value to understand the specific role of those metal ions in radical chemistry, and how are their functions regulated by the sequence, structure and dynamics of the biomolecules to which they bind. More perplexing is the role of redox-inactive ions such as zinc and aluminum. Although they are not capable of generating radical species directly, they are present in many proteins that are relevant to neurodegenerative disorders (e.g. metallothionein) and are believed to participate in many reactions indirectly. Is their role mainly structural, or do they influence the redox properties of other metals through electrostatic interaction? How are the binding properties of the metal ions regulated, and what is the consequence of their binding on protein conformations? These are questions that are ideal for computational studies.

One system of great interest is the Cu, Zn-superoxide dismutase (CZSOD), an enzyme that employs Cu/Zn to convert superoxide to dioxygen and hydrogen peroxide and therefore is the major defense against superoxide. Strikingly, one mutation (e.g. A4V) can transform this antioxidant into a toxic pro-oxidant that causes amyotrophic lateral sclerosis (ALS). Recently, it was found that ALS-related mutations cause a dramatic loss in the Zn binding affinity of CZSOD. The Zn-deficient CZSOD was proposed to be a stronger oxidant, and can react with cellular reductants and generates superoxide, which may react with NO to form a strong pro-oxidant that was sufficient to induce apoptosis in cultured neurons. In earlier works, however, it was found that Zn-deficient Cu-apoSOD has a similar reduction rate as the wild type. It was proposed that the major role of the zinc ion is to facilitate the product release via an internal displacement reaction, forcing the superoxide into an axial position, which is suitable for dissociation. To better understand the role of the zinc ion in CZSOD, computational work will be carried out to probe the redox property of the copper site, pK of active site residues and energetics of relevant chemical steps for both the wild type enzyme and mutants known to be involved in ALS. The results will yield a detailed view on the function of CZSOD, and possibly some general features of metalloenzymes that employ more than one metal ion in the active site.