Studies improve understanding of drug targets

Researchers have developed a new structural understanding of how the two key subunits of kinases, one of the most important classes of enzymes, work together. kinases have increasingly become prime targets for drugs to treat an array of diseases.

These kinds of studies could lead to a novel class of drugs that inhibit specific kinases to treat diseases. Most of the highly specific inhibitors, such as Gleevec, interfere with the ATP binding site of the kinase. However this kind of understanding of PKA presents an opportunity to identify other molecules that could target other sites on these enzymes.

Protein kinase A and approximately 600 "cousin" kinases are among the cell's most important switching components as they control activity of other proteins by attaching phosphate groups to them. Protein kinase A (PKA) alone regulates a variety of processes including growth, development, memory, metabolism, gene activation and lipid breakdown.

The researchers believe their latest findings offer insights that extend beyond the workings of PKA and serve as a general model for understanding how kinases function. Such functional insights offer new ideas for developing drugs to treat disease.

PKA consists of a dual-lobed catalytic subunit that performs two central functions. The small lobe accepts the molecular phosphate source, the energy-rich adenosine triphosphate. And the larger lobe docks with the target protein that is to be phosphorylated. That phosphorylation takes place in a key region of the enzyme, called the active site, in a cleft that opens during activation.

The process of protein phosphorylation is an important regulation mechanism in eukaryotic cells. The kinases serve as switches to turn pathways on and turn them off. They constitute one of the largest gene families, accounting for two per cent of mammalian genes.

The researchers, led by Susan Taylor, at the University of California at San Diego, published their findings in the February 4, 2005, issue of Science.

According to Taylor, the enzyme is a good exemplar for studying kinases because the protein is easily purified and manipulated. "Since then, PKA has provided the template for the entire field of kinase studies," said Taylor.

The research centres on the discovery of a regulatory subunit with domains that bind to the chemical messenger molecule cyclic AMP (cAMP), which triggers PKA into action. That regulatory subunit features a flexible extension that inhibits the catalytic subunit by docking with the active site. This maintains PKA in a dormant state until it is triggered by cAMP.

Cyclic AMP is a messenger that serves as a universal signalling molecule. Its primary responsibility is to sense changes in the environment outside the cell and communicate those changes to structures in the interior of the cell to trigger a response.

The researchers also discovered molecular features on its surface that enable it to integrate into tightly regulated signalling cell machinery. The cAMP activates PKA by plugging into the regulatory subunit, triggering it to release the catalytic subunit. The catalytic subunit opens the active site cleft, which proceeds to phosphorylate the target protein. The regulatory subunits also bind to scaffold proteins thereby creating signalling units in close proximity to substrates.

There is a feeling in the scientific community of a major gap in the understanding of PKA. Scientists are still struggling to determine the critical interface between the catalytic and regulatory subunits.

The latest research focuses on this area, about how the catalytic and regulatory subunits interact at the molecular level. At the outset of the studies, the researchers constructed a special version of the two bound subunits that was stable enough to be crystallised and subjected to structural analysis using x-ray crystallography.

The resulting structure of the PKA subunits revealed precisely how the inhibitor sequence on the regulatory subunit docks to the active site, and how cAMP binding leads to activation. The structure also reveals that the large lobe of the catalytic subunit acts as a stable scaffold for such functions as binding the regulatory subunit.

In contrast, the new structure reveals that the regulatory subunit undergoes major conformational changes during cAMP binding and activation.

The insights from the new structure also reveal which individual amino acid units, or residues, in this lobe are common among kinases, and which ones could contribute to the diversity that enables kinases to insert themselves into the vast array of signalling mechanisms in the cell.

"Protein kinase is a sophisticated enzyme," said Taylor.

The enzyme not only carries out catalysis, but binds to other proteins. They use their surface to recognise other proteins, in a sense using different sets of surfaces as a complex molecular `language'.

"When they are in an inhibited state, they interact with one set of surfaces (molecules) and when active, they interact with a different set of molecules. They bring together a signalling complex of proteins by adding phosphates and interacting with other proteins."

Taylor added that rules they were discovering for how the regulatory subunit binds to the catalytic subunit of PKA were enabling the team to ask what some of the general rules for kinases as their role in regulation is so important.

"We can begin to computationally dissect these molecules and understand how they function. And from there, we can extend our understanding to how they build signalling networks with other proteins, as well as how they functional internally, for example, how the binding of a molecule at one end of the protein can be sensed at the other end," she added.