Research Interests

Cyclic Nucleotide Dependent Protein Kinase–Binding Proteins in Bovine Cardiac Tissues

 

Rationale for Project: 

Approximately 5 million Americans are afflicted with some form of heart failure or cardiac disease at an estimated cost of 40 billion dollars annually (Olson and Molkentin, 1999).  The major symptom associated with heart failure or cardiac disease is the inability of the heart to circulate oxygenated blood as well as it should.  This decrease in pumping efficiency is often caused by blockages in coronary arteries (arteries that supply blood to the heart itself), high blood pressure, or a defect in the cardiac walls or valves.  The inability of the heart muscle to adequately deliver oxygenated blood to peripheral tissues leads to fatigue, weakness, and shortness of breath in the patient making everyday tasks a tiring chore thus decreasing the quality of life for said victims.  In most instances, heart failure and heart disease can be managed by administration of medications but patients continue to lead a lifestyle of reduced activity (American Heart Association, 2000).

Even though much is known about the causes and effects of heart failure and disease, the underlying molecular mechanisms have yet to be elucidated.  We must therefore, through scientific laboratory research, develop an understanding of the biochemistry of molecules in the cardiac tissue.  Knowledge of how these molecules interact with each other is of utmost importance to the subsequent development of novel pharmaceuticals to treat and prevent heart failure and cardiac disease.  Progress has recently been made on this basic medical research front with the discovery that a pair of enzymes known as the cyclic nucleotide-dependent protein kinases are intrinsically involved with maintenance of normal cardiac function. 

The two known cyclic nucleotide-dependent protein kinases in mammals are the cyclic AMP-dependent protein kinase (PKA) and the cyclic GMP-dependent protein kinase (PKG).  These two enzymes are closely related in that they have similar amino acid sequences and similar functions in the cell (Francis and Corbin, 1994).  In response to various cellular signals, each kinase is responsible for the transfer of a phosphate group from adenosine triphosphate (ATP) to a set of target proteins in a process termed phosphorylation.  It has recently been discovered that PKA is responsible for the phosphorylation of the major cardiac proteins, phospholamban and troponin (Sulakhe and Vo, 1995, Ardelt et al, 1998).  Olson and Molkentin (1999) have hypothesized that PKA phosphorylation of phospholamban and troponin are vitally important in the development of cardiac hypertrophy which often accompanies heart failure and cardiac disease.

In separate studies, a novel paradigm for the control or regulation of protein kinases is gaining acceptance.  This novel paradigm is that kinases can have other proteins bound to them for the purpose of regulating the activity of the kinase.  For example, in the brain, PKA is bound to and consequently regulated by another protein named AKAP (A-kinase anchoring protein) (Skalhegg and Tasken, 2000).  Protein kinases other than PKA and PKG have been shown to complex with a different class of enzymes called phosphatases (Westphal et al, 1998).  It is highly probable that either PKA or PKG forms a complex in cardiac tissues with other protein molecules and that said complex is responsible for the control and regulation of PKA or PKG in cardiac tissues. 

The hypothesis of my research is that cyclic nucleotide-dependent protein kinases in cardiac tissues do indeed complex with other proteins (binding proteins).  Identification of these binding proteins would be a major advancement toward the understanding of the regulation of PKA and PKG in normal and heart disease conditions.  Therefore, a major goal of my research is to isolate and identify proteins in cardiac tissues that bind to and regulate the activity of PKA and PKG through the use of standardized biochemical techniques.

Description of Project Methods:

            Isolation and identification of cyclic nucleotide-dependent protein kinase binding proteins are done using bovine (cow) hearts as the model system.  The major advantage to using the cow heart is the ease of procuring the quantity of hearts needed to begin a protein purification project such as this.  Typically four hearts are obtained from a regional slaughterhouse for one attempt to purify any PKA- or PKG-binding proteins.  The hearts are dissected into small pieces and homogenized in 10 liters of cold buffer solution to produce a crude cellular extract as has been previously performed for bovine lungs (Reed et al, 1996).

            A variety of chromatographic techniques are employed to attempt to isolate the binding proteins.  Chromatography techniques typically use a gel-like matrix that has specific molecules adhered to it.  When the extract is passed over the matrix, only proteins of interest in the extract adhere to the molecules of the matrix.  The proteins that remain bound to the matrix can then be eluted off the matrix by changing the conditions in the buffer solution.  This procedure thus provides a measure of purification for specific proteins in the extract.

One type of chromatography used has cyclic AMP molecules adhered to the matrix (Reed et al, 1997).  Both PKA and PKG will adhere to this matrix as would any proteins specifically bound to PKA or PKG.  Theoretically, all other proteins would pass on through this matrix without binding to it.  PKA, PKG, and their binding proteins are eluted off the matrix by adding cAMP to the buffer solution thus separating these proteins from the rest of the extract proteins.  A second type of chromatography system takes advantage of the fact that both PKA and PKG are negatively charged and will therefore adhere to a chromatography matrix that is positively charged.  Proteins that specifically bind PKA and PKG would also be associated with this type of chromatography matrix and could be eluted from it by increasing the ionic strength of the buffer (Smith et al, 2000).

An alternative method of identifying proteins that bind to PKA or PKG is to use antibodies raised against PKA or PKG in experiments called immunoprecipitations.  For this type of experiment, the extracts are incubated with the aforementioned antibodies.  The antibodies are then collected by centrifugation based upon their characteristic adherence to the bacterial protein A that had been conjugated to a matrix bead.  The collected antibodies can then be analyzed for the presence of binding proteins by a technique called electrophoresis.  In this technique, proteins are separated from each other by an electrical field which pulls proteins through a matrix at a rate proportional to the size of the individual proteins.  The separated proteins can be visualized by application of Coomassie Blue, an organic dye that specifically stains proteins.  PKA and PKG-binding proteins that have been separated by electrophoresis are then to be extracted from the electrophoresis matrix in a highly purified state.  By a process known as Edman degradation peptide sequencing, the identity of the protein/s may be determined.

At the “heart” of any science is the objective to acquire more knowledge.  The main reason, therefore, to performing biochemical experiments is to learn more about the functioning of an organism at the molecular level.  It is anticipated that conclusions drawn from these studies in the bovine heart would increase our understanding of the functioning of both the normal human heart and the diseased human heart since the hearts of these two organisms are remarkably similar.  The type of research proposed here should be classified as basic medical research since the direct application of this research is unclear at present.  The objective behind this basic medical research is to discover new information that one day may be directly applied to the treatment of human heart disease through the development of new drugs or other technologies.

 

Future Goals of Project:

            It has once been said that a good research project actually results in the asking of many more questions than it answered.  It is the hope that this preliminary research project would ask more questions than it answers.  These questions would then be the springboard for future research projects.  For example, what is the exact molecular nature of the interaction between the kinases and their binding proteins?  How do the PKA- and PKG-binding proteins regulate the function of these kinases in cardiac tissues?  Is the PKA- or PKG-binding protein complex affected by hormone influence?  Do these PKA- and PKG-binding proteins play similar roles of regulation in other tissues where PKA and PKG are known to function?  The data collected from the successful completion of this research project would be incorporated into a much larger research grant proposal aimed at attracting extramural funding from such resources as the American Heart Association (AHA) or the National Institutes of Health (NIH).

Follow-up studies to this project would be dictated by the results obtained from research of the project proposed here.  It is conceivable that future studies might require the isolation of genes that encode these novel PKA- and PKG-binding proteins thus requiring techniques in molecular biology.  Understanding of the regulation and function of a PKA- or PKG-binding protein complex may only be discovered through in vivo experiments involving heart cells (cardiomyocytes) grown in tissue culture.  The hope is that future studies might provide opportunities for unique intramural collaborations with other scientists here at A.P.S.U. and other institutions.

References

American Heart Association (2000)  http://www.americanheart.org

Ardelt, P., Dorka, P., Jaquet, K., Heilmeyer, L.M., Jr., Kortkle, H., Korfer, R., and Notohamiprodjo, G.  (1998)  Biol. Chem.  379, 341-347.

Francis, S.H., and Corbin, J.D.  (1994)  Annu. Rev. Physiol.  56, 237-272.

Olson, E.N. and Molkentin, J.D.  (1999)  Circulation Research, 84, 623-632.

Reed, R.B., Sandberg, M., Jahnsen, T., Lohmann, S.M., Francis, S.H., and Corbin, J.D.  (1996)  J. Biol. Chem. 271, 17570-17575.

Reed, R.B., Sandberg, M., Jahnsen, T., Lohmann, S.M., Francis, S.H., and Corbin, J.D.  (2000)  Signal Transduction in Health and Disease  31, 205-217.

Skalhegg, B.S., and Tasken, K.  (2000)  Front. Biosci.  5, D678-693.

Smith, J.A., Reed, R.B., Francis, S.H., Grimes, K., and Corbin, J.D.  (2000)  J. Biol. Chem. 275, 154-158.

Sulakhe, P.V., and Vo, X.T.  (1995)  Mol. Cell Biochem.  149-150, 103-126.

Westphal, R.S., Anderson, K.A., Means, A.R., and Wadzinski, B.E.  (1998)  Science 280, 1258-1261.

 

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