Dopamine Decarboxylase

Craig O'Neill '04 and John Paul Barringer '04


Biomolecules Index

Contents:


I. Introduction

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  DOPA decarboxylase synthesizes important neurotransmitters dopamine and serotonin.  The catecholamine biosynthetic pathway was first characterized from the enzyme DOPA decarboxylase (Christenson et al., 1972).  Highly purified preparations from guinea pig kidneys were used to find DOPA decarboxylase acts in both serotonin and dopamine pathways through its ability to decarboxylate all the naturally occurring aromatic amino acids (Christenson et al., 1972).   However, its physiological function in the kidneys and liver is still unknown (Krieger et al., 1991).  Early research used drosophila as an animal model to understand the different forms of the enzyme dopa decarboxylase (AADC) produced in specific tissues.  The ADDC mRNA of the hypodermis is not the same as the AADC mRNA found in neurons.  Krieger et al. (1991) has demonstrated that two mRNA AADC differ in their 5’ untranslated region.  The enzyme is of great interest to researchers, because the body’s inability to regulate serotonin and dopamine levels causes many diseases, such as Parkinson’s disease (PD).
        Parkinson’s disease (PD) is a chronic, progressive neurological disorder.  It’s symptoms are characterized by tremors, bradykinesia, rigidity and postural instability.  Although the case is unknown, it is hypothesized that the degeneration of dopamine-producing cells in the substantia nigra of the brain causes the disease.    The pathway used for the synthesis of dopamine comes from the L-3,4-dihyroxyphenylalanine (L-DOPA).  L-DOPA is derived from dietary tyrosine.   The enzyme used to catalyze the reaction is vitamin B6-dependent aromatic amino acid decarboxylase (DOPA decarboxylase, DDC).  It is primarily found in the nervous system and the kidney.  Therefore, if L-DOPA is supplemented into the blood stream, it is rapidly converted to dopamine creating an effective treatment for PD.  However, supplementing dopamine directly into the blood stream is ineffective because it cannot pass through the blood-brain barrier.  Administering dietary L-DOPA bypasses this problem and increases dopamine in nerve cells.  The newly synthesized dopamine is stored in granulae in dopaminergic nerve terminals and is released into the synapse following electric stimulation from the axon.  PD gradually decreases the number of dopaminergic cells.  The brain compensates by developing new synaptic contacts on remaining neurons and also by increasing the sensitivity and number of dopamine receptor cells.  However, L-DOPA is rapidly converted to dopamine when administered as drug so only a small amount will reach the nervous system.  The addition of a DDC inhibitor such as the LDOPA products carbiDOPA or benserazide increases the amount of L-DOPA, which can reach the brain.  Therefore, more dopamine is in the blood stream and nervous system, which allows for the reduction of PD side effects while simultaneously reducing the effects of high concentration of L-DOPA in the bloodstream (nausa, daytime sleepiness and involuntary movements).  Burkhard et al. (2001) in the following paper presents the crystal structures of pig kidney DDC in complex with carbiDOPA at 2.6 and 2.25 A resolution.  This provides evidence for the mode of binding of the inhibitor and suggests ways to design more specific DDC inhibitors, which could potentially benefit millions of people who suffer from PD.


II. General Structure

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Burkhard et al. (2001) describes the three-dimensional x-ray crystallography structure of DDC (ligand-free form) in complex with the anti-Parkinson drug carbiDOPA.  DDC is tightly coupled with a2-dimer.  It is a typical fold of the a-family of pyridoxal a-family of pyridoxal 5’-phosphate (PLOP)-dependent enzymes.  The enzyme aspartate aminotransferase (AAT) is the prototype for this family.  The two monomers shown to the  right are each composed of three distinct domains.  The DDC’s large domain contains the PLP binding site , which consists of a central, seven-stranded mixed beta-sheet enclosed by eight alpha-helices in a alpha/beta fold.  Directly opposite of the large domain is a small domain compacted against it.  The small domain consists of a  four-stranded antiparallel beta-sheet with three helices.   DDC also contains an additional N-terminal domain (see residues 1-85).  The N-terminal domain  is composed of two parallel helices linked by an extended strand.  The structure of this domain flaps over the top of the second subunit.  The first helix of one subunit aligns antiparallel to the equivalent helix of the other subunit.  Residues 75-77(N-terminal) and residues 433-435(small domain) form a short two-stranded B-sheet.   If the structure of DDC is compared to two other members of the family; bacterial ornithine decarboxylase (OrnDC) and dialkylglycine (DGD). The large and small domains of DDC and OrnDC look very similar upon initial examination.  However, their N-terminal domains differ significantly and the C-terminal domain of OrnDC (residues 620-730) is not present in DDC at all.  Structural equivalence between these two starts from residue 114 within the forth a-helix of DDC when looking from the N-terminus.  DDC and DGD are structurally equivalent starting from residue 86 within a-helix 3 of DDC. 


III. Active Site

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 The active site of DDC is composed mainly of residues from single monomer, which his located near the monomer-monomer interface.  A Schiff base linkage binds Lys 303 to the cofactor PLP (Pyridoxal 5'-phosphate-dependent enzyme) in the internal aldimine form of the ligand-free DDC.  The obligatory carbanionic intermediates are stabilized by a strong electron sink formed from the salt bridge between the carboxylate group of Asp 271 and the  protonated pyridine nitrogen of the cofactor.  The phosphate group of the cofactor is further anchored to the protein through an extended hydrogen bond network

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The positive pole of the helix dipole balances the negative charge of the phosphate moiety.  The amino acids Ile 101’ and Phe103’ provide two active site residues, which belong to the substrate binding pocket.  They are in van der Waals contact with the catechol ring of the inhibitor carbiDOPA.  In a previous experiment carried out by Dominici et al, the Cys 111 was replaced by an Ala residue or the formation of a disulfide bridge abolishes enzyme activity (Burkhard et al., 2001).  This is because in both structures the sulfhydryl group of Cys 100’ is only 4.1 A apart from that of Cys 111.


IV. Inhibitor Binding Mechanism

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The inhibitor binds by mimicking the external aldimine enzyme-substrate intermediate.  The inhibitor carbiDOPA binds to the PLP cofactor by forming a hydrazone linkage   through its hydrazine moiety.  The catechol ring of carbiDOPA is implanted in the active site cleft and penetrates behind the cofactor ring plane.  At the bottom of the active site cleft, there is the 4’ catechol hydroxyl group of the inhibitor bonded to the hydroxyl group of Thr 82.  The phosphate group receives a hydrogen bond from the 3’ catechol hydroxyl group of carbiDOPA to aid in substrate binding.  The imidazole ring of His 192 is a highly conserved residue stacked in front of the cofactor pyridine ring.  A hydrogen bond forms between the carboxylate group of carbiDOPA and His 192.  The imidazole ring of His 192 possibly could play an important role in catalytic activity, because H192A mutants loose catalytic activity completely.  Burkhard et al (2001) hypothesizes that His 192 catalytically activates the side chain of Tyr 332.  In the active site Lys 303 displaces the amino group of the product through a nucleophilic attack on the imine bond resulting in the product releasing.  The reaction is controlled by the specificity of PLP-dependent enzymes, in which the external aldimine intermediate orients itself perpendicularly to the coenzyme p-bonding system.  Therefore, the reaction is optimized, because the s-p orbital overlap in transition state is maximized.  Upon close examination of the complex, the carboxylate moiety of the inhibitor is oriented with the Ca-CO2- bond approximately orthogonal to the plane of the coenzyme ring.  The orientation allows the complex to take advantage of stereoelectric effects, which control the reactions specificity.


V. Catalytic Loop (not visible in PDB file)

 The residues form a short stretch of 11 amino acids (residues 328-339) creating a mobile loop (not visible in the crystal structure) that plays an important role in the catalytic mechanism (Burkhard et al., 2001).  DDC lacking the loop is catalytically inactive.  The loop adopts a less solvent and protease-exposed conformation during catalysis.  The loop is located at the dimmer interface and extends towards the active site of the other monomer in a closed conformation.  Some of the loop residues take part in the catalytic mechanism by closing the active site cleft from the solvent during catalysis.  There are also highly conserved residues in the flexible loop of DDC essential for the catalytic reaction.  The most conserved residues are Tyr332 and residue 334 as either Lys or Arg.  The conserved residues are located in the middle of the loop.  If the loop is closed than these residues are placed in close proximity to the active site cleft.  The carboxylate moiety of the inhibitor is exposed to the solvent within the crystal structure.  Therefore, there could be a hydrogen-bonding ionic interaction between Lys 334 and the carboxylate group of the substrates.  The result is two structural water molecules are replaced.  The loop might also explain why the there aren’t differences between the ligand-free and complex structures.  Therefore, a likely explanation is that some of the loop residues interact with the inhibitor, specifically Try residues act as a proton donor for the quinonoid Ca during catalysis.  Evidence to support this hypothesis come from the fact that if Y332F is substituted then the enzyme is catalytically inactive.

IV. References

    Burkhard, P., Dominici, P., Borri-Voltattorni, C., Jansonius, J. N., Malashkevich, V. N.: Structural Insight Into Parkinson's Disease Treatment Gained from Drug-Inhibited Dopa Decarboxylase Nat.Struct.Biol. 8 pp. 963 (2001)

    Cumming, Paul; Gjedde, Albert. Compartmental analysis of dopa decarboxylation in living brain from dynamic positron emission tomograms Synapse Volume: 29, Issue: 1, May 1998. pp. 37 - 61.

  Christenson, James G.; Dairman, Wallace;  Udenfriend, Sidney. On the Identity of DOPA Decarboxylase and 5-hydroxytryptophan Decarboxylase Proceedings of the National Academy of Sciences of the United States of America, Vol. 69, No. 2. (Feb., 1972), pp. 343-347.

     Deep, Paul; Dagher, Alain; Sadikot, Abbas; Gjedde, Albert; Cumming, Paul. Stimulation of dopa decarboxylase activity in striatum of healthy human brain secondary to NMDA receptor antagonism with a low dose of amantadine Synapse Volume: 34, Issue: 4, 15 December 1999. pp. 313 - 318.

     Krieger, Monique; Coge, Francis; Gros, Francois; Thibault, Jean. Different mRNAs Code for Dopa Decarboxylase in Tissues of Neuronal and Nonneuronal Origin Proceedings of the National Academy of Sciences of the United States of America, Vol. 88, No. 6. (Mar. 15, 1991), pp. 2161-2165.

    Moore, Ps; Dominici, P; Borri Voltattorni, C. Transaldimination induces coenzyme reorientation in pig kidney Dopa decarboxylase Biochimie Volume: 77, Issue: 9, 1995. pp. 724-728.


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