CMB

Lecture on amino acid degradation and the urea cycle

D. Nelson, last modified Dec. 5, 2005

Reading: Berg, Tymoczko and Stryer 5th edition, Chapter 23

Biochemical pathways are all linked together. Fatty acids and cholesterol are made from acetyl CoA generated by the TCA cycle. These carbons are exported to the cytosol as citrate and reconverted to acetyl CoA and oxaloacetate by ATP citrate lyase. Nucleotides are made starting with amino acids and sugars. To see these interconnections look at Fig. 14.2 p. 375 Notice the large number of lines in this figure that connect to pyruvate and acetyl CoA, just above the TCA cycle. The degradation of amino acids is also linked to pyruvate, Acetyl CoA and the TCA cycle. in fact: ALL TWENTY AMINO ACIDS ARE BROKEN DOWN INTO PYRUVATE, ACETOACETATE AND FOUR TCA CYCLE INTERMEDIATES. (see Fig. 23.21 p. 649).

REMOVAL OF AMINO NITROGEN

One of the key steps in amino acid degradation is removal of the alpha amino group. There are two routes used to remove alpha amino groups. These are transamination and deamination. Transamination is the most common method. Nearly all transaminases use pyridoxal 5' phosphate as a coenzyme to transfer the amino group. For a review of pyridoxal phosphate and its numerous roles in enzymes see pp. 640-641. For the specific involvment of pyridoxal phosphate in transaminations see Fig. 23.10 p. 641.

Before substrate is bound, pyridoxal phosphate exists as a Schiff base with an active site lysine. This is an easily reversible condition and the substrate amino group can compete with the active site lysine amino group to form the Schiff base with the pyridoxal phosphate. The Schiff base is hydrolyzed to release the alpha keto backbone of the amino acid without the amino group, which remains attached to the pyridoxal phosphate as pyridoxamine phosphate. At this point, another alpha keto acid can react with the pyridoxamine to reform the Schiff base. The enzyme active site lysine can then displace the substrate and reform the Schiff base with the pyridoxal phosphate. The net result is transfer of the alpha amino group from an amino acid to an alpha keto acid. This forms a new amino acid and a new alpha keto acid, as in glutamate and oxaloacetate reacting to form aspartate and alpha ketoglutarate.

Transamination moves the amino acid from one carbon skeleton to another. It does not eliminate the amino group as ammonia. The elimination of the alpha amino group requires oxidative deamination. One enzyme that does this reaction is glutamate dehydrogenase. The main function of transamination is to funnel amino nitrogen into just a few amino acids so enzymes like glutamate dehydrogenase can deaminate them. This is economical since the cell does not have to make 19 different dehydrogenases. (Remember that proline is an imino acid, so it could not be handled in the same way in a deamination reaction).

The glutamate dehydrogenase enzyme is reversible and it can act in both directions, in biosynthesis of glutamate and in the breakdown of glutamate. (see text on p. 640) The oxidative deamination reaction uses NAD+, while the synthetic reaction uses NADPH.

In the deamination mode, glutamate is oxidized by a hydride transfer of two electrons and one proton to NAD+ (a two electron acceptor) to form NADH. Ammonia is released when a lysine amino group on the enzyme displaces the alpha nitrogen to form a temporary covalent adduct with the alpha carbon. This is hydrolyzed to release alpha ketoglutarate. The product, alpha ketoglutarate, can be used in further transamination reactions to feed alpha amino groups into this pathway for elimination as ammonia.

What happens to the ammonia? Ammonia is toxic and must be excreted. It takes a lot of water to eliminate ammonia and keep its concentration relatively low. This is no problem for microorganisms and animals that live in water. They can eliminate ammonia by diffusion. It is a problem for land animals that need to conserve water. One solution used in many animals including humans is conversion of ammonia to urea. Urea is a more concentrated form of nitrogen, with two nitrogens per molecule and it is less toxic and highly water soluble. Birds are even more water conservative and they excrete uric acid. Uric acid is a more concentrated form of nitrogen with four nitrogens per molecule. It is a purine. Uric acid is not very soluble and in birds, it is excreted as crystals.

THE UREA CYCLE

(fig 23.16 p. 644, text from pp. 644-649) Urea is formed in the urea cycle. The last step is cleavage of arginine to form urea and ornithine. If this last step is not taken, then the urea cycle enzymes catalyze the last three steps in the synthesis of arginine. There are only four enzymes in the urea cycle, but in mammals, they are located in two different compartments, the cytosol and the mitochondria, so two intermediates, ornithine and citrulline, need to be transported back and forth across the mitochondrial inner membrane for the cycle to work. This is done by an ornithine mitochondrial carrier and a citrulline mitochondrial carrier, from the same family as the ADP/ATP carrier and the phosphate carrier. The human ornithine carrier called ORNT1 was just shown to cause the HHH syndrome (hyperornthinaemia, hyperammonaemia, homocitrullinuria) when mutated (Nature Genetics 22, 151-158 1999). Ammonia and ornithine are elevated because the ornithine cannot be transported into the mitochondria, thus ammonia cannot be properly removed. The homocitrulline probably comes from carbamylphosphate condensing with lysine in the absence of ornithine in the mitochondria.

In yeast, all the enzymes of the urea cycle are cytosolic. However, ornithine, which is needed for the first step in the cycle, is made by a five enzyme pathway in the mitochondria, so ornithine must be exchanged across the mitochondrial inner membrane to make arginine in the cytosol. In mammals, ornithine biosynthesis is cytosolic. Though yeast and mammals have some of their enzymes in different compartments, ornithine still has to move back and forth across the inner membrane.

The urea cycle is a means to convert ammonia into urea. The first reaction in this process is not part of the urea cycle, but it produces carbamoyl phosphate that is needed in the first step. The urea cycle cannot go forward without carbamoyl phosphate. This is made from bicarbonate and ammonia by an enzyme called carbamoyl phosphate synthase I.

In mammals, there are two carbamoyl phosphate synthase genes, CPS I and CPS II. CPS I is mitochondrial and is committed to biosynthesis of arginine and the urea cycle. It is the most abundant protein in the mitochondrial matrix, making up 15-26% of the matrix protein. CPS II is cytosolic and committed to the de novo pyrimidine biosynthesis pathway. CPS II is a mulifunctional enzyme with three enzymes coded in one polypeptide chain. These are CPS, aspartate transcarbamoylase (ATCase) and dihydroorotase. The intermediates channel from one enzyme active site to the next without exchanging with the cytosolic pool.

The situation is similar in yeast. There are still two CPS enzymes, one is committed to the urea cycle and arginine biosynthesis, The other is part of a multifunctional enzyme complex found in the nucleus called URA2. URA2 has three enzymatic activities and a non- functional domain from the fourth enzyme in this pathway. These are glutamine amidotransferase, glutamine dependent carbamoyl phosphate synthetase, aspartate transcarbamoylase (ATCase) and a part of dihydroorotase. This last enzyme is encoded in an active form by the URA4 gene.

The CPS II and the yeast URA2 (for pyrimidine biosynthesis) both get their amino group from glutamine rather than ammonia.

Let us concentrate now on the CPS I that is tied to the urea cycle and arginine biosynthesis. This enzyme requires bicarbonate, ammonia and 2 ATP to form carbamoyl phosphate (p. 645). The first ATP reacts with bicarbonate to form carbonyl phosphate and ADP. The carbonyl phosphate reacts with ammonia to release phosphate and form carbamate. The carbamate reacts with the second ATP to form carbamoyl phosphate and another ADP. It is expensive to make this compound. However, a portion of this energy is used in the first step of the cycle, when ornithine reacts with carbamoyl phosphate to form citrulline catalyzed by ornithine transcarbamylase. On Sept. 17, 1999 an 18 year old patient with a defect in OTCase died as a result of a gene therapy experiment with an adenovirus vector delivering OTCase to his liver. You need to keep in mind when you study these pathways that they are not just details to memorize, but they have human consequences.

Citrulline then must be exported from the mitochondrion. The citrulline molecule has one nitrogen that came from ammonia generated by oxidative deamination. In the next step of the cycle, a second nitrogen is donated by aspartate. Citrulline is activated by addition of an AMP group to the oxygen that came from carbamoyl phosphate. This costs two high energy phosphate bonds, since the pyrophosphate PPi is hydrolyzed. The AMP group is displaced by the alpha amino group of aspartate to form agininosuccinate. This is then cleaved by agininosuccinate lyase (or argininiosuccinase) to make arginine and fumarate, a TCA cycle intermediate. Notice that the fumarate cleavage was not done by hydrolysis, since that would have given citrulline again and wasted two high energy phosphate bonds. The fumarate can move through the TCA cycle to oxaloacetate where it can be transaminated back to aspartate. This pathway in conjunction with the urea cycle is sometimes called the Krebs bicycle.

The last step in the pathway is cleavage of the arginine by arginase to make urea and ornithine. Notice that ornithine is an amino acid that is like lysine, but it is one methylene group shorter.

There are two arginase genes in humans. ARG1 codes for a protein in the cytosol and accounts for about 98% of liver arginase activity. The other, ARG2 codes for a protein in mitochondria, as outlined in OMIM. These are expressed in different tissues. It was noticed that researchers working on the Shope papilloma virus had low arginine levels. Patients that are defective in arginase have high arginine levels. Experimental infection of fibroblast cell lines of arginase defective patients showed that arginase levels were restored. This suggested that patients with this disorder might benefit from infection with this virus. This observation was made in 1973, but OMIM does not say that this method was actually used on patients.

The urea cycle is mainly located in the liver. Therefore, ammonia made in other tissues must be transported to the liver to be converted to urea. Ammonia is not transported in the blood, rather it is converted to glutamine by glutamine synthase. Glutamic acid reacts with ammonia and ATP to form glutamine. Once in the liver, glutamine is converted back to glutamic acid and ammonia by glutaminase.

An alternative method to transport amino groups is on alanine. This can be formed by transamination of pyruvate. Once in the liver, alanine can transaminate alpha ketoglutarate to make glutamate and pyruvate. The glutamate can be oxidatively deaminated by glutamate dehydrogenase to form ammonia.

AMINO ACID DEGRADATION PATHWAYS

There are twenty amino acids from proteins that have to be degraded when they are in excess. Therefore, there are 20 pathways for this degradation. Do not panic! All twenty amino acids break down into pyruvate, acetyl CoA or four other compounds of the TCA cycle. (see fig. 23.21 p. 649) If they go to pyruvate (3 carbons) or TCA cycle intermediates(4 or 5 carbons), they can be used to make glucose and they are called glucogenic. If they go directly to acetyl CoA they cannot be made into glucose. These can be made into ketone bodies, so they are called ketogenic. Some amino acids are broken down into different fragments that are independently ketogenic or glucogenic. The pathways converge to some common routes and they will be considered in groups.

I WILL TEACH THIS MATERIAL AT A MORE DETAILED LEVEL THAN IS COVERED IN THE BOOK. YOU WILL ONLY BE TESTED ON AMINO ACID DEGRADATION PATHWAYS COVERED ON PAGES 650-655 and points of interest made in these notes concerning similarities between pathways. You will not have to draw out any pathways.

THE C3 FAMILY OF AMINO ACIDS

Several amino acids are broken down into pyruvate. Some only have one part of the molecule that is made into pyruvate, like trp. The other part of trp is converted to alpha ketoadipate and this is degraded like a fatty acid.

The simplest member of the C3 amino acids to degrade is alanine. Transamination between alanine and alpha ketoglutarate give pyruvate and glutamate. Serine and Cysteine are also converted to pyruvate. Serine is converted in one step by serine dehydratase releasing pyruvate, ammonia and water.

Glycine has only two carbon atoms, so in its degradation, it is actually built up to a three carbon serine molecule by donation of a hydroxymethyl group by N5 N10 methylene tetrahydrofolate.

Threonine is broken in half, with one half becoming glycine, and the other half reacting with CoA to form acetyl CoA.

Cysteine is modified by different pathways in different organisms. In bacteria H2S can be made. In mammals the SH group is oxidized by a dioxygenase, then the amino group is transaminated to form glutamate and the SO2 group is removed to form pyruvate. The first intermediate is converted to taurine, a component of bile acids.

Dioxygenases are frequently used in amino acid degradation. They incorporate two atoms of oxygen into product, as opposed to a monooxygenase that puts one oxygen atom into water. These are often used to break aromatic rings, which is hard to do.

Trp has a long pathway for degradation. I will show it to you, but do not memorize it. The first step is a dioxygenase reaction to break the five membered ring. Note that no oxygen is used in amino acid synthesis, but it is used in breakdown. The enzyme is called tryptophan dioxygenase. Defects in this enzyme lead to abnormal levels of serotonin which is a neurotransmitter made from trp. This is thought to be involved in several behavioral disorders such as alcoholism, depression and Tourette syndrome.

The third enzyme of trp breakdown is a monooxygenase that oxidizes the remaining aromatic ring. The fourth step releases alanine that goes on to pyruvate. This make trp a member of the C3 amino acids. The fifth step is another dioxygenase reaction that breaks the aromatic ring. This forms an intermediate in nicotinamide synthesis. Three more steps result in alpha ketoadipate. The pathway of lysine breakdown also leads to this compound. We will talk about the futher processing of this compound when we talk about lysine degradation.

THE C4 FAMILY OF AMINO ACIDS

The C4 family of amino acids is very small. It consists of only two amino acids, aspartate and asparagine. As you may suspect, aspartate can be transaminated to form oxaloacetate, a four carbon intermediate of the TCA cycle. Asparagine can be converted to aspartic acid by asparaginase. Aspartate can also be degraded to fumarate in the urea cycle or the purine nucleotide cycle, as we saw earlier.

THE C5 FAMILY OF AMINO ACIDS

All of these amino acids are converted to glutamate and then to alpha ketoglutarate by glutamate dehydrogenase. These include glutamine that can be converted to glutamate by glutaminase.

The glutamate side chain is an acid. The side chain can also exist as an aldehyde. The compound is then called glutamate gamma semialdehyde. This is an intermediate in the biosynthesis of proline and the degradation of arginine and proline. Remember arginine is cleaved to from ornithine and urea. Oxidative removal of the delta amino group from ornithine to form the aldehyde leads to glutamate gamma semialdehyde.

Proline is converted to the same intermediate by proline oxidase forming a double bond in the five membered ring. The double bond is then hydrolyzed spontaneously to form glutamate gamma semialdehyde.

Histidine is converted to glutamate in four steps. Defects in the first two enzymes in this pathway, histidase and urocanase cause histidinemia that leads to mental retardation.

That leaves only seven amino acids.

METHIONINE, ISOLEUCINE, VALINE AND LEUCINE

Three of these: methionine, valine and isoleucine are all converted to propionyl CoA and this is made into succinyl CoA (pp. 652-653) I will show you the individual reactions, but you will not be held responsible for these on an exam.

Isoleucine and valine are branched chain amino acids with the branch on the beta carbon. Leucine has the branch on the gamma carbon, so it is handled in a slightly different manner. However, the first three enzymes are the same in all three branched chain amino acid degradation pathways.

Isoleucine and valine are first transaminated to form the alpha keto acids. The next step is exactly analogous to pyruvate dehydrogenase conversion of pyruvate to acetyl CoA. A similar enzyme complex does this job and some of the subunits are identical in the pyruvate dehydrogenase (PDH) complex and the branch chain keto acid dehydrogenase (BCKDH) complex. A defect in this enzyme causes maple syrup urine disease, where the alpha keto acids of the three branch chain amino acids build up in the blood. The urine smells like maple syrup from the alpha keto acid of isoleucine. (Smell the vial of isoleucine that I pass around the classroom.) One form of this disease is due to a lower affinity of the complex for thiamine pyrophosphate, and it can be treated by giving patients thiamine. The two CoA products are oxidized to form a double bond between the alpha and beta carbons. Water is added across this double bond and then the two pathways diverge slightly. The isoleucine pathway oxidizes the new hydroxyl from the hydration reaction to make a ketone. The valine pathway cannot do this since there is no methyl group attached to the beta carbon. Instead, CoA is released. In the final step, the CoA is added back on the opposite side of the molecule to the aldehyde and the carboxyl is released as CO2 to form the propionyl CoA. The isoleucine pathway is simpler, there is just a transfer of the acetyl group to CoA to form acetyl CoA and propionyl CoA as the two products.

The propionyl CoA is converted to succinyl CoA, exactly as seen in beta oxidation of odd chain fatty acids, (see fig. 23.26 p. 652 and pp. 611-614) This is a three carbon compound being made into a four carbon compound. The extra carbon is added on as a carboxyl group in a reaction that requires biotin. Biotin is usually involved in carboxylation reactions. The product of the reaction has to undergo an unusual carbon skeleton rearrangement that is done by two enzymes, methylmalonyl CoA racemase and methylmalonyl CoA mutase. The mutase enzyme uses coenzyme B12, (5' deoxyadenosyl cobalamin). The cobalamin part is a heme-like corrin ring with cobalt in the center. The sixth ligand to this cobalt is the deoxyadenosyl group, that is covalently bound to the cobalt. This is the only known example of a cobalt carbon bond in biology. (figure 22.12 p. 612)

In the reaction, a proton is abstracted from the methyl group. Then the carboxyl-CoA group migrates to the methyl group. This results in converting the branched methymalonyl CoA into the linear succinyl CoA.

EXCERPT FROM OMIM ON A MURDER MYSTERY

Hoffman (1991) recounted the story of Patricia Stallings who was sentenced to life in prison for the presumed murder of her infant son with ethylene glycol, an ingredient of antifreeze.[THIS CAUSES ACIDOSIS THAT CAN BE FATAL] While in prison, the woman gave birth to a second son, who was found to have methylmalonicacidemia. William Sly and James Shoemaker at St. Louis University performed analyses of the first son's blood and did not detect ethylene glycol; Piero Rinaldo at Yale University demonstrated the biochemical features of methylmalonicacidemia and found no evidence of ethylene glycol in the body fluids. All charges against Patricia Stallings were dropped. [THIS WAS PROBABLY DUE TO A METHYMALONYL CoA MUTASE DEFECT] Shoemaker et al. (1992) determined that the gas chromatographic peak that had been identified as ethylene glycol by a clinical laboratory was actually due to propionic acid. [BREAKDOWN PRODUCT OF PROPIONYL CoA] Woolf et al. (1992) indicated that the opposite situation can obtain: intentional infantile ethylene glycol poisoning being misinterpreted as an inborn error of metabolism leading to recurrent infantile metabolic acidosis. Hoffman, M. : Scientific sleuths solve a murder mystery. Science 254, 931 (1991).

The methionine pathway is notable for its first step that couples methionine to an adenosyl group of ATP, releasing PPi and S-adenosylmethionine. This is used as a methyl donor in many reactions. Once the methyl group is donated, the S-adenosylmethionine cannot be directly remade. Instead it is hydrolyzed to produce homocysteine and adenosine. The homocysteine reacts with serine to form cystathionine, which is deaminated and cleaved to form cysteine and alpha ketobutyrate. This compound is processed by another enzyme complex (alpha keto acid dehydrogenase) similar to pyruvate dehydrogenase to make propionyl CoA.

Leucine as was mentioned earlier has a branch at the gamma carbon. This changes its fate from the isoleucine and valine pathways. The five carbon CoA compound is carboxylated to make it a six carbon CoA. Then water is added across a double bond as was seen for the other branched chain amino acids. Then the six carbon unit is cleaved to make acetyl CoA and acetoacetate.

Now we have lysine, phenylalanine and tyrosine to consider.

LYSINE

Lysine is degraded in 11 steps. One important thing to remember is that lysine and tryptophan degradation converge at alpha ketoadipate. A Point of interest is the conversion of alpha keto adipate to glutaryl CoA that is done by the same enzyme that acted on alpha keto butyrate in the methionine pathway. This is alpha keto acid dehydrogenase, similar to pyruvate dehydrogenase. Several of the steps downstream from this are just beta oxidation of fatty acids. The last intermediate before production of the final products is HMG CoA (hydroxy methylglutaryl CoA). This was the same in the leucine degradation pathway, and the products are the same acetoacetate and acetyl CoA.

PHENYLALANINE AND TYROSINE

Phenylalanine and tyrosine are very similar in structure and they are both degraded by the same pathway. Phenylalanine is converted to tyrosine by oxidation of the aromatic ring. This is not the usual way for tyrosine to be synthesized, but it keeps tyrosine from being an essential amino acid in humans. The oxidation of an aromatic ring is tough chemistry and it requires a special coenzyme tetrahydrobiopterin. The enzyme is called phenylalanine hydroxylase. Deficiency of this enzyme causes phenylketonuria(PKU). Every baby born in the US is tested for PKU, since it leads to mental retardation if a low phenylalanine diet is not followed immediately. Soft drinks that use Aspartame have warnings on the labels that the drinks contain phenylalanine. The result of a lack of the phenyalanine hydroxylase is a buildup of phenylpyruvate in the blood. This is the transaminated product of phenylalanine. Phenylpyruvate is an inhibitor of the brain pyruvate dehydrogenase complex, but it is not very effective against the liver PDH. There is a possibility that inhibition of PDH in the brain causes the mental retardation seen in untreated PKU.

The breakdown of tyrosine still requires breakage of the aromatic ring. This is done by two successive dioxygenase reactions. The first requires ascorbate (vitamin C). The second cleaves the ring of homogentisate to make a product that is isomerized and cleaved to form fumarate and acetoacetate. The enzyme is called homogentisate 1,2 dioxygenase (HGO). Failure to cleave homogentisate causes alkaptonuria(AKU). The Sept. 1996 issue of Nature Genetics(available in my office) has a two page summary of the history of this disease, and an article that shows finally that AKU, the disease, is caused by mutations in HGO, the enzyme.

The story is summarized here. Homogentisic acid (HGA) causes urine to turn black on standing in patients with black urine disease. This was discovered in 1898 by Archibald Garrod. In 1902 he wrote a paper that showed this disease was an autosomal recessive genetic trait, only two years after Mendel's laws of genetic inheritance were rediscovered. They had been published in 1859 and lay unknown for 40 years. In 1908 Garrod proposed this disease was an inborn error of metabolism. It then took 50 years before a lowered level of HGO activity could be shown. Another 36 years went by before the AKU trait in humans was mapped to chromosome 3q2. Workers next cloned an HGO gene from a fungus and blast searched the human EST database to find the human homolog. Then they used fluorescence in situ hybridization (FISH) to map the human gene to 3q21-q23, the same site as the AKU trait. Patients with the disease were shown to have mutations in the gene and these when expressed in E. coli had no activity, so the genotype matched the phenotype and AKU was proven to be caused by mutations in HGO. It only took 98 years.

Tyrosine is also the direct precursor of dopa, used in making dopamine. Dopa can also go on to form melanin, the pigment in human skin. The tyrosinase (tyrosine hydroxylase) enzymes used in tryosine degradation and dopamine biosynthesis are different enzymes and they are found in different tissues. This is an example of the same product (dopa) being used for different purposes in different compartments. Lack of tyrosinase in melanocytes causes albinism, due to the inability to synthesize melanin.