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The second regulatory site, the substrate specificity site, can bind either ATP, dTTP, dGTP, or dATP, and the substrate specificity of the enzyme is determined by which of these nucleoti

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enzyme must be turned on and off in response to the need for dNTPs Second,

the relative amounts of each NDP substrate transformed into dNDP must be

con-trolled so that the right balance of dATP⬊dGTP⬊dCTP⬊dTTP is produced The

two different effector-binding sites on ribonucleotide reductase, discrete from the

substrate-binding catalytic site, are designed to serve these purposes As noted

previ-ously, these two regulatory sites are designated the overall activity site and the

sub-strate specificity site Only ATP and dATP are able to bind at the overall activity site.

ATP is an allosteric activator and dATP is an allosteric inhibitor, and they compete

for the same site If ATP is bound, the enzyme is active, whereas if its deoxy

coun-terpart, dATP, occupies this site, the enzyme is inactive That is, ATP is a positive

effector and dATP is a negative effector with respect to enzyme activity, and they

compete for the same site.

The second regulatory site, the substrate specificity site, can bind either ATP,

dTTP, dGTP, or dATP, and the substrate specificity of the enzyme is determined

by which of these nucleotides occupies this site If ATP is in the substrate specificity

site, ribonucleotide reductase preferentially binds pyrimidine nucleotides (UDP

or CDP) at its active site and reduces them to dUDP and dCDP With dTTP in the

specificity-determining site, GDP is the preferred substrate When dGTP binds to

the specificity site, ADP becomes the favored substrate for reduction The

ratio-nale for these varying affinities is as follows (Figure 26.23): High [ATP] is

consis-tent with cell growth and division and, consequently, the need for DNA synthesis.

Thus, ATP binds in the overall activity site of ribonucleotide reductase, turning it

on and promoting production of dNTPs for DNA synthesis Under these

condi-tions, ATP is also likely to occupy the substrate specificity site, so UDP and CDP are

bound at the catalytic site and reduced to dUDP and dCDP Both of these

pyrimi-dine deoxynucleoside diphosphates are precursors to dTTP Thus, elevation of

dUDP and dCDP levels leads to an increase in [dTTP] High dTTP levels increase

the likelihood that it will occupy the substrate specificity site, in which case GDP

be-comes the preferred substrate and dGTP levels rise Upon dGTP association with

the substrate specificity site, ADP is the favored substrate, leading to ADP reduction

and the eventual accumulation of dATP Binding of dATP to the overall activity site

then shuts the enzyme down In summary, the relative affinities of the three

classes of nucleotide binding sites in ribonucleotide reductase for the various

sub-strates, activators, and inhibitors are such that the formation of dNDPs proceeds

in an orderly and balanced fashion As these dNDPs are formed in amounts

con-sistent with cellular needs, their phosphorylation by nucleoside diphosphate

ki-nases produces dNTPs, the actual substrates of DNA synthesis.

26.8 How Are Thymine Nucleotides Synthesized?

The synthesis of thymine nucleotides proceeds from other pyrimidine

deoxyri-bonucleotides Cells have no requirement for free thymine ribonucleotides and

do not synthesize them Small amounts of thymine ribonucleotides do occur in

tRNA (tRNA is notable for having unusual nucleotides), but these Ts arise via

methylation of U residues already incorporated into the tRNA Both dUDP and

1

2

3

4

5

6

Energy status of cell is robust; [ATP] is high Make DNA:

ATP occupies activity site A: ribonucleotide reductase ON

ATP in specificity site S favors CDP or UDP in catalytic site C [dCDP], [dUDP]

dCDP

dTTP occupies specificity site S, favoring GDP or ADP in catalytic site C

dGTP occupies specificity site S, favoring ADP in catalytic site C [dADP]

dATP replaces ATP in activity site A: ribonucleotide reductase OFF

GDP dGDP dGTP

FIGURE 26.23 Regulation of deoxynucleotide biosyn-thesis: the rationale for the various affinities displayed

by the two nucleotide-binding regulatory sites on ribo-nucleotide reductase

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834 Chapter 26 Synthesis and Degradation of Nucleotides

dCDP can lead to formation of dUMP, the immediate precursor for dTMP syn-thesis (Figure 26.24) Interestingly, formation of dUMP from dUDP passes

through dUTP, which is then cleaved by dUTPase, a pyrophosphatase that

re-moves PPifrom dUTP The action of dUTPase prevents dUTP from serving as a substrate in DNA synthesis An alternative route to dUMP formation starts with

From dUDP: dUDP From dCDP: dCDP

dUTP dCMP

dUMP dUMP

dTMP dTMP

FIGURE 26.24 Pathways of dTMP synthesis dTMP

pro-duction is dependent on dUMP formation from dCDP

and dUDP

A DEEPER LOOK

Fluoro-Substituted Analogs as Therapeutic Agents

Carbon–fluorine bonds are exceedingly rare in nature, and

fluo-rine is an uncommon constituent of biological molecules F has

three properties attractive to drug designers: (1) It is the smallest

replacement for an H atom in organic synthesis, (2) fluorine is

the most electronegative element, and (3) the FOC bond is

rela-tively unreactive This steric compactness and potential for strong

inductive effects through its electronegativity renders F a useful

substituent in the construction of inhibitory analogs of enzyme

substrates One interesting strategy is to devise fluorinated

pre-cursors that are taken up and processed by normal metabolic

pathways to generate a potent antimetabolite A classic example is

fluoroacetate FCH2COOis exceptionally toxic because it is

read-ily converted to fluorocitrate by citrate synthase of the citric acid

cycle (see Chapter 19) In turn, fluorocitrate is a powerful

in-hibitor of aconitase The metabolic transformation of an

other-wise innocuous compound into a poisonous derivative is termed

lethal synthesis 5-Fluorouracil and 5-fluorocytosine are also

exam-ples of this strategy (see Human Biochemistry on page 835)

Unlike hydrogen, which is often abstracted from substrates as

H, electronegative fluorine cannot be readily eliminated as the

corresponding F Thus, enzyme inhibitors can be fashioned in

which F replaces H at positions where catalysis involves H removal

as H Thymidylate synthase catalyzes removal of H from dUMP

as Hthrough a covalent catalysis mechanism A thiol group on this

enzyme normally attacks the 6-position of the uracil moiety

of 2-deoxyuridylic acid so that C-5 can act as a carbanion in attack

on the methylene carbon of N5,N10-methylene-THF (see

accompa-nying figure) Regeneration of free enzyme then occurs through

loss of the C-5 H atom as Hand dissociation of product dTMP If

F replaces H at C-5 as in 2-deoxy-5-fluorouridylate (FdUMP), the

enzyme is immobilized in a very stable ternary [enzyme⬊FdUMP⬊

methylene-THF] complex and effectively inactivated Enzyme

in-hibitors like FdUMP whose adverse properties are elicited only

through direct participation in the catalytic cycle are variously

called mechanism-based inhibitors, suicide substrates, or Trojan

horse substrates.

+

dR

dR

dR

H

H2N N

O

N

N

N H H

CH2 N

H2C

R

H

2 3 4 1

8 7

6 9 10 5

N

H

2 3 4

1 6 5

O H

O

Cys SH

N

H

2 3 4

1 6 5

O H

O

S Cys

N

N

H

O H

Cys

CH2

F N

H2N N

O

N

N

H

H

CH2 H

2 3 4

6 9

10 5

E

E

E

R H

H

H

N5,N10 -methylene- THF

Ternary complex

䊳 The effect of the 5-fluoro substitution on the mechanism of action

of thymidylate synthase An enzyme thiol group (from a Cys side chain)

ordinarily attacks the 6-position of dUMP so that C-5 can react as a

carbanion with N5,N10-methylene-THF Normally, free enzyme is

regenerated following release of the hydrogen at C-5 as a proton

Because release of fluorine as Fcannot occur, the ternary (three-part)

complex of [enzyme⬊fluorouridylate⬊methylene-THF] is stable and

per-sists, preventing enzyme turnover (The N5,N10-methylene-THF structure

is given in abbreviated form.)

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dCDP, which is dephosphorylated to dCMP and then deaminated by dCMP

deaminase (Figure 26.25), leaving dUMP dCMP deaminase provides a second

point for allosteric regulation of dNTP synthesis; it is allosterically activated by

dCTP and feedback-inhibited by dTTP Of the four dNTPs, only dCTP does not

interact with either of the regulatory sites on ribonucleotide reductase (see

Fig-ure 26.20) Instead, it acts upon dCMP deaminase.

Synthesis of dTMP from dUMP is catalyzed by thymidylate synthase (Figure

26.26) This enzyme methylates dUMP at the 5-position to create dTMP; the

methyl donor is the one-carbon folic acid derivative N5,N10-methylene-THF The

reaction is actually a reductive methylation in which the one-carbon unit is

trans-ferred at the methylene level of reduction and then reduced to the methyl level.

The THF cofactor is oxidized at the expense of methylene reduction to yield

DHF DHFR then reduces DHF back to THF for service again as a one-carbon

vehicle (see panel a of the figure in A Deeper Look on page 816) Thymidylate

synthase sits at a junction connecting dNTP synthesis with folate metabolism

dCMP deaminase

NH2

O

O

N

N

H

OH

dCMP

NH4

O O

N N

H OH

dUMP

O H

+

H++ H2O

FIGURE 26.25 (a) The dCMP deaminase reaction (b) Trimeric dCMP deaminase Each chain has a bound dCTP

molecule (purple) and a Mg2ion (orange) (pdb id  1XS4)

HUMAN BIOCHEMISTRY

Fluoro-Substituted Pyrimidines in Cancer Chemotherapy, Fungal Infections,

and Malaria

5-Fluorouracil (5-FU; see part a of the figure) is a thymine analog It

is converted in vivo to 5 -fluorouridylate by a PRPP-dependent

phos-phoribosyltransferase and passes through the reactions of dNTP

synthesis, culminating ultimately as 2 -deoxy-5-fluorouridylic acid, a

potent inhibitor of dTMP synthase (see A Deeper Look on page

834) 5-FU is used as a chemotherapeutic agent in the treatment of

human cancers Similarly, 5-fluorocytosine (see part b) is used as an

antifungal drug because fungi, unlike mammals, can convert it to

2-deoxy-5-fluorouridylate Furthermore, malarial parasites can use

exogenous orotate to make pyrimidines for nucleic acid synthesis,

whereas mammals cannot Thus, 5-fluoroorotate (see part c) is an

effective antimalarial drug because it is selectively toxic to these

parasites

NH2

O–

O

H N N

O F

H

O

N N F

H

O

H N N F

H

O

5-Fluorouracil 5-Fluorocytosine

5-Fluoroorotate

(a)

(c)

(b)

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26.1 Can Cells Synthesize Nucleotides? Nucleotides are ubiquitous

constituents of life and nearly all cells are capable of synthesizing them

“from scratch” via de novo pathways Rapidly proliferating cells must

make lots of purine and pyrimidine nucleotides to satisfy demands for

DNA and RNA synthesis Nucleotide biosynthetic pathways are attractive

targets for the clinical control of rapidly dividing cells such as cancers or

infectious bacteria Many antibiotics and anticancer drugs are inhibitors

of purine or pyrimidine nucleotide biosynthesis

26.2 How Do Cells Synthesize Purines? The nine atoms of the purine

ring system are derived from aspartate (N-1), glutamine (N-3 and N-9),

glycine (C-4, C-5, and N-7), CO2(C-6), and THF one-carbon derivatives

(C-2 and C-8) The atoms of the purine ring are successively added to

ribose-5-phosphate, so purines begin as nucleotide derivatives through

as-sembly of the purine ring system directly on the ribose Because purine

biosynthesis depends on folic acid derivatives, it is sensitive to inhibition

by folate analogs Distinct, two-step metabolic pathways diverge from IMP,

one leading to AMP and the other to GMP Purine biosynthesis is regu-lated at several stages: Reaction 1 (ribose-5-phosphate pyrophosphoki-nase) is feedback-inhibited by ADP and GDP; the enzyme catalyzing re-action 2 (glutamine phosphoribosyl pyrophosphate amidotransferase) has two inhibitory allosteric sites, one where adenine nucleotides bind and another where guanine nucleotides bind PRPP is a “feed-forward” activator of this enzyme The first reaction in the conversion of IMP to AMP involves adenylosuccinate synthetase, which is inhibited by AMP; the first step in the conversion of IMP to GMP is catalyzed by IMP dehydro-genase and is inhibited by GMP ATP-dependent kinases form nucleoside diphosphates and triphosphates from AMP and GMP

26.3 Can Cells Salvage Purines? Purine ring systems represent a meta-bolic investment by cells, and salvage pathways exist to recover them when degradation of nucleic acids releases free purines in the form of adenine, guanine, and hypoxanthine (the base in IMP) Hypoxanthine-guanine phosphoribosyltransferase (HGPRT) acts on either

hypoxan-836 Chapter 26 Synthesis and Degradation of Nucleotides

It has become a preferred target for inhibitors designed to disrupt DNA synthe-sis An indirect approach is to employ folic acid precursors or analogs as anti-metabolites of dTMP synthesis (see panel b of the figure in A Deeper Look on page 818) Purine synthesis is affected as well because it is also dependent on THF (see Figure 26.3).

dR

O

O–

H N N O

H

H2N N

O

N

N

N H H

CH2 N

H2C

R

H H

2

7

6

9 10 5

H

H2N N

O

N

N

N

H H

CH2 N H

R

H H

H

H

R O

H N N

O

CH3

H

H2N N

O

N

N

H

CH2 N R H O

C

CH2

+H3N

O C CH +H3N

CH2 OH

N5,N10 -methylene-THF

Thymidylate synthase

Dihydrofolic acid (DHF) Serine

hydroxymethyl-transferase

Dihydrofolate reductase

Tetrahydrofolic acid (THF)

(a)

NADP+

Glycine

NADPH + H+

(b)

FIGURE 26.26 (a) The thymidylate synthase reaction The 5-CH3group is ultimately derived from the -carbon

of serine (b) Thymidylate synthase dimer Each monomer has a bound folate analog (green) and dUMP (light

blue) (pdb id  1JUJ)

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Preparing for an exam? Create your own study path for this

chapter at www.cengage.com/login

1.Draw the purine and pyrimidine ring structures, indicating the

metabolic source of each atom in the rings

2.Starting from glutamine, aspartate, glycine, CO2 and N10

-formyl-THF, how many ATP equivalents are expended in the synthesis of

(a) ATP, (b) GTP, (c) UTP, and (d) CTP?

3.Illustrate the key points of regulation in (a) the biosynthesis of IMP,

AMP, and GMP; (b) E coli pyrimidine biosynthesis; and (c)

mam-malian pyrimidine biosynthesis

4.Indicate which reactions of purine or pyrimidine metabolism are

af-fected by the inhibitors (a) azaserine, (b) methotrexate, (c)

sulfon-amides, (d) allopurinol, and (e) 5-fluorouracil

5.Since dUTP is not a normal component of DNA, why do you

sup-pose ribonucleotide reductase has the capacity to convert UDP to

dUDP?

6.Describe the underlying rationale for the regulatory effects exerted

on ribonucleotide reductase by ATP, dATP, dTTP, and dGTP

7.(Integrates with Chapters 18–20 and 22.) By what pathway(s) does

the ribose released upon nucleotide degradation enter intermediary

metabolism and become converted to cellular energy? How many

ATP equivalents can be recovered from one equivalent of ribose?

8.(Integrates with Chapter 25.) At which steps does the purine

biosyn-thetic pathway resemble the pathway for biosynthesis of the amino

acid histidine?

9.Write reasonable chemical mechanisms for steps 6, 8, and 9 in

purine biosynthesis (see Figure 26.3)

10.Write a balanced equation for the conversion of aspartate to

fu-marate by the purine nucleoside cycle in skeletal muscle

11.Write a balanced equation for the oxidation of uric acid to glyoxylic

acid, CO2, and NH3, showing each step in the process and naming

all of the enzymes involved

12. (Integrates with Chapter 15.) E coli aspartate transcarbamoylase

(ATCase) displays classic allosteric behavior This 66 enzyme is activated by ATP and feedback-inhibited by CTP In analogy with the behavior of glycogen phosphorylase shown in Figure 15.14,

il-lustrate the allosteric v versus [aspartate] curves for ATCase (a) in

the absence of effectors, (b) in the presence of CTP, and (c) in the presence of ATP

*13. (Integrates with Chapter 15.) Unlike its allosteric counterpart glyco-gen phosphorylase (an 2enzyme), E coli ATCase has a heteromeric

(66) organization The -subunits bind aspartate and are

consid-ered catalytic subunits, whereas the -subunits bind CTP or ATP and

are considered regulatory subunits How would you describe the sub-unit organization of ATCase from a functional point of view?

14. (Integrates with Chapter 20.) Starting from HCO3 , glutamine, as-partate, and ribose-5-P, how many ATP equivalents are consumed in the synthesis of dTTP in a eukaryotic cell, assuming dihydroorotate oxidation is coupled to oxidative phosphorylation? How does this result compare with the ATP costs of purine nucleotide biosynthe-sis calculated in problem 2?

15. Write a balanced equation for the synthesis of dTMP from UMP and

N5,N10-methylene-THF Thymidylate synthase has four active-site arginine residues (Arg23, Arg178, Arg179, and Arg218) involved in substrate binding Postulate a role for the side chains of these Arg residues

16. Enzymes that bind phosphoribosyl-5-phosphate (PRPP) have a com-mon structural fold, the PRT fold, which unites them as a structural family PRT here refers to the phosphoribosyl transferase activity dis-played by some family members Typically, in such reactions, PPiis displaced from PRPP by a nitrogen-containing nucleophile Several such reactions occur in purine metabolism Identify two such reac-tions where the enzyme involved is likely to be a PRT family member

17. The crystal structure of E coli dihydrofolate reductase (DFR) with

NADPand folate bound can be found in the Protein Data Bank

thine to form IMP or guanine to form GMP; an absence of HGPRT is the

basis of Lesch-Nyhan syndrome

26.4 How Are Purines Degraded? Dietary nucleic acids are digested

to nucleotides by various nucleases and phosphodiesterases, the

nu-cleotides are converted to nucleosides by base-specific nucleotidases

and nonspecific phosphatases, and then nucleosides are hydrolyzed to

release the purine base Only the pentoses of nucleotides serve as

sources of metabolic energy In humans, the purine ring is oxidized to

uric acid by xanthine oxidase and excreted Gout occurs when bodily

fluids accumulate an excess of uric acid Skeletal muscle operates a

purine nucleoside cycle as an anaplerotic pathway

26.5 How Do Cells Synthesize Pyrimidines? In contrast to formation of

the purine ring system, the pyrimidine ring system is completed before a

ribose-5-P moiety is attached Only two precursors, carbamoyl-P and

as-partate, contribute atoms to the six-membered pyrimidine ring The first

step in humans is catalyzed by CPS-II ATCase then links carbamoyl-P with

aspartate Subsequent reactions close the ring and oxidize it before

adding ribose-5-P, using -PRPP as donor Decarboxylation gives UMP In

mammals, the six enzymatic activities of pyrimidine biosynthesis are

dis-tributed among only three proteins, two of which are multifunctional

polypeptides Purine and pyrimidine synthesis in mammals are two

prominent examples of metabolic channeling UMP leads to UTP, the

substrate for formation of CTP via CTP synthetase Regulation of

pyrimi-dine synthesis in animals occurs at CPS-II UDP and UTP are feedback

inhibitors, whereas PRPP and ATP are allosteric activators In bacteria,

regulation acts at ATCase through feedback inhibition by CTP (or UTP)

and activation by ATP

26.6 How Are Pyrimidines Degraded? Degradation of the pyrimi-dine ring generates -alanine, CO2, and ammonia In humans, pyrim-idines are recycled from nucleosides, but free pyrimidine bases are not salvaged

26.7 How Do Cells Form the Deoxyribonucleotides That Are Necessary for DNA Synthesis? 2-Deoxyribonucleotides are formed from ribonu-cleotides through reduction at the 2-position of the ribose ring in NDPs The reaction, catalyzed by ribonucleotide reductase, involves a free radi-cal mechanism that replaces the 2-OH by a hydride ion (H⬊) Thiore-doxin provides the reducing power for ribonucleotide reduction Class Ia ribonucleotide reductases have three different nucleotide-binding sites: the catalytic site (or active site), which binds substrates (ADP, CDP, GDP, and UDP); the substrate specificity site, which can bind ATP, dATP, dGTP,

or dTTP; and the overall activity site, which binds either the activator ATP

or the negative effector dATP The relative affinities of the three classes of nucleotide binding sites in ribonucleotide reductase for the various sub-strates, activators, and inhibitors are such that the various dNDPs are formed in amounts consistent with cellular needs

26.8 How Are Thymine Nucleotides Synthesized? Both dUDP and dCDP can lead to formation of dUMP, the immediate precursor for dTMP synthesis Formation of dTMP from dUMP is catalyzed by thymidylate syn-thase through reductive methylation of dUMP at the 5-position The

methyl donor is the one-carbon folic acid derivative N5,N10 -methylene-THF Fluoro-substituted pyrimidine analogs such as 5-fluorouracil (5-FU), 5-fluorocytosine, and 5-fluoroorotate can be converted to FdUMP, which inhibits thymidylate synthase These fluoro compounds have found a range of therapeutic uses in treating diseases from cancer to malaria

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838 Chapter 26 Synthesis and Degradation of Nucleotides

(www.rcsb.org/pdb) as file 7DFR Go to this website, enter “7DFR”

in the search line, and click on “KiNG” under “Display options”

when the 7DFR page comes up Explore the KiNG graphic of the

DFR structure to visualize how its substrates are bound (If you hold

down the left button on your mouse and move the cursor over the

image, you can rotate the structure to view it from different

per-spectives.) Note in particular the spatial relationship between the

nicotinamide ring of NADPand the pterin ring of folate Do you

now have a better appreciation for how this enzyme works? Note

also the location of polar groups on the two substrates in relation to

the DFR structure

18.E coli aspartate transcarbamoylase is an allosteric enzyme (see

problem 12) composed of six catalytic (C) subunits and six

regula-tory (R) subunits Protein Data Bank file 1RAA shows one-third of

the ATCase holoenzyme (two C subunits and two R subunits; CTP

molecules are bound to the R subunits) Explore this structure

us-ing the KiNG display option What secondary structural motif

dom-inates the R subunit structure? Protein Data Bank file 2IPO also

shows one-third of the ATCase holoenzyme (two C subunits and two R subunits), but in this structure molecules of the substrate

analog N-(2-phosphonoacetyl)-L-asparagine are bound to the C

subunits Explore this structure using the KiNG display option Note the distance separating the ATCase active site from its al-losteric site Interpret what you see in terms of the Monod– Wyman–Changeux model for allosteric regulation (see Chapter 15) Which of these structures corresponds to the MWC R-state, and which corresponds to the T-state?

Preparing for the MCAT Exam

19.Examine Figure 26.6 and predict the relative rates of the regulated reactions in the purine biosynthetic pathway from ribose-5-P to GMP and AMP under conditions in which GMP levels are very high

20.Decide from Figures 18.1, 25.31, 26.26, and the Deeper Look box

on page 817 which carbon atom(s) in glucose would be most likely

to end up as the 5-CH3carbon in dTMP

FURTHER READING

Purine Metabolism

Kisker, C., Schindelin, H., and Rees, D C., 1997 Molybdenum-containing

enzymes: Structure and mechanism Annual Review of Biochemistry

66:233–267

Mueller, E J., et al., 1994 N5-carboxyaminoimidazole ribonucleotide:

Evidence for a new intermediate and two new enzymatic activities in

the de novo purine biosynthetic pathway of Escherichia coli

Biochem-istry 33:2269–2278.

Watts, R W E., 1983 Some regulatory and integrative aspects of purine

nucleotide synthesis and its control: An overview Advances in Enzyme

Regulation 21:33–51.

Wilson, D K., Rudolph, F B., and Quiocho, F A., 1991 Atomic

struc-ture of adenosine deaminase complexed with a transition-state

analog: Understanding catalysis and immunodeficient mutations

Science 252:1279–1284.

Pyrimidine Metabolism

Connolly, G P., and Duley, J A., 1999 Uridine and its nucleotides:

Bio-logical actions, therapeutical potentials Trends in PhrmacoBio-logical

Sci-ences 20:218–225.

Graves, L M., et al., 2000 Regulation of carbamoyl phosphate

synthe-tase by MAP kinase Nature 403:328–331.

Jones, M E., 1980 Pyrimidine nucleotide biosynthesis in animals: Genes,

enzymes and regulation of UMP biosynthesis Annual Review of

Bio-chemistry 49:253–279.

Metabolic Disorders of Purine and Pyrimidine Metabolism

Löffler, M., et al., 2005 Pyrimidine pathways in health and disease

Trends in Molecular Medicine 11:430–437.

Nyhan, W L., 2005 Disorders of purine and pyrimidine metabolism

Molecular Genetics and Metabolism 86:25–33.

Scriver, C R., et al., 1995 The Metabolic Bases of Inherited Disease, 7th ed.

New York: McGraw-Hill

Metabolic Channeling

Benkovic, S J., 1984 The transformylase enzymes in de novo purine

biosynthesis Trends in Biochemical Sciences 9:320–322.

Henikoff, S., 1987 Multifunctional polypeptides for purine de novo

syn-thesis BioEssays 6:8–13.

Huang, X., Holden, H M., and Raushel, F M., 2001 Channeling of

sub-strates and intermediates in enzyme-catalyzed reactions Annual

Re-view of Biochemistry 70:149–180.

Srere, P A., 1987 complexes of sequential metabolic enzymes Annual

Review of Biochemistry 56:89–124.

Deoxyribonucleotide Biosynthesis

Carreras, C W., and Santi, D V., 1995 The catalytic mechanism and

struc-ture of thymidylate synthase Annual Review of Biochemistry 64:721–762.

Frey, P A., 2001 Radical mechanisms of enzymatic catalysis Annual

Re-view of Biochemistry 70:121–148.

Herrick, J., and Sciavi, B., 2007 Ribonucleotide reductase and the reg-ulation of DNA replication: An old story and an ancient heritage

Molecular Microbiology 63:22–34.

Jordan, A., and Reichard, P., 1998 Ribonucleotide reductases Annual

Review of Biochemistry 67:71–98.

Licht, S., Gerfen, G J., and Stubbe, J., 1996 Thiyl radicals in

ribonu-cleotide reductases Science 271:477–481.

Marsh, E N G., 1995 A radical approach to enzyme catalysis BioEssays

17:431–441

Reichard, P., 1988 Interactions between deoxyribonucleotide and DNA

synthesis Annual Review of Biochemistry 57:349–374.

Stubbe, J., Ge, J., and Yee, C S., 2001 The evolution of ribonucleotide

reduction revisited Trends in Biochemical Sciences 26:93–99.

Inhibitors of Purine, Pyrimidine, and Deoxyribonucleotide Biosynthesis as Therapeutic Agents

Abeles, R H., and Alston, T A., 1990 Enzyme inhibition by fluoro

com-pounds Journal of Biological Chemistry 265:16705–16708.

Galmarini, C M., Mackey, J R., and Dumontet, C., 2002 Nucleoside

analogues and nucleobases in cancer treatment Lancet Oncology

3:415–424

Hitchings, G H., 1992 Antagonists of nucleic acid derivatives as

medic-inal agents Annual Review of Pharmacology and Toxicology 32:1–9.

Park, B K., Kitteringham, N R., and O’Neill, P M., 2001 Metabolism of

fluorine-containing drugs Annual Review of Pharmacology and

Toxi-cology 41:443–470.

Zrenner, R., et al., 2006 Pyrimidine and purine biosynthesis and

degra-dation in plants Annual Review of Plant Biology 57:805–836.

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Copyright © 2008 W

and Organ Specialization

In the preceding chapters, we have explored the major metabolic pathways—

glycolysis, the citric acid cycle, electron transport and oxidative phosphorylation,

photosynthesis, gluconeogenesis, fatty acid oxidation, lipid biosynthesis, amino

acid metabolism, and nucleotide metabolism Several of these pathways are

cata-bolic and serve to generate chemical energy useful to the cell; others are anacata-bolic

and use this energy to drive the synthesis of essential biomolecules Despite their

opposing purposes, these reactions typically occur at the same time as nutrient

molecules are broken down to provide the building blocks and energy for ongoing

biosynthesis Cells maintain a dynamic steady state through processes that involve

considerable metabolic flux The metabolism that takes place in just a single cell is

so complex that it defies detailed quantitative description However, an

apprecia-tion of overall relaapprecia-tionships can be achieved by stepping back and considering

in-termediary metabolism at a systems level of organization.

27.1 Can Systems Analysis Simplify the Complexity

of Metabolism?

The metabolism of a typical heterotrophic cell can be portrayed by a schematic

diagram consisting of just three interconnected functional blocks: (1) catabolism,

(2) anabolism, and (3) macromolecular synthesis and growth (Figure 27.1).

1 Catabolism Energy-yielding nutrients are oxidized to CO2and H2O in

catabo-lism, and most of the electrons liberated are passed to oxygen via an

electron-transport pathway coupled to oxidative phosphorylation, resulting in the

forma-tion of ATP Some electrons go to reduce NADP to NADPH, the source of

reducing power for anabolism Glycolysis, the citric acid cycle, electron transport

and oxidative phosphorylation, and the pentose phosphate pathway are the

prin-cipal pathways within this block The metabolic intermediates in these pathways

also serve as substrates for processes within the anabolic block.

2 Anabolism The biosynthetic reactions that form the many cellular molecules

collectively comprise anabolism For thermodynamic reasons, the chemistry of

an-abolism is more complex than that of catan-abolism (that is, it takes more energy [and

often more steps] to synthesize a molecule than can be produced from its

degrada-tion) Metabolic intermediates derived from glycolysis and the citric acid cycle are

the precursors for this synthesis, with NADPH supplying the reducing power and

ATP the coupling energy.

3 Macromolecular Synthesis and Growth The organic molecules produced in

anabolism are the building blocks for creation of macromolecules Like anabolism,

The Washington, D.C., Metro map The coordinated flow of passengers along different transit lines is an apt metaphor for metabolic regulation

Study of an enzyme, a reaction, or a sequence can

be biologically relevant only if its position in the hierarchy of function is kept in mind

Daniel E Atkinson

Cellular Energy Metabolism and Its Regulation (1977)

KEY QUESTIONS

27.1 Can Systems Analysis Simplify the Complexity of Metabolism?

27.2 What Underlying Principle Relates ATP Coupling to the Thermodynamics of Metabolism?

27.3 Is There a Good Index of Cellular Energy Status?

27.4 How Is Overall Energy Balance Regulated

in Cells?

27.5 How Is Metabolism Integrated in

a Multicellular Organism?

27.6 What Regulates Our Eating Behavior?

27.7 Can You Really Live Longer by Eating Less?

ESSENTIAL QUESTIONS

Cells are systems in a dynamic steady state, maintained by a constant flux of

nutri-ents that serve as energy sources or as raw material for the maintenance of cellular

structures Catabolism and anabolism are ongoing, concomitant processes.

What principles underlie the integration of catabolism and energy production

with anabolism and energy consumption? How is metabolism integrated in

complex organisms with multiple organ systems?

Create your own study path for this chapter with tutorials, simulations, animations,

and Active Figures at www.cengage.com/login.

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840 Chapter 27 Metabolic Integration and Organ Specialization

macromolecular synthesis is driven by energy from ATP, although indirectly in some cases: GTP is the principal energy source for protein synthesis, CTP for phospholipid synthesis, and UTP for polysaccharide synthesis However, keep in mind that ATP is the principal phosphoryl donor for formation of GTP, CTP, and UTP from GDP, CDP, and UDP, respectively Macromolecules are the agents of biological function and information—proteins, nucleic acids, lipids that self-assemble into membranes, and

so on Growth can be represented as cellular accumulation of macromolecules and the partitioning of these materials of function and information into daughter cells in the process of cell division.

Only a Few Intermediates Interconnect the Major Metabolic Systems

Despite the complexity of processes taking place within each block, the connections between blocks involve only a limited number of substances Just ten or so kinds of catabolic intermediates from glycolysis, the pentose phosphate pathway, and the cit-ric acid cycle serve as the raw material for most of anabolism: four kinds of sugar phosphates (triose-P, tetrose-P, pentose-P, and hexose-P), three -keto acids

(pyru-vate, oxaloacetate, and -ketoglutarate), two coenzyme A derivatives (acetyl-CoA and

succinyl-CoA), and PEP (phosphoenolpyruvate)

ATP and NADPH Couple Anabolism and Catabolism

Metabolic intermediates are consumed by anabolic reactions and must be continu-ously replaced by catabolic processes In contrast, the energy-rich compounds ATP and NADPH are recycled rather than replaced When these substances are used in

Carbohydrates

CATABOLISM Fat

Protein

ANABOLISM

Triose-P Tetrose-P Pentose-P Hexose-P PEP Pyruvate Acetyl-CoA

-KG

Succinyl-CoA Oxaloacetate

Amino acids Nucleotides Fatty acids, etc

MACROMOLECULAR SYNTHESIS AND ACCUMULATION (GROWTH)

Proteins Nucleic acids Complex lipids

Membranes Organelles Cell walls, etc

+

FIXATION

h 

ATP

ADP

NTP

NDP NADP+

NADPH

ATP

ADP

H2O

H2O

O2

CO2

CO2

NADP+

NADPH

FIGURE 27.1 Block diagram of intermediary metabolism

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biosynthesis, the products are ADP and NADP, and ATP and NADPH are

regener-ated during catabolism ATP and NADPH are unique in that they are the only

com-pounds whose purpose is to couple the energy-yielding processes of catabolism to the

energy-consuming reactions of anabolism Certainly, other coupling agents serve

es-sential roles in metabolism For example, NADH and [FADH2] participate in the

transfer of electrons from substrates to O2during oxidative phosphorylation

How-ever, these reactions are solely catabolic, and the functions of NADH and [FADH2]

are fulfilled within the block called catabolism

Phototrophs Have an Additional Metabolic System—

The Photochemical Apparatus

The systems in Figure 27.1 reviewed thus far are representative only of metabolism as

it exists in aerobic heterotrophs The photosynthetic production of ATP and NADPH

in photoautotrophic organisms entails a fourth block, the photochemical system

(Fig-ure 27.1) This block consumes H2O and releases O2 When this fourth block operates,

energy production within the catabolic block can be largely eliminated Yet another

block, one to account for the fixation of carbon dioxide into carbohydrates, is also

re-quired for photoautotrophs The inputs to this fifth block are the products of the

pho-tochemical system (ATP and NADPH) and CO2derived from the environment The

carbohydrate products of this block may enter catabolism, but not primarily for energy

production In photoautotrophs, carbohydrates are fed into catabolism to generate

the metabolic intermediates needed to supply the block of anabolism Although these

diagrams are oversimplifications of the total metabolic processes in heterotrophic or

phototrophic cells, they are useful illustrations of functional relationships between the

major metabolic subdivisions This general pattern provides an overall perspective on

metabolism, making its purpose easier to understand.

27.2 What Underlying Principle Relates ATP Coupling

to the Thermodynamics of Metabolism?

Virtually every metabolic pathway either consumes or produces ATP The amount of

ATP involved—that is, the stoichiometry of ATP synthesis or hydrolysis—lies at the

heart of metabolic relationships The overall thermodynamic efficiency of any

meta-bolic sequence, be it catameta-bolic or anameta-bolic, is determined by ATP coupling In every

case, the overall reaction mediated by any metabolic pathway is energetically favorable because of

its particular ATP stoichiometry In the highly exergonic reactions of catabolism, much of

the energy released is captured in ATP synthesis In turn, the thermodynamically

un-favorable reactions of anabolism are driven by energy released upon ATP hydrolysis

To illustrate this principle, we must first consider the three types of

stoichi-ometries The first two are fixed by the laws of chemistry, but the third is unique to

living systems and reveals a fundamental difference between the inanimate world of

chemistry and physics and the world of biological function, as shaped by evolution—

that is, the world of living organisms The fundamental difference is the

stoichiome-try of ATP coupling.

1 Reaction Stoichiometry This is simple chemical stoichiometry—the number of

each kind of atom in any chemical reaction remains the same, and thus equal

num-bers must be present on both sides of the equation This requirement holds even

for a process as complex as cellular respiration:

C6H12O6 6 O2⎯⎯→ 6 CO2 6 H2O The six carbons in glucose appear as 6 CO2, the 12 H of glucose appear as the 12 H

in six molecules of water, and the 18 oxygens are distributed between CO2and H2O.

2 Obligate Coupling Stoichiometry Cellular respiration is an oxidation–reduction

process, and the oxidation of glucose is coupled to the reduction of NADand [FAD].

(Brackets here denote that the relevant FAD is covalently linked to succinate

dehy-Stoichiometry is the measurement of the

amounts of chemical elements and molecules involved in chemical reactions (from the Greek

stoicheion, meaning “element,” and metria,

mean-ing “measure”)

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842 Chapter 27 Metabolic Integration and Organ Specialization

drogenase; see Chapter 20) The NADH and [FADH2] thus formed are oxidized in the electron-transport pathway:

(a) C6H12O6 10 NADⴙ 2 [FAD]  6 H2O ⎯⎯→

6 CO2 10 NADH  10 H 2 [FADH2] (b) 10 NADH  10 Hⴙ 2 [FADH2]  6 O2⎯⎯→ 12 H2O  10 NADⴙ 2 [FAD] Sequence (a) accounts for the oxidation of glucose via glycolysis and the citric acid cycle Sequence (b) is the overall equation for electron transport per glucose The

stoichiometry of coupling by the biological ecarriers, NADand FAD, is fixed by the

chemistry of electron transfer; each of the coenzymes serves as an epair acceptor

Re-duction of each O atom takes an epair Metabolism must obey these facts of

chem-istry: Biological oxidation of glucose releases 12 epairs, creating a requirement for

12 equivalents of epair acceptors, which transfer the electrons to 12 O atoms By evo-lutionary chance, NAD/NADH and FAD/FADH2carry these electrons, but the stoi-chiometry is fixed by the chemistry.

3 Evolved Coupling Stoichiometries The participation of ATP is fundamentally different from the role played by pyridine nucleotides and flavins The stoichiome-try of adenine nucleotides in metabolic sequences is not fixed by chemical neces-sity Instead, the “stoichiometries” we observe are the consequences of evolutionary design The overall equation for cellular respiration,1 including the coupled for-mation of ATP by oxidative phosphorylation, is

C6H12O6 6 O2 38 ADP  38 Pi⎯⎯→ 6 CO2 38 ATP  44 H2O The “stoichiometry” of ATP formation, 38 ADP  38 Pi⎯ →38 ATP  38 H2O, can-not be predicted from any chemical considerations The value of 38 ATP is an end result of biological adaptation It is a trait that evolved through interactions between chemistry, heredity, and the environment over the course of evolution Like any evolved character, ATP stoichiometry is the result of compromise The final trait is one particularly suited to the fitness of the organism.

The number 38 is not magical Recall that in eukaryotes, the consensus value for the net yield of ATP per glucose is 30 to 32, not 38 (see Table 20.4) Also, the value

of 38 was established a long time ago in evolution, when the prevailing atmospheric conditions and the competitive situation were undoubtedly very different from those today The significance of this number is that it provides a high yield of ATP for each glucose molecule, yet the yield is still low enough that essentially all of the glucose is metabolized.

ATP Coupling Stoichiometry Determines the Keqfor Metabolic Sequences

The fundamental biological purpose of ATP as an energy-coupling agent is to drive thermodynamically unfavorable reactions In effect, the energy release accompa-nying ATP hydrolysis is transmitted to the unfavorable reaction so that the overall free energy change for the coupled process is negative (that is, favorable) The in-volvement of ATP serves to alter the free energy change for a reaction; or to put it another way, the role of ATP is to change the equilibrium ratio of [reactants] to [products] for a reaction (See the A Deeper Look box on page 67.)

Another way of viewing these relationships is to note that, at equilibrium, the concentrations of ADP and Piwill be vastly greater than that of ATP because G°

for ATP hydrolysis is a large negative number.2However, the cell where this reaction

1This overall equation for cellular respiration is for the reaction within an uncompartmentalized (prokaryotic) cell In eukaryotes, where much of the cellular respiration is compartmentalized within mitochondria, mitochondrial ADP/ATP exchange imposes a metabolic cost on the proton gradient

of 1 Hper ATP, so the overall yield of ATP per glucose is 32, not 38

2Since G°  30.5 kJ/mol, ln Keq  12.3 So Keq 2.2  105 Choosing starting conditions of [ATP] 8 mM, [ADP]  8 mM, and [Pi] 1 mM, we can assume that, at equilibrium, [ATP] has fallen to some insignificant value x, [ADP]  approximately 16 mM, and [Pi] approximately 9 mM The concentration of ATP at equilibrium, x, then calculates to be about 1 nM.

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