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In general, proteins whose folding is chaperone-dependent pass down a pathway in which Hsp70 acts first on the newly synthesized protein and then passes the partially folded intermediate

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O2N C C

OH

H

CH2OH

H

NH C CHCl2 O

Chloramphenicol

H3C

CH3 O

CHOH

CH2

N H

Cycloheximide

O

CH3

H3C HO

O

H3C HO

CH3

CH3

OH

CH3

O

O H

OCH3

CH3 H

CH3 H

HO

O

O H

N(CH3)2

CH3

H

H

O

Erythromycin

HO

CH3

H

CH3

H

HO

CH3

H

O

C OCH3 COOH

CH3

H3C

Fusidic acid

H

OH

NH2+

HN

C

NH2+

H2N

H HO

H O

O H

H3C

CHO H

OH O

H

O H

H

CH2OH

H3CNH

HO

Streptomycin

OH

H3C OH

N(CH3)2 OH

O C

NH2

Tetracycline

HO

N

N

N

H3C CH3

O

OH HN H

CH2

CH

NH3+

Puromycin

O

N

N

N

O

OH O H

CH2

CH

NH3+

Tyrosyl-tRNA

P O O

O H

CH3

FIGURE 30.31 The structures of various antibiotics that act as protein synthesis inhibitors Puromycin mimics

the structure of aminoacyl-tRNA in that it resembles the 3-terminus of a Tyr-tRNA (shaded box)

HO O

O

H2N

NH2

O

HO

HO

(a)

NH2

H3C

H3CNH

H3C

OH

O

1406 1408

1495 1493 1492

C G U C

C A C C

3

A A A

G C U G

G U G G

FIGURE 30.32 (a) Structure of geneticin, a

representa-tive aminoglycoside antibiotic Note the characteristic 2-deoxystreptamine (2-DOS) core structure, in red

(b) The base sequence of the small RNA loop within

the 16S rRNA decoding center Note that unpaired adenine residues 1408, 1492, and 1493 constitute the internal loop structure.(Adapted from Figure 1 in

Her-mann, T., 2005 Drugs targeting the ribosome Current Opinion

in Structural Biology 15:355–366.)

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984 Chapter 30 Protein Synthesis

The most common effect of antibiotics that interact with the PTC is to occupy space within this center, such that the amino acid or peptidyl chain linked at the 3-end of a tRNA cannot be positioned properly for the peptide-bond forming re-action This mode of inhibition is consistent with the catalytic role of PTC in pre-cisely orienting the substrates so that the peptide bond-forming reaction can occur This effect is more common for aminoacyl-tRNAs in the A site, although some drugs can bridge the A and P sites and affect both aminoacyl-tRNA and peptidyl-tRNA ori-entation Ribosomes with long peptidyl chains attached to the tRNA in the P site are less susceptible to macrolide antibiotics.

SUMMARY

30.1 What Is the Genetic Code? The genetic code is the code of bases

that specifies the sequence of amino acids in a protein The genetic code

is a triplet code Given the four RNA bases—A, C, G, and U—a total of

43 64 three-letter codons are available to specify the 20 amino acids

found in proteins Of these 64 codons, 61 are used for amino acids, and

the remaining 3 are nonsense, or “stop,” codons The genetic code is

unambiguous, degenerate, and universal

30.2 How Is an Amino Acid Matched with Its Proper tRNA? During

protein synthesis, aminoacyl-tRNAs recognize the codons through base

pairing using their anticodon loops A second genetic code exists, the

code by which each aminoacyl-tRNA synthetase adds its amino acid to

tRNAs that can interact with the codons that specify its amino acid A

common set of rules does not govern tRNA recognition by

aminoacyl-tRNA synthetases The aminoacyl-tRNA features recognized are not limited to the

anticodon and in some instances do not even include the anticodon

Usually, an aminoacyl-tRNA synthetase recognizes a set of sequence

ele-ments in its cognate tRNAs

30.3 What Are the Rules In Codon–Anticodon Pairing? Anticodons are

paired with codons in antiparallel orientation There are more codons

than there are amino acids, and considerable degeneracy exists in the

ge-netic code at the third base position The first two bases of the codon and

the last two bases of the anticodon form canonical Watson–Crick base

pairs, but pairing between the third base of the codon and the first base

of the anticodon follows less stringent rules, allowing some anticodons to

recognize more than one codon, in accordance with Crick’s wobble

hy-pothesis Some codons for a particular amino acid are used more than

the others Nonsense suppression occurs when suppressor tRNAs read

nonsense codons

30.4 What Is the Structure of Ribosomes, and How Are They

Assem-bled? Ribosomes are ribonucleoprotein particles that act as

mechano-chemical systems in protein synthesis They move along mRNA

tem-plates, orchestrating the interactions between successive codons and the

corresponding anticodons presented by aminoacyl-tRNAs Ribosomes

catalyze the formation of peptide bonds Prokaryotic ribosomes consist

of two subunits, 30S and 50S, which are composed of 50 different

pro-teins and 3 rRNAs—16S, 23S, and 5S The general shapes of the

riboso-mal subunits are determined by their rRNA molecules; ribosoriboso-mal

pro-teins serve a largely structural role in ribosomes Ribosomes sponta-neously self-assemble in vitro The 30S subunit provides the decoding center that matches up the tRNA anticodons with the mRNA codons The 50S subunit has the peptidyl transferase center that catalyzes pep-tide bond formation This center consists solely of 23S rRNA; the ribo-some is a ribozyme Eukaryotic cytosolic riboribo-somes are larger than prokaryotic ribosomes

30.5 What Are the Mechanics of mRNA Translation? Ribosomes move along the mRNA in the 5→3 direction, recruiting aminoacyl-tRNAs whose anticodons match up with successive codons and joining amino acids in peptide bonds in a polymerization process that forms a particular protein Protein synthesis proceeds in three distinct phases: initiation, elongation, and termination Elongation involves two steps: peptide bond formation and translocation of the ribosome one codon further along the mRNA At each stage, energy is provided by GTP hydrolysis, and specific soluble protein factors participate Many of these soluble proteins are G-protein family members Initiation involves binding of mRNA by the small ribosomal subunit, followed by binding of f Met-tRNAif Metthat rec-ognizes the first codon Elongation is accomplished via a repetitive cycle in which successive aminoacyl-tRNAs add to the ribosome⬊mRNA complex

as directed by codon binding, the 50S subunit catalyzes peptide bond for-mation, and the polypeptide chain grows by one amino acid at a time Ribosomes have three tRNA-binding sites: the A site, where incoming aminoacyl-tRNAs bind; the P site, where the growing peptidyl-tRNA chain

is bound; and the E site, where deacylated tRNAs exit the ribosome Ter-mination occurs when the ribosome encounters a stop codon in the mRNA Polysomes are the active structures in protein synthesis

30.6 How Are Proteins Synthesized in Eukaryotic Cells? The process

of protein synthesis in eukaryotes strongly resembles that in prokary-otes, but the events are more complicated Eukaryotic mRNAs have 5-terminal7methyl G caps and 3-polyadenylylated tails Initiation of eu-karyotic protein synthesis involves three stages and multiple proteins This complexity offers many opportunities for regulation, and eukary-otic cells employ a variety of mechanisms for post-transcriptional regu-lation of gene expression Many antibiotics are specific inhibitors of prokaryotic protein synthesis, making them particularly useful for the treatment of bacterial infections and diseases

PROBLEMS

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

chapter at www.cengage.com/login

1. (Integrates with Chapter 12.) The following sequence represents

part of the nucleotide sequence of a cloned cDNA:

CAATACGAAGCAATCCCGCGACTAGACCTTAAC

Can you reach an unambiguous conclusion from these data about

the partial amino acid sequence of the protein encoded by this

cDNA?

2.A random (AG) copolymer was synthesized using a mixture of 5 parts adenine nucleotide to 1 part guanine nucleotide as substrate If this random copolymer is used as an mRNA in a cell-free protein synthe-sis system, which amino acids will be incorporated into the polypep-tide product? What will be the relative abundances of these amino acids in the product?

3.Review the evidence establishing that aminoacyl-tRNA synthetases bridge the information gap between amino acids and codons Indi-cate the various levels of specificity possessed by aminoacyl-tRNA

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synthetases that are essential for high-fidelity translation of

messen-ger RNA molecules

4.(Integrates with Chapter 11.) Draw base-pair structures for (a) a

G⬊C base pair, (b) a C⬊G base pair, (c) a G⬊U base pair, and (d) a

U⬊G base pair Note how these various base pairs differ in the

po-tential hydrogen-bonding patterns they present within the major

groove and minor groove of a double-helical nucleic acid

5.Point out why Crick’s wobble hypothesis would allow fewer than

61 anticodons to be used to translate the 61 sense codons How

might “wobble” tend to accelerate the rate of translation?

6.How many codons can mutate to become nonsense codons through

a single base change? Which amino acids do they encode?

7.Nonsense suppression occurs when a suppressor mutant arises that

reads a nonsense codon and inserts an amino acid, as if the nonsense

codon were actually a sense codon Which amino acids do you think

are most likely to be incorporated by nonsense suppressor mutants?

8.Why do you suppose eukaryotic protein synthesis is only 10% as fast

as prokaryotic protein synthesis?

9.If the tunnel through the large ribosomal subunit is 10 nm long, how

many amino acid residues might be contained within it? (Assume

that the growing polypeptide chain is in an extended -sheet–like

conformation.)

10.Eukaryotic ribosomes are larger and more complex than

prokary-otic ribosomes What advantages and disadvantages might this

greater ribosomal complexity bring to a eukaryotic cell?

11.What ideas can you suggest to explain why ribosomes invariably exist

as two-subunit structures, instead of a larger, single-subunit entity?

12.How do prokaryotic cells determine whether a particular

methionyl-tRNAMetis intended to initiate protein synthesis or to deliver a Met

residue for internal incorporation into a polypeptide chain? How do

the Met codons for these two different purposes differ? How do

eu-karyotic cells handle these problems?

13.What is the Shine–Dalgarno sequence? What does it do? The

effi-ciency of protein synthesis initiation may vary by as much as 100-fold

for different mRNAs How might the Shine–Dalgarno sequence be

responsible for this difference?

14.In the protein synthesis elongation events described under the section

on translocation, which of the following seems the most apt account

of the peptidyl transfer reaction: (a) The peptidyl-tRNA delivers its

peptide chain to the newly arrived aminoacyl-tRNA situated in the A

site, or (b) the aminoacyl end of the aminoacyl-tRNA moves toward

the P site to accept the peptidyl chain? Which of these two scenarios

makes more sense to you? Why?

15. (Integrates with Chapter 15.) Why might you suspect that the elon-gation factors EF-Tu and EF-Ts are evolutionarily related to the

G proteins of membrane signal transduction pathways described in Chapter 15?

16. How many ATP equivalents are consumed for each amino acid added to an elongating polypeptide chain during the process of protein synthesis?

17. Go to www.pdb.org and bring up PDB file 1GIX, which shows the 30S

ribosomal subunit, the three tRNAs, and mRNA In the box on the right titled “Images and Visualization,” click “All Images,” and then scroll down to look at the Interactive View By moving your cursor over the image, you can rotate it to view it from any perspective

a How are the ribosomal proteins represented in the image?

b How is the 16S rRNA portrayed?

c Rotate the image to see how the tRNAs stick out from the struc-ture Which end of the tRNA is sticking out?

d Where will these ends of the tRNAs lie when the 50S subunit binds

to this complex?

18. Go back to www.pdb.org and bring up PDB file 1FFK, which shows

the 50S ribosomal subunit In the box titled “Images and Visualiza-tion,” click “All Images.” Scroll down to look at the Interactive View Right-click the image to discover more information and tools

a How many atoms are represented in this structure?

b Are the bases of the nucleotides visible anywhere in the structure?

c Can you find double helical regions of RNA?

d Right-click and, under “Select,” select all proteins Right-click again and select “Render,” then “Scheme,” and then “CPK Space-fill” to highlight the ribosomal proteins Go back and cancel the protein selection Then select “Nucleic,” and render nucleic acid

in “CPK Spacefill.” Which macromolecular species seems to pre-dominate the structure?

Preparing for the MCAT Exam

19. Review the list of Shine–Dalgarno sequences in Figure 30.18 and se-lect the one that will interact best with the 3-end of E coli 16S rRNA

20. Chloramphenicol (Figure 30.31) inhibits the peptidyl transferase ac-tivity of the 50S ribosomal subunit The 50S peptidyl transferase active site consists solely of functionalities provided by the 23S rRNA What sorts of interactions do you think take place when chloramphenicol binds to the peptidyl transferase center? Which groups on chloram-phenicol might be involved in these interactions?

FURTHER READING

General

Cech, T R., Atkins, J F., and Gesteland, R F., 2005 The RNA World, 3rd

ed Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press

Lewin, B., 2008 Genes IX Sudbury, MA: Jones and Bartlett.

The Genetic Code

Cedergren, R., and Miramontes, P., 1996 The puzzling origin of the

ge-netic code Trends in Biochemical Sciences 21:199–200.

Huttenhofer, A., and Bock, A., 1998 RNA structures involved in

seleno-protein synthesis In RNA Structure and Function, Simons, R W., and

Grunberg-Monago, M., eds., pp 603–639 Cold Spring Harbor, NY:

Cold Spring Harbor Laboratory Press

Khorana, H G., et al., 1966 Polynucleotide synthesis and the genetic

code Cold Spring Harbor Symposium on Quantitative Biology 31:39–49.

The use of synthetic polyribonucleotides in elucidating the genetic

code

Knight, R D., et al., 1999 Selection, history, and chemistry: Three faces

of the genetic code Trends in Biochemical Sciences 24:241–247.

Nirenberg, M W., and Leder, P., 1964 RNA codewords and protein

syn-thesis Science 145:1399–1407.

Nirenberg, M W., and Matthaei, J H., 1961 The dependence of

cell-free protein synthesis in E coli upon naturally occurring or synthetic polyribonucleotides Proceedings of the National Academy of Sciences

U.S.A 47:1588–1602.

Wang, L., Xie, J., and Schultz, P G., 2006 Expanding the genetic code

Annual Review of Biophysics and Biomolecular Structure 35:225–249.

Aminoacylation of tRNAs and the Second Genetic Code

Arnez, J G., and Moras, D., 1997 Structural and functional

considera-tions of the aminoacylation reaction Trends in Biochemical Sciences

22:211–216

Carter, C W., Jr., 1993 Cognition, mechanism, and evolutionary

rela-tionships in aminoacyl-tRNA synthetases Annual Review of

Biochem-istry 62:715–748.

Hale, S P., et al., 1997 Discrete determinants in transfer RNA for

edit-ing and aminoacylation Science 276:1250–1252.

Ibba, M., Curnow, A W., and Söll, D., 1997 Aminoacyl-tRNA synthesis:

Divergent routes to a common goal Trends in Biochemical Sciences

22:39–42

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986 Chapter 30 Protein Synthesis

Normanly, J., and Abelson, J., 1989 tRNA identity Annual Review of

Bio-chemistry 58:1029–1049 Review of the structural features of tRNA

that are recognized by aminoacyl-tRNA synthetases

Park, S G., Ewalt, K L., and Kim, S 2005 Function expansion of

aminoacyl-tRNA synthetases and their interacting factors: New

per-spectives on housekeepers Trends in Biochemical Sciences 30:569–574.

Perona, J J., and Hou, Y M., 2007 Indirect readout of tRNA for

amino-acylation Biochemistry 46:10419–10432.

Schimmel, P., and Schmidt, E., 1995 Making connections:

RNA-depen-dent amino acid recognition Trends in Biochemical Sciences 20:1–2.

Sheppard, K., Yuan, J., Hohn, M J., Jester B., Devine K M., and Söll, D.,

2008 From one amino acid to another: tRNA-dependent amino

acid biosynthesis Nucleic Acids Research 36:1813–1825.

Codon–Anticodon Recognition

Crick, F H C., 1966 Codon–anticodon pairing: The wobble hypothesis

Journal of Molecular Biology 19:548–555 Crick’s original paper on

wobble interactions between tRNAs and mRNA

Crick, F H C., et al., 1961 General nature of the genetic code for

pro-teins Nature 192:1227–1232 An insightful paper on insertion/

deletion mutants providing convincing genetic arguments that the

genetic code was a triplet code, read continuously from a fixed

start-ing point This genetic study foresaw the nature of the genetic code,

as later substantiated by biochemical results

Ribosome Structure and Function

Ban, N., et al., 2000 The complete atomic structure of the large

riboso-mal subunit at 2.4 Å resolution Science 289:905–920.

Carter, A P., et al., 2000 Functional insights from the structure of the

30S ribosomal subunit and its interactions with antibiotics Nature

407:340–348

Cate, J H., et al., 1999 X-ray crystal structure of 70S functional

riboso-mal complexes Science 285:2095–2104.

Kaminishi, T., Wilson, D N., Takemoto, C., Harms, J M., et al., 2007 A

snapshot of the 30S ribosomal subunit capturing mRNA via the

Shine-Dalgarno interaction Structure 15:289–297.

Korostelev, A., and Noller, H F., 2007 The ribosome in focus: New

struc-tures bring new insights Trends in Biochemical Sciences 32:434–441.

Moore, P B., and Steitz, T A., 2002 The involvement of RNA in

ribo-some function Nature 418:229–235.

Ogle, J M., Carter, A P., and Ramakrishnan, V., 2003 Insights into the

decoding mechanism from recent ribosome structures Trends in

Biochemical Sciences 28:259–266.

Ramakrishnan, V., 2002 Ribosome structure and the mechanism of

translation Cell 108:557–572.

Spahn, C M T., et al., 2001 Structure of the 80S ribosome from

Sac-charomyces cerevisiae –tRNA-ribosome and subunit–subunit

interac-tions Cell 107:373–386.

Stark, H., et al., 2002 Ribosome interactions of aminoacyl-tRNA and

elongation factor Tu in the codon-recognition complex Nature

Structural Biology 9:849–854.

Tenson, T., and Ehrenberg, M., 2002 Regulatory nascent peptides in

the ribosomal tunnel Cell 108:591–594.

Valle, M., et al., 2002 Locking and unlocking of ribosomal motions Cell

114:123–134

The Ribosome Is a Ribozyme

Cech, T R., 2000 The ribosome is a ribozyme Science 289:878–879.

Green, R., Samaha, R R., and Noller, H F., 1997 Mutations at

nu-cleotides G2251 and U2585 of 23 S rRNA perturb the peptidyl

trans-ferase center of the ribosome Journal of Molecular Biology 266:40–50.

Green, R., Switzer, C., and Noller, H F., 1998 Ribosome-catalyzed

peptide-bond formation with an A-site substrate covalently linked to

23S ribosomal RNA Science 280:286–289.

Protein Synthesis: Initiation, Elongation, and Termination Factors

Allen, G S., Zavialov, A., Gursky, R., Ehrenberg, M., and Frank, J., 2005

The cryo-EM structure of a translation initiation complex from

Escherichia coli Cell 121:703–712.

Beringer, M., 2008 Modulating the activity of the peptidyl transferase

center of the ribosome RNA 14:795–801.

Beringer, M., and Rodnina, M V., 2007 The ribosomal peptidyl

trans-ferase Molecular Cell 26:311–321.

Bieling, P., Beringer, M., Adio, S., and Rodnina, M V., 2006 Peptide bond formation does not involve acid–base catalysis by ribosomal

residues Nature Structural and Molecular Biology 13:423–428.

Clark, B F C., and Nyborg, J., 1997 The ternary complex of EF-Tu and

its role in protein synthesis Current Opinion in Structural Biology

7:110–116

Clark, B F C., et al., eds., 1996 Prokaryotic and eukaryotic translation

factors Biochimie 78:1119–1122.

Dever, T E., 1999 Translation initiation: Adept at adapting Trends in

Biochemical Sciences 24:398–403.

Ehrenberg, M., and Tenson, T., 2002 A new beginning to the end of

translation Nature Structural Biology 9:85–87.

Nissen, P., et al., 1995 Crystal structure of the ternary complex of Phe-tRNAPhe, Ef-Tu, and a GTP analog Science 270:1464–1472.

Ogle, J M., and Ramakrishnan, R., 2005 Structural insights into

trans-lational fidelity Annual Review of Biochemistry 74:129–177.

Poole, E S., Askarian-Amiri, M E., Major, L L., McCaughan, K K., et al., 2003 Molecular mimicry in the decoding of translational stop

signals Progress in Nucleic Acids Research and Molecular Biology 74:

83–121

Voss, N R., Gerstein, M., Steitz, T A., and Moore, P B., 2006 The

geometry of the ribosomal polypeptide exit tunnel Journal of

Molec-ular Biology 360:893–906.

Zavialov, A V., and Ehrenberg, M., 2003 Peptidyl-tRNA regulates the

GTPase activity of translation factors Cell 114:113–122.

Eukaryotic Protein Synthesis

Gingras, A-C., et al., 1999 eIF-4 initiation factors: Effectors of mRNA

re-cruitment to ribosomes and regulators of translation Annual Review

of Biochemistry 68:913–963.

Hinnebush, A G., 2006 eIF3: A versatile scaffold for translation

initia-tion complexes Trends in Biochemical Sciences 31:553–562.

Matsuo, H., et al 1997 Structure of translation factor eIF4E bound to

7mGDP and interaction with 4E-binding protein Nature Structural

Biology 4:717–724.

Pain, V M., 1996 Initiation of protein synthesis in eukaryotic cells

Eu-ropean Journal of Biochemistry 236:747–771.

Rhoads, R E., 1999 Signal transduction pathways that regulate

eukary-otic protein synthesis Journal of Biological Chemistry 274:30337–30340.

Rhoads, R., Dinkova, T D., and Komeeva, N L., 2006 Mechanism and

regulation of translation in C elegans WormBook 28:1–18.

Sachs, A B., and Varani, G., 2000 Eukaryotic translation initiation:

There are two sides (at least) to every story Nature Structural Biology

7:356–361

Samuel, C E., 1993 The eIF-2a protein kinases, regulators of

transla-tion in eukaryotes from yeast to humans Journal of Biological

Chem-istry 268:7603–7606.

Tarun, S Z., Jr., et al., 1997 Translation factor eIF4G mediates in vitro

poly(A) tail dependent translation Proceedings of the National

Acad-emy of Sciences U.S.A 94:9046–9051.

Protein Synthesis Inhibitors

Endo, Y., et al., 1987 The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes The site and the characteristics of

the modification in 28S ribosomal RNA caused by the toxins

Jour-nal of Biological Chemistry 262:5908–5912.

Hermann, T., 2005 Drugs targeting the ribosome Current Opinion in

Structural Biology 15:355–366.

Polacek, N., and Mankin, A S., 2005 The ribosomal peptidyl

trans-ferase center: Structure, function, evolution, inhibition Critical

Re-views in Biochemistry and Molecular Biology 40:285–311.

Schlünzen, F., et al., 2000 Structural basis for the interaction of

antibi-otics with the peptidyl transferase center in eubacteria Nature 413:

814–821

Yonath, A., 2005 Antibiotics targeting ribosomes: Resistance, selectivity,

synergism, and cellular regulation Annual Review of Biochemistry 74:

649–679

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Gabriel V

Cycle: Folding, Processing, and Degradation

The human genome apparently contains about 20,500 genes, but some estimates

suggest that the total number of proteins in the human proteome may approach

1 million What processes introduce such dramatically increased variation into the

products of protein-encoding genes? We’ve reviewed (or will soon cover) many of

these processes; a partial list (with examples) includes:

1 Gene rearrangements (immunoglobulin G)

2 Alternative splicing (fast skeletal muscle troponin T)

3 RNA editing (apolipoprotein B)

4 Proteolytic processing (chymotrypsinogen or prepro-opiomelanocortin; see

Chapter 32)

5 Isozymes (lactate dehydrogenase)

6 Protein sharing (the glycolytic enzyme enolase is identical to -crystallin in the eye)

7 Protein–protein interactions at many levels (oligomerization, supramolecular

complexes, assembly of signaling pathway protein complexes upon scaffold

proteins)

8 Covalent modifications of many kinds (phosphorylation or glycosylation, with

multisite phosphorylation or variable degrees of glycosylation, to name just two

of the dozens of possibilities)

Thus, the nascent polypeptide emerging from a ribosome is not yet the agent

of biological function that is its destiny First, the polypeptide must fold into its

na-tive tertiary structure Even then, seldom is the nascent, folded protein in its final

functional state Proteins often undergo various proteolytic processing reactions

and covalent modifications as steps in their maturation to functional molecules.

Finally, at the end of their usefulness, damaged by chemical reactions or

dena-tured due to partial unfolding, they are degraded In addition, some proteins are

targeted for early destruction as part of regulatory programs that carefully control

available amounts of particular proteins Damaged or misfolded proteins are a

se-rious hazard; accumulation of protein aggregates can be a cause of human

dis-ease, including the prion diseases (see Chapter 28) and diseases of amyloid

accu-mulation, such as Alzheimer’s, Parkinson’s, or Huntington’s disease.

31.1 How Do Newly Synthesized Proteins Fold?

As Christian Anfinsen pointed out 40 years ago, the information for folding each

pro-tein into its unique three-dimensional architecture resides within its amino acid

sequence or primary structure (see Chapter 6) Proteins begin to fold even before

their synthesis by ribosomes is completed (Figure 31.1a) However, the cytosolic

envi-ronment is a very crowded place, with effective protein concentrations as high as

0.3 grams/mL Macromolecular crowding enhances the likelihood of nonspecific

pro-tein association and aggregation The primary driving force for propro-tein folding is the

burial of hydrophobic side chains away from the aqueous solvent and reduction in

Vong’s Flying Crane Origami—the Asian art of paper

folding—arose in China almost 2000 years ago when paper was rare and expensive and the folded shape added special meaning Protein folding, like origami, takes a functionless form and creates a structure with unique identity and purpose

Life is a process of becoming, a combination of states we have to go through.

Anais Nin (1903–1977)

KEY QUESTIONS

31.1 How Do Newly Synthesized Proteins Fold?

31.2 How Are Proteins Processed Following Translation?

31.3 How Do Proteins Find Their Proper Place

in the Cell?

31.4 How Does Protein Degradation Regulate Cellular Levels of Specific Proteins?

ESSENTIAL QUESTION

Proteins are the agents of biological function Protein turnover (synthesis and decay)

is a fundamental aspect of each protein’s natural history.

How are newly synthesized polypeptide chains transformed into mature, active

proteins, and how are undesired proteins removed from cells?

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

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

Nascent means “undergoing the process of

being born” or, in the molecular sense,“newly synthesized.”

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988 Chapter 31 Completing the Protein Life Cycle: Folding, Processing, and Degradation

solvent-accessible surface area (see Chapter 6) The folded protein typically has a buried hydrophobic core and a hydrophilic surface Protein aggregation is typically driven by hydrophobic interactions, so burial of hydrophobic regions through fold-ing is a crucial factor in preventfold-ing aggregation To evade such problems, nascent

pro-teins are often assisted in folding by a family of helper propro-teins known as molecular

chaperones (see Chapter 6), because, like the chaperones at a prom, their purpose is

to prevent inappropriate liaisons Chaperones also serve to shepherd proteins to their ultimate cellular destinations Also, mature proteins that have become partially un-folded may be rescued by chaperone-assisted refolding.

Chaperones Help Some Proteins Fold

A number of chaperone systems are found in all cells Many of the proteins in these

systems are designated by the acronym Hsp (for heat shock protein) and a number

indicating their relative mass in kilodaltons (as in Hsp60) Hsps were originally observed as abundant proteins in cells given brief exposure to high temperature

(42° C or so) The principal Hsp chaperones are Hsp70, Hsp60 (the chaperonins), and Hsp90 In general, proteins whose folding is chaperone-dependent pass down

a pathway in which Hsp70 acts first on the newly synthesized protein and then passes the partially folded intermediate to a chaperonin for completion of folding Nascent polypeptide chains exiting the large ribosomal subunits are met by

ribosome-associated chaperones (TF, or trigger factor, in Escherichia coli; NAC

HUMAN BIOCHEMISTRY

Alzheimer’s, Parkinson’s, and Huntington’s Disease Are Late-Onset

Neurodegenerative Disorders Caused by the Accumulation of Protein Deposits

As noted in Chapter 6, protein misfolding problems can cause

dis-ease by a variety of mechanisms For example, protein aggregates

can impair cell function Amyloid plaques (so named because they

resemble the intracellular starch, or amyloid, deposits found in plant

cells) and neurofibrillary tangles (NFTs) are proteinaceous deposits

found in the brains of individuals suffering from any of several

neu-rogenerative diseases In each case, the protein is different In

Alzheimer’s, disease is caused both by extracellular amyloid deposits

composed of proteolytic fragments of the amyloid precursor protein

(APP) termed amyloid-␤ (A␤) and intracellular NFTs composed of

the microtubule-binding protein tau (␶) A is a peptide 39 to

43 amino acids long that polymerizes to form long, highly ordered,

insoluble fibrils consisting of a hydrogen-bonded parallel -sheet

structure in which identical residues on adjacent chains are aligned

directly, in register (see accompanying figure) Why A aggregates

in some people but not others is not clear In Parkinson’s, the culprit

is NFTs composed of polymeric ; no amyloid plaques are evident In

Huntington’s disease, the protein deposits occur as nuclear

inclu-sions composed of polyglutamine (polyQ) aggregates PolyQ

aggre-gates arise from mutant forms of huntingtin, a protein that

charac-teristically has a stretch of glutamine residues close to its N-terminus

Huntingtin is a 3144-residue protein encoded by the ITI5 gene,

which has 67 exons Exon 1 encodes the polyglutamine region

In-dividuals whose huntingtin gene has fewer that 35 CAG (glutamine

codon) repeats never develop the disease; those with 40 or more

al-ways develop the disease within a normal lifetime The nuclear

in-clusions in Huntington’s disease are huntingtin-derived

polygluta-mine fragments that have aggregated to form -sheet–containing

amyloid fibrils

Impairment of cellular function by proteinaceous deposits

may be a general phenomenon In vitro experiments have

demonstrated that aggregates of proteins not associated with

dis-ease can be cytotoxic, and the ability to form amyloid deposits is

a general property of proteins The evolution of chaperones to assist protein folding and proteasomes to destroy improperly folded proteins may have been driven by the necessity to prevent protein aggregation

12

Fibril axis

24

30 40

䊱 A model for the A1–40structural unit in -amyloid fibrils Fibrils

con-tain-strands perpendicular to the fibril axis, with interstrand hydrogen

bonding parallel to the fiber axis The top face of the -sheet is

hydro-phobic and presumably interacts with neighboring A molecules in fibril

formation.(Figure adapted from Figure 1 in Thompson, L K., 2003 Unraveling the secrets of Alzheimer’s -amyloid fibrils Proceedings of the National Academy of

Sciences, U.S.A 100:383–385.)

Trang 7

[nascent chain-associated complex] in eukaryotes) In E coli, the 50S ribosomal

pro-tein L23, which is situated at the peptide exit tunnel, serves as the docking site for

TF, directly linking protein synthesis with chaperone-assisted protein folding TF

and NAC mediate transfer of the emerging nascent polypeptide chain to the Hsp70

class of chaperones, although many proteins do not require this step for proper

folding.

Hsp70 Chaperones Bind to Hydrophobic Regions of Extended

Polypeptides

In Hsp70-assisted folding, proteins of the Hsp70 class bind to nascent polypeptide

chains while they are still on ribosomes (Figure 31.1b) Hsp70 (known as DnaK in

E coli ) recognizes exposed, extended regions of polypeptides that are rich in

hydro-phobic residues By interacting with these regions, Hsp70 prevents nonproductive

associations and keeps the polypeptide in an unfolded (or partially folded) state

until productive folding interactions can occur Completion of folding requires

re-lease of the protein from Hsp70; rere-lease is energy-dependent and is driven by ATP

hydrolysis.

Hsp70 proteins such as DnaK consist of two domains: a 44-kD N-terminal

ATP-binding domain and an 18-kD central domain that binds polypeptides with exposed

hydrophobic regions (Figure 31.2a) The DnaK⬊ATP complex receives an unfolded

(or partially folded) polypeptide chain from DnaJ (Figure 31.2b) DnaJ is an Hsp40

family member Interaction of DnaK with DnaJ triggers the ATPase activity of DnaK;

the DnaK⬊ADP complex forms a stable complex with the unfolded polypeptide,

pre-venting its aggregation with other proteins A third protein, GrpE, catalyzes

nucleo-tide exchange on DnaK, replacing ADP with ATP, which converts DnaK back to a

conformational form having low affinity for its polypeptide substrate Release of the

polypeptide gives it the opportunity to fold Multiple cycles of interaction with DnaK

(or Hsp70) give rise to partially folded intermediates or, in some cases, completely

folded proteins The partially folded intermediates may be passed along to the

Hsp60/chaperonin system for completion of folding (Figure 31.1c).

GroEL

GroES Hsp70

FIGURE 31.1 Protein folding pathways (a)

Chaperone-independent folding.The protein folds as it is synthesized

on the ribosome (green) (or shortly thereafter) (b)

Hsp70-assisted protein folding Hsp70 (gray) binds to nascent

polypeptide chains as they are synthesized and assists

their folding (c) Folding assisted by Hsp70 and

chaper-onin complexes.The chaperchaper-onin complex in E coli is

GroES–GroEL.The majority of proteins fold by pathways (a) or (b).(Adapted from Figure 2 in Netzer, W J., and Hartl, F U.,

1998 Protein folding in the cytosol: Chaperonin-dependent and

-independent mechanisms Trends in Biochemical Sciences 23:

68–73; and Figure 2 in Hartl, F U., and Hayer-Hartl, M., 2002 Molec-ular chaperones in the cytosol: From nascent chain to folded

pro-tein, Science 295:1852–1858.)

ATPase domain

N

N C

C

C D

A

L1,2

L3,4 L4,5

L5,6 6 5 1

7 8 4

3

Peptide-binding domain

Domain organization and structure of the Hsp70 family

member, DnaK

(a)

ATP

J

J J

ATP

ADP

I N

GroEL

DnaJ

DnaK

DnaJ-U

U, I

ADP, DnaJ

GrpE

Pi

DnaK mechanism of action

(b)

FIGURE 31.2 Structure and function of DnaK: (a) Domain organization and structure of the Hsp70 family

mem-ber, DnaK The ribbon diagram on the lower left is the ATP-binding domain of the DnaK analog, bovine Hsc70;

bound ADP is shown as a stick diagram (purple) The ribbon diagram on the lower right is the

polypeptide-binding domain of DnaK The small blue ovals highlight the position of the polypeptide substrate; the protein

regions that bind the polypeptide substrate are blue-green (b) DnaK mechanism of action: DnaJ binds an

un-folded protein (U) or partially un-folded intermediate (I) and delivers it to the DnaK⬊ATP complex.The nucleotide

exchange protein GrpE replaces ADP with ATP on DnaK and the partially folded intermediate ([I]) is released

I has several possible fates: It may fold into the native state, N; it may undergo another cycle of interaction with

DnaJ and DnaK; or it may be become a substrate for folding by the GroEL chaperonin system.(Adapted from

Figures 1a and 2a in Frydman, J., 2001 Folding of newly translated proteins in vivo: The role of molecular chaperones Annual

Review of Biochemistry 70:603–647.)

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990 Chapter 31 Completing the Protein Life Cycle: Folding, Processing, and Degradation

The GroES–GroEL Complex of E coli Is an Hsp60 Chaperonin

The Hsp60 class of chaperones, also known as chaperonins, assists some partially

folded proteins to complete folding after their release from ribosomes Chaperonins sequester partially folded molecules from one another (and from extraneous inter-actions), allowing folding to proceed in a protected environment This protected

environment is sometimes referred to as an “Anfinsen cage” because it provides an

enclosed space where proteins fold spontaneously, free from the possibility of aggre-gation with other proteins Chaperonins are large, cylindrical protein complexes formed from two stacked rings of subunits The chaperonins have been organized into two groups, I and II, on the basis of their source and structure Group I chaper-onins are found in bacteria, group II in archaea and eukaryotes The group I

chap-eronin in E coli is the GroES–GroEL complex (Figure 31.1c) GroEL is made of two

stacked seven-membered rings of 60-kD subunits that form a cylindrical 14oligomer

15 nm high and 14 nm wide (Figure 31.3) Each GroEL ring has a 5-nm central cav-ity where folding can take place This cavcav-ity can accommodate proteins up to 60 kD

in size GroES, sometimes referred to as a co-chaperonin, consists of a single

seven-membered ring of 10-kD subunits that sits like a dome on one end of GroEL (Figure

A DEEPER LOOK

How Does ATP Drive Chaperone-Mediated Protein Folding?

The chaperones that mediate protein folding do so in an

ATP-dependent manner, as illustrated in Figures 31.2 and 31.3 The

affinity of chaperones for their unfolded or misfolded protein

sub-strates is determined by the nature of the nucleotide bound by the

ATP-binding domain of these proteins, which functions as an

ATPase If ATP is bound, the chaperone adopts a conformation with

an open substrate-binding pocket ATP increases the rate of

associ-ation of the chaperone Hsp70 (DnaK) with an unfolded peptide or

protein substrate by 100-fold, but it increases the rate of dissociation

of the unfolded protein from the chaperone even more, by a factor

of 1000 Overall, the chaperone’s affinity for an unfolded protein

substrate decreases 10-fold (or more) when it binds ATP

On the other hand, if the substrate-binding site on the

peptide-binding domain of DnaK is occupied by an unfolded protein

sub-strate in conjunction with binding of the co-chaperone (DnaJ in

Figure 31.2), ATP hydrolysis by the ATPase domain is triggered

The presence of ADP in the ATP-binding (ATPase) domain causes

a shift in the substrate-binding site of the peptide-binding domain

to a closed conformation, high-affinity state Thus, ATP-dependent

chaperones cycle between two stable conformational states, just

like allosteric proteins Bound ATP favors the open conformation

for the protein substrate-binding site, and ADP favors the closed

conformation (When ADP is released and no nucleotide occupies

the ATP-binding site of the ATPase domain, the peptide-binding

site remains in the closed, high-affinity conformation; see Figure

31.2) What is the underlying mechanism that controls these

ATP-regulated conformational changes?

The ATP-Dependent Allosteric Regulation of Hsp70 Chaperones

Is Controlled by a Proline Switch

Clearly, the two domains of Hsp70 (DnaK)—the peptide-binding

domain and the ATP-binding (or ATPase) domain—communicate

with each other, because the nature of the nucleotide bound to the

ATP domain determines the affinity of the peptide-binding domain

for unfolded substrates Markus Vogel, Bernd Bukau, and Matthais

Mayer of the Center for Molecular Biology at the University of

Heidelberg (Germany) argue that four distinct elements are

needed for communication between these separate domains: an

ATP sensor (which must include residues within the ATP-binding

site), a transducer (to communicate the presence of ATP to the

dis-tant peptide-binding site), a lever (operated by the ATP-binding

domain to exert its effect on the distant peptide-binding domain),

and a switch that controls the lever (the switch is needed to lock the

protein in either the open conformation or the closed conforma-tion so that either alternative conformaconforma-tion is stable)

The switch that controls the conformational transitions of Hsp70 involves two universally conserved residues in the ATPase domain of Hsp70 family members, a proline (Pro143) and a surface-exposed arginine (Arg151; panel a of the figure) Pro143is the switch, and Arg151is a relay for the lever Replacement of either

of these residues by amino acid substitutions disrupts and/or destabilizes the switch Other nearby residues, Glu171 and Lys70, function as ATP sensors It is believed that Lys70also serves as the nucleophile that initiates ATP hydrolysis through attack on the

-phosphate of ATP Arg151acts as a relay between Pro143, events occurring during ATP hydrolysis, and the peptide-binding domain (panels b–d of the figure) When ATP binding is sensed by Lys70

and Glu171(panel b), Pro143is shifted, which causes Arg151to move

in the direction of the peptide-binding domain of DnaK (panel c)

In turn, this protein-binding domain assumes the open, low-affinity conformation The interaction of DnaK with an unfolded protein substrate and co-chaperone DnaJ moves Arg151back to-ward Pro143, which causes Lys70and Glu171to initiate ATP hydroly-sis (panel d) ADP now occupies the nucleotide-binding site of the ATPase domain, and the protein-binding domain of DnaK is locked in the closed, high-affinity conformation

The consequence of these events is that DnaK cycles between binding and releasing unfolded (or partially folded) proteins, fueled by ATP hydrolysis within the ATPase domain In effect, ATP binding and hydrolysis drive DnaK from an open, low-affinity con-formational state to a closed, high-affinity concon-formational state When unfolded (or partially folded) proteins are not held by DnaK, they have the opportunity to fold so that any solvent-accessible hydrophobic surfaces they might still retain are buried Once a pro-tein has adopted a stable folded state, it lacks exposed hydrophobic surfaces and thus escapes the cycle of binding and release by DnaK More generally, Hsp70 provides an elegant example of protein con-formational transitions based on the binding of ATP versus ADP at

an effector site, with the added dimension that the effector site in this case is also an ATPase

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31.3) The end of GroEL where GroES is sitting is referred to as the apical end Each

GroEL subunit has two structural domains: an equatorial domain that binds ATP and

interacts with neighbors in the other 7ring and an apical domain with hydrophobic

residues that can interact with hydrophobic regions on partially folded proteins The

apical domain hydrophobic patches face the interior of the central cavity An

un-folded (or partially un-folded) protein binds to the apical patches and is delivered to the

central cavity of the upper 7ring (Figure 31.3c) ATP binding to the subunits of the

upper 7ring causes rapid (100 msec), forced unfolding of the substrate protein,

followed by two events that occur on a slower time scale (⬃1 sec): (1) GroES is

re-cruited to GroEL, and (2) the -subunits undergo a conformational change that

buries their hydrophobic patches The -subunits now present a hydrophilic surface

to the central cavity This change displaces the bound partially folded polypeptide

into the sheltered hydrophilic environment of the central cavity, where it can fold,

free from danger of aggregation with other proteins GroES also promotes ATP

hy-drolysis (Figure 31.3c) The GroEL⬊ADP⬊GroES complex dissociates when ATP binds

to the subunits of the other (lower) 7ring Dissociation of GroES allows the partially

folded (or folded) protein to escape from GroEL If the protein has achieved its

na-tive conformation, its hydrophobic residues will be buried in its core and the

hy-(a)

O P O O

O

O

O

Mg

E171 w

O

w w

w w O O

R151

K70 P143 ATP

sensors Switch

Relay

(b)

P143

O P O

O

O

O

O

Mg w

O

w w

w w O O

E171

R151 K70

E171

R151

K70 P143

(c)

ATP sensors Switch

O P O O

O

O

O

Mg w O

w w

w w O O

K70

E171

R151

K70 P143

(d)

ATPase catalysts Switch

Relay

(a)Side chains involved in the ATP- and ADP-dependent allosteric regulation of the Hsp70 family

member DnaK Lower numbers indicate DnaK amino acid residues; upper numbers indicate the

cor-responding residues in Hsc70 (the human counterpart to DnaK) This illustration highlights

residues in or near the ATP-binding site of the ATPase domain The site is occupied by ADP, Pi, one

Mg2, and two Kions See Figure 31.2a for the location of this site within the ATPase domain

Carbon atoms are gray; oxygen, red; nitrogen, blue; and phosphorus, yellow P143 sits at the center

of an H-bonded network of residues, which includes K70, Y145, F146, R151, and E171 (b–d) The

mechanism of ATP- and ADP-dependent allosteric transitions in Hsp70 Events in the ATP-binding

site of the ATPase domain are communicated to the protein-binding site of the peptide-binding

domain through K70 and E171, which act as ATP sensors; P143, which acts as the switch; and R151,

which is part of the lever that relays the events from the ATPase domain to the other domain

(a: Adapted from Figure 1 in Vogel, M., Bukau, B., and Mayer, M P., 2006 Allosteric regulation of Hsp70 chaperones by a

proline switch Molecular Cell 21:359–367 Courtesy of Bernd Bukau and Matthias Mayer b–d: Adapted from Figure 6 in

Vogel, M., Bukau, B., and Mayer, M P., 2006 Allosteric regulation of Hsp70 chaperones by a proline switch Molecular Cell

21:359–367.)

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992 Chapter 31 Completing the Protein Life Cycle: Folding, Processing, and Degradation

drophobic patches on the 7rings will have no affinity for it On the other hand, if the protein is only partially folded, it may be bound again, gaining access to the Anfinsen cage of the 7ring and another cycle of folding The folding of rhodanese,

a 33-kD protein, requires the hydrolysis of about 130 equivalents of ATP

The group II chaperonin and eukaryotic analog of GroEL, CCT (also called

TriC ) is also a double-ring structure, but each ring consists of eight different sub-units that vary in size from 50 to 60 kD Furthermore, group II chaperonins lack a

GroES counterpart Prefoldin (also known as GimC), a hexameric protein

com-posed of six subunits from two related classes (two  and four ), can serve as a

co-chaperone for CCT, much as GroES does for GroEL However, prefoldin also acts like an Hsp70 protein, because it binds unfolded polypeptide chains emerging from ribosomes and delivers them to CCT Prefoldin resembles a jellyfish, with six tentacle-like coiled coils extending from a barrel-shaped body The ends of the ten-tacles have hydrophobic patches for binding unfolded proteins.

Prior to substrate protein binding, CCT exists in a partly open state ATP bind-ing opens the rbind-ing even more, a state in which prefoldin delivers the substrate pro-tein ATP hydrolysis closes the chamber and drives the folding process ATP-induced conformation changes that promote protein folding propagate from one subunit to the next around the ring structure.

The Eukaryotic Hsp90 Chaperone System Acts on Proteins

of Signal Transduction Pathways

Hsp 90 constitutes 1% to 2% of the total cytosolic proteins of eukaryotes, its abundance reflecting its importance Like other Hsp chaperones, its action depends on cyclic binding and hydrolysis of ATP Conformational regulation of signal transduction mol-ecules seems to be a major purpose of Hsp90 Receptor tyrosine kinases, soluble

tyro-( b )

U, I

(c)

~15 sec

~1 sec

< 100 ms

N

FIGURE 31.3 Structure and function of the GroEL–GroES

complex (a) Structure and overall dimensions of

GroEL–GroES (top view, left; side view, right) (pdb id 

1AON) (b) Section through the center of the complex

to reveal the central cavity (c) Model of the GroEL

cylin-der (blue) in action An unfolded (U) or partially folded (I)

polypeptide binds to hydrophobic patches on the

api-cal ring of 7-subunits, followed by ATP binding, forced

protein unfolding, and GroES (red) association.

( a )

140 A°

80 A°

10 A°

33 A°

80 A°

71 A°

184 A°

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