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Tiêu đề Top-down MS, a powerful complement to the high capabilities of proteolysis proteomics
Tác giả Fred W. McLafferty, Kathrin Breuker, Mi Jin, Xuemei Han, Giuseppe Infusini, Honghai Jiang, Xianglei Kong, Tadhg P. Begley
Trường học Cornell University; University of Innsbruck
Chuyên ngành Proteomics / Mass spectrometry
Thể loại Minireview
Năm xuất bản 2007
Thành phố Ithaca, NY, USA
Định dạng
Số trang 13
Dung lượng 0,94 MB

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MS⁄ MS dissociation of molecular ions of an individual peptide can yield fragment masses that are indicative of its sequence.. In bot-tom-up identifications, the partial or full sequence

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2 Institute of Organic Chemistry and Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Austria

Introduction

The MS techniques of ESI [1] and MALDI [2] have

been available for only two decades, but they have

rev-olutionized the introduction of large, nonvolatile

mole-cules such as proteins into the mass spectrometer [3,4]

Here we discuss two general types of such MS

‘proteo-mics’ applications: (a) the identification of a protein

from among those predicted from the parent genome’s DNA; and (b) the structural characterization of a pro-tein, such as identifying and locating post-translational modifications (PTMs) or errors in the predicted sequence Currently, by far the most common method-ology for these in useful applications involves initial protein proteolysis, an approach that we have termed

‘bottom-up’ [5] The ‘top-down’ [5] approach described

Keywords

electron capture dissociation; MS; protein

characterization; protein identification;

post-translational modifications; top-down

proteomics

Correspondence

F W McLafferty, Baker Chemistry

Laboratory, Cornell University, Ithaca,

NY 14853, USA

Fax: +607 255 4137

E-mail: fwm5@cornell.edu

(Received 30 May 2007, revised 12 October

2007, accepted 17 October 2007)

doi:10.1111/j.1742-4658.2007.06147.x

For the characterization of protein sequences and post-translational modifi-cations by MS, the ‘top-down’ proteomics approach utilizes molecular and fragment ion mass data obtained by ionizing and dissociating a protein in the mass spectrometer This requires more complex instrumentation and methodology than the far more widely used ‘bottom-up’ approach, which instead uses such data of peptides from the protein’s digestion, but the top-down data are far more specific The ESI MS spectrum of a 14 protein mixture provides full separation of its molecular ions for MS⁄ MS dissocia-tion of the individual components False-positive rates for the identificadissocia-tion

of proteins are far lower with the top-down approach, and quantitation of multiply modified isomers is more efficient Bottom-up proteolysis destroys the information on the size of the protein and the connectivities of the pep-tide fragments, but it has no size limit for protein digestion In contrast, the top-down approach has a  500 residue,  50 kDa limitation for the extensive molecular ion dissociation required Basic studies indicate that this molecular ion intractability arises from greatly strengthened electro-static interactions, such as hydrogen bonding, in the gas-phase molecular ions This limit is now greatly extended by variable thermal and collisional activation just after electrospray (‘prefolding dissociation’) This process can cleave 287 inter-residue bonds in the termini of a 1314 residue (144 kDa) protein, specify previously unidentified disulfide bonds between eight of 27 cysteines in a 1714 residue (200 kDa) protein, and correct sequence predictions in two proteins, one of 2153 residues (229 kDa)

Abbreviations

BCA, bovine carbonic anhydrase; CAD, collisionally-activated dissociation; ECD, electron-capture dissociation; HAD, 3-hydroxyanthranilate-3,4-dioxygenase; IRMPD, infrared multiphoton dissociation; PFD, prefolding dissociation; PTM, post-translational modification;

PurL, formylglycinamide ribonucleotide amidotransferase.

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here directly introduces the proteins into the mass

spectrometer, providing far higher specificity at the

expense of far higher experimental requirements As

predicted in a prescient 2004 review [6], the top-down

method is being exploited increasingly in unique

appli-cations, with 18% of proteomics papers⁄ posters at the

2007 meeting of the American Society for Mass

Spec-trometry concerning this newer approach

Although ESI spectra of proteins larger than

mega-daltons have been reported [7,8], the great majority

of ESI spectra measured are those of the small

(< 3 kDa) peptides produced by the bottom-up

prote-omics methodology [9–13] The sample is digested with

a protease such as trypsin to produce a mixture of

small peptides from each protein, and is applicable to

even a complex mixture of proteins (e.g the ‘shotgun

approach’) [10] A common next step is the separation

of the total mixture into fractions by HPLC, followed

by their on-line introduction into the mass

spectrome-ter to yield ESI spectra showing molecular ions, and

thus molecular mass values, of the peptides MS⁄ MS

dissociation of molecular ions of an individual peptide

can yield fragment masses that are indicative of its

sequence These results can then be matched against

the molecular mass and MS⁄ MS peptide masses

expected for the individual proteins predicted from the

parent genome’s DNA In contrast [14], the ‘top-down’

methodology [5,6,14–22] can directly subject a mixture

of proteins, even of > 10 components, to ESI to yield

a spectrum of their molecular ions that indicates the

molecular mass values of individual proteins MS⁄ MS

of the mass-selected ions of a protein then provides

fragment mass values for its structural

characteriza-tion

In general, the bottom-up method is widely accepted

for the routine identification of proteins in complex

mixtures Usually, the identification of the gene that

encodes the protein is more important than full

struc-tural characterization of the protein Its quantitative

analysis by the bottom-up method under normal and

abnormal conditions can then provide a direct

indica-tion of the upregulaindica-tion or downregulaindica-tion of the

gene If, however, more extensive or specific data are

needed, such as on polymorphisms or PTMs, the

com-plementary top-down approach can often provide

these in a very straightforward manner This review

also discusses alleviation of a serious previous

prob-lem: top-down molecular ion dissociations have given

few product ions for proteins > 50 kDa The far

higher masses measured with the top-down approach

require correspondingly higher MS resolving power,

so the instrument of choice has been the expensive

Fourier transform mass spectrometer (FT MS)

[3,5,23,24] FT MS has the added advantage that it can give MS⁄ MS spectra by electron-capture dissocia-tion (ECD) [25–27], which provides far more fragment ion information than either collisionally-activated dissociation (CAD) [28] or infrared multiphoton disso-ciation (IRMPD) [29] However, ECD’s descendant, electron-transfer dissociation [30], works well with less expensive MS instruments, and can be applied to pep-tides and smaller proteins [31] with versatile ion–ion reactions [32] Of special promise for routine top-down applications is the recently developed Orbitrap mass spectrometer, which has resolution and mass accuracy capabilities approaching those of FT MS, with very promising cost advantages [33] ECD and electron-transfer dissociation are less sensitive than CAD or IRMPD, in part because they produce far more product ions

Identification

To date, by far the largest use of MS proteomics has been to identify unknown proteins, usually by match-ing mass values against those from a list of sequences predicted from the precursor DNA The quantities of these proteins that are expressed can differ by many orders of magnitude, so that a specific problem often requires preconcentration⁄ separation (e.g LC) In bot-tom-up identifications, the partial or full sequence of

an individual peptide is predicted from its molecular mass and MS⁄ MS mass values, with the number and uniqueness of these values determining the peptide identification accuracy The matching of multiple pep-tide sequences with that of a predicted protein increases the bottom-up identification accuracy, although it is possible that the same peptide data could also match those of another protein in the mixture (identified peptides that do not match a predicted pro-tein are typically ignored) Several bottom-up approaches achieve  1% identification accuracy in routine applications [9–13] Sensitivity, automation and throughput can also be of vital importance, but these depend on the combination of separation methods,

MS instrumentation, and computation employed Top-down MS⁄ MS of the selected molecular ion mass representing a specific protein produces far more fragments that have much higher masses, and are thus more unique, and the more expensive FT MS instru-mentation used with the top-down approach also pro-vides much higher mass accuracy [6,18,23,34] Furthermore, these fragment mass values originate from the same molecular ions, so they must all be characteristic of that protein’s sequence and molecular mass value Thus, top-down data can give an accuracy

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of identification that is orders of magnitude higher

[6,23,35] For example, Begley and co-workers [21]

iso-lated an enzyme YjbV involved in the B subtilis

thia-mine biosynthesis pathway for which 1D SDS-PAGE

analysis indicated an approximate mass of 3 kDa

(Fig 1) The top-down ESI⁄ FT MS spectrum of this

protein with nozzle-skimmer CAD dissociation (Fig 1)

confirmed the YjbV sequence and demonstrated the

absence of any post translational modifications Not

only does the measured molecular mass value of

31 407.1 agree with the predicted mass from the DNA

sequence at 31 406.9 Da, within the limits of

experi-mental accuracy, but also there are 23 top-down

frag-ment mass values that agree with those expected from

single backbone cleavages (Fig 1) Thus, each

frag-ment contains either the N-terminus or C-terminus,

providing extensive confirmatory sequence information

(see below) for this SDS⁄ PAGE-purified protein

For protein identifications in complex mixtures, a

dramatic advantage of the top-down approach is

that a final separation stage can be done in the

FT MS instrument For example, after rough

separa-tion of the proteins from Arabidopsis thaliana, the

stromal protein fraction was introduced directly by

ESI into the FT MS instrument to yield an ESI

mass spectrum in which the molecular ions from 14

different proteins can be distinguished (Fig 2) [20]

Figure 3 shows a protein’s molecular ion isotopic

cluster that yielded a measured molecular mass of

20 211.3 Da An obvious identification was the

DNA-predicted protein At1g06680, whose molecular mass is

20211.9 Da As a convincing confirmation, the CAD

MS⁄ MS spectrum of this isolated ion cluster included eight peaks of 8246–9308 Da whose mass differences matched those expected in the predicted protein for the sequence A-V-X4-F-G-G-(S + E) (Fig 3) [20] Extending this to mixtures of large proteins (see below), nozzle-skimmer dissociation spectra of 1 : 1,

2 : 1 and 3 : 1 mixtures of 144 and 116 kDa proteins showed the corresponding molecular ions and, for each, 11–17 different mass values of 1–10 kDa that represented their b or y fragment ions with a standard deviation of 5 p.p.m [36]

ECD The development of ECD [25] has made possible a dramatic increase in the proportion of inter-residue backbone bonds that can be cleaved in molecular ions The high-energy ( 5 eV) recombination of an electron with the multiply protonated ion makes differences in bond dissociation energies much less important and leads to much more indiscriminate protein backbone cleavages For example, 250 of the 258 inter-residue bonds could be cleaved (as assigned by the terminus-containing ions c, z., a., b and y) in bovine carbonic anhydrase (BCA) molecular ions in 25 ECD⁄ CAD spectra [19], with 183 bonds being cleaved in a single

‘plasma ECD’ spectrum (Fig 4) [26] Obviously, this amount of mass spectral information makes possible even higher identification reliabilities, and also extensive

de novosequencing and structural characterization

Fig 1 Left: 1D SDS ⁄ PAGE chromatograms

of ThiD from E coli and of unknown YjbV from B subtilis Right, above: ESI spectrum

of YjbV, molecular ion isotopic peaks Right, below: nozzle-skimmer dissociation spectral data, YjbV fragment peaks The ‘ ) 20’ after the molecular mass value signifies that the main component ion of the most abundant isotopic peak contains 20 13 C atoms and has this mass value.

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The high specificity of the top-down approach for

pro-tein structural characterization is due to the extensive

molecular connectivity information that it provides;

this is not destroyed by proteolysis The peptides from

proteolysis usually represent substantially less than

100% coverage of the protein sequence, so that even when their mass information is consistent with a previ-ously identified protein, the sample protein could have missing or extra parts In the top-down approach, an incorrect molecular mass value directly indicates the presence of PTMs and⁄ or an incorrect sequence In another ESI mass spectrum of proteins isolated from

Fig 2 ESI mass spectrum of the isolated

stromal proteins from A thaliana with their

measured molecular mass values [20].

Fig 3 ESI mass spectrum of the isolated chloroplast proteins from A thaliana (top) The 20 211.3 Da 19+ ions (< 10% abundance) were subjected to top-down MS⁄ MS to yield the CAD spectrum (bottom), which is consistent with the predicted sequence of At1g06680, molec-ular mass 20 211.9 Da.

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A thaliana [20], molecular ions representing a 5%

component gave a molecular mass of 16 309.7 Da, but

this matched none of the DNA-predicted proteins

MS⁄ MS of these ions gave the C-terminal sequence of

Fig 5 These and all other peaks of that spectrum did

match those expected for the predicted protein

At4g21280, although its molecular mass of

16 123.4 Da is lower than that found by 186 Da

Dissociation of the 16 121.8 Da fragment peak

(MS⁄ MS ⁄ MS, Fig 5) showed a fragment ion resulting

from an initial loss of 186.0 Da, followed by cleavages

corresponding to the N-terminal sequence of the

pre-dicted protein; the cleavage loss of the signal peptide

left two more amino acids on the protein than

pre-dicted Even if the bottom-up approach did provide

mass data on a peptide containing these amino acids,

these data would have been ignored in most protocols

However, even measuring a molecular mass value

that is the same as that predicted is not a guarantee

that the predicted sequence is correct In an early

(1993) example of top-down identification [23], our

measured molecular mass value, 29 024.2 Da, of BCA

matched well the value that was calculated,

29 024.7 Da, from the published sequence

Further-more, MS⁄ MS (nozzle-skimmer CAD) of the

molecu-lar ions gave 21 terminal fragment ions that were also

consistent with the published sequence However, our

2003 plasma ECD spectrum of BCA (Fig 4; 183

cleavage sites) gave 512 mass values [26], of which 45

were in error by ) 1 Da; these values all represented

cleavages in the region of residues 10–31 This is

strong evidence that the residue reported as Asp10

should be Asn10, and Asn31 should be Asp31

(Asp CO-OH, Asn CO-NH2, Dm ¼ –1 Da; note that

these changes do not affect the molecular mass value

of the protein) Detecting this error in the usual bot-tom-up approach would be difficult, as peptides that incorporate residues 10 or 31 would not match a pre-dicted sequence and so would be ignored Worse yet,

in our 1999 top-down study of BCA [5], + 1.00 Da and + 0.99 Da errors found for peptides Phe19– Asp33 and Asp18–Lys35 were termed ‘unexpected (and unexplained) anomalies’ Obviously, the precision

of locating such sequence errors or PTMs is depen-dent on obtaining fragment ion masses representing nearby dissociations on either side of the error; in the unusual Fig 4 case of nearby offsetting errors, having multiple ions representing cleavages between almost all neighboring residues made it clear that these were not ‘anomalies’

Post-translational modifications are the most com-mon challenge for the structural characterization of proteins Special bottom-up techniques have been developed for specific PTMs, e.g affinity separation of the protein digest to concentrate all glycosylated or all phosphorylated peptides for MS⁄ MS For a sample containing proteins modified on different sites, the bot-tom-up approach cannot characterize individual pro-teins In contrast, the top-down approach can select molecular ions with a molecular mass value cor-responding to, for example, a single substitution;

MS⁄ MS will then show the substituent positions of dif-ferent isomers A problem for MS⁄ MS of either the peptides for the bottom-up approach or of the proteins for the top-down approach is that backbone dissocia-tion techniques such as CAD or IRMPD can also cleave off side-chain substituents such as glycosylated, phosphorylated or sulfonated components, thus

Fig 4 A single plasma ECD spectrum of BCA whose 512 different m ⁄ z values define

183 of its 258 inter-residue cleavage sites [26] Of these m ⁄ z values, 45 are 1 Da higher than those predicted by the protein database sequence, and all represent cleav-ages between the proposed Asp10 and Asn31 This shows that these identifications are reversed, an error that does not affect the molecular mass value and a sequence consistent with those of sheep and human carbonic anhydrases.

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destroying information on their backbone location.

However, the energetic (‘nonergodic’) dissociation of

ECD is localized on the backbone, with little

accompa-nying cleavage of weaker side-chain modifications such

as glycosylated [37] and phosphorylated structures [38]

(and even of noncovalent bonding and conformational

tertiary protein structures; see below) Top-down ECD

and CAD of b-casein gave 126 out of the possible 208

backbone cleavages (Fig 6); the ECD cleavages not

only indicate the five phosphorylation sites without

loss of these side chains, but also that these cleavages

are so positioned that they would have specified

phos-phorylation if it had occurred at any of the other 21

possible sites (Ser, Thr, Tyr) of b-casein [38] Although

ECD requires the more expensive FT MS

instrumen-tation, it measures all product ions simultaneously,

which is of particular value for repeated quantitative

measurements, e.g variable phosphorylation of isolated

b-casein samples

Unexpected modifications are especially difficult for

classic and bottom-up methods, which must be selected

or tailored for the specific PTM In the biosynthesis of NAD, the enzyme 3-hydroxyanthranilate-3,4-dioxygen-ase (HAD) catalyzes the oxidative ring opening of 3-hydroxyanthranilate, which, with cyclization, forms a quinolinate [39] Excess quinolinate is implicated in neurological disorders such as stroke and Huntington’s disease, and 4-halohydroxyanthranilates have been found to be specific and potent HAD inhibitors To check for covalent modifications of the enzyme, the effect of the inhibitor on the molecular mass value of HAD was measured; instead of an adduct increase, or

no change, the value had unexpectedly decreased from

22 417.0 Da to 22 413.2 Da, a loss of 4 Da MS⁄ MS

of these molecular ions (Fig 7) cleaved 144 of the 193 inter-residue bonds (78 uniquely from ECD), confirm-ing almost completely the predicted sequence of the first 75 residues after eliminating the mistakenly pre-dicted N-terminal Met The fragment ions containing the C-terminus have the predicted mass values going back 10 residues to Cys183, but after Cys180 they are all  2 Da lower than predicted until Cys149 and

Fig 5 Partial CAD spectrum (top) of the

16+ ions of molecular mass 16 309.7 Da

(5% abundance) from ESI of the thylakoid

peripheral proteins isolated from A thaliana.

This spectrum matched the masses

pre-dicted for the C-terminus of the protein

At4G21280, molecular mass 16 123.4 Da.

A partial CAD spectrum (bottom) of the

16 121.8 Da 15+ fragment ions

(MS⁄ MS ⁄ MS) matched that protein’s

N-ter-minus plus two signal peptide amino acids

whose mass corresponds to the 186 Da

dis-crepancy in the protein molecular mass

value.

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Cys146, after which they are low by  4 Da, the

decrease of the molecular mass value The most

proba-ble reason for a 2 Da decrease is the formation of an

S–S bond; although this was totally unexpected and

unprecedented, the top-down approach efficiently gave

a specific characterization of the inhibitor mechanism

[39] Even if two S–S bonds had been suspected,

identi-fying for each their two specific cysteines cut of the

10 possible for the five cysteines (including Cys127),

would be difficult by classic or bottom-up methods

Deamidation of Asn or Gln in proteins has

impor-tant effects on enzyme activity and folding, and has

even been proposed as a biological clock [40] How-ever, changing –CO-NH2to –CO-OH only produces a mass increase of 1 Da; as in Fig 4, this makes the ability of FT MS to resolve protein ion isotopic peaks

of critical importance for such a mass shift determina-tion The most abundant of the 13+ molecular ions of reduced RNase A before deamidation (Fig 8A) shows

Fig 7 ECD, CAD and IRMPD spectral data of HAD treated with

inhibitor [22] C-terminal fragment ions 1–4 Da below the mass

values predicted for untreated HAD clearly indicate the unexpected

S–S bonds Cys146 to Cys149 and Cys183 to Cys186.

Fig 6 Inter-residue backbone fragmentations from the ECD

spect-rum of b-casein’s three variants, molecular masses 24 008.2 Da,

23 968.2 Da, and 24 077.2 Da [38] These fragmentations are

con-sistent with the known phosphorylations at Ser15, Ser17, Ser18,

Ser19, and Ser35 These fragmentations would also specifically

indicate any phosphorylation that occurred at the other 21 possible

Ser, Thr and Tyr sites.

Fig 8 Molecular ion isotopic clusters from ESI of the product mix-tures from deamidation of RNase A over increasing time periods Deamidation of any one of the 17 Asn and Gln sites of RNase A produces a 1 Da increase in the mass, –CO-NH 2 fi –CO-OH, of the molecular ions of that product The observed isotopic abun-dances give calculated best fits for the average increases of 0.0, 1.0, 1.8, 3.7 and 4.4 Da, respectively, in the masses of the prod-ucts [40].

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a mass of 13 689.3 Da versus the calculated value

13 689.3 Da The circles represent the calculated

abun-dance distribution for the isotopic peaks whose

maxi-mum peak contains mainly 13C8, whereas the squares

represent the distribution 1 Da higher To determine

the mass increase with increasing time of deamidation

(pH 9.6), the best fit of calculated intensity values

(squares) was determined (Fig 9B–E) The

correspond-ing mass increase values in the ECD and CAD

frag-ment ions were determined similarly and are plotted

for the four product samples in Fig 9 as mass

increases (decreases) for the N-terminal

(C-terminal)-containing fragment ions Thus, for the + 1.0 Da

sam-ple (Fig 8B), the N-terminal fragment ions show little

increase in mass with increasing size until Asn67, with

this increase of  1.0 Da staying constant for larger

N-terminal ions and with the C-terminal ions showing

the complementary decrease This demonstrates

directly that Asn67, the only deamidation site found

previously, is indeed deamidated before any other

resi-due In a similar fashion, the samples with 1.8, 3.7 and

4.4 Da increases show that Asn71 and Asn94 are

nearly equally reactive as the next sites, followed by

Asn34 and then Gln74 [40] Other examples show the utility of top-down MS⁄ MS for such kinetic studies [17,22,41]

Top-down quantitative analysis Measuring the differences in protein expression levels that result from disease states, environment, etc is critically important in many biomedical investiga-tions The protein quantities in cases of normal and perturbed expression are compared accurately by iso-topically labeling the proteins from one and compar-ing in their mixture the correspondcompar-ing peaks of their respective peptides, usually differing by three or more mass units [9–12] The kinetic deamidation study above (Fig 9), in a similar fashion, compares the quantities of proteins differing in the position of deamidation (only a + l Da change) with the multi-ple MS⁄ MS spectral peaks, providing multiple mea-surements of the quantities The top-down approach should be the method of choice for quantitation of position isomers of proteins containing multiple mod-ifications [42]

Fig 9 ECD spectral data from the RNase A deamidation samples of Fig 8 Deamidation at an individual residue of a specific product causes

a 1 Da increase in any fragment ion containing that residue The average mass gain of N-terminal and C-terminal fragment ions are plotted

as positive and negative, respectively, mass increases, with the molecular ion mass increases of Fig 8 designated on the right ordinate [40].

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dissociation used for the bottom-up approach is far

more generally applicable than the gas-phase MS⁄ MS

dissociation methods used with protein molecular ions

for the top-down approach With increasing protein

size, the hydrophilic (e.g hydrogen bonds) and

hydro-phobic tertiary bonding becomes more complex and

stabilizing Such native conformer structures of

pro-teins in solution are easily destroyed by various

reac-tive agents, but top-down dissociation methods for

gaseous protein ions, such as CAD and IRMPD, are

unimolecular, and so require the use of increasing

amounts of energy for the dissociation of increasingly

large protein ions Basic studies over the past 15 years

have shown fundamental differences in protein

confor-mations in solution versus the gas phase, with H⁄ D

exchange identifying reactive regions of the

conforma-tion [43–45], ion mobility measuring conformaconforma-tional

cross-sections [46,47], ECD identifying regions of

ter-tiary noncovalent bonding, as these are preserved when

backbone bonds are cleaved [48,49], and infrared

photodissociation spectroscopy characterizing

func-tional group environments [44,50] For example,

charge sites, such as the protonated side chains of

basic residues, in solution are solvated out into the

aqueous phase, while in the gas phase they are instead

solvated onto the protein backbone, with this

appar-ently favored if the backbone is in an a-helical

struc-ture [44–50]

ECD itself causes negligible cleavage of this tertiary

structure However, its noncovalent bonds have

sub-stantially lower bond dissociation energies, in general,

so that limited activation by earlier or concurrent

this tertiary structure has become so strong and exten-sive that conventional activation by CAD or IRMPD gives few or no backbone cleavages, making the top-down approach ineffective [51]

A possible solution to this problem was indicated by the study of conformational changes occurring during solvent evaporation immediately after electrospray introduction into the FT mass spectrometer [52] Solu-tion protein conformaSolu-tions are actually unfolded dur-ing electrospray; use of native ECD [53] showed that ECD could occur without externally added electrons when electrosprayed native cytochrome c unfolded in the inlet capillary, exposing basic residues that attracted electrons and caused ECD Solvent removal reduces or destroys hydrophobic bonding Further-more, in solution, water molecules solvate the protein’s protonated side chains; on solvent removal, these are immediately available for new hydrogen bonding Thus, supplying thermal and collisional energy during solvent evaporation can slow the new folding stabiliza-tion of the protein ions, while also providing sufficient excitation to effect cleavage before the gaseous confor-mation becomes too stable [52]

This new technique of prefolding dissociation (PFD) has now been successfully applied to 116, 144, 200 and

229 kDa proteins [36], using a 6 Tesla FT MS instru-ment [15–17] ESI of formylglycinamide ribonucleotide amidotransferase (PurL) (1315 residues), whose reported sequence [54] corresponds to a molecular mass of 143 635 Da, gave the Fig 10 spectrum indicating a molecular mass of 143 500 ± 23 Da Our nozzle-skimmer dissociation system can vary the ion

Fig 10 ESI mass spectrum of PurL Isotopic peaks are not resolved; deconvolution yields a molecular mass of 143 500 ± 23 Da [36].

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accelerating voltage for CAD both in the  1 Torr

pressure region before the skimmer (Vpre) and in the

 10)3Torr region after the skimmer (Vpost) In

gen-eral, Vpre produces many low-energy collisions to

cleave noncovalent bonds, whereas Vpost produces

fewer collisions with energies approaching the

acceler-ating voltage to cleave backbone bonds Different

combinations of Vpre, Vpost and capillary temperature

values in 11 PFD spectra gave 173 different

inter-resi-due backbone cleavages (Fig 11) In a serendipitous

discovery, additives to the ESI solution such as

ammo-nium tartrate increased the number of cleavages by

 50%, with a total of 21 spectra showing 287

differ-ent cleavages (Fig 11) [36] These are only between the

first  240 residues from each end, so that here they

provide extensive ( 60%) sequence coverage For

example, these data clearly show that the predicted

N-terminal Met is not present; this changes the

pre-dicted molecular mass value to 143 504 Da, in good

agreement with that found of 143 500 ± 23 Da

How-ever, no information has been obtained from the

central  900 residues; we picture this gaseous protein

conformation as a ‘ball of spaghetti’, for which the

energetic activation has denatured the free ends or has

prevented them from folding Possibly, the highly

ener-getic ECD in the capillary-skimmer region could effect

a few cleavages in the center of the protein to form

additional loose ends to be denatured out of the ball

of spaghetti

The ESI spectrum of the 200 kDa human

comple-ment C4 glycoprotein (of 1714 residues in three chains

connected by three S–S bonds) [55] had no molecular

ions Nearly complete deglycosylation (of predicted

molecular mass 186 437 Da) was indicated, as gentle

PFD gave fragment ions of 20 838 Da (b-185 of the

b-chain) and 165 746 ± 80 Da, with the total

186 584 ± 80 Da indicating < 0.1% remaining

glyco-sylation This was confirmed by stronger PFD, with

which 87 fragment ions were found to correspond to

different cleavages of the deglycosylated protein This contains 27 Cys residues, but it was not known which are still in the –SH form or which form S–S bonds, and what are the connectivities for the latter As for HAD [39] above, the presence of an S–S bond in a ter-minal fragment ion causes the PFD fragment mass to

be 2 Da less than the sequence-predicted value, and fragment ions are usually not observed from cleavages between the Cys residues, as they are held together by the S–S bond With this, eight additional S–S bonds could be specified [36]

The largest protein examined, mycoserosic acid synthase, had a predicted [56] molecular mass of

229 067 da (2154 residues), whereas ESI gave

228 934 ± 60 Da Five PFD spectra designated 62 cleavages by omitting the predicted N-terminal Met, correcting the molecular mass value to 228 936 Da to agree with that measured Its ‘ball of spaghetti’ is more difficult to unravel; cleavages were limited to 134 and

182 residues from the N-terminus and C-terminus, respectively Very recently in collaboration with

M Boyne and N Kelleher, (University of Illinois, Urbana, IL) PFD has also been implemented on an 8.4 Tesla FT MS instrument, despite its substantially different ion entrance system, which includes an ion funnel and octupole for ion storage

Conclusions The top-down and bottom-up proteomics approaches are obviously complementary The identification of proteins from among those predicted by the DNA sequence still has by far the largest sample demands

In most cases, the bottom-up approach, requiring less sophisticated instrumentation and expertise, should be tried first for qualitative identification, although increas-ing demands for more accurate quantitation provide a promising area for the top-down approach [36,57,58] Reliability of identification can be far superior with the

Fig 11 PFD spectral data of PurL Inter-residue backbone fragmentations are indicated by: N-terminal-containing b fragment ions (left, above line); C-terminal-containing y ions (right, above line); and secondary fragment ions (below line) Top line: 173 different fragmentations from

11 spectra using various values of capillary temperature and preskimmer and postskimmer accelerating voltages Bottom: 287 in total, including 10 additional spectra with ammonium tartrate added to the ESI solution.

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