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Improving the Analytical Capabilities of Biomolecular Mass Spectrometry for Proteome and Lipidome Analysis

 

A major goal within the emerging fields of proteomics and lipidomics is the systematic identification, characterization and quantitative analysis of all the biomolecules (e.g., proteins, peptides and lipids), their co- or post-translational modifications, and their specific functional protein-protein or protein-lipid interactions, that are involved in the regulation / deregulation of normal cellular function. The outcome of this research will enable a more complete understanding of the processes that control cellular biochemistry, and ultimately, will enhance the capacity of researchers in the field to identify and validate novel biomarkers of potential therapeutic value that can subsequently be exploited with rational drug design. To date, the application of tandem mass spectrometry (MS/MS) based approaches to generate structural information from the dissociation of intact peptide, protein or lipid ions formed by soft ionization methods (ESI or MALDI), together with the development and application of sophisticated bioinformatic tools for interrogation of the resultant product ion spectra, have provided a powerful analytical platform toward achieving these goals. These efforts have been underpinned by concurrent advances in our understanding of the mechanisms and other factors that influence the gas-phase fragmentation reactions of the various classes of ions of interest. However, despite significant efforts over the past two decades or more, it is fair to say that these studies are still a ‘work in progress’, particularly with respect to understanding the influence of process-induced or post-translational modifications on the observed fragmentation behaviors. Thus, the current generally limited ability to (i) accurately predict in silico the appearance of the product ion spectra resulting from the dissociation of the various precursor ion classes of interest, and (ii) selectively control or direct the gas-phase fragmentation reactions of these ions toward the formation of analytically useful products, has placed significant limitations on the application of mass spectrometry and associated methodologies for comprehensive proteome and lipidome analysis.

 

Research in the Reid laboratory at Michigan State University is, to a large extent, motivated by a desire to address these issues. Specific aspects of this research include:

 

 

(i)                            Understanding the mechanisms and other factors that influence the gas-phase fragmentation reactions of peptide ions containing in vivo or ex vivo modifications

 

Determination of the mechanisms responsible for the gas-phase fragmentation reactions of peptide and protein ions have been the subject of significant interest over the years.  These studies have been critical to understanding the fundamental gas-phase chemistry of these ions, and, within the context of large scale proteomics studies, have underpinned the development of automated MS/MS data analysis programs for sequence ion assignment and subsequent protein identification. The mechanisms for the formation of ‘sequence’ ions, i.e., those resulting from dissociations along the amide backbone to yield complementary b- and y- type product ions, are now relatively well understood. However, a common feature arising from the low energy collision induced dissociation (CID) tandem mass spectrometry (MS/MS) of peptide ions containing many in-vivo or ex-vivo modifications is the competitive formation of dominant ‘non-sequence’ ions resulting from the loss of small molecules (e.g., RSOH, H3PO4) from the modified amino acid side chains. Although the observation of these ‘non-sequence’ ions can be useful in providing diagnostic information regarding the presence of the modified amino acid residue within a peptide, thereby potentially improving the specificity of subsequent database search analysis strategies, their formation at high abundance may ‘suppress’ the formation of desired ‘sequence’ ion information, thereby limiting the utility of ‘de-novo’ analysis strategies or current database search algorithms employed for the identification and characterization of the modified peptide ions. Thus, it is important to determine the conditions, such as charge state and peptide composition (i.e., proton mobility), under which these non-sequence fragmentation pathways are observed as dominant processes. Furthermore, given that MS3 dissociation of abundant non-sequence product ions is often employed to obtain additional sequence information to facilitate further structural characterization, it is also important to determine the mechanisms responsible for their formation, and the structures of the resultant product ions.

 

Beginning with independent research carried out from 2002-2004 at the Ludwig Institute for Cancer Research, and continuing at Michigan State University since August 2004, we have been working toward developing an improved understanding of the mechanisms and other factors (e.g., peptide ion charge state, amino acid composition, site specific amino acid location, or peptide conformation) that influence the formation and relative abundance of ‘sequence’ versus ‘non-sequence’ ions from the fragmentation of peptide ions containing a range of in-vivo (phosphorylation) and ex-vivo (oxidation, alkylation, chemically cross-linked) modifications.

 

Kapp, E.A., Schütz, F., Reid, G.E., Eddes, J.S., Moritz, R.L., O’Hair, R.A.J., Speed, T.P. and Simpson, R.J. (2003) Mining a tandem mass spectrometry database to determine the trends and global factors influencing peptide fragmentation. Anal. Chem. 75: 6251-6264.

 

Hohmann, L.J., Eng, J.K., Gemmill, A., Klimek, J., Vitek, O., Reid, G.E. and Martin D. B.  (2008) Quantification of the Compositional Information Provided by Immonium Ions on a Quadrupole-TOF Mass Spectrometer. Anal. Chem. 80: 5596-5606.

 

Lioe, H., O’Hair, R.A.J. and Reid, G.E. (2004) A Mass Spectrometric and Molecular Orbital Study of H2O Loss from Tryptophan and Oxidized Tryptophan Derivatives. Rapid Commun. Mass Spectrom. 18: 978-988.

 

Lioe, H., O’Hair, R.A.J. and Reid, G.E. (2004) Gas-Phase Reactions of Protonated Tryptophan. J. Am. Soc. Mass Spectrom. 15: 65-76.

 

 

Oxidation

 

Oxidation is one of the more common ex-vivo (i.e, process-induced) modifications encountered during the sequence analysis of proteins by tandem mass spectrometry. We have shown, by statistical analysis of a large database of methionine sulfoxide containing peptide product ion spectra indicated that the structurally diagnostic ‘non-sequence ion’ neutral loss of methane sulfenic acid (CH3SOH, 64Da) from the side chain of methionine sulfoxide residues is the dominant fragmentation process ions under conditions of low proton mobility, i.e., when ionizing proton(s) are sequestered at strongly basic amino acids such as arginine, lysine or histidine. Multistage MS/MS of several methionine sulfoxide containing model ‘tryptic’ peptides, combined with regioselective structural and isotopic labeling, independent solution phase chemical synthesis of proposed gas-phase product ions and ab initio molecular orbital calculations, indicated that the pathway for this loss proceeded via a ‘charge remote’ cis-elimination mechanism process.

 

Reid, G.E., Roberts, K.D., Kapp, E.A. and Simpson, R.J. (2004) Statistical and Mechanistic Approaches to Understanding the Gas-phase Fragmentation Behaviour of Methionine Sulfoxide Containing Peptides. J. Prot. Res. 3: 751-759.

 

Further insights into the factors controlling the fragmentation behavior of methionine sulfoxide containing peptides have been obtained from the results of a theoretical and experimental study (in collaboration with Professors Scott Gronert (Virginia Commonwealth University) and Richard O’Hair (University of Melbourne)) to determine the proton affinities of methionine sulfoxide and a series of methionine sulfoxide containing model peptide derivatives. These results indicate that oxidation of methionine to methionine sulfoxide results in an increase in proton affinity, and indicated the important role of hydrogen bonding in stabilizing the structures of both neutral and protonated methionine or methionine sulfoxide derivatives. The energetics and dynamics associated with preferential cleavage of the methionine sulfoxide side chain via the loss of CH3SOH (64Da), and preferential cleavage of the amide bond C-terminal to aspartic acid, from model protonated methionine sulfoxide or aspartic acid containing peptides, respectively, have also been examined using energy- and time-resolved surface induced dissociation in a Fourier transform ion-cyclotron resonance mass spectrometer, in a study performed in collaboration with Dr Julia Laskin (Pacific Northwest National Laboratories) and Prof. Richard O’Hair (University of Melbourne).

 

Lioe, H., Laskin, J., Reid, G.E. and O’Hair, R.A.J. (2007) Energetics and Dynamics of the Fragmentation Reactions of Protonated Peptides containing Methionine Sulfoxide or Aspartic Acid via Energy- and Time-Resolved Surface Induced Dissociation. J. Phys. Chem. A. 111: 10580-10588.

 

Lioe, H., O'Hair, R.A.J. Gronert, S., Austin, A. and Reid, G.E. (2007) Experimental and Theoretical proton affinities of Methionine, Methionine sulfoxide and their N- and C-terminal derivatives. Int. J. Mass Spectrom. 267: 220-232.

 

Other studies have also been carried out to examine the mechanisms responsible for the ‘non-sequence’ fragmentation reactions of S-alkyl cysteine sulfoxide containing peptides prepared by reaction with the common alkylating reagents iodomethane, iodoacetamide, iodoacetic acid, acrylamide or 4-vinylpyridine, then followed by oxidation with hydrogen peroxide, using multistage tandem mass spectrometry, hydrogen/deuterium exchange and molecular orbital calculations (at the B3LYP/6-31+G(d,p) level of theory). Consistent with earlier reports in the literature, CID-MS/MS of the S-alkyl cysteine sulfoxide-containing peptide ions results in the dominant ‘non-sequence’ neutral loss of an alkyl sulfenic acid (XSOH) from the modified cysteine side chains under conditions of low proton mobility, irrespective of the alkylating reagent employed. However, the mechanisms responsible for this loss had not previously been determined. Dissociation of uniformly deuterated peptide precursor ions was employed to determine that the mechanism for loss of alkyl sulfenic acid in each case occurred via a ‘charge-remote’ five-centered cis-1,2 elimination reaction to yield a dehydroalanine containing product ion.  Similarly, the charge state dependence to the mechanisms and product ion structures for the losses of CO2, CO2+H2O and CO2+CH2O from S-carboxymethyl cysteine sulfoxide-containing peptides, and for the losses of CH2CHCONH2 and CH2CHC5H4N, respectively from S-amidoethyl and S-pyridylethyl cysteine sulfoxide-containing peptide ions have also been determined. The results from these studies indicate that both the proton mobility of the peptide precursor ion and the nature of the S-alkyl substituent have a significant influence on the abundances and charge states of the product ions resulting from the various competing fragmentation pathways.

 

Froelich J.M. and Reid, G.E. (2007) Mechanisms for the Proton Mobility Dependant Gas-Phase Fragmentation Reactions of S-alkyl Cysteine Sulfoxide-containing Peptide Ions. J. Am. Soc. Mass Spectrom. 18: 1690-1705.

 

We have also directed efforts toward determining the conditions for selectively controlling oxidative peptide modifications prior to their analysis by tandem mass spectrometry, and to evaluate the effect of ‘non-sequence’ fragmentations resulting from oxidative modifications on the efficacy of database search algorithms for automated peptide identification and characterization. The origin of increased oxidation levels were found to be predominantly associated with the extensive ex vivo sample handling steps required for gel electrophoresis and/or in-gel proteolytic digestion of proteins prior to analysis by mass spectrometry. Subsequently, conditions for deliberately controlling the oxidation state (either oxidation or reduction) of these peptides have been determined. Quantitative analysis of the product ion abundances within the spectra obtained from the fragmentation of a series of methionine sulfoxide or S-alkyl cysteine sulfoxide containing peptides clearly indicates that an increase in the abundance of the ‘non-sequence’ product ions corresponding to the characteristic ‘non-sequence’ side chain neutral loss of RSOH from these peptides results in a corresponding decrease in the magnitude of the database search scores, and in some cases, results in an inability to identify the peptide by database search methods.

 

Froelich, J.M. and Reid, G.E. (2008). The Origin and Control of Ex Vivo Oxidative Peptide Modifications Prior to Mass Spectrometry Analysis. Proteomics. 8: 1334-1345.

 

 

Phosphorylation

 

The development of strategies directed toward comprehensive analysis of the phosphoproteome have undoubtedly been facilitated by recent advances in the application of ion trap tandem mass spectrometry-based techniques for routine phosphopeptide identification. However, when multiple potential sites of phosphorylation exist within a phosphorylated peptide sequence, unambiguous characterization of the site of phosphorylation remains a significant challenge.  Recently, we have carried out a series of fundamental studies to systematically determine the mechanisms and other factors that influence the multistage gas-phase fragmentation reactions of phosphoserine and phosphothreonine containing peptides. From this study, it was found that the magnitude of product ions formed via the neutral loss of 98 Da (typically assigned as phosphoric acid (H3PO4)) were highly dependent on the proton mobility of the precursor ion. A mechanism for this loss, involving a ‘charge remote’ pathway had previously been accepted in the literature for a period of over 10 years. However, using regioselective and uniformly deuterium labeled peptides, as well as MS3 of the initial [M+nH-98]n+ product ions, our data clearly indicated that ‘charge-directed’ mechanisms were responsible for the observed fragmentation behavior. Furthermore, the observation of product ions corresponding to the loss of formaldehyde (CH2O, 30 Da or CD2O, 32 Da) or acetaldehyde (CH3CHO, 44 Da) upon MS3 dissociation of the [M+nH-98]n+ product ions from phosphoserine- and phosphothreonine-containing peptide ions, respectively, provided direct experimental evidence for an SN2 neighboring group participation reaction, resulting in the formation of a cyclic product ion. It was initially hoped that these ‘diagnostic’ MS3 product ions could be employed to provide additional information to facilitate the characterization of phosphopeptides containing multiple potential phosphorylation sites. However, upon examining the collision CID-MS/MS and -MS3 fragmentation reactions of a series of independently synthesized phospho-serine, -threonine and -tyrosine peptides containing multiple potential phosphorylation sites in a linear quadrupole ion trap, it was unexpectedly found that 45% of the peptides gave rise to MS/MS and/or MS3 product ions that indicated the site of phosphorylation was located at the ‘incorrect’ position. The origin of the ‘erroneous’ MS/MS product ions were found to arise from an initial gas-phase transfer of a phosphate group from the phosphorylated residue to an unmodified hydroxyl-containing amino acid residue upon CID-MS/MS, but prior to peptide dissociation. The propensity for this rearrangement was found to be highly dependant on the precursor ion charge state and amino acid composition (i.e, proton mobility) of the peptide, and was observed predominantly for peptides under ‘non-mobile’ or ‘partially-mobile’ protonation conditions. ‘Erroneous’ MS3 product ions could be formed due to competing fragmentation reactions for the neutral loss of 98 Da from these precursor ions (i.e., the loss of H3PO4 versus the combined losses of HPO3 and H2O), indicating that CID-MS3 of [M+nH-98]n+ ions may not be used for unambiguous phosphorylation site localization. Importantly, the observation of these rearrangement reactions, and/or the lack of product ions that provide definitive evidence for the correct site of phosporylation, was found to limit the ability to unambiguously assign the correct site of phosphorylation to only 36% of the peptides.

 

Palumbo, A.M., Tepe, J.J. and Reid, G.E. (2008) Mechanistic Insights into the Multistage Gas-Phase Fragmentation Behavior of Phosphoserine- and Phosphothreonine-containing Peptides. J. Proteome Res. 7: 771-779.

 

Palumbo, A.M and Reid, G.E. (2008) Evaluation of Gas-Phase Rearrangement and Competing Fragmentation Reactions on Protein Phosphorylation Site Assignment using CID-MS/MS and MS3. Anal. Chem. In Press.

 

Dunn, J.D., Igrisan, E.A., Palumbo, A.M., Reid, G.E. and Bruening, M.L. (2008) Phosphopeptide Enrichment Using MALDI Plates Modified with High-capacity Polymer Brushes. Anal. Chem. 80: 5727-5735.

 

Froelich, J.M. and Reid, G.E. (2008) The Effect of Post-translational and Process-induced Modifications on the Multistage Gas-Phase Fragmentation Reactions of Protonated Peptide Ions. Combinatorial Chemistry and High Throughput Screening. In Press.

 

Taken together, the above studies clearly demonstrate the role of peptide modifications on fragmentation behavior, and highlights the need to develop improved database search methods for peptide identification and characterization that incorporate the fragmentation ‘rules’ arising from this work.

 

 

(ii)                           Chemical Methods and Tandem Mass Spectrometry Strategies for ‘Targeted’ Proteome Analysis

 

As a direct result of the improved mechanistic understanding of ‘non-sequence’ ion peptide fragmentation reactions obtained above, we have developed a novel strategy for selective protein identification and differential quantitative analysis, termed 'Selected Extraction of  Labelled Entities by Charge derivatization and Tandem mass spectrometry' (SELECT). This strategy involves the introduction of a 'fixed-charge' sulfonium ion to peptides or proteins containing certain structural features (e.g., the side chains of selected amino acids). MS/MS of these peptide ions results in exclusive loss of the derivatized side chain and the formation of a single characteristic product ion, independently of the peptide ion charge state or amino acid composition.  Thus, fixed charge containing peptide ions may be selectively identified from complex mixtures by, for example, automated selective neutral loss or precursor ion scan mode MS/MS methods, without requirement for purification or otherwise enrichment prior to analysis, and with an increase in selectively and sensitivity of several orders of magnitude over existing MS based approaches. Further structural interrogation of identified peptide ions is readily achieved by subjecting the characteristic MS/MS product ion to multistage MS/MS (MS3) in a quadrupole ion trap mass spectrometer, or by energy resolved 'pseudo' MS3 in a triple quadrupole mass spectrometer The general principles underlying this fixed charge derivatization approach have been demonstrated by MS/MS, MS3 and 'pseudo' MS3 analysis of side chain fixed-charge sulfonium ion derivatives of peptides containing methionine and cysteine. Furthermore, the incorporation of 'light' and ‘heavy’ isotopically encoded labels into the fixed-charge derivatives has also enabled the application of this approach to the quantitative analysis of differential protein expression, via measurement of the relative abundances of the neutral loss product ions generated by dissociation of the light and heavy labelled peptide ions.

 

Reid, G.E., Roberts, K.D., Simpson, R.J., O'Hair, R.A.J. (2005) Selective Identification and Quantitative Analysis of Methionine Containing Peptides by Charge derivatization and Tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 16: 1131-1150.

 

Froelich, J.M., Kaplinghat, S. and Reid, G.E. (2008) Automated Neutral Loss and Data Dependent Energy Resolved “Pseudo MS3” for the Targeted Identification, Characterization and Quantitative Analysis of Methionine-Containing Peptides. Eur. J. Mass Spectrom. 14: 219-229.

 

Roberts, K.D. and Reid, G.E. (2007) Leaving Group Effects on the Selectivity of the Gas-Phase Fragmentation Reactions of Side Chain Fixed Charge Containing Peptide Ions. J. Mass Spectrom. 42: 187-198.

 

Froelich, J.M., Lu, Y. and Reid, G.E. (2008) Chemical Derivatization and Multistage Tandem Mass Spectrometry for Protein Structural Characterization. In: Practical Aspects of Trapped Ion Mass Spectrometry. Vol. 5: Applications. (R.E. March and J.F.J. Todd. Ed), CRC Press. In Press.

 

The mechanisms responsible for the fragmentation of 'fixed-charge' phenacylsulfonium ion derivatized methionine containing peptide ions have been determined, by experimental evidence obtained from multistage dissociation of a regioselectively deuterated methionine derivatized sulfonium ion containing tryptic peptide, as well as by molecular orbital calculations performed on a simple peptide model, to occur via SN2 reactions involving the N-and C-terminal amide bonds adjacent to the methionine side chain, resulting in the formation of stable cyclic five- and six-membered iminohydrofuran and oxazine product ions, respectively. These studies further indicated that the rings formed via these neighboring group reactions are stable to further dissociation by MS3. The effect of various para-substituents on the multistage (MS/MS and MS3) fragmentation reactions of the methionine side chain fixed charge phenacylsulfonium ion containing peptides have also been examined. Loss of the methylphenacylsulfide side chain fragment as neutral versus protonated species were observed to be dependent on the proton mobility of the precursor ion and the identity of the para-substituent. The log of the ratio of neutral versus charged losses of the derivatized side chain were found to exhibit a linear dependence on the proton affinity of the side chain fragmentation product, as well as the proton affinities of the peptide product ions.

 

Amunugama, M., Roberts, K.D. and Reid, G.E. (2006) Mechanisms for the Selective Gas-phase Fragmentation Reactions of Methionine Side Chain Fixed Charge Sulfonium Ion Containing Peptides. J. Am. Soc. Mass Spectrom. 17: 1631-1642.

 

Sierakowski, J., Amunugama, M., Roberts, K.D and Reid, G.E. (2007) Substituent Effects on the Gas-Phase Fragmentation Reactions of Sulfonium Ion Containing Peptides. Rapid Commun. Mass Spectrom. 21: 1230-1238.

 

More recently, this sulfonium ion derivatization approach has also been extended toward the development of an improved MS/MS based analysis strategy for the characterization of protein structure, protein folding and protein-protein interactions. Chemical cross-linking combined with proteolytic digestion and mass spectrometry (MS) is a promising approach to provide inter- and intramolecular distance constraints for the structural characterization of protein topologies and functional multi-protein complexes. Despite the relative straightforwardness of these methodologies, the identification and characterization of cross-linked proteins presents a significant analytical challenge, due to the complexity of the resultant peptide mixtures, as well as the array of inter-, intra- or “dead-end”- cross-linked peptides that may be generated from a single cross-linking experiment. To address these issues, we recently described the synthesis, characterization and initial evaluation of a novel “fixed charge” sulfonium ion containing cross-linking reagent, S-methyl 5,5’-thiodipentanoylhydroxysuccinimide. The peptide products obtained by reaction with this reagent are all shown to fragment exclusively via facile cleavage of the C-S bond directly adjacent to the fixed charge during CID-MS/MS, resulting in the formation of characteristic products ions that enable the presence and type (i.e., inter-, intra- or dead-end) of the cross-linked products to be readily determined, independently of the “proton mobility” of the precursor ion. Subsequent isolation and dissociation of these products by MS3 provides additional structural information required for identification of the peptide sequences involved in the cross-linking reactions, as well as for characterization of the specific site(s) at which cross-linking has occurred. The specificity of these gas-phase fragmentation reactions, as well as the solubility and stability of the cross-linking reagent under aqueous conditions, suggest that this strategy holds great promise for use in future studies aimed at the structural analysis of large proteins or multi-protein assemblies.

 

Lu, Y., Tanasova, M., Borhan, B. and Reid, G.E. (2008) An Ionic Reagent for Controlling the Gas-Phase Fragmentation Reactions of Cross-Linked Peptides. Anal. Chem. In Press.

 

 

(iii)    Top Down Protein Characterization

 

The key advantage of ‘top-down’ approaches to protein identification and characterization, involving the dissociation of intact protein ions rather than their 'bottom-up' proteolytically derived peptides, is that the entire sequence of the protein is available for interrogation, thereby enabling protein identification to be potentially be achieved in a single step, including the characterization of any co- or post-translational modifications.

 

Reid, G.E. Characterization of Proteins by Mass Spectrometry. (2003) In: 'Purifiying Proteins: A Laboratory Manual' (Simpson, R.J. Ed.) Cold Spring Harbor Laboratory Press. Chapter 21, pp 489-516.

 

We have carried out a study to determine the role of the active site residues within the Staphylococcus aureus Dihydroneopterin aldolase (SaDHNA) enzyme by ‘top-down’ tandem mass spectrometry methods. In this study, the gas-phase fragmentation reactions of a series of active-site directed mutagenesis products of SaDHNA have been examined in order to (i) evaluate the utility of a linear quadrupole ion trap mass spectrometer for routine 'top-down' recombinant protein characterization, (ii) examine the precursor ion charge state dependence on the gas-phase fragmentation behavior of these proteins, and (iii) confirm the mutation sites. Although proving to be successful for the majority of the protein mutants examined, this work highlighted the need for further studies to characterize the charge state, sequence and structural dependence to the fragmentation behavior of multiply protonated intact protein ions, and will form the basis for further efforts in our laboratory in the future.

 

Scherperel, G., Yan, H., Wang, Y. and Reid, G.E. (2006) Characterization of dihydroneopterin aldolase site directed mutagenesis products from Staphylococcus Aureus by 'top down' multistage tandem mass spectrometry in a linear quadrupole ion trap. The Analyst. 131: 291-302.

 

This work has been extended toward the analysis of the structure-function role that a conserved active-site Y61 residue plays within the DHNA sequence, by the identification of a novel product arising from the reaction of the Y61F mutant protein with the enzyme substrate 7,8-dihydroneopterin (DHNP). This result led to the proposal that the active site Y61F mutant acts as an oxygenase rather than an aldolase.

 

Wang, Y., Scherperel, G., Roberts, K.D., Jones, A.D., Reid, G.E. and Yan, H. (2006) A Point Mutation Converts Dihydroneopterin Aldolase to a Cofactor-Independent Oxygenase. J. Am. Chem. Soc. 128: 13216-13223.

 

A short ‘educational’ overview of the current strategies employed for top-down protein characterization, and the key technical challenges and solutions associated with their implementation on a range of mass spectrometry instrument platforms, was published as an invited review article to the Education i-section of The Analyst.

 

Scherperel, G. and Reid, G.E. (2007) Emerging methods in Proteomics: Multistage Tandem Mass Spectrometry for Top-down Protein Characterization. The Analyst. 132: 500 – 506.

 

 

(iv)    Identification and Characterization of Lipids by Multistage Tandem Mass Spectrometry.

 

The identification of biomarkers that enable the early detection and prognosis of disease, or that facilitate measurement of the efficacy of response to a specific therapeutic intervention, holds great promise in advancing the capabilities of individualized medicine.  Recent technological advances in mass spectrometry have enabled large scale biomarker discovery efforts to be initiated, including in the field of lipidomics, without prior requirement for detailed insights into the mechanisms responsible for the disease. Lipids are a diverse group of compounds, including fatty acyls, sterols, glycerolipids, glycerophospholipids and sphingolipids, that play key biological roles as the main structural component of cell membranes, in energy storage and metabolism, and in cell signaling. A large number of studies have demonstrated that the disruption of lipid metabolism or signaling pathways can play a key role in the onset and progression of human disease, including diabetes, diabetic complications and cancer. In some instances, monitoring changes in the abundance of particular lipid species between diseased and normal tissue has been shown to provide a greater ability to detect the disease at an earlier stage of progression compared to conventional protein biomarkers.   Thus, a comprehensive comparative analysis of changes in individual lipids, or lipid profiles, that are observed between normal and diseased cells, tissues or organs, and correlation of the changes observed in the end organs of the disease with those occurring in blood fractions (e.g., plasma, erythrocytes or leukocytes), may enable the identification and characterization of lipids that can serve as effective biomarker signatures of the disease.

 

A necessary prerequisite to the quantitative mass spectrometry based characterization of changes in lipid profiles that occur as a function of the onset and progression of disease in a particular cell, tissue or organ, is to first develop effective strategies for identification of the individual lipid components that may be present, without need for extensive sample handling or fractionation. To address this requirement, we have initiated a series of studies to systematically examine the gas-phase fragmentation reactions of various lipid classes that may be observed in the mass spectrometer in various ionic forms, from within a complex crude lipid extracts

 

Zhang, X., and Reid, G.E. (2006) Multistage Tandem Mass Spectrometry of Anionic Phosphatidylcholine Lipid Adducts Reveals Novel Dissociation Pathways. Int. J. Mass Spectrom. 252: 242-255.

 

Zhang, X., Ferguson-Miller, S.M. and Reid, G.E. (2009) Characterization of Ornithine and Glutamine Lipids Extracted from Cell Membranes of Rhodobacter sphaeroides. J. Am. Soc. Mass Spectrom. In Press. doi:10.1016/j.jasms.2008.08.017

 

The results from these and related fundamental gas-phase lipid ion chemistry studies are now being applied toward the development of comprehensive ‘shotgun’ MS/MS based approaches using multiple lipid-class specific precursor ion and neutral loss scan mode experiments in a triple quadrupole mass spectrometer, or multistage (MSn)  tandem mass spectrometry in a quadrupole ion trap mass spectrometer, to (i) identify and quantify the role of integral lipids in the structure and function of the membrane protein complex, cytochrome c oxidase (in collaboration with Prof. Shelagh Ferguson-Miller, Dept. Biochem. and Mol. Biol. MSU), and (ii) to identify and quantify the temporal changes in lipid profiles associated with the onset of diabetic retinopathy in rat models of type 1 diabetes (in collaboration with Prof. Julia Busik, Dept. Physiol. MSU) and the development of hepatocellular carcinoma in a transgenic mouse model (in collaboration with Prof. Rheal Towner, Oklahoma Medical Research Foundation, Oklahoma).

 

Griffitts, J., Tesiram, Y., Reid, G.E., Saunders, D., Floyd, R. and Towner, R. (2009) In Vivo magnetic resonance spectroscopy (MRS) assessment of altered fatty acyl unsaturation in liver tumor formation of a TGFα/c-myc transgenic mouse model. J. Lipid. Res. In Press.

 

 

 


This page maintained by Gavin Reid. Last Updated: October 18th, 2008