Advances in quantitative proteomics

Abstract

Large-scale protein quantification has become a major proteomics application in many areas of biological and medical research. During the past years, different techniques have been developed, including gel-based such as differential in-gel electrophoresis (DIGE) and liquid chromatography-based such as isotope labeling and label-free quantification. These quantitative proteomics tools hold significant promise for biomarker discovery, diagnostic and therapeutic applications. They are also important for research in functional genomics and systems biology towards basic understanding of molecular networks and pathway interactions. In this review, we summarize current technologies in quantitative proteomics and discuss recent applications of the technologies.

Keywords

two dimensional gel / liquid chromatography-mass spectrometry (LC-MS) / stable isotope / quantification / application

References

[1] Alban A, David S O, Bjorkesten L, Andersson C, Sloge E, Lewis S, Currie I (2003). A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics, 3(1): 36-44

[2] America A H, Cordewener J H (2008). Comparative LC-MS: a landscape of peaks and valleys. Proteomics, 8(4): 731-749

[4] Anderson K S, Ramachandran N, Wong J, Raphael J V, Hainsworth E, Demirkan G, Cramer D, Aronzon D, Hodi F S, Harris L, Logvinenko T, LaBaer J (2008). Application of protein microarrays for multiplexed detection of antibodies to tumor antigens in breast cancer. J Proteome Res, 7(4): 1490-1499

[3] Anderson L, Hunter C L (2006). Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol Cell Proteomics, 5(4): 573-588

[5] Asara J M, Christofk H R, Freimark L M, Cantley L C (2008). A label-free quantification method by MS/MS TIC compared to SILAC and spectral counting in a proteomics screen. Proteomics, 8(5): 994-999

[6] Bertone P, Snyder M (2005). Advances in functional protein microarray technology. FEBS J, 272(21): 5400-5411

[7] Blackburn J M, Hart D J (2005). Fabrication of protein function microarrays for systems-oriented proteomic analysis. Methods Mol Biol, 310: 197-216

[8] Bosch G, Skovran E, Xia Q, Wang T, Taub F, Miller J A, Lidstrom M E, Hackett M (2008). Comprehensive proteomics of Methylobacterium extorquens AM1 metabolism under single carbon and nonmethylotrophic conditions. Proteomics, 8(17): 3494-3505

[9] Casati P, Zhang X, Burlingame A L, Walbot V (2005). Analysis of leaf proteome after UV-B irradiation in maize lines differing in sensitivity. Mol Cell Proteomics, 4(11): 1673-1685

[9] Chen S, Harmon A (2006). Advances in plant proteomics. Proteomics, 6(20): 5504–5516

[10] Cheng F Y, Blackburn K, Lin Y M, Goshe M B, Williamson J D (2009). Absolute protein quantification by LC/MS(^E) for global analysis of salicylic acid-induced plant protein secretion responses. J Proteome Res, 8(1): 82-93

[11] Cravatt B F, Simon G M, Yates J R 3rd (2007). The biological impact of mass-spectrometry-based proteomics. Nature, 450(7172): 991-1000

[12] Cretich M, Damin F, Pirri G, Chiari M (2006). Protein and peptide arrays: recent trends and new directions. Biomol Eng, 23(2-3): 77-88

[13] Dayon L, Hainard A, Licker V, Turck N, Kuhn K, Hochstrasser D F, Burkhard P R, Sanchez J C (2008). Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags. Anal Chem, 80(8): 2921-2931

[14] DeSouza L V, Taylor A M, Li W, Minkoff M S, Romaschin A D, Colgan T J, Siu K W (2008). Multiple reaction monitoring of mTRAQ-labeled peptides enables absolute quantification of endogenous levels of a potential cancer marker in cancerous and normal endometrial tissues. J Proteome Res, 7(8): 3525-3534

[15] Fu C, Hu J, Liu T, Ago T, Sadoshima J, Li H (2008). Quantitative analysis of redox-sensitive proteome with DIGE and ICAT. J Proteome Res, 7(9): 3789-3802

[16] Gevaert K, Impens F, Ghesquière B, Van Damme P, Lambrechts A, Vandekerckhove J (2008). Stable isotopic labeling in proteomics. Proteomics, 8(23-24): 4873-4885

[17] Gharbi S, Gaffney P, Yang A, Zvelebil M J, Cramer R, Waterfield M D, Timms J F (2002). Evaluation of two-dimensional differential gel electrophoresis for proteomic expression analysis of a model breast cancer cell system. Mol Cell Proteomics, 1(2): 91-98

[18] Görg A, Weiss W, Dunn M J (2004). Current two-dimensional electrophoresis technology for proteomics. Proteomics, 4(12): 3665-3685

[19] Graumann J, Hubner N C, Kim J B, Ko K, Moser M, Kumar C, Cox J, Schöler H, Mann M (2008). Stable isotope labeling by amino acids in cell culture (SILAC) and proteome quantitation of mouse embryonic stem cells to a depth of 5,111 proteins. Mol Cell Proteomics, 7(4): 672-683

[20] Greengauz-Roberts O, Stöppler H, Nomura S, Yamaguchi H, Goldenring J R, Podolsky R H, Lee J R, Dynan W S (2005). Saturation labeling with cysteine-reactive cyanine fluorescent dyes provides increased sensitivity for protein expression profiling of laser-microdissected clinical specimens. Proteomics, 5(7): 1746-1757

[21] Gruhler A, Olsen J V, Mohammed S, Mortensen P, Faergeman N J, Mann M, Jensen O N (2005). Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol Cell Proteomics, 4: 310-327

[22] Gu S, Pan S, Bradbury E M, Chen X (2003). Precise peptide sequencing and protein quantification in the human proteome through in vivo lysine-specific mass tagging. J Am Soc Mass Spectrom, 14(1): 1-7

[23] Gygi S P, Rist B, Gerber S A, Turecek F, Gelb M H, Aebersold R (1999). Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol, 17(10): 994-999

[24] Gygi S P, Corthals G L, Zhang Y, Rochon Y, Aebersold R (2000). Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proc Natl Acad Sci U S A, 97(17): 9390-9395

[25] Hamelinck D, Zhou H, Li L, Verweij C, Dillon D, Feng Z, Costa J, Haab B B (2005). Optimized normalization for antibody microarrays and application to serum-protein profiling. Mol Cell Proteomics, 4(6): 773-784

[26] Hansen K C, Schmitt-Ulms G, Chalkley R J, Hirsch J, Baldwin M A, Burlingame A L (2003). Mass spectrometric analysis of protein mixtures at low levels using cleavable ¹³C-isotope-coded affinity tag and multidimensional chromatography. Mol Cell Proteomics, 2(5): 299-314

[27] Hjernø K, Alm R, Canbäck B, Matthiesen R, Trajkovski K, Björk L, Roepstorff P, Emanuelsson C (2006). Down-regulation of the strawberry Bet v 1-homologous allergen in concert with the flavonoid biosynthesis pathway in colorless strawberry mutant. Proteomics, 6(5): 1574-1587

[28] Hurd T R, Prime T A, Harbour M E, Lilley K S, Murphy M P (2007). Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling. J Biol Chem, 282(30): 22040-22051

[29] Iliuk A, Galan J, Tao W A (2009). Playing tag with quantitative proteomics. Anal Bioanal Chem, 393(2): 503-513

[30] Karp N A, Spencer M, Lindsay H, O’Dell K, Lilley K S (2005). Impact of replicate types on proteomic expression analysis. J Proteome Res, 4(5): 1867-1871

[31] Kitteringham N R, Jenkins R E, Lane C S, Elliott V L, Park B K (2009). Multiple reaction monitoring for quantitative biomarker analysis in proteomics and metabolomics. J Chromatogr B Analyt Technol Biomed Life Sci, 877(13): 1229-1239

[32] Krüger M, Moser M, Ussar S, Thievessen I, Luber C A, Forner F, Schmidt S, Zanivan S, Fässler R, Mann M (2008). SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell, 134(2): 353-364

[33] Langenfeld E, Zanger U M, Jung K, Meyer H E, Marcus K (2009). Mass spectrometry-based absolute quantification of microsomal cytochrome P450 2D6 in human liver. Proteomics, 9(9): 2313-2323

[34] Letarte S, Brusniak M Y, Campbell D, Eddes J, Kemp C J, Lau H, Mueller L, Schmidt A, Shannon P, Kelly-Spratt K S, Vitek O, Zhang H, Aebersold R, Watts J D (2008). Differential plasma glycoproteome of p19ARF skin cancer mouse model using the corra label-free LC-MS proteomics platform. Clin Proteomics, 4(3-4): 105-116

[35] Li X J, Yi E C, Kemp C J, Zhang H, Aebersold R (2005). A software suite for the generation and comparison of peptide arrays from sets of data collected by liquid chromatography-mass spectrometry. Mol Cell Proteomics, 4(9): 1328-1340

[36] Liu H, Sadygov R G, Yates J R 3rd (2004). A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem, 76(14): 4193-4201

[37] Lucitt M B, Price T S, Pizarro A, Wu W, Yocum A K, Seiler C, Pack M A, Blair I A, Fitzgerald G A, Grosser T (2008). Analysis of the zebrafish proteome during embryonic development. Mol Cell Proteomics, 7(5): 981-994

[38] Neubert H, Bonnert T P, Rumpel K, Hunt B T, Henle E S, James I T (2008). Label-free detection of differential protein expression by LC/MALDI mass spectrometry. J Proteome Res, 7(6): 2270-2279

[39] Oda Y, Huang K, Cross F R, Cowburn D, Chait B T (1999). Accurate quantitation of protein expression and site-specific phosphorylation. Proc Natl Acad Sci U S A, 96(12): 6591-6596

[40] Old W M, Meyer-Arendt K, Aveline-Wolf L, Pierce K G, Mendoza A, Sevinsky J R, Resing K A, Ahn N G (2005). Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics, 4(10): 1487-1502

[42] Ong S E, Blagoev B, Kratchmarova I, Kristensen D B, Steen H, Pandey A, Mann M (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics, 1(5): 376-386

[43] Ong S E, Kratchmarova I, Mann M (2003). Properties of ¹³C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC). J Proteome Res, 2(2): 173-181

[41] Ong S E, Mann M (2006). A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc, 1(6): 2650-2660

[44] Ong S E, Mittler G, Mann M (2004). Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat Methods, 1(2): 119-126

[45] Orenes-Piñero E, Cortón M, González-Peramato P, Algaba F, Casal I, Serrano A, Sánchez-Carbayo M (2007). Searching urinary tumor markers for bladder cancer using a two-dimensional differential gel electrophoresis (2D-DIGE) approach. J Proteome Res, 6(11): 4440-4448

[46] Ow S Y, Cardona T, Taton A, Magnuson A, Lindblad P, Stensjö K, Wright P C (2008). Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. J Proteome Res, 7(4): 1615-1628

[47] Patel V J, Thalassinos K, Slade S E, Connolly J B, Crombie A, Murrell J C, Scrivens J H (2009). A comparison of labeling and label-free mass spectrometry-based proteomics approaches. J Proteome Res, 8(7): 3752-3759

[48] Ptacek J, Devgan G, Michaud G, Zhu H, Zhu X, Fasolo J, Guo H, Jona G, Breitkreutz A, Sopko R, McCartney R R, Schmidt M C, Rachidi N, Lee S J, Mah A S, Meng L, Stark M J, Stern D F, De Virgilio C, Tyers M, Andrews B, Gerstein M, Schweitzer B, Predki P F, Snyder M (2005). Global analysis of protein phosphorylation in yeast. Nature, 438(7068): 679-684

[49] Rajcevic U, Petersen K, Knol J C, Loos M, Bougnaud S, Klychnikov O, Li K W, Pham T V, Wang J, Miletic H, Peng Z, Bjerkvig R, Jimenez C R, Niclou S P (2009). iTRAQ-based proteomics profiling reveals increased metabolic activity and cellular cross-talk in angiogenic compared with invasive glioblastoma phenotype. Mol Cell Proteomics, 8(11): 2595-2612

[50] Ramachandran N, Larson D N, Stark P R, Hainsworth E, LaBaer J (2005). Emerging tools for real-time label-free detection of interactions on functional protein microarrays. FEBS J, 272(21): 5412-5425

[51] Rao P V, Reddy A P, Lu X, Dasari S, Krishnaprasad A, Biggs E, Roberts C T, Nagalla S R (2009). Proteomic identification of salivary biomarkers of type-2 diabetes. J Proteome Res, 8(1): 239-245

[52] Ross P L, Huang Y N, Marchese J N, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin D J (2004). Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics, 3(12): 1154-1169

[53] Shaw J, Rowlinson R, Nickson J, Stone T, Sweet A, Williams K, Tonge R (2003). Evaluation of saturation labelling two-dimensional difference gel electrophoresis fluorescent dyes. Proteomics, 3(7): 1181-1195

[54] Shevchenko A, Jensen O N, Podtelejnikov A V, Sagliocco F, Wilm M, Vorm O, Mortensen P, Shevchenko A, Boucherie H, Mann M (1996). Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci U S A, 93(25): 14440-14445

[55] Shui W, Gilmore S A, Sheu L, Liu J, Keasling J D, Bertozzi C R (2009). Quantitative proteomic profiling of host-pathogen interactions: the macrophage response to Mycobacterium tuberculosis lipids. J Proteome Res, 8(1): 282-289

[56] Silva J C, Denny R, Dorschel C, Gorenstein M V, Li G Z, Richardson K, Wall D, Geromanos S J (2006). Simultaneous qualitative and quantitative analysis of the Escherichia coli proteome: a sweet tale. Mol Cell Proteomics, 5(4): 589-607

[57] Tang W, Deng Z, Oses-Prieto J A, Suzuki N, Zhu S, Zhang X, Burlingame A L, Wang Z Y (2008). Proteomics studies of brassinosteroid signal transduction using prefractionation and two-dimensional DIGE. Mol Cell Proteomics, 7(4): 728-738

[58] Thelen J J, Peck S C (2007). Quantitative proteomics in plants: choices in abundance. Plant Cell, 19(11): 3339-3346

[59] Thompson A, Schäfer J, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed A K, Hamon C (2003). Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem, 75(8): 1895-1904

[60] Tonge R, Shaw J, Middleton B, Rowlinson R, Rayner S, Young J, Pognan F, Hawkins E, Currie I, Davison M (2001). Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics, 1(3): 377-396

[61] Unlü M, Morgan M E, Minden J S (1997). Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis, 18(11): 2071-2077

[62] Unwin R D, Griffiths J R, Leverentz M K, Grallert A, Hagan I M, Whetton A D (2005). Multiple reaction monitoring to identify sites of protein phosphorylation with high sensitivity. Mol Cell Proteomics, 4(8): 1134-1144

[63] Wang Y, Ao X, Vuong H, Konanur M, Miller F R, Goodison S, Lubman D M (2008). Membrane glycoproteins associated with breast tumor cell progression identified by a lectin affinity approach. J Proteome Res, 7(10): 4313-4325

[64] Whiteaker J R, Zhang H, Zhao L, Wang P, Kelly-Spratt K S, Ivey R G, Piening B D, Feng L C, Kasarda E, Gurley K E, Eng J K, Chodosh L A, Kemp C J, McIntosh M W, Paulovich A G (2007). Integrated pipeline for mass spectrometry-based discovery and confirmation of biomarkers demonstrated in a mouse model of breast cancer. J Proteome Res, 6(10): 3962-3975

[65] Zhang R, Regnier F E (2002). Minimizing resolution of isotopically coded peptides in comparative proteomics. J Proteome Res, 1(2): 139-147

[66] Zhang B, VerBerkmoes N C, Langston M A, Uberbacher E, Hettich R L, Samatova N F (2006). Detecting differential and correlated protein expression in label-free shotgun proteomics. J Proteome Res, 5: 2909-2918

[68] Zhou F, Galan J, Geahlen R L, Tao W A (2007). A novel quantitative proteomics strategy to study phosphorylation-dependent peptide-protein interactions. J Proteome Res, 6(1): 133-140

[67] Zhou H, Ranish J A, Watts J D, Aebersold R (2002). Quantitative proteome analysis by solid-phase isotope tagging and mass spectrometry. Nat Biotechnol, 20(5): 512-515

[69] Zhu M, Simons B, Zhu N, Oppenheimer D G, Chen S (2010). Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging. J Proteomics, 73(4): 790-805

[70] Zybailov B, Friso G, Kim J, Rudella A, Rodríguez V R, Asakura Y, Sun Q, van Wijk K J (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol Cell Proteomics, 8(8): 1789-1810

Acknowledgements

The proteomics work in our collaborative orted by funding from the University of Florida, the National Science Foundation (MCB 0818051,CAREER 0845162onal Institute of Health (1S10RR025418-01) of the USA to S CHEN, and the National Science Foundation of China (No. 30871566) and the Natural Science Foundation of Heilongjiang Province (No. C2007-37) to H LI.

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