Challenges in plasma membrane phosphoproteomics

Expert Review of Proteomics

Volumn 8, Issue 4, 2011, Pages 483-494

  Orsburn, Benjamin C ^a   Stockwin, Luke H ^a   Newton, Dianne L ^a  

^a SAIC FREDERICK INC   (United States)

Author keywords

CID; enrichment; ETD; HCD; neutral loss; phosphopeptide; phosphoproteomics; plasma membrane

Indexed keywords

PHOSPHOPEPTIDE;

CELL MEMBRANE; FRAGMENTATION REACTION; HUMAN; MASS SPECTROMETRY; NONHUMAN; PHOSPHOPROTEOMICS; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; SOLUBILIZATION;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; SOLUBILITY;

EID: 80051717802     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/epr.11.40     Document Type: Review

References (94)

1. Macek B, Mann M, Olsen JV. Global and site-specific quantitative phosphoproteomics: Principles and applications. Annu. Rev. Pharmacol. Toxicol. 49, 199-221 (2009).
2. Ding SJ, Qian WJ, Smith RD. Quantitative proteomic approaches for studying phosphotyrosine signaling. Expert Rev. Proteomics 4(1), 13-23 (2007). (Pubitemid 46239469)
3. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature 411(6835), 355-365 (2001). Excellent review on phospho-state regulation and cancer.
4. Thingholm TE, Jensen ON, Larsen MR. Analytical strategies for phosphoproteomics. Proteomics 9(6), 1451-1468 (2009).
5. Beausoleil SA, Jedrychowski M, Schwartz D et al. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl Acad. Sci. USA 101(33), 12130-12135 (2004). (Pubitemid 39145408)
6. Brill LM, Salomon AR, Ficarro SB, Mukherji M, Stettler-Gill M, Peters EC. Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. Anal. Chem. 76(10), 2763-2772 (2004). (Pubitemid 38657701)
7. Li X, Gerber SA, Rudner AD et al. Large-scale phosphorylation analysis of a-factor-arrested Saccharomyces cerevisiae. J. Proteome Res. 6(3), 1190-1197 (2007). (Pubitemid 46480484)
8. Old WM, Shabb JB, Houel S et al. Functional proteomics identifies targets of phosphorylation by B-Raf signaling in melanoma. Mol. Cell 34(1), 115-131 (2009).
9. Olsen JV, Blagoev B, Gnad F et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127(3), 635-648 (2006). (Pubitemid 44647421)
10. Olsen JV, Vermeulen M, Santamaria A et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3(104), ra3 (2010).
11. Wu CC, Yates JR 3rd. The application of mass spectrometry to membrane proteomics. Nat. Biotechnol. 21(3), 262-267 (2003). (Pubitemid 36314809)
12. Yeagle P. The Membranes of Cells. Academic Press, Buffalo, NY, USA (1987).
13. Jain M. Introduction to Biological Membranes. John Wiley and Sons, NY, USA (1988).
14. Navarre C, Degand H, Bennett KL, Crawford JS, Mortz E, Boutry M. Subproteomics: Identification of plasma membrane proteins from the yeast Saccharomyces cerevisiae. Proteomics 2(12), 1706-1714 (2002). (Pubitemid 36015506)
15. Pasquali C, Fialka I, Huber LA. Subcellular fractionation, electromigration analysis and mapping of organelles. J. Chromatogr. B Biomed. Sci. Appl. 722(1-2), 89-102 (1999). (Pubitemid 29142504)
16. Zhang L, Xie J, Wang X et al. Proteomic analysis of mouse liver plasma membrane: Use of differential extraction to enrich hydrophobic membrane proteins. Proteomics 5(17), 4510-4524 (2005). (Pubitemid 41739929)
17. Wisniewski JR. Tools for phospho- and glycoproteomics of plasma membranes. Amino Acids DOI: 10.1007/s00726-010-0796-0798 (2010) (Epub ahead of print).
18. Staubach S, Hanisch FG. Lipid rafts: Signaling and sorting platforms of cells and their roles in cancer. Expert Rev. Proteomics 8(2), 263-277 (2011).
19. Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl Acad. Sci. USA 100(10), 5813-5818 (2003). (Pubitemid 36576890)
20. Olsen JV, Nielsen PA, Andersen JR, Mann M, Wisniewski JR. Quantitative proteomic profiling of membrane proteins from the mouse brain cortex, hippocampus, and cerebellum using the HysTag reagent: Mapping of neurotransmitter receptors and ion channels. Brain Res. 1134(1), 95-106 (2007). (Pubitemid 46135536)
21. Groen AJ, Lilley KS. Proteomics of total membranes and subcellular membranes. Expert Rev. Proteomics 7(6), 867-878 (2010).
22. Hoang VM, Conrads TP, Veenstra TD et al. Quantitative proteomics employing primary amine affinity tags. J. Biomol. Tech. 14(3), 216-223 (2003).
23. Peirce MJ, Cope AP, Wait R. Proteomic analysis of the lymphocyte plasma membrane using cell surface biotinylation and solution-phase isoelectric focusing. Methods Mol. Biol. 528, 135-140 (2009).
24. Elschenbroich S, Kim Y, Medin JA, Kislinger T. Isolation of cell surface proteins for mass spectrometry-based proteomics. Expert Rev. Proteomics 7(1), 141-154 (2010).
25. Ghosh D, Krokhin O, Antonovici M et al. Lectin affinity as an approach to the proteomic analysis of membrane glycoproteins. J. Proteome Res. 3(4), 841-850 (2004). (Pubitemid 39166246)
26. Vercoutter-Edouart AS, Slomianny MC, Dekeyzer-Beseme O, Haeuw JF, Michalski JC. Glycoproteomics and glycomics investigation of membrane N-glycosylproteins from human colon carcinoma cells. Proteomics 8(16), 3236-3256 (2008).
27. McDonald CA, Yang JY, Marathe V, Yen TY, Macher BA. Combining results from lectin affinity chromatography and glycocapture approaches substantially improves the coverage of the glycoproteome. Mol. Cell Proteomics 8(2), 287-301 (2009).
28. Everberg H, Leiding T, Schioth A, Tjerneld F, Gustavsson N. Efficient and non-denaturing membrane solubilization combined with enrichment of membrane protein complexes by detergent/polymer aqueous two-phase partitioning for proteome analysis. J. Chromatogr. 1122(1-2), 35-46 (2006). (Pubitemid 44041363)
29. Jones MN. Surfactants in membrane solubilisation. Int. J. Pharmaceut. 177(2), 137-159 (1999). (Pubitemid 29073411)
30. Wisniewski JR, Zougman A, Mann M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J. Proteome Res. 8(12), 5674-5678 (2009).
31. Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat. Methods 6(5), 359-362 (2009). Introduction and instruction for the filter-aided sample preparation methodology.
32. Yu YQ, Gilar M, Gebler JC. A complete peptide mapping of membrane proteins: A novel surfactant aiding the enzymatic digestion of bacteriorhodopsin. Rapid Commun. Mass Spectrom. 18(6), 711-715 (2004). (Pubitemid 38428885)
33. Li M, Powell MJ, Razunguzwa TT, O'Doherty GA. A general approach to anionic acid-labile surfactants with tunable properties. J. Org. Chem. 75(18), 6149-6153 (2010). Valuable resource detailing several mass spectrometry- compatible detergents.
34. Blonder J, Conrads TP, Yu LR et al. A detergent- and cyanogen bromide-free method for integral membrane proteomics: Application to Halobacterium purple membranes and the human epidermal membrane proteome. Proteomics 4(1), 31-45 (2004). (Pubitemid 38140873)
35. Macher BA, Yen TY. Proteins at membrane surfaces-a review of approaches. Mol. Biosyst. 3(10), 705-713 (2007). (Pubitemid 47449625)
36. D'Amici GM, Huber CG, Zolla L. Separation of thylakoid membrane proteins by sucrose gradient ultracentrifugation or blue native-SDS-PAGE two-dimensional electrophoresis. Methods Mol. Biol. 528, 61-70 (2009).
37. Nguyen DN, Becker GW, Riggin RM. Protein mass spectrometry: Applications to analytical biotechnology. J. Chromatogr. 705(1), 21-45 (1995).
38. Gauci S, Helbig AO, Slijper M, Krijgsveld J, Heck AJ, Mohammed S. Lys-N and trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal. Chem. 81(11), 4493-4501 (2009).
39. van Montfort BA, Doeven MK, Canas B, Veenhoff LM, Poolman B, Robillard GT. Combined in-gel tryptic digestion and CNBr cleavage for the generation of peptide maps of an integral membrane protein with MALDI-TOF mass spectrometry. Biochim. Biophys. Acta 1555(1-3), 111-115 (2002). (Pubitemid 35246015)
40. Washburn MP, Wolters D, Yates JR 3rd. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19(3), 242-247 (2001). (Pubitemid 32220565)
41. Pramanik BN, Mirza UA, Ing YH et al. Microwave-enhanced enzyme reaction for protein mapping by mass spectrometry: A new approach to protein digestion in minutes. Protein Sci. 11(11), 2676-2687 (2002). (Pubitemid 35191141)
42. Zhong H, Marcus SL, Li L. Microwave-assisted acid hydrolysis of proteins combined with liquid chromatography MALDI MS/MS for protein identification. J. Am. Soc. Mass Spec. 16(4), 471-481 (2005). (Pubitemid 40410033)
43. Chen WY, Chen YC. Functional Fe3O4@ZnO magnetic nanoparticle-assisted enrichment and enzymatic digestion of phosphoproteins from saliva. Anal. Bioanal. Chem. 398(5), 2049-2057 (2010).
44. Hasan N, Wu HF, Li YH, Nawaz M. Two-step on-particle ionization/ enrichment via a washing- and separation-free approach: Multifunctional TiO2 nanoparticles as desalting, accelerating, and affinity probes for microwave-assisted tryptic digestion of phosphoproteins in ESI-MS and MALDI-MS: Comparison with microscale TiO2. Anal. Bioanal. Chem. 396(8), 2909-2919 (2010).
45. Rogers LD, Foster LJ. Phosphoproteomics - finally fulfilling the promise? Mol. Biosyst. 5(10), 1122-1129 (2009).
46. Demus H. Subcellular fractionation of human lymphocytes. Isolation of two plasma membrane fractions and comparison of the protein components of the various lymphocytic organelles. Biochim. Biophys. Acta 291(1), 93-106 (1973).
47. Villen J, Gygi SP. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protocols 3(10), 1630-1638 (2008).
48. Puente LG, Megeney LA. Isolation of phosphoproteins. Methods Mol. Biol. 424, 365-372 (2008).
49. Schumacher JA, Crockett DK, Elenitoba-Johnson KS, Lim MS. Evaluation of enrichment techniques for mass spectrometry: Identification of tyrosine phosphoproteins in cancer cells. J. Mol. Diagn. 9(2), 169-177 (2007). (Pubitemid 47305083)
50. Rush J, Moritz A, Lee KA et al. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23(1), 94-101 (2005). (Pubitemid 41724631)
51. Nagano K, Shinkawa T, Yabuki N et al. Integration of proteomic analyses to monitor the activity status of phosphorylation signaling. J. Proteomics 74(3), 319-326 (2011).
52. Zheng H, Hu P, Quinn DF, Wang YK. Phosphotyrosine proteomic study of interferon alpha signaling pathway using a combination of immunoprecipitation and immobilized metal affinity chromatography. Mol. Cell Proteomics 4(6), 721-730 (2005). (Pubitemid 40879601)
53. Cooper JA, Sefton BM, Hunter T. Detection and quantification of phosphotyrosine in proteins. Methods Enzymol. 99, 387-402 (1983).
54. Gronborg M, Kristiansen TZ, Stensballe A et al. A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: Identification of a novel protein, Frigg, as a protein kinase A substrate. Mol. Cell Proteomics 1(7), 517-527 (2002).
55. Wisniewski JR, Nagaraj N, Zougman A, Gnad F, Mann M. Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. J. Proteome Res. 9(6), 3280-3289 (2010). Introduction of the filter-aided antibody capturing and elution method for phosphoproteomics.
56. Ballif BA, Villen J, Beausoleil SA, Schwartz D, Gygi SP. Phosphoproteomic analysis of the developing mouse brain. Mol. Cell Proteomics 3(11), 1093-1101 (2004). (Pubitemid 40012102)
57. Dephoure N, Zhou C, Villen J et al. A quantitative atlas of mitotic phosphorylation. Proc. Natl Acad. Sci. USA 105(31), 10762-10767 (2008).
58. Villen J, Beausoleil SA, Gerber SA, Gygi SP. Large-scale phosphorylation analysis of mouse liver. Proc. Natl Acad. Sci. USA 104(5), 1488-1493 (2007). (Pubitemid 46214617)
59. Morandell S, Stasyk T, Grosstessner-Hain K et al. Phosphoproteomics strategies for the functional analysis of signal transduction. Proteomics 6(14), 4047-4056 (2006).
60. Nuhse TS, Peck SC. Peptide-based phosphoproteomics with immobilized metal ion chromatography. Methods Mol. Biol. 323, 431-436 (2006).
61. Nuhse TS, Bottrill AR, Jones AM, Peck SC. Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J. 51(5), 931-940 (2007). (Pubitemid 47301663)
62. Nuhse TS, Stensballe A, Jensen ON, Peck SC. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16(9), 2394-2405 (2004). (Pubitemid 39247080)
63. Chenau J, Michelland S, Sidibe J, Seve M. Peptides OFFGEL electrophoresis: A suitable pre-analytical step for complex eukaryotic samples fractionation compatible with quantitative iTRAQ labeling. Proteome Sci. 6, 9 (2008).
64. Horth P, Miller CA, Preckel T, Wenz C. Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis. Mol. Cell Proteomics 5(10), 1968-1974 (2006). (Pubitemid 44688204)
65. Gauci S, van Breukelen B, Lemeer SM, Krijgsveld J, Heck AJ. A versatile peptide pI calculator for phosphorylated and N-terminal acetylated peptides experimentally tested using peptide isoelectric focusing. Proteomics 8(23-24), 4898-4906 (2008).
66. Maccarrone G, Kolb N, Teplytska L et al. Phosphopeptide enrichment by IEF. Electrophoresis 27(22), 4585-4595 (2006). First of several studies employing isoelectric focusing for phosphopeptide separation and enrichment.
67. Xu CF, Wang H, Li D, Kong XP, Neubert TA. Selective enrichment and fractionation of phosphopeptides from peptide mixtures by isoelectric focusing after methyl esterification. Anal. Chem. 79(5), 2007-2014 (2007). (Pubitemid 46355232)
68. Hung CW, Kubler D, Lehmann WD. pI-based phosphopeptide enrichment combined with nanoESI-MS. Electrophoresis 28(12), 2044-2052 (2007). (Pubitemid 47040410)
69. Xu Y, Sprung R, Kwon SW, Kim SC, Zhao Y. Isolation of phosphopeptides by pI-difference-based electrophoresis. J. Proteome Res. 6(3), 1153-1157 (2007).
70. Zuo X, Lee K-B, Speicher DW. Fractionation of Complex Proteomes by Microscale Solution Isoelectrofocusing Using ZOOM- IEF Fractionators to Improve Protein Profiling. In:The Proteomics Protocols Handbook. Walker JM (Ed.). Humana Press, NJ, USA, 97-117 (2005).
71. McNulty DE, Annan RS. Hydrophilic interaction chromatography for fractionation and enrichment of the phosphoproteome. Methods Mol. Biol. 527, 93-105 (2009).
72. McNulty DE, Annan RS. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell Proteomics 7(5), 971-980 (2008). (Pubitemid 351737096)
73. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol. Cell Proteomics 7(7), 1389-1396 (2008). (Pubitemid 352038280)
74. Ficarro SB, McCleland ML, Stukenberg PT et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20(3), 301-305 (2002). (Pubitemid 34205425)
75. Ficarro SB, Salomon AR, Brill LM et al. Automated immobilized metal affinity chromatography/nano-liquid chromatography/electrospray ionization mass spectrometry platform for profiling protein phosphorylation sites. Rapid Commun. Mass Spectrom. 19(1), 57-71 (2005). (Pubitemid 40065069)
76. Collins MO, Yu L, Coba MP et al. Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280(7), 5972-5982 (2005). (Pubitemid 40280081)
77. Porath J. Immobilized metal ion affinity chromatography. Protein Exp. Purification 3(4), 263-281 (1992).
78. Kokubu M, Ishihama Y, Sato T, Nagasu T, Oda Y. Specificity of immobilized metal affinity-based IMAC/C18 tip enrichment of phosphopeptides for protein phosphorylation analysis. Anal. Chem. 77(16), 5144-5154 (2005). (Pubitemid 41140831)
79. Pinkse MW, Uitto PM, Hilhorst MJ, Ooms B, Heck AJ. Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal. Chem. 76(14), 3935-3943 (2004). (Pubitemid 38943662)
80. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jorgensen TJ. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell Proteomics 4(7), 873-886 (2005). (Pubitemid 41309146)
81. Sano A, Nakamura H. Evaluation of titanium and titanium oxides as chemo-affinity sorbents for the selective enrichment of organic phosphates. Anal. Sci. 23(11), 1285-1289 (2007).
82. Jensen SS, Larsen MR. Evaluation of the impact of some experimental procedures on different phosphopeptide enrichment techniques. Rapid Commun. Mass Spectrom. 21(22), 3635-3645 (2007). (Pubitemid 350124632)
83. Bodenmiller B, Mueller LN, Mueller M, Domon B, Aebersold R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 4(3), 231-237 (2007). (Pubitemid 46358873)
84. Thingholm TE, Jensen ON, Robinson PJ, Larsen MR. SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol. Cell Proteomics 7(4), 661-671 (2008). (Pubitemid 351597478)
85. Gafken PR, Lampe PD. Methodologies for characterizing phosphoproteins by mass spectrometry. Cell Comm. Adhesion 13(5-6), 249-262 (2006). (Pubitemid 44895997)
86. Molina H, Horn DM, Tang N, Mathivanan S, Pandey A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl Acad. Sci. USA 104(7), 2199-2204 (2007). Details the use of electron transfer dissociation fragmentation of phosphopeptides in a global context. (Pubitemid 46391375)
87. Schroeder MJ, Shabanowitz J, Schwartz JC, Hunt DF, Coon JJ. A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 76(13), 3590-3598 (2004). (Pubitemid 38868819)
88. Andreas F. Hühmer ZH, Sadygov R, Biringer RG, Schwartz JC. Analysis of phosphopeptides by linear ion trap mass spectrometry using multistage activation. Thermo Electron Corporation Application Note 30093.
89. Zubarev RA, Horn DM, Fridriksson EK et al. Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem. 72(3), 563-573 (2000). (Pubitemid 33595293)
90. Wu J, Warren P, Shakey Q et al. Integrating titania enrichment, iTRAQ labeling, and Orbitrap CID-HCD for global identification and quantitative analysis of phosphopeptides. Proteomics 10(11), 2224-2234 (2010).
91. Zhang Y, Ficarro SB, Li S, Marto JA. Optimized Orbitrap HCD for quantitative analysis of phosphopeptides. J. Am. Soc. Mass Spec. 20(8), 1425-1434 (2009).
92. Nagaraj N, D'Souza RC, Cox J, Olsen JV, Mann M. Feasibility of large scale phosphoproteomics with HCD fragmentation. J. Proteome Res. 9(12), 6786-6794 (2010).
93. Olsen JV, Schwartz JC, Griep-Raming J et al. A dual pressure linear ion trap Orbitrap instrument with very high sequencing speed. Mol. Cell Proteomics 8(12), 2759-2769 (2009).
94. Swaney DL, McAlister GC, Coon JJ. Decision tree-driven tandem mass spectrometry for shotgun proteomics. Nat. Methods 5(11), 959-964 (2008).