Complementary IMAC enrichment methods for HLA-associated phosphopeptide identification by mass spectrometry

Nature Protocols

Volumn 10, Issue 9, 2015, Pages 1308-1318

  Abelin, Jennifer G ^a   Trantham, Paisley D ^a   Penny, Sarah A ^b   Patterson, Andrea M ^c   Ward, Stephen T ^b   Hildebrand, William H ^c   Cobbold, Mark ^b   Bai, Dina L ^a   Shabanowitz, Jeffrey ^a   Hunt, Donald F ^a,d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETONITRILE; ASCORBIC ACID; DIGLYCINE; EDETIC ACID; FERRIC ION; FORMAMIDE; HLA ANTIGEN; HLA ANTIGEN CLASS 1; NITRILOTRIACETIC ACID; PHOSPHOPEPTIDE; PHOSPHORIC ACID; HISTOCOMPATIBILITY ANTIGEN;

ANTIGEN SPECIFICITY; ARTICLE; CELL CULTURE; CHEMICAL PROCEDURES; CHEMICAL REACTION; COMPUTER PROGRAM; CONTROLLED STUDY; ESTERIFICATION; FEMALE; FLOW RATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMORTALIZED CELL LINE; MASS SPECTROMETRY; PEPTIDE ANALYSIS; PEPTIDE DESALTING; PHOSPHORYLATION; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN DEPLETION; PROTEIN ISOLATION; AFFINITY CHROMATOGRAPHY; METABOLISM; PROCEDURES;

CHROMATOGRAPHY, AFFINITY; HISTOCOMPATIBILITY ANTIGENS; MASS SPECTROMETRY; PHOSPHOPEPTIDES;

EID: 84940552740     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2015.086     Document Type: Article

References (41)

1. Mohammed, F. et al. Phosphorylation-dependent interaction between antigenic peptides and MHC class I: a molecular basis for the presentation of transformed self. Nat. Immunol. 9, 1236-1243 (2008).
2. Zarling, A.L. et al. Identifcation of class I MHC-associated phosphopeptides as targets for cancer immunotherapy. Proc. Natl. Acad. Sci. USA 103, 14889-14894 (2006).
3. Engelhard, V.H., Brickner, A.G. & Zarling, A.L. Insights into antigen processing gained by direct analysis of the naturally processed class I MHC associated peptide repertoire. Mol. Immunol. 39, 127-137 (2002).
4. Zarling, A.L. et al. Phosphorylated peptides are naturally processed and presented by major Histocompatibility complex class I molecules in vivo. J. Exp. Med. 192, 1755-1762 (2000).
5. Cobbold, M. et al. MHC class I-associated phosphopeptides are the targets of memory-like immunity in leukemia. Sci. Transl. Med. 5, 203ra125 (2013).
6. Vanneman, M. & Dranoff, G. Combining immunotherapy and targeted therapies in cancer treatment. Nat. Rev. Cancer 12, 237-251 (2012).
7. Vivier, E., Ugolini, S., Blaise, D., Chabannon, C. & Brossay, L. Targeting natural killer cells and natural killer T cells in cancer. Nat. Rev. Immunol. 12, 239-252 (2012).
8. Neefjes, J., Jongsma, M.L.M., Paul, P. & Bakke, O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11, 823-836 (2011).
9. Hansen, T.H. & Bouvier, M. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9, 503-513 (2009).
10. Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252-264 (2012).
11. Hanahan, D. & Weinberg, R.A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
12. Ficarro, S.B. et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20, 301-305 (2002).
13. Ficarro, S. et al. Phosphoproteome analysis of capacitated human sperm: evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J. Biol. Chem. 278, 11579-11589 (2003).
14. Olsen, J.V. et al. Global, in vivo, and site-specifc phosphorylation dynamics in signaling networks. Cell 127, 635-648 (2006).
15. Villen, J. & Gygi, S.P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protoc. 3, 1630-1638 (2008).
16. Steen, H., Stensballe, A. & Jensen, O.N. Phosphopeptide purifcation by IMAC with Fe(III) and Ga(III). Cold Spring Harb. Protoc. 2007, pdb. prot4607 (2007).
17. Thingholm, T. & Jensen, O. Enrichment and characterization of phosphopeptides by immobilized metal affnity chromatography (IMAC) and mass spectrometry in Phospho-Proteomics: Methods and protocols (ed. Graauw, M.) 527, 47-56 (Humana Press, 2009).
18. Ye, J. et al. Optimized IMACIMAC protocol for phosphopeptide recovery from complex biological samples. J. Proteome Res. 9, 3561-3573 (2010).
19. Dunn, J.D., Reid, G.E. & Bruening, M.L. Techniques for phosphopeptide enrichment prior to analysis by mass spectrometry. Mass Spectrom. Rev. 29, 29-54 (2010).
20. Zhou, H. et al. Robust phosphoproteome enrichment using monodisperse microsphere-based immobilized titanium (IV) ion affnity chromatography. Nat. Protoc. 8, 461-480 (2013).
21. Thingholm, T.E., Jorgensen, T.J.D., Jensen, O.N. & Larsen, M.R. Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nat. Protoc. 1, 1929-1935 (2006).
22. Ruprecht, B. et al. Comprehensive and reproducible phosphopeptide enrichment using Fe-IMAC columns. Mol. Cell. Proteomics 14, 205-215 (2015).
23. Ficarro, S.B. et al. Online nanofow multidimensional fractionation for high effciency phosphopeptide analysis. Mol. Cell. Proteomics 10, O111.011064 (2011).
24. Mertins, P. et al. Integrated proteomic analysis of post-translational modifcations by serial enrichment. Nat. Methods 10, 634-637 (2013).
25. Mertins, P. et al. Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol. Cell. Proteomics 13, 1690-1704 (2014).
26. Mazanek, M. et al. Titanium dioxide as a chemo-affnity solid phase in offine phosphopeptide chromatography prior to HPLC-MS/MS analysis. Nat. Protoc. 2, 1059-1069 (2007).
27. 2 using a massive synthetic library and human cell digests. Anal. Chem. 86, 8312-8320 (2014).
28. Zhou, H. et al. Specifc phosphopeptide enrichment with immobilized titanium ion affnity chromatography adsorbent for phosphoproteome analysis. J. Proteome Res. 7, 3957-3967 (2008).
29. Jedrychowski, M.P. et al. Evaluation of HCD- and CID-type fragmentation within their respective detection platforms for murine phosphoproteomics. Mol. Cell. Proteomics 10, M111.009910 (2011).
30. Zhang, Y., Ficarro, S., Li, S. & Marto, J. Optimized orbitrap HCD for quantitative analysis of phosphopeptides. J. Am. Soc. Mass Spectrom. 20, 1425-1434 (2009).
31. Syka, J.E.P., Coon, J.J., Schroeder, M.J., Shabanowitz, J. & Hunt, D.F. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 101, 9528-9533 (2004).
32. Udeshi, N.D., Compton, P.D., Shabanowitz, J., Hunt, D.F. & Rose, K.L. Methods for analyzing peptides and proteins on a chromatographic timescale by electron-transfer dissociation mass spectrometry. Nat. Protoc. 3, 1709-1717 (2008).
33. Schroeder, M.J., Shabanowitz, J., Schwartz, J.C., Hunt, D.F. & Coon, J.J. A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal. Chem. 76, 3590-3598 (2004).
34. Earley, L. et al. Front-end electron transfer dissociation: a new ionization source. Anal. Chem. 85, 8385-8390 (2013).
35. Wiesner, J., Premsler, T. & Sickmann, A. Application of electron transfer dissociation (ETD) for the analysis of posttranslational modifcations. Proteomics 8, 4466-4483 (2008).
36. Mommen, G.P.M. et al. Expanding the detectable HLA peptide repertoire using electron-transfer/higher-energy collision dissociation (EThcD). Proc. Natl Acad. Sci. USA 111, 4507-4512 (2014).
37. Martin, S.E., Shabanowitz, J., Hunt, D.F. & Marto, J.A. Subfemtomole MS and MS/MS peptide sequence analysis using nano-HPLC micro-ESI Fourier transform ion cyclotron resonance mass spectrometry. Anal. Chem. 72, 4266-4274 (2000).
38. Prilliman, K. et al. Large-scale production of class I bound peptides: assigning a signature to HLA-B∗1501. Immunogenetics 45, 379-385 (1997).
39. Hawkins, O.E. et al. Identifcation of breast cancer peptide epitopes presented by HLA-A∗0201. J. Proteome Res. 7, 1445-1457 (2008).
40. Purcell, A. Isolation and characterization of naturally processed MHC-bound peptides from the surface of antigen-presenting cells. in HPLC of Peptides and Proteins: Methods and Protocols (ed. Aguilar, M.-I.) 251, 291-306 (Springer New York, 2004).
41. Geer, L.Y. et al. Open mass spectrometry search algorithm. J. Proteome Res. 3, 958-964 (2004).