Direct identification of tyrosine sulfation by using ultraviolet photodissociation mass spectrometry

Journal of the American Society for Mass Spectrometry

Volumn 25, Issue 8, 2014, Pages 1461-1471

  Robinson, Michelle R ^a   Moore, Kevin L ^b,c   Brodbelt, Jennifer S ^a  

^a University of Texas at Austin   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

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

Author keywords

Sulfation; Sulfopeptide; Tyrosine; Ultraviolet photodissociation

Indexed keywords

CHEMICAL REACTIONS; IONS; MASS SPECTROMETRY; PEPTIDES; PHOTODISSOCIATION;

COLLISIONAL ACTIVATION; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; POST-TRANSLATIONAL MODIFICATIONS; SULFATION; SULFOPEPTIDE; TYROSINE; TYROSINE PHOSPHORYLATION; ULTRAVIOLET PHOTODISSOCIATION;

AMINO ACIDS;

ANION; CERULETIDE; CIONIN; FIBRINOGEN; LEUCINE ENKEPHALIN; SULFATE; TYROSINE; UNCLASSIFIED DRUG; NEUROPEPTIDE; OLIGOPEPTIDE; PEPTIDE FRAGMENT;

AMINO ACID SEQUENCE; ARTICLE; LIMIT OF DETECTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PEPTIDE ANALYSIS; PRECURSOR; PROTEIN PHOSPHORYLATION; SULFATION; ULTRAVIOLET PHOTODISSOCIATION MASS SPECTROMETRY; ULTRAVIOLET SPECTROPHOTOMETRY; ANIMAL; BOVINE; CHEMICAL DATABASE; CHEMISTRY; COMPARATIVE STUDY; ELECTROCHEMICAL ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LASER; METABOLISM; PROTEIN PROCESSING; TANDEM MASS SPECTROMETRY; X RAY PHOTOELECTRON SPECTROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CERULETIDE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DATABASES, CHEMICAL; ELECTROCHEMICAL TECHNIQUES; ENKEPHALIN, LEUCINE; FIBRINOGEN; HUMANS; LASERS; LIMIT OF DETECTION; MASS SPECTROMETRY; MICROCHEMISTRY; NEUROPEPTIDES; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PHOTOELECTRON SPECTROSCOPY; PROTEIN PROCESSING, POST-TRANSLATIONAL; SULFATES; TANDEM MASS SPECTROMETRY; TYROSINE;

EID: 84904898956     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-014-0910-3     Document Type: Article

References (62)

1. Mann, M., Jensen, O.N.: Proteomic analysis of post-translational modifications. Nat. Biotechnol. 21, 255-261 (2003)
2. Bettelheim, F.R.: Tyrosine-o-sulfate in a peptide from fibrinogen. J. Am. Chem. Soc. 76, 2838-2839 (1954)
3. Huttner, W.B.: Sulphation of tyrosine residues-a widespread modification of proteins. Nature 299, 273-276 (1982)
4. Baeuerle, P.A., Huttner, W.B.: Tyrosine sulfation of yolk proteins 1, 2, and 3 in Drosophila melanogaster. J. Biol. Chem. 260, 6434-6439 (1985)
5. Beisswanger, R., Corbeil, D., Vannier, C., Thiele, C., Dohrmann, U., Ashman, R.K., Niehrs, K.C., Huttner, W.B.: Existence of distinct tyrosylprotein sulfotransferase genes: molecular characterization of tyrosylprotein sulfotransferase-2. Proc. Natl. Acad. Sci. U. S. A. 95, 11134-11139 (1998)
6. Ouyang, Y.-B., Lane, W.S., Moore, K.L.: Tyrosylprotein sulfotransferase: purification and molecular cloning of an enzyme that catalyzes tyrosine O-sulfation, a common post-translational modification of eukaryotic proteins. Proc. Natl. Acad. Sci. U. S. A. 95, 2896-2901 (1998)
7. Ouyang, Y.-B., Moore, K.L.: Molecular cloning and expression of human and mouse tyrosylprotein sulfotransferase-2 and a tyrosylprotein sulfotransferase homologue in Caenorhabditis elegans. J. Biol. Chem. 273, 24770-24774 (1998)
8. Seibert, C., Cadene, M., Sanfiz, A., Chait, B.T., Sakmar, T.P.: Tyrosine sulfation of CCR5 N-terminal peptide by tyrosylprotein sulfotransferases 1 and 2 follows a discrete pattern and temporal sequence. Proc. Natl. Acad. Sci. U. S. A. 99, 11031-11036 (2002)
9. Danan, L.M., Yu, Z., Hoffhines, A.J., Moore, K.L., Leary, J.A.: Mass spectrometric kinetic analysis of human tyrosylprotein sulfotransferase-1 and -2. J. Am. Soc. Mass Spectrom. 19, 1459-1466 (2008)
10. Danan, L.M., Yu, Z., Ludden, P.J., Jia, W., Moore, K.L., Leary, J.A.: Catalytic mechanism of Golgi-resident human tyrosylprotein sulfotransferase-2: a mass spectrometry approach. J. Am. Soc. Mass Spectrom. 21, 1633-1642 (2010)
11. Moore, K.L.: The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278, 24243-24246 (2003)
12. Huttner, W.B.: Tyrosine sulfation and the secretory pathway. Annu. Rev. Physiol. 50, 363-376 (1988)
13. Stone, M.J., Chuang, S., Hou, X., Shoham, M., Zhu, J.Z.: Tyrosine sulfation: an increasingly recognised post-translational modification of secreted proteins. New Biotechnol. 25, 299-317 (2009)
14. Hille, A., Huttner, W.B.: Occurrence of tyrosine sulfate in proteins - a balance sheet. 2. Membrane proteins. Eur. J. Biochem. 188, 587-596 (1990)
15. Kehoe, J.W., Bertozzi, C.R.: Tyrosine sulfation: a modulator of extracellular protein-protein interactions. Chem. Biol. 7, R57-R61 (2000)
16. Hortin, G.: Sulfation of tyrosine residues in coagulation factor V. Blood 76, 946-952 (1990)
17. Farzan, M., Mirzabekov, T., Kolchinsky, P., Wyatt, R., Cayabyab, M., Gerard, N.P., Gerard, C., Sodroski, J., Choe, H.: Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96, 667-676 (1999)
18. Monigatti, F., Hekking, B., Steen, H.: Protein sulfation analysis - a primer. Biochim. Biophys. Acta 1764, 1904-1913 (2006)
19. Seibert, C., Sakmar, T.P.: Toward a framework for sulfoproteomics: synthesis and characterization of sulfotyrosine-containing peptides. Biopolymers 90, 459-477 (2008)
20. Nemeth-Cawley, J.F., Karnik, S., Rouse, J.C.: Analysis of sulfated peptides using positive electrospray ionization tandem mass spectrometry. J. Mass Spectrom. 36, 1301-1311 (2001)
21. Wolfender, J.-L., Chu, F., Ball, H., Wolfender, F., Fainzilber, M., Baldwin, M.A., Burlingame, A.L.: Identification of tyrosine sulfation in Conus pennaceus conotoxins α-PnIA and α-PnIB: further investigation of labile sulfo- and phosphopeptides by electrospray, matrix-assisted laser desorption/ionization (MALDI) and atmospheric pressure MALDI mass spectrometry. J. Mass Spectrom. 34, 447-454 (1999)
22. Medzihradszky, K.F., Guan, S., Maltby, D.A., Burlingame, A.L.: Sulfopeptide fragmentation in electron-capture and electron-transfer dissociation. J. Am. Soc. Mass Spectrom. 18, 1617-1624 (2007)
23. Mikesh, L.M., Ueberheide, B., Chi, A., Coon, J.J., Syka, J.E.P., Shabanowitz, J., Hunt, D.F.: The utility of ETD mass spectrometry in proteomic analysis. Biochim. Biophys. Acta 1764, 1811-1822 (2006)
24. Yagami, T., Kitagawa, K., Aida, C., Fujiwara, H., Futaki, S.: Stabilization of a tyrosine O-sulfate residue by a cationic functional group: formation of a conjugate acid-base pair. J. Peptide Res. 56, 239-249 (2000)
25. Liu, H., Håkansson, K.: Electron capture dissociation of tyrosine O-sulfated peptides complexed with divalent metal cations. Anal. Chem. 78, 7570-7576 (2006)
26. Cantel, S., Brunel, L., Ohara, K., Enjalbal, C., Martinez, J., Vasseur, J.-J., Smietana, M.: An innovative strategy for sulfopeptides analysis using MALDI-TOF MS reflectron positive ion mode. Proteomics 12, 2247-2257 (2012)
27. Yu, Y., Hoffhines, A.J., Moore, K.L., Leary, J.A.: Determination of the sites of tyrosine O-sulfation in peptides and proteins. Nat. Methods 4, 583-588 (2007)
28. Kim, J.-S., Song, S.-U., Kim, H.-J.: Simultaneous identification of tyrosine phosphorylation and sulfation sites utilizing tyrosine-specific bromination. J. Am. Soc. Mass Spectrom. 22, 1916-1925 (2011)
29. Drake, S.K., Hortin, G.L.: Improved detection of intact tyrosine sulfate-containing peptides by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in linear negative ion mode. Int. J. Biochem. Cell Biol. 42, 174-179 (2010)
30. Edelson-Averbukh, M., Shevchenko, A., Pipkorn, R., Lehmann, W.: Discrimination between peptide O-sulfo- and O-phosphotyrosine residues by negative ion mode electrospray tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 22, 2256-2268 (2011)
31. Gibson, B.W., Cohen, P.: Liquid secondary ion mass spectrometry of phosphorylated and sulfated peptides and proteins. In: McCloskey, J.A. (ed.) Methods in enzymology, pp. 480-501. Academic Press, New York (1990).
32. Cook, S., Jackson, G.: Metastable Atom-activated dissociation mass spectrometry of phosphorylated and sulfonated peptides in negative ion mode. J. Am. Soc. Mass Spectrom. 22, 1088-1099 (2011)
33. Hersberger, K.E., Håkansson, K.: Characterization of O-sulfopeptides by negative ion mode tandem mass spectrometry: superior performance of negative ion electron capture dissociation. Anal. Chem. 84, 6370-6377 (2012)
34. Brodbelt, J.S.: Shedding light on the frontier of photodissociation. J. Am. Soc. Mass Spectrom. 22, 197-206 (2011)
35. Ly, T., Julian, R.R.: Ultraviolet photodissociation: developments towards applications for mass-spectrometry-based proteomics. Angew. Chem. Int. Ed. 48, 7130-7137 (2009)
36. Reilly, J.P.: Ultraviolet photofragmentation of biomolecular ions. Mass Spectrom. Rev. 28, 425-447 (2009)
37. Madsen, J.A., Boutz, D.R., Brodbelt, J.S.: Ultrafast ultraviolet photodissociation at 193 nm and its applicability to proteomic workflows. J. Proteome Res. 9, 4205-4214 (2010)
38. Madsen, J.A., Kaoud, T.S., Dalby, K.N., Brodbelt, J.S.: 193-nm photodissociation of singly and multiply charged peptide anions for acidic proteome characterization. Proteomics 11, 1329-1334 (2011)
39. Madsen, J.A., Xu, H., Robinson, M.R., Horton, A.P., Shaw, J.B., Giles, D.K., Kaoud, T.S., Dalby, K.N., Trent, M.S., Brodbelt, J.S.: High-throughput database search and large-scale negative polarity LC-MS/MS with ultraviolet photodissociation for complex proteomic samples. Mol. Cell. Proteomics 12, 2604-2614 (2013)
40. Shaw, J., Madsen, J., Xu, H., Brodbelt, J.: Systematic comparison of ultraviolet photodissociation and electron transfer dissociation for peptide anion characterization. J. Am. Soc. Mass Spectrom. 23, 1707-1715 (2012)
41. Madsen, J.A., Ko, B.J., Robotham, S.A., Xu, H., Horton, A.P., Iwashkiw, J.A., Shaw, J.B., Feldman, M.F., Brodbelt, J.S.: Concurrent automated sequencing of the glycan and peptide portions of O-linked glycopeptide anions. Anal. Chem. 85, 9253-9261 (2013)
42. Han, S.-W., Lee, S.-W., Bahar, O., Schwessinger, B., Robinson, M.R., Shaw, J.B., Madsen, J.A., Brodbelt, J.S., Ronald, P.C.: Tyrosine sulfation in a Gram-negative bacterium. Nat. Commun. 3, 1153 (2012)
43. Vasicek, L., Ledvina, A., Shaw, J., Griep-Raming, J., Westphall, M., Coon, J., Brodbelt, J.: Implementing photodissociation in an Orbitrap mass spectrometer. J. Am. Soc. Mass Spectrom. 22, 1105-1108 (2011)
44. Shaw, J.B., Li, W., Holden, D.D., Zhang, Y., Griep-Raming, J., Fellers, R.T., Early, B.P., Thomas, P.M., Kelleher, N.L., Brodbelt, J.S.: Complete protein characterization using top-down mass spectrometry and ultraviolet photodissociation. J. Am. Chem. Soc. 135, 12646-12651 (2013)
45. Xu, H., Freitas, M.: A mass accuracy sensitive probability based scoring algorithm for database searching of tandem mass spectrometry data. BMC Bioinforma. 8, 133 (2007)
46. Xu, H., Yang, L., Freitas, M.: A robust linear regression based algorithm for automated evaluation of peptide identifications from shotgun proteomics by use of reversed-phase liquid chromatography retention time. BMC Bioinforma. 9, 347 (2008)
47. Xu, H., Freitas, M.A.: MassMatrix: a database search program for rapid characterization of proteins and peptides from tandem mass spectrometry data. Proteomics 9, 1548-1555 (2009)
48. Xu, H., Freitas, M.A.: Monte Carlo simulation-based algorithms for analysis of shotgun proteomic data. J. Proteome Res. 7, 2605-2615 (2008)
49. Yagami, T., Kitagawa, K., Aida, C., Fujiwara, H., Futaki, S.: Stabilization of a tyrosine O-sulfate residue by a cationic functional group: formation of a conjugate acid-base pair. J. Peptide Res. 56, 239-249 (2000)
50. Antoine, R., Joly, L., Tabarin, T., Broyer, M., Dugourd, P., Lemoine, J.: Photo-induced formation of radical anion peptides. Electron photodetachment dissociation experiments. Rapid Commun. Mass Spectrom. 21, 265-268 (2007)
51. Rumachik, N., McAlister, G., Russell, J., Bailey, D., Wenger, C., Coon, J.: Characterizing peptide neutral losses induced by negative electron-transfer dissociation (NETD). J. Am. Soc. Mass Spectrom. 23, 718-727 (2012)
52. Sun, Q., Nelson, H., Ly, T., Stoltz, B.M., Julian, R.R.: Side chain chemistry mediates backbone fragmentation in hydrogen deficient peptide radicals. J. Proteome Res. 8, 958-966 (2008)
53. Straub, R.F., Voyksner, R.D.: Negative ion formation in electrospray mass spectrometry. J. Am. Soc. Mass Spectrom. 4, 578-587 (1993)
54. Yamashita, M., Fenn, J.B.: Negative ion production with the electrospray ion source. J. Phys. Chem. 88, 4671-4675 (1984)
55. Hiraoka, K., Kudaka, I.: Negative-mode electrospray-mass spectrometry using nonaqueous solvents. Rapid Commun. Mass Spectrom. 6, 265-268 (1992)
56. Cech, N.B., Enke, C.G.: Practical implications of some recent studies in electrospray ionization fundamentals. Mass Spectrom. Rev. 20, 362-387 (2001)
57. Zhang, X., Clausen, M.R., Zhao, X., Zheng, H., Bertram, H.C.: Enhancing the power of liquid chromatography-mass spectrometry-based urine metabolomics in negative ion mode by optimization of the additive. Anal. Chem. 84, 7785-7792 (2012)
58. McAlister, G.C., Russell, J.D., Rumachik, N.G., Hebert, A.S., Syka, J.E.P., Geer, L.Y., Westphall, M.S., Pagliarini, D.J., Coon, J.J.: Analysis of the acidic proteome with negative electron-transfer dissociation mass spectrometry. Anal. Chem. 84, 2875-2882 (2012)
59. Balsved, D., Bundgaard, J.R., Sen, J.W.: Stability of tyrosine sulfate in acidic solutions. Anal. Biochem. 363, 70-76 (2007)
60. Balderrama, G.D., Meneses, E.P., Orihuela, L.H., Hernández, O.V., Franco, R.C., Robles, V.P., Batista, C.V.F.: Analysis of sulfated peptides from the skin secretion of the Pachymedusa dacnicolor frog using IMAC-Ga enrichment and high-resolution mass spectrometry. Rapid Commun. Mass Spectrom. 25, 1017-1027 (2011)
61. Amano, Y., Shinohara, H., Sakagami, Y., Matsubayashi, Y.: Ion-selective enrichment of tyrosine-sulfated peptides from complex protein digests. Anal. Biochem. 346, 124-131 (2005)
62. Hoffhines, A.J., Damoc, E., Bridges, K.G., Leary, J.A., Moore, K.L.: Detection and purification of tyrosine-sulfated proteins using a novel anti-sulfotyrosine monoclonal antibody. J. Biol. Chem. 281, 37877-37887 (2006)