When is mass spectrometry combined with affinity approaches essential? A case study of tyrosine nitration in proteins

Journal of the American Society for Mass Spectrometry

Volumn 23, Issue 11, 2012, Pages 1831-1840

  Petre, Brînduşa Alina ^a,c   Ulrich, Martina ^b   Stumbaum, Mihaela ^a   Bernevic, Bogdan ^a   Moise, Adrian ^a   Döring, Gerd ^b   Przybylski, Michael ^a  

^a Laboratory of Analytical Chemistry and Biopolymer Structure Analysis and Steinbeis Research   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c ALEXANDRU IOAN CUZA UNIVERSITY OF IASI   (Romania)

Author keywords

Affinity mass spectrometry combination; Eosinophil proteins; False positive identification; Nitro tyrosine antibodies; Protein tyrosine nitration; Proteolytic affinity extraction mass spectrometry; Quantification of nitrations

Indexed keywords

AFFINITY EXTRACTION; AFFINITY-MASS SPECTROMETRY COMBINATION; ALZHEIMER'S DISEASE; BIOLOGICAL SAMPLES; CYSTIC FIBROSIS; EDMAN SEQUENCING; EOSINOPHIL-GRANULE; NANOMOLAR; NITRATION MECHANISM; NITROTYROSINE; PHYSIOLOGIC CONDITIONS; POSITIVELY CHARGED; PROTEIN STRUCTURES; SEQUENCE MOTIFS; STRUCTURAL CHANGE; STRUCTURE MODELING; TYROSINE NITRATION;

AMINO ACIDS; ANTIBODIES; MASS SPECTROMETRY; PEPTIDES;

NITRATION;

3 NITROTYROSINE; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHIL PEROXIDASE; EOSINOPHIL PROTEIN X; LACTOFERRIN; PROTEIN ANTIBODY;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CYSTIC FIBROSIS; ELECTROSPRAY MASS SPECTROMETRY; FALSE POSITIVE RESULT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NANOANALYSIS; NITRATION; NONHUMAN; ONLINE SYSTEM; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN MODIFICATION; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, IMMOBILIZED; BINDING SITES; CYSTIC FIBROSIS; EOSINOPHIL GRANULE PROTEINS; HUMANS; IMMUNOCHROMATOGRAPHY; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; TYROSINE;

EID: 84868247595     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-012-0461-4     Document Type: Article

References (54)

1. Haddad, I.Y., Pataki, G., Hu, P., Galliani, C., Beckman, J.S., Matalon, S.: Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J. Clin. Invest. 94, 2407-2413 (1994)
2. Beckmann, J.S., Ye, Y.Z., Anderson, P.G., Chen, J., Accavitti, M.A., Tarpey, M.M., White, C.R.: Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe Seyler 375, 81-88 (1994)
3. Ulrich, M., Petre, A., Youhnovski, N., Promm, F., Schirle, M., Schumm, M., Pero, R.S., Doyle, A., Checkel, J., Kita, H., Thiyagarajan, N., Acharya, K.R., Schmid-Grendelmeier, P., Simon, H.U., Schwarz, H., Tsutsui, M., Shimokawa, H., Bellon, G., Lee, J.J., Przybylski, M., Doring, G.: Post-translational tyrosine nitration of eosinophil granule toxins mediated by eosinophil peroxidase. J. Biol. Chem. 283, 28629-28640 (2008)
4. Hanazawa, T., Kharitonov, S.A., Barnes, P.J.: Increased nitrotyrosine in exhaled breath condensate of patients with asthma. Am. J. Respir. Crit. Care Med. 162, 1273-1276 (2000)
5. Giasson, B.I., Duda, J.E., Murray, I.V., Chen, Q., Souza, J.M., Hurtig, H.I., Ischiropoulos, H., Trojanowski, J.Q., Lee, V.M.: Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290, 985-989 (2000)
6. Teunissen, C.E., de Vente, J., Steinbusch, H.W., De Bruijn, C.: Biochemical markers related to Alzheimer's dementia in serum and cerebrospinal fluid. Neurobiol. Aging 23, 485-508 (2002)
7. Cuzzocrea, S., Zingarelli, B., Villari, D., Caputi, A.P., Longo, G.: Evidence for in vivo peroxynitrite production in human chronic hepatitis. Life Sci. 63, PL25-PL30 (1998)
8. Garcia-Monzon, C., Majano, P.L., Zubia, I., Sanz, P., Apolinario, A., Moreno-Otero, R.: Intrahepatic accumulation of nitrotyrosine in chronic viral hepatitis is associated with histological severity of liver disease. J. Hepatol. 32, 331-338 (2000)
9. Ceriello, A., Mercuri, F., Quagliaro, L., Assaloni, R., Motz, E., Tonutti, L., Taboga, C.: Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia 44, 834-838 (2001)
10. Souza, J.M., Daikhin, E., Yudkoff, M., Raman, C.S., Ischiropoulos, H.: Factors determining the selectivity of protein tyrosine nitration. Arch. Biochem. Biophys. 371, 169-178 (1999)
11. Ischiropoulos, H.: Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305, 776-783 (2003)
12. Kuhn, D.M., Sadidi, M., Liu, X., Kreipke, C., Geddes, T., Borges, C., Watson, J.T.: Peroxynitrite-induced nitration of tyrosine hydroxylase: identification of tyrosines 423, 428, and 432 as sites of modification by matrix-assisted laser desorption ionization time-of-flight mass spectrometry and tyrosine-scanning mutagenesis. J. Biol. Chem. 277, 14336-14342 (2002)
13. Quijano, C., Hernandez-Saavedra, D., Castro, L., McCord, J.M., Freeman, B.A., Radi, R.: Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal center in decomposition kinetics and nitration. J. Biol. Chem. 276, 11631-11638 (2001)
14. Daiber, A., Bachschmid, M.: Enzyme Inhibition by Peroxynitrite-Mediated Tyrosine Nitration and Thiol Oxidation. Curr. Enzym. Inhib. 3, 103-117 (2007)
15. Khan, J., Brennand, D.M., Bradley, N., Gao, B., Bruckdorfer, R., Jacobs, M.: 3-Nitrotyrosine in the proteins of human plasma determined by an ELISA method. Biochem. J. 330, 795-801 (1998)
16. Hinson, J.A., Michael, S.L., Ault, S.G., Pumford, N.R.: Western blot analysis for nitrotyrosine protein adducts in livers of saline-treated and acetaminophen-treated mice. Toxicol. Sci. 53, 467-473 (2000)
17. Duda, J.E., Giasson, B.I., Chen, Q., Gur, T.L., Hurtig, H.I., Stern, M.B., Gollomp, S.M., Ischiropoulos, H., Lee, V.M., Trojanowski, J.Q.: Widespread nitration of pathological inclusions in neurodegenerative synucleinopathies. Am. J. Pathol. 157, 1439-1445 (2000)
18. ter Steege, J.C., Koster-Kamphuis, L., van Straaten, E.A., Forget, P.P., Buurman, W.A.: Nitrotyrosine in plasma of celiac disease patients as detected by a new sandwich ELISA. Free Radic. Biol. Med. 25, 953-963 (1998)
19. Franze, T., Weller, M.G., Niessner, R., Poschl, U.: Enzyme immuno-assays for the investigation of protein nitration by air pollutants. Analyst 128, 824-831 (2003)
20. Heijnen, H.F., van Donselaar, E., Slot, J.W., Fries, D.M., Blachard-Fillion, B., Hodara, R., Lightfoot, R., Polydoro, M., Spielberg, D., Thomson, L., Regan, E.A., Crapo, J., Ischiropoulos, H.: Subcellular localization of tyrosine-nitrated proteins is dictated by reactive oxygen species generating enzymes and by proximity to nitric oxide synthase. Free Radic. Biol. Med. 40, 1903-1913 (2006)
21. Castegna, A., Thongboonkerd, V., Klein, J.B., Lynn, B., Markesbery, W.R., Butterfield, D.A.: Proteomic identification of nitrated proteins in Alzheimer's disease brain. J. Neurochem. 85, 1394-1401 (2003)
22. Turko, I.V., Li, L., Aulak, K.S., Stuehr, D.J., Chang, J.Y., Murad, F.: Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J. Biol. Chem. 278, 33972-33977 (2003)
23. Abello, N., Kerstjens, H.A., Postma, D.S., Bischoff, R.: Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins. J. Proteome Res. 8, 3222-3238 (2009)
24. Sarver, A., Scheffler, N.K., Shetlar, M.D., Gibson, B.W.: Analysis of peptides and proteins containing nitrotyrosine by matrix-assisted laser desorption/ionization mass spectrometry. J. Am. Soc. Mass Spectrom. 12, 439-448 (2001)
25. Petre, B.A., Youhnovski, N., Lukkari, J., Weber, R., Przybylski, M.: Structural characterization of tyrosine-nitrated peptides by ultraviolet and infrared matrix-assisted laser desorption/ionization Fourier transform ion cyclotron resonance mass spectrometry. Eur. J. Mass Spectrom. 11, 513-518 (2005)
26. Willard, B.B., Ruse, C.I., Keightley, J.A., Bond, M., Kinter, M.: Site-specific quantitation of protein nitration using liquid chromatography/tandem mass spectrometry. Anal. Chem. 75, 2370-2376 (2003)
27. Wang, Z., Paik, D.C., Dillon, J.P., Gaillard, E.R.: Tyrosine nitration site specificity identified by LC/MS in nitrite-modified collagen type IV. Exp. Mol. Med. 39, 74-83 (2007)
28. Schmidt, P., Youhnovski, N., Daiber, A., Balan, A., Arsic, M., Bachschmid, M., Przybylski, M., Ullrich, V.: Specific nitration at tyrosine 430 revealed by high resolution mass spectrometry as basis for redox regulation of bovine prostacyclin synthase. J. Biol. Chem. 278, 12813-12819 (2003)
29. McLaurin, J., Cecal, R., Kierstead, M.E., Tian, X., Phinney, A.L., Manea, M., French, J.E., Lambermon, M.H., Darabie, A.A., Brown, M.E., Janus, C., Chishti, M.A., Horne, P., Westaway, D., Fraser, P.E., Mount, H.T., Przybylski, M., St George-Hyslop, P.: Therapeutically effective antibodies against amyloid-beta peptide target amyloid-beta residues 4-10 and inhibit cytotoxicity and fibrillogenesis. Nat. Med. 8, 1263-1269 (2002)
30. Suckau, D., Kohl, J., Karwath, G., Schneider, K., Casaretto, M., Bitter-Suermann, D., Przybylski, M.: Molecular epitope identification by limited proteolysis of an immobilized antigen-antibody complex and mass spectrometric peptide mapping. Proc. Natl. Acad. Sci. U. S. A. 87, 9848-9852 (1990)
31. Tian, X., Cecal, R., McLaurin, J., Manea, M., Stefanescu, R., Grau, S., Harnasch, M., Amir, S., Ehrmann, M., St George-Hyslop, P., Kohlmann, M., Przybylski, M.: Identification and structural characterization of carboxy-terminal polypeptides and antibody epitopes of Alzheimer's amyloid precursor protein using high-resolution mass spectrometry. Eur. J. Mass Spectrom. 11, 547-556 (2005)
32. Stefanescu, R., Iacob, R.E., Damoc, E.N., Marquardt, A., Amstalden, E., Manea, M., Perdivara, I., Maftei, M., Paraschiv, G., Przybylski, M.: Mass spectrometric approaches for elucidation of antigenantibody recognition structures in molecular immunology. Eur. J. Mass Spectrom. 13, 69-75 (2007)
33. Petre, B.A., Dragusanu, M., Przybylski, M.: Molecular recognition specificity of anti-3-nitrotyrosine antibodies revealed by affinity-mass spectrometry and immunoanalytical methods. In: Applications of Mass Spectrometry in Life Safety. NATO Science for Peace and Security Series A: Chemistry and Biology, Springer, 55-67 (2008)
34. Abu-Ghazaleh, R.I., Dunnette, S.L., Loegering, D.A., Checkel, J.L., Kita, H., Thomas, L.L., Gleich, G.J.: Eosinophil granule proteins in peripheral blood granulocytes. J. Leukoc. Biol. 52, 611-618 (1992)
35. Rosenberg, H.F., Tenen, D.G., Ackerman, S.J.: Molecular cloning of the human eosinophil-derived neurotoxin: A member of the ribonuclease gene family. Proc. Natl. Acad. Sci. U. S. A. 86, 4460-4464 (1989)
36. http://kops.ub.uni-konstanz.de/volltexte/2009/8502/pdf/ A-Petre-Dissertation.pdf
37. Domachowske, J.B., Dyer, K.D., Adams, A.G., Leto, T.L., Rosenberg, H.F.: Eosinophil cationic protein/RNase 3 is another RNase A-family ribonuclease with direct antiviral activity. Nucleic Acids Res. 26, 3358-3363 (1998)
38. Wu, W., Chen, Y., Hazen, S.L.: Eosinophil peroxidase nitrates protein tyrosyl residues. Implications for oxidative damage by nitrating intermediates in eosinophilic inflammatory disorders. J. Biol. Chem. 274, 25933-25944 (1999)
39. Parastatidis, I., Thomson, L., Fries, D.M., Moore, R.E., Tohyama, J., Fu, X., Hazen, S.L., Heijnen, H.F.J., Dennehy, M.K., Liebler, D.C., Rader, D.J., Ischiropoulos, H.: Increased protein nitration burden in the atherosclerotic lesions and plasma of Apolipoprotein A-I-deficient mice. Circ. Res. 101, 368-376 (2007)
40. Stevens, S.M., Prokai-Tatrai, K., Prokai, L.: Factors that contribute to the misidentification of tyrosine nitration by shotgun proteomics. Mol. Cell. Proteomics 7, 2442-2451 (2008)
41. Prokai, L.: Misidentification of nitrated peptides: Comments on Hong, S.J., Gokulrangan, G., Schöneich, C. 2007. Proteomic analysis of age dependent nitration of rat cardiac proteins by solution isoelectric focusing coupled to nanoHPLC tandem mass spectrometry. Exp. Gerontol. 44, 367-369 (2009)
42. Aslan, M., Ryan, T.M., Townes, T.M., Coward, L., Kirk, M.C., Barnes, S., Alexander, C.B., Rosenfeld, S.S., Freeman, B.A.: Nitric oxide-dependent generation of raective species in sickle cell disease. J. Biol. Chem. 278, 4194-4204 (2003)
43. Mohan, C.G., Boix, E., Evans, H.R., Nikolovski, Z., Nogues, M.V., Cuchillo, C.M., Acharya, K.R.: The crystal structure of eosinophil cationic protein in complex with 2′,5′-ADP at 2.0 A resolution reveals the details of the ribonucleolytic active site. Biochemistry 41, 12100-12106 (2002)
44. Mosimann, S.C., Newton, D.L., Youle, R.J., James, M.N.: X-ray crystallographic structure of recombinant eosinophil-derived neurotoxin at 1.83 A resolution. J. Mol. Biol. 260, 540-552 (1996)
45. Tsodikov, O.V., Record Jr., M.T., Sergeev, Y.V.: Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J. Comput. Chem. 23, 600-609 (2002)
46. Dragusanu, M., Petre, B.A., Przybylski, M.: Epitope motif of an anti-nitrotyrosine antibody specific for tyrosine-nitrated peptides revealed by a combination of affinity approaches and mass spectrometry. J. Peptide Sci. 17, 184-191 (2011)
47. Gow, A.J., Farkouh, C.R., Munson, D.A., Posencheg, M.A., Ischiropoulos, H.: Biological significance of nitric oxide-mediated protein modifications. Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L262-L268 (2004)
48. Lin, H.L., Myshkin, E., Waskell, Hollenberg, P.: Peroxynitrite inactivation of human cytochrome P40s 2B6 and 2E1: Heme modification and and site-specific nitrotyrosine formation. Chem. Res. Toxicol. 20, 1612-1622 (2007)
49. Kemp, B.E., Pearson, R.B.: Protein kinase recognition sequence motifs. Trends Biochem. Sci. 15, 342-346 (1990)
50. Dragusanu, M., Petre, B.A., Slamnoiu, S., Vlad, C., Tu, T., Przybylski, M.: On-line bioaffinity-electrospray mass spectrometry for simultaneous detection, identification, and quantification of protein-ligand interactions. J. Am. Soc. Mass Spectrom. 21, 1643-1648 (2010)
51. Gronewold, T.M.: Surface acoustic wave sensors in the bioanalytical field: Recent trends and challenges. Anal. Chim. Acta 603, 119-128 (2007)
52. Bai, Y., Galetskiy, D., Damoc, E., Paschen, C., Liu, Z., Griese, M., Liu, S., Przybylski, M.: High resolution mass spectrometric alveolar proteomics: Identification of surfactant protein SP-A and SP-D modifications in proteinosis and cystic fibrosis patients. Proteomics 4, 2300-2309 (2004)
53. Bai, Y., Galetskiy, D., Damoc, E., Ripper, J., Woischnik, M., Griese, M., Liu, Z., Liu, S., Przybylski, M.: Lung alveolar proteomics of bronchoalveolar lavage from a pulmonary alveolar proteinosis patient using high-resolution FTICR mass spectrometry. Anal. Bioanal. Chem. 389, 1075-1085 (2007)
54. Doering, G., Goldstein, W., Botzenhart, K., Kharazmi, A., Schiotz, P.O., Hoiby, N., Dasgupta, M.: Elastase from polymorphonuclear leucocytes: A regulatory enzyme in immune complex disease. Clin. Exp. Immunol. 64, 597-605 (1986)