An analysis of the phosphoproteome of immune cell lines exposed to the immunomodulatory mycotoxin deoxynivalenol

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 7, 2011, Pages 850-857

  Nogueira Da Costa, André ^a,d   Keen, Jeffrey N ^b   Wild, Christopher P ^a   Findlay, John B C ^b,c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^d INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

Biomarker; Deoxynivalenol; Mycotoxin; Phosphoproteomics

Indexed keywords

BIOLOGICAL MARKER; ELONGATION FACTOR 2; GROWTH FACTOR RECEPTOR; HEAT SHOCK COGNATE PROTEIN 71; HEAT SHOCK PROTEIN; INITIATION FACTOR 3; MYCOTOXIN; NUCLEOSIDE DIPHOSPHATE KINASE A; PHOSPHOPROTEIN; PROTEIN SUBUNIT; PROTEOME; TETRAHYDROFOLIC ACID; UNCLASSIFIED DRUG; VOMITOXIN;

ARTICLE; BIOSYNTHESIS; CARBON METABOLISM; CELL LINE; CONCENTRATION (PARAMETERS); EUKARYOTE; EXPERIMENT; FLOW CYTOMETRY; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; IMMUNE FUNCTION TEST; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LEUKEMIA CELL LINE; LYMPHOCYTE; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; REPRODUCIBILITY; SIGNAL TRANSDUCTION;

B-LYMPHOCYTES; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLOW CYTOMETRY; HUMANS; LYMPHOCYTES; MYCOTOXINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; T-LYMPHOCYTES; TIME FACTORS; TRICHOTHECENES;

EUKARYOTA;

EID: 79957600783     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.04.001     Document Type: Article

References (63)

1. B.A. Rotter, D.B. Prelusky, and J.J. Pestka Toxicology of deoxynivalenol (vomitoxin) J. Toxicol. Environ. Health 48 1996 1 34
2. F.Q. Li, Y.W. Li, X.Y. Luo, and T. Yoshizawa Fusarium toxins in wheat from an area in Henan Province, PR China, with a previous human red mould intoxication episode Food Addit. Contam. 19 2002 163 167 (Pubitemid 34092966)
3. C.P. Wild, and A.J. Hall Epidemiology of mycotoxin related diseases H. Miller, The Mycota VI. Human and Animal Relationships 1996 Springer-Verlag Berlin 213 225
4. D.M. Hughes, M.J. Gahl, C.H. Graham, and S.L. Grieb Overt signs of toxicity to dogs and cats of dietary deoxynivalenol J. Anim. Sci. 77 1999 693 700 (Pubitemid 129599681)
5. F. Iverson, C. Armstrong, E. Nera, J. Truelove, S. Fernie, P. Scott, R. Stapley, S. Hayward, and S. Gunner Chronic feeding study of deoxynivalenol in B6C3F1 male and female mice Teratog. Carcinog. Mutagen. 15 1995 283 306 (Pubitemid 26159568)
6. A. Gutzwiller, L. Czegledi, P. Stoll, and L. Bruckner Effects of Fusarium toxins on growth, humoral immune response and internal organs in weaner pigs, and the efficacy of apple pomace as an antidote J. Anim. Physiol. Anim. Nutr. 91 2007 432 438 (Pubitemid 47382871)
7. J. van de Walle, B. Romier, Y. Larondelle, and Y.-J. Schneider Influence of deoxynivalenol on NF-kappaB activation and IL-8 secretion in human intestinal Caco-2 cells Toxicol. Lett. 177 2008 205 214
8. C.J. Amuzie, J. Shinozuka, and J.J. Pestka Induction of suppressors of cytokine signaling by the trichothecene deoxynivalenol in the mouse Toxicol. Sci. 111 2009 277 287
9. P. Pinton, F. Accensi, E. Beauchamp, A.M. Cossalter, P. Callu, F. Grosjean, and I.P. Oswald Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses Toxicol. Lett. 177 2008 215 222
10. X.A. Wu, M. Kohut, J. Cunnick, T. Bailey, and S. Hendrich Deoxynivalenol suppresses circulating and splenic leukocyte subpopulations in BALB/c mice: dose response, time course and sex differences Food Addit. Contam. A Chem. Anal. Control Expo. Risk Assess. 26 2009 1070 1080
11. J.J. Pestka, and A.T. Smolinski Deoxynivalenol: toxicology and potential effects on humans J. Toxicol. Environ. Health B Crit. Rev. 8 2005 39 69 (Pubitemid 40066025)
12. F.A. Meky, P.C. Turner, A.E. Ashcroft, J.D. Miller, Y.L. Qiao, M.J. Roth, and C.P. Wild Development of a urinary biomarker of human exposure to deoxynivalenol Food Chem. Toxicol. 41 2003 265 273 (Pubitemid 35447876)
13. P.C. Turner, R.P. Hopton, Y. Lecluse, K.L.M. White, J. Fisher, and P. Lebailly Determinants of urinary deoxynivalenol and de-epoxy deoxynivalenol in male farmers from Normandy, France J. Agric. Food Chem. 58 2010 5206 5212
14. P.C. Turner, J.A. Rothwell, K.L.M. White, Y. Gong, J.E. Cade, and C.P. Wild Urinary deoxynivalenol is correlated with cereal intake in individuals from the United Kingdom Environ. Health Perspect. 116 2008 21 25
15. E.J. Kim, S.H. Jeong, J.H. Cho, H.O. Ku, H.M. Pyo, H.G. Kang, and K.H. Choi Plasma haptoglobin and immunoglobulins as diagnostic indicators of deoxynivalenol intoxication J. Vet. Sci. 9 2008 257 266
16. A. Nogueira da Costa, R.S. Mijal, J.N. Keen, J.B.C. Findlay, C.P. Wild, Proteomic analysis of the effects of the immunomodulatory mycotoxin deoxynivalenol, Proteomics (2011) Mar 9. doi:10.1002/pmic.201000580.
17. L. Severino, R. Russo, D. Luongo, R. De Luna, R. Ciarcia, and M. Rossi Immune effects of four Fusarium-toxins (FB1, ZEA, NIV, DON) on the proliferation of Jurkat cells and porcine lymphocytes: in vitro study Vet. Res. Commun. 32 Suppl 1 2008 S311 S313
18. R.R. Bartelt, N. Cruz-Orcutt, M. Collins, and J.C.D. Houtman Comparison of T cell receptor-induced proximal signaling and downstream functions in immortalized and primary T cells PLoS One 4 2009 e5430
19. P.C. Turner, V.J. Burley, J.A. Rothwell, K.L.M. White, J.E. Cade, and C.P. Wild Deoxynivalenol: rationale for development and application of a urinary biomarker Food Addit. Contam. 25 2008 864 871 (Pubitemid 351917194)
20. R.T. Abraham, and A. Weiss Jurkat T cells and development of the T-cell receptor signalling paradigm Nat. Rev. Immunol. 4 2004 301 308 (Pubitemid 38478665)
21. W. Parson, R. Kirchebner, R. Muhlmann, K. Renner, A. Kofler, S. Schmidt, and R. Kofler Cancer cell line identification by short tandem repeat profiling: power and limitations FASEB J. 19 2005 434 436 (Pubitemid 40316541)
22. K.S.A. Khabar, L. al-Haj, F. al-Zoghaibi, M. Marie, M. Dhalla, S.J. Polyak, and B.R.G. Williams Expressed gene clusters associated with cellular sensitivity and resistance towards anti-viral and anti-proliferative actions of interferon J. Mol. Biol. 342 2004 833 846 (Pubitemid 39165653)
23. Y. Sugita-Konishi, and J.J. Pestka Differential upregulation of TNF-alpha, IL-6, and IL-8 production by deoxynivalenol (vomitoxin) and other 8-ketotrichothecenes in a human macrophage model J. Toxicol. Environ. Health A 64 2001 619 636 (Pubitemid 33132017)
24. R.L. Uzarski, Z. Islam, and J.J. Pestka Potentiation of trichothecene-induced leukocyte cytotoxicity and apoptosis by TNF-alpha and Fas activation Chem. Biol. Interact. 146 2003 105 119 (Pubitemid 37323875)
25. M. Murakami, R. Kaul, P. Kumar, and E.S. Robertson Nucleoside diphosphate kinase/Nm23 and Epstein-Barr virus Mol. Cell. Biochem. 329 2009 131 139
26. J. Biggs, E. Hersperger, P.S. Steeg, L.A. Liotta, and A. Shearn A drosophila gene that is homologous to a mammalain gene associated with tumor metastasis codes for a nucleoside diphosphate kinase Cell 63 1990 933 940 (Pubitemid 120034934)
27. N. Hailat, D.R. Keim, R.F. Melhem, X.X. Zhu, C. Eckerskorn, G.M. Brodeur, C.P. Reynolds, R.C. Seeger, F. Lottspeich, J.R. Strahler, and S.M. Hanash High levels of p19/nm23 protein in neuroblastoma are associated with advanced stage disease and with N-myc gene amplification J. Clin. Invest. 88 1991 341 345
28. J. Okabe-Kado, T. Kasukabe, Y. Honma, H. Kobayashi, N. Maseki, and Y. Kaneko Extracellular NM23 protein promotes the growth and survival of primary cultured human acute myelogenous leukemia cells Cancer Sci. 100 2009 1885 1894
29. B. Youn, H.D. Kim, and J. Kim Nm23-H1/nucleoside diphosphate kinase as a key molecule in breast tumor angiogenesis Expert Opin. Ther. Targets 12 2008 1419 1430
30. V. Mayya, D.H. Lundgren, S.I. Hwang, K. Rezaul, L.F. Wu, J.K. Eng, V. Rodionov, and D.K. Han Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein - protein interactions Sci. Signal. 2 2009 A37 A52
31. J. Okabe-Kado, T. Kasukabe, Y. Honma, H. Kobayashi, N. Maseki, and Y. Kaneko Extracellular NM23-H1 protein inhibits the survival of primary cultured normal human peripheral blood mononuclear cells and activates the cytokine production Int. J. Hematol. 90 2009 143 152
32. A.J. MacFarlane, C.A. Perry, H.H. Girnary, D. Gao, R.H. Allen, S.P. Stabler, B. Shane, and P.J. Stover MTDHFD1 is an essential gene in mice and alters biomarkers of impaired one-carbon metabolism J. Biol. Chem. 284 2009 1533 1539
33. K.M. Howard, S.J. Muga, L.W. Zhang, A.E. Thigpen, and D.R. Appling Characterization of the rat cytoplasmic C-1-tetrahydrofolate synthase gene and analysis of its expression in liver regeneration and fetal development Gene 319 2003 85 97 (Pubitemid 37346203)
34. S. Gez, B. Crossett, and R.I. Christopherson Differentially expressed cytosolic proteins in human leukemia and lymphoma cell lines correlate with lineages and functions Biochim. Biophys. Acta Proteins Proteomics 1774 2007 1173 1183 (Pubitemid 47333247)
35. T. Ivanovic, M.A. Agosto, K. Chandran, and M.L. Nibert A role for molecular chaperone Hsc70 in reovirus outer capsid disassembly J. Biol. Chem. 282 2007 12210 12219 (Pubitemid 47100676)
36. S.L. Nunes, and S.K. Calderwood Heat shock gactor I and the heat shock cognate 70 protein associate in high molecular weight complexes in the cytoplasm of NIH-3T3 cells Biochem. Biophys. Res. Commun. 213 1995 1 6
37. M.U. Alam, J.A. Harken, A.M. Knorn, A.R. Elford, K. Wigmore, P.S. Ohashi, and D.G. Millar Transgenic expression of Hsc70 in pancreatic islets enhances autoimmune diabetes in response to beta cell damage J. Immunol. 183 2009 5728 5737
38. M. Egerton, R.L. Moritz, R. Druker, A. Kelso, and L.J. Simpson Identification of the 70kD heat shock cognate protein (Hsc70) and alpha-actinin-1 as novel phosphotyrosine-containing proteins in T lymphocytes Biochem. Biophys. Res. Commun. 224 1996 666 674 (Pubitemid 26278644)
39. P.S. Wehner, B. Nielsen, and M. Hokland Expression levels of hsc70 and hsp60 are developmentally regulated during B-cell maturation and not associated to childhood c-ALL at presentation or relapse Eur. J. Haematol. 71 2003 100 108 (Pubitemid 36951642)
40. N. Zou, L.H. Ao, J.C. Cleveland, X.P. Yang, X. Su, G.Y. Cai, A. Banerjee, D.A. Fullerton, and X.Z. Meng Critical role of extracellular heat shock cognate protein 70 in the myocardial inflammatory response and cardiac dysfunction after global ischemia-reperfusion Am. J. Physiol. Heart Circ. Physiol. 294 2008 H2805 H2813
41. C.M. Fletcher, T.V. Pestova, C.U.T. Hellen, and G. Wagner Structure and interactions of the translation initiation factor eIF1 EMBO J. 18 1999 2631 2637 (Pubitemid 29213292)
42. N. Methot, M.S. Song, and N. Sonenberg A region rich in aspartic acid, arginine, tyrosine, and glycine (DRYG) mediates eukaryotic initiation factor 4B (eIF4B) self-association and interaction with eIF3 Mol. Cell. Biol. 16 1996 5328 5334 (Pubitemid 26315051)
43. L. Valasek, K.H. Nielsen, and A.G. Hinnebusch Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo EMBO J. 21 2002 5886 5898 (Pubitemid 35315286)
44. X.H. Chen, S.B. Fu, F. Chen, H.Y. Chen, and Z. Chen Identification of tumor-associated antigens in human hepatocellular carcinoma by autoantibodies Oncol. Rep. 20 2008 979 985
45. W.Y. Shen, H. Liu, and Y.N. Yu Translation initiation proteins, ubiquitin-proteasome system related proteins, and 14-3-3 proteins as response proteins in FL cells exposed to anti-benzo[a]pyrene-7,8-dihydrodiol-9,10-epoxide Proteomics 8 2008 3450 3468
46. H.R. Zhou, A.S. Lau, and J.J. Pestka Role of double-stranded RNA-activated protein kinase R (PKR) in deoxynivalenol-induced ribotoxic stress response Toxicol. Sci. 74 2003 335 344 (Pubitemid 36958302)
47. J.I. Azconaolivera, Y. Ouyang, J. Murtha, F.S. Chu, and J.J. Pestka Induction of cytokine messenger-RNAs in mice after oral -exposure to the trichothecene vomitoxin (deoxynivalenol) - Relationship to toxin distribution and protein-synthesis inhibition Toxicol. Appl. Pharmacol. 133 1995 109 120
48. Y.J. Chung, H.R. Zhou, and J.J. Pestka Transcriptional and posttranscriptional roles for p38 mitogen-activated protein kinase in upregulation of TNF-alpha expression by deoxynivalenol (vomitoxin) Toxicol. Appl. Pharmacol. 193 2003 188 201 (Pubitemid 37476434)
49. A.M. Osman, J.L.A. Pennings, M. Blokland, A. Peijnenburg, and H. van Loveren Protein expression profiling of mouse thymoma cells upon exposure to the trichothecene deoxynivalenol (DON): implications for its mechanism of action J. Immunotoxicol. 7 2010 147 156
50. L. Miranda, S. Horman, I. De Potter, L. Hue, J. Jensen, and M.H. Rider Effects of contraction and insulin on protein synthesis, AMP-activated protein kinase and phosphorylation state of translation factors in rat skeletal muscle Pflugers Arch. Eur. J. Physiol. 455 2008 1129 1140 (Pubitemid 351169983)
51. N.T. Redpath, N.T. Price, K.V. Severinov, and C.G. Proud Regulation of elongation factor-2 by multisite phosphorylation Eur. J. Biochem. 213 1993 689 699 (Pubitemid 23125638)
52. A.G. Ryazanov, E.A. Shestakova, and P.G. Natapov Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation Nature 334 1988 170 173
53. J.E. Kim, S.R. Tannenbaum, and F.M. White Global phosphoproteome of HT-29 human colon adenocarcinoma cells J. Proteome Res. 4 2005 1339 1346 (Pubitemid 41208690)
54. L. Orsatti, E. Forte, L. Tomei, M. Caterino, A. Pessi, and F. Talamo 2-D Difference in gel electrophoresis combined with Pro-Q Diamond staining: a successful approach for the identification of kinase/phosphatase targets Electrophoresis 30 2009 2469 2476
55. S. Doll, J.A. Schrickx, S. Danicke, and J. Fink-Gremmels Deoxynivalenol-induced cytotoxicity, cytokines and related genes in unstimulated or lipopolysaccharide stimulated primary porcine macrophages Toxicol. Lett. 184 2009 97 106
56. S.G. Li, A.D. Couvillon, B.B. Brasher, and R.A. Van Etten Tyrosine phosphorylation of Grb2 by Bcr/Abl and epidermal growth factor receptor: a novel regulatory mechanism for tyrosine kinase signaling EMBO J. 20 2001 6793 6804 (Pubitemid 33134209)
57. E. Haines, P. Minoo, Z. Feng, N. Resalatpanah, X.M. Nie, M. Campiglio, L. Alvarez, E. Cocolakis, M. Ridha, M. Di Fulvio, J. Gomez-Cambronero, J.J. Lebrun, and S. Ali Tyrosine phosphorylation of GRB2: role in prolactin/epidermal growth factor cross talk in mammary epithelial cell growth and differentiation Mol. Cell. Biol. 29 2009 2505 2520
58. N. Engels, L.M. Konig, C. Heemann, J. Lutz, T. Tsubata, S. Griep, V. Schrader, and J. Wienands Recruitment of the cytoplasmic adaptor Grb2 to surface IgG and IgE provides antigen receptor-intrinsic costimulation to class-switched B cells Nat. Immunol. 10 2009 1018 1764
59. T. Kaji, S. Hachimura, W. Ise, and S. Kaminogawa Proteome analysis reveals caspase activation in hyporesponsive CD4 T lymphocytes induced in vivo by the oral administration of antigen J. Biol. Chem. 278 2003 27836 27843 (Pubitemid 36899976)
60. Y. Liu, and W.G. Zhang Identification of a new transmembrane adaptor protein that constitutively binds Grb2 in B cells J. Leukoc. Biol. 84 2008 842 851
61. Y. Moon, H. Yang, and S.H. Lee Modulation of early growth response gene I and interieukin-8 expression by ribotoxin deoxynivalenol (vomitoxin) via ERK1/2 in human epithelial intestine 407 cells Biochem. Biophys. Res. Commun. 362 2007 256 262 (Pubitemid 47332399)
62. J.J. Pestka, R.L. Uzarski, and Z. Islam Induction of apoptosis and cytokine production in the Jurkat human T cells by deoxynivalenol: role of mitogen-activated protein kinases and comparison to other 8-ketotrichothecenes Toxicology 206 2005 207 219 (Pubitemid 39601033)
63. H.R. Zhou, Z. Islam, and J.J. Pestka Rapid, sequential activation of mitogen-activated protein kinases and transcription factors precedes proinflammatory cytokine mRNA expression in spleens of mice exposed to the trichothecene vomitoxin Toxicol. Sci. 72 2003 130 142 (Pubitemid 36336442)