Quantitative phosphoproteomic analysis of IL-33-mediated signaling

Proteomics

Volumn 15, Issue 2-3, 2015, Pages 532-544

  Pinto, Sneha M ^a,b,c   Nirujogi, Raja Sekhar ^a,d   Rojas, Pamela Leal ^c,e   Patil, Arun H ^a,f   Manda, Srikanth S ^a,d   Subbannayya, Yashwanth ^a   Roa, Juan Carlos ^g   Chatterjee, Aditi ^a   Prasad, T S Keshava ^a,b   Pandey, Akhilesh ^c,h,i  

^a INSTITUTE OF BIOINFORMATICS   (India)

^b MANIPAL UNIVERSITY   (India)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d PONDICHERRY UNIVERSITY   (India)

^e UNIVERSIDAD DE LA FRONTERA   (Chile)

^f KIIT UNIVERSITY   (India)

^g Biofísica y Bioinformática   (Chile)

^h ADRIENNE HELIS MALVIN MEDICAL RESEARCH FOUNDATION   (United States)

ⁱ Diana Helis Henry Medical Research Foundation   (United States)

Author keywords

Cell biology; Immune disorders; Immunoaffinity purification; Inflammation; RhoGTPases

Indexed keywords

INTERLEUKIN 33; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 2; NICOTINAMIDE ADENINE DINUCLEOTIDE KINASE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 12; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RECEPTOR INTERACTING SERINE THREONINE KINASE 1; SYNAPTOJANIN; UNCLASSIFIED DRUG; INTERLEUKIN 6; PHOSPHOPEPTIDE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; ASTHMA; CONTROLLED STUDY; MACROPHAGE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; IMMUNOLOGY; MACROPHAGE; MASS SPECTROMETRY; MOLECULAR GENETICS; MOUSE; PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; INTERLEUKIN-6; MACROPHAGES; MASS SPECTROMETRY; MICE; MOLECULAR SEQUENCE DATA; PHOSPHOPEPTIDES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN INTERACTION MAPS; PROTEIN KINASES; PROTEINS; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84921321002     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400303     Document Type: Article

References (59)

1. Schmitz, J., Owyang, A., Oldham, E., Song, Y. et al., IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005, 23, 479-490.
2. Carriere, V., Roussel, L., Ortega, N., Lacorre, D. A. et al., IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. USA 2007, 104, 282-287.
3. Baekkevold, E. S., Roussigne, M., Yamanaka, T., Johansen, F. E. et al., Molecular characterization of NF-HEV, a nuclear factor preferentially expressed in human high endothelial venules. Am. J. Pathol. 2003, 163, 69-79.
4. Moussion, C., Ortega, N., Girard, J. P., The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'? PLoS One 2008, 3, e3331.
5. Cayrol, C., Girard, J. P., The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc. Natl. Acad. Sci. USA 2009, 106, 9021-9026.
6. + T cells: induction of type 2 cytokine production by T1/ST2 cross-linking. J. Immunol. 2001, 166, 3143-3150.
7. Allakhverdi, Z., Smith, D. E., Comeau, M. R., Delespesse, G., Cutting edge: the ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J. Immunol. 2007, 179, 2051-2054.
8. Besnard, A. G., Togbe, D., Guillou, N., Erard, F. et al., IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur. J. Immunol. 2011, 41, 1675-1686.
9. Komai-Koma, M., Gilchrist, D. S., McKenzie, A. N., Goodyear, C. S. et al., IL-33 activates B1 cells and exacerbates contact sensitivity. J. Immunol. 2011, 186, 2584-2591.
10. Villarreal, D. O., Wise, M. C., Walters, J. N., Reuschel, E. L. et al., Alarmin IL-33 acts as an immunoadjuvant to enhance antigen-specific tumor immunity. Cancer Res. 2014, 74, 1789-1800.
11. + T cells. Eur. J. Immunol. 2011, 41, 3351-3360.
12. Seki, K., Sanada, S., Kudinova, A. Y., Steinhauser, M. L. et al., Interleukin-33 prevents apoptosis and improves survival after experimental myocardial infarction through ST2 signaling. Circ. Heart Fail. 2009, 2, 684-691.
13. Funakoshi-Tago, M., Tago, K., Hayakawa, M., Tominaga, S. et al., TRAF6 is a critical signal transducer in IL-33 signaling pathway. Cell. Signal. 2008, 20, 1679-1686.
14. Prefontaine, D., Lajoie-Kadoch, S., Foley, S., Audusseau, S. et al., Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J. Immunol. 2009, 183, 5094-5103.
15. Guo, Z., Wu, J., Zhao, J., Liu, F. et al., IL-33 promotes airway remodeling and is a marker of asthma disease severity. J. Asthma 2014, 51, 863-869
16. Savinko, T., Matikainen, S., Saarialho-Kere, U., Lehto, M. et al., IL-33 and ST2 in atopic dermatitis: expression profiles and modulation by triggering factors. J. Invest. Dermatol. 2012, 132, 1392-1400.
17. Imai, Y., Yasuda, K., Sakaguchi, Y., Haneda, T. et al., Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. Proc. Natl. Acad. Sci. USA 2013, 110, 13921-13926.
18. Marvie, P., Lisbonne, M., L'Helgoualc'h, A., Rauch, M. et al., Interleukin-33 overexpression is associated with liver fibrosis in mice and humans. J. Cell. Mol. Med. 2010, 14, 1726-1739.
19. Rankin, A. L., Mumm, J. B., Murphy, E., Turner, S. et al., IL-33 induces IL-13-dependent cutaneous fibrosis. J. Immunol. 2010, 184, 1526-1535.
20. McHedlidze, T., Waldner, M., Zopf, S., Walker, J. et al., Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 2013, 39, 357-371.
21. Pushparaj, P. N., Li, D., Komai-Koma, M., Guabiraba, R. et al., Interleukin-33 exacerbates acute colitis via interleukin-4 in mice. Immunology 2013, 140, 70-77.
22. Beltran, C. J., Nunez, L. E., Diaz-Jimenez, D., Farfan, N. et al., Characterization of the novel ST2/IL-33 system in patients with inflammatory bowel disease. Inflamm. Bowel Dis. 2010, 16, 1097-1107.
23. Ross, R., Ross, X. L., Ghadially, H., Lahr, T. et al., Mouse Langerhans cells differentially express an activated T cell-attracting CC chemokine. J. Invest. Dermatol. 1999, 113, 991-998.
24. Hong, J., Bae, S., Jhun, H., Lee, S. et al., Identification of constitutively active interleukin 33 (IL-33) splice variant. J. Biol. Chem. 2011, 286, 20078-20086.
25. Yang, Z., Grinchuk, V., Urban, J. F., Jr., Bohl, J. et al., Macrophages as IL-25/IL-33-responsive cells play an important role in the induction of type 2 immunity. PLoS One 2013, 8, e59441.
26. Harsha, H. C., Molina, H., Pandey, A., Quantitative proteomics using stable isotope labeling with amino acids in cell culture. Nat. Protoc. 2008, 3, 505-516.
27. Rush, J., Moritz, A., Lee, K. A., Guo, A. et al., Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23, 94-101.
28. Rappsilber, J., Ishihama, Y., Mann, M., Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75, 663-670.
29. Selvan, L. D., Renuse, S., Kaviyil, J. E., Sharma, J. et al., Phosphoproteome of Cryptococcus neoformans. J. Proteomics 2014, 97, 287-295.
30. Vizcaino, J. A., Deutsch, E. W., Wang, R., Csordas, A. et al., ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 2014, 32, 223-226.
31. Mi, H., Muruganujan, A., Casagrande, J. T., Thomas, P. D., Large-scale gene function analysis with the PANTHER classification system. Nat. Protoc. 2013, 8, 1551-1566.
32. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M. et al., Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014, 42, D199-D205.
33. Huang da, W., Sherman, B. T., Lempicki, R. A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4, 44-57.
34. Chou, M. F., Schwartz, D., Biological sequence motif discovery using motif-x. Curr. Protoc. Bioinformatics 2011, Chapter 13, Unit 13, 15-24.
35. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., Jorgensen, T. J., Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 2005, 4, 873-886.
36. Brint, E. K., Fitzgerald, K. A., Smith, P., Coyle, A. J. et al., Characterization of signaling pathways activated by the interleukin 1 (IL-1) receptor homologue T1/ST2. A role for Jun N-terminal kinase in IL-4 induction. J. Biol. Chem. 2002, 277, 49205-49211.
37. Choi, Y. S., Choi, H. J., Min, J. K., Pyun, B. J. et al., Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production. Blood 2009, 114, 3117-3126.
38. Tare, N., Li, H., Morschauser, A., Cote-Sierra, J. et al., KU812 cells provide a novel in vitro model of the human IL-33/ST2L axis: functional responses and identification of signaling pathways. Exp. Cell Res. 2010, 316, 2527-2537.
39. Yagami, A., Orihara, K., Morita, H., Futamura, K. et al., IL-33 mediates inflammatory responses in human lung tissue cells. J. Immunol. 2010, 185, 5743-5750.
40. Yang, Y., Xia, F., Hermance, N., Mabb, A. et al., A cytosolic ATM/NEMO/RIP1 complex recruits TAK1 to mediate the NF-kappaB and p38 mitogen-activated protein kinase (MAPK)/MAPK-activated protein 2 responses to DNA damage. Mol. Cell. Biol. 2011, 31, 2774-2786.
41. Shim, J. H., Xiao, C., Paschal, A. E., Bailey, S. T. et al., TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 2005, 19, 2668-2681.
42. Ben-Levy, R., Leighton, I. A., Doza, Y. N., Attwood, P. et al., Identification of novel phosphorylation sites required for activation of MAPKAP kinase-2. EMBO J. 1995, 14, 5920-5930.
43. Engel, K., Schultz, H., Martin, F., Kotlyarov, A. et al., Constitutive activation of mitogen-activated protein kinase-activated protein kinase 2 by mutation of phosphorylation sites and an A-helix motif. J. Biol. Chem. 1995, 270, 27213-27221.
44. Feng, J., Ito, M., Ichikawa, K., Isaka, N. et al., Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J. Biol. Chem. 1999, 274, 37385-37390.
45. Weiner, O. D., Neilsen, P. O., Prestwich, G. D., Kirschner, M. W. et al., A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 2002, 4, 509-513.
46. Nobes, C. D., Hall, A., Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81, 53-62.
47. Yndestad, A., Marshall, A. K., Hodgkinson, J. D., Tham el, L. et al., Modulation of interleukin signalling and gene expression in cardiac myocytes by endothelin-1. Int. J. Biochem. Cell Biol. 2010, 42, 263-272.
48. Chow, J. Y., Wong, C. K., Cheung, P. F., Lam, C. W., Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: implications for allergic inflammation. Cell. Mol. Immunol. 2010, 7, 26-34.
49. Funakoshi-Tago, M., Tago, K., Sato, Y., Tominaga, S., Kasahara, T., JAK2 is an important signal transducer in IL-33-induced NF-kappaB activation. Cell. Signal. 2011, 23, 363-370.
50. Garton, A. J., Tonks, N. K., PTP-PEST: a protein tyrosine phosphatase regulated by serine phosphorylation. EMBO J. 1994, 13, 3763-3771.
51. Habets, G. G., Scholtes, E. H., Zuydgeest, D., van der Kammen, R. A. et al., Identification of an invasion-inducing gene, Tiam-1, that encodes a protein with homology to GDP-GTP exchangers for Rho-like proteins. Cell 1994, 77, 537-549.
52. Hordijk, P. L., ten Klooster, J. P., van der Kammen, R. A., Michiels, F. et al., Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 1997, 278, 1464-1466.
53. Kunda, P., Paglini, G., Quiroga, S., Kosik, K., Caceres, A., Evidence for the involvement of Tiam1 in axon formation. J. Neurosci. 2001, 21, 2361-2372.
54. Satoh, A., Nakanishi, H., Obaishi, H., Wada, M. et al., Neurabin-II/spinophilin. An actin filament-binding protein with one pdz domain localized at cadherin-based cell-cell adhesion sites. J. Biol. Chem. 1998, 273, 3470-3475.
55. Yamamoto, K., Murata, H., Putranto, E. W., Kataoka, K. et al., DOCK7 is a critical regulator of the RAGE-Cdc42 signaling axis that induces formation of dendritic pseudopodia in human cancer cells. Oncol. Rep. 2013, 29, 1073-1079.
56. Vadlamudi, R. K., Li, F., Adam, L., Nguyen, D. et al., Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 2002, 4, 681-690.
57. O'Neill, L. A., Bird, T. A., Gearing, A. J., Saklatvala, J., Interleukin-1 signal transduction. Increased GTP binding and hydrolysis in membranes of a murine thymoma line (EL4). J. Biol. Chem. 1990, 265, 3146-3152.
58. Singh, R., Wang, B., Shirvaikar, A., Khan, S. et al., The IL-1 receptor and Rho directly associate to drive cell activation in inflammation. J. Clin. Invest. 1999, 103, 1561-1570.
59. Bagrodia, S., Derijard, B., Davis, R. J., Cerione, R. A., Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 1995, 270, 27995-27998.