Interactome-wide analysis identifies end-binding protein 1 as a crucial component for the speck-like particle formation of activated absence in melanoma 2 (AIM2) inflammasomes

Molecular and Cellular Proteomics

Volumn 11, Issue 11, 2012, Pages 1230-1244

  Wang, Li Jie ^a   Hsu, Chia Wei ^a   Chen, Chiu Chin ^b   Liang, Ying ^b   Chen, Lih Chyang ^b   Ojcius, David M ^b,d   Tsang, Ngan Ming ^c   Hsueh, Chuen ^b,c   Wu, Chih Ching ^a,b   Chang, Yu Sun ^a,b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSENCE IN MELANOMA 2 INFLAMMASOME; BINDING PROTEIN; CASPASE; CRYOPYRIN; END BINDING PROTEIN 1; HYDROGEN PEROXIDE; INFLAMMASOME; INTERLEUKIN 1BETA; RETINOIC ACID INDUCIBLE PROTEIN I; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ADOLESCENT; ADULT; AGED; ARTICLE; CANCER TISSUE; CARCINOMA CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; FEMALE; FLUORESCENCE MICROSCOPY; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MALE; NASOPHARYNX CARCINOMA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; UNINDEXED SEQUENCE;

ADOLESCENT; ADULT; AGED; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; CYTOSKELETAL PROTEINS; FEMALE; HUMANS; INFLAMMASOMES; ISOTOPE LABELING; MALE; MASS SPECTROMETRY; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; NASOPHARYNGEAL NEOPLASMS; NUCLEAR PROTEINS; POLY DA-DT; PROTEIN BINDING; SIGNAL TRANSDUCTION; YOUNG ADULT;

HUMAN HERPESVIRUS 4;

EID: 84869219269     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.020594     Document Type: Article

References (64)

1. Chan, A. T. (2010) Nasopharyngeal carcinoma. Ann. Oncol. 21 Suppl 7, vii308-312
2. Sriamporn, S., Vatanasapt, V., Pisani, P., Yongchaiyudha, S., and Rungpitarangsri, V. (1992) Environmental risk factors for nasopharyngeal carcinoma: a case-control study in northeastern Thailand. Cancer Epidemiol. Biomarkers Prev. 1, 345-348
3. Bei, J. X., Li, Y., Jia, W. H., Feng, B. J., Zhou, G., Chen, L. Z., Feng, Q. S., Low, H. Q., Zhang, H., He, F., Tai, E. S., Kang, T., Liu, E. T., Liu, J., and Zeng, Y. X. (2010) A genome-wide association study of nasopharyngeal carcinoma identifies three new susceptibility loci. Nat. Genet. 42, 599-603
4. Chang, K. P., Chang, Y. T., Wu, C. C., Liu, Y. L., Chen, M. C., Tsang, N. M., Hsu, C. L., Chang, Y. S., and Yu, J. S. (2011) Multiplexed immunobeadbased profiling of cytokine markers for detection of nasopharyngeal carcinoma and prognosis of patient survival. Head Neck 33, 886-897
5. Apte, R. N., Dotan, S., Elkabets, M., White, M. R., Reich, E., Carmi, Y., Song, X., Dvozkin, T., Krelin, Y., and Voronov, E. (2006) The involvement of IL-1 in tumorigenesis, tumor invasiveness, metastasis and tumor-host interactions. Cancer Metastasis Rev. 25, 387-408 (Pubitemid 44922357)
6. Xie, L., Xu, L., He, Z., Zhou, W., Wang, L., Zhang, L., Lan, K., Ren, C., Liu, W., and Yao, K. (2000) Identification of differentially expressed genes in nasopharyngeal carcinoma by means of the Atlas human cancer cDNA expression array. J. Cancer Res. Clin. Oncol. 126, 400-406 (Pubitemid 30436376)
7. Zhu, Y., Xu, Y., Wei, Y., Liang, W., Liao, M., and Zhang, L. (2008) Association of IL-1B gene polymorphisms with nasopharyngeal carcinoma in a Chinese population. Clin. Oncol. 20, 207-211
8. Martinon, F., Burns, K., and Tschopp, J. (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10, 417-426 (Pubitemid 35007355)
9. Davis, B. K., Wen, H., and Ting, J. P. (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29, 707-735
10. Bryant, C., and Fitzgerald, K. A. (2009) Molecular mechanisms involved in inflammasome activation. Trends Cell Biol. 19, 455-464
11. Duncan, J. A., Bergstralh, D. T., Wang, Y., Willingham, S. B., Ye, Z., Zimmermann, A. G., and Ting, J. P. (2007) Cryopyrin/NALP3 binds ATP/ dATP, is an ATPase, and requires ATP binding to mediate inflammatory signaling. Proc. Natl. Acad. Sci. U.S.A. 104, 8041-8046 (Pubitemid 47185872)
12. Zhou, R., Tardivel, A., Thorens, B., Choi, I., and Tschopp, J. (2010) Thiore-doxin- interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136-140
13. Fernandes-Alnemri, T., Yu, J. W., Datta, P., Wu, J., and Alnemri, E. S. (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509-513
14. Poeck, H., Bscheider, M., Gross, O., Finger, K., Roth, S., Rebsamen, M., Hannesschläger, N., Schlee, M., Rothenfusser, S., Barchet, W., Kato, H., Akira, S., Inoue, S., Endres, S., Peschel, C., Hartmann, G., Hornung, V., and Ruland, J. (2010) Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat. Immunol. 11, 63-69
15. Allen, I. C., TeKippe, E. M., Woodford, R. M., Uronis, J. M., Holl, E. K., Rogers, A. B., Herfarth, H. H., Jobin, C., and Ting, J. P. (2010) The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J. Exp. Med. 207, 1045-1056
16. Zaki, M. H., Vogel, P., Body-Malapel, M., Lamkanfi, M., and Kanneganti, T. D. (2010) IL-18 production downstream of the Nlrp3 inflammasome confers protection against colorectal tumor formation. J. Immunol. 185, 4912-4920
17. Dunn, J. H., Ellis, L. Z., and Fujita, M. (2012) Inflammasomes as molecular mediators of inflammation and cancer: potential role in melanoma. Cancer Lett. 314, 24-33
18. Samanta, M., Iwakiri, D., Kanda, T., Imaizumi, T., and Takada, K. (2006) EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J. 25, 4207-4214 (Pubitemid 44435218)
19. Mayor, A., Martinon, F., De Smedt, T., Pétrilli, V., and Tschopp, J. (2007) A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat. Immunol. 8, 497-503 (Pubitemid 46605918)
20. Matsumiya, T., Imaizumi, T., Yoshida, H., Satoh, K., Topham, M. K., and Stafforini, D. M. (2009) The levels of retinoic acid-inducible gene I are regulated by heat shock protein 90-alpha. J. Immunol. 182, 2717-2725
21. Davis, B. K., Roberts, R. A., Huang, M. T., Willingham, S. B., Conti, B. J., Brickey, W. J., Barker, B. R., Kwan, M., Taxman, D. J., Accavitti-Loper, M. A., Duncan, J. A., and Ting, J. P. (2011) Cutting edge: NLRC5-dependent activation of the inflammasome. J. Immunol. 186, 1333-1337
22. Eitel, J., Meixenberger, K., van Laak, C., Orlovski, C., Hocke, A., Schmeck, B., Hippenstiel, S., N'Guessan, P. D., Suttorp, N., and Opitz, B. (2012) Rac1 regulates the NLRP3 inflammasome which mediates IL-1beta production in Chlamydophila pneumoniae infected human mononuclear cells. PLoS One 7, e30379
23. Muller, A. J., Hoffmann, C., Galle, M., Van Den Broeke, A., Heikenwalder, M., Falter, L., Misselwitz, B., Kremer, M., Beyaert, R., and Hardt, W. D. (2009) The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 6, 125-136
24. Schotte, P., Denecker, G., Van Den Broeke, A., Vandenabeele, P., Cornelis, G. R., and Beyaert, R. (2004) Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1beta. J. Biol. Chem. 279, 25134-25142 (Pubitemid 38756762)
25. Ridley, A. J. (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529
26. Jiang, K., and Akhmanova, A. (2011) Microtubule tip-interacting proteins: a view from both ends. Curr. Opin. Cell Biol. 23, 94-101
27. Berrueta, L., Kraeft, S. K., Tirnauer, J. S., Schuyler, S. C., Chen, L. B., Hill, D. E., Pellman, D., and Bierer, B. E. (1998) The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc. Natl. Acad. Sci. U.S.A. 95, 10596-10601 (Pubitemid 28413113)
28. Wen, Y., Eng, C. H., Schmoranzer, J., Cabrera-Poch, N., Morris, E. J., Chen, M., Wallar, B. J., Alberts, A. S., and Gundersen, G. G. (2004) EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6, 820-830 (Pubitemid 39207247)
29. Morrison, E. E. (2009) The APC-EB1 interaction. Adv. Exp. Med. Biol. 656, 41-50
30. Wang, Y., Zhou, X., Zhu, H., Liu, S., Zhou, C., Zhang, G., Xue, L., Lu, N., Quan, L., Bai, J., Zhan, Q., and Xu, N. (2005) Overexpression of EB1 in human esophageal squamous cell carcinoma (ESCC) may promote cellular growth by activating beta-catenin/TCF pathway. Oncogene 24, 6637-6645
31. Schober, J. M., Cain, J. M., Komarova, Y. A., and Borisy, G. G. (2009) Migration and actin protrusion in melanoma cells are regulated by EB1 protein. Cancer Lett. 284, 30-36
32. Chen, L. C., Chung, I. C., Hsueh, C., Tsang, N. M., Chi, L. M., Liang, Y., Chen, C. C., Wang, L. J., and Chang, Y. S. (2010) The antiapoptotic protein, FLIP, is regulated by heterogeneous nuclear ribonucleoprotein K and correlates with poor overall survival of nasopharyngeal carcinoma patients. Cell Death Differ. 17, 1463-1473
33. Chen, L. C., Chen, C. C., Liang, Y., Tsang, N. M., Chang, Y. S., and Hsueh, C. (2011) A novel role for TNFAIP2: its correlation with invasion and metastasis in nasopharyngeal carcinoma. Mod. Pathol. 24, 175-184
34. Chen, L. C., Liu, H. P., Li, H. P., Hsueh, C., Yu, J. S., Liang, C. L., and Chang, Y. S. (2009) Thymidine phosphorylase mRNA stability and protein levels are increased through ERK-mediated cytoplasmic accumulation of hnRNP K in nasopharyngeal carcinoma cells. Oncogene 28, 1904-1915
35. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (Pubitemid 41830195)
36. Griffin, T. J., Xie, H., Bandhakavi, S., Popko, J., Mohan, A., Carlis, J. V., and Higgins, L. (2007) iTRAQ reagent-based quantitative proteomic analysis on a linear ion trap mass spectrometer. J. Proteome Res. 6, 4200-4209 (Pubitemid 350158498)
37. Bantscheff, M., Boesche, M., Eberhard, D., Matthieson, T., Sweetman, G., and Kuster, B. (2008) Robust and sensitive iTRAQ quantification on an LTQ Orbitrap mass spectrometer. Mol. Cell. Proteomics 7, 1702-1713
38. Liu, H. P., Wu, C. C., Kao, H. Y., Huang, Y. C., Liang, Y., Chen, C. C., Yu, J. S., and Chang, Y. S. (2011) Proteome-wide dysregulation by PRA1 depletion delineates a role of PRA1 in lipid transport and cell migration. Mol. Cell. Proteomics 10, 10.1074/mcp.M900641-MCP200
39. Mueller, L. N., Brusniak, M. Y., Mani, D. R., and Aebersold, R. (2008) An assessment of software solutions for the analysis of mass spectrometry based quantitative proteomics data. J. Proteome Res. 7, 51-61 (Pubitemid 351171115)
40. Nesvizhskii, A. I., Vitek, O., and Aebersold, R. (2007) Analysis and validation of proteomic data generated by tandem mass spectrometry. Nat. Methods 4, 787-797 (Pubitemid 350055575)
41. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (Pubitemid 35215372)
42. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (Pubitemid 37082259)
43. Khan, A. P., Poisson, L. M., Bhat, V. B., Fermin, D., Zhao, R., Kalyana- Sundaram, S., Michailidis, G., Nesvizhskii, A. I., Omenn, G. S., Chinnaiyan, A. M., and Sreekumar, A. (2010) Quantitative proteomic profiling of prostate cancer reveals a role for miR-128 in prostate cancer. Mol. Cell. Proteomics 9, 298-312
44. Chen, L. C., Hsueh, C., Tsang, N. M., Liang, Y., Chang, K. P., Hao, S. P., Yu, J. S., and Chang, Y. S. (2008) Heterogeneous ribonucleoprotein k and thymidine phosphorylase are independent prognostic and therapeutic markers for nasopharyngeal carcinoma. Clin. Cancer Res. 14, 3807-3813
45. Yu, C. J., Chang, K. P., Chang, Y. J., Hsu, C. W., Liang, Y., Yu, J. S., Chi, L. M., Chang, Y. S., and Wu, C. C. (2011) Identification of guanylatebinding protein 1 as a potential oral cancer marker involved in cell invasion using omics-based analysis. J. Proteome Res. 10, 3778-3788
46. Chang, Y. T., Wu, C. C., Shyr, Y. M., Chen, T. C., Hwang, T. L., Yeh, T. S., Chang, K. P., Liu, H. P., Liu, Y. L., Tsai, M. H., Chang, Y. S., and Yu, J. S. (2011) Secretome-based identification of ULBP2 as a novel serum marker for pancreatic cancer detection. PloS one 6, e20029
47. Hu, B., Elinav, E., and Flavell, R. A. (2011) Inflammasome-mediated suppression of inflammation-induced colorectal cancer progression is mediated by direct regulation of epithelial cell proliferation. Cell Cycle 10, 1936-1939
48. Verma, D., Bivik, C., Farahani, E., Synnerstad, I., Fredrikson, M., Enerback, C., Rosdahl, I., and Soderkvist, P. (2012) Inflammasome polymorphisms confer susceptibility to sporadic malignant melanoma. Pigment Cell Melanoma Res., in press
49. McCartney, R. G., Rice, J. E., Sanderson, S. J., Bunik, V., Lindsay, H., and Lindsay, J. G. (1998) Subunit interactions in the mammalian alphaketoglutarate dehydrogenase complex. Evidence for direct association of the alpha-ketoglutarate dehydrogenase and dihydrolipoamide dehydrogenase components. J. Biol. Chem. 273, 24158-24164 (Pubitemid 28435762)
50. Panagiotidis, C. A., Huang, S. C., Tsirka, S. A., Kyriakidis, D. A., and Canellakis, E. S. (1988) Regulation of polyamine biosynthesis in Escherichia coli by the acidic antizyme and the ribosomal proteins S20 and L34. Adv. Exp. Med. Biol. 250, 13-24
51. Bessat, M., and Ersfeld, K. (2009) Functional characterization of cohesin SMC3 and separase and their roles in the segregation of large and minichromosomes in Trypanosoma brucei. Mol. Microbiol. 71, 1371-1385
52. Kazerounian, S., Yee, K. O., and Lawler, J. (2008) Thrombospondins in cancer. Cell. Mol. Life Sci. 65, 700-712
53. Krüger, M., and Linke, W. A. (2009) Titin-based mechanical signalling in normal and failing myocardium. J. Mol. Cell Cardiol. 46, 490-498
54. Broz, P., and Monack, D. M. (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunol. Rev. 243, 174-190
55. Sahab, Z. J., Hall, M. D., Zhang, L., Cheema, A. K., and Byers, S. W. (2010) Tumor Suppressor RARRES1 Regulates DLG2, PP2A, VCP, EB1, and Ankrd26. J. Cancer 1, 14-22
56. Orimo, T., Ojima, H., Hiraoka, N., Saito, S., Kosuge, T., Kakisaka, T., Yokoo, H., Nakanishi, K., Kamiyama, T., Todo, S., Hirohashi, S., and Kondo, T. (2008) Proteomic profiling reveals the prognostic value of adenomatous polyposis coli-end-binding protein 1 in hepatocellular carcinoma. Hepatology 48, 1851-1863
57. Ralhan, R., Desouza, L. V., Matta, A., Chandra Tripathi, S., Ghanny, S., Datta Gupta, S., Bahadur, S., and Siu, K. W. (2008) Discovery and verification of head-and-neck cancer biomarkers by differential protein expression analysis using iTRAQ labeling, multidimensional liquid chromatography, and tandem mass spectrometry. Mol. Cell. Proteomics 7, 1162-1173 (Pubitemid 351943962)
58. Agard, N. J., Maltby, D., and Wells, J. A. (2010) Inflammatory stimuli regulate caspase substrate profiles. Mol. Cell. Proteomics 9, 880-893
59. Lamkanfi, M., Kanneganti, T. D., Van Damme, P., Vanden Berghe, T., Vanoverberghe, I., Vandekerckhove, J., Vandenabeele, P., Gevaert, K., and Nunez, G. (2008) Targeted peptidecentric proteomics reveals caspase-7 as a substrate of the caspase-1 inflammasomes. Mol. Cell. Proteomics 7, 2350-2363
60. Patel, P. C., Fisher, K. H., Yang, E. C., Deane, C. M., and Harrison, R. E. (2009) Proteomic analysis of microtubule-associated proteins during macrophage activation. Mol. Cell. Proteomics 8, 2500-2514
61. Dagenais, M., Skeldon, A., and Saleh, M. (2012) The inflammasome: in memory of Dr. Jurg Tschopp. Cell Death Differ. 19, 5-12
62. Honnappa, S., Gouveia, S. M., Weisbrich, A., Damberger, F. F., Bhavesh, N. S., Jawhari, H., Grigoriev, I., van Rijssel, F. J., Buey, R. M., Lawera, A., Jelesarov, I., Winkler, F. K., Wuthrich, K., Akhmanova, A., and Steinmetz, M. O. (2009) An EB1-binding motif acts as a microtubule tip localization signal. Cell 138, 366-376
63. Jin, T., Perry, A., Jiang, J., Smith, P., Curry, J. A., Unterholzner, L., Jiang, Z., Horvath, G., Rathinam, V. A., Johnstone, R. W., Hornung, V., Latz, E., Bowie, A. G., Fitzgerald, K. A., and Xiao, T. S. (2012) Structures of the HIN Domain:DNA Complexes Reveal Ligand Binding and Activation Mechanisms of the AIM2 Inflammasome and IFI16 Receptor. Immunity 36, 561-571
64. Okamoto, M., Liu, W., Luo, Y., Tanaka, A., Cai, X., Norris, D. A., Dinarello, C. A., and Fujita, M. (2010) Constitutively active inflammasome in human melanoma cells mediating autoinflammation via caspase-1 processing and secretion of interleukin-1beta. J. Biol. Chem. 285, 6477-6488