SNObase, a database for S-nitrosation modification

Abstract

S-Nitros(yl)ation is a ubiquitous redox-based posttranslational modification of protein cysteine thiols by nitric oxide or its derivatives, which transduces the bioactivity of nitric oxide (NO) by regulation of protein conformation, activity, stability, localization and protein- protein interactions. These years, more and more S-nitrosated proteins were identified in physiological and pathological processes and the number is still growing. Here we developed a database named SNObase (http://www.nitrosation.org), which collected S-nitrosation targets extracted from literatures up to June 1st, 2012. SNObase contained 2561 instances, and provided information about S-nitrosation targets, sites, biological model, related diseases, trends of S-nitrosation level and effects of S-nitrosation on protein function. With SNObase, we did functional analysis for all the SNO targets: In the gene ontology (GO) biological process category, some processes were discovered to be related to S-nitrosation (“response to drug”, “regulation of cell motion”) besides the previously reported related processes. In the GO cellular component category, cytosol and mitochondrion were both enriched. From the KEGG pathway enrichment results, we found SNO targets were enriched in different diseases, which suggests possible significant roles of S-nitrosation in the progress of these diseases. This SNObase means to be a database with precise, comprehensive and easily accessible information, an environment to help researchers integrate data with comparison and relevancy analysis between different groups or works, and also an SNO knowledgebase offering feasibility for systemic and global analysis of S-nitrosation in interdisciplinary studies.

Key words： S-nitrosation; S-nitrosylation; database; S-Nitrosothiol (SNO)

References

[1] Atochina-Vasserman, E.N., Winkler, C., Abramova, H., Schaumann, F., Krug, N., Gow, A.J., Beers, M.F., and Hohlfeld, J.M. (2011). Segmental allergen challenge alters multimeric structure and function of surfactant protein D in humans. Am J Respir Crit Care Med 183, 856-864 .10.1164/rccm.201004-0654OC
[2] Broillet, M.C. (1999). S-nitrosylation of proteins. Cell Mol Life Sci 55, 1036-1042 .10.1007/s000180050354
[3] Carvalho-Filho, M.A., Ueno, M., Hirabara, S.M., Seabra, A.B., Carvalheira, J.B., de Oliveira, M.G., Velloso, L.A., Curi, R., and Saad, M.J. (2005). S-nitrosation of the insulin receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance. Diabetes 54, 959-967 .10.2337/diabetes.54.4.959
[4] Chanvorachote, P., Nimmannit, U., Stehlik, C., Wang, L., Jiang, B.H., Ongpipatanakul, B., and Rojanasakul, Y. (2006). Nitric oxide regulates cell sensitivity to cisplatin-induced apoptosis through S-nitrosylation and inhibition of Bcl-2 ubiquitination. Cancer Res 66, 6353-6360 .10.1158/0008-5472.CAN-05-4533
[5] Cheah, J.H., Kim, S.F., Hester, L.D., Clancy, K.W., Patterson, S.E., 3rd, Papadopoulos, V., and Snyder, S.H. (2006). NMDA receptor-nitric oxide transmission mediates neuronal iron homeostasis via the GTPase Dexras1. Neuron 51, 431-440 .10.1016/j.neuron.2006.07.011
[6] Chernorudskiy, A.L., Garcia, A., Eremin, E.V., Shorina, A.S., Kondratieva, E.V., and Gainullin, M.R. (2007). UbiProt: a database of ubiquitylated proteins. BMC Bioinformatics 8, 126.10.1186/1471-2105-8-126
[7] Chung, K.K., Thomas, B., Li, X., Pletnikova, O., Troncoso, J.C., Marsh, L., Dawson, V.L., and Dawson, T.M. (2004). S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304, 1328-1331 .10.1126/science.1093891
[8] Gnad, F., Ren, S., Cox, J., Olsen, J.V., Macek, B., Oroshi, M., and Mann, M. (2007). PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol 8, R250.10.1186/gb-2007-8-11-r250
[9] Hansen, J.E., Lund, O., Nielsen, J.O., and Brunak, S. (1996). O-GLYCBASE: a revised database of O-glycosylated proteins. Nucleic Acids Res 24, 248-252 .10.1093/nar/24.1.248
[10] Hara, M.R., Agrawal, N., Kim, S.F., Cascio, M.B., Fujimuro, M., Ozeki, Y., Takahashi, M., Cheah, J.H., Tankou, S.K., Hester, L.D., . (2005). S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7, 665-674 .10.1038/ncb1268
[11] Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., and Stamler, J.S. (2005). Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6, 150-166 .10.1038/nrm1569
[12] Huang da, W., Sherman, B.T., Tan, Q., Kir, J., Liu, D., Bryant, D., Guo, Y., Stephens, R., Baseler, M.W., Lane, H.C., . (2007). DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 35, W169-175 .
[13] Huang, Y., Man, H.Y., Sekine-Aizawa, Y., Han, Y., Juluri, K., Luo, H., Cheah, J., Lowenstein, C., Huganir, R.L., and Snyder, S.H. (2005). S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors. Neuron 46, 533-540 .10.1016/j.neuron.2005.03.028
[14] Lane, P., Hao, G., and Gross, S.S. (2001). S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: head-to-head comparison with O-phosphorylation. Sci STKE 2001, re1.10.1126/stke.2001.86.re1
[15] Liu, Z., Cao, J., Gao, X., Zhou, Y., Wen, L., Yang, X., Yao, X., Ren, J., and Xue, Y. (2011). CPLA 1.0: an integrated database of protein lysine acetylation. Nucleic Acids Res 39, D1029-1034 .10.1093/nar/gkq939
[16] Mannick, J.B., Hausladen, A., Liu, L., Hess, D.T., Zeng, M., Miao, Q.X., Kane, L.S., Gow, A.J., and Stamler, J.S. (1999). Fas-induced caspase denitrosylation. Science 284, 651-654 .10.1126/science.284.5414.651
[17] Marozkina, N.V., Yemen, S., Borowitz, M., Liu, L., Plapp, M., Sun, F., Islam, R., Erdmann-Gilmore, P., Townsend, R.R., Lichti, C.F., . (2010). Hsp 70/Hsp 90 organizing protein as a nitrosylation target in cystic fibrosis therapy. Proc Natl Acad Sci U S A 107, 11393-11398 .10.1073/pnas.0909128107
[18] Mohr, S., Stamler, J.S., and Brune, B. (1996). Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment. J Biol Chem 271, 4209-4214 .10.1074/jbc.271.8.4209
[19] Molina y Vedia, L., McDonald, B., Reep, B., Brune, B., Di Silvio, M., Billiar, T.R., and Lapetina, E.G. (1992). Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation. J Biol Chem 267, 24929-24932 .
[20] Nakamura, T., Wang, L., Wong, C.C., Scott, F.L., Eckelman, B.P., Han, X., Tzitzilonis, C., Meng, F., Gu, Z., Holland, E.A., . (2010). Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Mol Cell 39, 184-195 .10.1016/j.molcel.2010.07.002
[21] Saura, M., Zaragoza, C., McMillan, A., Quick, R.A., Hohenadl, C., Lowenstein, J.M., and Lowenstein, C.J. (1999). An antiviral mechanism of nitric oxide: inhibition of a viral protease. Immunity 10, 21-28 .10.1016/S1074-7613(00)80003-5
[22] Seth, D., and Stamler, J.S. (2011). The SNO-proteome: causation and classifications. Curr Opin Chem Biol 15, 129-136 .10.1016/j.cbpa.2010.10.012
[23] Sun, J., Picht, E., Ginsburg, K.S., Bers, D.M., Steenbergen, C., and Murphy, E. (2006). Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 98, 403-411 .10.1161/01.RES.0000202707.79018.0a
[24] Uys, J.D., Xiong, Y., and Townsend, D.M. (2011). Nitrosative stress-induced S-glutathionylation of protein disulfide isomerase. Methods Enzymol 490, 321-332 .10.1016/B978-0-12-385114-7.00018-0