Insights into K-Ras 4B regulation by post-translational lysine acetylation

References

Baines, A.T., Xu, D., and Der, C.J. (2011). Inhibition of Ras for cancer treatment: the search continues. Future Med. Chem. 3, 1787–1808.10.4155/fmc.11.121Suche in Google Scholar PubMed PubMed Central

Boriack-Sjodin, P.A., Margarit, S.M., Bar-Sagi, D., and Kuriyan, J. (1998). The structural basis of the activation of Ras by Sos. Nature 394, 337–343.10.1038/28548Suche in Google Scholar PubMed

Bos, J.L. (1989). Ras oncogenes in human cancer: a review. Cancer Res. 49, 4682–4689.Suche in Google Scholar

Bos, J.L., Rehmann, H., and Wittinghofer, A. (2007). GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865–877.10.1016/j.cell.2007.05.018Suche in Google Scholar PubMed

Buhrman, G., Holzapfel, G., Fetics, S., and Mattos, C. (2010). Allosteric modulation of ras positions Q61 for a direct role in catalysis. Proc. Natl. Acad. Sci. USA 107, 4931–4936.10.1073/pnas.0912226107Suche in Google Scholar PubMed PubMed Central

Cacev, T., Radosevic, S., Spaventi, R., Pavelic, K., and Kapitanovic, S. (2005). NF1 gene loss of heterozygosity and expression analysis in sporadic colon cancer. Gut 54, 1129–1135.10.1136/gut.2004.053348Suche in Google Scholar PubMed PubMed Central

Capella, G., Cronauer-Mitra, S., Pienado, M.A., and Perucho, M. (1991). Frequency and spectrum of mutations at codons 12 and 13 of the c-K-ras gene in human tumors. Environ. Health Perspect 93, 125–131.10.1289/ehp.9193125Suche in Google Scholar PubMed PubMed Central

Castellano, E. and Santos, E. (2011). Functional specificity of ras isoforms: so similar but so different. Genes Cancer 2, 216–231.10.1177/1947601911408081Suche in Google Scholar PubMed PubMed Central

Choudhary, C., Kumar, C., Gnad, F., Nielsen, M.L., Rehman, M., Walther, T.C., Olsen, J.V., and Mann, M. (2009). Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834–840.10.1126/science.1175371Suche in Google Scholar PubMed

Cogoi, S., Codognotto, A., Rapozzi, V., Meeuwenoord, N., van der Marel, G., and Xodo, L.E. (2005). Transcription inhibition of oncogenic KRAS by a mutation-selective peptide nucleic acid conjugated to the PKKKRKV nuclear localization signal peptide. Biochemistry 44, 10510–10519.10.1021/bi0505215Suche in Google Scholar PubMed

Corbeel, L. and Freson, K. (2008). Rab proteins and rab-associated proteins: major actors in the mechanism of protein-trafficking disorders. Eur. J. Pediatr. 167, 723–729.10.1007/s00431-008-0740-zSuche in Google Scholar PubMed PubMed Central

Cox, J., Neuhauser, N., Michalski, A., Scheltema, R.A., Olsen, J.V., and Mann, M. (2011). Andromeda: a peptide search engine integrated into the maxquant environment. J. Proteome Res. 10, 1794–1805.10.1021/pr101065jSuche in Google Scholar PubMed

D’Souza-Schorey, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347–358.10.1038/nrm1910Suche in Google Scholar PubMed

de Boor, S., Knyphausen, P., Kuhlmann, N., Wroblowski, S., Brenig, J., Scislowski, L., Baldus, L., Nolte, H., Kruger, M., and Lammers, M. (2015). Small GTP-binding protein ran is regulated by posttranslational lysine acetylation. Proc. Natl. Acad. Sci. USA 112, E3679–E3688.10.1073/pnas.1505995112Suche in Google Scholar PubMed PubMed Central

Deacon, S.W. and Gelfand, V.I. (2001). Of yeast, mice, and men. Rab proteins and organelle transport. J. Cell Biol. 152, F21–F24.10.1083/jcb.152.4.F21Suche in Google Scholar

DeLano, W.L. (2002). The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.Suche in Google Scholar

Der, C.J. (1989). The ras family of oncogenes. Cancer Treat Res 47, 73–119.10.1007/978-1-4613-1599-5_4Suche in Google Scholar PubMed

Dhomen, N. and Marais, R. (2007). New insight into BRAF mutations in cancer. Curr. Opin. Genet. Dev. 17, 31–39.10.1016/j.gde.2006.12.005Suche in Google Scholar PubMed

Dutta, D. and Donaldson, J.G. (2015). Rab and Arf G proteins in endosomal trafficking. Methods Cell Biol. 130, 127–138.10.1016/bs.mcb.2015.04.004Suche in Google Scholar PubMed PubMed Central

Fernandez-Medarde, A. and Santos, E. (2011). Ras in cancer and developmental diseases. Genes. Cancer 2, 344–358.10.1177/1947601911411084Suche in Google Scholar PubMed PubMed Central

Fujimoto, H., Higuchi, M., Koike, M., Ode, H., Pinak, M., Bunta, J.K., Nemoto, T., Sakudoh, T., Honda, N., Maekawa, H., et al. (2012). A possible overestimation of the effect of acetylation on lysine residues in KQ mutant analysis. J. Comput. Chem. 33, 239–246.10.1002/jcc.21956Suche in Google Scholar PubMed

Garnett, M.J. and Marais, R. (2004). Guilty as charged: B-RAF is a human oncogene. Cancer Cell 6, 313–319.10.1016/j.ccr.2004.09.022Suche in Google Scholar PubMed

Gasper, R., Meyer, S., Gotthardt, K., Sirajuddin, M., and Wittinghofer, A. (2009). It takes two to tango: regulation of G proteins by dimerization. Nat. Rev. Mol. Cell Biol. 10, 423–429.10.1038/nrm2689Suche in Google Scholar PubMed

Gelb, B.D. and Tartaglia, M. (2006). Noonan syndrome and related disorders: dysregulated RAS-mitogen activated protein kinase signal transduction. Hum. Mol. Genet. 15 Spec No 2, R220–R226.10.1093/hmg/ddl197Suche in Google Scholar PubMed

Giehl, K. (2005). Oncogenic Ras in tumour progression and metastasis. Biol. Chem. 386, 193–205.10.1515/BC.2005.025Suche in Google Scholar PubMed

Gremer, L., Gilsbach, B., Ahmadian, M.R., and Wittinghofer, A. (2008). Fluoride complexes of oncogenic Ras mutants to study the Ras-RasGap interaction. Biol. Chem. 389, 1163–1171.10.1515/BC.2008.132Suche in Google Scholar PubMed

Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509–514.10.1126/science.279.5350.509Suche in Google Scholar PubMed

Hall, A. (2012). Rho family GTPases. Biochem. Soc. Trans. 40, 1378–1382.10.1042/BST20120103Suche in Google Scholar PubMed

Iversen, L., Tu, H.L., Lin, W.C., Christensen, S.M., Abel, S.M., Iwig, J., Wu, H.J., Gureasko, J., Rhodes, C., Petit, R.S., et al. (2014). Molecular kinetics. Ras activation by SOS: allosteric regulation by altered fluctuation dynamics. Science 345, 50–54.10.1126/science.1250373Suche in Google Scholar PubMed PubMed Central

James, G., Goldstein, J.L., and Brown, M.S. (1996). Resistance of K-RasBV12 proteins to farnesyltransferase inhibitors in Rat1 cells. Proc. Natl. Acad. Sci. USA 93, 4454–4458.10.1073/pnas.93.9.4454Suche in Google Scholar PubMed PubMed Central

Johnson, B., Goldberg-Strassler, D., Gripp, K., Thacker, M., Leoni, C., and Stevenson, D. (2015). Function and disability in children with Costello syndrome and Cardiofaciocutaneous syndrome. Am. J. Med. Genet. A 167A, 40–44.10.1002/ajmg.a.36828Suche in Google Scholar PubMed

Jorge, A.A., Malaquias, A.C., Arnhold, I.J., and Mendonca, B.B. (2009). Noonan syndrome and related disorders: a review of clinical features and mutations in genes of the RAS/MAPK pathway. Horm. Res. 71, 185–193.10.1159/000201106Suche in Google Scholar PubMed

Jura, N., Scotto-Lavino, E., Sobczyk, A., and Bar-Sagi, D. (2006). Differential modification of Ras proteins by ubiquitination. Mol. Cell 21, 679–687.10.1016/j.molcel.2006.02.011Suche in Google Scholar PubMed

Knyphausen, P., Kuhlmann, N., de Boor, S., and Lammers, M. (2015). Lysine-acetylation as a fundamental regulator of Ran function: implications for signaling of proteins of the Ras-superfamily. Small GTPases 6, 189–195.10.1080/21541248.2015.1103399Suche in Google Scholar PubMed PubMed Central

Kompier, L.C., Lurkin, I., van der Aa, M.N., van Rhijn, B.W., van der Kwast, T.H., and Zwarthoff, E.C. (2010). FGFR3, HRAS, KRAS, NRAS and PIK3CA mutations in bladder cancer and their potential as biomarkers for surveillance and therapy. PLoS One 5, e13821.10.1371/journal.pone.0013821Suche in Google Scholar PubMed PubMed Central

Kratz, C.P., Schubbert, S., Bollag, G., Niemeyer, C.M., Shannon, K.M., and Zenker, M. (2006). Germline mutations in components of the Ras signaling pathway in Noonan syndrome and related disorders. Cell Cycle 5, 1607–1611.10.4161/cc.5.15.3128Suche in Google Scholar PubMed

Kuhlmann, N., Wroblowski, S., Knyphausen, P., de Boor, S., Brenig, J., Zienert, A.Y., Meyer-Teschendorf, K., Praefcke, G.J., Nolte, H., Kruger, M., et al. (2016a). Structural and mechanistic insights into the regulation of the fundamental Rho regulator RhoGDIα by lysine acetylation. J. Biol. Chem. 291, 5484–5499.10.1074/jbc.M115.707091Suche in Google Scholar PubMed PubMed Central

Kuhlmann, N., Wroblowski, S., Scislowski, L., and Lammers, M. (2016b). RhoGDIα acetylation at K127 and K141 affects binding toward nonprenylated RhoA. Biochemistry 55, 304–312.10.1021/acs.biochem.5b01242Suche in Google Scholar PubMed

Lammers, M., Neumann, H., Chin, J.W., and James, L.C. (2010). Acetylation regulates cyclophilin A catalysis, immunosuppression and HIV isomerization. Nat. Chem. Biol. 6, 331–337.10.1038/nchembio.342Suche in Google Scholar PubMed PubMed Central

Lerner, E.C., Qian, Y., Blaskovich, M.A., Fossum, R.D., Vogt, A., Sun, J., Cox, A.D., Der, C.J., Hamilton, A.D., and Sebti, S.M. (1995). Ras CAAX peptidomimetic FTI-277 selectively blocks oncogenic Ras signaling by inducing cytoplasmic accumulation of inactive Ras-Raf complexes. J. Biol. Chem. 270, 26802–26806.10.1074/jbc.270.45.26802Suche in Google Scholar PubMed

Lerner, E.C., Zhang, T.T., Knowles, D.B., Qian, Y., Hamilton, A.D., and Sebti, S.M. (1997). Inhibition of the prenylation of K-Ras, but not H- or N-Ras, is highly resistant to CAAX peptidomimetics and requires both a farnesyl transferase and a geranylgeranyl transferase I inhibitor in human tumor cell lines. Oncogene. 15, 1283–1288.10.1038/sj.onc.1201296Suche in Google Scholar PubMed

Lin, W.C., Iversen, L., Tu, H.L., Rhodes, C., Christensen, S.M., Iwig, J.S., Hansen, S.D., Huang, W.Y., and Groves, J.T. (2014). H-Ras forms dimers on membrane surfaces via a protein-protein interface. Proc. Natl. Acad. Sci. USA 111, 2996–3001.10.1073/pnas.1321155111Suche in Google Scholar PubMed PubMed Central

Lundby, A., Lage, K., Weinert, B.T., Bekker-Jensen, D.B., Secher, A., Skovgaard, T., Kelstrup, C.D., Dmytriyev, A., Choudhary, C., Lundby, C., et al. (2012). Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep. 2, 419–431.10.1016/j.celrep.2012.07.006Suche in Google Scholar

Marais, R., Light, Y., Paterson, H.F., Mason, C.S., and Marshall, C.J. (1997). Differential regulation of Raf-1, A-Raf, and B-Raf by oncogenic ras and tyrosine kinases. J. Biol. Chem. 272, 4378–4383.10.1074/jbc.272.7.4378Suche in Google Scholar

Margarit, S.M., Sondermann, H., Hall, B.E., Nagar, B., Hoelz, A., Pirruccello, M., Bar-Sagi, D., and Kuriyan, J. (2003). Structural evidence for feedback activation by Ras.GTP of the Ras-specific nucleotide exchange factor SOS. Cell 112, 685–695.10.1016/S0092-8674(03)00149-1Suche in Google Scholar

McCormick, F. (1997). The superfamily of Ras-related GTPases. Jpn. J. Cancer Res. 88, inside front cover.Suche in Google Scholar

Melchior, F. (2001). Ran GTPase cycle: oOne mechanism -- two functions. Curr. Biol. 11, R257–260.10.1016/S0960-9822(01)00132-4Suche in Google Scholar

Muratcioglu, S., Chavan, T.S., Freed, B.C., Jang, H., Khavrutskii, L., Freed, R.N., Dyba, M.A., Stefanisko, K., Tarasov, S.G., Gursoy, A., et al. (2015). GTP-dependent K-Ras dimerization. Structure 23, 1325–1335.10.1016/j.str.2015.04.019Suche in Google Scholar PubMed PubMed Central

Myers, A., Bernstein, J.A., Brennan, M.L., Curry, C., Esplin, E.D., Fisher, J., Homeyer, M., Manning, M.A., Muller, E.A., Niemi, A.K., et al. (2014). Perinatal features of the RASopathies: Noonan syndrome, cardiofaciocutaneous syndrome and Costello syndrome. Am. J. Med. Genet. A 164A, 2814–2821.10.1002/ajmg.a.36737Suche in Google Scholar PubMed

Nam, J.S., Ino, Y., Sakamoto, M., and Hirohashi, S. (2002). Ras farnesylation inhibitor FTI-277 restores the E-cadherin/catenin cell adhesion system in human cancer cells and reduces cancer metastasis. Jpn J. Cancer Res. 93, 1020–1028.10.1111/j.1349-7006.2002.tb02479.xSuche in Google Scholar PubMed PubMed Central

Nan, X., Tamguney, T.M., Collisson, E.A., Lin, L.J., Pitt, C., Galeas, J., Lewis, S., Gray, J.W., McCormick, F., and Chu, S. (2015). Ras-GTP dimers activate the mitogen-activated protein kinase (MAPK) pathway. Proc. Natl. Acad. Sci. USA 112, 7996–8001.10.1073/pnas.1509123112Suche in Google Scholar PubMed PubMed Central

Nava, C., Hanna, N., Michot, C., Pereira, S., Pouvreau, N., Niihori, T., Aoki, Y., Matsubara, Y., Arveiler, B., Lacombe, D., et al. (2007). Cardio-facio-cutaneous and noonan syndromes due to mutations in the RAS/MAPK signalling pathway: genotype-phenotype relationships and overlap with Costello syndrome. J. Med. Genet. 44, 763–771.10.1136/jmg.2007.050450Suche in Google Scholar PubMed PubMed Central

Neumann, H., Peak-Chew, S.Y., and Chin, J.W. (2008). Genetically encoding N(epsilon)-acetyllysine in recombinant proteins. Nat. Chem. Biol. 4, 232–234.10.1038/nchembio.73Suche in Google Scholar PubMed

Omholt, K., Karsberg, S., Platz, A., Kanter, L., Ringborg, U., and Hansson, J. (2002). Screening of N-ras codon 61 mutations in paired primary and metastatic cutaneous melanomas: mutations occur early and persist throughout tumor progression. Clin. Cancer Res. 8, 3468–3474.Suche in Google Scholar

Pai, E.F., Kabsch, W., Krengel, U., Holmes, K.C., John, J., and Wittinghofer, A. (1989). Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature 341, 209–214.10.1038/341209a0Suche in Google Scholar

Pai, E.F., Krengel, U., Petsko, G.A., Goody, R.S., Kabsch, W., and Wittinghofer, A. (1990). Refined crystal structure of the triphosphate conformation of H-ras p21 at 1.35 a resolution: implications for the mechanism of GTP hydrolysis. EMBO. J. 9, 2351–2359.10.1002/j.1460-2075.1990.tb07409.xSuche in Google Scholar

Pincus, M.R. (2004). Development of new anti-cancer peptides from conformational energy analysis of the oncogenic ras-p21 protein and its complexes with target proteins. Front. Biosci. 9, 3486–3509.10.2741/1496Suche in Google Scholar

Pylayeva-Gupta, Y., Grabocka, E., and Bar-Sagi, D. (2011). RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer 11, 761–774.10.1038/nrc3106Suche in Google Scholar

Rappsilber, J., Mann, M., and Ishihama, Y. (2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protocols 2, 1896–1906.10.1038/nprot.2007.261Suche in Google Scholar

Rojas, A.M., Fuentes, G., Rausell, A., and Valencia, A. (2012). The Ras protein superfamily: evolutionary tree and role of conserved amino acids. J. Cell Biol. 196, 189–201.10.1083/jcb.201103008Suche in Google Scholar

Sasaki, A.T., Carracedo, A., Locasale, J.W., Anastasiou, D., Takeuchi, K., Kahoud, E.R., Haviv, S., Asara, J.M., Pandolfi, P.P., and Cantley, L.C. (2011). Ubiquitination of K-Ras enhances activation and facilitates binding to select downstream effectors. Sci. Signal 4, ra13.10.1126/scisignal.2001518Suche in Google Scholar

Scheffzek, K., Ahmadian, M.R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997). The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333–338.10.1126/science.277.5324.333Suche in Google Scholar

Scheidig, A.J., Burmester, C., and Goody, R.S. (1999). The pre-hydrolysis state of p21(ras) in complex with GTP: new insights into the role of water molecules in the GTP hydrolysis reaction of ras-like proteins. Structure 7, 1311–1324.10.1016/S0969-2126(00)80021-0Suche in Google Scholar

Schlichting, I., Wittinghofer, A., and Rosch, P. (1988). Proton NMR studies of the GDP.Mg²⁺ complex of the Ha-ras oncogene product p21. Biochem. Biophys. Res. Commun. 150, 444–448.10.1016/0006-291X(88)90540-2Suche in Google Scholar

Siegelin, M.D. and Borczuk, A.C. (2014). Epidermal growth factor receptor mutations in lung adenocarcinoma. Lab. Invest. 94, 129–137.10.1038/labinvest.2013.147Suche in Google Scholar

Song, E.H., Oh, W., Ulu, A., Carr, H.S., Zuo, Y., and Frost, J.A. (2015). Acetylation of the RhoA GEF Net1A controls its subcellular localization and activity. J. Cell Sci. 128, 913–922.10.1242/jcs.158121Suche in Google Scholar

Sot, B., Behrmann, E., Raunser, S., and Wittinghofer, A. (2013). Ras GTPase activating (RasGAP) activity of the dual specificity GAP protein rasal requires colocalization and C2 domain binding to lipid membranes. Proc. Natl. Acad Sci. USA 110, 111–116.10.1073/pnas.1201658110Suche in Google Scholar

Spoerner, M., Nuehs, A., Ganser, P., Herrmann, C., Wittinghofer, A., and Kalbitzer, H.R. (2005). Conformational states of Ras complexed with the GTP analogue GppNHp or GppCH2p: implications for the interaction with effector proteins. Biochemistry 44, 2225–2236.10.1021/bi0488000Suche in Google Scholar

Stark, Z., Gillessen-Kaesbach, G., Ryan, M.M., Cirstea, I.C., Gremer, L., Ahmadian, M.R., Savarirayan, R., and Zenker, M. (2012). Two novel germline KRAS mutations: expanding the molecular and clinical phenotype. Clin. Genet. 81, 590–594.10.1111/j.1399-0004.2011.01754.xSuche in Google Scholar

Unni, S., Huang, Y., Hanson, R.M., Tobias, M., Krishnan, S., Li, W.W., Nielsen, J.E., and Baker, N.A. (2011). Web servers and services for electrostatics calculations with APBS and PDB2PQR. J. Comput. Chem. 32, 1488–1491.10.1002/jcc.21720Suche in Google Scholar

Vetter, I.R. and Wittinghofer, A. (2001). The guanine nucleotide-binding switch in three dimensions. Science 294, 1299–1304.10.1126/science.1062023Suche in Google Scholar

Vigil, D., Cherfils, J., Rossman, K.L., and Der, C.J. (2010). Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat. Rev. Cancer 10, 842–857.10.1038/nrc2960Suche in Google Scholar

Wan, P.T., Garnett, M.J., Roe, S.M., Lee, S., Niculescu-Duvaz, D., Good, V.M., Jones, C.M., Marshall, C.J., Springer, C.J., Barford, D., et al. (2004). Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116, 855–867.10.1016/S0092-8674(04)00215-6Suche in Google Scholar

Wey, M., Lee, J., Jeong, S.S., Kim, J., and Heo, J. (2013). Kinetic mechanisms of mutation-dependent Harvey ras activation and their relevance for the development of costello syndrome. Biochemistry 52, 8465–8479.10.1021/bi400679qSuche in Google Scholar PubMed PubMed Central

Whyte, D.B., Kirschmeier, P., Hockenberry, T.N., Nunez-Oliva, I., James, L., Catino, J.J., Bishop, W.R., and Pai, J.K. (1997). K- and N-Ras are geranylgeranylated in cells treated with farnesyl protein transferase inhibitors. J. Biol. Chem. 272, 14459–14464.10.1074/jbc.272.22.14459Suche in Google Scholar PubMed

Wittinghofer, A. (2005). Signaling via GTP-binding proteins of the Ras superfamily. Febs. J. 272, 5–5.Suche in Google Scholar

Yang, M.H., Nickerson, S., Kim, E.T., Liot, C., Laurent, G., Spang, R., Philips, M.R., Shan, Y., Shaw, D.E., Bar-Sagi, D., et al. (2012). Regulation of RAS oncogenicity by acetylation. Proc. Natl. Acad. Sci. USA 109, 10843–10848.10.1073/pnas.1201487109Suche in Google Scholar PubMed PubMed Central

Yang, M.H., Laurent, G., Bause, A.S., Spang, R., German, N., Haigis, M.C., and Haigis, K.M. (2013). HDAC6 and SIRT2 regulate the acetylation state and oncogenic activity of mutant K-RAS. Mol. Cancer Res. 11, 1072–1077.10.1158/1541-7786.MCR-13-0040-TSuche in Google Scholar PubMed PubMed Central

Yu, S.H., Wang, T.H., and Au, L.C. (2009). Specific repression of mutant K-RAS by 10-23 DNAzyme: sensitizing cancer cell to anti-cancer therapies. Biochem. Biophys. Res. Commun. 378, 230–234.10.1016/j.bbrc.2008.11.027Suche in Google Scholar PubMed

Zimmermann, G., Papke, B., Ismail, S., Vartak, N., Chandra, A., Hoffmann, M., Hahn, S.A., Triola, G., Wittinghofer, A., Bastiaens, P.I., et al. (2013). Small molecule inhibition of the KRAS-PDEδ interaction impairs oncogenic KRAS signalling. Nature 497, 638–642.10.1038/nature12205Suche in Google Scholar PubMed