1,257
Views
47
CrossRef citations to date
0
Altmetric
Research Paper

An improved isoprenylcysteine carboxylmethyltransferase inhibitor induces cancer cell death and attenuates tumor growth in vivo

, , , , , , & show all
Pages 1280-1291 | Received 06 May 2014, Accepted 22 Jun 2014, Published online: 27 Jun 2014

References

  • Berndt N, Hamilton AD, Sebti SM. Targeting protein prenylation for cancer therapy. Nat Rev Cancer 2011; 11:775 - 91; http://dx.doi.org/10.1038/nrc3151; PMID: 22020205
  • Gao J, Liao J, Yang GY. CAAX-box protein, prenylation process and carcinogenesis. Am J Transl Res 2009; 1:312 - 25; PMID: 19956441
  • Ahearn IM, Haigis K, Bar-Sagi D, Philips MR. Regulating the regulator: post-translational modification of RAS. Nat Rev Mol Cell Biol 2012; 13:39 - 51; http://dx.doi.org/10.1038/nrm3255; PMID: 22189424
  • Casey PJ, Seabra MC. Protein prenyltransferases. J Biol Chem 1996; 271:5289 - 92; http://dx.doi.org/10.1074/jbc.271.10.5289; PMID: 8621375
  • Otto JC, Kim E, Young SG, Casey PJ. Cloning and characterization of a mammalian prenyl protein-specific protease. J Biol Chem 1999; 274:8379 - 82; http://dx.doi.org/10.1074/jbc.274.13.8379; PMID: 10085068
  • Dai Q, Choy E, Chiu V, Romano J, Slivka SR, Steitz SA, Michaelis S, Philips MR. Mammalian prenylcysteine carboxyl methyltransferase is in the endoplasmic reticulum. J Biol Chem 1998; 273:15030 - 4; http://dx.doi.org/10.1074/jbc.273.24.15030; PMID: 9614111
  • Wright LP, Court H, Mor A, Ahearn IM, Casey PJ, Philips MR. Topology of mammalian isoprenylcysteine carboxyl methyltransferase determined in live cells with a fluorescent probe. Mol Cell Biol 2009; 29:1826 - 33; http://dx.doi.org/10.1128/MCB.01719-08; PMID: 19158273
  • Yang J, Kulkarni K, Manolaridis I, Zhang Z, Dodd RB, Mas-Droux C, Barford D. Mechanism of isoprenylcysteine carboxyl methylation from the crystal structure of the integral membrane methyltransferase ICMT. Mol Cell 2011; 44:997 - 1004; http://dx.doi.org/10.1016/j.molcel.2011.10.020; PMID: 22195972
  • Bergo MO, Leung GK, Ambroziak P, Otto JC, Casey PJ, Gomes AQ, Seabra MC, Young SG. Isoprenylcysteine carboxyl methyltransferase deficiency in mice. J Biol Chem 2001; 276:5841 - 5; http://dx.doi.org/10.1074/jbc.C000831200; PMID: 11121396
  • Bergo MO, Gavino BJ, Hong C, Beigneux AP, McMahon M, Casey PJ, Young SG. Inactivation of Icmt inhibits transformation by oncogenic K-Ras and B-Raf. J Clin Invest 2004; 113:539 - 50; http://dx.doi.org/10.1172/JCI200418829; PMID: 14966563
  • Wahlstrom AM, Cutts BA, Liu M, Lindskog A, Karlsson C, Sjogren AK, Andersson KM, Young SG, Bergo MO. Inactivating Icmt ameliorates K-RAS-induced myeloproliferative disease. Blood 2008; 112:1357 - 65; http://dx.doi.org/10.1182/blood-2007-06-094060; PMID: 18502828
  • Baines AT, Xu D, Der CJ. Inhibition of Ras for cancer treatment: the search continues. Future Med Chem 2011; 3:1787 - 808; http://dx.doi.org/10.4155/fmc.11.121; PMID: 22004085
  • Slebos RJ, Hoppin JA, Tolbert PE, Holly EA, Brock JW, Zhang RH, Bracci PM, Foley J, Stockton P, McGregor LM, et al. K-ras and p53 in pancreatic cancer: association with medical history, histopathology, and environmental exposures in a population-based study. Cancer Epidemiol Biomarkers Prev 2000; 9:1223 - 32; PMID: 11097231
  • John J, Sohmen R, Feuerstein J, Linke R, Wittinghofer A, Goody RS. Kinetics of interaction of nucleotides with nucleotide-free H-ras p21. Biochemistry 1990; 29:6058 - 65; http://dx.doi.org/10.1021/bi00477a025; PMID: 2200519
  • Ostrem JM, Peters U, Sos ML, Wells JA, Shokat KM. K-Ras(G12C) inhibitors allosterically control GTP affinity and effector interactions. Nature 2013; 503:548 - 51; http://dx.doi.org/10.1038/nature12796; PMID: 24256730
  • James GL, Goldstein JL, Brown MS. Polylysine and CVIM sequences of K-RasB dictate specificity of prenylation and confer resistance to benzodiazepine peptidomimetic in vitro. J Biol Chem 1995; 270:6221 - 6; http://dx.doi.org/10.1074/jbc.270.11.6221; PMID: 7890759
  • Whyte DB, Kirschmeier P, Hockenberry TN, Nunez-Oliva I, James L, Catino JJ, Bishop WR, Pai JK. K- and N-Ras are geranylgeranylated in cells treated with farnesyl protein transferase inhibitors. J Biol Chem 1997; 272:14459 - 64; http://dx.doi.org/10.1074/jbc.272.22.14459; PMID: 9162087
  • Winter-Vann AM, Baron RA, Wong W, dela Cruz J, York JD, Gooden DM, Bergo MO, Young SG, Toone EJ, Casey PJ. A small-molecule inhibitor of isoprenylcysteine carboxyl methyltransferase with antitumor activity in cancer cells. Proc Natl Acad Sci U S A 2005; 102:4336 - 41; http://dx.doi.org/10.1073/pnas.0408107102; PMID: 15784746
  • Wang M, Tan W, Zhou J, Leow J, Go M, Lee HS, Casey PJ. A small molecule inhibitor of isoprenylcysteine carboxymethyltransferase induces autophagic cell death in PC3 prostate cancer cells. J Biol Chem 2008; 283:18678 - 84; http://dx.doi.org/10.1074/jbc.M801855200; PMID: 18434300
  • Cushman I, Casey PJ. Role of isoprenylcysteine carboxylmethyltransferase-catalyzed methylation in Rho function and migration. J Biol Chem 2009; 284:27964 - 73; http://dx.doi.org/10.1074/jbc.M109.025296; PMID: 19651782
  • Cushman I, Casey PJ. RHO methylation matters: a role for isoprenylcysteine carboxylmethyltransferase in cell migration and adhesion. Cell Adh Migr 2011; 5:11 - 5; http://dx.doi.org/10.4161/cam.5.1.13196; PMID: 20798596
  • Go ML, Leow JL, Gorla SK, Schüller AP, Wang M, Casey PJ. Amino derivatives of indole as potent inhibitors of isoprenylcysteine carboxyl methyltransferase. J Med Chem 2010; 53:6838 - 50; http://dx.doi.org/10.1021/jm1002843; PMID: 20809634
  • Ramanujulu PM, Yang T, Yap SQ, Wong FC, Casey PJ, Wang M, Go ML. Functionalized indoleamines as potent, drug-like inhibitors of isoprenylcysteine carboxyl methyltransferase (Icmt). Eur J Med Chem 2013; 63:378 - 86; http://dx.doi.org/10.1016/j.ejmech.2013.02.007; PMID: 23514631
  • Bergo MO, Leung GK, Ambroziak P, Otto JC, Casey PJ, Young SG. Targeted inactivation of the isoprenylcysteine carboxyl methyltransferase gene causes mislocalization of K-Ras in mammalian cells. J Biol Chem 2000; 275:17605 - 10; http://dx.doi.org/10.1074/jbc.C000079200; PMID: 10747846
  • Davies BS, Fong LG, Yang SH, Coffinier C, Young SG. The posttranslational processing of prelamin A and disease. Annu Rev Genomics Hum Genet 2009; 10:153 - 74; http://dx.doi.org/10.1146/annurev-genom-082908-150150; PMID: 19453251
  • Ibrahim MX, Sayin VI, Akula MK, Liu M, Fong LG, Young SG, Bergo MO. Targeting isoprenylcysteine methylation ameliorates disease in a mouse model of progeria. Science 2013; 340:1330 - 3; http://dx.doi.org/10.1126/science.1238880; PMID: 23686339
  • Wang M, Hossain MS, Tan W, Coolman B, Zhou J, Liu S, Casey PJ. Inhibition of isoprenylcysteine carboxylmethyltransferase induces autophagic-dependent apoptosis and impairs tumor growth. Oncogene 2010; 29:4959 - 70; http://dx.doi.org/10.1038/onc.2010.247; PMID: 20622895
  • Zhu WL, Hossain MS, Guo DY, Liu S, Tong H, Khakpoor A, Casey PJ, Wang M. A role for Rac3 GTPase in the regulation of autophagy. J Biol Chem 2011; 286:35291 - 8; http://dx.doi.org/10.1074/jbc.M111.280990; PMID: 21852230
  • Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3:452 - 60; PMID: 17534139
  • Yang YP, Liang ZQ, Gu ZL, Qin ZH. Molecular mechanism and regulation of autophagy. Acta Pharmacol Sin 2005; 26:1421 - 34; http://dx.doi.org/10.1111/j.1745-7254.2005.00235.x; PMID: 16297339
  • Wang M, Khoo YM, Zhou J, Casey P, Lee HS. A high-performance liquid chromatography method for the quantification of cysmethynil, an inhibitor of isoprenylcysteine carboxylmethyl transferase, in mouse plasma. J Chromatogr B Analyt Technol Biomed Life Sci 2009; 877:553 - 7; http://dx.doi.org/10.1016/j.jchromb.2008.12.067; PMID: 19157999
  • Kobayashi K, Hagiwara K. Epidermal growth factor receptor (EGFR) mutation and personalized therapy in advanced nonsmall cell lung cancer (NSCLC). Target Oncol 2013; 8:27 - 33; http://dx.doi.org/10.1007/s11523-013-0258-9; PMID: 23361373
  • Ono M, Hirata A, Kometani T, Miyagawa M, Ueda S, Kinoshita H, Fujii T, Kuwano M. Sensitivity to gefitinib (Iressa, ZD1839) in non-small cell lung cancer cell lines correlates with dependence on the epidermal growth factor (EGF) receptor/extracellular signal-regulated kinase 1/2 and EGF receptor/Akt pathway for proliferation. Mol Cancer Ther 2004; 3:465 - 72; PMID: 15078990
  • Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58:621 - 81; http://dx.doi.org/10.1124/pr.58.3.10; PMID: 16968952
  • Han W, Pan H, Chen Y, Sun J, Wang Y, Li J, Ge W, Feng L, Lin X, Wang X, et al. EGFR tyrosine kinase inhibitors activate autophagy as a cytoprotective response in human lung cancer cells. PLoS One 2011; 6:e18691; http://dx.doi.org/10.1371/journal.pone.0018691; PMID: 21655094
  • Cheng Y, Zhang Y, Zhang L, Ren X, Huber-Keener KJ, Liu X, Zhou L, Liao J, Keihack H, Yan L, et al. MK-2206, a novel allosteric inhibitor of Akt, synergizes with gefitinib against malignant glioma via modulating both autophagy and apoptosis. Mol Cancer Ther 2012; 11:154 - 64; http://dx.doi.org/10.1158/1535-7163.MCT-11-0606; PMID: 22057914
  • Dragowska WH, Weppler SA, Wang JC, Wong LY, Kapanen AI, Rawji JS, Warburton C, Qadir MA, Donohue E, Roberge M, et al. Induction of autophagy is an early response to gefitinib and a potential therapeutic target in breast cancer. PLoS One 2013; 8:e76503; http://dx.doi.org/10.1371/journal.pone.0076503; PMID: 24146879
  • Al-Lazikani B, Banerji U, Workman P. Combinatorial drug therapy for cancer in the post-genomic era. Nat Biotechnol 2012; 30:679 - 92; http://dx.doi.org/10.1038/nbt.2284; PMID: 22781697
  • Delbaldo C, Michiels S, Syz N, Soria JC, Le Chevalier T, Pignon JP. Benefits of adding a drug to a single-agent or a 2-agent chemotherapy regimen in advanced non-small-cell lung cancer: a meta-analysis. JAMA 2004; 292:470 - 84; http://dx.doi.org/10.1001/jama.292.4.470; PMID: 15280345
  • Zimmermann GR, Lehár J, Keith CT. Multi-target therapeutics: when the whole is greater than the sum of the parts. Drug Discov Today 2007; 12:34 - 42; http://dx.doi.org/10.1016/j.drudis.2006.11.008; PMID: 17198971
  • Sakuma Y, Matsukuma S, Nakamura Y, Yoshihara M, Koizume S, Sekiguchi H, Saito H, Nakayama H, Kameda Y, Yokose T, et al. Enhanced autophagy is required for survival in EGFR-independent EGFR-mutant lung adenocarcinoma cells. Lab Invest 2013; 93:1137 - 46; http://dx.doi.org/10.1038/labinvest.2013.102; PMID: 23938604
  • Zhai B, Hu F, Jiang X, Xu J, Zhao D, Liu B, Pan S, Dong X, Tan G, Wei Z, et al. Inhibition of akt reverses the acquired resistance to sorafenib by switching protective autophagy to autophagic cell death in hepatocellular carcinoma. Mol Cancer Ther 2014; 13:1589 - 98; http://dx.doi.org/10.1158/1535-7163.MCT-13-1043; PMID: 24705351
  • Court H, Amoyel M, Hackman M, Lee KE, Xu R, Miller G, Bar-Sagi D, Bach EA, Bergö MO, Philips MR. Isoprenylcysteine carboxylmethyltransferase deficiency exacerbates KRAS-driven pancreatic neoplasia via Notch suppression. J Clin Invest 2013; 123:4681 - 94; http://dx.doi.org/10.1172/JCI65764; PMID: 24216479
  • Hamer PJ, Trimpe KL, Pullano T, Ng S, LaVecchio JA, Petit DA, DeLellis R, Wolfe H, Carney WP. Production and characterization of anti-RAS p21 monoclonal antibodies. Hybridoma 1990; 9:573 - 87; http://dx.doi.org/10.1089/hyb.1990.9.573; PMID: 2076896
  • Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, Figg N, Shroff R, Skepper J, Shanahan CM. Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation 2010; 121:2200 - 10; http://dx.doi.org/10.1161/CIRCULATIONAHA.109.902056; PMID: 20458013
  • Shiwarski DJ, Dagda RK, Chu CT. Red and Green Puncta Colocalization Macro. 2014
  • Pampliega O, Orhon I, Patel B, Sridhar S, Díaz-Carretero A, Beau I, Codogno P, Satir BH, Satir P, Cuervo AM. Functional interaction between autophagy and ciliogenesis. Nature 2013; 502:194 - 200; http://dx.doi.org/10.1038/nature12639; PMID: 24089209

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.