86
Views
67
CrossRef citations to date
0
Altmetric
Article

Identification of a Novel Prenyl and Palmitoyl Modification at the CaaX Motif of Cdc42 That Regulates RhoGDI Binding

&
Pages 1417-1429 | Received 17 Oct 2012, Accepted 23 Jan 2013, Published online: 20 Mar 2023

REFERENCES

  • Jaffe AB, Hall A. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247–269.
  • Erickson JW, Cerione RA. 2001. Multiple roles for Cdc42 in cell regulation. Curr. Opin. Cell Biol. 13:153–157.
  • Heasman SJ, Ridley AJ. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9:690–701.
  • Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, Burridge K. 2010. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat. Cell Biol. 12:477–483.
  • Adamson P, Marshall CJ, Hall A, Tilbrook PA. 1992. Post-translational modifications of p21rho proteins. J. Biol. Chem. 267:20033–20038.
  • Ahearn IM, Haigis K, Bar-Sagi D, Philips MR. 2012. Regulating the regulator: post-translational modification of RAS. Nat. Rev. Mol. Cell Biol. 13:39–51.
  • Cook LA, Schey KL, Wilcox MD, Dingus J, Ettling R, Nelson T, Knapp DR, Hildebrandt JD. 2006. Proteomic analysis of bovine brain G protein gamma subunit processing heterogeneity. Mol. Cell. Proteomics 5:671–685.
  • Bergo MO, Gavino BJ, Hong C, Beigneux AP, McMahon M, Casey PJ, Young SG. 2004. Inactivation of Icmt inhibits transformation by oncogenic K-Ras and B-Raf. J. Clin. Invest. 113:539–550.
  • Michaelson D, Ali W, Chiu VK, Bergo M, Silletti J, Wright L, Young SG, Philips M. 2005. Postprenylation CAAX processing is required for proper localization of Ras but not Rho GTPases. Mol. Biol. Cell 16:1606–1616.
  • Roberts PJ, Mitin N, Keller PJ, Chenette EJ, Madigan JP, Currin RO, Cox AD, Wilson O, Kirschmeier P, Der CJ. 2008. Rho Family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J. Biol. Chem. 283:25150–25163.
  • Cushman I, Casey PJ. 2009. Role of isoprenylcysteine carboxylmethyltransferase-catalyzed methylation in Rho function and migration. J. Biol. Chem. 284:27964–27973.
  • Hanker AB, Mitin N, Wilder RS, Henske EP, Tamanoi F, Cox AD, Der CJ. 2010. Differential requirement of CAAX-mediated posttranslational processing for Rheb localization and signaling. Oncogene 29:380–391.
  • Johnson JL, Erickson JW, Cerione RA. 2012. C-terminal di-arginine motif of Cdc42 protein is essential for binding to phosphatidylinositol 4,5-bisphosphate-containing membranes and inducing cellular transformation. J. Biol. Chem. 287:5764–5774.
  • Wang DA, Sebti SM. 2005. Palmitoylated cysteine 192 is required for RhoB tumor-suppressive and apoptotic activities. J. Biol. Chem. 280:19243–19249.
  • Navarro-Lérida I, Sanchez-Perales S, Calvo M, Rentero C, Zheng Y, Enrich C, Del Pozo MA. 2012. A palmitoylation switch mechanism regulates Rac1 function and membrane organization. EMBO J. 31:534–551.
  • Linder ME, Deschenes RJ. 2007. Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8:74–84.
  • Rocks O, Gerauer M, Vartak N, Koch S, Huang ZP, Pechlivanis M, Kuhlmann J, Brunsveld L, Chandra A, Ellinger B, Waldmann H, Bastiaens PI. 2010. The palmitoylation machinery is a spatially organizing system for peripheral membrane proteins. Cell 141:458–471.
  • Marks PW, Kwiatkowski DJ. 1996. Genomic organization and chromosomal location of murine Cdc42. Genomics 38:13–18.
  • Shinjo K, Koland JG, Hart MJ, Narasimhan V, Johnson DI, Evans T, Cerione RA. 1990. Molecular cloning of the gene for the human placental GTP-binding protein Gp (G25K): identification of this GTP-binding protein as the human homolog of the yeast cell-division-cycle protein CDC42. Proc. Natl. Acad. Sci. U. S. A. 87:9853–9857.
  • Munemitsu S, Innis MA, Clark R, McCormick F, Ullrich A, Polakis P. 1990. Molecular cloning and expression of a G25K cDNA, the human homolog of the yeast cell cycle gene CDC42. Mol. Cell. Biol. 10:5977–5982.
  • Kang R, Wan J, Arstikaitis P, Takahashi H, Huang K, Bailey AO, Thompson JX, Roth AF, Drisdel RC, Mastro R, Green WN, Yates JRIII, Davis NG, El-Husseini A. 2008. Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456:904–909.
  • Berzat AC, Buss JE, Chenette EJ, Weinbaum CA, Shutes A, Der CJ, Minden A, Cox AD. 2005. Transforming activity of the Rho family GTPase, Wrch-1, a Wnt-regulated Cdc42 homolog, is dependent on a novel carboxyl-terminal palmitoylation motif. J. Biol. Chem. 280:33055–33065.
  • Charron G, Zhang MM, Yount JS, Wilson J, Raghavan AS, Shamir E, Hang HC. 2009. Robust fluorescent detection of protein fatty-acylation with chemical reporters. J. Am. Chem. Soc. 131:4967–4975.
  • Martin BR, Cravatt BF. 2009. Large-scale profiling of protein palmitoylation in mammalian cells. Nat. Methods 6:135–138.
  • Forrester MT, Hess DT, Thompson JW, Hultman R, Moseley MA, Stamler JS, Casey PJ. 2011. Site-specific analysis of protein S-acylation by resin-assisted capture. J. Lipid Res. 52:393–398.
  • Leung KF, Baron R, Ali BR, Magee AI, Seabra MC. 2007. Rab GTPases containing a CAAX motif are processed post-geranylgeranylation by proteolysis and methylation. J. Biol. Chem. 282:1487–1497.
  • Chelsky D, Gutterson NI, Koshland DEJr. 1984. A diffusion assay for detection and quantitation of methyl-esterified proteins on polyacrylamide gels. Anal. Biochem. 141:143–148.
  • Webb Y, Hermida-Matsumoto L, Resh MD. 2000. Inhibition of protein palmitoylation, raft localization, and T cell signaling by 2-bromopalmitate and polyunsaturated fatty acids. J. Biol. Chem. 275:261–270.
  • Falsetti SC, Wang DA, Peng H, Carrico D, Cox AD, Der CJ, Hamilton AD, Sebti SM. 2007. Geranylgeranyltransferase I inhibitors target RalB to inhibit anchorage-dependent growth and induce apoptosis and RalA to inhibit anchorage-independent growth. Mol. Cell. Biol. 27:8003–8014.
  • Zeng Q, Si X, Horstmann H, Xu Y, Hong W, Pallen CJ. 2000. Prenylation-dependent association of protein-tyrosine phosphatases PRL-1, -2, and -3 with the plasma membrane and the early endosome. J. Biol. Chem. 275:21444–21452.
  • Hoffman GR, Nassar N, Cerione RA. 2000. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100:345–356.
  • Lin Q, Fuji RN, Yang W, Cerione RA. 2003. RhoGDI is required for Cdc42-mediated cellular transformation. Curr. Biol. 13:1469–1479.
  • Greaves J, Chamberlain LH. 2011. DHHC palmitoyl transferases: substrate interactions and (patho)physiology. Trends Biochem. Sci. 36:245–253.
  • Lan TH, Liu Q, Li C, Wu G, Lambert NA. 2012. Sensitive and high resolution localization and tracking of membrane proteins in live cells with BRET. Traffic 13:1450–1456.
  • Nalbant P, Hodgson L, Kraynov V, Toutchkine A, Hahn KM. 2004. Activation of endogenous Cdc42 visualized in living cells. Science 305:1615–1619.
  • Hill CS, Wynne J, Treisman R. 1995. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81:1159–1170.
  • Lin R, Bagrodia S, Cerione R, Manor D. 1997. A novel Cdc42Hs mutant induces cellular transformation. Curr. Biol. 7:794–797.
  • Li Y, Martin BR, Cravatt BF, Hofmann SL. 2012. DHHC5 protein palmitoylates flotillin-2 and is rapidly degraded on induction of neuronal differentiation in cultured cells. J. Biol. Chem. 287:523–530.
  • Ivaldi C, Martin BR, Kieffer-Jaquinod S, Chapel A, Levade T, Garin J, Journet A. 2012. Proteomic analysis of S-acylated proteins in human B cells reveals palmitoylation of the immune regulators CD20 and CD23. PLoS One 7:e37187. doi:10.1371/journal.pone.0037187.
  • Martin BR, Wang C, Adibekian A, Tully SE, Cravatt BF. 2012. Global profiling of dynamic protein palmitoylation. Nat. Methods 9:84–89.
  • Anant JS, Ong OC, Xie HY, Clarke S, O'Brien PJ, Fung BK. 1992. In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits. J. Biol. Chem. 267:687–690.
  • Christiansen JR, Kolandaivelu S, Bergo MO, Ramamurthy V. 2011. RAS-converting enzyme 1-mediated endoproteolysis is required for trafficking of rod phosphodiesterase 6 to photoreceptor outer segments. Proc. Natl. Acad. Sci. U. S. A. 108:8862–8866.
  • Jenkins CM, Han X, Yang J, Mancuso DJ, Sims HF, Muslin AJ, Gross RW. 2003. Purification of recombinant human cPLA2 gamma and identification of C-terminal farnesylation, proteolytic processing, and carboxymethylation by MALDI-TOF-TOF analysis. Biochemistry 42:11798–11807.
  • Tucker DE, Stewart A, Nallan L, Bendale P, Ghomashchi F, Gelb MH, Leslie CC. 2005. Group IVC cytosolic phospholipase A2gamma is farnesylated and palmitoylated in mammalian cells. J. Lipid Res. 46:2122–2133.
  • Heilmeyer LMJr, Serwe M, Weber C, Metzger J, Hoffmann-Posorske E, Meyer HE. 1992. Farnesylcysteine, a constituent of the alpha and beta subunits of rabbit skeletal muscle phosphorylase kinase: localization by conversion to S-ethylcysteine and by tandem mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 89:9554–9558.
  • Ohno Y, Kihara A, Sano T, Igarashi Y. 2006. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim. Biophys. Acta 1761:474–483.
  • Lobo S, Greentree WK, Linder ME, Deschenes RJ. 2002. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J. Biol. Chem. 277:41268–41273.
  • Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, Phinney BS, Yates JRIII, Davis NG. 2006. Global analysis of protein palmitoylation in yeast. Cell 125:1003–1013.
  • Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, Philips MR. 2001. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152:111–126.
  • Norton AW, Hosier S, Terew JM, Li N, Dhingra A, Vardi N, Baehr W, Cote RH. 2005. Evaluation of the 17-kDa prenyl-binding protein as a regulatory protein for phototransduction in retinal photoreceptors. J. Biol. Chem. 280:1248–1256.
  • Zhang H, Li S, Doan T, Rieke F, Detwiler PB, Frederick JM, Baehr W. 2007. Deletion of PrBP/delta impedes transport of GRK1 and PDE6 catalytic subunits to photoreceptor outer segments. Proc. Natl. Acad. Sci. U. S. A. 104:8857–8862.
  • Nancy V, Callebaut I, El Marjou A, de Gunzburg J. 2002. The delta subunit of retinal rod cGMP phosphodiesterase regulates the membrane association of Ras and Rap GTPases. J. Biol. Chem. 277:15076–15084.
  • Wilson SJ, Smyth EM. 2006. Internalization and recycling of the human prostacyclin receptor is modulated through its isoprenylation-dependent interaction with the delta subunit of cGMP phosphodiesterase 6. J. Biol. Chem. 281:11780–11786.
  • Bhagatji P, Leventis R, Rich R, Lin CJ, Silvius JR. 2010. Multiple cellular proteins modulate the dynamics of K-ras association with the plasma membrane. Biophys. J. 99:3327–3335.
  • Chandra A, Grecco HE, Pisupati V, Perera D, Cassidy L, Skoulidis F, Ismail SA, Hedberg C, Hanzal-Bayer M, Venkitaraman AR, Wittinghofer A, Bastiaens PI. 2012. The GDI-like solubilizing factor PDEdelta sustains the spatial organization and signalling of Ras family proteins. Nat. Cell Biol. 14:148–158.
  • Bodemann BO, White MA. 2008. Ral GTPases and cancer: linchpin support of the tumorigenic platform. Nat. Rev. Cancer 8:133–140.
  • Bessette DC, Qiu D, Pallen CJ. 2008. PRL PTPs: mediators and markers of cancer progression. Cancer Metastasis Rev. 27:231–252.
  • Winter-Vann AM, Casey PJ. 2005. Post-prenylation-processing enzymes as new targets in oncogenesis. Nat. Rev. Cancer 5:405–412.
  • Holstein SA, Hohl RJ. 2012. Is there a future for prenyltransferase inhibitors in cancer therapy? Curr. Opin. Pharmacol. 12:704–709.
  • Reid TS, Terry KL, Casey PJ, Beese LS. 2004. Crystallographic analysis of CaaX prenyltransferases complexed with substrates defines rules of protein substrate selectivity. J. Mol. Biol. 343:417–433.

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.