Structure, regulation and cellular functions of Rab geranylgeranyl transferase and its cellular partner Rab Escort Protein

References

• Alory C, Balch WE. 2001. Organization of the Rab-GDI/CHM superfamily: The functional basis for choroideremia disease. Traffic 2:532–543.
   PubMed Web of Science ®Google Scholar
• Alory C, Balch WE. 2003. Molecular evolution of the Rab-escort-protein/guanine-nucleotide-dissociation-inhibitor superfamily. Mol Biol Cell 14:3857–3867.
   Google Scholar
• Bauer BE, Lorenzetti S, Miaczynska M, Bui DM, Schweyen RJ, Ragnini A. 1996. Amino- and carboxy-terminal domains of the yeast Rab escort protein are both required for binding of Ypt small G proteins. Mol Biol Cell 7:1521–1533.
   PubMed Web of Science ®Google Scholar
• Benes CH, Wu N, Elia AE, Dharia T, Cantley LC, Soltoff SP. 2005. The C2 domain of PKCdelta is a phosphotyrosine binding domain. Cell 121:271–280.
   PubMed Web of Science ®Google Scholar
• Bialek-Wyrzykowska U, Bauer BE, Wagner W, Kohlwein SD, Schweyen RJ, Ragnini A. 2000. Low levels of Ypt protein prenylation cause vesicle polarization defects and thermosensitive growth that can be suppressed by genes involved in cell wall maintenance. Mol Microbiol 35:1295–1311.
   Google Scholar
• Chen EJ, Frand AR, Chitouras E, Kaiser CA. 1998. A link between secretion and pre-mRNA processing defects in Saccharomyces cerevisiae and the identification of a novel splicing gene, RSE1. Mol Cell Biol 18:7139–7146.
   PubMedGoogle Scholar
• Chia WJ, Tang BL. 2009. Emerging roles for Rab family GTPases in human cancer. Biochim Biophys Acta 1795:110–116.
   PubMed Web of Science ®Google Scholar
• Coussa RG, Traboulsi EI. 2011. Choroideremia: A review of general findings and pathogenesis. Ophthalmic Genet Oct 21; in press.
   Google Scholar
• Cremers FP, Armstrong SA, Seabra MC, Brown MS, Goldstein JL. 1994. REP-2, a Rab escort protein encoded by the choroideremialike gene. J Biol Chem 269:2111–2117.
   PubMed Web of Science ®Google Scholar
• Detter JC, Zhang Q, Mules EH, Novak EK, Mishra VS, Li W, 2000. Rab geranylgeranyl transferase alpha mutation in the gunmetal mouse reduces Rab prenylation and platelet synthesis. Proc Natl Acad Sci USA 97:4144–4149.
   PubMed Web of Science ®Google Scholar
• Dursina B, Thoma NH, Sidorovitch V, Niculae A, Iakovenko A, Rak A, 2002. Interaction of yeast Rab geranylgeranyl transferase with its protein and lipid substrates. Biochemistry 41:6805–6816.
   Google Scholar
• Esposito G, De Falco F, Tinto N, Testa F, Vitagliano L, Tandurella IC, 2011. Comprehensive mutation analysis (20 families) of the choroideremia gene reveals a missense variant that prevents the binding of REP1 with Rab geranylgeranyl transferase. Hum Mutat 32(12):1460–1469.
   PubMed Web of Science ®Google Scholar
• Fujimura K, Tanaka K, Nakano A, Toh-e A. 1994. The Saccharomyces cerevisiae MSI4 gene encodes the yeast counterpart of component A of Rab geranylgeranyltransferase. J Biol Chem 269:9205–9212.
   Google Scholar
• Garcia-Hoyos M, Lorda-Sanchez I, Gomez-Garre P, Villaverde C, Cantalapiedra D, Bustamante A, 2008. New type of mutations in three Spanish families with choroideremia. Invest Ophthalmol Vis Sci 49:1315–1321.
   PubMed Web of Science ®Google Scholar
• Gerber E, Hemmerlin A, Hartmann M, Heintz D, Hartmann MA, Mutterer J, 2009. The plastidial 2-C-methyl-D-erythritol 4-phosphate pathway provides the isoprenyl moiety for protein geranylgeranylation in tobacco BY-2 cells. Plant Cell 21:285–300.
   Google Scholar
• Guo Z, Wu YW, Das D, Delon C, Cramer J, Yu S, 2008. Structures of RabGGTase-substrate/product complexes provide insights into the evolution of protein prenylation. EMBO J 27:2444–2456.
   PubMed Web of Science ®Google Scholar
• Hala M, Elias M, Zarsky V. 2005. A specific feature of the angiosperm Rab escort protein (REP) and evolution of the REP/GDI superfamily. J Mol Biol 348:1299–1313.
   PubMedGoogle Scholar
• Hala M, Soukupova H, Synek L, Zarsky V. 2010. Arabidopsis RAB geranylgeranyl transferase beta-subunit mutant is constitutively photomorphogenic, and has shoot growth and gravitropic defects. Plant J 62:615–627.
   PubMed Web of Science ®Google Scholar
• Hutagalung AH, Novick PJ. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91:119–149.
   PubMed Web of Science ®Google Scholar
• Jacoby JJ, Nilius SM, Heinisch JJ. 1998. A screen for upstream components of the yeast protein kinase C signal transduction pathway identifies the product of the SLG1 gene. Mol Gen Genet 258:148–155.
   PubMedGoogle Scholar
• Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, Tyers M. 2004. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 18:2491–2505.
   PubMed Web of Science ®Google Scholar
• Keiser NW, Tang W, Wei Z, Bennett J. 2005. Spatial and temporal expression patterns of the choroideremia gene in the mouse retina. Mol Vis 11:1052–1060.
   Google Scholar
• Kobe B, Kajava AV. 2001. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725–732.
   PubMed Web of Science ®Google Scholar
• Krock BL, Bilotta J, Perkins BD. 2007. Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia. Proc Natl Acad Sci USA 104:4600–4605.
   PubMed Web of Science ®Google Scholar
• Lachance V, Cartier A, Genier S, Munger S, Germain P, Labrecque P, 2011. Regulation of β2-adrenergic receptor maturation and anterograde trafficking by an interaction with Rab geranylgeranyltransferase: Modulation of Rab geranylgeranylation by the receptor. J Biol Chem 286:40802–40813.
   Google Scholar
• Lawson M, Coulton L, Ebetino F, Vanderkerken K, Croucher P. 2008. Geranylgeranyl transferase type II inhibition prevents myeloma bone disease. Biochem Biophys Res Commun 377:453–457.
   PubMed Web of Science ®Google Scholar
• Lempiainen H, Uotila A, Urban J, Dohnal I, Ammerer G, Loewith R, 2009. Sfp1 interaction with TORC1 and Mrs6 reveals feedback regulation on TOR signaling. Mol Cell 33:704–716.
   Google Scholar
• Leung KF, Baron R, Seabra MC. 2006. Thematic review series: Lipid posttranslational modifications; geranylgeranylation of Rab GTPases. J Lipid Res 47:467–475.
   PubMed Web of Science ®Google Scholar
• Li W, Detter JC, Weiss HJ, Cramer EM, Zhang Q, Novak EK, 2000. 5′-UTR structural organization, transcript expression, and mutational analysis of the human Rab geranylgeranyl transferase alpha-subunit (RABGGTA) gene. Mol Genet Metab 71:599–608.
   Google Scholar
• Lund RD, Kwan AS, Keegan DJ, Sauvé Y, Coffey PJ, Lawrence JM. 2001. Cell transplantation as a treatment for retinal disease. Prog Retin Eye Res 20:415–449.
   PubMed Web of Science ®Google Scholar
• MacDonald IM, Sereda C, McTaggart K, Mah D. 2004. Choroideremia gene testing. Expert Rev Mol Diagn 4:478–484.
   PubMed Web of Science ®Google Scholar
• MacDonald IM, Smaoui N, Seabra MC. Choroideremia. 1993. In: Pagon RA, Bird TD, Dolan CR, Stephens K, Adam MP, editors. GeneReviews™, Seattle (WA); University of Washington. Seattle: 1993–2003; [updated 3 June 2010].
   Google Scholar
• Miaczynska M, Lorenzetti S, Bialek U, Benito-Moreno RM, Schweyen RJ, Ragnini A. 1997. The yeast Rab escort protein binds intracellular membranes in vivo and in vitro. J Biol Chem 272:16972–16977.
   Google Scholar
• Miaczynska M, Wagner W, Bauer BE, Schweyen RJ, Ragnini A. 2001. Ypt protein prenylation depends on the interplay among levels of Rab escort protein and geranylgeranyl diphosphate in yeast cells. Yeast 18:697–709.
   Google Scholar
• Mitra S, Cheng KW, Mills GB. 2011. Rab GTPases implicated in inherited and acquired disorders. Semin Cell Dev Biol 22:57–68.
   PubMed Web of Science ®Google Scholar
• Moosajee M, Tulloch M, Baron RA, Gregory-Evans CY, Pereira-Leal JB, Seabra MC. 2009. Single choroideremia gene in nonmammalian vertebrates explains early embryonic lethality of the zebrafish model of choroideremia. Invest Ophthalmol Vis Sci 50:3009–3016.
   PubMed Web of Science ®Google Scholar
• Nalefski EA, Falke JJ. 1996. The C2 domain calcium-binding motif: Structural and functional diversity. Protein Sci 5:2375–2390.
   PubMed Web of Science ®Google Scholar
• Newman AP, Ferro-Novick S. 1987. Characterization of new mutants in the early part of the yeast secretory pathway isolated by a (3H)mannose suicide selection. J Cell Biol 105:1587–1594.
   PubMedGoogle Scholar
• Nguyen UT, Goody RS, Alexandrov K. 2010. Understanding and exploiting protein prenyltransferases. ChemBioChem 11:1194–1201.
   PubMed Web of Science ®Google Scholar
• Nguyen UT, Guo Z, Delon C, Wu Y, Deraeve C, Fränzel B, 2009. Analysis of the eukaryotic prenylome by isoprenoid affinity tagging. Nat Chem Biol 5:227–235.
   PubMed Web of Science ®Google Scholar
• Pandit S, Paul S, Zhang L, Chen M, Durbin N, Harrison SM, 2009. Spp382p interacts with multiple yeast splicing factors, including possible regulators of Prp43 DExD/H-Box protein function. Genetics 183:195–206.
   Google Scholar
• Pylypenko O, Rak A, Reents R, Niculae A, Sidorovitch V, Cioaca MD, 2003. Structure of Rab escort protein-1 in complex with Rab geranylgeranyltransferase. Mol Cell 11:483–494.
   PubMed Web of Science ®Google Scholar
• Ragnini A, Teply R, Waldherr M, Voskova A, Schweyen RJ. 1994. The yeast protein Mrs6p, a homologue of the rabGDI and human choroideraemia proteins, affects cytoplasmic and mitochondrial functions. Curr Genet 26:308–314.
   Google Scholar
• Rak A, Pylypenko O, Niculae A, Pyatkov K, Goody RS, Alexandrov K. 2004. Structure of the Rab7:REP-1 complex: Insights into the mechanism of Rab prenylation and choroideremia disease. Cell 117:749–760.
   PubMed Web of Science ®Google Scholar
• Rak A, Reents R, Pylypenko O, Niculae A, Sidorovitch V, Thoma NH, 2001. Crystallization and preliminary X-ray diffraction analysis of the Rab escort protein-1 in complex with Rab geranylgeranyltransferase. J Struct Biol 136:158–161.
   Google Scholar
• Rasteiro R, Pereira-Leal JB. 2007. Multiple domain insertions and losses in the evolution of the Rab prenylation complex. BMC Evol Biol 7:140.
   Google Scholar
• Rodrigues MM, Ballintine EJ, Wiggert BN, Lee L, Fletcher RT, Chader GJ. 1984. Choroideremia: A clinical, electron microscopic, and biochemical report. Ophthalmology 91:873–883.
   PubMedGoogle Scholar
• Rogers MJ, Crockett JC, Coxon FP, Monkkonen J. 2011. Biochemical and molecular mechanisms of action of bisphosphonates. Bone 49:34–41.
   PubMed Web of Science ®Google Scholar
• Scriver CR, Sly WS. Beaud, Valle D, editors. 1995. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill, Inc.
   Google Scholar
• Seabra MC, Ho YK, Anant JS. 1995. Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J Biol Chem 270:24420–24427.
   PubMed Web of Science ®Google Scholar
• Seabra MC. 1996. New insights into the pathogenesis of choroideremia: A tale of two REPs. Ophthalmic Genet 17:43–46.
   PubMed Web of Science ®Google Scholar
• Sergeev YV, Smaoui N, Sui R, Stiles D, Gordiyenko N, Strunnikova N, 2009. The functional effect of pathogenic mutations in Rab escort protein 1. Mutat Res 665:44–50.
   PubMed Web of Science ®Google Scholar
• Shi W, van den Hurk JA, Alamo-Bethencourt V, Mayer W, Winkens HJ, Ropers HH, 2004. Choroideremia gene product affects trophoblast development and vascularization in mouse extra-embryonic tissues. Dev Biol 272:53–65.
   PubMed Web of Science ®Google Scholar
• Si X, Zeng Q, Ng CH, Hong W, Pallen CJ. 2001. Interaction of farnesylated PRL-2, a protein-tyrosine phosphatase, with the beta-subunit of geranylgeranyltransferase II. J Biol Chem 276:32875–32882.
   Google Scholar
• Singh J, Tyers M. 2009. A Rab escort protein integrates the secretion system with TOR signaling and ribosome biogenesis. Genes Dev 23:1944–1958.
   PubMed Web of Science ®Google Scholar
• Skorupinska-Tudek K, Poznanski J, Wojcik J, Bienkowski T, Szostkiewicz I, Zelman-Femiak M, 2008. Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of dolichols in plants. J Biol Chem 283:21024–21035.
   Google Scholar
• Starr CJ, Kappler JA, Chan DK, Kollmar R, Hudspeth AJ. 2004. Mutation of the zebrafish choroideremia gene encoding Rab escort protein 1 devastates hair cells. Proc Natl Acad Sci USA 101:2572–2577.
   PubMed Web of Science ®Google Scholar
• Strunnikova NV, Barb J, Sergeev YV, Thiagarajasubramanian A, Silvin C, Munson PJ, 2009. Loss-of-function mutations in Rab escort protein 1 (REP-1) affect intracellular transport in fibroblasts and monocytes of choroideremia patients. PLoS One 4:e8402.
   PubMed Web of Science ®Google Scholar
• Tanaka D, Kameyama K, Okamoto H, Doi M. 2008. Caenorhabditis elegans Rab escort protein (REP-1) differently regulates each Rab protein function and localization in a tissue-dependent manner. Genes Cells 13:1141–1157.
   PubMed Web of Science ®Google Scholar
• Taylor A, Mules EH, Seabra MC, Helfrich MH, Rogers MJ, Coxon FP. 2011. Impaired prenylation of Rab GTPases in the gunmetal mouse causes defects in bone cell function. Small Gtpases 2:131–142.
   PubMedGoogle Scholar
• Thoma NH, Iakovenko A, Goody RS, Alexandrov K. 2001a. Phosphoisoprenoids modulate association of Rab geranylgeranyltransferase with REP-1. J Biol Chem 276:48637–48643.
   Google Scholar
• Thoma NH, Niculae A, Goody RS, Alexandrov K. 2001b. Double prenylation by RabGGTase can proceed without dissociation of the mono-prenylated intermediate. J Biol Chem 276:48631–48636.
   Google Scholar
• Tolmachova T, Anders R, Abrink M, Bugeon L, Dallman MJ, Futter CE, 2006. Independent degeneration of photoreceptors and retinal pigment epithelium in conditional knockout mouse models of choroideremia. J Clin Invest 116:386–394.
   PubMed Web of Science ®Google Scholar
• Tolmachova T, Tolmachov OE, Wavre-Shapton ST, Tracey-White D, Futter CE, Seabra MC. 2012. CHM/REP1 cDNA delivery by lentiviral vectors provides functional expression of the transgene in the RPE of choroideremia mice. J Gene Med 14(3):158-68.
   PubMed Web of Science ®Google Scholar
• van den Hurk JA, Hendriks W, van de Pol DJ, Oerlemans F, Jaissle G, Rüther K, 1997. Mouse choroideremia gene mutation causes photoreceptor cell degeneration and is not transmitted through the female germline. Hum Mol Genet 6:851–858.
   PubMed Web of Science ®Google Scholar
• van Gele M, Dynoodt P, Lambert J. 2009. Griscelli syndrome: A model system to study vesicular trafficking. Pigment Cell Melanoma Res 22:268–282.
   PubMed Web of Science ®Google Scholar
• Vincent K, Wang Q, Jay S, Hobbs K, Rymond BC. 2003. Genetic interactions with CLF1 identify additional pre-mRNA splicing factors and a link between activators of yeast vesicular transport and splicing. Genetics 164:895–907.
   PubMedGoogle Scholar
• Waldherr M, Ragnini A, Schweyer RJ, Boguski MS. 1993. MRS6-yeast homologue of the choroideraemia gene. Nat Genet 3:193–194.
   PubMedGoogle Scholar
• Witter DJ, Poulter CD. 1996. Yeast geranylgeranyltransferase type-II: Steady state kinetic studies of the recombinant enzyme. Biochemistry 35:10454–10463.
   Google Scholar
• Wojtas M, Swiezewski S, Sarnowski TJ, Plochocka D, Chelstowska A, Tolmachova T, 2007. Cloning and characterization of Rab Escort Protein (REP) from Arabidopsis thaliana. Cell Biol Int 31:246–251.
   Google Scholar
• Wu YW, Goody RS, Abagyan R, Alexandrov K. 2009. Structure of the disordered C terminus of Rab7 GTPase induced by binding to the Rab geranylgeranyl transferase catalytic complex reveals the mechanism of Rab prenylation. J Biol Chem 284:13185–13192.
   PubMed Web of Science ®Google Scholar
• Zhang H, Seabra MC, Deisenhofer J. 2000. Crystal structure of Rab geranylgeranyltransferase at 2.0 A resolution. Struct Fold Des 8:241–251.
   Google Scholar