Farnesylation or geranylgeranylation? Efficient assays for testing protein prenylation in vitro and in vivo

BMC Biochemistry

Volumn 7, Issue , 2006, Pages

  Benetka, Wolfgang ^a   Koranda, Manfred ^a   Maurer Stroh, Sebastian ^a,b   Pittner, Fritz ^c   Eisenhaber, Frank ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

GERANYLTRANSFERASE; GLUTATHIONE TRANSFERASE; PROTEIN FARNESYLTRANSFERASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; ASSAY; IN VITRO STUDY; IN VIVO STUDY; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PRENYLATION; PROTEIN PROCESSING; RABBIT; RETICULOCYTE; TECHNIQUE; THIN LAYER CHROMATOGRAPHY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CHROMATOGRAPHY, THIN LAYER; GTP-BINDING PROTEINS; HUMANS; MICE; PROTEIN PRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; RABBITS; SENSITIVITY AND SPECIFICITY;

ORYCTOLAGUS CUNICULUS;

EID: 33646363597     PISSN: 14712091     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-7-6     Document Type: Article

References (70)

1. Glomset JA, Gelb MH, Farnsworth CC: Prenyl proteins in eukaryotic cells: a new type of membrane anchor. Trends Biochem Sci 1990, 15:139-14
2. Moores SL, Schaber MD, Mosser SD, Rands E, O'Hara MB, Garsky VM, Marshall MS, Pompliano DL, Gibbs JB: Sequence dependence of protein isoprenylation. J Biol Chem 1991, 266:14603-14610.
3. Caplin BE, Hettich LA, Marshall MS: Substrate characterization of the Saccharomyces cerevisiae protein farnesyltransferase and type-I protein geranylgeranyltransferase. Biochim Biophys Acta 1994, 1205:39-48.
4. Zhang FL, Casey PJ: Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 1996, 65:241-269.
5. Maurer-Stroh S, Washietl S, Eisenhaber F: Protein prenyltransferases. Genome Biol 2003, 4:212.
6. Maurer-Stroh S, Washietl S, Eisenhaber F: Protein prenyltransferases: anchor size, pseudogenes and parasites. Biol Chem 2003, 384:977-989.
7. Maurer-Stroh S, Eisenhaber F: Refinement and prediction of protein prenylation motifs. Genome Biol 2005, 6:R55.
8. Rilling HC, Breunger E, Epstein WW, Crain PF: Prenylated proteins: the structure of the isoprenoid group. Science 1990, 247:318-320.
9. Glomset JA, Farnsworth CC: Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu Rev Cell Biol 1994, 10:181-205.
10. Fukada Y, Takao T, Ohguro H, Yoshizawa T, Akino T, Shimonishi Y: Farnesylated gamma-subunit of photoreceptor G protein indispensable for GTP-binding. Nature 1990, 346:658-660.
11. Maltese WA, Wilson AL, Erdman RA: Prenylation-dependent interaction of Rab proteins with GDP dissociation inhibitors. Biochem Soc Trans 1996, 24:703-708.
12. Kloog Y, Cox AD: Prenyl-binding domains: potential targets for Ras inhibitors and anti-cancer drugs. Semin Cancer Biol 2004, 14:253-261.
13. Kuroda Y, Suzuki N, Kataoka T: The effect of posttranslational modifications on the interaction of Ras2 with adenylyl cyclase. Science 1993, 259:683-686.
14. Musha T, Kawata M, Takai Y: The geranylgeranyl moiety but not the methyl moiety of the smg-25A/rab3A protein is essential for the interactions with membrane and its inhibitory GDP/GTP exchange protein. J Biol Chem 1992, 267:9821-9825.
15. Porfiri E, Evans T, Chardin P, Hancock JF: Prenylation of Ras proteins is required for efficient hSOS1-promoted guanine nucleotide exchange. J Biol Chem 1994, 269:22672-22677.
16. Kisselev O, Ermolaeva M, Gautam N: Efficient interaction with a receptor requires a specific type of prenyl group on the G protein gamma subunit. J Biol Chem 1995, 270:25356-25358.
17. Hancock JF, Magee AI, Childs JE, Marshall CJ: All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 1989, 57:1167-1177.
18. Casey PJ, Solski PA, Der CJ, Buss JE: p21ras is modified by a farnesyl isoprenoid. Proc Natl Acad Sci U S A 1989, 86:8323-8327.
19. Cox AD, Der CJ: The ras/cholesterol connection: implications for ras oncogenicity. Crit Rev Oncog 1992, 3:365-400.
20. Bos JL: ras oncogenes in human cancer: a review. Cancer Res 1989, 49:4682-4689.
21. Malumbres M, Barbacid M: RAS oncogenes: the first 30 years. Nat Rev Cancer 2003, 3:459-465.
22. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA: Creation of human tumour cells with defined genetic elements. Nature 1999, 400:464-468.
23. Schlessinger J: Cell signaling by receptor tyrosine kinases. Cell 2000, 103:211-225.
24. Gschwind A, Fischer OM, Ullrich A: The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer 2004, 4:361-370.
25. Jaffe AB, Hall A: Rho GTPases in transformation and metastasis. Adv Cancer Res 2002, 84:57-80.
26. Sahai E, Marshall CJ: RHO-GTPases and cancer. Nat Rev Cancer 2002, 2:133-142.
27. Ishida D, Kometani K, Yang H, Kakugawa K, Masuda K, Iwai K, Suzuki M, Itohara S, Nakahata T, Hiai H, Kawamoto H, Hattori M, Minato N: Myeloproliferative stem cell disorders by deregulated Rap1 activation in SPA-1-deficient mice. Cancer Cell 2003, 4:55-65.
28. Marshall MS, Davis LJ, Keys RD, Mosser SD, Hill WS, Scolnick EM, Gibbs JB: Identification of amino acid residues required for Ras p21 target activation. Mol Cell Biol 1991, 11:3997-4004.
29. Hori Y, Kikuchi A, Isomura M, Katayama M, Miura Y, Fujioka H, Kaibuchi K, Takai Y: Post-translational modifications of the C-terminal region of the rho protein are important for its interaction with membranes and the stimulatory and inhibitory GDP/GTP exchange proteins. Oncogene 1991, 6:515-522.
30. Der CJ, Cox AD: Isoprenoid modification and plasma membrane association: critical factors for ras oncogenicity. Cancer Cells 1991, 3:331-340.
31. Kato K, Cox AD, Hisaka MM, Graham SM, Buss JE, Der CJ: Isoprenoid addition to Ras protein is the critical modification for its membrane association and transforming activity. Proc Natl Acad Sci U S A 1992, 89:6403-6407.
32. Kohl NE, Mosser SD, deSolms SJ, Giuliani EA, Pompliano DL, Graham SL, Smith RL, Scolnick EM, Oliff A, Gibbs JB: Selective inhibition of ras-dependent transformation by a farnesyltransferase inhibitor. Science 1993, 260:1934-1937.
33. Gibbs JB, Oliff A, Kohl NE: Farnesyltransferase inhibitors: Ras research yields a potential cancer therapeutic. Cell 1994, 77:175-178.
34. Kohl NE, Omer CA, Conner MW, Anthony NJ, Davide JP, deSolms SJ, Giuliani EA, Gomez RP, Graham SL, Hamilton K, .: Inhibition of farnesyltransferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat Med 1995, 1:792-797.
35. Mazieres J, Pradines A, Favre G: Perspectives on farnesyl transferase inhibitors in cancer therapy. Cancer Lett 2004, 206:159-167.
36. Doll RJ, Kirschmeier P, Bishop WR: Farnesyltransferase inhibitors as anticancer agents: critical crossroads. Curr Opin Drug Discov Devel 2004, 7:478-486.
37. Glenn JS, Watson JA, Havel CM, White JM: Identification of a prenylation site in delta virus large antigen. Science 1992, 256:1331-1333.
38. Kamiya Y, Sakurai A, Tamura S, Takahashi N: Structure of rhodotorucine A, a novel lipopeptide, inducing mating tube formation in Rhodosporidium toruloides. Biochem Biophys Res Commun 1978, 83:1077-1083.
39. Caldwell GA, Naider F, Becker JM: Fungal lipopeptide mating pheromones: a model system for the study of protein prenylation. Microbiol Rev 1995, 59:406-422.
40. Stimmel JB, Deschenes RJ, Volker C, Stock J, Clarke S: Evidence for an S-farnesylcysteine methyl ester at the carboxyl terminus of the Saccharomyces cerevisiae RAS2 protein. Biochemistry 1990, 29:9651-9659.
41. Marcus S, Caldwell GA, Xue CB, Naider F, Becker JM: Total in vitro maturation of the Saccharomyces cerevisiae a-factor lipopeptide mating pheromone. Biochem Biophys Res Commun 1990, 172:1310-1316.
42. Schmidt RA, Schneider CJ, Glomset JA: Evidence for post-translational incorporation of a product of mevalonic acid into Swiss 3T3 cell proteins. J Biol Chem 1984, 259:10175-10180.
43. Schwindinger WF, Robishaw JD: Heterotrimeric G-protein betagamma-dimers in growth and differentiation. Oncogene 2001, 20:1653-1660.
44. Lutz RJ, Trujillo MA, Denham KS, Wenger L, Sinensky M: Nucleoplasmic localization of prelamin A: implications for prenylation-dependent lamin A assembly into the nuclear lamina. Proc Natl Acad Sci U S A 1992, 89:3000-3004.
45. Farnsworth CC, Wolda SL, Gelb MH, Glomset JA: Human lamin B contains a farnesylated cysteine residue. J Biol Chem 1989, 264:20422-20429.
46. Eisenhaber B, Eisenhaber F, Maurer-Stroh S, Neuberger G: Prediction of sequence signals for lipid post-translational modifications: insights from case studies. Proteomics 2004, 4:1614-1625.
47. Hancock JF: Reticulocyte lysate assay for in vitro translation and posttranslational modification of Ras proteins. Methods Enzymol 1995, 255:60-65.
48. Wilson AL, Maltese WA: Coupled translation/prenylation of Rab proteins in vitro. Methods Enzymol 1995, 250:79-91.
49. Wang DA, Sebti SM: Palmitoylated cysteine 192 is required for RhoB tumor-suppressive and apoptotic activities. J Biol Chem 2005, 280:19243-19249.
50. Farrell FX, Yamamoto K, Lapetina EG: Prenyl group identification of rap2 proteins: a ras superfamily member other than ras that is farnesylated. Biochem J 1993, 289 ( Pt 2):349-355.
51. Yokoyama K, Zimmerman K, Scholten J, Gelb MH: Differential prenyl pyrophosphate binding to mammalian protein geranylgeranyltransferase-I and protein farnesyltransferase and its consequence on the specificity of protein prenylation. J Biol Chem 1997, 272:3944-3952.
52. Vargiu P, De Abajo R, Garcia-Ranea JA, Valencia A, Santisteban P, Crespo P, Bernal J: The small GTP-binding protein, Rhes, regulates signal transduction from G protein-coupled receptors. Oncogene 2004, 23:559-568.
53. 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, 272:14459-14464.
54. Katayama M, Kawata M, Yoshida Y, Horiuchi H, Yamamoto T, Matsuura Y, Takai Y: The posttranslationally modified C-terminal structure of bovine aortic smooth muscle rhoA p21. J Biol Chem 1991, 266:12639-12645.
55. Solski PA, Helms W, Keely PJ, Su L, Der CJ: RhoA biological activity is dependent on prenylation but independent of specific isoprenoid modification. Cell Growth Differ 2002, 13:363-373.
56. Lerner EC, Zhang TT, Knowles DB, Qian Y, Hamilton AD, Sebti SM: Inhibition of the prenylation of K-Ras, but not H- or N-Ras, is highly resistant to CAAX peptidomimetics and requires both a farnesyltransferase and a geranylgeranyltransferase I inhibitor in human tumor cell lines. Oncogene 1997, 15:1283-1288.
57. Rilling HC, Bruenger E, Leining LM, Buss JE, Epstein WW: Differential prenylation of proteins as a function of mevalonate concentration in CHO cells. Arch Biochem Biophys 1993, 301:210-215.
58. Trainin T, Shmuel M, Delmer DP: In Vitro Prenylation of the Small GTPase Rac13 of Cotton. Plant Physiol 1996, 112:1491-1497.
59. McLeod SJ, Shum AJ, Lee RL, Takei F, Gold MR: The Rap GTPases regulate integrin-mediated adhesion, cell spreading, actin polymerization, and Pyk2 tyrosine phosphorylation in B lymphocytes. J Biol Chem 2004, 279:12009-12019.
60. Torti M, Bertoni A, Canobbio I, Sinigaglia F, Lapetina EG, Balduini C: Interaction of the low-molecular-weight GTP-binding protein rap2 with the platelet cytoskeleton is mediated by direct binding to the actin filaments. J Cell Biochem 1999, 75:675-685.
61. Ohba Y, Mochizuki N, Matsuo K, Yamashita S, Nakaya M, Hashimoto Y, Hamaguchi M, Kurata T, Nagashima K, Matsuda M: Rap2 as a slowly responding molecular switch in the Rap1 signaling cascade. Mol Cell Biol 2000, 20:6074-6083.
62. Falk JD, Vargiu P, Foye PE, Usui H, Perez J, Danielson PE, Lerner DL, Bernal J, Sutcliffe JG: Rhes: A striatal-specific Ras homolog related to Dexras1. J Neurosci Res 1999, 57:782-788.
63. Chan SL, Monks LK, Gao H, Deaville P, Morgan NG: Identification of the monomeric G-protein, Rhes, as an efaroxan-regulated protein in the pancreatic beta-cell. Br J Pharmacol 2002, 136:31-36.
64. Spano D, Branchi I, Rosica A, Pirro MT, Riccio A, Mithbaokar P, Affuso A, Arra C, Campolongo P, Terracciano D, Macchia V, Bernal J, Alleva E, Di Lauro R: Rhes is involved in striatal function. Mol Cell Biol 2004, 24:5788-5796.
65. Ehrhardt A, Ehrhardt GR, Guo X, Schrader JW: Ras and relatives - job sharing and networking keep an old family together. Exp Hematol 2002, 30:1089-1106.
66. Ellis CA, Clark G: The importance of being K-Ras. Cell Signal 2000, 12:425-434.
67. Ridley AJ: Rho family proteins: coordinating cell responses. Trends Cell Biol 2001, 11:471-477.
68. Etienne-Manneville S, Hall A: Rho GTPases in cell biology. Nature 2002, 420:629-635.
69. Hall A: Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
70. Doetzlhofer A, Rotheneder H, Lagger G, Koranda M, Kurtev V, Brosch G, Wintersberger E, Seiser C: Histone deacetylase 1 can repress transcription by binding to Sp1. Mol Cell Biol 1999, 19:5504-5511.