Identification of a novel class of farnesylation targets by structure-based modeling of binding specificity

PLoS Computational Biology

Volumn 7, Issue 10, 2011, Pages

  London, Nir ^a   Lamphear, Corissa L ^b   Hougland, James L ^c,d   Fierke, Carol A ^b,c   Schueler Furman, Ora ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d SYRACUSE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C (PROGRAMMING LANGUAGE); SUBSTRATES;

BASED MODELLING; BINDING SPECIFICITIES; CAAX MOTIFS; FARNESYLATION; FARNESYLTRANSFERASE; IN-VITRO; LARGER SUBSTRATES; POST-TRANSLATIONAL MODIFICATIONS; STRUCTURAL MODELING; STRUCTURE-BASED;

PEPTIDES;

PROTEIN FARNESYLTRANSFERASE; FARNESYL TRANS TRANSFERASE; PEPTIDE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME SPECIFICITY; FARNESYLATION; IN VITRO STUDY; INTERMETHOD COMPARISON; MOLECULAR MODEL; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; BINDING SITE; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; HUMAN; METABOLISM; PROTEIN DATABASE; PROTEIN PRENYLATION; PROTEIN PROCESSING;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; BINDING SITES; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; FARNESYLTRANSTRANSFERASE; HUMANS; MODELS, MOLECULAR; PEPTIDES; PROTEIN PRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SUBSTRATE SPECIFICITY;

EID: 80055068044     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002170     Document Type: Article

References (62)

1. Maurer-Stroh S, Washietl S, Eisenhaber F, (2003) Protein prenyltransferases. Genome Biol 4: 212.
2. Zhang FL, Casey PJ, (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65: 241-269.
3. Fu HW, Casey PJ, (1999) Enzymology and biology of CaaX protein prenylation. Recent Prog Horm Res 54: 315-342; discussion 342-313.
4. Long SB, Casey PJ, Beese LS, (2002) Reaction path of protein farnesyltransferase at atomic resolution. Nature 419: 645-650.
5. Marshall CJ, (1993) Protein prenylation: a mediator of protein-protein interactions. Science 259: 1865-1866.
6. Casey PJ, (1994) Lipid modifications of G proteins. Curr Opin Cell Biol 6: 219-225.
7. Maurer-Stroh S, Eisenhaber F, (2005) Refinement and prediction of protein prenylation motifs. Genome Biol 6: R55.
8. Maurer-Stroh S, Koranda M, Benetka W, Schneider G, Sirota FL, et al. (2007) Towards complete sets of farnesylated and geranylgeranylated proteins. PLoS Comput Biol 3: e66.
9. 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.
10. Sousa SF, Fernandes PA, Ramos MJ, (2008) Farnesyltransferase inhibitors: a detailed chemical view on an elusive biological problem. Curr Med Chem 15: 1478-1492.
11. Sebti SM, Hamilton AD, (2000) Farnesyltransferase and geranylgeranyltransferase I inhibitors and cancer therapy: lessons from mechanism and bench-to-bedside translational studies. Oncogene 19: 6584-6593.
12. Cox AD, (2001) Farnesyltransferase inhibitors: potential role in the treatment of cancer. Drugs 61: 723-732.
13. Nallan L, Bauer KD, Bendale P, Rivas K, Yokoyama K, et al. (2005) Protein farnesyltransferase inhibitors exhibit potent antimalarial activity. J Med Chem 48: 3704-3713.
14. Buckner FS, Eastman RT, Yokoyama K, Gelb MH, Van Voorhis WC, (2005) Protein farnesyl transferase inhibitors for the treatment of malaria and African trypanosomiasis. Curr Opin Investig Drugs 6: 791-797.
15. Sebti SM, Der CJ, (2003) Opinion: Searching for the elusive targets of farnesyltransferase inhibitors. Nat Rev Cancer 3: 945-951.
16. Hicks KA, Hartman HL, Fierke CA, (2005) Upstream polybasic region in peptides enhances dual specificity for prenylation by both farnesyltransferase and geranylgeranyltransferase type I. Biochemistry 44: 15325-15333.
17. Hougland JL, Hicks KA, Hartman HL, Kelly RA, Watt TJ, et al. (2010) Identification of novel peptide substrates for protein farnesyltransferase reveals two substrate classes with distinct sequence selectivities. J Mol Biol 395: 176-190.
18. Hougland JL, Lamphear CL, Scott SA, Gibbs RA, Fierke CA, (2009) Context-dependent substrate recognition by protein farnesyltransferase. Biochemistry 48: 1691-1701.
19. Lane KT, Beese LS, (2006) Thematic review series: lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 47: 681-699.
20. Raveh B, London N, Schueler-Furman O, (2010) Sub-angstrom modeling of complexes between flexible peptides and globular proteins. Proteins 78: 2029-2040.
21. Das R, Baker D, (2008) Macromolecular modeling with rosetta. Annu Rev Biochem 77: 363-382.
22. Rohl CA, Strauss CE, Misura KM, Baker D, (2004) Protein structure prediction using Rosetta. Methods Enzymol 383: 66-93.
23. Krzysiak AJ, Aditya AV, Hougland JL, Fierke CA, Gibbs RA, (2010) Synthesis and screening of a CaaL peptide library versus FTase reveals a surprising number of substrates. Bioorg Med Chem Lett 20: 767-770.
24. Bairoch A, Bougueleret L, Altairac S, Amendolia V, Auchincloss A, et al. (2009) The Universal Protein Resource (UniProt) 2009. Nucleic Acids Res 37: D169-174.
25. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
26. Pais JE, Bowers KE, Stoddard AK, Fierke CA, (2005) A continuous fluorescent assay for protein prenyltransferases measuring diphosphate release. Anal Biochem 345: 302-311.
27. Pickett JS, Bowers KE, Hartman HL, Fu HW, Embry AC, et al. (2003) Kinetic studies of protein farnesyltransferase mutants establish active substrate conformation. Biochemistry 42: 9741-9748.
28. Pais JE, Bowers KE, Fierke CA, (2006) Measurement of the alpha-secondary kinetic isotope effect for the reaction catalyzed by mammalian protein farnesyltransferase. J Am Chem Soc 128: 15086-15087.
29. Fersht A, (1999) Structure and mechanism in protein science: a guide to enzyme catalysis and protein folding. New York W.H. Freeman.
30. Troutman JM, Andres DA, Spielmann HP, (2007) Protein farnesyl transferase target selectivity is dependent upon peptide stimulated product release. Biochemistry 46: 11299-11309.
31. Tschantz WR, Furfine ES, Casey PJ, (1997) Substrate binding is required for release of product from mammalian protein farnesyltransferase. J Biol Chem 272: 9989-9993.
32. Kho Y, Kim S, Jiang C, Barma D, Kwon S, et al. (2004) A tagging-via-substrate technology for detection and proteomics of farnesylated proteins. Proc Natl Acad Sci U S A 101: 12479-12484.
33. Price CT, Al-Quadan T, Santic M, Jones SC, Abu Kwaik Y, (2010) Exploitation of conserved eukaryotic host cell farnesylation machinery by an F-box effector of Legionella pneumophila. J Exp Med 207: 1713-1726.
34. Ivanov S, Charron G, Hang H, Roy C, (2010) Lipidation by the host prenyltransferase machinery facilitates membrane localization of Legionella pneumophila effector proteins. J Biol Chem 285: 34686-34698.
35. Price C, Jones S, Amundson K, Abu Kwaik Y, (2010) Host-mediated post-translational prenylation of novel Dot/Icm-translocated effectors of Legionella pneumophila. Front Microbiol doi:10.3389/fmicb.2010.00131.
36. Pucharcos C, Estivill X, de la Luna S, (2000) Intersectin 2, a new multimodular protein involved in clathrin-mediated endocytosis. FEBS Lett 478: 43-51.
37. McGavin M, Badour K, Hardy L, Kubiseski T, Zhang J, et al. (2001) Intersectin 2, a new multimodular protein involved in clathrin-mediated endocytosis. J Exp Med 194: 1777-1787.
38. Ridley AJ, (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16: 522-529.
39. Tsyba L, Nikolaienko O, Dergai O, Dergai M, Novokhatska O, et al. (2011) Intersectin multidomain adaptor proteins: Regulation of functional diversity. Gene 473: 67-75.
40. Snyder JT, Rossman KL, Baumeister MA, Pruitt WM, Siderovski DP, et al. (2001) Quantitative analysis of the effect of phosphoinositide interactions on the function of Dbl family proteins. J Biol Chem 276: 45868-45875.
41. Rizo J, Sudhof TC, (1998) C2-domains, structure and function of a universal Ca2+-binding domain. J Biol Chem 273: 15879-15882.
42. Brouns MR, Matheson SF, Hu KQ, Delalle I, Caviness VS, et al. (2000) The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development. Development 127: 4891-4903.
43. Schroder WA, Buck M, Cloonan N, Hancock JF, Suhrbier A, et al. (2007) Human Sin1 contains Ras-binding and pleckstrin homology domains and suppresses Ras signalling. Cell Signal 19: 1279-1289.
44. Ozawa H, Ashizawa S, Naito M, Yanagihara M, Ohnishi N, et al. (2004) Paired-like homeodomain protein ESXR1 possesses a cleavable C-terminal region that inhibits cyclin degradation. Oncogene 23: 6590-6602.
45. Levental I, Grzybek M, Simons K, (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49: 6305-6316.
46. Dorn M, Weiwad M, Markwardt F, Laug L, Rudolph R, et al. (2009) Identification of a disulfide bridge essential for transport function of the human proton-coupled amino acid transporter hPAT1. J Biol Chem 284: 22123-22132.
47. Brauers A, Schurmann A, Massmann S, Muhl-Zurbes P, Becker W, et al. (1996) Alternative mRNA splicing of the novel GTPase Rab28 generates isoforms with different C-termini. Eur J Biochem 237: 833-840.
48. Colicelli J, (2004) Human RAS superfamily proteins and related GTPases. Sci STKE 2004 RE13.
49. Grigoryan G, Reinke AW, Keating AE, (2009) Design of protein-interaction specificity gives selective bZIP-binding peptides. Nature 458: 859-864.
50. Goldschmidt L, Teng PK, Riek R, Eisenberg D, (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc Natl Acad Sci U S A 107: 3487-3492.
51. Kota P, Summers DW, Ren HY, Cyr DM, Dokholyan NV, (2009) Identification of a consensus motif in substrates bound by a Type I Hsp40. Proc Natl Acad Sci U S A 106: 11073-11078.
52. Mandell DJ, Kortemme T, (2009) Backbone flexibility in computational protein design. Curr Opin Biotechnol 20: 420-428.
53. Smith CA, Kortemme T, (2008) Backrub-like backbone simulation recapitulates natural protein conformational variability and improves mutant side-chain prediction. J Mol Biol 380: 742-756.
54. Humphris EL, Kortemme T, (2008) Prediction of protein-protein interface sequence diversity using flexible backbone computational protein design. Structure 16: 1777-1788.
55. Fu X, Apgar JR, Keating AE, (2007) Modeling backbone flexibility to achieve sequence diversity: the design of novel alpha-helical ligands for Bcl-xL. J Mol Biol 371: 1099-1117.
56. Chaudhury S, Gray JJ, (2009) Identification of structural mechanisms of HIV-1 protease specificity using computational peptide docking: implications for drug resistance. Structure 17: 1636-1648.
57. Terry KL, Casey PJ, Beese LS, (2006) Conversion of protein farnesyltransferase to a geranylgeranyltransferase. Biochemistry 45: 9746-9755.
58. Kaufmann K, Shen N, Mizoue L, Meiler J, (2011) A physical model for PDZ-domain/peptide interactions. J Mol Model 17: 315-24.
59. Petsalaki E, Russell RB, (2008) Peptide-mediated interactions in biological systems: new discoveries and applications. Curr Opin Biotechnol 19: 344-350.
60. Kuhlman B, Baker D, (2000) Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci U S A 97: 10383-10388.
61. Kersey PJ, Duarte J, Williams A, Karavidopoulou Y, Birney E, et al. (2004) The International Protein Index: an integrated database for proteomics experiments. Proteomics 4: 1985-1988.
62. Huang da W, Sherman B, Lempicki R, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.