Identification of an atypical peptidyl-prolyl cis/trans isomerase from trypanosomatids

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1803, Issue 9, 2010, Pages 1028-1037

  Erben, Esteban D ^a   Valguarnera, Ezequiel ^a   Nardelli, Sheila ^b   Chung, Janete ^b   Daum, Sebastian ^c   Potenza, Mariana ^a   Schenkman, Sergio ^b   Téllez Iñón, María T ^a  

^a INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

Author keywords

Par45; Parvulin; Peptidyl prolyl cis trans isomerase; Pin1 type PPIase

Indexed keywords

ALANINE; ARGININE; PAR45 PROTEIN; PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE PIN1; PHENYLALANINE; PROLINE; UNCLASSIFIED DRUG; CELL EXTRACT;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL PROLIFERATION; CHEMICAL BOND; CONTROLLED STUDY; EUKARYOTIC CELL; GENE SILENCING; GROWTH INHIBITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA INTERFERENCE; TRYPANOSOMA CRUZI; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CHEMISTRY; GENETIC COMPLEMENTATION; GENETIC TRANSFECTION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; KINETOPLASTIDA; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE HOMOLOGY; TISSUE DISTRIBUTION; TRANSGENIC ORGANISM; YEAST;

EUKARYOTA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

AMINO ACID SEQUENCE; ANIMALS; CELL EXTRACTS; CELLS, CULTURED; CLONING, MOLECULAR; GENETIC COMPLEMENTATION TEST; HUMANS; MOLECULAR SEQUENCE DATA; ORGANISMS, GENETICALLY MODIFIED; PEPTIDYLPROLYL ISOMERASE; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; TISSUE DISTRIBUTION; TRANSFECTION; TRYPANOSOMATINA; YEASTS;

EID: 77954952486     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.05.006     Document Type: Article

References (52)

1. Schiene C., Fischer G. Enzymes that catalyse the restructuring of proteins. Curr. Opin. Struct. Biol. 2000, 10:40-45.
2. Lu K.P., Finn G., Lee T.H., Nicholson L.K. Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol. 2007, 3:619-629.
3. Fischer G., Aumuller T. Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes. Rev. Physiol. Biochem. Pharmacol. 2003, 148:105-150.
4. Lu K.P., Hanes S.D., Hunter T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 1996, 380:544-547.
5. Ranganathan R., Lu K.P., Hunter T., Noel J.P. Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 1997, 89:875-886.
6. Yaffe M.B., Schutkowski M., Shen M., Zhou X.Z., Stukenberg P.T., Rahfeld J.U., Xu J., Kuang J., Kirschner M.W., Fischer G., Cantley L.C., Lu K.P. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 1997, 278:1957-1960.
7. Shen M., Stukenberg P.T., Kirschner M.W., Lu K.P. The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins. Genes Dev. 1998, 12:706-720.
8. Zhou X., Kops O., Werner A., Lu P., Shen M., Stoller G., Kullertz G., Stark M., Fischer G., Lu K. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol. Cell 2000, 6:873-883.
9. Hani J., Schelbert B., Bernhardt A., Domdey H., Fischer G., Wiebauer K., Rahfeld J. Mutations in a peptidyl prolyl-cis/trans-isomerase gene lead to a defect in 3′-end formation of a pre-mRNA in Saccharomyces cerevisiae. J. Biol. Chem. 1999, 274:108-116.
10. Landrieu I., De Veylder L., Fruchart J.S., Odaert B., Casteels P., Portetelle D., Van Montagu M., Inze D., Lippens G. The Arabidopsis thaliana PIN1At gene encodes a single-domain phosphorylation-dependent peptidyl prolyl cis/trans isomerase. J. Biol. Chem. 2000, 275:10577-10581.
11. Metzner M., Stoller G., Rucknagel K.P., Lu K.P., Fischer G., Luckner M., Kullertz G. Functional replacement of the essential ESS1 in yeast by the plant parvulin DlPar13. J. Biol. Chem. 2001, 276:13524-13529.
12. Yao J.L., Kops O., Lu P.J., Lu K.P. Functional conservation of phosphorylation-specific prolyl isomerases in plants. J. Biol. Chem. 2001, 276:13517-13523.
13. Uchida T., Fujimori F., Tradler T., Fischer G., Rahfeld J.U. Identification and characterization of a 14kDa human protein as a novel parvulin-like peptidyl prolyl cis/trans isomerase. FEBS Lett. 1999, 446:278-282.
14. Sudol M. Structure and function of the WW domain. Prog. Biophys. Mol. Biol. 1996, 65:113-132.
15. Rippmann J.F., Hobbie S., Daiber C., Guilliard B., Bauer M., Birk J., Nar H., Garin-Chesa P., Rettig W.J., Schnapp A. Phosphorylation-dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis. Cell Growth Differ. 2000, 11:409-416.
16. Xu Y.X., Hirose Y., Zhou X.Z., Lu K.P., Manley J.L. Pin1 modulates the structure and function of human RNA polymerase II. Genes Dev. 2003, 17:2765-2776.
17. Xu Y.X., Manley J.L. Pin1 modulates RNA polymerase II activity during the transcription cycle. Genes Dev. 2007, 21:2950-2962.
18. Wilcox C.B., Rossettini A., Hanes S.D. Genetic interactions with C-terminal domain (CTD) kinases and the CTD of RNA Pol II suggest a role for ESS1 in transcription initiation and elongation in Saccharomyces cerevisiae. Genetics 2004, 167:93-105.
19. Wu X., Rossettini A., Hanes S.D. The ESS1 prolyl isomerase and its suppressor BYE1 interact with RNA Pol II to inhibit transcription elongation in Saccharomyces cerevisiae. Genetics 2003, 165:1687-1702.
20. Surmacz T.A., Bayer E., Rahfeld J.U., Fischer G., Bayer P. The N-terminal basic domain of human parvulin hPar14 is responsible for the entry to the nucleus and high-affinity DNA-binding. J. Mol. Biol. 2002, 321:235-247.
21. Reimer T., Weiwad M., Schierhorn A., Ruecknagel P.K., Rahfeld J.U., Bayer P., Fischer G. Phosphorylation of the N-terminal domain regulates subcellular localization and DNA binding properties of the peptidyl-prolyl cis/trans isomerase hPar14. J. Mol. Biol. 2003, 330:955-966.
22. Uchida T., Takamiya M., Takahashi M., Miyashita H., Ikeda H., Terada T., Matsuo Y., Shirouzu M., Yokoyama S., Fujimori F., Hunter T. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol. 2003, 10:15-24.
23. Fujiyama-Nakamura S., Yoshikawa H., Homma K., Hayano T., Tsujimura-Takahashi T., Izumikawa K., Ishikawa H., Miyazawa N., Yanagida M., Miura Y., Shinkawa T., Yamauchi Y., Isobe T., Takahashi N. Parvulin (Par14), a peptidyl-prolyl cis-trans isomerase, is a novel rRNA processing factor that evolved in the metazoan lineage. Mol. Cell Proteomics 2009, 8:1552-1565.
24. Erben E.D., Daum S., Tellez-Inon M.T. The Trypanosoma cruzi PIN1 gene encodes a parvulin peptidyl-prolyl cis/trans isomerase able to replace the essential ESS1 in Saccharomyces cerevisiae. Mol. Biochem. Parasitol. 2007, 153:186-193.
25. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., Claverie J.M., Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36:W465-469.
26. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
27. Janowski B., Wollner S., Schutkowski M., Fischer G. A protease-free assay for peptidyl prolyl cis/trans isomerases using standard peptide substrates. Anal. Biochem. 1997, 252:299-307.
28. Wu X., Wilcox C.B., Devasahayam G., Hackett R.L., Arevalo-Rodriguez M., Cardenas M.E., Heitman J., Hanes S.D. The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J. 2000, 19:3727-3738.
29. van den Hoff M.J.B., Moorman A.F.M., Lamers W.H. Electroporation in 'intracellular' buffer increases cell survival. Nucl. Acids Res. 1992, 20:2902.
30. Wang Z., Morris J.C., Drew M.E., Englund P.T. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 2000, 275:40174-40179.
31. Wirtz E., Leal S., Ochatt C., Cross G.A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 1999, 99:89-101.
32. Shen S., Arhin G.K., Ullu E., Tschudi C. In vivo epitope tagging of Trypanosoma brucei genes using a one step PCR-based strategy. Mol. Biochem. Parasitol. 2001, 113:171-173.
33. Galanti N., Dvorak J.A., Grenet J., McDaniel J.P. Hydroxyurea-induced synchrony of DNA replication in the Kinetoplastida. Exp. Cell Res. 1994, 214:225-230.
34. Fischer G. Peptidyl-prolyl cis/trans isomerases and their effectors. Angewandte Chemie International Edition 1994, 33:1415-1436.
35. Hofmann K., Bucher P. The FHA domain: a putative nuclear signalling domain found in protein kinases and transcription factors. Trends Biochem. Sci. 1995, 20:347-349.
36. Behrsin C.D., Bailey M.L., Bateman K.S., Hamilton K.S., Wahl L.M., Brandl C.J., Shilton B.H., Litchfield D.W. Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution. J. Mol. Biol. 2007, 365:1143-1162.
37. Hennig L., Christner C., Kipping M., Schelbert B., Rucknagel K., Grabley S., Kullertz G., Fischer G. Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry 1998, 37:5953-5960.
38. Sekerina E., Rahfeld J.U., Muller J., Fanghanel J., Rascher C., Fischer G., Bayer P. NMR solution structure of hPar14 reveals similarity to the peptidyl prolyl cis/trans isomerase domain of the mitotic regulator hPin1 but indicates a different functionality of the protein. J. Mol. Biol. 2000, 301:1003-1017.
39. Terada T., Shirouzu M., Fukumori Y., Fujimori F., Ito Y., Kigawa T., Yokoyama S., Uchida T. Solution structure of the human parvulin-like peptidyl prolyl cis/trans isomerase, hPar14. J. Mol. Biol. 2001, 305:917-926.
40. Bellofatto V., Palenchar J.B. RNA interference as a genetic tool in trypanosomes. Methods Mol. Biol. 2008, 442:83-94.
41. DaRocha W.D., Otsu K., Teixeira S.M., Donelson J.E. Tests of cytoplasmic RNA interference (RNAi) and construction of a tetracycline-inducible T7 promoter system in Trypanosoma cruzi. Mol. Biochem. Parasitol. 2004, 133:175-186.
42. Lu P., Zhou X., Shen M., Lu K. Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 1999, 283:1325-1328.
43. Lu P.J., Zhou X.Z., Liou Y.C., Noel J.P., Lu K.P. Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J. Biol. Chem. 2002, 277:2381-2384.
44. Rahfeld J.U., Rucknagel K.P., Schelbert B., Ludwig B., Hacker J., Mann K., Fischer G. Confirmation of the existence of a third family among peptidyl-prolyl cis/trans isomerases. Amino acid sequence and recombinant production of parvulin. FEBS Lett. 1994, 352:180-184.
45. Vazquez M.P., Levin M.J. Functional analysis of the intergenic regions of TcP2beta gene loci allowed the construction of an improved Trypanosoma cruzi expression vector. Gene 1999, 239:217-225.
46. Gemmill T.R., Wu X., Hanes S.D. Vanishingly low levels of Ess1 prolyl-isomerase activity are sufficient for growth in Saccharomyces cerevisiae. J. Biol. Chem. 2005, 280:15510-15517.
47. Li H., Byeon I.J., Ju Y., Tsai M.D. Structure of human Ki67 FHA domain and its binding to a phosphoprotein fragment from hNIFK reveal unique recognition sites and new views to the structural basis of FHA domain functions. J. Mol. Biol. 2004, 335:371-381.
48. Boudrez A., Beullens M., Waelkens E., Stalmans W., Bollen M. Phosphorylation-dependent interaction between the splicing factors SAP155 and NIPP1. J. Biol. Chem. 2002, 277:31834-31841.
49. Reynolds D., Shi B.J., McLean C., Katsis F., Kemp B., Dalton S. Recruitment of Thr 319-phosphorylated Ndd1p to the FHA domain of Fkh2p requires Clb kinase activity: a mechanism for CLB cluster gene activation. Genes Dev. 2003, 17:1789-1802.
50. Hanes S.D., Shank P.R., Bostian K.A. Sequence and mutational analysis of ESS1, a gene essential for growth in Saccharomyces cerevisiae. Yeast 1989, 5:55-72.
51. Lu K., Hanes S., Hunter T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 1996, 380:544-547.
52. Rahfeld J.U., Schierhorn A., Mann K., Fischer G. A novel peptidyl-prolyl cis/trans isomerase from Escherichia coli. FEBS Lett. 1994, 343:65-69.