Atypical caseinolytic protease homolog from Plasmodium falciparum possesses unusual substrate preference and a functional nuclear localization signal

Parasitology Research

Volumn 105, Issue 6, 2009, Pages 1715-1722

  Lin, Wenjie ^a   Chan, Maurice ^a   Sim, Tiow Suan ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEIN SUBUNIT; PROTEINASE;

ARTICLE; BINDING SITE; CHLOROPLAST; GENE; GENE AMPLIFICATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; MOLECULAR CLONING; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENICITY; PFCLPP GENE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CLONING, MOLECULAR; ENDOPEPTIDASE CLP; FEMALE; GENE EXPRESSION; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SUBSTRATE SPECIFICITY;

EUKARYOTA; MAMMALIA; PLASMODIUM FALCIPARUM;

EID: 70350238220     PISSN: 09320113     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00436-009-1612-9     Document Type: Article

References (39)

1. P Acharya R Kumar U Tatu 2007 Chaperoning a cellular upheaval in malaria: Heat shock proteins in Plasmodium falciparum Mol Biochem Parasitol 153 2 85 94 10.1016/j.molbiopara.2007.01.009 1:CAS:528:DC%2BD2sXkslenurs%3D 17307260 (Pubitemid 46654240)
2. Z Adam A Rudella KJ van Wijk 2006 Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts Curr Opin Plant Biol 9 3 234 240 10.1016/j.pbi.2006.03.010 1:CAS:528:DC%2BD28XktVGgtb8%3D 16603408
3. BS Andresen TJ Corydon M Wilsbech P Bross LD Schroeder TF Hindkjaer L Bolund N Gregersen 2000 Characterization of mouse Clpp protease cDNA, gene, and protein Mamm Genome 4 275 280 10.1007/s003350010052 (Pubitemid 30171658)
4. J Arribas JG Castano 1993 A comparative study of the chymotrypsin-like activity of the rat liver multicatalytic proteinase and the ClpP from Escherichia coli J Biol Chem 268 28 21165 21171 1:CAS:528:DyaK3sXlsFClt7o%3D 8407953
5. K Becker L Tilley JL Vennerstrom D Roberts S Rogerson H Ginsburg 2004 Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions Int J Parasitol 34 2 163 189 10.1016/j.ijpara.2003.09.011 1:CAS:528:DC%2BD2cXhsFWgtLs%3D 15037104 (Pubitemid 38229822)
6. A Bender GG van Dooren SA Ralph GI McFadden G Schneider 2003 Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum Mol Biochem Parasitol 132 59 66 10.1016/j.molbiopara.2003.07.001 1:CAS:528:DC%2BD3sXos1OmsLs%3D 14599665 (Pubitemid 37352901)
7. Z Bozdech M Llinas BL Pulliam ED Wong J Zhu JL DeRisi 2003 The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum PLoS Biol 1 1 E5 10.1371/journal.pbio.0000005 12929205 (Pubitemid 39112195)
8. M Chan DS Tan SH Wong TS Sim 2006 A relevant in vitro eukaryotic live-cell system for the evaluation of plasmodial protein localization Biochimie 88 10 1367 1375 10.1016/j.biochi.2006.05.021 1:CAS:528:DC%2BD28XhtFOhsrrL 16839657 (Pubitemid 44755226)
9. D Chandu D Nandi 2004 Comparative genomics and functional roles of the ATP-dependent proteases Lon and Clp during cytosolic protein degradation Res Microbiol 155 9 710 719 10.1016/j.resmic.2004.06.003 1:CAS:528: DC%2BD2cXovV2hs7k%3D 15501647 (Pubitemid 39389126)
10. CE Chwieralski T Welte F Buhling 2006 Cathepsin-regulated apoptosis Apoptosis 11 2 143 149 10.1007/s10495-006-3486-y 1:CAS:528:DC%2BD28XhvVSrtb0%3D 16502253 (Pubitemid 43291015)
11. MT Cohn H Ingmer F Mulholland K Jørgensen JM Wells L Brøndsted 2007 Contribution of conserved ATP-dependent proteases of Campylobacter jejuni to stress tolerance and virulence Appl Environ Microbiol 73 24 7803 7813 10.1128/AEM.00698-07 1:CAS:528:DC%2BD1cXotlWk 17933920 (Pubitemid 350308795)
12. M Cokol R Nair B Rost 2000 Finding nuclear localization signals EMBO Rep 1 5 411 415 10.1093/embo-reports/kvd092 1:CAS:528:DC%2BD3MXjtF2hsLk%3D 11258480
13. TJ Corydon P Bross HU Holst S Neve K Kristiansen N Gregersen L Bolund 1998 A human homologue of Escherichia coli ClpP caseinolytic protease: recombinant expression, intracellular processing and subcellular localization Biochem J 331 Pt 1 309 316 1:CAS:528:DyaK1cXisVWktL0%3D 9512494
14. BJ Foth SA Ralph CJ Tonkin NS Struck M Fraunholz DS Roos AF Cowman GI McFadden 2003 Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum Science 299 5607 705 708 10.1126/science.1078599 1:CAS:528:DC%2BD3sXntFWitA%3D%3D 12560551 (Pubitemid 36159484)
15. O Gaillot E Pellegrini S Bregenholt S Nair P Berche 2000 The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes Mol Microbiol 35 6 1286 1294 10.1046/j.1365-2958.2000.01773.x 1:CAS:528:DC%2BD3cXis1Wrsbo%3D 10760131 (Pubitemid 30175506)
16. SM Gantt JM Myung MR Briones WD Li EJ Corey S Omura V Nussenzweig P Sinnis 1998 Proteasome inhibitors block development of Plasmodium spp Antimicrob Agents Chemother 42 10 2731 2738 1:CAS:528:DyaK1cXms1GjsLo%3D 9756786
17. U Gerth H Kock I Kusters S Michalik RL Switzer M Hecker 2008 Clp-dependent proteolysis down-regulates central metabolic pathways in glucose-starved Bacillus subtilis J Bacteriol 190 1 321 331 10.1128/JB.01233-07 1:CAS:528:DC%2BD1cXhsF2rsQ%3D%3D 17981983
18. LL Goh T Barkham TS Sim 2005 Molecular cloning and functional characterization of fumarases C in Neisseria species Antonie van Leeuwenhoek 87 3 205 213 10.1007/s10482-004-3719-4 1:CAS:528:DC%2BD2MXivVKhs7c%3D 15803386 (Pubitemid 41349046)
19. N Guex MC Peitsch 1997 SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling Electrophoresis 18 15 2714 2723 10.1002/elps.1150181505 1:CAS:528:DyaK1cXhvFaks70%3D 9504803 (Pubitemid 28059943)
20. T Halperin B Zheng H Itzhaki AK Clarke Z Adam 2001 Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease Plant Mol Biol 45 4 461 468 10.1023/A:1010677220323 1:CAS:528: DC%2BD3MXjslWisbY%3D 11352464 (Pubitemid 32382758)
21. T Hatabu M Hagiwara N Taguchi M Kiyozawa M Suzuki S Kano K Sato 2006 Plasmodium falciparum: the fungal metabolite gliotoxin inhibits proteasome proteolytic activity and exerts a plasmodicidal effect on P. falciparum Exp Parasitol 112 3 179 183 10.1016/j.exppara.2005.11.012 1:CAS:528: DC%2BD28Xhs1Sns7k%3D 16384554 (Pubitemid 43247778)
22. CM Haynes K Petrova C Benedetti Y Yang D Ron 2007 ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans Dev Cell 13 4 467 480 10.1016/j.devcel.2007.07.016 1:CAS:528:DC%2BD2sXht1SjsrjM 17925224 (Pubitemid 47500805)
23. U Jenal T Fuchs 1998 An essential protease involved in bacterial cell-cycle control EMBO J 17 19 5658 5669 10.1093/emboj/17.19.5658 1:CAS:528:DyaK1cXmvVyjs7c%3D 9755166 (Pubitemid 28445977)
24. SG Kang J Ortega SK Singh N Wang NN Huang AC Steven MR Maurizi 2002 Functional proteolytic complexes of the human mitochondrial ATP-dependent protease, hClpXP J Biol Chem 277 23 21095 21102 10.1074/jbc.M201642200 1:CAS:528:DC%2BD38XkslWntr8%3D 11923310 (Pubitemid 34967421)
25. SG Kang MR Maurizi M Thompson T Mueser B Ahvazi 2004 Crystallography and mutagenesis point to an essential role for the N-terminus of human mitochondrial ClpP J Struct Biol 148 3 338 352 10.1016/j.jsb.2004.07.004 1:CAS:528: DC%2BD2cXpt1Squr0%3D 15522782 (Pubitemid 39441371)
26. A Kreidenweiss PG Kremsner B Mordmüller 2008 Comprehensive study of proteasome inhibitors against Plasmodium falciparum laboratory strains and field isolates from Gabon Malar J 7 187 10.1186/1475-2875-7-187 18816382
27. HY Kwon SW Kim MH Choi AD Ogunniyi JC Paton SH Park SN Pyo DK Rhee 2003 Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae Infect Immun 71 7 3757 3765 10.1128/IAI.71.7.3757- 3765.2003 1:CAS:528:DC%2BD3sXms1WjtrY%3D 12819057 (Pubitemid 36753696)
28. E Manser HY Huang TH Loo XQ Chen JM Dong T Leung L Lim 1997 Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes Mol Cell Biol 17 3 1129 1143 1:CAS:528:DyaK2sXhtlGisbs%3D 9032240
29. MR Maurizi WP Clark Y Katayama S Rudikoff J Pumphrey B Bowers S Gottesman 1990 Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli J Biol Chem 265 21 12536 12545 1:CAS:528:DyaK3MXis1Gl 2197275
30. B Mordmüller R Fendel A Kreidenweiss C Gille R Hurwitz WG Metzger JF Kun T Lamkemeyer A Nordheim PG Kremsner 2006 Plasmodia express two threonine-peptidase complexes during asexual development Mol Biochem Parasitol 148 1 79 85 10.1016/j.molbiopara.2006.03.001 16616382 (Pubitemid 43795866)
31. JB Peltier J Ytterberg DA Liberles P Roepstorffm KJ van Wijk 2001 Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana J Biol Chem 276 19 16318 16327 10.1074/jbc.M010503200 1:CAS:528:DC%2BD3MXjvFakurw%3D 11278690
32. T Schweder KH Lee O Lomovskaya A Matin 1996 Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease J Bacteriol 178 2 470 476 1:CAS:528:DyaK28Xjs1Wnug%3D%3D 8550468
33. JD Thompson DG Higgins TJ Gibson 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 22 4673 4680 10.1093/nar/22.22.4673 1:CAS:528:DyaK2MXitlSgu74%3D 7984417
34. M Vedadi J Lew J Artz M Amani Y Zhao A Dong GA Wasney M Gao T Hills S Brokx W Qiu S Sharma A Diassiti Z Alam M Melone A Mulichak A Wernimont J Bray P Loppnau O Plotnikova K Newberry E Sundararajan S Houston J Walker W Tempel A Bochkarev I Kozieradzki A Edwards C Arrowsmith D Roos K Kain R Hui 2007 Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms Mol Biochem Parasitol 151 1 100 110 10.1016/j.molbiopara.2006.10.011 1:CAS:528:DC%2BD28XhtlaktbvO 17125854 (Pubitemid 44911074)
35. J Wang JA Hartling JM Flanagan 1997 The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis Cell 91 4 447 456 10.1016/S0092-8674(00)80431-6 1:CAS:528:DyaK2sXnsFGmtb0%3D 9390554
36. KM Woo WJ Chung DB Ha AL Goldberg CH Chung 1989 Protease Ti from Escherichia coli requires ATP hydrolysis for protein breakdown but not for hydrolysis of small peptides J Biol Chem 264 4 2088 2091 1:CAS:528: DyaL1MXhsFSgt70%3D 2644253
37. AY Yu WA Houry 2007 ClpP: a distinctive family of cylindrical energy-dependent serine proteases FEBS Lett 581 19 3749 3757 10.1016/j.febslet.2007.04.076 1:CAS:528:DC%2BD2sXotlaisb0%3D 17499722 (Pubitemid 47082517)
38. B Zheng TM MacDonald S Sutinen V Hurry AK Clarke 2006 A nuclear-encoded ClpP subunit of the chloroplast ATP-dependent Clp protease is essential for early development in Arabidopsis thaliana Planta 224 5 1103 1115 10.1007/s00425-006-0292-2 1:CAS:528:DC%2BD28XpvVartL0%3D 16705403 (Pubitemid 44435861)
39. J Zuegge S Ralph M Schmuker GI McFadden G Schneider 2001 Deciphering apicoplast targeting signals-feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins Gene 280 19 26 10.1016/S0378- 1119(01)00776-4 1:CAS:528:DC%2BD3MXovFCrtb8%3D 11738814 (Pubitemid 34014880)