Direct evidence of O-GlcNAcylation in the apicomplexan Toxoplasma gondii: A biochemical and bioinformatic study

Amino Acids

Volumn 40, Issue 3, 2011, Pages 847-856

  Perez Cervera, Yobana ^a   Harichaux, Grégoire ^a   Schmidt, Jörg ^b   Debierre Grockiego, Françoise ^b,c   Dehennaut, Vanessa ^a,d   Bieker, Ulrike ^b   Meurice, Edwige ^a   Lefebvre, Tony ^a   Schwarz, Ralph T ^a,b  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c CEMAGREF   (France)

^d INSTITUT DE BIOLOGIE DE LILLE   (France)

Author keywords

O GlcNAc; O GlcNAc transferase; O GlcNAcylation; OGT; Plasmodium falciparum; Toxoplasma gondii

Indexed keywords

GLYCOSYLTRANSFERASE; HEAT SHOCK PROTEIN 70; N ACETYLGLUCOSAMINE;

ACYLATION; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; SKIN FIBROBLAST; TOXOPLASMA GONDII; VERO CELL;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; COMPUTATIONAL BIOLOGY; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; N-ACETYLGLUCOSAMINYLTRANSFERASES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TOXOPLASMA;

APICOMPLEXA; PLASMODIUM FALCIPARUM; PROTISTA; TOXOPLASMA GONDII;

EID: 79954428169     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-010-0702-4     Document Type: Article

References (49)

1. KT Andrews TN Tran NC Wheatley DP Fairlie 2009 Targeting histone deacetylase inhibitors for anti-malarial therapy Curr Top Med Chem 9 292 308 1:CAS:528:DC%2BD1MXntVCitrg%3D 10.2174/156802609788085313 19355992
2. S Banerjee PW Robbins J Samuelson 2009 Molecular characterization of nucleocytosolic O-GlcNAc transferases of Giardia lamblia and Cryptosporidium parvum Glycobiology 19 331 336 1:CAS:528:DC%2BD1MXivFSnurs%3D 10.1093/glycob/cwn107 18948359
3. F Berger V Goulet Y Le Strat JC Desenclos 2009 Toxoplasmosis among pregnant women in France: risk factors and change of prevalence between 1995 and 2003 Rev Epidemiol Sante Publique 57 241 248 1:STN:280:DC%2BD1MrjvVCnsA%3D%3D 10.1016/j.respe.2009.03.006 19577390
4. L Braun D Cannella AM Pinheiro S Kieffer H Belrhali J Garin MA Hakimi 2009 The small ubiquitin-like modifier (SUMO)-conjugating system of Toxoplasma gondii Int J Parasitol 39 81 90 1:CAS:528:DC%2BD1cXhsFahurvM 10.1016/j.ijpara.2008.07.009 18761012
5. C Butkinaree K Park GW Hart 2010 O-linked beta-N-acetylglucosamine (O-GlcNAc): extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress Biochim Biophys Acta 1800 96 106 1:CAS:528:DC%2BC3cXotVWitQ%3D%3D 19647786
6. BL Cantarel PM Coutinho C Rancurel T Bernard V Lombard B Henrissat 2009 The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Nucleic Acids Res 37 D233 D238 1:CAS:528:DC%2BD1cXhsFejtL7K 10.1093/nar/gkn663 18838391
7. D Chakrabarti T Da Silva J Barger S Paquette H Patel S Patterson CM Allen 2002 Protein farnesyltransferase and protein prenylation in Plasmodium falciparum J Biol Chem 277 42066 42073 1:CAS:528:DC%2BD38XotF2gt7s%3D 10.1074/jbc.M202860200 12194969 (Pubitemid 35257521)
8. DW Chung N Ponts S Cervantes KG Le Roch 2009 Post-translational modifications in Plasmodium: more than you think! Mol Biochem Parasitol 168 123 134 10.1016/j.molbiopara.2009.08.001 19666057
9. AJ Clarke R Hurtado-Guerrero S Pathak AW Schüttelkopf V Borodkin SM Shepherd AF Ibrahim DM van Aalten 2008 Structural insights into mechanism and specificity of O-GlcNAc transferase EMBO J 27 2780 2788 1:CAS:528: DC%2BD1cXht1KrtLnF 10.1038/emboj.2008.186 18818698
10. FI Comer K Vosseller L Wells MA Accavitti GW Hart 2001 Characterization of a mouse monoclonal antibody specific for O-linked N-acetylglucosamine Anal Biochem 293 169 177 1:CAS:528:DC%2BD3MXkt1Shurc%3D 10.1006/abio.2001.5132 11399029 (Pubitemid 32547901)
11. L Cui J Miao T Furuya X Li XZ Su L Cui 2007 PfGCN5-mediated histone H3 acetylation plays a key role in gene expression in Plasmodium falciparum Eukaryot Cell 6 1219 1227 1:CAS:528:DC%2BD2sXotlGmsbw%3D 10.1128/EC.00062-07 17449656 (Pubitemid 47077173)
12. L Cui Q Fan L Cui J Miao 2008 Histone lysine methyltransferases and demethylases in Plasmodium falciparum Int J Parasitol 38 1083 1097 1:CAS:528:DC%2BD1cXms1SrsLc%3D 10.1016/j.ijpara.2008.01.002 18299133
13. F Debierre-Grockiego N Molitor RT Schwarz CG Lüder 2009 Toxoplasma gondii glycosylphosphatidylinositols up-regulate major histocompatibility complex (MHC) molecule expression on primary murine macrophages Innate Immun 15 25 32 1:CAS:528:DC%2BD1MXktVSktr0%3D 10.1177/1753425908099936 19201822
14. A Dieckmann-Schuppert S Bender M Odenthal-Schnittler E Bause RT Schwarz 1992 Apparent lack of N-glycosylation in the asexual intraerythrocytic stage of Plasmodium falciparum Eur J Biochem 205 815 825 1:CAS:528:DyaK38XitlWlsbc%3D 10.1111/j.1432-1033.1992.tb16846.x 1374032
15. A Dieckmann-Schuppert E Bause RT Schwarz 1993 Studies on O-glycans of Plasmodium-falciparum-infected human erythrocytes. Evidence for O-GlcNAc and O-GlcNAc-transferase in malaria parasites Eur J Biochem 216 779 788 1:CAS:528:DyaK3sXmt1eju7w%3D 10.1111/j.1432-1033.1993.tb18198.x 8404896 (Pubitemid 23284122)
16. D Dorin-Semblat N Quashie J Halbert A Sicard C Doerig E Peat L Ranford-Cartwright C Doerig 2007 Functional characterization of both MAP kinases of the human malaria parasite Plasmodium falciparum by reverse genetics Mol Microbiol 65 1170 1180 1:CAS:528:DC%2BD2sXhtVWnur%2FI 10.1111/j.1365-2958.2007. 05859.x 17651389 (Pubitemid 47262821)
17. S Fauquenoy W Morelle A Hovasse A Bednarczyk C Slomianny C Schaeffer A Van Dorsselaer S Tomavo 2008 Proteomics and glycomics analyses of N-glycosylated structures involved in Toxoplasma gondii-host cell interactions Mol Cell Proteomics 7 891 910 1:CAS:528:DC%2BD1cXmtFehsLY%3D 10.1074/mcp.M700391-MCP200 18187410 (Pubitemid 351737090)
18. EM Frickel V Quesada L Muething MJ Gubbels E Spooner H Ploegh K Artavanis-Tsakonas 2007 Apicomplexan UCHL3 retains dual specificity for ubiquitin and Nedd8 throughout evolution Cell Microbiol 9 1601 1610 1:CAS:528:DC%2BD2sXmt1Cisro%3D 10.1111/j.1462-5822.2007.00896.x 17371404 (Pubitemid 46774029)
19. P Gerold A Dieckmann-Schuppert RT Schwarz 1994 Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malarial parasite, Plasmodium falciparum. Candidates for plasmodial glycosylphosphatidylinositol membrane anchor precursors and pathogenicity factors J Biol Chem 269 2597 2606 1:CAS:528:DyaK2cXht12hs78%3D 8300589
20. BG Grimwood K Hechemy RW Stevens 1979 Toxoplasma gondii: purification of trophozoites propagated in cell culture Exp Parasitol 48 282 286 1:STN:280:DyaL3c%2Fgtlykuw%3D%3D 10.1016/0014-4894(79)90110-3 477817 (Pubitemid 10247760)
21. C Guinez ME Losfeld R Cacan JC Michalski T Lefebvre 2006 Modulation of HSP70 GlcNAc-directed lectin activity by glucose availability and utilization Glycobiology 16 22 28 1:CAS:528:DC%2BD2MXhtlagtbvM 10.1093/glycob/cwj041 16177265 (Pubitemid 43009804)
22. GW Hart MP Housley C Slawson 2007 Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins Nature 446 1017 1022 1:CAS:528:DC%2BD2sXksFersr4%3D 10.1038/nature05815 17460662 (Pubitemid 46676063)
23. LM Hartweck CL Scott NE Olszewski 2002 Two O-linked N-acetylglucosamine transferase genes of Arabidopsis thaliana L. Heynh have overlapping functions necessary for gamete and seed development Genetics 161 1279 1291 1:CAS:528:DC%2BD38XmsF2qsrY%3D 12136030 (Pubitemid 34831451)
24. AT Heaslip JM Leung KL Carey F Catti DM Warshaw NJ Westwood BA Ballif GE Ward 2010 A small-molecule inhibitor of T. gondii motility induces the posttranslational modification of myosin light chain-1 and inhibits myosin motor activity PLoS Pathog 6 e1000720 10.1371/journal.ppat.1000720 20084115
25. Hoessli DC, Poincelet M, Gupta R, Ilangumaran S, Nasir-ud-Din (2003) Plasmodium falciparum merozoite surface protein 1. Eur J Biochem 270:366-375
26. GD Holt CM Snow A Senior RS Haltiwanger L Gerace GW Hart 1987 Nuclear pore complex glycoproteins contain cytoplasmically disposed O-linked N-acetylglucosamine J Cell Biol 104 1157 1164 1:CAS:528:DyaL2sXksFCgurg%3D 10.1083/jcb.104.5.1157 3571327 (Pubitemid 17084473)
27. P Horrocks CI Newbold 2000 Intraerythrocytic polyubiquitin expression in Plasmodium falciparum is subjected to developmental and heat-shock control Mol Biochem Parasitol 105 115 125 1:CAS:528:DyaK1MXnsVKlt74%3D 10.1016/S0166- 6851(99)00174-7 10613704
28. Y Hu J Suarez E Fricovsky H Wang BT Scott SA Trauger W Han Y Hu MO Oyeleye WH Dillmann 2009 Increased enzymatic O-GlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose J Biol Chem 284 547 555 1:CAS:528:DC%2BD1cXhsFCjtLvK 10.1074/jbc.M808518200 19004814
29. BD Lazarus MD Roos JA Hanover 2005 Mutational analysis of the catalytic domain of O-linked N-acetylglucosaminyl transferase J Biol Chem 280 35537 35544 1:CAS:528:DC%2BD2MXhtFWmur3E 10.1074/jbc.M504948200 16105839 (Pubitemid 41532745)
30. BD Lazarus DC Love JA Hanover 2009 O-GlcNAc cycling: implications for neurodegenerative disorders Int J Biochem Cell Biol 41 2134 2146 1:CAS:528:DC%2BD1MXhtFyntL3J 10.1016/j.biocel.2009.03.008 19782947
31. FC Luk TM Johnson CJ Beckers 2008 N-linked glycosylation of proteins in the protozoan parasite Toxoplasma gondii Mol Biochem Parasitol 157 169 178 1:CAS:528:DC%2BD1cXot1yluw%3D%3D 10.1016/j.molbiopara.2007.10.012 18096254
32. C Martinez-Fleites MS Macauley Y He DL Shen DJ Vocadlo GJ Davies 2008 Structure of an O-GlcNAc transferase homolog provides insight into intracellular glycosylation Nat Struct Mol Biol 15 764 765 1:CAS:528:DC%2BD1cXotVeqtrw%3D 10.1038/nsmb.1443 18536723 (Pubitemid 351932003)
33. C Martinez-Fleites Y He GJ Davies 2010 Structural analyses of enzymes involved in the O-GlcNAc modification Biochim Biophys Acta 1800 122 133 1:CAS:528:DC%2BC3cXotVSqsw%3D%3D 19647042
34. C Nicolle L Manceaux 1908 Sur une infection à corps de Leshman (ou organismes voisons) du gondi CR Acad Sci 147 763
35. D Nolte U Müller 2002 Human O-GlcNAc transferase (OGT): genomic structure, analysis of splice variants, fine mapping in Xq13.1 Mamm Genome 13 62 64 1:CAS:528:DC%2BD38XjsVWqtQ%3D%3D 10.1007/s00335-001-2108-9 11773972 (Pubitemid 34008428)
36. U Plessmann I Reiter-Owona KF Lechtreck 2004 Posttranslational modifications of alpha-tubulin of Toxoplasma gondii Parasitol Res 94 386 389 10.1007/s00436-004-1220-7 15549389 (Pubitemid 40022311)
37. A Schmidt RT Schwarz P Gerold 1998 Plasmodium falciparum: asexual erythrocytic stages synthesize two structurally distinct free and protein-bound glycosylphosphatidylinositols in a maturation-dependent manner Exp Parasitol 88 95 102 1:CAS:528:DyaK1cXisVKnsbw%3D 10.1006/expr.1998.4241 9538863 (Pubitemid 28375799)
38. AG Schneider O Mercereau-Puijalon 2005 A new Apicomplexa-specific protein kinase family: multiple members in Plasmodium falciparum, all with an export signature BMC Genomics 6 30 10.1186/1471-2164-6-30 15752424 (Pubitemid 41357705)
39. R Shafi SP Iyer LG Ellies N O'Donnell KW Marek D Chui GW Hart JD Marth 2000 The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny Proc Natl Acad Sci USA 97 5735 5739 1:CAS:528:DC%2BD3cXjvFaktrY%3D 10.1073/pnas.100471497 10801981 (Pubitemid 30367467)
40. A Shen HD Kamp A Gründling DE Higgins 2006 A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression Genes Dev 20 283 295
41. CM Snow A Senior L Gerace 1987 Monoclonal antibodies identify a group of nuclear pore complex glycoproteins J Cell Biol 104 1143 1156 1:CAS:528:DyaL2sXksFKhuro%3D 10.1083/jcb.104.5.1143 2437126 (Pubitemid 17084472)
42. B Striepen CF Zinecker JB Damm PA Melgers GJ Gerwig M Koolen JF Vliegenthart JF Dubremetz RT Schwarz 1997 Molecular structure of the "low molecular weight antigen" of Toxoplasma gondii: a glucose alpha 1-4 N-acetylgalactosamine makes free glycosyl-phosphatidylinositols highly immunogenic J Mol Biol 266 797 813 1:CAS:528:DyaK2sXhvVOksLk%3D 10.1006/jmbi.1996.0806 9102470 (Pubitemid 27113217)
43. CF Teo S Ingale MA Wolfert GA Elsayed LG Nöt JC Chatham L Wells GJ Boons 2010 Glycopeptide-specific monoclonal antibodies suggest new roles for O-GlcNAc Nat Chem Biol 6 338 343 1:CAS:528:DC%2BC3cXjs1egsro%3D 10.1038/nchembio.338 20305658
44. P Ward L Equinet J Packer C Doerig 2004 Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote BMC Genomics 5 79 10.1186/1471-2164-5-79 15479470 (Pubitemid 39546640)
45. LM Weiss A Fiser RH Angeletti K Kim 2009 Toxoplasma gondii proteomics Expert Rev Proteomics 6 303 313 1:CAS:528:DC%2BD1MXms12nu7s%3D 10.1586/epr.09.16 19489701
46. D Wichmann RT Schwarz V Ruppert S Ehrhardt JP Cramer GD Burchard B Maisch F Debierre-Grockiego 2007 Plasmodium falciparum glycosylphosphatidylinositol induces limited apoptosis in liver and spleen mouse tissue Apoptosis 12 1037 1041 10.1007/s10495-006-0033-9 17260185 (Pubitemid 46701603)
47. JO Wrabl NV Grishin 2001 Homology between O-linked GlcNAc transferases and proteins of the glycogen phosphorylase superfamily J Mol Biol 314 365 374 1:CAS:528:DC%2BD38XivFGltA%3D%3D 10.1006/jmbi.2001.5151 11846551 (Pubitemid 33131841)
48. H Xiao K El Bissati P Verdier-Pinard B Burd H Zhang K Kim A Fiser RH Angeletti LM Weiss 2010 Post-translational modifications to Toxoplasma gondii alpha- and beta-tubulins include novel C-terminal methylation Proteome Res 9 359 372 1:CAS:528:DC%2BD1MXhsVensrbM 10.1021/pr900699a
49. X Yang PP Ongusaha PD Miles JC Havstad F Zhang WV So JE Kudlow RH Michell JM Olefsky SJ Field RM Evans 2008 Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance Nature 451 964 969 1:CAS:528: DC%2BD1cXit1yns74%3D 10.1038/nature06668 18288188 (Pubitemid 351301737)