MJD and OTU deubiquitinating enzymes in Schistosoma mansoni

Parasitology Research

Volumn 114, Issue 8, 2015, Pages 2835-2843

  Pereira, Roberta Verciano ^a   de Souza Gomes, Matheus ^b   Costa, Marcela Pereira ^a   Jannotti Passos, Liana Konovaloff ^c   de Castro Borges, William ^a   Guerra Sá, Renata ^a  

^a FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

^b FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Deubiquitinating enzymes; Deubiquitination activity; Differential expression; Josephin and OTU domains

Indexed keywords

ASPARAGINE; ASPARTIC ACID; ATAXIN 3; CYSTEINE; DEUBIQUITINASE; HELMINTH PROTEIN; HISTIDINE; MJD PROTEIN; OTU PROTEIN; SM ATAXIN 3; SM JOSEPHIN; SM OTU1; SM OTU3; SM OTU5A; SM OTU6B; SM OTUBAIN; UNCLASSIFIED DRUG; PROTEASOME; PROTEINASE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CERCARIA; COMPUTER MODEL; CONTROLLED STUDY; ENZYME STRUCTURE; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; MICROBIAL GENOME; MOUSE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SCHISTOSOMULUM; ANIMAL; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LIFE CYCLE STAGE; METABOLISM; PROTEIN PROCESSING; UBIQUITINATION;

SCHISTOSOMA MANSONI;

ANIMALS; CERCARIA; ENDOPEPTIDASES; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HELMINTH PROTEINS; HUMANS; LIFE CYCLE STAGES; PHYLOGENY; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; SCHISTOSOMA MANSONI; UBIQUITINATION;

EID: 84938953780     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-015-4484-1     Document Type: Article

References (46)

1. Basch P, DiConza J (1977) In vitro development of Schistosoma mansoni cercariae. J Parasitol 63:245–249
2. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42(Web Server issue):W252–8
3. Blackford AN, Stewart GS (2010) When cleavage is not attractive: non-catalytic inhibition of ubiquitin chains at DNA double-strand breaks by OTUB1. DNA Repair (Amst) 10(2):245–9
4. Borodovsky A, Ovaa H, Kolli N, Gan-Erdene T, Wilkinson KD, Ploegh HL, Kessler BM (2002) Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem Biol 10:1149–59
5. Callis J (2014) The ubiquitination machinery of the ubiquitin system. Arabidopsis Book 12, e0174
6. Castro-Borges W, Cartwright J, Ashton PD, Braschi S, Guerra-Sá R, Rodrigues V, Wilson RA, Curwen RS (2007) The 20S proteasome of Schistosoma mansoni: a proteomic analysis. Proteomics 7:1065–1075
7. Clague MJ, Barsukov I, Coulson JM, Liu H, Rigden DJ, Urbé S (2013) Deubiquitylases from genes to organism. Physiol Rev 93(3):1289–315
8. Eletr ZM, Wilkinson KD (2014) Regulation of proteolysis by human deubiquitinating enzymes. Biochim Biophys Acta 1843(1):114–28
9. Faesen AC, Luna-Vargas MPA, Geurink PP, Clerici M, Merkx R, van Dijk WJ, Hameed DS, El Oualid F, Ovaa H, Sixma TK (2011) The differential modulation of USP activity by internal regulatory domains, interactors and eight ubiquitin chain types. Chem Biol 18:1550–1561
10. Ferro A, Carvalho AL, Teixeira-Castro A, Almeida C, Tomé RJ, Cortes L, Rodrigues AJ, Logarinho E, Sequeiros J, Macedo-Ribeiro S, Maciel P (2007) NEDD8: a new ataxin-3 interactor. Biochim Biophys Acta 1773(11):1619–27
11. Fishelson Z, Amiri P, Friend DS, Marikovsky M, Petitt M, Newport G, McKerrow JH (1992) Schistosoma mansoni: cell-specific expression and secretion of a serine protease during development of cercariae. Exp Parasitol 75:87–98
12. Guerra-Sá R, Castro-Borges W, Evangelista EA, Kettelhut IC, Rodrigues V (2005) Schistosoma mansoni: functional proteasomes are required for development in the vertebrate host. Exp Parasitol 109:228–236
13. Harrop R, Wilson RA (1993) Protein synthesis and release by cultured schistosomula of Schistosoma mansoni. Parasitology 107:265–274
14. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–79
15. Ju HL, Kang JM, Noh HS, Kim DR, Hong Y, Sohn WM, Na BK (2014) Characterization of a novel otubain-like cysteine protease of Cryptosporidium parvum. Parasitol Int 63(4):580–3
16. Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C, O’Rourke KM, Eby M, Pietras E, Cheng G, Bazan JF, Zhang Z, Arnott D, Dixit VM (2007) DUBA: a deubiquitinase that regulates type I interferon production. Science 318:1628–1632
17. Komander D, Clague MJ, Urbe S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10:550–563
18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–8
19. Li Y, Sun XX, Elferich J, Shinde U, David LL, Dai MS (2014) Monoubiquitination is critical for ovarian tumor domain-containing ubiquitin aldehyde binding protein 1 (Otub1) to suppress UbcH5 enzyme and stabilize p53 protein. J Biol Chem 289(8):5097–108
20. Liu S, Cai P, Hou N, Piao X, Wang H, Hung T, Chen Q (2012) Genome-wide identification and characterization of a panel of house-keeping genes in Schistosoma japonicum. Mol Biochem Parasitol 182(1-2):75–82
21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta DeltaC(T)) Method”. Methods 25:402–408
22. Makarova KS, Aravind L, Koonin EV (2000) A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci 25:50–2
23. Masino L, Nicastro G, De Simone A, Calder L, Molloy J, Pastore A (2011) The Josephin domain determines the morphological and mechanical properties of ataxin-3 fibrils. Biophys J 100(8):2033–42
24. McGouran JF, Gaertner SR, Altun M, Kramer HB, Kessler BM (2013) Deubiquitinating enzyme specificity for ubiquitin chain topology profiled by di-ubiquitin activity probes. Chem Biol 20(12):1447–55
25. McKerrow JH, Salter J (2002) Invasion of skin by Schistosoma cercariae. Trends Parasitol 18:193–195
26. McNicholas S, Potterton, Wilson KS, Noble ME (2011) Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr D Biol Crystallogr 67(Pt 4):386–94
27. Messick TE, Russell NS, Iwata AJ, Sarachan KL, Shiekhattar R, Shanks JR, Reyes-Turcu FE, Wilkinson KD, Marmorstein R (2008) Structural basis for ubiquitin recognition by the Otu1 ovarian tumor domain protein. J Biol Chem 283(16):11038–49
28. Mevissen TE, Hospenthal MK, Geurink PP, Elliott PR, Akutsu M, Arnaudo N, Ekkebus R, Kulathu Y, Wauer T, El Oualid F, Freund SM, Ovaa H, Komander D (2013) OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell 154(1):169–84
29. Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, Juang YC, O’Donnell L, Kumakubo A, Munro M, Sicheri F, Gingras AC, Natsume T, Suda T, Durocher D (2010) Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466(7309):941–6
30. Nicastro G, Masino L, Esposito V, Menon RP, De Simone A, Fraternali F, Pastore A (2009) Josephin domain of ataxin-3 contains two distinct ubiquitin-binding sites. Biopolymers 91(12):1203–14
31. Nicastro G, Menon RP, Masino L, Knowles PP, McDonald NQ, Pastore A (2005) The solution structure of the Josephin domain of ataxin-3: structural determinants for molecular recognition. Proc Natl Acad Sci U S A 102(30):10493–8
32. Pereira RV, Vieira HG, Oliveira VF, Gomes MD, Passos LK, Borges WD, Guerra-Sá R (2014) Conservation and developmental expression of ubiquitin isopeptidases in Schistosoma mansoni. Mem Inst Oswaldo Cruz 109(1):1–8
33. Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acids Res 38:227–233
34. Rawlings ND, Morton FR, Kok CY, Kong J, Barrett AJ (2008) MEROPS: the peptidase database. Nucleic Acids Res 36:320–325
35. Reina CP, Zhong X, Pittman RN (2010) Proteotoxic stress increases nuclear localization of ataxin-3. Hum Mol Genet 19(2):235–49
36. Reyes-Turcu FE, Wilkinson KD (2009) Polyubiquitin binding and disassembly by deubiquitinating enzymes. Chem Rev 109:1495–1508
37. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
38. Sato Y, Yamagata A, Goto-Ito S, Kubota K, Miyamoto R, Nakada S, Fukai S (2012) Molecular basis of Lys-63-linked polyubiquitination inhibition by the interaction between human deubiquitinating enzyme OTUB1 and ubiquitin-conjugating enzyme UBC13. J Biol Chem 287(31):25860–8
39. Seki T, Gong L, Williams AJ, Sakai N, Todi SV, Paulson HL (2013) JosD1, a membrane-targeted deubiquitinating enzyme, is activated by ubiquitination and regulates membrane dynamics, cell motility, and endocytosis. J Biol Chem 288(24):17145–55
40. Stirewalt MA (1974) Schistosoma mansoni: cercaria to schistosomule. Adv Parasitol 12:115–182
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5. Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–9
42. Tzvetkov N, Breuer P (2007) Josephin domain-containing proteins from a variety of species are active de-ubiquitination enzymes. Biol Chem 388(9):973–8
43. Xu Z, Zheng Y, Zhu Y, Kong X, Hu L (2011) Evidence for OTUD-6B participation in B lymphocytes cell cycle after cytokine stimulation. PLoS One 6(1), e14514
44. Weeks SD, Grasty KC, Hernandez-Cuebas L, Loll PJ (2011) Crystal structure of a Josephin-ubiquitin complex: evolutionary restraints on ataxin-3 deubiquitinating activity. J Biol Chem 286(6):4555–65
45. Wiener R, Zhang X, Wang T, Wolberger C (2012) The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature 483(7391):618–22
46. Winborn BJ, Travis SM, Todi SV, Scaglione KM, Xu P, Williams AJ, Cohen RE, Peng J, Paulson HL (2008) The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J Biol Chem 283(39):26436–43