#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Bioinformatic analysis of a novel Echinococcus granulosus nuclear receptor with two DNA binding domains


Autoři: Gabriela Alvite aff001;  Ximena Riera aff001;  Saira Cancela aff001;  Margot Paulino aff002;  Adriana Esteves aff001
Působiště autorů: Biochemistry Section, Faculty of Sciences, Universidad de la República, Montevideo, Uruguay aff001;  Center of Bioinformatics, Departamento de Experimentación y Teoría de la Materia, Faculty of Chemistry, Universidad de la República, Montevideo, Uruguay aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224703

Souhrn

Nuclear receptors are ligand-activated transcription factors capable of regulating the expression of complex gene networks. The family includes seven subfamilies of proteins with a wide phylogenetic distribution. A novel subfamily with two DNA-binding domains (2DBDs) has been reported in Schistosoma mansoni (Platyhelminth, Trematoda). This work describes the cDNA cloning and bioinformatics analysis of Eg2DBDα, a 2DBD nuclear receptor isoform from the parasite Echinococcus granulosus (Platyhelminth, Cestoda). The Eg2DBDα gene coding domain structure was analysed. Although two additional 2DBD nuclear receptors are reported in the parasite database GeneDB, they are unlikely to be expressed in the larval stage. Phylogenetic relationships between these atypical proteins from different cestodes are also analysed including S. mansoni 2DBD nuclear receptors. The presence of two DNA binding domains confers particular interest to these nuclear receptors, not only concerning their function but to the development of new antihelminthic drugs.

Klíčová slova:

DNA-binding proteins – Sequence alignment – Sequence motif analysis – Protein domains – DNA sequence analysis – Sequence databases – Schistosoma mansoni – Cestodes


Zdroje

1. Jensen EV. “On the Mechanism of Estrogen Action.” Perspectives in Biology and Medicine. 1962;6: 47–60. doi: 10.1353/pbm.1963.0005 13957617

2. Evans RM, David J, Mangelsdorf DJ. Nuclear Receptors, RXR, and the Big Bang. Cell. 2014;157: 255–266. doi: 10.1016/j.cell.2014.03.012 24679540

3. Weikum ER, Liu X, Ortlund EA. The nuclear receptor superfamily: A structural perspective. Protein Sci. 2018;27:1876–1892. doi: 10.1002/pro.3496 30109749

4. Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell. 1995;83: 841–850. doi: 10.1016/0092-8674(95)90200-7 8521508

5. Enmark E, Gustafsson JA. Orphan nuclear receptors: the first eight years. Mol Endocrinol. 1996;10: 1293–307. doi: 10.1210/mend.10.11.8923456 8923456

6. Bridgham JT, Eick GN, Larroux C, Deshpande K, Harms MJ, Gauthier ME, Ortlund EA, Degnan BM, Thornton JW. Protein evolution by molecular tinkering: diversification of the nuclear receptor superfamily from a ligand-dependent ancestor. PLoS Biol. 2010;8i: e1000497.

7. Escriva H, Bertrand S, Laudet V. The evolution of the nuclear receptor superfamily. Essay Biochem. 2004;40: 11–26.

8. Laudet V, Auwerx J, Gustafsson JA, Wahli W. A unified nomenclature system for the nuclear receptor superfamily. Cell. 1999;97: 161–163. doi: 10.1016/s0092-8674(00)80726-6 10219237

9. Wu W, Niles EG, El-Sayed N, Berriman M, LoVerde PT. Schistosoma mansoni (Platyhelminthes, Trematoda) nuclear receptors: sixteen new members and a novel subfamily. Gene. 2006;366: 303–15. doi: 10.1016/j.gene.2005.09.013 16406405

10. Giguère V, Hollenberg SM, Rosenfeld MG, Evans RM. Functional domains of the human glucocorticoid receptor. Cell. 1986;46: 645–52. doi: 10.1016/0092-8674(86)90339-9 3742595

11. Germain P, Staels B, Dacquet C, Spedding M, Laudet V. Overview of nomenclature of nuclear receptors. Pharmacol. Rev. 2006;58: 685–704. doi: 10.1124/pr.58.4.2 17132848

12. Pawlak M, Lefebvre P, Staels B. General molecular biology and architecture of nuclear receptors. Curr Top Med Chem. 2012;12:486–504. doi: 10.2174/156802612799436641 22242852

13. Laudet G, Adelmant G. Nuclear receptors. Lonesome orphans. Curr Biol. 1995;5: 124–126. doi: 10.1016/s0960-9822(95)00031-5 7743173

14. Bain D, Heneghan AE, Connaghan-Jones KD, Miura MT. Nuclear receptor structure: implications for function. Annu Rev Physiol. 2007; 69: 201–220. doi: 10.1146/annurev.physiol.69.031905.160308 17137423

15. Melvin VS, Roemer SC, Churchill ME, Edwards DP. The C-terminal extension (CTE) of the nuclear hormone receptor DNA binding domain determines interactions and functional response to the HMGB-1/-2 co-regulatory proteins. J Biol Chem. 2002;277: 25115–25124. doi: 10.1074/jbc.M110400200 12006575

16. Wurtz JM, Bourguet W, Renaud JP, Vivat V., Chambon P., Moras D, et al. A canonical structure for the ligand-binding domain of nuclear receptors. Nat Struct Biol. 1996;3: 87–94. doi: 10.1038/nsb0196-87 8548460

17. Thompson RCA. Biology and Systematics of Echicococcus. In: Echinococcus and Hydatid Disease. CAB International Publication, Oxford University Press, Oxford, England. 1995

18. Escriva H, Safi R, Hanni C, Anglois MC, Saumitou-Aprade P. Stehelin, et al. Ligand binding was acquired during evolution of nuclear receptors. Proc Natl Acad Sci USA. 1997;94: 6803–6808. doi: 10.1073/pnas.94.13.6803 9192646

19. Freebern WJ, Niles EG, LoVerde PT. RXR-2, a member of the retinoid x receptor family in Schistosoma mansoni. Gene, 1999; 233: 33–8. doi: 10.1016/s0378-1119(99)00161-4 10375618

20. Freebern WJ, Osman A, Niles EG, Christen L, LoVerde PT. Identification of a cDNA encoding a retinoid X receptor homologue from Schistosoma mansoni. Evidence for a role in female-specific gene expression. J Biol Chem. 1999;274: 4577–85. doi: 10.1074/jbc.274.8.4577 9988692

21. De Mendonça RL, Escriva H, Bouton D, Zelus D, Vanacker JM, Bonnelye E, Cornette J, Pierce RJ, Laudet V. Structural and functional divergence of a nuclear receptor of the RXR family from the trematode parasite Schistosoma mansoni. Eur J Biochem. 2000; 267: 3208–19. doi: 10.1046/j.1432-1327.2000.01344.x 10824105

22. De Mendonça RL, Bouton D, Bertin B, Escriva H, Noël C, Vanacker JM, Cornette J, Laudet V, Pierce RJ. A functionally conserved member of the FTZ-F1 nuclear receptor family from Schistosoma mansoni. Eur J Biochem. 2002; 269: 5700–11. doi: 10.1046/j.1432-1033.2002.03287.x 12423370

23. Esteves A, Dallagiovanna B, Ehrlich R. A developmentally regulated gene of Echinococcus granulosus codes for a 15.5-kilodalton polypeptide related to fatty acid binding proteins. Mol Biochem Parasitol. 1993;58: 215–222. doi: 10.1016/0166-6851(93)90043-w 8479446

24. Sievers F, Wilm A, Dineen D, Gibson TJ., Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011;7: 539. doi: 10.1038/msb.2011.75 21988835

25. Milburn D, Laskowski RA, Thornton JM. Sequences annotated by structure: a tool to facilitate the use of structural information in sequence analysis. Prot. Eng. 1998;11: 855–859.

26. Roy A, Xu D, Poisson J, Zhang Y. A Protocol for Computer-Based Protein Structure and Function Prediction. J Vis Exp. 2011;57: e3259.

27. Kumar S., Stecher G., Li M., Knyaz C., and Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution. 2018;35:1547–1549. doi: 10.1093/molbev/msy096 29722887

28. Jones D.T., Taylor W.R., and Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences. 1992;8: 275–282. doi: 10.1093/bioinformatics/8.3.275 1633570

29. Wu W, Niles EG, Hirohisa Hirai H, LoVerde PT. Evolution of a novel subfamily of nuclear receptors with members that each contain two DNA binding domains. BMC Evolutionary Biology. 2007; 7: 27. doi: 10.1186/1471-2148-7-27 17319953

30. Laudet V, Hanni C, Coll J, Catzeflis F, Stehelin D. Evolution of the nuclear receptor gene superfamily. EMBO J. 1992;1: 1003–1013.

31. Brelivet Y, Kammerer S, Rochel N, Poch O, Moras D. Signature of the oligomeric behaviour of nuclear receptors at the sequence and structural level. EMBO Rep. 2004;5: 423–9. doi: 10.1038/sj.embor.7400119 15105832

32. Yang M, Li J, Wu J Wang H, Guo B, Wu C, et al.Cloning and characterization of an Echinococcus granulosus ecdysteroid hormone nuclear receptor HR3-like gene. Parasite 2017;24: 36. doi: 10.1051/parasite/2017037 28971798

33. Dingwall C, Laskey RA. Nuclear targeting sequences a consensus? Trends Biochem. Sci. 1991;16: 478–481. doi: 10.1016/0968-0004(91)90184-w 1664152

34. Picard D, Yamamoto KR. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J. 1987;6: 3333–3340. 3123217

35. Sessler RJ, Noy N. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol Cell. 2005;18: 343–53. doi: 10.1016/j.molcel.2005.03.026 15866176

36. Walther RF, Atlas E, Carrigan A, Rouleau Y, Edgecombe A, Visentin L, et al. A Serine/Threonine-rich motif is one of three nuclear localization signals that determine unidirectional transport of the mineralocorticoid receptor to the nucleus. J Biol Chem. 2005;280: 17549–17561. doi: 10.1074/jbc.M501548200 15737989

37. Ayers SD, Nedrow KL. Gillilan RE, Noy N. Continuous nucleocytoplasmic shuttling underlies transcriptional activation of PPARγ by FABP4. Biochemistry. 2007;46: 6744–6752. doi: 10.1021/bi700047a 17516629

38. Escobedo G, Larralde C, Chavarria A, Cerbón MA, Morales-Montor J. Molecular mechanisms involved in the differential effects of sex steroids on the reproduction and infectivity of Taenia crassiceps. J Parasitol. 2004;90: 1235–1244. doi: 10.1645/GE-297R 15715212

39. Pakharukova MY, Ershov NI, Vorontsova EV, Shilov AG., Merkulova TI, Mordvinov VA. Identification of thyroid hormone receptor homologs in the fluke Opisthorchis felineus (Platyhelminthes). Mol Biochem Parasitol. 2014;194: 64–68. doi: 10.1016/j.molbiopara.2014.04.009 24798031

40. Wu W, LoVerde PT. Nuclear hormone receptors in parasitic helminths. Mol Cell Endocrinol. 2011;334: 56–66. doi: 10.1016/j.mce.2010.06.011 20600585

41. Förster S, Günthel D, Kiss F, Brehm K. Molecular characterisation of a serum-responsive, DAF-12-like nuclear hormone receptor of the fox-tapeworm Echinococcus multilocularis. J Cell Biochem. 2011; 112: 1630–1642. doi: 10.1002/jcb.23073 21328613

42. Nicolao MC, Elissondo MC, Denegri GM, Goya AB, Cumino AC. In vitro and in vivo effects of tamoxifen against larval stage Echinococcus granulosus. Antimicrob Agents Chemother. 2014;58: 5146–5154. doi: 10.1128/AAC.02113-13 24936598

43. Liu S, Zhou X, Hao L, Piao X, Hou N, Chen Q. Genome-wide Transcriptome analysis reveals extensive alternative splicing events in the protoscoleces of Echinococcus granulosus and Echinococcus multilocularis. Front Microbiol. 2017;8: 929. doi: 10.3389/fmicb.2017.00929 28588571

44. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Ann Rev Biochem. 2003;72: 291–336. doi: 10.1146/annurev.biochem.72.121801.161720 12626338

45. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature, 2008;456: 470–476. doi: 10.1038/nature07509 18978772

46. Gibilisco L, Zhou Q, Mahajan S, Bachtrog D. Alternative splicing within and between Drosophila species, sexes, tissues, and developmental stages. PLoS Genetics. 2016;12, e1006464. doi: 10.1371/journal.pgen.1006464 27935948

47. Umesono K, Evans RM. Determinants of target gene specificity for steroid/thyroid hormone receptors. Cell. 1989;57: 1139–1146. doi: 10.1016/0092-8674(89)90051-2 2500251

48. Luisi BF, Xu WX, Otwinowski Z, Freedman LP, Yamamoto KR, Sigler PB. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature. 1991;352: 497–505. doi: 10.1038/352497a0 1865905

49. Zechel C, Shen Xi-Q, Chambon P, Hinrich Gronemeyer H. Dimerization interfaces formed between the DNA binding domains determine the cooperative binding of RXR/RAR and RXR/TR heterodimers to DR5 and DR4 elements. EMBO J. 1994;13: 1414–1424. 8137825

50. Alvite G, Esteves A. Echinococcus granulosus fatty acid binding proteins subcelullar localization. Exp Parasitol. 2016;164: 1–4 doi: 10.1016/j.exppara.2016.02.002 26873273

51. Kalderon D, Roberts BL, Richardson WD, Smith AE. A short amino acid sequence able to specify nuclear location. Cell. 1984;39: 499–509. doi: 10.1016/0092-8674(84)90457-4 6096007

52. Hodel MR, Corbett AH, Hodel AE. Dissection of a nuclear localization signal. J Biol Chem. 2001;276: 1317–1325. doi: 10.1074/jbc.M008522200 11038364

53. Robbins J, Dilworth SM, Laskey RA, Dingwall C. Two interdependent basic domains in nucleoplasmin targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell. 1991;64: 615–623. doi: 10.1016/0092-8674(91)90245-t 1991323

54. Hickey CM, Wilson NR, Hochstrasser M. Function and regulation of SUMOproteases. Nat Rev Mol Cell Biol. 2012;13: 755–766. doi: 10.1038/nrm3478 23175280

55. Sentis S, Le Romancer, M, Bianchin C, Rostan M-C, Corbo L. Sumoylation of the estrogen receptor hinge region regulates its transcriptional activity. Mol. Endocrinol. 2006;19: 2671–2684.

56. Pourcet B, Pineda-Torra I, Derudas B, Staelsm B, Glineurm, C. SUMOylation of human peroxisome proliferator-activated receptor alpha inhibits its trans-activity through the recruitment of the nuclear corepressor NCoR. J Biol Chem. 2010;285: 5983–5992. doi: 10.1074/jbc.M109.078311 19955185

57. Pascual G, Fong AL, Ogawa S, Gamliel A, Li AC, Perissi V, et al. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature. 2005;437: 759–763. doi: 10.1038/nature03988 16127449

58. Venteclef N, Jakobsson T, Ehrlund A, Damdimopoulos A, Mikkonen L, Ellis E, et al. GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev. 2010;24: 381–395. doi: 10.1101/gad.545110 20159957

59. Treuter E, Venteclef N. Transcriptional control of metabolic and inflammatory pathways by nuclear receptor SUMOylation. Biochim Biophys Acta. 2011;1812: 909–918. doi: 10.1016/j.bbadis.2010.12.008 21172431

60. Wang Z, Schaffer NE, Kliewer SA, Mangelsdorf DJ. Nuclear receptors: emerging drug targets for parasitic diseases. J. Clin. Invest. 2017;127: 1165–1171. doi: 10.1172/JCI88890 28165341

61. Overington JP, Al-Lazikani B, Hopkins AL. How many drug targets are there? Nat. Rev Drug Discov. 2006;5: 993–996. doi: 10.1038/nrd2199 17139284


Článok vyšiel v časopise

PLOS One


2019 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#