#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

THAP11F80L cobalamin disorder-associated mutation reveals normal and pathogenic THAP11 functions in gene expression and cell proliferation


Autoři: Harmonie Dehaene aff001;  Viviane Praz aff001;  Philippe Lhôte aff001;  Maykel Lopes aff001;  Winship Herr aff001
Působiště autorů: Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland aff001;  Vital-IT, Swiss Institute of Bioinformatics, University of Lausanne, Lausanne, Switzerland aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224646

Souhrn

Twelve human THAP proteins share the THAP domain, an evolutionary conserved zinc-finger DNA-binding domain. Studies of different THAP proteins have indicated roles in gene transcription, cell proliferation and development. We have analyzed this protein family, focusing on THAP7 and THAP11. We show that human THAP proteins possess differing homo- and heterodimer formation properties and interaction abilities with the transcriptional co-regulator HCF-1. HEK-293 cells lacking THAP7 were viable but proliferated more slowly. In contrast, HEK-293 cells were very sensitive to THAP11 alteration. Nevertheless, HEK-293 cells bearing a THAP11 mutation identified in a patient suffering from cobalamin disorder (THAP11F80L) were viable although proliferated more slowly. Cobalamin disorder is an inborn vitamin deficiency characterized by neurodevelopmental abnormalities, most often owing to biallelic mutations in the MMACHC gene, whose gene product MMACHC is a key enzyme in the cobalamin (vitamin B12) metabolic pathway. We show that THAP11F80L selectively affected promoter binding by THAP11, having more deleterious effects on a subset of THAP11 targets, and resulting in altered patterns of gene expression. In particular, THAP11F80L exhibited a strong effect on association with the MMACHC promoter and led to a decrease in MMACHC gene transcription, suggesting that the THAP11F80L mutation is directly responsible for the observed cobalamin disorder.

Klíčová slova:

Gene expression – DNA-binding proteins – Mutation – Sequence motif analysis – Immunoprecipitation – Cell proliferation – Cobalamins – Transcriptional control


Zdroje

1. Roussigne M, Kossida S, Lavigne A-C, Clouaire T, Ecochard V, Glories A, et al. The THAP domain: a novel protein motif with similarity to the DNA-binding domain of P element transposase. Trends Biochem Sci. 2003;28: 66–9. doi: 10.1016/S0968-0004(02)00013-0 12575992

2. Clouaire T, Roussigne M, Ecochard V, Mathe C, Amalric F, Girard J-P. The THAP domain of THAP1 is a large C2CH module with zinc-dependent sequence-specific DNA-binding activity. Proc Natl Acad Sci U S A. 2005;102: 6907–12. doi: 10.1073/pnas.0406882102 15863623

3. Bessière D, Lacroix C, Campagne S, Ecochard V, Guillet V, Mourey L, et al. Structure-function analysis of the THAP zinc finger of THAP1, a large C2CH DNA-binding module linked to Rb/E2F pathways. J Biol Chem. 2008;283: 4352–4363. doi: 10.1074/jbc.M707537200 18073205

4. Gervais V, Campagne S, Durand J, Muller I, Milon A. NMR studies of a new family of DNA binding proteins: The THAP proteins. J Biomol NMR. 2013;56: 3–15. doi: 10.1007/s10858-012-9699-1 23306615

5. Dejosez M, Levine SS, Frampton GM, Whyte WA, Stratton SA, Barton MC, et al. Ronin/Hcf-1 binds to a hyperconserved enhancer element and regulates genes involved in the growth of embryonic stem cells. Genes Dev. 2010;24: 1479–1484. doi: 10.1101/gad.1935210 20581084

6. Sabogal A, Lyubimov AY, Corn JE, Berger JM, Rio DC. THAP proteins target specific DNA sites through bipartite recognition of adjacent major and minor grooves. Nat Struct Mol Biol. 2010;17: 117–124. doi: 10.1038/nsmb.1742 20010837

7. Balakrishnan MP, Cilenti L, Ambivero C, Goto Y, Takata M, Turkson J, et al. THAP5 is a DNA-binding transcriptional repressor that is regulated in melanoma cells during DNA damage-induced cell death. Biochem Biophys Res Commun. 2011;404: 195–200. doi: 10.1016/j.bbrc.2010.11.092 21110952

8. Macfarlan T, Parker JB, Nagata K, Chakravarti D. Thanatos-associated protein 7 associates with template activating factor-Ibeta and inhibits histone acetylation to repress transcription. Mol Endocrinol. 2006;20: 335–47. doi: 10.1210/me.2005-0248 16195249

9. Macfarlan T, Kutney S, Altman B, Montross R, Yu J, Chakravarti D. Human THAP7 is a chromatin-associated, histone tail-binding protein that represses transcription via recruitment of HDAC3 and nuclear hormone receptor corepressor. J Biol Chem. 2005;280: 7346–7358. doi: 10.1074/jbc.M411675200 15561719

10. Miele A, Medina R, Van Wijnen AJ, Stein GS, Stein JL. The interactome of the histone gene regulatory factor HiNF-P suggests novel cell cycle related roles in transcriptional control and RNA processing. J Cell Biochem. 2007;102: 136–148. doi: 10.1002/jcb.21284 17577209

11. Dejosez M, Krumenacker JS, Zitur LJ, Passeri M, Chu LF, Songyang Z, et al. Ronin Is Essential for Embryogenesis and the Pluripotency of Mouse Embryonic Stem Cells. Cell. 2008;133: 1162–1174. doi: 10.1016/j.cell.2008.05.047 18585351

12. Parker JB, Palchaudhuri S, Yin H, Wei J, Chakravarti D. A Transcriptional Regulatory Role of the THAP11-HCF-1 Complex in Colon Cancer Cell Function. Mol Cell Biol. 2012;32: 1654–1670. doi: 10.1128/MCB.06033-11 22371484

13. Zhu CY, Li CY, Li Y, Zhan YQ, Li YH, Xu CW, et al. Cell growth suppression by thanatos-associated protein 11(THAP11) is mediated by transcriptional downregulation of c-Myc. Cell Death Differ. 2009;16: 395–405. doi: 10.1038/cdd.2008.160 19008924

14. Nakamura S, Yokota D, Tan L, Nagata Y, Takemura T, Hirano I, et al. Down-regulation of Thanatos-associated protein 11 by BCR-ABL promotes CML cell proliferation through c-Myc expression. Int J Cancer. 2012;130: 1046–1059. doi: 10.1002/ijc.26065 21400515

15. Parker JB, Yin H, Vinckevicius A, Chakravarti D. Host cell factor-1 recruitment to E2F-bound and cell-cycle-control genes is mediated by THAP11 and ZNF143. Cell Rep. 2014;9: 967–82. doi: 10.1016/j.celrep.2014.09.051 25437553

16. Michaud J, Praz V, Faresse NJ, JnBaptiste CK, Tyagi S, Schütz F, et al. HCFC1 is a common component of active human CpG-island promoters and coincides with ZNF143, THAP11, YY1, and GABP transcription factor occupancy. Genome Res. 2013;23: 907–916. doi: 10.1101/gr.150078.112 23539139

17. Fujita J, Freire P, Coarfa C, Benham AL, Gunaratne P, Schneider MD, et al. Ronin Governs Early Heart Development by Controlling Core Gene Expression Programs. Cell Rep. 2017;21: 1562–1573. doi: 10.1016/j.celrep.2017.10.036 29117561

18. Durruthy-Durruthy J, Wossidlo M, Pai S, Takahashi Y, Kang G, Omberg L, et al. Spatiotemporal Reconstruction of the Human Blastocyst by Single-Cell Gene-Expression Analysis Informs Induction of Naive Pluripotency. Dev Cell. 2016;38: 100–115. doi: 10.1016/j.devcel.2016.06.014 27404362

19. Seifert BA, Dejosez M, Zwaka TP. Ronin influences the DNA damage response in pluripotent stem cells. Stem Cell Res. 2017;23: 98–104. doi: 10.1016/j.scr.2017.06.014 28715716

20. Kong XZ, Yin RH, Ning HM, Zheng WW, Dong XM, Yang Y, et al. Effects of THAP11 on erythroid differentiation and megakaryocytic differentiation of K562 cells. PLoS One. 2014;9. doi: 10.1371/journal.pone.0091557 24637716

21. Poché RA, Zhang M, Rueda EM, Tong X, McElwee ML, Wong L, et al. RONIN Is an Essential Transcriptional Regulator of Genes Required for Mitochondrial Function in the Developing Retina. Cell Rep. 2016;14: 1684–1697. doi: 10.1016/j.celrep.2016.01.039 26876175

22. Quintana AM, Yu HC, Brebner A, Pupavac M, Geiger EA, Watson A, et al. Mutations in THAP11 cause an inborn error of cobalamin metabolism and developmental abnormalities. Hum Mol Genet. 2017;26: 2838–2849. doi: 10.1093/hmg/ddx157 28449119

23. Ozelius LJ, Bressman SB. Genetic and clinical features of primary torsion dystonia. Neurobiol Dis. 2011;42: 127–135. doi: 10.1016/j.nbd.2010.12.012 21168499

24. Bragg DC, Armata IA, Nery FC, Breakefield XO, Sharma N. Molecular pathways in dystonia. Neurobiol Dis. 2011;42: 136–147. doi: 10.1016/j.nbd.2010.11.015 21134457

25. LeDoux MS, Xiao J, Rudzińska M, Bastian RW, Wszolek ZK, Van Gerpen JA, et al. Genotype-phenotype correlations in THAP1 dystonia: Molecular foundations and description of new cases. Park Relat Disord. 2012;18: 414–425. doi: 10.1016/j.parkreldis.2012.02.001 22377579

26. Balakrishnan MP, Cilenti L, Mashak Z, Popat P, Alnemri ES, Zervos AS. THAP5 is a human cardiac-specific inhibitor of cell cycle that is cleaved by the proapoptotic Omi/HtrA2 protease during cell death. Am J Physiol Heart Circ Physiol. 2009;297: H643–53. doi: 10.1152/ajpheart.00234.2009 19502560

27. Li Y, Ning Q, Shi J, Chen Y, Jiang M, Gao L, et al. A novel epigenetic AML1‐ETO/THAP10/miR‐383 mini‐circuitry contributes to t(8;21) leukaemogenesis. EMBO Mol Med. 2017;9: 933–949. doi: 10.15252/emmm.201607180 28539478

28. Gladitz J, Klink B, Seifert M. Network-based analysis of oligodendrogliomas predicts novel cancer gene candidates within the region of the 1p/19q co-deletion. Acta Neuropathol Commun. 2018;6: 49. doi: 10.1186/s40478-018-0544-y 29890994

29. Abate F, da Silva-Almeida AC, Zairis S, Robles-Valero J, Couronne L, Khiabanian H, et al. Activating mutations and translocations in the guanine exchange factor VAV1 in peripheral T-cell lymphomas. Proc Natl Acad Sci. 2017;114: 764–769. doi: 10.1073/pnas.1608839114 28062691

30. de Souza Santos E, de Bessa SA, Netto MM, Nagai MA. Silencing of LRRC49 and THAP10 genes by bidirectional promoter hypermethylation is a frequent event in breast cancer. Int J Oncol. 2008;33: 25–31. 18575747

31. Johnson RA, Wright KD, Poppleton H, Mohankumar KM, Finkelstein D, Pounds SB, et al. Cross-species genomics matches driver mutations and cell compartments to model ependymoma. Nature. 2010;466: 632–636. doi: 10.1038/nature09173 20639864

32. Lian WX, Yin RH, Kong XZ, Zhang T, Huang XH, Zheng WW, et al. THAP11, a novel binding protein of PCBP1, negatively regulates CD44 alternative splicing and cell invasion in a human hepatoma cell line. FEBS Lett. 2012;586: 1431–1438. doi: 10.1016/j.febslet.2012.04.016 22673507

33. Sloan JL, Carrillo N, Adams D, Venditti CP. Disorders of Intracellular Cobalamin Metabolism. GeneReviews®. 2018. Available: http://www.ncbi.nlm.nih.gov/pubmed/20301503

34. Freiman RN, Herr W. Viral mimicry: Common mode of association with HCF by VP16 and the cellular protein LZIP. Genes Dev. 1997;11: 3122–3127. doi: 10.1101/gad.11.23.3122 9389645

35. Lu R, Yang P, Padmakumar S, Misra V. The herpesvirus transactivator VP16 mimics a human basic domain leucine zipper protein, luman, in its interaction with HCF. J Virol. 1998;72: 6291–6297. 9658067

36. Burkhard P, Stetefeld J, Strelkov S V. Coiled coils: A highly versatile protein folding motif. Trends Cell Biol. 2001;11: 82–88. doi: 10.1016/s0962-8924(00)01898-5 11166216

37. Sanghavi HM, Mallajosyala SS, Majumdar S. Classification of the human THAP protein family identifies an evolutionarily conserved coiled coil region. 2019; 2–11.

38. Lupas A, Van Dyke M, Stock J. Predicting coiled coils from protein sequences. Science. 1991;252: 1162–4. doi: 10.1126/science.252.5009.1162 2031185

39. McDonnell A V, Jiang T, Keating AE, Berger B. Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics. 2006;22: 356–8. doi: 10.1093/bioinformatics/bti797 16317077

40. Dehaene H. THAP proteins in the transcriptional control of cell proliferation. Doctoral dissertation. University of Lausanne. 2019. Available: https://serval.unil.ch/notice/serval:BIB_02ABC667C655

41. Cukier CD, Maveyraud L, Saurel O, Guillet V, Milon A, Gervais V. The C-terminal region of the transcriptional regulator THAP11 forms a parallel coiled-coil domain involved in protein dimerization. J Struct Biol. 2016;194: 337–346. doi: 10.1016/j.jsb.2016.03.010 26975212

42. Wilson AC, LaMarco K, Peterson MG, Herr W. The VP16 accessory protein HCF is a family of polypeptides processed from a large precursor protein. Cell. 1993;74: 115–125. doi: 10.1016/0092-8674(93)90299-6 8392914

43. Kristie TM, Pomerantz JL, Twomey TC, Parent SA, Sharp PA. The cellular C1 factor of the herpes simplex virus enhancer complex is a family of polypeptides. J Biol Chem. 1995;270: 4387–94. doi: 10.1074/jbc.270.9.4387 7876203

44. Wilson AC, Freiman RN, Goto H, Nishimoto T, Herr W. VP16 targets an amino-terminal domain of HCF involved in cell cycle progression. Mol Cell Biol. 1997;17: 6139–46. Available: http://www.ncbi.nlm.nih.gov/pubmed/9315674 doi: 10.1128/mcb.17.10.6139 9315674

45. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337: 816–21. doi: 10.1126/science.1225829 22745249

46. Costa Y, Ding J, Theunissen TW, Faiola F, Hore TA, Shliaha P V., et al. NANOG-dependent function of TET1 and TET2 in establishment of pluripotency. Nature. 2013;495: 370–374. doi: 10.1038/nature11925 23395962

47. Ngondo-Mbongo RP, Myslinski E, Aster JC, Carbon P. Modulation of gene expression via overlapping binding sites exerted by ZNF143, Notch1 and THAP11. Nucleic Acids Res. 2013;41: 4000–4014. doi: 10.1093/nar/gkt088 23408857

48. Sengel C, Gavarini S, Sharma N, Ozelius LJ, Bragg DC. Dimerization of the DYT6 dystonia protein, THAP1, requires residues within the coiled-coil domain. J Neurochem. 2011;118: 1087–1100. doi: 10.1111/j.1471-4159.2011.07386.x 21752024

49. Richter A, Hollstein R, Hebert E, Vulinovic F, Eckhold J, Osmanovic A, et al. In-depth Characterization of the Homodimerization Domain of the Transcription Factor THAP1 and Dystonia-Causing Mutations Therein. J Mol Neurosci. 2017;62: 11–16. doi: 10.1007/s12031-017-0904-2 28299530

50. Lek M, Karczewski KJ, Minikel E V., Samocha KE, Banks E, Fennell T, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016;536: 285–291. doi: 10.1038/nature19057 27535533

51. Fuchs T, Gavarini S, Saunders-Pullman R, Raymond D, Ehrlich ME, Bressman SB, et al. Mutations in the THAP1 gene are responsible for DYT6 primary torsion dystonia. Nat Genet. 2009;41: 286–288. doi: 10.1038/ng.304 19182804

52. Frederick NM, Shah P V, Didonna A, Langley MR, Kanthasamy AG, Opal P. Loss of the dystonia gene Thap1 leads to transcriptional deficits that converge on common pathogenic pathways in dystonic syndromes. Hum Mol Genet. 2019;28: 1343–1356. doi: 10.1093/hmg/ddy433 30590536

53. Xiromerisiou G, Houlden H, Scarmeas N, Stamelou M, Kara E, Hardy J, et al. THAP1 Mutations And Dystonia Phenotypes: Genotype Phenotype Correlations. 2012;27: 1290–1294. doi: 10.1002/mds.25146 22903657

54. Campagne S, Muller I, Milon A, Gervais V. Towards the classification of DYT6 dystonia mutants in the DNA-binding domain of THAP1. Nucleic Acids Res. 2012;40: 9927–9940. doi: 10.1093/nar/gks703 22844099

55. Gavarini S, Cayrol C, Fuchs T, Lyons N, Ehrlich ME, Girard JP, et al. Direct interaction between causative genes of DYT1 and DYT6 primary dystonia. Ann Neurol. 2010;68: 549–553. doi: 10.1002/ana.22138 20865765

56. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8: 2281–2308. doi: 10.1038/nprot.2013.143 24157548

57. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23: 127–8. doi: 10.1093/bioinformatics/btl529 17050570

58. Letunic I, Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011;39: W475–8. doi: 10.1093/nar/gkr201 21470960

59. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29: 15–21. doi: 10.1093/bioinformatics/bts635 23104886

60. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12: 323. doi: 10.1186/1471-2105-12-323 21816040

61. Li B, Ruotti V, Stewart RM, Thomson JA, Dewey CN. RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics. 2010;26: 493–500. doi: 10.1093/bioinformatics/btp692 20022975

62. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281

63. The Gene Ontology Consortium. Expansion of the Gene Ontology knowledgebase and resources. Nucleic Acids Res. 2017;45: D331–D338. doi: 10.1093/nar/gkw1108 27899567

64. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25: 25–9. doi: 10.1038/75556 10802651

65. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9: R137. doi: 10.1186/gb-2008-9-9-r137 18798982

66. Renaud M, Praz V, Vieu E, Florens L, Washburn MP, L’Hôte P, et al. Gene duplication and neofunctionalization: POLR3G and POLR3GL. Genome Res. 2014;24: 37–51. doi: 10.1101/gr.161570.113 24107381

67. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al. The Human Genome Browser at UCSC. Genome Res. 2002;12: 996–1006. doi: 10.1101/gr.229102 12045153


Článok vyšiel v časopise

PLOS One


2020 Číslo 1
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#