The Rheumatoid Arthritis Risk Variant CCR6DNP Regulates CCR6 via PARP-1

PLoS Genetics

Volumn 12, Issue 9, 2016, Pages

  Li, Gang ^a   Cunin, Pierre ^a   Wu, Di ^a,b,c,i   Diogo, Dorothée ^a,d,j   Yang, Yu ^a   Okada, Yukinori ^e,f,g   Plenge, Robert M ^a,j   Nigrovic, Peter A ^a,h  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MONASH UNIVERSITY   (Australia)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^f Institute of Physical and Chemical Research   (Japan)

^g OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^h BOSTON CHILDREN S HOSPITAL   (United States)

ⁱ UNIVERSITY OF NORTH CAROLINA   (United States)

^j MERCK RESEARCH LABORATORIES   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR6; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; TRANSCRIPTION FACTOR; CCR6 PROTEIN, HUMAN; PARP1 PROTEIN, HUMAN;

ALLELE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA DETERMINATION; DNA POLYMORPHISM; ENZYME ACTIVITY; ENZYME INHIBITION; FLANKING RESTRICTION ENHANCED PULLDOWN ASSAY; GENE LOCUS; GENE SEQUENCE; GENE TARGETING; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC RISK; GENETIC VARIABILITY; HUMAN; HUMAN CELL; INTRON; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATOR GENE; RHEUMATOID ARTHRITIS; CELL LINE; GENETIC POLYMORPHISM; GENETICS; HCT 116 CELL LINE; METABOLISM;

ARTHRITIS, RHEUMATOID; CELL LINE; HCT116 CELLS; HUMANS; POLY (ADP-RIBOSE) POLYMERASE-1; POLYMORPHISM, GENETIC; RECEPTORS, CCR6;

EID: 84990196661     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006292     Document Type: Article

References (46)

1. McInnes IB, Schett G, (2011) The pathogenesis of rheumatoid arthritis. N Engl J Med365: 2205–2219. doi: 10.1056/NEJMra100496522150039
2. Okada Y, Wu D, Trynka G, Raj T, Terao C, et al. (2014) Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature506: 376–381. doi: 10.1038/nature1287324390342
3. (2014) Little boxes. Nat Genet46: 659. doi: 10.1038/ng.302824965724
4. Kochi Y, Okada Y, Suzuki A, Ikari K, Terao C, et al. (2010) A regulatory variant in CCR6 is associated with rheumatoid arthritis susceptibility. Nat Genet42: 515–519. doi: 10.1038/ng.58320453841
5. Lee AY, Korner H, (2014) CCR6 and CCL20: emerging players in the pathogenesis of rheumatoid arthritis. Immunol Cell Biol92: 354–358. doi: 10.1038/icb.2013.9724394994
6. Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, et al. (2007) Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med204: 2803–2812. 18025126
7. Koumakis E, Bouaziz M, Dieude P, Ruiz B, Riemekasten G, et al. (2013) A regulatory variant in CCR6 is associated with susceptibility to antitopoisomerase-positive systemic sclerosis. Arthritis Rheum65: 3202–3208. doi: 10.1002/art.3813623983073
8. Garcia S, Conde C, (2015) The Role of Poly(ADP-ribose) Polymerase-1 in Rheumatoid Arthritis. Mediators Inflamm 2015: 837250. doi: 10.1155/2015/83725026339143
9. Sanjana NE, Cong L, Zhou Y, Cunniff MM, Feng G, et al. (2012) A transcription activator-like effector toolbox for genome engineering. Nat Protoc7: 171–192. doi: 10.1038/nprot.2011.43122222791
10. Gibson BA, Kraus WL, (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol13: 411–424. doi: 10.1038/nrm337622713970
11. Langelier MF, Pascal JM, (2013) PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr Opin Struct Biol23: 134–143. doi: 10.1016/j.sbi.2013.01.00323333033
12. Wu KK, (2006) Analysis of protein-DNA binding by streptavidin-agarose pulldown. Methods Mol Biol338: 281–290. 16888365
13. Tong WM, Cortes U, Hande MP, Ohgaki H, Cavalli LR, et al. (2002) Synergistic role of Ku80 and poly(ADP-ribose) polymerase in suppressing chromosomal aberrations and liver cancer formation. Cancer Res62: 6990–6996. 12460917
14. Zheng YD, Xu XQ, Peng F, Yu JZ, Wu H, (2011) The poly(ADP-ribose) polymerase-1 inhibitor 3-aminobenzamide suppresses cell growth and migration, enhancing suppressive effects of cisplatin in osteosarcoma cells. Oncol Rep25: 1399–1405. doi: 10.3892/or.2011.121221399878
15. Xia Q, Deliard S, Yuan CX, Johnson ME, Grant SF, (2015) Characterization of the transcriptional machinery bound across the widely presumed type 2 diabetes causal variant, rs7903146, within TCF7L2. Eur J Hum Genet23: 103–109. doi: 10.1038/ejhg.2014.4824667787
16. Pelham C, Jimenez T, Rodova M, Rudolph A, Chipps E, et al. (2013) Regulation of HFE expression by poly(ADP-ribose) polymerase-1 (PARP1) through an inverted repeat DNA sequence in the distal promoter. Biochim Biophys Acta1829: 1257–1265. doi: 10.1016/j.bbagrm.2013.10.00224184271
17. Lodhi N, Kossenkov AV, Tulin AV, (2014) Bookmarking promoters in mitotic chromatin: poly(ADP-ribose)polymerase-1 as an epigenetic mark. Nucleic Acids Res42: 7028–7038. doi: 10.1093/nar/gku41524861619
18. Beranger GE, Momier D, Rochet N, Quincey D, Guigonis JM, et al. (2006) RANKL treatment releases the negative regulation of the poly(ADP-ribose) polymerase-1 on Tcirg1 gene expression during osteoclastogenesis. J Bone Miner Res21: 1757–1769. 17002555
19. Chiba-Falek O, Kowalak JA, Smulson ME, Nussbaum RL, (2005) Regulation of alpha-synuclein expression by poly (ADP ribose) polymerase-1 (PARP-1) binding to the NACP-Rep1 polymorphic site upstream of the SNCA gene. Am J Hum Genet76: 478–492. 15672325
20. Yu Z, Kuncewicz T, Dubinsky WP, Kone BC, (2006) Nitric oxide-dependent negative feedback of PARP-1 trans-activation of the inducible nitric-oxide synthase gene. J Biol Chem281: 9101–9109. 16464859
21. Yazdany J, Davis J, (2004) The role of CD40 ligand in systemic lupus erythematosus. Lupus13: 377–380. 15230296
22. Frizzell KM, Gamble MJ, Berrocal JG, Zhang T, Krishnakumar R, et al. (2009) Global analysis of transcriptional regulation by poly(ADP-ribose) polymerase-1 and poly(ADP-ribose) glycohydrolase in MCF-7 human breast cancer cells. J Biol Chem284: 33926–33938. doi: 10.1074/jbc.M109.02387919812418
23. Ambrose HE, Papadopoulou V, Beswick RW, Wagner SD, (2007) Poly-(ADP-ribose) polymerase-1 (Parp-1) binds in a sequence-specific manner at the Bcl-6 locus and contributes to the regulation of Bcl-6 transcription. Oncogene26: 6244–6252.
24. Nirodi C, NagDas S, Gygi SP, Olson G, Aebersold R, et al. (2001) A role for poly(ADP-ribose) polymerase in the transcriptional regulation of the melanoma growth stimulatory activity (CXCL1) gene expression. J Biol Chem276: 9366–9374. 11112786
25. Huang K, Tidyman WE, Le KU, Kirsten E, Kun E, et al. (2004) Analysis of nucleotide sequence-dependent DNA binding of poly(ADP-ribose) polymerase in a purified system. Biochemistry43: 217–223. 14705948
26. Petrucco S, Percudani R, (2008) Structural recognition of DNA by poly(ADP-ribose)polymerase-like zinc finger families. FEBS J275: 883–893. doi: 10.1111/j.1742-4658.2008.06259.x18215166
27. Bonicalzi ME, Haince JF, Droit A, Poirier GG, (2005) Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when?Cell Mol Life Sci62: 739–750. 15868399
28. Thomas C, Tulin AV, (2013) Poly-ADP-ribose polymerase: machinery for nuclear processes. Mol Aspects Med34: 1124–1137. doi: 10.1016/j.mam.2013.04.00123624145
29. Kim MY, Zhang T, Kraus WL, (2005) Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev19: 1951–1967. 16140981
30. Schiewer MJ, Goodwin JF, Han S, Brenner JC, Augello MA, et al. (2012) Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov2: 1134–1149. doi: 10.1158/2159-8290.CD-12-012022993403
31. Martinez-Zamudio R, Ha HC, (2012) Histone ADP-ribosylation facilitates gene transcription by directly remodeling nucleosomes. Mol Cell Biol32: 2490–2502. doi: 10.1128/MCB.06667-1122547677
32. Ji Y, Tulin AV, (2010) The roles of PARP1 in gene control and cell differentiation. Curr Opin Genet Dev20: 512–518. doi: 10.1016/j.gde.2010.06.00120591646
33. Ji Y, Tulin AV, (2009) Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res37: 3501–3513. doi: 10.1093/nar/gkp21819346337
34. Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, et al. (2008) Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science319: 819–821. doi: 10.1126/science.114925018258916
35. Di Giammartino DC, Shi Y, Manley JL, (2013) PARP1 represses PAP and inhibits polyadenylation during heat shock. Mol Cell49: 7–17. doi: 10.1016/j.molcel.2012.11.00523219533
36. Ji Y, Tulin AV, (2012) Poly(ADP-ribose) controls DE-cadherin-dependent stem cell maintenance and oocyte localization. Nat Commun3: 760. doi: 10.1038/ncomms175922453833
37. Pavri R, Lewis B, Kim TK, Dilworth FJ, Erdjument-Bromage H, et al. (2005) PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol Cell18: 83–96. 15808511
38. Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andriantsitohaina R, et al. (1999) Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J18: 4446–4454. 10449410
39. Zingarelli B, Hake PW, Burroughs TJ, Piraino G, O'Connor M, et al. (2004) Activator protein-1 signalling pathway and apoptosis are modulated by poly(ADP-ribose) polymerase-1 in experimental colitis. Immunology113: 509–517. 15554929
40. Veres B, Radnai B, Gallyas F, Jr.Varbiro G, Berente Z, et al. (2004) Regulation of kinase cascades and transcription factors by a poly(ADP-ribose) polymerase-1 inhibitor, 4-hydroxyquinazoline, in lipopolysaccharide-induced inflammation in mice. J Pharmacol Exp Ther310: 247–255. 14999056
41. Garcia S, Bodano A, Gonzalez A, Forteza J, Gomez-Reino JJ, et al. (2006) Partial protection against collagen antibody-induced arthritis in PARP-1 deficient mice. Arthritis Res Ther8: R14. 16356201
42. Gonzalez-Rey E, Martinez-Romero R, O'Valle F, Aguilar-Quesada R, Conde C, et al. (2007) Therapeutic effect of a poly(ADP-ribose) polymerase-1 inhibitor on experimental arthritis by downregulating inflammation and Th1 response. PLoS One2: e1071. 17971849
43. Ahmad SF, Attia SM, Zoheir KM, Ashour AE, Bakheet SA, (2014) Attenuation of the progression of adjuvant-induced arthritis by 3-aminobenzamide treatment. Int Immunopharmacol19: 52–59. doi: 10.1016/j.intimp.2014.01.00524444779
44. Ahmad SF, Zoheir KM, Bakheet SA, Ashour AE, Attia SM, (2014) Poly(ADP-ribose) polymerase-1 inhibitor modulates T regulatory and IL-17 cells in the prevention of adjuvant induced arthritis in mice model. Cytokine68: 76–85. doi: 10.1016/j.cyto.2014.04.00624845796
45. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, et al. (2012) Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med366: 1382–1392. doi: 10.1056/NEJMoa110553522452356
46. Noss EH, Nguyen HN, Chang SK, Watts GF, Brenner MB, (2015) Genetic polymorphism directs IL-6 expression in fibroblasts but not selected other cell types. Proc Natl Acad Sci U S A112: 14948–14953. doi: 10.1073/pnas.152086111226578807