Regulation of HFE expression by poly(ADP-ribose) polymerase-1 (PARP1) through an inverted repeat DNA sequence in the distal promoter

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 12, 2013, Pages 1257-1265

  Pelham, Christopher ^a   Jimenez, Tamara ^a   Rodova, Marianna ^a   Rudolph, Angela ^a   Chipps, Elizabeth ^a   Islam, M Rafiq ^a  

^a NORTHWEST MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Cruciform; HAMP; HFE; Inverted repeat; Negative element; PARP1

Indexed keywords

HEMIN; HEMOCHROMATOSIS PROTEIN; HEPCIDIN; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PLASMA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEK293; DNA SEQUENCE; EMBRYO; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INVERTED REPEAT; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; TRANSCRIPTION REGULATION;

CRUCIFORM; HAMP; HEMOCHROMATOSIS; HEMOCHROMATOSIS PROTEIN; HFE; HH; INVERTED REPEAT; NEGATIVE ELEMENT; PARP1; POLY(ADP-RIBOSE) POLYMERASE-1;

BLOTTING, WESTERN; CHLORIDES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FERRIC COMPOUNDS; GENE EXPRESSION REGULATION; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HEP G2 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INVERTED REPEAT SEQUENCES; LUCIFERASES; MEMBRANE PROTEINS; NOXAE; PEPTIDE FRAGMENTS; POLY(ADP-RIBOSE) POLYMERASES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84887506992     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.10.002     Document Type: Article

References (52)

1. Gan E.K., Powell L.W., Olynyk J.K. Natural history and management of HFE-hemochromatosis. Semin. Liver Dis. 2011, 31:293-301.
2. Feder J.N., Gnirke A., Thomas W., Tsuchihashi Z., Ruddy D.A., Basava A., Dormishian, Domingo R., Ellis M.C., Fullan A., Hinton L.M., Jones N.L., Kimmel B.E., Kronmal G.S., Lauer P., Lee V.K., Loeb D.B., Mapa F.A., McClelland E., Meyer N.C., Mintier G.A., Moeller N., Moore T., Morikang E., Prass C.E., Quintana L., Starnes S.M., Schatzman R.C., Brunke K.J., Drayna D.T., Risch N.J., Bacon B.R., Wolff R.K. A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat. Genet. 1996, 13:399-408.
3. Babitt J.L., Lin H.Y. The molecular pathogenesis of hereditary hemochromatosis. Semin. Liver Dis. 2011, 31:280-292.
4. Swinkels D.W., Fleming R.E. Novel observations in hereditary hemochromatosis: potential implications for clinical strategies. Haematologica 2011, 96:485-488.
5. Ajioka R.S., Levy J.E., Andrews N.C., Kushner J.P. Regulation of iron absorption in Hfe mutant mice. Blood 2002, 100:1465-1469.
6. Zhou X.Y., Tomatsu S., Fleming R.E., Parkkila S., Waheed A., Jiang J., Fei Y., Brunt E.M., Ruddy D.A., Prass C.E., Schatzman R.C., O'Neill R., Britton R.S., Bacon B.R., Sly W.S. HFE gene knockout produces mouse model of hereditary hemochromatosis. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:2492-2497.
7. Tomatsu S., Orii K.O., Fleming R.E., Holden C.C., Waheed A., Britton R.S., Gutierrez M.A., Velez-Castrillon S., Bacon B.R., Sly W.S. Contribution of the H63D mutation in HFE to murine hereditary hemochromatosis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15788-15793.
8. Drakesmith H., Townsend A. The structure and function of HFE. Bioessays 2000, 22:595-598.
9. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342:249-268.
10. Bonicalzi M.E., Haince J.F., Droit A., Poirier G.G. Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when?. Cell. Mol. Life Sci. 2005, 62:739-750.
11. Krishnakumar R., Kraus W.L. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 2010, 39:8-24.
12. Hakmé A., Wong H.K., Dantzer F., Schreiber V. The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Rep. 2008, 9:1094-1100.
13. Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 2006, 7:517-528.
14. Krishnakumar R., Gamble M.J., Frizzell K.M., Berrocal J.G., Kininis M., Kraus W.L. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 2008, 319:819-821.
15. Brázda V., Laister R.C., Jagelská E.B., Arrowsmith C. Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol. Biol. 2011, 12:33-40.
16. Chasovskikh S., Dimtchev A., Smulson M., Dritschilo A. DNA transitions induced by binding of PARP-1 to cruciform structures in supercoiled plasmids. Cytometry A 2005, 68:21-27.
17. Nirodi C., NagDas S., Gygi S.P., Olson G., Aebersold R., Richmond A. A role for poly(ADP-ribose) polymerase in the transcriptional regulation of the melanoma growth stimulatory activity (CXCL1) gene expression. J. Biol. Chem. 2001, 276:9366-9374.
18. Kim M.Y., Mauro S., Gévry N., Lis J.T., Kraus W.L. NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 2004, 119:803-814.
19. Cervellera M.N., Sala A. Poly(ADP-ribose) polymerase is a B-MYB coactivator. J. Biol. Chem. 2000, 275:10692-10696.
20. Hassa P.O., Covic M., Hasan S., Imhof R., Hottiger M.O. The enzymatic and DNA binding activity of PARP-1 are not required for NF-kappa B coactivator function. J. Biol. Chem. 2001, 276:45588-45597.
21. Pavri R., Lewis B., Kim T.K., Dilworth F.J., Erdjument-Bromage H., Tempst P., de Murcia G., Evans R., Chambon P., Reinberg D. PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol. Cell 2005, 18:83-96.
22. Islam M.R., Jimenez T., Pelham C., Rodova M., Puri S., Magenheimer B.S., Maser R.L., Widmann C., Calvet J.P. MAP/ERK kinase kinase 1 (MEKK1) mediates transcriptional repression by interacting with polycystic kidney disease-1 (PKD1) promoter-bound p53 tumor suppressor protein. J. Biol. Chem. 2010, 285:38818-38831.
23. Rodova M., Jayini R., Singasani R., Chipps E., Islam M.R. CMV promoter is repressed by p53 and activated by JNK Pathway. Plasmid 2013, 69:223-230.
24. Baker A.S., Pelham C., Dong Z., Islam M.R. Probes biotinylation by A-tailing and use in DNA-protein interactions. Am. Biotechnol. Lab. 2008, 26:26-27.
25. Mura C., Le Gac G., Jacolot S., Férec C. Transcriptional regulation of the human HFE gene indicates high liver expression and erythropoiesis coregulation. FASEB J. 2004, 18:1922-1924.
26. Pugh B.F., Tjian R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 1990, 61:1187-1197.
27. Rodriguez-Lopez R., Donoso M., Fernandez-Cavada M., Gonzalez L.M., Margallo A., Corral C., Gallego M., Garcia de Caceres M.T., Herrera T., Gonzalez C., Vagace J.M., Gervasini G. Diagnostic utility of HFE variants in Spanish patients: association with HLA alleles and role in susceptibility to acute lymphoblastic leukemia. Gene 2013, 514:31-35.
28. Martins R., Silva B., Proença D., Faustino P. Differential HFE gene expression is regulated by alternative splicing in human tissues. PLoS One 2011, 6:e17542.
29. Beranger G.E., Momier D., Rochet N., Quincey D., Guigonis J.M., Samson M., Carle G.F., Scimeca J.C. RANKL treatment releases the negative regulation of the poly(ADP-ribose) polymerase-1 on Tcirg1 gene expression during osteoclastogenesis. J. Bone Miner. Res. 2006, 21:1757-1769.
30. Chiba-Falek O., Kowalak J.A., Smulson M.E., Nussbaum R.L. 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. Genet. 2005, 76:478-492.
31. Yu Z., Kuncewicz T., Dubinsky W.P., Kone B.C. Nitric oxide-dependent negative feedback of PARP-1 trans-activation of the inducible nitric-oxide synthase gene. J. Biol. Chem. 2006, 281:9101-9109.
32. Soldatenkov V.A., Chasovskikh S., Potaman V.N., Trofimova I., Smulson M.E., Dritschilo A. Transcriptional repression by binding of poly(ADP-ribose) polymerase to promoter sequences. J. Biol. Chem. 2002, 277:665-670.
33. Frizzell K.M., Gamble M.J., Berrocal J.G., Zhang T., Krishnakumar R., Cen Y., Sauve A.A., Kraus W.L. 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. Chem. 2009, 284:33926-33938.
34. Huang K., Tidyman W.E., Le K.U., Kirsten E., Kun E., Ordahl C.P. Analysis of nucleotide sequence-dependent DNA binding of poly(ADP-ribose) polymerase in a purified system. Biochemistry 2004, 43:217-223.
35. Salama M.F., Bayele H.K., Srai S.S. Tumour necrosis factor alpha downregulates human hemojuvelin expression via a novel response element within its promoter. J. Biomed. Sci. 2012, 19:83-95.
36. Soldani C., Scovassi A.I. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 2002, 7:321-328.
37. Gobeil S., Boucher C.C., Nadeau D., Poirier G.G. Characterization of the necrotic cleavage of poly(ADP-ribose) polymerase (PARP-1): implication of lysosomal proteases. Cell Death Differ. 2001, 8:588-594.
38. Kraus W.L. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell Biol. 2008, 20:294-302.
39. Amiri K.I., Ha H.C., Smulson M.E., Richmond A. Differential regulation of CXC ligand 1 transcription in melanoma cell lines by poly(ADP-ribose) polymerase-1. Oncogene 2006, 25:7714-7722.
40. Ambrose H.E., Papadopoulou V., Beswick R.W., Wagner S.D. 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. Oncogene 2007, 26:6244-6252.
41. Andrews N.C., Schmidt P.J. Iron homeostasis. Annu. Rev. Physiol. 2007, 69:69-85.
42. Luo X., Kraus W.L. On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev. 2012, 26:417-432.
43. Kobayashi T. Suppression of matrix metalloproteinase-9 expression in undifferentiated, non-apoptotic keratinocytes is abrogated by the cleavage of poly(ADP-ribose) polymerase-1. Apoptosis 2011, 16:1205-1216.
44. Sukumari-Ramesh S., Laird M.D., Singh N., Vender J.R., Alleyne C.H., Dhandapani K.M. Astrocyte-derived glutathione attenuates hemin-induced apoptosis in cerebral microvascular cells. Glia 2010, 58:1858-1870.
45. Wang J., Pantopoulos K. Regulation of cellular iron metabolism. Biochem. J. 2011, 434:365-381.
46. Subramaniam V.N., McDonald C.J., Ostini L., Lusby P.E., Wockner L.F., Ramm G.A. Hepatic iron deposition does not predict extrahepatic iron loading in mouse models of hereditary hemochromatosis. Am. J. Pathol. 2012, 181:1173-1179.
47. Bridle K.R., Frazer D.M., Wilkins S.J., Dixon J.L., Purdie D.M., Crawford D.H., Subramaniam V.N., Powell L.W., Anderson G.J., Ramm G.A. Disrupted hepcidin regulation in HFE-associated haemochromatosis and the liver as a regulator of body iron homoeostasis. Lancet 2003, 361(9358):669-673.
48. Hietakangas V., Poukkula M., Heiskanen K.M., Karvinen J.T., Sistonen L., Eriksson J.E. Erythroid differentiation sensitizes K562 leukemia cells to TRAIL-induced apoptosis by downregulation of c-FLIP. Mol. Cell. Biol. 2003, 23:1278-1291.
49. Chow J.M., Huang G.C., Shen H.Y.S.C., Yang L.Y., Chen Y.C. Cytotoxic effects of metal protoporphyrins in glioblastoma cells: roles of albumin, reactive oxygen species, and heme oxygenase-1. Toxicol. Lett. 2008, 177:97-107.
50. Lange T.S., Kim K.K., Singh R.K., Strongin R.M., McCourt C.K., Brard L. Iron(III)-salophene: an organometallic compound with selective cytotoxic and anti-proliferative properties in platinum-resistant ovarian cancer cells. PLoS ONE 2008, 3(5):e2303. 10.1371/journal.pone.0002303.
51. Cañuelo A., Martínez-Romero R., Martínez-Lara E., Sánchez-Alcázar J.A., Siles E. The hypoxic preconditioning agent deferoxamine induces poly(ADP-ribose) polymerase-1-dependent inhibition of the mitochondrial respiratory chain. Mol. Cell. Biochem. 2012, 363:101-108.
52. Gardenghi S., Marongiu M.F., Ramos P., Guy E., Breda L., Chadburn A., Liu Y., Amariglio N., Rechavi G., Rachmilewitz E.A., Breuer W., Cabantchik Z.I., Wrighting D.M., Andrews N.C., de Sousa M., Giardina P.J., Grady R.W., Rivella Stefano Ineffective erythropoiesis in β-thalassemia is characterized by increased iron absorption mediated by down-regulation of hepcidin and up-regulation of ferroportin. Blood 2007, 109:5027-5035.