5-Lipoxygenase is a direct p53 target gene in humans

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 8, 2015, Pages 1003-1016

  Gilbert, Bianca ^a   Ahmad, Khalil ^a   Roos, Jessica ^a   Lehmann, Christoph ^f   Chiba, Tomohiro ^b   Ulrich Rückert, Sandra ^a   Smeenk, Leonie ^e   van Heeringen, Simon ^d   Maier, Thorsten J ^a,g   Groner, Bernd ^c   Steinhilber, Dieter ^a  

^a GOETHE UNIVERSITY   (Germany)

^b KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^f FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^g AARHUS UNIVERSITY   (Denmark)

Author keywords

5 Lipoxygenase; Chromatin immunoprecipitation; Leukemia; Leukotriene; P21; p53

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; DACTINOMYCIN; ETOPOSIDE; LEUKOTRIENE; MESSENGER RNA; PROTEIN P53; ALOX5 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ALOX5 GENE; ARTICLE; BINDING SITE; BIOSYNTHESIS; CARCINOGENESIS; CELL FREE SYSTEM; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; GENOTOXICITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPATHOLOGY; IMMUNOPRECIPITATION; INTRON; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; STRESS; TRANSCRIPTION INITIATION SITE; TUMOR GROWTH; U2OS CELL LINE; DNA DAMAGE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; HELA CELL LINE; PHYSIOLOGY; PROMOTER REGION; TUMOR CELL CULTURE;

ARACHIDONATE 5-LIPOXYGENASE; BINDING SITES; DACTINOMYCIN; DNA DAMAGE; ETOPOSIDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HUMANS; PROMOTER REGIONS, GENETIC; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84934958501     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.06.004     Document Type: Article

References (58)

1. Linzer D.I., Levine A.J. Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell 1979, 17:43-52.
2. Lane D.P., Crawford L.V. T antigen is bound to a host protein in SV40-transformed cells. Nature 1979, 278:261-263.
3. Smeenk L., Lohrum M. Behind the scenes: unravelling the molecular mechanisms of p53 target gene selectivity (review). Int. J. Oncol. 2010, 37:1061-1070.
4. Miyashita T., Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995, 80:293-299.
5. Baker S.J., Fearon E.R., Nigro J.M., Hamilton S.R., Preisinger A.C., Jessup J.M., et al. Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. Science 1989, 244:217-221.
6. Nigro J.M., Baker S.J., Preisinger A.C., Jessup J.M., Hostetter R., Cleary K., et al. Mutations in the p53 gene occur in diverse human tumour types. Nature 1989, 342:705-708.
7. el-Deiry W.S., Tokino T., Velculescu V.E., Levy D.B., Parsons R., Trent J.M., et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993, 75:817-825.
8. Chipuk J.E., Green D.R. PUMA cooperates with direct activator proteins to promote mitochondrial outer membrane permeabilization and apoptosis. Cell Cycle 2009, 8:2692-2696.
9. Hermeking H., Lengauer C., Polyak K., He T.C., Zhang L., Thiagalingam S., et al. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1997, 1:3-11.
10. Oda E., Ohki R., Murasawa H., Nemoto J., Shibue T., Yamashita T., et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000, 288:1053-1058.
11. Vogelstein B., Lane D., Levine A.J. Surfing the p53 network. Nature 2000, 408:307-310.
12. Ko L.J., Prives C. p53: puzzle and paradigm. Genes Dev. 1996, 10:1054-1072.
13. de Vries A., Flores E.R., Miranda B., Hsieh H.-M., van Oostrom C.T.M., Sage J., et al. Targeted point mutations of p53 lead to dominant-negative inhibition of wild-type p53 function. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2948-2953.
14. el-Deiry W.S., Kern S.E., Pietenpol J.A., Kinzler K.W., Vogelstein B. Definition of a consensus binding site for p53. Nat. Genet. 1992, 1:45-49.
15. Espinosa J.M. Mechanisms of regulatory diversity within the p53 transcriptional network. Oncogene 2008, 27:4013-4023.
16. Hupp T.R., Meek D.W., Midgley C.A., Lane D.P. Regulation of the specific DNA binding function of p53. Cell 1992, 71:875-886.
17. Steinhilber D., Fischer A.S., Metzner J., Steinbrink S.D., Roos J., Ruthardt M., et al. 5-Lipoxygenase: underappreciated role of a pro-inflammatory enzyme in tumorigenesis. Front. Pharmacol. 2010, 1:143.
18. Shimizu T., Izumi T., Seyama Y., Tadokoro K., Rådmark O., Samuelsson B. Characterization of leukotriene A4 synthase from murine mast cells: evidence for its identity to arachidonate 5-lipoxygenase. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:4175-4179.
19. Rouzer C.A., Matsumoto T., Samuelsson B. Single protein from human leukocytes possesses 5-lipoxygenase and leukotriene A4 synthase activities. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:857-861.
20. Werz O. 5-Lipoxygenase: cellular biology and molecular pharmacology. Curr. Drug Targets Inflamm. Allergy 2002, 1:23-44.
21. Chen Y., Hu Y., Zhang H., Peng C., Li S. Loss of the Alox5 gene impairs leukemia stem cells and prevents chronic myeloid leukemia. Nat. Genet. 2009, 41:783-792.
22. Roos J., Oancea C., Heinssmann M., Khan D., Held H., Kahnt A.S., et al. 5-Lipoxygenase is a candidate target for therapeutic management of stem cell-like cells in acute myeloid leukemia. Cancer Res. 2014, 74:5244-5255.
23. Boado R.J., Pardridge W.M., Vinters H.V., Black K.L. Differential expression of arachidonate 5-lipoxygenase transcripts in human brain tumors: evidence for the expression of a multitranscript family. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:9044-9048.
24. Gupta S., Srivastava M., Ahmad N., Sakamoto K., Bostwick D.G., Mukhtar H. Lipoxygenase-5 is overexpressed in prostate adenocarcinoma. Cancer 2001, 91:737-743.
25. Hennig R., Ding X.-Z., Tong W.-G., Schneider M.B., Standop J., Friess H., et al. 5-Lipoxygenase and leukotriene B(4) receptor are expressed in human pancreatic cancers but not in pancreatic ducts in normal tissue. Am. J. Pathol. 2002, 161:421-428.
26. Jiang W.G., Douglas-Jones A., Mansel R.E. Levels of expression of lipoxygenases and cyclooxygenase-2 in human breast cancer. Prostaglandins Leukot. Essent. Fat. Acids 2003, 69:275-281.
27. Ohd J.F., Nielsen C.K., Campbell J., Landberg G., Löfberg H., Sjölander A. Expression of the leukotriene D4 receptor CysLT1, COX-2, and other cell survival factors in colorectal adenocarcinomas. Gastroenterology 2003, 124:57-70.
28. Jiang W.G., Douglas-Jones A.G., Mansel R.E. Aberrant expression of 5-lipoxygenase-activating protein (5-LOXAP) has prognostic and survival significance in patients with breast cancer. Prostaglandins Leukot. Essent. Fat. Acids 2006, 74:125-134.
29. Brungs M., Rådmark O., Samuelsson B., Steinhilber D. Sequential induction of 5-lipoxygenase gene expression and activity in Mono Mac 6 cells by transforming growth factor beta and 1,25-dihydroxyvitamin D3. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:107-111.
30. Rådmark O., Werz O., Steinhilber D., Samuelsson B. 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 2007, 32:332-341.
31. Catalano A., Caprari P., Soddu S., Procopio A., Romano M. 5-Lipoxygenase antagonizes genotoxic stress-induced apoptosis by altering p53 nuclear trafficking. FASEB J. 2004, 18:1740-1742.
32. Denissov S., van Driel M., Voit R., Hekkelman M., Hulsen T., Hernandez N., et al. Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J. 2007, 26:944-954.
33. Smeenk L., van Heeringen S.J., Koeppel M., van Driel M.A., Bartels S.J.J., Akkers R.C., et al. Characterization of genome-wide p53-binding sites upon stress response. Nucleic Acids Res. 2008, 36:3639-3654.
34. Smeenk L., van Heeringen S.J., Koeppel M., Gilbert B., Janssen-Megens E., Stunnenberg H.G., et al. Role of p53 serine 46 in p53 target gene regulation. PLoS One 2011, 6:e17574.
35. T method. Methods 2001, 25:402-408.
36. Uhl J., Klan N., Rose M., Entian K.-D., Werz O., Steinhilber D. The 5-lipoxygenase promoter is regulated by DNA methylation. J. Biol. Chem. 2002, 277:4374-4379.
37. Klan N., Seuter S., Schnur N., Jung M., Steinhilber D. Trichostatin A and structurally related histone deacetylase inhibitors induce 5-lipoxygenase promoter activity. Biol. Chem. 2003, 384:777-785.
38. Sambrook J., Russell D.W. Molecular Cloning - Sambrook & Russel - Vol. 1, 2, 3.pdf 2001.
39. Brázdová M., Quante T., Tögel L., Walter K., Loscher C., Tichý V., et al. Modulation of gene expression in U251 glioblastoma cells by binding of mutant p53 R273H to intronic and intergenic sequences. Nucleic Acids Res. 2009, 37:1486-1500.
40. Choong M.L., Yang H., Lee M.A., Lane D.P. Specific activation of the p53 pathway by low dose actinomycin D: a new route to p53 based cyclotherapy. Cell Cycle 2009, 8:2810-2818.
41. Karpinich N.O., Tafani M., Rothman R.J., Russo M.A., Farber J.L. The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. J. Biol. Chem. 2002, 277:16547-16552.
42. Menendez D., Inga A., Resnick M.A. The expanding universe of p53 targets. Nat. Rev. Cancer 2009, 9:724-737.
43. Cawley S., Bekiranov S., Ng H.H., Kapranov P., Sekinger E.A., Kampa D., et al. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004, 116:499-509.
44. Wei C.-L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
45. Funk C.D., Hoshiko S., Matsumoto T., Rdmark O., Samuelsson B. Characterization of the human 5-lipoxygenase gene. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:2587-2591.
46. Silverman E.S., Du J., De Sanctis G.T., Rådmark O., Samuelsson B., Drazen J.M., et al. Egr-1 and Sp1 interact functionally with the 5-lipoxygenase promoter and its naturally occurring mutants. Am. J. Respir. Cell Mol. Biol. 1998, 19:316-323.
47. In K.H., Silverman E.S., Asano K., Beier D., Fischer A.R., Keith T.P., et al. Mutations in the human 5-lipoxygenase gene. Clin. Rev. Allergy Immunol. 1999, 17:59-69.
48. Hoshiko S., Rådmark O., Samuelsson B. Characterization of the human 5-lipoxygenase gene promoter. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:9073-9077.
49. Schnur N., Seuter S., Katryniok C., Rådmark O., Steinhilber D. The histone deacetylase inhibitor trichostatin A mediates upregulation of 5-lipoxygenase promoter activity by recruitment of Sp1 to distinct GC-boxes. Biochim. Biophys. Acta 2007, 1771:1271-1282.
50. Melo C.A., Drost J., Wijchers P.J., van de Werken H., de Wit E., Oude Vrielink J.A.F., et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol. Cell 2013, 49:524-535.
51. Thukral S.K., Lu Y., Blain G.C., Harvey T.S., Jacobsen V.L. Discrimination of DNA binding sites by mutant p53 proteins. Mol. Cell. Biol. 1995, 15:5196-5202.
52. Bargonetti J., Manfredi J.J., Chen X., Marshak D.R., Prives C. A proteolytic fragment from the central region of p53 has marked sequence-specific DNA-binding activity when generated from wild-type but not from oncogenic mutant p53 protein. Genes Dev. 1993, 7:2565-2574.
53. Steinhilber D., Rådmark O., Samuelsson B. Transforming growth factor beta upregulates 5-lipoxygenase activity during myeloid cell maturation. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:5984-5988.
54. Seuter S., Väisänen S., Rådmark O., Carlberg C., Steinhilber D. Functional characterization of vitamin D responding regions in the human 5-lipoxygenase gene. Biochim. Biophys. Acta 2007, 1771:864-872.
55. Stoffers K.L., Sorg B.L., Seuter S., Rau O., Rådmark O., Steinhilber D. Calcitriol upregulates open chromatin and elongation markers at functional vitamin D response elements in the distal part of the 5-lipoxygenase gene. J. Mol. Biol. 2010, 395:884-896.
56. Avis I.M., Jett M., Boyle T., Vos M.D., Moody T., Treston a.M., et al. Growth control of lung cancer by interruption of 5-lipoxygenase-mediated growth factor signaling. J. Clin. Invest. 1996, 97:806-813.
57. Hong S.H., Avis I., Vos M.D., Martínez A., Treston A.M., Mulshine J.L. Relationship of arachidonic acid metabolizing enzyme expression in epithelial cancer cell lines to the growth effect of selective biochemical inhibitors. Cancer Res. 1999, 59:2223-2228.
58. Ghosh J., Myers C.E. Inhibition of arachidonate 5-lipoxygenase triggers massive apoptosis in human prostate cancer cells. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13182-13187.