Targeting MYC Expression through G-Quadruplexes

Genes and Cancer

Volumn 1, Issue 6, 2010, Pages 641-649

  Brooks, Tracy A ^a   Hurley, Laurence H ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

G quadruplex; MYC; supercoiling; transcriptional control

Indexed keywords

EID: 79952763614     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601910377493     Document Type: Article

References (89)

1. Morange M. What history tells us IX. Z-DNA: when nature is not opportunistic. J Biosci 2007;32:657-61.
2. Rich A, Zhang S. Timeline: Z-DNA. The long road to biological function. Nat Rev Genet 2003;4:566-72.
3. Gellert M, Lipsett MN, Davies DR. Helix formation by guanylic acid. Proc Natl Acad Sci U S A 1962;48:2013-8.
4. Sen D, Gilbert W. Formation of parallel fourstranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature 1988;334:364-6.
5. Schaffitzel C, Berger I, Postberg J, Hanes J, Lipps HJ, Plückthun A. In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei. Proc Natl Acad Sci U S A 2001;98:8572-7.
6. Sun D, Thompson B, Cathers BE, et al. Inhibition of human telomerase by a G-quadruplex-interactive compound. J Med Chem 1997;40:2113-6.
7. Hurley LH. DNA and associated targets for drug design. J Med Chem 1989;32:2027-33.
8. Simonsson T, Pecinka P, Kubista M. DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res 1998;26:1167-72.
9. Michelotti EF, Michelotti GA, Aronsohn AI, Levens D. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol Cell Biol 1996;16:2350-60.
10. Michelotti EF, Tomonaga T, Krutzsch H, Levens D. Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene. J Biol Chem 1995;270:9494-9.
11. Tomonaga T, Levens D. Heterogeneous nuclear ribonucleoprotein K is a DNA-binding transactivator. J Biol Chem 1995;270:4875-81.
12. Michelotti GA, Michelotti EF, Pullner A, Duncan RC, Eick D, Levens D. Multiple single-stranded cis elements are associated with activated chromatin of the human c-myc gene in vivo. Mol Cell Biol 1996;16:2656-69.
13. Grand CL, Han H, Muñoz RM, et al. The cationic porphyrin TMPyP4 down-regulates c-MYC and human telomerase reverse transcriptase expression and inhibits tumor growth in vivo. Mol Cancer Ther 2002;1:565-73.
14. Siddiqui-Jain A, Grand CL, Bearss DJ, Hurley LH. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc Natl Acad Sci U S A 2002;99:11593-8.
15. Brooks TA, Hurley LH. The role of supercoiling in transcriptional control of MYC and its importance in molecular therapeutics. Nat Rev Cancer 2009;9:849-61.
16. Kouzine F, Sanford S, Elisha-Feil Z, Levens D. The functional response of upstream DNA to dynamic supercoiling in vivo. Nat Struct Mol Biol 2008;15:146-54.
17. Kouzine F, Liu J, Sanford S, Chung HJ, Levens D. The dynamic response of upstream DNA to transcription-generated torsional stress. Nat Struct Mol Biol 2004;11:1092-100.
18. Sun D, Hurley LH. The importance of negative superhelicity in inducing the formation of G-quadruplex and i-motif structures in the c-Myc promoter: implications for drug targeting and control of gene expression. J Med Chem 2009;52:2863-74.
19. Seenisamy J, Rezler EM, Powell TJ, et al. The dynamic character of the G-quadruplex element in the c-MYC promoter and modification by TMPyP4. J Am Chem Soc 2004;126:8702-9.
20. Phan AT, Modi YS, Patel DJ. Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J Am Chem Soc 2004;126: 8710-6.
21. Simonsson T, Pribylova M, Vorlickova M. A nuclease hypersensitive element in the human c-myc promoter adopts several distinct i-tetraplex structures. Biochem Biophys Res Commun 2000;278:158-66.
22. Ginisty H, Sicard H, Roger B, Bouvet P. Structure and functions of nucleolin. J Cell Sci 1999;112:761-72.
23. Grinstein E, Du Y, Santourlidis S, Christ J, Uhrberg M, Wernet P. Nucleolin regulates gene expression in CD34-positive hematopoietic cells. J Biol Chem 2007;282:12439-49.
24. Grinstein E, Wernet P, Snijders PJ, et al. Nucleolin as activator of human papillomavirus type 18 oncogene transcription in cervical cancer. J Exp Med 2002;196:1067-78.
25. Mongelard F, Bouvet P. Nucleolin: a multiFACeTed protein. Trends Cell Biol 2007;17:80-6.
26. Storck S, Shukla M, Dimitrov S, Bouvet P. Functions of the histone chaperone nucleolin in diseases. Subcell Biochem 2007;41:125-44.
27. Bugler B, Caizergues-Ferrer M, Bouche G, Bourbon H, Amalric F. Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein. Eur J Biochem 1982;128:475-80.
28. Ghisolfi L, Joseph G, Amalric F, Erard M. The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J Biol Chem 1992;267:2955-9.
29. Bates PJ, Kahlon JB, Thomas SD, Trent JO, Miller DM. Antiproliferative activity of G-rich oligonucleotides correlates with protein binding. J Biol Chem 1999;274:26369-77.
30. Dempsey LA, Sun H, Hanakahi LA, Maizels N. G4 DNA binding by LR1 and its subunits, nucleolin and hnRNP D: a role for G-G pairing in immunoglobulin switch recombination. J Biol Chem 1999;274:1066-71.
31. Hanakahi LA, Sun H, Maizels N. High affinity interactions of nucleolin with G-G-paired rDNA. J Biol Chem 1999;274:15908-12.
32. González V, Guo K, Hurley L, Sun D. Identification and characterization of nucleolin as a c-myc G-quadruplex-binding protein. J Biol Chem 2009;284:23622-35.
33. Lacombe ML, Milon L, Munier A, Mehus JG, Lambeth DO. The human Nm23/nucleoside diphosphate kinases. J Bioenerg Biomembr 2000;32:247-58.
34. Lascu I, Gonin P. The catalytic mechanism of nucleoside diphosphate kinases. J Bioenerg Biomembr 2000;32:237-46.
35. Steeg PS, Bevilacqua G, Kopper L, et al. Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 1988;80:200-4.
36. Janin J, Dumas C, Moréra S, et al. Threedimensional structure of nucleoside diphosphate kinase. J Bioenerg Biomembr 2000;32:215-25.
37. Postel EH, Berberich SJ, Flint SJ, Ferrone CA. Human c-myc transcription factor PuF identified as nm23-H2 nucleoside diphosphate kinase, a candidate suppressor of tumor metastasis. Science 1993;261:478-80.
38. Berberich SJ, Postel EH. PuF/NM23-H2/NDPKB transactivates a human c-myc promoter-CAT gene via a functional nuclease hypersensitive element. Oncogene 1995;10:2343-7.
39. Bevilacqua G. NM23 gene expression and human breast cancer metastases. Pathol Biol (Paris) 1990;38:774-5.
40. 1. Mol Cancer Ther 2009;8:1363-77.
41. Thakur RK, Kumar P, Halder K, et al. Metastases suppressor NM23-H2 interaction with G-quadruplex DNA within c-MYC promoter nuclease hypersensitive element induces c-MYC. Nucleic Acids Res 2009;37:172-83.
42. Marcu KB, Bossone SA, Patel AJ. myc function and regulation. Annu Rev Biochem 1992;61:809-60.
43. Spencer CA, Groudine M. Control of c-myc regulation in normal and neoplastic cells. Adv Cancer Res 1991;56:1-48.
44. D’Cruz CM, Gunther EJ, Boxer RB, et al. c-MYC induces mammary tumorigenesis by means of a preferred pathway involving spontaneous Kras2 mutations. Nat Med 2001;7:235-9.
45. Lutz W, Leon J, Eilers M. Contributions of Myc to tumorigenesis. Biochim Biophys Acta 2002;1602:61-71.
46. Pelengaris S, Khan M, Evan G. c-MYC: more than just a matter of life and death. Nat Rev Cancer 2002;2:764-76.
47. Pelengaris S, Khan M, Evan GI. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 2002;109:321-34.
48. Cory S, Gerondakis S, Corcoran LM, Bernard O, Webb E, Adams JM. Activation of the c-myc oncogene in B and T lymphoid tumors. Curr Top Microbiol Immunol 1984;113:161-5.
49. Dalla-Favera R, Bregni M, Erikson J, Patterson D, Gallo RC, Croce CM. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A 1982;79:7824-7.
50. Stasik CJ, Nitta H, Zhang W, et al. Increased MYC gene copy number correlates with increased mRNA levels in diffuse large B-cell lymphoma. Haematologica 2010;95:597-603.
51. Dang CV, Lee LA. c-Myc function in neoplasia. Austin, TX: RG Landes Co; 1995.
52. Eilers M, Eisenman RN. Myc’s broad reach. Genes Dev 2008;22:2755-66.
53. Meyer N, Penn LZ. Reflecting on 25 years with MYC. Nat Rev Cancer 2008;8:976-90.
54. Wierstra I, Alves J. The c-myc promoter: still MysterY and Challenge. Adv Cancer Res 2008;99:113-333.
55. Musgrove EA, Sergio CM, Loi S, et al. Identification of functional networks of estrogen-and c-Myc-responsive genes and their relationship to response to tamoxifen therapy in breast cancer. PLoS ONE 2008;3:e2987.
56. Arango D, Corner GA, Wadler S, Catalano PJ,Augenlicht LH. c-myc/p53 interaction determines sensitivity of human colon carcinoma cells to 5-fluorouracil in vitro and in vivo. Cancer Res 2001;61:4910-5.
57. Weinstein IB, Joe A. Oncogene addiction. Cancer Res 2008;68:3077-80.
58. Shachaf CM, Gentles AJ, Elchuri S, et al. Genomic and proteomic analysis reveals a threshold level of MYC required for tumor maintenance. Cancer Res 2008;68:5132-42.
59. Soucek L, Whitfield J, Martins CP, et al. Modelling Myc inhibition as a cancer therapy. Nature 2008;455:679-83.
60. Soldatenkov VA, Vetcher AA, Duka T, Ladame S. First evidence of a functional interaction between DNA quadruplexes and poly(ADP-ribose) polymerase-1. ACS Chem Biol 2008;3:214-9.
61. Ou TM, Lu YJ, Zhang C, et al. Stabilization of G-quadruplex DNA and down-regulation of oncogene c-myc by quindoline derivatives. J Med Chem 2007;50:1465-74.
62. Kang HJ, Park HJ. Novel molecular mechanism for actinomycin D activity as an oncogenic promoter G-quadruplex binder. Biochemistry 2009;48:7392-8.
63. Duan W, Rangan A, Vankayalapati H, et al. Design and synthesis of fluoroquinophenoxazines that interact with human telomeric G-quadruplexes and their biological effects. Mol Cancer Ther 2001;1:103-20.
64. Drygin D, Siddiqui-Jain A, O’Brien S, et al. Anticancer activity of CX-3543: a direct inhibitor of rRNA biogenesis. Cancer Res 2009;69:7653-61.
65. Daniely Y, Borowiec JA. Formation of a complex between nucleolin and replication protein A after cell stress prevents initiation of DNA replication. J Cell Biol 2000;149:799-810.
66. Wang Y, Guan J, Wang H, Wang Y, Leeper D, Iliakis G. Regulation of DNA replication after heat shock by replication protein A-nucleolin interactions. J Biol Chem 2001;276:20579-88.
67. Daniely Y, Dimitrova DD, Borowiec JA. Stressdependent nucleolin mobilization mediated by p53-nucleolin complex formation. Mol Cell Biol 2002;22:6014-22.
68. Jin CH, Rice WG, Siddiqui-Jain A, et al. In vivo efficacy of CX-3543: a novel c-Myc oncogene inhibitor [abstract LB-243]. 95th Annual Meeting Proceedings; 2004 Mar 27-31; Orlando, FL; 2004. p. 110.
69. Huppert JL, Balasubramanian S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res 2005;33:2908-16.
70. Huppert JL, Balasubramanian S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res 2007;35:406-13.
71. Verma A, Halder K, Halder R, et al. Genomewide computational and expression analyses reveal G-quadruplex DNA motifs as conserved cis-regulatory elements in human and related species. J Med Chem 2008;51:5641-9.
72. Dexheimer TS, Sun D, Hurley LH. Deconvoluting the structural and drug-recognition complexity of the G-quadruplex-forming region upstream of the bcl-2 P1 promoter. J Am Chem Soc 2006;128:5404-15.
73. Guo K, Gokhale V, Hurley LH, Sun D. Intramolecularly folded G-quadruplex and i-motif structures in the proximal promoter of the vascular endothelial growth factor gene. Nucleic Acids Res 2008;36:4598-608.
74. Sun D, Guo K, Rusche JJ, Hurley LH. Facilitation of a structural transition in the polypurine/ polypyrimidine tract within the proximal promoter region of the human VEGF gene by the presence of potassium and G-quadruplex-interactive agents. Nucleic Acids Res 2005;33:6070-80.
75. De Armond R, Wood S, Sun D, Hurley LH, Ebbinghaus SW. Evidence for the presence of a guanine quadruplex forming region within a polypurine tract of the hypoxia inducible factor 1α promoter. Biochemistry 2005;44:16341-50.
76. Qin Y, Rezler EM, Gokhale V, Sun D, Hurley LH. Characterization of the G-quadruplexes in the duplex nuclease hypersensitive element of the PDGF-A promoter and modulation of PDGFA promoter activity by TMPyP4. Nucleic Acids Res 2007;35:7698-713.
77. Qin Y, Fortin JS, Tye D, Gleason-Guzman M, Brooks TA, Hurley LH. Molecular cloning of the human platelet-derived growth factor receptor β (PDGFR-β) promoter and drug targeting of the G-quadruplex-forming region to repress PDGFR-β expression. Biochemistry 2010;49:4208-19.
78. Palumbo SL, Memmott RM, Uribe DJ, Krotova-Khan Y, Hurley LH, Ebbinghaus SW. A novel G-quadruplex-forming GGA repeat region in the c-myb promoter is a critical regulator of promoter activity. Nucleic Acids Res 2008;36:1755-69.
79. Palumbo SL, Ebbinghaus SW, Hurley LH. Formation of a unique end-to-end stacked pair of G-quadruplexes in the hTERT core promoter with implications for inhibition of telomerase by G-quadruplex-interactive ligands. J Am Chem Soc 2009;131:10878-91.
80. Bejugam M, Sewitz S, Shirude PS, Rodriguez R, Shahid R, Balasubramanian S. Trisubstituted isoalloxazines as a new class of G-quadruplex binding ligands: small molecule regulation of c-kit oncogene expression. J Am Chem Soc 2007;129:12926-7.
81. Hsu ST, Varnai P, Bugaut A, Reszka AP, Neidle S, Balasubramanian S. A G-rich sequence within the c-kit oncogene promoter forms a parallel G-quadruplex having asymmetric G-tetrad dynamics. J Am Chem Soc 2009;131:13399-409.
82. Phan AT, Kuryavyi V, Burge S, Neidle S, Patel DJ. Structure of an unprecedented G-quadruplex scaffold in the human c-kit promoter. J Am Chem Soc 2007;129:4386-92.
83. Cogoi S, Xodo LE. G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription. Nucleic Acids Res 2006;34:2536-49.
84. Xu Y, Sugiyama H. Formation of the G-quadruplex and i-motif structures in retinoblastoma susceptibility genes (Rb). Nucleic Acids Res 2006;34:949-54.
85. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
86. Brooks TA, Kendrick S, Dexheimer TS, Hurley LH. Diversity of G-quadruplexes in promoter regions and their biological consquences. FEBS J 2009. In press.
87. 1: function and regulation. Annu Rev Pharmacol Toxicol 2010;50:111-29.
88. Levens D. You don’t muck with MYC. Genes & Cancer 2010;1:547-54.
89. Kendrick S, Hurley LH. The role of G-quadruplex/ i-motif secondary structures as cis-acting regulatory elements. Pure Appl Chem 2010;82:1609-21.