Regulation of DNA damage following termination of hedgehog (HH) survival signaling at the level of the GLI genes in human colon cancer

Oncotarget

Volumn 3, Issue 8, 2012, Pages 851-865

  Agyeman, Akwasi ^a   Mazumdar, Tapati ^a   Houghton, Janet A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Colon cancer; DNA damage; GANT61; GLI1 GLI2 inhibition; Hedgehog

Indexed keywords

ATM PROTEIN; HISTONE H2AX; NIBRIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2;

ARTICLE; ATM GENE; CELL DEATH; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GAMMA H2AX GENE; GENE; GENE ACTIVATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCATION; GENE OVEREXPRESSION; GLI1 GENE; GLI2 GENE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MDC1 GENE; NBS1 GENE; TRANSCRIPTION REGULATION;

EID: 84868616969     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.586     Document Type: Article

References (72)

1. Katoh Y & Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med. 2009; 9: 873-886.
2. Yu M. Gipp J, Yoon JW, Iannaccone P, Walterhouse D, Bushman W. Sonic hedgehog-responsive genes in the fetal prostate. J Biol Chem. 2009; 284: 5620-5629.
3. Thiyagarajan S, Bhatia N, Reagan-Shaw S, Cozma D, Thomas-Tikhonenko A, Ahmad N, Spiegelman VS. Role of GLI2 transcription factor in growth and tumorigenicity of prostate cells. Cancer Res. 2007; 67: 10642-10646.
4. Ikram MS, Neill GW, Regl G, Eichberger T, Frischauf AM, Aberger F, Quinn A, Philpott M. GLI2 is expressed in normal human epidermis and BCC and induces GLI1 expression by binding to its promoter. J Invest Dermatol. 2004; 122: 1503-1509.
5. Bai CB, Auerbach W, Lee JS, Stephen D & Joyner AL. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development. 2002; 129: 4753-4761.
6. Eichberger T, Sander V, Schnidar H, Regl G, Kasper M, Schmid C, Plamberger S, Kaser A, Aberger F, Frischauf AM. Overlapping and distinct transcriptional regulator properties of the GLI1 and GLI2 oncogenes. Genomics. 2006; 87: 616-632.
7. Ruiz IAA, Mas C & Stecca B. The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol. 2007; 17: 438-447.
8. Mill P, Mo R, Fu H, Grachtchouk M, Kim PC, Dlugosz AA, Hui CC. Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev. 2003; 17: 282-294.
9. Stecca B, Mas C, Clement V, Zbinden M, Correa R, Piguet V, Beermann F, Ruiz I Altaba A. Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci U S A. 2007; 104: 5895-5900.
10. Sanchez P, Hernández AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, Beyna M, Datta MW, Datta S, Ruizi Altaba A. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci U S A. 2004; 101: 12561-12566.
11. Varnat,F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, Ruizi Altaba A. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med. 2009; 1: 338-351.
12. Ecke I, Rosenberger A, Obenauer S, Dullin C, Aberger F, Kimmina S, Schweyer S, Hahn H. Cyclopamine treatment of full-blown Hh/Ptch-associated RMS partially inhibits Hh/Ptch signaling, but not tumor growth. Mol Carcinog. 2008, 47: 361-372.
13. Sarangi A, Valadez JG, Rush S, Abel TW, Thompson RC, Cooper MK. Targeted inhibition of the Hedgehog pathway in established malignant glioma xenografts enhances survival. Oncogene. 2009; 28: 3468-3476.
14. Mas C & Ruiz IAA. Small molecule modulation of HH-GLI signaling: current leads, trials and tribulations. Biochem Pharmacol. 2010; 80: 712-723.
15. Robarge KD, Brunton SA, Castanedo GM, Cui Y, Dina MS, Goldsmith R, Gould SE, Guichert O, Gunzner JL, Halladay J, Jia W, Khojasteh C, Koehler MF, Kotkow K, La H, Lalonde RL, et al. GDC-0449-a potent inhibitor of the hedgehog pathway. Bioorg Med Chem Lett. 2009; 19: 5576-5581.
16. Low JA. & de Sauvage FJ. Clinical experience with Hedgehog pathway inhibitors. J Clin Oncol. 2010; 28: 5321-5326.
17. De SE, Ferretti E & Gulino A. Vismodegib, a small-molecule inhibitor of the hedgehog pathway for the treatment of advanced cancers. Curr Opin Investig Drugs. 2010; 11: 707-718.
18. Lorusso PM, Rudin CM, Reddy JC, Tibes R, Weiss GJ, Borad MJ, Hann CL, Brahmer JR, Chang I, Darbonne WC, Graham RA, Zerivitz KL, Low JA, Von Hoff DD. Phase I Trial of Hedgehog Pathway Inhibitor Vismodegib (GDC- 0449) in Patients with Refractory, Locally Advanced or Metastatic Solid Tumors. Clin Cancer Res. 2011; 17: 2502- 2511.
19. Von Hoff DD, LoRusso PM, Rudin CM, Reddy JC, Yauch RL, Tibes R, Weiss GJ, Borad MJ, Hann CL, Brahmer JR, Mackey HM, Lum BL, Darbonne WC, Marsters JC Jr, de Sauvage FJ, Low JA. Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N Engl J Med. 2009; 361: 1164-1172.
20. Dierks C. GDC-0449-targeting the hedgehog signaling pathway. Recent Results Cancer Res. 2010; 184: 235-238.
21. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, Holcomb T, Stinson J, Gould SE, Coleman B, LoRusso PM, Von Hoff DD, de Sauvage FJ, Low JA. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N Engl J Med. 2009; 361: 1173-1178.
22. Ji Z, Mei FC, Xie J & Cheng X. Oncogenic KRAS activates hedgehog signaling pathway in pancreatic cancer cells. J Biol Chem. 2007; 282: 14048-14055.
23. Yauch RL, Dijkgraaf GJ, Alicke B, Januario T, Ahn CP, Holcomb T, Pujara K, Stinson J, Callahan CA, Tang T, Bazan JF, Kan Z, Seshagiri S, Hann CL, Gould SE, Low JA, et al. Smoothened mutation confers resistance to a Hedgehog pathway inhibitor in medulloblastoma. Science. 2009; 326: 572-574.
24. Yoshikawa K, Shimada M, Miyamoto H, Higashijima J, Miyatani T, Nishioka M, Kurita M, Iwata T, Uehara H. Sonic hedgehog relates to colorectal carcinogenesis. J Gastroenterol. 2009; 44: 1113-1117.
25. Bian YH, Huang SH, Yang L, Ma XL, Xie JW, Zhang HW. Sonic hedgehog-Gli1 pathway in colorectal adenocarcinomas. World J Gastroenterol. 2007; 13: 1659- 1665.
26. Shi T, Mazumdar T, Devecchio J, Duan ZH, Agyeman A, Aziz M, Houghton. cDNA microarray gene expression profiling of hedgehog signaling pathway inhibition in human colon cancer cells. PLoS One. 2010; 5: e13054.
27. Mazumdar T, DeVecchio J, Shi T, Jones J, Agyeman A, Houghton JA. Hedgehog signaling drives cellular survival in human colon carcinoma cells. Cancer Res. 2011; 71: 1092-1102.
28. Frappart PO, Lee Y, Russell HR, Chalhoub N, Wang YD, Orii KE, Zhao J, Kondo N, Baker SJ, McKinnon PJ. Recurrent genomic alterations characterize medulloblastoma arising from DNA double-strand break repair deficiency. Proc Natl Acad Sci U S A. 2009; 106: 1880-1885.
29. Leonard JM, Ye H, Wetmore C & Karnitz LM. Sonic Hedgehog signaling impairs ionizing radiation-induced checkpoint activation and induces genomic instability. J Cell Biol. 2008; 183: 385-391.
30. Snijders AM, Huey B, Connelly ST, Roy R, Jordan RC, Schmidt BL, Albertson DG. Stromal control of oncogenic traits expressed in response to the overexpression of GLI2, a pleiotropic oncogene. Oncogene 2009; 28, 625-637.
31. Grady WM. Genomic instability and colon cancer. Cancer Metastasis Rev. 2004; 23: 11-27.
32. Mazumdar T, Devecchio J, Agyeman A, Shi T & Houghton JA. Blocking Hedgehog survival signaling at the level of the GLI genes induces DNA damage and extensive cell death in human colon carcinoma cells. Cancer Res. 2011; 71: 5904-5914.
33. Mazumdar T, DeVecchio J, Agyeman A, Shi T & Houghton JA. The GLI genes as the molecular switch in disrupting Hedgehog signaling in colon cancer. Oncotarget 2011; 2: 638-645.
34. Schnidar H, Eberl M, Klingler S, Mangelberger D, Kasper M, Hauser-Kronberger C, Regl G, Kroismayr R, Moriggl R, Sibilia M, Aberger F. Epidermal growth factor receptor signaling synergizes with Hedgehog/GLI in oncogenic transformation via activation of the MEK/ERK/JUN pathway. Cancer Res. 2009; 69: 1284-1292.
35. Yoon JW, Kita Y, Frank DJ, Majewski RR, Konicek BA, Nobrega MA, Jacob H, Walterhouse D, Iannaccone P. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem. 2002; 277: 5548-5555.
36. Marampon F, Bossi G, Ciccarelli C, Di Rocco A, Sacchi A, Pestell RG, Zani BM. MEK/ERK inhibitor U0126 affects in vitro and in vivo growth of embryonal rhabdomyosarcoma. Mol Cancer Ther. 2009; 8: 543-551.
37. Bedogni B, Welford SM, Kwan AC, Ranger-Moore J, Saboda K, Powell MB. Inhibition of phosphatidylinositol- 3-kinase and mitogen-activated protein kinase kinase 1/2 prevents melanoma development and promotes melanoma regression in the transgenic TPRas mouse model. Mol Cancer Ther. 2006; 5: 3071-3077.
38. Hinoue T, Weisenberger DJ, Pan F, Campan M, Kim M, Young J, Whitehall VL, Leggett BA, Laird PW. Analysis of the association between CIMP and BRAF in colorectal cancer by DNA methylation profiling. PLoS One. 2009; 4: e8357.
39. Lauth M, Bergstrom A, Shimokawa T & Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci U S A. 2007; 104: 8455-8460.
40. Ruiz IAA. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development. 1999; 126: 3205-3216.
41. Stucki M & Jackson SP. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst). 2006; 5: 534-543.
42. Deckbar D, Birraux J, Krempler A, Tchouandong L, Beucher A, Walker S, Stiff T, Jeggo P, Löbrich M. Chromosome breakage after G2 checkpoint release. J Cell Biol. 2007; 176: 749-755.
43. Lobrich M, Shibata A, Beucher A, Fisher A, Ensminger M, Goodarzi AA, Barton O, Jeggo PA. gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle. 2010; 9: 662-669.
44. Redon CE, Nakamura AJ, Martin OA, Parekh PR, Weyemi US, Bonner WM. Recent developments in the use of gamma-H2AX as a quantitative DNA double-strand break biomarker. Aging (Albany NY) 2011; 3: 168-174.
45. Nakamura AJ, Rao VA, Pommier Y & Bonner WM. The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle. 2010; 9: 389-397.
46. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell. 2005; 123: 1213-1226.
47. Chapman JR. & Jackson SP. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 2008; 9: 795-801.
48. Canman CE. Checkpoint mediators: relaying signals from DNA strand breaks. Curr Biol. 2003; 13: R488-490.
49. Nojima H. G1 and S-phase checkpoints, chromosome instability, and cancer. Methods Mol Biol. 2004; 280: 3-49.
50. Lim DS, Kim ST, Xu B, Maser RS, Lin J, Petrini JH, Kastan MB. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature. 2000; 404: 613-617.
51. Zhao S, Weng YC, Yuan SS, Lin YT, Hsu HC, Lin SC, Gerbino E, Song MH, Zdzienicka MZ, Gatti RA, Shay JW, Ziv Y, Shiloh Y, Lee EY. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature. 2000; 405: 473-477.
52. Bai Y. & Murnane, J.P. Telomere instability in a human tumor cell line expressing NBS1 with mutations at sites phosphorylated by ATM. Mol Cancer Res. 2003; 1: 1058- 1069.
53. Rossi R, Lidonnici MR., Soza S, Biamonti G & Montecucco A. The dispersal of replication proteins after Etoposide treatment requires the cooperation of Nbs1 with the ataxia telangiectasia Rad3-related/Chk1 pathway. Cancer Res. 2006; 66: 1675-1683.
54. Olson E, Nievera CJ, Liu E, Lee AY, Chen L, Wu X. The Mre11 complex mediates the S-phase checkpoint through an interaction with replication protein A. Mol Cell Biol. 2007; 27: 6053-6067.
55. Olson E, Nievera CJ, Lee AY, Chen L & Wu X. The Mre11- Rad50-Nbs1 complex acts both upstream and downstream of ataxia telangiectasia mutated and Rad3-related protein (ATR) to regulate the S-phase checkpoint following UV treatment. J Biol Chem. 2007; 282: 22939-22952.
56. Wu L, Luo K, Lou Z & Chen J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc Natl Acad Sci U S A. 2008; 105: 11200-11205.
57. Williams GJ, Lees-Miller SP & Tainer JA. Mre11-Rad50- Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair (Amst). 2010; 9: 1299-1306.
58. Neale MJ, Pan J & Keeney S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature. 2005; 436: 1053-1057.
59. Hopfner KP, Karcher A, Craig L, Woo TT, Carney JP, Tainer JA. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell. 2001; 105: 473-485.
60. Bartek J, Lukas C & Lukas J. Checking on DNA damage in S phase. Nat Rev Mol Cell Biol. 2004; 5: 792-804.
61. Machida YJ, Hamlin JL & Dutta A. Right place, right time, and only once: replication initiation in metazoans. Cell. 2005; 123: 13-24.
62. Petermann E. & Caldecott, K.W. Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle. 2006; 5: 2203-2209.
63. Branzei D & Foiani M. Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst). 2007; 6: 994-1003.
64. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 2003; 22: 5612-5621.
65. Stracker TH, Theunissen JW, Morales M & Petrini JH. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst). 2004; 3: 845-854.
66. Paull TT & Lee JH. The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle. 2005; 4: 737-740.
67. Lee JH. & Paull TT. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science. 2005; 308: 551-554.
68. Melander F, Bekker-Jensen S, Falck J, Bartek J, Mailand N, Lukas J. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J Cell Biol. 2008; 181: 213-226.
69. Spycher C, Miller ES, Townsend K, Pavic L, Morrice NA, Janscak P, Stewart GS, Stucki M. Constitutive phosphorylation of MDC1 physically links the MRE11- RAD50-NBS1 complex to damaged chromatin. J Cell Biol. 2008; 181: 227-240.
70. Dodson GE, Limbo O, Nieto D & Russell P. Phosphorylation-regulated binding of Ctp1 to Nbs1 is critical for repair of DNA double-strand breaks. Cell Cycle. 2010; 9: 1516-1522.
71. Tillman DM, Izeradjene K, Szucs KS, Douglas L. & Houghton JA. Rottlerin sensitizes colon carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis via uncoupling of the mitochondria independent of protein kinase C. Cancer Res. 2003; 63: 5118-5125.
72. Drouet J, Delteil C, Lefrançois J, Concannon P, Salles B, Calsou P. DNA-dependent protein kinase and XRCC4- DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J Biol Chem. 2005; 280: 7060-7069