Non-small cell lung cancer is susceptible to induction of DNA damage responses and inhibition of angiogenesis by telomere overhang oligonucleotides

Cancer Letters

Volumn 343, Issue 1, 2014, Pages 14-23

  Puri, Neelu ^a   Pitman, Ryan T ^a   Mulnix, Richard E ^a   Erickson, Terrianne ^a   Iness, Audra N ^a   Vitali, Connie ^a   Zhao, Yutong ^b   Salgia, Ravi ^c  

^a UNIVERSITY OF ILLINOIS   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Angiogenesis; Apoptosis; Lung cancer; P53; Senescence; Telomere overhang

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; OLIGONUCLEOTIDE; PROTEIN P21; PROTEIN P33; PROTEIN P53; PROTEIN P73; TELOMERE OLIGONUCLEOTIDE; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; BRONCHUS; CANCER INHIBITION; CARCINOGENICITY; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFICACY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; SIGNAL TRANSDUCTION; TUMOR VOLUME; TUMOR XENOGRAFT;

EID: 84890858679     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.09.010     Document Type: Article

References (65)

1. Salgia R., Hensing T., Campbell N., Salama A.K., Maitland M., Hoffman P., Villaflor V., Vokes E.E. Personalized treatment of lung cancer. Semin. Oncol. 2011, 38:274-283.
2. Campling B.G., el-Deiry W.S. Clinical implications of p53 mutations in lung cancer. Methods Mol. Med. 2003, 75:53-77.
3. Kim M.Y., Vankayalapati H., Shin-Ya K., Wierzba K., Hurley L.H. Telomestatin, a potent telomerase inhibitor that interacts quite specifically with the human telomeric intramolecular g-quadruplex. J. Am. Chem. Soc. 2002, 124:2098-2099.
4. Gowan S.M., Heald R., Stevens M.F., Kelland L.R. Potent inhibition of telomerase by small-molecule pentacyclic acridines capable of interacting with G-quadruplexes. Mol. Pharmacol. 2001, 60:981-988.
5. Gowan S.M., Harrison J.R., Patterson L., Valenti M., Read M.A., Neidle S., Kelland L.R. A G-quadruplex-interactive potent small-molecule inhibitor of telomerase exhibiting in vitro and in vivo antitumor activity. Mol. Pharmacol. 2002, 61:1154-1162.
6. Dikmen Z.G., Wright W.E., Shay J.W., Gryaznov S.M. Telomerase targeted oligonucleotide thio-phosphoramidates in T24-luc bladder cancer cells. J. Cell. Biochem. 2008, 104:444-452.
7. Ruden M., Puri N. Novel anticancer therapeutics targeting telomerase. Cancer Treat. Rev. 2013, 39:444-456.
8. Brower V. Telomerase-based therapies emerging slowly. J. Natl. Cancer Inst. 2010, 102:520-521.
9. Rankin A.M., Faller D.V., Spanjaard R.A. Telomerase inhibitors and 'T-oligo' as cancer therapeutics: contrasting molecular mechanisms of cytotoxicity. Anticancer Drugs 2008, 19:329-338.
10. Karlseder J., Broccoli D., Dai Y., Hardy S., de Lange T. P53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 1999, 283:1321-1325.
11. Eller M.S., Puri N., Hadshiew I.M., Venna S.S., Gilchrest B.A. Induction of apoptosis by telomere 3' overhang-specific DNA. Exp. Cell Res. 2002, 276:185-193.
12. Eller M.S., Maeda T., Magnoni C., Atwal D., Gilchrest B.A. Enhancement of DNA repair in human skin cells by thymidine dinucleotides: evidence for a p53-mediated mammalian SOS response. Proc. Natl. Acad. Sci. USA 1997, 94:12627-12632.
13. Li G.Z., Eller M.S., Hanna K., Gilchrest B.A. Signaling pathway requirements for induction of senescence by telomere homolog oligonucleotides. Exp. Cell Res. 2004, 301:189-200.
14. Puri N., Eller M.S., Byers H.R., Dykstra S., Kubera J., Gilchrest B.A. Telomere-based DNA damage responses: a new approach to melanoma. Faseb J. 2004, 18:1373-1381.
15. Eller M.S., Li G.Z., Firoozabadi R., Puri N., Gilchrest B.A. Induction of a p95/Nbs1-mediated S phase checkpoint by telomere 3' overhang specific DNA. Faseb J. 2003, 17:152-162.
16. Li G.Z., Eller M.S., Firoozabadi R., Gilchrest B.A. Evidence that exposure of the telomere 3' overhang sequence induces senescence. Proc. Natl. Acad. Sci. USA 2003, 100:527-531.
17. Rankin A.M., Sarkar S., Faller D.V. Mechanism of T-oligo-induced cell cycle arrest in Mia-PaCa pancreatic cancer cells. J. Cell. Physiol. 2012, 227:2586-2594.
18. Lee M.S., Yaar M., Eller M.S., Runger T.M., Gao Y., Gilchrest B.A. Telomeric DNA induces p53-dependent reactive oxygen species and protects against oxidative damage. J. Dermatol. Sci. 2009, 56:154-162.
19. Yaar M., Eller M.S., Panova I., Kubera J., Wee L.H., Cowan K.H., Gilchrest B.A. Telomeric DNA induces apoptosis and senescence of human breast carcinoma cells. Breast Cancer Res. 2007, 9:R13.
20. Sarkar S., Faller D.V. T-oligos inhibit growth and induce apoptosis in human ovarian cancer cells. Oligonucleotides 2011, 21:47-53.
21. Gnanasekar M., Thirugnanam S., Zheng G., Chen A., Ramaswamy K. T-oligo induces apoptosis in advanced prostate cancer cells. Oligonucleotides 2009, 19:287-292.
22. Aoki H., Iwado E., Eller M.S., Kondo Y., Fujiwara K., Li G.Z., Hess K.R., Siwak D.R., Sawaya R., Mills G.B., Gilchrest B.A., Kondo S. Telomere 3' overhang-specific DNA oligonucleotides induce autophagy in malignant glioma cells. Faseb J. 2007, 21:2918-2930.
23. Longe H.O., Romesser P.B., Rankin A.M., Faller D.V., Eller M.S., Gilchrest B.A., Denis G.V. Telomere homolog oligonucleotides induce apoptosis in malignant but not in normal lymphoid cells: mechanism and therapeutic potential. Int. J. Cancer 2009, 124:473-482.
24. Coleman C., Levine D., Kishore R., Qin G., Thorne T., Lambers E., Sasi S.P., Yaar M., Gilchrest B.A., Goukassian D.A. Inhibition of melanoma angiogenesis by telomere homolog oligonucleotides. J. Oncol. 2010, 2010:928628.
25. Jiang H., Reinhardt H.C., Bartkova J., Tommiska J., Blomqvist C., Nevanlinna H., Bartek J., Yaffe M.B., Hemann M.T. The combined status of ATM and p53 link tumor development with therapeutic response. Genes Dev. 2009, 23:1895-1909.
26. Oliver T.G., Meylan E., Chang G.P., Xue W., Burke J.R., Humpton T.J., Hubbard D., Bhutkar A., Jacks T. Caspase-2-mediated cleavage of Mdm2 creates a p53-induced positive feedback loop. Mol. Cell. 2010, 43:57-71.
27. Shao C., Lu C., Chen L., Koty P.P., Cobos E., Gao W. P53-Dependent anticancer effects of leptomycin B on lung adenocarcinoma. Cancer Chemother. Pharmacol. 2011, 67:1369-1380.
28. Ling Y.H., Liebes L., Jiang J.D., Holland J.F., Elliott P.J., Adams J., Muggia F.M., Perez-Soler R. Mechanisms of proteasome inhibitor PS-341-induced G(2)-M-phase arrest and apoptosis in human non-small cell lung cancer cell lines. Clin. Cancer Res. 2003, 9:1145-1154.
29. Dubrez L., Coll J.L., Hurbin A., de Fraipont F., Lantejoul S., Favrot M.C. Cell cycle arrest is sufficient for p53-mediated tumor regression. Gene Ther. 2001, 8:1705-1712.
30. Courtois S., Caron de Fromentel C., Hainaut P. P53 protein variants: structural and functional similarities with p63 and p73 isoforms. Oncogene 2004, 23:631-638.
31. Takahashi T., Carbone D., Nau M.M., Hida T., Linnoila I., Ueda R., Minna J.D. Wild-type but not mutant p53 suppresses the growth of human lung cancer cells bearing multiple genetic lesions. Cancer Res. 1992, 52:2340-2343.
32. Zhao Y., He D., Saatian B., Watkins T., Spannhake E.W., Pyne N.J., Natarajan V. Regulation of lysophosphatidic acid-induced epidermal growth factor receptor transactivation and interleukin-8 secretion in human bronchial epithelial cells by protein kinase Cdelta Lyn kinase, and matrix metalloproteinases. J. Biol. Chem. 2006, 281:19501-19511.
33. Puri N., Salgia R. Synergism of EGFR and c-Met pathways, cross-talk and inhibition, in non-small cell lung cancer. J. Carcinog. 2008, 7:9.
34. Itahana K., Campisi J., Dimri G.P. Methods to detect biomarkers of cellular senescence: the senescence-associated beta-galactosidase assay. Methods Mol. Biol. 2007, 371:21-31.
35. Pao W., Miller V.A., Politi K.A., Riely G.J., Somwar R., Zakowski M.F., Kris M.G., Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2005, 2:e73.
36. Su F., Kozak K.R., Imaizumi S., Gao F., Amneus M.W., Grijalva V., Ng C., Wagner A., Hough G., Farias-Eisner G., Anantharamaiah G.M., Van Lenten B.J., Navab M., Fogelman A.M., Reddy S.T., Farias-Eisner R. Apolipoprotein A-I (apoA-I) and apoA-I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc. Natl. Acad. Sci. USA 2010, 107:19997-20002.
37. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 1995, 92:9363-9367.
38. Kowalik T.F., DeGregori J., Leone G., Jakoi L., Nevins J.R. E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2. Cell Growth Differ. 1998, 9:113-118.
39. He G., Siddik Z.H., Huang Z., Wang R., Koomen J., Kobayashi R., Khokhar A.R., Kuang J. Induction of p21 by p53 following DNA damage inhibits both Cdk4 and Cdk2 activities. Oncogene 2005, 24:2929-2943.
40. Weng D., Cunin M.C., Song B., Price B.D., Eller M.S., Gilchrest B.A., Calderwood S.K., Gong J. Radiosensitization of mammary carcinoma cells by telomere homolog oligonucleotide pretreatment. Breast Cancer Res. 2010, 12:R71.
41. Chang B.D., Broude E.V., Dokmanovic M., Zhu H., Ruth A., Xuan Y., Kandel E.S., Lausch E., Christov K., Roninson I.B. A senescence-like phenotype distinguishes tumor cells that undergo terminal proliferation arrest after exposure to anticancer agents. Cancer Res. 1999, 59:3761-3767.
42. Garkavtsev I., Grigorian I.A., Ossovskaya V.S., Chernov M.V., Chumakov P.M., Gudkov A.V. The candidate tumour suppressor p33ING1 cooperates with p53 in cell growth control. Nature 1998, 391:295-298.
43. He G., Kuang J., Huang Z., Koomen J., Kobayashi R., Khokhar A.R., Siddik Z.H. Upregulation of p27 and its inhibition of CDK2/cyclin E activity following DNA damage by a novel platinum agent are dependent on the expression of p21. Br. J. Cancer 2006, 95:1514-1524.
44. Bamford S., Dawson E., Forbes S., Clements J., Pettett R., Dogan A., Flanagan A., Teague J., Futreal P.A., Stratton M.R., Wooster R. The COSMIC (Catalogue of Somatic Mutations in Cancer) database and website. Br. J. Cancer 2004, 91:355-358.
45. Wang D., Stockard C.R., Harkins L., Lott P., Salih C., Yuan K., Buchsbaum D., Hashim A., Zayzafoon M., Hardy R.W., Hameed O., Grizzle W., Siegal G.P. Immunohistochemistry in the evaluation of neovascularization in tumor xenografts. Biotechnol. Histochem. 2008, 83:179-189.
46. Lund E.L., Thorsen C., Pedersen M.W., Junker N., Kristjansen P.E. Relationship between vessel density and expression of vascular endothelial growth factor and basic fibroblast growth factor in small cell lung cancer in vivo and in vitro. Clin. Cancer Res. 2000, 6:4287-4291.
47. Lawler P.R., Lawler J. Molecular basis for the regulation of angiogenesis by thrombospondin-1 and -2. Cold Spring Harbor Perspect. Med. 2012, 2:a006627.
48. Sarkar S., Faller D.V. Telomere-homologous G-rich oligonucleotides sensitize human ovarian cancer cells to TRAIL-induced growth inhibition and apoptosis. Nucleic Acid Ther. 2013, 23:167-174.
49. Pitman R.T., Wojdyla L., Puri N. Mechanism of DNA damage responses induced by exposure to an oligonucleotide homologous to the telomere overhang in melanoma. Oncotarget 2013, 4:761-771.
50. Roninson I.B., Broude E.V., Chang B.D. If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist Updat 2001, 4:303-313.
51. Brown J.M., Wouters B.G. Apoptosis, p53, and tumor cell sensitivity to anticancer agents. Cancer Res. 1999, 59:1391-1399.
52. Fang L., Lee S.W., Aaronson S.A. Comparative analysis of p73 and p53 regulation and effector functions. J. Cell Biol. 1999, 147:823-830.
53. Polager S., Ginsberg D. P53 and E2f: partners in life and death. Nat. Rev. Cancer 2009, 9:738-748.
54. Melino G., Bernassola F., Ranalli M., Yee K., Zong W.X., Corazzari M., Knight R.A., Green D.R., Thompson C., Vousden K.H. P73 Induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J. Biol. Chem. 2004, 279:8076-8083.
55. Jung M.S., Yun J., Chae H.D., Kim J.M., Kim S.C., Choi T.S., Shin D.Y. P53 and its homologues, p63 and p73, induce a replicative senescence through inactivation of NF-Y transcription factor. Oncogene 2001, 20:5818-5825.
56. Qian Y., Chen X. Senescence regulation by the p53 protein family. Methods Mol. Biol. 2013, 965:37-61.
57. Chatelut E., Delord J.P., Canal P. Toxicity patterns of cytotoxic drugs. Invest. New Drugs 2003, 21:141-148.
58. Widakowich C., de Castro G., de Azambuja E., Dinh P., Awada A. Review: side effects of approved molecular targeted therapies in solid cancers. Oncologist 2007, 12:1443-1455.
59. Fujiwara T., Grimm E.A., Mukhopadhyay T., Zhang W.W., Owen-Schaub L.B., Roth J.A. Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene. Cancer Res. 1994, 54:2287-2291.
60. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 1996, 16:4604-4613.
61. Teodoro J.G., Evans S.K., Green M.R. Inhibition of tumor angiogenesis by p53: a new role for the guardian of the genome. J. Mol. Med. 2007, 85:1175-1186. (Berlin).
62. Ren B., Yee K.O., Lawler J., Khosravi-Far R. Regulation of tumor angiogenesis by thrombospondin-1. Biochim. Biophys. Acta 2006, 1765:178-188.
63. Salimath B., Marme D., Finkenzeller G. Expression of the vascular endothelial growth factor gene is inhibited by p73. Oncogene 2000, 19:3470-3476.
64. Vikhanskaya F., Bani M.R., Borsotti P., Ghilardi C., Ceruti R., Ghisleni G., Marabese M., Giavazzi R., Broggini M., Taraboletti G. P73 Overexpression increases VEGF and reduces thrombospondin-1 production: implications for tumor angiogenesis. Oncogene 2001, 20:7293-7300.
65. Ji W., Zhang W., Xiao W. E2F-1 directly regulates thrombospondin 1 expression. PLoS One 2010, 5:e13442.