Oxidative stress-regulated lentiviral TK/GCV gene therapy for lung cancer treatment

Cancer Research

Volumn 72, Issue 23, 2012, Pages 6227-6235

  Leinonen, Hanna M ^a   Ruotsalainen, Anna Kaisa ^a   Määttä, Ann Marie ^c   Laitinen, Heidi M ^a   Kuosmanen, Suvi M ^a   Kansanen, Emilia ^a   Pikkarainen, Jere T ^a,c   Lappalainen, Jari P ^a   Samaranayake, Haritha ^a,c   Lesch, Hanna P ^c   Kaikkonen, Minna U ^a,c   Ylä Herttuala, Seppo ^a,b   Levonen, Anna Liisa ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

^c Finland Ark Therapeutics Oy   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

DIETHYLMALEATE; DOXORUBICIN; GANCICLOVIR; LENTIVIRUS VECTOR; MALEIC ACID; PHOSPHOGLYCERATE KINASE; THYMIDINE KINASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DRUG POTENTIATION; GENE EXPRESSION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; LUNG CANCER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; SUICIDE GENE THERAPY;

ADENOCARCINOMA; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; CELL LINE, TUMOR; GANCICLOVIR; GENETIC THERAPY; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LENTIVIRUS; LUNG NEOPLASMS; MALE; MICE; MICE, NUDE; MUTATION; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; THYMIDINE KINASE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84870316076     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1166     Document Type: Article

References (49)

1. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44-84. (Pubitemid 44566469)
2. Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 2010;38:96-109.
3. Akhdar H, Loyer P, Rauch C, Corlu A, Guillouzo A, Morel F. Involvement of Nrf2 activation in resistance to 5-fluorouracil in human colon cancer HT-29 cells. Eur J Cancer 2009;45:2219-27.
4. Brown DP, Chin-Sinex H, Nie B, Mendonca MS, Wang M. Targeting superoxide dismutase 1 to overcome cisplatin resistance in human ovarian cancer. Cancer Chemother Pharmacol 2009;63:723-30.
5. Young LC, Campling BG, Cole SP, Deeley RG, Gerlach JH. Multidrug resistance proteins MRP3, MRP1, and MRP2 in lung cancer: correlation of protein levels with drug response and messenger RNA levels. Clin Cancer Res 2001;7:1798-804. (Pubitemid 32708651)
6. Soini Y, Napankangas U, Jarvinen K, Kaarteenaho-Wiik R, Paakko P, Kinnula VL. Expression of gamma-glutamyl cysteine synthetase in nonsmall cell lung carcinoma. Cancer 2001;92:2911-9.
7. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007;47:89-116.
8. Motohashi H, O'Connor T, Katsuoka F, Engel JD, Yamamoto M. Integration and diversity of the regulatory network composed of maf and CNC families of transcription factors. Gene 2002;294:1-12. (Pubitemid 35291008)
9. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 2003;278:12029-38. (Pubitemid 36800179)
10. Hayashi A, Suzuki H, Itoh K, Yamamoto M, Sugiyama Y. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem Biophys Res Commun 2003;310:824-9. (Pubitemid 37188696)
11. Vollrath V, Wielandt AM, Iruretagoyena M, Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 2006;395:599-609.
12. Giudice A, Montella M. Activation of the Nrf2-ARE signaling pathway: a promising strategy in cancer prevention. Bioessays 2006;28:169-81.
13. Kensler TW, Wakabayashi N. Nrf2: friend or foe for chemoprevention? Carcinogenesis 2010;31:90-9.
14. Slocum SL, Kensler TW. Nrf2: control of sensitivity to carcinogens. Arch Toxicol 2011;85:273-84.
15. Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD. Dual roles of Nrf2 in cancer. Pharmacol Res 2008;58:262-70.
16. Homma S, Ishii Y, Morishima Y, Yamadori T, Matsuno Y, Haraguchi N, et al. Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer. Clin Cancer Res 2009;15:3423-32.
17. Ohta T, Iijima K, Miyamoto M, Nakahara I, Tanaka H, Ohtsuji M, et al. Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res 2008;68:1303-9. (Pubitemid 351346836)
18. Singh A, Misra V, Thimmulappa RK, Lee H, Ames S, Hoque MO, et al. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med 2006;3:e420.
19. Singh A, Boldin-Adamsky S, Thimmulappa RK, Rath SK, Ashush H, Coulter J, et al. RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy. Cancer Res 2008;68:7975-84.
20. Moolten FL. Tumor chemosensitivity conferred by inserted herpes thymidine kinase genes: paradigm for a prospective cancer control strategy. Cancer Res 1986;46:5276-81. (Pubitemid 16008301)
21. Shibata T, Giaccia AJ, Brown JM. Hypoxia-inducible regulation of a prodrug-activating enzyme for tumor-specific gene therapy. Neoplasia 2002;4:40-8. (Pubitemid 34075889)
22. Greco O, Joiner MC, Doleh A, Powell AD, Hillman GG, Scott SD. Hypoxia- and radiation-activated Cre/loxP 'molecular switch' vectors for gene therapy of cancer. Gene Ther 2006;13:206-15. (Pubitemid 43148643)
23. Policastro LL, Ibanez IL, Duran HA, Soria G, Gottifredi V, Podhajcer OL. Suppression of cancer growth by nonviral gene therapy based on a novel reactive oxygen species-responsive promoter. Mol Ther 2009;17:1355-64.
24. Shibata T, Ohta T, Tong KI, Kokubu A, Odogawa R, Tsuta K, et al. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc Natl Acad Sci U S A 2008;105:13568-73.
25. Hurttila H, Koponen JK, Kansanen E, Jyrkkänen HK, Kivelä A, Kylätie R, et al. Oxidative stress-inducible lentiviral vectors for gene therapy. Gene Ther 2008;15:1271-9.
26. Loimas S, Wahlfors J, Janne J. Herpes simplex virus thymidine kinase-green fluorescent protein fusion gene: new tool for gene transfer studies and gene therapy. Biotechniques 1998;24:614-8. (Pubitemid 28227468)
27. Mäkinen PI, Koponen JK, Kärkkäinen AM, Malm TM, Pulkkinen KH, Koistinaho J, et al. Stable RNA interference: comparison of U6 and H1 promoters in endothelial cells and in mouse brain. J Gene Med 2006;8:433-41.
28. Koponen JK, Kekarainen T, E Heinonen S, Laitinen A, Nystedt J, Laine J, et al. Umbilical cord blood-derived progenitor cells enhance muscle regeneration in mouse hindlimb ischemia model. Mol Ther 2007;15:2172-7. (Pubitemid 350148934)
29. Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011;16:123-40.
30. Wang R, An J, Ji F, Jiao H, Sun H, Zhou D. Hypermethylation of the Keap1 gene in human lung cancer cell lines and lung cancer tissues. Biochem Biophys Res Commun 2008;373:151-4.
31. Muscarella LA, Parrella P, D'Alessandro V, la Torre A, Barbano R, Fontana A, et al. Frequent epigenetics inactivation of KEAP1 gene in non-small cell lung cancer. Epigenetics 2011;6:710-9.
32. Kweon MH, Adhami VM, Lee JS, Mukhtar H. Constitutive overexpression of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J Biol Chem 2006;281:33761-72. (Pubitemid 46036754)
33. Hasegawa Y, Emi N, Shimokata K, Abe A, Kawabe T, Hasegawa T, et al. Gene transfer of herpes simplex virus type I thymidine kinase gene as a drug sensitivity gene into human lung cancer cell lines using retroviral vectors. Am J Respir Cell Mol Biol 1993;8:655-61.
34. Määttä AM, Tenhunen A, Pasanen T, Meriläinen O, Pellinen R, Mäkinen K, et al. Non-small cell lung cancer as a target disease for herpes simplex type 1 thymidine kinase-ganciclovir gene therapy. Int J Oncol 2004;24:943-9.
35. Gewirtz DA. Acritical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 1999;57:727-41. (Pubitemid 29094544)
36. Hayes JD, McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 2009;34:176-88.
37. Shibata T, Kokubu A, Gotoh M, Ojima H, Ohta T, Yamamoto M, et al. Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology 2008;135:1358-68.
38. Lister A, Nedjadi T, Kitteringham NR, Campbell F, Costello E, Lloyd B, et al. Nrf2 is overexpressed in pancreatic cancer: implications for cell proliferation and therapy. Mol Cancer 2011;10:37.
39. Inami Y, Waguri S, Sakamoto A, Kouno T, Nakada K, Hino O, et al. Persistent activation of Nrf2 through p62 in hepatocellular carcinoma cells. J Cell Biol 2011;193:275-84.
40. Konstantinopoulos PA, Spentzos D, Fountzilas E, Francoeur N, Sanisetty S, Grammatikos AP, et al. Keap1 mutations and Nrf2 pathway activation in epithelial ovarian cancer. Cancer Res 2011;71:5081-9.
41. Zhang R, Chen HZ, Liu JJ, Jia YY, Zhang ZQ, Yang RF, et al. SIRT1 suppresses activator protein-1 transcriptional activity and cyclooxygenase- 2 expression in macrophages. J Biol Chem 2010;285:7097-110.
42. Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008;29:1235-43. (Pubitemid 351958704)
43. Yamadori T, Ishii Y, Homma S, Morishima Y, Kurishima K, Itoh K, et al. Molecular mechanisms for the regulation of Nrf2-mediated cell proliferation in non-small-cell lung cancers. Oncogene. 2012 Jan 16. [Epub ahead of print].
44. Koshikawa N, Takenaga K, Tagawa M, Sakiyama S. Therapeutic efficacy of the suicide gene driven by the promoter of vascular endothelial growth factor gene against hypoxic tumor cells. Cancer Res 2000;60:2936-41. (Pubitemid 30395818)
45. Määttä AM, Korja S, Venhoranta H, Hakkarainen T, Pirinen E, Heikkinen S, et al. Transcriptional targeting of virus-mediated gene transfer by the human hexokinase II promoter. Int J Mol Med 2006;18:901-8.
46. Wang XJ, Hayes JD, Wolf CR. Generation of a stable antioxidant response element-driven reporter gene cell line and its use to show redox-dependent activation of nrf2 by cancer chemotherapeutic agents. Cancer Res 2006;66:10983-94. (Pubitemid 44876998)
47. McDonald JT, Kim K, Norris AJ, Vlashi E, Phillips TM, Lagadec C, et al. Ionizing radiation activates the Nrf2 antioxidant response. Cancer Res 2010;70:8886-95.
48. Bhutia SK, Mallick SK, Maiti TK. Tumour escape mechanisms and their therapeutic implications in combination tumour therapy. Cell Biol Int 2010;34:553-63.
49. Cao S, Cripps A, Wei MQ. New strategies for cancer gene therapy: progress and opportunities. Clin Exp Pharmacol Physiol 2010;37: 108-14.