Induction of oxidants distinguishes susceptibility of prostate carcinoma cell lines to p53 gene transfer mediated by an improved adenoviral vector

Human Gene Therapy

Volumn 28, Issue 8, 2017, Pages 639-653

  Tamura, Rodrigo Esaki ^a   Hunger, Aline ^a   Fernandes, Denise C ^b   Laurindo, Francisco R ^b   Costanzi Strauss, Eugenia ^b   Strauss, Bryan E ^a  

^a Anesthesia Department Cancer Institute of the State of Sao Paulo   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

adenovirus; NOX1; oxidants ROS; p53; prostate carcinoma

Indexed keywords

ADENOVIRUS VECTOR; CATALASE; HISTONE H2AX; MESSENGER RNA; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; OXIDIZING AGENT;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DEATH; CELL KILLING; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; FLUORESCENCE; GENE; GENE EXPRESSION; GENE TRANSFER; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LONG TERM SURVIVAL; MALE; MEDIAN SURVIVAL TIME; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MTT ASSAY; NONHUMAN; PIG3 GENE; POLYMERASE CHAIN REACTION; PROSTATE CARCINOMA; QUANTITATIVE ANALYSIS; SESTRIN2 GENE; TUMOR GROWTH; VIRAL GENE DELIVERY SYSTEM; ADENOVIRIDAE; ADMINISTRATION AND DOSAGE; ANIMAL; DISEASE MODEL; DRUG SCREENING; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; METABOLISM; MITOCHONDRION; PATHOLOGY; PROSTATE TUMOR; REPORTER GENE; TUMOR CELL CULTURE; TUMOR CELL LINE;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DNA DAMAGE; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENES, REPORTER; GENETIC THERAPY; GENETIC VECTORS; HUMANS; MALE; MICE; MITOCHONDRIA; OXIDANTS; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85020598437     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2016.139     Document Type: Article

References (56)

1. Siegel R, Ma J, Zou Z, et al. Cancer statistics, 2014. CA Cancer J Clin 2014; 64: 9-29.
2. Chen J. The cell-cycle arrest and apoptotic functions of p53 in tumor initiation and progression. Cold Spring Harb Perspect Med 2016; 6: a026104.
3. Lane DP. Cancer. p53, guardian of the genome. Nature 1992; 358: 15+16.
4. Shi J, Zheng D. An update on gene therapy in China. Curr Opin Mol Ther 2009; 11: 547-553.
5. Ma G, Shimada H, Hiroshima K, et al. Gene medicine for cancer treatment: commercially available medicine and accumulated clinical data in China. Drug Des Devel Ther 2009; 2: 115-122.
6. Ko SC, Gotoh A, Thalmann GN, et al. Molecular therapy with recombinant p53 adenovirus in an androgen-independent, metastatic human prostate cancer model. Hum Gene Ther 1996; 7: 1683-1691.
7. Asgari K, Sesterhenn IA, McLeod DG, et al. Inhibition of the growth of pre-established subcutaneous tumor nodules of human prostate cancer cells by single injection of the recombinant adenovirus p53 expression vector. Int J Cancer 1997; 71: 377-382.
8. Sasaki R, Shirakawa T, Zhang ZJ, et al. Additional gene therapy with Ad5CMV-p53 enhanced the efficacy of radiotherapy in human prostate cancer cells. Int J Radiat Oncol Biol Phys 2001; 51: 1336-1345.
9. Cowen D, Salem N, Ashoori F, et al. Prostate cancer radiosensitization in vivo with adenovirusmediated p53 gene therapy. Clin Cancer Res 2000; 6: 4402-4408.
10. Yang C, Cirielli C, Capogrossi MC, et al. Adenovirus-mediated wild-Type p53 expression induces apoptosis and suppresses tumorigenesis of prostatic tumor cells. Cancer Res 1995; 55: 4210-4213.
11. Schumacher G, Bruckheimer EM, Beham AW, et al. Molecular determinants of cell death induction following adenovirus-mediated gene transfer of wild-Type p53 in prostate cancer cells. Int J Cancer 2001; 91: 159-166.
12. Eastham JA, Hall SJ, Sehgal I, et al. In vivo gene therapy with p53 or p21 adenovirus for prostate cancer. Cancer Res 1995; 55: 5151-5155.
13. Eastham JA, Grafton W, Martin CM, et al. Suppression of primary tumor growth and the progression to metastasis with p53 adenovirus in human prostate cancer. J Urol 2000; 164: 814-819.
14. Zhang L, Li J, Zong L, et al. Reactive oxygen species and targeted therapy for pancreatic cancer. Oxid Med Cell Longev 2016; 2016: 1616781.
15. Valko M, Izakovic M, Mazur M, et al. Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 2004; 266: 37-56.
16. Valko M, Leibfritz D, Moncol J, et al. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39: 44-84.
17. Roy K, Wu Y, Meitzler JL, et al. NADPH oxidases and cancer. Clin Sci (Lond) 2015; 128: 863-875.
18. Jeong CH, Joo SH. Downregulation of reactive oxygen species in apoptosis. J Cancer Prev 2016; 21: 13-20.
19. Maillet A, Pervaiz S. Redox regulation of p53, redox effectors regulated by p53: a subtle balance. Antioxid Redox Signal 2012; 16: 1285-1294.
20. Vurusaner B, Poli G, Basaga H. Tumor suppressor genes and ROS: complex networks of interactions. Free Radic Biol Med 2012; 52: 7-18.
21. Ladelfa MF, Toledo MF, Laiseca JE, et al. Interaction of p53 with tumor suppressive and oncogenic signaling pathways to control cellular reactive oxygen species production. Antioxid Redox Signal 2011; 15: 1749-1761.
22. Liu B, Chen Y, St Clair DK. ROS and p53: a versatile partnership. Free Radic Biol Med 2008; 44: 1529-1535.
23. Li PF, Dietz R, von Harsdorf R. p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome cindependent apoptosis blocked by Bcl-2. EMBO J 1999; 18: 6027-6036.
24. Montero J, Dutta C, van Bodegom D, et al. p53 regulates a non-Apoptotic death induced by ROS. Cell Death Differ 2013; 20: 1465-1474.
25. Strauss BE, Costanzi-Strauss E. pCLPG: a p53-driven retroviral system. Virology 2004; 321: 165-172.
26. Bajgelman MC, Strauss BE. Development of an adenoviral vector with robust expression driven by p53. Virology 2008; 371: 8-13.
27. Bajgelman MC, Medrano RF, Carvalho AC, et al. AAVPG: a vigilant vector where transgene expression is induced by p53. Virology 2013; 447: 166-171.
28. Tamura RE, da Silva Soares RB, Costanzi-Strauss E, et al. Autoregulated expression of p53 from an adenoviral vector confers superior tumor inhibition in a model of prostate carcinoma gene therapy. Cancer Biol Ther 2016; 17: 1221-1230.
29. Dmitriev I, Krasnykh V, Miller CR, et al. An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. J Virol 1998; 72: 9706-9713.
30. Mizuguchi H, Koizumi N, Hosono T, et al. A simplified system for constructing recombinant adenoviral vectors containing heterologous peptides in the HI loop of their fiber knob. Gene Ther 2001; 8: 730-735.
31. Shen YH, Yang F, Wang H, et al. Arg-Gly-Asp (RGD)-Modified E1A/E1B double mutant adenovirus enhances antitumor activity in prostate cancer cells in vitro and in mice. PLoS One 2016; 11: e0147173.
32. Merkel CA, Medrano RF, Barauna VG, et al.combined p19Arf and interferon-beta gene transfer enhances cell death of B16 melanoma in vitro and in vivo. Cancer Gene Ther 2013; 20: 317-325.
33. Hunger A, Medrano RFV, Zanatta DB, Valle PRD, Merkel CA, Salles TA, et al. Reestablishment of p53/Arf and interferon-b pathways mediated by a novel adenoviral vector potentiates antiviral response and immunogenic cell death. Cell Death Discov 2017; In press
34. Peng HH, Wu S, Davis JJ, et al. A rapid and efficient method for purification of recombinant adenovirus with arginine-glycine-Aspartic acidmodified fibers. Anal Biochem 2006; 354: 140-147.
35. Merkel CA, da Silva Soares RB, de Carvalho AC, et al. Activation of endogenous p53 by combined p19Arf gene transfer and nutlin-3 drug treatment modalities in the murine cell lines B16 and C6. BMC Cancer 2010; 10: 316.
36. Ranayhossaini DJ, Rodriguez AI, Sahoo S, et al. Selective recapitulation of conserved and nonconserved regions of putative NOXA1 protein activation domain confers isoform-specific inhibition of Nox1 oxidase and attenuation of endothelial cell migration. J Biol Chem 2013; 288: 36437-36450.
37. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989; 24: 148-154.
38. Puca R, Nardinocchi L, Starace G, et al. Nox1 is involved in p53 deacetylation and suppression of its transcriptional activity and apoptosis. Free Radic Biol Med 2010; 48: 1338-1346.
39. Garufi A, D Orazi V, Arbiser JL, et al. Gentian violet induces wtp53 transactivation in cancer cells. Int J Oncol 2014; 44: 1084-1090.
40. Li JM, Fan LM, George VT, et al. Nox2 regulates endothelial cell cycle arrest and apoptosis via p21cip1 and p53. Free Radic Biol Med 2007; 43: 976-986.
41. Boudreau HE, Casterline BW, Burke DJ, et al. Wild-Type and mutant p53 differentially regulate NADPH oxidase 4 in TGF-b-mediated migration of human lung and breast epithelial cells. Br J Cancer 2014; 110: 2569-2582.
42. Flatt PM, Polyak K, Tang LJ, et al. p53-dependent expression of PIG3 during proliferation, genotoxic stress, and reversible growth arrest. Cancer Lett 2000; 156: 63-72.
43. Polyak K, Xia Y, Zweier JL, et al. A model for p53-induced apoptosis. Nature 1997; 389: 300-305.
44. Lehar SM, Nacht M, Jacks T, et al. Identification and cloning of EI24, a gene induced by p53 in etoposide-Treated cells. Oncogene 1996; 12: 1181-1187.
45. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009; 458: 1127-1130.
46. Hu J, Yao H, Gan F, et al. Interaction of OKL38 and p53 in regulating mitochondrial structure and function. PLoS One 2012; 7: e43362.
47. Yao H, Li P, Venters BJ, et al. Histone Arg modifications and p53 regulate the expression of OKL38, a mediator of apoptosis. J Biol Chem 2008; 283: 20060-20068.
48. Ahmad IM, Abdalla MY, Aykin-Burns N, et al. 2-Deoxyglucose combined with wild-Type p53 overexpression enhances cytotoxicity in human prostate cancer cells via oxidative stress. Free Radic Biol Med 2008; 44: 826-834.
49. el-Deiry WS, Harper JW, O Connor PM, et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res 1994; 54: 1169-1174.
50. el-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75: 817-825.
51. Tamura RE, de Vasconcellos JF, Sarkar D, et al. GADD45 proteins: central players in tumorigenesis. Curr Mol Med 2012; 12: 634-651.
52. Budanov AV, Karin M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 2008; 134: 451-460.
53. Maiuri MC, Malik SA, Morselli E, et al. Stimulation of autophagy by the p53 target gene Sestrin2. Cell Cycle 2009; 8: 1571-1576.
54. Ambrosini G, Adida C, Altieri DC. A novel antiapoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 1997; 3: 917-921.
55. Asanuma K, Moriai R, Yajima T, et al. Survivin as a radioresistance factor in pancreatic cancer. Jpn J Cancer Res 2000; 91: 1204-1209.
56. Li Q, Lozano G. Molecular pathways: targeting Mdm2 and Mdm4 in cancer therapy. Clin Cancer Res 2013; 19: 34-41.