Valproic acid inhibits glioblastoma multiforme cell growth via paraoxonase 2 expression

Oncotarget

Volumn 8, Issue 9, 2017, Pages 14666-14679

  Tseng, Jen Ho ^a,b   Chen, Cheng Yi ^c   Chen, Pei Chun ^c   Hsiao, Sheng Huang ^a,d   Fan, Chi Chen ^c   Liang, Yu Chih ^e   Chen, Chie Pein ^c,e  

^a TAIPEI CITY HOSPITAL   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c MACKAY MEMORIAL HOSPITAL   (Taiwan)

^d NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Cell growth; Glioblastoma multiforme; Histone deacetylase; Paraoxonase 2; Valproic acid

Indexed keywords

ARYLDIALKYLPHOSPHATASE 2; BIM PROTEIN; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; PROTEIN BCL XL; PROTEIN P21; PROTEIN P27; REACTIVE OXYGEN METABOLITE; TEMOZOLOMIDE; VALPROIC ACID; ARYLDIALKYLPHOSPHATASE; GABAERGIC RECEPTOR AFFECTING AGENT; PON2 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; DOWN REGULATION; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIZATION; G2 PHASE CELL CYCLE CHECKPOINT; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PON2 GENE; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BRAIN NEOPLASMS; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUDE MOUSE; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ARYLDIALKYLPHOSPHATASE; BCL-2-LIKE PROTEIN 11; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; GABA AGENTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MICE, INBRED BALB C; MICE, NUDE; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; VALPROIC ACID; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85014119931     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14716     Document Type: Article

References (67)

1. McLendon RE, Halperin EC. Is the long-term survival of patients with intracranial glioblastoma multiforme overstated? Cancer. 2003; 98:1745-1748.
2. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009; 10:459-466.
3. Yeow WS, Ziauddin MF, Maxhimer JB, Shamimi-Noori S, Baras A, Chua A, Schrump DS, Nguyen DM. Potentiation of the anticancer effect of valproic acid, an antiepileptic agent with histone deacetylase inhibitory activity, by the kinase inhibitor Staurosporine or its clinically relevant analogue UCN-01. Br J Cancer. 2006; 94:1436-1445.
4. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem. 2001; 276:36734-36741.
5. Masoudi A, Elopre M, Amini E, Nagel ME, Ater JL, Gopalakrishnan V, Wolff JE. Influence of valproic acid on outcome of high-grade gliomas in children. Anticancer Res. 2008; 28:2437-2442.
6. Driever PH, Knupfer MM, Cinatl J, Wolff JE. Valproic acid for the treatment of pediatric malignant glioma. Klin Padiatr. 1999; 211:323-328.
7. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y, Carrier F. Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res. 2003; 63:7291-7300.
8. Witt O, Schweigerer L, Driever PH, Wolff J, Pekrun A. Valproic acid treatment of glioblastoma multiforme in a child. Pediatr Blood Cancer. 2004; 43:181.
9. Driever PH, Wagner S, Hofstadter F, Wolff JE. Valproic acid induces differentiation of a supratentorial primitive neuroectodermal tumor. Pediatr Hematol Oncol. 2004; 21:743-751.
10. Oberndorfer S, Piribauer M, Marosi C, Lahrmann H, Hitzenberger P, Grisold W. P450 enzyme inducing and non-enzyme inducing antiepileptics in glioblastoma patients treated with standard chemotherapy. J Neurooncol. 2005; 72:255-260.
11. Guthrie GD, Eljamel S. Impact of particular antiepileptic drugs on the survival of patients with glioblastoma multiforme. J Neurosurg. 2013; 118:859-865.
12. Das CM, Aguilera D, Vasquez H, Prasad P, Zhang M, Wolff JE, Gopalakrishnan V. Valproic acid induces p21 and topoisomerase-II (alpha/beta) expression and synergistically enhances etoposide cytotoxicity in human glioblastoma cell lines. J Neurooncol. 2007; 85:159-170.
13. Bangert A, Cristofanon S, Eckhardt I, Abhari BA, Kolodziej S, Hacker S, Vellanki SH, Lausen J, Debatin KM, Fulda S. Histone deacetylase inhibitors sensitize glioblastoma cells to TRAIL-induced apoptosis by c-myc-mediated downregulation of cFLIP. Oncogene. 2012; 31:4677-4688.
14. Camphausen K, Cerna D, Scott T, Sproull M, Burgan WE, Cerra MA, Fine H, Tofilon PJ. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int J Cancer. 2005; 114:380-386.
15. Chinnaiyan P, Cerna D, Burgan WE, Beam K, Williams ES, Camphausen K, Tofilon PJ. Postradiation sensitization of the histone deacetylase inhibitor valproic acid. Clin Cancer Res. 2008; 14:5410-5415.
16. Shabason JE, Tofilon PJ, Camphausen K. Grand rounds at the National Institutes of Health: HDAC inhibitors as radiation modifiers, from bench to clinic. J Cell Mol Med. 2011; 15:2735-2744.
17. Pourahmad J, Eskandari MR, Kaghazi A, Shaki F, Shahraki J, Fard JK. A new approach on valproic acid induced hepatotoxicity: involvement of lysosomal membrane leakiness and cellular proteolysis. Toxicol In Vitro. 2012; 26:545-551.
18. Sha K, Winn LM. Characterization of valproic acid-initiated homologous recombination. Birth Defects Res B Dev Reprod Toxicol. 2010; 89:124-132.
19. Hassett C, Richter RJ, Humbert R, Chapline C, Crabb JW, Omiecinski CJ, Furlong CE. Characterization of cDNA clones encoding rabbit and human serum paraoxonase: the mature protein retains its signal sequence. Biochemistry. 1991; 30:10141-10149.
20. Shih DM, Lusis AJ. The roles of PON1 and PON2 in cardiovascular disease and innate immunity. Curr Opin Lipidol. 2009; 20:288-292.
21. Blatter MC, James RW, Messmer S, Barja F, Pometta D. Identification of a distinct human high-density lipoprotein subspecies defined by a lipoprotein-associated protein, K-45. Identity of K-45 with paraoxonase. Eur J Biochem. 1993; 211:871-879.
22. Ng CJ, Wadleigh DJ, Gangopadhyay A, Hama S, Grijalva VR, Navab M, Fogelman AM, Reddy ST. Paraoxonase-2 is a ubiquitously expressed protein with antioxidant properties and is capable of preventing cellmediated oxidative modification of low density lipoprotein. J Biol Chem. 2001; 276:44444-44449.
23. Elkiran ET, Mar N, Aygen B, Gursu F, Karaoglu A, Koca S. Serum paraoxonase and arylesterase activities in patients with lung cancer in a Turkish population. BMC Cancer. 2007; 7:48-55.
24. Aksoy-Sagirli P, Cakmakoglu B, Isbir T, Kaytan-Saglam E, Kizir A, Topuz E, Berkkan H. Paraoxonase-1 192/55 polymorphisms and the risk of lung cancer in a Turkish population. Anticancer Res. 2011; 31:2225-2229.
25. Vecka M, Jachymova M, Vavrova L, Kodydkova J, Macasek J, Urbanek M, Krechler T, Slaby A, Duskova J, Muravska A, Zak A. Paraoxonase-1 (PON1) status in pancreatic cancer: relation to clinical parameters. Folia Biol (Praha). 2012; 58:231-237.
26. Schweikert EM, Devarajan A, Witte I, Wilgenbus P, Amort J, Forstermann U, Shabazian A, Grijalva V, Shih DM, Farias-Eisner R, Teiber JF, Reddy ST, Horke S. PON3 is upregulated in cancer tissues and protects against mitochondrial superoxide-mediated cell death. Cell Death Differ. 2012; 19:1549-1560.
27. Salcher S, Hagenbuchner J, Geiger K, Seiter MA, Rainer J, Kofler R, Hermann M, Kiechl-Kohlendorfer U, Ausserlechner MJ, Obexer P. C10ORF10/DEPP, a transcriptional target of FOXO3, regulates ROS-sensitivity in human neuroblastoma. Mol Cancer. 2014; 13:224-240.
28. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O. Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc. 2009; 4:1798-1806.
29. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov. 2006; 5:769-784.
30. Chavez-Blanco A, Perez-Plasencia C, Perez-Cardenas E, Carrasco-Legleu C, Rangel-Lopez E, Segura-Pacheco B, Taja-Chayeb L, Trejo-Becerril C, Gonzalez-Fierro A, Candelaria M, Cabrera G, Duenas-Gonzalez A. Antineoplastic effects of the DNA methylation inhibitor hydralazine and the histone deacetylase inhibitor valproic acid in cancer cell lines. Cancer Cell Int. 2006; 6:2-10.
31. Horke S, Witte I, Wilgenbus P, Kruger M, Strand D, Forstermann U. Paraoxonase-2 reduces oxidative stress in vascular cells and decreases endoplasmic reticulum stress-induced caspase activation. Circulation. 2007; 115:2055-2064.
32. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008; 455:1061-1068.
33. Chen CY, Chung IH, Tsai MM, Tseng YH, Chi HC, Tsai CY, Lin YH, Wang YC, Chen CP, Wu TI, Yeh CT, Tai DI, Lin KH. Thyroid hormone enhanced human hepatoma cell motility involves brain-specific serine protease 4 activation via ERK signaling. Mol Cancer. 2014; 13:162-178.
34. Chen CY, Chi LM, Chi HC, Tsai MM, Tsai CY, Tseng YH, Lin YH, Chen WJ, Huang YH, Lin KH. Stable isotope labeling with amino acids in cell culture (SILAC)-based quantitative proteomics study of a thyroid hormoneregulated secretome in human hepatoma cells. Mol Cell Proteomics. 2012; 11:M111 011270-19.
35. Singh RK, Cho K, Padi SK, Yu J, Haldar M, Mandal T, Yan C, Cook G, Guo B, Mallik S, Srivastava DK. Mechanism of N-Acylthiourea-mediated activation of human histone deacetylase 8 (HDAC8) at molecular and cellular levels. J Biol Chem. 2015; 290:6607-6619.
36. Singh RK, Mandal T, Balsubramanian N, Viaene T, Leedahl T, Sule N, Cook G, Srivastava DK. Histone deacetylase activators: N-acetylthioureas serve as highly potent and isozyme selective activators for human histone deacetylase-8 on a fluorescent substrate. Bioorg Med Chem Lett. 2011; 21:5920-5923.
37. Weller M, Gorlia T, Cairncross JG, van den Bent MJ, Mason W, Belanger K, Brandes AA, Bogdahn U, Macdonald DR, Forsyth P, Rossetti AO, Lacombe D, Mirimanoff RO, et al. Prolonged survival with valproic acid use in the EORTC/NCIC temozolomide trial for glioblastoma. Neurology. 2011; 77:1156-1164.
38. Bredel M, Bredel C, Juric D, Harsh GR, Vogel H, Recht LD, Sikic BI. Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYCinteracting genes in human gliomas. Cancer Res. 2005; 65:8679-8689.
39. Ververis K, Hiong A, Karagiannis TC, Licciardi PV. Histone deacetylase inhibitors (HDACIs): multitargeted anticancer agents. Biologics. 2013; 7:47-60.
40. Li XN, Shu Q, Su JM, Perlaky L, Blaney SM, Lau CC. Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol Cancer Ther. 2005; 4:1912-1922.
41. Fu J, Shao CJ, Chen FR, Ng HK, Chen ZP. Autophagy induced by valproic acid is associated with oxidative stress in glioma cell lines. Neuro Oncol. 2010; 12:328-340.
42. Kawamoto H, Koizumi H, Uchikoshi T. Expression of the G2-M checkpoint regulators cyclin B1 and cdc2 in nonmalignant and malignant human breast lesions: immunocytochemical and quantitative image analyses. Am J Pathol. 1997; 150:15-23.
43. Campone M, Noel B, Couriaud C, Grau M, Guillemin Y, Gautier F, Gouraud W, Charbonnel C, Campion L, Jezequel P, Braun F, Barre B, Coqueret O, et al. c-Myc dependent expression of pro-apoptotic Bim renders HER2-overexpressing breast cancer cells dependent on antiapoptotic Mcl-1. Mol Cancer. 2011; 10:110-123.
44. Gottlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 2001; 20:6969-6978.
45. Rajaraman P, Hutchinson A, Rothman N, Black PM, Fine HA, Loeffler JS, Selker RG, Shapiro WR, Linet MS, Inskip PD. Oxidative response gene polymorphisms and risk of adult brain tumors. Neuro Oncol. 2008; 10:709-715.
46. Zhao P, Zhao L, Zou P, Lu A, Liu N, Yan W, Kang C, Fu Z, You Y, Jiang T. Genetic oxidative stress variants and glioma risk in a Chinese population: a hospital-based case-control study. BMC Cancer. 2012; 12:617-626.
47. Altenhofer S, Witte I, Teiber JF, Wilgenbus P, Pautz A, Li H, Daiber A, Witan H, Clement AM, Forstermann U, Horke S. One enzyme, two functions: PON2 prevents mitochondrial superoxide formation and apoptosis independent from its lactonase activity. J Biol Chem. 2010; 285:24398-24403.
48. Li Y, Tang R, Xu H, Qiu M, Chen Q, Chen J, Fu Z, Ying K, Xie Y, Mao Y. Discovery and analysis of hepatocellular carcinoma genes using cDNA microarrays. J Cancer Res Clin Oncol. 2002; 128:369-379.
49. Ribarska T, Ingenwerth M, Goering W, Engers R, Schulz WA. Epigenetic inactivation of the placentally imprinted tumor suppressor gene TFPI2 in prostate carcinoma. Cancer Genomics Proteomics. 2010; 7:51-60.
50. Witte I, Altenhofer S, Wilgenbus P, Amort J, Clement AM, Pautz A, Li H, Forstermann U, Horke S. Beyond reduction of atherosclerosis: PON2 provides apoptosis resistance and stabilizes tumor cells. Cell Death Dis. 2011; 2:e112.
51. Pise-Masison CA, Radonovich M, Mahieux R, Chatterjee P, Whiteford C, Duvall J, Guillerm C, Gessain A, Brady JN. Transcription profile of cells infected with human T-cell leukemia virus type I compared with activated lymphocytes. Cancer Res. 2002; 62:3562-3571.
52. Kang H, Chen IM, Wilson CS, Bedrick EJ, Harvey RC, Atlas SR, Devidas M, Mullighan CG, Wang X, Murphy M, Ar K, Wharton W, Borowitz MJ, et al. Gene expression classifiers for relapse-free survival and minimal residual disease improve risk classification and outcome prediction in pediatric B-precursor acute lymphoblastic leukemia. Blood. 2010; 115:1394-1405.
53. Kim HJ, Bae SC. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res. 2011; 3:166-179.
54. Bermudez-Lugo JA, Perez-Gonzalez O, Rosales-Hernandez MC, Ilizaliturri-Flores I, Trujillo-Ferrara J, Correa-Basurto J. Exploration of the valproic acid binding site on histone deacetylase 8 using docking and molecular dynamic simulations. J Mol Model. 2012; 18:2301-2310.
55. Akbasak A, Toevs CC, Laske DW. Reconstituted basement membrane (matrigel) enhances the growth of human glioma cell lines in nude mice. J Neurooncol. 1996; 27:23-30.
56. Karen J, Rodriguez A, Friman T, Dencker L, Sundberg C, Scholz B. Effects of the histone deacetylase inhibitor valproic acid on human pericytes in vitro. PLoS One. 2011; 6:e24954.
57. Jung M, Velena A, Chen B, Petukhov PA, Kozikowski AP, Dritschilo A. Novel HDAC inhibitors with radiosensitizing properties. Radiat Res. 2005; 163:488-493.
58. Van Nifterik KA, Van den Berg J, Slotman BJ, Lafleur MV, Sminia P, Stalpers LJ. Valproic acid sensitizes human glioma cells for temozolomide and gamma-radiation. J Neurooncol. 2012; 107:61-67.
59. Chen Y, Tsai YH, Tseng SH. Valproic acid affected the survival and invasiveness of human glioma cells through diverse mechanisms. J Neurooncol. 2012; 109:23-33.
60. Zhou Y, Xu Y, Wang H, Niu J, Hou H, Jiang Y. Histone deacetylase inhibitor, valproic acid, radiosensitizes the C6 glioma cell line. Oncol Lett. 2014; 7:203-208.
61. Kerkhof M, Dielemans JC, van Breemen MS, Zwinkels H, Walchenbach R, Taphoorn MJ, Vecht CJ. Effect of valproic acid on seizure control and on survival in patients with glioblastoma multiforme. Neuro Oncol. 2013; 15:961-967.
62. Zhao GX, Xu LH, Pan H, Lin QR, Huang MY, Cai JY, Ouyang DY, He XH. The BH3-mimetic gossypol and noncytotoxic doses of valproic acid induce apoptosis by suppressing cyclin-A2/Akt/FOXO3a signaling. Oncotarget. 2015; 6:38952-38966. doi: 10.18632/oncotarget.5731.
63. Tsai HC, Wei KC, Tsai CN, Huang YC, Chen PY, Chen SM, Lu YJ, Lee ST. Effect of valproic acid on the outcome of glioblastoma multiforme. Br J Neurosurg. 2012; 26:347-354.
64. Thotala D, Karvas RM, Engelbach JA, Garbow JR, Hallahan AN, DeWees TA, Laszlo A, Hallahan DE. Valproic acid enhances the efficacy of radiation therapy by protecting normal hippocampal neurons and sensitizing malignant glioblastoma cells. Oncotarget. 2015; 6:35004-35022. doi: 10.18632/oncotarget.5253.
65. Chiou HY, Lai WK, Huang LC, Huang SM, Chueh SH, Ma HI, Hueng DY. Valproic acid promotes radiosensitization in meningioma stem-like cells. Oncotarget. 2015; 6:9959-9969. doi: 10.18632/oncotarget.3692.
66. Barker CA, Bishop AJ, Chang M, Beal K, Chan TA. Valproic acid use during radiation therapy for glioblastoma associated with improved survival. Int J Radiat Oncol Biol Phys. 2013; 86:504-509.
67. Brunton LL, Chabner BA, Knollmann BC. Goodman & Gilman's the Pharmacological Basis of Therapeutics, 12e. Pharmacotherapy of the Epilepsies, Valproic Acid. 2011.