Non-competitive heme oxygenase-1 activity inhibitor reduces non-small cell lung cancer glutathione content and regulates cell proliferation.
A549 Cells
Carcinoma, Non-Small-Cell Lung
/ drug therapy
Cell Proliferation
/ drug effects
Cell Survival
/ drug effects
Down-Regulation
Enzyme Inhibitors
/ chemistry
Glutathione
/ metabolism
Heme Oxygenase-1
/ antagonists & inhibitors
Humans
Hydrocarbons, Brominated
/ chemistry
Imidazoles
/ chemistry
Lung Neoplasms
/ drug therapy
Mitochondria
/ drug effects
Oxidative Stress
Glutathione
Heme oxygenase
Lung cancer
Oxidative stress
Journal
Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234
Informations de publication
Date de publication:
Mar 2020
Mar 2020
Historique:
received:
06
09
2019
accepted:
29
01
2020
revised:
24
01
2020
pubmed:
15
2
2020
medline:
11
11
2020
entrez:
15
2
2020
Statut:
ppublish
Résumé
Non-small cell lung cancer (NSCLC) remains the leading cause of cancer-related death mainly due to its high metastatic rate. Impairment of redox homeostasis mechanisms has been previously described in NSCLC and is associated with the disease itself as well as with comorbidities such as smoking. The aim of the present in vitro study was to evaluate the effect of selective and non-competitive inhibition of heme oxygenase-1 (HO-1) on cancer redox homeostasis with particular regards to glutathione (GSH) metabolism related enzymes. NSCLC cell line (A549) was treated with the HO-1 activity inhibitor VP13/47 (10 µM) and we further evaluated cell viability, apoptosis, mitochondrial dysfunction and oxidative stress. Our results showed that VP13/47 significantly reduced HO-1 expression and total HO activity thus, resulting in a significant reduction of cell viability, proliferation and increased apoptosis, mitochondrial dysfunction and oxidative stress. Consistently with increased oxidative stress, we also showed that reduced GSH was significantly decreased and such effect was also accompanied by a significant downregulation of the enzymes involved in its biosynthesis. Taken all together our results show that selective HO-1 inhibition significantly impairs NSCLC progression and may represent a possible pharmacological strategy for new chemotherapy agents.
Identifiants
pubmed: 32056044
doi: 10.1007/s11033-020-05292-y
pii: 10.1007/s11033-020-05292-y
doi:
Substances chimiques
Enzyme Inhibitors
0
Hydrocarbons, Brominated
0
Imidazoles
0
VP13-47 compound
0
HMOX1 protein, human
EC 1.14.14.18
Heme Oxygenase-1
EC 1.14.14.18
Glutathione
GAN16C9B8O
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1949-1964Subventions
Organisme : Università di Catania
ID : FIR2016-2018
Organisme : Università di Catania (IT)
ID : FIR 2016-2018
Références
Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA (2008) Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc 83(5):584–594. https://doi.org/10.4065/83.5.584
doi: 10.4065/83.5.584
pubmed: 18452692
pmcid: 2718421
Oshita F, Morita A, Ito H, Kameda Y, Tsuchiya E, Asai S, Miyagi Y (2010) Proteomic screening of completely resected tumors in relation to survival in patients with stage I non-small cell lung cancer. Oncol Rep 24(3):637–645
doi: 10.3892/or_00000902
Fahrmann JF, Grapov D, Phinney BS, Stroble C, DeFelice BC, Rom W, Gandara DR, Zhang Y, Fiehn O, Pass H, Miyamoto S (2016) Proteomic profiling of lung adenocarcinoma indicates heightened DNA repair, antioxidant mechanisms and identifies LASP1 as a potential negative predictor of survival. Clin Proteomics 13:31. https://doi.org/10.1186/s12014-016-9132-y
doi: 10.1186/s12014-016-9132-y
pubmed: 27799870
pmcid: 5084393
Scire A, Cianfruglia L, Minnelli C, Bartolini D, Torquato P, Principato G, Galli F, Armeni T (2019) Glutathione compartmentalization and its role in glutathionylation and other regulatory processes of cellular pathways. BioFactors 45(2):152–168. https://doi.org/10.1002/biof.1476
doi: 10.1002/biof.1476
pubmed: 30561781
Narayanankutty A, Jdevagiri JT, Narayanankutty V (2019) Glutathione, an antioxidant tripeptide: dual roles in carcinogenesis and chemoprevention. Curr Protein Pept Sci. https://doi.org/10.2174/1389203720666190206130003
doi: 10.2174/1389203720666190206130003
pubmed: 30727890
Battino M, Giampieri F, Pistollato F, Sureda A, de Oliveira MR, Pittala V, Fallarino F, Nabavi SF, Atanasov AG, Nabavi SM (2018) Nrf2 as regulator of innate immunity: a molecular Swiss army knife! Biotechnol Adv 36(2):358–370. https://doi.org/10.1016/j.biotechadv.2017.12.012
doi: 10.1016/j.biotechadv.2017.12.012
pubmed: 29277308
Barbagallo I, Marrazzo G, Frigiola A, Zappala A, Li Volti G (2012) Role of carbon monoxide in vascular diseases. Curr Pharm Biotechnol 13(6):787–796. https://doi.org/10.2174/138920112800399086
doi: 10.2174/138920112800399086
pubmed: 22201604
Barbagallo I, Nicolosi A, Calabrese G, David S, Cimino S, Madonia M, Cappello F (2014) The role of the heme oxygenase system in the metabolic syndrome. Curr Pharm Des 20(31):4970–4974. https://doi.org/10.2174/1381612819666131206103824
doi: 10.2174/1381612819666131206103824
pubmed: 24320035
Vanella L, Barbagallo I, Tibullo D, Forte S, Zappala A, Li Volti G (2016) The non-canonical functions of the heme oxygenases. Oncotarget 7(42):69075–69086. https://doi.org/10.18632/oncotarget.11923
doi: 10.18632/oncotarget.11923
pubmed: 27626166
pmcid: 5356613
Maines MD, Abrahamsson PA (1996) Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution. Urology 47(5):727–733
doi: 10.1016/S0090-4295(96)00010-6
Noh SJ, Bae JS, Jamiyandorj U, Park HS, Kwon KS, Jung SH, Youn HJ, Lee H, Park BH, Chung MJ, Moon WS, Kang MJ, Jang KY (2013) Expression of nerve growth factor and heme oxygenase-1 predict poor survival of breast carcinoma patients. BMC Cancer 13:516. https://doi.org/10.1186/1471-2407-13-516
doi: 10.1186/1471-2407-13-516
pubmed: 24180625
pmcid: 3818967
Degese MS, Mendizabal JE, Gandini NA, Gutkind JS, Molinolo A, Hewitt SM, Curino AC, Coso OA, Facchinetti MM (2012) Expression of heme oxygenase-1 in non-small cell lung cancer (NSCLC) and its correlation with clinical data. Lung Cancer 77(1):168–175. https://doi.org/10.1016/j.lungcan.2012.02.016
doi: 10.1016/j.lungcan.2012.02.016
pubmed: 22418244
Mayerhofer M, Florian S, Krauth MT, Aichberger KJ, Bilban M, Marculescu R, Printz D, Fritsch G, Wagner O, Selzer E, Sperr WR, Valent P, Sillaber C (2004) Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res 64(9):3148–3154
doi: 10.1158/0008-5472.CAN-03-1200
Tibullo D, Barbagallo I, Giallongo C, La Cava P, Parrinello N, Vanella L, Stagno F, Palumbo GA, Li Volti G, Di Raimondo F (2013) Nuclear translocation of heme oxygenase-1 confers resistance to imatinib in chronic myeloid leukemia cells. Curr Pharm Des 19(15):2765–2770
doi: 10.2174/1381612811319150012
Lin X, Fang Q, Chen S, Zhe N, Chai Q, Yu M, Zhang Y, Wang Z, Wang J (2015) Heme oxygenase-1 suppresses the apoptosis of acute myeloid leukemia cells via the JNK/c-JUN signaling pathway. Leuk Res 39(5):544–552. https://doi.org/10.1016/j.leukres.2015.02.009
doi: 10.1016/j.leukres.2015.02.009
pubmed: 25828744
Salerno L, Romeo G, Modica MN, Amata E, Sorrenti V, Barbagallo I, Pittala V (2017) Heme oxygenase-1: a new druggable target in the management of chronic and acute myeloid leukemia. Eur J Med Chem 142:163–178. https://doi.org/10.1016/j.ejmech.2017.07.031
doi: 10.1016/j.ejmech.2017.07.031
pubmed: 28756878
Raninga PV, Di Trapani G, Vuckovic S, Tonissen KF (2016) Cross-talk between two antioxidants, thioredoxin reductase and heme oxygenase-1, and therapeutic implications for multiple myeloma. Redox Biol 8:175–185. https://doi.org/10.1016/j.redox.2016.01.007
doi: 10.1016/j.redox.2016.01.007
pubmed: 26795735
pmcid: 4732019
Liu ZM, Chen GG, Ng EK, Leung WK, Sung JJ, Chung SC (2004) Upregulation of heme oxygenase-1 and p21 confers resistance to apoptosis in human gastric cancer cells. Oncogene 23(2):503–513. https://doi.org/10.1038/sj.onc.1207173
doi: 10.1038/sj.onc.1207173
pubmed: 14647439
Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Kunzli B, Autschbach F, Meuer S, Buchler MW, Friess H (2005) Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res Off J Am Assoc Cancer Res 11(10):3790–3798. https://doi.org/10.1158/1078-0432.CCR-04-2159
doi: 10.1158/1078-0432.CCR-04-2159
Kweon MH, Adhami VM, Lee JS, Mukhtar H (2006) Constitutive overexpression of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J Biol Chem 281(44):33761–33772. https://doi.org/10.1074/jbc.M604748200
doi: 10.1074/jbc.M604748200
pubmed: 16950787
Liu YS, Li HS, Qi DF, Zhang J, Jiang XC, Shi K, Zhang XJ, Zhang XH (2014) Zinc protoporphyrin IX enhances chemotherapeutic response of hepatoma cells to cisplatin. World J Gastroenterol 20(26):8572–8582. https://doi.org/10.3748/wjg.v20.i26.8572
doi: 10.3748/wjg.v20.i26.8572
pubmed: 25024611
pmcid: 4093706
Kongpetch S, Kukongviriyapan V, Prawan A, Senggunprai L, Kukongviriyapan U, Buranrat B (2012) Crucial role of heme oxygenase-1 on the sensitivity of cholangiocarcinoma cells to chemotherapeutic agents. PLoS ONE 7(4):e34994. https://doi.org/10.1371/journal.pone.0034994
doi: 10.1371/journal.pone.0034994
pubmed: 22514698
pmcid: 3325916
Kocanova S, Buytaert E, Matroule JY, Piette J, Golab J, de Witte P, Agostinis P (2007) Induction of heme-oxygenase 1 requires the p38MAPK and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy. Apoptosis 12(4):731–741. https://doi.org/10.1007/s10495-006-0016-x
doi: 10.1007/s10495-006-0016-x
pubmed: 17219054
Sorrenti V, Pittala V, Romeo G, Amata E, Dichiara M, Marrazzo A, Turnaturi R, Prezzavento O, Barbagallo I, Vanella L, Rescifina A, Floresta G, Tibullo D, Di Raimondo F, Intagliata S, Salerno L (2018) Targeting heme oxygenase-1 with hybrid compounds to overcome imatinib resistance in chronic myeloid leukemia cell lines. Eur J Med Chem 158:937–950. https://doi.org/10.1016/j.ejmech.2018.09.048
doi: 10.1016/j.ejmech.2018.09.048
pubmed: 30261468
Li Volti G, Tibullo D, Vanella L, Giallongo C, Di Raimondo F, Forte S, Di Rosa M, Signorelli SS, Barbagallo I (2017) The heme oxygenase system in hematological malignancies. Antioxid Redox Signal 27(6):363–377. https://doi.org/10.1089/ars.2016.6735
doi: 10.1089/ars.2016.6735
pubmed: 28257621
Salerno L, Floresta G, Ciaffaglione V, Gentile D, Margani F, Turnaturi R, Rescifina A, Pittala V (2019) Progress in the development of selective heme oxygenase-1 inhibitors and their potential therapeutic application. Eur J Med Chem 167:439–453. https://doi.org/10.1016/j.ejmech.2019.02.027
doi: 10.1016/j.ejmech.2019.02.027
pubmed: 30784878
Farhan M, Malik A, Ullah MF, Afaq S, Faisal M, Farooqi AA, Biersack B, Schobert R, Ahmad A (2019) Garcinol sensitizes NSCLC cells to standard therapies by regulating EMT-modulating miRNAs. Int J Mol Sci. https://doi.org/10.3390/ijms20040800
doi: 10.3390/ijms20040800
pubmed: 30781783
pmcid: 6413107
Malfa GA, Tomasello B, Sinatra F, Villaggio G, Amenta F, Avola R, Renis M (2014) “Reactive” response evaluation of primary human astrocytes after methylmercury exposure. J Neurosci Res 92(1):95–103. https://doi.org/10.1002/jnr.23290
doi: 10.1002/jnr.23290
pubmed: 24123177
Acquaviva R, Sorrenti V, Santangelo R, Cardile V, Tomasello B, Malfa G, Vanella L, Amodeo A, Genovese C, Mastrojeni S, Pugliese M, Ragusa M, Di Giacomo C (2016) Effects of an extract of Celtis aetnensis (Tornab.) Strobl twigs on human colon cancer cell cultures. Oncol Rep 36(4):2298–2304. https://doi.org/10.3892/or.2016.5035
doi: 10.3892/or.2016.5035
pubmed: 27573437
Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86(2):583–650. https://doi.org/10.1152/physrev.00011.2005
doi: 10.1152/physrev.00011.2005
pubmed: 16601269
Vanella L, Russo GI, Cimino S, Fragala E, Favilla V, Li Volti G, Barbagallo I, Sorrenti V, Morgia G (2014) Correlation between lipid profile and heme oxygenase system in patients with benign prostatic hyperplasia. Urology 83(6):1444.e7-1444.e13. https://doi.org/10.1016/j.urology.2014.03.007
doi: 10.1016/j.urology.2014.03.007
Barbagallo I, Vanella L, Cambria MT, Tibullo D, Godos J, Guarnaccia L, Zappala A, Galvano F, Li Volti G (2015) Silibinin regulates lipid metabolism and differentiation in functional human adipocytes. Front Pharmacol 6:309. https://doi.org/10.3389/fphar.2015.00309
doi: 10.3389/fphar.2015.00309
pubmed: 26834634
Palmeri R, Monteleone JI, Spagna G, Restuccia C, Raffaele M, Vanella L, Li Volti G, Barbagallo I (2016) Olive leaf extract from Sicilian cultivar reduced lipid accumulation by inducing thermogenic pathway during adipogenesis. Front Pharmacol 7:143. https://doi.org/10.3389/fphar.2016.00143
doi: 10.3389/fphar.2016.00143
pubmed: 27303302
pmcid: 4885843
Salerno L, Pittala V, Romeo G, Modica MN, Siracusa MA, Di Giacomo C, Acquaviva R, Barbagallo I, Tibullo D, Sorrenti V (2013) Evaluation of novel aryloxyalkyl derivatives of imidazole and 1,2,4-triazole as heme oxygenase-1 (HO-1) inhibitors and their antitumor properties. Bioorg Med Chem 21(17):5145–5153. https://doi.org/10.1016/j.bmc.2013.06.040
doi: 10.1016/j.bmc.2013.06.040
pubmed: 23867390
Furfaro AL, Traverso N, Domenicotti C, Piras S, Moretta L, Marinari UM, Pronzato MA, Nitti M (2016) The Nrf2/HO-1 axis in cancer cell growth and chemoresistance. Oxid Med Cell Longev 2016:1958174. https://doi.org/10.1155/2016/1958174
doi: 10.1155/2016/1958174
pubmed: 26697129
Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG (1994) Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA 91(13):5987–5991
doi: 10.1073/pnas.91.13.5987
Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, Choi AM (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272(9):5375–5381
doi: 10.1074/jbc.272.9.5375
Tsai JR, Wang HM, Liu PL, Chen YH, Yang MC, Chou SH, Cheng YJ, Yin WH, Hwang JJ, Chong IW (2012) High expression of heme oxygenase-1 is associated with tumor invasiveness and poor clinical outcome in non-small cell lung cancer patients. Cell Oncol 35(6):461–471. https://doi.org/10.1007/s13402-012-0105-5
doi: 10.1007/s13402-012-0105-5
Lignitto L, LeBoeuf SE, Homer H, Jiang S, Askenazi M, Karakousi TR, Pass HI, Bhutkar AJ, Tsirigos A, Ueberheide B, Sayin VI, Papagiannakopoulos T, Pagano M (2019) Nrf2 activation promotes lung cancer metastasis by inhibiting the degradation of Bach1. Cell 178(2):316-329.e18. https://doi.org/10.1016/j.cell.2019.06.003
doi: 10.1016/j.cell.2019.06.003
pubmed: 31257023
pmcid: 31257023
Podkalicka P, Mucha O, Jozkowicz A, Dulak J, Loboda A (2018) Heme oxygenase inhibition in cancers: possible tools and targets. Contemp Oncol (Pozn) 22(1A):23–32. https://doi.org/10.5114/wo.2018.73879
doi: 10.5114/wo.2018.73879
Ignarro LJ, Ballot B, Wood KS (1984) Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. J Biol Chem 259(10):6201–6207
pubmed: 6144676
Luo D, Vincent SR (1994) Metalloporphyrins inhibit nitric oxide-dependent cGMP formation in vivo. Eur J Pharmacol 267(3):263–267. https://doi.org/10.1016/0922-4106(94)90149-x
doi: 10.1016/0922-4106(94)90149-x
pubmed: 7522180
Sorrenti V, Guccione S, Di Giacomo C, Modica MN, Pittala V, Acquaviva R, Basile L, Pappalardo M, Salerno L (2012) Evaluation of imidazole-based compounds as heme oxygenase-1 inhibitors. Chem Biol Drug Des 80(6):876–886. https://doi.org/10.1111/cbdd.12015
doi: 10.1111/cbdd.12015
pubmed: 22882835
Greish KF, Salerno L, Al Zahrani R, Amata E, Modica MN, Romeo G, Marrazzo A, Prezzavento O, Sorrenti V, Rescifina A, Floresta G, Intagliata S, Pittala V (2018) Novel structural insight into inhibitors of heme oxygenase-1 (HO-1) by new imidazole-based compounds: biochemical and in vitro anticancer activity evaluation. Molecules. https://doi.org/10.3390/molecules23051209
doi: 10.3390/molecules23051209
pubmed: 29783634
pmcid: 6099553
Floresta G, Amata E, Dichiara M, Marrazzo A, Salerno L, Romeo G, Prezzavento O, Pittala V, Rescifina A (2018) Identification of potentially potent heme oxygenase 1 inhibitors through 3D-QSAR coupled to scaffold-hopping analysis. ChemMedChem 13(13):1336–1342. https://doi.org/10.1002/cmdc.201800176
doi: 10.1002/cmdc.201800176
pubmed: 29693778
Floresta G, Pittala V, Sorrenti V, Romeo G, Salerno L, Rescifina A (2018) Development of new HO-1 inhibitors by a thorough scaffold-hopping analysis. Bioorg Chem 81:334–339. https://doi.org/10.1016/j.bioorg.2018.08.023
doi: 10.1016/j.bioorg.2018.08.023
pubmed: 30189413
Amata E, Marrazzo A, Dichiara M, Modica MN, Salerno L, Prezzavento O, Nastasi G, Rescifina A, Romeo G, Pittala V (2017) Heme oxygenase database (HemeOxDB) and QSAR analysis of Isoform 1 inhibitors. ChemMedChem 12(22):1873–1881. https://doi.org/10.1002/cmdc.201700321
doi: 10.1002/cmdc.201700321
pubmed: 28708269
Amata E, Marrazzo A, Dichiara M, Modica MN, Salerno L, Prezzavento O, Nastasi G, Rescifina A, Romeo G, Pittala V (2017) Comprehensive data on a 2D-QSAR model for heme oxygenase isoform 1 inhibitors. Data Brief 15:281–299. https://doi.org/10.1016/j.dib.2017.09.036
doi: 10.1016/j.dib.2017.09.036
pubmed: 29034293
pmcid: 5635207
Nastasi G, Miceli C, Pittala V, Modica MN, Prezzavento O, Romeo G, Rescifina A, Marrazzo A, Amata E (2017) S2RSLDB: a comprehensive manually curated, internet-accessible database of the sigma-2 receptor selective ligands. J Cheminform 9:3. https://doi.org/10.1186/s13321-017-0191-5
doi: 10.1186/s13321-017-0191-5
pubmed: 28123452
pmcid: 5250622
Salerno L, Amata E, Romeo G, Marrazzo A, Prezzavento O, Floresta G, Sorrenti V, Barbagallo I, Rescifina A, Pittala V (2018) Potholing of the hydrophobic heme oxygenase-1 western region for the search of potent and selective imidazole-based inhibitors. Eur J Med Chem 148:54–62. https://doi.org/10.1016/j.ejmech.2018.02.007
doi: 10.1016/j.ejmech.2018.02.007
pubmed: 29454190
Hum M, McLaughlin BE, Roman G, Vlahakis JZ, Szarek WA, Nakatsu K (2010) The effects of azole-based heme oxygenase inhibitors on rat cytochromes P450 2E1 and 3A1/2 and human cytochromes P450 3A4 and 2D6. J Pharmacol Exp Ther 334(3):981–987. https://doi.org/10.1124/jpet.110.168492
doi: 10.1124/jpet.110.168492
pubmed: 20501634
Roh JL, Jang H, Kim EH, Shin D (2017) Targeting of the glutathione, thioredoxin, and Nrf2 antioxidant systems in head and neck cancer. Antioxid Redox Signal 27(2):106–114. https://doi.org/10.1089/ars.2016.6841
doi: 10.1089/ars.2016.6841
pubmed: 27733046
Harris IS, Treloar AE, Inoue S, Sasaki M, Gorrini C, Lee KC, Yung KY, Brenner D, Knobbe-Thomsen CB, Cox MA, Elia A, Berger T, Cescon DW, Adeoye A, Brustle A, Molyneux SD, Mason JM, Li WY, Yamamoto K, Wakeham A, Berman HK, Khokha R, Done SJ, Kavanagh TJ, Lam CW, Mak TW (2015) Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell 27(2):211–222. https://doi.org/10.1016/j.ccell.2014.11.019
doi: 10.1016/j.ccell.2014.11.019
pubmed: 25620030
pmcid: 25620030
Korashy HM, Maayah ZH, Al Anazi FE, Alsaad AM, Alanazi IO, Belali OM, Al-Atawi FO, Alshamsan A (2017) Sunitinib inhibits breast cancer cell proliferation by inducing apoptosis, cell-cycle arrest and DNA repair while inhibiting NF-kappaB signaling pathways. Anticancer Res 37(9):4899–4909. https://doi.org/10.21873/anticanres.11899
doi: 10.21873/anticanres.11899
pubmed: 28870911
Furfaro AL, Piras S, Domenicotti C, Fenoglio D, De Luigi A, Salmona M, Moretta L, Marinari UM, Pronzato MA, Traverso N, Nitti M (2016) Role of Nrf2, HO-1 and GSH in neuroblastoma cell resistance to bortezomib. PLoS ONE 11(3):e0152465. https://doi.org/10.1371/journal.pone.0152465
doi: 10.1371/journal.pone.0152465
pubmed: 27023064
pmcid: 4811586
Nakamura H, Bai J, Nishinaka Y, Ueda S, Sasada T, Ohshio G, Imamura M, Takabayashi A, Yamaoka Y, Yodoi J (2000) Expression of thioredoxin and glutaredoxin, redox-regulating proteins, in pancreatic cancer. Cancer Detect Prev 24(1):53–60
pubmed: 10757123
Cha MK, Suh KH, Kim IH (2009) Overexpression of peroxiredoxin I and thioredoxin1 in human breast carcinoma. J Exp Clin Cancer Res CR 28:93. https://doi.org/10.1186/1756-9966-28-93
doi: 10.1186/1756-9966-28-93
pubmed: 19566940
Fath MA, Ahmad IM, Smith CJ, Spence J, Spitz DR (2011) Enhancement of carboplatin-mediated lung cancer cell killing by simultaneous disruption of glutathione and thioredoxin metabolism. Clin Cancer Res Off J Am Assoc Cancer Res 17(19):6206–6217. https://doi.org/10.1158/1078-0432.CCR-11-0736
doi: 10.1158/1078-0432.CCR-11-0736
Scarbrough PM, Mapuskar KA, Mattson DM, Gius D, Watson WH, Spitz DR (2012) Simultaneous inhibition of glutathione- and thioredoxin-dependent metabolism is necessary to potentiate 17AAG-induced cancer cell killing via oxidative stress. Free Radic Biol Med 52(2):436–443. https://doi.org/10.1016/j.freeradbiomed.2011.10.493
doi: 10.1016/j.freeradbiomed.2011.10.493
pubmed: 22100505
Saydam N, Kirb A, Demir O, Hazan E, Oto O, Saydam O, Guner G (1997) Determination of glutathione, glutathione reductase, glutathione peroxidase and glutathione S-transferase levels in human lung cancer tissues. Cancer Lett 119(1):13–19
doi: 10.1016/S0304-3835(97)00245-0
Hopkins J, Tudhope GR (1973) Glutathione peroxidase in human red cells in health and disease. Br J Haematol 25(5):563–575
doi: 10.1111/j.1365-2141.1973.tb01768.x
Doroshow JH, Akman S, Chu FF, Esworthy S (1990) Role of the glutathione–glutathione peroxidase cycle in the cytotoxicity of the anticancer quinones. Pharmacol Ther 47(3):359–370
doi: 10.1016/0163-7258(90)90062-7
Yamamoto T, Takano N, Ishiwata K, Ohmura M, Nagahata Y, Matsuura T, Kamata A, Sakamoto K, Nakanishi T, Kubo A, Hishiki T, Suematsu M (2014) Reduced methylation of PFKFB3 in cancer cells shunts glucose towards the pentose phosphate pathway. Nat Commun 5:3480. https://doi.org/10.1038/ncomms4480
doi: 10.1038/ncomms4480
pubmed: 24633012
pmcid: 3959213
He L, He T, Farrar S, Ji L, Liu T, Ma X (2017) Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 44(2):532–553. https://doi.org/10.1159/000485089
doi: 10.1159/000485089
Putnam CD, Arvai AS, Bourne Y, Tainer JA (2000) Active and inhibited human catalase structures: ligand and NADPH binding and catalytic mechanism. J Mol Biol 296(1):295–309. https://doi.org/10.1006/jmbi.1999.3458
doi: 10.1006/jmbi.1999.3458
pubmed: 10656833
Kinnula VL, Crapo JD (2003) Superoxide dismutases in the lung and human lung diseases. Am J Respir Crit Care Med 167(12):1600–1619. https://doi.org/10.1164/rccm.200212-1479SO
doi: 10.1164/rccm.200212-1479SO
pubmed: 12796054
Yoo DG, Song YJ, Cho EJ, Lee SK, Park JB, Yu JH, Lim SP, Kim JM, Jeon BH (2008) Alteration of APE1/ref-1 expression in non-small cell lung cancer: the implications of impaired extracellular superoxide dismutase and catalase antioxidant systems. Lung Cancer 60(2):277–284. https://doi.org/10.1016/j.lungcan.2007.10.015
doi: 10.1016/j.lungcan.2007.10.015
pubmed: 18061304
Malhotra JD, Kaufman RJ (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9(12):2277–2293. https://doi.org/10.1089/ars.2007.1782
doi: 10.1089/ars.2007.1782
pubmed: 17979528
Song S, Tan J, Miao Y, Zhang Q (2018) Crosstalk of ER stress-mediated autophagy and ER-phagy: involvement of UPR and the core autophagy machinery. J Cell Physiol 233(5):3867–3874. https://doi.org/10.1002/jcp.26137
doi: 10.1002/jcp.26137
pubmed: 28777470
Alasiri G, Fan LY, Zona S, Goldsbrough IG, Ke HL, Auner HW, Lam EW (2018) ER stress and cancer: the FOXO forkhead transcription factor link. Mol Cell Endocrinol 462(Pt B):67–81. https://doi.org/10.1016/j.mce.2017.05.027
doi: 10.1016/j.mce.2017.05.027
pubmed: 28572047
Li Y, Guo Y, Tang J, Jiang J, Chen Z (2014) New insights into the roles of CHOP-induced apoptosis in ER stress. Acta Biochim Biophys Sin 46(8):629–640. https://doi.org/10.1093/abbs/gmu048
doi: 10.1093/abbs/gmu048
pubmed: 25016584