Gaseous Signaling Molecules and Their Application in Resistant Cancer Treatment: From Invisible to Visible

References

• Mayur YC Peters GJ Prasad VV Lemo C Sathish NK . Design of new drug molecules to be used in reversing multidrug resistance in cancer cells . Curr. Cancer Drug Targets9 ( 3 ), 298 – 306 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Krishna R Mayer LD . Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs . Eur. J. Pharm. Sci.11 ( 4 ), 265 – 283 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Palmeira A Sousa E Vasconcelos MH Pinto MM . Three decades of P-gp inhibitors: skimming through several generations and scaffolds . Curr. Med. Chem.19 ( 13 ), 1946 – 2025 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Falasca M Linton KJ . Investigational ABC transporter inhibitors . Expert Opin. Investig. Drugs21 ( 5 ), 657 – 666 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Yuan TZ Zhang HH Lin XL et al. MicroRNA-125b reverses the multidrug resistance of nasopharyngeal carcinoma cells via targeting of Bcl-2 . Mol. Med. Rep.15 ( 4 ), 2223 – 2228 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• An X Sarmiento C Tan T Zhu H . Regulation of multidrug resistance by microRNAs in anti-cancer therapy . Acta Pharm. Sin. B7 ( 1 ), 38 – 51 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• He M Wei MJ . Reversing multidrug resistance by tyrosine kinase inhibitors . Chin. J. Cancer31 ( 3 ), 126 – 133 ( 2012 ).
   PubMedGoogle Scholar
• Li W Zhang H Assaraf YG et al. Overcoming ABC transporter-mediated multidrug resistance: molecular mechanisms and novel therapeutic drug strategies . Drug Resist. Updat.27 , 14 – 29 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Fan YF Zhang W Zeng L et al. Dacomitinib antagonizes multidrug resistance (MDR) in cancer cells by inhibiting the efflux activity of ABCB1 and ABCG2 transporters . Cancer Lett.421 , 186 – 198 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Rogan AM Hamilton TC Young RC Klecker RJ Ozols RF . Reversal of adriamycin resistance by verapamil in human ovarian cancer . Science224 ( 4652 ), 994 – 996 ( 1984 ).
   PubMed Web of Science ®Google Scholar
• Ferreira RJ Baptista R Moreno A et al. Optimizing the flavanone core toward new selective nitrogen-containing modulators of ABC transporters . Future Med. Chem.10 ( 7 ), 725 – 741 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Baptista R Ferreira RJ Dos SD Fernandes MX Ferreira MJ . Optimizing the macrocyclic diterpenic core toward the reversal of multidrug resistance in cancer . Future Med. Chem.8 ( 6 ), 629 – 645 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Kathawala RJ Gupta P Ashby CJ Chen ZS . The modulation of ABC transporter-mediated multidrug resistance in cancer: a review of the past decade . Drug Resist. Updat.18 , 1 – 17 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Shukla S Chen ZS Ambudkar SV . Tyrosine kinase inhibitors as modulators of ABC transporter-mediated drug resistance . Drug Resist. Updat.15 ( 1–2 ), 70 – 80 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Shen F Bailey BJ Chu S et al. Dynamic assessment of mitoxantrone resistance and modulation of multidrug resistance by valspodar (PSC833) in multidrug resistance human cancer cells . J. Pharmacol. Exp. Ther.330 ( 2 ), 423 – 429 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Korde CS Sridharan G Gadbail A Poornima V . Nitric oxide and oral cancer: a review . Oral Oncol.48 ( 6 ), 475 – 483 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• De Bels D Corazza F Germonpre P Balestra C . The normobaric oxygen paradox: a novel way to administer oxygen as an adjuvant treatment for cancer?Med. Hypotheses.76 ( 4 ), 467 – 470 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Hellmich MR Szabo C . Hydrogen sulfide and cancer . Handb. Exp. Pharmacol.230 , 233 – 241 ( 2015 ).
   PubMedGoogle Scholar
• Vitek L Gbelcova H Muchova L et al. Antiproliferative effects of carbon monoxide on pancreatic cancer . Dig. Liver Dis.46 ( 4 ), 369 – 375 ( 2014 ).
   PubMedGoogle Scholar
• Oliveira C Benfeito S Fernandes C Cagide F Silva T Borges F . NO and HNO donors, nitrones, and nitroxides: past, present, and future . Med. Res. Rev.38 ( 4 ), 1159 – 1187 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Ohta S . Recent progress toward hydrogen medicine: potential of molecular hydrogen for preventive and therapeutic applications . Curr. Pharm. Des.17 ( 22 ), 2241 – 2252 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Choudhari SK Chaudhary M Bagde S Gadbail AR Joshi V . Nitric oxide and cancer: a review . World J. Surg. Oncol.11 , 118 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Teas J Cunningham JE Cone L et al. Can hyperbaric oxygen therapy reduce breast cancer treatment-related lymphedema? A pilot study . J. Womens Health (Larchmt.)13 ( 9 ), 1008 – 1018 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Flannigan KL Wallace JL . Hydrogen sulfide-based anti-inflammatory and chemopreventive therapies: an experimental approach . Curr. Pharm. Des.21 ( 21 ), 3012 – 3022 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Wang R . Gasotransmitters: growing pains and joys . Trends Biochem. Sci.39 ( 5 ), 227 – 232 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Mustafa AK Gadalla MM Snyder SH . Signaling by gasotransmitters . Sci. Signal.2 ( 68 ), e2 ( 2009 ).
   Web of Science ®Google Scholar
• Chinta KC Saini V Glasgow JN et al. The emerging role of gasotransmitters in the pathogenesis of tuberculosis . Nitric Oxide59 , 28 – 41 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Dallas ML . Gaseous regulation of Ca2+ homeostasis; for better or worse?J. Physiol.594 ( 15 ), 4117 – 4118 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Chen J Shangguan ZP Zheng HL . The function of hydrogen sulphide in iron availability: sulfur nutrient or signaling molecule?Plant Signal. Behav.11 ( 6 ), e1132967 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Iijima M Gombodorj N Tachibana Y et al. Development of single nanometer-sized ultrafine oxygen bubbles to overcome the hypoxia-induced resistance to radiation therapy via the suppression of hypoxia-inducible factor 1 alpha . Int. J. Oncol.52 ( 3 ), 679 – 686 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Reynolds MM Witzeling SD Damodaran VB et al. Applications for nitric oxide in halting proliferation of tumor cells . Biochem. Biophys. Res. Commun.431 ( 4 ), 647 – 651 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Shao L Gu YY Jiang CH et al. Carbon monoxide releasing molecule-2 suppresses proliferation, migration, invasion, and promotes apoptosis in non-small cell lung cancer Calu-3 cells . Eur. Rev. Med. Pharmacol. Sci.22 ( 7 ), 1948 – 1957 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Jones RG Thompson CB . Tumor suppressors and cell metabolism: a recipe for cancer growth . Genes Dev.23 ( 5 ), 537 – 548 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Yttersian SK Tveitaras MK Lu N et al. Oxygen-dependent regulation of tumor growth and metastasis in human breast cancer xenografts . PLoS ONE12 ( 8 ), e183254 ( 2017 ).
   Web of Science ®Google Scholar
• Vaupel P Kelleher DK Hockel M . Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy . Semin. Oncol.28 ( 2; Suppl. 8 ), 29 – 35 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Hockel M Vaupel P . Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects . J. Natl Cancer Inst.93 ( 4 ), 266 – 276 ( 2001 ).
   PubMedGoogle Scholar
• Carmeliet P Dor Y Herbert JM et al. Role of HIF-1 alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis . Nature394 ( 6692 ), 485 – 490 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Talks KL Turley H Gatter KC et al. The expression and distribution of the hypoxia-inducible factors HIF-1 alpha and HIF-2 alpha in normal human tissues, cancers, and tumor-associated macrophages . Am. J. Pathol.157 ( 2 ), 411 – 421 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Fukuda K Hibiya Y Mutoh M Koshiji M Akao S Fujiwara H . Inhibition of activator protein 1 activity by berberine in human hepatoma cells . Planta Med.65 ( 4 ), 381 – 383 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Xu L Wang X Wang J et al. Hypoxia-induced secretion of IL-10 from adipose-derived mesenchymal stem cell promotes growth and cancer stem cell properties of Burkitt lymphoma . Tumour Biol.37 ( 6 ), 7835 – 7842 ( 2016 ).
   PubMedGoogle Scholar
• Wartenberg M Ling FC Muschen M et al. Regulation of the multidrug resistance transporter P-glycoprotein in multicellular tumor spheroids by hypoxia-inducible factor (HIF-1) and reactive oxygen species . FASEB J.17 ( 3 ), 503 – 505 ( 2003 ).
   PubMedGoogle Scholar
• Xie G Liu Y Yao Q et al. Hypoxia-induced angiotensin II by the lactate-chymase-dependent mechanism mediates radioresistance of hypoxic tumor cells . Sci. Rep.7 , 42396 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Bahr O Wick W Weller M . Modulation of MDR/MRP by wild-type and mutant p53 . J. Clin. Invest.107 ( 5 ), 643 – 646 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Teicher BA Lazo JS Sartorelli AC . Classification of antineoplastic agents by their selective toxicities toward oxygenated and hypoxic tumor cells . Cancer Res.41 ( 1 ), 73 – 81 ( 1981 ).
   PubMed Web of Science ®Google Scholar
• Wada Y Hirose K Harada T et al. Impact of oxygen status on 10B-BPA uptake into human glioblastoma cells, referring to significance in boron neutron capture therapy . J. Radiat. Res.59 ( 2 ), 122 – 128 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Zitta K Meybohm P Bein B et al. Salicylic acid induces apoptosis in colon carcinoma cells grown in-vitro: influence of oxygen and salicylic acid concentration . Exp. Cell Res.318 ( 7 ), 828 – 834 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Pinzon-Daza ML Cuellar-Saenz Y Nualart F et al. Oxidative stress promotes doxorubicin-induced Pgp and BCRP expression in colon cancer cells under hypoxic conditions . J. Cell. Biochem.118 ( 7 ), 1868 – 1878 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Li W Li J Wang R Xie H Jia Z . MDR1 will play a key role in pharmacokinetic changes under hypoxia at high altitude and its potential regulatory networks . Drug Metab. Rev.47 ( 2 ), 191 – 198 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Fetsch PA Abati A Litman T et al. Localization of the ABCG2 mitoxantrone resistance-associated protein in normal tissues . Cancer Lett.235 ( 1 ), 84 – 92 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Krishnamurthy P Ross DD Nakanishi T et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme . J. Biol. Chem.279 ( 23 ), 24218 – 24225 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Wilson WR Hay MP . Targeting hypoxia in cancer therapy . Nat. Rev. Cancer11 ( 6 ), 393 – 410 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Huang L Boling W Zhang JH . Hyperbaric oxygen therapy as adjunctive strategy in treatment of glioblastoma multiforme . Med. Gas Res.8 ( 1 ), 24 – 28 ( 2018 ).
   PubMedGoogle Scholar
• Eisenbrey JR Shraim R Liu JB et al. Sensitization of hypoxic tumors to radiation therapy using ultrasound-sensitive oxygen microbubbles . Int. J. Radiat. Oncol. Biol. Phys.101 ( 1 ), 88 – 96 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Chen J Luo H Liu Y et al. Oxygen-self-produced nanoplatform for relieving hypoxia and breaking resistance to sonodynamic treatment of pancreatic cancer . ACS Nano11 ( 12 ), 12849 – 12862 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Li F Mei H Gao Y et al. Co-delivery of oxygen and erlotinib by aptamer-modified liposomal complexes to reverse hypoxia-induced drug resistance in lung cancer . Biomaterials145 , 56 – 71 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Mungrue IN Bredt DS Stewart DJ Husain M . From molecules to mammals: what's NOS got to do with it?Acta Physiol. Scand.179 ( 2 ), 123 – 135 ( 2003 ).
   PubMedGoogle Scholar
• Knowles RG Moncada S . Nitric oxide synthases in mammals . Biochem. J.298 ( Pt 2 ), 249 – 258 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Yang L Wang Y Guo L Wang L Chen W Shi B . The expression and correlation of iNOS and p53 in oral squamous cell carcinoma . Biomed. Res. Int.2015 , 637853 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Yang M Li H Li Y Ruan Y Quan C . Identification of genes and pathways associated with MDR in MCF-7/MDR breast cancer cells by RNA-seq analysis . Mol. Med. Rep.17 ( 5 ), 6211 – 6226 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Yu S Jia L Zhang Y et al. Increased expression of activated endothelial nitric oxide synthase contributes to antiandrogen resistance in prostate cancer cells by suppressing androgen receptor transactivation . Cancer Lett.328 ( 1 ), 83 – 94 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Matsunaga T Yamaji Y Tomokuni T et al. Nitric oxide confers cisplatin resistance in human lung cancer cells through upregulation of aldo-keto reductase 1B10 and proteasome . Free Radic. Res.48 ( 11 ), 1371 – 1385 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Li Y Ma C Shi X et al. Effect of nitric oxide synthase on multiple drug resistance is related to Wnt signaling in non-small cell lung cancer . Oncol. Rep.32 ( 4 ), 1703 – 1708 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Wang J Hussain SP . NO* and pancreatic cancer: a complex interaction with therapeutic potential . Antioxid. Redox Signal.26 ( 17 ), 1000 – 1008 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Tran AN Boyd NH Walker K Hjelmeland AB . NOS expression and NO function in glioma and implications for patient therapies . Antioxid. Redox Signal.26 ( 17 ), 986 – 999 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Walsh EM Keane MM Wink DA Callagy G Glynn SA . Review of triple negative breast cancer and the impact of inducible nitric oxide synthase on tumor biology and patient outcomes . Crit. Rev. Oncog.21 ( 5–6 ), 333 – 351 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Kumar A Ehrenshaft M Tokar EJ Mason RP Sinha BK . Nitric oxide inhibits topoisomerase II activity and induces resistance to topoisomerase II-poisons in human tumor cells . Biochim. Biophys. Acta1860 ( 7 ), 1519 – 1527 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Sharma NK Kumar A Kumari A et al. Nitric oxide down-regulates topoisomerase I and induces camptothecin resistance in human breast MCF-7 tumor cells . PLoS ONE10 ( 11 ), e141897 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Chanvorachote P Pongrakhananon V Chunhacha P . Prolonged nitric oxide exposure enhances anoikis resistance and migration through epithelial-mesenchymal transition and caveolin-1 upregulation . Biomed. Res. Int.2014 , 941359 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Sinha BK Kumar A Bhattacharjee S Espey MG Mason RP . Effect of nitric oxide on the anticancer activity of the topoisomerase-active drugs etoposide and adriamycin in human melanoma cells . J. Pharmacol. Exp. Ther.347 ( 3 ), 607 – 614 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Huang Z Fu J Zhang Y . Nitric oxide donor-based cancer therapy: advances and prospects . J. Med. Chem.60 ( 18 ), 7617 – 7635 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Davila-Gonzalez D Choi DS Rosato RR et al. Pharmacological inhibition of NOS activates ASK1/JNK pathway augmenting docetaxel-mediated apoptosis in triple-negative breast cancer . Clin. Cancer Res.24 ( 5 ), 1152 – 1162 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Fahey JM Stancill JS Smith BC Girotti AW . Nitric oxide antagonism to glioblastoma photodynamic therapy and mitigation thereof by BET bromodomain inhibitor JQ1 . J. Biol. Chem.293 ( 14 ), 5345 – 5359 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Fahey JM Girotti AW . Nitric oxide-mediated resistance to photodynamic therapy in a human breast tumor xenograft model: improved outcome with NOS2 inhibitors . Nitric Oxide62 , 52 – 61 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Yin M Tan S Bao Y Zhang Z . Enhanced tumor therapy via drug co-delivery and in situ vascular-promoting strategy . J. Control. Release258 , 108 – 120 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Ojeda PG Wang CK Craik DJ . Chlorotoxin: structure, activity, and potential uses in cancer therapy . Biopolymers106 ( 1 ), 25 – 36 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Wiranowska M Colina LO Johnson JO . Clathrin-mediated entry and cellular localization of chlorotoxin in human glioma . Cancer Cell Int.11 , 27 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Safdar S Payne CA Tu NH Taite LJ . Targeted nitric oxide delivery preferentially induces glioma cell chemosensitivity via altered p53 and O(6) -methylguanine-DNA methyltransferase activity . Biotechnol. Bioeng.110 ( 4 ), 1211 – 1220 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Oronsky B Scicinski J Ning S et al. Rockets, radiosensitizers, and RRx-001: an origin story part I . Discov. Med.21 ( 115 ), 173 – 180 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Oronsky B Scicinski J Ning S et al. RRx-001, a novel dinitroazetidine radiosensitizer . Invest. New Drugs34 ( 3 ), 371 – 377 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Scicinski J Fisher G Carter C et al. The development Of RRx-001, a novel nitric-oxide-mediated epigenetically active anticancer agent . Redox Biol.5 , 422 ( 2015 ).
   PubMedGoogle Scholar
• Brzezniak C Oronsky B Aggarwal R . A complete metabolic response of metastatic castration-resistant neuroendocrine carcinoma of the prostate after treatment with RRx-001 and reintroduced platinum doublets . Eur. Urol.73 ( 2 ), 306 – 307 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Cottrill H Cason S Caroen S Oronsky B Donaldson E . A recurrent platinum refractory ovarian cancer patient with a partial response after RRx-001 resensitization to platinum doublet . J. Investig. Med. High Impact Case Rep.6 , 1559742064 ( 2018 ).
   Google Scholar
• Oronsky B Paulmurugan R Foygel K et al. RRx-001: a systemically non-toxic M2-to-M1 macrophage stimulating and prosensitizing agent in Phase II clinical trials . Expert Opin. Investig. Drugs26 ( 1 ), 109 – 119 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Brzezniak C Oronsky B Scicinski J et al. Conversion of platinum-etoposide-resistant to sensitive SCLC after treatment with the Epi-Immunotherapeutic RRx-001: a case report . Oncol. Res. Treat.39 ( 11 ), 720 – 723 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Oronsky B Caroen S Zeman K et al. A partial response to reintroduced chemotherapy in a resistant small cell lung cancer patient after priming with RRx-001 . Clin. Med. Insights Oncol.10 , 105 – 108 ( 2016 ).
   PubMedGoogle Scholar
• Weyerbrock A Osterberg N Psarras N et al. JS-K, a glutathione S-transferase-activated nitric oxide donor with antineoplastic activity in malignant gliomas . Neurosurgery70 ( 2 ), 497 – 510 , 510 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Kiziltepe T Anderson KC Kutok JL et al. JS-K has potent anti-angiogenic activity in vitro and inhibits tumour angiogenesis in a multiple myeloma model in vivo . J. Pharm. Pharmacol.62 ( 1 ), 145 – 151 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Simeone AM McMurtry V Nieves-Alicea R et al. TIMP-2 mediates the anti-invasive effects of the nitric oxide-releasing prodrug JS-K in breast cancer cells . Breast Cancer Res.10 ( 3 ), R44 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Qiu M Chen L Tan G et al. A reactive oxygen species activation mechanism contributes to JS-K-induced apoptosis in human bladder cancer cells . Sci. Rep.5 , 15104 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Maciag AE Chakrapani H Saavedra JE et al. The nitric oxide prodrug JS-K is effective against non-small-cell lung cancer cells in vitro and in vivo: involvement of reactive oxygen species . J. Pharmacol. Exp. Ther.336 ( 2 ), 313 – 320 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Kiziltepe T Hideshima T Ishitsuka K et al. JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells . Blood110 ( 2 ), 709 – 718 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Qiu M Ke L Zhang S Zeng X Fang Z Liu J . JS-K, a GST-activated nitric oxide donor prodrug, enhances chemo-sensitivity in renal carcinoma cells and prevents cardiac myocytes toxicity induced by Doxorubicin . Cancer Chemother. Pharmacol.80 ( 2 ), 275 – 286 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Heckler M Osterberg N Guenzle J et al. The nitric oxide donor JS-K sensitizes U87 glioma cells to repetitive irradiation . Tumour Biol.39 ( 6 ), 1393385742 ( 2017 ).
   Google Scholar
• Shami PJ Maciag AE Eddington JK et al. JS-K, an arylating nitric oxide (NO) donor, has synergistic anti-leukemic activity with cytarabine (ARA-C) . Leuk. Res.33 ( 11 ), 1525 – 1529 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Liu J Li C Qu W et al. Nitric oxide prodrugs and metallochemotherapeutics: JS-K and CB-3-100 enhance arsenic and cisplatin cytolethality by increasing cellular accumulation . Mol. Cancer Ther.3 ( 6 ), 709 – 714 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Kang F Ai Y Zhang Y Huang Z . Design and synthesis of new hybrids from 2-cyano-3,12-dioxooleana- 9-dien-28-oic acid and O(2)-(2,4-dinitrophenyl) diazeniumdiolate for intervention of drug-resistant lung cancer . Eur. J. Med. Chem.149 , 269 – 280 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Li Q Zou P Sun J Chen L . O(2)-(2,4-dinitrophenyl)diazeniumdiolates derivatives: design, synthesis, cytotoxic evaluation and reversing MDR in MCF-7/ADR cells . Eur. J. Med. Chem.143 , 732 – 744 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Kogias E Osterberg N Baumer B et al. Growth-inhibitory and chemosensitizing effects of the glutathione-S-transferase-pi-activated nitric oxide donor PABA/NO in malignant gliomas . Int. J. Cancer130 ( 5 ), 1184 – 1194 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Ren Z Gu X Lu B et al. Anticancer efficacy of a nitric oxide-modified derivative of bifendate against multidrug-resistant cancer cells . J. Cell Mol. Med.20 ( 6 ), 1095 – 1105 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Guo Y Wang Y Li H et al. Novel nitric oxide donors of phenylsulfonylfuroxan and 3-benzyl coumarin derivatives as potent antitumor agents . ACS Med. Chem. Lett.9 ( 5 ), 502 – 506 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Rajendra PV Deepak RG Kathmann I Amareswararao M Peters GJ . Nitric oxide releasing acridone carboxamide derivatives as reverters of doxorubicin resistance in MCF7/Dx cancer cells . Bioorg. Chem.64 , 51 – 58 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Rapozzi V Della PE Bonavida B . Dual roles of nitric oxide in the regulation of tumor cell response and resistance to photodynamic therapy . Redox Biol.6 , 311 – 317 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Bonavida B Baritaki S . Inhibition of epithelial-to-mesenchymal transition (EMT) in cancer by nitric oxide: pivotal roles of nitrosylation of NF-kappaB, YY1 and Snail . For. Immunopathol. Dis. Therap.3 ( 2 ), 125 – 133 ( 2012 ).
   PubMedGoogle Scholar
• Bonavida B Baritaki S . Dual role of NO donors in the reversal of tumor cell resistance and EMT: downregulation of the NF-kappaB/Snail/YY1/RKIP circuitry . Nitric Oxide24 ( 1 ), 1 – 7 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Nagai H Yasuda H Hatachi Y et al. Nitric oxide (NO) enhances pemetrexed cytotoxicity via NOcGMP signaling in lung adenocarcinoma cells in vitro and in vivo . Int. J. Oncol.41 ( 1 ), 24 – 30 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Frederiksen LJ Sullivan R Maxwell LR et al. Chemosensitization of cancer in vitro and in vivo by nitric oxide signaling . Clin. Cancer Res.13 ( 7 ), 2199 – 2206 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Muir CP Adams MA Graham CH . Nitric oxide attenuates resistance to doxorubicin in three-dimensional aggregates of human breast carcinoma cells . Breast Cancer Res. Treat.96 ( 2 ), 169 – 176 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Maksimovic-Ivanic D Mijatovic S Miljkovic D et al. The antitumor properties of a nontoxic, nitric oxide-modified version of saquinavir are independent of Akt . Mol. Cancer Ther.8 ( 5 ), 1169 – 1178 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Rothweiler F Michaelis M Brauer P et al. Anticancer effects of the nitric oxide-modified saquinavir derivative saquinavir-NO against multidrug-resistant cancer cells . Neoplasia12 ( 12 ), 1023 – 1030 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Donia M Maksimovic-Ivanic D Mijatovic S et al. In vitro and in vivo anticancer action of Saquinavir-NO, a novel nitric oxide-derivative of the protease inhibitor saquinavir, on hormone resistant prostate cancer cells . Cell Cycle10 ( 3 ), 492 – 499 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Stewart GD Nanda J Brown DJ Riddick AC Ross JA Habib FK . NO-sulindac inhibits the hypoxia response of PC-3 prostate cancer cells via the Akt signalling pathway . Int. J. Cancer124 ( 1 ), 223 – 232 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Bratasz A Selvendiran K Wasowicz T et al. NCX-4040, a nitric oxide-releasing aspirin, sensitizes drug-resistant human ovarian xenograft tumors to cisplatin by depletion of cellular thiols . J. Transl. Med.6 , 9 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Gazzano E Chegaev K Rolando B et al. Overcoming multidrug resistance by targeting mitochondria with NO-donating doxorubicins . Bioorg. Med. Chem.24 ( 5 ), 967 – 975 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Pedrini I Gazzano E Chegaev K et al. Liposomal nitrooxy-doxorubicin: one step over caelyx in drug-resistant human cancer cells . Mol. Pharm.11 ( 9 ), 3068 – 3079 ( 2014 ).
   PubMedGoogle Scholar
• Gazzano E Rolando B Chegaev K et al. Folate-targeted liposomal nitrooxy-doxorubicin: an effective tool against P-glycoprotein-positive and folate receptor-positive tumors . J. Control. Release270 , 37 – 52 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Riganti C Rolando B Kopecka J et al. Mitochondrial-targeting nitrooxy-doxorubicin: a new approach to overcome drug resistance . Mol. Pharm.10 ( 1 ), 161 – 174 ( 2013 ).
   PubMedGoogle Scholar
• Chegaev K Fraix A Gazzano E et al. Light-regulated NO release as a novel strategy to overcome doxorubicin multidrug resistance . ACS Med. Chem. Lett.8 ( 3 ), 361 – 365 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Kilburn KH Thrasher JD Gray MR . Low-level hydrogen sulfide and central nervous system dysfunction . Toxicol. Ind. Health26 ( 7 ), 387 – 405 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Lee ZW Deng LW . Role of H2S donors in cancer biology . Handb. Exp. Pharmacol.230 , 243 – 265 ( 2015 ).
   PubMedGoogle Scholar
• Wu D Si W Wang M Lv S Ji A Li Y . Hydrogen sulfide in cancer: friend or foe?Nitric Oxide50 , 38 – 45 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Zhen Y Pan W Hu F et al. Exogenous hydrogen sulfide exerts proliferation/anti-apoptosis/angiogenesis/migration effects via amplifying the activation of NF-kappaB pathway in PLC/PRF/5 hepatoma cells . Int. J. Oncol.46 ( 5 ), 2194 – 2204 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Yang CT Chen L Xu S Day JJ Li X Xian M . Recent development of hydrogen sulfide releasing/stimulating reagents and their potential applications in cancer and glycometabolic disorders . Front. Pharmacol.8 , 664 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Untereiner AA Pavlidou A Druzhyna N Papapetropoulos A Hellmich MR Szabo C . Drug resistance induces the upregulation of H2S-producing enzymes in HCT116 colon cancer cells . Biochem. Pharmacol.149 , 174 – 185 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Untereiner AA Olah G Modis K Hellmich MR Szabo C . H2S-induced S-sulfhydration of lactate dehydrogenase a (LDHA) stimulates cellular bioenergetics in HCT116 colon cancer cells . Biochem. Pharmacol.136 , 86 – 98 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Hellmich MR Szabo C . Hydrogen sulfide and cancer . Handb. Exp. Pharmacol.230 , 233 – 241 ( 2015 ).
   PubMedGoogle Scholar
• Szabo C Coletta C Chao C et al. Tumor-derived hydrogen sulfide, produced by cystathionine-beta-synthase, stimulates bioenergetics, cell proliferation, and angiogenesis in colon cancer . Proc. Natl Acad. Sci. USA110 ( 30 ), 12474 – 12479 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Ma Y Yan Z Deng X et al. Anticancer effect of exogenous hydrogen sulfide in cisplatinresistant A549/DDP cells . Oncol. Rep.39 ( 6 ), 2969 – 2977 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Zhao H Zhu W Jia L et al. Phase I study of topical epigallocatechin-3-gallate (EGCG) in patients with breast cancer receiving adjuvant radiotherapy . Br. J. Radiol.89 ( 1058 ), 20150665 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Bae J Kumazoe M Yamashita S Tachibana H . Hydrogen sulphide donors selectively potentiate a green tea polyphenol EGCG-induced apoptosis of multiple myeloma cells . Sci. Rep.7 ( 1 ), 6665 ( 2017 ).
   PubMedGoogle Scholar
• Frantzias J Logan JG Mollat P et al. Hydrogen sulphide-releasing diclofenac derivatives inhibit breast cancer-induced osteoclastogenesis in vitro and prevent osteolysis ex vivo . Br. J. Pharmacol.165 ( 6 ), 1914 – 1925 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Chegaev K Rolando B Cortese D et al. H2S-donating doxorubicins may overcome cardiotoxicity and multidrug resistance . J. Med. Chem.59 ( 10 ), 4881 – 4889 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Bigagli E Luceri C De Angioletti M et al. New NO- and H2S-releasing doxorubicins as targeted therapy against chemoresistance in castration-resistant prostate cancer: in vitro and in vivo evaluations . Invest. New Drug36 ( 6 ), 985 – 998 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Vaupel P Thews O Hoeckel M . Treatment resistance of solid tumors: role of hypoxia and anemia . Med. Oncol.18 ( 4 ), 243 – 259 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Maines MD Abrahamsson PA . Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution . Urology47 ( 5 ), 727 – 733 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Loboda A Jozkowicz A Dulak J . HO-1/CO system in tumor growth, angiogenesis and metabolism – targeting HO-1 as an anti-tumor therapy . Vascul. Pharmacol.74 , 11 – 22 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Otterbein LE Hedblom A Harris C Csizmadia E Gallo D Wegiel B . Heme oxygenase-1 and carbon monoxide modulate DNA repair through ataxia-telangiectasia mutated (ATM) protein . Proc. Natl Acad. Sci. USA108 ( 35 ), 14491 – 14496 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Wegiel B Gallo D Csizmadia E et al. Carbon monoxide expedites metabolic exhaustion to inhibit tumor growth . Cancer Res.73 ( 23 ), 7009 – 7021 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Cascone T McKenzie JA Mbofung RM et al. Increased tumor glycolysis characterizes immune resistance to adoptive T cell therapy . Cell Metab.27 ( 5 ), 977 – 987 ( 2018 ).
   PubMed Web of Science ®Google Scholar
• Cui Q Wen S Huang P . Targeting cancer cell mitochondria as a therapeutic approach: recent updates . Future Med. Chem.9 ( 9 ), 929 – 949 ( 2017 ).
   PubMed Web of Science ®Google Scholar
• Zheng DW Li B Li CX et al. Photocatalyzing CO2 to CO for enhanced cancer therapy . Adv. Mater.29 ( 44 ), e1703822 ( 2017 ).
   Web of Science ®Google Scholar
• Bhattacharyya S Saha S Giri K et al. Cystathionine beta-synthase (CBS) contributes to advanced ovarian cancer progression and drug resistance . PLoS ONE8 ( 11 ), e79167 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Sen S Kawahara B Gupta D et al. Role of cystathionine beta-synthase in human breast cancer . Free Radic. Biol. Med.86 , 228 – 238 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Puranik M Weeks CL Lahaye D et al. Dynamics of carbon monoxide binding to cystathionine beta-synthase . J. Biol. Chem.281 ( 19 ), 13433 – 13438 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Yamamoto T Takano N Ishiwata K et al. Reduced methylation of PFKFB3 in cancer cells shunts glucose towards the pentose phosphate pathway . Nat. Commun.5 , 3480 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Al-Owais MM Scragg JL Dallas ML et al. Carbon monoxide mediates the anti-apoptotic effects of heme oxygenase-1 in medulloblastoma DAOY cells via K+ channel inhibition . J. Biol. Chem.287 ( 29 ), 24754 – 24764 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Bonnet S Archer SL Allalunis-Turner J et al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth . Cancer Cell11 ( 1 ), 37 – 51 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Kashfi K Chattopadhyay M Kodela R . NOS H-sulindac (AV T-18A) is a novel nitric oxide- and hydrogen sulfide-releasing hybrid that is gastrointestinal safe and has potent anti-inflammatory, analgesic, antipyretic, anti-platelet, and anti-cancer properties . Redox Biol.6 , 287 – 296 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Chattopadhyay M Kodela R Olson KR Kashfi K . NOS H-aspirin (NB S-1120), a novel nitric oxide- and hydrogen sulfide-releasing hybrid is a potent inhibitor of colon cancer cell growth in vitro and in a xenograft mouse model . Biochem. Biophys. Res. Commun.419 ( 3 ), 523 – 528 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Verma R Akhtar Y Singh S . A review of patents on therapeutic potential and delivery of hydrogen sulfide . Recent Pat. Drug Deliv. Formul.11 ( 2 ), 114 – 123 ( 2017 ).
   PubMedGoogle Scholar
• Yang CT Chen L Xu S Day JJ Li X Xian M . Recent development of hydrogen sulfide releasing/stimulating reagents and their potential applications in cancer and glycometabolic disorders . Front. Pharmacol.8 , 664 ( 2017 ).
   PubMed Web of Science ®Google Scholar