Nitric oxide (NO) enhances pemetrexed cytotoxicity via NO-cGMP signaling in lung adenocarcinoma cells in vitro and in vivo

International Journal of Oncology

Volumn 41, Issue 1, 2012, Pages 24-30

  Nagai, Hiroki ^a   Yasuda, Hiroyasu ^b,c   Hatachi, Yukimasa ^a   Xue, Deng ^b   Sasaki, Takahiko ^d   Yamaya, Mutsuo ^d   Sakamori, Yuichi ^a   Togashi, Yousuke ^a   Masago, Katsuhiro ^a   Ito, Isao ^a   Kim, Young Hak ^a   Mio, Tadashi ^a   Mishima, Michiaki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c Sendai Advanced Medical Research Institute   (Japan)

^d TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cyclic guanosine monophosphate; Hypoxia; Nitric oxide; Nitroglycerin; Pemetrexed

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; 8 BROMO CYCLIC GMP; CYCLIC GMP; FOLYLPOLYGLUTAMATE SYNTHASE; GAMMA GLUTAMYL HYDROLASE; GLYCERYL TRINITRATE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 5; NITRIC OXIDE; NITRIC OXIDE DONOR; PEMETREXED; REDUCED FOLATE CARRIER; RNA 18S; SODIUM CHLORIDE; THYMIDYLATE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CARCINOMA CELL; CELL ASSAY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG METABOLISM; DRUG SENSITIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEWIS CARCINOMA; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TREATMENT DURATION; TREATMENT OUTCOME; TUMOR GROWTH; TUMOR VOLUME;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMATES; GUANINE; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED C57BL; NITRIC OXIDE DONORS; NITROGLYCERIN; NITROSO COMPOUNDS; PEPTIDE SYNTHASES; REPLICATION PROTEIN C; SECOND MESSENGER SYSTEMS; TUMOR BURDEN;

EID: 84862835071     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1461     Document Type: Article

References (45)

1. National Comprehensive Cancer Network: NCCN Clinical Practice Guidelines in Oncology: Non-Small Cell Lung Cancer, 2011.
2. Schiller JH, Harrington D, Belani CP, et al: Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 346: 92-98, 2002. (Pubitemid 34438899)
3. Scagliotti GV, Parikh P, von Pawel J, et al: Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 26: 3543-3551, 2008.
4. Brown JM and Giaccia AJ: The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res 58: 1408-1416, 1998. (Pubitemid 28193601)
5. Grunt TW, Lametschwandtner A and Staindl O: The vascular pattern of basal cell tumors: light microscopy and scanning electron microscopic study on vascular corrosion casts. Microvasc Res 29: 371-386, 1985. (Pubitemid 16158231)
6. Dewhirst MW, Tso CY, Oliver R, Gustafson CS, Secomb TW and Gross JF: Morphologic and hemodynamic comparison of tumor and healing normal tissue microvasculature. Int J Radiat Oncol Biol Phys 17: 91-99, 1989. (Pubitemid 19173243)
7. Shah-Yukich AA and Nelson AC: Characterization of solid tumor microvasculature: a three-dimensional analysis using the polymer casting technique. Lab Invest 58: 236-244, 1988. (Pubitemid 18075285)
8. Mueller-Klieser W, Vaupel P, Manz R and Schmidseder R: Intracapillary oxyhemoglobin saturation of malignant tumors in humans. Int J Radiat Oncol Biol Phys 7: 1397-1404, 1981. (Pubitemid 12241705)
9. Sutherland RM: Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240: 177-184, 1988.
10. Sutherland RM: Importance of critical metabolites and cellular interactions in the biology of microregions of tumors. Cancer 58: 1668-1680, 1986.
11. Hockel M and Vaupel P: Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 93: 266-276, 2001. (Pubitemid 32219813)
12. Vaupel P and Mayer A: Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26: 225-239, 2007. (Pubitemid 47101660)
13. Moeller BJ and Dewhirst MW: HIF-1 and tumour radiosensitivity. Br J Cancer 95: 1-5, 2006. (Pubitemid 43980546)
14. Fels DR and Koumenis C: HIF-1alpha and p53: the ODD couple? Trends Biochem Sci 30: 426-429, 2005.
15. Hofer T, Wenger H and Gassmann M: Oxygen sensing, HIF-1alpha stabilization and potential therapeutic strategies. Pflugers Arch 443: 503-507, 2002. (Pubitemid 34185054)
16. Lowe SW, Ruley HE, Jacks T and Housman DE: p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74: 957-967, 1993. (Pubitemid 23289454)
17. Liang BC: Effects of hypoxia on drug resistance phenotype and genotype in human glioma cell lines. J Neurooncol 29: 149-155, 1996.
18. Semenza GL, Roth PH, Fang HM and Wang GL: Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757-23763, 1994. (Pubitemid 24293585)
19. Gordan JD, Thompson CB and Simon MC: HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 12: 108-113, 2007. (Pubitemid 47199124)
20. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD and Semenza GL: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613, 1996. (Pubitemid 26272112)
21. Comerford KM, Wallace TJ, Karhausen J, Louis NA, Montalto MC and Colgan SP: Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res 62: 3387-3394, 2002. (Pubitemid 34651384)
22. Comerford KM, Cummins EP and Taylor CT: c-Jun NH2-terminal kinase activation contributes to hypoxia-inducible factor 1alpha-dependent P-glycoprotein expression in hypoxia. Cancer Res 64: 9057-9061, 2004. (Pubitemid 39665517)
23. Rand MJ and Li CG: Nitric oxide as a neurotransmitter in peripheral nerves: nature of transmitter and mechanism of transmission. Annu Rev Physiol 57: 659-682, 1995.
24. Moncada S and Higgs EA: The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 147 (Suppl 1): S193-S201, 2006. (Pubitemid 43077277)
25. Callapina M, Zhou J, Schmid T, Kohl R and Brune B: NO restores HIF-1alpha hydroxylation during hypoxia: role of reactive oxygen species. Free Radic Biol Med 39: 925-936, 2005.
26. Hagen T, Taylor CT, Lam F and Moncada S: Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302: 1975-1978, 2003. (Pubitemid 37523507)
27. Dreher MR, Liu W, Michelich CR, Dewhirst MW, Yuan F and Chilkoti A: Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers. J Natl Cancer Inst 98: 335-344, 2006. (Pubitemid 43338213)
28. Riganti C, Miraglia E, Viarisio D, et al: Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux. Cancer Res 65: 516-525, 2005.
29. Yasuda H, Nakayama K, Watanabe M, et al: Nitroglycerin may increase response to anticancer drugs in non-small cell lung cancer via reduction of HIF-1a pathway. Nitric Oxide 17: S15, A24, 2007.
30. Frederiksen LJ, Sullivan R, Maxwell LR, et al: Chemosensitization of cancer in vitro and in vivo by nitric oxide signaling. Clin Cancer Res 13: 2199-2206, 2007. (Pubitemid 46649890)
31. Yasuda H, Yanagihara K, Nakayama K, et al: Therapeutic applications of nitric oxide for malignant tumor in animal models and human studies. In: Nitric Oxide and Cancer: Prognosis, Prevention and Therapy. Bonavida B (ed). Springer Inc., New York, NY, pp419-441, 2010.
32. Assaraf YG: Molecular basis of antifolate resistance. Cancer Metastasis Rev 26: 153-181, 2007.
33. Carlsson G, Gullberg B and Hafstrom L: Estimation of liver tumor volume using different formulas - an experimental study in rats. J Cancer Res Clin Oncol 105: 20-23, 1983. (Pubitemid 13194363)
34. Yasuda H: Solid tumor physiology and hypoxia-induced chemo/radio- resistance: novel strategy for cancer therapy: nitric oxide donor as a therapeutic enhancer. Nitric Oxide 19: 205-216, 2008.
35. Bonavida B, Baritaki S, Huerta-Yepez S, Vega MI, Chatterjee D and Yeung K: Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases. Nitric Oxide 19: 152-157, 2008.
36. Huerta S, Chilka S and Bonavida B: Nitric oxide donors: novel cancer therapeutics (Review). Int J Oncol 33: 909-927, 2008.
37. Siemens DR, Heaton JP, Adams MA, Kawakami J and Graham CH: Phase II study of nitric oxide donor for men with increasing prostate-specific antigen level after surgery or radiotherapy for prostate cancer. Urology 74: 878-883, 2009.
38. Yasuda H, Yamaya M, Nakayama K, et al: Randomized phase II trial comparing nitroglycerin plus vinorelbine and cisplatin with vinorelbine and cisplatin alone in previously untreated stage IIIB/IV non-small-cell lung cancer. J Clin Oncol 24: 688-694, 2006. (Pubitemid 46630435)
39. Sigmond J, Backus HH, Wouters D, Temmink OH, Jansen G and Peters GJ: Induction of resistance to the multitargeted antifolate pemetrexed (ALIMTA) in WiDr human colon cancer cells is associated with thymidylate synthase overexpression. Biochem Pharmacol 66: 431-438, 2003. (Pubitemid 36937028)
40. Moscow JA, Connolly T, Myers TG, Cheng CC, Paull K and Cowan KH: Reduced folate carrier gene (RFC1) expression and anti-folate resistance in transfected and non-selected cell lines. Int J Cancer 72: 184-190, 1997. (Pubitemid 27314657)
41. Liani E, Rothem L, Bunni MA, Smith CA, Jansen G and Assaraf YG: Loss of folylpoly-gamma-glutamate synthetase activity is a dominant mechanism of resistance to polyglutamylation-dependent novel antifolates in multiple human leukemia sublines. Int J Cancer 103: 587-599, 2003. (Pubitemid 36091461)
42. Stark M and Assaraf YG: Loss of Sp1 function via inhibitory phosphorylation in antifolate-resistant human leukemia cells with down-regulation of the reduced folate carrier. Blood 107: 708-715, 2006. (Pubitemid 43076397)
43. Illi B, Dello Russo C, Colussi C, et al: Nitric oxide modulates chromatin folding in human endothelial cells via protein phosphatase 2A activation and class II histone deacetylases nuclear shuttling. Circ Res 102: 51-58, 2008.
44. Hofseth LJ, Hussain SP, Wogan GN and Harris CC: Nitric oxide in cancer and chemoprevention. Free Radic Biol Med 34: 955-968, 2003. (Pubitemid 36398556)
45. Edwards P, Cendan JC, Topping DB, Moldawer LL, MacKay S, Copeland E and Lind DS: Tumor cell nitric oxide inhibits cell growth in vitro, but stimulates tumorigenesis and experimental lung metastasis in vivo. J Surg Res 63: 49-52, 1996. (Pubitemid 26197175)