Nexavar/Stivarga and Viagra Interact to Kill Tumor Cells

Journal of Cellular Physiology

Volumn 230, Issue 9, 2015, Pages 2281-2298

  Tavallai, Mehrad ^a   Hamed, Hossein A ^a   Roberts, Jane L ^a   Cruickshanks, Nichola ^a   Chuckalovcak, John ^b   Poklepovic, Andrew ^c   Booth, Laurence ^a   Dent, Paul ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b BIO RAD LABORATORIES   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; BECLIN 1; CASPASE 8; EPIDERMAL GROWTH FACTOR RECEPTOR; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FINGOLIMOD; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; HEAT SHOCK PROTEIN 90; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHODIESTERASE V; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE B; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REGORAFENIB; S6 KINASE; SCATTER FACTOR RECEPTOR; SILDENAFIL; SORAFENIB; SPHINGOSINE 1 PHOSPHATE RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TADALAFIL; VARDENAFIL; CARBANILAMIDE DERIVATIVE; NICOTINAMIDE; PHOSPHODIESTERASE V INHIBITOR; PIPERAZINE DERIVATIVE; PURINE DERIVATIVE; SULFONAMIDE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL KILLING; COLON CANCER; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME INACTIVATION; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIVER CANCER; LIVER CANCER CELL LINE; MOUSE; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SERUM; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HEPG2 CELL LINE; NEOPLASMS; PATHOLOGY;

APOPTOSIS; CELL PROLIFERATION; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; DRUG SYNERGISM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HUMANS; NEOPLASM PROTEINS; NEOPLASMS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PHOSPHODIESTERASE 5 INHIBITORS; PIPERAZINES; PURINES; SIGNAL TRANSDUCTION; SULFONAMIDES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84929773802     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24961     Document Type: Article

References (52)

1. Benavides GA, Liang Q, Dodson M, Darley-Usmar V, Zhang J. 2013. Inhibition of autophagy and glycolysis by nitric oxide during hypoxia-reoxygenation impairs cellular bioenergetics and promotes cell death in primary neurons. Free Radic Biol Med 65:1215-1228.
2. Black KL, Yin D, Ong JM, Hu J, Konda BM, Wang X, Ko MK, Bayan JA, Sacapano MR, Espinoza A, Irvin DK, Shu Y. 2008. PDE5 inhibitors enhance tumor permeability and efficacy of chemotherapy in a rat brain tumor model. Brain Res 1230:290-302.
3. Booth L, Roberts JL, Cruickshanks N, Conley A, Durrant DE, Das A, Fisher PB, Kukreja RC, Grant S, Poklepovic A, Dent P. 2014. Phosphodiesterase 5 inhibitors enhance chemotherapy killing in gastrointestinal/genitourinary cancer cells. Mol Pharmacol 85:408-419.
4. Booth L, Roberts JL, Cruickshanks N, Tavallai S, Webb T, Samuel P, Conley A, Binion B, Young HF, Poklepovic A, Spiegel S, Dent P. 2015. PDE5 inhibitors enhance Celecoxib killing in multiple tumor types. J Cell Physiol 230:1115-1127.
5. Carr BI, D'Alessandro R, Refolo MG, Iacovazzi PA, Lippolis C, Messa C, Cavallini A, Correale M, Di Carlo A. 2013. Effects of low concentrations of regorafenib and sorafenib on human HCC cell AFP, migration, invasion, and growth in vitro. J Cell Physiol 228:1344-1350.
6. Choi CY, Park KR, Lee JH, Jeon YJ, Liu KH, Oh S, Kim DE, Yea SS. 2007. Isoeugenol suppression of inducible nitric oxide synthase expression is mediated by down-regulation of NF-kappaB, ERK1/2, and p38 kinase. Eur J Pharmacol 576:151-159.
7. Cruickshanks N, Hamed HA, Booth L, Tavallai S, Syed J, Sajithlal GB, Grant S, Poklepovic A, Dent P. 2013. Histone deacetylase inhibitors restore toxic BH3 domain protein expression in anoikis-resistant mammary and brain cancer stem cells, thereby enhancing the response to anti-ERBB1/ERBB2 therapy. Cancer Biol Ther 14:982-996.
8. Das A, Xi L, Kukreja RC. 2008. Protein kinase G-dependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3beta. J Biol Chem 283:29572-29585.
9. Das A, Durrant D, Mitchell C, Mayton E, Hoke NN, Salloum FN, Park MA, Qureshi I, Lee R, Dent P, Kukreja RC. 2010. Sildenafil increases chemotherapeutic efficacy of doxorubicin in prostate cancer and ameliorates cardiac dysfunction. Proc Natl Acad Sci USA 107:18202-18207.
10. Deguchi A, Thompson WJ, Weinstein IB. 2004. Activation of protein kinase G is sufficient to induce apoptosis and inhibit cell migration in colon cancer cells. Cancer Res 64:3966-3973.
11. Elser C, Siu LL, Winquist E, Agulnik M, Pond GR, Chin SF, Francis P, Cheiken R, Elting J, McNabola A, Wilkie D, Petrenciuc O, Chen EX. 2007. Phase II trial of sorafenib in patients with recurrent or metastatic squamous cell carcinoma of the head and neck or nasopharyngeal carcinoma. J Clin Oncol 25:3766-3773.
12. Felley-Bosco E. 1998. Role of nitric oxide in genotoxicity: implication for carcinogenesis. Cancer Metastasis Rev 17:25-37.
13. Florio T, Arena S, Pattarozzi A, Thellung S, Corsaro A, Villa V, Massa A, Diana F, Spoto G, Forcella S, Damonte G, Filocamo M, Benatti U, Schettini G. 2003. Basic fibroblast growth factor activates endothelial nitric-oxide synthase in CHO-K1 cells via the activation of ceramide synthesis. Mol Pharmacol 63:297-310.
14. Francis SH, Busch JL, Corbin JD, Sibley D. 2010. CGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 62:525-563.
15. Gandelman M, Levy M, Cassina P, Barbeito L, Beckman JS. 2013. P2×7 receptor-induced death of motor neurons by a peroxynitrite/FAS-dependent pathway. J Neurochem 126:382-388.
16. González R, Ferrín G, Aguilar-Melero P, Ranchal I, Linares CI, Bello RI, De la Mata M, Gogvadze V, Bárcena JA, Alamo JM, Orrenius S, Padillo FJ, Zhivotovsky B, Muntané J. 2013. Targeting hepatoma using nitric oxide donor strategies. Antioxid Redox Signal 18:491-506.
17. Ha KS, Kim KM, Kwon YG, Bai SK, Nam WD, Yoo YM, Kim PK, Chung HT, Billiar TR, Kim YM. 2003. Nitric oxide prevents 6-hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/Akt activation. FASEB J 17:1036-1047.
18. Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S, Spiegel S. 2009. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325:1254-1257.
19. Hait NC, Wise LE, Allegood JC, O'Brien M, Avni D, Reeves TM, Knapp PE, Lu J, Luo C, Miles MF, Milstien S, Lichtman AH, Spiegel S. 2014. Active, phosphorylated fingolimod inhibits histone deacetylases and facilitates fear extinction memory. Nat Neurosci 17:971-980.
20. Haklar G, Sayin-Ozveri E, Yüksel M, Aktan AO, Yalçin AS. 2001. Different kinds of reactive oxygen and nitrogen species were detected in colon and breast tumors. Cancer Lett 165:219-224.
21. Hayden MA, Lange PA, Nakayama DK. 2001. Nitric oxide and cyclic guanosine monophosphate stimulate apoptosis via activation of the Fas-FasL pathway. J Surg Res 101:183-189.
22. Hirst DG, Robson T. 2007. Nitrosative stress in cancer therapy. Front Biosci 12:3406-3418.
23. Hotte SJ, Hirte HW. 2002. BAY 43-9006: Early clinical data in patients with advanced solid malignancies. Curr Pharm Des 8:2249-2253.
24. Inaba H, Rubnitz JE, Coustan-Smith E, Li L, Furmanski BD, Mascara GP, Heym KM, Christensen R, Onciu M, Shurtleff SA, Pounds SB, Pui CH, Ribeiro RC, Campana D, Baker SD. 2001. Phase I pharmacokinetic and pharmacodynamics study of the multi-kinase inhibitor sorafenib in combination with clofarabine and cytarabine in pediatric relapsed/refractory leukemia. J Clin Oncol 29:3293-3300.
25. Komalavilas P, Shah PK, Jo H, Lincoln TM. 1999. Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem 274:34301-34309.
26. Kots AY, Bian K, Murad F. 2011. Nitric oxide and cyclic GMP signaling pathway as a focus for drug development. Curr Med Chem 18:3299-3305.
27. Li L, Zhao M, Navid F, Pratz K, Smith BD, Rudek MA, Baker SD. 2010. Quantitation of sorafenib and its active metabolite sorafenib N-oxide in human plasma by liquid chromatography-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 878:3033-3038.
28. Liang J, Nagahashi M, Kim EY, Harikumar KB, Yamada A, Huang WC, Hait NC, Allegood JC, Price MM, Avni D, Takabe K, Kordula T, Milstien S, Spiegel S. 2013. Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitis-associated cancer. Cancer Cell 23:107-120.
29. Martin AP, Park MA, Mitchell C, Walker T, Rahmani M, Thorburn A, Häussinger D, Reinehr R, Grant S, Dent P. 2009. BCL-2 family inhibitors enhance histone deacetylase inhibitor and sorafenib lethality via autophagy and overcome blockade of the extrinsic pathway to facilitate killing. Mol Pharmacol 76:327-341.
30. Musicki B, Bivalacqua TJ, Champion HC, Burnett AL. 2014. Sildenafil promotes eNOS activation and inhibits NADPH oxidase in the transgenic sickle cell mouse penis. J Sex Med 11:424-430.
31. Negi G, Kumar A, Sharma SS. 2010. Concurrent targeting of nitrosative stress-PARP pathway corrects functional, behavioral and biochemical deficits in experimental diabetic neuropathy. Biochem Biophys Res Commun 391:102-106.
32. Park MA, Zhang G, Martin AP, Hamed H, Mitchell C, Hylemon PB, Graf M, Rahmani M, Ryan K, Liu X, Spiegel S, Norris J, Fisher PB, Grant S, Dent P. 2008. Vorinostat and sorafenib increase ER stress, autophagy and apoptosis via ceramide-dependent CD95 and PERK activation. Cancer Biol Ther 7:1648-1662.
33. Park MA, Reinehr R, Häussinger D, Voelkel-Johnson C, Ogretmen B, Yacoub A, Grant S, Dent P. 2010a. Sorafenib activates CD95 and promotes autophagy and cell death via Src family kinases in gastrointestinal tumor cells. Mol Cancer Ther 9:2220-2231.
34. Park MA, Mitchell C, Zhang G, Yacoub A, Allegood J, Häussinger D, Reinehr R, Larner A, Spiegel S, Fisher PB, Voelkel-Johnson C, Ogretmen B, Grant S, Dent P. 2010b. Vorinostat and sorafenib increase CD95 activation in gastrointestinal tumor cells through a Ca(2+)-de novo ceramide-PP2A-reactive oxygen species-dependent signaling pathway. Cancer Res 70:6313-6324.
35. Pratz KW, Cho E, Levis MJ, Karp JE, Gore SD, McDevitt M, Stine A, Zhao M, Baker SD, Carducci MA, Wright JJ, Rudek MA, Smith BD. 2010. A pharmacodynamic study of sorafenib in patients with relapsed and refractory acute leukemias. Leukemia 24:1437-1444.
36. Rahmani M, Davis EM, Crabtree TR, Habibi JR, Nguyen TK, Dent P, Grant S. 2007. The kinase inhibitor sorafenib induces cell death through a process involving induction of endoplasmic reticulum stress. Mol Cell Biol 27:5499-5513.
37. Rahmani M, Davis EM, Bauer C, Dent P, Grant S. 2005. Apoptosis induced by the kinase inhibitor BAY 43-9006. J Biol Chem 280:35217-35227.
38. Reinehr R, Görg B, Höngen A, Häussinger D. 2004. CD95-tyrosine nitration inhibits hyperosmotic and CD95 ligand-induced CD95 activation in rat hepatocytes. J Biol Chem 279:10364-10373.
39. Roberts JL, Conley A, Booth L, Cruickshanks N, Malkin M, Kukreja RC, Grant S, Poklepovic A, Dent P. 2014. PDE5 inhibitors enhance the lethality of standard of care chemotherapy in pediatric CNS tumor cells. Cancer Biol Ther 15:758-767.
40. Russwurm M, Russwurm C, Koesling D, Mergia E. 2013. NO/cGMP: The past, the present, and the future. Methods Mol Biol 1020:1-16.
41. Sarfati M, Mateo V, Baudet S, Rubio M, Fernandez C, Davi F, Binet JL, Delic J, Merle-Beral H. 2003. Sildenafil and vardenafil, types 5 and 6 phosphodiesterase inhibitors, induce caspase-dependent apoptosis of B-chronic lymphocytic leukemia cells. Blood 101:265-269.
42. Shen C, Yan J, Erkocak OF, Zheng XF, Chen XD. 2014. Nitric oxide inhibits autophagy via suppression of JNK in meniscal cells. Rheumatology (Oxford) 53:1022-1033.
43. Smith MA, Houghton P. 2013. A proposal regarding reporting of in vitro testing results. Clin Cancer Res 19:2828-2833.
44. Tang Y, Hamed HA, Cruickshanks N, Fisher PB, Grant S, Dent P. 2012. Obatoclax and lapatinib interact to induce toxic autophagy through NOXA. Mol Pharmacol 81:527-540.
45. Thompson WJ, Piazza GA, Li H, Liu L, Fetter J, Zhu B, Sperl G, Ahnen D, Pamukcu R. 2000. Exisulind induction of apoptosis involves guanosine 3′, 5′-cyclic monophosphate phosphodiesterase inhibition, protein kinase G activation, and attenuated beta-catenin. Cancer Res 60:3338-3342.
46. Tripathi DN, Chowdhury R, Trudel LJ, Tee AR, Slack RS, Walker CL, Wogan GN. 2013. Reactive nitrogen species regulate autophagy through ATM-AMPK-TSC2-mediated suppression of mTORC1. Proc Natl Acad Sci USA 110:E2950-E2957.
47. Valez V, Cassina A, Batinic-Haberle I, Kalyanaraman B, Ferrer-Sueta G, Radi R. 2013. Peroxynitrite formation in nitric oxide-exposed submitochondrial particles: Detection, oxidative damage and catalytic removal by Mn-porphyrins. Arch Biochem Biophys 529:45-54.
48. Watanabe H, Ohashi K, Takeuchi K, Yamashita K, Yokoyama T, Tran QK, Satoh H, Terada H, Ohashi H, Hayashi H. 2002. Sildenafil for primary and secondary pulmonary hypertension. Clin Pharmacol Ther 71:398-402.
49. Yu Y, Fan SM, Yuan SJ, Tashiro S, Onodera S, Ikejima T. 2012. Nitric oxide (•NO) generation but not ROS plays a major role in silibinin-induced autophagic and apoptotic death in human epidermoid carcinoma A431 cells. Free Radic Res 46:1346-1360.
50. Zhu B, Strada S, Stevens T. 2005a. Cyclic GMP-specific phosphodiesterase 5 regulates growth and apoptosis in pulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 289:L196-L206.
51. Zhu B, Vemavarapu L, Thompson WJ, Strada SJ. 2005b. Suppression of cyclic GMP-specific phosphodiesterase 5 promotes apoptosis and inhibits growth in HT29 cells. J Cell Biochem 94:336-350.
52. Zhu B, Zhang L, Alexeyev M, Alvarez DF, Strada SJ, Stevens T. 2009. Type 5 phosphodiesterase expression is a critical determinant of the endothelial cell angiogenic phenotype. Am J Physiol Lung Cell Mol Physiol 296:L220-L228.