Indolyl-quinuclidinols inhibit ENOX activity and endothelial cell morphogenesis while enhancing radiation-mediated control of tumor vasculature

FASEB Journal

Volumn 23, Issue 9, 2009, Pages 2986-2995

  Geng, Ling ^a   Rachakonda, Girish ^a   Morré, D James ^b   Morré, Dorothy M ^c   Crooks, Peter A ^d   Sonar, Vijayakumar N ^d,f   Roti Roti, Joseph L ^e   Rogers, Buck E ^e   Greco, Suellen ^e   Ye, Fei ^a   Salleng, Kenneth J ^a   Sasi, Soumya ^a   Freeman, Michael L ^a,g   Sekhar, Konjeti R ^a,g  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b PURDUE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d University of Kentucky   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Apotex Pharmachem India Pvt Ltd   (India)

^g VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

(Z) ( ); 2 (1 benzylindol 3 ylmethylene) 1 azabicyclo 2. 2.2 octan 3 ol; Angiogenesis

Indexed keywords

2 (1 BENZENESULFONYLINDOL 3 YLMETHYLENE) 1 AZABICYCLO[2.2.2]OCTAN 3 OL; 2 (1 BENZYLINDOL 3 YLMETHYLENE) 1 AZABICYCLO[2.2.2]OCTAN 3 OL; 2 (1H INDOL 3 YLMETHYLENE) 1 AZABICYCLO[2.2.2]OCTAN 3 OL; ANTINEOPLASTIC AGENT; CASPASE 3; INDOLE DERIVATIVE; MATRIGEL; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOCHEMISTRY; CANCER CONTROL; CANCER INHIBITION; CARBON NUCLEAR MAGNETIC RESONANCE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG HALF LIFE; DRUG SCREENING; DRUG STRUCTURE; ENDOTHELIUM CELL; FEMALE; GENE REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; ISOGRAFT; LEWIS CARCINOMA; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTON NUCLEAR MAGNETIC RESONANCE; RADIATION; RADIATION DOSE; RADIATION RESPONSE; RETROVIRUS; TUMOR VASCULARIZATION; X IRRADIATION; XENOGRAFT;

CELL MOVEMENT; CELL SHAPE; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; INDOLES; MEMBRANE PROTEINS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); QUINUCLIDINES; TRANSCRIPTION FACTORS;

EID: 70349331685     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-130005     Document Type: Article

References (42)

1. Li, C. Y., Shan, S., Huang, Q., Braun, R. D., Lanzen, J., Hu, K., Lin, P., and Dewhirst, M. W. (2000) Initial stages of tumor cell-induced angiogenesis: evaluation via skin window chambers in rodent models. J. Natl. Cancer Inst. 92, 143-147 (Pubitemid 30089871)
2. Sessa, C., Guibal, A., Del Conte, G., and Ruegg, C. (2008) Biomarkers of angiogenesis for the development of antiangiogenic therapies in oncology: tools or decorations? Nat. Clin. Pract. Oncol. 5, 378-391 (Pubitemid 351958963)
3. Fischer, C., Mazzone, M., Jonckx, B., and Carmeliet, P. (2008) FLT1 and its ligands VEGFB and PlGF: drug targets for antiangiogenic therapy? Nat. Rev. Cancer 8, 942-956
4. Folkman, J. (2006) Antiangiogenesis in cancer therapy- endostatin and its mechanisms of action. Exp. Cell. Res. 312, 594-607 (Pubitemid 43290336)
5. Duda, D. G., Jain, R. K., and Willett, C. G. (2007) Antiangiogenics: the potential role of integrating this novel treatment modality with chemoradiation for solid cancers. J. Clin. Oncol. 25, 4033-4042
6. Jones, M. K., Wang, H., Peskar, B. M., Levin, E., Itani, R. M., Sarfeh, I. J., and Tarnawski, A. S. (1999) Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing. Nat. Med. 5, 1418-1423
7. Pearce, H. R., Kalia, N., Bardhan, K. D., and Brown, N. J. (2003) Effects of aspirin and indomethacin on endothelial cell proliferation in vitro. J. Gastroenterol. Hepatol. 18, 1180-1187 (Pubitemid 37410049)
8. Rozic, J. G., Chakraborty, C., and Lala, P. K. (2001) Cyclooxygenase inhibitors retard murine mammary tumor progression by reducing tumor cell migration, invasiveness and angiogenesis. Int. J. Cancer 93, 497-506 (Pubitemid 32701408)
9. Wang, H. M., and Zhang, G. Y. (2005) Indomethacin suppresses growth of colon cancer via inhibition of angiogenesis in vivo. World J. Gastroenterol. 11, 340-343
10. Hull, M. A., Gardner, S. H., and Hawcroft, G. (2003) Activity of the non-steroidal anti-inflammatory drug indomethacin against colorectal cancer. Cancer Treat. Rev. 29, 309-320 (Pubitemid 37069661)
11. Gangadhar, N. M., and Stockwell, B. R. (2007) Chemical genetic approaches to probing cell death. Curr. Opin. Chem. Biol. 11, 83-87
12. Yagoda, N., von Rechenberg, M., Zaganjor, E., Bauer, A. J., Yang, W. S., Fridman, D. J., Wolpaw, A. J., Smukste, I., Peltier, J. M., Boniface, J. J., Smith, R., Lessnick, S. L., Sahasrabudhe, S., and Stockwell, B. R. (2007) RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864-868 (Pubitemid 46920135)
13. Morré, D. M., Lenaz, G., and Morré, D. J. (2000) Surface oxidase and oxidative stress propagation in aging. J. Exp. Biol. 203, 1513-1521 (Pubitemid 30354721)
14. Morré, D. J. (2004) Quinone oxidoreductases of the plasma membrane. Methods Enzymol. 378, 179-199
15. Brightman, A. O., Wang, J., Miu, R. K., Sun, I. L., Barr, R., Crane, F. L., and Morré, D. J. (1992) A growth factor- and hormone-stimulated NADH oxidase from rat liver plasma membrane. Biochim. Biophys. Acta 1105, 109-117
16. Lee, S., Li, R., Kim, B., Palvolgyi, R., Ho, T., Yang, Q. Z., Xu, J., Szeto, W. L., Honda, H., and Berliner, J. A. (2009) Ox-PAPC activation of plasma membrane electron transport (PMET) system increases expression of heme oxygenase 1 (HO-1) in human aortic endothelial cell (HAEC). J. Lipid Res. 50, 265-274
17. Liu, S. C., Yang, J. J., Shao, K. N., and Chueh, P. J. (2008) RNA interference targeting tNOX attenuates cell migration via a mechanism that involves membrane association of Rac. Biochem. Biophys. Res. Commun. 365, 672-677
18. Mauceri, H. J., Hanna, N. N., Beckett, M. A., Gorski, D. H., Staba, M. J., Stellato, K. A., Bigelow, K., Heimann, R., Gately, S., Dhanabal, M., Soff, G. A., Sukhatme, V. P., Kufe, D. W., and Weichselbaum, R. R. (1998) Combined effects of angiostatin and ionizing radiation in antitumour therapy. Nature 394, 287-291 (Pubitemid 28335042)
19. Shinohara, E. T., Geng, L., Tan, J., Chen, H., Shir, Y., Edwards, E., Halbrook, J., Kesicki, E. A., Kashishian, A., and Hallahan, D. E. (2005) DNA-dependent protein kinase is a molecular target for the development of noncytotoxic radiation-sensitizing drugs. Cancer Res. 65, 4987-4992 (Pubitemid 40827302)
20. Ogawa, K., Boucher, Y., Kashiwagi, S., Fukumura, D., Chen, D., and Gerweck, L. E. (2007) Influence of tumor cell and stroma sensitivity on tumor response to radiation. Cancer Res. 67, 4016-4021 (Pubitemid 46815045)
21. Sekhar, K. R., Crooks, P. A., Sonar, V. N., Friedman, D. B., Chan, J. Y., Meredith, M. J., Starnes, J. H., Kelton, K. R., Summar, S. R., Sasi, S., and Freeman, M. L. (2003) NADPH oxidase activity is essential for Keap1/Nrf2-mediated induction of GCLC in response to 2-indol-3-yl- methylenequinuclidin-3-ols. Cancer Res. 63, 5636-5645 (Pubitemid 37139889)
22. Sekhar, K. R., Sonar, V. N., Muthusamy, V., Sasi, S., Laszlo, A., Sawani, J., Horikoshi, N., Higashikubo, R., Bristow, R. G., Borrelli, M. J., Crooks, P. A., Lepock, J. R., Roti Roti, J. L., and Freeman, M. L. (2007) Novel chemical enhancers of heat shock increase thermal radiosensitization through a mitotic catastrophe pathway. Cancer Res. 67, 695-701 (Pubitemid 46192209)
23. Sonar, V. N., Thirupathi Reddy, Y., Sekhar, K. R., Sasi, S., Freeman, M. L., and Crooks, P. A. (2007) Novel substituted (Z)-2-(N-benzylindol-3- ylmethylene)quinuclidin-3-one and (Z)- (+/-)-2-(N-benzylindol-3-ylmethylene) quinuclidin-3-ol derivatives as potent thermal sensitizing agents. Bioorg. Med. Chem. Lett. 17, 6821-6824 (Pubitemid 350061311)
24. Osusky, K. L., Hallahan, D. E., Fu, A., Ye, F., Shyr, Y., and Geng, L. (2004) The receptor tyrosine kinase inhibitor SU11248 impedes endothelial cell migration, tubule formation, and blood vessel formation in vivo, but has little effect on existing tumor vessels. Angiogenesis 7, 225-233
25. Yazlovitskaya, E. M., Linkous, A. G., Thotala, D. K., Cuneo, K. C., and Hallahan, D. E. (2008) Cytosolic phospholipase A(2) regulates viability of irradiated vascular endothelium. Cell Death Differ. 15, 1641-1653
26. Yagiz, K., Morre, D. J., and Morre, D. M. (2006) Transgenic mouse line overexpressing the cancer-specific tNOX protein has an enhanced growth and acquired drug-response phenotype. J. Nutr. Biochem. 17, 750-759 (Pubitemid 44557048)
27. Edwards, E., Geng, L., Tan, J., Onishko, H., Donnelly, E., and Hallahan, D. E. (2002) Phosphatidylinositol 3-kinase/Akt signaling in the response of vascular endothelium to ionizing radiation. Cancer Res. 62, 4671-4677 (Pubitemid 34898594)
28. Wild, R., Ramakrishnan, S., Sedgewick, J., and Griffioen, A. W. (2000) Quantitative assessment of angiogenesis and tumor vessel architecture by computer-assisted digital image analysis: effects of VEGF-toxin conjugate on tumor microvessel density. Microvasc. Res. 59, 368-376 (Pubitemid 30322264)
29. Geng, L., Donnelly, E., McMahon, G., Lin, P. C., Sierra-Rivera, E., Oshinka, H., and Hallahan, D. E. (2001) Inhibition of vascular endothelial growth factor receptor signaling leads to reversal of tumor resistance to radiotherapy. Cancer Res. 61, 2413-2419 (Pubitemid 32685816)
30. Scarlett, D. J., Herst, P. M., and Berridge, M. V. (2005) Multiple proteins with single activities or a single protein with multiple activities: the conundrum of cell surface NADH oxidoreductases. Biochim. Biophys. Acta 1708, 108-119
31. Morré, D. J. (1999) NADH oxidase: a multifunctional ectroprotein of the eukaryotic cell surface. In Plasma Membrane Redox Systems and Their Role in Biological Stress and Disease (Asard, H., Berczi, A., and Caubergs, R. J., eds) pp. 121-156, Kluwer Academic Publishers, Dordrecht, The Netherlands
32. Montagne, J., Stewart, M. J., Stocker, H., Hafen, E., Kozma, S. C., and Thomas, G. (1999) Drosophila S6 kinase: a regulator of cell size. Science 285, 2126-2129 (Pubitemid 29451430)
33. Dufner, A., and Thomas, G. (1999) Ribosomal S6 kinase signaling and the control of translation. Exp. Cell. Res. 253, 100-109
34. Shinohara, E. T., Cao, C., Niermann, K., Mu, Y., Zeng, F., Hallahan, D. E., and Lu, B. (2005) Enhanced radiation damage of tumor vasculature by mTOR inhibitors. Oncogene 24, 5414-5422 (Pubitemid 43080085)
35. Al-Ghananeem, A. M., Albayati, Z. F., Malkawi, A., Sonar, V. N., Freeman, M. L., and Crooks, P. A. (2007) A pharmacokinetic study on Z-(+/-)-2-(1- benzylindole-3-yl-methylene)azabicyclo [2.2.2]octane-3-ol; a novel radio-sensitization agent. Cancer Chemother. Pharmacol. 60, 915-919 (Pubitemid 47389384)
36. Poon, R. T., Ng, I. O., Lau, C., Yu, W. C., Yang, Z. F., Fan, S. T., and Wong, J. (2002) Tumor microvessel density as a predictor of recurrence after resection of hepatocellular carcinoma: a prospective study. J. Clin. Oncol. 20, 1775-1785 (Pubitemid 34273266)
37. Mobius, C., Demuth, C., Aigner, T., Wiedmann, M., Wittekind, C., Mossner, J., Hauss, J., and Witzigmann, H. (2007) Evaluation of VEGF A expression and microvascular density as prognostic factors in extrahepatic cholangiocarcinoma. Eur. J. Surg. Oncol. 33, 1025-1029 (Pubitemid 47408741)
38. Shibuya, M., and Claesson-Welsh, L. (2006) Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp. Cell. Res. 312, 549-560 (Pubitemid 43290332)
39. Buck, E., Eyzaguirre, A., Brown, E., Petti, F., McCormack, S., Haley, J. D., Iwata, K. K., Gibson, N. W., and Griffin, G. (2006) Rapamycin synergizes with the epidermal growth factor receptor inhibitor erlotinib in non-small-cell lung, pancreatic, colon, and breast tumors. Mol. Cancer Ther. 5, 2676-2684 (Pubitemid 44848994)
40. Brown, J. M., and Wilson, G. (2003) Apoptosis genes and resistance to cancer therapy: what does the experimental and clinical data tell us? Cancer Biol. Ther. 2, 477-490
41. Zhang, P., Castedo, M., Tao, Y., Violot, D., Metivier, D., Deutsch, E., Kroemer, G., and Bourhis, J. (2006) Caspase independence of radio-induced cell death. Oncogene 25, 7758-7770 (Pubitemid 44967970)
42. Harada, H., Andersen, J. S., Mann, M., Terada, N., and Korsmeyer, S. J. (2001) p70S6 kinase signals cell survival as well as growth, inactivating the pro-apoptotic molecule BAD. Proc. Natl. Acad. Sci. U. S. A. 98, 9666-9670 (Pubitemid 32769360)