Smac mimetic enables the anticancer action of BCG-stimulated neutrophils through TNF-α but not through TRAIL and FasL

Journal of Leukocyte Biology

Volumn 92, Issue 1, 2012, Pages 233-244

  Goodwin Jinesh, G ^a   Chunduru, Srixinivas ^b   Kamat, Ashish M ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b TetraLogic Pharmaceuticals   (United States)

Author keywords

C IAPS; Caspase; FADD; Neutralizing antibodies; XIAP

Indexed keywords

DEATH RECEPTOR 4; DEATH RECEPTOR 5; FAS ANTIGEN; FAS LIGAND; IMMUNOMODULATING AGENT; NEUTRALIZING ANTIBODY; RECOMBINANT FAS LIGAND; RECOMBINANT PROTEIN; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMAC MIMETIC; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BCG VACCINATION; BLADDER CANCER; CANCER CELL; CANCER IMMUNOTHERAPY; CELL STIMULATION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG MECHANISM; HUMAN; HUMAN CELL; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

BLOTTING, WESTERN; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FAS LIGAND PROTEIN; HUMANS; MOLECULAR MIMICRY; MYCOBACTERIUM BOVIS; NEUTROPHIL ACTIVATION; NEUTROPHILS; OLIGOPEPTIDES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA; URINARY BLADDER NEOPLASMS;

EID: 84863499007     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1211623     Document Type: Article

References (40)

1. Martinez-Pineiro, J. A., Martinez-Pineiro, L. (1997) BCG update: intra-vesical therapy. Eur. Urol. 31 (Suppl. 1), 31-41.
2. Kamat, A. M., Lamm, D. L. (2000) Intravesical therapy for bladder cancer. Urology 55, 161-168.
3. Kemp, T. J., Ludwig, A. T., Earel, J. K., Moore, J. M., Vanoosten, R. L., Moses, B., Leidal, K., Nauseef, W. M., Griffith, T. S. (2005) Neutrophil stimulation with Mycobacterium bovis bacillus Calmette-Guerin (BCG) results in the release of functional soluble TRAIL/Apo-2L. Blood 106, 3474-3482.
4. Simons, M. P., Nauseef, W. M., Griffith, T. S. (2007) Neutrophils and TRAIL: insights into BCG immunotherapy for bladder cancer. Immunol. Res. 39, 79-93.
5. Oliveira, R. B., Moraes, M. O., Oliveira, E. B., Sarno, E. N., Nery, J. A., Sampaio, E. P. (1999) Neutrophils isolated from leprosy patients release TNF-α and exhibit accelerated apoptosis in vitro. J. Leukoc. Biol. 65, 364-371.
6. Rosevear, H. M., Lightfoot, A. J., O'Donnell, M. A., Griffith, T. S. (2009) The role of neutrophils and TNF-related apoptosis-inducing ligand (TRAIL) in bacillus Calmette-Guerin (BCG) immunotherapy for urothelial carcinoma of the bladder. Cancer Metastasis Rev. 28, 345-353.
7. Simons, M. P., O'Donnell, M. A., Griffith, T. S. (2008) Role of neutrophils in BCG immunotherapy for bladder cancer. Urol. Oncol. 26, 341-345.
8. Dovedi, S. J., Davies, B. R. (2009) Emerging targeted therapies for bladder cancer: a disease waiting for a drug. Cancer Metastasis Rev. 28, 355-367.
9. Shiozaki, E. N., Shi, Y. (2004) Caspases, IAPs and Smac/DIABLO: mechanisms from structural biology. Trends Biochem. Sci. 29, 486-494.
10. Petersen, S. L., Wang, L., Yalcin-Chin, A., Li, L., Peyton, M., Minna, J., Harran, P., Wang, X. (2007) Autocrine TNF α signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 12, 445-456.
11. Wang, L., Du, F., Wang, X. (2008) TNF-α induces two distinct caspase-8 activation pathways. Cell 133, 693-703.
12. Wu, H., Tschopp, J., Lin, S. C. (2007) Smac mimetics and TNF α: a dangerous liaison? Cell 131, 655-658.
13. Condon, S. M. (2011) The discovery and development of Smac mimetics-small molecule antagonists of the inhibitor of apoptosis proteins. In Annual Reports in Medicinal Chemistry (Macor, ed.), J. A. American Chemical Society, Washington, DC, 46, Chapter 13.
14. Zobel, K, Wang, L., Varfolomeev, E., Franklin, M. C, Elliott, L. O., Wallweber, H. J., Okawa, D. C, Flygare, J. A., Vucic, D., Fairbrother, W. J., Deshayes, K. (2006) Design, synthesis, and biological activity of a potent Smac mimetic that sensitizes cancer cells to apoptosis by antagonizing IAPs. ACS Chem. Biol. 1, 525-533.
15. Varfolomeev, E., Blankenship, J. W., Wayson, S. M., Fedorova, A. V., Kayagaki, N., Garg, P., Zobel, K, Dynek, J. N., Elliott, L. O., Wallweber, H. J., Flygare, J. A., Fairbrother, W. J., Deshayes, K, Dixit, V. M., Vucic, D. (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kB activation, and TNFα -dependent apoptosis. Cell 131, 669-681.
16. Vince, J. E., Wong, W. W, Khan, N., Feltham, R., Chau, D., Ahmed, A. U., Benetatos, C. A., Chunduru, S. K, Condon, S. M., McKinlay, M., Brink, R., Leverkus, M., Tergaonkar, V., Schneider, P., Callus, B. A., Koentgen, F., Vaux, D. L., Silke, J. (2007) IAP antagonists target cIAP1 to induce TNFα -dependent apoptosis. Cell 131, 682-693.
17. Feltham, R., Bettjeman, B., Budhidarmo, R., Mace, P. D., Shirley, S., Condon, S. M., Chunduru, S. K, McKinlay, M. A., Vaux, D. L., Silke, J., Day, C. L. (2011) Smac mimetics activate the E3 ligase activity of cIAP1 protein by promoting RING domain dimerization. J. Biol. Chem. 286, 17015-17028.
18. Metwalli, A. R., Khanbolooki, S., Jinesh, G., Sundi, D., Shah, J. B., Shrader, M., Choi, W., Lashinger, L. M., Chunduru, S., McConkey, D. J., McKinlay, M., Kamat, A. M. (2010) Smac mimetic reverses resistance to TRAIL and chemotherapy in human urothelial cancer cells. Cancer Biol. Ther. 10, 885-892.
19. Griffith, T. S., Kucaba, T. A., O'Donnell, M. A., Burns, J., Benetatos, C, McKinlay, M. A., Condon, S., Chunduru, S. (2011) Sensitization of human bladder tumor cells to TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis with a small molecule IAP antagonist. Apoptosis 16, 13-26.
20. Clark, R. A., Nauseef, W. M. (2001) Isolation and functional analysis of neutrophils. Curr. Protoc. Immunol. Chapter 7, Unit 7.23.
21. Kamat, A. M., Tharakan, S. T., Sung, B., Aggarwal, B. B. (2009) Cur-cumin potentiates the antitumor effects of bacillus Calmette-Guerin against bladder cancer through the downregulation of NF-kB and up-regulation of TRAIL receptors. Cancer Res. 69, 8958-8966.
22. Jonsson, G., Paulie, S., Grandien, A. (2003) cIAP-2 block apoptotic events in bladder cancer cells. Anticancer Res. 23, 3311-3316.
23. Tang, Y., Simoneau, A. R., Xie, J., Shahandeh, B., Zi, X. (2008) Effects of the kava chalcone flavokawain A differ in bladder cancer cells with wild-type versus mutant p53. Cancer Prev. Res. (Phila) 1, 439-451.
24. Bertrand, M. J., Milutinovic, S., Dickson, K. M., Ho, W. C, Boudreault, A., Durkin, J., Gillard, J. W., Jaquith, J. B., Morris, S. J., Barker, P. A. (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700.
25. Liu, X., Yue, P., Chen, S., Hu, L., Lonial, S., Khuri, F. R., Sun, S. Y (2007) The proteasome inhibitor PS-341 (bortezomib) up-regulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite up-regulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res. 67, 4981-4988.
26. Takimoto, R., El-Deiry, W. S. (2000) Wild-type p53 transactivates the KILLER/DR5 gene through an intronic sequence-specific DNA-binding site. Oncogene 19, 1735-1743.
27. Scott, F. L., Denault, J. B., Riedl, S. J., Shin, H., Renatus, M., Salvesen, G S. (2005) XIAP inhibits caspase-3 and -7 using two binding sites: evo-lutionarily conserved mechanism of IAPs. EMBOJ. 24, 645-655.
28. Conus, S., Perozzo, R., Reinheckel, T., Peters, C, Scapozza, L., Yousefi, S., Simon, H. U. (2008) Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J. Exp. Med. 205, 685-698.
29. Perez-Cruz, I., Carcamo, J. M., Golde, D. W. (2003) Vitamin C inhibits FAS-induced apoptosis in monocytes and U937 cells. Blood 102, 336-343.
30. Amiri, K. I., Horton, L. W., LaFleur, B. J., Sosman, J. A., Richmond, A. (2004) Augmenting chemosensitivity of malignant melanoma tumors via proteasome inhibition: implication for bortezomib (VELCADE, PS-341) as a therapeutic agent for malignant melanoma. Cancer Res. 64, 4912-4918.
31. Mustafa, T., Phyu, S., Nilsen, R., Bjune, G., Jonsson, R. (1999) Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis? Inflammation 23, 507-521.
32. Kirkin, V., Cahuzac, N., Guardiola-Serrano, F., Huault, S., Luckerath, K, Friedmann, E., Novac, N., Wels, W. S., Martoglio, B., Hueber, A. O., Zornig, M. (2007) The Fas ligand intracellular domain is released by ADAM10 and SPPL2a cleavage in T-cells. Cell Death Differ. 14, 1678-1687.
33. De Boer, E. C, de Jong, W. H., van der Meijden, A. P., Steerenberg, P. A., Witjes, F., Vegt, P. D., Debruyne, F. M., Ruitenberg, E.J. (1991) Leukocytes in the urine after intravesical BCG treatment for superficial bladder cancer A flow cytofluorometric analysis. Urol. Res. 19, 45-50.
34. Ethuin, F., Gerard, B., Benna, J. E., Boutten, A., Gougereot-Pocidalo, M. A., Jacob, L., Chollet-Martin, S. (2004) Human neutrophils produce interferon 7 upon stimulation by interleukin-12. Lab. Invest. 84, 1363-1371.
35. De Jager, R., Guinan, P., Lamm, D., Khanna, O., Brosman, S., De Ker-nion, J., Williams, R., Richardson, C, Muenz, L., Reitsma, D. (1991) Long-term complete remission in bladder carcinoma in situ with intravesical TICE bacillus Calmette Guerin. Overview analysis of six phase II clinical trials. Urology 38, 507-513.
36. Alessenko, A. V., Boikov, P., Filippova, G. N., Khrenov, A. V., Loginov, A. S., Makarieva, E. D. (1997) Mechanisms of cycloheximide-induced apoptosis in liver cells. FEBS Lett. 416, 113-116.
37. Kleeff, J., Kornmann, M., Sawhney, H., Korc, M. (2000) Actinomycin D induces apoptosis and inhibits growth of pancreatic cancer cells. Int. J. Cancer 86, 399-407.
38. Krakstad, C, Christensen, A. E., Doskeland, S. O. (2004) cAMP protects neutrophils against TNF-α-induced apoptosis by activation of cAMP-de-pendent protein kinase, independently of exchange protein directly activated by cAMP (Epac). J. Leukoc. Biol. 76, 641-647.
39. Chen, Y L., Chen, S. H., Wang, J. Y, Yang, B. C. (2003) Fas ligand on tumor cells mediates inactivation of neutrophils. J. Immunol. 171, 1183-1191.
40. Diessenbacher, P., Hupe, M., Sprick, M. R., Kerstan, A., Geserick, P., Haas, T. L., Wachter, T., Neumann, M., Walczak, H., Silke, J., Leverkus, M. (2008) NF-kB inhibition reveals differential mechanisms of TNF versus TRAIL-induced apoptosis upstream or at the level of caspase-8 activation independent of cIAP2.J. Invest. Dermatol. 128, 1134-1147.