Sigma-2 receptor ligand as a novel method for delivering a SMAC mimetic drug for treating ovarian cancer

British Journal of Cancer

Volumn 109, Issue 9, 2013, Pages 2368-2377

  Zeng, C ^a   Vangveravong, S ^a   Mcdunn, J E ^b   Hawkins, W G ^c   Mach, R H ^a,c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b METABOLON INC   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

drug delivery; IAPs; ovarian cancer; sigma 2 receptor; Smac

Indexed keywords

1 [3,3 DIMETHYL 2 [2 (METHYLAMINO)PROPANAMIDO]BUTANOYL] N (1,2,3,4 TERAHYDRONAPHTHALEN 1 YL)PYRROLIDINE 2 CARBOXAMIDE OXALATE; 9 [10 [[1 [[3,3 DIMETHYL 1 OXO 1 [2 [(1,2,3,4 TETRAHYDRONAPHTHALEN 1 YL)CARBAMOYL]PYRROLIDIN 1 YL]BUTAN 2 YL]AMINO] 1 OXOPROPAN 2 YL]AMINO]DECYL] 9 AZABICYCLO[3.3.1]NONAN 3 YL (2 METHOXY 5 METHYLPHENYL)CARBAMATE; CASPASE 3; CASPASE 8; CASPASE 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SIGMA 2 OPIATE RECEPTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; OVARY CANCER; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION;

EID: 84887021104     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.593     Document Type: Article

References (40)

1. Aggarwal BB (2003) Signalling pathways of the TNF superfamily: A doubleedged sword. Nat Rev Immunol 3: 745-756.
2. BemWT, Thomas GE, Mamone JY, Homan SM, Levy BK, Johnson FE, Coscia CJ (1991) Overexpression of sigma receptors in nonneural human tumors. Cancer Res 51: 6558-6562.
3. Dehdashti F, Laforest R, Gao F, Shoghi SI, Aft RL, Nussenbaum B, Kreisel FH, Bartlett NL, Cashen A, Wagner-Johnson N, Mach RH (2013) Assessment of cellular proliferation in tumors by positron emission tomography using [18F]ISO-1. J Nucl Med 53: 350-357.
4. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17: 2215-2223.
5. Dinh P, Harnett P, Piccart-Gebhart MJ, Awada A (2008) New therapies for ovarian cancer: Cytotoxics and molecularly targeted agents. Crit Rev Oncol Hematol 67: 103-112.
6. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42.
7. Gyrd-Hansen M, Meier P (2010) IAPs: From caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 10: 561-574.
8. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362.
9. Hornick JR, Vangveravong S, Spitzer D, Abate C, Berardi F, Goedegebuure P, Mach RH, Hawkins WG (2012) Lysosomal membrane permeabilization is an early event in Sigma-2 receptor ligand mediated cell death in pancreatic cancer. J Exp Clin Cancer Res 31: 41.
10. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59: 225-249.
11. Mach RH, Smith CR, al-Nabulsi I, Whirrett BR, Childers SR, Wheeler KT (1997) Sigma 2 receptors as potential biomarkers of proliferation in breast cancer. Cancer Res 57: 156-161.
12. Oost TK, Sun C, Armstrong RC, Al-Assaad AS, Betz SF, Deckwerth TL, Ding H, Elmore SW, Meadows RP, Olejniczak ET, Oleksijew A, Oltersdorf T, Rosenberg SH, Shoemaker AR, Tomaselli KJ, Zou H, Fesik SW (2004) Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer. J Med Chem 47: 4417-4426.
13. Petersen SL, Wang L, Yalcin-Chin A, Li L, Peyton M, Minna J, Harran P, Wang X (2007) Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 12: 445-456.
14. Petrucci E, Pasquini L, Bernabei M, Saulle E, Biffoni M, Accarpio F, Sibio S, Di Giorgio A, Di Donato V, Casorelli A, Benedetti-Panici P, Testa U (2012) A small molecule SMAC mimic LBW242 potentiates TRAIL- and anticancer drug-mediated cell death of ovarian cancer cells. PLoS One 7: E35073.
15. Petrucci E, Pasquini L, Petronelli A, Saulle E, Mariani G, Riccioni R, Biffoni M, Ferretti G, Benedetti-Panici P, Cognetti F, Scambia G, Humphreys R, Peschle C, Testa U (2007) A small molecule Smac mimic potentiates TRAIL-mediated cell death of ovarian cancer cells. Gynecol Oncol 105: 481-492.
16. Rothe M, Pan MG, Henzel WJ, Ayres TM, Goeddel DV (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83: 1243-1252.
17. Schug ZT, Gonzalvez F, Houtkooper RH, Vaz FM, Gottlieb E (2011) BID is cleaved by caspase-8 within a native complex on the mitochondrial membrane. Cell Death Differ 18: 538-548.
18. Shiozaki EN, Shi Y (2004) Caspases, IAPs and Smac/DIABLO: Mechanisms from structural biology. Trends Biochem Sci 29: 486-494.
19. Spitzer D, Simon Jr. PO, Kashiwagi H, Xu J, Zeng C, Vangveravong S, Zhou D, Chang K, McDunn JE, Hornick JR, Goedegebuure P, Hotchkiss RS, Mach RH, Hawkins WG (2012) Use of multifunctional sigma-2 receptor ligand conjugates to trigger cancer-selective cell death signaling. Cancer Res 72: 201-209.
20. Stordal B, Pavlakis N, Davey R (2007) A systematic review of platinum and taxane resistance from bench to clinic: An inverse relationship. Cancer Treat Rev 33: 688-703.
21. Sun H, Nikolovska-Coleska Z, Yang CY, Qian D, Lu J, Qiu S, Bai L, Peng Y, Cai Q, Wang S (2008) Design of small-molecule peptidic and nonpeptidic Smac mimetics. Acc Chem Res 41: 1264-1277.
22. Sun SC (2012) The noncanonical NF-kappaB pathway. Immunol Rev 246: 125-140.
23. Torchilin VP (2010) Passive and active drug targeting: Drug delivery to tumors as an example. Handb Exp Pharmacol 197: 3-53.
24. Tu Z, Dence CS, Ponde DE, Jones L, Wheeler KT, Welch MJ, Mach RH (2005) Carbon-11 labeled sigma2 receptor ligands for imaging breast cancer. Nucl Med Biol 32: 423-430.
25. Tu Z, Xu J, Jones LA, Li S, Dumstorff C, Vangveravong S, Chen DL, Wheeler KT, Welch MJ, Mach RH (2007) Fluorine-18-labeled benzamide analogues for imaging the sigma2 receptor status of solid tumors with positron emission tomography. J Med Chem 50: 3194-3204.
26. Uren AG, Pakusch M, Hawkins CJ, Puls KL, Vaux DL (1996) Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-Associated factors. Proc Natl Acad Sci USA 93: 4974-4978.
27. Vangveravong S, Xu J, Zeng C, Mach RH (2006) Synthesis of N-substituted 9-Azabicyclo[3.3.1]nonan-3alpha-yl carbamate analogs as sigma2 receptor ligands. Bioorg Med Chem 14: 6988-6997.
28. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K, Dynek JN, Elliott LO, Wallweber HJ, Flygare JA, Fairbrother WJ, Deshayes K, Dixit VM, Vucic D (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 131: 669-681.
29. Viatour P, Merville MP, Bours V, Chariot A (2005) Phosphorylation of NF-kappaB and IkappaB proteins: Implications in cancer and inflammation. Trends Biochem Sci 30: 43-52.
30. Vilner BJ, Bowen WD (1993) Sigma receptor-Active neuroleptics are cytotoxic to C6 glioma cells in culture. Eur J Pharmacol 244: 199-201.
31. Vilner BJ, de Costa BR, Bowen WD (1995) Cytotoxic effects of sigma ligands: Sigma receptor-mediated alterations in cellular morphology and viability. J Neurosci 15: 117-134.
32. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, Brink R, Leverkus M, Tergaonkar V, Schneider P, Callus BA, Koentgen F, Vaux DL, Silke J (2007) IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 131: 682-693.
33. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin Jr. AS (1998) NF-kappaB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281: 1680-1683.
34. Wang S (2011) Design of small-molecule Smac mimetics as IAP antagonists. Curr Top Microbiol Immunol 348: 89-113.
35. Wheeler KT, Wang LM, Wallen CA, Childers SR, Cline JM, Keng PC, Mach RH (2000) Sigma-2 receptors as a biomarker of proliferation in solid tumours. Br J Cancer 82: 1223-1232.
36. Xu J, Tu Z, Jones LA, Vangveravong S, Wheeler KT, Mach RH (2005) [3H]N-[4-(3,4-dihydro-6,7-dimethoxyisoquinolin-2(1H)-yl)butyl]-2-methoxy-5 -methylbenzamide: A novel sigma-2 receptor probe. Eur J Pharmacol 525: 8-17.
37. Xu J, Zeng C, Chu W, Pan F, Rothfuss JM, Zhang F, Tu Z, Zhou D, Zeng D, Vangveravong S, Johnston F, Spitzer D, Chang KC, Hotchkiss RS, Hawkins WG, Wheeler KT, Mach RH (2011) Identification of the PGRMC1 protein complex as the putative sigma-2 receptor binding site. Nat Commun 2: 380.
38. Yang C, Davis JL, Zeng R, Vora P, Su X, Collins LI, Vangveravong S, Mach RH, Piwnica-Worms D, Weilbaecher KN, Faccio R, Novack DV (2013) Antagonism of inhibitor of apoptosis proteins increases bone metastasis via unexpected osteoclast activation. Cancer Discov 3: 212-223.
39. Zeng C, Vangveravong S, Jones LA, Hyrc K, Chang KC, Xu J, Rothfuss JM, Goldberg MP, Hotchkiss RS, Mach RH (2011) Characterization and evaluation of two novel fluorescent sigma-2 receptor ligands as proliferation probes. Mol Imaging 10: 420-433.
40. Zeng C, Vangveravong S, Xu J, Chang KC, Hotchkiss RS, Wheeler KT, Shen D, Zhuang ZP, Kung HF, Mach RH (2007) Subcellular localization of sigma-22 receptors in breast cancer cells using two-photon and confocal microscopy. Cancer Res 67: 6708-6716.