Discovery of an orally active small-molecule irreversible inhibitor of protein disulfide isomerase for ovarian cancer treatment

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 40, 2012, Pages 16348-16353

  Xu, Shili ^a   Butkevich, Alexey N ^a   Yamada, Roppei ^a   Zhou, Yu ^b   Debnath, Bikash ^a   Duncan, Roger ^a   Zandi, Ebrahim ^b,c   Petasis, Nicos A ^a,b   Neamati, Nouri ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

BODIPY conjugation; Drug resistance; Oral bioavailability

Indexed keywords

ANTINEOPLASTIC AGENT; CYSTINE; ISOMERASE INHIBITOR; PROPYNOIC ACID CARBAMOYL METHYL AMIDE DERIVATIVE; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; COVALENT BOND; DRUG CYTOTOXICITY; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME INHIBITION; FEMALE; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IC 50; IN VIVO STUDY; MASS SPECTROMETRY; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ALKYNES; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATOGRAPHY, LIQUID; CYSTEINE; DIPEPTIDES; DRUG DISCOVERY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HISTOLOGICAL TECHNIQUES; HUMANS; IMMUNOPRECIPITATION; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; OVARIAN NEOPLASMS; PROPIONATES; PROTEIN DISULFIDE-ISOMERASES; TANDEM MASS SPECTROMETRY; THIOPHENES;

EID: 84867095394     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1205226109     Document Type: Article

References (38)

1. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62: 10-29.
2. Petty R, Evans A, Duncan I, Kurbacher C, Cree I (1998) Drug resistance in ovarian cancer - the role of p53. Pathol Oncol Res 4:97-102. (Pubitemid 28394624)
3. Hatahet F, Ruddock LW (2009) Protein disulfide isomerase: A critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal 11:2807-2850.
4. Hoffstrom BG, et al. (2010) Inhibitors of protein disulfide isomerase suppress apoptosis induced by misfolded proteins. Nat Chem Biol 6:900-906.
5. Lovat PE, et al. (2008) Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res 68:5363-5369.
6. Gruber CW, Cemazar M, Heras B, Martin JL, Craik DJ (2006) Protein disulfide isomerase: The structure of oxidative folding. Trends Biochem Sci 31:455-464. (Pubitemid 44108657)
7. Haefliger S, et al. (2011) Protein disulfide isomerase blocks CEBPA translation and is up-regulated during the unfolded protein response in AML. Blood 117:5931-5940.
8. Bonome T, et al. (2008) A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer. Cancer Res 68:5478-5486.
9. Welsh JB, et al. (2001) Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res 61:5974-5978. (Pubitemid 32762523)
10. Beer DG, et al. (2002) Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med 8:816-824.
11. Basso K, et al. (2005) Reverse engineering of regulatory networks in human B cells. Nat Genet 37:382-390.
12. Goplen D, et al. (2006) Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer Res 66:9895-9902. (Pubitemid 44672041)
13. Rickman DS, et al. (2001) Distinctive molecular profiles of high-grade and low-grade gliomas based on oligonucleotide microarray analysis. Cancer Res 61:6885-6891. (Pubitemid 32896514)
14. Talantov D, et al. (2005) Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res 11:7234-7242. (Pubitemid 41507680)
15. Khan MM, et al. (2011) Discovery of a small molecule PDI inhibitor that inhibits reduction of HIV-1 envelope glycoprotein gp120. ACS Chem Biol 6:245-251.
16. Dickerhof N, Kleffmann T, Jack R, McCormick S (2011) Bacitracin inhibits the reductive activity of protein disulfide isomerase by disulfide bond formation with free cysteines in the substrate-binding domain. FEBS J 278:2034-2043.
17. Wang EJ, Snyder RD, Fielden MR, Smith RJ, Gu YZ (2008) Validation of putative genomic biomarkers of nephrotoxicity in rats. Toxicology 246:91-100.
18. Weston BS, Wahab NA, Roberts T, Mason RM (2001) Bacitracin inhibits fibronectin matrix assembly by mesangial cells in high glucose. Kidney Int 60:1756-1764. (Pubitemid 32999980)
19. Godin B, Touitou E (2004) Mechanism of bacitracin permeation enhancement through the skin and cellular membranes from an ethosomal carrier. J Control Release 94:365-379. (Pubitemid 38117147)
20. Yamada R, et al. (2011) Discovery and preclinical evaluation of a novel class of cytotoxic propynoic acid carbamoyl methyl amides (PACMAs). J Med Chem 54:2902-2914.
21. Roschke AV, et al. (2003) Karyotypic complexity of the NCI-60 drug-screening panel. Cancer Res 63:8634-8647. (Pubitemid 38064038)
22. Alvarez M, et al. (1995) Generation of a drug resistance profile by quantitation of mdr-1/P-glycoprotein in the cell lines of the National Cancer Institute Anticancer Drug Screen. J Clin Invest 95:2205-2214.
23. Townsend DM, et al. (2009) Nitrosative stress-induced s-glutathionylation of protein disulfide isomerase leads to activation of the unfolded protein response. Cancer Res 69:7626-7634.
24. Perez-Iratxeta C, Andrade-Navarro MA (2008) K2D2: Estimation of protein secondary structure from circular dichroism spectra. BMC Struct Biol 8:25.
25. Feige MJ, Hendershot LM (2011) Disulfide bonds in ER protein folding and homeostasis. Curr Opin Cell Biol 23:167-175.
26. Root P, Sliskovic I, Mutus B (2004) Platelet cell-surface protein disulphide-isomerase mediated S-nitrosoglutathione consumption. Biochem J 382:575-580. (Pubitemid 39243924)
27. Fonseca C, et al. (2009) Protein disulfide isomerases are antibody targets during immune-mediated tumor destruction. Blood 113:1681-1688.
28. Noiva R (1999) Protein disulfide isomerase: The multifunctional redox chaperone of the endoplasmic reticulum. Semin Cell Dev Biol 10:481-493.
29. Ejima K, et al. (1999) 17beta-estradiol induces protein thiol/disulfide oxidoreductases and protects cultured bovine aortic endothelial cells from oxidative stress. Eur J Endocrinol 140:608-613. (Pubitemid 29314725)
30. Primm TP, Gilbert HF (2001) Hormone binding by protein disulfide isomerase, a high capacity hormone reservoir of the endoplasmic reticulum. J Biol Chem 276:281-286. (Pubitemid 32050318)
31. Spillman MA, et al. (2010) Tissue-specific pathways for estrogen regulation of ovarian cancer growth and metastasis. Cancer Res 70:8927-8936.
32. Hashida T, Kotake Y, Ohta S (2011) Protein disulfide isomerase knockdown-induced cell death is cell-line-dependent and involves apoptosis in MCF-7 cells. J Toxicol Sci 36:1-7.
33. Singh J, Petter RC, Baillie TA, Whitty A (2011) The resurgence of covalent drugs. Nat Rev Drug Discov 10:307-317.
34. Jänne PA, et al. (2011) Phase I dose-escalation study of the pan-HER inhibitor, PF299804, in patients with advanced malignant solid tumors. Clin Cancer Res 17: 1131-1139.
35. Uehara T, et al. (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441:513-517. (Pubitemid 44050153)
36. LaMantia ML, Lennarz WJ (1993) The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity. Cell 74:899-908.
37. Vuori K, Myllylä R, Pihlajaniemi T, Kivirikko KI (1992) Expression and site-directed mutagenesis of human protein disulfide isomerase in Escherichia coli. This multifunctional polypeptide has two independently acting catalytic sites for the isomerase activity. J Biol Chem 267:7211-7214.
38. Kemmink J, Darby NJ, Dijkstra K, Nilges M, Creighton TE (1996) Structure determination of the N-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy. Biochemistry 35: 7684-7691.