Discovery of sulfonamidebenzamides as selective apoptotic CHOP pathway activators of the unfolded protein response

ACS Medicinal Chemistry Letters

Volumn 5, Issue 12, 2014, Pages 1278-1283

  Flaherty, Daniel P ^a   Miller, Justin R ^b   Garshott, Danielle M ^b   Hedrick, Michael ^c   Gosalia, Palak ^c   Li, Yujie ^c   Milewski, Monika ^c   Sugarman, Eliot ^c   Vasile, Stefan ^c   Salaniwal, Sumeet ^c   Su, Ying ^c   Smith, Layton H ^c   Chung, Thomas D Y ^c   Pinkerton, Anthony B ^c   Aubé, Jeffrey ^a   Callaghan, Michael U ^b   Golden, Jennifer E ^a   Fribley, Andrew M ^b   Kaufman, Randal J ^c  

^a UNIVERSITY OF KANSAS   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

anticancer; CHOP activator; UPR apoptotic pathway activator; UPR modulator

Indexed keywords

BENZAMIDE DERIVATIVE; CELL PROTEIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HYDROGEN; SORAFENIB; SULFONAMIDEBENZAMIDE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; DRUG DEVELOPMENT; DRUG STRUCTURE; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; GENE EXPRESSION; GROWTH INHIBITION; IN VIVO STUDY; METABOLIC DISORDER; MOUTH SQUAMOUS CELL CARCINOMA; MULTIPLE CANCER; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; ULTRAVIOLET SPECTROSCOPY; UNFOLDED PROTEIN RESPONSE;

EUKARYOTA;

EID: 84918587731     PISSN: None     EISSN: 19485875     Source Type: Journal    
DOI: 10.1021/ml5003234     Document Type: Article

References (40)

1. Rutkowski, D. T.; Kaufman, R. J. A trip to the ER: coping with stress Trends Cell Biol. 2004, 14, 20-28
2. Schröder, M.; Kaufman, R. J. The mammalian unfolded protein response Annu. Rev. Biochem. 2005, 74, 739-789
3. Kaufman, R. J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls Genes Dev. 1999, 13, 1211-1233
4. Bernales, S.; Papa, F. R.; Walter, P. Intracellular signaling by the unfolded protein response Annu. Rev. Cell Dev. Biol. 2006, 22, 487-508
5. Calfon, M.; Zeng, H.; Urano, F.; Till, J. H.; Hubbard, S. R.; Harding, H. P.; Clark, S. G.; Ron, D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA Nature 2002, 415, 92-96
6. Acosta-Alvear, D.; Zhou, Y.; Blais, A.; Tsikitis, M.; Lents, N. H.; Arias, C.; Lennon, C. J.; Kluger, Y.; Dynlacht, B. D. XBP1 controls diverse cell type-and condition-specific transcriptional regulatory networks Mol. Cell 2007, 27, 53-66
7. Hetz, C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond Nat. Rev. Mol. Cell Biol. 2012, 13, 89-102
8. Marciniak, S. J.; Yun, C. Y.; Oyadomari, S.; Novoa, I.; Zhang, Y.; Jungreis, R.; Nagata, K.; Harding, H. P.; Ron, D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum Genes Dev. 2004, 18, 3066-3077
9. Matsumoto, M.; Minami, M.; Takeda, K.; Sakao, Y.; Akira, S. Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells FEBS Lett. 1996, 395, 143-147
10. Oyadomari, S.; Mori, M. Roles of CHOP/GADD153 in endoplasmic reticulum stress Cell Death Differ. 2003, 11, 381-389
11. Han, J.; Back, S. H.; Hur, J.; Lin, Y.-H.; Gildersleeve, R.; Shan, J.; Yuan, C. L.; Krokowski, D.; Wang, S.; Hatzoglou, M.; Kilberg, M. S.; Sartor, M. A.; Kaufman, R. J. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death Nat. Cell Biol. 2013, 15, 481-490
12. Nakagawa, H.; Umemura, A.; Taniguchi, K.; Font-Burgada, J.; Dhar, D.; Ogata, H.; Zhong, Z.; Valasek, M. A.; Seki, E.; Hidalgo, J.; Koike, K.; Kaufman, R. J.; Karin, M. ER stress cooperates with hypernutrition to trigger TNF-dependent spontaneous HCC development Cancer Cell 2014, 26, 331-343
13. Roussel, B. D.; Kruppa, A. J.; Miranda, E.; Crowther, D. C.; Lomas, D. A.; Marciniak, S. J. Endoplasmic reticulum dysfunction in neurological disease Lancet Neurol. 2013, 12, 105-118
14. Kaser, A.; Flak, M. B.; Tomczak, M. F.; Blumberg, R. S. The unfolded protein response and its role in intestinal homeostasis and inflammation Exp. Cell Res. 2011, 317, 2772-2779
15. Cao, S. S.; Kaufman, R. J. Targeting endoplasmic reticulum stress in metabolic disease Expert Opin. Ther. Targets 2013, 17, 437-448
16. Scheuner, D.; Kaufman, R. J. The unfolded protein response: a pathway that links insulin demand with β-cell failure and diabetes Endocr. Rev. 2008, 29, 317-333
17. Moenner, M.; Pluquet, O.; Bouchecareilh, M.; Chevet, E. Integrated endoplasmic reticulum stress responses in cancer Cancer Res. 2007, 67, 10631-10634
18. Cross, B. C.; Bond, P. J.; Sadowski, P. G.; Jha, B. K.; Zak, J.; Goodman, J. M.; Silverman, R. H.; Neubert, T. A.; Baxendale, I. R.; Ron, D. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule Proc. Natl. Acad. Sci. U.S.A. 2012, 109, E869-E878
19. Papandreou, I.; Denko, N. C.; Olson, M.; Van Melckebeke, H.; Lust, S.; Tam, A.; Solow-Cordero, D. E.; Bouley, D. M.; Offner, F.; Niwa, M. Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma Blood 2011, 117, 1311-1314
20. Axten, J. M.; Medina, J. s. R.; Feng, Y.; Shu, A.; Romeril, S. P.; Grant, S. W.; Li, W. H. H.; Heerding, D. A.; Minthorn, E.; Mencken, T. Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl) phenyl] acetyl}-2,3-dihydro-1 H -indol-5-yl)-7 H -pyrrolo[2,3- d ]pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK) J. Med. Chem. 2012, 55, 7193-7207
21. D'Arcy, P.; Brnjic, S.; Olofsson, M. H.; Fryknäs, M.; Lindsten, K.; De Cesare, M.; Perego, P.; Sadeghi, B.; Hassan, M.; Larsson, R. Inhibition of proteasome deubiquitinating activity as a new cancer therapy Nat. Med. 2011, 17, 1636-1640
22. Boyce, M.; Bryant, K. F.; Jousse, C.; Long, K.; Harding, H. P.; Scheuner, D.; Kaufman, R. J.; Ma, D.; Coen, D. M.; Ron, D. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress Science 2005, 307, 935-939
23. Fribley, A. M.; Cruz, P. G.; Miller, J. R.; Callaghan, M. U.; Cai, P.; Narula, N.; Neubig, R. R.; Showalter, H. D.; Larsen, S. D.; Kirchhoff, P. D.; Larsen, M. J.; Burr, D. A.; Schultz, P. J.; Jacobs, R. R.; Tamayo-Castillo, G.; Ron, D.; Sherman, D. H.; Kaufman, R. J. Complementary cell-based high-throughput screens identify novel modulators of the unfolded protein response J. Biomol. Screening 2011, 16, 825-35
24. Hetz, C.; Chevet, E.; Harding, H. P. Targeting the unfolded protein response in disease Nat. Rev. Drug Discovery 2013, 12, 703-719
25. Wilhelm, S. M.; Adnane, L.; Newell, P.; Villanueva, A.; Llovet, J. M.; Lynch, M. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling Mol. Cancer Ther. 2008, 7, 3129-3140
26. Smalley, K. S.; Xiao, M.; Villanueva, J.; Nguyen, T. K.; Flaherty, K. T.; Letrero, R.; Van Belle, P.; Elder, D. E.; Wang, Y.; Nathanson, K. L.; Herlyn, M. CRAF inhibition induces apoptosis in melanoma cells with non-V600E BRAF mutations Oncogene 2009, 28, 85-94
27. Magnaghi, P.; D'Alessio, R.; Valsasina, B.; Avanzi, N.; Rizzi, S.; Asa, D.; Gasparri, F.; Cozzi, L.; Cucchi, U.; Orrenius, C.; Polucci, P.; Ballinari, D.; Perrera, C.; Leone, A.; Cervi, G.; Casale, E.; Xiao, Y.; Wong, C.; Anderson, D. J.; Galvani, A.; Donati, D.; O'Brien, T.; Jackson, P. K.; Isacchi, A. Covalent and allosteric inhibitors of the ATPase VCP/p97 induce cancer cell death Nat. Chem. Biol. 2013, 9, 548-556
28. Brem, G. J.; Mylonas, I.; Bruning, A. Eeyarestatin causes cervical cancer cell sensitization to bortezomib treatment by augmenting ER stress and CHOP expression Gynecol. Oncol. 2013, 128, 383-90
29. Chou, T. F.; Brown, S. J.; Minond, D.; Nordin, B. E.; Li, K.; Jones, A. C.; Chase, P.; Porubsky, P. R.; Stoltz, B. M.; Schoenen, F. J.; Patricelli, M. P.; Hodder, P.; Rosen, H.; Deshaies, R. J. Reversible inhibitor of p97, DBeQ, impairs both ubiquitin-dependent and autophagic protein clearance pathways Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 4834-4839
30. Jhaveri, K.; Taldone, T.; Modi, S.; Chiosis, G. Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers Biochim. Biophys. Acta 2012, 1823, 742-755
31. Adams, J.; Kauffman, M. Development of the proteasome inhibitor velcade (bortezomib) Cancer Invest. 2004, 22, 304-311
32. Kisselev, A. F.; van der Linden, W. A.; Overkleeft, H. S. Proteasome inhibitors: an expanding army attacking a unique target Chem. Biol. 2012, 19, 99-115
33. Fribley, A.; Zeng, Q.; Wang, C.-Y. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells Mol. Cell. Biol. 2004, 24, 9695-9704
34. Fribley, A. M.; Evenchik, B.; Zeng, Q.; Park, B. K.; Guan, J. Y.; Zhang, H.; Hale, T. J.; Soengas, M. S.; Kaufman, R. J.; Wang, C. Y. Proteasome inhibitor PS-341 induces apoptosis in cisplatin-resistant squamous cell carcinoma cells by induction of Noxa J. Biol. Chem. 2006, 281, 31440-31447
35. Mitsiades, N.; Mitsiades, C. S.; Poulaki, V.; Chauhan, D.; Fanourakis, G.; Gu, X.; Bailey, C.; Joseph, M.; Libermann, T. A.; Treon, S. P.; Munshi, N. C.; Richardson, P. G.; Hideshima, T.; Anderson, K. C. Molecular sequelae of proteasome inhibition in human multiple myeloma cells Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 14374-14379
36. Leung-Hagesteijn, C.; Erdmann, N.; Cheung, G.; Keats, J. J.; Stewart, A. K.; Reece, D. E.; Chung, K. C.; Tiedemann, R. E. Xbp1s-negative tumor B cells and pre-plasmablasts mediate therapeutic proteasome inhibitor resistance in multiple myeloma Cancer Cell 2013, 24, 289-304
37. Fribley, A. M.; Miller, J. R.; Brownell, A. L.; Garshott, D. M.; Zeng, Q.; Reist, T. E.; Narula, N.; Cai, P.; Xi, Y.; Callaghan, M. U.; Kodali, V.; Kaufman, R. J. Celastrol induces unfolded protein response-dependent cell death in head and neck cancer Exp. Cell Res. 2014, 10.1016/j.yexcr.2014.08.014
38. Harding, H. P.; Zhang, Y.; Khersonsky, S.; Marciniak, S.; Scheuner, D.; Kaufman, R. J.; Javitt, N.; Chang, Y.-T.; Ron, D. Bioactive small molecules reveal antagonism between the integrated stress response and sterol-regulated gene expression Cell Metab. 2005, 2, 361-371
39. Back, S. H.; Lee, K.; Vink, E.; Kaufman, R. J. Cytoplasmic IRE1α-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress J. Biol. Chem. 2006, 281, 18691-18706
40. Hayashi, S.; Nakamoto, T.; Minoura, M.; Nakanishi, W. Evidence for effective p(Z)-π(Ar) conjugations (Z = S, Se, and Te, as Well as Z = O) in 9-(arylchalcogenyl)triptycenes: experimental and theoretical investigations J. Org. Chem. 2009, 74, 4763-4771