A small molecule inhibitor of atypical protein kinase C signaling inhibits pancreatic cancer cell transformed growth and invasion

Oncotarget

Volumn 6, Issue 17, 2015, Pages 15297-15310

  Butler, Amanda M ^a   Scotti Buzhardt, Michele L ^b   Erdogan, Eda ^c   Li, Shuhua ^a   Inman, Kristin S ^a   Fields, Alan P ^a   Murray, Nicole R ^a  

^a MAYO CLINIC   (United States)

^b Genoptix Inc   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Atypical PKCs; Aurothiomalate; Invasion; Pancreatic cancer; Transformed growth

Indexed keywords

AUROTHIOMALATE; ISOENZYME; PARD6A PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN KINASE C LAMBDA; PROTEIN KINASE C ZETA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA;

ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; CELL TRANSFORMATION; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; PANCREAS TUMOR; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR INVASION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GOLD SODIUM THIOMALATE; HUMANS; ISOENZYMES; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; PROTEIN BINDING; PROTEIN KINASE C; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84934299787     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3812     Document Type: Article

References (34)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62:10-29.
2. Scotti ML, Bamlet WR, Smyrk TC, Fields AP and Murray NR. Protein kinase Cι is required for pancreatic cancer cell transformed growth and tumorigenesis. Cancer Research. 2010; 70:2064-2074.
3. Butler AM, Scotti Buzhardt ML, Li S, Smith KE, Fields AP and Murray NR. Protein kinase C zeta regulates human pancreatic cancer cell transformed growth and invasion through a STAT3-dependent mechanism. PLoS ONE. 2013; 8:e72061.
4. Erdogan E, Lamark T, Stallings-Mann M, Lee J, Pellecchia M, Thompson EA, Johansen T and Fields AP. Aurothiomalate inhibits transformed growth by targeting the PB1 domain of protein kinase Ciota. J Biol Chem. 2006; 281:28450-28459.
5. Regala RP, Davis RK, Kunz A, Khoor A, Leitges M and Fields AP. Atypical protein kinase Cι is required for bronchioalveolar stem cell expansion and lung tumorigenesis. Cancer Research. 2009; 69:7603-7611.
6. Stallings-Mann M, Jamieson L, Regala RP, Weems C, Murray NR and Fields AP. A novel small-molecule inhibitor of protein kinase Ciota blocks transformed growth of non-small-cell lung cancer cells. Cancer Res. 2006; 66:1767-1774.
7. Wang Y, Hill KS and Fields AP. PKCiota Maintains a Tumor-initiating Cell Phenotype That Is Required for Ovarian Tumorigenesis. Mol Cancer Res. 2013; 11:1624-1635.
8. Ardito CM, Gruner BM, Takeuchi KK, Lubeseder-Martellato C, Teichmann N, Mazur PK, Delgiorno KE, Carpenter ES, Halbrook CJ, Hall JC, Pal D, Briel T, Herner A, Trajkovic-Arsic M, Sipos B, Liou GY, et al. EGF receptor is required for KRAS-induced pancreatic tumorigenesis. Cancer Cell. 2012; 22:304-317.
9. Frederick LA, Matthews JA, Jamieson L, Justilien V, Thompson EA, Radisky DC and Fields AP. Matrix metalloproteinase-10 is a critical effector of protein kinase C?-Par6a-mediated lung cancer. Oncogene. 2008; 27:4841-4853.
10. Murray NR, Jamieson L, Yu W, Zhang J, Gokmen-Polar Y, Sier D, Anastasiadis P, Gatalica Z, Thompson EA and Fields AP. Protein kinase C{iota} is required for Ras transformation and colon carcinogenesis in vivo. J Cell Biol. 2004; 164:797-802.
11. Zhang J, Anastasiadis, P. Z., Liu, Y., Thompson, E.A. and Fields, A.P. Protein Kinase C βII Induces Cell Invasion Through a Ras/MEK-, PKCiota/RAC 1-dependent Signaling Pathway. J Biol Chem. 2004; 279:22118-22123.
12. Calcagno SR, Li S, Colon M, Kreinest PA, Thompson EA, Fields AP and Murray NR. Oncogenic K-ras promotes early carcinogenesis in the mouse proximal colon. Int J Cancer. 2008; 122:2462-2470.
13. Murray NR, Weems C, Chen L, Leon J, Yu W, Davidson LA, Jamieson L, Chapkin RS, Thompson EA and Fields AP. Protein kinase C betaII and TGFbetaRII in omega-3 fatty acid-mediated inhibition of colon carcinogenesis. J Cell Biol. 2002; 157:915-920.
14. Fields AP, Calcagno SR, Krishna M, Rak S, Leitges M and Murray NR. Protein kinase Cbeta is an effective target for chemoprevention of colon cancer. Cancer Res. 2009; 69:1643-1650.
15. Selbie LA, Schmitz-Peiffer C, Sheng Y and Biden TJ. Molecular cloning and characterization of PKC iota, an atypical isoform of protein kinase C derived from insulin-secreting cells. J Biol Chem. 1993; 268:24296-24302.
16. Lamark T, Perander M, Outzen H, Kristiansen K, Overvatn A, Michaelsen E, Bjorkoy G and Johansen T. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem. 2003; 278:34568-34581.
17. Gao L, Joberty G and Macara IG. Assembly of epithelial tight junctions is negatively regulated by Par6. Curr Biol. 2002; 12:221-225.
18. Regala RP, Weems C, Jamieson L, Copland JA, Thompson EA and Fields AP. Atypical protein kinase Ciota plays a critical role in human lung cancer cell growth and tumorigenicity. J Biol Chem. 2005; 280:31109-31115.
19. Regala RP, Thompson EA and Fields AP. Atypical protein kinase C iota expression and aurothiomalate sensitivity in human lung cancer cells. Cancer Res. 2008; 68:5888-5895.
20. Pia Rigobello M, Messori L, Marcon G, Agostina Cinellu M, Bragadin M, Folda A, Scutari G and Bindoli A. Gold complexes inhibit mitochondrial thioredoxin reductase: consequences on mitochondrial functions. J Inorg Biochem. 2004; 98:1634-1641.
21. Murray NR, Kalari KR and Fields AP. Protein kinase Ciota expression and oncogenic signaling mechanisms in cancer. Journal of Cellular Physiology. 2011; 226:879-887.
22. Regala RP, Weems C, Jamieson L, Khoor A, Edell ES, Lohse CM and Fields AP. Atypical protein kinase C iota is an oncogene in human non-small cell lung cancer. Cancer Res. 2005; 65:8905-8911.
23. Messori L and Marcon G. Gold complexes in the treatment of rheumatoid arthritis. Met Ions Biol Syst. 2004; 41:279-304.
24. Becker K, Gromer S, Schirmer RH and Muller S. Thioredoxin reductase as a pathophysiological factor and drug target. Eur J Biochem. 2000; 267:6118-6125.
25. Jeon KI, Jeong JY and Jue DM. Thiol-reactive metal compounds inhibit NF-kappa B activation by blocking I kappa B kinase. J Immunol. 2000; 164:5981-5989.
26. Kim NH, Lee MY, Park SJ, Choi JS, Oh MK and Kim IS. Auranofin blocks interleukin-6 signalling by inhibiting phosphorylation of JAK1 and STAT3. Immunology. 2007; 122:607-614.
27. Han S, Kim K, Kim H, Kwon J, Lee YH, Lee CK, Song Y, Lee SJ, Ha N and Kim K. Auranofin inhibits overproduction of pro-inflammatory cytokines, cyclooxygenase expression and PGE2 production in macrophages. Arch Pharm Res. 2008; 31:67-74.
28. Kim NH, Park HJ, Oh MK and Kim IS. Antiproliferative effect of gold(I) compound auranofin through inhibition of STAT3 and telomerase activity in MDA-MB 231 human breast cancer cells. BMB Rep. 2013; 46:59-64.
29. Liu N, Li X, Huang H, Zhao C, Liao S, Yang C, Liu S, Song W, Lu X, Lan X, Chen X, Yi S, Xu L, Jiang L, Dong X, Zhou P, et al. Clinically used antirheumatic agent auranofin is a proteasomal deubiquitinase inhibitor and inhibits tumor growth. Oncotarget. 2014; 5:5453-5471.
30. Fiskus W, Saba N, Shen M, Ghias M, Liu J, Gupta SD, Chauhan L, Rao R, Gunewardena S, Schorno K, Austin CP, Maddocks K, Byrd J, Melnick A, Huang P, Wiestner A, et al. Auranofin induces lethal oxidative and endoplasmic reticulum stress and exerts potent preclinical activity against chronic lymphocytic leukemia. Cancer Res. 2014; 74:2520-2532.
31. Marzano C, Gandin V, Folda A, Scutari G, Bindoli A and Rigobello MP. Inhibition of thioredoxin reductase by auranofin induces apoptosis in cisplatin-resistant human ovarian cancer cells. Free Radic Biol Med. 2007; 42:872-881.
32. Tiekink ER. Gold derivatives for the treatment of cancer. Crit Rev Oncol Hematol. 2002; 42:225-248.
33. Mirabelli CK, Johnson RK, Hill DT, Faucette LF, Girard GR, Kuo GY, Sung CM and Crooke ST. Correlation of the in vitro cytotoxic and in vivo antitumor activities of gold(I) coordination complexes. J Med Chem. 1986; 29:218-223.
34. Mansfield AS, Fields AP, Jatoi A, Qi Y, Adjei AA, Erlichman C and Molina JR. Phase I dose escalation study of the PKCiota inhibitor aurothiomalate for advanced non-small-cell lung cancer, ovarian cancer, and pancreatic cancer. Anticancer Drugs. 2013; 24:1079-1083.