A mechanistic study of the proapoptotic effect of tolfenamic acid: Involvement of NF-κB activation

Carcinogenesis

Volumn 34, Issue 10, 2013, Pages 2350-2360

  Jeong, Jin Boo ^a   Yang, Xuyu ^a   Clark, Ruth ^a   Choi, Jieun ^a   Baek, Seung Joon ^b   Lee, Seong Ho ^b  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEASOME; PROTEIN P53; SERINE; SYNAPTOTAGMIN I; TOLFENAMIC ACID;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DRUG MECHANISM; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; COLORECTAL NEOPLASMS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; I-KAPPA B PROTEINS; NF-KAPPA B; ORTHO-AMINOBENZOATES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PHYTOCHEMICALS; PROTEIN BINDING; PROTEIN TRANSPORT; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84885148316     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt224     Document Type: Article

References (56)

1. Siegel, R. et al. (2012) Cancer statistics, 2012. CA. Cancer J. Clin., 62, 10-29.
2. Huls, G. et al. (2003) Non-steroidal anti-inflammatory drugs and molecular carcinogenesis of colorectal carcinomas. Lancet, 362, 230-232.
3. Thun, M.J. et al. (1993) Aspirin use and risk of fatal cancer. Cancer Res., 53, 1322-1327.
4. Gupta, R.A. et al. (2001) Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat. Rev. Cancer, 1, 11-21.
5. Grösch, S. et al. (2001) COX-2 independent induction of cell cycle arrest and apoptosis in colon cancer cells by the selective COX-2 inhibitor celecoxib. FASEB J., 15, 2742-2744.
6. Sheng, H. et al. (1997) Inhibition of human colon cancer cell growth by selective inhibition of cyclooxygenase-2. J. Clin. Invest., 99, 2254-2259.
7. Leahy, K.M. et al. (2002) Cyclooxygenase-2 inhibition by celecoxib reduces proliferation and induces apoptosis in angiogenic endothelial cells in vivo. Cancer Res., 62, 625-631.
8. Tsujii, M. et al. (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell, 93, 705-716.
9. Yao, M. et al. (2003) Inhibition of cyclooxygenase-2 by rofecoxib attenuates the growth and metastatic potential of colorectal carcinoma in mice. Cancer Res., 63, 586-592.
10. Hansen, P.E. (1994) Tolfenamic acid in acute and prophylactic treatment of migraine: a review. Pharmacol. Toxicol., 75 (suppl. 2), 81-82.
11. Abdelrahim, M. et al. (2006) Tolfenamic acid and pancreatic cancer growth, angiogenesis, and Sp protein degradation. J. Natl Cancer Inst., 98, 855-868.
12. Kang, S.U. et al. (2012) Tolfenamic acid induces apoptosis and growth inhibition in head and neck cancer: involvement of NAG-1 expression. PLoS One, 7, e34988.
13. Lee, S.H. et al. (2008) ESE-1/EGR-1 pathway plays a role in tolfenamic acid-induced apoptosis in colorectal cancer cells. Mol. Cancer Ther., 7, 3739-3750.
14. Lee, S.H. et al. (2010) Activating transcription factor 2 (ATF2) controls tolfenamic acid-induced ATF3 expression via MAP kinase pathways. Oncogene, 29, 5182-5192.
15. Vane, J.R. (1971) Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat. New Biol., 231, 232-235.
16. Alberts, D.S. et al. (1995) Do NSAIDs exert their colon cancer chemoprevention activities through the inhibition of mucosal prostaglandin synthetase? J. Cell. Biochem. Suppl., 22, 18-23.
17. Hanif, R. et al. (1996) Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin- independent pathway. Biochem. Pharmacol., 52, 237-245.
18. Elder, D.J. et al. (1997) Induction of apoptotic cell death in human colorectal carcinoma cell lines by a cyclooxygenase-2 (COX-2)-selective nonsteroidal anti-inflammatory drug: independence from COX-2 protein expression. Clin. Cancer Res., 3, 1679-1683.
19. Piazza, G.A. et al. (1997) Apoptosis primarily accounts for the growthinhibitory properties of sulindac metabolites and involves a mechanism that is independent of cyclooxygenase inhibition, cell cycle arrest, and p53 induction. Cancer Res., 57, 2452-2459.
20. Yamamoto, Y. et al. (1999) Sulindac inhibits activation of the NF-kappaB pathway. J. Biol. Chem., 274, 27307-27314.
21. Shao, J. et al. (2000) Overexpression of the wild-type p53 gene inhibits NF-kappaB activity and synergizes with aspirin to induce apoptosis in human colon cancer cells. Oncogene, 19, 726-736.
22. Takada, Y. et al. (2004) Nonsteroidal anti-inflammatory agents differ in their ability to suppress NF-kappaB activation, inhibition of expression of cyclooxygenase-2 and cyclin D1, and abrogation of tumor cell proliferation. Oncogene, 23, 9247-9258.
23. Greten, F.R. et al. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell, 118, 285-296.
24. Stark, L.A. et al. (2005) Nucleolar sequestration of RelA (p65) regulates NF-kappaB-driven transcription and apoptosis. Mol. Cell. Biol., 25, 5985-6004.
25. Pahl, H.L. (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene, 18, 6853-6866.
26. Verma, I.M. (2004) Nuclear factor (NF)-kappaB proteins: therapeutic targets. Ann. Rheum. Dis., 63 (suppl. 2), ii57-ii61.
27. Kim, H.J. et al. (2006) NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ., 13, 738-747.
28. Baud, V. et al. (2009) Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov., 8, 33-40.
29. Perkins, N.D. et al. (2006) Good cop, bad cop: the different faces of NF-kappaB. Cell Death Differ., 13, 759-772.
30. Farhana, L. et al. (2005) Apoptosis induction by a novel retinoid-related molecule requires nuclear factor-kappaB activation. Cancer Res., 65, 4909-4917.
31. Jin, F. et al. (2005) Activation of nuclear factor-kappaB contributes to induction of death receptors and apoptosis by the synthetic retinoid CD437 in DU145 human prostate cancer cells. Cancer Res., 65, 6354-6363.
32. Stark, L.A. et al. (2001) Aspirin-induced activation of the NF-kappaB signaling pathway: a novel mechanism for aspirin-mediated apoptosis in colon cancer cells. FASEB J., 15, 1273-1275.
33. Kasperczyk, H. et al. (2005) Betulinic acid as new activator of NF-kappaB: molecular mechanisms and implications for cancer therapy. Oncogene, 24, 6945-6956.
34. Surh, Y.J. (2003) Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer, 3, 768-780. 35. Nihira, K. et al. (2010) Pim-1 controls NF-kappaB signalling by stabilizing RelA/p65. Cell Death Differ., 17, 689-698.
35. Nihira, K. et al. (2010) Pim-1 controls NF-kappaB signalling by stabilizing RelA/p65. Cell Death Differ., 17, 689-698.
36. Joo, J.H. et al. (2008) NF-kappaB-dependent transcriptional activation in lung carcinoma cells by farnesol involves p65/RelA(Ser276) phosphorylation via the MEK-MSK1 signaling pathway. J. Biol. Chem., 283, 16391-16399.
37. Kefaloyianni, E. et al. (2006) ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-kappaB transactivation during oxidative stress in skeletal myoblasts. Cell. Signal., 18, 2238-2251.
38. Bohuslav, J. et al. (2004) p53 induces NF-kappaB activation by an IkappaB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1. J. Biol. Chem., 279, 26115-26125.
39. Ryan, K.M. et al. (2000) Role of NF-kappaB in p53-mediated programmed cell death. Nature, 404, 892-897.
40. She, Q.B. et al. (2000) ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J. Biol. Chem., 275, 20444-20449.
41. Kawauchi, K. et al. (2008) Activated p53 induces NF-kappaB DNA binding but suppresses its transcriptional activation. Biochem. Biophys. Res. Commun., 372, 137-141.
42. Kawauchi, K. et al. (2008) p53 regulates glucose metabolism through an IKK-NF-kappaB pathway and inhibits cell transformation. Nat. Cell Biol., 10, 611-618.
43. Schneider, G. et al. (2010) Cross talk between stimulated NF-kappaB and the tumor suppressor p53. Oncogene, 29, 2795-2806.
44. Okazaki, T. et al. (2007) Induction of Fas (CD95/APO-1) ligand is essential for p53-dependent apoptosis in an in vitro renal carcinoma model system. J. Cancer Res. Clin. Oncol., 133, 581-588.
45. Müller, M. et al. (1997) Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J. Clin. Invest., 99, 403-413.
46. Kasibhatla, S. et al. (1998) DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol. Cell, 1, 543-551.
47. Ryo, A. et al. (2003) Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell, 12, 1413-1426.
48. Saccani, S. et al. (2004) Degradation of promoter-bound p65/RelA is essential for the prompt termination of the nuclear factor kappaB response. J. Exp. Med., 200, 107-113.
49. Carmody, R.J. et al. (2007) Negative regulation of toll-like receptor signaling by NF-kappaB p50 ubiquitination blockade. Science, 317, 675-678.
50. Maine, G.N. et al. (2007) COMMD1 promotes the ubiquitination of NF-kappaB subunits through a cullin-containing ubiquitin ligase. EMBO J., 26, 436-447.
51. Haupt, Y. et al. (1997) Mdm2 promotes the rapid degradation of p53. Nature, 387, 296-299.
52. Kubbutat, M.H. et al. (1997) Regulation of p53 stability by Mdm2. Nature, 387, 299-303.
53. Fujioka, S. et al. (2004) Stabilization of p53 is a novel mechanism for proapoptotic function of NF-kappaB. J. Biol. Chem., 279, 27549-27559.
54. Campbell, K.J. et al. (2004) Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B. Mol. Cell, 13, 853-865.
55. Matsui, K. et al. (1998) Identification of two NF-?B sites in mouse CD95 ligand (Fas ligand) promoter: functional analysis in T cell hybridoma. J. Immunol., 161, 3469-3473.
56. Mondor, I. et al. (2005) RelA regulates the survival of activated effector CD8 T cells. Cell Death Differ., 12, 1398-1406