Induction but not inhibition of COX-2 confers human lung cancer cell apoptosis by celecoxib

Journal of Lipid Research

Volumn 54, Issue 11, 2013, Pages 3116-3129

  Ramer, Robert ^a   Walther, Udo ^a   Borchert, Philipp ^a   Laufer, Stefan ^b   Linnebacher, Michael ^a   Hinz, Burkhard ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cyclooxygenase 2; Nonsteroidal antiinflammatory drugs; Peroxisome proliferator activated receptor gamma; Prostaglandins

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; CELECOXIB; CYCLOOXYGENASE 2; MESSENGER RNA; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN D2; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLOOD LEVEL; CANCER CELL CULTURE; CELL TRANSPORT; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; HUMAN; HUMAN CELL; IC 50; LUNG CANCER; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; UPREGULATION;

CYCLOOXYGENASE-2; NONSTEROIDAL ANTIINFLAMMATORY DRUGS; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDINS;

ANILIDES; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL NUCLEUS; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; ENZYME INDUCTION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SPACE; LUNG NEOPLASMS; NITROBENZENES; PPAR GAMMA; PROSTAGLANDINS; PROTEIN TRANSPORT; PYRAZOLES; SULFONAMIDES;

EID: 84886024736     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M042283     Document Type: Article

References (68)

1. McAdam, B. F., F. Catella Lawson, I. A. Mardini, S. Kapoor, J. A. Lawson, and G. A. FitzGerald. 1999. Systemic biosynthesis of prostacyclin by cyclooxygenase (COX)-2: the human pharmacology of a selective inhibitor of COX-2. Proc. Natl. Acad. Sci. USA. 96: 272-277. (Pubitemid 29036089)
2. Steinbach, G., P. M. Lynch, R. K. Phillips, M. H. Wallace, E. Hawk, G. B. Gordon, N. Wakabayashi, B. Saunders, Y. Shen, T. Fujimura, et al. 2000. The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N. Engl. J. Med. 342: 1946-1952. (Pubitemid 30419089)
3. Bertagnolli, M. M., C. J. Eagle, A. G. Zauber, M. Redston, S. D. Solomon, K. Kim, J. Tang, R. B. Rosenstein, J. Wittes, D. Corle, et al. 2006. Celecoxib for the prevention of sporadic colorectal adenomas. N. Engl. J. Med. 355: 873-884. (Pubitemid 44315980)
4. Edelman, M. J., D. Watson, X. Wang, C. Morrison, R. A. Kratzke, S. Jewell, L. Hodgson, A. M. Mauer, A. Gajra, G. A. Masters, et al. 2008. Eicosanoid modulation in advanced lung cancer: cyclooxygenase-2 expression is a positive predictive factor for celecoxib + chemotherapy-Cancer and Leukemia Group B Trial 30203. J. Clin. Oncol. 26: 848-855. (Pubitemid 351398075)
5. Wang, Z., J. Duan, Q. Guo, Z. Wei, W. Xue, M. Wu, J. Zhao, L. Yang, T. An, X. Liu, et al. 2008. A phase II clinical trial of celecoxib combined with platinum-based chemotherapy in the treatment of patients with advanced NSCLC as first-line treatment [article in Chinese]. Zhongguo Fei Ai Za Zhi. 11: 425-430. (Pubitemid 351976681)
6. Kim, E. S., W. K. Hong, J. J. Lee, L. Mao, R. C. Morice, D. D. Liu, C. A. Jimenez, G. A. Eapen, R. Lotan, X. Tang, et al. 2010. Biological activity of celecoxib in the bronchial epithelium of current and former smokers. Cancer Prev. Res. (Phila.). 3: 148-159.
7. Mao, J. T., M. D. Roth, M. C. Fishbein, D. R. Aberle, Z. F. Zhang, J. Y. Rao, D. P. Tashkin, L. Goodglick, E. C. Holmes, R. B. Cameron, et al. 2011. Lung cancer chemoprevention with celecoxib in former smokers. Cancer Prev. Res. (Phila.). 4: 984-993.
8. Altorki, N. K., R. S. Keresztes, J. L. Port, D. M. Libby, R. J. Korst, D. B. Flieder, C. A. Ferrara, D. F. Yankelevitz, K. Subbaramaiah, M. W. Pasmantier, et al. 2003. Celecoxib, a selective cyclo-oxygenase-2 inhibitor, enhances the response to preoperative paclitaxel and carboplatin in early-stage non-small-cell lung cancer. J. Clin. Oncol. 21: 2645-2650. (Pubitemid 46606306)
9. Ferlay, J., H. R. Shin, F. Bray, D. Forman, C. Mathers, and D. M. Parkin. 2010. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer. 127: 2893-2917.
10. Masferrer, J. L., K. M. Leahy, A. T. Koki, B. S. Zweifel, S. L. Settle, B. M. Woerner, D. A. Edwards, A. G. Flickinger, R. J. Moore, and K. Seibert. 2000. Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors. Cancer Res. 60: 1306-1311. (Pubitemid 30151999)
11. Williams, C. S., A. J. Watson, H. Sheng, R. Helou, J. Shao, and R. N. DuBois. 2000. Celecoxib prevents tumor growth in vivo without toxicity to normal gut: lack of correlation between in vitro and in vivo models. Cancer Res. 60: 6045-6051.
12. Grösch, S., I. Tegeder, E. Niederberger, L. Bräutigam, and G. Geisslinger. 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.
13. Blumenthal, R. D., C. Waskewich, D. M. Goldenberg, W. Lew, C. Flefleh, and J. Burton. 2001. Chronotherapy and chronotoxicity of the cyclooxygenase-2 inhibitor, celecoxib, in athymic mice bearing human breast cancer xenografts. Clin. Cancer Res. 7: 3178-3185. (Pubitemid 32963841)
14. Shaik, M. S., A. Chatterjee, T. Jackson, and M. Singh. 2006. Enhancement of antitumor activity of docetaxel by celecoxib in lung tumors. Int. J. Cancer. 118: 396-404. (Pubitemid 41779079)
15. Grösch, S., T. J. Maier, S. Schiffmann, and G. Geisslinger. 2006. Cyclooxygenase-2 (COX-2)-independent anticarcinogenic effects of selective COX-2 inhibitors. J. Natl. Cancer Inst. 98: 736-747. (Pubitemid 43983297)
16. Zhang, X., S. G. Morham, R. Langenbach, and D. A. Young. 1999. Malignant transformation and antineoplastic actions of nonsteroidal antiinflammatory drugs (NSAIDs) on cyclooxygenase-null embryo fibroblasts. J. Exp. Med. 190: 451-459. (Pubitemid 29395373)
17. Hwang, D. H., V. Fung, and A. J. Dannenberg. 2002. National Cancer Institute workshop on chemopreventive properties of nonsteroidal anti-inflammatory drugs: role of COX-dependent and -independent mechanisms. Neoplasia. 4: 91-97. (Pubitemid 34218676)
18. Denkert, C., A. Fürstenberg, P. T. Daniel, I. Koch, M. Kobel, W. Weichert, A. Siegert, and S. Hauptmann. 2003. Induction of G0/G1 cell cycle arrest in ovarian carcinoma cells by the anti-inflammatory drug NS-398, but not by COX-2-specific RNA interference. Oncogene. 22: 8653-8661. (Pubitemid 38010488)
19. Tsujii, M., and R. N. DuBois. 1995. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell. 83: 493-501.
20. Gupta, R. A., and R. N. Dubois. 2001. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat. Rev. Cancer. 1: 11-21. (Pubitemid 33741877)
21. Xu, Z., S. Choudhary, O. Voznesensky, M. Mehrotra, M. Woodard, M. Hansen, H. Herschman, and C. Pilbeam. 2006. Overexpression of COX-2 in human osteosarcoma cells decreases proliferation and increases apoptosis. Cancer Res. 66: 6657-6664. (Pubitemid 44085622)
22. Bol, D. K., R. B. Rowley, C. P. Ho, B. Pilz, J. Dell, M. Swerdel, K. Kiguchi, S. Muga, R. Klein, and S. M. Fischer. 2002. Cyclooxygenase-2 overexpression in the skin of transgenic mice results in suppression of tumor development. Cancer Res. 62: 2516-2521. (Pubitemid 34462728)
23. Maccarrone, M., R. Pauselli, M. Di Rienzo, and A. Finazzi-Agrò. 2002. Binding, degradation and apoptotic activity of stearoylethanolamide in rat C6 glioma cells. Biochem. J. 366: 137-144. (Pubitemid 34971812)
24. Munkarah, A. R., Z. Genhai, R. Morris, V. V. Baker, G. Deppe, M. P. Diamond, and G. M. Saed. 2003. Inhibition of paclitaxel-induced apoptosis by the specific COX-2 inhibitor, NS-398, in epithelial ovarian cancer cells. Gynecol. Oncol. 88: 429-433. (Pubitemid 36332001)
25. Hinz, B., R. Ramer, K. Eichele, U. Weinzierl, and K. Brune. 2004. Up-regulation of cyclooxygenase-2 expression is involved in R(+)-methanandamide- induced apoptotic death of human neuroglioma cells. Mol. Pharmacol. 66: 1643-1651. (Pubitemid 39564792)
26. Na, H. K., H. Inoue, and Y. J. Surh. 2005. ET-18-O-CH3-induced apoptosis is causally linked to COX-2 upregulation in H-ras transformed human breast epithelial cells. FEBS Lett. 579: 6279-6287. (Pubitemid 41546279)
27. Eichele, K., R. Ramer, and B. Hinz. 2008. Decisive role of cyclooxygenase-2 and lipocalin-type prostaglandin D synthase in chemotherapeutics-induced apoptosis of human cervical carcinoma cells. Oncogene. 27: 3032-3044. (Pubitemid 351668009)
28. Eichele, K., R. Ramer, and B. Hinz. 2009. R(+)-methanandamideinduced apoptosis of human cervical carcinoma cells involves a cyclooxygenase-2- dependent pathway. Pharm. Res. 26: 346-355.
29. Elrod, H. A., P. Yue, F. R. Khuri, and S. Y. Sun. 2009. Celecoxib antagonizes perifosine's anticancer activity involving a cyclooxygenase-2- dependent mechanism. Mol. Cancer Ther. 8: 2575-2585.
30. Kuc, C., A. Jenkins, and R. T. Van Dross. 2012. Arachidonoyl ethanolamide (AEA)-induced apoptosis is mediated by J-series prostaglandins and is enhanced by fatty acid amide hydrolase (FAAH) blockade. Mol. Carcinog. 51: 139-149.
31. Clay, C. E., A. M. Namen, G. Atsumi, M. C. Willingham, H. P. High, T. E. Kute, A. J. Trimboli, A. N. Fonteh, P. A. Dawson, and F. H. Chilton. 1999. Influence of J series prostaglandins on apoptosis and tumorigenesis of breast cancer cells. Carcinogenesis. 20: 1905-1911. (Pubitemid 29476115)
32. Na, H. K., and Y. J. Surh. 2003. Peroxisome proliferator-activated receptor gamma (PPARgamma) ligands as bifunctional regulators of cell proliferation. Biochem. Pharmacol. 66: 1381-1391.
33. Kim, J., P. Yang, M. Suraokar, A. L. Sabichi, N. D. Llansa, G. Mendoza, V. Subbarayan, C. J. Logothetis, R. A. Newman, S. M. Lippman, et al. 2005. Suppression of prostate tumor cell growth by stromal cell prostaglandin D synthase-derived products. Cancer Res. 65: 6189-6198. (Pubitemid 40994404)
34. Dai, Y., L. Qiao, K. W. Chan, M. Yang, J. Ye, J. Ma, B. Zou, Q. Gu, J. Wang, R. Pang, et al. 2009. Peroxisome proliferator-activated receptor γ contributes to the inhibitory effects of Embelin on colon carcinogenesis. Cancer Res. 69: 4776-4783.
35. Schwab, M., V. Reynders, S. Loitsch, Y. M. Shastri, D. Steinhilber, O. Schröder, and J. Stein. 2008. PPARγ is involved in mesalazinemediated induction of apoptosis and inhibition of cell growth in colon cancer cells. Carcinogenesis. 29: 1407-1414.
36. Keshamouni, V. G., R. C. Reddy, D. A. Arenberg, B. Joel, V. J. Thannickal, G. P. Kalemkerian, and T. J. Standiford. 2004. Peroxisome proliferator-activated receptor γ activation inhibits tumor progression in non-small-cell lung cancer. Oncogene. 23: 100-108. (Pubitemid 38142244)
37. Chen, Z., X. Zhang, M. Li, Z. Wang, H. S. Wieand, J. R. Grandis, and D. M. Shin. 2004. Simultaneously targeting epidermal growth factor receptor tyrosine kinase and cyclooxygenase-2, an efficient approach to inhibition of squamous cell carcinoma of the head and neck. Clin. Cancer Res. 10: 5930-5939. (Pubitemid 39180975)
38. Bock, J. M., S. G. Menon, L. L. Sinclair, N. S. Bedford, P. C. Goswami, F. E. Domann, and D. K. Trask. 2007. Celecoxib toxicity is cell cycle phase specific. Cancer Res. 67: 3801-3808. (Pubitemid 46762167)
39. Fulzele, S. V., M. S. Shaik, A. Chatterjee, and M. Singh. 2006. Anticancer effect of celecoxib and aerosolized docetaxel against human non-small cell lung cancer cell line, A549. J. Pharm. Pharmacol. 58: 327-336. (Pubitemid 43344575)
40. Vaish, V., L. Tanwar, and S. N. Sanyal. 2010. The role of NF-κB and PPARγ in experimentally induced colorectal cancer and chemoprevention by cyclooxygenase-2 inhibitors. Tumour Biol. 31: 427-436.
41. Zhang, M., Z. G. Xu, Z. Shi, D. Shao, O. Li, W. Li, Z. J. Li, K. Z. Wang, and L. Chen. 2011. Inhibitory effect of celecoxib in lung carcinoma by regulation of cyclooxygenase-2/cytosolic phospholipase A 2 and peroxisome proliferator-activated receptor gamma. Mol. Cell. Biochem. 355: 233-240.
42. López-Parra, M., J. Clària, E. Titos, A. Planagumà, M. Párrizas, J. L. Masferrer, W. Jiménez, V. Arroyo, F. Rivera, and J. Rodés. 2005. The selective cyclooxygenase-2 inhibitor celecoxib modulates the formation of vasoconstrictor eicosanoids and activates PPARgamma. Influence of albumin. J. Hepatol. 42: 75-81. (Pubitemid 40038903)
43. Shibuya, A., K. Wada, A. Nakajima, M. Saeki, K. Katayama, T. Mayumi, T. Kadowaki, H. Niwa, and Y. Kamisaki. 2002. Nitration of PPARγ inhibits ligand-dependent translocation into the nucleus in a macrophage-like cell line, RAW 264. FEBS Lett. 525: 43-47.
44. Rousseaux, C., B. Lefebvre, L. Dubuquoy, P. Lefebvre, O. Romano, J. Auwerx, D. Metzger, W. Wahli, B. Desvergne, G. C. Naccari, et al. 2005. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator-activated receptor γ. J. Exp. Med. 201: 1205-1215. (Pubitemid 40629065)
45. Bocca, C., F. Bozzo, S. Francica, S. Colombatto, and A. Miglietta. 2007. Involvement of PPARγ and E-cadherin/beta-catenin pathway in the antiproliferative effect of conjugated linoleic acid in MCF-7 cells. Int. J. Cancer. 121: 248-256. (Pubitemid 46917692)
46. Paik, J. H., J. H. Ju, J. Y. Lee, M. D. Boudreau, and D. H. Hwang. 2000. Two opposing effects of non-steroidal anti-inflammatory drugs on the expression of the inducible cyclooxygenase. Mediation through different signaling pathways. J. Biol. Chem. 275: 28173-28179.
47. 12,14 -prostaglandin J 2 inhibits the synthesis of the acute phase protein SIP24 in cartilage: Involvement of COX-2 in resolution of inflammation. J. Cell. Physiol. 217: 433-441.
48. Ayoub, S. S., R. M. Botting, A. N. Joshi, M. P. Seed, and P. R. Colville-Nash. 2009. Activation of macrophage peroxisome proliferator-activated receptor-gamma by diclofenac results in the induction of cyclooxygenase-2 protein and the synthesis of anti-inflammatory cytokines. Mol. Cell. Biochem. 327: 101-110.
49. Wick, M., G. Hurteau, C. Dessev, D. Chan, M. W. Geraci, R. A. Winn, L. E. Heasley, and R. A. Nemenoff. 2002. Peroxisome proliferatoractivated receptor-gamma is a target of nonsteroidal anti-inflammatory drugs mediating cyclooxygenase-independent inhibition of lung cancer cell growth. Mol. Pharmacol. 62: 1207-1214. (Pubitemid 35222513)
50. Yamazaki, R., N. Kusunoki, T. Matsuzaki, S. Hashimoto, and S. Kawai. 2002. Nonsteroidal anti-inflammatory drugs induce apoptosis in association with activation of peroxisome proliferator-activated receptor gamma in rheumatoid synovial cells. J. Pharmacol. Exp. Ther. 302: 18-25. (Pubitemid 34680416)
51. Kusunoki, N., R. Yamazaki, and S. Kawai. 2002. Induction of apoptosis in rheumatoid synovial fibroblasts by celecoxib, but not by other selective cyclooxygenase 2 inhibitors. Arthritis Rheum. 46: 3159-3167. (Pubitemid 35453524)
52. 12,14 -prostaglandin J 2 enhances docetaxel anti-tumor activity against A549 and H460 non-small-cell lung cancer cell lines and xenograft tumors. Anticancer Drugs. 18: 65-78. (Pubitemid 44963416)
53. Lu, X., W. Xie, D. Reed, W. S. Bradshaw, and D. L. Simmons. 1995. Nonsteroidal anti-inflammatory drugs cause apoptosis and induce cyclooxygenases in chicken embryo fibroblasts. Proc. Natl. Acad. Sci. USA. 92: 7961-7965.
54. Lu, X., D. W. Fairbairn, W. S. Bradshaw, K. L. O'Neill, D. L. Ewert, and D. L. Simmons. 1997. NSAID-induced apoptosis in Rous sarcoma virus-transformed chicken embryo fibroblasts is dependent on v-src and c-myc and is inhibited by bcl-2. Prostaglandins. 54: 549-568. (Pubitemid 27444147)
55. Meade, E. A., T. M. McIntyre, G. A. Zimmerman, and S. M. Prescott. 1999. Peroxisome proliferators enhance cyclooxygenase-2 expression in epithelial cells. J. Biol. Chem. 274: 8328-8334.
56. Simmons, D. L., R. M. Botting, P. M. Robertson, M. L. Madsen, and J. R. Vane. 1999. Induction of an acetaminophen-sensitive cyclooxygenase with reduced sensitivity to nonsteroid antiinflammatory drugs. Proc. Natl. Acad. Sci. USA. 96: 3275-3280. (Pubitemid 29148881)
57. Elder, D. J., D. E. Halton, T. E. Crew, and C. Paraskeva. 2000. Apoptosis induction and cyclooxygenase-2 regulation in human colorectal adenoma and carcinoma cell lines by the cyclooxygenase-2 selective non-steroidal anti-inflammatory drug NS-398. Int. J. Cancer. 86: 553-560. (Pubitemid 30249738)
58. Elder, D. J., D. E. Halton, L. C. Playle, and C. Paraskeva. 2002. The MEK/ERK pathway mediates COX-2-selective NSAID-induced apoptosis and induced COX-2 protein expression in colorectal carcinoma cells. Int. J. Cancer. 99: 323-327. (Pubitemid 34495845)
59. Williams, J. L., N. Nath, J. Chen, T. R. Hundley, J. Gao, L. Kopelovich, K. Kashfi, and B. Rigas. 2003. Growth inhibition of human colon cancer cells by nitric oxide (NO)-donating aspirin is associated with cyclooxygenase-2 induction and beta-catenin/T-cell factor signaling, nuclear factor-kappaB, and NO synthase 2 inhibition: implications for chemoprevention. Cancer Res. 63: 7613-7618. (Pubitemid 37466683)
60. Niederberger, E., I. Tegeder, G. Vetter, A. Schmidtko, H. Schmidt, C. Euchenhofer, L. Bräutigam, S. Grösch, and G. Geisslinger. 2001. Celecoxib loses its anti-inflammatory efficacy at high doses through activation of NF-kappaB. FASEB J. 15: 1622-1624.
61. Cerella, C., C. Sobolewski, S. Chateauvieux, E. Henry, M. Schnekenburger, J. Ghelfi, M. Dicato, and M. Diederich. 2011. COX-2 inhibitors block chemotherapeutic agent-induced apoptosis prior to commitment in hematopoietic cancer cells. Biochem. Pharmacol. 82: 1277-1290.
62. Hausman, N., K. D. Beharry, K. C. Nishihara, Y. Akmal, and T. Asrat. 2003. Effect of the antenatal administration of celecoxib during the second and third trimesters of pregnancy on prostaglandin, cytokine, and nitric oxide levels in rabbits. Am. J. Obstet. Gynecol. 189: 1737-1743. (Pubitemid 38056453)
63. Hausman, N., K. Beharry, K. Nishihara, Y. Akmal, Y. Stavitsky, and T. Asrat. 2003. Response of fetal prostanoids, nitric oxide, and ductus arteriosus to the short- and long-term antenatal administration of celecoxib, a selective cyclo-oxygenase-2 inhibitor, in the pregnant rabbit. Am. J. Obstet. Gynecol. 189: 1744-1750. (Pubitemid 38056454)
64. Mitchell, J. A., M. Saunders, P. J. Barnes, R. Newton, and M. G. Belvisi. 1997. Sodium salicylate inhibits cyclo-oxygenase-2 activity independently of transcription factor (nuclear factor kappaB) activation: role of arachidonic acid. Mol. Pharmacol. 51: 907-912. (Pubitemid 27249123)
65. Lucas, R., T. D. Warner, I. Vojnovic, and J. A. Mitchell. 2005. Cellular mechanisms of acetaminophen: role of cyclo-oxygenase. FASEB J. 19: 635-637. (Pubitemid 40471269)
66. Xu, Z., M. Zhang, X. Lv, D. Xiang, X. Zhang, and L. Chen. 2010. The inhibitory effect of celecoxib on mouse hepatoma H22 cell line on the arachidonic acid metabolic pathway. Biochem. Cell Biol. 88: 603-609.
67. Schiffmann, S., T. J. Maier, I. Wobst, A. Janssen, H. Corban-Wilhelm, C. Angioni, G. Geisslinger, and S. Grösch. 2008. The anti-proliferative potency of celecoxib is not a class effect of coxibs. Biochem. Pharmacol. 76: 179-187.
68. Maier, T. J., S. Schiffmann, I. Wobst, K. Birod, C. Angioni, M. Hoffmann, J. J. Lopez, C. Glaubitz, D. Steinhilber, G. Geisslinger, et al. 2009. Cellular membranes function as a storage compartment for celecoxib. J. Mol. Med. 87: 981-993.