9-cis-Retinoic acid inhibition of lung carcinogenesis in the A/J mouse model is accompanied by increased expression of RAR-β but no change in cyclooxygenase-2

Cancer Letters

Volumn 244, Issue 1, 2006, Pages 101-108

  Mernitz, Heather ^a   Smith, Donald E ^a   Zhu, Andrew X ^b   Wang, Xiang Dong ^a  

^a TUFTS UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

9 cis Retinoic acid; Cyclooxygenase 2; Lung cancer; RAR

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ALITRETINOIN; CELECOXIB; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; MESSENGER RNA; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INCIDENCE; CANCER INHIBITION; CANCER MODEL; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; DRUG RECEPTOR BINDING; GENETIC TRANSCRIPTION; LUNG CARCINOGENESIS; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPPLEMENTATION; UPREGULATION; WEIGHT REDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOGENS; CELL TRANSFORMATION, NEOPLASTIC; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; LUNG; LUNG NEOPLASMS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED A; NITROSAMINES; PYRAZOLES; RECEPTORS, RETINOIC ACID; SULFONAMIDES; TRETINOIN;

EID: 33749236979     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2005.12.001     Document Type: Article

References (69)

1. Munker M., Munker R., Saxton R.E., and Koeffler H.P. Effect of recombinant monokines, lymphokines, and other agents on clonal proliferation of human lung cancer cell lines. Cancer Res. 47 (1987) 4081-4085
2. Guzey M., Demirpence E., Criss W., and DeLuca H.F. Effects of retinoic acid (all-trans and 9-cis) on tumor progression in small-cell lung carcinoma. Biochem. Biophys. Res. Commun. 242 (1998) 369-375
3. Sun S.Y., Kurie J.M., Yue P., Dawson M.I., Shroot B., Chandraratna R.A., et al. Differential responses of normal, premalignant, and malignant human bronchial epithelial cells to receptor-selective retinoids. Clin. Cancer Res. 5 (1999) 431-437
4. Mangelsdorf D.J., Umesono K., and Evans R.M. The retinoid receptors. In: Sporn M.B., Roberts A.B., and Goodman D.S. (Eds). The Retinoids: Biology, Chemistry, and Medicine (1994), Raven Press, Ltd, New York 319-349 1994
5. Xu X.C., Sozzi G., Lee J.S., Lee J.J., Pastorino U., Pilotti S., et al. Suppression of retinoic acid receptor beta in non-small-cell lung cancer in vivo: implications for lung cancer development. J. Natl Cancer Inst. 89 (1997) 624-629
6. Xu X.C., Lee J.S., Lee J.J., Morice R.C., Liu X., Lippman S.M., et al. Nuclear retinoid acid receptor beta in bronchial epithelium of smokers before and during chemoprevention. J. Natl Cancer Inst. 91 (1999) 1317-1321
7. Qiu H., Zhang W., El-Naggar A.K., Lippman S.M., Lin P., Lotan R., and Xu X.C. Loss of retinoic acid receptor-beta expression is an early event during esophageal carcinogenesis. Am. J. Pathol. 155 (1999) 1519-1523
8. Sun S.Y., Wan H., Yue P., Hong W.K., and Lotan R. Evidence that retinoic acid receptor beta induction by retinoids is important for tumor cell growth inhibition. J. Biol. Chem. 275 (2000) 17149-17153
9. Heyman R.A., Mangelsdorf D.J., Dyck J.A., Stein R.B., Eichele G., Evans R.M., and Thaller C. 9-cis-Retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68 (1992) 397-406
10. Kurie J.M., Lotan R., Lee J.J., Lee J.S., Morice R.C., Liu D.D., et al. Treatment of former smokers with 9-cis-retinoic acid reverses loss of retinoic acid receptor-beta expression in the bronchial epithelium: results from a randomized placebo-controlled trial. J. Natl Cancer Inst. 95 (2003) 206-214
11. Lee H.Y., Chang Y.S., Han J.Y., Liu D.D., Lee J.J., Lotan R., et al. Effects of 9-cis-retinoic acid on the insulin-like growth factor axis in former smokers. J. Clin. Oncol. 23 (2005) 4439-4449
12. Rosati R., Ramnath N., Adil M.R., Ou X., Ali M.A., Heyman R.A., and Kalemkerian G.P. Activity of 9-cis-retinoic acid and receptor-selective retinoids in small cell lung cancer cell lines. Anticancer Res. 18 (1998) 4071-4075
13. Takahashi T., Kozaki K., Yatabe Y., Achiwa H., and Hida T. Increased expression of COX-2 in the development of human lung cancers. J. Environ. Pathol. Toxicol. 21 (2002) 177-181
14. Hida T., Yatabe Y., Achiwa H., Muramatsu H., Kozaki K., Nakamura S., et al. Increased expression of cyclooxygenase 2 occurs frequently in human lung cancers, specifically in adenocarcinomas. Cancer Res. 58 (1998) 3761-3764
15. Khuri F.R., Wu H., Lee J.J., Kemp B.L., Lotan R., Lippman S.M., et al. Cyclooxygenase-2 overexpression is a marker of poor prognosis in stage I non-small cell lung cancer. Clin. Cancer Res. 7 (2001) 861-867
16. Achiwa H., Yatabe Y., Hida T., Kuroishi T., Kozaki K., Nakamura S., et al. Prognostic significance of elevated cyclooxygenase 2 expression in primary, resected lung adenocarcinomas. Clin. Cancer Res. 5 (1999) 1001-1005
17. Wolff H., Saukkonen K., Anttila S., Karjalainen A., Vainio H., and Ristimaki A. Expression of cyclooxygenase-2 in human lung carcinoma. Cancer Res. 58 (1998) 4997-5001
18. Qadri S.S., Wang J.H., Redmond K.C., AF O.D., Aherne T., and Redmond H.P. The role of COX-2 inhibitors in lung cancer. Ann. Thorac. Surg. 74 (2002) 1648-1652
19. Duperron C., and Castonguay A. Chemopreventive efficacies of aspirin and sulindac against lung tumorigenesis in A/J mice. Carcinogenesis 18 (1997) 1001-1006
20. Rioux N., and Castonguay A. Prevention of NNK-induced lung tumorigenesis in A/J mice by acetylsalicylic acid and NS-398. Cancer Res. 58 (1998) 5354-5360
21. Harris R.E., Beebe-Donk J., and Schuller H.M. Chemoprevention of lung cancer by non-steroidal anti-inflammatory drugs among cigarette smokers. Oncol. Rep. 9 (2002) 693-695
22. Song S., and Xu X.C. Effect of benzo[a]pyrene diol epoxide on expression of retinoic acid receptor-beta in immortalized esophageal epithelial cells and esophageal cancer cells. Biochem. Biophys. Res. Commun. 281 (2001) 872-877
23. Li M., Song S., Lippman S.M., Zhang X.K., Liu X., Lotan R., and Xu X.C. Induction of retinoic acid receptor-beta suppresses cyclooxygenase-2 expression in esophageal cancer cells. Oncogene 21 (2002) 411-418
24. Kanekura T., Higashi Y., and Kanzaki T. Inhibitory effects of 9-cis-retinoic acid and pyrrolidinedithiocarbamate on cyclooxygenase (COX)-2 expression and cell growth in human skin squamous carcinoma cells. Cancer Lett. 161 (2000) 177-183
25. Merritt G., Aliprandis E.T., Prada F., Rigas B., and Kashfi K. The retinoid fenretinide inhibits proliferation and downregulates cyclooxygenase-2 gene expression in human colon adenocarcinoma cell lines. Cancer Lett. 164 (2001) 15-23
26. Tsukamoto H., Hishinuma T., Tayama R., Narahara K., Suzuki N., Tomioka Y., and Goto J. The induction of prostaglandin E synthase and upregulation of cyclooxygenase-2 by 9-cis-retinoic acid. Prostaglandins Other Lipid Mediat. 74 (2004) 61-74
27. Mestre J.R., Subbaramaiah K., Sacks P.G., Schantz S.P., Tanabe T., Inoue H., and Dannenberg A.J. Retinoids suppress epidermal growth factor-induced transcription of cyclooxygenase-2 in human oral squamous carcinoma cells. Cancer Res. 57 (1997) 2890-2895
28. Mestre J.R., Subbaramaiah K., Sacks P.G., Schantz S.P., Tanabe T., Inoue H., and Dannenberg A.J. Retinoids suppress phorbol ester-mediated induction of cyclooxygenase-2. Cancer Res. 57 (1997) 1081-1085
29. Subbaramaiah K., Cole P.A., and Dannenberg A.J. Retinoids and carnosol suppress cyclooxygenase-2 transcription by CREB-binding protein/p300-dependent and -independent mechanisms. Cancer Res. 62 (2002) 2522-2530
30. Kong G., Kim H.T., Wu K., DeNardo D., Hilsenbeck S.G., Xu X.C., et al. The retinoid X receptor-selective retinoid, LGD1069, down-regulates cyclooxygenase-2 expression in human breast cells through transcription factor crosstalk: implications for molecular-based chemoprevention. Cancer Res. 65 (2005) 3462-3469
31. Mestre J.R., Chan G., Zhang F., Yang E.K., Sacks P.G., Boyle J.O., et al. Inhibition of cyclooxygenase-2 expression. An approach to preventing head and neck cancer. Ann. NY Acad. Sci. 889 (1999) 62-71
32. Huang C., Ma W.-Y., Dawson M.I., Rincon M., Flavell R.A., and Dong Z. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc. Natl Acad. Sci. USA 94 (1997) 5826-5830
33. Reeves P.G., Nielsen F.H., and Fahey Jr. G.C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123 (1993) 1939-1951
34. Kurie J.M., Lee J.S., Griffin T., Lippman S.M., Drum P., Thomas M.P., et al. Phase I trial of 9-cis-retinoic acid in adults with solid tumors. Clin. Cancer Res. 2 (1996) 287-293
35. Masferrer J.L., Leahy K.M., Koki A.T., Zweifel B.S., Settle S.L., Woerner B.M., et al. Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors. Cancer Res. 60 (2000) 1306-1311
36. Gebert J.F., Moghal N., Frangioni J.V., Sugarbaker D.J., and Neel B.G. High frequency of retinoic acid receptor beta abnormalities in human lung cancer. Oncogene 6 (1991) 1859-1868
37. Geradts J., Chen J.Y., Russell E.K., Yankaskas J.R., Nieves L., and Minna J.D. Human lung cancer cell lines exhibit resistance to retinoic acid treatment. Cell Growth Differ. 4 (1993) 799-809
38. Murata H., Kawano S., Tsuji S., Tsuji M., Sawaoka H., Kimura Y., et al. Cyclooxygenase-2 overexpression enhances lymphatic invasion and metastasis in human gastric carcinoma. Am. J. Gastroenterol. 94 (1999) 451-455
39. Dohadwala M., Luo J., Zhu L., Lin Y., Dougherty G.J., Sharma S., et al. Non-small cell lung cancer cyclooxygenase-2-dependent invasion is mediated by CD44. J. Biol. Chem. 276 (2001) 20809-20812
40. Tsujii M., and DuBois R.N. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 83 (1995) 493-501
41. Ding X.Z., Tong W.G., and Adrian T.E. Blockade of cyclooxygenase-2 inhibits proliferation and induces apoptosis in human pancreatic cancer cells. Anticancer Res. 20 (2000) 2625-2631
42. Tsujii M., Kawano S., and DuBois R.N. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc. Natl Acad. Sci. USA 94 (1997) 3336-3340
43. Stolina M., Sharma S., Lin Y., Dohadwala M., Gardner B., Luo J., et al. Specific inhibition of cyclooxygenase 2 restores antitumor reactivity by altering the balance of IL-10 and IL-12 synthesis. J. Immunol. 164 (2000) 361-370
44. Huang M., Stolina M., Sharma S., Mao J.T., Zhu L., Miller P.W., et al. Non-small cell lung cancer cyclooxygenase-2-dependent regulation of cytokine balance in lymphocytes and macrophages: up-regulation of interleukin 10 and down-regulation of interleukin 12 production. Cancer Res. 58 (1998) 1208-1216
45. Hood W.F., Gierse J.K., Isakson P.C., Kiefer J.R., Kurumbail R.G., Seibert K., and Monahan J.B. Characterization of celecoxib and valdecoxib binding to cyclooxygenase. Mol. Pharmacol. 63 (2003) 870-877
46. Lin J., Hsiao P.-W., Chiu T.H., and Chao J.-I. Combination of cyclooxygenase-2 inhibitors and oxaliplatin increases the growth inhibition and death in human colon cancer cells. Biochem. Pharmacol. 70 (2005) 658-667
47. Sievers E.M., Bart R.D., Backhus L.M., Lin Y., Starnes M., Castanos R., et al. Evaluation of cyclooxygenase-2 inhibition in an orthotopic murine model of lung cancer for dose-dependent effect. J. Thorac. Cardiovasc. Surg. 129 (2005) 1242-1249
48. Chun K.-S., Kim S.-H., Song Y.-S., and Surh Y.-J. Celecoxib inhibits phorbol ester-induced expression of COX-2 and activation of AP-1 and p38 MAP kinase in mouse skin. Carcinogenesis 25 (2004) 713-722
49. Gupta S., Adhami V.M., Subbarayan M., MacLennan G.T., Lewin J.S., Hafeli U.O., et al. Suppression of prostate carcinogenesis by dietary supplementation of celecoxib in transgenic adenocarcinoma of the mouse prostate model. Cancer Res. 64 (2004) 3334-3343
50. Hashitani S., Urade M., Nishimura N., Maeda T., Takaoka K., Noguchi K., and Sakurai K. Apoptosis induction and enhancement of cytotoxicity of anticancer drugs by celecoxib, a selective cyclooxygenase-2 inhibitor, in human head and neck carcinoma cell lines. Int. J. Oncol. 23 (2003) 665-672
51. Swamy M.V., Cooma I., Patlolla J.M.R., Simi B., Reddy B.S., and Rao C.V. Modulation of cyclooxygenase-2 activities by the combined action of celecoxib and decosahexaenoic acid: novel strategies for colon cancer prevention and treatment. Mol. Cancer Ther. 3 (2004) 215-221
52. Sun S.Y., Yue P., Wu G.S., El-Deiry W.S., Shroot B., Hong W.K., and Lotan R. Implication of p53 in growth arrest and apoptosis induced by the synthetic retinoid CD437 in human lung cancer cells. Cancer Res. 59 (1999) 2829-2833
53. Sun S.Y., Yue P., Shroot B., Hong W.K., and Lotan R. Implication of c-Myc in apoptosis induced by the retinoid CD437 in human lung carcinoma cells. Oncogene 18 (1999) 3894-3901
54. Adachi H., Preston G., Harvat B., Dawson M.I., and Jetten A.M. Inhibition of cell proliferation and induction of apoptosis by the retinoid AHPN in human lung carcinoma cells. Am. J. Respir. Cell Mol. Biol. 18 (1998) 323-333
55. Hsu S., Hsu J., Liu M., Chen L., and Chang C. Retinoic acid-mediated G1 arrest is associated with induction of p27(Kip1) and inhibition of cyclin-dependent kinase 3 in human lung squamous carcinoma CH27 cells. Exp. Cell Res. 258 (2000) 322-331
56. Hsu S., Chen M., Chou Y., Hwang G., and Yin S. Induction of p21(CIP1/Waf1) and activation of p34(cdc2) involved in retinoic acid-induced apoptosis in human hepatoma Hep3B cells. Exp. Cell Res. 248 (1999) 87-96
57. Goralczyk R., Wertz K., Lenz B., Riss G., Buchwald Hunziker P., Geatrix B., et al. Beta-carotene interaction with NNK in the AJ-mouse model: effects on cell proliferation, tumor formation and retinoic acid responsive genes. Biochim. Biophys. Acta 1740 (2005) 179-188
58. Dahl A.R., Grossi I.M., Houchens D.P., Scovell L.J., Placke M.E., Imondi A.R., et al. Inhaled isotretinoin (13-cis-retinoic acid) is an effective lung cancer chemopreventive agent in A/J mice at low doses: a pilot study. Clin. Cancer Res. 6 (2000) 3015-3024
59. Xu X.C., Lee J.J., Wu T.T., Hoque A., Ajani J.A., and Lippman S.M. Increased retinoic acid receptor-β4 correlates in vivo with reduced retinoic acid receptor-β2 in esophageal squamous cell carcinoma. Cancer Epidemiol. Biomarkers Prev. 14 (2005) 826-829
60. Silverstein F.E., Faich G., Goldstein J.L., Simon L.S., Pincus T., Whelton A., et al. Gastrointestinal toxicity with celecoxib vs nonsteroidal anti-inflammatory drugs for osteoarthritis and rheumatoid arthritis: the CLASS study: a randomized controlled trial. J. Am. Med. Assoc. 284 (2000) 1247-1255
61. Langman M.J., Jensen D.M., Watson D.J., Harper S.E., Zhao P.L., Quan H., et al. Adverse upper gastrointestinal effects of rofecoxib compared with NSAIDs. J. Am. Med. Assoc. 282 (1999) 1929-1933
62. Bombardier C., Laine L., Reicin A., Shapiro D., Burgos-Vargas R., Davis B., et al. Comparison of upper gastrointestinal toxicity of rofecoxib and naproxen in patients with rheumatoid arthritis. N. Engl. J. Med. 343 (2000) 1520-1528
63. Laine L., Harper S., Simon T., Bath R., Johanson J., Schwartz H., et al. A randomized trial comparing the effect of rofecoxib, a cyclooxygenase 2-specific inhibitor, with that of ibuprofen on the gastroduodenal mucosa of patients with osteoarthritis. Rofecoxib Osteoarthritis Endoscopy Study Group. Gastroenterology 117 (1999) 776-783
64. Saukkonen K., Tomasetto C., Narko K., Rio M.-C., and Ristimaki A. Cyclooxygenase-2 expression and effect of celecoxib in gastric adenomas of trefoil factor 1-deficient mice. Cancer Res. 63 (2003) 3032-3036
65. Laine L., Maller E.S., Yu C., Quan H., and Simon T. Ulcer formation with low-dose enteric-coated aspirin and the effect of COX-2 selective inhibition: a double-blind trial. Gastroenterology 127 (2004) 395-402
66. Battistella M., Mamdami M.M., Juurlink D.N., Rabeneck L., and Laupacis A. Risk of upper gastrointestinal hemorrhage in warfarin users treated with nonselective NSAIDs or COX-2 inhibitors. Arch. Intern. Med. 165 (2005) 189-192
67. Halter F., Tarnawski A.S., Schmassmann A., and Peskar B.M. Cyclooxygenase 2-implications on maintenance of gastric mucosal integrity and ulcer healing: controversial issues and perspectives. Gut 49 (2001) 443-453
68. Wallace J.L., and Devchand P.R. Emerging roles for cyclooxygenase-2 in gastrointestinal mucosal defense. Br. J. Pharmacol. 145 (2005) 275-282
69. Jones M.K., Wang H., Peskar B.M., Levin E., Itani R.M., Sarfeh I.J., and Tarnawski A.S. Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing. Nat. Med. 5 (1999) 1418-1423