Inhibition of lung carcinogenesis by 1α,25-dihydroxyvitamin D 3 and 9-cis retinoic acid in the A/J mouse model: Evidence of retinoid mitigation of vitamin D toxicity

International Journal of Cancer

Volumn 120, Issue 7, 2007, Pages 1402-1409

  Mernitz, Heather ^a   Smith, Donald E ^a   Wood, Richard J ^a   Russell, Robert M ^a   Wang, Xiang Dong ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

1 ,25 dihydroxyvitamin D3; 9 cis retinoic acid; Lung cancer

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ALITRETINOIN; CALCITRIOL; CARCINOGEN; CYTOCHROME P450; CYTOCHROME P450 24; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CANCER PREVENTION; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; ISOTOPE LABELING; KIDNEY CALCIFICATION; KIDNEY PARENCHYMA; LUNG CARCINOGENESIS; LUNG CARCINOMA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RADIOIMMUNOASSAY; VITAMIN BLOOD LEVEL; VITAMIN D METABOLISM; VITAMIN INTAKE; WEIGHT REDUCTION;

ADENOMA; ANIMALS; ANTINEOPLASTIC AGENTS; CALCITRIOL; CARCINOGENS; CELL TRANSFORMATION, NEOPLASTIC; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; DRUG THERAPY, COMBINATION; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED A; NITROSAMINES; RETINOID X RECEPTORS; STEROID HYDROXYLASES; TRETINOIN; VITAMINS;

EID: 33847689364     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22462     Document Type: Article

References (54)

1. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, Feuer EJ, Thun MJ. Cancer Statistics, 2005. CA Cancer J Clin 2005;55:10-30.
2. Gudas LJ, Sporn MB, Roberts AB. Cellular biology and biochemistry of the retinoids. In: Sporn MB, Roberts AB, Goodman DS, eds. The retinoids: biology, chemistry, and medicine, 2nd edn. New York: Raven, 1994. 443-520.
3. Guzey M, Demirpence E, Criss W, DeLuca HF. Effects of retinoic acid (all-trans and 9-cis) on tumor progression in small-cell lung carcinoma. Biochem Biophys Res Commun 1998;242:369-75.
4. Saffiotti U, Montesano R, Sellakumar AR, Borg SA. Experimental cancer of the lung. Inhibition by vitamin A of the induction of tracheobronchial squamous metaplasia and squamous cell tumors. Cancer 1967;20:857-64.
5. Nettesheim P, Williams ML. The influence of vitamin A on the susceptibility of the rat lung to 3-methylcholanthrene. Int J Cancer 1976;17:351-7.
6. Dahl AR, Grossi IM, Houchens DP, Scovell LJ, Placke ME, Imondi AR, Stoner GD, De Luca LM, Wang D, Mulshine JL. 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 2000;6:3015-24.
7. Ki Hong WK, Itri LM. Retinoids and human cancer. In: Goodman DS, ed. The retinoids: biology, chemistry, and medicine, 2nd edn. New York: Raven, 1994. 597-630.
8. Kurie JM, Lee JS, Griffin T, Lippman SM, Drum P, Thomas MP, Weber C, Bader M, Massimini G, Hong WK. Phase I trial of 9-cis retinoic acid in adults with solid tumors. Clin Cancer Res 1996;2:287-93.
9. Lee JS, Lippman SM, Benner SE, Lee JJ, Ro JY, Lukeman JM, Morice RC, Peters EJ, Pang AC, Fritsche HA, Jr. Randomized placebo-controlled trial of isotretinoin in chemoprevention of bronchial squamous metaplasia. J Clin Oncol 1994;12:937-45.
10. Lippman SM, Lee JJ, Karp DD, Vokes EE, Benner SE, Goodman GE, Khuri FR, Marks R, Winn RJ, Fry W, Graziano SL, Gandara DR, et al. Randomized phase III intergroup trial of isotretinoin to prevent second primary tumors in stage I non-small-cell lung cancer. J Natl Cancer Inst 2001;93:605-18.
11. Pastorino U, Infante M, Maioli M, Chiesa G, Buyse M, Firket P, Rosmentz N, Clerici M, Soresi E, Valente M. Adjuvant treatment of stage I lung cancer with high-dose vitamin A. J Clin Oncol 1993;11:1216-22.
12. Mangelsdorf DJ, Umesono K, Evans RM. The retinoid receptors. In: Sporn MB, Roberts AB, Goodman DS, eds. The retinoids: biology, chemistry, and medicine, 2nd edn. New York: Raven, 1994. 319-49.
13. Kurie JM, Lotan R, Lee JJ, Lee JS, Morice RC, Liu DD, Xu XC, Khuri FR, Ro JY, Hittelman WN, Walsh GL, Roth JA, et al. Treatment of former smokers with 9-cis-retinoic acid reverses loss of retinoic acid receptor-β expression in the bronchial epithelium: results from a randomized placebo-controlled trial. J Natl Cancer Inst 2003;95:206-14.
14. Mernitz H, Smith DE, Zhu AX, Wang X-D. 9-cis Retinoic acid inhibition of lung carcinogenesis in the A/J mouse model is accompanied by increased expression of RARβ but no change in cyclooxygenase-2. Cancer Lett 2006;244:101-8.
15. Grant WB. Ecologic studies of solar UV-B radiation and cancer mortality rates. Recent Results Cancer Res 2003;164:371-7.
16. Garland C, Comstock G, Garland F, Helsing K, Shaw E, Gorham E. Serum 25-hydroxyvitamin D and colon cancer: eight-year prospective study. Lancet 1989;2:1176-8.
17. Corder EH, Guess HA, Hulka BS, Friedman GD, Sadler M, Vollmer RT, Lobaugh B, Drezner MK, Vogelman JH, Orentreich N. Vitamin D and prostate cancer: a prediagnostic study with stored sera. Cancer Epidemiol Biomarkers Prev 1993;2:467-72.
18. Lin R, Nagai Y, Sladek R, Bastien Y, Ho J, Petrecca K, Sotiropoulou G, Diamandis EP, Hudson TJ, White JH. Expression profiling in squamous carcinoma cells reveals pleiotropic effects of vitamin D3 analog EB1089 signaling on cell proliferation, differentiation, and immune system regulation. Mol Endocrinol 2002;16:1243-56.
19. Akutsu N, Lin R, Bastien Y, Bestawros A, Enepekides DJ, Black MJ, White JH. Regulation of gene expression by 1α,25-dihydroxyvitamin D3 and its analog EB1089 under growth-inhibitory conditions in squamous carcinoma cells. Mol Endocrinol 2001;15:1127-39.
20. 1-S phase-controlling machinery. Mol Endocrinol 2001;15:1370-80.
21. Nakagawa K, Kawaura A, Kato S, Takeda E, Okano T. Metastatic growth of lung cancer cells is extremely reduced in vitamin D receptor knockout mice. J Steroid Biochem Mol Biol 2004;89/90:545-7.
22. Zhou W, Suk R, Liu G, Park S, Neuberg DS, Wain JC, Lynch TJ, Giovannucci E, Christiani DC. Vitamin D is associated with improved survival in early-stage non-small cell lung cancer patients. Cancer Epidemiol Biomarkers Prev 2005;14:2303-9.
23. Kliewer SA, Umesono K, Mangelsdorf DJ, Evans RM. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 1992;355:446-9.
24. Elstner E, Linker-Israeli M, Le J, Umiel T, Michl P, Said JW, Binderup L, Reed JC, Koeffler HP. Synergistic decrease of clonal proliferation, induction of differentiation, and apoptosis of acute promyelocytic leukemia cells after combined treatment with novel 20-epi vitamin D3 analogs and 9-cis retinoic acid. J Clin Invest 1997;99:349-60.
25. Elstner E, Campbell MJ, Munker R, Shintaku P, Binderup L, Heber D, Said J, Koeffler HP. Novel 20-epi-vitamin D3 analog combined with 9-cis-retinoic acid markedly inhibits colony growth of prostate cancer cells. Prostate 1999;40:141-9.
26. Blutt SE, Allegretto EA, Pike JW, Weigel NL. 1,25-dihydroxyvitamin D3 and 9-cis-retinoic acid act synergistically to inhibit the growth of LNCaP prostate cells and cause accumulation of cells in G1. Endocrinology 1997;138:1491-7.
27. Stio M, Celli A, Treves C. Synergistic anti-proliferative effects of vitamin D derivatives and 9-cis retinoic acid in SH-SY5Y human neuroblastoma cells. J Steroid Biochem Mol Biol 2001;77:213-22.
28. Wang Q, Lee D, Sysounthone V, Chandraratna RAS, Christakos S, Korah R, Wieder R. 1,25-dihydroxyvitamin D3 and retonic acid analogues induce differentiation in breast cancer cells with function- and cell-specific additive effects. Breast Cancer Res Treat 2001;67:157-68.
29. Makishima M, Shudo K, Honma Y. Greater synergism of retinoic acid receptor (RAR) agonists with vitamin D3 than that of retinoid X receptor (RXR) agonists with regard to growth inhibition and differentiation induction in monoblastic leukemia cells. Biochem Pharmacol 1999;57:521-9.
30. Majewski S, Szmurlo A, Marczak M, Jablonska S, Bollag W. Inhibition of tumor cell-induced angiogenesis by retinoids, 1,25-dihydroxyvitamin D3 and their combination. Cancer Lett 1993;75:35-9.
31. Nakajima H, Kizaki M, Ueno H, Muto A, Takayama N, Matsushita H, Sonoda A, Ikeda Y. All-trans and 9-cis retinoic acid enhance 1,25-dihydroxyvitamin D3-induced monocytic differentiation of U937 cells. Leuk Res 1996;20:665-76.
32. Guzey M, Sattler C, DeLuca HF. Combinational effects of vitamin D3 and retinoic acid (all-trans and 9-cis) on proliferation, differentiation, and programmed cell death in two small cell lung carcinoma cell lines. Biochem Biophys Res Commun 1998;249:735-44.
33. Jensen TJ, Henriksen LO, Solvsten H, Kragballe K. Inhibition of the 1,25-dihydroxyvitamin D3-induced increase in vitamin D receptor (VDR) levels and binding of VDR-retinoid X receptor (RXR) to a direct repeat (DR)-3 type response element by an RXR-specific ligand in human keratinocyte cultures. Biochem Pharmacol 1998;55:767-73.
34. Sorensen S, Solvsten H, Politi Y, Kragballe K. Effects of vitamin D3 on keratinocyte proliferation and differentiation in vitro: modulation by ligands for retinoic acid and retinoid X receptors. Skin Pharmacol 1997;10:144-52.
35. Rohde CM, Manatt M, Clagett-Dame M, DeLuca HF. Vitamin A antagonizes the action of vitamin D in rats. J Nutr 1999;129:2246-50.
36. Kindmark A, Melhus H, Ljunghall S, Ljunggren O. Inhibitory effects of 9-cis and all-trans retinoic acid on 1,25(OH)2 vitamin D3-induced bone resorption. Calcif Tissue Int 1995;57:242-4.
37. Reeves PG, Nielsen FH, Fahey GC, Jr. 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 1993;123:1939-51.
38. Cope MB, Steele VE, Eto I, Juliana MM, Hill DL, Grubbs CJ. Prevention of methylnitrosourea-induced mammary cancers by 9-cis-retinoic acid and/or vitamin D3. Oncol Rep 2002;9:533-7.
39. Beer TM, Munar M, Henner WD. A Phase I trial of pulse calcitriol in patients with refractory malignancies: pulse dosing permits substantial dose escalation. Cancer 2001;91:2431-9.
40. Wang XD, Liu C, Bronson RT, Smith DE, Krinsky NI, Russell M. Retinoid signaling and activator protein-1 expression in ferrets given β-carotene supplements and exposed to tobacco smoke. J Natl Cancer Inst 1999;91:60-6.
41. Malkinson AM. Primary lung tumors in mice: an experimentally manipulable model of human adenocarcinoma. Cancer Res 1992;52(9Suppl.):2670s-2676s.
42. Belinsky SA, Stefanski SA, Anderson MW. The A/J mouse lung as a model for developing new chemointervention strategies. Cancer Res 1993;53:410-16.
43. Castonguay A, Rioux N. Inhibition of lung tumourigenesis by sulindac: comparison of two experimental protocols. Carcinogenesis 1997;18:491-6.
44. Rosati R, Ramnath N, Adil MR, Ou X, Ali MA, Heyman RA, Kalemkerian GP. Activity of 9-cis-retinoic acid and receptor-selective retinoids in small cell lung cancer cell lines. Anticancer Res 1998;18:4071-5.
45. Michaelsson K, Lithell H, Vessby B, Melhus H. Serum retinol levels and the risk of fracture. N Engl J Med 2003;348:287-94.
46. Feskanich D, Singh V, Willett WC, Colditz GA. Vitamin A intake and hip fractures among postmenopausal women. J Am Med Assoc 2002;287:47-54.
47. Promislow JH, Goodman-Gruen D, Slymen DJ, Barrett-Connor E. Retinol intake and bone mineral density in the elderly: the Rancho Bernardo Study. J Bone Miner Res 2002;17:1349-58.
48. Melhus H, Michaelsson K, Kindmark A, Bergstrom R, Holmberg L, Mallmin H, Wolk A, Ljunghall S. Excessive dietary intake of vitamin A is associated with reduced bone mineral density and increased risk for hip fracture. Ann Intern Med 1998;129:770-8.
49. Rohde CM, DeLuca HF. All-trans retinoic acid antagonizes the action of calciferol and its active metabolite, 1,25-dihydroxycholecalciferol, in rats. J Nutr 2005;135:1647-52.
50. Johansson S, Melhus H. Vitamin A antagonizes calcium response to vitamin D in man. J Bone Miner Res 2001;16:1899-905.
51. Parise RA, Egorin MJ, Kanterewicz B, Taimi M, Petkovich M, Lew AM, Chuang SS, Nichols M, El-Hefnawy T, Hershberger PA. CYP24, the enzyme that catabolizes the antiproliferative agent vitamin D, is increased in lung cancer. Int J Cancer 2006;119:1819-28.
52. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823-35.
53. Trechsel U, Fleisch H. Retinol and retinoic acid modulate the metabolism of 25-hydroxyvitamin D3 in kidney cell culture. FEBS Lett 1981;135:115-18.
54. Allegretto EA, Shevde N, Zou A, Howell SR, Boehm MF, Hollis BW, Pike JW. Retinoid X receptor acts as a hormone receptor in vivo to induce a key metabolic enzyme for 1,25-dihydroxyvitamin D3. J Biol Chem 1995;270:23906-9.