Retinoid metabolism and ALDH1A2 (RALDH2) expression are altered in the transgenic adenocarcinoma mouse prostate model

Biochemical Pharmacology

Volumn 78, Issue 9, 2009, Pages 1127-1138

  Touma, Sue Ellen ^a   Perner, Sven ^a   Rubin, Mark A ^a   Nanus, David M ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Carcinogenesis; Epithelial cells; Human prostate cancer; Retinoic acid; TRAMP

Indexed keywords

ALDEHYDE DEHYDROGENASE; CYTOCHROME P450 26A1; LECITHIN RETINOL ACYLTRANSFERASE; MESSENGER RNA; PARAFFIN; RETINAL DEHYDROGENASE; RETINOIC ACID RECEPTOR BETA; RETINOID; RETINOL; RETINOL ESTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DISEASE MODEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROSTATE; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; TRANSGENIC MOUSE; VITAMIN METABOLISM;

ADENOCARCINOMA; ALDEHYDE DEHYDROGENASE; ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; DNA PRIMERS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; PROSTATIC NEOPLASMS; RETINOIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 70249099518     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.06.022     Document Type: Article

References (67)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., et al. Cancer statistics, 2008. CA Cancer J Clin 58 (2008) 71-96
2. Lasnitzki I., and Goodman D.S. Inhibition of the effects of methylcholanthrene on mouse prostate in organ culture by vitamin A and its analogs. Cancer Res 34 (1974) 1564-1571
3. Chopra D.P., and Wilkoff L.J. Reversal by vitamin A analogues (retinoids) of hyperplasia induced by N-methyl-N′-nitro-N-nitrosoguanidine in mouse prostate organ cultures. J Natl Cancer Inst 58 (1977) 923-930
4. Chopra D.P., and Wilkoff L.J. Activity of retinoids against benzo(a)pyrene-induced hyperplasia in mouse prostate organ cultures. Eur J Cancer 15 (1979) 1417-1423
5. Mongan N.P., and Gudas L.J. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation 75 (2007) 853-870
6. Lotan R., and Lotan Y. Retinoic acid receptor beta2 hypermethylation: implications for prostate cancer detection, prevention, and therapy. Clin Cancer Res 10 (2004) 3935-3936
7. Nakayama T., Watanabe M., Yamanaka M., Hirokawa Y., Suzuki H., Ito H., et al. The role of epigenetic modifications in retinoic acid receptor beta2 gene expression in human prostate cancers. Lab Invest 81 (2001) 1049-1057
8. Pili R., Kruszewski M.P., Hager B.W., Lantz J., and Carducci M.A. Combination of phenylbutyrate and 13-cis retinoic acid inhibits prostate tumor growth and angiogenesis. Cancer Res 61 (2001) 1477-1485
9. Guo X., Knudsen B.S., Peehl D.M., Ruiz A., Bok D., Rando R.R., et al. Retinol metabolism and lecithin:retinol acyltransferase levels are reduced in cultured human prostate cancer cells and tissue specimens. Cancer Res 62 (2002) 1654-1661
10. Pasquali D., Thaller C., and Eichele G. Abnormal level of retinoic acid in prostate cancer tissues. J Clin Endocrinol Metab 81 (1996) 2186-2191
11. Kim H., Lapointe J., Kaygusuz G., Ong D.E., Li C., van de Rijn M., et al. The retinoic acid synthesis gene ALDH1a2 is a candidate tumor suppressor in prostate cancer. Cancer Res 65 (2005) 8118-8124
12. Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell 134 (2008) 921-931
13. Vasiliou V., Pappa A., and Estey T. Role of human aldehyde dehydrogenases in endobiotic and xenobiotic metabolism. Drug Metab Rev 36 (2004) 279-299
14. Douville J., Beaulieu R., and Balicki D. ALDH1 as a functional marker of cancer stem and progenitor cells. Stem Cells Dev (2008)
15. Niederreither K., and Dolle P. Retinoic acid in development: towards an integrated view. Nat Rev Genet 9 (2008) 541-553
16. Niederreither K., Subbarayan V., Dolle P., and Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21 (1999) 444-448
17. Trasino S.E., Harrison E.H., and Wang T.T. Androgen regulation of aldehyde dehydrogenase 1A3 (ALDH1A3) in the androgen-responsive human prostate cancer cell line LNCaP. Exp Biol Med (Maywood) 232 (2007) 762-771
18. Greenberg N.M., DeMayo F., Finegold M.J., Medina D., Tilley W.D., Aspinall J.O., et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 92 (1995) 3439-3443
19. Greenberg N.M., DeMayo F.J., Sheppard P.C., Barrios R., Lebovitz R., Finegold M., et al. The rat probasin gene promoter directs hormonally and developmentally regulated expression of a heterologous gene specifically to the prostate in transgenic mice. Mol Endocrinol 8 (1994) 230-239
20. Kaplan-Lefko P.J., Chen T.M., Ittmann M.M., Barrios R.J., Ayala G.E., Huss W.J., et al. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate 55 (2003) 219-237
21. Hurwitz A.A., Foster B.A., Allison J.P., Greenberg N.M., and Kwon E.D. The TRAMP mouse as a model for prostate cancer. Curr Protoc Immunol (2001) (Chapter 20: Unit 20.5)
22. Sargeant A.M., Rengel R.C., Kulp S.K., Klein R.D., Clinton S.K., Wang Y.C., et al. OSU-HDAC42, a histone deacetylase inhibitor, blocks prostate tumor progression in the transgenic adenocarcinoma of the mouse prostate model. Cancer Res 68 (2008) 3999-4009
23. Camoriano M., Kinney S.R., Moser M.T., Foster B.A., Mohler J.L., Trump D.L., et al. Phenotype-specific CpG island methylation events in a murine model of prostate cancer. Cancer Res 68 (2008) 4173-4182
24. Morey Kinney S.R., Smiraglia D.J., James S.R., Moser M.T., Foster B.A., and Karpf A.R. Stage-specific alterations of DNA methyltransferase expression, DNA hypermethylation, and DNA hypomethylation during prostate cancer progression in the transgenic adenocarcinoma of mouse prostate model. Mol Cancer Res 6 (2008) 1365-1374
25. Raina K., Rajamanickam S., Singh R.P., Deep G., Chittezhath M., and Agarwal R. Stage-specific inhibitory effects and associated mechanisms of silibinin on tumor progression and metastasis in transgenic adenocarcinoma of the mouse prostate model. Cancer Res 68 (2008) 6822-6830
26. Chung A.C., Zhou S., Liao L., Tien J.C., Greenberg N.M., and Xu J. Genetic ablation of the amplified-in-breast cancer 1 inhibits spontaneous prostate cancer progression in mice. Cancer Res 67 (2007) 5965-5975
27. McCabe M.T., Low J.A., Daignault S., Imperiale M.J., Wojno K.J., and Day M.L. Inhibition of DNA methyltransferase activity prevents tumorigenesis in a mouse model of prostate cancer. Cancer Res 66 (2006) 385-392
28. Raina K., Rajamanickam S., Deep G., Singh M., Agarwal R., and Agarwal C. Chemopreventive effects of oral gallic acid feeding on tumor growth and progression in TRAMP mice. Mol Cancer Ther 7 (2008) 1258-1267
29. Raina K., Rajamanickam S., Singh R.P., and Agarwal R. Chemopreventive efficacy of inositol hexaphosphate against prostate tumor growth and progression in TRAMP mice. Clin Cancer Res 14 (2008) 3177-3184
30. Singh S.V., Powolny A.A., Stan S.D., Xiao D., Arlotti J.A., Warin R., et al. Garlic constituent diallyl trisulfide prevents development of poorly differentiated prostate cancer and pulmonary metastasis multiplicity in TRAMP mice. Cancer Res 68 (2008) 9503-9511
31. Singh R.P., Raina K., Sharma G., and Agarwal R. Silibinin inhibits established prostate tumor growth, progression, invasion, and metastasis and suppresses tumor angiogenesis and epithelial-mesenchymal transition in transgenic adenocarcinoma of the mouse prostate model mice. Clin Cancer Res 14 (2008) 7773-7780
32. Bonorden M.J., Rogozina O.P., Kluczny C.M., Grossmann M.E., Grande J.P., Lokshin A., et al. Cross-sectional analysis of intermittent versus chronic caloric restriction in the TRAMP mouse. Prostate 69 (2009) 317-326
33. Adhami V.M., Siddiqui I.A., Sarfaraz S., Khwaja S.I., Hafeez B.B., Ahmad N., et al. Effective prostate cancer chemopreventive intervention with green tea polyphenols in the TRAMP model depends on the stage of the disease. Clin Cancer Res 15 (2009) 1947-1953
34. Wang L., Bonorden M.J., Li G.X., Lee H.J., Hu H., Zhang Y., et al. Methyl-selenium compounds inhibit prostate carcinogenesis in the transgenic adenocarcinoma of mouse prostate model with survival benefit. Cancer Prev Res (Phila PA) 2 (2009) 484-495
35. O'Mahony O.A., Steinkamp M.P., Albertelli M.A., Brogley M., Rehman H., and Robins D.M. Profiling human androgen receptor mutations reveals treatment effects in a mouse model of prostate cancer. Mol Cancer Res 6 (2008) 1691-1701
36. Venkateswaran V., Klotz L.H., Ramani M., Sugar L.M., Jacob L.E., Nam R.K., et al. A combination of micronutrients is beneficial in reducing the incidence of prostate cancer and increasing survival in the Lady transgenic model. Cancer Prev Res (Phila PA) 2 (2009) 473-483
37. Shappell S.B., Thomas G.V., Roberts R.L., Herbert R., Ittmann M.M., Rubin M.A., et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the mouse models of human cancer consortium prostate pathology committee. Cancer Res 64 (2004) 2270-2305
38. Berquin I.M., Min Y., Wu R., Wu H., and Chen Y.Q. Expression signature of the mouse prostate. J Biol Chem 280 (2005) 36442-36451
39. Deeb K.K., Michalowska A.M., Yoon C.Y., Krummey S.M., Hoenerhoff M.J., Kavanaugh C., et al. Identification of an integrated SV40 T/t-antigen cancer signature in aggressive human breast, prostate, and lung carcinomas with poor prognosis. Cancer Res 67 (2007) 8065-8080
40. Huss W.J., Lai L., Barrios R.J., Hirschi K.K., and Greenberg N.M. Retinoic acid slows progression and promotes apoptosis of spontaneous prostate cancer. Prostate 61 (2004) 142-152
41. Gillespie R.F., and Gudas L.J. Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol 372 (2007) 298-316
42. Niederreither K., Vermot J., Schuhbaur B., Chambon P., and Dolle P. Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse. Development 129 (2002) 3563-3574
43. Haselbeck R.J., Hoffmann I., and Duester G. Distinct functions for Aldh1 and Raldh2 in the control of ligand production for embryonic retinoid signaling pathways. Dev Genet 25 (1999) 353-364
44. Vernet N., Dennefeld C., Rochette-Egly C., Oulad-Abdelghani M., Chambon P., Ghyselinck N.B., et al. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 147 (2006) 96-110
45. Everts H.B., Sundberg J.P., and Ong D.E. Immunolocalization of retinoic acid biosynthesis systems in selected sites in rat. Exp Cell Res 308 (2005) 309-319
46. Saleem M., Adhami V.M., Ahmad N., Gupta S., and Mukhtar H. Prognostic significance of metastasis-associated protein S100A4 (Mts1) in prostate cancer progression and chemoprevention regimens in an autochthonous mouse model. Clin Cancer Res 11 (2005) 147-153
47. Abate-Shen C., and Shen M.M. Molecular genetics of prostate cancer. Genes Dev 14 (2000) 2410-2434
48. Cai K., and Gudas L.J. Retinoic acid receptors and GATA transcription factors activate the transcription of the human lecithin:retinol acyltransferase gene. Int J Biochem Cell Biol 41 (2009) 546-553
49. Guo X., Nanus D.M., Ruiz A., Rando R.R., Bok D., and Gudas L.J. Reduced levels of retinyl esters and vitamin A in human renal cancers. Cancer Res 61 (2001) 2774-2781
50. Guo X., Ruiz A., Rando R.R., Bok D., and Gudas L.J. Esterification of all-trans-retinol in normal human epithelial cell strains and carcinoma lines from oral cavity, skin and breast: reduced expression of lecithin:retinol acyltransferase in carcinoma lines. Carcinogenesis 21 (2000) 1925-1933
51. Poulin D.L., and DeCaprio J.A. Is there a role for SV40 in human cancer?. J Clin Oncol 24 (2006) 4356-4365
52. Abate-Shen C., and Shen M.M. Mouse models of prostate carcinogenesis. Trends Genet 18 (2002) S1-5
53. Sharma P., and Schreiber-Agus N. Mouse models of prostate cancer. Oncogene 18 (1999) 5349-5355
54. Peehl D.M., Wong S.T., Sellers R.G., Jin S., and Rhim J.S. Loss of response to epidermal growth factor and retinoic acid accompanies the transformation of human prostatic epithelial cells to tumorigenicity with v-Ki-ras. Carcinogenesis 18 (1997) 1643-1650
55. Ono Y., Fukuhara N., and Yoshie O. TAL1 and LIM-only proteins synergistically induce retinaldehyde dehydrogenase 2 expression in T-cell acute lymphoblastic leukemia by acting as cofactors for GATA3. Mol Cell Biol 18 (1998) 6939-6950
56. Rexer B.N., Zheng W.L., and Ong D.E. Retinoic acid biosynthesis by normal human breast epithelium is via aldehyde dehydrogenase 6, absent in MCF-7 cells. Cancer Res 61 (2001) 7065-7070
57. Yamashita S., Tsujino Y., Moriguchi K., Tatematsu M., and Ushijima T. Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2'-deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 97 (2006) 64-71
58. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1 (2007) 555-567
59. Tang D.G., Patrawala L., Calhoun T., Bhatia B., Choy G., Schneider-Broussard R., et al. Prostate cancer stem/progenitor cells: identification, characterization, and implications. Mol Carcinog 46 (2007) 1-14
60. Lawson D.A., and Witte O.N. Stem cells in prostate cancer initiation and progression. J Clin Invest 117 (2007) 2044-2050
61. Takao T., and Tsujimura A. Prostate stem cells: the niche and cell markers. Int J Urol 15 (2008) 289-294
62. Lawson D.A., Xin L., Lukacs R.U., Cheng D., and Witte O.N. Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci USA 104 (2007) 181-186
63. Oudes A.J., Campbell D.S., Sorensen C.M., Walashek L.S., True L.D., and Liu A.Y. Transcriptomes of human prostate cells. BMC Genomics 7 (2006) 92
64. Mao G.E., Reuter V.E., Cordon-Cardo C., Dalbagni G., Scher H.I., DeKernion J.B., et al. Decreased retinoid X receptor-alpha protein expression in basal cells occurs in the early stage of human prostate cancer development. Cancer Epidemiol Biomarkers Prev 13 (2004) 383-390
65. Huss W.J., Maddison L.A., and Greenberg N.M. Autochthonous mouse models for prostate cancer: past, present and future. Semin Cancer Biol 11 (2001) 245-260
66. Sprenger J., Lynn Fink J., Karunaratne S., Hanson K., and Hamilton N.A. Teasdale RD. LOCATE: a mammalian protein subcellular localization database. Nucleic Acids Res 36 (2008) D230-D233
67. King J.C., Xu J., Wongvipat J., Hieronymus H., Carver B.S., Leung D.H., et al. Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 41 (2009) 524-526