Mouse skin chemical carcinogenesis is inhibited by antizyme in promotion-sensitive and promotion-resistant genetic backgrounds

Molecular Carcinogenesis

Volumn 46, Issue 6, 2007, Pages 453-465

  Feith, David J ^a   Shantz, Lisa M ^a   Snoop, Paula L ^a   Keefer, Kerry A ^a   Prakashagowda, Chethana ^a   Pegg, Anthony E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Ornithine decarboxylase; Polyamine; Transgenic mice; Tumor promotion

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; ANTIZYME; CYCLINE; CYTOKERATIN 5; CYTOKERATIN 6; KERATIN; ORNITHINE DECARBOXYLASE; PHORBOL 13 ACETATE 12 MYRISTATE; POLYAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER SIZE; CELL PROLIFERATION; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; POLYAMINE SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; CARCINOGENS; DISEASE MODELS, ANIMAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; ORNITHINE DECARBOXYLASE; POLYAMINES; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEINS; SKIN NEOPLASMS;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 34250212942     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20294     Document Type: Article

References (56)

1. Gerner EW, Meyskens FL, Jr. Polyamines and cancer: Old molecules, new understanding. Nat Rev Cancer 2004;4: 781-792.
2. Wallace HM, Fraser AV, Hughes A. A perspective of polyamine metabolism. Biochem J 2003;376:1-14.
3. Pegg AE. Regulation of ornithine decarboxylase. J Biol Chem 2006;281:14529-14532.
4. Matsufuji S, Matsufuji T, Miyazaki Y, et al. Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell 1995;80:51-60.
5. Coffino P. Regulation of cellular polyamines by antizyme. Nat Rev Mol Cell Biol 2001;2:188-194.
6. Mangold U. The antizyme family: Polyamines and beyond. IUBMB Life 2005;57:671-676.
7. Pegg AE. Polyamine metabolism and its importance in neoplastic growth and as a target for chemotherapy. Cancer Res 1988;48:759-774.
8. Shantz LM, Pegg AE. Ornithine decarboxylase induction in transformation by H-Ras and RhoA. Cancer Res 1998;58: 2748-2753.
9. Feith DJ, Bol DK, Carboni JM, et al. Induction of ornithine decarboxylase activity is a necessary step for mitogen-activated protein kinase kinase-induced skin tumorigenesis. Cancer Res 2005;65:572-578.
10. Feith DJ, Origanti S, Shoop PL, Sass-Kuhn S, Shantz LM. Tumor suppressor activity of ODC antizyme in MEK-driven skin tumorigenesis. Carcinogenesis 2006;27:1090-1098.
11. Nilsson JA, Maclean KH, Keller UB, Pendeville H, Baudino TA, Cleveland JL. Mnt loss triggers Myc transcription targets, proliferation, apoptosis, and transformation. Mol Cell Biol 2004;24:1560-1569.
12. Martinez ME, O'Brien TG, Fultz KE, et al. Pronounced reduction in adenoma recurrence associated with aspirin use and a polymorphism in the ornithine decarboxylase gene. Proc Natl Acad Sci USA 2003;100:7859-7864.
13. Kemp CJ. Multistep skin cancer in mice as a model to study the evolution of cancer cells. Semin Cancer Biol 2005;15: 460-473.
14. DiGiovanni J. Multistage carcinogenesis in mouse skin. Pharmac Ther 1992;54:63-128.
15. Balmain A, Ramsden M, Bowden GT, Smith J. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature 1984;307:658-660.
16. Bizub D, Wood AW, Skalka AM. Mutagenesis of the Ha-ras oncogene in mouse skin tumors induced by polycyclic aromatic hydrocarbons. Proc Natl Acad Sci USA 1986;83: 6048-6052.
17. O'Brien TG, Simsiman RC, Boutwell RK. Induction of the polyamine-biosynthetic enzymes in mouse epidermis by tumor-promoting agents. Cancer Res 1975;35:1662-1670.
18. DiGiovanni J. Genetic determinants of cancer susceptibility. In: Bowden GT, Fischer SM, editors. Comprehensive Toxicology, Carcinogens and Anticarcinogens, Vol. 10. New York: Pergamon Press; 1997. pp 425-451.
19. Angel JM, DiGiovanni J. Genetics of skin tumor promotion. Prog Exp Tumor Res 1999;35:143-157.
20. Imamoto A, Beltran LM, Fujiki H, Chenicek KJ, DiGiovanni J. Enhanced induction of epidermal ornithine decarboxylase activity in C57BL/6 compared to DBA/2 mice by protein kinase C-activating skin tumor promoters: Relevance to genetically mediated differences in promotion susceptibility. Carcinogenesis 1992;13:177-182.
21. Riggs PK, Angel JM, Abel EL, DiGiovanni J. Differential gene expression in epidermis of mice sensitive and resistant to phorbol ester skin tumor promotion. Mol Carcinog 2005;44: 122-136.
22. Koza RA, Megosh LC, Palmieri M, O'Brien TG. Constitutively elevated levels of ornithine and polyamines in mouse epidermal papillomas. Carcinogenesis 1991;12:1619-1625.
23. Takigawa M, Verma AK, Simsiman RC, Boutwell RK. Polyamine biosynthesis and skin tumor promotion: Inhibition of 12-O-tetradecanoylphorbol-13-acetate- promoted mouse skin tumor formation by the irreversible inhibitor of ornithine decarboxylase alpha-difluoromethylomithine. Biochem Biophys Res Commun 1982;105:969-976.
24. Weeks CE, Herrmann AL, Nelson FR, Slaga TS. alpha- Difluoromethylornithine, an irreversible inhibitor of ornithine decarboxylase, inhibits tumor promoter-induced polyamine accumulation and carcinogenesis in mouse skin. Proc Natl Acad Sci USA 1982;79:6028-6032.
25. Guo Y, Cleveland JL, O'Brien TG. Haploinsufficiency for Odc modifies mouse skin tumor susceptibility. Cancer Res 2005;65:1146-1149.
26. O'Brien TG, Megosh LC, Gilliard G, Soler AP. Ornithine decarboxylase overexpression is a sufficient condition for tumor promotion in mouse skin. Cancer Res 1997;57:2630-2637.
27. Smith MK, Trempus CS, Gilmour SK. Co-operation between follicular ornithine decarboxylase and v-Ha-ras induces spontaneous papillomas and malignant conversion in transgenic skin. Carcinogenesis 1998;19:1409-1415.
28. Megosh L, Halpern M, Farkash E, O'Brien TG. Analysis of ras gene mutational spectra in epidermal papillomas from K6-ODC transgenic mice. Molecular Carcinogenesis 1998;22: 145-149.
29. Megosh LC, Hu J, George K, O'Brien TG. Genetic control of polyamine-dependent susceptibility to skin tumorigenesis. Genomics 2002;79:505-512.
30. Feith DJ, Shantz LM, Pegg AE. Targeted antizyme expression in the skin of transgenic mice reduces tumor promoter induction of ornithine decarboxylase and decreases sensitivity to chemical carcinogenesis. Cancer Res 2001;61:6073-6081.
31. Bottema CD, Sommer SS. PCR amplification of specific alleles: Rapid detection of known mutations and polymorphisms. Mutat Res 1993;288:93-102.
32. Jacoby RF, Marshall DJ, Newton MA, et al. Chemoprevention of spontaneous intestinal adenomas in the Apc Min mouse model by the nonsteroidal anti-inflammatory drug piroxicam. Cancer Res 1996;56:710-714.
33. Siegel PM, Shu W, Cardiff RD, Muller WJ, Massague J. Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc Natl Acad Sci USA 2003;100: 8430-8435.
34. Ackermann JM, Pegg AE, McCloskey DE. Drugs affecting the cell cycle via actions on the polyamine metabolic pathway. Prog Cell Cycle Res 2003;5:461-468.
35. Ramirez A, Vidal M, Bravo A, Larcher F, Jorcano JL. A 5′-upstream region of a bovine keratin 6 gene confers tissue-specific expression and hyperproliferation-related induction in transgenic mice. Proc Natl Acad Sci USA 1995;92:4783-4787.
36. Kennard MD, Kang DC, Montgomery RL, Butler AP. Expression of epidermal ornithine decarboxylase and nuclear proto-oncogenes in phorbol ester tumor promotion-sensitive and -resistant mice. Mol Carcinog 1995;12:14-22.
37. Verma AK, Hsiao KM, Ahrens H, et al. Superinduction of mouse epidermal ornithine decarboxylase activity by repeated 12-O-tetradecanoylphorbol- 13-acetate treatments. Mol Cell Biochem 1996;155:139-151.
38. Gilmour SK, Aglow E, O'Brien TG. Heterogeneity of ornitine decarboxylase expression in 12-O-tetradecanoylphorbol-13-acetate- treated mouse skin and in epidermal tumors. Carcinogenesis 1986;7:943-947.
39. Sundberg JP, Erickson AE, Roop DR, Binder RL. Ornithine decarboxylase expression in cutaneous papillomas in SENCAR mice is associated with altered expression of keratins 1 and 10. Cancer Res 1994;54:1344-1351.
40. Newman RM, Mobascher A, Mangold U, et al. Antizyme targets cyclin D1 for degradation. A novel mechanism for cell growth repression. J Biol Chem 2004;279:41504-41511.
41. Lin Y, Martin J, Gruendler C, et al. A novel link between the proteasome pathway and the signal transduction pathway of the bone morphogenetic proteins (BMPs). BMC Cell Biol 2002;3:15.
42. Tang X, Kim AL, Feith DJ, et al. Ornithine decarboxylase is a target for chemoprevention of basal and squamous cell carcinomas in Ptch1+/- mice. J Clin Invest 2004;113:867-875.
43. Takigawa M, Verma AK, Simsiman RC, Boutwell RK. Inhibition of mouse skin tumor promotion and of promoter-stimulated epidermal polyamine biosynthesis by alpha-difluoromethylornithine. Cancer Res 1983;43:3732-3738.
44. Peralta Soler A, Gilliard G, Megosh L, George K, O'Brien TG. Polyamines regulate expression of the neoplastic phenotype in mouse skin. Cancer Res 1998;58:1654-1659.
45. Arbeit JM, Riley RR, Huey B, et al. Difluoromethylornithine chemoprevention of epidermal carcinogenesis in K14-HPV16 transgenic mice. Cancer Res 1999;59:3610-3620.
46. Lan L, Hayes CS, Laury-Kleintop L, Gilmour SK. Suprabasal induction of ornithine decarboxylase in adult mouse skin is sufficient to activate keratinocytes. J Invest Dermatol 2005; 124:602-614.
47. Shore L, McLean P, Gilmour SK, Hodgins MB, Finbow ME. Polyamines regulate gap junction communication in connexin 43-expressing cells. Biochem J 2001;357:489-495.
48. Marques MR, Horner JS, Ihrie RA, Branson RT, Attardi LD. Mice lacking the p53/p63 target gene Perp are resistant to papilloma development. Cancer Res 2005;65:6551-6556.
49. Rodriguez-Puebla ML, Miliani de Marval PL, LaCava M, Moons DS, Kiyokawa H, Conti CJ. Cdk4 deficiency inhibits skin tumor development but does not affect normal keratinocyte proliferation. Am J Pathol 2002;161:405-411.
50. Jansen AP, Dreckschmidt NE, Verwiebe EG, Wheeler DL, Oberley TD, Verma AK. Relation of the induction of epidermal ornithine decarboxylase and hyperplasia to the different skin tumor-promotion susceptibilities of protein kinase C alpha, -delta and -epsilon transgenic mice. Int J Cancer 2001;93:635-643.
51. Jansen AP, Camalier CE, Colburn NH. Epidermal expression of the translation inhibitor programmed cell death 4 suppresses tumorigenesis. Cancer Res 2005;65:6034-6041.
52. Trempus CS, Bishop WR, Njoroge FG, et al. A farnesyl transferase inhibitor suppresses TPA-mediated skin tumor development without altering hyperplasia in the ras transgenic Tg·AC mouse. Mol Carcinog 2000;27:24-33.
53. Klatt P, Serrano M. Engineering cancer resistance in mice. Carcinogenesis 2003;24:817-826.
54. Fong LY, Feith DJ, Pegg AE. Antizyme overexpression in transgenic mice reduces cell proliferation, increases apoptosis, and reduces N-nitrosomethylbenzylamine-induced forestomach carcinogenesis. Cancer Res 2003;63:3945-3954.
55. Lan L, Trempus C, Gilmour SK. Inhibition of ornithine decarboxylase (ODC) decreases tumor vascularization and reverses spontaneous tumors in ODC/Ras transgenic mice. Cancer Res 2000;60:5696-5703.
56. Fischer SM, Lee M, Lubet RA. Difluoromethylornithine is effective as both a preventive and therapeutic agent against the development of UV carcinogenesis in SKH hairless mice. Carcinogenesis 2001;22:83-88.