Perillyl alcohol-mediated inhibition of lung cancer cell line proliferation: Potential mechanisms for its chemotherapeutic effects

Toxicology and Applied Pharmacology

Volumn 195, Issue 2, 2004, Pages 232-246

  Xu, Mian ^a   Floyd, Heather S ^a   Greth, Suzanne M ^a   Chang, Wen Chi L ^b   Lohman, Kurt ^a   Stoyanova, Radka ^b   Kucera, Gregory L ^a   Kute, Tim E ^a   Willingham, Mark C ^a   Miller, Mark Steven ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

4 ,6 diamidino 2 phenylindole; Apoptosis; DAPI; Ethanol; EtOH; LOH; Loss of heterozygosity; Lung cancer; Microarray; Monoterpene; Non small cell lung cancer; NSCLC; PARP; Perillyl alcohol; POH; Poly (ADP ribose) polymerase; Relative light unit; RLU; SRB

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; CASPASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PERILLYL ALCOHOL; SULFORHODAMINE B;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CELL ASSAY; CELL NUCLEUS; CELL PROLIFERATION; CLONOGENESIS; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; DRUG ACTIVITY; DRUG EFFECT; DRUG EXPOSURE; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LUNG CANCER; MICROSCOPY; NUCLEOTIDE SEQUENCE; STAINING; TIME; UNINDEXED SEQUENCE; UPREGULATION; VIDEORECORDING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 3; CASPASES; CELL DIVISION; CELL LINE, TUMOR; CLONING, MOLECULAR; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; GENES, P53; GENES, RAS; HUMANS; LUNG NEOPLASMS; MONOTERPENES; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLY(ADP-RIBOSE) POLYMERASES; UP-REGULATION;

EID: 10744230271     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.taap.2003.11.013     Document Type: Article

References (62)

1. Alexandrow M.G., Moses H.L. Transforming growth factor beta and cell cycle regulation. Cancer Res. 55:1995;1452-1457.
2. Bailey H.H., Levy D., Harris L.S., Schink J.C., Foss F., Beatty P., Wadler S. A phase II trial of daily perillyl alcohol in patients with advanced ovarian cancer: Eastern Cooperative Oncology Group Study E2E96. Gynecol. Oncol. 85:2002;464-468.
3. Bardon S., Picard K., Martel P. Monoterpenes inhibit cell growth, cell cycle progression, and cyclin D1 gene expression in human breast cancer cell lines. Nutr. Cancer. 32:1998;1-7.
4. Bardon S., Foussard V., Fournel S., Loubat A. Monoterpenes inhibit proliferation of human colon cancer cells by modulating cell cycle-related protein expression. Cancer Lett. 181:2002;187-194.
5. Barthelman M., Chen W., Gensler H.L., Huang C., Dong Z., Bowden G.T. Inhibitory effects of perillyl alcohol on UVB-induced murine skin cancer and AP-1 transactivation. Cancer Res. 58:1998;711-716.
6. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15:1999;269-290.
7. Chen Y.-R., Wang W., Kong A.-N., Tan T.-H. Molecular mechanisms of c-Jun N-terminal kinase-mediated apoptosis induced by anticarcinogenic isothiocyanates. J. Biol. Chem. 273:1998;1769-1775.
8. Cho H.M., Jun D.Y., Bae M.A., Ahn J.D., Kim Y.H. Nucleotide sequence and differential expression of the human 3-phosphoglycerate dehydrogenase gene. Gene. 245:2000;193-201.
9. Chow H.H., Salazar D., Hakim I.A. Pharmacokinetics of perillic acid in humans after a single dose administration of a citrus preparation rich in D-limonene content. Cancer Epidemiol., Biomarkers Prev. 11:2002;1472-1476.
10. Chung F.-L. Chemoprevention of lung carcinogenesis by aromatic isothiocyanates. Wattenberg L.W., Lipkin M., Boone C.W., Kelloff G.J. Cancer Chemoprevention. 1992;227-245 CRC Press, Boca Raton.
11. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 326(Pt 1):1997;1-16.
12. Collins J.A., Schandi C.A., Young K.K., Vesely J., Willingham M.C. Major DNA fragmentation is a late event in apoptosis. J. Histochem. Cytochem. 45:1997;923-934.
13. Crowell P.L., Gould M.N. Chemoprevention and therapy of cancer by D-limonene. Crit. Rev. Oncog. 5:1994;1-22.
14. Crowell P.L., Ren Z., Lin S., Vedejs E., Gould M.N. Structure-activity relationships among monoterpene inhibitors of protein isoprenylation and cell proliferation. Biochem. Pharmacol. 47:1994;1405-1415.
15. Davydov I.V., Bohmann D., Krammer P.H., Li-Weber M. Cloning of the cDNA encoding human C/EBP gamma, a protein binding to the PRE-I enhancer element of the human interleukin-4 promoter. Gene. 161:1995;271-275.
16. Elegbede J.A., Elson C.E., Qureshi A., Tanner M.A., Gould M.N. Inhibition of DMBA-induced mammary cancer by the monoterpene D-limonene. Carcinogenesis. 5:1984;661-664.
17. Fan W., Schandl C.A., Cheng L., Norris J.S., Willingham M.C. Glucocorticoids modulate taxol cytotoxicity in human solid tumor cells. Cell. Pharmacol. 3:1994;343-348.
18. Gelb M.H., Tamanoi F., Yokoyama K., Ghomashchi F., Esson K., Gould M.N. The inhibition of protein prenyltransferases by oxygenated metabolites of limonene and perillyl alcohol. Cancer Lett. 91:1995;169-175.
19. Gould M.N. Prevention and therapy of mammary cancer by monoterpenes. J. Cell. Biochem., Suppl. 22:1995;139-144.
20. Gould M.N., Moore C.J., Zhang R., Wang B., Kennan W.S., Haag J.D. Limonene chemoprevention of mammary carcinoma induction following direct in situ transfer of v-Ha-ras. Cancer Res. 54:1994;3540-3543.
21. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
22. Haag J.D., Gould M.N. Mammary carcinoma regression induced by perillyl alcohol, a hydroxylated analog of limonene. Cancer Chemother. Pharmacol. 34:1994;477-483.
23. Haag J.D., Lindstrom M.J., Gould M.N. Limonene-induced regression of mammary carcinomas. Cancer Res. 52:1992;4021-4026.
24. Homburger F., Treger A., Boger E. Inhibition of murine subcutaneous and intravenous benzo(rst)pentaphene. Carcinogenesis by sweet orange oils and D-limonene. Oncology. 25:1971;1-10.
25. Ishibashi K., Miyamoto K., Taketani Y., Morita K., Takeda E., Sasaki S., Imai M. Molecular cloning of a second human stanniocalcin homologue (STC2). Biochem. Biophys. Res. Commun. 250:1998;252-258.
26. Jemal A., Murray T., Samuels A., Ghafoor A., Ward E., Thun A.J. Cancer statistics, 2003. Ca: Cancer J. Clin. 53:2003;5-26.
27. Jirtle R.L., Haag J.D., Ariazi E.A., Gould M.N. Increased mannose 6-phosphate/insulin-like growth factor II receptor and transforming growth factor β1 levels during monoterpene-induced regression of mammary tumors. Cancer Res. 53:1993;3849-3852.
28. Kamb A. Cell-cycle regulators and cancer. Trends Genet. 11:1995;136-140.
29. Kaufman D., Chabner B. Clinical strategies for cancer treatment: the role of drugs. Chabner B.A., Longo D.L. Cancer Chemotherapy and Biotherapy: Principles and Practice. 1996;1-16 Lippincott-Raven, Philadelphia.
30. Kawamori T., Tanaka T., Hirose Y., Ohnishi M., Mori H. Inhibitory effects of D-limonene on the development of colonic aberrant crypt foci induced by azoxymethane in F344 rats. Carcinogenesis. 17:1996;369-372.
31. Kroll K.L., Salic A.N., Evans L.M., Kirschner M.W. Geminin, a neutralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development. 125:1998;3247-3258.
32. Lluria-Prevatt M., Morreale J., Gregus J., Alberts D.S., Kaper F., Giaccia A., Powell M.B. Effects of perillyl alcohol on melanoma in the TPras mouse model. Cancer Epidemiol., Biomarkers Prev. 11:2002;573-579.
33. Maltzman T.H., Hurt L.M., Elson C.E., Tanner M.A., Gould M.N. The prevention of nitrosomethylurea-induced mammary tumors by D-limonene and orange oil. Carcinogenesis. 10:1989;781-783.
34. Matsumoto-Taniura N., Pirollet F., Monroe R., Gerace L., Westendorf J.M. Identification of novel M phase phosphoproteins by expression cloning. Mol. Biol. Cell. 7:1996;1455-1469.
35. McGarry T.J., Kirschner M.W. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell. 93:1998;1043-1053.
36. Mills J.J., Chari R.S., Boyer I.J., Gould M.N., Jirtle R.L. Induction of apoptosis in liver tumors by the monoterpene perillyl alcohol. Cancer Res. 55:1995;979-983.
37. Olivier M., Eeles R., Hollstein M., Khan M.A., Harris C.C., Hainaut P. The IARC TP53 database: new online mutation analysis and recommendations to users. Hum. Mutat. 19:2002;607-614.
38. Patel T., Gores G.J., Kaufmann S.H. The role of proteases during apoptosis. FASEB J. 10:1996;587-597.
39. Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 78:1994;59-66.
40. Pulkkinen J.O., Elomaa L., Joensuu H., Martikainen P., Servomaa K., Grenman R. Paclitaxel-induced apoptotic changes followed by time-lapse video microscopy in cell lines established from head and neck cancer. J. Cancer Res. Clin. Oncol. 122:1996;214-218.
41. Reddy B.S., Wang C.X., Samaha H., Lubet R., Steele V.E., Kelloff G.J., Rao C.V. Chemoprevention of colon carcinogenesis by dietary perillyl alcohol. Cancer Res. 57:1997;420-425.
42. Ren Z., Gould M.N. Modulation of small G protein isoprenylation by anticancer monoterpenes in in situ mammary gland epithelial cells. Carcinogenesis. 19:1998;827-832.
43. Ripple G.H., Gould M.N., Stewart J.A., Tutsch K.D., Arzoomanian R.Z., Alberti D., Feierabend C., Pomplun M., Wilding G., Bailey H.H. Phase I clinical trial of perillyl alcohol administered daily. Clin. Cancer Res. 4:1998;1159-1164.
44. Ripple G.H., Gould M.N., Arzoomanian R.Z., Alberti D., Feierabend C., Simon K., Binger K., Tutsch K.D., Pomplun M., Wahamaki A., Marnocha R., Wilding G., Bailey H.H. Phase I clinical and pharmacokinetic study of perillyl alcohol administered four times a day. Clin. Cancer Res. 6:2000;390-396.
45. Ruch R.J., Sigler K. Growth inhibition of rat liver epithelial tumor cells by monoterpenes does not involve Ras plasma membrane association. Carcinogenesis. 15:1994;787-789.
46. Sherr C.J., Roberts J.M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1995;1149-1163.
47. Shi W., Gould M.N. Induction of differentiation in neuro-2A cells by the monoterpene perillyl alcohol. Cancer Lett. 95:1995;1-6.
48. Shi W., Gould M.N. Induction of cytostasis in mammary carcinoma cells treated with the anticancer agent perillyl alcohol. Carcinogenesis. 23:2002;131-142.
49. Sigal A., Rotter V. Oncogenic mutations of the p53 tumor suppressor: the demons of the guardian of the genome. Cancer Res. 60:2000;6788-6793.
50. Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica D., Warren J.T., Bokesch H., Kenney S., Boyd M.R. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst. 82:1990;1107-1112.
51. Stark M.J., Burke Y.D., McKinzie J.H., Ayoubi A.S., Crowell P.L. Chemotherapy of pancreatic cancer with the monoterpene perillyl alcohol. Cancer Lett. 96:1995;15-21.
52. Stayrook K.R., McKinzie J.H., Burke Y.D., Burke Y.A., Crowell P.L. Induction of the apoptosis-promoting protein Bak by perillyl alcohol in pancreatic ductal adenocarcinoma relative to untransformed ductal epithelial cells. Carcinogenesis. 18:1997;1655-1658.
53. Toyoshima H., Hunter T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell. 78:1994;67-74.
54. Waddick K.G., Uckun F.M. Innovative treatment programs against cancer. I. RAS oncoprotein as a molecular target. Biochem. Pharmacol. 56:1998;1411-1426.
55. Wattenberg L.W. Chemoprevention of cancer by naturally occurring and synthetic compounds. Wattenberg L.W., Lipkin M., Boone C.W., Kelloff G.J. Cancer Chemoprevention. 1992;19-39 CRC Press, Boca Raton.
56. Wattenberg L.W., Coccia J.B. Inhibition of 4-(methylnitrosamino)-1-(3- pyridyl)-1-butanone carcinogenesis in mice by D-limonene and citrus fruit oils. Carcinogenesis. 12:1991;115-117.
57. Wattenberg L.W., Sparnins V.L., Barany G. Inhibition of N-nitrosodiethylamine carcinogenesis in mice by naturally occurring organosulfur compounds and monoterpenes. Cancer Res. 49:1989;2689-2692.
58. Wei X., Si M.S., Imagawa D.K., Ji P., Tromberg B.J., Cahalan M.D. Perillyl alcohol inhibits TCR-mediated [Ca(2+)](i) signaling, alters cell shape and motility, and induces apoptosisin T lymphocytes. Cell. Immunol. 201:2000;6-13.
59. Williams S.C., Cantwell C.A., Johnson P.F. A family of C/EBP-related proteins capable of forming covalently linked leucine zipper dimers in vitro. Genes Dev. 5:1991;1553-1567.
60. Willingham M.C. Cytochemical methods for the detection of apoptosis. J. Histochem. Cytochem. 47:1999;1101-1110.
61. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J., Speed T.P. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:2002;e15.
62. Yu R., Mandlekar S., Harvey K.J., Ucker D.S., Kong A.-N. Chemopreventive isothiocyanates induce apoptosis and caspase-3-like protease activity. Cancer Res. 58:1998;402-408.