Effect of the phenolic compounds apigenin and carnosic acid on oral carcinogenesis in hamster induced by DMBA

Oral Diseases

Volumn 19, Issue 3, 2013, Pages 279-286

  Gomez Garcia F J ^a   Lopez Jornet M P ^a   Alvarez Sanchez N ^a   Castillo Sanchez N ^a   Benavente Garcia O ^a   Ortega, V Vicente ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

7,12 Dimethyl benzanthracene; Apigenin; Carnosic acid; Experimental study hamster; Oral carcinogenesis

Indexed keywords

ANTINEOPLASTIC AGENT; APIGENIN; CARNOSIC ACID; DIMETHYLBENZ[A]ANTHRACENE; 7,12 DIMETHYLBENZ[A]ANTHRACENE; ABIETANE DERIVATIVE; PLANT EXTRACT;

ACANTHOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INCIDENCE; CANCER INHIBITION; CANCER SIZE; CARCINOGENESIS; CELL MATURATION; CONTROLLED STUDY; DYSPLASIA; HISTOPATHOLOGY; HYPERKERATOSIS; HYPERPLASIA; KERATINIZATION; MALE; MOUTH CANCER; NONHUMAN; PAPILLOMATOSIS; PARAKERATOSIS; PRIORITY JOURNAL; SYRIAN HAMSTER; ANIMAL; CHEMICALLY INDUCED; DRUG SCREENING; HAMSTER; MOUTH NEOPLASMS;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; APIGENIN; CARCINOGENESIS; CRICETINAE; DITERPENES, ABIETANE; DRUG SCREENING ASSAYS, ANTITUMOR; MALE; MOUTH NEOPLASMS; PLANT EXTRACTS;

EID: 84876124412     PISSN: 1354523X     EISSN: 16010825     Source Type: Journal    
DOI: 10.1111/j.1601-0825.2012.01975.x     Document Type: Article

References (65)

1. Alcaraz M, Acevedo C, Castillo J et al (2009). Liposoluble antioxidants provide an effective radioprotective barrier. Br J Radiol 82: 605-609.
2. Altinier G, Sosa S, Aquino RP, Mencherini T, Della Loggia R, Tubaro A (2007). Characterization of topical antiinflammatory compounds in Rosmarinus officinalis L. J Agric Food Chem 55: 1718-1723.
3. Álvarez Sánchez N (2010). Efectos saludables de flavonoides. Estudio experimental in vitro e in vivo. Tesis Doctoral. Universidad de Murcia, Murcia.
4. del Bano MJ, Lorente J, Castillo J et al (2003). Phenolic diterpenes, flavones, and rosmarinic acid distribution during the development of leaves, flowers, stems, and roots of Rosmarinus officinalis. Antioxidant activity. J Agric Food Chem 51: 4247-4253.
5. Barnes L, Evenson JW, Reichart P, Sindransky D (2005). World Health Organization Classification of Tumours. Pathology and genetics of head and neck tumours. IARC Press: Lyon.
6. Benavente-García O, Castillo J (2008). Update on uses and properties of citrus flavonoids: new findings in anticancer, cardiovascular, and anti-inflammatory activity. J Agric Food Chem 56: 6185-6205.
7. Benavente-García O, Castillo J, Alcaraz M, Vicente V, Del Río JA, Ortuño A (2007). Beneficial action of Citrus flavonoids on multiple cancer-related biological pathways. Curr Cancer Drug Targets 7: 795-809.
8. Burda S, Oleszek W (2001). Antioxidant and antiradical activities of flavonoids. J Agric Food Chem 49: 2774-2779.
9. Cantrell CL, Richheimer SL, Nicholas GM, Schmidt BK, Bailey DT (2005). Seco-Hinokiol, a new abietane diterpenoid from Rosmarinus officinalis. J Nat Prod 68: 98-100.
10. Chen D, Landis-Piwowar KR, Chen MS, Dou QP (2007). Inhibition of proteasome activity by the dietary flavonoid apigenin is associated with growth inhibition in cultured breast cancer cells and xenografts. Breast Cancer Res 9: R80.
11. Cheung S, Tai J (2007). Anti-proliferative and antioxidant properties of rosemary Rosmarinus officinalis. Oncol Rep 17: 1525-1531.
12. Czernik M, Sroka J, Madeja Z, Czyz J (2008). Apigenin inhibits growth and motility but increases gap junctional coupling intensity in rat prostate carcinoma (MAT-LyLu) cell populations. Cell Mol Biol Lett 13: 327-338.
13. Feng L, Wang Z (2006). Chemopreventive effect of celecoxib in oral pre-cancers and cancers. Laryngoscope 116: 1842-1845.
14. Fotsis T, Pepper MS, Pepper MS et al (1997). Flavonoids, dietary-derived inhibitors of cell proliferation and "in vitro" angiogenesis. Cancer Res 57: 2946-2951.
15. Garg AK, Buchholz TA, Aggarwal BB (2005). Chemosensitization and radiosensitization of tumors by plant polyphenols. Antioxid Redox Signal 7: 1630-1647.
16. Gigante B, Santos C, Silva AM et al (2003). Catechols from abietic acid: synthesis and evaluation as bioactive compounds. Bioorg Med Chem 11: 1631-1638.
17. Grawish ME (2008). Effects of Spirulina platensis extract on Syrian hamster cheek pouch mucosa painted with 7,12-dimetylbenzanthracene. Oral Oncol 44: 956-962.
18. Gupta S, Afaq F, Mukhtar H (2001). Selective growth-inhibitory, cell-cycle deregulatory and apoptotic response of apigenin in normal versus human prostate carcinoma cells. Biochem Biophys Res Commun 287: 914-920.
19. Gupta S, Afaq F, Mukhtar H (2002). Involvement of nuclear factor-kappa B, Bax and Bcl-2 in induction of cell cycle arrest and apoptosis by apigenin in human prostate carcinoma cells. Oncogene 21: 3727-3738.
20. Hashibe M, Brennan P, Benhamou S et al (2007). Alcohol drinking in never users of tobacco, cigarette smoking in never drinkers, and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. J Natl Cancer Inst 99: 777-789.
21. Hashimoto N (2012). Expression of COX2 and p53 in rat esophageal cancer induced by reflux of duodenal contents. Gastroenterol. In press: doi:10.5402/2012/914824.
22. Havsteen BH (2002). The biochemistry and medical significance of the flavonoids. Pharmacol Ther 96: 67-202.
23. Hu XW, Meng D, Fang J (2008). Apigenin inhibited migration and invasion of human ovarian cancer A2780 cells through focal adhesion kinase. Carcinogenesis 29: 2369-2376.
24. Huang MT, Ho CT, Wang ZT et al (1994). Inhibition of skin tumorigenesis by rosemary and its constituents carnosol and ursolic acid. Cancer Res 54: 701-708.
25. Hussain AR, Khan AS, Ahmed SO et al (2010). Apigenin induces apoptosis via downregulation of S-phase kinase-associated protein 2-mediated induction of p27Kip1 in primary effusion lymphoma cells. Cell Prolif 43: 170-183.
26. Iwashita K, Kobori M, Yamaki K, Tsushida T (2000). Flavonoids inhibit cell growth and induce apoptosis in B16 melanoma 4A5 cells. Biosci Biotechnol Biochem 64: 1813-1820.
27. Kim JS, Kim JC, Shim SH et al (2006). Chemical constituents of the root of Dystaenia takeshimana and their anti-inflammatory activity. Arch Pharm Res 29: 617-623.
28. Lambert JD, Hong J, Yang G, Liao J, Yang CS (2005). Inhibition of carcinogenesis by polyphenols: evidence from laboratory investigations. Am J Clin Nutr 81Suppl: 284S-291S.
29. Lee WJ, Chen WK, Wang CJ, Lin WL, Tseng TH (2008). Apigenin inhibits HGF-promoted invasive growth and metastasis involving blocking PI3K/Akt pathway and beta 4 integrin function in MDA-MBB breast cancer cells. Toxicol Appl Pharmacol 226: 178-191.
30. Letchoumy PV, Mohan KV, Stegeman JJ, Gelboin HV, Hara Y, Nagini S (2008). In vitro antioxidative potential of lactoferrin and black tea polyphenols and protective effects in vivo on carcinogen activation, DNA damage, proliferation, invasion, and angiogenesis during experimental oral carcinogenesis. Oncol Res 17: 193-203.
31. Lindenmeyer F, Li H, Menashi S, Soria C, Lu H (2001). Apigenin acts on the tumor cell invasion process and regulates protease production. Nutr Cancer 39: 139-147.
32. Manach C, Donovan JL (2004). Pharmacokinetics and metabolism of dietary flavonoids in humans. Free Radic Res 38: 771 -785.
33. Manoharan S, Balakrishnan S, Menon VP, Alias LM, Reena AR (2009). Chemopreventive efficacy of curcumin and piperine during 7,12-dimethylbenz[a]anthracene-induced hamster buccal pouch carcinogenesis. Singapore Med J 50: 139-146.
34. Manoharan S, Balakrishnan S, Vinothkumar V, Silvan S (2010a). Anti-clastogenic potential of carnosic acid against 7,12-dimethylbenz(a)anthracene (DMBA)-induced clastogenesis. Pharmacol Rep 62: 1170-1177.
35. Manoharan S, VasanthaSelvan M, Silvan S, Baskaran N, Kumar Singh A, Vinoth Kumar V (2010b). Carnosic acid: a potent chemopreventive agent against oral carcinogenesis. Chem Biol Interact 188: 616-622.
36. Masuda T, Inaba Y, Takeda Y (2001). Antioxidant mechanism of carnósico acid: structural identification of two oxidation products. J Agric Food Chem 49: 5560-5565.
37. Moreno S, Scheyer T, Romano CS, Vpjnov AA (2006). Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radic Res 40: 223-231.
38. Nicholas C, Batra S, Vargo MA et al (2007). Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-{kappa} B through the suppression of p65 phosphorylation. J Immunol 179: 7121.
39. Ninomiya K, Matsuda H, Shimoda H et al (2004). Carnosic acid, a new class of lipid absorption inhibitor from sage. Bioorg Med Chem Lett 14: 1943-1946.
40. Offord EA, Mace K, Ruffieux C, Malnoe A, Pfeifer AMA (1995). Rosemary components inhibit benzo[a]pyrene-induced genotoxicity in human bronchial cells. Carcinogenesis 16: 2057-2062.
41. Offord EA, Mace K, Avanti O, Pfeifer AMA (1997). Mechanism involved in the chemoprotective effects of rosemary extract studied in human liver and bronchial cells. Cancer Lett 114: 275-281.
42. Oluwatuyi M, Kaatz GW, Gibbson S (2004). Antibacterial and resistance modifying activity of Rosmarinus officinalis. Phytochemsitry 65: 3249-3254.
43. Patel D, Shukla S, Gupta S (2007). Apigenin and cancer chemoprevention: progress, potential and promise (review). Int J Oncol 30: 233-245.
44. Prasad S, Phromnoi K, Yadav VR, Chaturvedi MM, Aggarwal BB (2010). Targeting inflammatory pathways by flavonoids for prevention and treatment of cancer. Planta Med 76: 1044-1063.
45. Rezai-Zadeh K, Ehrhart J, Bai Y et al (2008). Apigenin and luteolin modulate microglial activation via inhibition of STAT1-induced CD40 expression. J Neuroinflammation 5: 41.
46. Salley JJ (1954). Experimental carcinogenesis in the cheek pouch of the Syrian hamster. J Dent Res 33: 253-262.
47. Saroja M, Balasenthil S, Ramachandran CR, Nagini S (2001). Coffee enhances development of 7,12-dymethylbenz[a]anthracene (DMBA)-induced hamster buccal pouch carcinomas. Oral Oncol 37: 172-176.
48. Sawant SS, Kandarkar SV (2000). Role of vitamins C and E as chemopreventive agents in the hamster cheek pouch treated with the oral carcinogen DMBA. Oral Dis 6: 241-247.
49. Scully C, Bagan JV (2007). Recent advances in oral oncology. Oral Oncol 43: 107-115.
50. Shukla S, Gupta S (2006). Molecular targets for apigenininduced cell cycle arrest and apoptosis in prostate cancer cell xenograft. Mol Cancer Ther 5: 843-852.
51. Shukla S, Gupta S (2008). Apigenin-induced prostate cancer cell death is initiated by reactive oxygen species and p53 activation. Free Radic Biol Med 44: 1833-1845.
52. Shukla S, Gupta S (2010). Apigenin: a promising molecule for cancer prevention. Pharm Res 27: 962-978.
53. Silvan S, Manoharan S, Baskaran N, Singh AK (2010). Apigenin: a potent antigenotoxic and anticlastogenic agent. Biomed Pharmacother. In press: doi:10.1016/j.biopha.2010.08.005.
54. Silvan S, Manoharan S, Baskaran N, Anusuya C, Karthikeyan S, Prabhakar MM (2011). Chemopreventive potential of apigenin in 7,12-dimethylbenz(a)anthracene induced experimental oral carcinogenesis. Eur J Pharmacol 670: 571-577.
55. Singletary KW, Nelshoppen JM (1991). Inhibition of 7,12-dimethylbenz[ a]anthrazene (DMBA)-induced mammary tumorigenesis and of in vivo formation of mammary DMBA-DNA adducts by rosemary extract. Cancer Lett 60: 169-175.
56. Slamenova D, Kuboskova K, Horvathova E, Robichova S (2002). Rosemary-stimulated reduction of DNA strand breaks and FPGsensitive sites in mammalian cells treated with H2O2 or visible light-excited Methylene Blue. Cancer Lett 177: 145-153.
57. Vairaktaris E, Spyridonidou S, Papakosta V et al (2008). The hamster model of sequential oral oncogenesis. Oral Oncol 44: 315-324.
58. Van Dross RT, Hong X, Pelling JC (2005). Inhibition of TPAinduced cyclooxygenase-2 (COX-2) expression by apigenin through downregulation of Akt signal transduction in human keratinocytes. Mol Carcinog 44: 83-91.
59. Van Dross R, Hong X, Essengue S, Fischer S, Pelling J (2007). Modulation of UVB-induced and basal cyclooxygenase-2 (COX-2) expression by apigenin in mouse keratinocytes: role of USF transcription factors. Mol Carcinog 46: 303-314.
60. Visanji JM, Thompson DG, Padfield PJ (2006). Induction of G2/ M phase cell cycle arrest by carnosol and carnosic acid is associated with alteration of cyclin A and cyclin B1 levels. Cancer Lett 237: 130-136.
61. Yang Y, Zhou ZT, Ge JP (2006). Effect of genistein on DMBAinduced oral carcinogenesis in hamster. Carcinogenesis 27: 578-583.
62. Yang SF, Yang WE, Kuo WH, Chang HR, Chu SC, Hsieh YS (2008). Antimetastatic potential of flavones on oral cancer cell via an inhibition of matrix-degrading proteases. Arch Oral Biol 93: 287-294.
63. Yesil-Celiktas O, Sevimil C, Bedir E, Vardar-Sukan F (2010). Inhibitory effects of rosemary extracts, carnosic acid and rosmarinic acid on the growth of various human cancer cell lines. Plant Food Hum Nutr 65: 158-163.
64. Zhang Q, Zhao XH, Wang ZJ (2009). Cytotoxicity of flavones and flavonols to a human esophageal squamous cell carcinoma cell line (KYSE-510) by induction of G2/M arrest and apoptosis. Toxicol In Vitro 23: 797-807.
65. Zhou ZT, Yang Y, Ge JP (2006). The preventive effect of salvianolic acid B on malignant transformation of DMBAinduced oral premalignant lesions in hamsters. Carcinogenesis 27: 826-832.