Resveratrol enhances cell-mediated immune response to DMBA through TLR4 and prevents DMBA induced cutaneous carcinogenesis

Molecular Carcinogenesis

Volumn 48, Issue 8, 2009, Pages 713-723

  Yusuf, Nabiha ^a,b   Nasti, Tahseen H ^a   Meleth, Sreelatha ^a   Elmets, Craig A ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

7,12 dimethylbenz(a)anthracene (DMBA); Chemoprevention; Resveratrol; Skin carcinogenesis; Toll like receptor 4 (TLR4)

Indexed keywords

DIMETHYLBENZ[A]ANTHRACENE; GAMMA INTERFERON; INTERLEUKIN 12; RESVERATROL; TOLL LIKE RECEPTOR 4; 7,12 DIMETHYLBENZ[A]ANTHRACENE; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; CARCINOGEN; MESSENGER RNA; STILBENE DERIVATIVE; TLR4 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SURVIVAL; CELLULAR IMMUNITY; CHEMOPROPHYLAXIS; CONTACT ALLERGY; CONTROLLED STUDY; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; SKIN TUMOR; TUMOR VOLUME; ANIMAL; C3H MOUSE; CELL PROLIFERATION; CHEMICALLY INDUCED DISORDER; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MUS; VITACEAE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CARCINOGENS; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNITY, CELLULAR; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SKIN NEOPLASMS; STILBENES; TOLL-LIKE RECEPTOR 4;

EID: 68849113447     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20517     Document Type: Article

References (55)

1. Takeda K, Kaisho T, Akira S. Toll like receptors. Annu Rev Immunol 2003;21:335-376.
2. Byrd-Liefer CA, Block EF, Takeda K, Akira S, Ding A. The role of MyD88 and TLR4 in the LPS-mimetic activity of taxol. Eur J Immunol 2001;31:2448-2457. (Pubitemid 32785364)
3. Okamura Y, Watari M, Jerud ES, et al. The extra domain A of fibronectin activates toll-like receptor 4. J Biol Chem 2001; 276:10229-10233. (Pubitemid 37391934)
4. Termeer C, Benedix F, Sleeman J, et al. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002;195:99-111. (Pubitemid 34074500)
5. Ohashi K, Burkart V, Flohé S, Kolb H. Cutting edge: Heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 2000;164:558-561. (Pubitemid 30043672)
6. Bauer AK, Dixon D, DeGraff LM, et al. Toll-like receptor 4 in butylated hydroxytoluene-induced mouse pulmonary inflammation and tumorigenesis. J Natl Cancer Inst 2005; 97:1778-1781. (Pubitemid 41782287)
7. Yusuf N, Nasti TH, Long JA, et al. Protective role of toll-like receptor 4 during the initiation stage of cutaneous chemical carcinogenesis. Cancer Res 2008;68:615-622.
8. McInturff JE, Modlin RL, Kim J. The role of toll-like receptors in the pathogenesis and treatment of dermatological disease. J Invest Dermatol 2005;125:1-8. (Pubitemid 40981417)
9. Rozis G, Benlahrech A, Duraisingham S, Gotch F, Patterson S. Human Langerhans' cells and dermal-type dendritic cells generated from CD34 stem cells express different toll-like receptors and secrete different cytokines in response to toll-like receptor ligands. Immunology 2008;124:329-338. (Pubitemid 351793465)
10. Athar M, Back JH, Tang X, et al. Resveratrol: A review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 2007;224:274-283. (Pubitemid 47575677)
11. Feng YH, Zhou WL, Wu QL, Li XY, Zhao WM, Zou JP. Low dose of resveratrol enhancedimmune response of mice. Acta Pharmacol Sin 2002;23:893-897.
12. Yang Y, Paik JH, Cho D, Cho JA, Kim CW. Resveratrol induces the suppression of tumor-derived CD4+CD25+ regulatory T cells. Int Immunopharmacol 2008;8:542-547.
13. Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997;275:218-220. (Pubitemid 127696281)
14. Afaq F, Adhami VM, Ahmad N, Mukhtar H. Botanical antioxidants for chemoprevention of photocarcinogenesis. Front Biosci 2002;7:d784-d792.
15. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63. (Pubitemid 14203433)
16. Klemme JC, Mukhtar H, Elmets CA. Induction of contact hypersensitivity to dimethylbenz(a)anthracene and benzo(a)- pyrene in C3H/HeN mice. Cancer Res 1987;47:6074-6078. (Pubitemid 18018756)
17. Ishihara Y, Nishikawa T, Iijima H, Matsunaga K. Expression of matrix metalloproteinase, tissue inihibitors of metalloproteinase and adhesion molecules in silicotic mice with lung tumor metastasis. Toxicol Lett 2003;142:71-75. (Pubitemid 36369216)
18. Wu J, Liu J, Waalkes MP, et al. High dietary fat exacerbates arsenic-induced liver fibrosis in mice. Exp Biol Med 2008;233: 377-384. (Pubitemid 351328579)
19. Shan S, Robson ND, Cao Y, et al. Responses of vascular endothelial cells to angiogenic signaling are important for tumor cell survival. FASEB J 2004;18:238-326.
20. Risau W. Differentiation of endothelium. FASEB J 1995;9: 926-933.
21. Yusuf N, Nasti TH, Katiyar SK, et al. Antagonistic roles of CD4+ and CD8+ T-cells in 7,12 dimethylbenz(a)anthracene cutaneous carcinogenesis. Cancer Res 2008;68:3924-3930.
22. Anderson C, Hehr A, Robbins R, et al. Metabolic requirements for induction of contact hypersensitivity to immunotoxic polyaromatic hydrocarbons. J Immunol 1995;155: 3530-3537.
23. Elmets CA, Athar M, Tubesing KA, Rothaupt D, Xu H, Mukhtar H. Susceptibility to the biological effects of polyaromatic hydrocarbons is influenced by genes of the major histocompatibility complex. Proc Natl Acad Sci USA 1998;95:14915-14919. (Pubitemid 29003731)
24. Athar M, Back JH, Tang X, et al. Resveratrol: A review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 2007;224:274-283. (Pubitemid 47575677)
25. Aziz MH, Reagan-Shaw S, Wu J, Longley BJ, Ahmad N. Chemoprevention of skin cancer by grape constituent resveratrol: Relevance to human disease? FASEB J 2005;19: 1193-1195.
26. Reagan-Shaw S, Afaq F, Aziz MH, Ahmad N. Modulations of critical cell cycle regulatory events during chemoprevention of ultraviolet B-mediated responses by resveratrol in SKH-1 hairless mouse skin. Oncogene 2004;23:5151-5160. (Pubitemid 38980348)
27. Aziz MH, Afaq F, Ahmad N. Prevention of ultraviolet-B radiation damage by resveratrol in mouse skin is mediated via modulation in survivin. Photochem Photobiol 2005;81: 25-31. (Pubitemid 40327556)
28. Boutwell RK, Bosch DK. The carcinogenicity of creosote oil: Its role in the induction of skin tumors in mice. Cancer Res 1958;18:1171-1175.
29. Friedmann PS, Wilkinson M. Occupational dermatoses. In: Bolognia JL, Jorizzo JL, Rapini RP, Horn TD, Mascaro JM, Saurat J-H, Mancini AJ, Salasche SJ, Stingl G, editors. Dermatology. London: Mosby; 2007.
30. Letzel S, Drexler H. Occupationally related tumors in tar refinery workers. J Am Acad Dermatol 1998;39:712-720. (Pubitemid 28519023)
31. Cookson HA. Epithelioma of the skin after prolonged exposure to creosote. Br Med J 1924;1:368.
32. Emmett EA. Occupational skin cancer: A review. J Occup Med 1975;17:44-449.
33. O'Donovan WJ. Epitheliomatous ulceration among tar workers. Br J Dermatol 1920;32:215-228.
34. O'Donovan WJ. Epitheliomatous ulceration among tar workers. Br J Dermatol 1920;32:245-252.
35. Pott P. Chirurgical works of Percivall Pott. In: Williams J, editor. Cancer Scroti. Dublin: James Williams; 1775. p. 403.
36. Boffetta P, Jourenkova N, Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control 1997;8: 444-472. (Pubitemid 27297808)
37. Fisher REW. Occupational skin cancer in a group of tar workers. Arch Ind Hyg Occup Med 1953;7:12-18.
38. Hueper WC, Payne WW. Carcinogenic studies on petroleum asphalt, cooling oil and coal tar. Arch Pathol 1960;70:372-384.
39. DiGiovanni J. Multistage carcinogenesis in mouse skin. Pharmacol Ther 1992;54:63-128.
40. DiGiovanni J. Genetic factors controlling responsiveness to skin tumor promotion in mice. Prog Clin Biol Res 1995; 391:195-212.
41. Angel JM, DiGiovanni J. Genetics of skin tumor promotion. Prog Exp Tumor Res 1999;35:143-157.
42. Gupta S, Mukhtar H. Chemoprevention of skin cancer: Current status and future prospects. Cancer Metastasis Rev 2002;21:363-380. (Pubitemid 36071921)
43. Bickers DR, Athar M. Novel approaches to chemoprevention of skin cancer. J Dermatol 2000;27:691-695. (Pubitemid 32015640)
44. Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4- dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-1059. (Pubitemid 47517504)
45. Hold GL, Rabkin CS, Chow WH, et al. A functional polymorphism of toll-like receptor 4 gene increases risk of gastric carcinoma and its precursors. Gastroenterology 2007;132:905-912.
46. Fukata M, Chen A, Vamadevan AS, et al. Toll-like receptor-4 promotes the development of colitis-associated colorectal tumors. Gastroenterology 2007;133:1869-1881. (Pubitemid 350186162)
47. Chen YC, Giovannucci E, Lazarus R, Kraft P, Ketkar S, Hunter DJ. Sequence variants of Toll-like receptor 4 and susceptibility to prostate cancer. Cancer Res 2005;65:11771-11778. (Pubitemid 41821739)
48. Del Vecchio M, Bajetta E, Canova S, et al. Interleukin-12: Biological properties and clinical application. Clin Cancer Res 2007;13:4677-4685. (Pubitemid 47294773)
49. Katiyar SK. UV-induced immune suppression and photo-carcinogenesis: Chemoprevention by dietary botanical agents. Cancer Lett 2007;255:1-11.
50. Müller-Decker K, Manegold G, Butz H, et al. Inhibition of cell proliferation by bacterial lipopolysaccharides in TLR4-positive epithelial cells: Independence of nitric oxide and cytokine release. J Invest Dermatol 2005;124:553-561. (Pubitemid 40381578)
51. Coughlin CM, Salhany KE, Wysocka M, et al. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J Clin Invest 1998;101:1441-1452. (Pubitemid 28145262)
52. Lehner M, Bailo M, Stachel D, Roesler W, Parolini O, Holter W. Caspase-8 dependent apoptosis induction in malignant myeloid cells by TLR stimulation in the presence of IFN-alpha. Leuk Res 2007;12:1729-1735.
53. Tano T, Okamoto M, Oshikawa T, Ahmed SU, Sasai A, Sato M. Induction of apoptosis in human head and neck cancer cell lines by an active component of OK-432 through p53- independent pathway via toll-like receptor (TLR) 4 signaling. Gan To Kagaku Ryoho 2005;32:1562-1564.
54. Akazawa T, Masuda H, Saeki Y, et al. Adjuvant-mediated tumor regression and tumor-specific cytotoxic response are impaired in MyD88-deficient mice. Cancer Res 2004;64: 757-764. (Pubitemid 38120920)
55. Soleas GJ, Angelini M, Grass L, Diamandis EP, Goldberg DM. Absorption of trans-resveratrol in rats. Methods Enzymol 2001;335:145-154.