Inhibition of ultraviolet B-induced AP-1 activation by theaflavins from black tea

Molecular Carcinogenesis

Volumn 28, Issue 3, 2000, Pages 148-155

  Nomura, Masaaki ^a   Ma, Wei Ya ^a   Huang, Chuanshu ^a   Yang, Chung S ^b   Bowden, G Tim ^c   Miyamoto, Ken Ichi ^d   Dong, Zigang ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d KANAZAWA UNIVERSITY   (Japan)

Author keywords

C jun NH2 terminal kinases; Extracellular signal regulated protein kinases; Mitogen activated protein kinases; Tea polyphenols

Indexed keywords

EPIGALLOCATECHIN GALLATE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; POLYPHENOL; STRESS ACTIVATED PROTEIN KINASE; THEAFLAVIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER PREVENTION; CARCINOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TEA; ULTRAVIOLET B RADIATION;

ANIMALS; ANTICARCINOGENIC AGENTS; BIFLAVONOIDS; CAFFEINE; CATECHIN; CELL LINE; DEPRESSION, CHEMICAL; ENZYME ACTIVATION; EPIDERMIS; GENE EXPRESSION REGULATION; GENES, REPORTER; LUCIFERASES; MAP KINASE SIGNALING SYSTEM; MICE; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; TEA; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TRANSFECTION; ULTRAVIOLET RAYS;

CAMELLIA SINENSIS;

EID: 0033852003     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/1098-2744(200007)28:3<148::AID-MC3>3.0.CO;2-Q     Document Type: Article

References (62)

1. Shea CR, Parrish JA. Nonionizing radiation and the skin. In: Goldsmith LA, editor. Physiology, biochemistry and molecular biology of the skin New York: Oxford University Press; 1991. p 910-927.
2. Epstein JH. Photocarcinogenesis, skin cancer and aging. J Am Acad Dermatol 1983;9:487-507.
3. Mukhtar H, Elmets CA. Photocarcinogenesis: Mechanisms, models and human health implications. Photochem Photobiol 1996;63:356-357.
4. De Gruijl FR, Forbes PD. UV-induced skin cancer in a hairless mouse model. Bioessays 1995;17:651-660.
5. Ley RD. Photoreactivation in humans. Proc Natl Acad Sci USA 1993;90:4337.
6. Matsui MS, de Leo VA. Mechanisms and human relevance. In: Mukhtar H, editor. Skin cancer. Boca Raton: CRC Press; 1995. p 21-30.
7. Ananthaswamy HN, Pierceall WE. Molecular mechanisms of ultraviolet radiation carcinogenesis. Photochem Photobiol 1990;52:1119-1136.
8. Staberg B, Wulf HC, Klemp P, Poulsen T, Brodthagen H. The carcinogenic effect of UVA irradiation. J Invest Dermatol 1983;81:517-519.
9. Isoherranen K, Westermarck J, Kahari VM, Jansen C, Punnonen K. Differential regulation of the AP-1 family members by UV irradiation in vitro and in vivo. Cell Signal 1998;10:191-195.
10. Huang C, Ma WY, Bowden GT, Dong Z. Ultraviolet B-induced activated protein-1 activation does not require epidermal growth factor receptor but is blocked by a dominant negative PKCλ/ι. J Biol Chem 1996;27: 31262-31268.
11. Huang C, Ma WY, Dong Z. The extracellular-signal-regulated protein kinases (Erks) are required for UV-induced AP-1 activation in JB6 cells. Oncogene 1999;18:2828-2835.
12. Bender K, Göttlicher M, Whiteside S, Rahmsdorf HJ, Herrlich P. Sequential DNA damage-independent and dependent activation of NF-κB by UV. EMBO J 1998;17:5170-5181.
13. Chen W, Borchers AH, Dong Z, Powell MB, Bowden GT. UVB irradiation-induced activator protein-1 activation correlates with increased c-fos gene expression in a human keratinocyte cell line. J Biol Chem 1998;273:32176-32181.
14. Dong Z, Colburn NH. A molecular target for prevention of carcinogenesis. In: Srivastava S, Lippman SM, Hong WK, Mulshine JL, editors. Early detection of cancer. New York: Futura Publishing; 1994. p 123-130.
15. Angel P. The role and regulation of the Jun proteins in response to phorbol ester and UV light. In: Baeurle PA, editor. Induced gene expression. Boston: Birkhauser; 1995. p 62-92.
16. Derijard B, Hibi M, Wu IH, et al. JNK1: A protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 1994;76: 1025-1037.
17. Devary Y, Gottlieb RA, Lau LF, Karn M. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol 1991;11:2804-2811.
18. Dong Z, Birrer MJ, Watts RG, Matrisian LM, Colburn NH. Blocking tumor promoter induced AP-1 activity inhibits transformation in JB6 cells. Proc Natl Acad Sci 1994;91: 609-613.
19. Dong Z, Watts SG, Sun Y, Colburn NH. Progressive elevation of AP-1 activity during preneoplastic-to-neoplastic progression as modeled in mouse JB6 cell variants. Int J Oncol 1995;7:359-364.
20. Yang CS, Wang ZY. Tea and cancer: A review. J Natl Cancer Inst 1993;58:1038-1049.
21. Yang CS, Yang GY, Lee ML, Chen L. Mechanistic considerations of the inhibition of carcinogenesis by tea. In: Ohigashi H, editor. Proceedings of the international conference on food factors in cancer prevention. Tokyo: Springer-Verlag; 1997 p 113-117.
22. Kaiyar SK, Mukhtar H. Tea in chemoprevention of cancer: Epidemiologic and experimental studies. Int J Oncol 1996;8: 221-238.
23. Dreosti IE, Wargovich MJ, Yang CS. Inhibition of carcinogenesis by tea: The evidence from experimental studies. Crit Rev Food Sci Nutr 1997;37:761-770.
24. Gensler HL, Timmermann BN, Valcic S, et al. Prevention of photocarcinogenesis by topical administration of pure epigallocatechin gallate isolated from green tea. Nutr Cancer 1996;26:325-335.
25. Lin JK, Lee SF. Inhibition of tumor promotion through blocking signal transduction. Zool Stud 1995;34:67-81.
26. Barthelman M, Bair WB 3rd, Stickland KK, et al. (-)-Epigallocatechin-3-gallate inhibition of ultraviolet B-induced AP-1 activity. Carcinogenesis 1998;19: 2201-2204.
27. Chen W, Dong Z, Valcic S, Timmermann BN, Bowden GT. Inhibition of ultraviolet B-induced c-fos gene expression and p38 mitogen-activated protein kinase activation by (-)-epigallocatechin gallate in a human keratinocyte cell line. Mol Carcinog 1999;24:79-84.
28. Lu YP, Lou YR, Xie JG, Yen P, Huang MT, Conney AH. Inhibitory effect of black tea on the growth of established skin tumors in mice: Effects on tumor size, apoptosis, mitosis and bromodeoxyuridine incorporation into DNA. Carcinogenesis 1997;18:2163-2169.
29. Dong Z, Ma WY, Huang C, Yang CS. Inhibition of tumor promoter-induced activator protein 1 activation and cell transformation by tea polyphenols, (-)-epigallocatechin gallate, and theaflavins. Cancer Res 1997;57:4414-4419.
30. Record IR, Dreosti IE. Protection by black tea and green tea against UVB and UVA+B induced skin cancer in hairless mice. Mutat Res 1998;422:191-199.
31. Huang MT, Xie JG, Wange ZY, et al. Effects of tea, decaffeinated tea, and caffeine on UVB light-induced complete carcinogenesis in SKH-1 mice: Demonstration of caffeine as a biologically important constituent of tea. Cancer Res 1997;57:2623-2629.
32. Chung JY, Huang C, Meng X, et al. Inhibition of activator protein 1 activity and cell growth by purified green tea and black tea polyphenols in H-ras-transformed cells: Structure-activity relationship and mechanisms involved. Cancer Res 1999;58:4610-4617.
33. Huang C, Ma WY, Ding M, Bowden GT, Dong Z. Direct evidence for an important role of sphingomyelinase in ultraviolet-induced activation of c-Jun N-terminal kinase. J Biol Chem 1997;272:27753-27757.
34. Yang GY, Liu Z, Seril DN, et al. Black tea constituents, theaflavins, inhibit 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK)-induced lung tumorigenesis in A/J mice. Carcinogenesis 1997;18:2361-2365.
35. Liang YC, Chen YC, Lin YL, Lin-Shiau SY, Ho CT, Lin JK. Suppression of extracellular signals and cell proliferation by the black tea polyphenol, theaflavin-3,3′-digallate. Carcinogenesis 1999;20:733-736.
36. Mukhtar H, Ahmad N, Mechanism of cancer chemopreventive activity of green tea. Proc Soc Exp Biol Med 1999; 220:234-238.
37. Shiraki M, Hara Y, Osawa T, Kumon H, Nakayama T, Kawakishi S. Antioxidative and antimutagenic effects of theaflavins from black tea. Mutat Res 1994;323:29-34.
38. Lin YL, Tsai SH, Lin-Shiau SY, Ho CT, Lin JK. Theaflavin-3,3′-digallate from black tea blocks the nitric oxide synthase by down-regulating the activity of NF-κB in macrophage. Eur J Phalmacol 1999;367:379-388.
39. Marshall CJ. Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 1995;80:179-185.
40. Hunter T. Protein kinases and phosphatases: The yin and yang of protein phosphorylation and signaling. Cell 1995; 80:225-236.
41. Hill CS, Triesman R. Transcriptional regulation by extracellular signals: Mechanisms and specificity Cell 1995;80: 199-211.
42. Cowley S, Paterson H, Kemp P, Marshall CJ. Activation of MAP kinase is necessary and sufficient for PC 12 differentiation and for transformation of NIH 3T3 cells. Cell 1994;77: 841-852.
43. Buscher M, Rahmsdorf HJ, Litfin M, Karin M, Herrlich P. Activation of the c-fos gene by UV and phorbol ester: Different signal transduction pathways converge to the same enhancer element Oncogene 1988;3:301-311.
44. Ludwig S, Engel K, Hoffmeyer A, et al. 3pK, a novel mitogen-activated protein (MAP) kinase-activated protein kinase, is targeted by three MAP kinase pathways. Mol Cell Biol 1996;16:6687-6697.
45. Minden A, Lin A, McMahon M, et al. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 1994;266:1719-1723.
46. Sanchez I, Hughes RT, Mayer BJ, et al. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature 1994;372:794-798.
47. Dalton S, Treisman R. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell 1992;68:597-612.
48. L'Allemain G, Her JH, Wu J, Sturgill TW, Weber MJ. Growth factor-induced activation of a kinase activity which causes regulatory phosphorylation of p42/microtubule-associated protein kinase. Mol Cell Biol 1992;12:2222-2229.
49. Pages G, Lenormand P, L'Allemain G, Chambard JC, Meloche S, Pouyssegur J. Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc Natl Acad Sci 1993;90:8319-8323.
50. Wan Y, Kurosaki T, Huang XY. Tyrosine kinases in activation of the MAP kinase cascade by G-protein-coupled receptors. Nature 1996;380:541-544.
51. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995;270:1326-1331.
52. Adler V, Pincus MR, Polotskaya A, Montano X, Friedman FK, Ronai Z. Activation of c-Jun-NH2-kinase by UV irradiation is dependent on p21ras. J Biol Chem 1996;271:23304-23309.
53. Adler V, Polotskaya A, Kim J, et al. Dose rate and mode of exposure are key factors in JNK activation by UV irradiation. Carcinogenesis. 1996;17:2073-2076.
54. Ben-Ari ET, Bernstein LR, Colburn NH. Differential c-jun expression in response to tumor promoters in JB6 cells sensitive or resistant to neoplastic transformation. Mol Carcinog 1992;5:62-74.
55. Bernstein LR, Colburn NH. AP1/jun function is differentially induced in promotion-sensitive and resistant JB6 cells. Science 1989;244:566-569.
56. Chen N, Ma WY, Yang CS, Dong Z. Inhibition of arsenic-induced apoptosis and AP-1 activity in JB6 cells by EGCG and Theaflavins. J Environ Pathol Toxicol Oncol. In Press, 2000.
57. Alani R, Brown P, Binetruy B, et al. The transactivating domain of the c-Jun proto-oncoprotein is required for cotransformation of rat embryo cells. Mol Cell Biol 1991;11: 6286-6295.
58. Domann FE, Levy JP, Birrer MJ, Bowden GT. Stable expression of a c-JUN deletion mutant in two malignant mouse epidermal cell lines blocks tumor formation in nude mice. Cell Growth Differ 1994;5:9-16.
59. Chen N, Ma WY, Huang C, Dong Z. Translocation of protein kinase Cε and protein kinase Cδ to membrane is required for ultraviolet B-induced activation of mitogen-activated protein kinases and apoptosis. J Biol Chem 1999;274: 15389-15394.
60. Huang C, Li J, Chen N, Ma WY, Bowden GT, Dong Z. Inhibition of atypical PKC blocks ultraviolet-induced AP-1 activation by specifically inhibiting ERKs activation Mol Carcinog 2000;27:65-75.
61. Hu G, Han C, Chen J. Inhibition of oncogen expression by green tea and (-)-epigallocatechin gallate in mice. Nutr Cancer 1995;24:203-209.
62. Chen YC, Liang YC, Lin-Shiau SY, Ho CT, Lin JK. Inhibition of TPA-induced protein kinase C and transcription activator protein-1 binding activities by theaflavin-3,3′-digallate from black tea in NIH 3T3 cells. J Agric Food Chem 1999; 47:1416-1421.