Kaempferol targets RSK2 and MSK1 to Suppress UV radiation-induced skin cancer

Cancer Prevention Research

Volumn 7, Issue 9, 2014, Pages 958-967

  Dong, Zigang ^a   Yao, Ke ^a,b   Chen, Hanyong ^a   Liu, Kangdong ^a,b   Langfald, Alyssa ^a   Yang, Ge ^a,b   Zhang, Yi ^a,b   Yu, Dong Hoon ^a   Kim, Myoung Ok ^a,c   Lee, Mee Hyun ^a,d   Li, Haitao ^a   Bae, Ki Beom ^a   Kim, Hong Gyum ^a   Ma, Wei Ya ^a   Bode, Ann M ^a   Dong, Ziming ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b ZHENGZHOU UNIVERSITY   (China)

^c Kyungpook National University   (South Korea)

^d The Catholic University of Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CAMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTONE H3; KAEMPFEROL; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN; PROTEIN C FOS; RIBOSOMAL S6 KINASE PROTEIN; S6 KINASE; SEPHAROSE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; KAEMPFEROL DERIVATIVE; MITOGEN AND STRESS-ACTIVATED PROTEIN KINASE 1; RIBOSOMAL PROTEIN S6 KINASE, 90KDA, POLYPEPTIDE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING SITE; BROCCOLI; CANCER GROWTH; CANCER INCIDENCE; CANCER THERAPY; CELL PROLIFERATION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DRUG MECHANISM; DRUG SAFETY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GRAPE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PLANT PRODUCT; PROTEIN PHOSPHORYLATION; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; SKIN CANCER; SKIN CARCINOGENESIS; SKIN CELL; SOLAR RADIATION; SOLAR ULTRAVIOLET RADIATION; SQUAMOUS CELL CARCINOMA; TEA; ULTRAVIOLET RADIATION; UPREGULATION; ADVERSE EFFECTS; ANIMAL; CARCINOMA, SQUAMOUS CELL; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RADIATION RESPONSE; SKIN NEOPLASMS; SUNLIGHT;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; HUMANS; IMMUNOHISTOCHEMISTRY; KAEMPFEROLS; MICE; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SKIN NEOPLASMS; SUNLIGHT; ULTRAVIOLET RAYS;

EID: 84907287826     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-14-0126     Document Type: Article

References (48)

1. Stern RS. Prevalence of a history of skin cancer in 2007: results of an incidence-based model. Arch Dermatol 2010;146:279-82.
2. Robinson JK. Sun exposure, sun protection, and vitamin D. JAMA 2005;294:1541-3.
3. Berwick M, Lachiewicz A, Pestak C, Thomas N. Solar UV exposure and mortality from skin tumors. Adv Exp Med Biol 2008;624:117-24.
4. de Gruijl FR. Skin cancer and solar UV radiation. Eur J Cancer 1999; 35:2003-9.
5. Chang L, Karin M.MammalianMAPkinase signalling cascades. Nature 2001;410:37-40.
6. Bode AM, Dong Z. Mitogen-activated protein kinase activation in UVinduced signal transduction. Sci STKE 2003;2003:RE2.
7. Dhillon AS, Hagan S, Rath O, Kolch W. MAP kinase signalling pathways in cancer. Oncogene 2007;26:3279-90.
8. Li J, Malakhova M, Mottamal M, Reddy K, Kurinov I, Carper A, et al. Norathyriol suppresses skin cancers induced by solar ultraviolet radiation by targeting ERK kinases. Cancer Res 2012;72:260-70.
9. Liu K, Yu D, Cho YY, Bode AM,MaW, Yao K, et al. Sunlight UV-induced skin cancer relies upon activation of the p38alpha signaling pathway. Cancer Res 2013;73:2181-8.
10. Frodin M, Jensen CJ, Merienne K, Gammeltoft S. A phosphoserineregulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J 2000;19:2924-34.
11. Kim HG, Lee KW, Cho YY, Kang NJ, Oh SM, Bode AM, et al. Mitogen-and stress-activated kinase 1-mediated histone H3 phosphorylation is crucial for cell transformation. Cancer Res 2008; 68:2538-47.
12. Cho YY, Yao K, Pugliese A, Malakhova ML, Bode AM, Dong Z. A regulatory mechanism for RSK2 NH(2)-terminal kinase activity. Cancer Res 2009;69:4398-406.
13. Cho YY, Lee MH, Lee CJ, Yao K, Lee HS, Bode AM, et al. RSK2 as a key regulator in human skin cancer. Carcinogenesis 2012;33:2529-37.
14. Chang S, Iversen L, Kragballe K, Arthur JS, Johansen C. Mice lacking MSK1 and MSK2 show reduced skin tumor development in a two-stage chemical carcinogenesis model. Cancer Invest 2011; 29:240-5.
15. Liu H, Hwang J, Li W, Choi TW, Liu K, Huang Z, et al. A derivative of chrysin suppresses two-stage skin carcinogenesis by inhibiting mitogen-and stress-activated kinase 1. Cancer Prev Res 2014; 7:74-85.
16. Li ZD, Hu XW, Wang YT, Fang J. Apigenin inhibits proliferation of ovarian cancer A2780 cells through Id1. FEBS Lett 2009;583:1999-2003.
17. Zhou Q, Yan B, Hu X, Li XB, Zhang J, Fang J. Luteolin inhibits invasion of prostate cancer PC3 cells through E-cadherin. Mol Cancer Ther 2009;8:1684-91.
18. Byun S, Lee KW, Jung SK, Lee EJ, Hwang MK, Lim SH, et al. Luteolin inhibits protein kinase C(epsilon) and c-Src activities and UVB-induced skin cancer. Cancer Res 2010;70:2415-23.
19. Schrodinger. Schrodinger Suite 2013. Schrodinger, LLC, New York, NY; 2013.
20. Trempus CS, Morris RJ, Bortner CD, Cotsarelis G, Faircloth RS, Reece JM, et al. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol 2003;120:501-11.
21. Zaidi MR, De Fabo EC, Noonan FP, Merlino G. Shedding light on melanocyte pathobiology in vivo. Cancer Res 2012;72:1591-5.
22. Cho YY, Yao K, Kim HG, Kang BS, Zheng D, Bode AM, et al. Ribosomal S6 kinase 2 is a key regulator in tumor promoter induced cell transformation. Cancer Res 2007;67:8104-12.
23. Scaltriti M, Baselga J. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res 2006;12:5268-72.
24. Oi N, Chen H, Ok Kim M, Lubet RA, Bode AM, Dong Z. Taxifolin suppresses UV-induced skin carcinogenesis by targeting EGFR and PI3K. Cancer Prev Res 2012;5:1103-14.
25. Geryk-Hall M, Yang Y, Hughes DP. Driven to death: inhibition of farnesylation increases Ras activity in osteosarcoma and promotes growth arrest and cell death. Mol Cancer Ther 2010;9:1111-9.
26. Tsao H, Chin L, Garraway LA, Fisher DE. Melanoma: from mutations to medicine. Genes Dev 2012;26:1131-55.
27. Katiyar SK, Athar M. Grape seeds: ripe for cancer chemoprevention. Cancer Prev Res 2013;6:617-21.
28. Liu K, Cho YY, Yao K, Nadas J, Kim DJ, Cho EJ, et al. Eriodictyol inhibits RSK2-ATF1 signaling and suppresses EGF-induced neoplastic cell transformation. J Biol Chem 2011;286:2057-66.
29. Keum YS, Kim HG, Bode AM, Surh YJ, Dong Z. UVB-induced COX-2 expression requires histone H3 phosphorylation at Ser10 and Ser28. Oncogene 2013;32:444-52.
30. Cho YY, He Z, Zhang Y, Choi HS, Zhu F, Choi BY, et al. The p53 protein is a novel substrate of ribosomal S6 kinase 2 and a critical intermediary for ribosomal S6 kinase 2 and histone H3 interaction. Cancer Res 2005;65:3596-603.
31. 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;18:2828-35.
32. Wang J, Ouyang W, Li J, Wei L, Ma Q, Zhang Z, et al. Loss of tumor suppressor p53 decreases PTEN expression and enhances signaling pathways leading to activation of activator protein 1 and nuclear factor kappaB induced by UV radiation. Cancer Res 2005;65:6601-11.
33. Peng C, Cho YY, Zhu F, Xu YM, Wen W, Ma WY, et al. RSK2 mediates NF-kB activity through the phosphorylation of IkappaBalpha in the TNF-R1 pathway. FASEB J 2010;24:3490-9.
34. Gambichler T, Boms S, Stucker M, Moussa G, Kreuter A, Sand M, et al. Acute skin alterations following ultraviolet radiation investigated by optical coherence tomography and histology. Arch Dermatol Res 2005;297:218-25.
35. Cole N, Sou PW, Ngo A, Tsang KH, Severino JA, Arun SJ, et al. Topical 'Sydney' propolis protects against UV-radiation-induced inflammation, lipid peroxidation and immune suppression in mouse skin. Int Arch Allergy Immunol 2010;152:87-97.
36. Vicentini FT, Fonseca YM, Pitol DL, IyomasaMM,Bentley MV, Fonseca MJ. Evaluation of protective effect of a water-in-oil microemulsion incorporating quercetin against UVB-induced damage in hairless mice skin. J Pharm Pharm Sci 2010;13:274-85.
37. Jin XJ, Kim EJ, Oh IK, Kim YK, Park CH, Chung JH. Prevention of UVinduced skin damages by 11,14,17-eicosatrienoic acid in hairless mice in vivo. J Korean Med Sci 2010;25:930-7.
38. Bowden GT. Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat Rev Cancer 2004;4:23-35.
39. Leiter U, Garbe C. Epidemiology of melanoma and nonmelanoma skin cancer-the role of sunlight. Adv Exp Med Biol 2008;624:89-103.
40. Filipowicz E, Adegboyega P, Sanchez RL, Gatalica Z. Expression of CD95 (Fas) in sun-exposed human skin and cutaneous carcinomas. Cancer 2002;94:814-9.
41. Zhang Y, Dong Z, Bode AM, Ma WY, Chen N. Induction of EGFRdependent and EGFR-independent signaling pathways by ultraviolet A irradiation. DNA Cell Biol 2001;20:769-79.
42. Chen W, Tang Q, Gonzales MS, Bowden GT. Role of p38 MAP kinases and ERK in mediating ultraviolet-B induced cyclooxygenase-2 gene expression in human keratinocytes. Oncogene 2001; 20:3921-6.
43. Satoh Y, Kobayashi Y, Takeuchi A, Pages G, Pouyssegur J, Kazama T. Deletion of ERK1 and ERK2 in the CNS causes cortical abnormalities and neonatal lethality: Erk1 deficiency enhances the impairment of neurogenesis in Erk2-deficient mice. J Neurosci 2011;31:1149-55.
44. Park J, Al-Ramahi I, Tan Q, Mollema N, Diaz-Garcia JR, Gallego-Flores T, et al. RAS-MAPK-MSK1 pathway modulates ataxin 1 protein levels and toxicity in SCA1. Nature 2013;498:325-31.
45. Lee CC, Lin YH, Chang WH, Lin PC, Wu YC, Chang JG. Squamocin modulates histone H3 phosphorylation levels and induces G1 phase arrest and apoptosis in cancer cells. BMC Cancer 2011; 11:58.
46. Sweeney SE, Firestein GS. Mitogen activated protein kinase inhibitors: where are we now and where are we going? Ann Rheum Dis 2006;65 Suppl 3:iii83-8.
47. Saud SM, Young MR, Jones-Hall YL, Ileva L, Evbuomwan MO, Wise J, et al. Chemopreventive activity of plant flavonoid isorhamnetin in colorectal cancer is mediated by oncogenic Src and beta-catenin. Cancer Res 2013;73:5473-84.
48. Ren W, Qiao Z, Wang H, Zhu L, Zhang L. Flavonoids: promising anticancer agents. Med Res Rev 2003;23:519-34.