Ursolic acid differentially modulates apoptosis in skin melanoma and retinal pigment epithelial cells exposed to UV-VIS broadband radiation

Apoptosis

Volumn 19, Issue 5, 2014, Pages 816-828

  Lee, Yuan Hao ^a   Wang, Exing ^b   Kumar, Neeru ^b   Glickman, Randolph D ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b University of Texas Health Science Center   (United States)

Author keywords

NF B; p53; Photo oxidative stress; Phytochemical; Ursolic acid

Indexed keywords

DNA; HYDROETHIDINE; PLANT MEDICINAL PRODUCT; PROTEIN P53; RAPAMYCIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TRANSCRIPTION FACTOR; TRITERPENOID; URSOLIC ACID; VISUAL PIGMENT;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; ASSAY; CARCINOMA CELL; CELL CYCLE ARREST; CELL PROLIFERATION; CELL PROTECTION; CLONOGENIC ASSAY; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFECT; ENZYME ACTIVATION; EPITHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LIGHT; MELANOMA; MEMBRANE PERMEABILITY; MICROSCOPY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOGENESIS; OPTICS; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHOTOOXIDATION; PHOTOTOXICITY; PRIORITY JOURNAL; RADIATION; SPECIES; STARVATION; SURVIVAL; TRAFFIC AND TRANSPORT; ULTRAVIOLET RADIATION; WESTERN BLOTTING;

ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTIOXIDANTS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE; CELL PROLIFERATION; HUMANS; LIGHT; MELANOMA; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; RETINAL PIGMENT EPITHELIUM; SIROLIMUS; SKIN NEOPLASMS; TRANSCRIPTION FACTOR RELA; TRITERPENES; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 84898875044     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0962-z     Document Type: Article

References (65)

1. Glickman RD (2002) Phototoxicity to the retina: mechanisms of damage. Int J Toxicol 21:473-490 (Pubitemid 36090837)
2. Niemz M (2007) Laser-tissue interactions: fundamentals and applications. Springer, Berlin, pp 47-58
3. Sen CK, Sies H, Baeuerle PA (2000) Antioxidant and redox regulation of genes. Academic Press, San Diego, pp 3-20
4. Dalton TP, Shertzer HG, Puga A (1999) Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol Toxicol 39:67-101 (Pubitemid 29222552)
5. Subrahmanyam YY, McGirr LG, O'Brien PJ (1987) Glutathione oxidation during peroxidase catalysed drug metabolism. Chem Biol Interact 61:45-59 (Pubitemid 17021754)
6. Gibbs LS, Del Vecchio PJ, Shaffer JB (1992) Mn and Cu/Zn SOD expression in cells from LPS-sensitive and LPS-resistant mice. Free Rad Biol Med 12:107-111
7. Deby C, Goutier R (1990) New perspectives on the biochemistry of superoxide anion and the efficiency of superoxide dismutases. Biochem Pharmacol 39:399-405 (Pubitemid 20041905)
8. Godley BF, Shamsi FA, Liang FQ, Jarrett SG, Davies S, Boulton M (2005) Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem 280(22):21061-21066 (Pubitemid 40805665)
9. Ravanat JL, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B 63(1-3):88-102 (Pubitemid 33040727)
10. Akca HA, Demiray Tokgun O, Yokota J (2011) Invasiveness and anchorage independent growth ability augmented by PTEN inactivation through the PI3 K/AKT/NF-κB pathway in lung cancer cells. Lung Cancer 73:302-309
11. Chen AC-H, Arany PR, Huang Y-Y, Tomkinson EM, Sharma SK, Kharkwal GB, Saleem T, Mooney D, Yull FE, Blackwell TS, Hamblin MR (2011) Low-level laser therapy activates NF-κB via generation of reactive oxygen species in mouse embryonic fibroblasts. PLoS ONE 6:e22453
12. Tibbetts RS, Brumbaugh KM, Williams JM, Sarkaria JN, Cliby WA, Shieh S-Y, Taya Y, Prives C, Abraham RT (1999) A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 13:152-157 (Pubitemid 29061945)
13. Chipuk JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, Green DR (2005) PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 9:1732-1735 (Pubitemid 41285944)
14. Mohan M, Taneja TK, Sahdev S, Mohareer K, Begum R, Athar M, Sah NK, Hasnain SE (2003) Antioxidants prevent UV-induced apoptosis by inhibiting mitochondrial cytochrome c release and caspase activation in Spodoptera frugiperda (Sf9) cells. Cell Biol Int 27:483-490 (Pubitemid 36687836)
15. Sharma PK, Dwarakanath BS, Varshney R (2012) Radiosensitization by 2-deoxy-d-glucose and 6-aminonicotinamide involves activation of redox sensitive ASK1-JNK/p38MAPK signaling in head and neck cancer cells. Free Radic Biol Med 53:1500-1513
16. Bode AM, Dong Z (2003) Mitogen-activated protein kinase activation in UV-induced signal transduction. Sci STKE 2003:115
17. Kim JH, Park JM, Kim E-K, Lee JO, Lee SK, Jung JH, You GY, Park SH, Suh P-G, Kim H (2010) Curcumin stimulates glucose uptake through AMPK-p38 MAPK pathways in L6 myotube cells. J Cell Physiol 223:771-778
18. Tabidi I, Saggerson D (2012) Inactivation of the AMP-activated protein kinase by glucose in cardiac myocytes: a role for the pentose phosphate pathway. Biosci Rep 32:229-239
19. Lomonosova E, Ryerse J, Chinnadurai G (2009) BAX/BAK - independent mitoptosis during cell death induced by proteasome inhibition? Mol Cancer Res 7:1268-1284
20. Le SB, Hailer MK, Buhrow S, Wang Q, Flatten K, Pediaditakis P, Bible KC, Lewis LD, Sausville EA, Pang YP, Ames MM, Lemasters JJ, Holmuhamedov EL, Kaufmann SH (2007) Inhibition of mitochondrial respiration as a source of adaphostin-induced reactive oxygen species and cytotoxicity. J Biol Chem 282:8860-8872 (Pubitemid 47093495)
21. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780-787 (Pubitemid 34809230)
22. Ly JD, Grubb DR, Lawen A (2003) The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 8:115-128 (Pubitemid 36553052)
23. Suen D-F, Norris KL, Youle RJ (2008) Mitochondrial dynamics and apoptosis. Genes Dev 22:1577-1590 (Pubitemid 351846838)
24. Martin-Aragon S, de las Heras B, Sanchez-Reus MI, Benedi J (2001) Pharmacological modification of endogenous antioxidant enzymes by ursolic acid on tetrachloride-induced liver damage in rats and primary cultures of rat hepatocytes. Exp Toxicol Pathol 53(2-3):199-206 (Pubitemid 32625764)
25. Liu J (1995) Pharmacology of oleanolic acid and ursolic acid. J Ethnopharmacol 49(2):57-68 (Pubitemid 26010740)
26. Ramachandran S, Prasad NR (2008) Effect of ursolic acid, a triterpenoid antioxidant, on ultraviolet-B radiation-induced cytotoxicity, lipid peroxidation and DNA damage in human lymphocytes. Chem Biol Interact 176(2-3):99-107
27. Liobikas J, Majiene D, Trumbeckaite S, Kursvietiene L, Masteikova R, Kopustinskiene DM, Savickas A, Bernatoniene J (2011) Uncoupling and antioxidant effects of ursolic acid in isolated rat heart mitochondria. J Nat Prod 74(7):1640-1644
28. Bayer M, Proksch P, Felsner I, Brenden H, Kohne Z, Walli R, Duong TN, Götz C, Krutmann J, Grether-Beck S (2011) Photoprotection against UVAR: effective triterpenoids require a lipid raft stabilizing chemical structure. Exp Dermatol 20(11):955-958
29. Chen K-C, Chang H-H, Ko W-S, Wu C-L, Chiu W-T, Hsieh C-L, Peng RY (2009) UV-induced damages eliminated by arbutin and ursolic acid in cell model of human dermal fibroblast WS-1 cells. Egypt Dermatol J 5(1):1-15
30. Soo Lee Y, Jin DQ, Beak SM, Lee ES, Kim JA (2003) Inhibition of ultraviolet-A-modulated signaling pathways by asiatic acid and ursolic acid in HaCaT human keratinocytes. Eur J Pharmacol 476(3):173-178 (Pubitemid 37272144)
31. Rotolo J, Stancevic B, Zhang J, Hua G, Fuller J, Yin X, Haimovitz-Friedman A, Kim K, Qian M, Cardó-Vila M, Fuks Z, Pasqualini R, Arap W, Kolesnick R (2012) Anti-ceramide antibody prevents the radiation gastrointestinal syndrome in mice. J Clin Invest 122(5):1786-1790
32. Wilkinson K, Boyd JD, Glicksman M, Moore KJ, El Khoury J (2011) A high content drug screen identifies ursolic acid as an inhibitor of amyloid beta protein interactions with its receptor CD36. J Biol Chem 286(40):34914-34922
33. Handberg A, Lopez-Bermejo A, Bassols J, Vendrell J, Ricart W, Fernandez-Real JM (2009) Circulating soluble CD36 is associated with glucose metabolism and interleukin-6 in glucose-intolerant men. Diab Vasc Dis Res 6(1):15-20
34. Wang L, Wang GL, Liu JH, Li D, Zhu DZ, Wu LN (2012) Effects of ursolic acid in ameliorating insulin resistance in liver of KKAy mice via peroxisome proliferator-activated receptors α and γ. Zhong Xi Yi Jie He Xue Bao 10(7):793-799
35. Jung SH, Ha YJ, Shim EK, Choi SY, Jin JL, Yun-Choi HS, Lee JR (2007) Insulin-mimetic and insulin-sensitizing activities of a pentacyclic triterpenoid insulin receptor activator. Biochem J 403:243-250 (Pubitemid 46596579)
36. Derdak Z, Lang CH, Villegas KA, Tong M, Mark NM, de la Monte SM, Wands JR (2011) Activation of p53 enhances apoptosis and insulin resistance in a rat model of alcoholic liver disease. J Hepatol 54:164-172
37. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ, Thompson CB (2005) AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 18:283-293 (Pubitemid 41350534)
38. Samovski D, Su X, Xu Y, Abumrad NA, Stahl PD (2012) Insulin and AMPK regulate FA translocase/CD36 plasma membrane recruitment in cardiomyocytes via Rab GAP AS160 and Rab8a Rab GTPase. J Lipid Res 53:709-717
39. Chen W, Jiang T, Wang H, Tao S, Lau A, Fang D, Zhang DD (2012) Does Nrf2 contribute to p53-mediated control of cell survival and death? Antioxid Redox Signal 17:1670-1675
40. Liu W, Tan X, Shu L, Sun H, Song J, Jin P, Yu S, Sun M, Jia X (2012) Ursolic acid inhibits cigarette smoke extract-induced human bronchial epithelial cell injury and prevents development of lung cancer. Molecules 17:9104-9115
41. Ditch S, Paull TT (2012) The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem Sci 37:15-22
42. Neary CL, Pastorino JG (2013) Akt inhibition promotes hexokinase 2 redistribution and glucose uptake in cancer cells. J Cell Physiol. doi: 10.1002/jcp.24361
43. Yu YX, Gu ZL, Yin JL, Chou WH, Kwok CY, Qin ZH, Liang ZQ (2010) Ursolic acid induces human hepatoma cell line SMMC-7721 apoptosis via p53-dependent pathway. Chin Med J (Engl) 123(14):1915-1923
44. Manu KA, Kuttan G (2008) Ursolic acid induces apoptosis by activating p53 and caspase-3 gene expressions and suppressing NF-κB mediated activation of bcl-2 in B16F-10 melanoma cells. Int Immunopharmacol 8(7):974-981
45. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, Gottlieb E, Vousden KH (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126(1):107-120 (Pubitemid 44040989)
46. Salminen A, Kaarniranta K (2010) Glycolysis links p53 function with NF-κB signaling: impact on cancer and aging process. J Cell Physiol 224(1):1-6
47. Kunkel SD, Elmore CJ, Bongers KS, Ebert SM, Fox DK, Dyle MC, Bullard SA, Adams CM (2012) Ursolic acid increases skeletal muscle and brown fat and decreases diet-induced obesity, glucose intolerance and fatty liver disease. PLoS ONE 7(6):e39332. doi: 10.1371/journal.pone.0039332
48. Jia Y, Bhuiyan MJ, Jun HJ, Lee JH, Hoang MH, Lee HJ, Kim N, Lee D, Hwang KY, Hwang BY, Choi DW, Lee SJ (2011) Ursolic acid is a PPAR-α agonist that regulates hepatic lipid metabolism. Bioorg Med Chem Lett 21(19):5876-5880. doi: 10.1016/j.bmcl
49. Carkeet C, Grann K, Randolph RK, Venzon DS, Izzy SM (2012) Phytochemicals: health promotion and therapeutic potential. CRC Press, Florida, pp 120-128
50. 2-induced apoptosis in human skin keratinocytes. J Biol Chem 283(43):28897-28908
51. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ, Thompson CB (2005) AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 18(3):283-293 (Pubitemid 41350534)
52. Zheng Q-Y, Jin F-S, Yao C, Zhang T, Zhang G-H, Ai X (2012) Ursolic acid-induced AMP-activated protein kinase (AMPK) activation contributes to growth inhibition and apoptosis in human bladder cancer T24 cells. Biochem Biophys Res Commun 419:741-747
53. Priebe A, Tan L, Wahl H, Kueck A, He G, Kwok R, Opipari A, Liu JR (2011) Glucose deprivation activates AMPK and induces cell death through modulation of Akt in ovarian cancer cells. Gynecol Oncol 122(2):389-395
54. Yeh CT, Wu CH, Yen GC (2010) Ursolic acid, a naturally occurring triterpenoid, suppresses migration and invasion of human breast cancer cells by modulating c-Jun N-terminal kinase, Akt and mammalian target of rapamycin signaling. Mol Nutr Food Res 54:1285-1295
55. Lu J, Wu DM, Zheng YL, Hu B, Cheng W, Zhang ZF, Shan Q (2011) Ursolic acid improves high fat diet-induced cognitive impairments by blocking endoplasmic reticulum stress and IκB kinase β/nuclear factor-κB-mediated inflammatory pathways in mice. Brain Behav Immun 25:1658-1667
56. Lee Y-H, Kumar N, Glickman RD (2012) Modulation of photochemical damage in normal and malignant cells by naturally occurring compounds. Photochem Photobiol 88:1385-1395
57. Tang C, Lu YH, Xie JH, Wang F, Zou JN, Yang JS, Xing YY, Xi T (2009) Downregulation of survivin and activation of caspase-3 through the PI3 K/Akt pathway in ursolic acid-induced HepG2 cell apoptosis. Anticancer Drugs 20:249-258
58. Lee C-H (2011) Glucose starvation induces apoptosis of Tsc-/-cells in a P53-dependent manner. ProQuest, UMI, Dissertation publishing, Michigan
59. Natarajan M, Nayak BK, Galindo C, Mathur SP, Roldan FN, Meltz ML (2006) Nuclear translocation and DNA-binding activity of NF-κB after exposure of human monocytes to pulsed ultra-wideband electromagnetic fields (1 kV/cm) fails to transactivate kappaB-dependent gene expression. Radiat Res 165:645-654 (Pubitemid 43831013)
60. Tessem M-B, Bathen TF, Čejková J, Midelfart A (2005) Effect of UVA and UVB irradiation on the metabolic profile of aqueous humor in rabbits analyzed by 1H NMR spectroscopy. Invest Ophthalmol Vis Sci 46:776-781 (Pubitemid 41321011)
61. Lattimore MR Jr (1989) Effect of ultraviolet radiation on the energy metabolism of the corneal epithelium of the rabbit. Photochem Photobiol 49:175-180
62. Halse R, Bonavaud SM, Armstrong JL, McCormack JG, Yeaman SJ (2001) Control of glycogen synthesis by glucose, glycogen, and insulin in cultured human muscle cells. Diabetes 50:720-726 (Pubitemid 32242626)
63. Tsirigotis DT (2011) Insulin-stimulated phosphate transport and ATP synthesis in skeletal muscle. ProQuest, UMI, Dissertation publishing, Michigan
64. Weng L-P, Smith WM, Brown JL, Eng C (2001) PTEN inhibits insulin-stimulated MEK/MAPK activation and cell growth by blocking IRS-1 phosphorylation and IRS-1/Grb-2/Sos complex formation in a breast cancer model. Hum Mol Genet 10:605-616 (Pubitemid 32229365)
65. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D, Christofk HR, Wagner G, Rabinowitz JD, Asara JM, Cantley LC (2010) Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 329:1492-1499