Time course changes of anti- and pro-apoptotic proteins in apigenin-induced genotoxicity

Chinese Medicine (United Kingdom)

Volumn 8, Issue 1, 2013, Pages

  Papachristou, Fotini ^a   Chatzaki, Ekaterini ^a   Petrou, Athanasios ^a   Kougioumtzi, Ioanna ^a   Katsikogiannis, Nikolaos ^a   Papalambros, Alexandros ^a   Tripsianis, Grigorios ^a   Simopoulos, Constantinos ^a   Tsaroucha, Alexandra K ^a  

^a DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

APIGENIN; APOPTOSIS REGULATORY PROTEIN; FAS ANTIGEN; FAS LIGAND; PROTEIN BAX; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME ABERRATION; CONTROLLED STUDY; CYTOSTASIS; CYTOTOXICITY; DNA DAMAGE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENOTOXICITY; HUMAN; HUMAN CELL; MITOSIS; PROTEIN EXPRESSION; SISTER CHROMATID EXCHANGE; UPREGULATION;

EID: 84877948667     PISSN: None     EISSN: 17498546     Source Type: Journal    
DOI: 10.1186/1749-8546-8-9     Document Type: Article

References (93)

1. Wang Z, Wang N, Chen J, Shen J. Emerging glycolysis targeting and drug discovery from Chinese medicine in cancer therapy. Evid Based Complement Alternat Med 2012, 2012:873175. 3403522, 22844340.
2. Carmady B, Smith CA. Use of Chinese medicine by cancer patients: a review of surveys. Chin Med 2011, 6:22. 10.1186/1749-8546-6-22, 3148205, 21651825.
3. Cragg GM, Newman DJ. Plants as a source of anti-cancer agents. J Ethnopharmacol 2005, 100:72-79. 10.1016/j.jep.2005.05.011, 16009521.
4. Kim DI, Lee TK, Lim IS, Kim H, Lee YC, Kim CH. Regulation of IGF-I production and proliferation of human leiomyomal smooth muscle cells by Scutellaria barbata D. Don in vitro: isolation of flavonoids of apigenin and luteolin as acting compounds. Toxicol Appl Pharmacol 2005, 205:213-224. 10.1016/j.taap.2004.10.007, 15922007.
5. Cao Y, Chu Q, Fang Y, Ye J. Analysis of flavonoids in Ginkgo biloba L. and its phytopharmaceuticals by capillary electrophoresis with electrochemical detection. Anal Bioanal Chem 2002, 374:294-299. 10.1007/s00216-002-1436-2, 12324852.
6. Zheng QS, Sun XL, Xu B, Li G, Song M. Mechanisms of apigenin-7-glucoside as a hepatoprotective agent. Biomed Environ Sci 2005, 18:65-70.
7. Tsai CH, Lin FM, Yang YC, Lee MT, Cha TL, Wu GJ, Hsieh SC, Hsiao PW. Herbal extract of Wedelia chinensis attenuates androgen receptor activity and orthotopic growth of prostate cancer in nude mice. Clin Cancer Res 2009, 15:5435-5444. 10.1158/1078-0432.CCR-09-0298, 19690196.
8. Chao WW, Lin BF. Isolation and identification of bioactive compounds in Andrographis paniculata (Chuanxinlian). Chin Med 2010, 5:17. 10.1186/1749-8546-5-17, 2881933, 20465823.
9. Lu XY, Sun DL, Chen ZJ, Chen T, Li LP, Xu ZH, Jiang HD, Zeng S. Relative contribution of small and large intestine to deglycosylation and absorption of flavonoids from Chrysanthemun morifolium extract. J Agric Food Chem 2010, 58:10661-10667. 10.1021/jf102992r, 20853834.
10. Chen Z, Kong S, Song F, Li L, Jiang H. Pharmacokinetic study of luteolin, apigenin, chrysoeriol and diosmetin after oral administration of Flos Chrysanthemi extract in rats. Fitoterapia 2012, 83:1616-1622. 10.1016/j.fitote.2012.09.011, 22999990.
11. Kuo ML, Lee KC, Lin JK. Genotoxicities of nitropyrenes and their modulation by apigenin, tannic acid, ellagic acid and indole-3-carbinol in the Salmonella and CHO systems. Mutat Res 1992, 270:87-95. 10.1016/0027-5107(92)90119-M, 1383740.
12. Myhrstad MC, Carlsen H, Nordstrom O, Blomhoff R, Moskaug JO. Flavonoids increase the intracellular glutathione level by transactivation of the gamma-glutamylcysteine synthetase catalytical subunit promoter. Free Radic Biol Med 2002, 32:386-393. 10.1016/S0891-5849(01)00812-7, 11864778.
13. Liang YC, Huang YT, Tsai SH, Lin-Shiau SY, Chen CF, Lin JK. Suppression of inducible cyclooxygenase and inducible nitric oxide synthase by apigenin and related flavonoids in mouse macrophages. Carcinogenesis 1999, 20:1945-1952. 10.1093/carcin/20.10.1945, 10506109.
14. Wei H, Tye L, Bresnick E, Birt DF. Inhibitory effect of apigenin, a plant flavonoid, on epidermal ornithine decarboxylase and skin tumor promotion in mice. Cancer Res 1990, 50:499-502.
15. Birt DF, Mitchell D, Gold B, Pour P, Pinch HC. Inhibition of ultraviolet light induced skin carcinogenesis in SKH-1 mice by apigenin, a plant flavonoid. Anticancer Res 1997, 17:85-91.
16. Van Dross R, Xue Y, Knudson A, Pelling JC. The chemopreventive bioflavonoid apigenin modulates signal transduction pathways in keratinocyte and colon carcinoma cell lines. J Nutr 2003, 133(Supp 1):3800-3804.
17. McVean M, Xiao H, Isobe K, Pelling JC. Increase in wild-type p53 stability and transactivational activity by the chemopreventive agent apigenin in keratinocytes. Carcinogenesis 2000, 21:633-639. 10.1093/carcin/21.4.633, 10753197.
18. Wang W, Heideman L, Chung CS, Pelling JC, Koehler KJ, Birt DF. Cell-cycle arrest at G2/M and growth inhibition by apigenin in human colon carcinoma cell lines. Mol Carcinog 2000, 28:102-110. 10.1002/1098-2744(200006)28:2<102::AID-MC6>3.0.CO;2-2, 10900467.
19. Zheng P-W, Chiang L-C, Lin C-C. Apigenin induced apoptosis through p53-dependent pathway in human cervical carcinoma cells. Life Sci 2005, 76:1367-1379. 10.1016/j.lfs.2004.08.023, 15670616.
20. Patel SD, Shukla S, Gupta S. Apigenin and cancer chemoprevention: Progress, potential and promise (Review). Int J Oncol 2007, 30:233-245.
21. Xu Y, Xin Y, Diao Y, Lu C, Fu J, Luo L, Yin Z. Synergistic effects of apigenin and paclitaxel on apoptosis of cancer cells. PLoS One 2011, 6:e29169. 10.1371/journal.pone.0029169, 3244456, 22216199.
22. Miyoshi N, Naniwa K, Yamada T, Osawa T, Nakamura Y. Dietary flavonoid apigenin is a potential inducer of intracellular oxidative stress: the role in the interruptive apoptotic signal. Arch Biochem Biophys 2007, 466:274-282. 10.1016/j.abb.2007.07.026, 17870050.
23. Crespo I, García-Mediavilla MV, Almar M, González P, Tuñón MJ, Sánchez-Campos S, González-Gallego J. Differential effects of dietary flavonoids on reactive oxygen and nitrogen species generation and changes in antioxidant enzyme expression induced by proinflammatory cytokines in Chang Liver cells. Food Chem Toxicol 2008, 46:1555-1569. 10.1016/j.fct.2007.12.014, 18234413.
24. Jeyabal PVS, Syed MB, Venkataraman M, Sambandham JK, Sakthisekaran D. Apigenin inhibits oxidative stress-induced macromolecular damage in N-nitrosodiethylamine (NDEA)-induced hepatocellular carcinogenesis in Wistar albino rats. Mol Carcinog 2005, 44:11-20. 10.1002/mc.20115, 15924350.
25. Chiang L-C, Ng LT, Lin I-C, Kuo P-L, Lin C-C. Anti-proliferative effect of apigenin and its apoptotic induction in human HepG2 cells. Cancer Lett 2006, 237:207-214. 10.1016/j.canlet.2005.06.002, 16023288.
26. Khan TH, Sultana S. Apigenin induces apoptosis in HepG2 cells: possible role of TNF-a and IFN-a. Toxicology 2006, 217:206-212. 10.1016/j.tox.2005.09.019, 16289292.
27. Choi SI, CS J, Cho SY, YS L. Mechanisms of apoptosis induced by apigenin in HepG2 human hepatoma cells: Involvement of reactive oxygen species generated by NADPH oxidase. Arch Pharm Res 2007, 30:1328-1335. 10.1007/BF02980274, 18038912.
28. Valdameri G, Trombetta-Lima M, Worfel PR, Pires AR, Martinez GR, Noleto GR, Cadena SM, Sogayar MC, Winnischofer SM, Rocha ME. Involvement of catalase in the apoptotic mechanism induced by apigenin in HepG2 human hepatoma cells. Chem Biol Interact 2011, 193:180-189. 10.1016/j.cbi.2011.06.009, 21756884.
29. Shukla S, Gupta S. Apigenin: A promising molecule for cancer prevention. Pharm Res 2010, 27:962-978. 10.1007/s11095-010-0089-7, 2874462, 20306120.
30. Wang IK, Lin-Shiau SY, Lin JK. Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaemia HL-60 cells. Eur J Cancer 1999, 35:1517-1525. 10.1016/S0959-8049(99)00168-9, 10673981.
31. Shukla S, Gupta S. Molecular mechanisms for apigenin-induced cell-cycle arrest and apoptosis of hormone refractory human prostate carcinoma DU145 cells. Mol Carcinog 2004, 39:114-126. 10.1002/mc.10168, 14750216.
32. Shukla S, Gupta S. Apigenin-induced prostate cancer cell death is initiated by reactive oxygen species and p53 activation. Free Radic Biol Med 2008, 44:1833-1845. 10.1016/j.freeradbiomed.2008.02.007, 2538676, 18342637.
33. Lu HF, Chie YS, Tan TW, Wu SH, Ma YS, Ip SW, Chung JG. Apigenin induces caspase-dependent apoptosis in human lung cancer A549 cells through Bax- and Bcl-2-triggered mitochondrial pathway. Int J Oncol 2010, 36:1477-1484.
34. Rithidech KN, Tungjai M, Whorton EB. Protective effect of apigenin on radiation-induced chromosomal damage in human lymphocytes. Mutat Res 2005, 585:96-104. 10.1016/j.mrgentox.2005.04.003, 15886050.
35. Khan TH, Jahangir T, Prasad L, Sarwat S. Inhibitory effect of apigenin on benzo(a) pyrene-mediated genotoxicity in Swiss albino mice. J Pharm Pharmacol 2006, 58:1655-1660. 10.1211/jpp.58.12.0013, 17331330.
36. Siddique YH, Ara G, Beg T, Afzal M. Anticlastogenic effect of apigenin in human lymphocytes treated with ethinylestradiol. Fitoterapia 2010, 81:590-594. 10.1016/j.fitote.2010.02.003, 20176089.
37. Snyder RD, Gillies PJ. Evaluation of the clastogenic, DNA intercalative, and topoisomerase II-interactive properties of bioflavonoids in Chinese hamster V79 cells. Environ Mol Mutagen 2002, 40:266-276. 10.1002/em.10121, 12489117.
38. Noel S, Kasinathan M, Rath SK. Evaluation of apigenin using in vitro cytochalasin blocked micronucleus assay. Toxicol in Vitro 2006, 20:1168-1172. 10.1016/j.tiv.2006.03.007, 16759833.
39. Nafisi S, Hashemi M, Rajabi M, Tajmir-Riahi HA. DNA adducts with antioxidant flavonoids: morin, apigenin, and naringin. DNA Cell Biol 2008, 27:433-442. 10.1089/dna.2008.0735, 18491957.
40. Kanakis CD, Nafisi S, Rajabi M, Shadaloi A, Tarantilis PA, Polissiou MG, Bariyanga J, Tajmir-Riahi HA. Structural analysis of DNA and RNA interactions with antioxidant flavonoids. Spectroscopy 2009, 23:29-43.
41. Ross WE, Bradley MO. DNA double-strand breaks in mammalian cells after exposure to intercalating agents. Biochim Biophys Acta 1981, 654:129-134. 10.1016/0005-2787(81)90145-3, 7272306.
42. Pommier Y, Schwartz RE, Zwelling LA, Kohn KW. Effects of DNA intercalating agents on topoisomerase II induced DNA strand cleavage in isolated mammalian cell nuclei. Biochemistry 1985, 24:6406-6410. 10.1021/bi00344a014, 3002439.
43. Albertini RJ, Anderson D, Douglas GK, Hagmar L, Hemminki K, Merlo F, Natarajan AT, Norppa H, Shuker DE, Tice R, Waters MD, Aitio A. IPCS guidelines for the monitoring of genotoxic effects of carcinogens in humans. Mutat Res 2000, 463:111-172. 10.1016/S1383-5742(00)00049-1, 10913908.
44. Pandey M, Kaur P, Shukla S, Abbas A, Fu P, Gupta S. Plant flavone apigenin inhibits HDAC and remodels chromatin to induce growth arrest and apoptosis in human prostate cancer cells: in vitro and in vivo study. Mol Carcinog 2012, 51:952-962. 10.1002/mc.20866, 22006862.
45. Thurn KT, Thomas S, Moore A, Munster PN. Rational therapeutic combinations with histone deacetylase inhibitors for the treatment of cancer. Future Oncol 2011, 7:263-283. 10.2217/fon.11.2, 3127396, 21345145.
46. Morris SM, Casciano DA, Casto BC. Detection of carcinogens based in in vitro mammalian cytogenetic tests. Handbook of carcinogen testing 1994, 100-115. New Jersey: Noyes Publications, Milman HA, Weisburger EK, 2.
47. Solomon E, Bobrow M. Sister chromatid exchanges-a sensitive assay of agents damaging human chromosomes. Mutat Res 1975, 30:273-278.
48. Nakanishi Y, Schneider EL. In vivo sister-chromatid exchange: a sensitive measure of DNA damage. Mutat Res 1979, 60:329-337. 10.1016/0027-5107(79)90023-X, 113672.
49. Das BC. Factors that influence formation of sister chromatid exchanges in human blood lymphocytes. Crit Rev Toxicol 1988, 19:43-86. 10.3109/10408448809040817, 3056658.
50. Marzano C, Bettio F, Baccichetti F, Trevisan A, Giovagnini L, Fregona D. Antitumor activity of a new platinum (II) complex with low nephrotoxicity and genotoxicity. Chem Biol Interact 2004, 148:37-48. 10.1016/j.cbi.2004.04.002, 15223355.
51. Lialiaris T, Lyratzopoulos E, Papachristou F, Simopoulou M, Mourelatos C, Nikolettos N. Supplementation of melatonin protects human lymphocytes in vitro from the genotoxic activity of melphalan. Mutagenesis 2008, 23:347-354. 10.1093/mutage/gen020, 18502769.
52. Lialiaris TS, Kotsiou E, Pouliliou S, Kareli D, Makrinou H, Kouskoukis A, Papachristou F, Koukourakis M. Cytoprotective activity of amifostine on cultured human lymphocytes exposed to irinotecan. Food Chem Toxicol 2009, 47:2445-2449. 10.1016/j.fct.2009.06.042, 19577607.
53. Lialiaris TS, Papachristou F, Mourelatos C, Simopoulou M. Antineoplastic and cytogenetic effects of chlorpromazine on human lymphocytes in vitro and on Ehrlich ascites tumor cells in vivo. Anti Cancer Drugs 2009, 20:746-751. 10.1097/CAD.0b013e32832f567b, 19584706.
54. Turkez H, Tatar A, Hacimuftuoglu A, Ozdemir E. Boric acid as a protector against paclitaxel genotoxicity. Acta Biochim Pol 2010, 57:95-97.
55. Tofilon P, Basic I, Milas L. Prediction of in vivo tumour response to chemotherapeutic agents by the in vitro SCE assay. Cancer Res 1985, 45:2025-2030.
56. Denn DF, Kendall LA, Marton LJ, Tofilon P. Prediction of human tumour cell chemosensitivity using the SCE assay. Cancer Res 1986, 46:1599-1602.
57. Swierenga SHH, Heddle JA, Sigal EA, Gilman JPW, Brillinger RL, Douglas GR, Nestmann ER. Recommended protocols on a survey of current practice in genotoxicity testing laboratories, IV. Chromosome aberrations and sister chromatid exchanges in Chinese Hamster Ovary V79. Chinese Hamster lung and human lymphocyte cultures. Mutat Res 1991, 246:301-322. 10.1016/0027-5107(91)90050-X, 1996126.
58. Hagmar L, Bonassi S, Stromberg U, Brøgger A, Knudsen LE, Norppa H, Reuterwall C. European study group on cytogenetic biomarkers and health: chromosomal aberration in human lymphocytes predict human cancer: a report from the European study group on cytogenetic biomarkers and health (ESCH). Cancer Res 1998, 58:4117-4121.
59. El-Deiry WS. Regulation of p53 downstream genes. Semin Cancer Biol 1988, 8:345-357.
60. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW. Participation of p53 protein in the cellular response to DNA damage. Cancer Res 1991, 51:6304-6311.
61. Clarke AR, Gledhill S, Hooper ML, Bird CC, Wyllie AH. p53 dependence of early apoptotic and proliferative responses within the mouse intestinal epithelium following gamma-irradiation. Oncogene 1994, 9:1767-1773.
62. Perry P, Wolff S. New Giemsa method for the differential staining of sister chromatids. Nature 1974, 251(5471):156-158. 10.1038/251156a0, 4138930.
63. Lamberti L, Bigatti Ponzetto P, Ardito G. Cell kinetics and sister chromatid exchange frequency in human lymphocytes. Mutat Res 1983, 120:193-199. 10.1016/0165-7992(83)90163-X, 6843582.
64. Galloway SM, Wolff S. The relation between chemically induced sister-chromatid exchanges and chromatid breakage. Mutat Res 1979, 61:297-307. 10.1016/0027-5107(79)90135-0, 90339.
65. Ikushima T. Role of sister chromatid exchanges in chromatid aberration formation. Nature 1977, 268:235-236. 10.1038/268235a0, 887153.
66. Gebhart E. Sister chromatid exchange (SCE) and chromosome aberrations in mutagenicity testing. Hum Genet 1981, 58:235-254. 10.1007/BF00294917, 6459983.
67. Latt SA. Sister chromatid exchanges, indices of human chromosome damage and repair: detection by fluorescence and induction by mitomycin C. Proc Natl Acad Sci USA 1974, 71:3162-3166. 10.1073/pnas.71.8.3162, 388642, 4137928.
68. Siddique YH, Beg T, Afzal M. Antigenotoxic effect of apigenin against anti-cancerous drugs. Toxicol in Vitro 2008, 22:625-631. 10.1016/j.tiv.2007.12.002, 18206345.
69. Begum N, Prasad NR, Kanimozhi G, Hasan AQ. Apigenin ameliorates gamma radiation-induced cytogenetic alterations in cultured human blood lymphocytes. Mutat Res 2012, 747:71-76. 10.1016/j.mrgentox.2012.04.001, 22516036.
70. Simon D, Aden DP, Knowle BB. Chromosomes of human hepatoma cell lines. Int J Cancer 1982, 30:27-33. 10.1002/ijc.2910300106, 6288577.
71. Zimonjic DB, Keck CL, Thorgeirsson SS, Popescu NC. Novel recurrent genetic imbalances in human hepatocellular carcinoma cell lines identified by comparative genomic hybridization. Hepatology 1999, 29:1208-1214. 10.1002/hep.510290410, 10094966.
72. Wong N, Lai P, Pang E, Leung TW-T, Lau JW-Y, Johnson PJ. A comprehensive karyotypic study on human hepatocellular carcinoma by spectral karyotyping. Hepatology 2000, 32:1060-1068. 10.1053/jhep.2000.19349, 11050057.
73. Dronkert ML, Kanaar R. Repair of DNA interstrand cross-links. Mutat Res 2001, 486:217-247. 10.1016/S0921-8777(01)00092-1, 11516927.
74. Helleday T. Pathways for mitotic homologous recombination in mammalian cells. Mutat Res 2003, 532:103-115. 10.1016/j.mrfmmm.2003.08.013, 14643432.
75. Johnson DR, Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J 2000, 19:3398-3407. 10.1093/emboj/19.13.3398, 313931, 10880452.
76. Iijima K, Muranaka C, Kobayashi J, Sakamoto S, Komatsu K, Matsuura S, Kubota N, Tauchia H. NBS1 regulates a novel apoptotic pathway through Bax activation. DNA Repair 2008, 7:1705-1716. 10.1016/j.dnarep.2008.06.013, 18644472.
77. Berkovich E, Monnat RJ, Kastan MB. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat Cell Biol 2007, 9:683-690. 10.1038/ncb1599, 17486112.
78. Bergamaschi D, Samuels Y, Jin B, Duraisingham S, Crook T, Lu X. ASPP1 and ASPP2: common activators of p53 family members. Mol Cell Biol 2004, 24:1341-1350. 10.1128/MCB.24.3.1341-1350.2004, 321425, 14729977.
79. Rozan LM, El-Deiry WS. p53 downstream target genes and tumor suppression: a classical view in evolution. Cell Death Differ 2007, 14:3-9. 10.1038/sj.cdd.4402058, 17068503.
80. Strasser A, Harris AW, Jacks T, Cory S. DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 1994, 79:329-339. 10.1016/0092-8674(94)90201-1, 7954799.
81. Chao DT, Linette GP, Boise LH, White LS, Thompson CB, Korsmeyer SJ. Bcl-xL and Bcl-2 repress a common pathway of cell death. J Exp Med 1995, 182:821-828. 10.1084/jem.182.3.821, 2192158, 7650488.
82. Meikrantz W, Bergom MA, Memisoglu A, Samson L. O6-Alkylguanine DNA lesions trigger apoptosis. Carcinogenesis 1998, 19:369-372. 10.1093/carcin/19.2.369, 9498291.
83. Zhang J, Reedy MC, Hannun YA, Obeid LM. Inhibition of caspases inhibits the release of apoptotic bodies: Bcl-2 inhibits the initiation of formation of apoptotic bodies in chemotherapeutic agent-induced apoptosis. J Cell Biol 1999, 145:99-108. 10.1083/jcb.145.1.99, 2148221, 10189371.
84. Ochs K, Kaina B. Apoptosis induced by DNA Damage O -Methylguanine is Bcl-2 and Caspase-9/3 regulated and Fas/Caspase-8 independent. Cancer Res 2000, 60:5815-5824.
85. Friesen C, Herr I, Krammer PH, Debatin KM. Involvement of the CD95 (APO-1/Fas) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat Med 1996, 2:574-577. 10.1038/nm0596-574, 8616718.
86. Mueller M, Strand S, Hug H, Heinemann E-M, Walczak H, Hofmann WJ, Stremmel W, Krammer PH, Galle PR. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J Clin Inves 1997, 99:403-413.
87. Leithäuser F, Dhein J, Mechtersheimer G, Koretz K, Brüderlein S, Henne C, Schmidt A, Debatin K-M, Krammer PH, Moller P. Constitutive and induced expression of APO-1, a new member of the nerve growth factor/tumor necrosis factor receptor superfamily, in normal and neoplastic cells. Lab Invest 1993, 69:415-429.
88. Cheng J, Zhou T, Liu C, Shapiro JP, Brauer MJ, Kiefer MC, Barr PJ, Mountz JD. Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science 1994, 263:1759-1762. 10.1126/science.7510905, 7510905.
89. Cascino I, Fiucci G, Papoff G, Ruberti G. Three functional soluble forms of the human apoptosis-inducing Fas molecule are produced by alternative splicing. J Immunol 1995, 154:2706-2713.
90. Cascino I, Papoff G, Eramo A, Ruberti G. Soluble Fas/Apo-1 splicing variants and apoptosis. Front Biosci 1996, 1:d12-d18.
91. Filippov V, Schmidt EL, Filippova M, Duerksen-Hughes PJ. Splicing and splice factor SRp55 participate in the response to DNA damage by changing isoform ratios of target genes. Gene 2008, 420:34-41. 10.1016/j.gene.2008.05.008, 2562212, 18571879.
92. Izquierdo JM, Majós N, Bonnal S, Martínez C, Castelo R, Guigó R, Bilbao R, Valcárcel J. Regulation of Fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition. Molec Cell 2005, 19:475-484. 10.1016/j.molcel.2005.06.015, 16109372.
93. Busa R, Geremia R, Sette C. Genotoxic stress causes the accumulation of the splicing regulator Sam68 in nuclear foci of transcriptionally active chromatin. Nucleic Acids Res 2010, 38:3005-3018. 10.1093/nar/gkq004, 2875014, 20110258.