NF-κB-associated mechanisms underlying the response of embryonic cells to Doxorubicin

Toxicology in Vitro

Volumn 27, Issue 2, 2013, Pages 804-811

  Savion, S ^a   Oserov, G ^a   Orenstein, H ^a   Torchinsky, A ^a   Fein, A ^a   Toder, V ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Apoptosis; Cell cycle; Doxorubicin; MEFs; NF B; P65

Indexed keywords

DOXORUBICIN; I KAPPA B ALPHA; PROTEIN BCL 2; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CELL DENSITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG RESPONSE; EMBRYO; EMBRYO CELL; FIBROBLAST; G2 PHASE CELL CYCLE CHECKPOINT; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TERATOGENICITY; WILD TYPE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DOXORUBICIN; EMBRYO, MAMMALIAN; FIBROBLASTS; MICE; MICE, KNOCKOUT; TRANSCRIPTION FACTOR RELA;

EID: 84872440860     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2012.12.017     Document Type: Article

References (58)

1. Abu-Hijleh G., Qi B.Q., Williams A.K., Beasley S.W. Development of the bones and synovial joints in the rat model of the VATER association. J. Orthop. Sci. 2000, 5:390-396.
2. Acquaah-Mensah G.K., Kehrer J.P., Leslie S.W. In utero ethanol suppresses cerebellar activator protein-1 and nuclear factor-kappa B transcriptional activation in a rat fetal alcohol syndrome model. J. Pharmacol. Exp. Ther. 2002, 301:277-283.
3. Adli M., Baldwin A.S. IKK-i/IKKε controls constitutive, cancer cell-associated NF-κB activity via regulation of Ser-536 p65/RelA phosphorylation. J. Biol. Chem. 2006, 281:26976-26984.
4. Arlt A., Vorndamm J., Breitenbroich M., Folsch U.R., Kalthoff H., Schmidt W.E., Schafer H. Inhibition of NF-κB sensitizes human pancreatic carcinoma cells to apoptosis induced by etoposide (VP16) or doxorubicin. Oncogene 2001, 20:859-868.
5. Beg A.A., Sha W.C., Bronson R.T., Ghosh S., Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappaB. Nature 1995, 376:167-170.
6. Bernotti S., Seidman E., Sinnett D., Brunet S., Dionne S., Delvin E., Levy E. Inflammatory reaction without endogenous antioxidant response in Caco-2 cells exposed to iron/ascorbate-mediated lipid peroxidation. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:898-906.
7. Bogdanovic G., Kojic V., Dordevic A., Canadanovic-Brunet J., Vojinovic- Miloradov M., Baltic V.V. Modulating activity of fullerol C60 (OH)22 on doxorubicin-induced cytotoxicity. Toxicol. In Vitro. 2004, 18:629-637.
8. Bours V., Bentries-Alj M., Hellin A.C., Viatour P., Robe P., Delhalle S., Benoit V., Merville M.P. Nuclear factor-κB, cancer and apoptosis. Biochem. Pharmacol. 2000, 60:1085-1090.
9. Brengauz-Breitmann M., Friedman E., Savion S., Torchinsky A., Fein A., Toder V. Involvement of NF-kappaB in the response of embryonic cells to methotrexate. Reprod. Toxicol. 2006, 14:469-478.
10. Chua C.C., Liu X., Gao J., Hamdy R.C., Chua B.H. Multiple actions of pifithrin on doxorubicin-induced apoptosis in rat myoblastic H9C2 cells. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H2606-H2613.
11. Cory S., Adams J.M. The bcl-2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2002, 2:647-656.
12. Culmsee C., Siewe J., Junker V., Retiounskaia M., Schwarz S., Camandola S., El-Metainy S., Behnke H., Mattson M.P., Krieglstein J. Reciprocal inhibition of p53 and nuclear factor-κB transcriptional activities determines cell survival or death in neurons. J. Neurosci. 2003, 23:8586-8595.
13. Curry H.A., Clemens R.A., Shah S., Bradbury C.M., Botero A., Goswami P. Heat shock inhibits radiation-induced activation of NF-kappaB via inhibition of I-kappaB kinase. J. Biol. Chem. 1999, 274:23061-23067.
14. Dawrant M.J., Giles S., Bannigan J., Puri P. Adriamycin produces a reproducible teratogenic model of vertebral, anal, cardiovascular, tracheal, esophageal, renal and limb anomalies in the mouse. J. Pediatr. Surg. 2007, 42:1652-1658.
15. El-Deiry W.S. The role of p53 in chemosensitivity and radiosensitivity. Oncogene 2003, 22:7486-7495.
16. Fernandez E.L., Gustafson A.L., Andersson M., Hellman B., Dencker L. Cadmium-induced changes in apoptotic gene expression levels and DNA damage in mouse embryos are blocked by zinc. Toxicol. Sci. 2003, 76:162-170.
17. Fridman J.S., Lowe S.W. Control of apoptosis by p53. Oncogene 2003, 22:9030-9040.
18. Gillick J., Mooney E., Giles S., Bannigan J., Puri P. Notochord anomalies in the adriamycin rat model: a morphologic and molecular basis for the vacterl association. J. Pediatr. Sur. 2003, 38:469-473.
19. Gu L., Findley H.W., Zhou M. MDM2 induces NF-κB/p65 expression transcriptionally through Sp1-binding sites: a novel p53-independent role of MDM2 in doxorubicin resistance in acute lymphoblastic leukemia. Blood 2002, 99:3367-3375.
20. Gundogan F., Elwood G., Mark P., Feijoo A., Longato L., Tong M., de la Monte S.M. Ethanol-induced oxidative stress and mitochondrial dysfunction in rat placenta: relevance to pregnancy loss. Alcohol.: Clin. Exp. Res. 2010, 34:415-423.
21. Hansen J.M., Gong S.G., Philbert M., Harris C. Misregulation of gene expression in the redox-sensitive NF-kappab-dependent limb outgrowth pathway by thalidomide. Dev. Dyn. 2002, 225:186-194.
22. Ioannides A.S., Chaudhry B., Henderson D.J., Spitz L., Copp A.J. Dorsoventral patterning in oesophageal atresia with tracheo-oesophageal fistula: evidence from a new mouse model. J. Pediatr. Surg. 2002, 37:185-191.
23. Jacobson M.D., Weil M., Raff M.C. Programmed cell death in animal development. Cell 1997, 88:347-354.
24. Kalter H. Teratology in the 20th century: environmental causes of congenital malformations in humans and how they were established. Neurotoxicol. Teratol. 2003, 25:131-282.
25. Keifer J.A., Guttridge D.C., Ashburner B.P., Baldwin A.S. Inhibition of NF-kappa B activity by thalidomide through suppression of IkappaB kinase activity. J. Biol. Chem. 2001, 276:22382-22387.
26. Kennedy J.C., Memet S., Wells P.G. Antisense evidence for nuclear factor-kappaB-dependent embryopathies initiated by phenytoin-enhanced oxidative stress. Mol. Pharmacol. 2004, 66:404-412.
27. Knudsen T.V. Cell death. Drug Toxicity in Embryonic Development I 1997, 211-244. Springer-Verlag, Berlin, Heidelberg. R.J. Kavlock, G.P. Daston (Eds.).
28. Kucharczak J., Simmons M.J., Fan Y., Gélinas C. To be, or not to be: NF-kappaB is the answer: role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 2003, 22:8961-8982.
29. Lai P.B.S., Chi T.Y., Chen G.G. Different levels of p53 induced either apoptosis or cell cycle arrest in a doxycycline-regulated hepatocellular carcinoma cell line in vitro. Apoptosis 2007, 12:387-393.
30. Lavon I., Pikarsky E., Gutkovich E., Goldberg I., Bar J., Oren M., Ben-Neriah Y. Nuclear factor-kappa B protects the liver against genotoxic stress and functions independently of p53. Cancer Res. 2003, 63:25-30.
31. Li J., Liu H., Ramachandran S., Waypa G.B., Yin J.J., Li C.Q., Han M., Huang H.H., Sillard W.W., Vanden, Hoek T.L., Shao Z.H. Grape seed proanthocyanidins ameliorate doxorubicin-induced cardiotoxicity. Am. J. Chin. Med. 2010, 38:569-584.
32. Liu J., Mao W., Ding B., Liang C.S. ERKs/p53 signal transduction pathway is involved in doxorubicin-induced apoptosis in H9c2 cells and cardiomyocytes. J. Physiol. Heart Circ. Physiol. 2008, 295:H1956-H1965.
33. Ma S., Tang J., Feng J., Xu Y., Yu X., Deng Q., Lu Y. Induction of p21 by p65 in p53 null cells treated with doxorubicin. Biochim. Biophys. Acta 2008, 1783:935-940.
34. Mammon K., Savion S., Keshet R., Aroch I., Orenstein H., Fein A., Torchinsky A., Toder V. Expression of apoptosis-associated molecules in the fetoplacental unit of cyclophosphamide-treated mice. Reprod., Toxicol. 2006, 22:774-782.
35. Mi J., Zhang X., Rabbani Z.N., Liu Y., Reddy S.K., Su Z., Salahuddin F.K., Viles K., Giangrande P.H., Dewhirst M.W., Sullenger B.A., Kontos C.D., Clary B.M. RNA aptamer-targeted inhibition of NF-κB suppresses non-small cell lung cancer resistance to doxorubicin. Mol. Ther. 2008, 16:66-73.
36. Menegola E., Broccia M.L., Renzo F.D. Teratogenic effects of doxorubicin in rats at midgestation and at term. Teratogen. Carcinogen. Mutagen. 2001, 21:283-293.
37. Molestina R.E., Payne T.M., Coppens I., Sinai A.P. Activation of NF-kappaB by toxoplasma gondii correlates with increased expression of anti apoptotic genes and localization of phosphorylated IkappaB to the parasitophorous vacuole membrane. J. Cell Sci. 2003, 116:4359-4371.
38. Miyata S., Wang L.Y., Wang N.L., Yao X.S., Kitanaka S. Selective inhibition of the growth of cancer cells by diterpenes selected with embryonic cells of Xenopus. Cell Biol. Int. 2004, 28:179-184.
39. Mori M., Matsubara K., Abe E., Matsubara Y., Katayama T., Fujioka T., Kusanagi Y., Ito M. Prenatal diagnosis of persistent cloaca associated with VATER (Vertebral defects, anal atresia, tracheo-esophageal fistula and renal dysplasia). Tohoku J. Exp. Med. 2007, 213:291-295.
40. Orford J., Manglick P., Cass D.T., Tam P.P.L. Mechanisms for the development of esophageal atresia. J. Pediatr. Surg. 2001, 36:985-994.
41. Panaretakis T., Pokrovskaja K., Shoshan M.C., Grandér D. Activation of Bak, Bax, and BH3-only proteins in the apoptotic response to doxorubicin. J. Biol. Chem. 2002, 15:44317-44326.
42. Pekar O., Molotski N., Savion S., Fein A., Toder V., Torchinsky A. P53 regulates cyclophosphamide teratogenesis by controlling caspases 3, 8, 9 activation and NF-B DNA binding. Reproduction 2007, 134:379-388.
43. Poyurovsky M.V., Prives C. Unleashing the power of p53: lessons from mice and men. Genes Dev. 2006, 20:125-131.
44. Raffoul J.J., Wang Y., Kucuk O., Forman J.D., Sarkar F.H., Hillman G.G. Genistein inhibits radiation-induced activation of NF-κB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer 2006, 6:107-116.
45. Roussel R.R., Barchowsky A. Arsenic inhibits NF-kappaB-mediated gene transcription by blocking IkappaB kinase activity and IkappaBalpha phosphorylation and degradation. Arch. Biochem. Biophys. 2000, 377:204-212.
46. Rozalski M., Mirowski M., Balcerczak1 E., Krajewska U., Mynarski W., Wierzbicki R. Induction of caspase 3 activity, bcl-2, bax and p65 gene expression modulation in human acute promyelocytic leukemia HL-60 cells by doxorubicin with amifostine. Pharmacol. Report. 2005, 57:360-366.
47. Sadler T.W., Hunter E.S. Principles of abnormal development: past, present and future. Developmental Toxicology 1994, 53-63. Raven Press, New York. C.A. Kimmel, J. Beulke-Sam (Eds.).
48. Safa M., Kazemi A., Zand H., Azarkeivan A., Zaker F., Hayat P. Inhibitory role of cAMP on doxorubicin-induced apoptosis in pre-B ALL cells through dephosphorylation of p53 serine residues. Apoptosis 2010, 15:196-203.
49. Savion S., Shtelman E., Orenstein H., Torchinsky A., Fein A., Toder V. Bax-associated mechanisms underlying the response of embryonic cells to methotrexate. Toxicol. In Vitro. 2009, 23:1062-1068.
50. Savion S., Sofer M., Brengauz-Breitmann M., Fein A., Torchinsky A., Toder V. NF-kappaB regulates the response of embryonic cells to heat shock. Int. J. Hyperther. 2007, 23:277-286.
51. Shah D., Sharma S., Faridi M.M.A., Mishra K. VACTERL association with prune-belly syndrome. Ind. Pediatr. 2004, 41:845-847.
52. Shimizu A., Nishida J., Ueoka Y., Kato K., Hachiya T., Kuriaki Y., Wake N. Cyclin G contributes to G2/M arrest of cells in response to DNA damage. Biochem. Biophys. Res. Commun. 1998, 242:529-533.
53. Sokal R.R., Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research 1995, Freeman and Company, New York, San Francisco.
54. Tergaonkar V., Pando M., Vafa O., Wahl G., Inder Verma I. P53 stabilization is decreased upon NF-κB activation: a role for NF-κB in acquisition of resistance to chemotherapy. Cancer Cell. 2002, 1:493-503.
55. Torchinsky A., Lishanski L., Wolstein O., Shepshelovich J., Orenstein H., Savion S., Zaslavsky Z., Carp H., Brill A., Dikstein R., Toder V., Fein A. NF-kappaB DNA-binding activity in embryos responding to a teratogen, cyclophosphamide. BMC Dev. Biol. 2002, 2:2-12.
56. Tyagi A.K., Singh R.P., Agarwal C., Chan D.C.F., Agarwal R. Silibinin strongly synergizes human prostate carcinoma DU145 cells to doxorubicin-induced growth inhibition, G2-M arrest and apoptosis. Clin. Cancer Res. 2002, 8:3512-3519.
57. Wang S., Kotamraju S., Konorev E., Kalivendi S., Joseph J., Kalyanraman B. Activation of nuclear factor-κB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. Biochem. J. 2002, 367:729-740.
58. Wuerzberger-Davis S.M., Chang P.Y., Berchtold C., Miyamoto S. Enhanced G2-M arrest by nuclear factor-KB-dependent p21waf1/cip1 induction. Mol. Cancer Res. 2005, 3:345-353.