Redox balance influences differentiation status of neuroblastoma in the presence of all-trans retinoic acid

Redox Biology

Volumn 7, Issue , 2016, Pages 88-96

  Silvis, Anne M ^a   McCormick, Michael L ^b   Spitz, Douglas R ^b   Kiningham, Kinsley K ^c  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^c BELMONT UNIVERSITY   (United States)

Author keywords

Differentiation; MnSOD; Neuroblastoma; Reactive oxygen species; Retinoic acid

Indexed keywords

CATALASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; NEUROFILAMENT M PROTEIN; OXYGEN; RETINOIC ACID; SMALL INTERFERING RNA; 2',7'-DICHLORODIHYDROFLUORESCEIN; ANTINEOPLASTIC AGENT; FLUORESCEIN DERIVATIVE; NEUROFILAMENT PROTEIN; TRANSCRIPTION FACTOR SOX;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NEUROBLASTOMA; NEUROBLASTOMA CELL LINE; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL DIFFERENTIATION; CELL LINE, TUMOR; FLUORESCEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROGEN PEROXIDE; NEUROBLASTOMA; NEUROFILAMENT PROTEINS; OXIDATION-REDUCTION; SOX TRANSCRIPTION FACTORS; TRETINOIN;

EID: 84949293262     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2015.11.012     Document Type: Article

References (47)

1. Allen R.G., Tresini M. Oxidative stress and gene regulation. Free Radic. Biol. Med. 2000, 28(3):463-499.
2. Altucci L., Gronemeyer H. The promise of retinoids to fight against cancer. Nat. Rev. Cancer 2001, 1(3):181-193.
3. Anderson M.E. Handbook of Methods for Oxygen Radical Research 1985, CRC Press, Boca Raton, Florida.
4. Carystinos G.D., Alaoui-Jamali M.A., Phipps J., Yen L., Batist G. Upregulation of gap junctional intercellular communication and connexin 43 expression by cyclic-AMP and all-trans-retinoic acid is associated with glutathione depletion and chemosensitivity in neuroblastoma cells. Cancer Chemother. Pharmacol. 2001, 47(2):126-132.
5. Cassano S., Agnese S., D'Amato V., Papale M., Garbi C., Castagnola P., Ruocco M.R., Castellano I., De Vendittis E., Santillo M., Amente S., Porcellini A., Avvedimento E.V. Reactive oxygen species, Ki-Ras, and mitochondrial superoxide dismutase cooperate in nerve growth factor-induced differentiation of PC12 cells. J. Biol. Chem. 2010, 285(31):24141-24153.
6. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59(3):527-605.
7. Chomienne C., Ballerini P., Balitrand N., Daniel M.T., Fenaux P., Castaigne S., Degos L. All-trans retinoic acid in acute promyelocytic leukemias. II. In vitro studies: structure-function relationship. Blood 1990, 76(9):1710-1717.
8. Culotta V.C., Yang M., O'Halloran T.V. Activation of superoxide dismutases: putting the metal to the pedal. Biochim. Biophys. Acta 2006, 1763(7):747-758.
9. Donato L.J., Suh J.H., Noy N. Suppression of mammary carcinoma cell growth by retinoic acid: the cell cycle control gene Btg2 is a direct target for retinoic acid receptor signaling. Cancer Res. 2007, 67(2):609-615.
10. Erlejman A.G., Oteiza P.I. The oxidant defense system in human neuroblastoma IMR-32 cells predifferentiation and postdifferentiation to neuronal phenotypes. Neurochem. Res. 2002, 27(11):1499-1506.
11. Freemantle S.J., Spinella M.J., Dmitrovsky E. Retinoids in cancer therapy and chemoprevention: promise meets resistance. Oncogene 2003, 22(47):7305-7315.
12. Gelain D.P., Moreira J.C. Evidence of increased reactive species formation by retinol, but not retinoic acid, in PC12 cells. Toxicol. In Vitro 2008, 22(3):553-558.
13. Gelinas S., Chapados C., Beauregard M., Gosselin I., Martinoli M.G. Effect of oxidative stress on stability and structure of neurofilament proteins. Biochem. Cell Biol. 2000, 78(6):667-674.
14. Gopalakrishna R., Gundimeda U., Schiffman J.E., McNeill T.H. A direct redox regulation of protein kinase C isoenzymes mediates oxidant-induced neuritogenesis in PC12 cells. J. Biol. Chem. 2008, 283(21):14430-14444.
15. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106(1):207-212.
16. Kamata H., Tanaka C., Yagisawa H., Matsuda S., Gotoh Y., Nishida E., Hirata H. Suppression of nerve growth factor-induced neuronal differentiation of PC12 cells. N-acetylcysteine uncouples the signal transduction from ras to the mitogen-activated protein kinase cascade. J. Biol. Chem. 1996, 271(51):33018-33025.
17. Kiningham K.K., Cardozo Z.A., Cook C., Cole M.P., Stewart J.C., Tassone M., Coleman M.C., Spitz D.R. All-trans-retinoic acid induces manganese superoxide dismutase in human neuroblastoma through NF-kappaB. Free Radic. Biol. Med. 2008, 44(8):1610-1616.
18. Konopka R., Kubala L., Lojek A., Pachernik J. Alternation of retinoic acid induced neural differentiation of P19 embryonal carcinoma cells by reduction of reactive oxygen species intracellular production. Neuro Endocrinol. Lett. 2008, 29(5):770-774.
19. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416(1):15-18.
20. Lasorella A., Iavarone A., Israel M.A. Differentiation of neuroblastoma enhances Bcl-2 expression and induces alterations of apoptosis and drug resistance. Cancer Res. 1995, 55(20):4711-4716.
21. Lawrence R.A., Burk R.F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 1976, 71(4):952-958.
22. LeBel C.P., Ischiropoulos H., Bondy S.C. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 1992, 5(2):227-231.
23. Lebovitz R.M., Zhang H., Vogel H., Cartwright J., Dionne L., Lu N., Huang S., Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. USA 1996, 93(18):9782-9787.
24. Li Y., Huang T.T., Carlson E.J., Melov S., Ursell P.C., Olson J.L., Noble L.J., Yoshimura M.P., Berger C., Chan P.H., Wallace D.C., Epstein C.J. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 1995, 11(4):376-381.
25. McCord J.M., Keele B.B., Fridovich I. An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc. Natl. Acad. Sci. USA 1971, 68(5):1024-1027.
26. Melino G. Discussion: differentiation. Advances in Neuroblastoma Research 1994, 215. Wiley-Liss, New York. A.E. Evans, G.M. Biedler, G. Brodeur, G.J. D'Angio, A. Nakagawara (Eds.).
27. Nitti M., Furfaro A.L., Cevasco C., Traverso N., Marinari U.M., Pronzato M.A., Domenicotti C. PKC delta and NADPH oxidase in retinoic acid-induced neuroblastoma cell differentiation. Cell. Signal. 2010, 22(5):828-835.
28. Oberley T.D., Schultz J.L., Li N., Oberley L.W. Antioxidant enzyme levels as a function of growth state in cell culture. Free Radic. Biol. Med. 1995, 19(1):53-65.
29. Oh J.E., Karlmark Raja K., Shin J.H., Hengstschlager M., Pollak A., Lubec G. The neuronal differentiation process involves a series of antioxidant proteins. Amino Acids 2005, 29(3):273-282.
30. Pizzi M., Boroni F., Bianchetti A., Moraitis C., Sarnico I., Benarese M., Goffi F., Valerio A., Spano P. Expression of functional NR1/NR2B-type NMDA receptors in neuronally differentiated SK-N-SH human cell line. Eur. J. Neurosci. 2002, 16(12):2342-2350.
31. Privalle C.T., Fridovich I. Induction of superoxide dismutase in Escherichia coli by heat shock. Proc. Natl. Acad. Sci. USA 1987, 84(9):2723-2726.
32. Reddy N.M., Kleeberger S.R., Cho H.Y., Yamamoto M., Kensler T.W., Biswal S., Reddy S.P. Deficiency in Nrf2-GSH signaling impairs type II cell growth and enhances sensitivity to oxidants. Am. J. Respir. Cell Mol. Biol. 2007, 37(1):3-8.
33. Reddy N.M., Kleeberger S.R., Yamamoto M., Kensler T.W., Scollick C., Biswal S., Reddy S.P. Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiol. Genom. 2007, 32(1):74-81.
34. Reynolds C.P., Lemons R.S. Retinoid therapy of childhood cancer. Hematol. Oncol. Clin. N. Am. 2001, 15(5):867-910.
35. Schneider L., Giordano S., Zelickson B.R., M S.J., G A.B., Ouyang X., Fineberg N., Darley-Usmar V.M., Zhang J. Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radic. Biol. Med. 2011, 51(11):2007-2017.
36. Shinjyo N., Kita K. Relationship between reactive oxygen species and heme metabolism during the differentiation of Neuro2a cells. Biochem. Biophys. Res. Commun. 2007, 358(1):130-135.
37. Sidell N., Altman A., Haussler M.R., Seeger R.C. Effects of retinoic acid (RA) on the growth and phenotypic expression of several human neuroblastoma cell lines. Exp. Cell Res. 1983, 148(1):21-30.
38. Sohal R.S., Weindruch R. Oxidative stress, caloric restriction, and aging. Science 1996, 273(5271):59-63.
39. Spitz D.R., Oberley L.W. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal. Biochem. 1989, 179(1):8-18.
40. St Clair D.K., Oberley T.D., Muse K.E., St Clair W.H. Expression of manganese superoxide dismutase promotes cellular differentiation. Free Radic. Biol. Med. 1994, 16(2):275-282.
41. Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R., Kamata T. Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J. Biol. Chem. 2000, 275(18):13175-13178.
42. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552(Pt 2):335-344.
43. Valko M., Rhodes C.J., Moncol J., Izakovic M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006, 160(1):1-40.
44. Veal G.J., Errington J., Redfern C.P., Pearson A.D., Boddy A.V. Influence of isomerisation on the growth inhibitory effects and cellular activity of 13-cis and all-trans retinoic acid in neuroblastoma cells. Biochem. Pharmacol. 2002, 63(2):207-215.
45. Voccoli V., Colombaioni L. Mitochondrial remodeling in differentiating neuroblasts. Brain Res. 2009, 1252:15-29.
46. Yen A., Albright K.L. Evidence for cell cycle phase-specific initiation of a program of HL-60 cell myeloid differentiation mediated by inducer uptake. Cancer Res. 1984, 44(6):2511-2515.
47. Zhang Y.T., Zheng Q.S., Pan J., Zheng R.L. Oxidative damage of biomolecules in mouse liver induced by morphine and protected by antioxidants. Basic Clin. Pharmacol. Toxicol. 2004, 95(2):53-58.