Certain carotenoids enhance the intracellular glutathione level in a murine cultured macrophage cell line by inducing glutamate-cysteine-ligase

Molecular Nutrition and Food Research

Volumn 58, Issue 6, 2014, Pages 1291-1300

  Akaboshi, Teppei ^a   Yamanishi, Rintaro ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Glutamate cysteine ligase; Glutathione; Macrophage; Carotene; Cryptoxanthin

Indexed keywords

ANTHRA(1,9-CD)PYRAZOL-6(2H)-ONE; ANTHRACENE DERIVATIVE; BETA CAROTENE; BUTHIONINE SULFOXIMINE; CRYPTOXANTHIN; CYCLOHEXIMIDE; DACTINOMYCIN; ENZYME INHIBITOR; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; XANTHOPHYLL;

ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; MACROPHAGE; METABOLISM; MOUSE; PHOSPHORYLATION; UPREGULATION;

ANIMALS; ANTHRACENES; BETA CAROTENE; BUTHIONINE SULFOXIMINE; CELL LINE; CRYPTOXANTHINS; CYCLOHEXIMIDE; DACTINOMYCIN; ENZYME INHIBITORS; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUTEIN; MACROPHAGES; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 3; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RNA, MESSENGER; UP-REGULATION;

EID: 84901945830     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300753     Document Type: Article

References (45)

1. Bray, T. M., Taylor, C. G., Tissue glutathione, nutrition, and oxidative stress. Can. J. Physiol. Pharmacol. 1993, 71, 746-751.
2. Toroser, D., Yarian, C. S., Orr, W. C., Sohal, R. S., Mechanisms of γ-glutamylcysteine ligase regulation. Biochim. Biophys. Acta 2006, 1760, 233-244.
3. Stipanuk, M. H., Dominy, J. E., Jr., Lee, J. I., Coloso, R. M., Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J. Nutr. 2006, 136, 1652S-1659S.
4. Seelig, G. F., Simondsen, R. P., Meister, A., Reversible dissociation of γ-glutamylcysteine synthetase into two subunits. J. Biol. Chem. 1984, 259, 9345-9347.
5. Wild, A. C., Mulcahy, R. T., Regulation of γ-glutamylcysteine synthetase subunit gene expression: insights into transcriptional control of antioxidant defenses. Free Radic. Res. 2000, 32, 281-301.
6. Huang, C. S., Chang, L. S., Anderson, M. E., Meister, A., Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 1993, 268, 19675-19680.
7. Soltaninassab, S. R., Sekhar, K. R., Meredith, M. J., Freeman, M. L., Multi-faceted regulation of γ-glutamylcysteine synthetase. J. Cell Physiol. 2000, 182, 163-170.
8. Jeannin, P., Delneste, Y., Lecoanet-Henchoz, S., Gauchat, J. F. et al., Thiols decrease human interleukin (IL) 4 production and IL-4-induced immunoglobulin synthesis. J. Exp. Med. 1995, 182, 1785-1792.
9. Yanagihara, Y., Basaki, Y., Kajiwara, K., Ikizawa, K., A thiol antioxidant regulates IgE isotype switching by inhibiting activation of nuclear factor-κB. J. Allergy Clin. Immunol. 1997, 100, S33-S38.
10. Gosset, P., Wallaert, B., Tonnel, A. B., Fourneau, C., Thiol regulation of the production of TNF-α, IL-6 and IL-8 by human alveolar macrophages. Eur. Respir. J. 1999, 14, 98-105.
11. Kim, H. J., Barajas, B., Wang, M., Nel, A. E., Nrf2 activation by sulforaphane restores the age-related decrease of T(H)1 immunity: role of dendritic cells. J. Allergy Clin. Immunol. 2008, 121, 1255-1261.
12. Fraternale, A., Paoletti, M. F., Dominici, S., Caputo, A. et al., The increase in intra-macrophage thiols induced by new pro-GSH molecules directs the Th1 skewing in ovalbumin immunized mice. Vaccine 2010, 28, 7676-7682.
13. Alam, K., Ghousunnissa, S., Nair, S., Valluri, V. L. et al., Glutathione-redox balance regulates c-rel-driven IL-12 production in macrophages: possible implications in antituberculosis immunotherapy. J. Immunol. 2010, 184, 2918-2929.
14. Katsuura, S., Imamura, T., Bando, N., Yamanishi, R., β-Carotene and β-cryptoxanthin but not lutein evoke redox and immune changes in RAW264 murine macrophages. Mol. Nutr. Food Res. 2009, 53, 1396-1405.
15. Imamura, T., Bando, N., Yamanishi, R., β-Carotene modulates the immunological function of RAW264, a murine macrophage cell line, by enhancing the level of intracellular glutathione. Biosci. Biotechnol. Biochem. 2006, 70, 2112-2120.
16. Bhat, N. R., Zhang, P., Hydrogen peroxide activation of multiple mitogen-activated protein kinases in an oligodendrocyte cell line: role of extracellular signal-regulated kinase in hydrogen peroxide-induced cell death. J. Neurochem. 1999, 72, 112-119.
17. Bogoyevitch, M. A., Gillespie-Brown, J., Ketterman, A. J., Fuller, S. J. et al., Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart. p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion. Circ. Res. 1996, 79, 162-173.
18. Wang, X., Martindale, J. L., Liu, Y., Holbrook, N. J., The cellular response to oxidative stress: influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem. J. 1998, 333, 291-300.
19. Bertram, J. S., Pung, A., Churley, M., Kappock, T. J. T. et al., Diverse carotenoids protect against chemically induced neoplastic transformation. Carcinogenesis 1991, 12, 671-678.
20. Zhang, L. X., Cooney, R. V., Bertram, J. S., Carotenoids enhance gap junctional communication and inhibit lipid peroxidation in C3H/10T1/2 cells: relationship to their cancer chemopreventive action. Carcinogenesis 1991, 12, 2109-2114.
21. Prakash, P., Russell, R. M., Krinsky, N. I., In vitro inhibition of proliferation of estrogen-dependent and estrogen-independent human breast cancer cells treated with carotenoids or retinoids. J. Nutr. 2001, 131, 1574-1580.
22. Anderson, M. E., Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol. 1985, 113, 548-555.
23. Nierenberg, D. W., Stukel, T. A., Baron, J. A., Dain, B. J. et al., Determinants of increase in plasma concentration of β-carotene after chronic oral supplementation. The Skin Cancer Prevention Study Group. Am. J. Clin. Nutr. 1991, 53, 1443-1449.
24. Prince, M. R., Frisoli, J. K., β-Carotene accumulation in serum and skin. Am. J. Clin. Nutr. 1993, 57, 175-181.
25. Albanes, D., Virtamo, J., Taylor, P. R., Rautalahti, M. et al., Effects of supplemental β-carotene, cigarette smoking, and alcohol consumption on serum carotenoids in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Am. J. Clin. Nutr. 1997, 66, 366-372.
26. Pan, Z., Perez-Polo, R., Regulation of γ-glutamylcysteine synthetase activity by nerve growth factor. Int. J. Dev. Neurosci. 1996, 14, 559-566.
27. Cai, J., Huang, Z. Z., Lu, S. C., Differential regulation of γ-glutamylcysteine synthetase heavy and light subunit gene expression. Biochem. J. 1997, 326, 167-172.
28. Galloway, D. C., Blake, D. G., Shepherd, A. G., McLellan, L. I., Regulation of human γ-glutamylcysteine synthetase: co-ordinate induction of the catalytic and regulatory subunits in HepG2 cells. Biochem. J. 1997, 328, 99-104.
29. Sekhar, K. R., Long, M., Long, J., Xu, Z. Q. et al., Alteration of transcriptional and post-transcriptional expression of γ-glutamylcysteine synthetase by diethyl maleate. Radiat. Res. 1997, 147, 592-597.
30. Yao, K. S., Godwin, A. K., Johnson, S. W., Ozols, R. F. et al., Evidence for altered regulation of γ-glutamylcysteine synthetase gene expression among cisplatin-sensitive and cisplatin-resistant human ovarian cancer cell lines. Cancer Res. 1995, 55, 4367-4374.
31. Koizumi, T., Bando, N., Terao, J., Yamanishi, R., Feeding with both β-carotene and supplemental α-tocopherol enhances type 1 helper T cell activity among splenocytes isolated from DO11.10 mice. Biosci. Biotechnol. Biochem. 2006, 70, 3042-3045.
32. Hughes, D. A., Hughes, D. A., Darlington, L. G., Bendich, A. (Eds.), Diet and Human Immune Function, Humana Press, Totowa, NJ 2004, pp. 165-183.
33. Goto, T., Takahashi, N., Kato, S., Kim, Y. I. et al., Bixin activates PPARα and improves obesity-induced abnormalities of carbohydrate and lipid metabolism in mice. J. Agric. Food Chem. 2012, 60, 11952-11958.
34. Albanes, D., Heinonen, O. P., Taylor, P. R., Virtamo, J. et al., α-Tocopherol and β-carotene supplements and lung cancer incidence in the alpha-tocopherol, beta-carotene cancer prevention study: effects of base-line characteristics and study compliance. J. Natl. Cancer Inst. 1996, 88, 1560-1570.
35. Omenn, G. S., Goodman, G. E., Thornquist, M. D., Balmes, J. et al., Risk factors for lung cancer and for intervention effects in CARET, the β-Carotene and Retinol Efficacy Trial. J. Natl. Cancer Inst. 1996, 88, 1550-1559.
36. Foote, C. S., Denny, R. W., Chemistry of singlet oxygen. VIII. Quenching by β-carotene. J. Am. Chem. Soc. 1968, 90, 6233-6235.
37. Palozza, P., Can β-carotene regulate cell growth by a redox mechanism? An answer from cultured cells. Biochim. Biophys. Acta. 2005, 1740, 215-221.
38. Kikugawa, K., Hiramoto, K., Hirama, A., β-Carotene generates thiobarbituric acid-reactive substances by interaction with nitrogen dioxide in air. Free Radic. Res. 1999, 31, 517-523.
39. Linnewiel, K., Ernst, H., Caris-Veyrat, C., Ben-Dor, A. et al., Structure activity relationship of carotenoid derivatives in activation of the electrophile/antioxidant response element transcription system. Free Radic. Biol. Med. 2009, 47, 659-667.
40. Dickinson, D. A., Iles, K. E., Watanabe, N., Iwamoto, T. et al., 4-hydroxynonenal induces glutamate cysteine ligase through JNK in HBE1 cells. Free Radic. Biol. Med. 2002, 33, 974.
41. Hehner, S. P., Breitkreutz, R., Shubinsky, G., Unsoeld, H. et al., Enhancement of T cell receptor signaling by a mild oxidative shift in the intracellular thiol pool. J. Immunol. 2000, 165, 4319-4328.
42. Liu, C. L., Chiu, Y. T., Hu, M. L., Fucoxanthin enhances HO-1 and NQO1 expression in murine hepatic BNL CL.2 cells through activation of the Nrf2/ARE system partially by its pro-oxidant activity. J. Agric. Food Chem. 2011, 59, 11344-11351.
43. Sharoni, Y., Linnewiel-Hermoni, K., Khanin, M., Salman, H. et al., Carotenoids and apocarotenoids in cellular signaling related to cancer: a review. Mol. Nutr. Food Res. 2012, 56, 259-269.
44. Palozza, P., Catalano, A., Simone, R., Cittadini, A., Lycopene as a guardian of redox signalling. Acta. Biochim. Pol. 2012, 59, 21-25.
45. Li, Z., Dong, X., Liu, H., Chen, X. et al., Astaxanthin protects ARPE-19 cells from oxidative stress via upregulation of Nrf2-regulated phase II enzymes through activation of PI3K/Akt. Mol. Vis. 2013, 19, 1656-1666.