Treatment of doxorubicin-resistant MCF7/Dx cells with nitric oxide causes histone glutathionylation and reversal of drug resistance

Biochemical Journal

Volumn 440, Issue 2, 2011, Pages 175-183

  De Luca, Anastasia ^a   Moroni, Noemi ^b   Serafino, Annalucia ^b   Primavera, Alessandra ^a   Pastore, Anna ^c   Pedersen, Jens Z ^a   Petruzzelli, Raffaele ^d   Farrace, Maria Grazia ^a   Pierimarchi, Pasquale ^b   Moroni, Gabriella ^a   Federici, Giorgio ^a,b   Sinibaldi Vallebona, Paola ^a   Lo Bello, Mario ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^c BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^d UNIVERSITY OF CHIETI   (Italy)

Author keywords

Drug resistance; Glutathione; Glutathione transferase P1 1 (GSTP1 1); Histones,; Nitric oxide (NO); Tumour cell

Indexed keywords

CYTOTOXIC FACTOR; DOXORUBICIN; GLUTATHIONE TRANSFERASE P1; HISTONE; NITRIC OXIDE; S NITROSOGLUTATHIONE;

ARTICLE; CANCER CELL CULTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BREAST NEOPLASMS; COORDINATION COMPLEXES; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GLUTATHIONE; GLUTATHIONE S-TRANSFERASE PI; HISTONES; HUMANS; NITRIC OXIDE; S-NITROSOGLUTATHIONE;

EID: 81155154369     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111333     Document Type: Article

References (37)

1. Riganti, C., Miraglia, E., Viarisio, D., Costamagna, C., Pescarmona, G., Ghigo, D. and Bosia, A. (2005) Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux. Cancer Res. 65, 516-525
2. Watts, R. N., Hawkins, C., Ponka, P. and Richardson, D. R. (2006) Nitrogen monoxide (NO)-mediated iron release from cells is linked to NO-induced glutathione efflux via multidrug resistance-associated protein 1. Proc. Natl. Acad. Sci. U.S.A. 103, 7670-7675
3. Townsend, D. M. and Tew, K. D. (2003) The role of glutathione S-transferase in anti-cancer drug resistance. Oncogene 22, 7369-7375
4. Bratasz, A., Weir, N. M., Parinandi, N. L., Zweier, J. L., Sridhar, R., Ignarro, L. J. and Kuppusamy, P. (2006) Reversal to cisplatin sensitivity in recurrent human ovarian cancer cells by NCX-4016, a nitro derivative of aspirin. Proc. Natl. Acad. Sci. U.S.A. 103, 3914-3919 (Pubitemid 43376655)
5. Moncada, S. (1994) Nitric oxide. J. Hypertens. 12, 35-39
6. Ignarro, L. J., Buga, G. M., Wei, L. H., Bauer, P. M., Wu, G. and Del Soldato, P. (2001) Role of the arginine-nitric oxide pathway in the regulation of vascular smooth muscle cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 98, 4202-4208 (Pubitemid 32249922)
7. Stamler, J. S., Simon, D. I., Jaraki, O., Osborne, J. A., Francis, S., Mullins, M., Singel, D. and Loscalzo, J. (1992) S-nitrosylation of tissue-type plasminogen activator confers vasodilatory and antiplatelet properties on the enzyme. Proc. Natl. Acad. Sci. U.S.A. 89, 8087-8091
8. Ghezzi, P. and Di Simplicio, P. (2007) Glutathionylation pathways in drug response. Curr. Opin. Pharmacol. 7, 398-403 (Pubitemid 47289262)
9. Lo Bello, M., Nuccetelli, M., Caccuri, A. M., Stella, L., Parker, M. W., Rossjohn, J., McKinstry, W. J., Mozzi, A. F., Federici, G., Polizio, F. et al. (2001) Human glutathione transferase P1-1 and nitric oxide carriers; a new role for an old enzyme. J. Biol. Chem. 276, 42138-42145
10. Cesareo, E., Parker, L. J., Pedersen, J. Z., Nuccetelli, M., Mazzetti, A. P., Pastore, A., Federici, G., Caccuri, A. M., Ricci, G., Adams, J. J. et al. (2005) Nitrosylation of human glutathione transferase P1-1 with dinitrosyl diglutathionyl iron complex in vitro and in vivo. J. Biol. Chem. 280, 42172-42180 (Pubitemid 43023187)
11. De Maria, F., Pedersen, J. Z., Caccuri, A. M., Antonini, G., Turella, P., Stella, L., Lo Bello, M., Federici, G. and Ricci, G. (2003) The specific interaction of dinitrosyl-diglutathionyl-iron complex, a natural NO carrier, with the glutathione transferase superfamily: suggestion for an evolutionary pressure in the direction of the storage of nitric oxide. J. Biol. Chem. 278, 42283-42293 (Pubitemid 37310496)
12. Richardson, D. R. and Lok, H. C. (2008) The nitric oxide-iron interplay in mammalian cells: transport and storage of dinitrosyl iron complexes. Biochim. Biophys. Acta 1780, 638-651
13. Hayes, D.H., Flanagan, J. U. and Jowsey, I. R. (2008) Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88 (Pubitemid 40261798)
14. Cairns, P., Esteller, M., Herman, J. G., Schoenberg, M., Jeronimo, C., Sanchez-Cespedes, M., Chow, N. H., Grasso, M., Wu, L., Westra, W. B. et al. (2001) Molecular detection of prostate cancer in urine by GSTP1 hypermethylation. Clin. Cancer Res. 7, 2727-2730 (Pubitemid 32911377)
15. Pastore, A., Tozzi, G., Gaeta, L. M., Bertini, E., Serafini, V., Di Cesare, S., Bonetto, V., Casoni, F., Carrozzo, R., Federici, G. et al. (2003) Actin glutathionylation increases in fibroblasts of patients with Friedreich's ataxia: a potential role in the pathogenesis of the disease. J. Biol. Chem. 278, 42588-42594
16. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
17. Pedersen, J. Z. and Cox, R. P. (1988) Use of flat glass capillaries as ESR aqueous sample cells. J. Magn. Reson. 77, 369-371
18. Habig, W. H. and Jakoby, W. B. (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol. 77, 398-405
19. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354 (Pubitemid 9256559)
20. Piredda, L., Farrace, M. G., Lo Bello, M., Malorni, W., Melino, G., Petruzzelli, R. and Piacentini, M. (1999) Identification of tissue transglutaminase binding proteins in neural cells committed to apoptosis. FASEB J. 13, 355-364 (Pubitemid 29072413)
21. Wang, C., Zhang, J. X., Shen, X. L., Wan, C. K., Tse, A. K. and Fong, W. F. (2004) Reversal of P-glycoprotein-mediated multidrug resistance by Alisol B 23-acetate. Biochem. Pharmacol. 68, 843-855 (Pubitemid 39044513)
22. Yang, C. H., Huang, C. J., Yang, C. S., Chu, Y. C., Cheng, A. L., Whang-Peng, J. and Yang, P. C. (2005) Gefitinib reverses chemotherapy resistance in gefitinib-insensitive multidrug resistant cancer cells expressing ATP-binding cassette family protein. Cancer Res. 65, 6943-6949 (Pubitemid 41060734)
23. Matsudaira, P. (1987) Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262, 10035-10038
24. Pedersen, J. Z., De Maria, F., Turella, P., Federici, G., Mattei, M., Fabrini, R., Dawood, K. F., Massimi, M., Caccuri, A. M. and Ricci, G. (2007) Glutathione transferases sequester toxic dinitrosyl-iron complexes in cells: a protection mechanism against excess nitric oxide. J. Biol. Chem. 282, 6364-6371 (Pubitemid 47100847)
25. Lambert, S. J., Nicholson, J. M., Chantalat, L., Reid, A. J., Donovan, M. J. and Baldwin, J. P. (1999) Purification of histone core octamers and 215Å X-ray analysis of crystals in KCl/phosphate. Acta Crystallogr. D55, 1048-1051 (Pubitemid 29235603)
26. Shukla, A., Chaurasia, P. and Bhaumik, S. R. (2009) Histone methylation and ubiquitination with their cross-talk and roles in gene expression and stability. Cell. Mol. Life Sci. 8, 1419-1433
27. Li, F., Adam, L., Vadlamudi, R. K., Zhou, H., Sen, S., Chernoff, J., Mandal, M. and Kumar, R. (2002) p21-activated kinase 1 interacts with and phosphorylates histone H3 in breast cancer cells. EMBO Rep. 3, 767-773 (Pubitemid 34966016)
28. Soriano, F. X., Papadia, S., Bell, K. F. and Hardingham, G. E. (2009) Role of histone acetylation in the activity-dependent regulation of sulfiredoxin and sestrin 2. Epigenetics 3, 152-158
29. Baldini, N., Scotlandi, K., Serra, M., Shikita, T., Zini, N., Ognibene, A., Santi, S., Ferracini, R. and Maraldi, N. M. (1995) Nuclear immunolocalization of P-glycoprotein in multidrug-resistant cell lines showing similar mechanisms of doxorubicin distribution. Eur. J. Cell. Biol. 68, 226-239
30. Gaudiano, G., Koch, T. H., Lo Bello, M., Nuccetelli, M., Ravagnan, G., Serafino, A. and Sinibaldi-Vallebona, P. (2000) Lack of glutathione conjugation to adriamycin in human breast cancer MCF-7/DOX cells. Inhibition of glutathione S-transferase P1-1 by glutathione conjugates from anthracyclines. Biochem. Pharmacol. 60, 1915-1923
31. Gehrmann, M. L., Fenselau, C. and Hathout, Y. (2004) Highly altered protein expression profile in the adriamycin resistant MCF-7 cell line. J. Proteome Res. 3, 403-409 (Pubitemid 39207343)
32. Lin, X. and Nelson, W. G. (2003) Methyl-CpG-binding domain protein-2 mediates transcriptional repression associated with hypermethylated GSTP1 CpG islands in MCF-7 cancer cells. Cancer Res. 63, 498-504 (Pubitemid 36152513)
33. Tew, K. D. (2007) Redox in redux: emergent roles for glutathione S-transferase P (GSTP) in regulation of cell signaling and S-glutathionylation. Biochem. Pharmacol. 73, 1257-1269
34. Townsend, D. M., Manevich, Y., He, L., Hutchens, S., Pazoles, C. J. and Tew, K. D. (2009) Novel role for glutathione S-transferase pi. Regulator of protein S-glutathionylation following oxidative and nitrosative stress. J. Biol. Chem. 284, 436-445
35. Manevich, Y., Feinstein, S. I. and Fisher, A. B. (2004) Activation of the antioxidant enzyme 1-Cys peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc. Natl. Acad. Sci. U.S.A. 101, 3780-3785 (Pubitemid 38381055)
36. Stella, L., Pallottini, V., Moreno, S., Leoni, S., De Maria, F., Turella, P., Federici, G., Fabrini, R., Dawood, K. F., Bello, M. L. et al. (2007) Electrostatic association of glutathione transferase to the nuclear membrane. Evidence of an enzyme defense barrier at the nuclear envelope. J. Biol. Chem. 282, 6372-6379 (Pubitemid 47100848)
37. Goto, S., Ihara, Y., Urata, Y., Izumi, S., Abe, K., Koji, T. and Kondo, T. (2001) Doxorubicin-induced DNA intercalation and scavenging by nuclear glutathione S-transferase pi. FASEB J. 15, 2702-2714 (Pubitemid 33131096)