Tumor-suppressive maspin functions as a reactive oxygen species scavenger: Importance of cysteine residues

Journal of Biological Chemistry

Volumn 288, Issue 16, 2013, Pages 11611-11620

  Mahajan, Nitin ^a   Shi, Heidi Y ^a   Lukas, Thomas J ^a   Zhang, Ming ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE RESIDUES; REACTIVE OXYGEN SPECIES; SCAVENGE REACTIVE OXYGEN SPECIES; TUMOR CELLS;

CELL PROLIFERATION; OXYGEN; TUMORS;

AMINO ACIDS;

CYSTEINE; MASPIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; REACTIVE OXYGEN METABOLITE; SULFENIC ACID; SULFENIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST TUMOR; CANCER INHIBITION; CELL GROWTH; CELL IMMORTALIZATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; TUMOR CELL LINE;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CYSTEINE; FEMALE; FREE RADICAL SCAVENGERS; MAP KINASE SIGNALING SYSTEM; MICE; MUTATION, MISSENSE; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SERPINS; TUMOR SUPPRESSOR PROTEINS;

EID: 84876569009     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.410852     Document Type: Article

References (46)

1. Weinberg, F., and Chandel, N. S. (2009) Reactive oxygen species-dependent signaling regulates cancer. Cell. Mol. Life Sci. 66, 3663-3673.
2. Khandrika, L., Kumar, B., Koul, S., Maroni, P., and Koul, H. K. (2009) Oxidative stress in prostate cancer. Cancer Lett. 282, 125-136.
3. Zou, Z., Anisowicz, A., Hendrix, M. J., Thor, A., Neveu, M., Sheng, S., Rafidi, K., Seftor, E., and Sager, R. (1994) Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science 263, 526-529.
4. Zhang, M., Volpert, O., Shi, Y. H., and Bouck, N. (2000) Maspin is an angiogenesis inhibitor. Nat. Med. 6, 196-199.
5. Endsley, M. P., Hu, Y., Deng, Y., He, X., Warejcka, D. J., Twining, S. S., Gonias, S. L., and Zhang, M. (2011) Maspin, the molecular bridge between the plasminogen activator system andα1 integrin that facilitates cell adhesion. J. Biol. Chem. 286, 24599-24607.
6. Qin, L., and Zhang, M. (2010) Maspin regulates endothelial cell adhesion and migration through an integrin signaling pathway. J. Biol. Chem. 285, 32360-32369.
7. Bodenstine, T. M., Seftor, R. E., Khalkhali-Ellis, Z., Seftor, E. A., Pemberton, P. A., and Hendrix, M. J. (2012) Maspin: molecular mechanisms and therapeutic implications. Cancer Metastasis Rev. 31, 529-551.
8. Jiang, N., Meng, Y., Zhang, S., Mensah-Osman, E., and Sheng, S. (2002) Maspin sensitizes breast carcinoma cells to induced apoptosis. Oncogene 21, 4089-4098.
9. Yin, S., Li, X., Meng, Y., Finley, R. L., Jr., Sakr, W., Yang, H., Reddy, N., and Sheng, S. (2005) Tumor-suppressive maspin regulates cell response to oxidative stress by direct interaction with glutathione S-transferase. J. Biol. Chem. 280, 34985-34996.
10. Bailey, C. M., Khalkhali-Ellis, Z., Kondo, S., Margaryan, N. V., Seftor, R. E., Wheaton, W. W., Amir, S., Pins, M. R., Schutte, B. C., and Hendrix, M. J. (2005) Mammary serine protease inhibitor (Maspin) binds directly to interferon regulatory factor 6. Identification of a novel serpin partnership. J. Biol. Chem. 280, 34210-34217.
11. Nawata, S., Shi, H. Y., Sugino, N., and Zhang, M. (2011) Evidence of posttranslational modification of the tumor suppressor maspin under oxidative stress. Int. J. Mol. Med. 27, 249-254.
12. Poole, L. B., Karplus, P. A., and Claiborne, A. (2004) Protein sulfenic acids in redox signaling. Annu. Rev. Pharmacol. Toxicol. 44, 325-347.
13. Poole, L. B., and Nelson, K. J. (2008) Discovering mechanisms of signalingmediated cysteine oxidation. Curr. Opin. Chem. Biol. 12, 18-24.
14. Nelson, K. J., Klomsiri, C., Codreanu, S. G., Soito, L., Liebler, D. C., Rogers, L. C., Daniel, L. W., and Poole, L. B. (2010) Use of dimedone-based chemical probes for sulfenic acid detection methods to visualize and identify labeled proteins. Methods Enzymol. 473, 95-115.
15. Klomsiri, C., Nelson, K. J., Bechtold, E., Soito, L., Johnson, L. C., Lowther, W. T., Ryu, S. E., King, S. B., Furdui, C. M., and Poole, L. B. (2010) Use of dimedone-based chemical probes for sulfenic acid detection evaluation of conditions affecting probe incorporation into redox-sensitive proteins. Methods Enzymol. 473, 77-94.
16. Law, R. H., Irving, J. A., Buckle, A. M., Ruzyla, K., Buzza, M., Bashtannyk-Puhalovich, T. A., Beddoe, T. C., Nguyen, K., Worrall, D. M., Bottomley, S. P., Bird, P. I., Rossjohn, J., and Whisstock, J. C. (2005) The high resolution crystal structure of the human tumor suppressor maspin reveals a novel conformational switch in the G-helix. J. Biol. Chem. 280, 22356-22364.
17. Al-Ayyoubi, M., Gettins, P. G., and Volz, K. (2004) Crystal structure of human maspin, a serpin with antitumor properties. Reactive center loop of maspin is exposed but constrained. J. Biol. Chem. 279, 55540-55544.
18. Zhang, W., Shi, H. Y., and Zhang, M. (2005) Maspin overexpression modulates tumor cell apoptosis through the regulation of Bcl-2 family proteins. BMC Cancer 5, 50.
19. Shi, H. Y., Stafford, L. J., Liu, Z., Liu, M., and Zhang, M. (2007) Maspin controls mammary tumor cell migration through inhibiting Rac1 and Cdc42, but not the RhoA GTPase. Cell Motil. Cytoskeleton 64, 338-346.
20. Gao, F., Shi, H. Y., Daughty, C., Cella, N., and Zhang, M. (2004) Maspin plays an essential role in early embryonic development. Development 131, 1479-1489.
21. Danielson, K. G., Oborn, C. J., Durban, E. M., Butel, J. S., and Medina, D. (1984) Epithelial mouse mammary cell line exhibiting normal morphogenesis in vivo and functional differentiation in vitro. Proc. Natl. Acad. Sci. U.S.A. 81, 3756-3760.
22. Eruslanov, E., and Kusmartsev, S. (2010) Identification of ROS using oxidized DCFDA and flow cytometry. Methods Mol. Biol. 594, 57-72.
23. Zielonka, J., and Kalyanaraman, B. (2010) Hydroethidine-and MitoSOXderived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic. Biol. Med. 48, 983-1001.
24. Pong, K., Doctrow, S. R., Huffman, K., Adinolfi, C. A., and Baudry, M. (2001) Attenuation of staurosporine-induced apoptosis, oxidative stress, and mitochondrial dysfunction by synthetic superoxide dismutase and catalase mimetics in cultured cortical neurons. Exp. Neurol. 171, 84-97.
25. Krohn, A. J., Preis, E., and Prehn, J. H. (1998) Staurosporine-induced apoptosis of cultured rat hippocampal neurons involves caspase-1-like proteases as upstream initiators and increased production of superoxide as a main downstream effector. J. Neurosci. 18, 8186-8197.
26. Corbett, S. A., Wilson, C. L., and Schwarzbauer, J. E. (1996) Changes in cell spreading and cytoskeletal organization are induced by adhesion to a fibronectin-fibrin matrix. Blood 88, 158-166.
27. Charles, R. L., Schroder, E., May, G., Free, P., Gaffney, P. R., Wait, R., Begum, S., Heads, R. J., and Eaton, P. (2007) Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol. Cell. Proteomics 6, 1473-1484.
28. Sabherwal, Y., Mahajan, N., Helseth, D. L., Gassmann, M., Shi, H., and Zhang, M. (2012) PDEF downregulates stathmin expression in prostate cancer. Int. J. Oncol. 40, 1889-1899.
29. Aghajanian, A., Wittchen, E. S., Campbell, S. L., and Burridge, K. (2009) Direct activation of RhoA by reactive oxygen species requires a redoxsensitive motif. PLoS ONE 4, e8045.
30. Hoffman, D. L., and Brookes, P. S. (2009) Oxygen sensitivity of mitochondrial reactive oxygen species generation depends on metabolic conditions. J. Biol. Chem. 284, 16236-16245.
31. Kulinskiǐ, V. I., and Kolesnichenko, L. S. (2009) Glutathione system. I. Synthesis, transport, glutathione transferases, glutathione peroxidases. Biomed. Khim. 55, 255-277.
32. Xiao, G. G., Wang, M., Li, N., Loo, J. A., and Nel, A. E. (2003) Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line. J. Biol. Chem. 278, 50781-50790.
33. Serru, V., Baudin, B., Ziegler, F., David, J. P., Cals, M. J., Vaubourdolle, M., and Mario, N. (2001) Quantification of reduced and oxidized glutathione in whole blood samples by capillary electrophoresis. Clin. Chem. 47, 1321-1324.
34. Shi, H. Y., Zhang, W., Liang, R., Abraham, S., Kittrell, F. S., Medina, D., and Zhang, M. (2001) Blocking tumor growth, invasion, and metastasis by maspin in a syngeneic breast cancer model. Cancer Res. 61, 6945-6951.
35. Li, Z., Shi, H. Y., and Zhang, M. (2005) Targeted expression of maspin in tumor vasculatures induces endothelial cell apoptosis. Oncogene 24, 2008-2019.
36. Schaefer, J. S., Sabherwal, Y., Shi, H. Y., Sriraman, V., Richards, J., Minella, A., Turner, D. P., Watson, D. K., and Zhang, M. (2010) Transcriptional regulation of p21/CIP1 cell cycle inhibitor by PDEF controls cell proliferation and mammary tumor progression. J. Biol. Chem. 285, 11258-11269.
37. Brown, M. D., and Sacks, D. B. (2009) Protein scaffolds in MAP kinase signalling. Cell. Signal. 21, 462-469.
38. Dalle-Donne, I., Rossi, R., Colombo, R., Giustarini, D., and Milzani, A. (2006) Biomarkers of oxidative damage in human disease. Clin. Chem. 52, 601-623.
39. Reddy, K. B., McGowen, R., Schuger, L., Visscher, D., and Sheng, S. (2001) Maspin expression inversely correlates with breast tumor progression in MMTV/TGF-β transgenic mouse model. Oncogene 20, 6538-6543.
40. Bailey, C. M., Khalkhali-Ellis, Z., Seftor, E. A., and Hendrix, M. J. (2006) Biological functions of maspin. J. Cell. Physiol. 209, 617-624.
41. Duan, H., Zhang, H. J., Yang, J. Q., Oberley, L. W., Futscher, B. W., and Domann, F. E. (2003) MnSOD up-regulates maspin tumor suppressor gene expression in human breast and prostate cancer cells. Antioxid. Redox Signal. 5, 677-688.
42. Li, J. J., Colburn, N. H., and Oberley, L. W. (1998) Maspin gene expression in tumor suppression induced by overexpressing manganese-containing superoxide dismutase cDNA in human breast cancer cells. Carcinogenesis 19, 833-839.
43. Wang, Y., Yang, J., and Yi, J. (2012) Redox sensing by proteins: oxidative modifications on cysteines and the consequent events. Antioxid. Redox Signal. 16, 649-657.
44. Seo, Y. H., and Carroll, K. S. (2009) Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies. Proc. Natl. Acad. Sci. U.S.A. 106, 16163-16168.
45. Cai, Z., Zhou, Y., Lei, T., Chiu, J. F., and He, Q. Y. (2009) Mammary serine protease inhibitor inhibits epithelial growth factor-induced epithelialmesenchymal transition of esophageal carcinoma cells. Cancer 115, 36-48.
46. Meng, T. C., Fukada, T., and Tonks, N. K. (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399.