Identification of phosphorylation sites on extracellular corneal epithelial cell maspin

Proteomics

Volumn 11, Issue 8, 2011, Pages 1382-1390

  Narayan, Malathi ^a   Mirza, Shama P ^a   Twining, Sally S ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b EYE INSTITUTE   (United States)

Author keywords

Cell biology; Cornea; LC MS MS; Maspin; Phosphorylation

Indexed keywords

MASPIN; SERINE; THREONINE; TYROSINE;

ARTICLE; CONTROLLED STUDY; CORNEA CELL; CORNEA EPITHELIUM; HUMAN; HUMAN CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

BLOTTING, WESTERN; CELL LINE; EPITHELIUM, CORNEAL; EXTRACELLULAR SPACE; HUMANS; IMMUNOPRECIPITATION; ISOELECTRIC FOCUSING; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERPINS; WOUND HEALING;

EID: 79953706279     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000362     Document Type: Article

References (39)

1. Zou, Z., Anisowicz, A., Hendrix, M. J., Thor, A. et al., Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science 1994, 263, 526-529.
2. Pemberton, P. A., Tipton, A. R., Pavloff, N., Smith, J. et al., Maspin is an intracellular serpin that partitions into secretory vesicles and is present at the cell surface. J. Histochem. Cytochem. 1997, 45, 1697-1706.
3. Ngamkitidechakul, C., Burke, J. M., O'Brien, W. J., Twining, S. S., Maspin: synthesis by human cornea and regulation of in vitro stromal cell adhesion to extracellular matrix. Invest. Ophthalmol. Vis. Sci. 2001, 42, 3135-3141.
4. Pemberton, P. A., Wong, D. T., Gibson, H. L., Kiefer, M. C. et al., The tumor suppressor maspin does not undergo the stressed to relaxed transition or inhibit trypsin-like serine proteases. Evidence that maspin is not a protease inhibitory serpin. J. Biol. Chem. 1995, 270, 15832-15837.
5. Yin, S., Lockett, J., Meng, Y., Biliran, H., Jr. et al., Maspin retards cell detachment via a novel interaction with the urokinase-type plasminogen activator/urokinase-type plasminogen activator receptor system. Cancer Res. 2006, 66, 4173-4181.
6. Cher, M. L., Biliran, H. R., Jr., Bhagat, S., Meng, Y. et al., Maspin expression inhibits osteolysis, tumor growth, and angiogenesis in a model of prostate cancer bone metastasis. Proc. Natl. Acad. Sci. USA 2003, 100, 7847-7852.
7. Abraham, S., Zhang, W., Greenberg, N., Zhang, M., Maspin functions as tumor suppressor by increasing cell adhesion to extracellular matrix in prostate tumor cells. J. Urol. 2003, 169, 1157-1161.
8. Ngamkitidechakul, C., Warejcka, D. J., Burke, J. M., O'Brien, W. J., Twining, S. S., Sufficiency of the reactive site loop of maspin for induction of cell-matrix adhesion and inhibition of cell invasion. Conversion of ovalbumin to a maspin-like molecule. J. Biol. Chem. 2003, 278, 31796-31806.
9. Zhang, M., Shi, Y., Magit, D., Furth, P. A., Sager, R., Reduced mammary tumor progression in WAP-TAg/WAP-maspin bitransgenic mice. Oncogene 2000, 19, 6053-6058.
10. Zhang, M., Volpert, O., Shi, Y. H., Bouck, N., Maspin is an angiogenesis inhibitor. Nat. Med. 2000, 6, 196-199.
11. Odero-Marah, V. A., Khalkhali-Ellis, Z., Schneider, G. B., Seftor, E. A. et al., Tyrosine phosphorylation of maspin in normal mammary epithelia and breast cancer cells. Biochem. Biophys. Res. Commun. 2002, 295, 800-805.
12. Halligan, B. D., Ruotti, V., Jin, W., Laffoon, S. et al., ProMoST (Protein Modification Screening Tool): a web-based tool for mapping protein modifications on two-dimensional gels. Nucleic Acids Res. 2004, 32, W638-44.
13. Halligan, B. D., ProMoST: a tool for calculating the pI and molecular mass of phosphorylated and modified proteins on two-dimensional gels. Methods Mol. Biol. 2009, 527, 283-298.
14. Cella, N., Contreras, A., Latha, K., Rosen, J. M., Zhang, M., Maspin is physically associated with [beta]1 integrin regulating cell adhesion in mammary epithelial cells. FASEB J. 2006, 20, 1510-1512.
15. Mirza, S. P., Halligan, B. D., Greene, A. S., Olivier, M., Improved methods for the analysis of membrane proteins by mass spectrometry. Physiol. Genomics 2007, 30, 89-94.
16. Cantin, G. T., Shock, T. R., Park, S. K., Madhani, H. D., Yates, J. R., 3rd, Optimizing TiO2-based phosphopeptide enrichment for automated multidimensional liquid chromatography coupled to tandem mass spectrometry. Anal. Chem. 2007, 79, 4666-4673.
17. Kweon, H. K., Hakansson, K., Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal. Chem. 2006, 78, 1743-1749.
18. Lam, Y. W., Yuan, Y., Isaac, J., Babu, C. V. et al., Comprehensive identification and modified-site mapping of S-nitrosylated targets in prostate epithelial cells. PLoS One 2010, 5, e9075.
19. Toillon, R. A., Lagadec, C., Page, A., Chopin, V. et al., Proteomics demonstration that normal breast epithelial cells can induce apoptosis of breast cancer cells through insulin-like growth factor-binding protein-3 and maspin. Mol. Cell. Proteomics 2007, 6, 1239-1247.
20. Nakashima, D., Uzawa, K., Kasamatsu, A., Koike, H. et al., Protein expression profiling identifies maspin and stathmin as potential biomarkers of adenoid cystic carcinoma of the salivary glands. Int. J. Cancer 2006, 118, 704-713.
21. Yuan, Q., An, J., Liu, D. G., Sun, L. et al., Proteomic analysis of differential protein expression in a human hepatoma revertant cell line by using an improved two-dimensional electrophoresis procedure combined with matrix assisted laser desorption/ionization-time of flight-mass spectrometry. Electrophoresis 2004, 25, 1160-1168.
22. Friedman, D. B., Wang, S. E., Whitwell, C. W., Caprioli, R. M., Arteaga, C. L., Multi-variable difference gel electrophoresis and mass spectrometry: a case study on TGF-beta and ErbB2 signaling. Mol. Cell. Proteomics 2007, 6, 150-169.
23. Wang, S. E., Narasanna, A., Whitell, C. W., Wu, F. Y. et al., Convergence of p53 and transforming growth factor beta (TGFbeta) signaling on activating expression of the tumor suppressor gene maspin in mammary epithelial cells. J. Biol. Chem. 2007, 282, 5661-5669.
24. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B. et al., Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648.
25. Boersema, P. J., Mohammed, S., Heck, A. J., Phosphopeptide fragmentation and analysis by mass spectrometry. J. Mass Spectrom. 2009, 44, 861-878.
26. Nakielny, S., Campbell, D. G., Cohen, P., The molecular mechanism by which adrenalin inhibits glycogen synthesis. Eur. J. Biochem. 1991, 199, 713-722.
27. Maik-Rachline, G., Seger, R., Variable phosphorylation states of pigment-epithelium-derived factor differentially regulate its function. Blood 2006, 107, 2745-2752.
28. Maik-Rachline, G., Shaltiel, S., Seger, R., Extracellular phosphorylation converts pigment epithelium-derived factor from a neurotrophic to an antiangiogenic factor. Blood 2005, 105, 670-678.
29. Teoh, S. S., Whisstock, J. C., Bird, P. I., Maspin (SERPINB5) is an obligate intracellular serpin. J. Biol. Chem. 2010, 285, 10862-10869.
30. Nickel, W., Rabouille, C., Mechanisms of regulated unconventional protein secretion. Nat. Rev. Mol. Cell Biol. 2009, 10, 148-155.
31. Nickel, W., Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 2005, 6, 607-614.
32. Nickel, W., The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 2003, 270, 2109-2119.
33. Torrado, L. C., Temmerman, K., Muller, H. M., Mayer, M. P. et al., An intrinsic quality-control mechanism ensures unconventional secretion of fibroblast growth factor 2 in a folded conformation. J. Cell. Sci. 2009, 122, 3322-3329.
34. Temmerman, K., Ebert, A. D., Muller, H. M., Sinning, I. et al., A direct role for phosphatidylinositol-4, 5-bisphosphate in unconventional secretion of fibroblast growth factor 2. Traffic 2008, 9, 1204-1217.
35. Caberoy, N. B., Li, W., Unconventional secretion of tubby and tubby-like protein 1. FEBS Lett. 2009, 583, 3057-3062.
36. Yu, X., Harris, S. L., Levine, A. J., The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res. 2006, 66, 4795-4801.
37. Chavez-Munoz, C., Kilani, R. T., Ghahary, A., Profile of exosomes related proteins released by differentiated and undifferentiated human keratinocytes. J. Cell. Physiol. 2009, 221, 221-231.
38. Nickoloff, B. J., Lingen, M. W., Chang, B. D., Shen, M. et al., Tumor suppressor maspin is up-regulated during keratinocyte senescence, exerting a paracrine antiangiogenic activity. Cancer Res. 2004, 64, 2956-2961.
39. Li, Z., Shi, H. Y., Zhang, M., Targeted expression of maspin in tumor vasculatures induces endothelial cell apoptosis. Oncogene 2005, 24, 2008-2019.