Isoform-specific expression and characterization of 14-3-3 proteins in human glioma tissues discovered by stable isotope labeling with amino acids in cell culture-based proteomic analysis

Proteomics - Clinical Applications

Volumn 3, Issue 6, 2009, Pages 743-753

  Liang, Shufang ^a   Shen, Guobo ^a   Liu, Qingping ^b   Xu, Yuhuan ^a   Zhou, Liangxue ^a   Xiao, Shiyin ^a   Xu, Zhizhong ^a   Gong, Fengming ^a   You, Chao ^a   Wei, Yuquan ^a  

^a SICHUAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

14 3 3 Isoforms; Glioma; Quantitative proteomics; Stable isotope labeling with amino acids in cell culture

Indexed keywords

PROTEIN 14 3 3;

AMINO ACID ANALYSIS; ARTICLE; BRAIN TISSUE; DNA METHYLATION; DOWN REGULATION; GLIOMA; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEOMICS; TISSUE SPECIFICITY; UPREGULATION; WESTERN BLOTTING;

EID: 70350090448     PISSN: 18628346     EISSN: None     Source Type: Journal    
DOI: 10.1002/prca.200800198     Document Type: Article

References (69)

1. Martin, H., Patel, Y., Jones, D., Robinson, K., Aitken, A., Antibodies against the major brain isoforms of 14-3-3 protein: an antibody specific for the N-acetylated amino-terminus of a protein. FEBS Lett. 1993, 331, 296-303.
2. Fu, H., Subramanian, R. R., Masters, S. C., 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 2000, 40, 617-647.
3. Bridges, D., Moorhead, G. B. G., 14-3-3 proteins: a number of functions for a numbered protein. Sci. STKE 2005, 296, 59-66.
4. Aitken, A., Functional specificity in 14-3-3 isoform interactions through dimmer formation and phosphorylation: chromosome location of mammalian isoforms and variants. Plant Mol. Biol. 2002, 50, 993-1010.
5. Kjarland, E., Keen, T. J., Kleppe, R., Does isoform diversity explain functional differences in the 14-3-3 protein family? Curr. Pharm.Biotechnol. 2006, 7, 217-223.
6. Baldin, V., 14-3-3 proteins and growth control. Prog. Cell Cycle Res. 2000, 4, 49-60.
7. van Hemert, M. J., Steensma, H. Y., van Heusden, G. P. H., 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. BioEssays 2001, 23, 936-946.
8. Mackintosh, C., Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. J. Biochem. 2004, 381, 329-342.
9. Hermeking, H., The 14-3-3 cancer connection. Nat. Rev. Cancer 2003, 3, 931-943.
10. Wilker, E., Yaffe, M. B., 14-3-3 proteins - a focus on cancer and human disease. J. Mol. Cell Cardiol. 2004, 37, 633-642.
11. Takihara, Y., Matsuda, Y., Hara, J., Role of the β isoform of 14-3-3 proteins in cellular proliferation and oncogenic transformation. Carcinogenesis 2000, 21, 2073-2077.
12. Sugiyama, A., Miyagi, Y., Komiya, Y., Kurabe, N. et al., Forced expression of antisense 14-3-3β RNA suppresses cancerous cell growth in vitro and in vivo. Carcinogenesis 2003, 24, 1549-1559.
13. Han, D. C., Rodriguez, L. G., Guan, J. L., Identification of a novel interaction between integrin beta1 and 14-3-3 beta. Oncogene 2001, 20, 346-357.
14. Wang, Y., Jacobs, C., Hook, K. E., Duan, H. J. et al., Binding of 14-3-3 β to the carboxyl terminus of Wee1 increases Wee1 stability, kinase activity, and G2-M cell population. Cell Growth Differ. 2000, 11, 211-219.
15. Cavet, M. E., Lehoux, S., Berk, B. C., 14-3-3β is a p90 ribosomal S6 kinase (RSK) isoform 1-binding protein that negatively regulates RSK kinase activity. J. Biol. Chem. 2003, 278, 18376-18383.
16. Sato, S., Chiba, T., Sakata, E., Kato, K. et al., 14-3-3η is a novel regulator of parkin ubiquitin ligase. EMBO J. 2006, 25, 211-221.
17. Chen, X. Q., Liu, S., Qin, L. Y., Wang, C. R. et al., Selective regulation of 14-3-3η in primary culture of cerebral cortical neurons and astrocytes during development. J. Neurosci. Res. 2005, 79, 114-118.
18. Kim, Y. S., Jang, S. W., Sung, H. J., Lee, H. J. et al., Role of 14-3-3η as a positive regulator of the glucocorticoid receptor transcriptional activation. Endocrinology 2005, 146, 3133-3140.
19. Gurusamy, N., Watanabe, K., Ma, M., Zhang, S. et al., Dominant negative 14-3-3 promotes cardiomyocyte apoptosis in early stage of type I diabetes mellitus through activation of JNK. Biochem. Biophys. Res. Commun. 2004, 320, 773-780.
20. Powell, D. W., Rane, M. J., Joughin, B. A., Kalmukova, R. et al., Proteomic identification of 14-3-3ζ as a mitogen-activated protein kinase-activated protein kinase 2 substrate: role in dimer formation and ligand binding. Mol. Cell. Biol. 2003, 23, 5376-5387.
21. Clark, G. J., Drugan, J. K., Rossman, K. L., Carpenter, J. W. et al., 14-3-3ζ negatively regulates Raf-1 activity by interactions with the Raf-1 cysteine-rich domain. J. Biol. Chem. 1997, 272, 20990-20993.
22. Hashiguchi, M., Sobue, K., Paudel, H. K., 14-3-3ζ is an effector of tau protein phosphorylation. J. Biol. Chem. 2000, 275, 25247-25254.
23. Agarwal-Mawal, A., Qureshi, H. Y., Cafferty, P. W., Yuan, Z. F. et al., 14-3-3 connects glycogen synthase kinase-3β to tau within a brain microtubule associated tau phosphorylation complex. J. Biol. Chem. 2003, 11, 12722-12728.
24. Matta, A., Bahadur, S., Duggal, R., Gupta, S. D. et al., Over-expression of 14-3-3 zeta is an early event in oral cancer. BMC Cancer 2007, 7, 169.
25. Isobe, T., Ichimura, T., Sunaya, T., Okuyama, T. et al., Distinct forms of the protein kinase dependent activator of tyrosine and tryptophan hydroxylases. J. Mol. Biol. 1991, 217, 125-132.
26. Watanabe, M., Isobe, T., Ichimura, T., Kuwano, R. et al., Molecular cloning of rat cDNAs for the ζ and θ subtypes of 14-3-3 protein and differential distributions of theirmRNAs in the brain. Brain Res. Mol. Brain. Res. 1994, 25, 113-121.
27. Pergo, L., Berruti, G., Molecular cloning and tissue-specific expression of the mouse homologue of the rat brain 14-3-3θ protein: characterization of its cellular and developmental pattern of expression in the male germ line. Mol. Reprod. Dev. 1997, 47, 370-337.
28. Qi, W. Q., Liu, X. B., Qiao, D. H., Martinez, J. D., Isoform-specific expression of 14-3-3 proteins in human lung cancer tissues. Int. J. Cancer 2005, 113, 359-363.
29. Bae, S., Xiao, Y., Li, G., Casiano, C. A., Zhang, L., Effect of maternal chronic hypoxic exposure during gestation on apoptosis in fetal rat heart. Am. J. Physiol. Heart Circ. Physiol. 2003, 285, H983-H990.
30. Shiga, Y.,Wakabayashi, H.,Miyazawa, K., Kido, H., Itoyama, Y., 14-3-3 protein levels and isoform patterns in the cerebrospinal fluid of Creutzfeldt-Jakob disease patients in the progressive and terminal stages. J. Clin. Neurosci. 2006, 13, 661-665.
31. Peyril, A., Weitzdoerfer, R., Gulesserian, T., Fountoulakis, M., Lubec, G., Aberrant expression of signaling-related proteins 14-3-3γ and RACK1 in fetal Down syndrome brain (trisomy 21). Electrophoresis 2002, 23, 152-157.
32. Zerr, I., Bodemer, M., Gefeller, O., Otto, M. et al., Detection of 14-3-3 protein in the cerebrospinal fluid supports the diagnosis of Creutzfeldt-Jakob disease. Ann. Neurol. 1998, 43, 32-40.
33. Huang, N., Marie, S. K., Livramento, J. A., Chammas, R., Nitrini, R., 14-3-3 protein in the CSF of patients with rapidly progressive dementia. Neurology 2003, 61, 354-357.
34. Watanabe, M., Isobe, T., Ichimura, T., Kuwano, R. et al., Molecular cloning of rat cDNAs for b and g subtypes of 14-3-3 protein and developmental changes in expression of their mRNAs in the nervous system. Brain Res. Mol. Brain Res. 1993, 17, 135-146.
35. Kato, M., Dobyns, W. B., Lissencephaly and the molecular basis of neuronal migration. Hum. Mol. Genet. 2003, 12, R89-R96.
36. Fountoulakis, M., Cairns, N., Lubec, G., Increased levels of 14-3-3γ and E proteins in brain of patients with Alzheimer's disease and Down syndrome. J. Neural. Transm. Suppl. 1999, 57, 323-335.
37. Layfield, R., Fergusson, J., Aitken, A., Lowe, J. et al., Neurofibrillary tangles of Alzheimer's disease brains contain 14-3-3 proteins. Neurosci. Lett. 1996, 209, 57-60.
38. Osada, H., Tatematsu, Y., Yatabe, Y., Nakagawa, T. et al., Frequent and histological type-specific inactivation of 14-3-3σ in human lung cancers. Oncogene 2002, 21, 2418-2424.
39. Suzuki, H., Itoh, F., Toyota, M., Kikuchi, T. et al., Inactivation of the 14-3-3 sigma gene is associated with 5′CpG island hypermethylation in human cancers. Cancer Res. 2000, 60, 4353-4357.
40. Akahira, J., Sugihashi, Y., Suzuki, T., Ito, K. et al., Decreased expression of 14-3-3σ is associated with advanced disease in human epithelial ovarian cancer: its correlation with aberrant DNA methylation. Clin. Cancer Res. 2004, 10, 2687-2693.
41. Urano, T., Takahashi, S., Suzuki, T., Fujimura, T. et al., 14-3-3σ is down-regulated in human prostate cancer. Biochem. Biophys. Res. Commun. 2004, 319, 795-800.
42. Iwata, N., Yamamoto, H., Sasaki, S., Itoh, F. et al., Frequent hypermethylation of CpG islands and loss of expression of the 14-3-3σ gene in human hepatocellular carcinoma. Oncogene 2000, 19, 5298-5302.
43. Liang, S. F., Xu, Y. H., Shen, G. B., Zhao, X. Y. et al., Gene expression and methylation status of 14-3-3σ in human renal carcinoma tissues. IUBMB Life 2008, 60, 534-540.
44. Hermeking, H., The 14-3-3 cancer connection. Nat. Rev. Cancer 2003, 3, 931-943.
45. Ramirez, J. L., Rosell, R., Taron, M., Sanchez-Ronco, M. et al., 14-3-3σ methylation in pretreatment serum circulating DNA of cisplatin-plus -gemcitabine-treated advanced non-small-cell lung cancer patients predicts survival: the Spanish Lung Cancer Group. J. Clin. Oncol. 2005, 23, 9105-9112.
46. Boston, P. F., Jackson, P., Thompson, R. J., Human 14-3-3 protein: radioimmunoassay, tissue disturbance, and cerebrospinal fluid levels in patients with neurological disorders. J. Neurochem. 1982, 38, 1475-1482.
47. Cao, W. D., Zhang, X., Zhang, J. N., Yang, Z. J. et al., Immunocytochemical detection of 14-3-3 in primary nervous system tumors. J. Neurooncol. 2006, 77, 125-130.
48. Moore, B. W., Perez, V. J., Specific Proteins of the Nervous System in Physiological and Biochemical Aspects of Nervous Integration, Prentice-Hall, Englewood Cliffs, New Jersey 1967, pp. 343-359.
49. Wakabayashi, H., Yano, M., Tachikawa, N., OKA, S. et al., Increased concentrations of 14-3-3E, γ and ζ isoforms in cerebrospinal fluid of AIDS patients with neuronal destruction. Clin. Chim. Acta 2001, 312, 97-105.
50. Hsich, G., Kenney, K., Gibbs, C. J., Lee, K. H. et al., The 14-3-3 brain protein in cerebrospinal fluid as a marker for transmissible spongiform encephalopathies. N. Engl. J. Med. 1996, 335, 924-930.
51. Berg, D., Riess, O., Bornemann, A., Specification of 14-3-3 proteins in lewy bodies. Ann. Neurol. 2003, 54, 135.
52. Kawamoto, Y., Akiguchi, I., Nakamura, S., Honjyo, Y. et al., 14-3-3 proteins in lewy bodies in parkinson disease and diffuse lewy body disease brains. J. Neuropathol. Exp. Neurol. 2002, 61, 245-253.
53. Kawamoto, Y., Akiguchi, I., Nakamura, S., Budka, H., Accumulation of 14-3-3 proteins in glial cytoplasmic inclusions in multiple system atrophy. Ann. Neurol. 2002, 52, 722-731.
54. Martinez-Yelamos, A., Saiz, A., Sanchez-Valle, R., Casado, V. et al., 14-3-3 protein in the CSF as prognosticmarker in early multiple sclerosis. Neurology 2001, 57, 722-724.
55. Komori, T., Ishizawa, K., Arai, N., Hirose, T. et al., Immunoexpression of 14-3-3 proteins in glial cytoplasmic inclusions of multiple system atrophy. Acta Neuropathol. 2003, 106, 66-70.
56. Cao, L., Cao, W. D., Zhang, W., Lin, H. et al., Identification of 14-3-3 protein isoforms in human astrocytoma by immunohistochemistry. Neurosci. Lett. 2008, 432, 94-99.
57. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B. et al., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1, 376-386.
58. Mann, M., Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 2006, 17, 952-959.
59. Ishihama, Y., Sato, T., Tabata, T., Miyamoto, N. et al., Quantitative mouse brain proteomics using culture-derived isotope tags as internal standards. Nat. Biotechnol. 2005, 23, 617-621.
60. Ling, B., Liang, S. F., Xu, Y. H., Zhao, X. Y. et al., Differential proteomic profiles of hela cells treated with honokiol using a quantitative proteomic strategy. Amino Acids 2008, 35, 115-122.
61. Liang, S., Xu, X., Lu, H., Yang, P., Development of deuterated-leucine labeling with immunoprecipitation to analyze cellular protein complex. J. Proteomics Bioinformatics 2008, 1, 293-301
62. Li, Z. G., Zhao, J., Du, Y. H., Park, H. R. et al., Down-regulation of 14-3-3ζ suppresses anchorage-independent growth of lung cancer cells through anoikis activation. Proc. Natl. Acad. Sci. USA 2008, 105, 162-167.
63. Niemantsverdriet, M., Wagner, K., Visser, M., Backendorf, C. et al., Cellular functions of 14-3-3ζ in apoptosis and cell adhesion emphasize its oncogenic character. Oncogene 2008, 27, 1315-1319.
64. Henrique, R., Jeronimo, C., Hoque, M. O., Carvalho, A. L. et al., Frequent 14-3-3σ promoter methylation in benign and malignant prostate lesions. DNA Cell Biol. 2005, 24, 264-269.
65. Herranz, M., Esteller, M., New therapeutic targets in cancer: the epigenetic connection. Clin. Transl. Oncol. 2006, 8, 242-249.
66. Ghoshal, K., Bai, S., DNA methyltransferases as targets for cancer therapy. Drugs Today (Barc) 2007, 43, 395-422.
67. Gollob, J. A., Sciambi, C. J., Peterson, B. L., Richmond, T. et al., Phase I trial of sequential low-dose 5-aza-2-deoxycytidine plus high-dose intravenous bolus interleukin-2 in patients with melanoma or renal cell carcinoma. Clin. Cancer Res. 2006, 12, 4619-4627.
68. Laronga, C., Yang, H. Y., Neal, C., Lee, M. H., Association of the cyclin-dependent kinases and 14-3-3σ negatively regulates cell cycle progression. J. Biol. Chem. 2000, 275, 23106-23112.
69. Yang, H. Y., Wen, Y. Y., Chen, C. H., Lozano, G. et al., 14-3-3σ positively regulates p53 and suppresses tumor growth. Mol. Cell. Biol. 2003, 23, 7096-7107.