Comparative proteomic analysis of mouse melanoma cell line B16, a metastatic descendant B16F10, and B16 overexpressing the metastasis-associated tyrosine phosphatase PRL-3

Oncology Research

Volumn 17, Issue 11-12, 2009, Pages 601-612

  Kim, Sang Hee ^a   Kim, Yongmo ^a   Kim, Moonil ^a   Kim, Dae Shick ^b   Lee, Sang Chul ^a   Chi, Seung Wook ^a   Lee, Do Hee ^a   Park, Sung Goo ^a   Park, Byoung Chul ^a   Bae, Kwang Hee ^a   Kang, Sunghyun ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

B16 Differential in gel electrophoresis (DIGE); Melanoma; Metastasis; Proteomics

Indexed keywords

ADENOSINE TRIPHOSPHATE SYNTHASE BETA SUBUNIT; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; FASCIN; FASCIN 1; HEAT SHOCK PROTEIN 70; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SEPTIN; SEPTIN 16; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; IMMEDIATE EARLY PROTEIN; PROTEIN TYROSINE PHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; PTP4A3 PROTEIN, MOUSE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; MASS SPECTROMETRY; MELANOMA B16; METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEOMICS; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; ANIMAL; CELL MOTION; CHEMISTRY; COMPARATIVE STUDY; EXPERIMENTAL MELANOMA; GENETICS; PATHOLOGY; TUMOR CELL LINE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL LINE, TUMOR; CELL MOVEMENT; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HSP70 HEAT-SHOCK PROTEINS; IMMEDIATE-EARLY PROTEINS; MELANOMA, EXPERIMENTAL; MICE; PROTEIN TYROSINE PHOSPHATASES; PROTEOMICS; PROTON-TRANSLOCATING ATPASES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 70350488083     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: 10.3727/096504009789745494     Document Type: Article

References (63)

1. Rivera, J.; Megias, D.; Bravo, J. Proteomics-based strategy to delineate the molecular mechanisms of the metastasis suppressor gene BRMS1. J. Proteome Res. 6:4006-4018; 2007.
2. Bashyam, M. D. Understanding cancer metastasis: An urgent need for using differential gene expression analysis. Cancer 94:1821-1829; 2002.
3. Boyd, D. Invasion and metastasis. Cancer Metastasis Rev. 15:77-89; 1996.
4. Bessette, D. C.; Qiu, D.; Pallen, C. J. PRL PTPs: Mediators and markers of cancer progression. Cancer Metastasis Rev. 27:231-252; 2008.
5. Cates, C. A.; Michael, R. L.; Stayrook, K. R.; Harvey, K. A.; Burke, Y. D.; Randall, S. K.; Crowell, P. L.; Crowell, D. N. Prenylation of oncogenic human PTP (CAAX) protein tyrosine phosphatases. Cancer Lett. 110: 49-55; 1996.
6. Wang, J.; Kirby, C. E.; Herbst, R. The tyrosine phosphatase PRL-1 localizes to the endoplasmic reticulum and the mitotic spindle and is required for normal mitosis. J. Biol. Chem. 277:46659-46668; 2002.
7. Min, S. H.; Kim, D. M.; Heo, Y. S.; Kim, Y. I.; Kim, H. M.; Kim, J.; Han, Y. M.; Kim, I. C.; Yoo, O. J. New p53 target, phosphatase of regenerating liver 1 (PRL-1) downregulates p53. Oncogene 28:545-554; 2009.
8. Wang, Q.; Holmes, D. I.; Powell, S. M.; Lu, Q. L.; Waxman, J. Analysis of stromal-epithelial interactions in prostate cancer identifies PTPCAAX2 as a potential oncogene. Cancer Lett. 175:63-69; 2002.
9. Diamond, R. H.; Cressman, D. E.; Laz, T. M.; Abrams, C. S.; Taub, R. PRL-1, a unique nuclear protein tyrosine phosphatase, affects cell growth. Mol. Cell. Biol. 14: 3752-3762; 1994.
10. Saha, S.; Bardelli, A.; Buckhaults, P.; Velculescu, V. E.; Rago, C.; St Croix, B.; Romans, K. E.; Choti, M. A.; Lengauer, C.; Kinzler, K. W.; Vogelstein, B. A phosphatase associated with metastasis of colorectal cancer. Science 294:1343-1346; 2001.
11. Radke, I.; Gotte, M.; Kersting, C.; Mattsson, B.; Kiesel, L.; Wulfing, P. Expression and prognostic impact of the protein tyrosine phosphatases PRL-1, PRL-2, and PRL-3 in breast cancer. Br. J. Cancer 95:347-354; 2006.
12. Miskad, U. A.; Semba, S.; Kato, H.; Yokozaki, H. Expression of PRL-3 phosphatase in human gastric carcinomas: close correlation with invasion and metastasis. Pathobiology 71:176-184; 2004.
13. Miskad, U. A.; Semba, S.; Kato, H.; Matsukawa, Y.; Kodama, Y.; Mizuuchi, E.; Maeda, N.; Yanagihara, K.; Yokozaki, H. High PRL-3 expression in human gastric cancer is a marker of metastasis and grades of malignancies: An in situ hybridization study. Virchows Arch. 450: 303-310; 2007.
14. Zeng, Q.; Dong, J. M.; Guo, K.; Li, J.; Tan, H. X.; Koh, V.; Pallen, C. J.; Manser, E.; Hong, W. PRL-3 and PRL-1 promote cell migration, invasion, and metastasis. Cancer Res. 63:2716-2722; 2003.
15. Wu, X.; Zeng, H.; Zhang, X.; Zhao, Y.; Sha, H.; Ge, X.; Zhang, M.; Gao, X.; Xu, Q. Phosphatase of regenerating liver-3 promotes motility and metastasis of mouse melanoma cells. Am. J. Pathol. 164:2039-2054; 2004.
16. Agrawal, S.; Reemtsma, K.; Bagiella, E.; Oluwole, S. F.; Braunstein, N. S. Role of TAP-1 and/or TAP-2 antigen presentation defects in tumorigenicity of mouse melanoma. Cell. Immunol. 228:130-137; 2004.
17. Chang, H. J.; Lee, M. R.; Hong, S. H.; Yoo, B. G; Shin, Y. K.; Jeong, J. Y.; Lim, S. B.; Choi, H. S.; Jeong, S. Y.; Park, J. G. Identification of mitochondrial F(o)F(1)-ATP synthase involved in liver metastasis of colorectal cancer. Cancer Sci. 98:1184-1191; 2007.
18. Melnikova, V. O.; Bolshakov, S. V.; Walker, C.; Ananthaswamy, H. N. Genomic alterations in spontaneous and carcinogen-induced murine melanoma cell lines. Oncogene 23:2347-2356; 2004.
19. Ortega, A.; Ferrer, P.; Carretero, J.; Obrador, E.; Asensi, M.; Pellicer, J. A.; Estrela, J. M. Down-regulation of glutathione and Bcl-2 synthesis in mouse B16 melanoma cells avoids their survival during interaction with the vascular endothelium. J. Biol. Chem. 278:39591-39599; 2003.
20. Blank, C.; Brown, I.; Kacha, A. K.; Markiewicz, M. A.; Gajewski, T. F. ICAM-1 contributes to but is not essential for tumor antigen cross-priming and CD8+ T cell-mediated tumor rejection in vivo. J. Immunol. 174:3416-3420; 2005.
21. Kashiwagi, S.; Izumi, Y.; Gohongi, T.; Demou, Z. N.; Xu, L.; Huang, P. L.; Buerk, D. G.; Munn, L. L.; Jain, R. K.; Fukumura, D. NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels. J. Clin. Invest. 115:1816-1827; 2005.
22. Kakuta, S.; Tagawa, Y.; Shibata, S.; Nanno, M.; Iwakura, Y. Inhibition of B16 melanoma experimental metastasis by interferon-gamma through direct inhibition of cell proliferation and activation of antitumour host mechanisms. Immunology 105:92-100; 2002.
23. Zhao, W.; Liu, H.; Xu, S.; Entschladen, F.; Niggemann, B.; Zanker, K. S.; Han, R. Migration and metalloproteinases determine the invasive potential of mouse melanoma cells, but not melanin and telomerase. Cancer Lett. 162(Suppl.):S49-S55; 2001.
24. D'Agostini, C.; Pica, F.; Febbraro, G.; Grelli, S.; Chiavaroli, C.; Garaci, E. Antitumour effect of OM-174 and cyclophosphamide on murine B16 melanoma in different experimental conditions. Int. Immunopharmacol. 5:1205-1212; 2005.
25. Dranoff, G.; Jaffee, E.; Lazenby, A.; Golumbek, P.; Levitsky, H.; Brose, K.; Jackson, V.; Hamada, H.; Pardoll, D.; Mulligan, R. C. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA 90:3539-3543; 1993.
26. van Elsas, A.; Hurwitz, A. A.; Allison, J. P. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med. 190:355-366; 1999.
27. Kurisu, S.; Suetsugu, S.; Yamazaki, D.; Yamaguchi, H.; Takenawa, T. Rac-WAVE2 signaling is involved in the invasive and metastatic phenotypes of murine melanoma cells. Oncogene 24:1309-1319; 2005.
28. Ishiguro, T.; Nakajima, M.; Naito, M.; Muto, T.; Tsuruo, T. Identification of genes differentially expressed in B16 murine melanoma sublines with different metastatic potentials. Cancer Res. 56:875-879; 1996.
29. Kang, S.; Kim, E. Y.; Bahn, Y. J.; Chung, J. W.; Lee do, H.; Park, S. G.; Yoon, T. S.; Park, B. C.; Bae, K. H. A proteomic analysis of the effect of mapk pathway activation on 1-glutamate-induced neuronal cell death. Cell. Mol. Biol. Lett. 12:139-147; 2007.
30. Kang, T. H.; Bae, K. H.; Yu, M. J.; Kim, W. K.; Hwang, H. R.; Jung, H.; Lee, P. Y.; Kang, S.; Yoon, T. S.; Park, S. G.; Ryu, S. E.; Lee, S. C. Phosphoproteomic analysis of neuronal cell death by glutamate-induced oxidative stress. Proteomics 7:2624-2635; 2007.
31. Van den Bergh, G.; Arckens, L. Fluorescent two-dimensional difference gel electrophoresis unveils the potential of gel-based proteomics. Curr. Opin. Biotechnol. 15:38-43; 2004.
32. Zhou, G.; Li, H.; DeCamp, D.; Chen, S.; Shu, H.; Gong, Y.; Flaig, M.; Gillespie, J. W.; Hu, N.; Taylor, P. R.; Emmert-Buck, M. R.; Liotta, L. A.; Petricoin, 3rd, E. F.; Zhao, Y. 2D differential in-gel electrophoresis for the identification of esophageal scans cell cancer-specific protein markers. Mol. Cell. Proteomics 1:117-124; 2002.
33. Unlu, M.; Morgan, M. E.; Minden, J. S. Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 18:2071-2077; 1997.
34. Huber, L. A.; Pfaller, K.; Vietor, I. Organelle proteomics: Implications for subcellular fractionation in proteomics. Circ. Res. 92:962-968; 2003.
35. Stephens, B. J.; Han, H.; Gokhale, V.; Von Hoff, D. D. PRL phosphatases as potential molecular targets in cancer. Mol. Cancer Ther. 4:1653-1661; 2005.
36. Fjeld, C. C.; Rice, A. E.; Kim, Y.; Gee, K. R.; Denu, J. M. Mechanistic basis for catalytic activation of mitogen-activated protein kinase phosphatase 3 by extracellular signal-regulated kinase. J. Biol. Chem. 275:6749-6757; 2000.
37. Farkas, B.; Hantschel, M.; Magyarlaki, M.; Becker, B.; Scherer, K.; Landthaler, M.; Pfister, K.; Gehrmann, M.; Gross, C.; Mackensen, A.; Multhoff, G. Heat shock protein 70 membrane expression and melanoma-associated marker phenotype in primary and metastatic melanoma. Melanoma Res. 13:147-152; 2003.
38. Kalogeraki, A.; Garbagnati, F.; Darivianaki, K.; Delides, G. S.; Santinami, M.; Stathopoulos, E. N.; Zoras, O. HSP-70, C-myc and HLA-DR expression in patients with cutaneous malignant melanoma metastatic in lymph nodes. Anticancer Res. 26:3551-3554; 2006.
39. Konstadoulakis, M. M.; Vezeridis, M.; Hatziyianni, E.; Karakousis, C. P.; Cole, B.; Bland, K. I.; Wanebo, H. J. Molecular oncogene markers and their significance in cutaneous malignant melanoma. Ann. Surg. Oncol. 5:253-260; 1998.
40. Torronteguy, C.; Frasson, A.; Zerwes, F.; Winnikov, E.; da Silva, V. D.; Menoret, A.; Bonorino, C. Inducible heat shock protein 70 expression as a potential predictive marker of metastasis in breast tumors. Cell Stress Chaperones 11:34-43; 2006.
41. Garcia-Bennejo, L.; Vilaboa, N. E.; Perez, C.; Galan, A.; De Bias, E.; Aller, P. Modulation of heat-shock protein 70 (HSP70) gene expression by sodium butyrate in U-937 promonocytic cells: Relationships with differentiation and apoptosis. Exp. Cell. Res. 236:268-274; 1997.
42. Lebret, T.; Watson, R. W.; Molinie, V.; O'Neill, A.; Gabriel, C.; Fitzpatrick, J. M.; Botto, H. Heat shock proteins HSP27, HSP60, HSP70, and HSP90: expression in bladder carcinoma. Cancer 98:970-977; 2003.
43. Deng, X. L.; Chen, W.; Cai, M. Y.; Wei, D. P. Expression of class I MHC molecule, HSP70 and TAP in human hepatocellular carcinoma. World J. Gastroenterol. 9:1853-1855; 2003.
44. Thanner, F.; Sutterlin, M. W.; Kapp, M.; Rieger, L.; Kristen, P.; Dietl, J.; Gassel, A. M.; Muller, T. Heat-shock protein 70 as a prognostic marker in node-negative breast cancer. Anticancer Res. 23:1057-1062; 2003.
45. Fisher, D. L.; Mandart, E.; Doree, M. Hsp90 is required for c-Mos activation and biphasic MAP kinase activation in Xenopus oocytes. EMBO J. 19:1516-1524; 2000.
46. Liu, H.; Vuyyuru, V. B.; Pham, C. D.; Yang, Y.; Singh, B. Evidence of an interaction between Mos and Hsp70: a role of the Mos residue serine 3 in mediating Hsp70 association. Oncogene 18:3461-3470; 1999.
47. Liu, L.; Zhao, L.; Zhang, Y.; Zhang, Q.; Ding, Y. Proteomic analysis of Tiam1-mediated metastasis in colorectal cancer. Cell Biol. Int. 31:805-814; 2007.
48. Minn, A. J.; Gupta, G. P.; Siegel, P. M.; Bos, P. D.; Shu, W.; Giri, D. D.; Viale, A.; Olshen, A. B.; Gerald, W. L.; Massague, J. Genes that mediate breast cancer metastasis to lung. Nature 436:518-524; 2005.
49. Adams, J. C. Fascin protrusions in cell interactions. Trends Cardiovasc. Med. 14:221-226; 2004.
50. Adams, J. C. Roles of fascin in cell adhesion and motility. Curr. Opin. Cell Biol. 16:590-596; 2004.
51. Anilkumar, N.; Parsons, M.; Monk, R.; Ng, T.; Adams, J. C. Interaction of fascin and protein kinase Calpha: A novel intersection in cell adhesion and motility. EMBO J. 22:5390-5402; 2003.
52. Hashimoto, Y.; Skacel, M.; Adams, J. C. Roles of fascin in human carcinoma motility and signaling: Prospects for a novel biomarker? Int. J. Biochem. Cell Biol. 37:1787-1804; 2005.
53. Buda, A.; Pignatelli, M. Cytoskeletal network in colon cancer: From genes to clinical application. Int. J. Biochem. Cell Biol. 36:759-765; 2004.
54. Pelosi, G.; Pastorino, U.; Pasini, F.; Maissoneuve, P.; Fraggetta, F.; Iannucci, A.; Sonzogni, A.; De Manzoni, G.; Terzi, A.; Durante, E.; Bresaola, E.; Pezzella, F.; Viale, G. Independent prognostic value of fascin immunoreactivity in stage I nonsmall cell lung cancer. Br. J. Cancer 88:537-547; 2003.
55. Peraud, A.; Mondal, S.; Hawkins, C.; Mastronardi, M.; Bailey, K.; Rutka, J. T. Expression of fascin, an actin-bundling protein, in astrocytomas of varying grades. Brain Tumor Pathol. 20:53-58; 2003.
56. Jaeger, J.; Koczan, D.; Thiesen, H. J.; Ibrahim, S. M.; Gross, G.; Spang, R.; Kunz, M. Gene expression signatures for tumor progression, tumor subtype, and tumor thickness in laser-microdissected melanoma tissues. Clin. Cancer Res. 13:806-815; 2007.
57. Collinson, I. R.; Runswick, M. J.; Buchanan, S. K.; Fearnley, I. M.; Skehel, J. M.; van Raaij, M. J.; Griffiths, D. E.; Walker, J. E. Fo membrane domain of ATP synthase from bovine heart mitochondria: Purification, subunit composition, and reconstitution with Fl-ATPase. Biochemistry 33:7971-7978; 1994.
58. Walker, J. E.; Fearnley, I. M.; Gay, N. J.; Gibson, B. W.; Northrop, F. D.; Powell, S. J.; Runswick, M. J.; Saraste, M.; Tybulewicz, V. L. Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J. Mol. Biol. 184:677-701; 1985.
59. Champagne, E.; Martinez, L. O.; Collet, X.; Barbaras, R. Ecto-F1Fo ATP synthase/F1 ATPase: metabolic and immunological functions. Curr. Opin. Lipidol. 17:279-284; 2006.
60. Espana, L.; Martin, B.; Aragues, R.; Chiva, C; Oliva, B.; Andreu, D.; Sierra, A. Bcl-x(L)-mediated changes in metabolic pathways of breast cancer cells: From survival in the blood stream to organ-specific metastasis. Am. J. Pathol. 167:1125-1137; 2005.
61. Dowling, P.; Meleady, P.; Dowd, A.; Henry, M.; Glynn, S.; Clynes, M. Proteomic analysis of isolated membrane fractions from superinvasive cancer cells. Biochim. Biophys. Acta 1774:93-101; 2007.
62. Chen, D.; Zhao, M.; Mundy, G. R. Bone morphogenetic proteins. Growth Factors 22:233-241; 2004.
63. Ide, H.; Katoh, M.; Sasaki, H.; Yoshida, T.; Aoki, K.; Nawa, Y.; Osada, Y.; Sugimura, T.; Terada, M. Cloning of human bone morphogenetic protein type IB receptor (BMPR-IB) and its expression in prostate cancer in comparison with other BMPRs. Oncogene 14:1377-1382; 1997.