Proteomic characterization of harvested pseudopodia with differential gel electrophoresis and specific antibodies

Laboratory Investigation

Volumn 85, Issue 3, 2005, Pages 316-327

  Beckner, Marie E ^a   Chen, Xuan ^b   An, Jiyan ^b   Day, Billy W ^b   Pollack, Ian F ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Differential gel electrophoresis; HGF; Mass spectrometry; Migration; Proteomics; Pseudopodia

Indexed keywords

ACTIN; ANTIBODY; ENOLASE; FLUORESCENT DYE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCOLYTIC ENZYME; HEPATOCYTE GROWTH FACTOR ALPHA; ISOPROTEIN; LIPOCORTIN 1; LIPOCORTIN 2; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL ENZYME; POLYCARBONATE; PROTEOME; PYRUVATE KINASE; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; TRANSKETOLASE; UNCLASSIFIED DRUG;

ARTICLE; ARTIFACT; ASTROCYTOMA; CANCER INHIBITION; CANCER INVASION; CELL LYSATE; CELL MIGRATION; COMPUTER ANALYSIS; DIFFERENTIAL GEL ELECTROPHORESIS; GEL ELECTROPHORESIS; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOREACTIVITY; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TARGETING; PROTEOMICS; PSEUDOPODIUM; TOPOGRAPHY; TWO DIMENSIONAL ELECTROPHORESIS;

ANNEXIN A1; ANNEXIN A2; ANTIBODIES, NEOPLASM; ASTROCYTOMA; BRAIN NEOPLASMS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FRUCTOSE-BISPHOSPHATE ALDOLASE; HEPATOCYTE GROWTH FACTOR; HUMANS; MITOGENS; NEOPLASM INVASIVENESS; PHOSPHOPYRUVATE HYDRATASE; PROTEOME; PSEUDOPODIA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 14744296225     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: 10.1038/labinvest.3700239     Document Type: Article

References (82)

1. Brockmann MA, Ulbricht U, Gruner K, et al. Glioblastoma and cerebral microvascular endothelial cell migration in response to tumor-associated growth factors. Neurosurgery 2003;52:1391-1399.
2. Koochekpour S, Jeffers M, Rulong S, et al. Met and hepatocyte growth factor/scatter factor expression in human gliomas. Cancer Res 1997;57:5391-5398.
3. Lamszus K, Schmidt NO, Jin L, et al. Scatter factor promotes motility of human glioma and neuromicrovascular endothelial cells. Int J Cancer 1998;75:19-28.
4. Lamszus K, Laterra J, Westphal M, et al. Scatter factor/hepatocyte growth factor (SF/HGF) content and function in human gliomas. Int J Dev Neurosci 1999;17: 517-530.
5. Derouiche A, Frotscher M. Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins. Glia 2001;36:330-341.
6. Unlu M, Morgan ME, Minden JS. Difference gel electrophoresis: a single gel method for detecting changes in cell extracts. Electrophoresis 1997;18: 2071-2077.
7. Horwitz AR, Parsons JT. Cell migration-movin' on. Science 1999;286:1102-1103.
8. Ridley AJ, Schwartz MA, Burridge K, et al. Cell migration: integrating signals from front to back. Science 2003;302:1704-1709.
9. Dong C, Aznavoorian S, Liotta LA. Two phases of pseudopod protrusion in tumor cells revealed by a micropipette. Microvasc Res 1994;47:55-67.
10. Nguyen TN, Wang HJ, Zalzal S, et al. Purification and characterization of beta-actin-rich tumor cell pseudopodia: role of glycolysis. Exp Cell Res 2000;258: 171-183.
11. Abounader R, Ranganathan S, Lal B, et al. Reversion of human glioblastoma malignancy by U1 small nuclear RNA/ribozyme targeting of scatter factor/hepatocyte growth factor and c-met expression. J Natl Cancer Inst 1999;91:1548-1556.
12. Hollborn M, Krausse C, Iandiev I, et al. Glial cell expression of hepatocyte growth factor in vitreoretinal proliferative disease. Lab Invest 2004;84:963-972.
13. Yamada T, Yoshiyama Y, Tsuboi Y, et al. Astroglial expression of hepatocyte growth factor and hepatocyte growth factor activator in human brain tissues. Brain Res 1997;762:251-255.
14. Welch WC, Kornblith PL, Michalopoulos GK, et al. Hepatocyte growth factor (HGF) and receptor (c-met) in normal and malignant astrocytic cells. Anticancer Res 1999;19:1635-1640.
15. Schmidt NO, Westphal M, Hagel C, et al. Levels of vascular endothelial growth factor, hepatocyte growth factor/scatter factor and basic fibroblast growth factor in human gliomas and their relation to angiogenesis. Int J Cancer 1999;84:10-18.
16. Yano H, Hara A, Murase S, et al. Expression of hepatocyte growth factor and matrix metalloproteinase-2 in human glioma. Brain Tumor Pathol 2001;18: 7-12.
17. Kaplan O, Firon M, Vivi A, et al. HGF/SF activates glycolysis and oxidative phosphorylation in DA3 murine mammary cancer cells. Neoplasia 2000;2: 365-377.
18. Skouteris GG, Schroder CH. The hepatocyte growth factor receptor kinase-mediated phosphorylation of lipocortin-1 transduces the proliferating signal of the hepatocyte growth factor. J Biol Chem 1996;271: 27266-27273.
19. Oudard S, Boitier E, Miccoli L, et al. Gliomas are driven by glycolysis: putative roles of hexokinase, oxidative phosphorylation and mitochondrial ultrastructure. Anticancer Res 1997;17:1903-1911.
20. Daum G, Keller K, Lange K. Association of glycolytic enzymes with the cytoplasmic side of the plasma membrane of glioma cells. Biochim Biophys Acta 1988;939:277-281.
21. Iwadate Y, Sakaida T, Hiwasa T, et al. Molecular classification and survival prediction in human gliomas based on proteome analysis. Cancer Res 2004;64: 2496-2501.
22. Beckner ME, Stracke ML, Liotta LA, et al. Glycolysis as primary energy source in tumor cell chemotaxis. J Natl Cancer Inst 1990;82:1836-1840.
23. Beckner ME, Pollack IF. Treatment of hypoxia-resistant astrocytoma cell migration with glucose inhibitors. Neuro-Oncology 2003;5:280.
24. Carlier MF, Wiesner S, Le Clainche C, et al. Actin-based motility as a self-organized system: mechanism and reconstitution in vitro. C R Biol 2003;326:161-170.
25. Bronstein WW, Knull HR. Interaction of muscle glycolytic enzymes with thin filament proteins. Can J Biochem 1981;59:494-499.
26. Durrieu C, Bernier-Valentin F, Rousset B. Binding of glyceraldehyde 3-phosphate dehydrogenase to microtubules. Mol Cell Biochem 1987;74:55-65.
27. Durrieu C, Bernier-Valentin F, Rousset B. Microtubules bind glyceraldehyde 3-phosphate dehydrogenase and modulate its enzyme activity and quaternary structure. Arch Biochem Biophys 1987;252:32-40.
28. Masters C. Interactions between glycolytic enzymes and components of the cytomatrix. J Cell Biol 1984;99 (1 Part 2):222s-225s.
29. Karkhoff-Schweizer R, Knull HR. Demonstration of tubulin-glycolytic enzyme interactions using a novel electrophoretic approach. Biochem Biophys Res Commun 1987;146:827-831.
30. Mejean C, Pons F, Benyamin Y, et al. Antigenic probes locate binding sites for the glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase, aldolase and phosphofructokinase on the actin monomer in microfilaments. Biochem J 1989;264:671-677.
31. Minaschek G, Groschel-Stewart U, Blum S, et al. Microcompartmentation of glycolytic enzymes in cultured cells. Eur J Cell Biol 1992;58:418-428.
32. Somers M, Engelborghs Y, Baert J. Analysis of the binding of glyceraldehyde-3-phosphate dehydrogenase to microtubules, the mechanism of bundle formation and the linkage effect. Eur J Biochem 1990;193:437-444.
33. Sirover MA. New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 1999;1432:159-184.
34. Walsh JL, Knull HR. Heteromerous interactions among glycolytic enzymes and of glycolytic enzymes with F-actin: effects of poly(ethylene glycol). Biochim Biophys Acta 1988;952:83-91.
35. Walsh JL, Keith TJ, Knull HR. Glycolytic enzyme interactions with tubulin and microtubules. Biochim Biophys Acta 1989;999:64-70.
36. Volker KW, Knull HR. Glycolytic enzyme-tubulin interactions: role of tubulin carboxy terminals. J Mol Recogn 1993;6:167-177.
37. Volker KW, Reinitz CA, Knull HR. Glycolytic enzymes and assembly of microtubule networks. Comp Biochem Physiol B Biochem Mol Biol 1995;112:503-514.
38. Volker KW, Knull H. A glycolytic enzyme binding domain on tubulin. Arch Biochem Biophys 1997;338: 237-243.
39. Carlier MF, Pantaloni D, Evans JA, et al. The hydrolysis of ATP that accompanies actin polymerization is essentially irreversible. FEBS Lett 1988;235:211-214.
40. Carlier MF. Nucleotide hydrolysis regulates the dynamics of actin filaments and microtubules. Philos Trans R Soc London B Biol Sci 1992;336:93-97.
41. Korn ED, Carlier MF, Pantaloni D. Actin polymerization and ATP hydrolysis. Science 1987;238:638-644.
42. Dufort PA, Lumsden CJ. How profilin/barbed-end synergy controls actin polymerization: a kinetic model of the ATP hydrolysis circuit. Cell Motil Cytoskeleton 1996;35:309-330.
43. Loisel TP, Boujemaa R, Pantaloni D, et al. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 1999;401:613-616.
44. Mitchison TJ. Evolution of a dynamic cytoskeleton. Philos Trans R Soc London B Biol Sci 1995;349: 299-304.
45. Le PU, Nguyen TN, Drolet-Savoie P, et al. Increased beta-actin expression in an invasive moloney sarcoma virus-transformed MDCK cell variant concentrates to the tips of multiple pseudopodia. Cancer Res 1998;58: 1631-1635.
46. Rescher U, Gerke V. Annexins-unique membrane binding proteins with diverse functions. J Cell Sci 2004;117(Part 13):2631-2639.
47. Fernandez MP, Morgan RO. Annexin Sequence Database, The New Nomenclature. European Annexin Homepage 2004;www.annexins.org.
48. Johnson MD, Kamso-Pratt J, Pepinsky RB; et al. Lipocortin-1 immunoreactivity in central and peripheral nervous system glial tumors. Hum Pathol 1989;20: 772-776.
49. Turgeon JL, Cooper RH, Waring DW. Membrane-specific association of annexin I and annexin II in anterior pituitary cells. Endocrinology 1991;128:96-102.
50. McLeod JD, Goodall A, Jelic P, et al. Changes in the cellular distribution of lipocortin-1 (Annexin-1) in C6 glioma cells after exposure to dexamethasone. Biochem Pharmacol 1995;50:1103-1107.
51. Mizuno H, Uemura K, Moriyama A, et al. Glucocorticoid induced the expression of mRNA and the secretion of lipocortin 1 in rat astrocytoma cells. Brain Res 1997;746:256-264.
52. Cirino G, Flower RJ. Human recombinant lipocortin 1 inhibits prostacyclin production by human umbilical artery in vitro. Prostaglandins 1987;34:59-62.
53. Minghetti L, Nicolini A, Polazzi E, et al. Downregulation of microglial cyclooxygenase-2 and inducible nitric oxide synthase expression by lipocortin 1. Br J Pharmacol 1999;126:1307-1314.
54. Sinha P, Hutter G, Kottgen E, et al. Increased expression of annexin I and thioredoxin detected by two-dimensional gel electrophoresis of drug resistant human stomach cancer cells. J Biochem Biophys Methods 1998;37:105-116.
55. Wu W, Tang X, Hu W, et al. Identification and validation of metastasis-associated proteins in head and neck cancer cell lines by two-dimensional electrophoresis and mass spectrometry. Clin Exp Metast 2002;19:319-326.
56. Cicek M, Samant RS, Kinter M, et al. Identification of metastasis-associated proteins through protein analysis of metastatic MDA-MB-435 and metastasis-suppressed BRMS1 transfected-MDA-MB-435 cells. Clin Exp Metast 2004;21:149-157.
57. Pencil SD, Toth M. Elevated levels of annexin I protein in vitro and in vivo in rat and human mammary adenocarcinoma. Clin Exp Metast 1998;16:113-121.
58. Masaki T, Tokuda M, Ohnishi M, et al. Enhanced expression of the protein kinase substrate annexin in human hepatocellular carcinoma. Hepatology 1996;24:72-81.
59. Ahn SH, Sawada H, Ro JY, et al. Differential expression of annexin I in human mammary ductal epithelial cells in normal and benign and malignant breast tissues. Clin Exp Metast 1997;15:151-156.
60. Lim MS, Elenitoba-Johnson KS. Proteomics in pathology research. Lab Invest 2004;84:1227-1244.
61. Diaz VM, Hurtado M, Thomson TM, et al. Specific interaction of tissue-type plasminogen activator (t-PA) with annexin II on the membrane of pancreatic cancer cells activates plasminogen and promotes invasion in vitro. Gut 2004;53:993-1000.
62. Hajjar KA, Acharya SS. Annexin II and regulation of cell surface fibrinolysis. Ann NY Acad Sci 2000;902: 265-271.
63. Roshy S, Sloane BF, Moin K. Pericellular cathepsin B and malignant progression. Cancer Metast Rev 2003; 22:271-286.
64. Jones PG, Moore GJ, Waisman DM. A nonapeptide to the putative F-actin binding site of annexin-II tetramer inhibits its calcium-dependent activation of actin filament bundling. J Biol Chem 1992;267: 13993-13997.
65. Roseman BJ, Bollen A, Hsu J, et al. Annexin II marks astrocytic brain tumors of high histologic grade. Oncol Res 1994;6:561-567.
66. Allen RT, Hunter Jr W, Agrawal DK. Morphological and biochemical characterization and analysis of apoptosis. J Pharmacol Toxicol Methods 1997;37: 215-228.
67. Townsend DM, Tew KD. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 2003;22:7369-7375.
68. Bagatell R, Beliakoff J, David CL, et al. Hsp90 inhibitors deplete key anti-apoptotic proteins in pediatric solid tumor cells and demonstrate synergistic anticancer activity with cisplatin. Int J Cancer 2005; 113:179-188.
69. Bagatell R, Whitesell L. Altered Hsp90 function in cancer: a unique therapeutic opportunity. Mol Cancer Ther 2004;3:1021-1030.
70. Beliakoff J, Bagatell R, Paine-Murrieta G, et al. Hormone-refractory breast cancer remains sensitive to the antitumor activity of heat shock protein 90 inhibitors. Clin Cancer Res 2003;9:4961-4971.
71. Workman P. Combinatorial attack on multistep oncogenesis by inhibiting the Hsp90 molecular chaperone. Cancer Lett 2004;206:149-157.
72. Myllyharju J. Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol 2003;22:15-24.
73. Pickart CM, Rose IA. Ubiquitin carboxyl-terminal hydrolase acts on ubiquitin carboxyl-terminal amides. J Biol Chem 1985;260:7903-7910.
74. Asai T, Tomita Y, Nakatsuka S, et al. VCP (p97) regulates NFkappaB signaling pathway, which is important for metastasis of osteosarcoma cell line. Jpn J Cancer Res 2002;93:296-304.
75. Tsujimoto Y, Tomita Y, Hoshida Y, et al. Elevated expression of valosin-containing protein (p97) is associated with poor prognosis of prostate cancer. Clin Cancer Res 2004;10:3007-3012.
76. Yamamoto S, Tomita Y, Hoshida Y, et al. Expression level of valosin-containing protein is strongly associated with progression and prognosis of gastric carcinoma. J Clin Oncol 2003;21:2537-2544.
77. Yamamoto S, Tomita Y, Nakamori S, et al. Elevated expression of valosin-containing protein (p97) in hepatocellular carcinoma is correlated with increased incidence of tumor recurrence. J Clin Oncol 2003;21: 447-452.
78. Yamamoto S, Tomita Y, Hoshida Y, et al. Expression of valosin-containing protein in colorectal carcinomas as a predictor for disease recurrence and prognosis. Clin Cancer Res 2004;10:651-657.
79. Yamamoto S, Tomita Y, Hoshida Y, et al. Increased expression of valosin-containing protein (p97) is associated with lymph node metastasis and prognosis of pancreatic ductal adenocarcinoma. Ann Surg Oncol 2004;11:165-172.
80. Yamamoto S, Tomita Y, Hoshida Y, et al. Expression level of valosin-containing protein (p97) is correlated with progression and prognosis of non-small-cell lung carcinoma. Ann Surg Oncol 2004;11:697-704.
81. Yamamoto S, Tomita Y, Hoshida Y, et al. Expression level of valosin-containing protein (VCP) as a prognostic marker for gingival squamous cell carcinoma. Ann Oncol 2004;15:1432-1438.
82. Yamamoto S, Tomita Y, Hoshida Y, et al. Expression level of valosin-containing protein (p97) is associated with prognosis of esophageal carcinoma. Clin Cancer Res 2004;10:5558-5565.