Mass spectrometric characterization of protein structure details refines the proteome signature for invasive ductal breast carcinoma

Journal of the American Society for Mass Spectrometry

Volumn 22, Issue 3, 2011, Pages 440-456

  Röwer, Claudia ^a   Koy, Cornelia ^a   Hecker, Michael ^a   Reimer, Toralf ^a   Gerber, Bernd ^a   Thiesen, Hans Jürgen ^a   Glocker, Michael O ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

2D gel electrophoresis; Breast carcinoma; Mass spectrometry; Peptide mapping; Protein expression signature; Protein structure characterization; Proteome analysis; Western blot validation

Indexed keywords

2D GEL ELECTROPHORESIS; BREAST CARCINOMA; PEPTIDE MAPPING; PROTEIN EXPRESSION SIGNATURE; PROTEIN STRUCTURE CHARACTERIZATION; PROTEOME ANALYSIS; WESTERN BLOTS;

AMINO ACIDS; DIAGNOSIS; DISEASES; ELECTROPHORESIS; ENZYMES; GELS; MASS SPECTROMETRY; PEPTIDES; PHOSPHORYLATION; REFINING; TUMORS;

PRINCIPAL COMPONENT ANALYSIS;

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; NUCLEOPHOSMIN; NUCLEOSIDE DIPHOSPHATE KINASE A; PYRUVATE KINASE; PYRUVATE KINASE M2; SERINE; UNCLASSIFIED DRUG;

ACCURACY; AGED; AMINO TERMINAL SEQUENCE; ARTICLE; CANCER PATIENT; CANCER TISSUE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; INTRADUCTAL CARCINOMA; MASTECTOMY; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEOMICS; STRUCTURE ACTIVITY RELATION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BLOTTING, WESTERN; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CASE-CONTROL STUDIES; CLUSTER ANALYSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HUMANS; MASS SPECTROMETRY; NEOPLASM PROTEINS; PEPTIDE MAPPING; PRINCIPAL COMPONENT ANALYSIS; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; TUMOR MARKERS, BIOLOGICAL;

EID: 79955770666     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-010-0031-6     Document Type: Article

References (87)

1. Olopade, O.I., Grushko, T., Nanda, R., Huo, D.: Advances in breast cancer: Pathways to personalized medicine. Clin. Cancer Res. 14, 7988-7999 (2008)
2. Boyd, Z.S., Wu, Q.J., O'Brien, C., Spoerke, J., Savage, H., Fielder, P.J., Amler, L., Yan, Y., Lackner, M.R.: Proteomic analysis of breast cancer molecular subtypes and biomarkers of response to targeted kinase inhibitors using reverse-phase protein microarrays. Mol. Cancer Ther. 7, 3695-3706 (2008)
3. Callesen, A.K., Vach, W., Jørgensen, P.E., Cold, S., Mogensen, O., Kruse, T.A., Jensen, O.N., Madsen, J.S.: Reproducibility of mass spectrometry based protein profiles for diagnosis of breast cancer across clinical studies: A systematic review. J. Proteome Res. 7, 1395-1402 (2008)
4. Hondermarck, H., Tastet, C., El Yazidi-Belkoura, I., Toillon, R.-A., Le Bourhis, X.: Proteomics of breast cancer: The quest for markers and therapeutic targets. J. Proteome Res. 7, 1403-1411 (2008)
5. Kuramitsu, Y., Kazuyuki, N.: Proteomic analysis of cancer tissues: Shedding light on carcinogenesis and possible biomarkers. Proteomics 6, 5650-5661 (2006) (Pubitemid 44683228)
6. Pastwa, E., Somiari, S.B., Czyz, M., Somiari, R.I.: Proteomics in human cancer research. Proteom. Clin. Appl. 1, 4-17 (2007)
7. Abbott, K.L., Aoki, K., Lim, J.-M., Porterfield, M., Johnson, R., O'Regan, R.M., Wells, L., Tiemeyer, M., Michael, P.: Targeted glycoproteomic identification of biomarkers for human breast carcinoma. J. Proteome Res. 7, 1470-1480 (2008)
8. Chen, S.-T., Pan, T.-L., Juan, H.-F., Chen, T.-Y., Lin, Y.-S., Huang, C.-M.: Breast tumor microenvironment: Proteomics highlights the treatments targeting secretome. J. Proteome Res. 7, 1379-1387 (2008)
9. Hawkins, O.E., VanGundy, R.S., Eckerd, A.M., Bardet, W., Buchli, R., Weidanz, J.A., Hildebrand, W.H.: Identification of breast cancer peptide epitopes presented by HLA-A*0201. J. Proteome Res. 7, 1445-1457 (2008)
10. He, Q., Zhang, S.-Q., Chu, Y.-L., Jia, X.-L., Zhao, L.-H., Wang, X.-L.: Separation and identification of differentially expressed nuclaer matrix proteins in breast barcinoma forming. Acta Oncol. 49, 76-84 (2010)
11. Kang, U.-B., Ahn, Y., Lee, J.W., Kim, Y.-H., Kim, J., Yu, M.-H., Noh, D.-Y., Lee, C.; Differential profiling of breast cancer plasma proteome by isotope-coded affinity tagging method reveals biotinidase as a breast cancer biomarker. BMC Cancer 10, 113 (2010)
12. Lu, H., Goodell, V., Disis, M.L.: Humoral immunity directed against tumor-associated antigens as potential biomarkers for the early diagnosis of cancer. J. Proteome Res. 7, 1388-1394 (2008)
13. Ou, K., Yu, K., Kesuma, D., Hooi, M., Huang, N., Chen, W., Lee, S.Y., Pei Goh, X., Tan, L.K., Liu, J., Soon, S.Y., Rashid, S.B.A., Putti, T.C., Jikuya, H., Ichikawa, T., Nishimura, O., Salto-Tellez, M., Tan, P.: Novel breast cancer biomarkers identified by integrative proteomic and gene expression mapping. J. Proteome Res. 7, 1518-1528 (2008)
14. Pucci-Minafra, I., Cancemi, P., Marabeti, M.R., Albanese, N.N., Di Cara, G., Taomina, P., Marrazzo, A.: Proteomic profiling of 13 paired ductal infiltrating breast carcinomas and non-tumoral adjacent counterparts. Proteom. Clin. Appl. 1, 118-129 (2007)
15. Sanders, M.E., Dias, E.C., Xu, B.J., Mobley, J.A., Billheimer, D., Roder, H., Grigorieva, J., Dowsett, M., Arteaga, C.L., Caprioli, R. M.: Differentiating proteomic biomarkers in breast cancer by laser capture microdissection and MALDI MS. J. Proteome Res. 7, 1500-1507 (2008)
16. Slamon, D.J., Clark, G.M., Wong, S.G., Levin, W.J., Ullrich, A., McGuire, W.: Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177-182 (1987) (Pubitemid 17231334)
17. Dowsett, M., Dunbier, A.K.: Emerging biomarkers and new understanding of traditional markers in personalized therapy for breast cancer. Clin. Cancer Res. 14, 8019-8026 (2008)
18. Paik, S., Tang, G., Shak, S., Kim, C., Baker, J., Kim, W., Cronin, M., Baehner, F.L., Watson, D., Bryant, J., Costantino, J.P., Geyer Jr., C.E., Wickerham, D.L., Wolmark, N.: Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J. Clin. Oncol. 24, 3726-3734 (2006) (Pubitemid 46622311)
19. Umar, A., Kang, H., Timmermans, A.M., Look, M.P., Meijer-van-Gelder, M.E., den Bakker, M.A., Jaitly, N., Martens, J.W.M., Luider, T. M., Foekens, J.A.: Pasa-tolic identification of a putative protein profile associated with tamoxifen therapy resistance in breast cancer. Mol. Cell. Proteom. 8, 1278-1294 (2009)
20. Willipinski-Stapelfeldt, B., Riethdorf, S., Assmann, V., Woelfle, U., Rau, T., Sauter, G., Heukeshoven, J., Pantel, K.: Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clin. Cancer Res. 11, 8006-8014 (2005) (Pubitemid 41698741)
21. Alldridge, L., Metodieva, G., Greenwood, C., Al-Janabi, K., Thwaites, L., Sauven, P., Metodiev, M.: Proteome profiling of breast tumors by gel electrophoresis and nanoscale electrospray ionization mass spectrometry. J. Proteome Res. 7, 1458-1469 (2008)
22. Seike, M., Kondo, T., Fujii, K., Yamada, T., Gemma, A., Kudoh, S., Hirohashi, S.: Proteomic signature of human cancer cells. Proteomics 4, 2776-2788 (2004) (Pubitemid 39202177)
23. Wang, M., You, J., Bemis, K.G., Tegeler, T.J., Brown, D.P.G.: Label-free mass spectrometry-based protein quantification technologies in proteomic analysis. Brief Funct. Genomic. Proteomic. 7, 329-339 (2008)
24. Yamada, M., Fujii, K., Koyama, K., Hirohashi, S., Kondo, T.: The proteomic profile of pancreatic cancer cell lines corresponding to carcinogenesis and metastasis. J. Proteom. Bioinform. 2, 1-18 (2009)
25. Brennan, D.J., Gallagher, W.M.; Prognostic Ability of a Panel of Immunohistochemistry Markers-Retailoring of an "Old Solution." Breast Cancer Res. 10, 102 (2008)
26. Röwer, C., Vissers, J.P.C., Koy, C., Kipping, M., Hecker, M., Reimer, T., Gerber, B., Thiesen, H.-J., Glocker, M.O.: Towards a proteome signature for invasive ductal breast carcinoma derived from label-free nanoscale LC-MS protein expression profiling of tumorous and glandular tissue. Anal. Bioanal. Chem. 395, 2443-2456 (2009)
27. Wulfkuhle, J.D., Speer, R., Pierobon, M., Laird, J., Espina, V., Deng, J., Mammano, E., Yang, S.X., Swain, S.M., Nitti, D., Essermann, L.J., Belluco, C., Liotta, L.A., Petricoin, E.F.: III. Multiplexed cell signaling analysis of human breast cancer applications for personalized therapy. J. Proteome Res.7, 1508-1517 (2008)
28. Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M., Baehner, F. L., Walker, M.G., Watson, D., Park, T., Hiller, W., Fisher, E.R., Wickerham, D.L., Bryant, J., Wolmark, N.: A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817-2826 (2004) (Pubitemid 40051905)
29. Sparano, J.A., Paik, S.: Development of the 21-gene assay and its application in clinical practice and clinical trials. J. Clin. Oncol. 26, 721-728 (2008) (Pubitemid 351264384)
30. van de Vijver, M.J., He, Y.D., van't Veer, L.J., Dai, H., Hart, A.A. M., Voskuil, D.W., Schreiber, G.J., Peterse, J.L., Roberts, C., Marton, M.J., Parrish, M., Atsma, D., Witteveen, A.T., Glas, A., Delahaye, L., Van der Velde, T., Bartelink, H., Rodenhuis, S., Rutgers, E.T., Friend, S.H., Bernards, R.: A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (2002) (Pubitemid 35461656)
31. van't Veer, L.J., Dai, H., van de Vijver, M.J., He, Y.D., Hart, A.A.M., Bernards, R., Friend, S.H.: Expression profiling predicts outcome in breast cancer. Breast Cancer Res. 5, 57-58 (2002)
32. Kondo, T.: Tissue proteomics for cancer biomarker development: Laser microdissection and 2D-DIGE. BMB Rep. 41, 626-634 (2008)
33. Zhang, X., Li, L., Wei, D., Yap, Y., Chen, F.: Moving cancer diagnostics from bench to bedside. Trends Biotechnol. 25, 166-173 (2007) (Pubitemid 46420716)
34. Just, T., Gafumbegete, E., Gramberg, J., Prüfer, I., Mikkat, S., Ringel, B., Pau, H.W., Glocker, M.O.: Differential proteome analysis of tonsils from children with chronic tonsillitis or with hyperplasia reveals disease-associated protein expression differences. Anal. Bioanal. Chem. 384, 1134-1144 (2006) (Pubitemid 43333995)
35. Bradford, M.M.A.: Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976)
36. Lorenz, P., Bantscheff, M., Ibrahim, S.M., Thiesen, H.-J., Glocker, M.O.: Proteome analysis of diseased joints from mice suffering from collagen-induced arthritis. Clin. Chem. Lab. Med. 41, 1622-1632 (2003) (Pubitemid 38055013)
37. Sinz, A., Bantscheff, M., Mikkat, S., Ringel, B., Drynda, S., Kekow, J., Thiesen, H.-J., Glocker, M.O.: Mass spectrometric proteome analyses of synovial fluids and plasmas from patients suffering from rheumatoid arthritis and comparison to reactive arthritis or osteoarthritis. Electrophoresis 23, 3445-3456 (2002) (Pubitemid 35230230)
38. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970)
39. Bantscheff, M., Ringel, B., Madi, A., Schnabel, R., Glocker, M.O., Thiesen, H.-J.: Differential proteome analysis and mass spectrometric characterization of germ line development-related proteins of caenorhabditis elegans. Proteomics 4, 2283-2295 (2004) (Pubitemid 39025328)
40. Neuhoff, V., Arold, N., Taube, D., Ehrhardt, W.: Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using coomassie brilliant blue G-250 and R-250. Electrophoresis 9, 255-262 (1988)
41. Heitner, J.C., Koy, C., Reimer, T., Kreutzer, M., Gerber, B., Glocker, M.O.: Differentiation of HELLP patients from healthy pregnant women by proteome analysis. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 840, 10-19 (2006) (Pubitemid 44108804)
42. Kienbaum, M., Koy, C., Montgomery, H.V., Drynda, S., Lorenz, P., Illges, H., Tanaka, K., Kekow, J., Guthke, R., Thiesen, H.-J., Glocker, M.O.: Mass spectrometric characterization of apheresis samples from rheumatoid arthritis patients for the improvement of immunoadsorption therapy-A pilot study. Proteomics Clin. Appl. 3, 797-809 (2009)
43. Mikkat, S., Koy, C., Ulbrich, M., Ringel, B., Glocker, M.O.: Mass spectrometric protein structure characterization reveals cause of migration differences of haptoglobin a chains in two-dimensional gel electrophoresis. Proteomics 4, 3921-3932 (2004) (Pubitemid 39657467)
44. Larsen, M.R., Thingholm, T.E., Jensen, O.N., Roepstorff, P., Jorgensen, T.J.D.: Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteom. 4, 873-886 (2005) (Pubitemid 41309146)
45. Mikkat, S., Lorenz, P., Scharf, C., Yu, X., Glocker, M.O., Ibrahim, S. M.: MS characterization of qualitative protein polymorphisms in the spinal cords of inbred mouse strains. Proteomics 10, 1050-1062 (2010)
46. Koy, C., Mikkat, S., Raptakis, E., Sutton, C., Resch, M., Tanaka, K., Glocker, M.O.: Matrix-assisted laser desorption/ionization-quadrupole ion trap-time of flight mass spectrometry sequencing resolves structures of unidentified peptides obtained by in-gel tryptic digestion of haptoglobin derivatives from human plasma proteomes. Proteomics 3, 851-858 (2003) (Pubitemid 36801671)
47. Jollife, J.T.: Principal component analysis. Springer Verlag, New York (1986)
48. Eisen, M.B., Spellmann, P.T., Brown, P.O., Botstein, D.: Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95, 14863-14868 (1998) (Pubitemid 29003722)
49. Elston, C.W.: Classification and grading of invasive breast carcinoma. Verh. Dtsch Ges. Pathol. 89, 35-44 (2005)
50. Remmele, W., Stegner, H.E.: Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe 8, 138-140 (1987)
51. Petrak, J., Ivanek, R., Toman, O., Cmejla, R., Cmejlova, J., Vyoral, D., Zivny, J., Vulpe, C.D.: Déjà Vu in Proteomics. A Hit Parade of Repeatedly Identified Differentially Expressed Proteins. Proteomics 8, 1744-1749 (2008)
52. Wang, P., Bouwman, F.G., Mariman, E.C.M.: Generally detected proteins in comparative proteomics-a matter of cellular stress response? Proteomics 9, 2955-2966 (2009)
53. Christofk, H.R., Vander Heiden, M.G., Harris, M.H., Ramanathan, A., Gerszten, R.E., Wei, R., Fleming, M.D., Schreiber, S.L., Cantley, L.C.: The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumor growth. Nature 452, 230-233 (2008) (Pubitemid 351380249)
54. Presek, P., Glossmann, H., Eigenbrodt, E., Schoner, W., Rübsamen, H., Friis, R.R., Bauer, H.: Similarities between a phosphoprotein (pp 60arc)-associated protein kinase of rous sarcoma virus and a cyclic adenosine 3':5'-monophosphate-independent protein kinase that phosphorylates pyruvate kinase Type M2. Cancer Res. 40, 1733-1741 (1980) (Pubitemid 10102025)
55. Presek, P., Reinacher, M., Eigenbrodt, E.: Pyruvate kinase Type M2 is phosphorylated at tyrosine residues in cells transformed by rous sarcoma virus. FEBS Lett. 242, 194-198 (1988) (Pubitemid 19012276)
56. Presek, P., Reuter, C., Findik, D., Bette, P.: High-yield purification of a pp 60c-src related protein-tyrosine Kinase from human platelets. Biochim. Biophys. Acta 969, 271-280 (1988)
57. Acebo, P., Giner, D., Calvo, P., Blanco-Rivero, A., Ortega, Á.D., Fernández, P.L., Roncador, G., Fernández-Malavé, E., Chamorro, M., Cuezva, J.M.: Cancer abolishes the tissue type-specific differences in the phenotype of energetic metabolism. Transl. Oncol. 2, 138-145 (2009)
58. Mazurek, S., Zwerschke, W., Jansen-Dürr, P., Eigenbrodt, E.: Effects of the human papilloma virus HPV-16 E7 oncoprotein on glycolysis and glutaminolysis: Role of pyruvate kinase Type M2 and the glycolytic-enzyme complex. Biochem. J. 356, 247-256 (2001) (Pubitemid 34275727)
59. Mazurek, S., Zwerschke, W., Jansen-Dürr, P., Eigenbrodt, E.: Metabolic cooperation between different oncogenes during cell transformation: Interaction between activated ras and HPV-16 E7. Oncogene 20, 6891-6899 (2001)
60. Steták, A., Veress, R., Ovádi, J., Csermely, P., Kéri, G., Ullrich, A.: Nuclear translocation of the tumor marker pyruvate kinase M2 induces programmed cell death. Cancer Res. 67, 1602-1608 (2007) (Pubitemid 46383385)
61. Grisendi, S., Mecucci, C., Falini, B., Pandolfi, P.P.: Nucleophosmin and Cancer. Nat. Rev. Cancer 6, 493-505 (2006) (Pubitemid 43980539)
62. Gu, Z., Lee, R.Y., Skaar, T.C., Bouker, K.B., Welch, J.N., Lu, J., Liu, A., Zhu, Y., Davis, N., Leonessa, F., Br?nner, N., Wang, Y., Clarke, R.: Association of interferon regulatory factor-1, Nucleophosmin, nuclear factor-B, and cyclic amp response element binding with acquired resistance to Faslodex (ICI 182, 780). Cancer Res. 62, 3428-3437 (2002) (Pubitemid 34651389)
63. Skaar, T.C., Prasad, S.C., Sharareh, S., Lippmann, M.E., Brünner, N., Clarke, R.: Two-dimensional gel electrophoresis analyses identify nucleophosmin as an estrogen regulated protein associated with acquired estrogen-independence in human breast cancer cells. J. Steroid Biochem. Mol. Biol. 67, 391-402 (1998) (Pubitemid 29049412)
64. Brady, S.N., Maggi, L.B.J., Winkeler, C.L., Toso, E.A., Gwinn, A.S., Pelletier, C.L., Weber, J.D.: Nucleophosmin protein expression level, but not threonine 198 phosphorylation, is essential in growth and proliferation. Oncogene 28, 3209-3220 (2009)
65. Brankin, B., Skaar, T.C., Brotzmann, M., Trock, B., Clarke, R.: Autoantibodies to the nucleolar phosphoprotein nucleophosmin in breast cancer patients. Cancer Epidemiol. Biomarkers Prev. 7, 1109-1115 (1998) (Pubitemid 29001667)
66. Kim, D.H., Noh, D.-Y., Lee, C., Yu, M.-H.: Proceedings of the HUPO 6th annual world congress. Seoul, South Korea (2007)
67. Graven, K.K., Troxler, R.F., Kornfeld, H., Panchenko, M.V., Farber, H. W.: Regulation of endothelial cell glyceraldehyde-3-phosphate dehydrogenase expression by hypoxia. J. Biol. Chem. 269, 24446-24453 (1994) (Pubitemid 24300996)
68. Brown, V.M., Krynetski, E.Y., Krynetskaia, N.F., Grieger, D., Mukatira, S.T., Murti, K.G., Slaughter, C.A., Park, H.-W., Evans, W. E.: A novel CRM1-mediated nuclear export signal governs nuclear accumulation of glyceraldehyde-3-phosphate dehydrogenase following genotoxic stress. J. Biol. Chem. 279, 5984-5992 (2004) (Pubitemid 38220631)
69. Sawa, A., Khan, A.A., Hester, L.D., Snyder, S.H.: Glyceraldehyde-3- phosphate dehydrogenase: Nuclear translocation participates in neuronal and nonneuronal cell death. Proc. Natl. Acad. Sci. U.S.A. 94, 11669-11674 (1997) (Pubitemid 27451056)
70. Engel, M., Mazurek, S., Eigenbrodt, E., Welter, C.: Phosphoglycerate mutase-derived polypeptide inhibits glycolytic flux and induces cell growth arrest in tumor cell lines. J. Biol. Chem. 279, 35803-35812 (2004) (Pubitemid 39100587)
71. Engel, M., Seifert, M., Theisinger, B., Seyfert, U., Welter, C.: Glyceraldeyde-3-phosphate dehydrogenase and Nm23-H1/nucleoside diposphate kinase A-two old enzymes combine for the novel Nm23 protein phosphotransferase function. J. Biol. Chem. 273, 20058-20065 (1998) (Pubitemid 28377558)
72. Salerno, M., Palmieri, D., Bouadis, A., Halverson, D., Steeg, P.S.: Nm23-H1 metastasis suppressor expression level influences the binding properties, stability, and function of the kinase suppressor of Ras1 (KSR1) erk scaffold in breast carcinoma cells. Mol. Cell. Biol. 25, 1379-1388 (2005) (Pubitemid 40204915)
73. Tee, Y.-T., Chen, G.-D., Lin, L.-Y., Ko, J.-L.,Wang, P.-H.: Nm23-H1: A metastasis-associated gene. Taiwan. J. Obstet. Gynecol. 45, 107-113 (2006) (Pubitemid 44047618)
74. Horak, C.E., Lee, J.H., Elkahloun, A.G., Boissan, M., Dumont, S., Maga, T.K., Arnaud-Dabernat, S., Palmieri, D., Stetler-Stevenson, W. G., Lacombe, M.-L., Meltzer, P.S., Steeg, P.S.: Nm23-H1 suppresses tumor cell motility by down-regulating the lysophosphatidic acid receptor EDG2. Cancer Res. 67, 7238-7246 (2007) (Pubitemid 47206552)
75. Steeg, P.S., Horak, C.E., Miller, K.D.: Clinical-translational approaches to the Nm23-H1 metastasis suppressor. Clin. Cancer Res. 14, 5006-5012 (2008)
76. Ouatas, T., Salerno, M., Palmieri, D., Steeg, P.S.: Basic and translational advances in cancer metastasis: Nm23. J. Bioenerg. Biomembr. 35, 73-79 (2003) (Pubitemid 36667583)
77. Steeg, P.S.: Metastasis suppressors alter the signal transduction of cancer cells. Nat. Rev. Cancer 3, 55-63 (2003) (Pubitemid 37328887)
78. D'Angelo, A., Garzia, L., André, A., Carotenuto, P., Aglio, V., Guardiola, O., Arrigoni, G., Cossu, A., Palmieri, G., Aravind, L., Zollo, M.: Prune cAMP phosphodiesterase binds nm23-H1 and promotes Ccancer metastasis. Cancer Cell 5, 137-149 (2004) (Pubitemid 38283800)
79. Garzia, L., D'Angelo, A., Amoresano, A., Knauer, S.K., Cirulli, C., Campanella, C., Stauber, R.H., Steegborn, C., Iolascon, A., Zollo, M.: Phosphorylation of nm23-H1 by CKI induces its complex formation with h-prune and promotes cell motility. Oncogene 27, 1853-1864 (2008) (Pubitemid 351430816)
80. Kaetzel, D.M., Zhang, Q., Yang, M., McCorkle, J.R., Ma, D., Craven, R.J.; Potential Roles of 3'-5' Exonuclease Activity of NM23-H1 in DNA Repair and Malignant Progression. J. Bioenerg. Biomembr. 2006, 3/4.
81. Jung, H., Seong, H.-A., Ha, H.: Direct interaction between NM23-H1 and macrophage migration inhibitory factor (MIF) is critical for alleviation of MIF-mediated suppression of p53 activity. J. Biol. Chem. 283, 32669-32679 (2006)
82. Bantscheff, M., Perraud, A.L., Bock, A., Rippe, K., Weiss, V., Glocker, M.O., Gross, R.: Structure-function relationships in the Bvg and Evg two-component phosphorelay systems. Int. J. Med. Microbiol. 290, 317-323 (2000)
83. Beier, D., Gross, R.: The BvgS/BvgA phosphorelay system of pathogenic bordetellae: Structure, function, and evolution. Adv. Exp. Med. Biol. 631, 149-160 (2008)
84. Marshall, J.-C., Lee, J.H., Steeg, P.S.: Clinical-translational strategies for the elevation of Nm23-H1 metastasis suppressor gene expression. Mol. Cell. Biochem. 329, 115-120 (2009)
85. Payne, D.J.: Microbiology. Desperately seeking new antibiotics. Science 321, 1644-1645 (2008)
86. Iiizumi, M., Liu, W., Paia, S.K., Furutaa, E., Watabe, K.: Drug development against metastasis-related genes and their pathways: A rationale for cancer therapy. Biochim. Biophys. Acta 1786, 87-104 (2008)
87. Isidoro, A., Casado, E., Redondo, A., Acebo, P., Espinosa, E., Alonso, A.M., Cejas, P., Hardisson, D., Fresno Vara, J.A., Belda-Iniesta, C., González-Barón, M., Cuezva, J.M.: Breast carcinomas fulfill the warburg hypothesis and provide metabolic markers of cancer prognosis. Carcinogenesis 26, 2095-2104 (2005) (Pubitemid 41672197)