Proteomic profiling of germ cell cancer cells treated with aaptamine, a marine alkaloid with antiproliferative activity

Journal of Proteome Research

Volumn 11, Issue 4, 2012, Pages 2316-2330

  Dyshlovoy, Sergey A ^a,b   Naeth, Ina ^a   Venz, Simone ^c   Preukschas, Michael ^a   Sievert, Henning ^a   Jacobsen, Christine ^a   Shubina, Larisa K ^b   Gesell Salazar, Manuela ^c   Scharf, Christian ^c   Walther, Reinhard ^c   Krepstakies, Marcel ^d   Priyadarshini, Poornima ^d   Hauber, Joachim ^d   Fedorov, Sergey N ^b   Bokemeyer, Carsten ^a   Stonik, Valentin A ^b   Balabanov, Stefan ^a   Honecker, Friedemann ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b PACIFIC INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

aaptamine; antiproliferative activity; differentiation; eIF5A; germ cell cancer; hypusination; marine alkaloids; proteome analysis

Indexed keywords

AAPTAMINE; ALPHA ENOLASE; CATHEPSIN D; COFILIN 1; COLD SHOCK PROTEIN; HYPUSINE; INITIATION FACTOR 5A; SEMAPIMOD;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYONAL CARCINOMA STEM CELL; G2 PHASE CELL CYCLE CHECKPOINT; GERM CELL TUMOR; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; BIOLOGICAL AGENTS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HEK293 CELLS; HUMANS; LYSINE; MOLECULAR SEQUENCE DATA; NAPHTHYRIDINES; NEOPLASMS, GERM CELL AND EMBRYONAL; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PEPTIDE INITIATION FACTORS; PROTEINS; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; RNA-BINDING PROTEINS;

AAPTOS AAPTOS; EUKARYOTA;

EID: 84859575429     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300170p     Document Type: Article

References (54)

1. Nakamura, H.; Kobayashi, J.; Ohizumi, Y. Isolation and structure of aaptamine a novel heteroaromatic substance possessing alpha-blocking activity from the sea sponge Aaptos-aaptos Tetrahedron Lett. 1982, 23 (52) 5555-5558
2. Shubina, L. K.; Kalinovsky, A. I.; Fedorov, S. N.; Radchenko, O. S.; Denisenko, V. A.; Dmitrenok, P. S.; Dyshlovoy, S. A.; Krasokhin, V. B.; Stonik, V. A. Aaptamine alkaloids from the Vietnamese sponge Aaptos sp Nat. Prod. Commun. 2009, 4 (8) 1085-1088
3. Nakamura, H.; Kobayashi, J.; Ohizumi, Y.; Hirata, Y. Physiologically active marine natural-products from porifera. 0.11. Aaptamines-novel benzo de 1,6 naphthyridines from the Okinawan marine sponge Aaptos-aaptos J. Chem. Soc., Perkin Trans. 1 1987, 1) 173-176
4. Calcul, L.; Longeon, A.; Al Mourabit, A.; Guyot, M.; Bourguet-Kondracki, M. L. Novel alkaloids of the aaptamine class from an Indonesian marine sponge of the genus Xestopongia Tetrahedron 2003, 59 (34) 6539-6544
5. Coutinho, A. F.; Chanas, B.; Souza, T.; Frugrulhetti, I.; Epifanio, R. D. Anti HSV-1 alkaloids from a feeding deterrent marine sponge of the genus Aaptos Heterocycles 2002, 57 (7) 1265
6. Shen, Y. C.; Lin, T. T.; Sheu, J. H.; Duh, C. Y. Structures and cytotoxicity relationship of isoaaptamine and aaptamine derivatives J. Nat. Prod. 1999, 62 (9) 1264-1267
7. Kaufman, T. S.; Larghi, E. L.; Bohn, M. L. Aaptamine and related products. Their isolation, chemical syntheses, and biological activity Tetrahedron 2009, 65 (22) 4257-4282
8. Hamann, M. T.; Bowling, J. J.; Pennaka, H. K.; Ivey, K.; Wahyuono, S.; Kelly, M.; Schinazi, R. F.; Valeriote, F. A.; Graves, D. E. Antiviral and anticancer optimization studies of the DNA-binding marine natural product aaptamine Chem. Biol. Drug Des. 2008, 71 (3) 205-215
9. Shubina, L. K.; Makarieva, T. N.; Dyshlovoy, S. A.; Fedorov, S. N.; Dmitrenok, P. S.; Stonik, V. A. Three new aaptamines from the marine sponge Aaptos sp. and their proapoptotic properties Nat. Prod. Commun. 2010, 5 (12) 1881-1884
10. Tsukamoto, S.; Yamanokuchi, R.; Yoshitomi, M.; Sato, K.; Ikeda, T.; Rotinsulu, H.; Mangindaan, R. E. P.; de Voogd, N. J.; van Soest, R. W. M.; Yokosawa, H. Aaptamine, an alkaloid from the sponge Aaptos suberitoides, functions as a proteasome inhibitor Bioorg. Med. Chem. Lett. 2010, 20 (11) 3341-3343
11. Aoki, S.; Kong, D. X.; Suna, H.; Sowa, Y.; Sakai, T.; Setiawan, A.; Kobayashi, M. Aaptamine, a spongean alkaloid, activates p21 promoter in a p53-independent manner Biochem. Biophys. Res. Commun. 2006, 342 (1) 101-106
12. Dyshlovoy, S.; Fedorov, S.; Shubina, L.; Honecker, F.; Stonik, V. Anticancer activity of aaptamine and its derivatives isolated from marine Vietnamese sponge Aaptos sp Ann. Oncol. 2011, 22, 33-33
13. Andrews, P. W. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell-line in vitro Dev. Biol. 1984, 103 (2) 285-293
14. Sieuwerts, A. M.; Klijn, J. G. M.; Peters, H. A.; Foekens, J. A. The Mtt tetrazolium salt assay scrutinized-how to use this assay reliably to measure metabolic activity of cell cultures in vitro for the assessment of growth characteristics, IC50 values and cell survival Eur. J. Clin. Chem. Clin. Biochem. 1995, 33 (11) 813-823
15. Glaesener, S.; Honecker, F.; Veltman, I. M.; Gillis, A. J. M.; Rohlfing, T.; Streichert, T.; Otto, B.; Brummendorf, T. H.; Looijenga, L. H. J.; Bokemeyer, C.; Balabanov, S. Comparative proteome, transcriptome, and genome analysis of a gonadal and an extragonadal germ cell tumor cell J. Proteome Res. 2008, 7 (9) 3890-3899
16. Ummanni, R.; Mundt, F.; Pospisil, H.; Venz, S.; Scharf, C.; Barett, C.; Falth, M.; Kollermann, J.; Walther, R.; Schlomm, T.; Sauter, G.; Bokemeyer, C.; Sultmann, H.; Schuppert, A.; Brummendorf, T. H.; Balabanov, S. Identification of clinically relevant protein targets in prostate cancer with 2D-DIGE coupled mass spectrometry and systems biology network platform PLoS One 2011, 6, 2
17. 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. 1976, 72, 248-54
18. Junker, H.; Venz, S.; Zimmermann, U.; Thiele, A.; Scharf, C.; Walther, R. Stage-related alterations in renal cell carcinoma-comprehensive quantitative analysis by 2D-DIGE and protein network analysis PLoS One 2011, 6, 7
19. Koch, S.; Mayer, F.; Honecker, F.; Schittenhelm, M.; Bokemeyer, C. Efficacy of cytotoxic agents used in the treatment of testicular germ cell tumours under normoxic and hypoxic conditions in vitro Br. J. Cancer 2003, 89 (11) 2133-2139
20. Nicoletti, I.; Migliorati, G.; Pagliacci, M. C.; Grignani, F.; Riccardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow-cytometry J. Immunol. Methods 1991, 139 (2) 271-279
21. Wolff, E. C.; Lee, S. B.; Park, M. H. Assay of deoxyhypusine synthase activity Methods Mol. Biol. 2011, 720, 195-205
22. Balabanov, S.; Ziegler, P.; Hartmann, U.; Kammer, W.; Copland, M.; Priemer, M.; Wilhelm, T.; Bokemeyer, C.; Kanz, L.; Holyoake, T.; Nordheim, A.; Bruemmendorf, T. Inhibition of hypusination of eukaryotic initiation factor 5a (eIF5A) as a novel a synergistic treatment strategy in imatinib-treated BCR-ABL positive leukemias identified by a global proteomics approach Blood 2005, 106 (11) 565a-566a
23. Sommer, M. N.; Bevec, D.; Klebl, B.; Flicke, B.; Holscher, K.; Freudenreich, T.; Hauber, I.; Hauber, J.; Mett, H. Screening assay for the identification of deoxyhypusine synthase inhibitors J. Biomol. Screening 2004, 9 (5) 434-438
24. Hauber, I.; Bevec, D.; Heukeshoven, J.; Kratzer, F.; Horn, F.; Choidas, A.; Harrer, T.; Hauber, J. Identification of cellular deoxyhypusine synthase as a novel target for antiretroviral therapy J. Clin. Invest. 2005, 115 (1) 76-85
25. Mueller, S.; Schittenhelm, M.; Honecker, F.; Malenke, E.; Lauber, K.; Wesselborg, S.; Hartmann, J. T.; Bokemeyer, C.; Mayer, F. Cell-cycle progression and response of germ cell tumors to cisplatin in vitro Int. J. Oncol. 2006, 29 (2) 471-479
26. Lee, S. B.; Park, J. H.; Folk, J. E.; Deck, J. A.; Pegg, A. E.; Sokabe, M.; Fraser, C. S.; Park, M. H. Inactivation of eukaryotic initiation factor 5A (eIF5A) by specific acetylation of its hypusine residue by spermidine/spermine acetyltransferase 1 (SSAT1) Biochem. J. 2011, 433, 205-213
27. Park, M. H. The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A) J Biochem 2006, 139 (2) 161-169
28. Klier, H.; Wohl, T.; Eckerskorn, C.; Magdolen, V.; Lottspeich, F. Determination and mutational analysis of the phosphorylation site in the hypusine-containing protein hyp2p FEBS Lett 1993, 334 (3) 360-364
29. Klier, H.; Csonga, R.; Joao, H. C.; Eckerskorn, C.; Auer, M.; Lottspeich, F.; Eder, J. Isolation and structural characterization of different isoforms of the hypusine-containing protein eif-5a from HeLa-cells Biochemistry 1995, 34 (45) 14693-14702
30. Kobayashi, M.; Nishita, M.; Mishima, T.; Ohashi, K.; Mizuno, K. MAPKAPK-2-mediated LIM-kinase activation is critical for VEGF-induced actin remodeling and cell migration EMBO J. 2006, 25 (4) 713-726
31. Heyworth, P. G.; Robinson, J. M.; Ding, J. B.; Ellis, B. A.; Badwey, J. A. Cofilin undergoes rapid dephosphorylation in stimulated neutrophils and translocates to ruffled membranes enriched in products of the NADPH oxidase complex. Evidence for a novel cycle of phosphorylation and dephosphorylation Histochem. Cell Biol. 1997, 108 (3) 221-233
32. Jakus, J.; Wolff, E. C.; Park, M. H.; Folk, J. E. Features of the spermidine-binding site of deoxyhypusine synthase as derived from inhibition studies-Effective inhibition by bis-guanylated and mono-guanylated diamines and polyamines J. Biol. Chem. 1993, 268 (18) 13151-13159
33. Bevec, D.; Kappel, B.; Jaksche, H.; Csonga, R.; Hauber, J.; Klier, H.; Steinkasserer, A. Molecular characterization of a cDNA encoding functional human deoxyhypusine synthase and chromosomal mapping of the corresponding gene locus FEBS Lett 1996, 378 (2) 195-198
34. Andrews, P. W.; Damjanov, I.; Simon, D.; Banting, G. S.; Carlin, C.; Dracopoli, N. C.; Fogh, J. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell-line tera-2-differentiation in vivo and in vitro Lab Invest 1984, 50 (2) 147-162
35. Trojanowicz, B.; Winkler, A.; Hammje, K.; Chen, Z. X.; Sekulla, C.; Glanz, D.; Schmutzler, C.; Mentrup, B.; Hombach-Klonisch, S.; Klonisch, T.; Finke, R.; Kohrle, J.; Dralle, H.; Hoang-Vu, C. Retinoic acid-mediated down-regulation of ENO1/MBP-1 gene products caused decreased invasiveness of the follicular thyroid carcinoma cell lines J. Mol. Endocrinol. 2009, 42 (3-4) 249-260
36. Subramanian, A.; Miller, D. M. Structural analysis of alpha-enolase-Mapping the functional domains involved in down-regulation of the c-myc protooncogene J. Biol. Chem. 2000, 275 (8) 5958-5965
37. Dihazi, H.; Dihazi, G. H.; Jahn, O.; Meyer, S.; Nolte, J.; Asif, A. R.; Mueller, G. A.; Engel, W. Multipotent adult germline stem cells and embryonic stem cells functional proteomics revealed an important role of eukaryotic initiation factor 5A (Eif5a) in stem cell differentiation J. Proteome Res. 2011, 10 (4) 1962-1973
38. Keezer, S. M.; Ivie, S. E.; Krutzsch, H. C.; Tandle, A.; Libutti, S. K.; Roberts, D. D. Angiogenesis inhibitors target the endothelial cell cytoskeleton through altered regulation of heat shock protein 27 and cofilin Cancer Res. 2003, 63 (19) 6405-6412
39. Arber, S.; Barbayannis, F. A.; Hanser, H.; Schneider, C.; Stanyon, C. A.; Bernard, O.; Caroni, P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase Nature 1998, 393 (6687) 805-809
40. Donato, L. J.; Noy, N. Suppression of mammary carcinoma growth by retinoic acid: Proapoptotic genes are targets for retinoic acid receptor and cellular retinoic acid-binding protein II signaling Cancer Res. 2005, 65 (18) 8193-8199
41. Budhu, A. S.; Noy, N. Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest Mol. Cell. Biol. 2002, 22 (8) 2632-2641
42. Borghi, R.; Vene, R.; Arena, G.; Schubert, D.; Albini, A.; Tosetti, F. Transient modulation of cytoplasmic and nuclear retinoid receptors expression in differentiating human teratocarcinoma NT2 cells J. Neurochem. 2003, 84 (1) 94-104
43. Park, M. H.; Wolff, E. C.; Folk, J. E. Hypusine-its posttranslational formation in eukaryotic initiation factor-5A and its potential role in cellular-regulation Biofactors 1993, 4 (2) 95-104
44. Tome, M. E.; Fiser, S. M.; Payne, C. M.; Gerner, E. W. Excess putrescine accumulation inhibits the formation of modified eukaryotic initiation factor 5A (eIF-5A) and induces apoptosis Biochem. J. 1997, 328 (Pt 3) 847-54
45. Zhang, J. T.; Dong, Z. Z.; Arnold, R. J.; Yang, Y. Y.; Park, M. H.; Hrncirova, P.; Mechref, Y.; Novotny, M. V. Modulation of differentiation-related gene 1 expression by cell cycle blocker mimosine, revealed by proteomic analysis Mol. Cell Proteomics 2005, 4 (7) 993-1001
46. Thompson, J. E.; Taylor, C. A.; Sun, Z.; Cliche, D. O.; Ming, H.; Eshaque, B.; Jin, S.; Hopkins, M. T.; Thai, B. Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumour necrosis factor alpha signalling Exp. Cell Res. 2007, 313 (3) 437-449
47. Hauber, J. Revisiting an old acquaintance: role for elF5A in diabetes J. Clin. Invest. 2010, 120 (6) 1806-1808
48. Maier, B.; Tersey, S. A.; Mirmira, R. G. Hypusine: a new target for therapeutic intervention in diabetic inflammation Discovery Med. 2010, 10 (50) 18-23
49. Kaiser, A. Translational control of eIF5A in various diseases Amino Acids 2011, 42, 679-684
50. Park, M. H.; Wolff, E. C.; Folk, J. E. Hypusine is essential for eukaryotic cell-proliferation Trends Biochem. Sci. 1993, 18 (12) 475-479
51. Luchessi, A. D.; Cambiaghi, T. D.; Hirabara, S. M.; Lambertucci, R. H.; Silveira, L. R.; Baptista, I. L.; Moriscot, A. S.; Costa-Neto, C. M.; Curi, R. Involvement of eukaryotic translation initiation factor 5A (eIF5A) in skeletal muscle stem cell differentiation J. Cell. Physiol. 2009, 218 (3) 480-489
52. Balabanov, S.; Gontarewicz, A.; Ziegler, P.; Hartmann, U.; Kammer, W.; Copland, M.; Brassat, U.; Priemer, M.; Hauber, I.; Wilhelm, T.; Schwarz, G.; Kanz, L.; Bokemeyer, C.; Hauber, J.; Holyoake, T. L.; Nordheim, A.; Brummendorf, T. H. Hypusination of eukaryotic initiation factor 5A (eIF5A): a novel therapeutic target in BCR-ABL-positive leukemias identified by a proteomics approach Blood 2007, 109 (4) 1701-11
53. Taylor, C. A.; Sun, Z.; Cliche, D. O.; Ming, H.; Eshaque, B.; Jin, S.; Hopkins, M. T.; Thai, B.; Thompson, J. E. Eukaryotic translation initiation factor 5A induces apoptosis in colon cancer cells and associates with the nucleus in response to tumour necrosis factor alpha signalling Exp. Cell Res. 2007, 313 (3) 437-449
54. Baldassarre, G.; Boccia, A.; Bruni, P.; Sandomenico, C.; Barone, M. V.; Pepe, S.; Angrisano, T.; Belletti, B.; Motti, M. L.; Fusco, A.; Viglietto, G. Retinoic acid induces neuronal differentiation of embryonal carcinoma cells by reducing proteasome-dependent proteolysis of the cyclin-dependent inhibitor p27 Cell Growth Differ. 2000, 11 (10) 517-526