Large-scale label-free comparative proteomics analysis of polo-like kinase 1 inhibition via the small-molecule inhibitor BI 6727 (volasertib) in BRAFV600E mutant melanoma cells

Journal of Proteome Research

Volumn 13, Issue 11, 2014, Pages 5041-5050

  Cholewa, Brian D ^a   Pellitteri Hahn, Molly C ^a   Scarlett, Cameron O ^a   Ahmad, Nihal ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

BI 6727; glycolysis; hnRNPC; LDHA; melanoma; p53; Plk1; polo like kinase 1; proteasome; proteomics

Indexed keywords

ASPARTATE AMINOTRANSFERASE ISOENZYME 2; GLUCOSE 6 PHOSPHATE ISOMERASE; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE A; LACTATE DEHYDROGENASE B; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE 1; POLO LIKE KINASE 1; RIBONUCLEOPROTEIN; TRANSKETOLASE; UNCLASSIFIED DRUG; VOLASERTIB; B RAF KINASE; BRAF PROTEIN, HUMAN; CELL CYCLE PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; HNRNPC PROTEIN, HUMAN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEASOME; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; PTERIDINE DERIVATIVE;

AREA UNDER THE CURVE; ARTICLE; CELL LYSATE; CELL METABOLISM; CELL POPULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MELANOMA CELL; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN UNFOLDING; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; ANTAGONISTS AND INHIBITORS; COMPARATIVE STUDY; DRUG EFFECTS; GENETICS; MELANOMA; METABOLISM; MUTATION; PATHOLOGY; PROCEDURES; SKIN NEOPLASMS; TUMOR CELL LINE;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP C; HUMANS; MELANOMA; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; PTERIDINES; SKIN NEOPLASMS; TANDEM MASS SPECTROMETRY;

EID: 84908892143     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5002516     Document Type: Article

References (61)

1. Sumara, I.; Gimenez-Abian, J. F.; Gerlich, D.; Hirota, T.; Kraft, C.; de la Torre, C.; Ellenberg, J.; Peters, J. M. Roles of polo-like kinase 1 in the assembly of functional mitotic spindles Curr. Biol. 2004, 14 (19) 1712-1722
2. Lane, H. A.; Nigg, E. A. Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes J. Cell Biol. 1996, 135 (6 Pt 2) 1701-1713
3. Seong, Y. S.; Kamijo, K.; Lee, J. S.; Fernandez, E.; Kuriyama, R.; Miki, T.; Lee, K. S. A spindle checkpoint arrest and a cytokinesis failure by the dominant-negative polo-box domain of Plk1 in U-2 OS cells J. Biol. Chem. 2002, 277 (35) 32282-32293
4. van Vugt, M. A.; van de Weerdt, B. C.; Vader, G.; Janssen, H.; Calafat, J.; Klompmaker, R.; Wolthuis, R. M.; Medema, R. H. Polo-like kinase-1 is required for bipolar spindle formation but is dispensable for anaphase promoting complex/Cdc20 activation and initiation of cytokinesis J. Biol. Chem. 2004, 279 (35) 36841-36854
5. Gray, P. J., Jr.; Bearss, D. J.; Han, H.; Nagle, R.; Tsao, M. S.; Dean, N.; Von Hoff, D. D. Identification of human polo-like kinase 1 as a potential therapeutic target in pancreatic cancer Mol. Cancer Ther. 2004, 3 (5) 641-646
6. Knecht, R.; Elez, R.; Oechler, M.; Solbach, C.; von Ilberg, C.; Strebhardt, K. Prognostic significance of polo-like kinase (PLK) expression in squamous cell carcinomas of the head and neck Cancer Res. 1999, 59 (12) 2794-2797
7. Mito, K.; Kashima, K.; Kikuchi, H.; Daa, T.; Nakayama, I.; Yokoyama, S. Expression of Polo-Like Kinase (PLK1) in non-Hodgkins lymphomas Leuk. Lymphoma 2005, 46 (2) 225-231
8. Salvatore, G.; Nappi, T. C.; Salerno, P.; Jiang, Y.; Garbi, C.; Ugolini, C.; Miccoli, P.; Basolo, F.; Castellone, M. D.; Cirafici, A. M.; Melillo, R. M.; Fusco, A.; Bittner, M. L.; Santoro, M. A cell proliferation and chromosomal instability signature in anaplastic thyroid carcinoma Cancer Res. 2007, 67 (21) 10148-10158
9. Schmit, T. L.; Zhong, W.; Setaluri, V.; Spiegelman, V. S.; Ahmad, N. Targeted depletion of Polo-like kinase (Plk) 1 through lentiviral shRNA or a small-molecule inhibitor causes mitotic catastrophe and induction of apoptosis in human melanoma cells J. Invest. Dermatol. 2009, 129 (12) 2843-2853
10. Takahashi, T.; Sano, B.; Nagata, T.; Kato, H.; Sugiyama, Y.; Kunieda, K.; Kimura, M.; Okano, Y.; Saji, S. Polo-like kinase 1 (PLK1) is overexpressed in primary colorectal cancers Cancer Sci. 2003, 94 (2) 148-152
11. Wolf, G.; Elez, R.; Doermer, A.; Holtrich, U.; Ackermann, H.; Stutte, H. J.; Altmannsberger, H. M.; Rubsamen-Waigmann, H.; Strebhardt, K. Prognostic significance of polo-like kinase (PLK) expression in non-small cell lung cancer Oncogene 1997, 14 (5) 543-549
12. Wolf, G.; Hildenbrand, R.; Schwar, C.; Grobholz, R.; Kaufmann, M.; Stutte, H. J.; Strebhardt, K.; Bleyl, U. Polo-like kinase: a novel marker of proliferation: correlation with estrogen-receptor expression in human breast cancer Pathol. Res. Pract. 2000, 196 (11) 753-759
13. Weichert, W.; Denkert, C.; Schmidt, M.; Gekeler, V.; Wolf, G.; Kobel, M.; Dietel, M.; Hauptmann, S. Polo-like kinase isoform expression is a prognostic factor in ovarian carcinoma Br. J. Cancer. 2004, 90 (4) 815-821
14. Strebhardt, K.; Kneisel, L.; Linhart, C.; Bernd, A.; Kaufmann, R. Prognostic value of pololike kinase expression in melanomas JAMA, J. Am. Med. Assoc. 2000, 283 (4) 479-480
15. Weichert, W.; Schmidt, M.; Gekeler, V.; Denkert, C.; Stephan, C.; Jung, K.; Loening, S.; Dietel, M.; Kristiansen, G. Polo-like kinase 1 is overexpressed in prostate cancer and linked to higher tumor grades Prostate 2004, 60 (3) 240-245
16. Hikichi, Y.; Honda, K.; Hikami, K.; Miyashita, H.; Kaieda, I.; Murai, S.; Uchiyama, N.; Hasegawa, M.; Kawamoto, T.; Sato, T.; Ichikawa, T.; Cao, S.; Nie, Z.; Zhang, L.; Yang, J.; Kuida, K.; Kupperman, E. TAK-960, a novel, orally available, selective inhibitor of polo-like kinase 1, shows broad-spectrum preclinical antitumor activity in multiple dosing regimens Mol. Cancer Ther. 2012, 11 (3) 700-709
17. Mross, K.; Frost, A.; Steinbild, S.; Hedbom, S.; Rentschler, J.; Kaiser, R.; Rouyrre, N.; Trommeshauser, D.; Hoesl, C. E.; Munzert, G. Phase I dose escalation and pharmacokinetic study of BI 2536, a novel Polo-like kinase 1 inhibitor, in patients with advanced solid tumors J. Clin. Oncol. 2008, 26 (34) 5511-5517
18. Jimeno, A.; Li, J.; Messersmith, W. A.; Laheru, D.; Rudek, M. A.; Maniar, M.; Hidalgo, M.; Baker, S. D.; Donehower, R. C. Phase I study of ON 01910.Na, a novel modulator of the Polo-like kinase 1 pathway, in adult patients with solid tumors J. Clin. Oncol. 2008, 26 (34) 5504-5510
19. Schoffski, P.; Awada, A.; Dumez, H.; Gil, T.; Bartholomeus, S.; Wolter, P.; Taton, M.; Fritsch, H.; Glomb, P.; Munzert, G. A phase I, dose-escalation study of the novel Polo-like kinase inhibitor volasertib (BI 6727) in patients with advanced solid tumours Eur. J. Cancer 2012, 48 (2) 179-186
20. Olmos, D.; Barker, D.; Sharma, R.; Brunetto, A. T.; Yap, T. A.; Taegtmeyer, A. B.; Barriuso, J.; Medani, H.; Degenhardt, Y. Y.; Allred, A. J.; Smith, D. A.; Murray, S. C.; Lampkin, T. A.; Dar, M. M.; Wilson, R.; de Bono, J. S.; Blagden, S. P. Phase I study of GSK461364, a specific and competitive Polo-like kinase 1 inhibitor, in patients with advanced solid malignancies Clin. Cancer. Res. 2011, 17 (10) 3420-3430
21. Ma, W. W.; Messersmith, W. A.; Dy, G. K.; Weekes, C. D.; Whitworth, A.; Ren, C.; Maniar, M.; Wilhelm, F.; Eckhardt, S. G.; Adjei, A. A.; Jimeno, A. Phase I study of Rigosertib, an inhibitor of the phosphatidylinositol 3-kinase and Polo-like kinase 1 pathways, combined with gemcitabine in patients with solid tumors and pancreatic cancer Clin. Cancer. Res. 2012, 18 (7) 2048-2055
22. Rudolph, D.; Steegmaier, M.; Hoffmann, M.; Grauert, M.; Baum, A.; Quant, J.; Haslinger, C.; Garin-Chesa, P.; Adolf, G. R. BI 6727, a Polo-like kinase inhibitor with improved pharmacokinetic profile and broad antitumor activity Clin. Cancer. Res. 2009, 15 (9) 3094-3102
23. Davies, H.; Bignell, G. R.; Cox, C.; Stephens, P.; Edkins, S.; Clegg, S.; Teague, J.; Woffendin, H.; Garnett, M. J.; Bottomley, W.; Davis, N.; Dicks, E.; Ewing, R.; Floyd, Y.; Gray, K.; Hall, S.; Hawes, R.; Hughes, J.; Kosmidou, V.; Menzies, A.; Mould, C.; Parker, A.; Stevens, C.; Watt, S.; Hooper, S.; Wilson, R.; Jayatilake, H.; Gusterson, B. A.; Cooper, C.; Shipley, J.; Hargrave, D.; Pritchard-Jones, K.; Maitland, N.; Chenevix-Trench, G.; Riggins, G. J.; Bigner, D. D.; Palmieri, G.; Cossu, A.; Flanagan, A.; Nicholson, A.; Ho, J. W.; Leung, S. Y.; Yuen, S. T.; Weber, B. L.; Seigler, H. F.; Darrow, T. L.; Paterson, H.; Marais, R.; Marshall, C. J.; Wooster, R.; Stratton, M. R.; Futreal, P. A. Mutations of the BRAF gene in human cancer Nature 2002, 417 (6892) 949-954
24. Spandidos, A.; Wang, X.; Wang, H.; Seed, B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification Nucleic Acids Res. 2010, 38 (Database issue) D792-D799
25. Neilson, K. A.; Ali, N. A.; Muralidharan, S.; Mirzaei, M.; Mariani, M.; Assadourian, G.; Lee, A.; van Sluyter, S. C.; Haynes, P. A. Less label, more free: approaches in label-free quantitative mass spectrometry Proteomics 2011, 11 (4) 535-553
26. Old, W. M.; Meyer-Arendt, K.; Aveline-Wolf, L.; Pierce, K. G.; Mendoza, A.; Sevinsky, J. R.; Resing, K. A.; Ahn, N. G. Comparison of label-free methods for quantifying human proteins by shotgun proteomics Mol. Cell. Proteomics 2005, 4 (10) 1487-1502
27. Zhu, W.; Smith, J. W.; Huang, C. M. Mass spectrometry-based label-free quantitative proteomics J. Biomed. Biotechnol. 2010, 2010, 840518
28. Fedorova, G.; Randak, T.; Lindberg, R. H.; Grabic, R. Comparison of the quantitative performance of a Q-Exactive high-resolution mass spectrometer with that of a triple quadrupole tandem mass spectrometer for the analysis of illicit drugs in wastewater Rapid. Commun. Mass. Sp. 2013, 27 (15) 1751-1762
29. Jones, K. A.; Kim, P. D.; Patel, B. B.; Kelsen, S. G.; Braverman, A.; Swinton, D. J.; Gafken, P. R.; Jones, L. A.; Lane, W. S.; Neveu, J. M.; Leung, H. C.; Shaffer, S. A.; Leszyk, J. D.; Stanley, B. A.; Fox, T. E.; Stanley, A.; Hall, M. J.; Hampel, H.; South, C. D.; de la Chapelle, A.; Burt, R. W.; Jones, D. A.; Kopelovich, L.; Yeung, A. T. Immunodepletion plasma proteomics by tripleTOF 5600 and Orbitrap elite/LTQ-Orbitrap Velos/Q exactive mass spectrometers J. Proteome Res. 2013, 12 (10) 4351-4365
30. Oppermann, F. S.; Klammer, M.; Bobe, C.; Cox, J.; Schaab, C.; Tebbe, A.; Daub, H. Comparison of SILAC and mTRAQ quantification for phosphoproteomics on a quadrupole orbitrap mass spectrometer J. Proteome Res. 2013, 12 (9) 4089-4100
31. Gamez-Pozo, A.; Sanchez-Navarro, I.; Calvo, E.; Agullo-Ortuno, M. T.; Lopez-Vacas, R.; Diaz, E.; Camafeita, E.; Nistal, M.; Madero, R.; Espinosa, E.; Lopez, J. A.; Fresno Vara, J. A. PTRF/cavin-1 and MIF proteins are identified as non-small cell lung cancer biomarkers by label-free proteomics PLoS One 2012, 7 (3) e33752
32. Guillaume, E.; Berger, B.; Affolter, M.; Kussmann, M. Label-free quantitative proteomics of two Bifidobacterium longum strains J. Proteomics 2009, 72 (5) 771-784
33. Lopez, M. F.; Sarracino, D. A.; Vogelsang, M.; Sutton, J. N.; Athanas, M.; Krastins, B.; Garces, A.; Prakash, A.; Peterman, S.; Demirjian, Z.; Inglessis-Azuaje, I.; Feeney, K.; Elia, M.; McMullin, D.; Dec, G. W.; Palacios, I.; Lo, E. H.; Buonanno, F.; Ning, M. Heart-brain signaling in patent foramen ovale-related stroke: differential plasma proteomic expression patterns revealed with a 2-pass liquid chromatography-tandem mass spectrometry discovery workflow J. Invest. Med. 2012, 60 (8) 1122-1130
34. Qu, J.; Lesse, A. J.; Brauer, A. L.; Cao, J.; Gill, S. R.; Murphy, T. F. Proteomic expression profiling of Haemophilus influenzae grown in pooled human sputum from adults with chronic obstructive pulmonary disease reveal antioxidant and stress responses BMC Microbiol. 2010, 10, 162
35. Sutton, J.; Richmond, T.; Shi, X.; Athanas, M.; Ptak, C.; Gerszten, R.; Bonilla, L. Performance characteristics of an FT MS-based workflow for label-free differential MS analysis of human plasma: standards, reproducibility, targeted feature investigation, and application to a model of controlled myocardial infarction Proteomics: Clin. Appl. 2008, 2 (6) 862-881
36. Tabata, T.; Sato, T.; Kuromitsu, J.; Oda, Y. Pseudo internal standard approach for label-free quantitative proteomics Anal. Chem. 2007, 79 (22) 8440-8445
37. Nilsson, T.; Mann, M.; Aebersold, R.; Yates, J. R., 3rd; Bairoch, A.; Bergeron, J. J. Mass spectrometry in high-throughput proteomics: ready for the big time Nat. Methods 2010, 7 (9) 681-685
38. Koppenol, W. H.; Bounds, P. L.; Dang, C. V. Otto Warburgs contributions to current concepts of cancer metabolism Nat. Rev. Cancer 2011, 11 (5) 325-337
39. Lin, S. J.; Guarente, L. Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease Curr. Opin. Cell Biol. 2003, 15 (2) 241-246
40. Sun, F.; Dai, C.; Xie, J.; Hu, X. Biochemical issues in estimation of cytosolic free NAD/NADH ratio PLoS One 2012, 7 (5) e34525
41. Zheng, J. Energy metabolism of cancer: Glycolysis versus oxidative phosphorylation (Review) Oncol. Lett. 2012, 4 (6) 1151-1157
42. Liu, X. S.; Li, H.; Song, B.; Liu, X. Polo-like kinase 1 phosphorylation of G2 and S-phase-expressed 1 protein is essential for p53 inactivation during G2 checkpoint recovery EMBO Rep. 2010, 11 (8) 626-632
43. Liu, X. S.; Song, B.; Elzey, B. D.; Ratliff, T. L.; Konieczny, S. F.; Cheng, L.; Ahmad, N.; Liu, X. Polo-like kinase 1 facilitates loss of PTEN tumor suppressor-induced prostate cancer formation J. Biol. Chem. 2011, 286 (41) 35795-35800
44. Padmanabhan, A.; Li, X.; Bieberich, C. J. Protein Kinase A Regulates MYC Protein through Transcriptional and Post-translational Mechanisms in a Catalytic Subunit Isoform-specific Manner J. Biol. Chem. 2013, 288 (20) 14158-14169
45. Song, M. S.; Salmena, L.; Pandolfi, P. P. The functions and regulation of the PTEN tumour suppressor Nat. Rev. Mol. Cell. Biol. 2012, 13 (5) 283-296
46. Tan, J.; Li, Z.; Lee, P. L.; Guan, P.; Aau, M. Y.; Lee, S. T.; Feng, M.; Lim, C. Z.; Lee, E. Y.; Wee, Z. N.; Lim, Y. C.; Karuturi, R. K.; Yu, Q. PDK1 signaling toward PLK1-MYC activation confers oncogenic transformation, tumor-initiating cell activation, and resistance to mTOR-targeted therapy Cancer Discovery 2013, 3 (10) 1156-1171
47. Shen, M.; Schmitt, S.; Buac, D.; Dou, Q. P. Targeting the ubiquitin-proteasome system for cancer therapy Expert Opin. Ther. Targets 2013, 17 (9) 1091-1108
48. Sahara, K.; Kogleck, L.; Yashiroda, H.; Murata, S. The mechanism for molecular assembly of the proteasome Adv. Biol. Regul. 2014, 54C, 51-58
49. Ando, K.; Ozaki, T.; Yamamoto, H.; Furuya, K.; Hosoda, M.; Hayashi, S.; Fukuzawa, M.; Nakagawara, A. Polo-like kinase 1 (Plk1) inhibits p53 function by physical interaction and phosphorylation J. Biol. Chem. 2004, 279 (24) 25549-26661
50. Bhat, U. G.; Halasi, M.; Gartel, A. L. FoxM1 is a general target for proteasome inhibitors PLoS One 2009, 4 (8) e6593
51. Dias, S. S.; Hogan, C.; Ochocka, A. M.; Meek, D. W. Polo-like kinase-1 phosphorylates MDM2 at Ser260 and stimulates MDM2-mediated p53 turnover FEBS Lett. 2009, 583 (22) 3543-3548
52. Fu, Z.; Malureanu, L.; Huang, J.; Wang, W.; Li, H.; van Deursen, J. M.; Tindall, D. J.; Chen, J. Plk1-dependent phosphorylation of FoxM1 regulates a transcriptional programme required for mitotic progression Nat. Cell Biol. 2008, 10 (9) 1076-1082
53. McKenzie, L.; King, S.; Marcar, L.; Nicol, S.; Dias, S. S.; Schumm, K.; Robertson, P.; Bourdon, J. C.; Perkins, N.; Fuller-Pace, F.; Meek, D. W. p53-dependent repression of polo-like kinase-1 (PLK1) Cell Cycle 2010, 9 (20) 4200-4212
54. Michael, D.; Oren, M. The p53-Mdm2 module and the ubiquitin system Semin. Cancer Biol. 2003, 13 (1) 49-58
55. Wierstra, I. FOXM1 (Forkhead box M1) in tumorigenesis: overexpression in human cancer, implication in tumorigenesis, oncogenic functions, tumor-suppressive properties, and target of anticancer therapy Adv. Cancer Res. 2013, 119, 191-419
56. Yang, X.; Li, H.; Zhou, Z.; Wang, W. H.; Deng, A.; Andrisani, O.; Liu, X. Plk1-mediated phosphorylation of Topors regulates p53 stability J. Biol. Chem. 2009, 284 (28) 18588-18592
57. Cholewa, B. D.; Liu, X.; Ahmad, N. The role of polo-like kinase 1 in carcinogenesis: cause or consequence? Cancer Res. 2013, 73 (23) 6848-6855
58. Burd, C. G.; Swanson, M. S.; Gorlach, M.; Dreyfuss, G. Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: a diversity of RNA binding proteins is generated by small peptide inserts Proc. Natl. Acad. Sci. U. S. A. 1989, 86 (24) 9788-9792
59. Krecic, A. M.; Swanson, M. S. hnRNP complexes: composition, structure, and function Curr. Opin. Cell Biol. 1999, 11 (3) 363-371
60. Sun, D. Q.; Wang, Y.; Liu, D. G. Overexpression of hnRNPC2 induces multinucleation by repression of Aurora B in hepatocellular carcinoma cells Oncol. Lett. 2013, 5 (4) 1243-1249
61. Christian, K. J.; Lang, M. A.; Raffalli-Mathieu, F. Interaction of heterogeneous nuclear ribonucleoprotein C1/C2 with a novel cis-regulatory element within p53 mRNA as a response to cytostatic drug treatment Mol. Pharmacol. 2008, 73 (5) 1558-1567