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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

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†Department of Dermatology, ‡Molecular and Environmental Toxicology Center, and §School of Pharmacy, University of Wisconsin, 1300 University Avenue, Madison, Wisconsin 53706, United States
∥ William S. Middleton Memorial VA Hospital, 2500 Overlook Terrace, Madison, Wisconsin 53705, United States
*Tel: (608) 263-5359. Fax: (608) 263-2919. E-mail: [email protected]
Cite this: J. Proteome Res. 2014, 13, 11, 5041–5050
Publication Date (Web):June 2, 2014
https://doi.org/10.1021/pr5002516
Copyright © 2014 American Chemical Society
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Abstract

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Polo-like kinase 1 (Plk1) is a serine/threonine kinase that plays a key role during the cell cycle by regulating mitotic entry, progression, and exit. Plk1 is overexpressed in a variety of human cancers and is essential to sustained oncogenic proliferation, thus making Plk1 an attractive therapeutic target. However, the clinical efficacy of Plk1 inhibition has not emulated the preclinical success, stressing an urgent need for a better understanding of Plk1 signaling. This study addresses that need by utilizing a quantitative proteomics strategy to compare the proteome of BRAFV600E mutant melanoma cells following treatment with the Plk1-specific inhibitor BI 6727. Employing label-free nano-LC–MS/MS technology on a Q-exactive followed by SIEVE processing, we identified more than 20 proteins of interest, many of which have not been previously associated with Plk1 signaling. Here we report the down-regulation of multiple metabolic proteins with an associated decrease in cellular metabolism, as assessed by lactate and NAD levels. Furthermore, we have also identified the down-regulation of multiple proteasomal subunits, resulting in a significant decrease in 20S proteasome activity. Additionally, we have identified a novel association between Plk1 and p53 through heterogeneous ribonucleoprotein C1/C2 (hnRNPC), thus providing valuable insight into Plk1’s role in cancer cell survival.

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Table S1. Complete protein list identified by nonunique peptide hits having a protein ratio of a high confidence level (p < 0.05), showing Swiss-Prot ID, protein description, number of peptides, frames, hits, and normalized ratio. Table S2. Complete protein list identified by unique peptide hits having a protein ratio of a high confidence level (p < 0.05), showing Swiss-Prot ID, protein description, number of peptides, frames, hits and normalized ratio. This material is available free of charge via the Internet at http://pubs.acs.org.

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Cited By

This article is cited by 20 publications.

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  2. Ritin Sharma, Inna Fedorenko, Paige T. Spence, Vernon K. Sondak, Keiran S. M. Smalley, and John M. Koomen . Activity-Based Protein Profiling Shows Heterogeneous Signaling Adaptations to BRAF Inhibition. Journal of Proteome Research 2016, 15 (12) , 4476-4489. https://doi.org/10.1021/acs.jproteome.6b00613
  3. Visith Thongboonkerd , Joshua LaBaer , Gilberto B. Domont . Recent Advances of Proteomics Applied to Human Diseases. Journal of Proteome Research 2014, 13 (11) , 4493-4496. https://doi.org/10.1021/pr501038g
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  10. Melissa J. Wilking-Busch, Mary A. Ndiaye, Xiaoqi Liu, Nihal Ahmad. RNA interference-mediated knockdown of SIRT1 and/or SIRT2 in melanoma: Identification of downstream targets by large-scale proteomics analysis. Journal of Proteomics 2018, 170 , 99-109. https://doi.org/10.1016/j.jprot.2017.09.002
  11. Nana Liu, Min Zheng, Shijie Li, Hui Bai, Zhouying Liu, Cui hong Hou, Shu Zhang, Jielin Pu. Genetic Mechanisms Contribute to the Development of Heart Failure in Patients with Atrioventricular Block and Right Ventricular Apical Pacing. Scientific Reports 2017, 7 (1) https://doi.org/10.1038/s41598-017-11211-2
  12. Irina Alimova, Angela M. Pierce, Peter Harris, Andrew Donson, Diane K. Birks, Eric Prince, Ilango Balakrishnan, Nicholas K. Foreman, Marcel Kool, Lindsey Hoffman, Sujatha Venkataraman, Rajeev Vibhakar. Targeting Polo-like kinase 1 in SMARCB1 deleted atypical teratoid rhabdoid tumor. Oncotarget 2017, 8 (57) , 97290-97303. https://doi.org/10.18632/oncotarget.21932
  13. Rosie Elizabeth Ann Gutteridge, Chandra K. Singh, Mary Ann Ndiaye, Nihal Ahmad. Targeted knockdown of polo-like kinase 1 alters metabolic regulation in melanoma. Cancer Letters 2017, 394 , 13-21. https://doi.org/10.1016/j.canlet.2017.02.013
  14. Zhixian Liu, Qingrong Sun, Xiaosheng Wang. PLK1, A Potential Target for Cancer Therapy. Translational Oncology 2017, 10 (1) , 22-32. https://doi.org/10.1016/j.tranon.2016.10.003
  15. J. Van den Bossche, F. Lardon, V. Deschoolmeester, I. De Pauw, J.B. Vermorken, P. Specenier, P. Pauwels, M. Peeters, A. Wouters. Spotlight on Volasertib: Preclinical and Clinical Evaluation of a Promising Plk1 Inhibitor. Medicinal Research Reviews 2016, 36 (4) , 749-786. https://doi.org/10.1002/med.21392
  16. Ha Linh Vu, Andrew E. Aplin. Targeting mutant NRAS signaling pathways in melanoma. Pharmacological Research 2016, 107 , 111-116. https://doi.org/10.1016/j.phrs.2016.03.007
  17. Eric Pujade-Lauraine, Frédéric Selle, Béatrice Weber, Isabelle-Laure Ray-Coquard, Ignace Vergote, Jozef Sufliarsky, Josep Maria Del Campo, Alain Lortholary, Anne Lesoin, Philippe Follana, Gilles Freyer, Beatriz Pardo, Laura Vidal, Bengt Tholander, Laurence Gladieff, Mouna Sassi, Pilar Garin-Chesa, Serge Nazabadioko, Kristell Marzin, Korinna Pilz, Florence Joly. Volasertib Versus Chemotherapy in Platinum-Resistant or -Refractory Ovarian Cancer: A Randomized Phase II Groupe des Investigateurs Nationaux pour l'Etude des Cancers de l'Ovaire Study. Journal of Clinical Oncology 2016, 34 (7) , 706-713. https://doi.org/10.1200/JCO.2015.62.1474
  18. CHUN XU, SEN LI, TENGFEI CHEN, HAIBO HU, CHENG DING, ZHENLEI XU, JUN CHEN, ZEYI LIU, ZHE LEI, HONG-TAO ZHANG, CHANG LI, JUN ZHAO. miR-296-5p suppresses cell viability by directly targeting PLK1 in non-small cell lung cancer. Oncology Reports 2016, 35 (1) , 497-503. https://doi.org/10.3892/or.2015.4392
  19. Christian Posch, Brian D. Cholewa, Igor Vujic, Martina Sanlorenzo, Jeffrey Ma, Sarasa T. Kim, Sonja Kleffel, Tobias Schatton, Klemens Rappersberger, Rosie Gutteridge, Nihal Ahmad, Susana Ortiz-Urda. Combined Inhibition of MEK and Plk1 Has Synergistic Antitumor Activity in NRAS Mutant Melanoma. Journal of Investigative Dermatology 2015, 135 (10) , 2475-2483. https://doi.org/10.1038/jid.2015.198
  20. Jun Yu, Jamie Wilson, Linda Taylor, Peter Polgar. DNA Microarray and Signal Transduction Analysis in Pulmonary Artery Smooth Muscle Cells From Heritable and Idiopathic Pulmonary Arterial Hypertension Subjects. Journal of Cellular Biochemistry 2015, 116 (3) , 386-397. https://doi.org/10.1002/jcb.24987

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