Elevated AKAP12 in paclitaxel-resistant serous ovarian cancer cells is prognostic and predictive of poor survival in patients

Journal of Proteome Research

Volumn 14, Issue 4, 2015, Pages 1900-1910

  Bateman, Nicholas W ^a   Jaworski, Elizabeth ^a   Ao, Wei ^a   Wang, Guisong ^a   Litzi, Tracy ^a   Dubil, Elizabeth ^a,b   Marcus, Charlotte ^a,b   Conrads, Kelly A ^a   Teng, Pang Ning ^a   Hood, Brian L ^a   Phippen, Neil T ^a,b   Vasicek, Lisa A ^a   McGuire, William P ^c   Paz, Keren ^d   Sidransky, David ^e   Hamilton, Chad A ^a,b   Maxwell, G Larry ^a,f   Darcy, Kathleen M ^a   Conrads, Thomas P ^a  

^a BETTY AND GUY BEATTY CENTER FOR INTEGRATED RESEARCH   (United States)

^b WALTER REED ARMY MEDICAL CENTER   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Champions Oncology Inc   (United States)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f INOVA FAIRFAX HOSPITAL   (United States)

Author keywords

AKAP12; Ovarian cancer; paclitaxel resistance; proteomics; secretome

Indexed keywords

AKAP12 PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; PACLITAXEL; UNCLASSIFIED DRUG; AKAP12 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER SURVIVAL; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MAJOR CLINICAL STUDY; OVARIAN CANCER CELL LINE; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEOMICS; SEROUS OVARIAN CANCER; COHORT ANALYSIS; DNA METHYLATION; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OUTCOME ASSESSMENT; OVARIAN NEOPLASMS; PHYSIOLOGY; PROCEDURES; PROGNOSIS; VALIDATION STUDY;

A KINASE ANCHOR PROTEINS; CELL CYCLE PROTEINS; COHORT STUDIES; DNA METHYLATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; OVARIAN NEOPLASMS; PACLITAXEL; PATIENT OUTCOME ASSESSMENT; PROGNOSIS; PROTEOMICS;

EID: 84926443630     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5012894     Document Type: Article

References (51)

1. A Snapshot of Ovarian Cancer; National Cancer Institute: Bethesda, MD, 2013.
2. Statistics; Ovarian Cancer National Alliance: Washington, DC; http://www.ovariancancer.org/about/statistics/.
3. SEER Cancer Statistics Factsheets: Ovary Cancer; National Cancer Institute: Bethesda, MD; http://seer.cancer.gov/statfacts/html/ovary.html.
4. McGuire, W. P.; Hoskins, W. J.; Brady, M. F.; Kucera, P. R.; Partridge, E. E.; Look, K. Y.; Clarke-Pearson, D. L.; Davidson, M. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer N. Engl. J. Med. 1996, 334, 1-6
5. Agarwal, R.; Kaye, S. B. Ovarian cancer: strategies for overcoming resistance to chemotherapy Nat. Rev. Cancer 2003, 3, 502-16
6. Sung, M.; Giannakakou, P. BRCA1 regulates microtubule dynamics and taxane-induced apoptotic cell signaling Oncogene 2014, 33, 1418-28
7. Misiukiewicz, K.; Gupta, V.; Bakst, R.; Posner, M. Taxanes in cancer of the head and neck Anticancer Drugs. 2014, 25, 561-70
8. Schiff, P. B.; Fant, J.; Horwitz, S. B. Promotion of microtubule assembly in vitro by taxol Nature 1979, 277, 665-7
9. Arnal, I.; Wade, R. H. How does taxol stabilize microtubules? Curr. Biol. 1995, 5, 900-8
10. Zasadil, L. M.; Andersen, K. A.; Yeum, D.; Rocque, G. B.; Wilke, L. G.; Tevaarwerk, A. J.; Raines, R. T.; Burkard, M. E.; Weaver, B. A. Cytotoxicity of paclitaxel in breast cancer is due to chromosome missegregation on multipolar spindles Sci. Transl. Med. 2014, 6, 229ra43
11. Bani, M. R.; Nicoletti, M. I.; Alkharouf, N. W.; Ghilardi, C.; Petersen, D.; Erba, E.; Sausville, E. A.; Liu, E. T.; Giavazzi, R. Gene expression correlating with response to paclitaxel in ovarian carcinoma xenografts Mol. Cancer Ther. 2004, 3, 111-21
12. Kumar, S.; Mahdi, H.; Bryant, C.; Shah, J. P.; Garg, G.; Munkarah, A. Clinical trials and progress with paclitaxel in ovarian cancer Int. J. Womens Health 2010, 2, 411-27
13. Landen, C. N., Jr.; Goodman, B.; Katre, A. A.; Steg, A. D.; Nick, A. M.; Stone, R. L.; Miller, L. D.; Mejia, P. V.; Jennings, N. B.; Gershenson, D. M.; Bast, R. C., Jr.; Coleman, R. L.; Lopez-Berestein, G.; Sood, A. K. Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer Mol. Cancer Ther. 2010, 9, 3186-99
14. Goto, T.; Takano, M.; Sakamoto, M.; Kondo, A.; Hirata, J.; Kita, T.; Tsuda, H.; Tenjin, Y.; Kikuchi, Y. Gene expression profiles with cDNA microarray reveal RhoGDI as a predictive marker for paclitaxel resistance in ovarian cancers Oncol. Rep. 2006, 15, 1265-71
15. Lee, D. H.; Chung, K.; Song, J. A.; Kim, T. H.; Kang, H.; Huh, J. H.; Jung, S. G.; Ko, J. J.; An, H. J. Proteomic identification of paclitaxel-resistance associated hnRNP A2 and GDI 2 proteins in human ovarian cancer cells J. Proteome Res. 2010, 9, 5668-76
16. Cicchillitti, L.; Di Michele, M.; Urbani, A.; Ferlini, C.; Donat, M. B.; Scambia, G.; Rotilio, D. Comparative proteomic analysis of paclitaxel sensitive A2780 epithelial ovarian cancer cell line and its resistant counterpart A2780TC1 by 2D-DIGE: the role of ERp57 J. Proteome Res. 2009, 8, 1902-12
17. Zhang, F. F.; Zhu, Y. F.; Zhao, Q. N.; Yang, D. T.; Dong, Y. P.; Jiang, L.; Xing, W. X.; Li, X. Y.; Xing, H.; Shi, M.; Chen, Y.; Bruce, I. C.; Jin, J.; Ma, X. Microvesicles mediate transfer of P-glycoprotein to paclitaxel-sensitive A2780 human ovarian cancer cells, conferring paclitaxel-resistance Eur. J. Pharmacol. 2014, 738, 83-90
18. Domcke, S.; Sinha, R.; Levine, D. A.; Sander, C.; Schultz, N. Evaluating cell lines as tumour models by comparison of genomic profiles Nat. Commun. 2013, 4, 2126
19. Teng, P. N.; Wang, G.; Hood, B. L.; Conrads, K. A.; Hamilton, C. A.; Maxwell, G. L.; Darcy, K. M.; Conrads, T. P. Identification of candidate circulating cisplatin-resistant biomarkers from epithelial ovarian carcinoma cell secretomes Br J. Cancer 2014, 110, 123-32
20. Bateman, N. W.; Sun, M.; Hood, B. L.; Flint, M. S.; Conrads, T. P. Defining central themes in breast cancer biology by differential proteomics: conserved regulation of cell spreading and focal adhesion kinase J. Proteome Res. 2010, 9, 5311-24
21. McDonald, J. H. Handbook of Biological Statistics; Sparky House Publishing: Baltimore, MD, 2009; pp 160-4.
22. Storey, J. D.; Tibshirani, R. Statistical significance for genomewide studies Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9440-5
23. Bonome, T.; Levine, D. A.; Shih, J.; Randonovich, M.; Pise-Masison, C. A.; Bogomolniy, F.; Ozbun, L.; Brady, J.; Barrett, J. C.; Boyd, J.; Birrer, M. J. A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer Cancer Res. 2008, 68, 5478-86
24. Denkert, C.; Budczies, J.; Darb-Esfahani, S.; Gyorffy, B.; Sehouli, J.; Konsgen, D.; Zeillinger, R.; Weichert, W.; Noske, A.; Buckendahl, A.-C.; Muller, B. M.; Dietel, M.; Lage, H. A prognostic gene expression index in ovarian cancer-validation across different independent data sets J. Pathol. 2009, 218, 273-80
25. Dressman, H. K.; Berchuck, A.; Chan, G.; Zhai, J.; Bild, A.; Sayer, R.; Cragun, J.; Clarke, J.; Whitaker, R. S.; Li, L.; Gray, J.; Marks, J.; Ginsburg, G. S.; Potti, A.; West, M.; Nevins, J. R.; Lancaster, J. M. An integrated genomic-based approach to individualized treatment of patients with advanced-stage ovarian cancer J. Clin Oncol. 2007, 25, 517-25
26. Mok, S. C.; Bonome, T.; Vathipadiekal, V.; Bell, A.; Johnson, M. E.; Wong, K.-k.; Park, D.-C.; Hao, K.; Yip, D. K. P.; Donninger, H.; Ozbun, L.; Samimi, G.; Brady, J.; Randonovich, M.; Pise-Masison, C. A.; Barrett, J. C.; Wong, W. H.; Welch, W. R.; Berkowitz, R. S.; Birrer, M. J. A gene signature predictive for outcome in advanced ovarian cancer identifies a survival factor: microfibril-associated glycoprotein 2 Cancer Cell 2009, 16, 521-32
27. Tothill, R. W.; Tinker, A. V.; George, J.; Brown, R.; Fox, S. B.; Lade, S.; Johnson, D. S.; Trivett, M. K.; Etemadmoghadam, D.; Locandro, B.; Traficante, N.; Fereday, S.; Hung, J. A.; Chiew, Y.-E.; Haviv, I.; Gertig, D.; DeFazio, A.; Bowtell, D. D. L. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome Clin. Cancer Res. 2008, 14, 5198-208
28. Cancer Genome Atlas Research Network Integrated genomic analyses of ovarian carcinoma Nature 2011, 474, 609-15
29. Crijns, A. P. G.; Fehrmann, R. S. N.; de Jong, S.; Gerbens, F.; Meersma, G. J.; Klip, H. G.; Hollema, H.; Hofstra, R. M. W.; te Meerman, G. J.; de Vries, E. G. E.; van der Zee, A. G. J. Survival-related profile, pathways, and transcription factors in ovarian cancer. PLoS Med. 2009, 6.
30. Yoshihara, K.; Tsunoda, T.; Shigemizu, D.; Fujiwara, H.; Hatae, M.; Fujiwara, H.; Masuzaki, H.; Katabuchi, H.; Kawakami, Y.; Okamoto, A.; Nogawa, T.; Matsumura, N.; Udagawa, Y.; Saito, T.; Itamochi, H.; Takano, M.; Miyagi, E.; Sudo, T.; Ushijima, K.; Iwase, H.; Seki, H.; Terao, Y.; Enomoto, T.; Mikami, M.; Akazawa, K.; Tsuda, H.; Moriya, T.; Tajima, A.; Inoue, I.; Tanaka, K.; Japanese Serous Ovarian Cancer Study Group High-risk ovarian cancer based on 126-gene expression signature is uniquely characterized by downregulation of antigen presentation pathway Clin. Cancer Res. 2012, 18, 1374-85
31. Ganzfried, B. F.; Riester, M.; Haibe-Kains, B.; Risch, T.; Tyekucheva, S.; Jazic, I.; Wang, X. V.; Ahmadifar, M.; Birrer, M. J.; Parmigiani, G.; Huttenhower, C.; Waldron, L. curatedOvarianData: clinically annotated data for the ovarian cancer transcriptome Database 2013, 2013, bat013
32. Lin, X.; Gelman, I. H. Reexpression of the major protein kinase C substrate, SSeCKS, suppresses v-src-induced morphological transformation and tumorigenesis Cancer Res. 1997, 57, 2304-12
33. Gelman, I. H. Emerging roles for SSeCKS/Gravin/AKAP12 in the control of cell proliferation, cancer malignancy, and barriergenesis Genes Cancer 2010, 1, 1147-56
34. Liu, X.; Valentine, S. J.; Plasencia, M. D.; Trimpin, S.; Naylor, S.; Clemmer, D. E. Mapping the human plasma proteome by SCX-LC-IMS-MS J. Am. Soc. Mass Spectrom. 2007, 18, 1249-64
35. Nanjappa, V.; Thomas, J. K.; Marimuthu, A.; Muthusamy, B.; Radhakrishnan, A.; Sharma, R.; Ahmad Khan, A.; Balakrishnan, L.; Sahasrabuddhe, N. A.; Kumar, S.; Jhaveri, B. N.; Sheth, K. V.; Kumar Khatana, R.; Shaw, P. G.; Srikanth, S. M.; Mathur, P. P.; Shankar, S.; Nagaraja, D.; Christopher, R.; Mathivanan, S.; Raju, R.; Sirdeshmukh, R.; Chatterjee, A.; Simpson, R. J.; Harsha, H. C.; Pandey, A.; Prasad, T. S. Plasma Proteome Database as a resource for proteomics research: 2014 update Nucleic Acids Res. 2014, 42, D959-65
36. Barnea, E.; Sorkin, R.; Ziv, T.; Beer, I.; Admon, A. Evaluation of prefractionation methods as a preparatory step for multidimensional based chromatography of serum proteins Proteomics 2005, 5, 3367-75
37. Farrah, T.; Deutsch, E. W.; Omenn, G. S.; Campbell, D. S.; Sun, Z.; Bletz, J. A.; Mallick, P.; Katz, J. E.; Malmstrom, J.; Ossola, R.; Watts, J. D.; Lin, B.; Zhang, H.; Moritz, R. L.; Aebersold, R. A high-confidence human plasma proteome reference set with estimated concentrations in PeptideAtlas Mol. Cell. Proteomics 2011, 10, M110.006353
38. Gelman, I. H.; Gao, L. SSeCKS/Gravin/AKAP12 metastasis suppressor inhibits podosome formation via RhoA- and Cdc42-dependent pathways Mol. Cancer Res. 2006, 4, 151-8
39. Su, B.; Zheng, Q.; Vaughan, M. M.; Bu, Y.; Gelman, I. H. SSeCKS metastasis-suppressing activity in MatLyLu prostate cancer cells correlates with vascular endothelial growth factor inhibition Cancer Res. 2006, 66, 5599-607
40. Choi, M. C.; Jong, H. S.; Kim, T. Y.; Song, S. H.; Lee, D. S.; Lee, J. W.; Kim, T. Y.; Kim, N. K.; Bang, Y. J. AKAP12/Gravin is inactivated by epigenetic mechanism in human gastric carcinoma and shows growth suppressor activity Oncogene 2004, 23, 7095-103
41. Jo, U.; Whang, Y. M.; Kim, H. K.; Kim, Y. H. AKAP12alpha is associated with promoter methylation in lung cancer Cancer Res. Treat. 2006, 38, 144-51
42. Bonazzi, V. F.; Irwin, D.; Hayward, N. K. Identification of candidate tumor suppressor genes inactivated by promoter methylation in melanoma Genes, Chromosomes Cancer 2009, 48, 10-21
43. Mardin, W. A.; Petrov, K. O.; Enns, A.; Senninger, N.; Haier, J.; Mees, S. T. SERPINB5 and AKAP12-expression and promoter methylation of metastasis suppressor genes in pancreatic ductal adenocarcinoma BMC Cancer. 2010, 10, 549
44. Hayashi, M.; Nomoto, S.; Kanda, M.; Okamura, Y.; Nishikawa, Y.; Yamada, S.; Fujii, T.; Sugimoto, H.; Takeda, S.; Kodera, Y. Identification of the A kinase anchor protein 12 (AKAP12) gene as a candidate tumor suppressor of hepatocellular carcinoma J. Surg. Oncol. 2012, 105, 381-6
45. Goeppert, B.; Schmidt, C. R.; Geiselhart, L.; Dutruel, C.; Capper, D.; Renner, M.; Vogel, M. N.; Zachskorn, C.; Zinke, J.; Campos, B.; Schmezer, P.; Popanda, O.; Wick, W.; Weller, M.; Meyermann, R.; Schittenhelm, J.; Harter, P. N.; Simon, P.; Weichert, W.; Schirmacher, P.; Plass, C.; Mittelbronn, M. Differential expression of the tumor suppressor A-kinase anchor protein 12 in human diffuse and pilocytic astrocytomas is regulated by promoter methylation J. Neuropathol. Exp. Neurol. 2013, 72, 933-41
46. Chappell, N. P.; Teng, P. N.; Hood, B. L.; Wang, G.; Darcy, K. M.; Hamilton, C. A.; Maxwell, G. L.; Conrads, T. P. Mitochondrial proteomic analysis of cisplatin resistance in ovarian cancer J. Proteome Res. 2012, 11, 4605-14
47. Chen, X.; Zhang, J.; Zhang, Z.; Li, H.; Cheng, W.; Liu, J. Cancer stem cells, epithelial-mesenchymal transition, and drug resistance in high-grade ovarian serous carcinoma Hum. Pathol. 2013, 44, 2373-84
48. Higgins, D. F.; Lappin, D. W.; Kieran, N. E.; Anders, H. J.; Watson, R. W.; Strutz, F.; Schlondorff, D.; Haase, V. H.; Fitzpatrick, J. M.; Godson, C.; Brady, H. R. DNA oligonucleotide microarray technology identifies fisp-12 among other potential fibrogenic genes following murine unilateral ureteral obstruction (UUO): modulation during epithelial-mesenchymal transition Kidney Int. 2003, 64, 2079-91
49. Borley, J.; Wilhelm-Benartzi, C.; Brown, R.; Ghaem-Maghami, S. Does tumour biology determine surgical success in the treatment of epithelial ovarian cancer? A systematic literature review Br. J. Cancer 2012, 107, 1069-74
50. Riester, M.; Wei, W.; Waldron, L.; Culhane, A. C.; Trippa, L.; Oliva, E.; Kim, S. H.; Michor, F.; Huttenhower, C.; Parmigiani, G.; Birrer, M. J. Risk prediction for late-stage ovarian cancer by meta-analysis of 1525 patient samples. J. Natl. Cancer Inst. 2014, 106.
51. Verhaak, R. G.; Tamayo, P.; Yang, J. Y.; Hubbard, D.; Zhang, H.; Creighton, C. J.; Fereday, S.; Lawrence, M.; Carter, S. L.; Mermel, C. H.; Kostic, A. D.; Etemadmoghadam, D.; Saksena, G.; Cibulskis, K.; Duraisamy, S.; Levanon, K.; Sougnez, C.; Tsherniak, A.; Gomez, S.; Onofrio, R.; Gabriel, S.; Chin, L.; Zhang, N.; Spellman, P. T.; Zhang, Y.; Akbani, R.; Hoadley, K. A.; Kahn, A.; Kobel, M.; Huntsman, D.; Soslow, R. A.; Defazio, A.; Birrer, M. J.; Gray, J. W.; Weinstein, J. N.; Bowtell, D. D.; Drapkin, R.; Mesirov, J. P.; Getz, G.; Levine, D. A.; Meyerson, M.; Cancer Genome Atlas Research Network Prognostically relevant gene signatures of high-grade serous ovarian carcinoma J. Clin. Invest. 2013, 123, 517-25