Predicting ovarian cancer patients' clinical response to platinum-based chemotherapy by their tumor proteomic signatures

Journal of Proteome Research

Volumn 15, Issue 8, 2016, Pages 2455-2465

  Yu, Kun Hsing ^a   Levine, Douglas A ^b   Zhang, Hui ^c   Chan, Daniel W ^c   Zhang, Zhen ^c   Snyder, Michael ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

bioinformatics; cancer biomarkers; drug resistance; ovarian cancer; tandem mass spectrometry

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA ACTININ 4; ANTINEOPLASTIC METAL COMPLEX; RAN PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE A2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE A6; UBIQUITIN C; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CISPLATIN; PLATINUM DERIVATIVE; TUMOR PROTEIN;

ADULT; ARTICLE; CANCER CHEMOTHERAPY; CELL CYCLE REGULATION; DNA REPAIR; FEMALE; HUMAN; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MIDDLE AGED; OVARIAN SEROUS CARCINOMA; OVARY CARCINOMA; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RNA TRANSPORT; SUPERVISED MACHINE LEARNING; TANDEM MASS SPECTROMETRY; TREATMENT RESPONSE; AGED; CHEMISTRY; CYSTADENOCARCINOMA, SEROUS; OVARIAN NEOPLASMS; PERSONALIZED MEDICINE; PREDICTIVE VALUE; PROCEDURES; STATISTICAL ANALYSIS; STATISTICS AND NUMERICAL DATA; TREATMENT OUTCOME;

AGED; ANTINEOPLASTIC AGENTS; CISPLATIN; CYSTADENOCARCINOMA, SEROUS; DATA INTERPRETATION, STATISTICAL; FEMALE; HUMANS; MIDDLE AGED; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PLATINUM COMPOUNDS; PRECISION MEDICINE; PREDICTIVE VALUE OF TESTS; PROTEOMICS; SUPERVISED MACHINE LEARNING; TREATMENT OUTCOME;

EID: 84981313253     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b01129     Document Type: Article

References (63)

1. Siegel, R.; Ma, J.; Zou, Z.; Jemal, A. Cancer statistics, 2014 Ca-Cancer J. Clin. 2014, 64, 9-29 10.3322/caac.21208
2. What are the key statistics about ovarian cancer? 2014. http://www.cancer.org/cancer/ovariancancer/detailedguide/ovarian-cancer-key-statistics (accessed December 11, 2014).
3. Goff, B. A.; Mandel, L. S.; Melancon, C. H.; Muntz, H. G. Frequency of symptoms of ovarian cancer in women presenting to primary care clinics Jama 2004, 291, 2705-12 10.1001/jama.291.22.2705
4. Olson, S. H.; Mignone, L.; Nakraseive, C.; Caputo, T. A.; Barakat, R. R.; Harlap, S. Symptoms of ovarian cancer Obstet. Gynecol. 2001, 98, 212-7 10.1097/00006250-200108000-00006
5. Goff, B. A.; Mandel, L.; Muntz, H. G.; Melancon, C. H. Ovarian carcinoma diagnosis Cancer 2000, 89, 2068-75 10.1002/1097-0142(20001115)89:10<2068::AID-CNCR6>3.0.CO;2-Z
6. Rosenthal, A. N.; Menon, U.; Jacobs, I. J. Screening for ovarian cancer Clin. Obstet. Gynecol. 2006, 49, 433-47 10.1097/00003081-200609000-00004
7. Buys, S. S.; Partridge, E.; Black, A. et al. Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial Jama 2011, 305, 2295-303 10.1001/jama.2011.766
8. Barnholtz-Sloan, J. S.; Schwartz, A. G.; Qureshi, F.; Jacques, S.; Malone, J.; Munkarah, A. R. Ovarian cancer: changes in patterns at diagnosis and relative survival over the last three decades Am. J. Obstet. Gynecol. 2003, 189, 1120-7 10.1067/S0002-9378(03)00579-9
9. du Bois, A.; Luck, H. J.; Meier, W. et al. A randomized clinical trial of cisplatin/paclitaxel versus carboplatin/paclitaxel as first-line treatment of ovarian cancer J. Natl. Cancer I 2003, 95, 1320-1329 10.1093/jnci/djg036
10. Eckstein, N. Platinum resistance in breast and ovarian cancer cell lines J. Exp. Clin. Cancer Res. 2011, 30, 91 10.1186/1756-9966-30-91
11. Stewart, D. J. Mechanisms of resistance to cisplatin and carboplatin Critical reviews in oncology/hematology 2007, 63, 12-31 10.1016/j.critrevonc.2007.02.001
12. Wang, D.; Lippard, S. J. Cellular processing of platinum anticancer drugs Nat. Rev. Drug Discovery 2005, 4, 307-20 10.1038/nrd1691
13. Lai, G. M.; Ozols, R. F.; Young, R. C.; Hamilton, T. C. Effect of glutathione on DNA repair in cisplatin-resistant human ovarian cancer cell lines J. Natl. Cancer Inst 1989, 81, 535-9 10.1093/jnci/81.7.535
14. Lai, G. M.; Ozols, R. F.; Smyth, J. F.; Young, R. C.; Hamilton, T. C. Enhanced DNA repair and resistance to cisplatin in human ovarian cancer Biochem. Pharmacol. 1988, 37, 4597-600 10.1016/0006-2952(88)90325-5
15. Nakayama, K.; Kanzaki, A.; Ogawa, K.; Miyazaki, K.; Neamati, N.; Takebayashi, Y. Copper-transporting P-type adenosine triphosphatase (ATP7B) as a cisplatin based chemoresistance marker in ovarian carcinoma: comparative analysis with expression of MDR1, MRP1, MRP2, LRP and BCRP Int. J. Cancer 2002, 101, 488-95 10.1002/ijc.10608
16. Mamenta, E. L.; Poma, E. E.; Kaufmann, W. K.; Delmastro, D. A.; Grady, H. L.; Chaney, S. G. Enhanced replicative bypass of platinum-DNA adducts in cisplatin-resistant human ovarian carcinoma cell lines Cancer Research 1994, 54, 3500-5
17. Eliopoulos, A. G.; Kerr, D. J.; Herod, J. et al. The control of apoptosis and drug resistance in ovarian cancer: influence of p53 and Bcl-2 Oncogene 1995, 11, 1217-28
18. Pujade-Lauraine, E. How to approach patients in relapse Annals of oncology: official journal of the European Society for Medical Oncology/ESMO 2012, 23 (Suppl 10) x128-31 10.1093/annonc/mds358
19. Friedlander, M.; Trimble, E.; Tinker, A. et al. Clinical trials in recurrent ovarian cancer International journal of gynecological cancer: official journal of the International Gynecological Cancer Society 2011, 21, 771-5 10.1097/IGC.0b013e31821bb8aa
20. Parmar, M. K.; Ledermann, J. A.; Colombo, N. et al. Paclitaxel plus platinum-based chemotherapy versus conventional platinum-based chemotherapy in women with relapsed ovarian cancer: the ICON4/AGO-OVAR-2.2 trial Lancet 2003, 361, 2099-106
21. Ledermann, J. A.; Kristeleit, R. S. Optimal treatment for relapsing ovarian cancer Annals of oncology: official journal of the European Society for Medical Oncology/ESMO 2010, 21 (Suppl 7) vii218-22 10.1093/annonc/mdq377
22. Gynecologic Oncology, G.; Markman, M.; Blessing, J. et al. Phase II trial of weekly paclitaxel (80 mg/m2) in platinum and paclitaxel-resistant ovarian and primary peritoneal cancers: a Gynecologic Oncology Group study Gynecol. Oncol. 2006, 101, 436-40 10.1016/j.ygyno.2005.10.036
23. Hartmann, L. C.; Lu, K. H.; Linette, G. P. et al. Gene expression profiles predict early relapse in ovarian cancer after platinum-paclitaxel chemotherapy Clin. Cancer Res. 2005, 11, 2149-55 10.1158/1078-0432.CCR-04-1673
24. Eitan, R.; Kushnir, M.; Lithwick-Yanai, G. et al. Tumor microRNA expression patterns associated with resistance to platinum based chemotherapy and survival in ovarian cancer patients Gynecol. Oncol. 2009, 114, 253-9 10.1016/j.ygyno.2009.04.024
25. Chaudhry, P.; Srinivasan, R.; Patel, F. D. Utility of gene promoter methylation in prediction of response to platinum-based chemotherapy in epithelial ovarian cancer (EOC) Cancer Invest. 2009, 27, 877-84 10.1080/07357900902849699
26. Oh, J. H.; Gao, J.; Nandi, A.; Gurnani, P.; Knowles, L.; Schorge, J. Diagnosis of early relapse in ovarian cancer using serum proteomic profiling Genome Informatics International Conference on Genome Informatics 2005, 16, 195-204
27. Yu, K. H.; Snyder, M. Omics profiling in precision oncology Mol. Cell. Proteomics 2016, mcp.O116.059253 10.1074/mcp.O116.059253
28. Han, C. L.; Chen, J. S.; Chan, E. C. et al. An informatics-assisted label-free approach for personalized tissue membrane proteomics: case study on colorectal cancer Mol. Cell. Proteomics 2011, 10, M110 003087 10.1074/mcp.M110.003087
29. Li, D.; Chan, D. W. Proteomic cancer biomarkers from discovery to approval: it's worth the effort Expert Rev. Proteomics 2014, 11, 135-6 10.1586/14789450.2014.897614
30. Longoria, T. C.; Ueland, F. R.; Zhang, Z. et al. Clinical performance of a multivariate index assay for detecting early-stage ovarian cancer Am. J. Obstet. Gynecol. 2014, 210 (78) e1-9 10.1016/j.ajog.2013.09.017
31. Zhang, Z.; Chan, D. W. The road from discovery to clinical diagnostics: lessons learned from the first FDA-cleared in vitro diagnostic multivariate index assay of proteomic biomarkers Cancer Epidemiol., Biomarkers Prev. 2010, 19, 2995-9 10.1158/1055-9965.EPI-10-0580
32. Snyder, M. Genomics and Personalized Medicine: What Everyone Needs to Know; Oxford University Press, 2016.
33. Zhang, H.; Liu, T.; Zhang, Z. et al. Integrated Proteogenomic Characterization of Human High-Grade Serous Ovarian Cancer Cell 2016, (Epub ahead of print) 10.1016/j.cell.2016.05.069
34. Yamamoto, S.; Tsuda, H.; Honda, K. et al. Actinin-4 gene amplification in ovarian cancer: a candidate oncogene associated with poor patient prognosis and tumor chemoresistance Mod. Pathol. 2009, 22, 499-507 10.1038/modpathol.2008.234
35. Macleod, K.; Mullen, P.; Sewell, J. et al. Altered ErbB receptor signaling and gene expression in cisplatin-resistant ovarian cancer Cancer Res. 2005, 65, 6789-800 10.1158/0008-5472.CAN-04-2684
36. Gong, F.; Peng, X.; Zeng, Z.; Yu, M.; Zhao, Y.; Tong, A. Proteomic analysis of cisplatin resistance in human ovarian cancer using 2-DE method Mol. Cell. Biochem. 2011, 348, 141-7 10.1007/s11010-010-0648-6
37. Simon, N.; Friedman, J.; Hastie, T.; Tibshirani, R. Regularization Paths for Cox's Proportional Hazards Model via Coordinate Descent J. Stat. Soft. 2011, 39, 1-13 10.18637/jss.v039.i05
38. Tibshirani, R. Regression shrinkage and selection via the Lasso J. Roy. Stat. Soc. B Met. 1996, 58, 267-88
39. Fong, P. C.; Yap, T. A.; Boss, D. S. et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval J. Clin. Oncol. 2010, 28, 2512-9 10.1200/JCO.2009.26.9589
40. Agarwal, R.; Kaye, S. B. Ovarian cancer: strategies for overcoming resistance to chemotherapy Nat. Rev. Cancer 2003, 3, 502-16 10.1038/nrc1123
41. Chuang, Y. T.; Chang, C. L. Extending platinum-free interval in partially platinum-sensitive recurrent ovarian cancer by a non-platinum regimen: its possible clinical significance Taiwanese journal of obstetrics & gynecology 2012, 51, 336-41 10.1016/j.tjog.2012.07.003
42. Bookman, M. A. Extending the platinum-free interval in recurrent ovarian cancer: the role of topotecan in second-line chemotherapy Oncologist 1999, 4, 87-94
43. Reedijk, J.; Lohman, P. H. Cisplatin: synthesis, antitumour activity and mechanism of action Pharm. Weekbl., Sci. Ed. 1985, 7, 173-80 10.1007/BF02307573
44. Reedijk, J. The Mechanism of Action of Platinum Antitumor Drugs Pure Appl. Chem. 1987, 59, 181-92 10.1351/pac198759020181
45. Honda, K.; Yamada, T.; Endo, R. et al. Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion J. Cell Biol. 1998, 140, 1383-93 10.1083/jcb.140.6.1383
46. Zhou, X.; Liao, J.; Hu, L.; Feng, L.; Omary, M. B. Characterization of the major physiologic phosphorylation site of human keratin 19 and its role in filament organization J. Biol. Chem. 1999, 274, 12861-6 10.1074/jbc.274.18.12861
47. Bernal, S. D.; Stahel, R. A. Cytoskeleton-associated proteins: their role as cellular integrators in the neoplastic process Critical reviews in oncology/hematology 1985, 3, 191-204 10.1016/S1040-8428(85)80026-3
48. Berglund, L.; Bjorling, E.; Oksvold, P. et al. A genecentric Human Protein Atlas for expression profiles based on antibodies Mol. Cell. Proteomics 2008, 7, 2019-27 10.1074/mcp.R800013-MCP200
49. Schelfhout, L. J.; Van Muijen, G. N.; Fleuren, G. J. Expression of keratin 19 distinguishes papillary thyroid carcinoma from follicular carcinomas and follicular thyroid adenoma Am. J. Clin. Pathol. 1989, 92, 654-8 10.1093/ajcp/92.5.654
50. Uenishi, T.; Kubo, S.; Yamamoto, T. et al. Cytokeratin 19 expression in hepatocellular carcinoma predicts early postoperative recurrence Cancer Sci. 2003, 94, 851-7 10.1111/j.1349-7006.2003.tb01366.x
51. Govaere, O.; Komuta, M.; Berkers, J. et al. Keratin 19: a key role player in the invasion of human hepatocellular carcinomas Gut 2014, 63, 674-85 10.1136/gutjnl-2012-304351
52. Mengual, L.; Burset, M.; Ars, E. et al. Partially degraded RNA from bladder washing is a suitable sample for studying gene expression profiles in bladder cancer Eur. Urol. 2006, 50, 1347-55, discussion 55-6. 10.1016/j.eururo.2006.05.039
53. Lee, H. J.; Nam, K. T.; Park, H. S. et al. Gene expression profiling of metaplastic lineages identifies CDH17 as a prognostic marker in early stage gastric cancer Gastroenterology 2010, 139, 213-25, e3. 10.1053/j.gastro.2010.04.008
54. Merlos-Suarez, A.; Barriga, F. M.; Jung, P. et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse Cell stem cell 2011, 8, 511-24 10.1016/j.stem.2011.02.020
55. Hayashi, N.; Yokoyama, N.; Seki, T.; Azuma, Y.; Ohba, T.; Nishimoto, T. RanBP1, a Ras-like nuclear G protein binding to Ran/TC4, inhibits RCC1 via Ran/TC4 Mol. Gen. Genet. 1995, 247, 661-9 10.1007/BF00290397
56. Rensen, W. M.; Roscioli, E.; Tedeschi, A. et al. RanBP1 downregulation sensitizes cancer cells to taxol in a caspase-3-dependent manner Oncogene 2009, 28, 1748-58 10.1038/onc.2009.24
57. Amato, R.; Scumaci, D.; D'Antona, L. et al. Sgk1 enhances RANBP1 transcript levels and decreases taxol sensitivity in RKO colon carcinoma cells Oncogene 2013, 32, 4572-8 10.1038/onc.2012.470
58. Stanulla, M.; Schaeffeler, E.; Flohr, T. et al. Thiopurine methyltransferase (TPMT) genotype and early treatment response to mercaptopurine in childhood acute lymphoblastic leukemia Jama 2005, 293, 1485-9 10.1001/jama.293.12.1485
59. Khrunin, A. V.; Khokhrin, D. V.; Moisseev, A. A.; Gorbunova, V. A.; Limborska, S. A. Pharmacogenomic assessment of cisplatin-based chemotherapy outcomes in ovarian cancer Pharmacogenomics 2014, 15, 329-37 10.2217/pgs.13.237
60. Chen, X.; Gu, X.; Shan, Y. et al. Identification of a novel human lactate dehydrogenase gene LDHAL6A, which activates transcriptional activities of AP1(PMA) Mol. Biol. Rep. 2009, 36, 669-76 10.1007/s11033-008-9227-2
61. Siddik, Z. H. Cisplatin: mode of cytotoxic action and molecular basis of resistance Oncogene 2003, 22, 7265-79 10.1038/sj.onc.1206933
62. Fuertes, M. A.; Castilla, J.; Alonso, C.; Perez, J. M. Cisplatin biochemical mechanism of action: from cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways Curr. Med. Chem. 2003, 10, 257-66 10.2174/0929867033368484
63. Grebe, S. K.; Singh, R. J. LC-MS/MS in the Clinical Laboratory-Where to From Here? Clinical Biochemist Reviews/Australian Association of Clinical Biochemists 2011, 32, 5-31