Cell-cycle protein expression in a population-based study of ovarian and endometrial cancers

Frontiers in Oncology

Volumn 5, Issue FEB, 2015, Pages

  Felix, Ashley S ^a   Sherman, Mark E ^a   Hewitt, Stephen M ^a   Gunja, Munira Z ^a   Yang, Hannah P ^a   Cora, Renata L ^a   Boudreau, Vicky ^a   Ylaya, Kris ^a   Lissowska, Jolanta ^b   Brinton, Louise A ^a   Wentzensen, Nicolas ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b INSTITUTE OF ONCOLOGY   (Poland)

Author keywords

Cell cycle; Gynecologic cancer; Molecular etiology; Prognosis

Indexed keywords

BIOLOGICAL MARKER; CELL MARKER; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 2A; KI 67 ANTIGEN;

ADULT; AGE; AGED; ANTIGEN RETRIEVAL; ARTICLE; CANCER GRADING; CANCER RISK; CANCER STAGING; CANCER SURVIVAL; CELL CYCLE; CELLULAR DISTRIBUTION; CLEAR CELL CARCINOMA; COLLOID CARCINOMA; CONFIDENCE INTERVAL; CORRELATION COEFFICIENT; ENDOMETRIUM CANCER; FEMALE; FOLLOW UP; GENETIC HETEROGENEITY; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MEDICAL RECORD; MIDDLE AGED; OVARY CANCER; OVERALL SURVIVAL; POPULATION BASED CASE CONTROL STUDY; PROPORTIONAL HAZARDS MODEL; PROTEIN EXPRESSION; QUESTIONNAIRE; RISK FACTOR; SENSITIVITY ANALYSIS; SMOKING; TISSUE MICROARRAY;

EID: 84923629257     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2015.00025     Document Type: Article

References (46)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell (2011) 144(5):646-74. doi: 10.1016/j.cell.2011.02.013
2. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell (1995) 81(3):323-30. doi:10.1016/0092-8674(95)90385-2
3. Milde-Langosch K, Riethdorf S. Role of cell-cycle regulatory proteins in gynecological cancer. J Cell Physiol (2003) 196(2):224-44. doi:10.1002/jcp.10286
4. Konecny GE, Winterhoff B, Kolarova T, Qi J, Manivong K, Dering J, et al. Expression of p16 and retinoblastoma determines response to CDK4/6 inhibition in ovarian cancer. Clin Cancer Res (2011) 17(6):1591-602. doi:10.1158/1078-0432.CCR-10-2307
5. Lee YH, Heo JH, Kim TH, Kang H, Kim G, Kim J, et al. Significance of cell cycle regulatory proteins as malignant and prognostic biomarkers in ovarian epithelial tumors. Int J Gynecol Pathol (2011) 30(3):205-17. doi:10.1097/PGP.0b013e3182063e71
6. Bilyk OO, Pande NT, Buchynska LG. Analysis of p53, p16(INK4a), pRb and Cyclin D1 expression and human papillomavirus in primary ovarian serous carcinomas. Exp Oncol (2011) 33(3):150-6.
7. Sui L, Dong Y, Ohno M, Goto M, Inohara T, Sugimoto K, et al. Inverse expression of Cdk4 and p16 in epithelial ovarian tumors. Gynecol Oncol (2000) 79(2):230-7. doi:10.1006/gyno.2000.5961
8. Dong Y, Walsh MD, McGuckin MA, Gabrielli BG, Cummings MC, Wright RG, et al. Increased expression of cyclin-dependent kinase inhibitor 2 (CDKN2A) gene product P16INK4A in ovarian cancer is associated with progression and unfavourable prognosis. Int J Cancer (1997) 74(1):57-63. doi:10.1002/(SICI)1097-0215(19970220)74:1<57::AID-IJC10>3.0.CO;2-F
9. Wiley A, Katsaros D, Chen H, Rigault de la Longrais IA, Beeghly A, Puopolo M, et al. Aberrant promoter methylation of multiple genes in malignant ovarian tumors and in ovarian tumors with low malignant potential. Cancer (2006) 107(2):299-308. doi:10.1002/cncr.21992
10. Kusume T, Tsuda H, Kawabata M, Inoue T, Umesaki N, Suzuki T, et al. The p16-cyclin D1/CDK4-pRb pathway and clinical outcome in epithelial ovarian cancer. Clin Cancer Res (1999) 5(12):4152-7.
11. Kommoss S, du Bois A, Ridder R, Trunk MJ, Schmidt D, Pfisterer J, et al. Independent prognostic significance of cell cycle regulator proteins p16(INK4a) and pRb in advanced-stage ovarian carcinoma including optimally debulked patients: a translational research subprotocol of a randomised study of the Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group. Br J Cancer (2007) 96(2):306-13. doi:10.1038/sj.bjc.6603531
12. Milde-Langosch K, Hagen M, Bamberger AM, Löning T. Expression and prognostic value of the cell-cycle regulatory proteins, Rb, p16MTS1, p21WAF1, p27KIP1, cyclin E, and cyclin D2, in ovarian cancer. Int J Gynecol Pathol (2003) 22(2):168-74. doi:10.1097/00004347-200304000-00009
13. Bali A, O'Brien PM, Edwards LS, Sutherland RL, Hacker NF, Henshall SM. Cyclin D1, p53, and p21Waf1/Cip1 expression is predictive of poor clinical outcome in serous epithelial ovarian cancer. Clin Cancer Res (2004) 10(15):5168-77. doi:10.1158/1078-0432.CCR-03-0751
14. Schmider-Ross A, Pirsig O, Gottschalk E, Denkert C, Lichtenegger W, Reles A. Cyclin-dependent kinase inhibitors CIP1 (p21) and KIP1 (p27) in ovarian cancer. J Cancer Res Clin Oncol (2006) 132(3):163-70. doi:10.1007/s00432-005-0057-5
15. Xu L, Cai J, Yang Q, Ding H, Wu L, Li T, et al. Prognostic significance of several biomarkers in epithelial ovarian cancer: a meta-analysis of published studies. J Cancer Res Clin Oncol (2013) 139(8):1257-77. doi:10.1007/s00432-013-1435-z
16. Newcomb EW, Sosnow M, Demopoulos RI, Zeleniuch-Jacquotte A, Sorich J, Speyer JL. Expression of the cell cycle inhibitor p27KIP1 is a new prognostic marker associated with survival in epithelial ovarian tumors. Am J Pathol (1999) 154(1):119-25. doi:10.1016/S0002-9440(10)65258-3
17. Masciullo V, Ferrandina G, Pucci B, Fanfani F, Lovergine S, Palazzo J, et al. p27Kip1 expression is associated with clinical outcome in advanced epithelial ovarian cancer: multivariate analysis. Clin Cancer Res (2000) 6(12):4816-22.
18. Semczuk A, Jakowicki JA. Alterations of pRb1-cyclin D1-cdk4/6-p16(INK4A) pathway in endometrial carcinogenesis. Cancer Lett (2004) 203(1):1-12. doi:10.1016/j.canlet.2003.09.012
19. Ito K, Sasano H, Matsunaga G, Sato S, Yajima A, Nasim S, et al. Correlations between p21 expression and clinicopathological findings, p53 gene and protein alterations, and survival in patients with endometrial carcinoma. J Pathol (1997) 183(3):318-24. doi:10.1002/(SICI)1096-9896(199711)183:3<318::AID-PATH925>3.0.CO;2-0
20. Schmitz MJ, Hendricks DT, Farley J, Taylor RR, Geradts J, Rose GS, et al. p27 and cyclin D1 abnormalities in uterine papillary serous carcinoma. Gynecol Oncol (2000) 77(3):439-45. doi:10.1006/gyno.2000.5814
21. Gezginc ST, Celik C, Dogan NU, Toy H, Tazegul A, Colakoglu MC. Expression of cyclin A, cyclin E and p27 in normal, hyperplastic and frankly malignant endometrial samples. J Obstet Gynaecol (2013) 33(5):508-11. doi:10.3109/01443615.2013.776024
22. Semczuk A, Miturski R, Skomra D, Jakowicki JA. Expression of the cell-cycle regulatory proteins (pRb, cyclin D1, p16INK4A and cdk4) in human endometrial cancer: correlation with clinicopathological features. Arch Gynecol Obstet (2004) 269(2):104-10. doi:10.1007/s00404-002-0449-6
23. Semczuk A, Boltze C, Marzec B, Szczygielska A, Roessner A, Schneider-Stock R. p16INK4A alterations are accompanied by aberrant protein immunostaining in endometrial carcinomas. J Cancer Res Clin Oncol (2003) 129(10):589-96. doi:10.1007/s00432-003-0482-2
24. Ignatov A, Bischoff J, Schwarzenau C, Krebs T, Kuester D, Herrmann K, et al. P16 alterations increase the metastatic potential of endometrial carcinoma. Gynecol Oncol (2008) 111(2):365-71. doi:10.1016/j.ygyno.2008.07.037
25. Semczuk A, Cybulski M, Tomaszewski J, Rechberger T, Jakowicki JA. Clinicoprognostic significance of pRb1 pathway alterations in uterine endometrial adenocarcinoma. Cancer Genet Cytogenet (2004) 154(2):186-9. doi:10.1016/j.cancergencyto.2004.05.016
26. Milde-Langosch K, Bamberger AM, Goemann C, Rössing E, Rieck G, Kelp B, et al. Expression of cell-cycle regulatory proteins in endometrial carcinomas: correlations with hormone receptor status and clinicopathologic parameters. J Cancer Res Clin Oncol (2001) 127(9):537-44. doi:10.1007/s004320100256
27. Salvesen HB, Das S, Akslen LA. Loss of nuclear p16 protein expression is not associated with promoter methylation but defines a subgroup of aggressive endometrial carcinomas with poor prognosis. Clin Cancer Res (2000) 6(1):153-9.
28. Brinton LA, Sakoda LC, Lissowska J, Sherman ME, Chatterjee N, Peplonska B, et al. Reproductive risk factors for endometrial cancer among Polish women. Br J Cancer (2007) 96(9):1450-6. doi:10.1038/sj.bjc.6603731
29. Garcia-Closas M, Brinton LA, Lissowska J, Richesson D, Sherman ME, Szeszenia-Dabrowska N, et al. Ovarian cancer risk and common variation in the sex hormone-binding globulin gene: a population-based case-control study. BMC Cancer (2007) 7:60. doi:10.1186/1471-2407-7-60
30. Kurman RJ, Shih IeM. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol (2010) 34(3):433-43. doi:10.1097/PAS.0b013e3181cf3d79
31. Cancer Genome Atlas Research Network, Integrated genomic analyses of ovarian carcinoma. Nature (2011) 474(7353):609-15. doi:10.1038/nature10166
32. Cancer Genome Atlas Research NetworkKandoth C, Schultz N, Cherniack AD, Akbani R, Liu Y, et al. Integrated genomic characterization of endometrial carcinoma. Nature (2013) 497(7447):67-73. doi:10.1038/nature12113
33. Weinberg RA. The Biology of Cancer. New York: Garland Science, Taylor and Francis Group, LLC (2007).
34. Szabova L, Yin C, Bupp S, Guerin TM, Schlomer JJ, Householder DB, et al. Perturbation of Rb, p53, and Brca1 or Brca2 cooperate in inducing metastatic serous epithelial ovarian cancer. Cancer Res (2012) 72(16):4141-53. doi:10.1158/0008-5472.CAN-11-3834
35. Anttila MA, Kosma VM, Hongxiu J, Puolakka J, Juhola M, Saarikoski S, et al. p21/WAF1 expression as related to p53, cell proliferation and prognosis in epithelial ovarian cancer. Br J Cancer (1999) 79(11-12):1870-8. doi:10.1038/sj.bjc.6690298
36. Schmider A, Gee C, Friedmann W, Lukas JJ, Press MF, Lichtenegger W, et al. p21 (WAF1/CIP1) protein expression is associated with prolonged survival but not with p53 expression in epithelial ovarian carcinoma. Gynecol Oncol (2000) 77(2):237-42. doi:10.1006/gyno.2000.5748
37. McLaughlin-Drubin ME, Crum CP, Munger K. Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc Natl Acad Sci U S A (2011) 108(5):2130-5. doi:10.1073/pnas.1009933108
38. Rosen DG, Yang G, Cai KQ, Bast RC Jr., Gershenson DM, Silva EG, et al. Subcellular localization of p27kip1 expression predicts poor prognosis in human ovarian cancer. Clin Cancer Res (2005) 11(2 Pt 1):632-7.
39. Duncan TJ, Al-Attar A, Rolland P, Harper S, Spendlove I, Durrant LG. Cytoplasmic p27 expression is an independent prognostic factor in ovarian cancer. Int J Gynecol Pathol (2010) 29(1):8-18. doi:10.1097/PGP.0b013e3181b64ec3
40. Psyrri A, Bamias A, Yu Z, Weinberger PM, Kassar M, Markakis S, et al. Subcellular localization and protein levels of cyclin-dependent kinase inhibitor p27 independently predict for survival in epithelial ovarian cancer. Clin Cancer Res (2005) 11(23):8384-90. doi:10.1158/1078-0432.CCR-05-1270
41. Milde-Langosch K, Riethdorf L, Bamberger AM, Löning T. P16/MTS1 and pRB expression in endometrial carcinomas. Virchows Arch (1999) 434(1):23-8. doi:10.1007/s004280050300
42. Singh M, Darcy KM, Brady WE, Clubwala R, Weber Z, Rittenbach JV, et al. Cadherins, catenins and cell cycle regulators: impact on survival in a gynecologic oncology group phase II endometrial cancer trial. Gynecol Oncol (2011) 123(2):320-8. doi:10.1016/j.ygyno.2011.07.005
43. Watanabe J, Sato H, Kanai T, Kamata Y, Jobo T, Hata H, et al. Paradoxical expression of cell cycle inhibitor p27 in endometrioid adenocarcinoma of the uterine corpus - correlation with proliferation and clinicopathological parameters. Br J Cancer (2002) 87(1):81-5. doi:10.1038/sj.bjc.6600434
44. Shih HC, Shiozawa T, Kato K, Imai T, Miyamoto T, Uchikawa J, et al. Immunohistochemical expression of cyclins, cyclin-dependent kinases, tumor-suppressor gene products, Ki-67, and sex steroid receptors in endometrial carcinoma: positive staining for cyclin A as a poor prognostic indicator. Hum Pathol (2003) 34(5):471-8. doi:10.1016/S0046-8177(03)00124-2
45. Köbel M, Kalloger SE, Boyd N, McKinney S, Mehl E, Palmer C, et al. Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med (2008) 5(12):e232. doi:10.1371/journal.pmed.0050232
46. Farley J, Smith LM, Darcy KM, Brady MF, Bell J, McGuire W, et al. Nuclear P27 expression in benign, borderline (LMP) and invasive tumors of the ovary and its association with prognosis: a gynecologic oncology group study. Gynecol Oncol (2011) 121(2):395-401. doi:10.1016/j.ygyno.2010.11.023