The role of 14-3-3 proteins in gynecological tumors

Frontiers in Bioscience - Landmark

Volumn 20, Issue 6, 2015, Pages 934-945

  Zhang, Wenwen ^a   Shen, Qi ^a   Chen, Miaomiao ^a   Wang, Ying ^a   Zhou, Qingfeng ^a   Tao, Xuejiao ^a   Zhu, Xueqiong ^a  

^a WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

14 3 3 protein; Gynecological tumors; HPV; Review

Indexed keywords

HUMAN PAPILLOMAVIRUS;

GENETIC MARKER; PROTEIN 14 3 3;

BREAST TUMOR; CARCINOGENESIS; FEMALE; FEMALE GENITAL TRACT TUMOR; GENETIC MARKER; GENETICS; HUMAN; PATHOLOGY; PHYSIOLOGY; PROGNOSIS;

14-3-3 PROTEINS; BREAST NEOPLASMS; CARCINOGENESIS; FEMALE; GENETIC MARKERS; GENITAL NEOPLASMS, FEMALE; HUMANS; PROGNOSIS;

EID: 84929159821     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4348     Document Type: Review

References (56)

1. Aitken A, Collinge DB, van Heusden BP, Isobe T, Roseboom PH, Rosenfeld G, Soll J: 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins. Trends Biochem Sci 17, 498-501 (1992) DOI: 10.1016/0968-0004(92)90339-B
2. Wang W, Shakes DC: Molecular evolution of the 14-3-3 protein family. J Mol Evol 43, 384-398 (1996) DOI: 10.1007/BF02339012
3. Hermeking H: The 14-3-3 cancer connection. Nat Rev Cancer 3, 931-943 (2003) DOI: 10.1038/nrc1230
4. Meek SE, Lane WS, Piwnica-Worms H: Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J Biol Chem 279, 32046-32054 (2004) DOI: 10.1074/jbc.M403044200 5.
5. van Hemert MJ, Steensma HY, van Heusden GP: 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays 23, 936-946 (2001) DOI: 10.1002/bies.1134
6. Martinez JD: 14-3-3 proteins: do they have a role in human cancer? Future Oncol 1, 631-633 (2005) DOI: 10.2217/14796694.1.5.631
7. Morrison DK: The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19, 16-23 (2009) DOI: 10.1016/j.tcb.2008.10.003
8. Tzivion G, Gupta VS, Kaplun L, Balan V: 14-3-3 proteins as potential oncogenes. Semin Cancer Biol 16, 203-213 (2006) DOI: 10.1016/j.semcancer.2006.03.004
9. Li Z, Liu JY, Zhang JT: 14-3-3sigma, the double-edged sword of human cancers. Am J Transl Res 1, 326-340 (2009) Doi not found.
10. Holm R, Ali T, Svendsrud DH, Nesland JM, Kristensen GB, Lyng H: Expression of 14-3- 3sigma in cervical squamous cell carcinomas: relationship with clinical outcome. Oncol Rep 22, 11-15 (2009) DOI: 10.3892/or-00000399
11. Ferguson AT, Evron E, Umbricht CB, Pandita TK, Chan TA, Hermeking H, Marks JR, Lambers AR, Futreal PA, Stampfer MR, Sukumar S: High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc Natl Acad Sci U S A 97, 6049-6054 (2000) DOI: 10.1073/pnas.100566997
12. Laronga C, Yang HY, Neal C, Lee MH: Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J Biol Chem 275, 23106-23112 (2000) DOI: 10.1074/jbc.M905616199
13. Higareda-Almaraz JC, Enríquez-Gasca Mdel R, Hernández-Ortiz M, Resendis-Antonio O, Encarnación-Guevara S: Proteomic patterns of cervical cancer cell lines, a network perspective. BMC Syst Biol 5, 96 (2011) DOI: 10.1186/1752-0509-5-96
14. Boon SS, Banks L: High-risk human papillomavirus E6 oncoproteins interact with 14-3-3æ in a PDZ binding motif-dependent manner. J Virol 87, 1586-1595 (2013) DOI: 10.1128/JVI.02074-12
15. Syrjänen S, Naud P, Sarian L, Derchain S, Roteli-Martins C, Longatto-Filho A, Tatti S, Branca M, Erzen M, Hammes LS, Costa S, Syrjänen K: Up-regulation of 14-3-3sigma (Stratifin) is associated with high-grade CIN and high-risk human papillomavirus (HPV) at baseline but does not predict outcomes of HR-HPV infections or incident CIN in the LAMS study. Am J Clin Pathol 133, 232-240 (2010) DOI: 10.1309/AJCP49DOITYDCTQJ
16. Kaefer CM, Milner JA: The role of herbs and spices in cancer prevention. J Nutr Biochem 19, 347-361 (2008) DOI: 10.1016/j.jnutbio.2007.11.003
17. Liu Q, Peng YB, Qi LW, Cheng XL, Xu XJ, Liu LL, Liu EH, Li P: The Cytotoxicity Mechanism of 6-Shogaol-Treated HeLa Human Cervical Cancer Cells Revealed by Label-Free Shotgun Proteomics and Bioinformatics Analysis. Evid Based Complement Alternat Med 2012, 278652 (2012) Doi not found.
18. Yue QX, Cao ZW, Guan SH, Liu XH, Tao L, Wu WY, Li YX, Yang PY, Liu X, Guo DA: Proteomics characterization of the cytotoxicity mechanism of ganoderic acid D and computerautomated estimation of the possible drug target network. Mol Cell Proteomics 7, 949-961 (2008) DOI: 10.1074/mcp.M700259-MCP200
19. Yue QX, Song XY, Ma C, Feng LX, Guan SH, Wu WY, Yang M, Jiang BH, Liu X, Cui YJ, Guo DA: Effects of triterpenes from Ganoderma lucidum on protein expression profile of HeLa cells. Phytomedicine 17, 606-613 (2010) DOI: 10.1016/j.phymed.2009.12.013
20. Moreira JM, Ohlsson G, Rank FE, Celis JE: Down-regulation of the tumor suppressor protein 14-3-3sigma is a sporadic event in cancer of the breast. Mol Cell Proteomics 4, 555-569 (2005) DOI: 10.1074/mcp.M400205-MCP200
21. Vercoutter-Edouart AS, Lemoine J, Le Bourhis X, Louis H, Boilly B, Nurcombe V, Révillion F, Peyrat JP, Hondermarck H: Proteomic analysis reveals that 14-3-3sigma is down-regulated in human breast cancer cells. Cancer Res 61, 76-80 (2001) Doi not found.
22. Simooka H, Oyama T, Sano T, Horiguchi J, Nakajima T: Immunohistochemical analysis of 14-3-3 sigma and related proteins in hyperplastic and neoplastic breast lesions, with particular reference to early carcinogenesis. Pathol Int 54, 595-602 (2004) DOI: 10.1111/j.1440-1827.2004.01668.x
23. Urano T, Saito T, Tsukui T, Fujita M, Hosoi T, Muramatsu M, Ouchi Y, Inoue S: Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature 417, 871-875 (2002) DOI: 10.1038/nature00826
24. Luo J, Feng J, Lu J, Wang Y, Tang X, Xie F, Li W: Aberrant methylation profile of 14-3-3 sigma and its reduced transcription/expression levels in Chinese sporadic female breast carcinogenesis. Med Oncol 27, 791-797 (2010) DOI: 10.1007/s12032-009-9287-8
25. Umbricht CB, Evron E, Gabrielson E, Ferguson A, Marks J, Sukumar S: Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene 20, 3348-3353 (2001) DOI: 10.1038/sj.onc.1204438
26. Liang S, Singh M, Gam LH: The differential expression of aqueous soluble proteins in breast normal and cancerous tissues in relation to ethnicity of the patients; Chinese, Malay and Indian. Dis Markers 28, 149-165 (2010) DOI: 10.1155/2010/704630
27. Zang L, Palmer Toy D, Hancock WS, Sgroi DC, Karger BL: Proteomic analysis of ductal carcinoma of the breast using laser capture microdissection, LC-MS, and 16O/18O isotopic labeling. J Proteome Res 3, 604-612 (2004) DOI: 10.1021/pr034131l
28. Song Y, Yang Z, Ke Z, Yao Y, Hu X, Sun Y, Li H, Yin J, Zeng C: Expression of 14-3-3ã in patients with breast cancer: correlation with clinicopathological features and prognosis. Cancer Epidemiol 36, 533-536 (2012) DOI: 10.1016/j.canep.2012.05.003
29. Li N, Wang H, Fan J, Tong C, Yang J, Wei H, Yi J, Ling R: Overexpression of 14-3-3è promotes tumor metastasis and indicates poor prognosis in breast carcinoma. Oncotarget 5, 249-257. (2014) Doi not found.
30. Kim Y, Kim H, Jang SW, Ko J: The role of 14-3- 3β in transcriptional activation of estrogen receptor α and its involvement in proliferation of breast cancer cells. Biochem Biophys Res Commun 414, 199-204 (2011) DOI: 10.1016/j.bbrc.2011.09.056
31. Li DQ, Wang L, Fei F, Hou YF, Luo JM; Wei- Chen, Zeng R, Wu J, Lu JS, Di GH, Ou ZL, Xia QC, Shen ZZ, Shao ZM: Identification of breast cancer metastasis-associated proteins in an isogenic tumor metastasis model using two-dimensional gel electrophoresis and liquid chromatography-ion trap-mass spectrometry. Proteomics 6, 3352-3368 (2006) DOI: 10.1002/pmic.200500617
32. Liang S, Singh M, Gam LH: The differential expression of aqueous soluble proteins in breast normal and cancerous tissues in relation to stage and grade of patients. J Biomed Biotechnol 2010, 516469 (2010) DOI: 10.1155/2010/516469
33. Gheibi A, Kazemi M, Baradaran A, Akbari M, Salehi M: Study of promoter methylation pattern of 14-3-3 sigma gene in normal and cancerous tissue of breast: A potential biomarker for detection of breast cancer in patients. Adv Biomed Res 1, 80 (2012) Doi not found.
34. Rui Z, Jian-Guo J, Yuan-Peng T, Hai P, Bing- Gen R: Use of serological proteomic methods to find biomarkers associated with breast cancer. Proteomics 3, 433-439 (2003) DOI: 10.1002/pmic.200390058
35. Martínez-Galán J, Torres B, Del Moral R, Muñoz-Gámez JA, Martín-Oliva D, Villalobos M, Núñez MI, Luna Jde D, Oliver FJ, Ruiz de Almodóvar JM: Quantitative detection of methylated ESR1 and 14-3-3-sigma gene promoters in serum as candidate biomarkers for diagnosis of breast cancer and evaluation of treatment efficacy. Cancer Biol Ther 7, 958-965 (2008) DOI: 10.4161/cbt.7.6.5966
36. Bergamaschi A, Katzenellenbogen BS: Tamoxifen downregulation of miR-451 increases 14-3-3æ and promotes breast cancer cell survival and endocrine resistance. Oncogene 31, 39-47 (2012) DOI: 10.1038/onc.2011.223
37. Bergamaschi A, Christensen BL, Katzenellenbogen BS: Reversal of endocrine resistance in breast cancer: interrelationships among 14-3-3æ, FOXM1, and a gene signature associated with mitosis. Breast Cancer Res 13, R70 (2011) DOI: 10.1186/bcr2913
38. Neal CL, Yao J, Yang W, Zhou X, Nguyen NT, Lu J, Danes CG, Guo H, Lan KH, Ensor J, Hittelman W, Hung MC, Yu D: 14-3-3zeta overexpression defines high risk for breast cancer recurrence and promotes cancer cell survival. Cancer Res 69, 3425-3432 (2009) DOI: 10.1158/0008-5472.CAN-08-2765
39. Chuthapisith S, Layfield R, Kerr ID, Hughes C, Eremin O: Proteomic profiling of MCF-7 breast cancer cells with chemoresistance to different types of anti-cancer drugs. Int J Oncol 30, 1545-1551 (2007) Doi not found.
40. Hodgkinson VC, ELFadl D, Agarwal V, Garimella V, Russell C, Long ED, Fox JN, McManus PL, Mahapatra TK, Kneeshaw PJ, Drew PJ, Lind MJ, Cawkwell L: Proteomic identification of predictive biomarkers of resistance to neoadjuvant chemotherapy in luminal breast cancer: a possible role for 14-3-3 theta/tau and tBID? J Proteomics 75, 1276-1283 (2012) DOI: 10.1016/j.jprot.2011.11.005
41. Hodgkinson VC, Agarwal V, ELFadl D, Fox JN, McManus PL, Mahapatra TK, Kneeshaw PJ, Drew PJ, Lind MJ, Cawkwell L: Pilot and feasibility study: comparative proteomic analysis by 2-DE MALDI TOF/TOF MS reveals 14-3-3 proteins as putative biomarkers of response to neoadjuvant chemotherapy in ER-positive breast cancer. J Proteomics 75, 2745-2752 (2012) DOI: 10.1016/j.jprot.2012.03.049
42. Wang B, Liu K, Lin HY, Bellam N, Ling S, Lin WC: 14-3-3Tau regulates ubiquitinindependent proteasomal degradation of p21, a novel mechanism of p21 downregulation in breast cancer. Mol Cell Biol 30, 1508-1527 (2010) DOI: 10.1128/MCB.01335-09
43. Cannistra SA, Bast RC Jr, Berek JS, Bookman MA, Crum CP, DePriest PD, Garber JE, Koh WJ, Markman M, McGuire WP 3rd, Rose PG, Rowinsky EK, Rustin GJ, Skates SJ, Vasey PA, King L: Progress in the management of gynecologic cancer: consensus summary statement. J Clin Oncol 21, 129s-132s (2003) DOI: 10.1200/JCO.2003.04.003
44. Kobayashi R, Deavers M, Patenia R, Rice-Stitt T, Halbe J, Gallardo S, Freedman RS: 14-3-3 zeta protein secreted by tumor associated monocytes/macrophages from ascites of epithelial ovarian cancer patients. Cancer Immunol Immunother 58, 247-258 (2009) DOI: 10.1007/s00262-008-0549-7
45. Kaneuchi M, Sasaki M, Tanaka Y, Shiina H, Verma M, Ebina Y, Nomura E, Yamamoto R, Sakuragi N, Dahiya R: Expression and methylation status of 14-3-3 sigma gene can characterize the different histological features of ovarian cancer. Biochem Biophys Res Commun 316, 1156-1162 (2004) DOI: 10.1016/j.bbrc.2004.02.171
46. He Y, Wu X, Liu X, Yan G, Xu C: LC-MS/MS analysis of ovarian cancer metastasis-related proteins using a nude mouse model: 14-3-3 zeta as a candidate biomarker. J Proteome Res 9, 6180-6190 (2010) DOI: 10.1021/pr100822v
47. Chen L, Yang B: 14-3-3 sigma is a useful immunohistochemical marker for diagnosing ovarian granulosa cell tumors and steroid cell tumors. Int J Gynecol Pathol 32, 156-162 (2013) DOI: 10.1097/PGP.0b013e31825a0353
48. Hatzipetros I, Gocze P, Koszegi T, Jaray A, Szereday L, Polgar B, Farkas N, Farkas B: Investigating the clinical potential for 14-3-3 zeta protein to serve as a biomarker for epithelial ovarian cancer. J Ovarian Res 6, 79 (2013) DOI: 10.1186/1757-2215-6-79
49. Mhawech-Fauceglia P, Herrmann FR, Andrews C, South S, Beck A, Lele S, Odunsi K: 14-3-3sigma expression and prognostic value in patients with epithelial ovarian carcinoma: a high throughput tissue microarray analysis. Eur J Surg Oncol 35, 763-767 (2009) DOI: 10.1016/j.ejso.2008.10.014
50. Ravi D, Chen Y, Karia B, Brown A, Gu TT, Li J, Carey MS, Hennessy BT, Bishop AJ: 14-3-3 ó expression effects G2/M response to oxygen and correlates with ovarian cancer metastasis. PLoS One 6, e15864 (2011) DOI: 10.1371/journal.pone.0015864
51. Nakayama H, Sano T, Motegi A, Oyama T, Nakajima T: Increasing 14-3-3 sigma expression with declining estrogen receptor alpha and estrogen-responsive finger protein expression defines malignant progression of endometrial carcinoma. Pathol Int 55, 707-715 (2005) DOI: 10.1111/j.1440-1827.2005.01900.x
52. Lee CH, Ou WB, Mariño-Enriquez A, Zhu M, Mayeda M, Wang Y, Guo X, Brunner AL, Amant F, French CA, West RB, McAlpine JN, Gilks CB, Yaffe MB, Prentice LM, McPherson A, Jones SJ, Marra MA, Shah SP, van de Rijn M, Huntsman DG, Dal Cin P, Debiec-Rychter M, Nucci MR, Fletcher JA: 14-3-3 fusion oncogenes in high-grade endometrial stromal sarcoma. Proc Natl Acad Sci U S A 109, 929-934 (2012) DOI: 10.1073/pnas.1115528109
53. Lv J, Zhu X, Dong K, Lin Y, Hu Y, Zhu C: Reduced expression of 14-3-3 gamma in uterine leiomyoma as identified by proteomics. Fertil Steril 90, 1892-1898 (2008) DOI: 10.1016/j.fertnstert.2007.08.039
54. Wang L, Huang H, Liu D, Fang S, Xian Y, Zhou J, Zuo Y, Wang F, Huang O, He M: Evaluation of 14-3-3 protein family levels and associated receptor expression of estrogen and progesterone in human uterine leiomyomas. Gynecol Endocrinol 28, 665-668 (2012) DOI: 10.3109/09513590.2012.650768
55. Wang Z, Tropè CG, Suo Z, Trøen G, Yang G, Nesland JM, Holm R: The clinicopathological and prognostic impact of 14-3-3 sigma expression on vulvar squamous cell carcinomas. BMC Cancer 8, 308 (2008) DOI: 10.1186/1471-2407-8-308
56. Wang Z, Nesland JM, Suo Z, Trope CG, Holm R: The prognostic value of 14-3-3 isoforms in vulvar squamous cell carcinoma cases: 14-3- 3β and å are independent prognostic factors for these tumors. PLoS One 6, e24843 (2011) DOI: 10.1371/journal.pone.0024843