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[1]Freeman AK, Morrison DK: 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin Cell Dev Biol 22(7),681-687 (2011)
[2]Aitken, A: 14-3-3 proteins: a historic overview.Semin. Cancer Biol 16(3), 162-172 (2006)
[3]Liang S, Shen G, Liu Q, Xu Y, Zhou L, Xiao S, Xu Z, Gong F, You C, Wei Y: Isoform-specific expression and characterization of 14-3-3 proteins in human glioma tissues discovered by stable isotope labeling with amino acids in cell culture-based proteomic analysis. Proteomics Clin Appl 3(6), 743-753 (2009)
[4]Nakayama H, Sano T, Motegi A, Oyama T, Nakajima T: Increasing 14-3-3 sigma expression with declining estrogen receptor α and estrogen-responsive finger protein expression defines malignant progression of endometrial carcinoma. Pathol Int 55(11), 707-715 (2005)
[5]Umbricht CB, Evron E, Gabrielson E, Fergusoon A, Marks J, Sukumar S: Hypermethyration of 14-3-3 σ (stratifin) is an early event in breast cancer. Oncogene 20(26), 3348–3353 (2001)
[6]Akahira J, Sugihashi Y, Suzuki T, Ito K, Niikura H, Moriya T, et al. Decreased expression of 14-3-3σ is associated with advanced disease in human epithelial ovarian cancer: Its correlation with aberrant DNA methylation. Clin Cancer Res 10(8), 2687–2693 (2004)
[7]Osada H, Tatematsu Y, Yatabe Y, Nakagawa T, Konishi H, Harano T, Nitta M, Okamura H, Inoue S, Sasano H, Okamura K, Yaegashi N: Frequent and histological type-specific inactivation of 14-3-3 σ in human lung cancers. Oncogene 21(15), 2418–2424 (2002)
[8]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(8), 665-668 (2012)
[9]Kambach DM, Sodi VL, Lelkes PI, Azizkhan-Clifford J, Reginato MJ: ErbB2, FoxM1 and 14-3-3ζ prime breast cancer cells for invasion in response to ionizing radiation: Oncogene 33(5), 589-598 (2014)
[10]Jang JS, Cho HY, Lee YJ, Ha WS, Kim HW: The differential proteome profile of stomach cancer: identification of the biomarker candidates. Oncol Res 14(10), 491–499 (2004)
[11]Li Z, Zhao J, Du Y, Park HR, Sun SY, Bernal-Mizrachi L, Aitken A, Khuri FR, Fu H: Down-regulation of 14-3-3zeta suppresses anchorage-independent growth of lung cancer cells through anoikis activation. Proc Natl Acad Sci U S A 105(1), 162-167 (2008)
[12]Zhao GY, Ding JY, Lu CL, Lin ZW, Guo J: The overexpression of 14-3-3ζ and Hsp27 promotes non–small cell lung cancer progression. Cancer 120(5), 652-663 (2014)
[13]Arora S, Matta A, Shukla NK, Deo SV, Ralhan R: Identification of differentially expressed genes in oral squamous cell carcinoma. Mol Carcinog 42(2), 97–108 (2005)
[14]Song Y, Yang Z, Ke Z, Yao Y, Hu X, Sun Y, Li H, Yin J, Zeng C: Expression of 14-3-3γ in patients with breast cancer: Correlation with clinicopathological features and prognosis. Cancer Epidemiol 36(6), 533-536 (2012)
[15]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(5), 1892-1898 (2008)
[16]Shen Q, Chen M, Wang Y, Zhou Q, Tao X, Zhang W, Zhu X: Effects of laparoscopic versus minilaparotomic myomectomy on uterine leiomyoma: a meta-analysis. J Minim Invasive Gynecol 22(2), 177-184 (2015)
[17]Yoshida S, Ohara N, Xu Q, Chen W, Wang J, Nakabayashi K, Sasaki H, Morikawa A, Maruo T: Cell-type specific actions of progesterone receptor modulators in the regulation of uterine leiomyoma growth. Semin Reprod Med 28(3), 260-273 (2010)
[18]Blake RE: Leiomyomata uteri: hormonal and molecular determinants of growth. J Natl Med Assoc 99(10), 1170-1184 (2007)
[19]Kim EH, Kim JY, Lee YH, Chong GO, Park JY, Hong DG: Comparison of estrogen receptor-α, progesterone receptor and calponin expression in gonadotrophin-releasing hormone agonist-sensitive and -resistant uterine fibroids. Obstet Gynecol Sci 57(2), 144-150 (2014)
[20]Russell KS, Haynes MP, Sinha D, Clerisme E, Bender JR: Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci U S A 97(11), 5930-5935 (2000)
[21]Jakimiuk AJ, Bogusiewicz M,Tarkowski R, Dziduch P, Adamiak A,Wróbel A, Haczyński J, Magoffin DA, Jakowicki JA: Estrogen receptor alpha and beta expression in uterine leiomyomas from premenopausal women. Fertil Steril 82, 1244-1249 (2004)
[22]Radhakrishnan VM, Martinez JD: 14-3-3gamma induces oncogenic transformation by stimulating MAP kinase and PI3K signaling. PLoS One 5(7), 1–10 (2010)
[23]Ajjappala BS, Kim YS, Kim MS, Lee MY, Lee KY, Ki HY, Cha DH, Baek KH: 14-3-3 is stimulated by IL-3 and promotes cell proliferation. J Immunol 182(2), 1050-1060 (2009)
[24]Radhakrishnan VM, Putnam CW, Qi W, Martinez JD: P53 suppresses expression of the 14-3-3gamma oncogene. BMC Cancer 11, 378 (2011)
[25]Wu Q, Liu CZ, Tao LY, Yu L, Liu W, Chen SS, He XD: The Clinicopathological and Prognostic Impact of 14-3-3 Protein Isoforms Expression in Human Cholangiocarcinoma by Immunohistochemistry. Asian Pac J Cancer Prev 13(4), 1253-1259 (2012)
[26]Liu Y, Tian RF, Li YM, Liu WP, Cao L, Yang XL, Cao WD, Zhang X: The expression of seven 14-3-3 isoforms in human meningioma. Brain Res 1336:98-102 (2010)
[27]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(4), 1156-1162 (2004)
[28]Ohara N: Selective estrogen receptor modulator and selective progesterone receptor modulator: therapeutic efficacy in the treatment of uterine leiomyoma. Clin Exp Obstet Gynecol 32(1),9-11 (2005)
[29]De Vries-van Leeuwen IJ, da Costa Pereira D, Flach KD, Piersma SR, Haase C, Bier D, Yalcin Z, Michalides R, Feenstra KA, Jiménez CR, de Greef TF,Brunsveld L, Ottmann C, Zwart W, de Boer AH: Interaction of 14-3-3 proteins with the Estrogen Receptor Alpha F domain provides a drug target interface. Proc Natl Acad Sci U S A 110(22), 8894-8899 (2013)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
1 Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, China
Abstract
We demonstrated that the expression of 14-3-3 gamma was lower in uterine leiomyomas compared to the adjacent normal myometrium. Here, we show that 14-3-3 gamma promoter is methylated more in leiomyomas than myometrium. The level of 14-3-3 gamma protein in leiomyomas did not change in respect to age, size, location, or the type of leiomyoma. ER-alpha, ER-beta, and PR proteins were also higher in leiomyomas and the level of these proteins negatively correlated with the level of 14-3-3 gamma protein. These results suggest that the hypermethylation of the 14-3-3 gene promoter accounts for the decreased 14-3-3 gamma in leiomyomas and that such a low level of expression may be involved in the pathogenesis of leiomyomas.
Keywords
- 14-3-3 Gamma
- Uterine Leiomyoma
- Menstrual Cycle
- Methylation
References
- [1] Freeman AK, Morrison DK: 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin Cell Dev Biol 22(7),681-687 (2011)
- [2] Aitken, A: 14-3-3 proteins: a historic overview.Semin. Cancer Biol 16(3), 162-172 (2006)
- [3] Liang S, Shen G, Liu Q, Xu Y, Zhou L, Xiao S, Xu Z, Gong F, You C, Wei Y: Isoform-specific expression and characterization of 14-3-3 proteins in human glioma tissues discovered by stable isotope labeling with amino acids in cell culture-based proteomic analysis. Proteomics Clin Appl 3(6), 743-753 (2009)
- [4] Nakayama H, Sano T, Motegi A, Oyama T, Nakajima T: Increasing 14-3-3 sigma expression with declining estrogen receptor α and estrogen-responsive finger protein expression defines malignant progression of endometrial carcinoma. Pathol Int 55(11), 707-715 (2005)
- [5] Umbricht CB, Evron E, Gabrielson E, Fergusoon A, Marks J, Sukumar S: Hypermethyration of 14-3-3 σ (stratifin) is an early event in breast cancer. Oncogene 20(26), 3348–3353 (2001)
- [6] Akahira J, Sugihashi Y, Suzuki T, Ito K, Niikura H, Moriya T, et al. Decreased expression of 14-3-3σ is associated with advanced disease in human epithelial ovarian cancer: Its correlation with aberrant DNA methylation. Clin Cancer Res 10(8), 2687–2693 (2004)
- [7] Osada H, Tatematsu Y, Yatabe Y, Nakagawa T, Konishi H, Harano T, Nitta M, Okamura H, Inoue S, Sasano H, Okamura K, Yaegashi N: Frequent and histological type-specific inactivation of 14-3-3 σ in human lung cancers. Oncogene 21(15), 2418–2424 (2002)
- [8] 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(8), 665-668 (2012)
- [9] Kambach DM, Sodi VL, Lelkes PI, Azizkhan-Clifford J, Reginato MJ: ErbB2, FoxM1 and 14-3-3ζ prime breast cancer cells for invasion in response to ionizing radiation: Oncogene 33(5), 589-598 (2014)
- [10] Jang JS, Cho HY, Lee YJ, Ha WS, Kim HW: The differential proteome profile of stomach cancer: identification of the biomarker candidates. Oncol Res 14(10), 491–499 (2004)
- [11] Li Z, Zhao J, Du Y, Park HR, Sun SY, Bernal-Mizrachi L, Aitken A, Khuri FR, Fu H: Down-regulation of 14-3-3zeta suppresses anchorage-independent growth of lung cancer cells through anoikis activation. Proc Natl Acad Sci U S A 105(1), 162-167 (2008)
- [12] Zhao GY, Ding JY, Lu CL, Lin ZW, Guo J: The overexpression of 14-3-3ζ and Hsp27 promotes non–small cell lung cancer progression. Cancer 120(5), 652-663 (2014)
- [13] Arora S, Matta A, Shukla NK, Deo SV, Ralhan R: Identification of differentially expressed genes in oral squamous cell carcinoma. Mol Carcinog 42(2), 97–108 (2005)
- [14] Song Y, Yang Z, Ke Z, Yao Y, Hu X, Sun Y, Li H, Yin J, Zeng C: Expression of 14-3-3γ in patients with breast cancer: Correlation with clinicopathological features and prognosis. Cancer Epidemiol 36(6), 533-536 (2012)
- [15] 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(5), 1892-1898 (2008)
- [16] Shen Q, Chen M, Wang Y, Zhou Q, Tao X, Zhang W, Zhu X: Effects of laparoscopic versus minilaparotomic myomectomy on uterine leiomyoma: a meta-analysis. J Minim Invasive Gynecol 22(2), 177-184 (2015)
- [17] Yoshida S, Ohara N, Xu Q, Chen W, Wang J, Nakabayashi K, Sasaki H, Morikawa A, Maruo T: Cell-type specific actions of progesterone receptor modulators in the regulation of uterine leiomyoma growth. Semin Reprod Med 28(3), 260-273 (2010)
- [18] Blake RE: Leiomyomata uteri: hormonal and molecular determinants of growth. J Natl Med Assoc 99(10), 1170-1184 (2007)
- [19] Kim EH, Kim JY, Lee YH, Chong GO, Park JY, Hong DG: Comparison of estrogen receptor-α, progesterone receptor and calponin expression in gonadotrophin-releasing hormone agonist-sensitive and -resistant uterine fibroids. Obstet Gynecol Sci 57(2), 144-150 (2014)
- [20] Russell KS, Haynes MP, Sinha D, Clerisme E, Bender JR: Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci U S A 97(11), 5930-5935 (2000)
- [21] Jakimiuk AJ, Bogusiewicz M,Tarkowski R, Dziduch P, Adamiak A,Wróbel A, Haczyński J, Magoffin DA, Jakowicki JA: Estrogen receptor alpha and beta expression in uterine leiomyomas from premenopausal women. Fertil Steril 82, 1244-1249 (2004)
- [22] Radhakrishnan VM, Martinez JD: 14-3-3gamma induces oncogenic transformation by stimulating MAP kinase and PI3K signaling. PLoS One 5(7), 1–10 (2010)
- [23] Ajjappala BS, Kim YS, Kim MS, Lee MY, Lee KY, Ki HY, Cha DH, Baek KH: 14-3-3 is stimulated by IL-3 and promotes cell proliferation. J Immunol 182(2), 1050-1060 (2009)
- [24] Radhakrishnan VM, Putnam CW, Qi W, Martinez JD: P53 suppresses expression of the 14-3-3gamma oncogene. BMC Cancer 11, 378 (2011)
- [25] Wu Q, Liu CZ, Tao LY, Yu L, Liu W, Chen SS, He XD: The Clinicopathological and Prognostic Impact of 14-3-3 Protein Isoforms Expression in Human Cholangiocarcinoma by Immunohistochemistry. Asian Pac J Cancer Prev 13(4), 1253-1259 (2012)
- [26] Liu Y, Tian RF, Li YM, Liu WP, Cao L, Yang XL, Cao WD, Zhang X: The expression of seven 14-3-3 isoforms in human meningioma. Brain Res 1336:98-102 (2010)
- [27] 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(4), 1156-1162 (2004)
- [28] Ohara N: Selective estrogen receptor modulator and selective progesterone receptor modulator: therapeutic efficacy in the treatment of uterine leiomyoma. Clin Exp Obstet Gynecol 32(1),9-11 (2005)
- [29] De Vries-van Leeuwen IJ, da Costa Pereira D, Flach KD, Piersma SR, Haase C, Bier D, Yalcin Z, Michalides R, Feenstra KA, Jiménez CR, de Greef TF,Brunsveld L, Ottmann C, Zwart W, de Boer AH: Interaction of 14-3-3 proteins with the Estrogen Receptor Alpha F domain provides a drug target interface. Proc Natl Acad Sci U S A 110(22), 8894-8899 (2013)