Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Novel Perspectives for the Diagnosis and Treatment of Gynecological Cancers using Dysregulation of PIWI Protein and PiRNAs as Biomarkers

Author(s): Bahman Yousefi, Fatemeh Sadoughi*, Zatollah Asemi, Mohammad Ali Mansournia and Jamal Hallajzadeh*

Volume 31, Issue 4, 2024

Published on: 24 March, 2023

Page: [453 - 463] Pages: 11

DOI: 10.2174/0929867330666230214101837

Price: $65

Abstract

The term “gynecological cancer” is used for a group of cancers occurring in the female reproductive system. Some of these cancers are ranked as the leading causes of death in developed and developing countries. The lack of proper diagnostic strategies is one of the most important reasons that make them lethal. PIWI-interacting RNAs or piRNAs are a class of small non-coding RNAs, which contain 24-32 nucleotides. These RNAs take part in some cellular mechanisms, and their role in diverse kinds of cancer is confirmed by accumulative evidence. In this review, we gather some information on the roles of these RNAs and members of the PIWI protein family to provide new insight into accurate diagnostic biomarkers and more effective anti-cancer drugs with fewer side effects.

Keywords: PIWI protein, piRNA, PIWIL2, ovarian cancer, cervical cancer, anti-cancer drug.

[1]
Crick, F. Central dogma of molecular biology. Nature, 1970, 227(5258), 561-563.
[http://dx.doi.org/10.1038/227561a0] [PMID: 4913914]
[2]
Yang, J.X.; Rastetter, R.H.; Wilhelm, D. Non-coding RNAs: An introduction. Adv. Exp. Med. Biol., 2016, 886, 13-32.
[http://dx.doi.org/10.1007/978-94-017-7417-8_2] [PMID: 26659485]
[3]
Elgar, G.; Vavouri, T. Tuning in to the signals: Noncoding sequence conservation in vertebrate genomes. Trends Genet., 2008, 24(7), 344-352.
[http://dx.doi.org/10.1016/j.tig.2008.04.005] [PMID: 18514361]
[4]
Romano, G.; Veneziano, D.; Acunzo, M.; Croce, C.M. Small non-coding RNA and cancer. Carcinogenesis, 2017, 38(5), 485-491.
[http://dx.doi.org/10.1093/carcin/bgx026] [PMID: 28449079]
[5]
Palazzo, A.F.; Lee, E.S. Non-coding RNA: What is functional and what is junk? Front. Genet., 2015, 6, 2.
[http://dx.doi.org/10.3389/fgene.2015.00002] [PMID: 25674102]
[6]
Siomi, M.C.; Sato, K.; Pezic, D.; Aravin, A.A. PIWI-interacting small RNAs: The vanguard of genome defence. Nat. Rev. Mol. Cell Biol., 2011, 12(4), 246-258.
[http://dx.doi.org/10.1038/nrm3089] [PMID: 21427766]
[7]
Ghildiyal, M.; Zamore, P.D. Small silencing RNAs: An expanding universe. Nat. Rev. Genet., 2009, 10(2), 94-108.
[http://dx.doi.org/10.1038/nrg2504] [PMID: 19148191]
[8]
Han, Y.N.; Li, Y.; Xia, S.Q.; Zhang, Y.Y.; Zheng, J.H.; Li, W. PIWI proteins and PIWI-interacting RNA: Emerging roles in cancer. Cell. Physiol. Biochem., 2017, 44(1), 1-20.
[http://dx.doi.org/10.1159/000484541] [PMID: 29130960]
[9]
Bartel, DP MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2), 281-97.
[10]
Mercer, T.R.; Dinger, M.E.; Mattick, J.S. Long non-coding RNAs: Insights into functions. Nat. Rev. Genet., 2009, 10(3), 155-159.
[http://dx.doi.org/10.1038/nrg2521] [PMID: 19188922]
[11]
Iwasaki, Y.W.; Siomi, M.C.; Siomi, H. PIWI-Interacting RNA: Its Biogenesis and Functions. Annu. Rev. Biochem., 2015, 84(1), 405-433.
[http://dx.doi.org/10.1146/annurev-biochem-060614-034258] [PMID: 25747396]
[12]
Aravin, A.A.; Naumova, N.M.; Tulin, A.V.; Vagin, V.V.; Rozovsky, Y.M.; Gvozdev, V.A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol., 2001, 11(13), 1017-1027.
[http://dx.doi.org/10.1016/S0960-9822(01)00299-8] [PMID: 11470406]
[13]
Ozata, D.M.; Gainetdinov, I.; Zoch, A.; O’Carroll, D.; Zamore, P.D. PIWI-interacting RNAs: Small RNAs with big functions. Nat. Rev. Genet., 2019, 20(2), 89-108.
[http://dx.doi.org/10.1038/s41576-018-0073-3] [PMID: 30446728]
[14]
Aravin, A.; Gaidatzis, D.; Pfeffer, S.; Lagos-Quintana, M.; Landgraf, P.; Iovino, N.; Morris, P.; Brownstein, M.J.; Kuramochi-Miyagawa, S.; Nakano, T.; Chien, M.; Russo, J.J.; Ju, J.; Sheridan, R.; Sander, C.; Zavolan, M.; Tuschl, T. A novel class of small RNAs bind to MILI protein in mouse testes. Nature, 2006, 442(7099), 203-207.
[http://dx.doi.org/10.1038/nature04916] [PMID: 16751777]
[15]
Cheng, J.; Guo, J.M.; Xiao, B.X.; Miao, Y.; Jiang, Z.; Zhou, H.; Li, Q.N. piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin. Chim. Acta, 2011, 412(17-18), 1621-1625.
[http://dx.doi.org/10.1016/j.cca.2011.05.015] [PMID: 21616063]
[16]
Cheng, J.; Deng, H.; Xiao, B.; Zhou, H.; Zhou, F.; Shen, Z.; Guo, J. piR-823, a novel non-coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells. Cancer Lett., 2012, 315(1), 12-17.
[http://dx.doi.org/10.1016/j.canlet.2011.10.004] [PMID: 22047710]
[17]
Hashim, A.; Rizzo, F.; Marchese, G.; Ravo, M.; Tarallo, R.; Nassa, G.; Giurato, G.; Santamaria, G.; Cordella, A.; Cantarella, C.; Weisz, A. RNA sequencing identifies specific PIWI-interacting small non-coding RNA expression patterns in breast cancer. Oncotarget, 2014, 5(20), 9901-9910.
[http://dx.doi.org/10.18632/oncotarget.2476] [PMID: 25313140]
[18]
Li, Y.; Wu, X.; Gao, H.; Jin, J.M.; Li, A.X.; Kim, Y.S.; Pal, S.K.; Nelson, R.A.; Lau, C.M.; Guo, C.; Mu, B.; Wang, J.; Wang, F.; Wang, J.; Zhao, Y.; Chen, W.; Rossi, J.J.; Weiss, L.M.; Wu, H. Piwi-interacting RNAs (piRNAs)are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer-specific survival. Mol. Med., 2015, 21(1), 381-388.
[http://dx.doi.org/10.2119/molmed.2014.00203] [PMID: 25998508]
[19]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2019. CA Cancer J. Clin., 2019, 69(1), 7-34.
[http://dx.doi.org/10.3322/caac.21551] [PMID: 30620402]
[20]
World cancer research fund. Global cancer incidence: Both sexes. 2018. Available from: https://www.wcrf.org/dietandcancer/cancer-trends/worldwide-cancer-data
[21]
Cohen, P.A.; Jhingran, A.; Oaknin, A.; Denny, L. Cervical cancer. Lancet, 2019, 393(10167), 169-182.
[http://dx.doi.org/10.1016/S0140-6736(18)32470-X] [PMID: 30638582]
[22]
Crosbie, E.J.; Einstein, M.H.; Franceschi, S.; Kitchener, H.C. Human papillomavirus and cervical cancer. Lancet, 2013, 382(9895), 889-899.
[http://dx.doi.org/10.1016/S0140-6736(13)60022-7] [PMID: 23618600]
[23]
Hosseini, E.S.; Meryet-Figuiere, M.; Sabzalipoor, H.; Kashani, H.H.; Nikzad, H.; Asemi, Z. Dysregulated expression of long noncoding RNAs in gynecologic cancers. Mol Cancer., 2017, 16(1), 107.
[http://dx.doi.org/10.1186/s12943-017-0671-2]
[24]
Goodman, A. HPV testing as a screen for cervical cancer. BMJ, 2015, 350, h2372.
[http://dx.doi.org/10.1136/bmj.h2372] [PMID: 26126623]
[25]
Tsikouras, P.; Zervoudis, S.; Manav, B.; Tomara, E.; Iatrakis, G.; Romanidis, C.; Bothou, A.; Galazios, G. Cervical cancer: Screening, diagnosis and staging. J. BUON, 2016, 21(2), 320-325.
[PMID: 27273940]
[26]
Hanley, K.Z.; Birdsong, G.G.; Mosunjac, M.B. Recent developments in surgical pathology of the uterine corpus. Arch. Pathol. Lab. Med., 2017, 141(4), 528-541.
[http://dx.doi.org/10.5858/arpa.2016-0284-SA] [PMID: 28353387]
[27]
Braun, M.M.; Overbeek-Wager, E.A.; Grumbo, R.J. Diagnosis and management of endometrial cancer. Am. Fam. Physician, 2016, 93(6), 468-474.
[PMID: 26977831]
[28]
Rizzo, S.; Femia, M.; Buscarino, V.; Franchi, D.; Garbi, A.; Zanagnolo, V.; Del Grande, M.; Manganaro, L.; Alessi, S.; Giannitto, C.; Ruju, F.; Bellomi, M. Endometrial cancer: An overview of novelties in treatment and related imaging keypoints for local staging. Cancer Imaging, 2018, 18(1), 45.
[http://dx.doi.org/10.1186/s40644-018-0180-6] [PMID: 30514387]
[29]
Kossaï, M.; Leary, A.; Scoazec, J.Y.; Genestie, C. Ovarian cancer: A heterogeneous disease. Pathobiology, 2018, 85(1-2), 41-49.
[http://dx.doi.org/10.1159/000479006] [PMID: 29020678]
[30]
Scaletta, G.; Plotti, F.; Luvero, D.; Capriglione, S.; Montera, R.; Miranda, A.; Lopez, S.; Terranova, C.; De Cicco Nardone, C.; Angioli, R. The role of novel biomarker HE4 in the diagnosis, prognosis and follow-up of ovarian cancer: A systematic review. Expert Rev. Anticancer Ther., 2017, 17(9), 827-839.
[http://dx.doi.org/10.1080/14737140.2017.1360138] [PMID: 28756722]
[31]
Doubeni, C.A.; Doubeni, A.R.; Myers, A.E. Diagnosis and management of ovarian cancer. Am. Fam. Physician, 2016, 93(11), 937-944.
[PMID: 27281838]
[32]
Brett M, R.; Brett M, R.; Jennifer B, P.; Thomas A, S.; Jennifer B, P.; Thomas A, S. Epidemiology of ovarian cancer: A review. Cancer Biol. Med., 2017, 14(1), 9-32.
[http://dx.doi.org/10.20892/j.issn.2095-3941.2016.0084] [PMID: 28443200]
[33]
Allemani, C.; Weir, H.K.; Carreira, H.; Harewood, R.; Spika, D.; Wang, X.S.; Bannon, F.; Ahn, J.V.; Johnson, C.J.; Bonaventure, A.; Marcos-Gragera, R.; Stiller, C.; Azevedo e Silva, G.; Chen, W.Q.; Ogunbiyi, O.J.; Rachet, B.; Soeberg, M.J.; You, H.; Matsuda, T.; Bielska-Lasota, M.; Storm, H.; Tucker, T.C.; Coleman, M.P. Global surveillance of cancer survival 1995-2009: Analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet, 2015, 385(9972), 977-1010.
[http://dx.doi.org/10.1016/S0140-6736(14)62038-9] [PMID: 25467588]
[34]
Zhang, W.; Lei, P.; Dong, X.; Men, X. Advances in tumor markers of ovarian cancer for early diagnosis. Indian J. Cancer, 2014, 51(7)(Suppl. 3), 72.
[http://dx.doi.org/10.4103/0019-509X.154049] [PMID: 25818738]
[35]
Shetty, A.S.; Menias, C.O. MR imaging of vulvar and vaginal cancer. Magn. Reson. Imaging Clin. N. Am., 2017, 25(3), 481-502.
[http://dx.doi.org/10.1016/j.mric.2017.03.013] [PMID: 28668156]
[36]
Rajaram, S.; Gupta, B. Management of vulvar cancer. Rev. Recent Clin. Trials, 2015, 10(4), 282-288.
[http://dx.doi.org/10.2174/1574887110666150923112723] [PMID: 26411953]
[37]
Rogers, L.J.; Cuello, M.A. Cancer of the vulva. Int. J. Gynaecol. Obstet., 2018, 143(Suppl. 2), 4-13.
[http://dx.doi.org/10.1002/ijgo.12609] [PMID: 30306583]
[38]
Hacker, N.F.; Barlow, E.L. Staging for vulvar cancer. Best Pract. Res. Clin. Obstet. Gynaecol., 2015, 29(6), 802-811.
[http://dx.doi.org/10.1016/j.bpobgyn.2015.01.004] [PMID: 25842047]
[39]
Weinberg, D.; Gomez-Martinez, R.A. Vulvar cancer. Obstet. Gynecol. Clin. North Am., 2019, 46(1), 125-135.
[http://dx.doi.org/10.1016/j.ogc.2018.09.008] [PMID: 30683259]
[40]
Queiroz, M.A.; Kubik-Huch, R.A.; Hauser, N.; Freiwald-Chilla, B.; von Schulthess, G.; Froehlich, J.M.; Veit-Haibach, P. PET/MRI and PET/CT in advanced gynaecological tumours: Initial experience and comparison. Eur. Radiol., 2015, 25(8), 2222-2230.
[http://dx.doi.org/10.1007/s00330-015-3657-8] [PMID: 26017734]
[41]
Adams, T.S.; Cuello, M.A. Cancer of the vagina. Int. J. Gynaecol. Obstet., 2018, 143(Suppl. 2), 14-21.
[http://dx.doi.org/10.1002/ijgo.12610] [PMID: 30306589]
[42]
Huang, X.; Fejes Tóth, K.; Aravin, A.A. piRNA Biogenesis in Drosophila melanogaster. Trends Genet., 2017, 33(11), 882-894.
[http://dx.doi.org/10.1016/j.tig.2017.09.002] [PMID: 28964526]
[43]
Brennecke, J.; Aravin, A.A.; Stark, A.; Dus, M.; Kellis, M.; Sachidanandam, R.; Hannon, G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell, 2007, 128(6), 1089-1103.
[http://dx.doi.org/10.1016/j.cell.2007.01.043] [PMID: 17346786]
[44]
Yu, Y.; Xiao, J.; Hann, S.S. The emerging roles of PIWI-interacting RNA in human cancers. Cancer Manag. Res., 2019, 11, 5895-5909.
[http://dx.doi.org/10.2147/CMAR.S209300] [PMID: 31303794]
[45]
Clark, J.P.; Lau, N.C. Piwi Proteins and piRNAs step onto the systems biology stage. Adv. Exp. Med. Biol., 2014, 825, 159-197.
[http://dx.doi.org/10.1007/978-1-4939-1221-6_5] [PMID: 25201106]
[46]
Hirakata, S.; Siomi, M.C. piRNA biogenesis in the germline: From transcription of piRNA genomic sources to piRNA maturation. Biochim. Biophys. Acta. Gene Regul. Mech., 2016, 1859(1), 82-92.
[http://dx.doi.org/10.1016/j.bbagrm.2015.09.002] [PMID: 26348412]
[47]
Nishida, K.M.; Sakakibara, K.; Iwasaki, Y.W.; Yamada, H.; Murakami, R.; Murota, Y.; Kawamura, T.; Kodama, T.; Siomi, H.; Siomi, M.C. Hierarchical roles of mitochondrial Papi and Zucchini in Bombyx germline piRNA biogenesis. Nature, 2018, 555(7695), 260-264.
[http://dx.doi.org/10.1038/nature25788] [PMID: 29489748]
[48]
Gunawardane, L.S.; Saito, K.; Nishida, K.M.; Miyoshi, K.; Kawamura, Y.; Nagami, T. A slicer-mediated mechanism for repeat-associated siRNA 5'end formation in Drosophila. Science, 2007, 315(5818), 1587-90.
[49]
Ross, R.J.; Weiner, M.M.; Lin, H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature, 2014, 505(7483), 353-359.
[http://dx.doi.org/10.1038/nature12987] [PMID: 24429634]
[50]
Czech, B.; Munafò, M.; Ciabrelli, F.; Eastwood, E.L.; Fabry, M.H.; Kneuss, E.; Hannon, G.J. piRNA-guided genome defense: From biogenesis to silencing. Annu. Rev. Genet., 2018, 52(1), 131-157.
[http://dx.doi.org/10.1146/annurev-genet-120417-031441] [PMID: 30476449]
[51]
Schoeberl, U.E.; Mochizuki, K. Keeping the soma free of transposons: Programmed DNA elimination in ciliates. J. Biol. Chem., 2011, 286(43), 37045-37052.
[http://dx.doi.org/10.1074/jbc.R111.276964] [PMID: 21914793]
[52]
Kazazian, H.H., J.r. Mobile elements: Drivers of genome evolution. Science, 2004, 303(5664), 1626-1632.
[http://dx.doi.org/10.1126/science.1089670] [PMID: 15016989]
[53]
Cordaux, R.; Batzer, M.A. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet., 2009, 10(10), 691-703.
[http://dx.doi.org/10.1038/nrg2640] [PMID: 19763152]
[54]
Ng, K.W.; Anderson, C.; Marshall, E.A.; Minatel, B.C.; Enfield, K.S.S.; Saprunoff, H.L.; Lam, W.L.; Martinez, V.D. PIWI-interacting RNAs in cancer: Emerging functions and clinical utility. Mol. Cancer, 2016, 15(1), 5.
[http://dx.doi.org/10.1186/s12943-016-0491-9] [PMID: 26768585]
[55]
Chénais, B. Transposable elements and human cancer: A causal relationship? Biochim. Biophys. Acta (BBA)-. Rev. Can., 2013, 1835(1), 28-35.
[56]
Mani, S.R.; Juliano, C.E. Untangling the web: The diverse functions of the PIWI/piRNA pathway. Mol. Reprod. Dev., 2013, 80(8), 632-664.
[http://dx.doi.org/10.1002/mrd.22195] [PMID: 23712694]
[57]
Huang, X.A.; Yin, H.; Sweeney, S.; Raha, D.; Snyder, M.; Lin, H. A major epigenetic programming mechanism guided by piRNAs. Dev. Cell, 2013, 24(5), 502-516.
[http://dx.doi.org/10.1016/j.devcel.2013.01.023] [PMID: 23434410]
[58]
A novel epigenetic mechanism in Drosophila somatic cells mediated by PIWI and piRNAs. In: Cold Spring Harbor symposia on quantitative biology; Lin, H.; Yin, H., Eds.; Cold Spring Harbor Laboratory Press, 2008.
[59]
Chalbatani, G.M.; Dana, H.; Memari, F.; Gharagozlou, E.; Ashjaei, S.; Kheirandish, P.; Marmari, V.; Mahmoudzadeh, H.; Mozayani, F.; Maleki, A.R.; Sadeghian, E.; Nia, E.Z.; Miri, S.R.; Nia, N.; Rezaeian, O.; Eskandary, A.; Razavi, N.; Shirkhoda, M.; Rouzbahani, F.N. Biological function and molecular mechanism of piRNA in cancer. Pract. Lab. Med., 2019, 13, e00113.
[http://dx.doi.org/10.1016/j.plabm.2018.e00113] [PMID: 30705933]
[60]
Liu, Y.; Dou, M.; Song, X.; Dong, Y.; Liu, S.; Liu, H.; Tao, J.; Li, W.; Yin, X.; Xu, W. The emerging role of the piRNA/PIWI complex in cancer. Mol. Cancer, 2019, 18(1), 123.
[http://dx.doi.org/10.1186/s12943-019-1052-9] [PMID: 31399034]
[61]
Tian, Y.; Simanshu, D.K.; Ma, J.B.; Patel, D.J. Structural basis for piRNA 2′-O-methylated 3′-end recognition by PIWI PAZ (PIWI/Argonaute/Zwille) domains. Proc. Natl. Acad. Sci. USA, 2011, 108(3), 903-910.
[http://dx.doi.org/10.1073/pnas.1017762108] [PMID: 21193640]
[62]
Lim, S.L.; Ricciardelli, C.; Oehler, M.K.; De Arao Tan, I.M.D.; Russell, D.; Grützner, F. Overexpression of piRNA pathway genes in epithelial ovarian cancer. PLoS One, 2014, 9(6), e99687.
[http://dx.doi.org/10.1371/journal.pone.0099687] [PMID: 24932571]
[63]
Lee, J.H.; Schütte, D.; Wulf, G.; Füzesi, L.; Radzun, H.J.; Schweyer, S.; Engel, W.; Nayernia, K. Stem-cell protein PIWIl2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum. Mol. Genet., 2006, 15(2), 201-211.
[http://dx.doi.org/10.1093/hmg/ddi430] [PMID: 16377660]
[64]
Ye, Y.; Yin, D.T.; Chen, L.; Zhou, Q.; Shen, R.; He, G.; Yan, Q.; Tong, Z.; Issekutz, A.C.; Shapiro, C.L.; Barsky, S.H.; Lin, H.; Li, J.J.; Gao, J.X. Identification of PIWIl2- like (PL2L) proteins that promote tumorigenesis. PLoS One, 2010, 5(10), e13406.
[http://dx.doi.org/10.1371/journal.pone.0013406] [PMID: 20975993]
[65]
Yao, Y.; Li, C.; Zhou, X.; Zhang, Y.; Lu, Y.; Chen, J.; Zheng, X.; Tao, D.; Liu, Y.; Ma, Y. PIWIL2 induces c-Myc expression by interacting with NME2 and regulates c-Myc-mediated tumor cell proliferation. Oncotarget, 2014, 5(18), 8466-8477.
[http://dx.doi.org/10.18632/oncotarget.2327] [PMID: 25193865]
[66]
Klattenhoff, C.; Theurkauf, W. Biogenesis and germline functions of piRNAs. Development, 2008, 135(1), 3-9.
[http://dx.doi.org/10.1242/dev.006486] [PMID: 18032451]
[67]
Wang, Q.E.; Han, C.; Milum, K.; Wani, A.A. Stem cell protein PIWIl2 modulates chromatin modifications upon cisplatin treatment. Mutat. Res., 2011, 708(1-2), 59-68.
[http://dx.doi.org/10.1016/j.mrfmmm.2011.02.001] [PMID: 21310163]
[68]
Liu, W.; Gao, Q.; Chen, K.; Xue, X.; Li, M.; Chen, Q.; Zhu, G.; Gao, Y. Hiwi facilitates chemoresistance as a cancer stem cell marker in cervical cancer. Oncol. Rep., 2014, 32(5), 1853-1860.
[http://dx.doi.org/10.3892/or.2014.3401] [PMID: 25119492]
[69]
Cox, D.N.; Chao, A.; Baker, J.; Chang, L.; Qiao, D.; Lin, H. A novel class of evolutionarily conserved genes defined by PIWI are essential for stem cell self-renewal. Genes Dev., 1998, 12(23), 3715-3727.
[http://dx.doi.org/10.1101/gad.12.23.3715] [PMID: 9851978]
[70]
Liu, W.K.; Jiang, X.Y.; Zhang, Z.X. Expression of PSCA, PIWIL1 and TBX2 and its correlation with HPV16 infection in formalin-fixed, paraffin-embedded cervical squamous cell carcinoma specimens. Arch. Virol., 2010, 155(5), 657-663.
[http://dx.doi.org/10.1007/s00705-010-0635-y] [PMID: 20229117]
[71]
He, G.; Chen, L.; Ye, Y.; Xiao, Y.; Hua, K.; Jarjoura, D.; Nakano, T.; Barsky, S.H.; Shen, R.; Gao, J.X. PIWIl2 expressed in various stages of cervical neoplasia is a potential complementary marker for p16. Am. J. Transl. Res., 2010, 2(2), 156-169.
[PMID: 20407605]
[72]
Dang, C.V. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol. Cell. Biol., 1999, 19(1), 1-11.
[http://dx.doi.org/10.1128/MCB.19.1.1] [PMID: 9858526]
[73]
Dang, C.V. MYC on the path to cancer. Cell, 2012, 149(1), 22-35.
[http://dx.doi.org/10.1016/j.cell.2012.03.003] [PMID: 22464321]
[74]
Su, C.; Ren, Z.J.; Wang, F.; Liu, M.; Li, X.; Tang, H. PIWIL4 regulates cervical cancer cell line growth and is involved in down-regulating the expression of p14ARF and p53. FEBS Lett., 2012, 586(9), 1356-1362.
[http://dx.doi.org/10.1016/j.febslet.2012.03.053] [PMID: 22483988]
[75]
Chen, C.; Liu, J.; Xu, G. Overexpression of PIWI proteins in human stage III epithelial ovarian cancer with lymph node metastasis. Cancer Biomark., 2013, 13(5), 315-321.
[http://dx.doi.org/10.3233/CBM-130360] [PMID: 24440970]
[76]
Tan, Y.; Liu, L.; Liao, M.; Zhang, C.; Hu, S.; Zou, M.; Gu, M.; Li, X. Emerging roles for PIWI proteins in cancer. Acta Biochim. Biophys. Sin. (Shanghai), 2015, 47(5), 315-324.
[http://dx.doi.org/10.1093/abbs/gmv018] [PMID: 25854579]
[77]
Singh, G.; Roy, J.; Rout, P.; Mallick, B. Genome-wide profiling of the PIWI-interacting RNA-mRNA regulatory networks in epithelial ovarian cancers. PLoS One, 2018, 13(1), e0190485.
[http://dx.doi.org/10.1371/journal.pone.0190485] [PMID: 29320577]
[78]
Bachmayr-Heyda, A.; Auer, K.; Sukhbaatar, N.; Aust, S.; Deycmar, S.; Reiner, A.T.; Polterauer, S.; Dekan, S.; Pils, D. Small RNAs and the competing endogenous RNA network in high grade serous ovarian cancer tumor spread. Oncotarget, 2016, 7(26), 39640-39653.
[http://dx.doi.org/10.18632/oncotarget.9243] [PMID: 27172797]
[79]
Ravo, M.; Cordella, A.; Rinaldi, A.; Bruno, G.; Alexandrova, E.; Saggese, P.; Nassa, G.; Giurato, G.; Tarallo, R.; Marchese, G.; Rizzo, F.; Stellato, C.; Biancardi, R.; Troisi, J.; Di Spiezio Sardo, A.; Zullo, F.; Weisz, A.; Guida, M. Small non-coding RNA deregulation in endometrial carcinogenesis. Oncotarget, 2015, 6(7), 4677-4691.
[http://dx.doi.org/10.18632/oncotarget.2911] [PMID: 25686835]
[80]
Chen, Z.; Che, Q.; He, X.; Wang, F.; Wang, H.; Zhu, M.; Sun, J.; Wan, X. Stem cell protein PIWIl1 endowed endometrial cancer cells with stem-like properties via inducing epithelial-mesenchymal transition. BMC Cancer, 2015, 15(1), 811.
[http://dx.doi.org/10.1186/s12885-015-1794-8] [PMID: 26506848]
[81]
Chen, Z.; Che, Q.; Jiang, F.Z.; Wang, H.H.; Wang, F.Y.; Liao, Y.; Wan, X.P. PIWIl1 causes epigenetic alteration of PTEN gene via upregulation of DNA methyltransferase in type I endometrial cancer. Biochem. Biophys. Res. Commun., 2015, 463(4), 876-880.
[http://dx.doi.org/10.1016/j.bbrc.2015.06.028] [PMID: 26056945]
[82]
Liu, W.K.; Jiang, X.Y.; Zhang, Z.X. Expression of PSCA, PIWIL1, and TBX2 in endometrial adenocarcinoma. Onkologie, 2010, 33(5), 241-245.
[http://dx.doi.org/10.1159/000305098] [PMID: 20502058]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy