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


Cite item

Full Text

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.

About the authors

Bahman Yousefi

Department of Medical Biochemistry and Biophysics, Tabriz University of Medical Sciences

Email: info@benthamscience.net

Fatemeh Sadoughi

Research Center for Biochemistry and Nutrition in Metabolic Diseases, Kashan University of Medical Sciences, Kashan, I.R. Iran, Kashan University of Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

Zatollah Asemi

6Research Center for Biochemistry and Nutrition in Metabolic Diseases, Kashan University of Medical Sciences, Kashan, I.R. Iran, Kashan University of Medical Sciences

Email: info@benthamscience.net

Mohammad Mansournia

Department of Epidemiology and Biostatistics, Tehran University of Medical Sciences

Email: info@benthamscience.net

Jamal Hallajzadeh

Department of Biochemistry and Nutrition, University of Maragheh

Author for correspondence.
Email: info@benthamscience.net

References

  1. Crick, F. Central dogma of molecular biology. Nature, 1970, 227(5258), 561-563. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1186/s12943-017-0671-2
  24. Goodman, A. HPV testing as a screen for cervical cancer. BMJ, 2015, 350, h2372. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.18632/oncotarget.2327 PMID: 25193865
  66. Klattenhoff, C.; Theurkauf, W. Biogenesis and germline functions of piRNAs. Development, 2008, 135(1), 3-9. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1128/MCB.19.1.1 PMID: 9858526
  73. Dang, C.V. MYC on the path to cancer. Cell, 2012, 149(1), 22-35. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1159/000305098 PMID: 20502058

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers