PIWI-interacting RNA (piRNA): a narrative review of its biogenesis, function, and emerging role in lung cancer

[1] Cai Z, Liu Q. Understanding the Global Cancer Statistics 2018: implications for cancer control. Sci China Life Sci. 2021; 64:1017–20. CaiZ LiuQ Understanding the Global Cancer Statistics 2018: implications for cancer control Sci China Life Sci 2021 64 1017 20 10.1007/s11427-019-9816-131463738 Search in Google Scholar

[2] Wong MCS, Lao XQ, Ho K-F, Goggins WB, Tse SLA. Incidence and mortality of lung cancer: global trends and association with socioeconomic status. Sci Rep. 2017; 7:14300. doi: 10.1038/s41598-017-14513-7 WongMCS LaoXQ HoK-F GogginsWB TseSLA Incidence and mortality of lung cancer: global trends and association with socioeconomic status Sci Rep 2017 7 14300 10.1038/s41598-017-14513-7 566273329085026 Open DOISearch in Google Scholar

[3] Nargis N, Yong H-H, Driezen P, Mbulo L, Zhao L, Fong GT, et al. Socioeconomic patterns of smoking cessation behavior in low and middle-income countries: emerging evidence from the Global Adult Tobacco Surveys and International Tobacco Control Surveys. PLoS One. 2019; 14:e02202232019. doi: 10.1371/journal.pone.0220223 NargisN YongH-H DriezenP MbuloL ZhaoL FongGT Socioeconomic patterns of smoking cessation behavior in low and middle-income countries: emerging evidence from the Global Adult Tobacco Surveys and International Tobacco Control Surveys PLoS One 2019 14 e02202232019 10.1371/journal.pone.0220223 673086931490958 Open DOISearch in Google Scholar

[4] Sonea L, Buse M, Gulei D, Onaciu A, Simon I, Braicu C, Berindan-Neagoe I. Decoding the emerging patterns exhibited in non-coding RNAs characteristic of lung cancer with regard to their clinical significance. Curr Genomics. 2018; 19:258–78. SoneaL BuseM GuleiD OnaciuA SimonI BraicuC Berindan-NeagoeI Decoding the emerging patterns exhibited in non-coding RNAs characteristic of lung cancer with regard to their clinical significance Curr Genomics 2018 19 258 78 10.2174/1389202918666171005100124593044829755289 Search in Google Scholar

[5] Litwin M, Szczepańska-Buda A, Piotrowska A, Dzięgiel P, Witkiewicz W. The meaning of PIWI proteins in cancer development. Oncol Lett. 2017; 13:3354–62. LitwinM Szczepańska-BudaA PiotrowskaA DzięgielP WitkiewiczW The meaning of PIWI proteins in cancer development Oncol Lett 2017 13 3354 62 10.3892/ol.2017.5932543146728529570 Search in Google Scholar

[6] Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development. 1997; 124:2463–76. LinH SpradlingAC A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary Development 1997 124 2463 76 10.1242/dev.124.12.24639199372 Search in Google Scholar

[7] Gan B, Chen S, Liu H, Min J, Liu K. Structure and function of eTudor domain containing TDRD proteins. Crit Rev Biochem Mol Biol. 2019; 54:119–32. GanB ChenS LiuH MinJ LiuK Structure and function of eTudor domain containing TDRD proteins Crit Rev Biochem Mol Biol 2019 54 119 32 10.1080/10409238.2019.160319931046474 Search in Google Scholar

[8] Huang X, Tóth KF, Aravin AA. piRNA biogenesis in Drosophila melanogaster. Trends Genet. 2017; 33:882–94. HuangX TóthKF AravinAA piRNA biogenesis in Drosophila melanogaster Trends Genet 2017 33 882 94 10.1016/j.tig.2017.09.002577312928964526 Search in Google Scholar

[9] Yu T, Koppetsch BS, Pagliarani S, Johnston S, Silverstein NJ, Luban J, et al. The piRNA response to retroviral invasion of the koala genome. Cell. 2019; 179:632–643.e12. doi: 10.1016/j.cell.2019.09.002 YuT KoppetschBS PagliaraniS JohnstonS SilversteinNJ LubanJ The piRNA response to retroviral invasion of the koala genome Cell 2019 179 632 643.e12 10.1016/j.cell.2019.09.002 680066631607510 Open DOISearch in Google Scholar

[10] Cox DN, 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; 12:3715–27. CoxDN ChaoA BakerJ ChangL QiaoD LinH A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal Genes Dev 1998 12 3715 27 10.1101/gad.12.23.37153172559851978 Search in Google Scholar

[11] Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, et al. A global profile of germline gene expression in C. elegans. Mol Cell. 2000; 6:605–16. ReinkeV SmithHE NanceJ WangJ Van DorenC BegleyR A global profile of germline gene expression in C. elegans Mol Cell 2000 6 605 16 10.1016/S1097-2765(00)00059-9 Search in Google Scholar

[12] Kuramochi-Miyagawa S, Kimura T, Yomogida K, Kuroiwa A, Tadokoro Y, Fujita Y, et al. Two mouse piwi-related genes: miwi and mili. Mech Dev. 2001; 108:121–33. Kuramochi-MiyagawaS KimuraT YomogidaK KuroiwaA TadokoroY FujitaY Two mouse piwi-related genes: miwi and mili Mech Dev 2001 108 121 33 10.1016/S0925-4773(01)00499-3 Search in Google Scholar

[13] Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, Weller KP, Hoffman R. Human CD34⁺ stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood. 2001; 97:426–34. SharmaAK NelsonMC BrandtJE WessmanM MahmudN WellerKP HoffmanR Human CD34⁺ stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi Blood 2001 97 426 34 10.1182/blood.V97.2.426 Search in Google Scholar

[14] Qiao D, Zeeman A-M, Deng W, Looijenga LHJ, Lin H. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene. 2002; 21:3988–99. QiaoD ZeemanA-M DengW LooijengaLHJ LinH Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas Oncogene 2002 21 3988 99 10.1038/sj.onc.1205505 Search in Google Scholar

[15] Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell. 2002; 110:689–99. MochizukiK FineNA FujisawaT GorovskyMA Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena Cell 2002 110 689 99 10.1016/S0092-8674(02)00909-1 Search in Google Scholar

[16] Tan CH, Lee TC, Weeraratne SD, Korzh V, Lim TM, Gong Z. Ziwi, the zebrafish homologue of the Drosophila piwi: co-localization with vasa at the embryonic genital ridge and gonad-specific expression in the adults. Mech Dev. 2002; 119(Suppl 1):S221–4. TanCH LeeTC WeeraratneSD KorzhV LimTM GongZ Ziwi, the zebrafish homologue of the Drosophila piwi: co-localization with vasa at the embryonic genital ridge and gonad-specific expression in the adults Mech Dev 2002 119 Suppl 1 S221 4 10.1016/S0925-4773(03)00120-5 Search in Google Scholar

[17] Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006; 442(7099):199–202. GirardA SachidanandamR HannonGJ CarmellMA A germline-specific class of small RNAs binds mammalian Piwi proteins Nature 2006 442 7099 199 202 10.1038/nature0491716751776 Search in Google Scholar

[18] Lee JH, Schütte D, Wulf G, Füzesi L, Radzun HJ, Schweyer S, et al. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-X_L pathway. Human Mol Genet. 2005; 15:201–11. LeeJH SchütteD WulfG FüzesiL RadzunHJ SchweyerS Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-X_L pathway Human Mol Genet 2005 15 201 11 10.1093/hmg/ddi43016377660 Search in Google Scholar

[19] Liu X, Sun Y, Guo J, Ma H, Li J, Dong B, et al. Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells. Int J Cancer. 2006; 118:1922–9. LiuX SunY GuoJ MaH LiJ DongB Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells Int J Cancer 2006 118 1922 9 10.1002/ijc.2157516287078 Search in Google Scholar

[20] Taubert H, Greither T, Kaushal D, Würl P, Bache M, Bartel F, et al. Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma. Oncogene. 2007; 26:1098–100. TaubertH GreitherT KaushalD WürlP BacheM BartelF Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma Oncogene 2007 26 1098 100 10.1038/sj.onc.120988016953229 Search in Google Scholar

[21] Grochola LF, Greither T, Taubert H, Möller P, Knippschild U, Udelnow A, et al. The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death. Br J Cancer. 2008; 99:1083–8. GrocholaLF GreitherT TaubertH MöllerP KnippschildU UdelnowA The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death Br J Cancer 2008 99 1083 8 10.1038/sj.bjc.6604653256707218781170 Search in Google Scholar

[22] He W, Wang Z, Wang Q, Fan Q, Shou C, Wang J, et al. Expression of HIWI in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. BMC Cancer. 2009; 9:426. doi: 10.1186/1471-2407-9-426 HeW WangZ WangQ FanQ ShouC WangJ Expression of HIWI in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis BMC Cancer 2009 9 426 10.1186/1471-2407-9-426 280151919995427 Open DOISearch in Google Scholar

[23] He G, Chen L, Ye Y, Xiao Y, Hua K, Jarjoura D, et al. Piwil2 expressed in various stages of cervical neoplasia is a potential complementary marker for p16^INK4a. Am J Transl Res. 2010; 2:156–69. HeG ChenL YeY XiaoY HuaK JarjouraD Piwil2 expressed in various stages of cervical neoplasia is a potential complementary marker for p16^INK4a Am J Transl Res 2010 2 156 69 Search in Google Scholar

[24] Liu JJ, Shen R, Chen L, Ye Y, He G, Hua K, et al. Piwil2 is expressed in various stages of breast cancers and has the potential to be used as a novel biomarker. Int J Clin Exp Pathol. 2010; 3:328–37. LiuJJ ShenR ChenL YeY HeG HuaK Piwil2 is expressed in various stages of breast cancers and has the potential to be used as a novel biomarker Int J Clin Exp Pathol 2010 3 328 37 Search in Google Scholar

[25] Sun G, Wang Y, Sun L, Luo H, Liu N, Fu Z, You Y. Clinical significance of Hiwi gene expression in gliomas. Brain Res. 2011; 1373:183–8. SunG WangY SunL LuoH LiuN FuZ YouY Clinical significance of Hiwi gene expression in gliomas Brain Res 2011 1373 183 8 10.1016/j.brainres.2010.11.09721138738 Search in Google Scholar

[26] 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; 412:1621–5. ChengJ GuoJ-M XiaoB-X MiaoY JiangZ ZhouH LiQ-N piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells Clin Chim Acta 2011 412 1621 5 10.1016/j.cca.2011.05.01521616063 Search in Google Scholar

[27] Yan ZE, Qu L-k, Lin M, Liu C-y, Bin D, Xing X-f, et al. HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chinese Med J (Engl). 2011; 124:2144–9. YanZE QuL-k LinM LiuC-y BinD XingX-f HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer Chinese Med J (Engl) 2011 124 2144 9 Search in Google Scholar

[28] 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; 315:12–7. ChengJ DengH XiaoB ZhouH ZhouF ShenZ GuoJ 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 12 7 10.1016/j.canlet.2011.10.00422047710 Search in Google Scholar

[29] Li D, Sun X, Yan D, Huang J, Luo Q, Tang H, Peng Z. Piwil2 modulates the proliferation and metastasis of colon cancer via regulation of matrix metallopeptidase 9 transcriptional activity. Exp Biol Med (Maywood). 2012; 237:1231–40. LiD SunX YanD HuangJ LuoQ TangH PengZ Piwil2 modulates the proliferation and metastasis of colon cancer via regulation of matrix metallopeptidase 9 transcriptional activity Exp Biol Med (Maywood) 2012 237 1231 40 10.1258/ebm.2012.01138023104504 Search in Google Scholar

[30] Chen C, Liu J, Xu G. Overexpression of PIWI proteins in human stage III epithelial ovarian cancer with lymph node metastasis. Cancer Biomark. 2013; 13:315–21. ChenC LiuJ XuG Overexpression of PIWI proteins in human stage III epithelial ovarian cancer with lymph node metastasis Cancer Biomark 2013 13 315 21 10.3233/CBM-13036024440970 Search in Google Scholar

[31] Zhang H, Ren Y, Xu H, Pang D, Duan C, Liu C. The expression of stem cell protein Piwil2 and piR-932 in breast cancer. Surg Oncol. 2013; 22:217–23. ZhangH RenY XuH PangD DuanC LiuC The expression of stem cell protein Piwil2 and piR-932 in breast cancer Surg Oncol 2013 22 217 23 10.1016/j.suronc.2013.07.00123992744 Search in Google Scholar

[32] Wang D-W, Wang Z-H, Wang L-L, Song Y, Zhang G-Z. Overexpression of hiwi promotes growth of human breast cancer cells. Asian Pac J Cancer Prev. 2014; 15:7553–8. WangD-W WangZ-H WangL-L SongY ZhangG-Z Overexpression of hiwi promotes growth of human breast cancer cells Asian Pac J Cancer Prev 2014 15 7553 8 10.7314/APJCP.2014.15.18.7553 Search in Google Scholar

[33] Yan H, Wu Q-L, Sun C-Y, Ai L-S, Deng J, Zhang L, et al. piRNA-823 contributes to tumorigenesis by regulating de novo DNA methylation and angiogenesis in multiple myeloma. Leukemia. 2015; 29:196–206. YanH WuQ-L SunC-Y AiL-S DengJ ZhangL piRNA-823 contributes to tumorigenesis by regulating de novo DNA methylation and angiogenesis in multiple myeloma Leukemia 2015 29 196 206 10.1038/leu.2014.13524732595 Search in Google Scholar

[34] Al-Janabi O, Wach S, Nolte E, Weigelt K, Rau TT, Stöhr C, et al. Piwi-like 1 and 4 gene transcript levels are associated with clinicopathological parameters in renal cell carcinomas. Biochim Biophys Acta. 2014; 1842:686–90. Al-JanabiO WachS NolteE WeigeltK RauTT StöhrC Piwi-like 1 and 4 gene transcript levels are associated with clinicopathological parameters in renal cell carcinomas Biochim Biophys Acta 2014 1842 686 90 10.1016/j.bbadis.2014.01.01424509249 Search in Google Scholar

[35] Liu W, Gao Q, Chen K, Xue X, Li M, Chen Q, et al. Hiwi facilitates chemoresistance as a cancer stem cell marker in cervical cancer. Oncol Rep. 2014; 32:1853–60. LiuW GaoQ ChenK XueX LiM ChenQ Hiwi facilitates chemoresistance as a cancer stem cell marker in cervical cancer Oncol Rep 2014 32 1853 60 10.3892/or.2014.340125119492 Search in Google Scholar

[36] Xie Y, Yang Y, Ji D, Zhang D, Yao X, Zhang X. Hiwi downregulation, mediated by shRNA, reduces the proliferation and migration of human hepatocellular carcinoma cells. Mol Med Rep. 2014; 11:1455–61. XieY YangY JiD ZhangD YaoX ZhangX Hiwi downregulation, mediated by shRNA, reduces the proliferation and migration of human hepatocellular carcinoma cells Mol Med Rep 2014 11 1455 61 10.3892/mmr.2014.284725370791 Search in Google Scholar

[37] Chu H, Hui G, Yuan L, Shi D, Wang Y, Du M, et al. Identification of novel piRNAs in bladder cancer. Cancer Lett. 2015; 356:561–7. ChuH HuiG YuanL ShiD WangY DuM Identification of novel piRNAs in bladder cancer Cancer Lett 2015 356 561 7 10.1016/j.canlet.2014.10.00425305452 Search in Google Scholar

[38] Fu A, Jacobs DI, Hoffman AE, Zheng T, Zhu Y. PIWI-interacting RNA 021285 is involved in breast tumorigenesis possibly by remodeling the cancer epigenome. Carcinogenesis. 2015; 36:1094–102. FuA JacobsDI HoffmanAE ZhengT ZhuY PIWI-interacting RNA 021285 is involved in breast tumorigenesis possibly by remodeling the cancer epigenome Carcinogenesis 2015 36 1094 102 10.1093/carcin/bgv105500615226210741 Search in Google Scholar

[39] Yang Y, Zhang X, Song D, Wei J. Piwil2 modulates the invasion and metastasis of prostate cancer by regulating the expression of matrix metalloproteinase-9 and epithelial-mesenchymal transitions. Oncol Lett. 2015; 10:1735–40. YangY ZhangX SongD WeiJ Piwil2 modulates the invasion and metastasis of prostate cancer by regulating the expression of matrix metalloproteinase-9 and epithelial-mesenchymal transitions Oncol Lett 2015 10 1735 40 10.3892/ol.2015.3392453327926622742 Search in Google Scholar

[40] Müller S, Raulefs S, Bruns P, Afonso-Grunz F, Plötner A, Thermann R, et al. Next-generation sequencing reveals novel differentially regulated mRNAs, lncRNAs, miRNAs, sdRNAs and a piRNA in pancreatic cancer. Mol Cancer. 2015; 14:94. doi: 10.1186/s12943-015-0358-5 MüllerS RaulefsS BrunsP Afonso-GrunzF PlötnerA ThermannR Next-generation sequencing reveals novel differentially regulated mRNAs, lncRNAs, miRNAs, sdRNAs and a piRNA in pancreatic cancer Mol Cancer 2015 14 94 10.1186/s12943-015-0358-5 441753625910082 Open DOISearch in Google Scholar

[41] Chu H, Xia L, Qiu X, Gu D, Zhu L, Jin J, et al. Genetic variants in noncoding PIWI-interacting RNA and colorectal cancer risk. Cancer. 2015; 121:2044–52. ChuH XiaL QiuX GuD ZhuL JinJ Genetic variants in noncoding PIWI-interacting RNA and colorectal cancer risk Cancer 2015 121 2044 52 10.1002/cncr.2931425740697 Search in Google Scholar

[42] Wang Y, Jiang Y, Ma N, Sang B, Hu X, Cong X, Liu Z. Overexpression of Hiwi inhibits the growth and migration of chronic myeloid leukemia cells. Cell Biochem Biophys. 2015; 73:117–24. WangY JiangY MaN SangB HuX CongX LiuZ Overexpression of Hiwi inhibits the growth and migration of chronic myeloid leukemia cells Cell Biochem Biophys 2015 73 117 24 10.1007/s12013-015-0651-325701408 Search in Google Scholar

[43] Chen YJ, Xiong XF, Wen SQ, Tian L, Cheng WL, Qi YQ. Expression and clinical significance of PIWIL2 in hilar cholangiocarcinoma tissues and cell lines. Genet Mol Res. 2015; 14:7053–61. ChenYJ XiongXF WenSQ TianL ChengWL QiYQ Expression and clinical significance of PIWIL2 in hilar cholangiocarcinoma tissues and cell lines Genet Mol Res 2015 14 7053 61 10.4238/2015.June.26.1526125915 Search in Google Scholar

[44] Busch J, Ralla B, Jung M, Wotschofsky Z, Trujillo-Arribas E, Schwabe P, et al. Piwi-interacting RNAs as novel prognostic markers in clear cell renal cell carcinomas. J Exp Clin Cancer Res. 2015; 34:61. doi: 10.1186/s13046-015-0180-3 BuschJ RallaB JungM WotschofskyZ Trujillo-ArribasE SchwabeP Piwi-interacting RNAs as novel prognostic markers in clear cell renal cell carcinomas J Exp Clin Cancer Res 2015 34 61 10.1186/s13046-015-0180-3 446720526071182 Open DOISearch in Google Scholar

[45] 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; 463:876–80. ChenZ CheQ JiangF-Z WangH-H WangF-Y LiaoY WanX-P Piwil1 causes epigenetic alteration of PTEN gene via upregulation of DNA methyltransferase in type I endometrial cancer Biochem Biophys Res Commun 2015 463 876 80 10.1016/j.bbrc.2015.06.02826056945 Search in Google Scholar

[46] Taubert H, Wach S, Jung R, Pugia M, Keck B, Bertz S, et al. Piwil 2 expression is correlated with disease-specific and progression-free survival of chemotherapy-treated bladder cancer patients. Mol Med. 2015; 21:371–80. TaubertH WachS JungR PugiaM KeckB BertzS Piwil 2 expression is correlated with disease-specific and progression-free survival of chemotherapy-treated bladder cancer patients Mol Med 2015 21 371 80 10.2119/molmed.2014.00250453447425998509 Search in Google Scholar

[47] Wang Z, Liu N, Shi S, Liu S, Lin H. The role of PIWIL4, an Argonaute family protein, in breast cancer. J Biol Chem. 2016; 291:10646–58. WangZ LiuN ShiS LiuS LinH The role of PIWIL4, an Argonaute family protein, in breast cancer J Biol Chem 2016 291 10646 58 10.1074/jbc.M116.723239486591326957540 Search in Google Scholar

[48] Firmino N, Martinez VD, Rowbotham DA, Enfield KS, Bennewith KL, Lam WL. HPV status is associated with altered PIWI-interacting RNA expression pattern in head and neck cancer. Oral Oncol. 2016; 55:43–8. FirminoN MartinezVD RowbothamDA EnfieldKS BennewithKL LamWL HPV status is associated with altered PIWI-interacting RNA expression pattern in head and neck cancer Oral Oncol 2016 55 43 8 10.1016/j.oraloncology.2016.01.012480843926852287 Search in Google Scholar

[49] Jacobs DI, Qin Q, Lerro MC, Fu A, Dubrow R, Claus EB, et al. PIWI-interacting RNAs in gliomagenesis: evidence from post-GWAS and functional analyses. Cancer Epidemiol Biomarkers Prev. 2016; 25:1073–80. JacobsDI QinQ LerroMC FuA DubrowR ClausEB PIWI-interacting RNAs in gliomagenesis: evidence from post-GWAS and functional analyses Cancer Epidemiol Biomarkers Prev 2016 25 1073 80 10.1158/1055-9965.EPI-16-004727197292 Search in Google Scholar

[50] Gambichler T, Kohsik C, Höh AK, Lang K, Käfferlein HU, Brüning T, et al. Expression of PIWIL3 in primary and metastatic melanoma. J Cancer Res Clin Oncol. 2017; 143:433–7. GambichlerT KohsikC HöhAK LangK KäfferleinHU BrüningT Expression of PIWIL3 in primary and metastatic melanoma J Cancer Res Clin Oncol 2017 143 433 7 10.1007/s00432-016-2305-227858163 Search in Google Scholar

[51] Sivagurunathan S, Arunachalam JP, Chidambaram S. PIWI-like protein, HIWI2 is aberrantly expressed in retinoblastoma cells and affects cell-cycle potentially through OTX2. Cell Mol Biol Lett. 2017; 22:17. doi: 10.1186/s11658-017-0048-y SivagurunathanS ArunachalamJP ChidambaramS PIWI-like protein, HIWI2 is aberrantly expressed in retinoblastoma cells and affects cell-cycle potentially through OTX2 Cell Mol Biol Lett 2017 22 17 10.1186/s11658-017-0048-y 557609528861107 Open DOISearch in Google Scholar

[52] Vychytilova-Faltejskova P, Stitkovcova K, Radova L, Sachlova M, Kosarova Z, Slaba K, et al. Circulating PIWI-interacting RNAs piR-5937 and piR-28876 are promising diagnostic biomarkers of colon cancer. Cancer Epidemiol Biomarkers Prev. 2018; 27:1019–28. Vychytilova-FaltejskovaP StitkovcovaK RadovaL SachlovaM KosarovaZ SlabaK Circulating PIWI-interacting RNAs piR-5937 and piR-28876 are promising diagnostic biomarkers of colon cancer Cancer Epidemiol Biomarkers Prev 2018 27 1019 28 10.1158/1055-9965.EPI-18-031829976566 Search in Google Scholar

[53] Jacobs DI, Qin Q, Fu A, Chen Z, Zhou J, Zhu Y. piRNA-8041 is downregulated in human glioblastoma and suppresses tumor growth in vitro and in vivo. Oncotarget. 2018; 9:37616–26. JacobsDI QinQ FuA ChenZ ZhouJ ZhuY piRNA-8041 is downregulated in human glioblastoma and suppresses tumor growth in vitro and in vivo Oncotarget 2018 9 37616 26 10.18632/oncotarget.26331634088530701019 Search in Google Scholar

[54] Gao C-L, Sun R, Li D-H, Gong F. PIWI-like protein 1 upregulation promotes gastric cancer invasion and metastasis. Onco Targets Ther. 2018; 11:8783–89. GaoC-L SunR LiD-H GongF PIWI-like protein 1 upregulation promotes gastric cancer invasion and metastasis Onco Targets Ther 2018 11 8783 89 10.2147/OTT.S186827628751230584336 Search in Google Scholar

[55] Eckstein M, Jung R, Weigelt K, Sikic D, Stöhr R, Geppert C, et al. Piwi-like 1 and-2 protein expression levels are prognostic factors for muscle invasive urothelial bladder cancer patients. Sci Rep. 2018; 8:17693. doi: 10.1038/s41598-018-35637-4 EcksteinM JungR WeigeltK SikicD StöhrR GeppertC Piwi-like 1 and-2 protein expression levels are prognostic factors for muscle invasive urothelial bladder cancer patients Sci Rep 2018 8 17693 10.1038/s41598-018-35637-4 628383830523270 Open DOISearch in Google Scholar

[56] Heng ZS, Lee JY, Subhramanyam CS, Wang C, Thanga LZ, Hu Q. The role of 17β-estradiol-induced upregulation of Piwi-like 4 in modulating gene expression and motility in breast cancer cells. Oncol Rep. 2018; 40:2525–35. HengZS LeeJY SubhramanyamCS WangC ThangaLZ HuQ The role of 17β-estradiol-induced upregulation of Piwi-like 4 in modulating gene expression and motility in breast cancer cells Oncol Rep 2018 40 2525 35 10.3892/or.2018.6676615187830226541 Search in Google Scholar

[57] Li B, Hong J, Hong M, Wang Y, Yu T, Zang S, Wu Q. piRNA-823 delivered by multiple myeloma-derived extracellular vesicles promoted tumorigenesis through re-educating endothelial cells in the tumor environment. Oncogene. 2019; 38:5227–38. LiB HongJ HongM WangY YuT ZangS WuQ piRNA-823 delivered by multiple myeloma-derived extracellular vesicles promoted tumorigenesis through re-educating endothelial cells in the tumor environment Oncogene 2019 38 5227 38 10.1038/s41388-019-0788-430890754 Search in Google Scholar

[58] Roy J, Das B, Jain N, Mallick B. PIWI-interacting RNA 39980 promotes tumor progression and reduces drug sensitivity in neuroblastoma cells. J Cell Physiol. 2020; 235:2286–99. RoyJ DasB JainN MallickB PIWI-interacting RNA 39980 promotes tumor progression and reduces drug sensitivity in neuroblastoma cells J Cell Physiol 2020 235 2286 99 10.1002/jcp.2913631478570 Search in Google Scholar

[59] Tan L, Mai D, Zhang B, Jiang X, Zhang J, Bai R, et al. PIWI-interacting RNA-36712 restrains breast cancer progression and chemoresistance by interaction with SEPW1 pseudogene SEPW1P RNA. Mol Cancer. 2019; 18:9. doi: 10.1186/s12943-019-0940-3 TanL MaiD ZhangB JiangX ZhangJ BaiR PIWI-interacting RNA-36712 restrains breast cancer progression and chemoresistance by interaction with SEPW1 pseudogene SEPW1P RNA Mol Cancer 2019 18 9 10.1186/s12943-019-0940-3 633050130636640 Open DOISearch in Google Scholar

[60] Lin Y, Holden V, Dhilipkannah P, Deepak J, Todd NW, Jiang F. A non-coding RNA landscape of bronchial epitheliums of lung cancer patients. Biomedicines. 2020; 8:88. doi: 10.3390/biomedicines8040088 LinY HoldenV DhilipkannahP DeepakJ ToddNW JiangF A non-coding RNA landscape of bronchial epitheliums of lung cancer patients Biomedicines 2020 8 88 10.3390/biomedicines8040088 723574432294932 Open DOISearch in Google Scholar

[61] Liu Y, Dong Y, He X, Gong A, Gao J, Hao X, et al. piR-hsa-211106 inhibits the progression of lung adenocarcinoma through pyruvate carboxylase and enhances chemotherapy sensitivity. Front Oncol. 2021; 11:651915. doi: 10.3389/fonc.2021.651915 LiuY DongY HeX GongA GaoJ HaoX piR-hsa-211106 inhibits the progression of lung adenocarcinoma through pyruvate carboxylase and enhances chemotherapy sensitivity Front Oncol 2021 11 651915. 10.3389/fonc.2021.651915 826094334249688 Open DOISearch in Google Scholar

[62] Li J, Wang N, Zhang F, Jin S, Dong Y, Dong X, et al. PIWI-interacting RNAs are aberrantly expressed and may serve as novel biomarkers for diagnosis of lung adenocarcinoma. Thorac Cancer. 2021; 12:2468–77. LiJ WangN ZhangF JinS DongY DongX PIWI-interacting RNAs are aberrantly expressed and may serve as novel biomarkers for diagnosis of lung adenocarcinoma Thorac Cancer 2021 12 2468 77 10.1111/1759-7714.14094844790534346164 Search in Google Scholar

[63] Fathizadeh H, Asemi Z. Epigenetic roles of PIWI proteins and piRNAs in lung cancer. Cell Biosci. 2019; 9:102. doi: 10.1186/s13578-019-0368-x FathizadehH AsemiZ Epigenetic roles of PIWI proteins and piRNAs in lung cancer Cell Biosci 2019 9 102 10.1186/s13578-019-0368-x 692584231890151 Open DOISearch in Google Scholar

[64] Dana PM, Mansournia MA, Mirhashemi SM. PIWI-interacting RNAs: new biomarkers for diagnosis and treatment of breast cancer. Cell Biosci. 2020; 10:44. doi: 10.1186/s13578-020-00403-5 DanaPM MansourniaMA MirhashemiSM PIWI-interacting RNAs: new biomarkers for diagnosis and treatment of breast cancer Cell Biosci 2020 10 44 10.1186/s13578-020-00403-5 709245632211149 Open DOISearch in Google Scholar

[65] Yu Y, Xiao J, Hann SS. The emerging roles of PIWI-interacting RNA in human cancers. Cancer Manag Res. 2019; 11:5895–909. YuY XiaoJ HannSS The emerging roles of PIWI-interacting RNA in human cancers Cancer Manag Res 2019 11 5895 909 10.2147/CMAR.S209300661201731303794 Search in Google Scholar

[66] Sokolova OA, Ilyin AA, Poltavets AS, Nenasheva VV, Mikhaleva EA, Shevelyov YY, Klenov MS. Yb body assembly on the flamenco piRNA precursor transcripts reduces genic piRNA production. Mol Biol Cell. 2019; 30:1544–54. SokolovaOA IlyinAA PoltavetsAS NenashevaVV MikhalevaEA ShevelyovYY KlenovMS Yb body assembly on the flamenco piRNA precursor transcripts reduces genic piRNA production Mol Biol Cell 2019 30 1544 54 10.1091/mbc.E17-10-0591672469530943101 Search in Google Scholar

[67] Ishizu H, Kinoshita T, Hirakata S, Komatsuzaki C, Siomi MC. Distinct and collaborative functions of Yb and Armitage in transposon-targeting piRNA biogenesis. Cell Rep. 2019; 27:1822-35.e8. doi: 10.1016/j.celrep.2019.04.029. IshizuH KinoshitaT HirakataS KomatsuzakiC SiomiMC Distinct and collaborative functions of Yb and Armitage in transposon-targeting piRNA biogenesis Cell Rep 2019 27 1822 35.e8 10.1016/j.celrep.2019.04.029 31067466 Open DOISearch in Google Scholar

[68] Saito K, Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, et al. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature. 2009; 461:1296–9. SaitoK InagakiS MituyamaT KawamuraY OnoY SakotaE A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila Nature 2009 461 1296 9 10.1038/nature0850119812547 Search in Google Scholar

[69] Aguiar ERGR, de Almeida JPP, Queiroz LR, Oliveira LS, Olmo RP, de Faria IJDS, et al. A single unidirectional piRNA cluster similar to the flamenco locus is the major source of EVE-derived transcription and small RNAs in Aedes aegypti mosquitoes. RNA. 2020; 26:581–94. AguiarERGR de AlmeidaJPP QueirozLR OliveiraLS OlmoRP de FariaIJDS A single unidirectional piRNA cluster similar to the flamenco locus is the major source of EVE-derived transcription and small RNAs in Aedes aegypti mosquitoes RNA 2020 26 581 94 10.1261/rna.073965.119716135431996404 Search in Google Scholar

[70] Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 2013; 27:390–9. Le ThomasA RogersAK WebsterA MarinovGK LiaoSE PerkinsEM Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state Genes Dev 2013 27 390 9 10.1101/gad.209841.112358955623392610 Search in Google Scholar

[71] Chen P, Luo Y, Aravin AA. RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility. PLoS Genet. 2021; 17:e1009591. doi: 10.1371/journal.pgen.1009591 ChenP LuoY AravinAA RDC complex executes a dynamic piRNA program during Drosophila spermatogenesis to safeguard male fertility PLoS Genet 2021 17 e1009591 10.1371/journal.pgen.1009591 841236434473737 Open DOISearch in Google Scholar

[72] Qi H, Watanabe T, Ku H-Y, Liu N, Zhong M, Lin H. The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J Biol Chem. 2011; 286:3789–97. QiH WatanabeT KuH-Y LiuN ZhongM LinH The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells J Biol Chem 2011 286 3789 97 10.1074/jbc.M110.193888303038021106531 Search in Google Scholar

[73] Pane A, Wehr K, Schüpbach T. zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell. 2007; 12:851–62. PaneA WehrK SchüpbachT zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline Dev Cell 2007 12 851 62 10.1016/j.devcel.2007.03.022194581417543859 Search in Google Scholar

[74] Olivieri D, Senti K-A, Subramanian S, Sachidanandam R, Brennecke J. The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol Cell. 2012; 47:954–69. OlivieriD SentiK-A SubramanianS SachidanandamR BrenneckeJ The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila Mol Cell 2012 47 954 69 10.1016/j.molcel.2012.07.021346380522902557 Search in Google Scholar

[75] Xie W, Sowemimo I, Hayashi R, Wang J, Burkard TR, Brennecke J, et al. Structure-function analysis of microRNA 3′-end trimming by Nibbler. Proc Natl Acad Sci U S A. 2020; 117:30370–79. XieW SowemimoI HayashiR WangJ BurkardTR BrenneckeJ Structure-function analysis of microRNA 3′-end trimming by Nibbler Proc Natl Acad Sci U S A 2020 117 30370 79 10.1073/pnas.2018156117772015333199607 Search in Google Scholar

[76] Ding D, Chen C. Zucchini: the key ingredient to unveil piRNA precursor processing. Biol Reprod. 2020; 103:452–54. DingD ChenC Zucchini: the key ingredient to unveil piRNA precursor processing Biol Reprod 2020 103 452 54 10.1093/biolre/ioaa090744277532524138 Search in Google Scholar

[77] Pippadpally S, Venkatesh T. Deciphering piRNA biogenesis through cytoplasmic granules, mitochondria and exosomes. Arch Biochem Biophys. 2020; 695:108597. doi: 10.1016/j.abb.2020.108597 PippadpallyS VenkateshT Deciphering piRNA biogenesis through cytoplasmic granules, mitochondria and exosomes Arch Biochem Biophys 2020 695 108597 10.1016/j.abb.2020.108597 32976825 Open DOISearch in Google Scholar

[78] Sokolova OA, Iakushev EIu, Stoliarenko AD, Mikhaleva EA, Gvozdev VA, Klenov MS. [The interplay of transposon silencing genes in the Drosophila melanogaster germline]. Mol Biol (Mosk). 2011; 45:633–41. [in Russian, English abstract] SokolovaOA IakushevEIu StoliarenkoAD MikhalevaEA GvozdevVA KlenovMS [The interplay of transposon silencing genes in the Drosophila melanogaster germline] Mol Biol (Mosk) 2011 45 633 41 [in Russian, English abstract] 10.1134/S0026893311030174 Search in Google Scholar

[79] Ozata DM, Gainetdinov I, Zoch A, O’Carroll D, Zamore PD. PIWI-interacting RNAs: small RNAs with big functions. Nat Rev Genet. 2019; 20:89–108. OzataDM GainetdinovI ZochA O’CarrollD ZamorePD PIWI-interacting RNAs: small RNAs with big functions Nat Rev Genet 2019 20 89 108 10.1038/s41576-018-0073-330446728 Search in Google Scholar

[80] Russell SJ, LaMarre J. Transposons and the PIWI pathway: genome defense in gametes and embryos. Reproduction. 2018; 156:R111–24. RussellSJ LaMarreJ Transposons and the PIWI pathway: genome defense in gametes and embryos Reproduction 2018 156 R111 24 10.1530/REP-18-021830037984 Search in Google Scholar

[81] Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007; 316:744–7. AravinAA SachidanandamR GirardA Fejes-TothK HannonGJ Developmentally regulated piRNA clusters implicate MILI in transposon control Science 2007 316 744 7 10.1126/science.114261217446352 Search in Google Scholar

[82] Pal-Bhadra M, Leibovitch BA, Gandhi SG, Chikka MR, Bhadra U, Birchler JA, Elgin SCR. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science. 2004; 303:669–72. Pal-BhadraM LeibovitchBA GandhiSG ChikkaMR BhadraU BirchlerJA ElginSCR Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery Science 2004 303 669 72 10.1126/science.109265314752161 Search in Google Scholar

[83] Teo RYW, Anand A, Sridhar V, Okamura K, Kai T. Heterochromatin protein 1a functions for piRNA biogenesis predominantly from pericentric and telomeric regions in Drosophila. Nat Commun. 2018; 9:1735. doi: 10.1038/s41467-018-03908-3 TeoRYW AnandA SridharV OkamuraK KaiT Heterochromatin protein 1a functions for piRNA biogenesis predominantly from pericentric and telomeric regions in Drosophila Nat Commun 2018 9 1735 10.1038/s41467-018-03908-3 593567329728561 Open DOISearch in Google Scholar

[84] Zhao K, Cheng S, Miao N, Xu P, Lu X, Zhang Y, et al. A Pandas complex adapted for piRNA-guided transcriptional silencing and heterochromatin formation. Nat Cell Biol. 2019; 21:1261–72. ZhaoK ChengS MiaoN XuP LuX ZhangY A Pandas complex adapted for piRNA-guided transcriptional silencing and heterochromatin formation Nat Cell Biol 2019 21 1261 72 10.1038/s41556-019-0396-031570835 Search in Google Scholar

[85] Watanabe T, Tomizawa SI, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science. 2011; 332:848–52. WatanabeT TomizawaSI MitsuyaK TotokiY YamamotoY Kuramochi-MiyagawaS Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus Science 2011 332 848 52 10.1126/science.1203919336850721566194 Search in Google Scholar

[86] Théron E, Maupetit-Mehouas S, Pouchin P, Baudet L, Brasset E, Vaury C. The interplay between the Argonaute proteins Piwi and Aub within Drosophila germarium is critical for oogenesis, piRNA biogenesis and TE silencing. Nucleic Acids Res. 2018; 46:10052–65. ThéronE Maupetit-MehouasS PouchinP BaudetL BrassetE VauryC The interplay between the Argonaute proteins Piwi and Aub within Drosophila germarium is critical for oogenesis, piRNA biogenesis and TE silencing Nucleic Acids Res 2018 46 10052 65 10.1093/nar/gky695621271430113668 Search in Google Scholar

[87] Zhang Y, Liu W, Li R, Gu J, Wu P, Peng C, et al. Structural insights into the sequence-specific recognition of Piwi by Drosophila Papi. Proc Natl Acad Sci U S A. 2018; 115:3374–79. ZhangY LiuW LiR GuJ WuP PengC Structural insights into the sequence-specific recognition of Piwi by Drosophila Papi Proc Natl Acad Sci U S A 2018 115 3374 79 10.1073/pnas.1717116115587967229531043 Search in Google Scholar

[88] Wenda JM, Homolka D, Yang Z, Spinelli P, Sachidanandam R, Pandey RR, Pillai RS. Distinct roles of RNA helicases MVH and TDRD9 in PIWI slicing-triggered mammalian piRNA biogenesis and function. Dev Cell. 2017; 41:623–637.e9. doi: 10.1016/j.devcel.2017.05.021 WendaJM HomolkaD YangZ SpinelliP SachidanandamR PandeyRR PillaiRS Distinct roles of RNA helicases MVH and TDRD9 in PIWI slicing-triggered mammalian piRNA biogenesis and function Dev Cell 2017 41 623 637.e9 10.1016/j.devcel.2017.05.021 548118628633017 Open DOISearch in Google Scholar

[89] Zhu J, Zhang D, Liu X, Yu G, Cai X, Xu C, et al. Zebrafish prmt5 arginine methyltransferase is essential for germ cell development. Development. 2019; 146:dev179572. doi: 10.1242/dev.179572 ZhuJ ZhangD LiuX YuG CaiX XuC Zebrafish prmt5 arginine methyltransferase is essential for germ cell development Development 2019 146 dev179572. 10.1242/dev.179572 31533925 Open DOISearch in Google Scholar

[90] Radion E, Morgunova V, Ryazansky S, Akulenko N, Lavrov S, Abramov Y, et al. Key role of piRNAs in telomeric chromatin maintenance and telomere nuclear positioning in Drosophila germline. Epigenetics Chromatin. 2018; 11:40. doi: 10.1186/s13072-018-0210-4 RadionE MorgunovaV RyazanskyS AkulenkoN LavrovS AbramovY Key role of piRNAs in telomeric chromatin maintenance and telomere nuclear positioning in Drosophila germline Epigenetics Chromatin 2018 11 40 10.1186/s13072-018-0210-4 604398430001204 Open DOISearch in Google Scholar

[91] Li Z, You L, Yan D, James AA, Huang Y, Tan A. Bombyx mori histone methyltransferase BmAsh2 is essential for silkworm piRNA-mediated sex determination. PLoS Genet. 2018; 14:e1007245. doi: 10.1371/journal.pgen.1007245 LiZ YouL YanD JamesAA HuangY TanA Bombyx mori histone methyltransferase BmAsh2 is essential for silkworm piRNA-mediated sex determination PLoS Genet 2018 14 e1007245 10.1371/journal.pgen.1007245 584182629474354 Open DOISearch in Google Scholar

[92] Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, et al. A broadly conserved pathway generates 3′UTR-directed primary piRNAs. Curr Biol. 2009; 19:2066–76. RobineN LauNC BallaS JinZ OkamuraK Kuramochi-MiyagawaS A broadly conserved pathway generates 3′UTR-directed primary piRNAs Curr Biol 2009 19 2066 76 10.1016/j.cub.2009.11.064281247820022248 Search in Google Scholar

[93] Rouget C, Papin C, Boureux A, Meunier A-C, Franco B, Robine N, et al. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature. 2010; 467(7319):1128–32. RougetC PapinC BoureuxA MeunierA-C FrancoB RobineN Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo Nature 2010 467 7319 1128 32 10.1038/nature09465450574820953170 Search in Google Scholar

[94] Dai P, Wang X, Gou L-T, Li Z-T, Wen Z, Chen Z-G, et al. A translation-activating function of MIWI/piRNA during mouse spermiogenesis. Cell. 2019; 179:1566–81.e16. doi: 10.1016/j.cell.2019.11.022 DaiP WangX GouL-T LiZ-T WenZ ChenZ-G A translation-activating function of MIWI/piRNA during mouse spermiogenesis Cell 2019 179 1566 81.e16 10.1016/j.cell.2019.11.022 813932331835033 Open DOISearch in Google Scholar

[95] Mani SR, Megosh H, Lin H. PIWI proteins are essential for early Drosophila embryogenesis. Dev Biol. 2014; 385:340–9. ManiSR MegoshH LinH PIWI proteins are essential for early Drosophila embryogenesis Dev Biol 2014 385 340 9 10.1016/j.ydbio.2013.10.017391587924184635 Search in Google Scholar

[96] Bahn JH, Zhang Q, Li F, Chan T-M, Lin X, Kim Y, et al. The landscape of microRNA, Piwi-interacting RNA, and circular RNA in human saliva. Clin Chem. 2015; 61:221–30. BahnJH ZhangQ LiF ChanT-M LinX KimY The landscape of microRNA, Piwi-interacting RNA, and circular RNA in human saliva Clin Chem 2015 61 221 30 10.1373/clinchem.2014.230433433288525376581 Search in Google Scholar

[97] Lenart P, Novak J, Bienertova-Vasku J. PIWI-piRNA pathway: setting the pace of aging by reducing DNA damage. Mech Ageing Dev. 2018; 173:29–38. LenartP NovakJ Bienertova-VaskuJ PIWI-piRNA pathway: setting the pace of aging by reducing DNA damage Mech Ageing Dev 2018 173 29 38 10.1016/j.mad.2018.03.00929580825 Search in Google Scholar

[98] Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell. 2012; 149:693–707. RajasethupathyP AntonovI SheridanR FreyS SanderC TuschlT KandelER A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity Cell 2012 149 693 707 10.1016/j.cell.2012.02.057344236622541438 Search in Google Scholar

[99] Kolliopoulou A, Santos D, Taning CNT, Wynant N, Vanden Broeck J, Smagghe G, Swevers L. PIWI pathway against viruses in insects. Wiley Interdiscip Rev RNA. 2019; 10:e1555. doi: 10.1002/wrna.1555 KolliopoulouA SantosD TaningCNT WynantN Vanden BroeckJ SmaggheG SweversL PIWI pathway against viruses in insects Wiley Interdiscip Rev RNA 2019 10 e1555 10.1002/wrna.1555 31183996 Open DOISearch in Google Scholar

[100] Henaoui IS, Jacovetti C, Mollet IG, Guay C, Sobel J, Eliasson L, Regazzi R. PIWI-interacting RNAs as novel regulators of pancreatic beta cell function. Diabetologia. 2017; 60:1977–86. HenaouiIS JacovettiC MolletIG GuayC SobelJ EliassonL RegazziR PIWI-interacting RNAs as novel regulators of pancreatic beta cell function Diabetologia 2017 60 1977 86 10.1007/s00125-017-4368-228711973 Search in Google Scholar

[101] Zhou S, Yang S, Li F, Hou J, Chang H. P-element Induced WImpy protein-like RNA-mediated gene silencing 2 regulates tumor cell progression, apoptosis, and metastasis in oral squamous cell carcinoma. J Int Med Res. 2021; 49:3000605211053158. doi: 10.1177/03000605211053158 ZhouS YangS LiF HouJ ChangH P-element Induced WImpy protein-like RNA-mediated gene silencing 2 regulates tumor cell progression, apoptosis, and metastasis in oral squamous cell carcinoma J Int Med Res 2021 49 3000605211053158. 10.1177/03000605211053158 857351834738477 Open DOISearch in Google Scholar

[102] Xie K, Zhang K, Kong J, Wang C, Gu Y, Liang C, et al. Cancer-testis gene PIWIL1 promotes cell proliferation, migration, and invasion in lung adenocarcinoma. Cancer Med. 2018; 7:157–66. XieK ZhangK KongJ WangC GuY LiangC Cancer-testis gene PIWIL1 promotes cell proliferation, migration, and invasion in lung adenocarcinoma Cancer Med 2018 7 157 66 10.1002/cam4.1248577400229168346 Search in Google Scholar

[103] Yao J, Wang YW, Fang BB, Zhang SJ, Cheng BL. piR-651 and its function in 95-D lung cancer cells. Biomed Rep. 2016; 4:546–50. YaoJ WangYW FangBB ZhangSJ ChengBL piR-651 and its function in 95-D lung cancer cells Biomed Rep 2016 4 546 50 10.3892/br.2016.628484078327123245 Search in Google Scholar

[104] Zhang S-J, Yao J, Shen B-Z, Li G-B, Kong S-S, Bi D-D, et al. Role of piwi-interacting RNA-651 in the carcinogenesis of non-small cell lung cancer. Oncol Lett. 2018; 15:940–6. ZhangS-J YaoJ ShenB-Z LiG-B KongS-S BiD-D Role of piwi-interacting RNA-651 in the carcinogenesis of non-small cell lung cancer Oncol Lett 2018 15 940 6 10.3892/ol.2017.7406577278829399156 Search in Google Scholar

[105] Li D, Luo Y, Gao Y, Yang Y, Wang Y, Xu Y, et al. piR-651 promotes tumor formation in non-small cell lung carcinoma through the upregulation of cyclin D1 and CDK4. Int J Mol Med. 2016; 38:927–36. LiD LuoY GaoY YangY WangY XuY piR-651 promotes tumor formation in non-small cell lung carcinoma through the upregulation of cyclin D1 and CDK4 Int J Mol Med 2016 38 927 36 10.3892/ijmm.2016.267127431575 Search in Google Scholar

[106] Reeves ME, Firek M, Jliedi A, Amaar YG. Identification and characterization of RASSF1C piRNA target genes in lung cancer cells. Oncotarget. 2017; 8:34268–82. ReevesME FirekM JliediA AmaarYG Identification and characterization of RASSF1C piRNA target genes in lung cancer cells Oncotarget 2017 8 34268 82 10.18632/oncotarget.15965547096628423657 Search in Google Scholar

[107] Chen S, Ben S, Xin J, Li S, Zheng R, Wang H, et al. The biogenesis and biological function of PIWI-interacting RNA in cancer. J Hematol Oncol. 2021; 14:93. doi: 10.1186/s13045-021-01104-3 ChenS BenS XinJ LiS ZhengR WangH The biogenesis and biological function of PIWI-interacting RNA in cancer J Hematol Oncol 2021 14 93 10.1186/s13045-021-01104-3 819980834118972 Open DOISearch in Google Scholar

[108] Rui, Y. piRNAs variants and lung cancer risk: a post-GWAS study [Masters Public Health thesis]. New Haven (CI): Yale Univ; 2016. Available from: https://elischolar.library.yale.edu/ysphtdl/1335 RuiY. piRNAs variants and lung cancer risk: a post-GWAS study [Masters Public Health thesis] New Haven (CI) Yale Univ 2016 Available from: https://elischolar.library.yale.edu/ysphtdl/1335 Search in Google Scholar

[109] Liang D, Dong M, Hu L-J, Fang Z-H, Xu X, Shi E-H, Yang Y-J. Hiwi knockdown inhibits the growth of lung cancer in nude mice. Asian Pac J Cancer Prev. 2013; 14:1067–72. LiangD DongM HuL-J FangZ-H XuX ShiE-H YangY-J Hiwi knockdown inhibits the growth of lung cancer in nude mice Asian Pac J Cancer Prev 2013 14 1067 72 10.7314/APJCP.2013.14.2.106723621188 Search in Google Scholar

[110] Reeves ME, Firek M, Chen ST, Amaar YG. Evidence that RASSF1C stimulation of lung cancer cell proliferation depends on IGFBP-5 and PIWIL1 expression levels. PloS One. 2014; 9:e101679. doi: 10.1371/journal.pone.0101679 ReevesME FirekM ChenST AmaarYG Evidence that RASSF1C stimulation of lung cancer cell proliferation depends on IGFBP-5 and PIWIL1 expression levels PloS One 2014 9 e101679 10.1371/journal.pone.0101679 409014825007054 Open DOISearch in Google Scholar

[111] Wang Y, Gable T, Ma MZ, Clark D, Zhao J, Zhang Y, et al. A piRNA-like small RNA induces chemoresistance to cisplatin-based therapy by inhibiting apoptosis in lung squamous cell carcinoma. Mol Ther Nucleic Acids. 2017; 6:269–78. WangY GableT MaMZ ClarkD ZhaoJ ZhangY A piRNA-like small RNA induces chemoresistance to cisplatin-based therapy by inhibiting apoptosis in lung squamous cell carcinoma Mol Ther Nucleic Acids 2017 6 269 78 10.1016/j.omtn.2017.01.003536350928325293 Search in Google Scholar

[112] Brock M, Mei Y. Protein functional effector sncRNAs (pfeRNAs) in lung cancer. Cancer Lett. 2017; 403:138–43. BrockM MeiY Protein functional effector sncRNAs (pfeRNAs) in lung cancer Cancer Lett 2017 403 138 43 10.1016/j.canlet.2017.06.01328642173 Search in Google Scholar

[113] Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646–74. HanahanD WeinbergRA Hallmarks of cancer: the next generation Cell 2011 144 646 74 10.1016/j.cell.2011.02.01321376230 Search in Google Scholar