Skip to main content
Top
Published in: Cancer Cell International 1/2021

Open Access 01-12-2021 | Colorectal Cancer | Review

Epigenetic roles of PIWI proteins and piRNAs in colorectal cancer

Authors: Fatemeh Sadoughi, Seyyed Mehdi Mirhashemi, Zatollah Asemi

Published in: Cancer Cell International | Issue 1/2021

Login to get access

Abstract

Small non‐coding RNAs (sncRNAs) are a subgroup of non‐coding RNAs, with less than 200 nucleotides length and no potential for coding proteins. PiRNAs, a member of sncRNAs, were first discovered more than a decade ago and have attracted researcher’s attention because of their gene regulatory function both in the nucleus and in the cytoplasm. Recent investigations have found that the abnormal expression of these sncRNAs is involved in many human diseases, including cancers. Colorectal cancer (CRC), as a common gastrointestinal malignancy, is one of the important causes of cancer‐related deaths through the entire world and appears to be a consequence of mutation in the genome and epigenetic alterations. The aim of this review is to realize whether there is a relationship between CRC and piRNAs or not.
Literature
1.
go back to reference Watson CN, Belli A, Di Pietro V. Small non-coding RNAs: new class of biomarkers and potential therapeutic targets in neurodegenerative disease. Front Genet. 2019;10:364.PubMedPubMedCentralCrossRef Watson CN, Belli A, Di Pietro V. Small non-coding RNAs: new class of biomarkers and potential therapeutic targets in neurodegenerative disease. Front Genet. 2019;10:364.PubMedPubMedCentralCrossRef
2.
go back to reference Hombach S, Kretz M. Non-coding RNAs: classification, biology and functioning. Adv Exp Med Biol. 2016;937:3–17.PubMedCrossRef Hombach S, Kretz M. Non-coding RNAs: classification, biology and functioning. Adv Exp Med Biol. 2016;937:3–17.PubMedCrossRef
4.
go back to reference Genomics PE. ENCODE project writes eulogy for junk DNA. Science. 2012;337(1159):61. Genomics PE. ENCODE project writes eulogy for junk DNA. Science. 2012;337(1159):61.
5.
go back to reference Han YN, Li Y, Xia SQ, Zhang YY, Zheng JH, Li W. PIWI proteins and PIWI-interacting rna: emerging roles in cancer. Cell Physiol Biochem. 2017;44:1–20.PubMedCrossRef Han YN, Li Y, Xia SQ, Zhang YY, Zheng JH, Li W. PIWI proteins and PIWI-interacting rna: emerging roles in cancer. Cell Physiol Biochem. 2017;44:1–20.PubMedCrossRef
8.
go back to reference Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol. 2011;12:246–58.PubMedCrossRef Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol. 2011;12:246–58.PubMedCrossRef
9.
go back to reference Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, et al. The small RNA profile during Drosophila melanogaster development. Dev Cell. 2003;5:337–50.PubMedCrossRef Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, et al. The small RNA profile during Drosophila melanogaster development. Dev Cell. 2003;5:337–50.PubMedCrossRef
10.
go back to reference Theurkauf WE, Klattenhoff C, Bratu DP, McGinnis-Schultz N, Koppetsch BS, Cook HA. rasiRNAs, DNA damage, and embryonic axis specification. Cold Spring Harb Symp Quant Biol. 2006;71:171–80.PubMedCrossRef Theurkauf WE, Klattenhoff C, Bratu DP, McGinnis-Schultz N, Koppetsch BS, Cook HA. rasiRNAs, DNA damage, and embryonic axis specification. Cold Spring Harb Symp Quant Biol. 2006;71:171–80.PubMedCrossRef
13.
go back to reference Iwasaki YW, Siomi MC, Siomi H. PIWI-interacting RNA: Its biogenesis and functions. Annu Rev Biochem. 2015;84:405–33.PubMedCrossRef Iwasaki YW, Siomi MC, Siomi H. PIWI-interacting RNA: Its biogenesis and functions. Annu Rev Biochem. 2015;84:405–33.PubMedCrossRef
14.
15.
go back to reference World Cancer Research Fund. Global cancer incidence: both sexes. 2018. World Cancer Research Fund. Global cancer incidence: both sexes. 2018.
16.
go back to reference Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 2019;16:713–32.PubMedCrossRef Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 2019;16:713–32.PubMedCrossRef
17.
go back to reference Song M, Chan AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology. 2020;158:322–40.PubMedCrossRef Song M, Chan AT, Sun J. Influence of the gut microbiome, diet, and environment on risk of colorectal cancer. Gastroenterology. 2020;158:322–40.PubMedCrossRef
18.
go back to reference Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI, Levin B, et al. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control. 2013;24:1207–22.PubMedPubMedCentralCrossRef Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI, Levin B, et al. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control. 2013;24:1207–22.PubMedPubMedCentralCrossRef
20.
go back to reference Ning Y, Wang L, Giovannucci EL. A quantitative analysis of body mass index and colorectal cancer: findings from 56 observational studies. Obes Rev. 2010;11:19–30.PubMedCrossRef Ning Y, Wang L, Giovannucci EL. A quantitative analysis of body mass index and colorectal cancer: findings from 56 observational studies. Obes Rev. 2010;11:19–30.PubMedCrossRef
21.
22.
go back to reference Yamashiro H, Siomi MC. PIWI-interacting RNA in drosophila: biogenesis, transposon regulation, and beyond. Chem Rev. 2018;118:4404–21.PubMedCrossRef Yamashiro H, Siomi MC. PIWI-interacting RNA in drosophila: biogenesis, transposon regulation, and beyond. Chem Rev. 2018;118:4404–21.PubMedCrossRef
23.
go back to reference Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006;442:199–202.PubMedCrossRef Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006;442:199–202.PubMedCrossRef
24.
go back to reference Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell. 2013;50:736–48.PubMedPubMedCentralCrossRef Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell. 2013;50:736–48.PubMedPubMedCentralCrossRef
25.
go back to reference Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006;442:203–7.PubMedCrossRef Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006;442:203–7.PubMedCrossRef
26.
27.
go back to reference Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature. 2012;491:284–7.PubMedCrossRef Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature. 2012;491:284–7.PubMedCrossRef
28.
go back to reference Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, et al. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 2010;24:2493–8.PubMedPubMedCentralCrossRef Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, et al. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 2010;24:2493–8.PubMedPubMedCentralCrossRef
29.
go back to reference Zamparini AL, Davis MY, Malone CD, Vieira E, Zavadil J, Sachidanandam R, et al. Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila. Development. 2011;138:4039–50.PubMedPubMedCentralCrossRef Zamparini AL, Davis MY, Malone CD, Vieira E, Zavadil J, Sachidanandam R, et al. Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila. Development. 2011;138:4039–50.PubMedPubMedCentralCrossRef
30.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
31.
go back to reference Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128:1089–103.PubMedCrossRef Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128:1089–103.PubMedCrossRef
32.
go back to reference Luteijn MJ, Ketting RF. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat Rev Genet. 2013;14:523–34.PubMedCrossRef Luteijn MJ, Ketting RF. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat Rev Genet. 2013;14:523–34.PubMedCrossRef
33.
go back to reference Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, et al. A slicer-mediated mechanism for repeat-associated siRNA 5’ end formation in Drosophila. Science. 2007;315:1587–90.PubMedCrossRef Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, et al. A slicer-mediated mechanism for repeat-associated siRNA 5’ end formation in Drosophila. Science. 2007;315:1587–90.PubMedCrossRef
35.
go back to reference Feltzin VL, Khaladkar M, Abe M, Parisi M, Hendriks GJ, Kim J, et al. The exonuclease Nibbler regulates age-associated traits and modulates pi RNA length in D rosophila. Aging Cell. 2015;14:443–52.PubMedPubMedCentralCrossRef Feltzin VL, Khaladkar M, Abe M, Parisi M, Hendriks GJ, Kim J, et al. The exonuclease Nibbler regulates age-associated traits and modulates pi RNA length in D rosophila. Aging Cell. 2015;14:443–52.PubMedPubMedCentralCrossRef
36.
37.
go back to reference Patil VS, Kai T. Repression of retroelements in Drosophila germline via piRNA pathway by the Tudor domain protein Tejas. Curr Biol. 2010;20:724–30.PubMedCrossRef Patil VS, Kai T. Repression of retroelements in Drosophila germline via piRNA pathway by the Tudor domain protein Tejas. Curr Biol. 2010;20:724–30.PubMedCrossRef
38.
go back to reference Anand A, Kai T. The tudor domain protein kumo is required to assemble the nuage and to generate germline piRNAs in Drosophila. EMBO J. 2012;31:870–82.PubMedCrossRef Anand A, Kai T. The tudor domain protein kumo is required to assemble the nuage and to generate germline piRNAs in Drosophila. EMBO J. 2012;31:870–82.PubMedCrossRef
39.
go back to reference Ott KM, Nguyen T, Navarro C. The DExH box helicase domain of spindle-E is necessary for retrotransposon silencing and axial patterning during Drosophila oogenesis. G3: Genes, Genomes, Genetics. 2014. 4:2247–2257. Ott KM, Nguyen T, Navarro C. The DExH box helicase domain of spindle-E is necessary for retrotransposon silencing and axial patterning during Drosophila oogenesis. G3: Genes, Genomes, Genetics. 2014. 4:2247–2257.
40.
41.
go back to reference Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31:785–99.PubMedPubMedCentralCrossRef Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31:785–99.PubMedPubMedCentralCrossRef
43.
45.
go back to reference Chenais B. Transposable elements and human cancer: a causal relationship? Biochim Biophys Acta. 2013;1835:28–35.PubMed Chenais B. Transposable elements and human cancer: a causal relationship? Biochim Biophys Acta. 2013;1835:28–35.PubMed
46.
go back to reference Konkel MK, Batzer MA. A mobile threat to genome stability: The impact of non-LTR retrotransposons upon the human genome. Semin Cancer Biol. 2010;20:211–21.PubMedPubMedCentralCrossRef Konkel MK, Batzer MA. A mobile threat to genome stability: The impact of non-LTR retrotransposons upon the human genome. Semin Cancer Biol. 2010;20:211–21.PubMedPubMedCentralCrossRef
47.
go back to reference Klenov MS, Lavrov SA, Korbut AP, Stolyarenko AD, Yakushev EY, Reuter M, et al. Impact of nuclear Piwi elimination on chromatin state in Drosophila melanogaster ovaries. Nucleic Acids Res. 2014;42:6208–18.PubMedPubMedCentralCrossRef Klenov MS, Lavrov SA, Korbut AP, Stolyarenko AD, Yakushev EY, Reuter M, et al. Impact of nuclear Piwi elimination on chromatin state in Drosophila melanogaster ovaries. Nucleic Acids Res. 2014;42:6208–18.PubMedPubMedCentralCrossRef
48.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
49.
go back to reference Mukandavire Z, Liao S, Wang J, Gaff H, Smith DL, Morris JG. Estimating the reproductive numbers for the 2008–2009 cholera outbreaks in Zimbabwe. Proc Natl Acad Sci. 2011;108:8767–72.PubMedPubMedCentralCrossRef Mukandavire Z, Liao S, Wang J, Gaff H, Smith DL, Morris JG. Estimating the reproductive numbers for the 2008–2009 cholera outbreaks in Zimbabwe. Proc Natl Acad Sci. 2011;108:8767–72.PubMedPubMedCentralCrossRef
50.
go back to reference Sienski G, Dönertas D, Brennecke J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 2012;151:964–80.PubMedPubMedCentralCrossRef Sienski G, Dönertas D, Brennecke J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 2012;151:964–80.PubMedPubMedCentralCrossRef
51.
52.
go back to reference Iwasaki YW, Murano K, Ishizu H, Shibuya A, Iyoda Y, Siomi MC, et al. Piwi modulates chromatin accessibility by regulating multiple factors including histone H1 to repress transposons. Mol Cell. 2016;63:408–19.PubMedCrossRef Iwasaki YW, Murano K, Ishizu H, Shibuya A, Iyoda Y, Siomi MC, et al. Piwi modulates chromatin accessibility by regulating multiple factors including histone H1 to repress transposons. Mol Cell. 2016;63:408–19.PubMedCrossRef
53.
go back to reference Lin H, Yin H, editors. A novel epigenetic mechanism in Drosophila somatic cells mediated by Piwi and piRNAs. Cold Spring Harbor symposia on quantitative biology; 2008. Cold Spring Harbor Laboratory Press. Lin H, Yin H, editors. A novel epigenetic mechanism in Drosophila somatic cells mediated by Piwi and piRNAs. Cold Spring Harbor symposia on quantitative biology; 2008. Cold Spring Harbor Laboratory Press.
54.
go back to reference Yin H, Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature. 2007;450:304.PubMedCrossRef Yin H, Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature. 2007;450:304.PubMedCrossRef
55.
go back to reference Meller VH, Joshi SS, Deshpande N. Modulation of chromatin by noncoding RNA. Annu Rev Genet. 2015;49:673–95.PubMedCrossRef Meller VH, Joshi SS, Deshpande N. Modulation of chromatin by noncoding RNA. Annu Rev Genet. 2015;49:673–95.PubMedCrossRef
56.
go back to reference Esposito T, Magliocca S, Formicola D, Gianfrancesco F. piR_015520 belongs to Piwi-associated RNAs regulates expression of the human melatonin receptor 1A gene. PLoS ONE. 2011;6:e22727.PubMedPubMedCentralCrossRef Esposito T, Magliocca S, Formicola D, Gianfrancesco F. piR_015520 belongs to Piwi-associated RNAs regulates expression of the human melatonin receptor 1A gene. PLoS ONE. 2011;6:e22727.PubMedPubMedCentralCrossRef
58.
go back to reference Kim VN. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev. 2006;20:1993–7.PubMedCrossRef Kim VN. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev. 2006;20:1993–7.PubMedCrossRef
59.
go back to reference Wang QX, Zhu YQ, Zhang H, Xiao J. Altered MiRNA expression in gastric cancer: a systematic review and meta-analysis. Cell Physiol Biochem. 2015;35:933–44.PubMedCrossRef Wang QX, Zhu YQ, Zhang H, Xiao J. Altered MiRNA expression in gastric cancer: a systematic review and meta-analysis. Cell Physiol Biochem. 2015;35:933–44.PubMedCrossRef
60.
go back to reference Feldman N, Gerson A, Fang J, Li E, Zhang Y, Shinkai Y, et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol. 2006;8:188–94.PubMedCrossRef Feldman N, Gerson A, Fang J, Li E, Zhang Y, Shinkai Y, et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol. 2006;8:188–94.PubMedCrossRef
61.
go back to reference Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim Biophys Acta. 2007;1775:138–62.PubMed Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim Biophys Acta. 2007;1775:138–62.PubMed
62.
go back to reference Guo Z, Maki M, Ding R, Yang Y, Zhang B, Xiong L. Genome-wide survey of tissue-specific microRNA and transcription factor regulatory networks in 12 tissues. Sci Rep. 2014;4:5150.PubMedPubMedCentralCrossRef Guo Z, Maki M, Ding R, Yang Y, Zhang B, Xiong L. Genome-wide survey of tissue-specific microRNA and transcription factor regulatory networks in 12 tissues. Sci Rep. 2014;4:5150.PubMedPubMedCentralCrossRef
63.
go back to reference Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8:286–98.PubMedCrossRef Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8:286–98.PubMedCrossRef
64.
65.
go back to reference Siddiqi S, Matushansky I. Piwis and piwi-interacting RNAs in the epigenetics of cancer. J Cell Biochem. 2012;113:373–80.PubMedCrossRef Siddiqi S, Matushansky I. Piwis and piwi-interacting RNAs in the epigenetics of cancer. J Cell Biochem. 2012;113:373–80.PubMedCrossRef
66.
go back to reference Martinez VD, Vucic EA, Thu KL, Hubaux R, Enfield KS, Pikor LA, et al. Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology. Sci Rep. 2015;5:10423.PubMedPubMedCentralCrossRef Martinez VD, Vucic EA, Thu KL, Hubaux R, Enfield KS, Pikor LA, et al. Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology. Sci Rep. 2015;5:10423.PubMedPubMedCentralCrossRef
67.
go back to reference Lee JH, Engel W, Nayernia K. Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Mol Reprod Dev. 2006;73:173–9.PubMedCrossRef Lee JH, Engel W, Nayernia K. Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Mol Reprod Dev. 2006;73:173–9.PubMedCrossRef
68.
go back to reference Sasaki T, Shiohama A, Minoshima S, Shimizu N. Identification of eight members of the Argonaute family in the human genome. Genomics. 2003;82:323–30.PubMedCrossRef Sasaki T, Shiohama A, Minoshima S, Shimizu N. Identification of eight members of the Argonaute family in the human genome. Genomics. 2003;82:323–30.PubMedCrossRef
69.
go back to reference Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi-Miyagawa S, Nakano T, et al. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem. 2009;284:6507–19.PubMedPubMedCentralCrossRef Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi-Miyagawa S, Nakano T, et al. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem. 2009;284:6507–19.PubMedPubMedCentralCrossRef
70.
go back to reference Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 2002;16:2733–42.PubMedCrossRef Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 2002;16:2733–42.PubMedCrossRef
71.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
72.
go back to reference Yan H, Wu QL, Sun CY, Ai LS, 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.PubMedCrossRef Yan H, Wu QL, Sun CY, Ai LS, 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.PubMedCrossRef
73.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
74.
go back to reference Liang D, Yang Y, Liu Y. The role Hiwi gene in the maintenance of lung cancer stem cell populations. Neoplasma. 2013. Liang D, Yang Y, Liu Y. The role Hiwi gene in the maintenance of lung cancer stem cell populations. Neoplasma. 2013.
75.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
76.
go back to reference Qiao D, Zeeman AM, Deng W, Looijenga LH, 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.PubMedCrossRef Qiao D, Zeeman AM, Deng W, Looijenga LH, 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.PubMedCrossRef
78.
go back to reference Taubert H, Greither T, Kaushal D, Wurl 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.PubMedCrossRef Taubert H, Greither T, Kaushal D, Wurl 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.PubMedCrossRef
79.
go back to reference Wang DW, Wang ZH, Wang LL, Song Y, Zhang GZ. Overexpression of hiwi promotes growth of human breast cancer cells. Asian Pac J Cancer Prev. 2014;15:7553–8.PubMedCrossRef Wang DW, Wang ZH, Wang LL, Song Y, Zhang GZ. Overexpression of hiwi promotes growth of human breast cancer cells. Asian Pac J Cancer Prev. 2014;15:7553–8.PubMedCrossRef
80.
go back to reference Wang X, Tong X, Gao H, Yan X, Xu X, Sun S, et al. Silencing HIWI suppresses the growth, invasion and migration of glioma cells. Int J Oncol. 2014;45:2385–92.PubMedCrossRef Wang X, Tong X, Gao H, Yan X, Xu X, Sun S, et al. Silencing HIWI suppresses the growth, invasion and migration of glioma cells. Int J Oncol. 2014;45:2385–92.PubMedCrossRef
81.
go back to reference 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. 2015;11:1455–61.PubMedCrossRef 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. 2015;11:1455–61.PubMedCrossRef
82.
go back to reference Lee JH, Schutte D, Wulf G, Fuzesi L, Radzun HJ, Schweyer S, et al. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Genet. 2006;15:201–11.PubMedCrossRef Lee JH, Schutte D, Wulf G, Fuzesi L, Radzun HJ, Schweyer S, et al. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Genet. 2006;15:201–11.PubMedCrossRef
83.
go back to reference Lu Y, Zhang K, Li C, Yao Y, Tao D, Liu Y, et al. Piwil2 suppresses p53 by inducing phosphorylation of signal transducer and activator of transcription 3 in tumor cells. PLoS ONE. 2012;7:e30999.PubMedPubMedCentralCrossRef Lu Y, Zhang K, Li C, Yao Y, Tao D, Liu Y, et al. Piwil2 suppresses p53 by inducing phosphorylation of signal transducer and activator of transcription 3 in tumor cells. PLoS ONE. 2012;7:e30999.PubMedPubMedCentralCrossRef
84.
go back to reference Su C, Ren ZJ, 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;586:1356–62.PubMedCrossRef Su C, Ren ZJ, 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;586:1356–62.PubMedCrossRef
85.
go back to reference Sugimoto K, Kage H, Aki N, Sano A, Kitagawa H, Nagase T, et al. The induction of H3K9 methylation by PIWIL4 at the p16Ink4a locus. Biochem Biophys Res Commun. 2007;359:497–502.PubMedCrossRef Sugimoto K, Kage H, Aki N, Sano A, Kitagawa H, Nagase T, et al. The induction of H3K9 methylation by PIWIL4 at the p16Ink4a locus. Biochem Biophys Res Commun. 2007;359:497–502.PubMedCrossRef
86.
go back to reference Huang G, Hu H, Xue X, Shen S, Gao E, Guo G, et al. Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol. 2013;15:563–8.PubMedCrossRef Huang G, Hu H, Xue X, Shen S, Gao E, Guo G, et al. Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol. 2013;15:563–8.PubMedCrossRef
87.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
88.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
89.
go back to reference Cheng J, Deng H, Xiao B, Zhou H, Zhou F, Shen Z, et al. 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.PubMedCrossRef Cheng J, Deng H, Xiao B, Zhou H, Zhou F, Shen Z, et al. 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.PubMedCrossRef
90.
go back to reference Cui L, Lou Y, Zhang X, Zhou H, Deng H, Song H, et al. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using piRNAs as markers. Clin Biochem. 2011;44:1050–7.PubMedCrossRef Cui L, Lou Y, Zhang X, Zhou H, Deng H, Song H, et al. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using piRNAs as markers. Clin Biochem. 2011;44:1050–7.PubMedCrossRef
91.
go back to reference Li Y, Wu X, Gao H, Jin JM, Li AX, Kim YS, et al. Piwi-Interacting RNAs (piRNAs) are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer-specific survival. Mol Med. 2015;21:381–8.PubMedPubMedCentralCrossRef Li Y, Wu X, Gao H, Jin JM, Li AX, Kim YS, et al. Piwi-Interacting RNAs (piRNAs) are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer-specific survival. Mol Med. 2015;21:381–8.PubMedPubMedCentralCrossRef
92.
go back to reference Law PT, Qin H, Ching AK, Lai KP, Co NN, He M, et al. Deep sequencing of small RNA transcriptome reveals novel non-coding RNAs in hepatocellular carcinoma. J Hepatol. 2013;58:1165–73.PubMedCrossRef Law PT, Qin H, Ching AK, Lai KP, Co NN, He M, et al. Deep sequencing of small RNA transcriptome reveals novel non-coding RNAs in hepatocellular carcinoma. J Hepatol. 2013;58:1165–73.PubMedCrossRef
93.
go back to reference Lim SL, Ricciardelli C, Oehler MK, Tan IM, Russell D, Grutzner F. Overexpression of piRNA pathway genes in epithelial ovarian cancer. PLoS ONE. 2014;9:e99687.PubMedPubMedCentralCrossRef Lim SL, Ricciardelli C, Oehler MK, Tan IM, Russell D, Grutzner F. Overexpression of piRNA pathway genes in epithelial ovarian cancer. PLoS ONE. 2014;9:e99687.PubMedPubMedCentralCrossRef
94.
go back to reference Li D, Sun X, Yan D, Huang J, Luo Q, Tang H, et al. 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.CrossRef Li D, Sun X, Yan D, Huang J, Luo Q, Tang H, et al. 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.CrossRef
95.
go back to reference El Bairi K, Tariq K, Himri I, Jaafari A, Smaili W, Kandhro AH, et al. Decoding colorectal cancer epigenomics. Cancer Genet. 2018;220:49–76.PubMedCrossRef El Bairi K, Tariq K, Himri I, Jaafari A, Smaili W, Kandhro AH, et al. Decoding colorectal cancer epigenomics. Cancer Genet. 2018;220:49–76.PubMedCrossRef
97.
go back to reference Migliore L, Migheli F, Spisni R, Coppede F. Genetics, cytogenetics, and epigenetics of colorectal cancer. J Biomed Biotechnol. 2011;2011:792362. Migliore L, Migheli F, Spisni R, Coppede F. Genetics, cytogenetics, and epigenetics of colorectal cancer. J Biomed Biotechnol. 2011;2011:792362.
98.
go back to reference Pellegrini ML, Argibay P. Gomez DE [Genetics and epigenetics of colorectal cancer]. Acta Gastroenterol Latinoam. 2011;41:247–61.PubMed Pellegrini ML, Argibay P. Gomez DE [Genetics and epigenetics of colorectal cancer]. Acta Gastroenterol Latinoam. 2011;41:247–61.PubMed
99.
go back to reference Porcellini E, Laprovitera N, Riefolo M, Ravaioli M, Garajova I, Ferracin M. Epigenetic and epitranscriptomic changes in colorectal cancer: Diagnostic, prognostic, and treatment implications. Cancer Lett. 2018;419:84–95.PubMedCrossRef Porcellini E, Laprovitera N, Riefolo M, Ravaioli M, Garajova I, Ferracin M. Epigenetic and epitranscriptomic changes in colorectal cancer: Diagnostic, prognostic, and treatment implications. Cancer Lett. 2018;419:84–95.PubMedCrossRef
100.
go back to reference Huang J, Peng J, Guo L. Non-coding RNA: a new tool for the diagnosis, prognosis, and therapy of small cell lung cancer. J Thorac Oncol. 2015;10:28–37.PubMedCrossRef Huang J, Peng J, Guo L. Non-coding RNA: a new tool for the diagnosis, prognosis, and therapy of small cell lung cancer. J Thorac Oncol. 2015;10:28–37.PubMedCrossRef
102.
go back to reference Li M, Izpisua Belmonte JC. Roles for noncoding RNAs in cell-fate determination and regeneration. Nat Struct Mol Biol. 2015;22:2–4.PubMedCrossRef Li M, Izpisua Belmonte JC. Roles for noncoding RNAs in cell-fate determination and regeneration. Nat Struct Mol Biol. 2015;22:2–4.PubMedCrossRef
103.
go back to reference Piccoli MT, Gupta SK, Thum T. Noncoding RNAs as regulators of cardiomyocyte proliferation and death. J Mol Cell Cardiol. 2015;89:59–67.PubMedCrossRef Piccoli MT, Gupta SK, Thum T. Noncoding RNAs as regulators of cardiomyocyte proliferation and death. J Mol Cell Cardiol. 2015;89:59–67.PubMedCrossRef
104.
go back to reference Zhong F, Zhou N, Wu K, Guo Y, Tan W, Zhang H, et al. A SnoRNA-derived piRNA interacts with human interleukin-4 pre-mRNA and induces its decay in nuclear exosomes. Nucleic Acids Res. 2015;43:10474–91.PubMedPubMedCentral Zhong F, Zhou N, Wu K, Guo Y, Tan W, Zhang H, et al. A SnoRNA-derived piRNA interacts with human interleukin-4 pre-mRNA and induces its decay in nuclear exosomes. Nucleic Acids Res. 2015;43:10474–91.PubMedPubMedCentral
106.
go back to reference Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012;26:2361–73.PubMedPubMedCentralCrossRef Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012;26:2361–73.PubMedPubMedCentralCrossRef
107.
go back to reference Zhang P, Kang JY, Gou LT, Wang J, Xue Y, Skogerboe G, et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 2015;25:193–207.PubMedPubMedCentralCrossRef Zhang P, Kang JY, Gou LT, Wang J, Xue Y, Skogerboe G, et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 2015;25:193–207.PubMedPubMedCentralCrossRef
108.
go back to reference Yin J, Jiang XY, Qi W, Ji CG, Xie XL, Zhang DX, et al. piR-823 contributes to colorectal tumorigenesis by enhancing the transcriptional activity of HSF1. Cancer Sci. 2017;108:1746–56.PubMedPubMedCentralCrossRef Yin J, Jiang XY, Qi W, Ji CG, Xie XL, Zhang DX, et al. piR-823 contributes to colorectal tumorigenesis by enhancing the transcriptional activity of HSF1. Cancer Sci. 2017;108:1746–56.PubMedPubMedCentralCrossRef
109.
go back to reference Al Zaid Siddiquee K, Turkson J. STAT3 as a target for inducing apoptosis in solid and hematological tumors. Cell Res. 2008.18:254–67. Al Zaid Siddiquee K, Turkson J. STAT3 as a target for inducing apoptosis in solid and hematological tumors. Cell Res. 2008.18:254–67.
111.
go back to reference Mai D, Ding P, Tan L, Zhang J, Pan Z, Bai R, et al. PIWI-interacting RNA-54265 is oncogenic and a potential therapeutic target in colorectal adenocarcinoma. Theranostics. 2018;8:5213–30.PubMedPubMedCentralCrossRef Mai D, Ding P, Tan L, Zhang J, Pan Z, Bai R, et al. PIWI-interacting RNA-54265 is oncogenic and a potential therapeutic target in colorectal adenocarcinoma. Theranostics. 2018;8:5213–30.PubMedPubMedCentralCrossRef
112.
go back to reference Mai D, Zheng Y, Guo H, Ding P, Bai R, Li M, et al. Serum piRNA-54265 is a new biomarker for early detection and clinical surveillance of human colorectal cancer. Theranostics. 2020;10:8468–78.PubMedPubMedCentralCrossRef Mai D, Zheng Y, Guo H, Ding P, Bai R, Li M, et al. Serum piRNA-54265 is a new biomarker for early detection and clinical surveillance of human colorectal cancer. Theranostics. 2020;10:8468–78.PubMedPubMedCentralCrossRef
113.
go back to reference Weng W, Liu N, Toiyama Y, Kusunoki M, Nagasaka T, Fujiwara T, et al. Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer. Mol Cancer. 2018;17:16.PubMedPubMedCentralCrossRef Weng W, Liu N, Toiyama Y, Kusunoki M, Nagasaka T, Fujiwara T, et al. Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer. Mol Cancer. 2018;17:16.PubMedPubMedCentralCrossRef
114.
go back to reference Cen H, Zheng S, Fang YM, Tang XP, Dong Q. Induction of HSF1 expression is associated with sporadic colorectal cancer. World J Gastroenterol. 2004;10:3122–6.PubMedPubMedCentralCrossRef Cen H, Zheng S, Fang YM, Tang XP, Dong Q. Induction of HSF1 expression is associated with sporadic colorectal cancer. World J Gastroenterol. 2004;10:3122–6.PubMedPubMedCentralCrossRef
115.
go back to reference Lianos GD, Alexiou GA, Mangano A, Mangano A, Rausei S, Boni L, et al. The role of heat shock proteins in cancer. Cancer Lett. 2015;360:114–8.PubMedCrossRef Lianos GD, Alexiou GA, Mangano A, Mangano A, Rausei S, Boni L, et al. The role of heat shock proteins in cancer. Cancer Lett. 2015;360:114–8.PubMedCrossRef
116.
go back to reference Beere HM. “The stress of dying”: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci. 2004;117:2641–51.PubMedCrossRef Beere HM. “The stress of dying”: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci. 2004;117:2641–51.PubMedCrossRef
117.
go back to reference Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci. 2006;31:164–72.PubMedCrossRef Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci. 2006;31:164–72.PubMedCrossRef
119.
go back to reference Sabbah NA, Abdalla WM, Mawla WA, AbdAlMonem N, Gharib AF, Abdul-Saboor A, et al. piRNA-823 Is a Unique Potential Diagnostic Non-Invasive Biomarker in Colorectal Cancer Patients. Genes. 2021;12. Sabbah NA, Abdalla WM, Mawla WA, AbdAlMonem N, Gharib AF, Abdul-Saboor A, et al. piRNA-823 Is a Unique Potential Diagnostic Non-Invasive Biomarker in Colorectal Cancer Patients. Genes. 2021;12.
120.
go back to reference Iyer DN, Wan TM, Man JH, Sin RW, Li X, Lo OS, et al. Small RNA Profiling of piRNAs in Colorectal Cancer Identifies Consistent Overexpression of piR-24000 That Correlates Clinically with an Aggressive Disease Phenotype. Cancers. 2020;12. Iyer DN, Wan TM, Man JH, Sin RW, Li X, Lo OS, et al. Small RNA Profiling of piRNAs in Colorectal Cancer Identifies Consistent Overexpression of piR-24000 That Correlates Clinically with an Aggressive Disease Phenotype. Cancers. 2020;12.
121.
go back to reference Koduru SV, Tiwari AK, Hazard SW, Mahajan M, Ravnic DJ. Exploration of small RNA-seq data for small non-coding RNAs in human colorectal cancer. J Genomics. 2017;5:16–31.PubMedPubMedCentralCrossRef Koduru SV, Tiwari AK, Hazard SW, Mahajan M, Ravnic DJ. Exploration of small RNA-seq data for small non-coding RNAs in human colorectal cancer. J Genomics. 2017;5:16–31.PubMedPubMedCentralCrossRef
122.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
123.
go back to reference Wang Z, Yang H, Ma D, Mu Y, Tan X, Hao Q, et al. Serum PIWI-interacting RNAs piR-020619 and piR-020450 are promising novel biomarkers for early detection of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2020;29:990–8.PubMedCrossRef Wang Z, Yang H, Ma D, Mu Y, Tan X, Hao Q, et al. Serum PIWI-interacting RNAs piR-020619 and piR-020450 are promising novel biomarkers for early detection of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2020;29:990–8.PubMedCrossRef
124.
go back to reference Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, Weller KP, et al. Human CD34(+) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood. 2001;97:426–34.PubMedCrossRef Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, Weller KP, et al. Human CD34(+) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood. 2001;97:426–34.PubMedCrossRef
125.
go back to reference Yang L, Bi L, Liu Q, Zhao M, Cao B, Li D, et al. Hiwi promotes the proliferation of colorectal cancer cells via upregulating global dna methylation. Dis Markers. 2015;2015:383056.PubMedPubMedCentralCrossRef Yang L, Bi L, Liu Q, Zhao M, Cao B, Li D, et al. Hiwi promotes the proliferation of colorectal cancer cells via upregulating global dna methylation. Dis Markers. 2015;2015:383056.PubMedPubMedCentralCrossRef
126.
go back to reference Zeng Y, Qu LK, Meng L, Liu CY, Dong B, Xing XF, et al. HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin Med J (Engl). 2011;124:2144–9. Zeng Y, Qu LK, Meng L, Liu CY, Dong B, Xing XF, et al. HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin Med J (Engl). 2011;124:2144–9.
127.
129.
go back to reference Klimenko OV, Shtilman M. Reprogramming of CaCo2 colorectal cancer cells after using the complex of poly-(N-vinylpyrrolidone) with small non-coding RNAs. Toxicol Rep. 2019;6:186–92.PubMedPubMedCentralCrossRef Klimenko OV, Shtilman M. Reprogramming of CaCo2 colorectal cancer cells after using the complex of poly-(N-vinylpyrrolidone) with small non-coding RNAs. Toxicol Rep. 2019;6:186–92.PubMedPubMedCentralCrossRef
130.
go back to reference Tosar JP, García-Silva MR, Cayota A. Circulating SNORD57 rather than piR-54265 is a promising biomarker for colorectal cancer: common pitfalls in the study of somatic piRNAs in cancer. RNA (New York, NY). 2021;27:403–10.CrossRef Tosar JP, García-Silva MR, Cayota A. Circulating SNORD57 rather than piR-54265 is a promising biomarker for colorectal cancer: common pitfalls in the study of somatic piRNAs in cancer. RNA (New York, NY). 2021;27:403–10.CrossRef
Metadata
Title
Epigenetic roles of PIWI proteins and piRNAs in colorectal cancer
Authors
Fatemeh Sadoughi
Seyyed Mehdi Mirhashemi
Zatollah Asemi
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2021
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-021-02034-3

Other articles of this Issue 1/2021

Cancer Cell International 1/2021 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine