Piwi-interacting RNAs (piRNAs) and Colorectal Carcinoma: Emerging Non-invasive diagnostic Biomarkers with Potential Therapeutic Target Based Clinical Implications

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Abstract

PIWI-interacting RNAs (piRNAs) constitute new small non-coding RNA molecules of around 24-31 nucleotides in length, mostly performing regulatory roles for the piwi protein family members. In recent times, developing evidence proposes that piRNAs are expressed in a tissue-specific way in various human tissues and act as moderate vital signalling pathways at the transcriptional or post-transcriptional level in addition to mammalian germline. Recent findings, however, show that the unusual expression of piRNAs is an exclusive and discrete feature in several diseases, including many human cancers. Recently, considerable evidence indicates that piRNAs could be dysregulated thus playing critical roles in tumorigenesis. The function and underlying mechanisms of piRNAs in cancer, particularly in colorectal carcinoma, are not fully understood to date. Abnormal expression of piRNAs is emerging as a critical player in cancer cell proliferation, apoptosis, invasion, and migration in vitro and in vivo. Functionally, piRNAs preserve genomic integrity and regulate the expression of downstream target genes through transcriptional or post-transcriptional mechanisms by repressing transposable elements' mobilization. However, little research has been done to check Piwi and piRNAs' potential role in cancer and preserve genome integrity by epigenetically silencing transposons via DNA methylation, especially in germline cancer stem cells. This review reveals emerging insights into piRNA functions in colorectal carcinoma, revealing novel findings behind various piRNA-mediated gene regulation mechanisms, biogenetic piRNA processes, and possible applications of piRNAs and piwi proteins in cancer diagnosis and their potential clinical significance in the treatment of colorectal carcinoma patients.

Keywords: piRNAs, piwi proteins, tumorigenesis, colorectal carcinoma, genomic integrity, gene regulation.

[1]
Liu P, Dong Y, Gu J, Puthiyakunnon S, Wu Y, Chen XG. Developmental piRNA profiles of the invasive vector mosquito Aedes albopictus. Parasit Vectors 2016; 9(1): 524.
[http://dx.doi.org/10.1186/s13071-016-1815-8] [PMID: 27686069]
[2]
Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature 2012; 489(7414): 101-8.
[http://dx.doi.org/10.1038/nature11233] [PMID: 22955620]
[3]
Aravin AA, Lagos-Quintana M, Yalcin A, et al. The small RNA profile during Drosophila melanogaster development. Dev Cell 2003; 5(2): 337-50.
[http://dx.doi.org/10.1016/S1534-5807(03)00228-4] [PMID: 12919683]
[4]
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.
[http://dx.doi.org/10.1101/sqb.2006.71.066] [PMID: 17381294]
[5]
Aravin A, Gaidatzis D, Pfeffer S, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006; 442(7099): 203-7.
[http://dx.doi.org/10.1038/nature04916] [PMID: 16751777]
[6]
Girard A, Sachidanandam R, Hannon GJ, Carmell MAA. A germline-specific class of small RNAs binds mammalian PIWI proteins. Nature 2006; 442(7099): 199-202.
[http://dx.doi.org/10.1038/nature04917] [PMID: 16751776]
[7]
Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006; 313(5785): 320-4.
[http://dx.doi.org/10.1126/science.1129333] [PMID: 16809489]
[8]
Lau NC, Seto AG, Kim J, et al. Characterization of the piRNA complex from rat testes. Science 2006; 313(5785): 363-7.
[http://dx.doi.org/10.1126/science.1130164] [PMID: 16778019]
[9]
Grivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 2006; 20(13): 1709-14.
[http://dx.doi.org/10.1101/gad.1434406] [PMID: 16766680]
[10]
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): 1-20.
[http://dx.doi.org/10.1159/000484541] [PMID: 29130960]
[11]
Liu Y, Dou M, Song X, et al. The emerging role of the piRNA/PIWI complex in cancer. Mol Cancer 2019; 18(1): 123.
[http://dx.doi.org/10.1186/s12943-019-1052-9] [PMID: 31399034]
[12]
Batista PJ, Ruby JG, Claycomb JM, et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 2008; 31(1): 67-78.
[http://dx.doi.org/10.1016/j.molcel.2008.06.002] [PMID: 18571452]
[13]
Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007; 316(5825): 744-7.
[http://dx.doi.org/10.1126/science.1142612] [PMID: 17446352]
[14]
Zhao S, Gou LT, Zhang M, et al. piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis. Dev Cell 2013; 24(1): 13-25.
[http://dx.doi.org/10.1016/j.devcel.2012.12.006] [PMID: 23328397]
[15]
Kozomara A, Griffiths-Jones S. miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014; 42(Database issue): D68-73.
[http://dx.doi.org/10.1093/nar/gkt1181] [PMID: 24275495]
[16]
Lu Y, Li C, Zhang K, et al. Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep 2010; 43(9): 635-41.
[http://dx.doi.org/10.5483/BMBRep.2010.43.9.635] [PMID: 20846497]
[17]
Cheng J, Guo JM, Xiao BX, et al. piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin Chim Acta 2011; 412(17-18): 1621-5.
[http://dx.doi.org/10.1016/j.cca.2011.05.015] [PMID: 21616063]
[18]
Huang G, Hu H, Xue X, et al. Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol 2013; 15(7): 563-8.
[http://dx.doi.org/10.1007/s12094-012-0966-0] [PMID: 23229900]
[19]
Reeves ME, Firek M, Jliedi A, Amaar YG. Identification and characterization of RASSF1C piRNA target genes in lung cancer cells. Oncotarget 2017; 8(21): 34268-82.
[http://dx.doi.org/10.18632/oncotarget.15965] [PMID: 28423657]
[20]
Lee JH, Jung C, Javadian-Elyaderani P, et al. Pathways of proliferation and antiapoptosis driven in breast cancer stem cells by stem cell protein piwil2. Cancer Res 2010; 70(11): 4569-79.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-2670] [PMID: 20460541]
[21]
Cheng J, Deng H, Xiao B, 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(1): 12-7.
[http://dx.doi.org/10.1016/j.canlet.2011.10.004] [PMID: 22047710]
[22]
Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144(5): 646-74.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[23]
Suzuki R, Honda S, Kirino Y. PIWI expression and function in cancer. Front Genet 2012; 3: 204.
[http://dx.doi.org/10.3389/fgene.2012.00204] [PMID: 23087701]
[24]
Costa FF, Le Blanc K, Brodin B. Concise review: Cancer/testis antigens, stem cells, and cancer. Stem Cells 2007; 25(3): 707-11.
[http://dx.doi.org/10.1634/stemcells.2006-0469] [PMID: 17138959]
[25]
Cheng YH, Wong EW, Cheng CY. Cancer/testis (CT) antigens, carcinogenesis and spermatogenesis. Spermatogenesis 2011; 1(3): 209-20.
[http://dx.doi.org/10.4161/spmg.1.3.17990] [PMID: 22319669]
[26]
Bamezai S, Rawat VP, Buske C. Concise review: The PIWI-piRNA axis: Pivotal beyond transposon silencing. Stem Cells 2012; 30(12): 2603-11.
[http://dx.doi.org/10.1002/stem.1237] [PMID: 22996918]
[27]
Watanabe T, Takeda A, Tsukiyama T, et al. Identification and characterization of two novel classes of small RNAs in the mouse germline: Retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 2006; 20(13): 1732-43.
[http://dx.doi.org/10.1101/gad.1425706] [PMID: 16766679]
[28]
Williams Z, Morozov P, Mihailovic A, et al. Discovery and characterization of piRNAs in the human fetal ovary. Cell Rep 2015; 13(4): 854-63.
[http://dx.doi.org/10.1016/j.celrep.2015.09.030] [PMID: 26489470]
[29]
Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: Progress and prospect. Annu Rev Cell Dev Biol 2009; 25: 355-76.
[http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175327] [PMID: 19575643]
[30]
Weick EM, Miska EA. piRNAs: From biogenesis to function. Development 2014; 141(18): 3458-71.
[http://dx.doi.org/10.1242/dev.094037] [PMID: 25183868]
[31]
Keam SP, Young PE, McCorkindale AL, et al. The human PIWI protein HIWI2 associates with tRNA-derived piRNAs in somatic cells. Nucleic Acids Res 2014; 42(14): 8984-95.
[http://dx.doi.org/10.1093/nar/gku620] [PMID: 25038252]
[32]
Zhong F, Zhou N, Wu K, 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(21): 10474-91.
[http://dx.doi.org/10.1093/nar/gkv954] [PMID: 26405199]
[33]
Krishnan P, Ghosh S, Wang B, et al. Genome-wide profiling of transfer RNAs and their role as novel prognostic markers for breast cancer. Sci Rep 2016; 6: 32843.
[http://dx.doi.org/10.1038/srep32843] [PMID: 27604545]
[34]
Olivieri D, Sykora MM, Sachidanandam R, Mechtler K, Brennecke J. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J 2010; 29(19): 3301-17.
[http://dx.doi.org/10.1038/emboj.2010.212] [PMID: 20818334]
[35]
Saito K, Ishizu H, Komai M, et al. Roles for the Yb body components armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 2010; 24(22): 2493-8.
[http://dx.doi.org/10.1101/gad.1989510] [PMID: 20966047]
[36]
Nishimasu H, Ishizu H, Saito K, et al. Structure and function of zucchini endoribonuclease in piRNA biogenesis. Nature 2012; 491(7423): 284-7.
[http://dx.doi.org/10.1038/nature11509] [PMID: 23064230]
[37]
Ipsaro JJ, Haase AD, Knott SR, Joshua-Tor L, Hannon GJ. The structural biochemistry of zucchini implicates it as a nuclease in piRNA biogenesis. Nature 2012; 491(7423): 279-83.
[http://dx.doi.org/10.1038/nature11502] [PMID: 23064227]
[38]
Ross RJ, Weiner MM, Lin H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature 2014; 505(7483): 353-9.
[http://dx.doi.org/10.1038/nature12987] [PMID: 24429634]
[39]
Han BW, Wang W, Li C, Weng Z, Zamore PD. Noncoding RNA. piRNA-guided transposon cleavage initiates zucchini-dependent, phased piRNA production. Science 2015; 348(6236): 817-21.
[http://dx.doi.org/10.1126/science.aaa1264] [PMID: 25977554]
[40]
Czech B, Hannon GJ. One loop to rule them all: The ping-pong cycle and piRNA-guided silencing. Trends Biochem Sci 2016; 41(4): 324-37.
[http://dx.doi.org/10.1016/j.tibs.2015.12.008] [PMID: 26810602]
[41]
Iwasaki YW, Siomi MC, Siomi H. PIWI-Interacting RNA: Its biogenesis and functions. Annu Rev Biochem 2015; 84: 405-33.
[http://dx.doi.org/10.1146/annurev-biochem-060614-034258] [PMID: 25747396]
[42]
Grishok A, Tabara H, Mello CC. Genetic requirements for inheritance of RNAi in C. elegans. Science 2000; 287(5462): 2494-7.
[http://dx.doi.org/10.1126/science.287.5462.2494] [PMID: 10741970]
[43]
Gao Y, Feng B, Han S, et al. MicroRNA-129 in human cancers: From Tumorigenesis to clinical treatment. Cell Physiol Biochem 2016; 39(6): 2186-202.
[http://dx.doi.org/10.1159/000447913] [PMID: 27802440]
[44]
Pak J, Fire A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 2007; 315(5809): 241-4.
[http://dx.doi.org/10.1126/science.1132839] [PMID: 17124291]
[45]
Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409(6818): 363-6.
[http://dx.doi.org/10.1038/35053110] [PMID: 11201747]
[46]
Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: The vanguard of genome defence. Nat Rev Mol Cell Biol 2011; 12(4): 246-58.
[http://dx.doi.org/10.1038/nrm3089] [PMID: 21427766]
[47]
Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136(2): 215-33.
[http://dx.doi.org/10.1016/j.cell.2009.01.002] [PMID: 19167326]
[48]
Brennecke J, Aravin AA, Stark A, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007; 128(6): 1089-103.
[http://dx.doi.org/10.1016/j.cell.2007.01.043] [PMID: 17346786]
[49]
Gu W, Lee HC, Chaves D, et al. CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell 2012; 151(7): 1488-500.
[http://dx.doi.org/10.1016/j.cell.2012.11.023] [PMID: 23260138]
[50]
Cecere G, Zheng GX, Mansisidor AR, Klymko KE, Grishok A. Promoters recognized by forkhead proteins exist for individual 21U-RNAs. Mol Cell 2012; 47(5): 734-45.
[http://dx.doi.org/10.1016/j.molcel.2012.06.021] [PMID: 22819322]
[51]
Luteijn MJ, Ketting RF. PIWI-interacting RNAs: From generation to transgenerational epigenetics. Nat Rev Genet 2013; 14(8): 523-34.
[http://dx.doi.org/10.1038/nrg3495] [PMID: 23797853]
[52]
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(25): 3988-99.
[http://dx.doi.org/10.1038/sj.onc.1205505] [PMID: 12037681]
[53]
Li D, Sun X, Yan D, 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(10): 1231-40.
[http://dx.doi.org/10.1258/ebm.2012.011380] [PMID: 23104504]
[54]
Liu X, Sun Y, Guo J, et al. Expression of HIWI gene in human gastric cancer was associated with proliferation of cancer cells. Int J Cancer 2006; 118(8): 1922-9.
[http://dx.doi.org/10.1002/ijc.21575] [PMID: 16287078]
[55]
Ye Y, Yin DT, Chen L, et al. Identification of Piwil2-like (PL2L) proteins that promote tumorigenesis. PLoS One 2010; 5(10): e13406.
[http://dx.doi.org/10.1371/journal.pone.0013406] [PMID: 20975993]
[56]
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(9): 1356-62.
[http://dx.doi.org/10.1016/j.febslet.2012.03.053] [PMID: 22483988]
[57]
Wang X, Tong X, Gao H, et al. Silencing HIWI suppresses the growth, invasion and migration of glioma cells. Int J Oncol 2014; 45(6): 2385-92.
[http://dx.doi.org/10.3892/ijo.2014.2673] [PMID: 25269862]
[58]
Lu Y, Zhang K, Li C, et al. Piwil2 suppresses p53 by inducing phosphorylation of signal transducer and activator of transcription 3 in tumor cells. PLoS One 2012; 7(1): e30999.
[http://dx.doi.org/10.1371/journal.pone.0030999] [PMID: 22303479]
[59]
Weng W, Li H, Goel A. PIWI-interacting RNAs (piRNAs) and cancer: Emerging biological concepts and potential clinical implications. BBA - Reviews on Cancer 2019; 1871: 160-9.
[60]
Oh SJ, Kim SM, Kim YO, Chang HK. Clinicopathologic implications of PIWIL2 expression in colorectal cancer. Korean J Pathol 2012; 46(4): 318-23.
[http://dx.doi.org/10.4132/KoreanJPathol.2012.46.4.318] [PMID: 23110023]
[61]
Li L, Yu C, Gao H, Li Y. Argonaute proteins: Potential biomarkers for human colon cancer. BMC Cancer 2010; 10: 38.
[http://dx.doi.org/10.1186/1471-2407-10-38] [PMID: 20146808]
[62]
Talmadge JE, Fidler IJ. AACR centennial series: The biology of cancer metastasis: Historical perspective. Cancer Res 2010; 70(14): 5649-69.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1040] [PMID: 20610625]
[63]
Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: Regulators of the tumor microenvironment. Cell 2010; 141(1): 52-67.
[http://dx.doi.org/10.1016/j.cell.2010.03.015] [PMID: 20371345]
[64]
Post C, Clark JP, Sytnikova YA, Chirn GW, Lau NC. The capacity of target silencing by Drosophila PIWI and piRNAs. RNA 2014; 20(12): 1977-86.
[http://dx.doi.org/10.1261/rna.046300.114] [PMID: 25336588]
[65]
Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 2008; 22(7): 908-17.
[http://dx.doi.org/10.1101/gad.1640708] [PMID: 18381894]
[66]
Chen Z, Che Q, He X, et al. Stem cell protein Piwil1 endowed endometrial cancer cells with stem-like properties via inducing epithelial-mesenchymal transition. BMC Cancer 2015; 15: 811.
[http://dx.doi.org/10.1186/s12885-015-1794-8] [PMID: 26506848]
[67]
Yao Y, Li C, Zhou X, et al. PIWIL2 induces c-Myc expression by interacting with NME2 and regulates c-Myc-mediated tumor cell proliferation. Oncotarget 2014; 5(18): 8466-77.
[http://dx.doi.org/10.18632/oncotarget.2327] [PMID: 25193865]
[68]
Qu X, Liu J, Zhong X, Li X, Zhang Q. PIWIL2 promotes progression of non-small cell lung cancer by inducing CDK2 and Cyclin A expression. J Transl Med 2015; 13: 301.
[http://dx.doi.org/10.1186/s12967-015-0666-y] [PMID: 26373553]
[69]
Yin J, Jiang XY, Qi W, et al. piR-823 contributes to colorectal tumorigenesis by enhancing the transcriptional activity of HSF1. Cancer Sci 2017; 108(9): 1746-56.
[http://dx.doi.org/10.1111/cas.13300] [PMID: 28618124]
[70]
Mai D, Ding P, Tan L, et al. PIWI-interacting RNA-54265 is oncogenic and a potential therapeutic target in colorectal adenocarcinoma. Theranostics 2018; 8(19): 5213-30.
[http://dx.doi.org/10.7150/thno.28001] [PMID: 30555542]
[71]
Siddiqi S, Terry M, Matushansky I. HIWI mediated tumorigenesis is associated with DNA hypermethylation. PLoS One 2012; 7(3): e33711.
[http://dx.doi.org/10.1371/journal.pone.0033711] [PMID: 22438986]
[72]
Levine AJ, Ting DT, Greenbaum BD. P53 and the defenses against genome instability caused by transposons and repetitive elements. BioEssays 2016; 38(6): 508-13.
[http://dx.doi.org/10.1002/bies.201600031] [PMID: 27172878]
[73]
Yin DT, Wang Q, Chen L, et al. Germline stem cell gene PIWIL2 mediates DNA repair through relaxation of chromatin. PLoS One 2011; 6(11): e27154.
[http://dx.doi.org/10.1371/journal.pone.0027154] [PMID: 22110608]
[74]
Kojima-Kita K, Kuramochi-Miyagawa S, Nagamori I, et al. MIWI2 as an effector of DNA methylation and gene silencing in embryonic male germ cells. Cell Rep 2016; 16(11): 2819-28.
[http://dx.doi.org/10.1016/j.celrep.2016.08.027] [PMID: 27626653]
[75]
Fu A, Jacobs DI, Zhu Y. Epigenome-wide analysis of piRNAs in gene-specific DNA methylation. RNA Biol 2014; 11(10): 1301-12.
[http://dx.doi.org/10.1080/15476286.2014.996091] [PMID: 25590657]
[76]
Yan H, Wu QL, Sun CY, et al. piRNA-823 contributes to tumorigenesis by regulating de novo DNA methylation and angiogenesis in multiple myeloma. Leukemia 2015; 29(1): 196-206.
[http://dx.doi.org/10.1038/leu.2014.135] [PMID: 24732595]
[77]
Le Thomas A, Rogers AK, Webster A, et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 2013; 27(4): 390-9.
[http://dx.doi.org/10.1101/gad.209841.112] [PMID: 23392610]
[78]
Ha H, Song J, Wang S, et al. A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. BMC Genomics 2014; 15(1): 545.
[http://dx.doi.org/10.1186/1471-2164-15-545] [PMID: 24981367]
[79]
Martinez VD, Vucic EA, Thu KL, et al. Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology. Sci Rep 2015; 5: 10423.
[http://dx.doi.org/10.1038/srep10423] [PMID: 26013764]
[80]
Zhang P, Kang JY, Gou LT, et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res 2015; 25(2): 193-207.
[http://dx.doi.org/10.1038/cr.2015.4] [PMID: 25582079]
[81]
Li D, Luo Y, Gao 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(3): 927-36.
[http://dx.doi.org/10.3892/ijmm.2016.2671] [PMID: 27431575]
[82]
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(5): 546-50.
[http://dx.doi.org/10.3892/br.2016.628] [PMID: 27123245]
[83]
Wang QE, Han C, Milum K, Wani AA. Stem cell protein Piwil2 modulates chromatin modifications upon cisplatin treatment. Mutat Res 2011; 708(1-2): 59-68.
[http://dx.doi.org/10.1016/j.mrfmmm.2011.02.001] [PMID: 21310163]
[84]
Dana H, Marmari V, Mahmoodi G, Mahmoodzadeh H, Ebrahimi M. CD166 as a stem cell marker? A potential target for therapy colorectal cancer? J Stem Cell Res Ther 2016; 1(6): 00041.
[http://dx.doi.org/10.15406/jsrt.2016.01.00041]
[85]
Zeng Y, Qu LK, Meng L, et al. HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin Med J (Engl) 2011; 124(14): 2144-9.
[PMID: 21933617]
[86]
Litwin M. Szczepaska-Buda A, Piotrowska A, Dzigiel P, Witkiewicz W. The meaning of PIWI proteins in cancer development. Oncol Lett 2017; 13(5): 3354-62.
[http://dx.doi.org/10.3892/ol.2017.5932] [PMID: 28529570]
[87]
Chu H, Xia L, Qiu X, et al. Genetic variants in noncoding PIWI-interacting RNA and colorectal cancer risk. Cancer 2015; 121(12): 2044-52.
[http://dx.doi.org/10.1002/cncr.29314] [PMID: 25740697]
[88]
Weng W, Liu N, Toiyama Y, 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(1): 16.
[http://dx.doi.org/10.1186/s12943-018-0767-3] [PMID: 29382334]
[89]
Mendillo ML, Santagata S, Koeva M, et al. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 2012; 150(3): 549-62.
[http://dx.doi.org/10.1016/j.cell.2012.06.031] [PMID: 22863008]
[90]
Jiang S, Tu K, Fu Q, et al. Multifaceted roles of HSF1 in cancer. Tumour Biol 2015; 36(7): 4923-31.
[http://dx.doi.org/10.1007/s13277-015-3674-x] [PMID: 26108999]
[91]
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(21): 3122-6.
[http://dx.doi.org/10.3748/wjg.v10.i21.3122] [PMID: 15457556]
[92]
Vychytilova-Faltejskova P, Stitkovcova K, Radova L, et al. Circulating PIWI-interacting RNAs piR-5937 and piR-28876 are promising diagnostic biomarkers of colon cancer. Cancer Epidemiol Biomarkers Prev 2018; 27(9): 1019-28.
[http://dx.doi.org/10.1158/1055-9965.EPI-18-0318] [PMID: 29976566]
[93]
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.
[http://dx.doi.org/10.7150/jgen.18856] [PMID: 28348640]
[94]
Yuan T, Huang X, Woodcock M, et al. Plasma extracellular RNA profiles in healthy and cancer patients. Sci Rep 2016; 6: 19413.
[http://dx.doi.org/10.1038/srep19413] [PMID: 26786760]
[95]
Li Y, Wu X, Gao H, et al. PIWI-interacting RNAs are dysregulated in renal cell carcinoma and associated with tumor metastasis and cancer specific survival. Mol Med 2015; 21: 381-8.
[http://dx.doi.org/10.2119/molmed.2014.00203] [PMID: 25998508]
[96]
Mei Y, Clark D, Mao L. Novel dimensions of piRNAs in cancer. Cancer Lett 2013; 336(1): 46-52.
[http://dx.doi.org/10.1016/j.canlet.2013.04.008] [PMID: 23603435]
[97]
Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105(30): 10513-8.
[http://dx.doi.org/10.1073/pnas.0804549105] [PMID: 18663219]
[98]
Peng L, Song L, Liu C, et al. piR-55490 inhibits the growth of lung carcinoma by suppressing mTOR signaling. Tumour Biol 2016; 37(2): 2749-56.
[http://dx.doi.org/10.1007/s13277-015-4056-0] [PMID: 26408181]
[99]
Wang J, Zhang P, Lu Y, et al. piRBase: A comprehensive database of piRNA sequences. Nucleic Acids Res 2019; 47(D1): D175-80.
[http://dx.doi.org/10.1093/nar/gky1043] [PMID: 30371818]
[100]
Zhang P, Si X, Skogerbø G, et al. piRBase: A web resource assisting piRNA functional study. Database (Oxford) 2014; 2014: bau110.
[http://dx.doi.org/10.1093/database/bau110] [PMID: 25425034]
[101]
Betel D, Sheridan R, Marks DS, Sander C. Computational analysis of mouse piRNA sequence and biogenesis. PLOS Comput Biol 2007; 3(11): e222.
[http://dx.doi.org/10.1371/journal.pcbi.0030222] [PMID: 17997596]
[102]
Zhang Y, Wang X, Kang L. A k-mer scheme to predict piRNAs and characterize locust piRNAs. Bioinformatics 2011; 27(6): 771-6.
[http://dx.doi.org/10.1093/bioinformatics/btr016] [PMID: 21224287]
[103]
Liu YJ, Zhang JY, Li AM, Liu ZW, Zhang YY, Sun XH. Detection of PIWI-interacting RNAs based on sequence features. Genet Mol Res 2016; 15(2): 15028638.
[http://dx.doi.org/10.4238/gmr.15028638] [PMID: 27323033]
[104]
Itou D, Shiromoto Y, Yukiho SY, et al. Induction of DNA methylation by artificial piRNA production in male germ cells. Curr Biol 2015; 25(7): 901-6.
[http://dx.doi.org/10.1016/j.cub.2015.01.060] [PMID: 25772451]
[105]
Xie T, Huang M, Wang Y, Wang L, Chen C, Chu X. MicroRNAs as regulators, biomarkers and therapeutic targets in the drug resistance of colorectal cancer. Cell Physiol Biochem 2016; 40(1-2): 62-76.
[http://dx.doi.org/10.1159/000452525] [PMID: 27842308]
[106]
Yuan Y, Wang H, Wu Y, et al. P53 contributes to cisplatin induced renal oxidative damage via regulating P66shc and MnSOD. Cell Physiol Biochem 2015; 37(4): 1240-56.
[http://dx.doi.org/10.1159/000430247] [PMID: 26431211]
[107]
Tan Y, Liu L, Liao M, et al. Emerging roles for PIWI proteins in cancer. Acta Biochim Biophys Sin (Shanghai) 2015; 47(5): 315-24.
[http://dx.doi.org/10.1093/abbs/gmv018] [PMID: 25854579]