The meaning of PIWI proteins in cancer development (Review)
- Authors:
- Monika Litwin
- Anna Szczepańska‑Buda
- Aleksandra Piotrowska
- Piotr Dzięgiel
- Wojciech Witkiewicz
-
Affiliations: Research and Development Centre, Regional Specialist Hospital in Wrocław, 51‑423 Wrocław, Poland, Department of Histology and Embryology, Wrocław Medical University, 50‑368 Wrocław, Poland - Published online on: March 28, 2017 https://doi.org/10.3892/ol.2017.5932
- Pages: 3354-3362
-
Copyright: © Litwin et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
 |
 |
 |
|
Kanwal R and Gupta S: Epigenetic modifications in cancer. Clin Genet. 81:303–311. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kristensen LS, Nielsen HM and Hansen LL: Epigenetics and cancer treatment. Eur J Pharmacol. 625:131–142. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, et al: A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 442:203–207. 2006.PubMed/NCBI | |
|
Girard A, Sachidanandam R, Hannon GJ and Carmell MA: A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 442:199–202. 2006.PubMed/NCBI | |
|
Grivna ST, Beyret E, Wang Z and Lin H: A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 1:1709–1714. 2006. View Article : Google Scholar | |
|
Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N and Imai H: 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. 1:1732–1743. 2006. View Article : Google Scholar | |
|
Martinez VD, Vucic EA, Thu KL, Hubaux R, Enfield KS, Pikor LA, Becker-Santos DD, Brown CJ, Lam S and Lam WL: Unique somatic and malignant expression patterns implicate PIWI-interacting RNAs in cancer-type specific biology. Sci Rep. 5:104232015. View Article : Google Scholar : PubMed/NCBI | |
|
Suzuki R, Honda S and Kirino Y: Piwi expression and function in cancer. Front Genet. 3:2042012. View Article : Google Scholar : PubMed/NCBI | |
|
Luteijn MJ and Ketting RF: PIWI-interacting RNAs: From generation to transgenerational epigenetics. Nat Rev Genet. 14:523–534. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, Blower MD and Lai EC: A broadly conserved pathway generates 3′UTR-directed primary piRNAs. Curr Biol. 19:2066–2076. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ku HY and Lin H: PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression. Natl Sci Rev. 1:205–218. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Llave C, Kasschau KD, Rector MA and Carrington JC: Endogenous and silencing associated small RNAs in plants. Plant Cell. 14:1605–1619. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Djikeng A, Shi H, Tschudi C and Ullu E: RNA interference in Trypanosoma brucei: Cloning of small interfering RNAs provides evidence for retroposon-derived 24–26 nucleotide RNAs. RNA. 7:1522–1530. 2001.PubMed/NCBI | |
|
Farazi TA, Juranek SA and Tuschl T: The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development. 135:1201–1214. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Simon B, Kirkpatrick JP, Eckhardt S, Reuter M, Rocha EA, Andrade-Navarro MA, Sehr P, Pillai RP and Carlopamgno T: Recognition of 2′-O-methylated 3′-end of piRNA by the PAZ domain of a Piwi protein. Structure. 19:172–180. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Jinek M and Doudna JA: A three dimensional view of the molecular machinery of RNA interference. Nature. 457:405–412. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S, Klein PS, Rigoutsos I, Jongens TA and Mourelatos Z: Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol. 11:652–658. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, Chuma S, Girard A, Sachidanandam R, Hannon GJ and Aravin AA: Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev. 23:1749–1762. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hashim A, Rizzo F, Marchese G, Ravo M, Taralllo R, Nassa G, Giurato G, Santamaria G, Cordella A, Cantarella C and Weisz A: RNA sequencing identifies specific PIWI-interacting small non-coding RNA expression patterns in breast cancer. Oncotarget. 5:9901–9910. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Juliano C, Wang J and Lin H: Uniting germline and stem cells: The function of Piwi proteins and the piRNA pathway in diverse organisms. Annu Rev Genet. 45:447–469. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Thomson T and Lin H: The biogenesis and function PIWI proteins and piRNAs: Progress and prospect. Annu Rev Cell Dev Biol. 25:355–376. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Sasaki T, Shiiohama A, Minoshima S and Shimizu N: Identification of eight members of the Argonaute family in the human genome. Genomics. 82:323–330. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Williams RW and Rubin GM: Argonautel is required for efficient RNA interference in Drosophila embryos. Proc Natl Acad Sci USA. 99:6889–6894. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Carmell MA, Xuan Y, Yhang MQ and Hannon HJ: The Argonaute family: Tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16:2733–2742. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG and Hannon GJ: MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell. 12:503–514. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, et al: Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 131:839–849. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Deng W and Lin H: Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell. 2:819–830. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Siddiqi S and Matushansky I: Piwis and piwi-interacting RNAs in the epigenetics of cancer. J Cell Biochem. 113:373–380. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, Weller KP and Hoffman R: Human CD34(+) stem cells express the HIWI gene, a human homologue of the Drosophila gene piwi. Blood. 97:426–434. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Tan Y, Liu L, Liao M, Zhang C, Hu S, Zou M, Gu M and Li X: Emerging roles for PIWI proteins in cancer. Acta Biochim Biophys Sin (Shanghai). 47:315–324. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Qiao D, Zeeman AM, Deng W, Looijenga LH and Lin H: Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated with seminomas. Oncogene. 21:3988–3999. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Taubert H, Greither T, Kaushal D, Würl P, Bache M, Bartel F, Kehlen A, Lautenschläger C, Harris L, Kraemer K, et al: Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma. Oncogene. 15:1098–1100. 2007. View Article : Google Scholar | |
|
Wang DW, Wang ZH, Wang LL, Song Y and Zhang GZ: Overexpression of hiwi promotes growth of human breast cancer cells. Asian Pac J Cancer Prev. 15:7553–7558. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cao J, Xu G, Lan J, Huang Q, Tang Z and Tian L: High expression of piwi-like RNA mediated gene silencing 1 is associated with poor prognosis via regulating transforming growth factor-β receptors and cyclin-dependent kinases in breast cancer. Mol Med Rep. 13:2829–2835. 2016.PubMed/NCBI | |
|
He W, Wang Z, Wang Q, Fan Q, Shou C, Wang J, Giercksky KE, Nesland JM and Suo Z: Expression of HIWI in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. BMC Cancer. 9:4262009. View Article : Google Scholar : PubMed/NCBI | |
|
Grochola LF, Greither T, Taubert H, Möller P, Knippschild U, Udelnow A, Henne-Bruns D and Würl P: The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: Expression and risk of tumor-related death. Br J Cancer. 99:1083–1088. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Liu Y, Shen X, Zhang X, Chen X, Yang C and Gao H: The PIWI protein acts as a predictive marker for human gastric cancer. Int J Clin Exp Pathol. 5:315–325. 2012.PubMed/NCBI | |
|
Liu JJ, Shen R, Chen L, Ye Y, He G, Hua K, Jarjoura D, Nakano T, Ramesh GK, Shapiro CL, 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. 3:328–337. 2010.PubMed/NCBI | |
|
Zeng Y, Qu LK, Meng L, Liu CY, Dong B, Xing XE, Wu J and Shou CC: HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin Med J (Engl). 124:2144–2149. 2011.PubMed/NCBI | |
|
Zhao YM, Zhou JM, Wang LR, He HW, Wang XL, Tao ZH, Sun HC, Wu WZ, Fan J, Tang ZY and Wang L: HIWI is associated with prognosis in patients with hepatocellular carcinoma after curative resection. Cancer. 118:2708–2717. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Liu W, Gao Q, Chen K, Xue X, Li M, Chen Q, Zhu G and Gao Y: Hiwi facilitates chemoresistance as a cancer stem cell marker in cervical cancer. Oncol Rep. 32:1853–1860. 2016. | |
|
Wang Y, Liu J, Wu G and Yang F: Manipulations in HIWI levels exerts influence on the proliferation of human non-small cell lung cancer cells. Exp Ther Med. 11:1971–1976. 2016.PubMed/NCBI | |
|
Yang L, Bi L, Liu Q, Zhao M, Cao B, Li D and Xiu J: Hiwi promotes the proliferation of colorectal cancer cells via upregulating global DNA methylation. Dis Markers. 2015:3830562015. View Article : Google Scholar : PubMed/NCBI | |
|
Ye Y, Yin DT, Chen L, Zhou Q, Shen R, He G, Yan Q, Tong Z, Issekutz AC, Shapiro CL, et al: Identification of Piwil2-like (PL2L) proteins that promote tumorigenesis. PLoS One. 5:e134062010. View Article : Google Scholar : PubMed/NCBI | |
|
Liu X, Sun Y, Guo J, Ma H, Li J, Dong B, Jin G, Zhang J, Wu J, Meng L and Shou C: Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells. Int J Cancer. 118:1922–1929. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
He G, Chen L, Ye Y, Xiao Y, Hua K, Jarjoura D, Nakano T, Barsky SH, Shen R and Gao JX: Piwil2 expressed in various stages of cervical neoplasia is a potential complementary marker for p16. Am J Transl Res. 2:156–169. 2010.PubMed/NCBI | |
|
Chen C, Liu J and Xu G: Overexpression of PIWI proteins in human stage III epithelial ovarian cancer with lymph node metastasis. Cancer Biomark. 13:315–321. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Yang Y, Zhang X, Song D and 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. 10:1735–1740. 2015.PubMed/NCBI | |
|
Oh SJ, Kim SM, Kim YO and Chang HK: Clinicopathologic implications of PIWIL2 expression in colorectal cancer. Korean J Pathol. 46:318–323. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Lee JH, Jung C, Javadian-Elyaderani P, Schweyer S, Schütte D, Shoukier M, Karimi-Busheri F, Weinfeld M, Rasouli-Nia A, Hengstler JG, et al: Pathway of proliferation and apoptosis driven in breast cancer stem cells by stem cell protein piwil2. Cancer Res. 70:4569–4579. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Lee JH, Schütte D, Wulf G, Füzesi L, Radzun HJ, Schweyer S, Engel W and Nayernia K: Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Genet. 15:201–211. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Gainetdinov IV, Skvortsova YV, Stukacheva EA, Bychenko OS, Kondratieva SA, Zinovieva MV and Azhikina TL: Expression profiles of PIWIL2 short isoforms differ in testicular germ cell tumors of various differentiation subtypes. PLoS One. 9:e1125282014. View Article : Google Scholar : PubMed/NCBI | |
|
Li D, Sun X, Yan D, Huang J, Luo Q, Tang H and Peng Z: Piwil2 modulates the proliferation and metastasis of colon cancer via regulation of matrix metallopeptidase 9 transcriptional activity. Exp Biol Med (Maywood). 237:1231–1240. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Litwin M, Dubis J, Arczyńska K, Piotrowska A, Frydlewicz A, Karczewski M, Dzięgiel P and Witkiewicz W: Correlation of HIWI and HILI expression with cancer stem cell markers in colorectal cancer. Anticancer Res. 35:3317–3324. 2015.PubMed/NCBI | |
|
Nikpour P, Forouzandeh-Moghaddam M, Ziaee SA, Dokun OY, Schulz WA and Mowla SJ: Absence of PIWIL2 (HILI) expression in human bladder cancer cell lines and tissues. Cancer Epidemiol. 33:271–275. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Su C, Ren ZJ, Wang F, Liu M, Li X and Tang H: PIWIL4 regulates cervical cancer cell line growth and is involved in down-regulating the expression of p14ARF and p53. FEBS Lett. 586:1356–1362. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Al-Janabi O, Wach S, Nolte E, Weigelt K, Rau TT, Stöhr C, Legal W, Schick S, Greither T, Hartmann A, et al: Piwi-like 1 and 4 gene transcript levels are associated with clinicopathological parameters in renal cell carcinoma. Biochim Biophys Acta. 1842:686–690. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Li D, Luo Y, Gao Y and Yang Y, Wang Y, Xu Y, Tan S, Zhang Y, Duan J and Yang Y: piR-651 promotes tumour formation in non-small cell lung carcinoma through the upregulation of cyclin D1 and CDK4. Int J Mol Med. 38:927–936. 2016.PubMed/NCBI | |
|
Cheng J, Guo JM, Xiao BX, Miao Y, Jaing Z, Zhou H and Li QN: piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clinica Chim Acta. 412:1621–1625. 2011. View Article : Google Scholar | |
|
Huang G, Hu H, Xue X, Shen S, Gao E, Guo G, Shen X and Zhang X: Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol. 15:563–568. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Siddigi S, Terry M and Matushansky I: Hiwi mediated tumorigenesis is associated with DNA hypermethylation. PLoS One. 7:e337112012. View Article : Google Scholar : PubMed/NCBI | |
|
Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T and Hannon GJ: A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 26:785–799. 2008. View Article : Google Scholar | |
|
Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, et al: DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22:908–917. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A and Hannon GJ: An epigenetic role for maternally inherited piRNAs in transposon silencing. Science. 322:1387–1392. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H and Siomi MC: Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 20:2214–2222. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Saito K: The epigenetic regulation of transposable elements by PIWI-interacting RNAs in Drosophila. Genes Genet Syst. 88:9–17. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
van Wolfswinkel JC and Ketting RF: The role of small non-coding RNAs in genome stability and chromatin organization. J Cell Sci. 123:1825–1839. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Lobo NA, Shimono Y, Qian D and Clarke MF: The biology of cancer stem cells. Annu Rev Cell Dev Biol. 23:675–699. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Pardal R, Clarke MF and Morrison SJ: Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 3:895–902. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Islam F, Gopalan V, Smith RA and Lam AK: Translational potential of cancer stem cells: A review of the detection of cancer stem cells and their roles in cancer recurrence and cancer treatment. Exp Cell Res. 335:135–147. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Yao J, Caballero OL, Yung WK, Weinstein JN, Riggins GJ, Strausberg RL and Zhao Q: Tumor subtype-specific cancer-testis antigens as potential biomarkers and immunotherapeutic targets for cancers. Cancer Immunol Res. 2:371–379. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J and Buck DW: AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 90:5002–5012. 1997.PubMed/NCBI | |
|
Salven P, Mustjoki S, Alitalo R, Alitalo K and Rafii S: VEGFR-3 and CD133 identify a population of CD34+lymphatic/vascular endothelial precursor cells. Blood. 101:168–172. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH and Weissman IL: Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA. 97:14720–14725. 2009. View Article : Google Scholar | |
|
Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J and Dirks PB: Identification of a cancer stem cell in human brain tumors. Cancer Res. 63:5821–5828. 2003.PubMed/NCBI | |
|
Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T and Moriwaki H: Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 351:820–824. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
O'Brien CA, Pollett A, Gallinger S and Dick JE: A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 445:106–110. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ and Heeschen C: Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 1:313–323. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Collins AT, Berry PA, Hyde C, Stower MJ and Maitland NJ: Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65:10946–10951. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K and Los M: Cancer stem cell markers in common cancers-therapeutic implications. Trends Mol Med. 14:445–460. 2008. View Article : Google Scholar | |
|
Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, Yang SX and Ivy SP: Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: Clinical update. Nat Rev Clin Oncol. 12:445–464. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Rao S, Chu J, Shen X, Levasseur DN, Theunissen TW and Orkin SH: A protein interaction network for pluripotency of embryonic stem cells. Nature. 444:364–368. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Niwa H, Miyazaki J and Smith AG: Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genet. 24:372–376. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, Chou SH, Chien CS, Ku HH and Lo JF: Positive correlations of Oct4 and Nanog in oral cancer stem-like cells and high grade oral squamous cell carcinoma. Clin Cancer Res. 14:4085–4095. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Guo Y, Liu S, Wang P, Zhao S, Wang F, Bing L, Zhang Y, Ling EA, Gao J and Hao A: Expression profile of embryonic stem cell-associated genes Oct4, Sox2 and Nanog in human glioma. Histopathology. 59:763–775. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Matsuoka J, Yashiro M, Sakuari K, Kubo N, Tanaka H, Muguruma K, Sawada T, Ohira M and Hirakawa K: Role of the stemness factors Sox2, Oct3/4, and Nanog in gastric carcinoma. J Surg Res. 174:130–135. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Saigusa S, Tanaka K, Toiyama Y, Yokoe T, Okugawa Y, Ioue Y, Miki C and Kusunoki M: Correlation of CD133, OCT4, and Sox2 in rectal cancer and their association with distant recurrence after chemoradiotherpy. Ann Surg Oncol. 16:3488–3498. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Yin X, Li YW, Jin JJ, Zhou Y, Ren ZG, Qiu SJ and Zhang BH: The clinical and prognostic implications of pluripotent stem cell gene expression in hepatocellular carcinoma. Oncol Lett. 5:1155–1162. 2013.PubMed/NCBI | |
|
Meng HM, Zheng P, Wang XY, Liu C, Sui HM, Wu SJ, Zhou J, Ding YQ and Li J: Overexpression of Nanog predicts tumor progression and poor prognosis in colorectal cancer. Cancer Biol Ther. 9:295–302. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Sholl LM, Barletta JA, Yeap BY, Chirieac LR and Hornick JL: Sox2 protein expression is an independent poor prognostic indicator in stage I lung adenocarcinoma. Am J Surg Pathol. 34:1193–1198. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Lengerke C, Fehm T, Kurth R, Neubauer H, Scheble V, Müller F, Schneider F, Petersen K, Wallwiener D, Kanz L, et al: Expression of the embryonic stem cell marker SOX2 in early-stage breast carcinoma. BMC Cancer. 11:422011. View Article : Google Scholar : PubMed/NCBI | |
|
Bareiss PM, Paczulla A, Wang H, Schairer R, Wiehr S, Kohlhofer U, Rothfuss OC, Fischer A, Perner S, Staebler A, et al: SOX2 expression associates with stem cell state in human ovarian carcinoma. Cancer Res. 73:5544–5555. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Sanada Y, Yoshida K, Ohara M, Oeda M, Konishi K and Tsutani Y: Histopathological evaluation of stepwise progression of pancreatic carcinoma with immunohistochemical analysis of gastric epithelial transcription factor SOX2: Comparison of expression patterns between invasive components and cancerous or nonneoplastic intraductal components. Pancreas. 32:164–170. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Takahashi K and Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 126:663–676. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Tiwari N, Meyer-Schaller N, Arnold P, Antoniadis H, Pachkov M, van Nimwegen E and Christofori G: Klf4 is a transcriptional regulator of genes critical for EMT, including Jnk1 (Mapk8). PLoS One. 8:e573292013. View Article : Google Scholar : PubMed/NCBI | |
|
Thiery JP, Aclogue H, Huang RY and Nieto MA: Epithelial-mesenchymal transitions in development and disease. Cell. 139:871–890. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Wu CY, Tsai YP, Wu MZ, Teng SC and Wu KJ: Epigenetic reprogramming and post-transcriptional regulation during the epithelial-mesenchymal transition. Trends Genet. 28:454–463. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Esteban MA, Bao X, Zhuang Q, Zhou T, Qin B and Pei D: The mesenchymal-to-epithelial transition in somatic cell reprogramming. Curr Opin Genet Dev. 22:423–428. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Singh A and Settleman J: EMT, cancer stem cells and drug resistance: An emerging role axis of evil in the war on cancer. Oncogene. 29:4741–4751. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Fan F, Samuel S, Evans KW, Lu J, Xia L, Zhou Y, Sceusi E, Tozzi F, Ye XC, Mani SA and Ellis LM: Overexpression of Snail induces epithelial-mesenchymal transition and a cancer stem cell-like phenotype in human colorectal cancer cells. Cancer Med. 1:5–16. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, Hsieh WJ, Chang HT, Chen YS, Lin TW, Hsu HS and Wu CW: Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res. 70:10433–10444. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Luo W, Li S, Peng B, Ye Y, Deng X and Yao K: Embryonic stem cell markers SOX2, OCT4 and Nanog expression and their correlations with epithelial-mesenchymal transition in nasopharyngeal carcinoma. PLoS One. 8:e563242013. View Article : Google Scholar : PubMed/NCBI | |
|
Chen KL, Pan F, Jiang H, Chen JF, Pei L, Xie FW and Liang HJ: Highly enriched CD133(+)CD44(+) stem-like cells with CD133(+)CD44(high) metastatic subset in HCT116 colon cancer cells. Clin Exp Metastasis. 28:751–763. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zhanga H, Renb Y, Xuc H, Pengd D, Duane C and Liua C: The expression of stem cell protein Piwil2 and piR-932 in breast cancer. Surgical Oncol. 22:217–223. 2013. View Article : Google Scholar | |
|
Botchkina IL, Rowehl RA, Rivadeneira DE, Karpeh MS Jr, Crawford H, Dufour A, Ju J, Wang Y, Leyfman Y and Botchkina GI: Phenotypic subpopulations of metastatic colon cancer stem cells: Genomic analysis. Cancer Genomic Proteomics. 6:19–30. 2009.PubMed/NCBI | |
|
Zou AE, Zheng H, Saad MA, Rahimy M, Ku J, Kuo SZ, Honda TK, Wang-Rodriguez J, Xuan Y, Korrapati A, et al: The non-coding landscape of head and neck squamous cell carcinoma. Oncotarget. 7:51211–51222. 2016.PubMed/NCBI | |
|
Watanabe T and Lin H: Posttranscriptional regulation of gene expression by Piwi proteins and piRNAs. Mol Cell. 56:18–27. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Moyano M and Stefani G: piRNA involvement in genome stability and human cancer. J Hematol Oncol. 8:382015. View Article : Google Scholar : PubMed/NCBI | |
|
Ng KW, Anderson C, Marshall EA, Minatel BC, Enfield KS, Saprunoff HL, Lam WL and Martinez VD: Piwi-interacting RNAs in cancer: Emerging functions and clinical utility. Mol Cancer. 15:52016. View Article : Google Scholar : PubMed/NCBI |
