Novel dimensions of piRNAs in cancer

Cancer Letters

Volumn 336, Issue 1, 2013, Pages 46-52

  Mei, Yuping ^a   Clark, David ^a   Mao, Li ^a,b  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Cancer; Diagnosis; PIWI interacting RNAs; Therapy

Indexed keywords

PIWI INTERACTING RNA; PIWI PROTEIN;

APOPTOSIS; BINDING AFFINITY; BINDING SITE; CANCER CELL; CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER PROGNOSIS; CARCINOGENESIS; CELL PROLIFERATION; CELL VIABILITY; DISEASE ACTIVITY; DISEASE ASSOCIATION; EPIGENETICS; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; ONCOGENE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN RNA BINDING; SHORT SURVEY; TRANSCRIPTION REGULATION; TUMOR INVASION; TUMOR SUPPRESSOR GENE; VIRUS INFECTION;

EID: 84878969890     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.04.008     Document Type: Review

References (77)

1. Amaral P.P., Dinger M.E., Mercer T.R., Mattick J.S. The eukaryotic genome as an RNA machine. Science 2008, 319:1787-1789.
2. Dawson M.A., Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell 2012, 150:12-27.
3. Aravin A.A., Naumova N.M., Tulin A.V., Vagin V.V., Rozovsky Y.M., Gvozdev V.A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 2001, 11:1017-1027.
4. Aravin A.A., Lagos-Quintana M., Yalcin A., Zavolan M., Marks D., Snyder B., Gaasterland T., Meyer J., Tuschl T. The small RNA profile during Drosophila melanogaster development. Dev. Cell 2003, 5:337-350.
5. Aravin A., Gaidatzis D., Pfeffer S., Lagos-Quintana M., Landgraf P., Iovino N., Morris P., Brownstein M.J., Kuramochi-Miyagawa S., Nakano T., Chien M., Russo J.J., Ju J., Sheridan R., Sander C., Zavolan M., Tuschl T. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
6. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
7. Grivna S.T., Beyret E., Wang Z., Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes. Dev. 2006, 20:1709-1714.
8. Ruby J.G., Jan C., Player C., Axtell M.J., Lee W., Nusbaum C., Ge H., Bartel D.P. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 2006, 127:1193-1207.
9. Aravin A.A., Sachidanandam R., Girard A., Fejes-Toth K., Hannon G.J. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007, 316:744-747.
10. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
11. Batista P.J., Ruby J.G., Claycomb J.M., Chiang R., Fahlgren N., Kasschau K.D., Chaves D.A., Gu W., Vasale J.J., Duan S., Conte D., Luo S., Schroth G.P., Carrington J.C., Bartel D.P., Mello C.C. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 2008, 31:67-78.
12. Das P.P., Bagijn M.P., Goldstein L.D., Woolford J.R., Lehrbach N.J., Sapetschnig A., Buhecha H.R., Gilchrist M.J., Howe K.L., Stark R., Matthews N., Berezikov E., Ketting R.F., Tavare S., Miska E.A. Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol. Cell 2008, 31:79-90.
13. Deng W., Miwi Lin H. A murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2002, 2:819-830.
14. Schupbach T., Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 1991, 129:1119-1136.
15. Cox D.N., Chao A., Lin H. Piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 2000, 127:503-514.
16. Deng W., Lin H. Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2002, 2:819-830.
17. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., Lin H., Matsuda Y., Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004, 131:839-849.
18. Zhao S., Gou L.T., Zhang M., Zu L.D., Hua M.M., Hua Y., Shi H.J., Li Y., Li J., Li D., Wang E.D., Liu M.F. PiRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis. Dev. Cell 2013, 24:13-25.
19. Lu Y., Li C., Zhang K., Sun H., Tao D., Liu Y., Zhang S., Ma Y. Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep. 2010, 43:635-641.
20. Cheng J., Guo J.M., Xiao B.X., Miao Y., Jiang Z., Zhou H., Li Q.N. PiRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin. Chim. Acta 2011, 412:1621-1625.
21. G. Huang, H. Hu, X. Xue, S. Shen, E. Gao, G. Guo, X. Shen, X. Zhang, Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol, 2012. November 15 (Epub ahead of print).
22. Cheng J., Deng H., Xiao B., Zhou H., Zhou F., Shen Z., Guo J. PiR-823, a novel non-coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells. Cancer Lett. 2012, 315:12-17.
23. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
24. Grishok A., Tabara H., Mello C.C. Genetic requirements for inheritance of RNAi in C. elegans. Science 2000, 287:2494-2497.
25. Pak J., Fire A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 2007, 315:241-244.
26. Siomi M.C., Sato K., Pezic D., Aravin A.A. PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 2011, 12:246-258.
27. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
28. Gu W., Lee H.C., Chaves D., Youngman E.M., Pazour G.J., Conte D., Mello C.C. CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell 2012, 151:1488-1500.
29. Cecere G., Zheng G.X., Mansisidor A.R., Klymko K.E., Grishok A. Promoters recognized by forkhead proteins exist for individual 21U-RNAs. Mol. Cell 2012, 47:734-745.
30. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 2008, 31:785-799.
31. Malone C.D., Brennecke J., Dus M., Stark A., McCombie W.R., Sachidanandam R., Hannon G.J. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009, 137:522-535.
32. Sijen T., Steiner F.A., Thijssen K.L., Plasterk R.H. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 2007, 315:244-247.
33. Sana J., Faltejskova P., Svoboda M., Slaby O. Novel classes of non-coding RNAs and cancer. J. Transl. Med. 2012, 10:103.
34. Samji T. PIWI, piRNAs, and germline stem cells: what's the link?. Yale J. Biol. Med. 2009, 82:121-124.
35. Thomson T., Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 2009, 25:355-376.
36. Klattenhoff C., Theurkauf W. Biogenesis and germline functions of piRNAs. Development 2008, 135:3-9.
37. Grimson A., Srivastava M., Fahey B., Woodcroft B.J., Chiang H.R., King N., Degnan B.M., Rokhsar D.S., Bartel D.P. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 2008, 455:1193-1197.
38. Beyret E., Liu N., Lin H. PiRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism. Cell Res. 2012, 22:1429-1439.
39. Suzuki R., Honda S., Kirino Y. PIWI expression and function in cancer. Front Genet. 2012, 3:204.
40. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
41. Simpson A.J., Caballero O.L., Jungbluth A., Chen Y.T., Old L.J. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 2005, 5:615-625.
42. Costa F.F., Le Blanc K., Brodin B. Concise review: cancer/testis antigens, stem cells, and cancer. Stem Cells 2007, 25:707-711.
43. He C., Zuo Z., Chen H., Zhang L., Zhou F., Cheng H., Zhou R. Genome-wide detection of testis- and testicular cancer-specific alternative splicing. Carcinogenesis 2007, 28:2484-2490.
44. Cheng Y.H., Wong E.W., Cheng C.Y. Cancer/testis (CT) antigens carcinogenesis and spermatogenesis. Spermatogenesis 2011, 1:209-220.
45. Chen Y., Pane A., Schupbach T. Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila. Curr. Biol. 2007, 17:637-642.
46. Sasaki T., Shiohama A., Minoshima S., Shimizu N. Identification of eight members of the Argonaute family in the human genome small star, filled. Genomics 2003, 82:323-330.
47. Qiao D., Zeeman A.M., Deng W., Looijenga L.H., Lin H. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene 2002, 21:3988-3999.
48. Taubert H., Greither T., Kaushal D., Wurl P., Bache M., Bartel F., Kehlen A., Lautenschlager C., Harris L., Kraemer K., Meye A., Kappler M., Schmidt H., Holzhausen H.J., Hauptmann S. Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma. Oncogene 2007, 26:1098-1100.
49. Lee J.H., Schutte D., Wulf G., Fuzesi L., Radzun H.J., Schweyer S., Engel W., Nayernia K. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum. Mol. Genet. 2006, 15:201-211.
50. Lu Y., Zhang K., Li C., Yao Y., Tao D., Liu Y., Zhang S., Ma Y. Piwil2 suppresses p53 by inducing phosphorylation of signal transducer and activator of transcription 3 in tumor cells. PLoS One 2012, 7:e30999.
51. Liu W.K., Jiang X.Y., Zhang Z.X. Expression of PSCA, PIWIL1 and TBX2 and its correlation with HPV16 infection in formalin-fixed, paraffin-embedded cervical squamous cell carcinoma specimens. Arch. Virol. 2010, 155:657-663.
52. He G., Chen L., Ye Y., Xiao Y., Hua K., Jarjoura D., Nakano T., Barsky S.H., Shen R., Gao J.X. Piwil2 expressed in various stages of cervical neoplasia is a potential complementary marker for p16. Am. J. Transl. Res. 2010, 2:156-169.
53. Li D., Sun X., Yan D., Huang J., Luo Q., Tang H., Peng Z. Piwil2 modulates the proliferation and metastasis of colon cancer via regulation of matrix metallopeptidase 9 transcriptional activity. Exp. Biol. Med. (Maywood) 2012, 237:1231-1240.
54. Grochola L.F., Greither T., Taubert H., Moller P., Knippschild U., Udelnow A., Henne-Bruns D., Wurl P. The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death. Br. J. Cancer 2008, 99:1083-1088.
55. Wang Y., Liu Y., Shen X., Zhang X., Chen X., Yang C., Gao H. The PIWI protein acts as a predictive marker for human gastric cancer. Int. J. Clin. Exp. Pathol. 2012, 5:315-325.
56. Oh S.J., Kim S.M., Kim Y.O., Chang H.K. Clinicopathologic implications of PIWIL2 expression in colorectal cancer. Korean J. Pathol. 2012, 46:318-323.
57. Sun G., Wang Y., Sun L., Luo H., Liu N., Fu Z., You Y. Clinical significance of Hiwi gene expression in gliomas. Brain Res. 2011, 1373:183-188.
58. Zhao Y.M., Zhou J.M., Wang L.R., He H.W., Wang X.L., Tao Z.H., Sun H.C., Wu W.Z., Fan J., Tang Z.Y., Wang L. HIWI is associated with prognosis in patients with hepatocellular carcinoma after curative resection. Cancer 2012, 118:2708-2717.
59. Zeng Y., Qu L.K., Meng L., Liu C.Y., Dong B., Xing X.F., Wu J., Shou C.C. HIWI expression profile in cancer cells and its prognostic value for patients with colorectal cancer. Chin. Med. J. (Engl.) 2011, 124:2144-2149.
60. He W., Wang Z., Wang Q., Fan Q., Shou C., Wang J., Giercksky K.E., Nesland J.M., Suo Z. Expression of HIWI in human esophageal squamous cell carcinoma is significantly associated with poorer prognosis. BMC Cancer 2009, 9:426.
61. Liu J.J., Shen R., Chen L., Ye Y., He G., Hua K., Jarjoura D., Nakano T., Ramesh G.K., Shapiro C.L., Barsky S.H., Gao J.X. Piwil2 is expressed in various stages of breast cancers and has the potential to be used as a novel biomarker. Int. J. Clin. Exp. Pathol. 2010, 3:328-337.
62. Antonovics J., Boots M., Abbate J., Baker C., McFrederick Q., Panjeti V. Biology and evolution of sexual transmission. Ann. NY Acad. Sci. 2011, 1230:12-24.
63. Shirayama M., Seth M., Lee H.C., Gu W., Ishidate T., Conte D., Mello C.C. PiRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 2012, 150:65-77.
64. Zhang F., Wang J., Xu J., Zhang Z., Koppetsch B.S., Schultz N., Vreven T., Meignin C., Davis I., Zamore P.D., Weng Z., Theurkauf W.E. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 2012, 151:871-884.
65. 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.
66. Britten R.J. Transposable element insertions have strongly affected human evolution. Proc. Natl. Acad. Sci. USA 2010, 107:19945-19948.
67. Hedges D.J., Belancio V.P. Restless genomes humans as a model organism for understanding host-retrotransposable element dynamics. Adv. Genet. 2011, 73:219-262.
68. Fang W., Wang X., Bracht J.R., Nowacki M., Landweber L.F. Piwi-interacting RNAs protect DNA against loss during oxytricha genome rearrangement. Cell 2012, 151:1243-1255.
69. Ashe A., Sapetschnig A., Weick E.M., Mitchell J., Bagijn M.P., Cording A.C., Doebley A.L., Goldstein L.D., Lehrbach N.J., Le Pen J., Pintacuda G., Sakaguchi A., Sarkies P., Ahmed S., Miska E.A. PiRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 2012, 150:88-99.
70. Lee H.C., Gu W., Shirayama M., Youngman E., Conte D., Mello C.C. C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 2012, 150:78-87.
71. Huang X.A., Yin H., Sweeney S., Raha D., Snyder M., Lin H. A major epigenetic programming mechanism guided by piRNAs. Dev. Cell 2013, 24:502-516.
72. Sytnikova Y., Lau N.C. Does the APC/C mark MIWI and piRNAs for a final farewell?. Dev. Cell 2013, 24:119-120.
73. P.T. Law, H. Qin, A.K. Ching, K.P. Lai, N.N. Co, M. He, R.W. Lung, A.W. Chan, T.F. Chan, N. Wong, Deep sequencing of small RNA transcriptome reveals novel non-coding RNAs in hepatocellular carcinoma. J. Hepatol., 2013 (doi: 10.1016/j.jhep.2013.01.032 Epub ahead of print).
74. Lee E., Iskow R., Yang L., Gokcumen O., Haseley P., Luquette L.J., Lohr J.G., Harris C.C., Ding L., Wilson R.K., Wheeler D.A., Gibbs R.A., Kucherlapati R., Lee C., Kharchenko P.V., Park P.J. Landscape of somatic retrotransposition in human cancers. Science 2012, 337:967-971.
75. Starr T.K., Allaei R., Silverstein K.A., Staggs R.A., Sarver A.L., Bergemann T.L., Gupta M., O'Sullivan M.G., Matise I., Dupuy A.J., Collier L.S., Powers S., Oberg A.L., Asmann Y.W., Thibodeau S.N., Tessarollo L., Copeland N.G., Jenkins N.A., Cormier R.T., Largaespada D.A. A transposon-based genetic screen in mice identifies genes altered in colorectal cancer. Science 2009, 323:1747-1750.
76. Chen L., Stuart L., Ohsumi T.K., Burgess S., Varshney G.K., Dastur A., Borowsky M., Benes C., Lacy-Hulbert A., Schmidt E.V. Transposon activation mutagenesis as a screening tool for identifying resistance to cancer therapeutics. BMC Cancer 2013, 10.1186/1471-2407-13-93.
77. Rajasethupathy P., Antonov I., Sheridan R., Frey S., Sander C., Tuschl T., Kandel E.R. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 2012, 149:693-707.