Overexpression of piRNA pathway genes in epithelial ovarian cancer

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Lim, Shu Ly ^a   Ricciardelli, Carmela ^a   Oehler, Martin K ^a   De Arao Tan, Izza M D ^a   Russell, Darryl ^a   Grützner, Frank ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PIWI INTERACTING RNA; ARGONAUTE PROTEIN; CARRIER PROTEIN; MAELSTROM PROTEIN, HUMAN; MESSENGER RNA; PIWIL1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ADULT; AGED; ARTICLE; CANCER CELL; CLINICAL ARTICLE; CONTROLLED STUDY; EXON; FEMALE; GENE; GENE DELETION; GENE FUNCTION; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MAEL GENE; MALE; NUCLEOTIDE SEQUENCE; OVARIAN CANCER CELL LINE; OVARY CARCINOMA; PIWIL1 GENE; PIWIL2 GENE; PIWIL3 GENE; PIWIL4 GENE; STOP CODON; STROMA CELL; TUMOR INVASION; UPREGULATION; CANCER STAGING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; NEOPLASM; OVARY; OVARY TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ARGONAUTE PROTEINS; BASE SEQUENCE; CARRIER PROTEINS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU HYBRIDIZATION; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM STAGING; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; OVARY; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84903316848     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099687     Document Type: Article

References (56)

1. Anttonen M, Ketola I, Parviainen H, Pusa AK, Heikinheimo M (2003) FOG-2 and GATA-4 Are coexpressed in the mouse ovary and can modulate mullerian-inhibiting substance expression. Biol Reprod 68: 1333-1340. (Pubitemid 36359122)
2. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71-96. (Pubitemid 351521864)
3. Ricciardelli C, Oehler MK (2009) Diverse molecular pathways in ovarian cancer and their clinical significance. Maturitas 62: 270-275.
4. Feinberg AP, Vogelstein B (1983) Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301: 89-92. (Pubitemid 13154475)
5. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921. (Pubitemid 32165345)
6. Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nature reviews Genetics 10: 691-703.
7. Smallwood SA, Kelsey G (2012) De novo DNA methylation: a germ cell perspective. Trends Genet 28: 33-42.
8. Aravin AA, Bourc'his D (2008) Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes & development 22: 970-975. (Pubitemid 351544235)
9. Sarot E, Payen-Groschene G, Bucheton A, Pelisson A (2004) Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166: 1313-1321. (Pubitemid 38507050)
10. Deng W, Lin H (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830. (Pubitemid 34650077)
11. Lim SL, Tsend-Ayush E, Kortschak RD, Jacob R, Ricciardelli C, et al. (2013) Conservation and Expression of piRNA Pathway Genes in Male and Female Adult Gonad of Amniotes. Biol Reprod.
12. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, et al. (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917. (Pubitemid 351482844)
13. Zhang D, Xiong H, Shan J, Xia X, Trudeau VL (2008) Functional insight into Maelstrom in the germline piRNA pathway: a unique domain homologous to the DnaQ-H 3′-5′ exonuclease, its lineage-specific expansion/loss and evolutionarily active site switch. Biol Direct 3: 48.
14. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747. (Pubitemid 46717682)
15. Qiao D, Zeeman AM, Deng W, Looijenga LH, Lin H (2002) Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene 21: 3988-3999. (Pubitemid 34679240)
16. Liu X, Sun Y, Guo J, Ma H, Li J, et al. (2006) Expression of hiwi gene in human gastric cancer was associated with proliferation of cancer cells. International journal of cancer Journal international du cancer 118: 1922-1929.
17. Liu JJ, Shen R, Chen L, Ye Y, He G, et al. (2010) Piwil2 is expressed in various stages of breast cancers and has the potential to be used as a novel biomarker. International journal of clinical and experimental pathology 3: 328-337.
18. Lee JH, Engel W, Nayernia K (2006) Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Molecular reproduction and development 73: 173-179. (Pubitemid 43054341)
19. Chen C, Liu J, Xu G (2013) Overexpression of PIWI proteins in human stage III epithelial ovarian cancer with lymph node metastasis. Cancer Biomark 13: 315-321.
20. Janic A, Mendizabal L, Llamazares S, Rossell D, Gonzalez C (2010) Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science 330: 1824-1827.
21. Sun G, Wang Y, Sun L, Luo H, Liu N, et al. (2011) Clinical significance of Hiwi gene expression in gliomas. Brain research 1373: 183-188.
22. Grochola LF, Greither T, Taubert H, Moller P, Knippschild U, et al. (2008) The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death. British journal of cancer 99: 1083-1088.
23. Taubert H, Greither T, Kaushal D, Wurl P, Bache M, et al. (2007) Expression of the stem cell self-renewal gene Hiwi and risk of tumour-related death in patients with soft-tissue sarcoma. Oncogene 26: 1098-1100.
24. Li L, Yu C, Gao H, Li Y (2010) Argonaute proteins: potential biomarkers for human colon cancer. BMC cancer 10: 38.
25. Xiao L, Wang Y, Zhou Y, Sun Y, Sun W, et al. (2010) Identification of a novel human cancer/testis gene MAEL that is regulated by DNA methylation. Mol Biol Rep 37: 2355-2360.
26. Shuangshoti S, Hourpai N, Pumsuk U, Mutirangura A (2007) Line-1 hypomethylation in multistage carcinogenesis of the uterine cervix. Asian Pacific journal of cancer prevention: APJCP 8: 307-309.
27. Iramaneerat K, Rattanatunyong P, Khemapech N, Triratanachat S, Mutirangura A (2011) HERV-K hypomethylation in ovarian clear cell carcinoma is associated with a poor prognosis and platinum resistance. International journal of gynecological cancer: official journal of the International Gynecological Cancer Society 21: 51-57.
28. Xi B, Yu N, Wang X, Xu X, Abassi YA (2008) The application of cell-based label-free technology in drug discovery. Biotechnology journal 3: 484-495. (Pubitemid 351618734)
29. Wolf CR, Hayward IP, Lawrie SS, Buckton K, McIntyre MA, et al. (1987) Cellular heterogeneity and drug resistance in two ovarian adenocarcinoma cell lines derived from a single patient. Int J Cancer 39: 695-702. (Pubitemid 17087868)
30. Eisenberg MC, Kim Y, Li R, Ackerman WE, Kniss DA, et al. (2011) Mechanistic modeling of the effects of myoferlin on tumor cell invasion. Proceedings of the National Academy of Sciences of the United States of America.
31. Cox DN, Chao A, Baker J, Chang L, Qiao D, et al. (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes & development 12: 3715-3727. (Pubitemid 29019652)
32. Siomi MC, Sato K, Pezic D, Aravin AA (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nature reviews Molecular cell biology 12: 246-258.
33. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Cervantes F, Sanchez J, et al. (2005) Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia. Oncogene 24: 7213-7223. (Pubitemid 41679283)
34. Piskareva O, Lackington W, Lemass D, Hendrick C, Doolan P, et al. (2011) The human L1 element: a potential biomarker in cancer prognosis, current status and future directions. Current molecular medicine 11: 286-303.
35. Grochola LF, Greither T, Taubert H, Moller P, Knippschild U, et al. (2008) The stem cell-associated Hiwi gene in human adenocarcinoma of the pancreas: expression and risk of tumour-related death. Br J Cancer 99: 1083-1088.
36. Xiao L, Wang Y, Zhou Y, Sun Y, Sun W, et al. (2010) Identification of a novel human cancer/testis gene MAEL that is regulated by DNA methylation. Molecular biology reports 37: 2355-2360.
37. Pek JW, Lim AK, Kai T (2009) Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev Cell 17: 417-424.
38. Foster R, Buckanovich RJ, Rueda BR (2013) Ovarian cancer stem cells: working towards the root of stemness. Cancer Lett 338: 147-157.
39. Sharma A, Apostolidou S, Burnell M, Campbell S, Habib M, et al. (2012) Risk of epithelial ovarian cancer in asymptomatic women with ultrasound-detected ovarian masses: a prospective cohort study within the UK collaborative trial of ovarian cancer screening (UKCTOCS). Ultrasound Obstet Gynecol 40: 338-344.
40. Alves G, Tatro A, Fanning T (1996) Differential methylation of human LINE-1 retrotransposons in malignant cells. Gene 176: 39-44. (Pubitemid 26375750)
41. Asch HL, Eliacin E, Fanning TG, Connolly JL, Bratthauer G, et al. (1996) Comparative expression of the LINE-1 p40 protein in human breast carcinomas and normal breast tissues. Oncol Res 8: 239-247. (Pubitemid 26357607)
42. Gualtieri A, Andreola F, Sciamanna I, Sinibaldi-Vallebona P, Serafino A, et al. (2013) Increased expression and copy number amplification of LINE-1 and SINE B1 retrotransposable elements in murine mammary carcinoma progression. Oncotarget 4: 1882-1893.
43. Soper SF, van der Heijden GW, Hardiman TC, Goodheart M, Martin SL, et al. (2008) Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15: 285-297.
44. Bass BL (2002) RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 71: 817-846.
45. Berasain C, Goni S, Castillo J, Latasa MU, Prieto J, et al. (2010) Impairment of pre-mRNA splicing in liver disease: mechanisms and consequences. World J Gastroenterol 16: 3091-3102.
46. Stahtea XN, Roussidis AE, Kanakis I, Tzanakakis GN, Chalkiadakis G, et al. (2007) Imatinib inhibits colorectal cancer cell growth and suppresses stromal-induced growth stimulation, MT1-MMP expression and pro-MMP2 activation. Int J Cancer 121: 2808-2814. (Pubitemid 350136431)
47. Gilles C, Polette M, Piette J, Munaut C, Thompson EW, et al. (1996) High level of MT-MMP expression is associated with invasiveness of cervical cancer cells. Int J Cancer 65: 209-213. (Pubitemid 26051683)
48. Cirri P, Chiarugi P (2011) Cancer associated fibroblasts: the dark side of the coin. Am J Cancer Res 1: 482-497.
49. Okada A, Bellocq JP, Rouyer N, Chenard MP, Rio MC, et al. (1995) Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas. Proc Natl Acad Sci U S A 92: 2730-2734.
50. Brown DC, Gatter KC (2002) Ki67 protein: the immaculate deception? Histopathology 40: 2-11. (Pubitemid 34107377)
51. Janic A, Mendizabal L, Llamazares S, Rossell D, Gonzalez C (2010) Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science 330: 1824-1827.
52. Liang D, Dong M, Hu LJ, Fang ZH, Xu X, et al. (2013) Hiwi knockdown inhibits the growth of lung cancer in nude mice. Asian Pac J Cancer Prev 14: 1067-1072.
53. Liu L, Dai Y, Chen J, Zeng T, Li Y, et al. (2014) Maelstrom promotes hepatocellular carcinoma metastasis by inducing epithelial-mesenchymal transition by way of Akt/GSK-3beta/Snail signaling. Hepatology 59: 531-543.
54. Shahali M, Kabir-Salmani M, Nayernia K, Soleimanpour-Lichaei HR, Vasei M, et al. (2013) A novel in vitro model for cancer stem cell culture using ectopically expressed piwil2 stable cell line. Cell J 15: 250-257.
55. Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, et al. (2001) Human CD34(+) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 97: 426-434. (Pubitemid 32060327)
56. Lu ZY, Dong R, Li D, Li WB, Xu FQ, et al. (2012) SNAI1 overexpression induces stemness and promotes ovarian cancer cell invasion and metastasis. Oncol Rep 27: 1587-1591.