Next generation sequencing analysis reveals segmental patterns of microRNA expression in mouse epididymal epithelial cells

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Nixon, Brett ^a   Stanger, Simone J ^a   Mihalas, Bettina P ^a   Reilly, Jackson N ^a   Anderson, Amanda L ^a   Dun, Matthew D ^b   Tyagi, Sonika ^c   Holt, Janet E ^b   McLaughlin, Eileen A ^a   Yenugu, Suresh ^d  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c Australian Genome Research Facility Ltd   (Australia)

^d UNIVERSITY OF HYDERABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; MICRORNA; MICRORNA 140 5P; MICRORNA 15A 5P; MICRORNA 17 5P; MICRORNA 193A 3P; MICRORNA 19B 3P; MICRORNA 200C 3P; MICRORNA 204 5P; MICRORNA 205 5P; MICRORNA 23A 3P; MICRORNA 24 3P; MICRORNA 27B 3P; MICRORNA 30A 3P; MICRORNA 30A 5P; MICRORNA 31 5P; MICRORNA 34A 5P; MICRORNA 375 3P; MICRORNA 410 3P; MICRORNA 467D 3P; MICRORNA 470; MICRORNA 486 5P; MICRORNA 7B 5P; MICRORNA 9 5P; MICRORNA 92A 3P; MICRORNA 96B 5P; MICRORNA LET 7A 5P; MICRORNA LET 7B 5P; MICRORNA LET 7C 5P; UNCLASSIFIED DRUG; UNINDEXED DRUG; MIRN196 MICRORNA, MOUSE; MIRN204 MICRORNA, MOUSE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EPIDIDYMIS; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE FUNCTION; HUMAN; HUMAN TISSUE; MALE; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTIBODY SPECIFICITY; CONSERVED SEQUENCE; CYTOLOGY; GENE EXPRESSION REGULATION; HIGH THROUGHPUT SEQUENCING; METABOLISM; NUCLEOTIDE SEQUENCE; PROCEDURES; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; EPIDIDYMIS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; MICE; MICRORNAS; ORGAN SPECIFICITY; RATS; SEQUENCE ANALYSIS, RNA;

EID: 84942890595     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135605     Document Type: Article

References (53)

1. Hermo L, Pelletier RM, Cyr D.G., Smith CE. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech. 2010; 73: 241-278. doi: 10.1002/jemt.20783 PMID: 19941293
2. Aitken RJ, Nixon B, Lin M., Koppers AJ, Lee YH, Baker MA. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl. 2007; 9: 554-564. PMID: 17589795
3. Johnston DS, Jelinsky SA, Bang H.J., DiCandeloro P., Wilson E, Kopf GS, et al The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod. 2005; 73: 404-413. PMID: 15878890
4. Dacheux JL, Belleannee C, Jones R, Labas V, Belghazi M, Guyonnet B, et al. Mammalian epididymal proteome. Mol Cell Endocrinol. 2009; 306: 45-50. doi: 10.1016/j.mce.2009.03.007 PMID: 19464100
5. Li Y, Wang HY, Wan F.C., Liu FJ, Liu J, Zhang N, et al Deep sequencing analysis of small non-coding RNAs reveals the diversity of microRNAs and piRNAs in the human epididymis. Gene. 2012; 497: 330-335. doi: 10.1016/j.gene.2012.01.038 PMID: 22313525
6. Ma W, Hu S, Yao G., Xie S, Ni M, Liu Q., et al. An androgen receptor-microrna-29a regulatory circuitry in mouse epididymis. J Biol Chem. 2013; 288: 29369-29381. doi: 10.1074/jbc.M113.454066 PMID: 23960076
7. Ma W, Xie S, Ni M, Huang X, Hu S, Liu Q, et al. MicroRNA-29a inhibited epididymal epithelial cell proliferation by targeting nuclear autoantigenic sperm protein (NASP). J Biol Chem. 2012; 287:10189-10199. doi: 10.1074/jbc.M111.303636 PMID: 22194605
8. Zhang J, Liu Q, Zhang W., Li J, Li Z, Tang Z., et al. Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides. Acta Biochim Biophys Sin (Shanghai). 2010; 42:145-153.
9. Zhang YL, Zhang JS, Zhou Y.C., Zhao Y., Ni MJ. Identification of microRNAs and application of RNA interference for gene targeting in vivo in the rat epididymis. J Androl. 2011; 32: 587-591. doi: 10.2164/jandrol.111.013060 PMID: 21764899
10. Zhou Y, Zheng M, Shi Q, Zhang L, Zhen W, Chen W, et al. An epididymis-specific secretory protein HongrES1 critically regulates sperm capacitation and male fertility. PLoSOne. 2008; 3: e4106. doi: 10.1371/journal.pone.0004106 PMID: 19116669
11. Belleannee C, Calvo E, Caballero J, Sullivan R. Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol Reprod. 2013; 89: 30. doi: 10.1095/biolreprod.113. 110486 PMID: 23803555
12. Belleannee C, Calvo E, Thimon V., Cyr DG, Legare C, Garneau L, et al Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoSOne. 2012; 7: e34996. doi: 10.1371/journal.pone.0034996 PMID: 22511979
13. Belleannee C, Legare C, Calvo E, Thimon V, Sullivan R. microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum Reprod. 2013; 28:1455-1467. doi: 10.1093/humrep/det088 PMID: 23539611
14. Truesdell SS, Mortensen RD, Seo M, Schroeder JC, Lee JH, LeTonqueze O, et al. MicroRNA-mediated mRNA translation activation in quiescent cells and oocytes involves recruitment of a nuclear microRNP. Sci Reports. 2012; 2: 842.
15. Ambros V. The functions of animal microRNAs. Nature. 2004; 431: 350-355. PMID: 15372042
16. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-297. PMID: 14744438
17. Bouhallier F, Allioli N, Lavial F., Chalmel F, Perrard MH, Durand P, et al. Role of miR-34c microRNA in the late steps of spermatogenesis. RNA. 2010; 16: 720-731. doi: 10.1261/rna.1963810 PMID: 20150330
18. He Z, Kokkinaki M, Pant D., Gallicano GI, Dym M. Small RNA molecules in the regulation of spermatogenesis. Reproduction. 2009; 137: 901-911. doi: 10.1530/REP-08-0494 PMID: 19318589
19. Liu D, Li L, Fu H., Li S, Li J. Inactivation of Dicer1 has a severe cumulative impact on the formation of mature germ cells in mouse testes. Biochem Biophys Res Commun. 2012; 422:114-120. doi: 10.1016/j.bbrc.2012.04.118 PMID: 22564735
20. McIver SC, Roman SD, Nixon B, McLaughlin EA. miRNA and mammalian male germ cells. Hum Reprod Update. 2012; 18: 44-59. doi: 10.1093/humupd/dmr041 PMID: 21989172
21. McIver SC, Stanger SJ, Santarelli DM, Roman S.D., Nixon B., McLaughlin EA. A unique combination of male germ cell miRNAs coordinates gonocyte differentiation. PLoS One. 2012; 7: e35553. doi: 10. 1371/journal.pone.0035553 PMID: 22536405
22. Nicholls PK, Harrison CA, Walton K.L., McLachlan RI, O'Donnell L, Stanton PG. Hormonal regulation of sertoli cell micro-RNAsatspermiation. Endocrinology. 2011; 152:1670-1683. doi: 10.1210/en.2010-1341 PMID: 21325043
23. Landgraf P, Rusu M, Sheridan R., Sewer A, Iovino N, Aravin A., et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007; 129:1401-1414. PMID: 17604727
24. Bjorkgren I, Gylling H, Turunen H., Huhtaniemi I, Strauss L, Poutanen M., et al. Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane. FASEB J. 2015; 29: 433-442. doi: 10.1096/fj.14-259382 PMID: 25366345
25. Bjorkgren I, Saastamoinen L, Krutskikh A., Huhtaniemi I, Poutanen M, Sipila P. Dicer1 ablation in the mouse epididymis causes dedifferentiation of the epithelium and imbalance in sex steroid signaling. PLoSOne. 2012; 7: e38457. doi: 10.1371/journal.pone.0038457 PMID: 22701646
26. Dun MD, Anderson AL, Bromfield E.G., Asquith KL, Emmett B, McLaughlin EA, et al. Investigation of the expression and functional significance of the novel mouse sperm protein, adisintegrin and metalloprotease with thrombospondin type 1 motifs Number 10 (ADAMTS10). Int J Androl. 2012; 35: 572-589. doi: 10.1111/j.1365-2605.2011.01235.x PMID: 22458710
27. Zuo WL, Li S, Huang J.H., Yang DL, Zhang G, Chen SL, et al Sodium coupled bicarbonate influx regulates intracellular and apical pH in cultured rat caput epididymal epithelium. PLoS One. 2011; 6: e22283. doi: 10.1371/journal.pone.0022283 PMID: 21887217
28. Edgar R, Domrachev M, Lash AE Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002; 30: 207-210. PMID: 11752295
29. Livak KJ, Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402-408. PMID: 11846609
30. Sipila P, Shariatmadari R, Huhtaniemi I.T., Poutanen M. Immortalization of epididymal epithelium in transgenic mice expressing simian virus 40 T antigen: characterization of cell lines and regulation of the polyoma enhancer activator 3. Endocrinology. 2004; 145: 437-446. PMID: 14527890
31. Jelinsky SA, Turner TT, Bang H.J., Finger JN, Solarz MK, Wilson E, et al. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol Reprod. 2007; 76: 561-570. PMID: 17167166
32. Johnston DS, Turner TT, Finger J.N., Owtscharuk TL, Kopf GS, Jelinsky SA. Identification of epididymis-specific transcripts in the mouse and rat by transcriptional profiling. Asian J Androl. 2007; 9: 522-527. PMID: 17589790
33. Roush S, Slack FJ The let-7 family of microRNAs. Trends Cell Biol. 2008; 18: 505-516. doi: 10.1016/j. tcb.2008.07.007 PMID: 18774294
34. Cooper TG. The epididymis, sperm maturation and fertilisation. Berlin: Springer-Verlag; 1986.
35. Ni MJ, Hu ZH, Liu Q, Liu M.F., Lu MH, Zhang JS, et al. Identification and characterization of a novel non-coding RNA involved in sperm maturation. PLoS One. 2011; 6: e26053. doi: 10.1371/journal.pone. 0026053 PMID: 22022505
36. Krawetz SA, Kruger A, Lalancette C, Tagett R., Anton E, Draghici S, et al A survey of small RNAs in human sperm. Hum Reprod. 2011; 26: 3401-3412. doi: 10.1093/humrep/der329 PMID: 21989093
37. Miller D, Briggs D, Snowden H., Hamlington J, Rollinson S, Lilford R., et al. A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis. Gene. 1999; 237: 385-392. PMID: 10521662
38. Miller D, Ostermeier GC Spermatozoal RNA: Why is it there and what does it do? Gynecol Obstet Fertil. 2006; 34: 840-846. PMID: 16971154
39. Ostermeier GC, Goodrich RJ, Diamond M.P., Dix DJ, Krawetz SA. Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil Steril. 2005; 83:1687-1694. PMID: 15950637
40. Guyonnet B, Dacheux F, Dacheux J.L., Gatti JL. The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J Androl. 2011; 32: 651-664. doi: 10.2164/jandrol.111. 013086 PMID: 21764898
41. Dacheux JL, Belghazi M, Lanson Y., Dacheux F. Human epididymal secretome and proteome. Mol Cell Endocrinol. 2006; 250: 36-42. PMID: 16431015
42. Dacheux JL, Castella S, Gatti JL, Dacheux F. Epididymal cell secretory activities and the role of proteins in boar sperm maturation. Theriogenology. 2005; 63: 319-341. PMID: 15626402
43. Wong N, Wang X. miRDB: an online resource for microRNA target prediction and functional annotations. Nucleic Acids Res. 2015; 43: D146-152. doi: 10.1093/nar/gku1104 PMID: 25378301
44. Nagaraju GP, Dontula R, El-Rayes BF, Lakka SS. Molecular mechanisms underlying the divergent roles of SPARC in human carcinogenesis. Carcinogenesis. 2014; 35: 967-973. doi: 10.1093/carcin/bgu072 PMID: 24675529
45. Yekta S, Tabin CJ, Bartel DP MicroRNAs in the Hox network: an apparent link to posterior prevalence. Nat Rev Genet. 2008; 9: 789-796. doi: 10.1038/nrg2400 PMID: 18781158
46. Bomgardner D, Hinton BT, Turner TT. Hox transcription factors may play a role in regulating segmental function of the adult epididymis. J Androl. 2001; 22: 527-531. PMID: 11451347
47. Bomgardner D, Hinton BT, Turner TT. 5' hox genes and meis 1, a hox-DNA binding cofactor, are expressed in the adult mouse epididymis. Biol Reprod. 2003; 68: 644-650. PMID: 12533430
48. Yeung CH, Wang K, Cooper TG. Why are epididymal tumours so rare? Asian J Androl. 2012; 14: 465-475. doi: 10.1038/aja.2012.20 PMID: 22522502
49. Wang K, Li N, Yeung C.H., Li JY, Wang HY, Cooper TG. Oncogenic Wnt/beta-catenin signalling pathways in the cancer-resistant epididymis have implications for cancer research. Mol Hum Reprod. 2013; 19: 57-71. doi: 10.1093/molehr/gas051 PMID: 23155044
50. Nadiminty N, Tummala R, Lou W, Zhu Y, Zhang J, Chen X, et al. MicroRNA let-7c suppresses androgen receptor expression and activity via regulation of Myc expression in prostate cancer cells. J Biol Chem. 2012; 287:1527-1537. doi: 10.1074/jbc.M111.278705 PMID: 22128178
51. Boyerinas B, Park SM, Hau A, Murmann A.E., Peter ME. The role of let-7 in cell differentiation and cancer. Endocrine-Related Cancer. 2010; 17: F19-36. doi: 10.1677/ERC-09-0184 PMID: 19779035
52. Johnson CD, Esquela-Kerscher A, Stefani G., Byrom M, Kelnar K, Ovcharenko D., et al. The let-7 micro-RNA represses cell proliferation pathways in human cells. Cancer Res. 2007; 67: 7713-7722. PMID: 17699775
53. Kim W, Kim M, Jho EH Wnt/beta-catenin signalling: from plasma membrane to nucleus. Biochem J. 2013; 450: 9-21. doi: 10.1042/BJ20121284 PMID: 23343194