Role of microRNAs in mammalian spermatogenesis and testicular germ cell tumors

Reproduction

Volumn 149, Issue 3, 2015, Pages R127-R137

  Wang, Li ^a,b   Xu, Chen ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Shanghai Key Laboratory of Reproductive Medicine   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; MICRORNA;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; EPIGENETICS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GERM CELL; GERM CELL TUMOR; HUMAN; MAMMAL; MEIOSIS; MITOSIS; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SEMINOMA; SERTOLI CELL; SOMATIC CELL; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIAL STEM CELL; SPERMATOGONIUM; SPERMATOZOON; STEM CELL; TESTIS; TESTIS NONSEMINOMA CANCER; ANIMAL; GENETICS; MALE; METABOLISM; NEOPLASM; TESTIS TUMOR;

MAMMALIA;

ANIMALS; HUMANS; MALE; MICRORNAS; NEOPLASMS, GERM CELL AND EMBRYONAL; SPERMATOGENESIS; TESTICULAR NEOPLASMS; TESTIS;

EID: 84922388774     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-14-0239     Document Type: Article

References (128)

1. Abu-Halima M, Hammadeh M, Schmitt J, Leidinger P, Keller A, Meese E & Backes C 2013 Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertility and Sterility 99 1249-1255.e16. (doi:10.1016/j.fertnstert.2012. 11.054)
2. Abu-HalimaM, Backes C, Leidinger P, Keller A, Lubbad AM, HammadehM & Meese E 2014 MicroRNA expression profiles in human testicular tissues of infertile men with different histopathologic patterns. Fertility and Sterility 101 78-86.e2. (doi:10.1016/j.fertnstert.2013.09.009)
3. Ambros V 2003 MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell 113 673-676. (doi:10.1016/S0092-8674 (03)00428-8)
4. Babiarz JE, Ruby JG, Wang Y, Bartel DP & Blelloch R 2008 Mouse ES cells express endogenous shRNAs, siRNAs, and other microprocessorindependent, Dicer-dependent small RNAs. Genes and Development 22 2773-2785. (doi:10.1101/gad.1705308)
5. Bao J, Li D, Wang L, Wu J, Hu Y, Wang Z, Chen Y, Cao X, Jiang C, Yan W et al. 2012 MicroRNA-449 andmicroRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. Journal of Biological Chemistry 287 21686-21698. (doi:10.1074/jbc.M111.328054)
6. Barad O, Meiri E, Avniel A, Aharonov R, Barzilai A, Bentwich I, Einav U, Gilad S, Hurban P, Karov Y et al. 2004 MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Research 14 2486-2494. (doi:10. 1101/gr.2845604)
7. Bjork JK, Sandqvist A, Elsing AN, Kotaja N & Sistonen L 2010 miR-18, a member of Oncomir-1, targets heat shock transcription factor 2 in spermatogenesis. Development 137 3177-3184. (doi:10.1242/dev. 050955)
8. Blakaj A & Lin H 2008 Piecing together the mosaic of early mammalian development through microRNAs. Journal of Biological Chemistry 283 9505-9508. (doi:10.1074/jbc.R800002200)
9. Bouhallier F, Allioli N, Lavial F, Chalmel F, Perrard MH, Durand P, Samarut J, Pain B & Rouault JP 2010 Role of miR-34c microRNA in the late steps of spermatogenesis. RNA 16 720-731. (doi:10.1261/rna. 1963810)
10. Brennecke J, Hipfner DR, Stark A, Russell RB & Cohen SM 2003 bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113 25-36. (doi:10.1016/S0092-8674(03)00231-9)
11. Buchold GM, Coarfa C, Kim J, Milosavljevic A, Gunaratne PH & Matzuk MM 2010 Analysis of microRNA expression in the prepubertal testis. PLoS ONE 5 e15317. (doi:10.1371/journal.pone.0015317)
12. Calin GA & Croce CM 2006 MicroRNA-cancer connection: the beginning of a new tale. Cancer Research 66 7390-7394. (doi:10.1158/0008-5472. CAN-06-0800)
13. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K et al. 2002 Frequent deletions and downregulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. PNAS 99 15524-15529. (doi:10.1073/pnas. 242606799)
14. Calin GA, Liu CG, Sevignani C, Ferracin M, Felli N, Dumitru CD, Shimizu M, Cimmino A, Zupo S, DonoMet al. 2004MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. PNAS 101 11755-11760. (doi:10.1073/pnas.0404432101)
15. Carmell MA & Hannon GJ 2004 RNase III enzymes and the initiation of gene silencing. Nature Structural & Molecular Biology 11 214-218. (doi:10.1038/nsmb729)
16. Carrington JC & Ambros V 2003 Role of microRNAs in plant and animal development. Science 301 336-338. (doi:10.1126/science.1085242)
17. Chen CZ, Li L, Lodish HF & Bartel DP 2004 MicroRNAs modulate hematopoietic lineage differentiation. Science 303 83-86. (doi:10.1126/ science.1091903)
18. Costinean S, Zanesi N, Pekarsky Y, Tili E, Volinia S, Heerema N & Croce CM 2006 Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. PNAS 103 7024-7029. (doi:10.1073/pnas.0602266103)
19. Dai L, Tsai-Morris CH, Sato H, Villar J, Kang JH, Zhang J & Dufau ML 2011 Testis-specific miRNA-469 up-regulated in gonadotropin-regulated testicular RNA helicase (GRTH/DDX25)-null mice silences transition protein 2 and protamine 2 messages at sites within coding region: implications of its role in germ cell development. Journal of Biological Chemistry 286 44306-44318. (doi:10.1074/jbc.M111.282756)
20. Damestoy A, Perrard MH, Vigier M, Sabido O & Durand P 2005 Transforming growth factor b-1 decreases the yield of the second meiotic division of rat pachytene spermatocytes in vitro. Reproductive Biology and Endocrinology 3 22. (doi:10.1186/1477-7827-3-22)
21. Dovere L, Fera S, Grasso M, Lamberti D, Gargioli C, Muciaccia B, Lustri AM, Stefanini M & Vicini E 2013 The niche-derived glial cell linederived neurotrophic factor (GDNF) induces migration of mouse spermatogonial stem/progenitor cells. PLoS ONE 8 e59431. (doi:10. 1371/journal.pone.0059431)
22. van den Driesche S, Sharpe RM, Saunders PT & Mitchell RT 2014 Regulation of the germ stem cell niche as the foundation for adult spermatogenesis: a role for miRNAs? Seminars in Cell & Developmental Biology 29 76-83. (doi:10.1016/j.semcdb.2014.04.006)
23. Dyce PW, Toms D & Li J 2010 Stem cells and germ cells: microRNA and gene expression signatures. Histology and Histopathology 25 505-513.
24. Dym M 1994 Spermatogonial stem cells of the testis. PNAS 91 11287-11289. (doi:10.1073/pnas.91.24.11287)
25. Esquela-Kerscher A & Slack FJ 2006 Oncomirs-microRNAs with a role in cancer. Nature Reviews. Cancer 6 259-269. (doi:10.1038/nrc1840)
26. Fok KL, Chen H, Ruan YC & Chan HC 2011 Novel regulators of spermatogenesis. Seminars in Cell & Developmental Biology 29 31-42. (doi:10.1016/j.semcdb.2014.02.008)
27. Foshay KM & Gallicano GI 2009 miR-17 family miRNAs are expressed during early mammalian development and regulate stem cell differentiation. Developmental Biology 326 431-443. (doi:10.1016/j.ydbio. 2008.11.016)
28. Gillis AJ, Stoop HJ, Hersmus R, Oosterhuis JW, Sun Y, Chen C, Guenther S, Sherlock J, Veltman I, Baeten J et al. 2007 High-throughput microRNAome analysis in human germ cell tumours. Journal of Pathology 213 319-328. (doi:10.1002/path.2230)
29. Goudarzi A, Shiota H, Rousseaux S & Khochbin S 2014 Genomescale acetylation-dependent histone eviction during spermatogenesis. Journal of Molecular Biology 426 3342-3349. (doi:10.1016/j.jmb.2014. 02.023)
30. Gregory RI & Shiekhattar R 2005 MicroRNA biogenesis and cancer. Cancer Research 65 3509-3512. (doi:10.1158/0008-5472.CAN-05-0298)
31. Grimaldi P, Di GD & Geremia R 2013 The endocannabinoid system and spermatogenesis. Frontiers in Endocrinology 4 192. (doi:10.3389/fendo. 2013.00192)
32. Gu S, Cheung HH, Lee TL, Lu G, Poon WS & Chan WY 2013 Molecular mechanisms of regulation and action of microRNA-199a in testicular germ cell tumor and glioblastomas. PLoS ONE 8 e83980. (doi:10.1371/ journal.pone.0083980)
33. Guo Y, Hai Y, Gong Y, Li Z & He Z 2014 Characterization, isolation, and culture of mouse and human spermatogonial stem cells. Journal of Cellular Physiology 229 407-413. (doi:10.1002/jcp.24471)
34. Havens MA, Reich AA, Duelli DM & Hastings ML 2012 Biogenesis of mammalian microRNAs by a non-canonical processing pathway. Nucleic Acids Research 40 4626-4640. (doi:10.1093/nar/gks026)
35. Hayashi K, de Sousa Lopes SMC, Kaneda M, Tang F, Hajkova P, Lao K, O'Carroll D, Das PP, Tarakhovsky A, Miska EA et al. 2008 MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS ONE 3 e1738. (doi:10.1371/journal.pone. 0001738)
36. He Z, Kokkinaki M, Pant D, Gallicano GI & Dym M 2009 Small RNA molecules in the regulation of spermatogenesis. Reproduction 137 901-911. (doi:10.1530/REP-08-0494)
37. He Z, Jiang J, Kokkinaki M, Tang L, Zeng W, Gallicano I, Dobrinski I & Dym M 2013 MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1. Stem Cells 31 2205-2217. (doi:10.1002/stem.1474)
38. Hess RA, Cooke PS, Hofmann MC &Murphy KM2006Mechanistic insights into the regulation of the spermatogonial stem cell niche. Cell Cycle 5 1164-1170. (doi:10.4161/cc.5.11.2775)
39. Hudson J, Duncavage E, Tamburrino A, Salerno P, Xi L, Raffeld M, Moley J & Chernock RD 2013 Overexpression of miR-10a and miR-375 and downregulation of YAP1 in medullary thyroid carcinoma. Experimental and Molecular Pathology 95 62-67. (doi:10.1016/j.yexmp.2013.05.001)
40. Huszar JM & Payne CJ 2013 MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice. Biology of Reproduction 88 15. (doi:10.1095/biolreprod.112.103747)
41. Hutvagner G, McLachlan J, Pasquinelli AE, Balint E, Tuschl T & Zamore PD 2001 A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293 834-838. (doi:10.1126/science.1062961)
42. Hwang HW& Mendell JT 2007 MicroRNAs in cell proliferation, cell death, and tumorigenesis. British Journal of Cancer 96 (Suppl 2) R40-R44.
43. Ito T, Yagi S & Yamakuchi M 2010 MicroRNA-34a regulation of endothelial senescence. Biochemical and Biophysical Research Communications 398 735-740. (doi:10.1016/j.bbrc.2010.07.012)
44. Ji Z, Lu R, Mou L, Duan YG, Zhang Q, Wang Y, Gui Y & Cai Z 2014 Expressions of miR-15a and its target gene HSPA1B in the spermatozoa of patients with varicocele. Reproduction 147 693-701. (doi:10.1530/REP-13-0656)
45. Kano M, Seki N, Kikkawa N, Fujimura L, Hoshino I, Akutsu Y, Chiyomaru T, Enokida H, Nakagawa M & Matsubara H 2010 miR-145, miR-133a and miR-133b: tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. International Journal of Cancer 127 2804-2814. (doi:10.1002/ijc.25284)
46. Kim VN, Han J & Siomi MC 2009 Biogenesis of small RNAs in animals. Nature Reviews. Molecular Cell Biology 10 126-139. (doi:10.1038/ nrm2632)
47. Korhonen HM, Meikar O, Yadav RP, Papaioannou MD, Romero Y, Da RM, Herrera PL, Toppari J, Nef S & Kotaja N 2011 Dicer is required for haploid male germ cell differentiation in mice. PLoS ONE 6 e24821. (doi:10.1371/journal.pone.0024821)
48. Kostereva N & Hofmann MC 2008 Regulation of the spermatogonial stem cell niche. Reproduction in Domestic Animals 43 (Suppl 2) 386-392. (doi:10.1111/j.1439-0531.2008.01189.x)
49. Kotaja N 2014 MicroRNAs and spermatogenesis. Fertility and Sterility 101 1552-1562. (doi:10.1016/j.fertnstert.2014.04.025)
50. Lai EC 2002 Micro RNAs are complementary to 30 UTR sequence motifs that mediate negative post-transcriptional regulation. Nature Genetics 30 363-364. (doi:10.1038/ng865)
51. Lee RC, Feinbaum RL & Ambros V 1993 The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75 843-854. (doi:10.1016/0092-8674(93)90529-Y)
52. Lee YS, Kim HK, Chung S, Kim KS & Dutta A 2005 Depletion of human micro-RNA miR-125b reveals that it is critical for the proliferation of differentiated cells but not for the down-regulation of putative targets during differentiation. Journal of Biological Chemistry 280 16635-16641. (doi:10.1074/jbc.M412247200)
53. Li C, Feng Y, Coukos G & Zhang L 2009 Therapeutic microRNA strategies in human cancer. AAPS Journal 11 747-757. (doi:10.1208/s12248-009-9145-9)
54. Li M, Yu M, Liu C, Zhu H, He X, Peng S & Hua J 2013 miR-34c works downstream of p53 leading to dairy goat male germline stem-cell (mGSCs) apoptosis. Cell Proliferation 46 223-231. (doi:10.1111/cpr. 12013)
55. Lian J, Zhang X, Tian H, Liang N, Wang Y, Liang C, Li X & Sun F 2009 Altered microRNA expression in patients with non-obstructive azoospermia. Reproductive Biology and Endocrinology 7 13. (doi:10.1186/ 1477-7827-7-13)
56. Liang X, Zhou D, Wei C, Luo H, Liu J, Fu R & Cui S 2012 MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1. PLoS ONE 7 e33861. (doi:10.1371/journal.pone.0033861)
57. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L & Hannon GJ 2004 Argonaute2 is the catalytic engine of mammalian RNAi. Science 305 1437-1441. (doi:10. 1126/science.1102513)
58. Liu X, Chen X, Yu X, Tao Y, Bode AM, Dong Z & Cao Y 2013a Regulation of microRNAs by epigenetics and their interplay involved in cancer. Journal of Experimental & Clinical Cancer Research 32 96. (doi:10.1186/ 1756-9966-32-96)
59. Liu T, Huang Y, Liu J, Zhao Y, Jiang L, Huang Q, Cheng W & Guo L 2013b MicroRNA-122 influences the development of sperm abnormalities from human induced pluripotent stem cells by regulating TNP2 expression. Stem Cells and Development 22 1839-1850. (doi:10.1089/scd.2012. 0653)
60. Looijenga LH, Hersmus R, Gillis AJ, Pfundt R, Stoop HJ, van Gurp RJ, Veltman J, Beverloo HB, van Drunen E, van Kessel AG et al. 2006 Genomic and expression profiling of human spermatocytic seminomas: primary spermatocyte as tumorigenic precursor and DMRT1 as candidate chromosome 9 gene. Cancer Research 66 290-302. (doi:10. 1158/0008-5472.CAN-05-2936)
61. Looijenga LH, Stoop H & Biermann K 2014 Testicular cancer: biology and biomarkers. Virchows Archiv 464 301-313. (doi:10.1007/s00428-013-1522-1)
62. Lu L, Katsaros D, de la Longrais IA, Sochirca O & Yu H 2007 Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Research 67 10117-10122. (doi:10.1158/0008-5472.CAN-07-2544)
63. Luo L, Ye L, Liu G, Shao G, Zheng R, Ren Z, Zuo B, Xu D, Lei M, Jiang S et al. 2010 Microarray-based approach identifies differentially expressed microRNAs in porcine sexually immature and mature testes. PLoS ONE 5 e11744. (doi:10.1371/journal.pone.0011744)
64. Maatouk DM, Loveland KL, McManus MT, Moore K & Harfe BD 2008 Dicer1 is required for differentiation of the mouse male germline. Biology of Reproduction 79 696-703. (doi:10.1095/biolreprod.108. 067827)
65. Manikandan J, Aarthi JJ, Kumar SD & Pushparaj PN 2008 Oncomirs: the potential role of non-coding microRNAs in understanding cancer. Bioinformation 2 330-334. (doi:10.6026/97320630002330)
66. Marcon E, Babak T, Chua G, Hughes T & Moens PB 2008 miRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Research 16 243-260. (doi:10.1007/s10577-007-1190-6)
67. Marczylo EL, Amoako AA, Konje JC, Gant TW & Marczylo TH 2012 Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern. Epigenetics 7 432-439. (doi:10.4161/epi.19794)
68. Mattie MD, Benz CC, Bowers J, Sensinger K, Wong L, Scott GK, Fedele V, Ginzinger D, Getts R & Haqq C 2006 Optimized high-throughput microRNA expression profiling provides novel biomarker assessment of clinical prostate and breast cancer biopsies. Molecular Cancer 5 24. (doi:10.1186/1476-4598-5-24)
69. McIver SC, Roman SD, Nixon B & McLaughlin EA 2012a miRNA and mammalian male germ cells. Human Reproduction Update 18 44-59. (doi:10.1093/humupd/dmr041)
70. McIver SC, Stanger SJ, Santarelli DM, Roman SD, Nixon B & McLaughlin EA 2012b A unique combination of male germ cell miRNAs coordinates gonocyte differentiation. PLoS ONE 7 e35553. (doi:10.1371/ journal.pone.0035553)
71. Miyaki S, Sato T, Inoue A, Otsuki S, Ito Y, Yokoyama S, Kato Y, Takemoto F, Nakasa T, Yamashita S et al. 2010 MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes and Development 24 1173-1185. (doi:10.1101/gad.1915510)
72. Moritoki Y, Hayashi Y, Mizuno K, Kamisawa H, Nishio H, Kurokawa S, Ugawa S, Kojima Y & Kohri K 2014 Expression profiling of micro-RNA in cryptorchid testes: miR-135a contributes to the maintenance of spermatogonial stem cells by regulating FoxO1. Journal of Urology 191 1174-1180. (doi:10.1016/j.juro.2013.10.137)
73. Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T & Shimotohno K 2006 Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 25 2537-2545. (doi:10.1038/sj.onc.1209283)
74. Murray MJ, Saini HK, van Dongen S, Palmer RD, Muralidhar B, Pett MR, Piipari M, Thornton CM, Nicholson JC, Enright AJ et al. 2010 The two most common histological subtypes of malignant germ cell tumour are distinguished by global microRNA profiles, associated with differential transcription factor expression. Molecular Cancer 9 290. (doi:10.1186/ 1476-4598-9-290)
75. Nana-Sinkam SP & Choi AM 2014 Epigenetics and the unfolded protein response in the lung: emerging role for microRNAs. American Journal of Respiratory and Critical Care Medicine 189 239-240. (doi:10.1164/ rccm.201312-2230ED)
76. Nicholls PK, Harrison CA, Walton KL, McLachlan RI, O'Donnell L & Stanton PG 2011 Hormonal regulation of sertoli cell micro-RNAs at spermiation. Endocrinology 152 1670-1683. (doi:10.1210/en.2010-1341)
77. Nicolas FE, Pais H, Schwach F, Lindow M, Kauppinen S, Moulton V & Dalmay T 2008 Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140. RNA 14 2513-2520. (doi:10. 1261/rna.1221108)
78. Niu Z, Goodyear SM, Rao S, Wu X, Tobias JW, Avarbock MR & Brinster RL 2011 MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. PNAS 108 12740-12745. (doi:10.1073/pnas.1109987108)
79. Okamura K, Hagen JW, Duan H, Tyler DM & Lai EC 2007 The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130 89-100. (doi:10.1016/j.cell.2007.06.028)
80. Oosterhuis JW & Looijenga LH 2005 Testicular germ-cell tumours in a broader perspective. Nature Reviews. Cancer 5 210-222. (doi:10.1038/ nrc1568)
81. Ostermeier GC, Goodrich RJ,Moldenhauer JS, DiamondMP & Krawetz SA 2005 A suite of novel human spermatozoal RNAs. Journal of Andrology 26 70-74.
82. Palmer RD, Murray MJ, Saini HK, van Dongen S, Abreu-Goodger C, Muralidhar B, Pett MR, Thornton CM, Nicholson JC, Enright AJ et al. 2010 Malignant germ cell tumors display common microRNA profiles resulting in global changes in expression of messenger RNA targets. Cancer Research 70 2911-2923. (doi:10.1158/0008-5472.CAN-09-3301)
83. Panneerdoss S, Chang YF, Buddavarapu KC, Chen HI, Shetty G, Wang H, Chen Y, Kumar TR & Rao MK 2012 Androgen-responsive microRNAs in mouse Sertoli cells. PLoS ONE 7 e41146. (doi:10.1371/journal.pone. 0041146)
84. Papaioannou MD, Lagarrigue M, Vejnar CE, Rolland AD, Kuhne F, Aubry F, Schaad O, Fort A, Descombes P, Neerman-Arbez M et al. 2011 Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice. Molecular & Cellular Proteomics 10 M900587MCP200. (doi:10. 1074/mcp.M900587-MCP200)
85. Peter ME 2010 Targeting of mRNAs by multiple miRNAs: the next step. Oncogene 29 2161-2164. (doi:10.1038/onc.2010.59)
86. Port M, Glaesener S, Ruf C, Riecke A, Bokemeyer C, Meineke V, Honecker F & Abend M 2011 Micro-RNA expression in cisplatin resistant germ cell tumor cell lines. Molecular Cancer 10 52. (doi:10. 1186/1476-4598-10-52)
87. Qiu T, Zhou X, Wang J, Du Y, Xu J, Huang Z, Zhu W, Shu Y & Liu P 2014 MiR-145, miR-133a and miR-133b inhibit proliferation, migration, invasion and cell cycle progression via targeting transcription factor Sp1 in gastric cancer. FEBS Letters 588 1168-1177. (doi:10.1016/ j.febslet.2014.02.054)
88. Radisky DC 2011 miR-200c at the nexus of epithelial-mesenchymal transition, resistance to apoptosis, and the breast cancer stem cell phenotype. Breast Cancer Research 13 110. (doi:10.1186/bcr2885)
89. Ro S, Park C, Sanders KM, McCarrey JR & Yan W 2007 Cloning and expression profiling of testis-expressed microRNAs. Developmental Biology 311 592-602. (doi:10.1016/j.ydbio.2007.09.009)
90. Romero Y, Meikar O, Papaioannou MD, Conne B, Grey C, Weier M, Pralong F, De Massy B, Kaessmann H, Vassalli JD et al. 2011 Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS ONE 6 e25241. (doi:10.1371/journal. pone.0025241)
91. Rosa A & Brivanlou AH 2011 A regulatory circuitry comprised of miR-302 and the transcription factors OCT4 and NR2F2 regulates human embryonic stem cell differentiation. EMBO Journal 30 237-248. (doi:10.1038/emboj.2010.319)
92. Sato F, Tsuchiya S, Meltzer SJ & Shimizu K 2011 MicroRNAs and epigenetics. FEBS Journal 278 1598-1609. (doi:10.1111/j.1742-4658. 2011.08089.x)
93. Silvan U, Diez-Torre A, Moreno P, Arluzea J, Andrade R, Silio M & Arechaga J 2013 The spermatogonial stem cell niche in testicular germ cell tumors. International Journal of Developmental Biology 57 185-195. (doi:10.1387/ijdb.130068ja)
94. Singh S & Li SS 2012 Epigenetic effects of environmental chemicals bisphenol A and phthalates. International Journal of Molecular Sciences 13 10143-10153. (doi:10.3390/ijms130810143)
95. Smorag L, Zheng Y, Nolte J, Zechner U, Engel W & Pantakani DV 2012 MicroRNA signature in various cell types of mouse spermatogenesis: evidence for stage-specifically expressed miRNA-221,-203 and-34b-5p mediated spermatogenesis regulation. Biology of the Cell 104 677-692. (doi:10.1111/boc.201200014)
96. Tanaka K, Kondo K, Kitajima K, Muraoka M, Nozawa A & Hara T 2013 Tumor-suppressive function of protein-tyrosine phosphatase nonreceptor type 23 in testicular germ cell tumors is lost upon overexpression of miR142-3p microRNA. Journal of Biological Chemistry 288 23990-23999. (doi:10.1074/jbc.M113.478891)
97. Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC, Sun YA, Lee C, Tarakhovsky A, Lao K & Surani MA 2007 Maternal microRNAs are essential for mouse zygotic development. Genes and Development 21 644-648. (doi:10.1101/gad.418707)
98. Tome M, Lopez-Romero P, Albo C, Sepulveda JC, Fernandez-Gutierrez B, Dopazo A, Bernad A & Gonzalez MA 2011 miR-335 orchestrates cell proliferation, migration and differentiation in human mesenchymal stem cells. Cell Death and Differentiation 18 985-995. (doi:10.1038/cdd. 2010.167)
99. Tong MH, Mitchell DA,McGowan SD, Evanoff R & Griswold MD 2012 Two miRNA clusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of spermatogonial differentiation in mice. Biology of Reproduction 86 72. (doi:10.1095/biolreprod.111.096313)
100. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y & Tokino T 2008 Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Research 68 4123-4132. (doi:10.1158/0008-5472.CAN-08-0325)
101. Udali S, Guarini P, Moruzzi S, Choi SW & Friso S 2013 Cardiovascular epigenetics: from DNA methylation to microRNAs. Molecular Aspects of Medicine 34 883-901. (doi:10.1016/j.mam.2012.08.001)
102. Ventela S, Makela JA, Kulmala J, Westermarck J & Toppari J 2012 Identification and regulation of a stage-specific stem cell niche enriched by Nanog-positive spermatogonial stem cells in the mouse testis. Stem Cells 30 1008-1020. (doi:10.1002/stem.1077)
103. Vogt M, Munding J, Gruner M, Liffers ST, Verdoodt B, Hauk J, Steinstraesser L, Tannapfel A & Hermeking H 2011 Frequent concomitant inactivation of miR-34a andmiR-34b/c by CpGmethylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Archiv 458 313-322. (doi:10.1007/s00428-010-1030-5)
104. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M et al. 2006 A microRNA expression signature of human solid tumors defines cancer gene targets. PNAS 103 2257-2261. (doi:10.1073/pnas.0510565103)
105. Voorhoeve PM, le SC, Schrier M, Gillis AJ, Stoop H, Nagel R, Liu YP, van Duijse J, Drost J, Griekspoor A et al. 2006 A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124 1169-1181. (doi:10.1016/j.cell.2006.02.037)
106. Voorhoeve PM, le SC, Schrier M, Gillis AJ, Stoop H, Nagel R, Liu YP, van Duijse J, Drost J, Griekspoor A et al. 2007 A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Advances in Experimental Medicine and Biology 604 17-46.
107. Wang X & Wang X 2006 Systematic identification ofmicroRNA functions by combining target prediction and expression profiling. Nucleic Acids Research 34 1646-1652. (doi:10.1093/nar/gkl068)
108. Wang F, Yu J, Yang GH,Wang XS & Zhang JW 2011 Regulation of erythroid differentiation by miR-376a and its targets. Cell Research 21 1196-1209. (doi:10.1038/cr.2011.79)
109. Wightman B, Ha I & Ruvkun G 1993 Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75 855-862. (doi:10.1016/0092-8674(93)90530-4)
110. Wu J, Bao J, Wang L, Hu Y & Xu C 2011 MicroRNA-184 downregulates nuclear receptor corepressor 2 in mouse spermatogenesis. BMC Developmental Biology 11 64. (doi:10.1186/1471-213X-11-64)
111. Wu Q, Song R, Ortogero N, Zheng H, Evanoff R, Small CL, Griswold MD, Namekawa SH, Royo H, Turner JM et al. 2012 The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. Journal of Biological Chemistry 287 25173-25190. (doi:10.1074/jbc. M112.362053)
112. Wu J, Bao J, Kim M, Yuan S, Tang C, Zheng H, Mastick GS, Xu C & Yan W 2014a Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. PNAS 111 E2851-E2857. (doi:10.1073/pnas.1407777111)
113. Wu J, Zhu H, Song W, Li M, Liu C, Li N, Tang F, Mu H, Liao M, Li X et al. 2014b Identification of conservative microRNAs in Saanen dairy goat testis through deep sequencing. Reproduction in Domestic Animals 49 32-40. (doi:10.1111/rda.12217)
114. Xu P, Vernooy SY, GuoM& Hay BA 2003 The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism. Current Biology 13 790-795. (doi:10.1016/S0960-9822(03)00250-1)
115. Yan N, Lu Y, Sun H, Tao D, Zhang S, Liu W & Ma Y 2007 A microarray for microRNA profiling in mouse testis tissues. Reproduction 134 73-79. (doi:10.1530/REP-07-0056)
116. Yan N, Lu Y, Sun H, QiuW, Tao D, Liu Y, Chen H, Yang Y, Zhang S, Li X et al. 2009 Microarray profiling of microRNAs expressed in testis tissues of developing primates. Journal of Assisted Reproduction and Genetics 26 179-186. (doi:10.1007/s10815-009-9305-y)
117. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T et al. 2006 Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9 189-198. (doi:10.1016/j.ccr.2006.01.025)
118. Yang Q, Hua J, Wang L, Xu B, Zhang H, Ye N, Zhang Z, Yu D, Cooke HJ, Zhang Y et al. 2013a MicroRNA and piRNA profiles in normal human testis detected by next generation sequencing. PLoS ONE 8 e66809. (doi:10.1371/journal.pone.0066809)
119. Yang QE, Racicot KE, Kaucher AV, Oatley MJ & Oatley JM 2013b MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells. Development 140 280-290. (doi:10. 1242/dev.087403)
120. Yi R, Poy MN, Stoffel M & Fuchs E 2008 A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452 225-229. (doi:10. 1038/nature06642)
121. Yu Z & Hecht NB 2008 The DNA/RNA-binding protein, translin, binds microRNA122a and increases its in vivo stability. Journal of Andrology 29 572-579. (doi:10.2164/jandrol.108.005090)
122. Yu Z, Raabe T & Hecht NB 2005 MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biology of Reproduction 73 427-433. (doi:10.1095/biolreprod.105.040998)
123. Yu M, Mu H, Niu Z, Chu Z, Zhu H & Hua J 2014 miR-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2. Journal of Cellular Biochemistry 115 232-242. (doi:10.1002/jcb.24655)
124. Zhang S, Yu M, Liu C,Wang L, Hu Y, Bai Y & Hua J 2012 MIR-34c regulates mouse embryonic stem cells differentiation into male germ-like cells through RARg. Cell Biochemistry and Function 30 623-632. (doi:10. 1002/cbf.2922)
125. Zheng J, Xue H, Wang T, Jiang Y, Liu B, Li J, Liu Y, Wang W, Zhang B & Sun M 2011 miR-21 downregulates the tumor suppressor P12 CDK2AP1 and stimulates cell proliferation and invasion. Journal of Cellular Biochemistry 112 872-880. (doi:10.1002/jcb.22995)
126. Zhong X, Li N, Liang S, Huang Q, Coukos G & Zhang L 2010 Identification of microRNAs regulating reprogramming factor LIN28 in embryonic stem cells and cancer cells. Journal of Biological Chemistry 285 41961-41971. (doi:10.1074/jbc.M110.169607)
127. Zovoilis A, Nolte J, Drusenheimer N, Zechner U, Hada H, Guan K, Hasenfuss G, Nayernia K & Engel W 2008 Multipotent adult germline stem cells and embryonic stem cells have similar microRNA profiles. Molecular Human Reproduction 14 521-529. (doi:10.1093/molehr/ gan044)
128. Zovoilis A, Pantazi A, Smorag L, Opitz L, Riester GS, Wolf M, Zechner U, Holubowska A, Stewart CL & EngelW2010 Embryonic stem cell-related miRNAs are involved in differentiation of pluripotent cells originating from the germ line. Molecular Human Reproduction 16 793-803. (doi:10.1093/molehr/gaq053)