Mir-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2

Journal of Cellular Biochemistry

Volumn 115, Issue 2, 2014, Pages 232-242

  Yu, Meng ^a   Mu, Hailong ^a   Niu, Zhiwei ^a   Chu, Zhili ^a   Zhu, Haijing ^a   Hua, Jinlian ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Differentiation; miR 34c; Nanos2; Spermatogonial Stem Cells (SSCs)

Indexed keywords

MICRORNA; MICRORNA 34C; PROTEIN NANOS2; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE INTERACTION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOGONIAL STEM CELL; STEM CELL; UPREGULATION; WESTERN BLOTTING;

DIFFERENTIATION; MIR-34C; NANOS2; SPERMATOGONIAL STEM CELLS (SSCS);

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MEIOSIS; MICE; MICRORNAS; RNA-BINDING PROTEINS;

EID: 84890521618     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24655     Document Type: Article

References (40)

1. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM, Page DC,. 2008. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci USA 105: 14976-14980.
2. 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.
3. 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.
4. Cannell IG, Kong YW, Johnston SJ, Chen ML, Collins HM, Dobbyn HC, Elia A, Kress TR, Dickens M, Clemens MJ, Heery DM, Gaestel M, Eilers M, Willis AE, Bushell M,. 2010. p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci USA 107: 5375-5380.
5. Cao H, Chu Y, Lv X, Qiu P, Liu C, Zhang H, Li D, Peng S, Dou Z, Hua J,. 2012. GSK3 inhibitor-BIO regulates proliferation of immortalized pancreatic mesenchymal stem cells (iPMSCs). PLoS ONE 7: e31502.
6. Cao H, Chu Y, Zhu H, Sun J, Pu Y, Gao Z, Yang C, Peng S, Dou Z, Hua J,. 2011. Characterization of immortalized mesenchymal stem cells derived from foetal porcine pancreas. Cell Prolif 44: 19-32.
7. Chu Z, Liu C, Bai Y, Zhu H, Hu Y, Hua J,. 2013. A three-dimensional (3D) environment to keep the integrity of mouse testicular can occurrence of meiosis. J Inter Agri 12: 1481-1488.
8. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY,. 2007. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 67: 8433-8438.
9. Curry E, Safranski TJ, Pratt SL,. 2011. Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76: 1532-1539.
10. Dweep H, Sticht C, Pandey P, Gretz N,. 2011. miRWalk-database: Prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 44: 839-847.
11. Hua J, Zhang S,. 2010. MicroRNAs and mammalian germ cell development. Chinese J Anat 33: 281-285.
12. Huszar JM, Payne CJ,. 2013. MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice. Biol Reprod 88: 15.
13. Jørgensen A, Nielsen JE, Almstrup K, Toft BG, Petersen BL, Rajpert-De Meyts E,. 2013. Dysregulation of the mitosis-meiosis switch in testicular carcinoma in situ. J Pathol 229: 588-598.
14. Julaton VT, Reijo Pera RA,. 2011. NANOS3 function in human germ cell development. Hum Mol Genet 20: 2238-2250.
15. Kee K, Angeles VT, Flores M, Nguyen HN, Reijo Pera RA,. 2009. Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 462: 222-225.
16. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC,. 2006. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA 103: 2474-2479.
17. 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 Prolif 46: 223-231.
18. 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.
19. Liu C, Yu M, Zhu HJ, Li MZ, Hua JL,. 2012. Construction of miR-34c lentiviral expression vector and its infection in dairy goat germ line stem cells. Scientia Agricultura Sinica 45: 3414-3421.
20. Liu WM, Pang RT, Chiu PC, Wong BP, Lao K, Lee KF, Yeung WS,. 2012. Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc Natl Acad Sci USA 109: 490-494.
21. Liu T, Huang Y, Liu J, Zhao Y, Jiang L, Huang Q, Cheng W, Guo L,. 2013. MicroRNA-122 influences the development of sperm abnormalities from human iPS cells by regulating TNP2 expression. Stem Cells Dev 22: 1839-1850.
22. Lize M, Pilarski S, Dobbelstein M,. 2010. E2F1-inducible microRNA 449a/b suppresses cell proliferation and promotes apoptosis. Cell Death Differ 17: 452-458.
23. Luo L, Ye L, Liu G, Shao G, Zheng R, Ren Z, Zuo B, Xu D, Lei M, Jiang S, Deng C, Xiong Y, Li F,. 2010. Microarray-based approach identifies differentially expressed microRNAs in porcine sexually immature and mature testes. PLoS ONE 5: e11744.
24. McIver SC, Roman SD, Nixon B, McLaughlin EA,. 2012a. miRNA and mammalian male germ cells. Hum Reprod Update 18: 44-59.
25. 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.
26. 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. Proc Natl Acad Sci USA 108: 12740-12745.
27. Olszewska M, Bujarski JJ, Kurpisz M,. 2012. P-bodies and their functions during mRNA cell cycle: Mini-review. Cell Biochem Funct 30: 177-182.
28. Ro S, Song R, Park C, Zheng H, Sanders KM, Yan W,. 2007. Cloning and expression profiling of small RNAs expressed in the mouse ovary. RNA 13: 2366-2380.
29. Sada A, Suzuki A, Suzuki H, Saga Y,. 2009. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325: 1394-1398.
30. Sada A, Hasegawa K, Pin PH, Saga Y,. 2012. NANOS2 acts downstream of glial cell line-derived neurotrophic factor signaling to suppress differentiation of spermatogonial stem cells. Stem Cells 30: 280-291.
31. Shen R, Xie T,. 2010. NANOS: A germline stem cell's Guardian Angel. J Mol Cell Biol 2: 76-77.
32. Suzuki A, Saga Y,. 2008. Nanos2 suppresses meiosis and promotes male germ cell differentiation. Genes Dev 22: 430-435.
33. 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. Biol Reprod 86: 72.
34. Wang X,. 2008. miRDB: A microRNA target prediction and functional annotation database with a wiki interface. RNA 14: 1012-1017.
35. Wu J, Bao J, Wang L, Hu Y, Xu C,. 2011. MicroRNA-184 downregulates nuclear receptor corepressor 2 in mouse spermatogenesis. BMC Dev Biol 11: 64.
36. Yan N, Lu Y, Sun H, Qiu W, Tao D, Liu Y, Chen H, Yang Y, Zhang S, Li X, Ma Y,. 2009. Microarray profiling of microRNAs expressed in testis tissues of developing primates. J Assist Reprod Genet 26: 179-186.
37. Zhang S, Sun J, Pan S, Zhu H, Wang L, Hu Y, Wang J, Wang F, Cao H, Yan X, Hua J,. 2011. Retinol (vitamin A) maintains self-renewal of pluripotent male germline stem cells (mGSCs) from adult mouse testis. J Cell Biochem 112: 1009-1021.
38. 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 Biochem Funct 30: 623-632.
39. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, Small C, Griswold MD,. 2008. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-sufficient postnatal murine testes. Biol Reprod 79: 35-42.
40. Zhu H, Liu C, Sun J, Li M, Hua J,. 2012. Effect of GSK-3 inhibitor on the proliferation of multipotent male germ line stem cells (mGSCs) derived from goat testis. Theriogenology 77: 1939-1950.