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

Volumn 86, Issue 3, 2012, Pages

  Tong, Ming Han ^a   Mitchell, Debra Ann ^a   Mcgowan, Samantha Dawn ^a   Evanoff, Ryan ^a   Griswold, Michael D ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Microrna; Mir 106b 25 cluster; Mir 17 92 cluster; Retinoic acid; Spermatogonial differentiation

Indexed keywords

BIM PROTEIN; MICRORNA; MICRORNA 106B 25; MICRORNA 17 92; RETINOIC ACID; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; MIRN106 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; DOWN REGULATION; EPIDIDYMIS; FEMALE; GERM CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPERMATOGONIUM; TESTIS; UPREGULATION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; GENETICS; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

MUS;

ANIMALS; CELL DIFFERENTIATION; DOWN-REGULATION; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS; TRETINOIN;

EID: 84860624552     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.096313     Document Type: Article

References (49)

1. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell selfrenewal in mammals. Annu Rev Cell Dev Biol 2008; 24:263-286.
2. de Rooij DG. Proliferation and differentiation of spermatogonial stem cells. Reproduction 2001; 121:347-354.
3. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 2010; 328:62-67.
4. Ambros V. The functions of animal microRNAs. Nature 2004; 431:350-355.
5. Mishima T, Takizawa T, Luo SS, Ishibashi O, Kawahigashi Y, Mizuguchi Y, Ishikawa T, Mori M, Kanda T, Goto T, Takizawa T. MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 2008; 136:811-822.
6. Ro S, Park C, Sanders KM, McCarrey JR, Yan W. Cloning and expression profiling of testis-expressed microRNAs. Dev Biol 2007; 311:592-602.
7. Yan N, Lu Y, Sun H, Qiu W, Tao D, Liu Y, Chen H, Yang Y, Zhang S, Li X, Ma Y. Microarray profiling of microRNAs expressed in testis tissues of developing primates. J Assist Reprod Genet 2009; 26:179-186.
8. Yan N, Lu Y, Sun H, Tao D, Zhang S, Liu W, Ma Y. A microarray for microRNA profiling in mouse testis tissues. Reproduction 2007; 134:73-79.
9. Buchold GM, Coarfa C, Kim J, Milosavljevic A, Gunaratne PH, Matzuk MM. Analysis of microRNA expression in the prepubertal testis. PLoS One 2010; 5:e15317.
10. Tong MH, Mitchell D, Evanoff R, Griswold MD. Expression of Mirlet7 family microRNAs in response to retinoic acid-induced spermatogonial differentiation in mice. Biol Reprod 2011; 85:189-197.
11. Niu Z, Goodyear SM, Rao S, Wu X, Tobias JW, Avarbock MR, Brinster RL. MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 2011; 108:12740-12745.
12. Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, Lao K, O'Carroll D, Das PP, Tarakhovsky A, Miska EA, Surani MA. MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 2008; 3:e1738.
13. Maatouk DM, Loveland KL, McManus MT, Moore K, Harfe BD. Dicer1 is required for differentiation of the mouse male germline. Biol Reprod 2008; 79:696-703.
14. Zhou Q, Li Y, Nie R, Friel P, Mitchell D, Evanoff RM, Pouchnik D, Banasik B, McCarrey JR, Small C, Griswold MD. Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biol Reprod 2008; 78:537-545.
15. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for selfrenewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 2004; 101:16489-16494.
16. Kubota H, Avarbock MR, Brinster RL. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 2004; 71:722-731.
17. 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.
18. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008; 132:875-886.
19. Gallardo T, Shirley L, John GB, Castrillon DH. Generation of a germ cellspecific mouse transgenic Cre line, Vasa-Cre. Genesis 2007; 45:413-417.
20. Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell 2008; 133:217-222.
21. Hendrickson DG, Hogan DJ, McCullough HL, Myers JW, Herschlag D, Ferrell JE, Brown PO. Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol 2009; 7:e1000238.
22. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010; 466:835-840.
23. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19:92-105.
24. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120:15-20.
25. Coultas L, Bouillet P, Loveland KL, Meachem S, Perlman H, Adams JM, Strasser A. Concomitant loss of proapoptotic BH3-only Bcl-2 antagonists Bik and Bim arrests spermatogenesis. EMBO J 2005; 24:3963-3973.
26. Rossi P, Sette C, Dolci S, Geremia R. Role of c-kit in mammalian spermatogenesis. J Endocrinol Invest 2000; 23:609-615.
27. Winnall WR, Muir JA, Hedger MP. Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro. J Leukoc Biol 2011; 90:133-143.
28. Oatley JM, Kaucher AV, Avarbock MR, Brinster RL. Regulation of mouse spermatogonial stem cell differentiation by STAT3 signaling. Biol Reprod 2010; 83:427-433.
29. Tamminga J, Kathiria P, Koturbash I, Kovalchuk O. DNA damageinduced upregulation of miR-709 in the germline downregulates BORIS to counteract aberrant DNA hypomethylation. Cell Cycle 2008; 7:3731-3736.
30. Choi Y, Qin Y, Berger MF, Ballow DJ, Bulyk ML, Rajkovic A. Microarray analyses of newborn mouse ovaries lacking Nobox. Biol Reprod 2007; 77:312-319.
31. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403:901-906.
32. Boyerinas B, Park SM, Hau A, Murmann AE, Peter ME. The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer 2010; 17:F19-F36.
33. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler MU, Ganser A, Eder M, Scherr M. Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood 2007; 109:4399-4405.
34. Mi S, Li Z, Chen P, He C, Cao D, Elkahloun A, Lu J, Pelloso LA, Wunderlich M, Huang H, Luo RT, Sun M, et al. Aberrant overexpression and function of the miR-17-92 cluster in MLL-rearranged acute leukemia. Proc Natl Acad Sci U S A 2010; 107:3710-3715.
35. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y, Takahashi T. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65:9628-9632.
36. Petrocca F, Vecchione A, Croce CM. Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res 2008; 68:8191-8194.
37. Zhang ZW, An Y, Teng CB. The roles of miR-17-92 cluster in mammal development and tumorigenesis [in Chinese]. Yi Chuan 2009; 31:1094-1100.
38. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006; 103:2257-2261.
39. Northeott PA, Fernandez-L A, Hagan JP, Ellison DW, Rutka JT, Croce CM, Kenney AM, Taylor MD. The mir-17/92 polycistron is amplified and upregulated in sonic hedgehog-driven medulloblastomas and induced by N-myc in sonic hedgehog-treated cerebellar neural precursors. Cancer Res 2009; 69:3249-3255.
40. Novotny GW, Sonne SB, Nielsen JE, Jonstrup SP, Hansen MA, Skakkebaek NE, Rajpert-De Meyts E, Kjems J, Leffers H. Translational repression of E2F1 mRNA in carcinoma in situ and normal testis correlates with expression of the miR-17-92 cluster. Cell Death Differ 2007; 14:879-882.
41. Budde H, Schmitt S, Fitzner D, Opitz L, Salinas-Riester G, Simons M. Control of oligodendroglial cell number by the miR-17-92 cluster. Development 2010; 137:2127-2132.
42. Griswold MD, Bishop PD, Kim KH, Ping R, Siiteri JE, Morales C. Function of vitamin A in normal and synchronized seminiferous tubules. Ann N Y Acad Sci 1989; 564:154-172.
43. Morales C, Griswold MD. Retinol-induced stage synchronization in seminiferous tubules of the rat. Endocrinology 1987; 121:432-434.
44. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, Small C, Griswold MD. 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 2008; 79:35-42.
45. Cory S, O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Huang DCS. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J 1998; 17:384-395.
46. Zhang M, Liu Q, Mi S, Liang X, Zhang Z, Su X, Liu J, Chen Y, Wang M, Zhang Y, Guo F, Yang R. Both miR-17-5p and miR-20a alleviate suppressive potential of myeloid-derived suppressor cells by modulating STAT3 expression. J Immunol 2011; 186:4716-4724.
47. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of micro-RNA processing by Lin28. Science 2008; 320:97-100.
48. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 2006; 38:1060-1065.
49. Chayka O, Corvetta D, Dews M, Caccamo AE, Piotrowska I, Santilli G, Gibson S, Sebire NJ, Himoudi N, Hogarty MD, Anderson J, Bettuzzi S, et al. Clusterin, a haploinsufficient tumor suppressor gene in neuroblastomas. J Natl Cancer Inst 2009; 101:663-677.