Dicer is required for haploid male germ cell differentiation in mice

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Korhonen, Hanna M ^a   Meikar, Oliver ^a   Yadav, Ram Prakash ^a   Papaioannou, Marilena D ^b   Romero, Yannick ^b   da Ros, Matteo ^a   Herrera, Pedro L ^b   Toppari, Jorma ^a   Nef, Serge ^b   Kotaja, Noora ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; MICRORNA; DEAD BOX PROTEIN; DICER1 PROTEIN, MOUSE; RIBONUCLEASE III;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DICER1 GENE; EPIDIDYMIS; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GERM CELL; HAPLOIDY; MALE; MORPHOLOGY; MOUSE; NONHUMAN; SEMINIFEROUS TUBULE; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON MATURATION; ANIMAL; ANTIBODY SPECIFICITY; CENTROMERE; ENZYMOLOGY; GENETICS; MALE INFERTILITY; MEIOSIS; METABOLISM; MOUSE MUTANT; NEWBORN; NUCLEOTIDE REPEAT; PATHOLOGY; SPERMATOZOON; TESTIS; TRANSPOSON; ULTRASTRUCTURE;

MUS;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CENTROMERE; DEAD-BOX RNA HELICASES; DNA TRANSPOSABLE ELEMENTS; GENE DELETION; HAPLOIDY; INFERTILITY, MALE; MALE; MEIOSIS; MICE; MICE, KNOCKOUT; ORGAN SPECIFICITY; REPETITIVE SEQUENCES, NUCLEIC ACID; RIBONUCLEASE III; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 80052856592     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024821     Document Type: Article

References (48)

1. Kimmins S, Kotaja N, Davidson I, Sassone-Corsi P, (2004) Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 128: 5-12.
2. Kimmins S, Sassone-Corsi P, (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434: 583-589.
3. Hess RA, Renato de Franca L, (2008) Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol 636: 1-15.
4. Gaucher J, Reynoird N, Montellier E, Boussouar F, Rousseaux S, et al. (2010) From meiosis to postmeiotic events: the secrets of histone disappearance. FEBS J 277: 599-604.
5. Ghildiyal M, Zamore PD, (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10: 94-108.
6. Lau NC, (2010) Small RNAs in the animal gonad: guarding genomes and guiding development. Int J Biochem Cell Biol 42: 1334-1347.
7. Ro S, Park C, Sanders KM, McCarrey JR, Yan W, (2007) Cloning and expression profiling of testis-expressed microRNAs. Dev Biol 311: 592-602.
8. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, et al. (2010) Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev 24: 992-1009.
9. Guo H, Ingolia NT, Weissman JS, Bartel DP, (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
10. Friedman RC, Farh KK, Burge CB, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
11. Siomi MC, Sato K, Pezic D, Aravin AA, (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
12. Aravin AA, Hannon GJ, Brennecke J, (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.
13. Krol J, Loedige I, Filipowicz W, (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610.
14. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, et al. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538.
15. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, et al. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
16. Song R, Hennig GW, Wu Q, Jose C, Zheng H, et al. (2011) Male germ cells express abundant endogenous siRNAs. Proc Natl Acad Sci U S A 108: 13159-13164.
17. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, et al. (2003) Dicer is essential for mouse development. Nat Genet 35: 215-217.
18. Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, et al. (2007) Critical roles for Dicer in the female germline. Genes Dev 21: 682-693.
19. Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC, et al. (2007) Maternal microRNAs are essential for mouse zygotic development. Genes Dev 21: 644-648.
20. Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, et al. (2008) MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3: e1738.
21. Maatouk DM, Loveland KL, McManus MT, Moore K, Harfe BD, (2008) Dicer1 is required for differentiation of the mouse male germline. Biol Reprod 79: 696-703.
22. Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, et al. (2009) Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326: 250-259.
23. Papaioannou MD, Lagarrigue M, Vejnar CE, Rolland AD, Kuhne F, et al. (2011) Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice. Mol Cell Proteomics 10: M900587MCP200.
24. Lomeli H, Ramos-Mejia V, Gertsenstein M, Lobe CG, Nagy A, (2000) Targeted insertion of Cre recombinase into the TNAP gene: excision in primordial germ cells. Genesis 26: 116-117.
25. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, et al. (2006) The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci U S A 103: 2647-2652.
26. Gonzalez-Gonzalez E, Lopez-Casas PP, del Mazo J, (2008) The expression patterns of genes involved in the RNAi pathways are tissue-dependent and differ in the germ and somatic cells of mouse testis. Biochim Biophys Acta 1779: 306-311.
27. Desgraz R, Herrera PL, (2009) Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development 136: 3567-3574.
28. Harfe BD, McManus MT, Mansfield JH, Hornstein E, Tabin CJ, (2005) The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci U S A 102: 10898-10903.
29. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, et al. (2004) Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 269: 447-458.
30. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
31. Kotaja N, Kimmins S, Brancorsini S, Hentsch D, Vonesch JL, et al. (2004) Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1: 249-254.
32. Hazzouri M, Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, et al. (2000) Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur J Cell Biol 79: 950-960.
33. Martianov I, Brancorsini S, Catena R, Gansmuller A, Kotaja N, et al. (2005) Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. Proc Natl Acad Sci U S A 102: 2808-2813.
34. Kaneko H, Dridi S, Tarallo V, Gelfand BD, Fowler BJ, et al. (2011) DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471: 325-330.
35. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, et al. (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501.
36. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ, (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci U S A 102: 12135-12140.
37. Song J, Xu Y, Hu X, Choi B, Tong Q, (2010) Brain expression of Cre recombinase driven by pancreas-specific promoters. Genesis 48: 628-634.
38. Catena R, Ronfani L, Sassone-Corsi P, Davidson I, (2006) Changes in intranuclear chromatin architecture induce bipolar nuclear localization of histone variant H1T2 in male haploid spermatids. Dev Biol 296: 231-238.
39. Martianov I, Brancorsini S, Gansmuller A, Parvinen M, Davidson I, et al. (2002) Distinct functions of TBP and TLF/TRF2 during spermatogenesis: requirement of TLF for heterochromatic chromocenter formation in haploid round spermatids. Development 129: 945-955.
40. Castaneda J, Genzor P, Bortvin A, (2011) piRNAs, transposon silencing, and germline genome integrity. Mutat Res May 11 [Epub ahead of print].
41. Moazed D, (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457: 413-420.
42. Khalil AM, Driscoll DJ, (2010) Epigenetic regulation of pericentromeric heterochromatin during mammalian meiosis. Cytogenet Genome Res 129: 280-289.
43. Sinkkonen L, Hugenschmidt T, Filipowicz W, Svoboda P, (2010) Dicer is associated with ribosomal DNA chromatin in mammalian cells. PLoS One 5: e12175.
44. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, et al. (2005) The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 24: 800-812.
45. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, et al. (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237-240.
46. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, et al. (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13: 1192-1200.
47. Malkov M, Fisher Y, Don J, (1998) Developmental schedule of the postnatal rat testis determined by flow cytometry. Biol Reprod 59: 84-92.
48. Guerif F, Cadoret V, Plat M, Magistrini M, Lansac J, et al. (2002) Characterization of the fertility of Kit haplodeficient male mice. Int J Androl 25: 358-368.