Mice deficient for a small cluster of Piwi-lnteracting RNAs Implicate Piwi-interacting RNAs in transposon control

Biology of Reproduction

Volumn 79, Issue 1, 2008, Pages 51-57

  Xu, Mingang ^a   You, Yun ^b   Hunsicker, Patricia ^b   Hori, Tamaki ^a   Small, Chris ^c   Griswold, Michael D ^c   Hecht, Norman B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Gametogenesis; Gene regulation; Male reproductive tract; piRNA; Spermatogenesis; Testis; Transposon

Indexed keywords

PIWI PROTEIN; PROTEIN; PROTEIN PIWIL1; PROTEIN PIWIL2; UNTRANSLATED RNA; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CHROMOSOME 2; GENE; GENE CONTROL; GENE EXPRESSION; GENE INACTIVATION; GENE MUTATION; GENE SILENCING; MALE FERTILITY; MOUSE; NCT1 GENE; NCT2 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; REPRODUCTION; SPERMATOGENESIS; TRANSPOSON; ANIMAL; C57BL MOUSE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LONG INTERSPERSED REPEAT; MALE; METABOLISM; MOUSE MUTANT; MULTIGENE FAMILY; MUTATION; PHYSIOLOGY; TESTIS;

MAMMALIA; MUS;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIGENE FAMILY; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCTION; RNA, SMALL INTERFERING; TESTIS;

EID: 52949123906     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.108.068072     Document Type: Article

References (43)

1. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006; 442:203-207.
2. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006; 442:199-202.
3. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE. Characterization of the piRNA complex from rat testes. Science 2006; 313:363-367.
4. Grivna ST, Pyhtila B, Lin H. MIWI associates with translational machinery and PIWI-interacting RNAs piRNAs in regulating spermato-genesis. Proc Natl Acad Sci U S A 2006; 103:13415-13420.
5. Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T. The small RNA profile during Drosophila melanogaster development. Dev Cell 2003; 5:337-350.
6. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006; 313:320-324.
7. Houwing S, Kamminga LM, Berezikov E. Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 2007; 129:69-82.
8. Yin H, Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 2007; 450:304-308.
9. Klattenhoff C, Theurkauf W. Biogenesis and germline functions of piRNAs. Development 2008; 135:3-9.
10. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007; 316:744-747.
11. Lin HF. piRNAs in the germ line. Science 2007; 316:397.
12. Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2002; 2:819-830.
13. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004; 31:839-849.
14. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, Hannon GJ. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 2007; 12:503-514.
15. Hartig JV, Tomari Y, Forstemann K. piRNAs-the ancient hunters of genome invaders. Genes Dev 2007; 21:1707-1713.
16. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007; 128:1089-1103.
17. O'Donnell KA, Boeke JD. Mighty Piwis defend the germline against genome intruders. Cell 2007; 129:37-44.
18. Cho YS, Iguchi N, Yang J, Handel MA, Hecht NB. Meiotic messenger RNA and noncoding RNA targets of the RNA-binding protein Translin TSN in mouse testis. Biol Reprod 2005; 73:840-847.
19. Iguchi N, Xu M, Hori T, Hecht NB. Non-coding RNAs of the mammalian testis: the meiotic transcripts Nct1 and 2 encode piRNAs. Ann N Y Acad Sci 2008; 1120:84-94.
20. Chick WS, Mentzer SE, Carpenter DA, Rinchik EM, Johnson D, You Y. X-ray-induced deletion complexes in embryonic stem cells on mouse Chromosome 15. Mamm Genome 2005; 16:661-671.
21. Liu P, Jenkins NA, Copeland NG. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 2003; 13:476-484.
22. Nagy A, Gertsenstein M, Vintersten K, Behringer RR. Manipulating the Mouse Embryo, A Laboratory Manual, 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2003
23. Valenzuela DM, Murphy AJ, Frendewey D, Gale NW, Economides AN, Auerbach W, Poueymirou WT, Adams NC, Rojas J, Yasenchak J, Chernomorsky R, Boucher M, et al. High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol 2003; 21:652-659.
24. Pall GS, Codony-Servat C, Byrne J, Ritchie L, Hamilton A. Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res 2007; 35:e60.
25. Eacker SM, Shima JE, Connolly CM, Sharma M, Holdcraft RW, Griswold MD, Braun RE. Transcriptional profiling of androgen receptor AR mutants suggests instructive and permissive roles of AR signaling in germ cell development. Mol Endocrinol 2007; 21:895-907.
26. Cho YS, Chennatliukuzhi VM, Handel MA, Eppig J, Hecht NB. The relative levels of translin-associated factor X TRAX and testis brain RNA-binding protein determine their nucleocytoplasmic distribution in male germ cells. J Biol Chem 2004; 279:31514-31523.
27. Sai Lakshmi S, Agrawal S. piRNABank: a web resource on classified and clustered Piwi-interacting RNAs. Nucleic Acids Res 2008; 36:D173-D177.
28. Pham CT, Maclvor DM, Hug BA, Heusel JW, Ley TJ. Long-range disruption of gene expression by a selectable marker cassette. Proc Natl Acad Sci U S A 1996; 93:13090-13095.
29. Seidl KJ, Manis JP, Bottaro A, Zhang J, Davidson L, Kisselgof A, Oettgen H, Alt FW. Position-dependent inhibition of class-switch recombination by PGK-neor cassettes inserted into the immunoglobulin heavy chain constant region locus. Proc Natl Acad Sci U S A 1999; 96:3000-3005.
30. Hellbusch CC, Sperandio M, Frommhold D, Yakubenia S, Wild MK, Popovici D, Vestweber D, Grone HJ, von Figura K, Lubke T, Korner C. Golgi GDP-fucose transporter-deficient mice mimic congenital disorder of glycosylation IIc/leukocyte adhesion deficiency II. J Biol Chem 2007; 282:10762-10772.
31. Babushok DV Jr., Kazazian HH. Progress in understanding the biology of the human mutagen LTNE-1. Hum Mutat 2007; 28:527-539.
32. Benihoud K, Bonardelle D, Soual-Hoebeke E, Durand-Gasselin I, Emilie D, Kiger N, Bobe P. Unusual expression of LINE-1 transposable element in the MRL autoimmune lymphoproliferative syndrome-prone strain. Oncogene 2002; 21:5593-5600.
33. Branciforte D, Martin SL. Developmental and cell type specificity of LTNE-1 expression in mouse testis: implications for transposition. Mol Cell Biol 1994; 14:2584-2592.
34. Ergün S, Buschmann C, Heukeshoven J, Dammann K, Schnieders F, Lauke H, Chalajour F, Kilic N, Strätling WH, Schumann GG. Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J Biol Chem 2004; 279:27753-27763.
35. Grivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 2006; 20:1709-1714.
36. Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H, Dus M, Zhou P. Elgin SC, Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 2007; 21:2300-2311.
37. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 2007; 315: 1587-1590.
38. Ostertag EM, DeBerardinis RJ, Goodier JL, Zhang Y, Yang N, Getton GL, Kazazian HH Jr. A mouse model of human LI retrotransposition. Nat Genet 2002; 32:655-660.
39. Hernández-Hernández A, Rincón-Arano H, Recillas-Targa F, Ortiz R, Valdes-Quezada C, Echeverría OM, Benavente R, Vázquez-Nin GH. Differential distribution and association of repeat DNA sequences in the lateral element of the synaptonemal complex in rat spermatocytes. Chromosoma 2008; 117:77-87.
40. Liang G, Chan MF, Tomigahara Y, Tsai YC, Gonzales FA, Li E, Laird PW, Jones PA. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol Cell Biol 2002; 22: 480-491.
41. Gaudet F, Rideout WM 3rd, Meissner A, Dausman J, Leonhardt H, Jaenisch R. Dnmt1 expression in pre- and postirnpiantation embryogenesis and the maintenance of IAP silencing. Mol Cell Biol 2004; 24:1640-1648.
42. Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004; 431:96-99.
43. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9:102-114.