Identification of MIWI-associated poly(A) RNAs by immunoprecipitation with an anti-MIWI monoclonal antibody

BioScience Trends

Volumn 6, Issue 5, 2012, Pages 248-261

  Nishibu, Takahiro ^a,b   Yukinobu Hayashida, Yukinobu ^a   Tani, Saori ^b   Kurono, Sadamu ^a,c   Kojima Kita, Kanako ^c   Ukekawa, Ryo ^a   Kurokawa, Tsutomu ^a   Kuramochi Miyagawa, Satomi ^c   Nakano, Toru ^c   Inoue, Kunio ^b   Honda, Susumu ^a  

^a FUJIFILM Wako Pure Chemical Corporation   (Japan)

^b KOBE UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

MIWI; Pachytene; piRNA; PIWI; Spermatogenesis

Indexed keywords

MONOCLONAL ANTIBODY; POLYADENYLIC ACID; RNA; SMALL INTERFERING RNA;

ANIMAL; ARTICLE; GENETICS; IMMUNOPRECIPITATION; MALE; METABOLISM; METHODOLOGY; MOUSE; PHYSIOLOGY; SPERMATOGENESIS; TESTIS;

ANIMALS; ANTIBODIES, MONOCLONAL; IMMUNOPRECIPITATION; MALE; MICE; POLY A; RNA; RNA, SMALL INTERFERING; SPERMATOGENESIS; TESTIS;

EID: 84872570920     PISSN: 18817815     EISSN: 18817823     Source Type: Journal    
DOI: 10.5582/bst.2012.v6.5.248     Document Type: Article

References (50)

1. Sasaki T, Shiohama A, Minoshima S, Shimizu N. Identification of eight members of the Argonaute family in the human genome small star, filled. Genomics. 2003; 82:323-330.
2. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ. Argonaute2 is the catalytic engine of mammalian RNAi. Science. 2004; 305:1437-1441.
3. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell. 2004; 15:185-197.
4. Pillai RS, Artus CG, Filipowicz W. Tethering of human Ago proteins to mRNA mimics the miRNAmediated repression of protein synthesis. RNA. 2004; 10:1518-1525.
5. Aravin A, Gaidatzis D, Pfeffer S, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006; 442:203-207.
6. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006; 442:199-202.
7. Grivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 2006; 20:1709-1714.
8. 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.
9. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H. Identification and characterization of two novel classes of small RNAs in the mouse germline: Retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 2006; 20:1732-1743.
10. Deng W, Lin H. Miwi, a murine homolog o f piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell. 2002; 2:819-830.
11. 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, Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 2004; 131:839-849.
12. 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.
13. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008; 31:785-799.
14. Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi- Miyagawa S, Nakano T, Lin H. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem. 2009; 284:6507-6519.
15. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008; 22:908-917.
16. 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.
17. Kojima K, Kuramochi-Miyagawa S, Chuma S, Tanaka T, Nakatsuji N, Kimura T, Nakano T. Associations between PIWI proteins and TDRD1/MTR-1 are critical for integrated subcellular localization in murine male germ cells. Genes Cells. 2009; 14:1155-1165.
18. Reuter M, Chuma S, Tanaka T, Franz T, Stark A, Pillai RS. Loss of the Mili-interacting Tudor domaincontaining protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat Struct Mol Biol. 2009; 16:639-646.
19. Shoji M, Tanaka T, Hosokawa M, et al. The TDRD9- MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell. 2009; 17:775-787.
20. Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, Chuma S, Girard A, Sachidanandam R, Hannon GJ, Aravin AA. Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev. 2009; 23:1749-1762.
21. Wang J, Saxe JP, Tanaka T, Chuma S, Lin H. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr Biol. 2009; 19:640-644.
22. Frost RJ, Hamra FK, Richardson JA, Qi X, Bassel-Duby R, Olson EN. MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwiinteracting RNAs. Proc Natl Acad Sci U S A. 2010; 107:11847-11852.
23. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010; 24:887-892.
24. Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, McLaughlin KJ, Stark A, Sachidanandam R, Pillai RS, Wang PJ. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwiinteracting RNA (piRNA) pathway. Proc Natl Acad Sci U S A. 2010; 107:11841-11846.
25. Chi YH, Cheng LI, Myers T, Ward JM, Williams E, Su Q, Faucette L, Wang JY,Jeang KT. Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA. Development. 2009; 136:965-973.
26. Ma L, Buchold GM, Greenbaum MP, Roy A, Burns KH, Zhu H, Han DY, Harris RA, Coarfa C, Gunaratne PH, Yan W, Matzuk MM. GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet. 2009; 5:e1000635.
27. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, Sachidanandam R, Pillai RS. Miwi catalysis is required for piRNA amplificationindependent LINE1 transposon silencing. Nature. 2011; 480:264-267.
28. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W,Sassone-Corsi P. 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. 2006; 103:2647-2652.
29. Grivna ST, Pyhtila B, Lin H. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A. 2006; 103:13415-13420.
30. 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.
31. Hayashida Y, Nishibu T, Inoue K,Kurokawa T. A useful approach to total analysis of RISC-associated RNA. BMC Res Notes. 2009; 2:169.
32. Iwasaki S, Kobayashi M, Yoda M, Sakaguchi Y, Katsuma S, Suzuki T, Tomari Y. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell. 2010; 39:292-299.
33. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. Discrete small RNAgenerating loci as master regulators of transposon activity in Drosophila. Cell. 2007; 128:1089-1103.
34. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. A slicermediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science. 2007; 315:1587-1590.
35. Bellve AR. Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol. 1993; 225:84-113.
36. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ. Cyclin A1 is required for meiosis in the male mouse. Nat Genet. 1998; 20:377-380.
37. Kawamata M, Nishimori K. Mice deficient in Dmrt7 show infertility with spermatogenic arrest at pachytene stage. FEBS Lett. 2006; 580:6442-6446.
38. Li B, Nair M, Mackay DR, Bilanchone V, Hu M, Fallahi M, Song H, Dai Q, Cohen PE, Dai X. Ovol1 regulates meiotic pachytene progression during spermatogenesis by repressing Id2 expression. Development. 2005; 132:1463-1473.
39. Malcov M, Cesarkas K, Stelzer G, Shalom S, Dicken Y, Naor Y, Goldstein RS, Sagee S, Kassir Y, Don J. Aym1, a mouse meiotic gene identified by virtue of its ability to activate early meiotic genes in the yeast Saccharomyces cerevisiae. Dev Biol. 2004; 276:111-123.
40. Beyret E, Lin H. Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. Dev Biol. 2011; 355:215-226.
41. 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.
42. 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, Draper BW, Ketting RF. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell. 2007; 129:69-82.
43. Iguchi N, Xu M, Hori T, Hecht NB. Noncoding RNAs of the mammalian testis: The meiotic transcripts Nct1 and Nct2 encode piRNAs. Ann N Y Acad Sci. 2007; 1120:84-94.
44. Ro S, Park C, Song R, Nguyen D, Jin J, Sanders KM, McCarrey JR, Yan W. Cloning and expression profiling of testis-expressed piRNA-like RNAs. RNA. 2007; 13:1693-1702.
45. Xu M, You Y, Hunsicker P, Hori T, Small C, Griswold MD, Hecht NB. Mice deficient for a small cluster of Piwi-interacting RNAs implicate Piwi-interacting RNAs in transposon control. Biol Reprod. 2008; 79:51-57.
46. Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, Blower MD, Lai EC. A broadly conserved pathway generates 3'UTR-directed primary piRNAs. Curr Biol. 2009; 19:2066-2076.
47. Nakada K, Sato A, Yoshida K, Morita T, Tanaka H, Inoue S, Yonekawa H,Hayashi J. Mitochondria-related male infertility. Proc Natl Acad Sci U S A. 2006; 103:15148-15153.
48. Treinin M,Simchen G. Mitochondrial activity is required for the expression of IME1, a regulator of meiosis in yeast. Curr Genet. 1993; 23:223-227.
49. Huang H, Gao Q, Peng X, Choi SY, Sarma K, Ren H, Morris AJ, Frohman MA. piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev Cell. 2011; 20:376-387.
50. Watanabe T, Chuma S, Yamamoto Y, Kuramochi- Miyagawa S, Totoki Y, Toyoda A, Hoki Y, Fujiyama A, Shibata T, Sado T, Noce T, Nakano T, Nakatsuji N, Lin H, Sasaki H. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev Cell. 2011; 20:364-375.