PiRNA-Triggered MIWI Ubiquitination and Removal by APC/C in Late Spermatogenesis

Developmental Cell

Volumn 24, Issue 1, 2013, Pages 13-25

  Zhao, Shuang ^a,b   Gou, Lan Tao ^a,b   Zhang, Man ^c   Zu, Li Dong ^a,b   Hua, Min Min ^a,b   Hua, Ye ^d   Shi, Hui Juan ^d   Li, Yong ^e   Li, Jinsong ^c   Li, Dangsheng ^b   Wang, En Duo ^a,b   Liu, Mo Fang ^a,b  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b Chinese Academy of Sciences   (China)

^c INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^d SHANGHAI INSTITUTE OF PLANNED PARENTHOOD RESEARCH   (China)

^e University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; PIWI INTERACTING RNA; UBIQUITIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GERM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SPERMATID; SPERMATOGENESIS; SPERMATOZOON MATURATION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; ARGONAUTE PROTEINS; BLOTTING, WESTERN; GERM CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID; SPERMATOGENESIS; TESTIS; UBIQUITINATION;

ANIMALIA; MURINAE;

EID: 84872385444     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.12.006     Document Type: Article

References (48)

1. Aravin A., Gaidatzis D., Pfeffer S., Lagos-Quintana M., Landgraf P., Iovino N., Morris P., Brownstein M.J., Kuramochi-Miyagawa S., Nakano T., et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
2. Aravin A.A., van der Heijden G.W., Castañeda J., Vagin V.V., Hannon G.J., Bortvin A. Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 2009, 5:e1000764.
3. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
4. Buschhorn B.A., Petzold G., Galova M., Dube P., Kraft C., Herzog F., Stark H., Peters J.M. Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1. Nat. Struct. Mol. Biol. 2011, 18:6-13.
5. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 2007, 12:503-514.
6. Cooper K.F., Strich R. Meiotic control of the APC/C: similarities & differences from mitosis. Cell Div. 2011, 6:16.
7. Cox D.N., Chao A., Baker J., Chang L., Qiao D., Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998, 12:3715-3727.
8. da Fonseca P.C., Kong E.H., Zhang Z., Schreiber A., Williams M.A., Morris E.P., Barford D. Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 2011, 470:274-278.
9. De Fazio S., Bartonicek N., Di Giacomo M., Abreu-Goodger C., Sankar A., Funaya C., Antony C., Moreira P.N., Enright A.J., O'Carroll D. The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 2011, 480:259-263.
10. de Planell-Saguer M., Rodicio M.C., Mourelatos Z. Rapid in situ codetection of noncoding RNAs and proteins in cells and formalin-fixed paraffin-embedded tissue sections without protease treatment. Nat. Protoc. 2010, 5:1061-1073.
11. Deng W., Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2002, 2:819-830.
12. Elkayam E., Kuhn C.D., Tocilj A., Haase A.D., Greene E.M., Hannon G.J., Joshua-Tor L. The structure of human argonaute-2 in complex with miR-20a. Cell 2012, 150:100-110.
13. Gerton G.L., Millette C.F. Stage-specific synthesis and fucosylation of plasma membrane proteins by mouse pachytene spermatocytes and round spermatids in culture. Biol. Reprod. 1986, 35:1025-1035.
14. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
15. Glotzer M., Murray A.W., Kirschner M.W. Cyclin is degraded by the ubiquitin pathway. Nature 1991, 349:132-138.
16. Grivna S.T., Beyret E., Wang Z., Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 2006, 20:1709-1714.
17. Gunawardane L.S., Saito K., Nishida K.M., Miyoshi K., Kawamura Y., Nagami T., Siomi H., Siomi M.C. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 2007, 315:1587-1590.
18. Harris A.N., Macdonald P.M. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 2001, 128:2823-2832.
19. Jin F., Hamada M., Malureanu L., Jeganathan K.B., Zhou W., Morbeck D.E., van Deursen J.M. Cdc20 is critical for meiosis I and fertility of female mice. PLoS Genet. 2010, 6:6.
20. King R.W., Glotzer M., Kirschner M.W. Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 1996, 7:1343-1357.
21. Kraft C., Gmachl M., Peters J.M. Methods to measure ubiquitin-dependent proteolysis mediated by the anaphase-promoting complex. Methods 2006, 38:39-51.
22. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004, 131:839-849.
23. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Takamatsu K., Chuma S., Kojima-Kita K., Shiromoto Y., Asada N., Toyoda A., Fujiyama A., et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010, 24:887-892.
24. La Salle S., Sun F., Handel M.A. Isolation and short-term culture of mouse spermatocytes for analysis of meiosis. Methods Mol. Biol. 2009, 558:279-297.
25. Lau N.C., Seto A.G., Kim J., Kuramochi-Miyagawa S., Nakano T., Bartel D.P., Kingston R.E. Characterization of the piRNA complex from rat testes. Science 2006, 313:363-367.
26. Lindon C., Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 2004, 164:233-241.
27. Liu M.L., Cheng Y.M., Jia M.C. LM23 is essential for spermatogenesis in Rattus norvegicus. Front Biosci (Elite Ed) 2010, 2:187-194.
28. Ma J.B., Ye K., Patel D.J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 2004, 429:318-322.
29. Mailand N., Diffley J.F. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 2005, 122:915-926.
30. Margottin-Goguet F., Hsu J.Y., Loktev A., Hsieh H.M., Reimann J.D., Jackson P.K. Prophase destruction of Emi1 by the SCF(betaTrCP/Slimb) ubiquitin ligase activates the anaphase promoting complex to allow progression beyond prometaphase. Dev. Cell 2003, 4:813-826.
31. Meikar O., Da Ros M., Korhonen H., Kotaja N. Chromatoid body and small RNAs in male germ cells. Reproduction 2011, 142:195-209.
32. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
33. Qiao X., Zhang L., Gamper A.M., Fujita T., Wan Y. APC/C-Cdh1: from cell cycle to cellular differentiation and genomic integrity. Cell Cycle 2010, 9:3904-3912.
34. Rape M., Reddy S.K., Kirschner M.W. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell 2006, 124:89-103.
35. Reuter M., Chuma S., Tanaka T., Franz T., Stark A., Pillai R.S. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat. Struct. Mol. Biol. 2009, 16:639-646.
36. Reuter M., Berninger P., Chuma S., Shah H., Hosokawa M., Funaya C., Antony C., Sachidanandam R., Pillai R.S. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 2011, 480:264-267.
37. Rouget C., Papin C., Boureux A., Meunier A.C., Franco B., Robine N., Lai E.C., Pelisson A., Simonelig M. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010, 467:1128-1132.
38. Royer C.A. Probing protein folding and conformational transitions with fluorescence. Chem. Rev. 2006, 106:1769-1784.
39. Saito K., Inagaki S., Mituyama T., Kawamura Y., Ono Y., Sakota E., Kotani H., Asai K., Siomi H., Siomi M.C. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461:1296-1299.
40. Saito K., Ishizu H., Komai M., Kotani H., Kawamura Y., Nishida K.M., Siomi H., Siomi M.C. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 2010, 24:2493-2498.
41. Shoji M., Tanaka T., Hosokawa M., Reuter M., Stark A., Kato Y., Kondoh G., Okawa K., Chujo T., Suzuki T., et al. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev. Cell 2009, 17:775-787.
42. Siomi M.C., Sato K., Pezic D., Aravin A.A. PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 2011, 12:246-258.
43. Thomson T., Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 2009, 25:355-376.
44. Wang J., Saxe J.P., Tanaka T., Chuma S., Lin H. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr. Biol. 2009, 19:640-644.
45. Watanabe T., Chuma S., Yamamoto Y., Kuramochi-Miyagawa S., Totoki Y., Toyoda A., Hoki Y., Fujiyama A., Shibata T., Sado T., et al. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 2011, 20:364-375.
46. Williamson A., Jin L., Rape M. Preparation of synchronized human cell extracts to study ubiquitination and degradation. Methods Mol. Biol. 2009, 545:301-312.
47. Yin H., Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 2007, 450:304-308.
48. Zhou Y., Zheng M., Shi Q., Zhang L., Zhen W., Chen W., Zhang Y. An epididymis-specific secretory protein HongrES1 critically regulates sperm capacitation and male fertility. PLoS ONE 2008, 3:e4106.