Characterization of Argonaute family members in the silkworm, Bombyx mori

Insect Science

Volumn 20, Issue 1, 2013, Pages 78-91

  Wang, Gen Hong ^a,b   Jiang, Liang ^a   Zhu, Li ^a   Cheng, Ting Cai ^a,b   Niu, Wei Huan ^b   Yan, Ya Fei ^b   Xia, Qing You ^a  

^a SOUTHWEST UNIVERSITY   (China)

^b CHONGQING UNIVERSITY   (China)

Author keywords

Argonaute; BmNPV; Bombyx mori; RNA silencing; Spermatogenesis

Indexed keywords

ARGONAUTE PROTEIN; INSECT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BMNPV; BOMBYX; BOMBYX MORI; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGY; POLYHEDROSIS VIRUS; RNA SILENCING; SEQUENCE ALIGNMENT; SPERMATOGENESIS; VIROLOGY;

ARGONAUTE; BMNPV; BOMBYX MORI; RNA SILENCING; SPERMATOGENESIS;

AMINO ACID SEQUENCE; ANIMALS; ARGONAUTE PROTEINS; BOMBYX; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NUCLEOPOLYHEDROVIRUS; PHYLOGENY; SEQUENCE ALIGNMENT;

ANIMALIA; BOMBYX MORI; BOMBYX MORI NPV; DNA VIRUSES; HEXAPODA; NUCLEOPOLYHEDROVIRUS;

EID: 84872772722     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1744-7917.2012.01555.x     Document Type: Article

References (84)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
2. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N., Morris, P., Brownstein, M.J., Kuramochi-Miyagawa, S., Nakano, T., Chien, M., Russo, J.J., Ju, J., Sheridan, R., Sander, C., Zavolan, M. and Tuschl, T. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature, 442, 203-207.
3. Aravin, A.A., Hannon, G.J. and Brennecke, J. (2007a) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science, 318, 761-764.
4. Aravin, A.A., Sachidanandam, R., Girard, A., Fejes-Toth, K. and Hannon, G.J. (2007b) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science, 316, 744-747.
5. Arenas-Mena, C., Cameron, A.R. and Davidson, E.H. (2000) Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. Development, 127, 4631-4643.
6. Baumberger, N. and Baulcombe, D.C. (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proceedings of the National Academy of Sciences of the United States of America, 102, 11928-11933.
7. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M. and Benning, C. (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. The EMBO Journal, 17, 170-180.
8. Carmell, M.A., Girard, A., van De Kant, H.J., Bourc'his, D., Bestor, T.H., De Rooij, D.G. and Hannon, G.J. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Developmental Cell, 12, 503-514.
9. Carmell, M.A., Xuan, Z., Zhang, M.Q. and Hannon, G.J. (2002) The Argonaute family: Tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes & Development, 16, 2733-2742.
10. Cerutti, L., Mian, N. and Bateman, A. (2000) Domains in gene silencing and cell differentiation proteins: The novel PAZ domain and redefinition of the Piwi domain. Trends in Biochemical Sciences, 25, 481-482.
11. Collins, R.E. and Cheng, X. (2005) Structural domains in RNAi. FEBS Letters, 579, 5841-5849.
12. Cox, D.N., Chao, A., Baker, J., Chang, L., Qiao, D. and Lin, H. (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes & Development, 12, 3715-3727.
13. Cox, D.N., Chao, A. and Lin, H. (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development, 127, 503-514.
14. De Castro, E., Sigrist, C.J., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P.S., Gasteiger, E., Bairoch, A. and Hulo, N. (2006) ScanProsite: Detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Research, 34, W362-W365.
15. Deng, W. and Lin, H. (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Developmental Cell, 2, 819-830.
16. Deshpande, G., Calhoun, G. and Schedl, P. (2005) Drosophila argonaute-2 is required early in embryogenesis for the assembly of centric/centromeric heterochromatin, nuclear division, nuclear migration, and germ-cell formation. Genes & Development, 19, 1680-1685.
17. Ding, S.W., Li, H., Lu, R., Li, F. and Li, W.X. (2004) RNA silencing: A conserved antiviral immunity of plants and animals. Virus Research, 102, 109-115.
18. Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America, 95, 14863-14868.
19. Faehnle, C.R. and Joshua-Tor, L. (2007) Argonautes confront new small RNAs. Current Opinion in Chemical Biology, 11, 569-577.
20. Florea, L., Hartzell, G., Zhang, Z., Rubin, G.M. and Miller, W. (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Research, 8, 967-974.
21. Girard, A., Sachidanandam, R., Hannon, G.J. and Carmell, M.A. (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature, 442, 199-202.
22. Grivna, S.T., Beyret, E., Wang, Z. and Lin, H. (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes & Development, 20, 1709-1714.
23. Hall, T.M. (2005) Structure and function of argonaute proteins. Structure, 13, 1403-1438.
24. Hammond, S.M. (2005) Dicing and slicing: The core machinery of the RNA interference pathway. FEBS Letters, 579, 5822-5829.
25. He, Z., Kokkinaki, M., Pant, D., Gallicano, G.I. and Dym, M. (2009) Small RNA molecules in the regulation of spermatogenesis. Reproduction, 137, 901-911.
26. Höck, J. and Meister, G. (2008) The Argonaute protein family. Genome Biology, 9: 210, 1-8.
27. Houwing, S., Kamminga, L.M., Berezikov, E., Cronembold, D., Girard, A., van Den Elst, H., Filippov, D.V., Blaser, H., Raz, E., Moens, C.B., Plasterk, R.H., Hannon, G.J., Draper, B.W. and Ketting, R.F. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell, 129, 69-82.
28. Hunter, C., Sun, H. and Poethig, R.S. (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Current Biology, 13, 1734-1739.
29. Hutvagner, G. and Simard, M.J. (2008) Argonaute proteins: Key players in RNA silencing. Nature Reviews Molecular Cell Biology, 9, 22-32.
30. The International Silkworm Genome Consortium (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochemistry and Molecular Biology, 38, 1036-1045.
31. Jinek, M. and Doudna, J.A. (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature, 457, 405-412.
32. Kalmykova, A.I., Klenov, M.S. and Gvozdev, V.A. (2005) Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline. Nucleic Acids Research, 33, 2052-2059.
33. Kapoor, M., Arora, R., Lama, T., Nijhawan, A., Khurana, J.P., Tyagi, A.K. and Kapoor, S. (2008) Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA Polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics, 9: 451, 1-17.
34. Kawaoka, S., Minami, K., Katsuma, S., Mita, K. and Shimada, T. (2008) Developmentally synchronized expression of two Bombyx mori Piwi subfamily genes, SIWI and BmAGO3 in germ-line cells. Biochemical and Biophysical Research Communications, 367, 755-760.
35. Keene, K.M., Foy, B.D., Sanchez-Vargas, I., Beaty, B.J., Blair, C.D. and Olson, K.E. (2004) RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proceedings of the National Academy of Sciences of the United States of America, 101, 17240-17245.
36. Kumar, S., Nei, M., Dudley, J. and Tamura, K. (2008) MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9, 299-306.
37. Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T.W., Isobe, T., Asada, N., Fujita, Y., Ikawa, M., Iwai, N., Okabe, M., Deng, W., Lin, H., Matsuda, Y. and Nakano, T. (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development, 131, 839-849.
38. Kuramochi-Miyagawa, S., Kimura, T., Yomogida, K., Kuroiwa, A., Tadokoro, Y., Fujita, Y., Sato, M., Matsuda, Y. and Nakano, T. (2001) Two mouse piwi-related genes: Miwi and mili. Mechanisms of Development, 108, 121-133.
39. Lau, N.C., Seto, A.G., Kim, J., Kuramochi-Miyagawa, S., Nakano, T., Bartel, D.P. and Kingston, R.E. (2006) Characterization of the piRNA complex from rat testes. Science, 313, 363-367.
40. Letunic, I., Doerks, T. and Bork, P. (2009) SMART 6: Recent updates and new developments. Nucleic Acids Research, 37, D229-D232.
41. Li, H., Li, W.X. and Ding, S.W. (2002) Induction and suppression of RNA silencing by an animal virus. Science, 296, 1319-1321.
42. Lingel, A. and Sattler, M. (2005) Novel modes of protein-RNA recognition in the RNAi pathway. Current Opinion in Structural Biology, 15, 107-115.
43. Lingel, A., Simon, B., Izaurralde, E. and Sattler, M. (2003) Structure and nucleic-acid binding of the Drosophila Argonaute2 PAZ domain. Nature, 426, 465-469.
44. Lingel, A., Simon, B., Izaurralde, E. and Sattler, M. (2004) Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain. Nature Structural & Molecular Biology, 11, 576-577.
45. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L. and Hannon, G.J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science, 305, 1437-1441.
46. Lu, R., Maduro, M., Li, F., Li, H.W., Broitman-Maduro, G., Li, W.X. and Ding, S.W. (2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature, 436, 1040-1043.
47. Lykke-Andersen, K., Gilchrist, M.J., Grabarek, J.B., Das, P., Miska, E. and Zernicka-Goetz, M. (2008) Maternal Argonaute 2 is essential for early mouse development at the maternal-zygotic transition. Molecular Biology of the Cell, 19, 4383-4392.
48. Ma, J.B., Ye, K. and Patel, D.J. (2004) Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature, 429, 318-322.
49. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G. and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Molecular Cell, 15, 185-197.
50. Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Wu, L., Li, S., Zhou, H., Long, C., Chen, S., Hannon, G.J. and Qi, Y. (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell, 133, 116-127.
51. Minokawa, T., Rast, J.P., Arenas-Mena, C., Franco, C.B. and Davidson, E.H. (2004) Expression patterns of four different regulatory genes that function during sea urchin development. Gene Expression Patterns, 4, 449-456.
52. Naqvi, A.R., Islam, M.N., Choudhury, N.R. and Haq, Q.M. (2009) The fascinating world of RNA interference. International Journal of Biological Sciences, 5, 97-117.
53. Nowotny, M., Gaidamakov, S.A., Crouch, R.J. and Yang, W. (2005) Crystal structures of RNase H bound to an RNA/DNA hybrid: Substrate specificity and metal-dependent catalysis. Cell, 121, 1005-1016.
54. Parker, J.S. and Barford, D. (2006) Argonaute: A scaffold for the function of short regulatory RNAs. Trends in Biochemical Sciences, 31, 622-630.
55. Parker, J.S., Roe, S.M. and Barford, D. (2004) Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. The EMBO Journal, 23, 4727-4737.
56. Parker, J.S., Roe, S.M. and Barford, D. (2005) Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature, 434, 663-666.
57. Peters, L. and Meister, G. (2007) Argonaute proteins: Mediators of RNA silencing. Molecular Cell, 26, 611-623.
58. Rashid, U.J., Paterok, D., Koglin, A., Gohlke, H., Piehler, J. and Chen, J.C. (2007) Structure of Aquifex aeolicus argonaute highlights conformational flexibility of the PAZ domain as a potential regulator of RNA-induced silencing complex function. The Journal of Biological Chemistry, 282, 13824-13832.
59. Rehwinkel, J., Natalin, P., Stark, A., Brennecke, J., Cohen, S.M. and Izaurralde, E. (2006) Genome-wide analysis of mRNAs regulated by Drosha and Argonaute proteins in Drosophila melanogaster. Molecular and Cellular Biology, 26, 2965-2975.
60. Rivas, F.V., Tolia, N.H., Song, J.J., Aragon, J.P., Liu, J., Hannon, G.J. and Joshua-Tor, L. (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nature Structural & Molecular Biology, 12, 340-349.
61. Ronemus, M., Vaughn, M.W. and Martienssen, R.A. (2006) MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell, 18, 1559-1574.
62. Saito, K., Nishida, K.M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H. and Siomi, M.C. (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes & Development, 20, 2214-2222.
63. Sasaki, T., Shiohama, A., Minoshima, S. and Shimizu, N. (2003) Identification of eight members of the Argonaute family in the human genome small star, filled. Genomics, 82, 323-330.
64. Song, J.J. and Joshua-Tor, L. (2006) Argonaute and RNA-getting into the groove. Current Opinion in Structural Biology, 16, 5-11.
65. Song, J.J., Smith, S.K., Hannon, G.J. and Joshua-Tor, L. (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science, 305, 1434-1437.
66. Steiner, F.A., Hoogstrate, S.W., Okihara, K.L., Thijssen, K.L., Ketting, R.F., Plasterk, R.H. and Sijen, T. (2007) Structural features of small RNA precursors determine Argonaute loading in Caenorhabditis elegans. Nature Structural & Molecular Biology, 14, 927-933.
67. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
68. Tamura, Y., Yoshida, M., Ohnishi, Y. and Hohjoh, H. (2009) Variation of gene silencing involving endogenous microRNA in mammalian cells. Molecular Biology Reports, 36, 1413-1420.
69. Tatsuke, T., Tsukioka, H., Sakashita, K., Mitsunobu, H., Lee, J., Kawaguchi, Y. and Kusakabe, T. (2007) Molecular cloning of Piwi and Aubergine homolog genes from the silkworm, Bombyx mori. Entomotech, 31, 43-46.
70. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
71. Tolia, N.H. and Joshua-Tor, L. (2007) Slicer and the argonautes. Nature Chemical Biology, 3, 36-43.
72. Tsukioka, H., Takahashi, M., Mon, H., Okano, K., Mita, K., Shimada, T., Lee, J.M., Kawaguchi, Y., Koga, K. and Kusakabe, T. (2006) Role of the silkworm argonaute2 homolog gene in double-strand break repair of extrachromosomal DNA. Nucleic Acids Research, 34, 1092-1101.
73. Unajak, S., Boonsaeng, V. and Jitrapakdee, S. (2006) Isolation and characterization of cDNA encoding Argonaute, a component of RNA silencing in shrimp (Penaeus monodon). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 145, 179-187.
74. Voinnet, O. (2005) Induction and suppression of RNA silencing: Insights from viral infections. Nature Reviews Genetics, 6, 206-220.
75. Wang, X.B., Wu, Q., Ito, T., Cillo, F., Li, W.X., Chen, X., Yu, J.L. and Ding, S.W. (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 107, 484-489.
76. Wang, X.H., Aliyari, R., Li, W.X., Li, H.W., Kim, K., Carthew, R., Atkinson, P. and Ding, S.W. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science, 312, 452-454.
77. Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N. and Imai, H. (2006) 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 & Development, 20, 1732-1743.
78. Xia, Q., Cheng, D., Duan, J., Wang, G., Cheng, T., Zha, X., Liu, C., Zhao, P., Dai, F., Zhang, Z., He, N., Zhang, L. and Xiang, Z. (2007) Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biology, 8, R162, 1-13.
79. Yamamoto, K., Narukawa, J., Kadono-Okuda, K., Nohata, J., Sasanuma, M., Suetsugu, Y., Banno, Y., Fujii, H., Goldsmith, M.R. and Mita, K. (2006) Construction of a single nucleotide polymorphism linkage map for the silkworm, Bombyx mori, based on bacterial artificial chromosome end sequences. Genetics, 173, 151-161.
80. Yamamoto, K., Nohata, J., Kadono-Okuda, K., Narukawa, J., Sasanuma, M., Sasanuma, S.I., Minami, H., Shimomura, M., Suetsugu, Y., Banno, Y., Osoegawa, K., De Jong, P.J., Goldsmith, M.R. and Mita, K. (2008) A BAC-based integrated linkage map of the silkworm Bombyx mori. Genome Biology, 9, R21.
81. Yang, L., Chen, D., Duan, R., Xia, L., Wang, J., Qurashi, A. and Jin, P. (2007) Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development, 134, 4265-4272.
82. Yigit, E., Batista, P.J., Bei, Y., Pang, K.M., Chen, C.C., Tolia, N.H., Joshua-Tor, L., Mitani, S., Simard, M.J. and Mello, C.C. (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell, 127, 747-757.
83. Yuan, Y.R., Pei, Y., Ma, J.B., Kuryavyi, V., Zhadina, M., Meister, G., Chen, H.Y., Dauter, Z., Tuschl, T. and Patel, D.J. (2005) Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Molecular Cell, 19, 405-419.
84. Zhou, R., Hotta, I., Denli, A.M., Hong, P., Perrimon, N. and Hannon, G.J. (2008) Comparative analysis of argonaute-dependent small RNA pathways in Drosophila. Molecular Cell, 32, 592-599.