A kinesin Klp10A mediates cell cycle-dependent shuttling of Piwi between nucleus and nuage
Autoři:
Zsolt G. Venkei aff001; Charlotte Choi aff002; Suhua Feng aff003; Cuie Chen aff001; Steven E. Jacobsen aff003; John K. Kim aff002; Yukiko M. Yamashita aff001; Charlotte P. Choi aff002
Působiště autorů:
Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, United States of America
aff001; Department of Biology, Johns Hopkins University, Baltimore, Maryland, United States of America
aff002; Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, California, United States of America
aff003; Eli and Edyth Broad Center of Regenerative Medicine and Stem Cell Research, University of California, Los Angeles, California, United States of America
aff004; Howard Hughes Medical Institute, University of California, Los Angeles, California, United States of America
aff005; Department of Cell and Developmental Biology, University of Michigan, Ann Arbor, Michigan, United States of America
aff006; Howard Hughes Medical Institute, University of Michigan Ann Arbor, Michigan, United States of America
aff007
Vyšlo v časopise:
A kinesin Klp10A mediates cell cycle-dependent shuttling of Piwi between nucleus and nuage. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008648
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008648
Souhrn
The piRNA pathway protects germline genomes from selfish genetic elements (e.g. transposons) through their transcript cleavage in the cytoplasm and/or their transcriptional silencing in the nucleus. Here, we describe a mechanism by which the nuclear and cytoplasmic arms of the piRNA pathway are linked. We find that during mitosis of Drosophila spermatogonia, nuclear Piwi interacts with nuage, the compartment that mediates the cytoplasmic arm of the piRNA pathway. At the end of mitosis, Piwi leaves nuage to return to the nucleus. Dissociation of Piwi from nuage occurs at the depolymerizing microtubules of the central spindle, mediated by a microtubule-depolymerizing kinesin, Klp10A. Depletion of klp10A delays the return of Piwi to the nucleus and affects piRNA production, suggesting the role of nuclear-cytoplasmic communication in piRNA biogenesis. We propose that cell cycle-dependent communication between the nuclear and cytoplasmic arms of the piRNA pathway may play a previously unappreciated role in piRNA regulation.
Klíčová slova:
Cell cycle and cell division – Drosophila melanogaster – Germ cells – Mitosis – MTS assay – RNA sequencing – Testes – Transposable elements
Zdroje
1. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–103. Epub 2007/03/10. doi: 10.1016/j.cell.2007.01.043 17346786.
2. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006;442(7099):199–202. Epub 2006/06/06. doi: 10.1038/nature04917 16751776.
3. Batista PJ, Ruby JG, Claycomb JM, Chiang R, Fahlgren N, Kasschau KD, et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell. 2008;31(1):67–78. Epub 2008/06/24. S1097-2765(08)00391-2 [pii] doi: 10.1016/j.molcel.2008.06.002 18571452; PubMed Central PMCID: PMC2570341.
4. Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, et al. The small RNA profile during Drosophila melanogaster development. Dev Cell. 2003;5(2):337–50. Epub 2003/08/16. doi: 10.1016/s1534-5807(03)00228-4 12919683.
5. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, et al. Large-Scale Sequencing Reveals 21U-RNAs and Additional MicroRNAs and Endogenous siRNAs in C. elegans. Cell. 2006;127(6):1193–207. doi: 10.1016/j.cell.2006.10.040 17174894
6. Wang W, Han BW, Tipping C, Ge DT, Zhang Z, Weng Z, et al. Slicing and Binding by Ago3 or Aub Trigger Piwi-Bound piRNA Production by Distinct Mechanisms. Mol Cell. 2015;59(5):819–30. doi: 10.1016/j.molcel.2015.08.007 26340424; PubMed Central PMCID: PMC4560842.
7. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, et al. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science. 2007;315(5818):1587–90. doi: 10.1126/science.1140494 17322028.
8. Nishida KM, Saito K, Mori T, Kawamura Y, Nagami-Okada T, Inagaki S, et al. Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA. 2007;13(11):1911–22. doi: 10.1261/rna.744307 17872506; PubMed Central PMCID: PMC2040086.
9. 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(5785):320–4. doi: 10.1126/science.1129333 16809489.
10. Li C, Vagin VV, Lee S, Xu J, Ma S, Xi H, et al. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell. 2009;137(3):509–21. Epub 2009/04/28. doi: 10.1016/j.cell.2009.04.027 19395009; PubMed Central PMCID: PMC2768572.
11. Wang W, Yoshikawa M, Han Bo W, Izumi N, Tomari Y, Weng Z, et al. The Initial Uridine of Primary piRNAs Does Not Create the Tenth Adenine that Is the Hallmark of Secondary piRNAs. Molecular Cell. 2014;56(5):708–16. doi: 10.1016/j.molcel.2014.10.016 25453759
12. Senti KA, Jurczak D, Sachidanandam R, Brennecke J. piRNA-guided slicing of transposon transcripts enforces their transcriptional silencing via specifying the nuclear piRNA repertoire. Genes Dev. 2015;29(16):1747–62. doi: 10.1101/gad.267252.115 26302790; PubMed Central PMCID: PMC4561483.
13. Sienski G, Batki J, Senti KA, Donertas D, Tirian L, Meixner K, et al. Silencio/CG9754 connects the Piwi-piRNA complex to the cellular heterochromatin machinery. Genes Dev. 2015;29(21):2258–71. doi: 10.1101/gad.271908.115 26494711; PubMed Central PMCID: PMC4647559.
14. Klenov MS, Lavrov SA, Korbut AP, Stolyarenko AD, Yakushev EY, Reuter M, et al. Impact of nuclear Piwi elimination on chromatin state in Drosophila melanogaster ovaries. Nucleic Acids Res. 2014;42(10):6208–18. Epub 2014/05/02. doi: 10.1093/nar/gku268 24782529; PubMed Central PMCID: PMC4041442.
15. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 2013;27(4):390–9. doi: 10.1101/gad.209841.112 23392610; PubMed Central PMCID: PMC3589556.
16. Zhang F, Wang J, Xu J, Zhang Z, Koppetsch BS, Schultz N, et al. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell. 2012;151(4):871–84. Epub 2012/11/13. doi: 10.1016/j.cell.2012.09.040 23141543; PubMed Central PMCID: PMC3499805.
17. Lim AK, Kai T. Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2007;104(16):6714–9. doi: 10.1073/pnas.0701920104 17428915.
18. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, et al. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell. 2009;137(3):522–35. Epub 2009/04/28. doi: 10.1016/j.cell.2009.03.040 19395010; PubMed Central PMCID: PMC2882632.
19. Ryazansky SS, Kotov AA, Kibanov MV, Akulenko NV, Korbut AP, Lavrov SA, et al. RNA helicase Spn-E is required to maintain Aub and AGO3 protein levels for piRNA silencing in the germline of Drosophila. Eur J Cell Biol. 2016;95(9):311–22. doi: 10.1016/j.ejcb.2016.06.001 27320195.
20. Snee MJ, Macdonald PM. Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components. J Cell Sci. 2004;117(Pt 10):2109–20. Epub 2004/04/20. doi: 10.1242/jcs.01059 15090597
21. Andress A, Bei Y, Fonslow BR, Giri R, Wu Y, Yates JR 3rd, et al. Spindle-E cycling between nuage and cytoplasm is controlled by Qin and PIWI proteins. J Cell Biol. 2016;213(2):201–11. Epub 2016/04/20. doi: 10.1083/jcb.201411076 27091448; PubMed Central PMCID: PMC5084268.
22. Gonzalez J, Qi H, Liu N, Lin H. Piwi Is a Key Regulator of Both Somatic and Germline Stem Cells in the Drosophila Testis. Cell Rep. 2015;12(1):150–61. doi: 10.1016/j.celrep.2015.06.004 26119740; PubMed Central PMCID: PMC4497877.
23. Zhang Z, Xu J, Koppetsch BS, Wang J, Tipping C, Ma S, et al. Heterotypic piRNA Ping-Pong requires qin, a protein with both E3 ligase and Tudor domains. Mol Cell. 2011;44(4):572–84. doi: 10.1016/j.molcel.2011.10.011 22099305; PubMed Central PMCID: PMC3236501.
24. Webster A, Li S, Hur JK, Wachsmuth M, Bois JS, Perkins EM, et al. Aub and Ago3 Are Recruited to Nuage through Two Mechanisms to Form a Ping-Pong Complex Assembled by Krimper. Mol Cell. 2015;59(4):564–75. doi: 10.1016/j.molcel.2015.07.017 26295961; PubMed Central PMCID: PMC4545750.
25. Sato K, Iwasaki YW, Shibuya A, Carninci P, Tsuchizawa Y, Ishizu H, et al. Krimper Enforces an Antisense Bias on piRNA Pools by Binding AGO3 in the Drosophila Germline. Mol Cell. 2015;59(4):553–63. Epub 2015/07/28. doi: 10.1016/j.molcel.2015.06.024 26212455.
26. Rogers GC, Rogers SL, Schwimmer TA, Ems-McClung SC, Walczak CE, Vale RD, et al. Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature. 2004;427(6972):364–70. Epub 2003/12/19. doi: 10.1038/nature02256 14681690.
27. Yamashita YM, Jones DL, Fuller MT. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science. 2003;301(5639):1547–50. Epub 2003/09/13. doi: 10.1126/science.1087795 12970569.
28. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science. 2007;315(5811):518–21. Epub 2007/01/27. doi: 10.1126/science.1134910 17255513; PubMed Central PMCID: PMC2563045.
29. Cheng J, Turkel N, Hemati N, Fuller MT, Hunt AJ, Yamashita YM. Centrosome misorientation reduces stem cell division during ageing. Nature. 2008;456(7222):599–604. Epub 2008/10/17. doi: 10.1038/nature07386 18923395; PubMed Central PMCID: PMC2712891.
30. Inaba M, Venkei ZG, Yamashita YM. The polarity protein Baz forms a platform for the centrosome orientation during asymmetric stem cell division in the Drosophila male germline. Elife. 2015;4. Epub 2015/03/21. doi: 10.7554/eLife.04960 25793442; PubMed Central PMCID: PMC4391501.
31. Venkei ZG, Yamashita YM. The centrosome orientation checkpoint is germline stem cell specific and operates prior to the spindle assembly checkpoint in Drosophila testis. Development. 2015;142(1):62–9. Epub 2014/12/07. doi: 10.1242/dev.117044 25480919.
32. Salzmann V, Chen C, Chiang CY, Tiyaboonchai A, Mayer M, Yamashita YM. Centrosome-dependent asymmetric inheritance of the midbody ring in Drosophila germline stem cell division. Mol Biol Cell. 2014;25(2):267–75. Epub 2013/11/15. doi: 10.1091/mbc.E13-09-0541 24227883; PubMed Central PMCID: PMC3890347.
33. Conduit PT, Raff JW. Cnn dynamics drive centrosome size asymmetry to ensure daughter centriole retention in drosophila neuroblasts. Curr Biol. 2010;20(24):2187–92. Epub 2010/12/15. S0960-9822(10)01521-6 [pii] doi: 10.1016/j.cub.2010.11.055 21145745.
34. Januschke J, Llamazares S, Reina J, Gonzalez C. Drosophila neuroblasts retain the daughter centrosome. Nat Commun. 2011;2:243. Epub 2011/03/17. ncomms1245 [pii] doi: 10.1038/ncomms1245 21407209.
35. Januschke J, Reina J, Llamazares S, Bertran T, Rossi F, Roig J, et al. Centrobin controls mother-daughter centriole asymmetry in Drosophila neuroblasts. Nature cell biology. 2013;15(3):241–8. Epub 2013/01/29. doi: 10.1038/ncb2671 23354166.
36. Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature. 2009;461(7266):947–55. Epub 2009/10/16. nature08435 [pii] doi: 10.1038/nature08435 19829375.
37. Chen C, Inaba M, Venkei ZG, Yamashita YM. Klp10A, a stem cell centrosome-enriched kinesin, balances asymmetries in Drosophila male germline stem cell division. Elife. 2016;5. Epub 2016/11/26. doi: 10.7554/eLife.20977 27885983; PubMed Central PMCID: PMC5235350.
38. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science. 2001;294(5551):2542–5. doi: 10.1126/science.1066707 11752574.
39. Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science. 2001;294(5551):2546–9. doi: 10.1126/science.1066700 11752575.
40. Schulz C, Kiger AA, Tazuke SI, Yamashita YM, Pantalena-Filho LC, Jones DL, et al. A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage. Genetics. 2004;167(2):707–23. Epub 2004/07/09. doi: 10.1534/genetics.103.023184 15238523; PubMed Central PMCID: PMC1470893.
41. Kawase E, Wong MD, Ding BC, Xie T. Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development. 2004;131(6):1365–75. doi: 10.1242/dev.01025 14973292.
42. Shivdasani AA, Ingham PW. Regulation of stem cell maintenance and transit amplifying cell proliferation by tgf-Beta signaling in Drosophila spermatogenesis. Curr Biol. 2003;13(23):2065–72. doi: 10.1016/j.cub.2003.10.063 14653996.
43. Toth KF, Pezic D, Stuwe E, Webster A. The piRNA Pathway Guards the Germline Genome Against Transposable Elements. Adv Exp Med Biol. 2016;886:51–77. doi: 10.1007/978-94-017-7417-8_4 26659487; PubMed Central PMCID: PMC4991928.
44. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006;442(7099):203–7. doi: 10.1038/nature04916 16751777
45. Kibanov MV, Egorova KS, Ryazansky SS, Sokolova OA, Kotov AA, Olenkina OM, et al. A novel organelle, the piNG-body, in the nuage of Drosophila male germ cells is associated with piRNA-mediated gene silencing. Mol Biol Cell. 2011;22(18):3410–9. doi: 10.1091/mbc.E11-02-0168 21775629; PubMed Central PMCID: PMC3172265.
46. Nagao A, Mituyama T, Huang H, Chen D, Siomi MC, Siomi H. Biogenesis pathways of piRNAs loaded onto AGO3 in the Drosophila testis. RNA. 2010. Epub 2010/10/29. rna.2270710 [pii] doi: 10.1261/rna.2270710 20980675
47. Pek JW, Kai T. A role for vasa in regulating mitotic chromosome condensation in Drosophila. Current biology: CB. 2011;21(1):39–44. Epub 2010/12/28. doi: 10.1016/j.cub.2010.11.051 21185189.
48. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31(6):785–99. Epub 2008/10/17. S1097-2765(08)00619-9 [pii] doi: 10.1016/j.molcel.2008.09.003 18922463; PubMed Central PMCID: PMC2730041.
49. Xiol J, Spinelli P, Laussmann MA, Homolka D, Yang Z, Cora E, et al. RNA Clamping by Vasa Assembles a piRNA Amplifier Complex on Transposon Transcripts. Cell. 2014;157(7):1698–711. doi: 10.1016/j.cell.2014.05.018 24910301.
50. Nishida KM, Iwasaki YW, Murota Y, Nagao A, Mannen T, Kato Y, et al. Respective functions of two distinct Siwi complexes assembled during PIWI-interacting RNA biogenesis in Bombyx germ cells. Cell Rep. 2015;10(2):193–203. doi: 10.1016/j.celrep.2014.12.013 25558067.
51. Cox DN, Chao A, Lin H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development. 2000;127(3):503–14. 10631171.
52. Moutinho-Pereira S, Matos I, Maiato H. Drosophila S2 cells as a model system to investigate mitotic spindle dynamics, architecture, and function. Methods Cell Biol. 2010;97:243–57. doi: 10.1016/S0091-679X(10)97014-3 20719275.
53. Li D, Morley G, Whitaker M, Huang JY. Recruitment of Cdc20 to the kinetochore requires BubR1 but not Mad2 in Drosophila melanogaster. Mol Cell Biol. 2010;30(13):3384–95. doi: 10.1128/MCB.00258-10 20421417; PubMed Central PMCID: PMC2897573.
54. Lau NC, Ohsumi T, Borowsky M, Kingston RE, Blower MD. Systematic and single cell analysis of <em>Xenopus</em> Piwi‐interacting RNAs and Xiwi. The EMBO Journal. 2009;28(19):2945. doi: 10.1038/emboj.2009.237 19713941
55. Rodriguez AJ, Seipel SA, Hamill DR, Romancino DP, Di Carlo M, Suprenant KA, et al. Seawi—a sea urchin piwi/argonaute family member is a component of MT-RNP complexes. RNA. 2005;11(5):646–56. doi: 10.1261/rna.7198205 15840816
56. Sato K, Nishida KM, Shibuya A, Siomi MC, Siomi H. Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC. Genes Dev. 2011;25(22):2361–73. doi: 10.1101/gad.174110.111 22085963; PubMed Central PMCID: PMC3222902.
57. Ivanov PA, Chudinova EM, Nadezhdina ES. Disruption of microtubules inhibits cytoplasmic ribonucleoprotein stress granule formation. Experimental Cell Research. 2003;290(2):227–33. doi: 10.1016/s0014-4827(03)00290-8 14567982
58. Loschi M, Leishman CC, Berardone N, Boccaccio GL. Dynein and kinesin regulate stress-granule and P-body dynamics. Journal of cell science. 2009;122(Pt 21):3973–82. Epub 2009/10/13. doi: 10.1242/jcs.051383 19825938.
59. Chernov KG, Barbet A, Hamon L, Ovchinnikov LP, Curmi PA, Pastré D. Role of Microtubules in Stress Granule Assembly: MICROTUBULE DYNAMICAL INSTABILITY FAVORS THE FORMATION OF MICROMETRIC STRESS GRANULES IN CELLS. Journal of Biological Chemistry. 2009;284(52):36569–80. doi: 10.1074/jbc.M109.042879 19843517
60. Shao J, Gao F, Zhang B, Zhao M, Zhou Y, He J, et al. Aggregation of SND1 in Stress Granules is Associated with the Microtubule Cytoskeleton During Heat Shock Stimulus. The Anatomical Record. 2017;300(12):2192–9. doi: 10.1002/ar.23642 28758359
61. Hernández-Vega A, Braun M, Scharrel L, Jahnel M, Wegmann S, Hyman BT, et al. Local Nucleation of Microtubule Bundles through Tubulin Concentration into a Condensed Tau Phase. Cell Rep. 2017;20(10):2304–12. doi: 10.1016/j.celrep.2017.08.042 28877466.
62. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, Gregory BD, et al. Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol. 2012;19(8):773–81. Epub 2012/07/31. doi: 10.1038/nsmb.2347 22842725; PubMed Central PMCID: PMC3414646.
63. Chang TH, Mattei E, Gainetdinov I, Colpan C, Weng Z, Zamore PD. Maelstrom Represses Canonical Polymerase II Transcription within Bi-directional piRNA Clusters in Drosophila melanogaster. Molecular Cell. 2019;73(2):291–303.e6. doi: 10.1016/j.molcel.2018.10.038 30527661
64. Sato K, Siomi MC. Two distinct transcriptional controls triggered by nuclear Piwi-piRISCs in the Drosophila piRNA pathway. Current Opinion in Structural Biology. 2018;53:69–76. doi: 10.1016/j.sbi.2018.06.005 29990672
65. Malone CD, Hannon GJ. Molecular Evolution of piRNA and Transposon Control Pathways in Drosophila. Cold Spring Harbor Symposia on Quantitative Biology. 2009;74:225–34. doi: 10.1101/sqb.2009.74.052 20453205
66. Spradling A. Developmental Genetics of Oogenesis. Martinez-Arias MBaA, editor: New York: Cold Spring Harbor Laboratory Press.; 1993.
67. Handler D, Olivieri D, Novatchkova M, Gruber FS, Meixner K, Mechtler K, et al. A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. The EMBO journal. 2011;30(19):3977–93. Epub 2011/08/25. doi: 10.1038/emboj.2011.308 21863019; PubMed Central PMCID: PMC3209783.
68. Olivieri D, Sykora MM, Sachidanandam R, Mechtler K, Brennecke J. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J. 2010;29(19):3301–17. doi: 10.1038/emboj.2010.212 20818334; PubMed Central PMCID: PMC2957214.
69. Inaba M, Buszczak M, Yamashita YM. Nanotubes mediate niche-stem-cell signalling in the Drosophila testis. Nature. 2015;523(7560):329–32. Epub 2015/07/02. doi: 10.1038/nature14602 26131929; PubMed Central PMCID: PMC4586072.
70. Sano H, Nakamura A, Kobayashi S. Identification of a transcriptional regulatory region for germline-specific expression of vasa gene in Drosophila melanogaster. Mech Dev. 2002;112(1–2):129–39. doi: 10.1016/s0925-4773(01)00654-2 11850184.
71. Lerit DA, Gavis ER. Transport of germ plasm on astral microtubules directs germ cell development in Drosophila. Current biology: CB. 2011;21(6):439–48. Epub 2011/03/08. doi: 10.1016/j.cub.2011.01.073 21376599; PubMed Central PMCID: PMC3062663.
72. Van Doren M, Williamson AL, Lehmann R. Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol. 1998;8(4):243–6. doi: 10.1016/s0960-9822(98)70091-0 9501989.
73. Zeidler MP, Perrimon N, Strutt DI. Polarity determination in the Drosophila eye: a novel role for unpaired and JAK/STAT signaling. Genes Dev. 1999;13(10):1342–53. Epub 1999/05/27. doi: 10.1101/gad.13.10.1342 10346822; PubMed Central PMCID: PMC316719.
74. Harris AN, Macdonald PM. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development. 2001;128(14):2823–32. 11526087.
75. Rusan NM, Peifer M. A role for a novel centrosome cycle in asymmetric cell division. J Cell Biol. 2007;177(1):13–20. doi: 10.1083/jcb.200612140 17403931.
76. Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana JS, et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell. 2009;138(6):1137–49. doi: 10.1016/j.cell.2009.07.014 19732946; PubMed Central PMCID: PMC2770713.
77. Patel NH, Snow PM, Goodman CS. Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell. 1987;48(6):975–88. doi: 10.1016/0092-8674(87)90706-9 3548998.
78. Walsh C. Synthesis and assembly of the cytoskeleton of Naegleria gruberi flagellates. J Cell Biol. 1984;98(2):449–56. doi: 10.1083/jcb.98.2.449 6363422; PubMed Central PMCID: PMC2113116.
79. Li MA, Alls JD, Avancini RM, Koo K, Godt D. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol. 2003;5(11):994–1000. doi: 10.1038/ncb1058 14578908.
80. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. doi: 10.1038/nmeth.2019 22743772; PubMed Central PMCID: PMC3855844.
81. Dunn KW, Kamocka MM, McDonald JH. A practical guide to evaluating colocalization in biological microscopy. American Journal of Physiology-Cell Physiology. 2011;300(4):C723–C42. doi: 10.1152/ajpcell.00462.2010 21209361
82. Adler J, Parmryd I. Quantifying colocalization by correlation: The Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry Part A. 2010;77A(8):733–42. doi: 10.1002/cyto.a.20896 20653013
83. Wickersheim ML, Blumenstiel JP. Terminator oligo blocking efficiently eliminates rRNA from Drosophila small RNA sequencing libraries. Biotechniques. 2013;55(5):269–72. doi: 10.2144/000114102 24215643
84. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404
85. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012;9:357. doi: 10.1038/nmeth.1923 https://www.nature.com/articles/nmeth.1923#supplementary-information. 22388286
86. Han BW, Wang W, Zamore PD, Weng Z. piPipes: a set of pipelines for piRNA and transposon analysis via small RNA-seq, RNA-seq, degradome- and CAGE-seq, ChIP-seq and genomic DNA sequencing. Bioinformatics. 2015;31(4):593–5. doi: 10.1093/bioinformatics/btu647 25342065
87. Roberts A, Pachter L. Streaming fragment assignment for real-time analysis of sequencing experiments. Nature Methods. 2012;10:71. doi: 10.1038/nmeth.2251 https://www.nature.com/articles/nmeth.2251#supplementary-information. 23160280
88. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281
89. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841–2. doi: 10.1093/bioinformatics/btq033 20110278
90. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi: 10.1093/bioinformatics/bts635 23104886
91. Jin Y, Tam OH, Paniagua E, Hammell M. TEtranscripts: a package for including transposable elements in differential expression analysis of RNA-seq datasets. Bioinformatics. 2015;31(22):3593–9. doi: 10.1093/bioinformatics/btv422 26206304
92. Cheng J, Hunt AJ. Time-lapse live imaging of stem cells in Drosophila testis. Curr Protoc Stem Cell Biol. 2009;Chapter 2:Unit 2E doi: 10.1002/9780470151808.sc02e02s11 19885824; PubMed Central PMCID: PMC2778854.
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