Молекулярная характеристика герминальной гранулы, участвующей в репрессии повторов Stellate в семенниках Drosophila melanogaster тема диссертации и автореферата по ВАК РФ 03.01.03, кандидат биологических наук Кибанов, Михаил Викторович

  • Кибанов, Михаил Викторович
  • кандидат биологических науккандидат биологических наук
  • 2011, Москва
  • Специальность ВАК РФ03.01.03
  • Количество страниц 115
Кибанов, Михаил Викторович. Молекулярная характеристика герминальной гранулы, участвующей в репрессии повторов Stellate в семенниках Drosophila melanogaster: дис. кандидат биологических наук: 03.01.03 - Молекулярная биология. Москва. 2011. 115 с.

Оглавление диссертации кандидат биологических наук Кибанов, Михаил Викторович

1. ОБЩАЯ ХАРАКТЕРИСТИКА РАБОТЫ.

1.1 Актуальность проблемы.

1.2 цель и задачи исследования.

1.3 Научная новизна результатов исследования.

1.4 Практическая ценность.

1.5 Апробация работы.

Объем диссертации.

2. ОБЗОР ЛИТЕРАТУРЫ.

2.1 рнк-сайленсинг и короткие РНК.

2.1.1 ¿¡РНК и еэгРНК.

2.1.2 т1РНК.

2.1.3. ргРНК.

2.2 Сперматогенез Бкозорниа меыыооавтея.

2.3 герминальные гранулы йКОБОРН1и МЕЫЫОвАЖЕЯ.

2.3.1 Полярные гранулы.

2.3.2 Nuage.

2.4 герминальные гранулы млекопитающих.

2.4.1 Р1 и ргР-Ьоф в гониоцитах млекопитающих.'.

2.4.2 Хроматоидное тельце: открытие и структура.

2.4.2 Подвижность хроматоидного тельца.

2.4.3 Компоненты хроматоиднцго тельца.

2.4.4. Транспорт в хроматоидное тельце.

2.4.5. Хроматоидное тельце и деградация белков в клетке.

2.4.6 Функции хроматоидного тельца.

2.5 метилирование белков терминальных гранул.

2.5.1 Аргининметилтрансферазы.

2.5.2 Метилирование белков системы р1РНК-сайленсинга.

2.5.3 Тийог-домен-содержащие белки.

2.5.4 Функциональное значение метилирования белков подсемейства РШ1.

3. МАТЕРИАЛЫ И МЕТОДЫ.

3.1 линии втзорнна меыыооазтея, использованные в работе.

3.2 иммунофлуоресцентное окрашивание препаратов целых семенников.

3.3 конфокальная микроскопия.

3.4 получение лизатов для электрофореза и вестерн-блот анализа.

3.5 электрофорез в денатурирующих условиях и вестерн-блот анализ.

3.6 антитела.

3.7 выделение тотальной РНК ОЯОЗОРШи для нозерн-блот гибридизации.

3.8 нозерн-блот гибридизация коротких молекул РНК.

4. РЕЗУЛЬТАТЫ.

4.1 герминальные гранулы в сперматоцитах Drosophila.

4.2 временная динамика существования ping-body.

4.3 Архитектура piNG-body.

4.4 Мутационный анализ: разрушение piNG-body и дерепрессия генов Stellate.

4.5 Влияние метилирования остатков аргинина на формирование piNG-body.

5.0БСУЖДЕНИЕ.

6. ВЫВОДЫ.

Рекомендованный список диссертаций по специальности «Молекулярная биология», 03.01.03 шифр ВАК

Заключение диссертации по теме «Молекулярная биология», Кибанов, Михаил Викторович

6. Выводы

1. В сперматоцитах Drosophila melanogaster среди множества мелких околоядерных гранул nuage, обнаружена крупная терминальная гранула (одна на клетку). Гранула обогащена белками, функционирующими в piPHK-пути (Vasa, Aubergine, AG03, Tudor, Spindle-E, Squash, Cutoff) и miPHK-пути сайленсинга (Belle и AGOl), а также содержит белок DCP1 - компонент системы деградации мРНК;

2. Крупная гранула состоит из нескольких периферийных долей, расположенных вокруг центральной доли. Белки Aubergine, Vasa, Tudor, Spindle-E, Squash, Cutoff, AGOl и DCP1 обнаружены в составе внешних долей, тогда как белок AG03 располагается в центре гранулы;

3. Дерепрессия тандемных повторов Stellate в результате нарушения образования piPHK на фоне мутаций в генах vasa, aub и ago3 ассоциирована с исчезновением крупных гранул в первичных сперматоцитах;

4. В отсутствие симметричного метилирования остатков аргинина в белке подсемейства PIWI Aubergine при мутации в гене аргининметилтрансферазы capsuleen наблюдается дерепрессия повторов Stellate, нарушение образования piPHK Su(Ste) и исчезновение крупных терминальных гранул.

Список литературы диссертационного исследования кандидат биологических наук Кибанов, Михаил Викторович, 2011 год

1. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221

2. Ameres SL, Martinez J, Schroeder R' (2007) Molecular basis for target RNA recognition and cleavage by human RISC. Cell 130: 101-112

3. Amikura R, Kashikawa M, Nakamura A', Kobayashi S (2001) Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc Natl Acad Sci USA 98: 9133-9138

4. Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R; Luhrmann R (2005) A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing« bodies. RNA 11: 717-727

5. Anne J, Olio R, Ephrussi A, Mechler BM (2007) Arginine methyltransferase Capsuleen is essential» for methylation of spliceosomal Sm< proteins and' germ- cell formation in Drosophila. Development 134: 137-146

6. Anton E (1983) Association of Golgi vesicles containing acid phosphatase with the chromatoid'body of rat spermatids. Experientia 39: 393-394

7. Aravin AA, Klenov MS, Vagin VV, Bantignies F, Cavalli G, Gvozdev VA (2004) Dissections of a natural RNA silencing process in the Drosophila melanogaster germ line. Mol Cell Biol 24: 6742-6750

8. Aravin AA, Naumova NM, Tulin AV, Vagin W, Rozovsky YM, Gvozdev VA (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 11: 1017-1027

9. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799

10. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747

11. Aravin AA, van der Heijden GW, Castaneda J, Vagin W, Hannon GJ, Bortvin A (2009) Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet 5: el000764

12. Arkov AL, Ramos A (2010) Building RNA-protein granules: insight from! the germline. Trends Cell Biol 20: 482-490

13. Arkov AL, Wang JY, Ramos A, Lehmann R (2006) The role of Tudor domains in germline development and polar granule architecture. Development 133: 4053-4062

14. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 22: 2773-2785

15. Baek D,' Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455: 64-71

16. Barker DD, Wang C, Moore J, Dickinson LK, Lehmann R (1992) Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev 6:2312-2326

17. Bartel DP, Chen CZ (2004) Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5: 396-400

18. Bedford MT (2007) Arginine methylation at a glance. J Cell Sci 120: 4243-4246

19. Bedford MT, Clarke SG (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33: 1-13

20. Bedford MT, Richard S (2005) Arginine methylation an emerging regulator of protein function. Mol Cell 18: 263-272

21. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC (2007) Mammalian mirtron genes. Mol Cell 28: 328-336

22. Bernstein E, Caudy A A, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366

23. Biggiogera M, Fakan S, Leser G, Martin TE, Gordon J (1990) Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Mol Reprod Dev 26: 150-158

24. Blendy JA, Kaestner KH, Weinbauer GF, Nieschlag E, Schutz G (1996) Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380: 162-165

25. Boisvert FM, Cote J, Boulanger MC, Cleroux P, Bachand F, Autexier C, Richard S (2002) Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J Cell Biol 159: 957-969

26. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123: 1279-1291

27. Boswell RE, Mahowald AP (1985) tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell A3: 97-104

28. Braun RE (1998) Post-transcriptional control of gene expression during spermatogenesis. Semin Cell Dev Biol 9: 483-489

29. Breitwieser W, Markussen FH, Horstmann H, Ephrussi A (1996) Oskar protein interaction with Vasa represents an essential step in polar granule assembly. Genes Dev 10: 2179-2188

30. Brengues M, Teixeira D, Parker R (2005) Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489N

31. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103

32. Brennecke J, Stark A, Russell RB, Cohen SM (2005) Principles of microRNA-target recognition. PLoS Biol 3: e85

33. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190

34. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22'. 268-280

35. Cai X, Hagedorn CH, Cullen BR (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10: 1957-1966

36. Carrera P, Johnstone O, Nakamura A, Casanova J, Jackie H, Lasko P (2000)* VASA mediates translation through interaction with a Drosophila yIF2 homolog. Mol Cell 5: 181187

37. Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci USA 97: 9585-9590

38. Caudy AA, Ketting RF, Hammond SM, Denli AM, Bathoorn AM, Tops BB, Silva JM, Myers MM, Hannon GJ, Plasterk RH (2003) A micrococcal nuclease homologue in RNAi effector complexes. Nature 425: 411-414

39. Caudy AA, Myers M, Hannon GJ, Hammond SM (2002) Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev 16: 2491-2496

40. Cenci G, Bonaccorsi S, Pisano C, Verni F, Gatti M (1994) Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J Cell Sci 107 ( Pt<12): 3521-3534

41. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation: Science 303: 1336

42. Chen C, Jin J, James DA, Adams-Cioaba MA, Park JG, Guo Y, Tenaglia E, Xu C, Gish G, Min J, Pawson T (2009) Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi. Proc Natl Acad Sci USA 106: 20336-20341

43. Chen Y, Pane A, Schupbach T (2007) Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila: Curr Biol 17: 637642

44. Chendrimada TP," Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436: 740-744

45. Chennathukuzhi V, Morales CR, El-Alfy M, Hecht NB (2003) The kinesin KIF17b and RNA-binding protein TB-RBP transport specific cAMP-responsive element modulatorregulated mRNAs in male germ cells. Proc Natl Acad Sci USA 100:15566-15571

46. Chuma S, Hiyoshi M, Yamamoto A, Hosokawa M, Takamune K, Nakatsuji N (2003) Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech Dev 120: 979-990

47. Chuma S, Hosokawa M, Tanaka T, Nakatsuji N (2009) Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol Cell Endocrinol 306: 17-23

48. Chung WJ, Okamura K, Martin R, Lai EC (2008) Endogenous RNA interference provides a somatic defense against Drosophila transposons. Curr Biol 18: 795-802

49. Clark JM, Eddy EM (1975) Fine structural observations on the origin and associations of primordial germ cells of the mouse. Dev Biol 47: 136-155

50. Coller J, Parker R (2005) General translational repression by activators of mRNA decapping. Cell 122: 875-886

51. Cote J, Richard S (2005) Tudor domains bind symmetrical dimethylated arginines. J Biol Chem 280: 28476-28483

52. Cougot N, Babajko S, Seraphin B (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165: 31-40

53. Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 12: 3715-3727

54. Cox DN, Chao j A, Lin H (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127: 503-514

55. Creed TM, Loganathan SN, Varonin D, Jackson CA, Arkov AL (2010) Novel role of specific Tudor domains in Tudor-Aubergine protein complex assembly and distribution during Drosophila oogenesis. Biochem Biophys Res Commun 402: 384-389

56. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, Hannon GJ, Brennecke J" (2008) An- endogenous small interfering RNA pathway in Drosophila. Nature 453: 798-802

57. Dalby B, Glover DM (1992) 3' non-translated sequences in Drosophila cyclin B transcripts direct posterior pole accumulation late in oogenesis and peri-nuclear association in syncytial embryos. Development 115: 989-997

58. Dansereau DA, Lasko P*(2008) The development of germline stem cells in Drosophila. Methods Mol Biol 450: 3-26'

59. Deng W, Lin H (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830

60. Denli AM, Tops BB, Plasterk RH, KettingRF, Hannon GJ (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432: 231-235

61. Desset S, Meignin C, Dastugue B, Vaury C (2003) COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164: 501-509

62. Ding D, Parkhurst SM, Halsell SR, Lipshitz HD (1993) Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. Mol Cell Biol 13: 3773-3781

63. Eddy EM (1970) Cytochemical observations on the chromatoid body of the male germ cells. Biol Reprod 2: 114-128

64. Eddy EM (1974) Fine structural observations on the form and distribution of nuage in germ cells of the rat. AnatRec 178: 731-757

65. Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43: 229-280

66. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001a) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian* cells. Nature 411: 494-498"

67. Elbashir SM, Lendeckel W, Tuschl T (2001b) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15: 188-200

68. Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358: 387392

69. Eulalio A, Behm-Ansmant I, Izaurralde E (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 8: 9-22

70. Fawcett DW, Eddy EM, Phillips DM (1970) Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol Reprod 2: 129153

71. Feral'C, Guellaen G, Pawlak A (2001) Human testis expresses a specific poly(A)-binding protein: Nucleic Acids Res 29: 1872-1883

72. Findley SD, Tamanaha M, Clegg NJ, Ruohola-Baker H (2003) Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDEl/AGOl homolog, Aubergine, in nuage. Development 130: 859-871.

73. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811

74. Fuller MT (1998) Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin Cell Dev Biol 9: 433-444

75. Fuller MT, Spradling AC (2007) Male and female Drosophila germline stem cells: two versions of immortality. Science 316: 402-404

76. Garcia-Mata R, Gao YS, Sztul E (2002) Hassles with taking out the garbage: aggravating aggresomes. Traffic 3: 388-396

77. Gavis ER, Lehmann R (1992) Localization of nanos RNA controls embryonic polarity. Cell 71: 301-313

78. Gavis ER, Lehmann R (1994) Translational regulation of nanos by RNA localization. Nature 369: 315-318

79. Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S, Xu J, Kittler EL, Zapp ML, Weng Z, Zamore PD (2008) Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320: 1077-1081

80. Ghildiyal. M, Xu J, Seitz H, Weng Z, Zamore PD (2010) Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA 16: 43-56

81. Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding'universe. Nat Rev Genet 10: 94-108

82. Ghosh-Roy A, Kulkarni M, Kumar. V, Shirolikar S, Ray K (2004) Cytoplasmic dynein-dynactin complex is required for spermatid growth but not axoneme assembly in Drosophila. MolBiol Cell 15: 2470-2483

83. Girard A, Sachidanandam R, Hannon GJ, Carmell MA (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202

84. Gonsalvez GB, Rajendra TK, TianL, Matera AG (2006) The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance. Curr Biol 16: 1077-1089

85. Gonsalvez GB, Tian L, ©spina JK, Boisvert FM, Lamond AI, Matera AG (2007) Two distinct arginine methyltransferases are required for biogenesis of Sm-class ribonucleoproteins. J Cell Biol 178: 733-740

86. Gracheva E, Dus M, Elgin SC (2009)1 Drosophila RISC component VIG and its homology Vig2 impact heterochromatin formation. PLoS One 4: e6182

87. Gregory RI, Yan» KP, Amuthan G, Chendrimada. T, Doratotaj B, Cooch N, Shiekhattar R (2004) The Microprocessor complex mediates the genesis of microRNAs. Nature 432: 235240

88. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-158

89. Grivna ST, Pyhtila B, Lin H' (2006) MIWF associates with translational machinery and PlWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci USA 103: 13415-13420

90. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC (2007) A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 315: 1587-1590

91. Guo S, Bao S (2010) srGAP2 arginine methylation regulates cell migration and cell spreading through promoting dimerization. J Biol Chem 285: 35133-35141

92. Gustafson EA, Wessel GM (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 32: 626-637

93. Haley B, Zamore PD (2004) Kinetic analysis of the RNAi enzyme complex. Nat Struct Mol Biol 11: 599-606

94. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286: 950-952

95. Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Hoshi K, Akasaki K, Yokota S (2005) Chromatoid bodies: aggresome-like characteristics and degradation sites for organelles of spermiogenic cells. JHistochem Cytochem 53: 455-465

96. Hardy RW, Lindsley DL, Livak KJ, Lewis B, Siversten AL, Joslyn GL, Edwards J, Bonaccorsi S (1984) Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster. Genetics 107: 591-610

97. Harris AN, Macdonald PM (2001) Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 28232832

98. Hay B; Jan LY, Jan YN (1988) A protein component of Drosophila1 polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55: 577-587

99. Hay B, Jan LY, Jan YN (1990) Localization of vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity. Development 109: 425-433

100. Head JR, Kresge CK (1985) Reaction* of the chromatoid body with a monoclonal antibody to a rat histocompatibility antigen. Biol Reprod 33: 1001-1008

101. Hess RA, Miller LA, Kirby JD, Margoliash E, Goldberg E (1993) Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol Reprod 48: 1299-1308

102. Horwich MD, Li C, Matranga C, Vagin V, Farley G, Wang P, Zamore PD (2007) The Drosophila RNA methyltransferase, DmHenl, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 17: 1265-1272

103. Hosokawa M, Shoji M, Kitamura K, Tanaka.T, Noce T, Chuma S, Nakatsuji N (2007) Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev Biol 301: 38-52

104. Jankowsky E, Bowers H (2006) Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res 34: 4181-4188

105. Jeon KW, Kennedy JR (1973) The primordial germ cells in early mouse embryos: light and electron microscopic studies. Dev Biol 31: 275-284

106. Jiang F, Ye X, Liu X, Fincher L, McKearin D, Liu Q (2005) Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev 19: 1674-1679

107. Jiang J, White-Cooper H (2003) Transcriptional activation in Drosophila spermatogenesis involves the mutually dependent function'of aly and a novel meiotic arrest gene cookie monster. Development 130: 563-573

108. Johnstone O, Deuring R, Bock R, Linder P, Fuller MT, Lasko P (2005) Belle is a Drosophila DEAD-box protein required for viability and in the germ line. Dev Biol 277: 92-101

109. Johnstone O, Lasko P (2004) Interaction with eIF5B is essential for Vasa function during development. Development 131: 4167-4178

110. Jongens TA, Hay B, Jan LY, Jan YN (1992) The germ cell-less gene product: a posteriorly localized component necessary for germ cell development in Drosophila. Cell 70: 569-584

111. Kashikawa M, Amikura R, Nakamura A, Kobayashi S (1999) Mitochondrial small ribosomal RNA is present on polar granules in early cleavage embryos of Drosophila melanogaster. Dev Growth Differ 41: 495-502

112. Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21: 3123-3134

113. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, Jr., Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA 103: 18002-18007

114. Kawamura Y, Saito K, Kin T, Ono Y, Asai K, Sunohara T, Okada TN, Siomi MC, Siomi H (2008) Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 453: 793-797

115. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169: 871-884

116. Kessel RG (1966) An electron microscope study of nuclear-cytoplasmic exchange in oocytes of Ciona intestinalis. J Ultrastruct Res 15: 181-196

117. Ketting RF, Fischer SE, Bernstein E, Sijen- T, Hannon GJ, Plasterk RH' (2001) Dicer functions) in RNA> interference and'in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15: 2654-2659'

118. Khvorova A, Reynolds A, Jayasena SD (2003) Functional siRNAs and miRNAs exhibit strand»bias. Cell 115: 209-216

119. Kim-Ha J, Kerr K, Macdonald PM (1995) Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 81: 403-412'

120. Kim-Ha J, SmithJL, Macdonald PM'(1991) oskar mRNA is localized.to the posterior pole of the Drosophila oocyte. Cell 66: 23-35

121. Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139

122. Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434: 583-589

123. Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S, Klein PS, Rigoutsos I, Jongens TA, Mourelatos Z (2009) Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol 11: 652-658

124. Kirino Y, Mourelatos Z (2007) Mouse Piwi-interacting RNAs are 2-O-methylated at their 3' termini. Nat Struct Mol Biol 14: 347-348"

125. Kirino Y, Vourekas A, Kim N, de Lima Alves F, Rappsilber J, Klein PS, Jongens TA, Mourelatos Z (2010a) Arginine methylation of vasa protein is conserved across phyla. J Biol Chem 285: 8148-8154

126. Kirino Y, Vourekas A, Sayed N, de Lima Alves F, Thomson T, Lasko P, Rappsilber J, Jongens TA, Mourelatos Z (2010b) Arginine methylation'of Aubergine mediates Tudor binding and germ plasm localization. RNA 16: 70-78

127. Klattenhoff C, Bratu DP, McGinnis-Schultz N, Koppetsch BS, Cook HA, Theurkauf WE (2007) Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response. Dev Cell 12: 45-55

128. Kleene KC (1993) Multiple controls over the efficiency of translation of the mRNAs encoding transition proteins, protamines, and the mitochondrial capsule selenoprotein in late spermatids in mice. Dev Biol 159: 720-731

129. Kleene KC (1996) Patterns of translational regulation in the mammalian testis. Mol Reprod Dev 43: 268-281

130. Knight SW, Bass BL (2001) A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 293: 2269-2271i

131. Kobayashi S, Amikura R, Okada M (1993) Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster. Science 260: 1521-1524

132. Kojima K, Kuramochi-Miyagawa S; Chuma S, Tanaka T, Nakatsuji N, Kimura T, Nakano T (2009) Associations between PIWI proteins and TDRD1/MTR-1 are critical for integrated subcellular localization in murine male germ cells. Genes Cells 14: 1155-1165

133. Komiya T, Itoh K, Ikenishi K, Furusawa M (1994) Isolation and characterization of a novel gene of the DEAD box protein family which is specifically expressed1 in germ cells of Xenopus laevis. Dev Biol 162: 354-363

134. Kopito RR (2000) Aggresomes, inclusion bodies and protehv aggregation. Trends Cell Biol 10:524-530

135. Kotaja N, Kimmins S, Brancorsini S, Hentsch D; Vonesch JL, Davidson I, Parvinen M, Sassone-Corsi P (2004) Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1: 249-254

136. Kotaja N, Lin H, Parvinen M, Sassone-Corsi P (2006b) Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. J Cell Sci 119: 28192825

137. Kotaja N, Macho B, Sassone-Corsi P (2005) Microtubule-independent and protein kinase A-mediated function of kinesin KIF17b controls the intracellular transport of activator of CREM in testis (ACT). J Biol Chem 280: 31739-31745

138. Kotaja N, Sassone-Corsi P (2007) The chromatoid body: a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8: 85-90«

139. Krause CD, Yang ZH, Kim YS, Lee JH, Cook JR, Pestka S (2007) Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol Ther 113: 50-87

140. Krimer DB, Esponda P (1980) Presence of polysaccharides and proteins in the chromatoid body of mouse spermatids. Cell Biol Int Rep 4: 265-270

141. 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 (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849

142. Kuramochi-Miyagawa S, Kimura T, Yomogida K, Kuroiwa A, Tadokoro Y, Fujita Y, Sato M, Matsuda Y, Nakano T (2001) Two mouse piwi-related genes: miwi and mili. Mech Dev 108: 121-133

143. Macho B, Brancorsini S, Fimia GM, Setou M, Hirokawa N, Sassone-Corsi P (2002) CREM-dependent transcription in male germ cells controlled by a kinesin. Science 298: 2388-2390

144. Mahowald AP (1971) Polar granules of Drosophila. 3. The continuity of polar granules during the life cycle of Drosophila. J ExpZool 176: 329-343

145. Majumder S, Alinari L, Roy S, Miller T, Datta J, Sif S, Baiocchi R, Jacob ST (2010) Methylation of histone H3 and H4 by PRMT5 regulates ribosomal RNA gene transcription. J Cell Biochem 109: 553-563

146. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522-535

147. Martin G, Ostareck-Lederer A, Chari A, Neuenkirchen N, Dettwiler S, Blank D, Ruegsegger U, Fischer U, Keller W (2010) Arginine methylation in subunits of mammalian1 pre-mRN A cleavage factor I. RNA 16: 1646-1659

148. Megosh HB, Cox DN, Campbell C, Lin H (2006) The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr Biol 16: 1884-1894

149. Meikar O, Da Ros M, Korhonen H, Kotaja N (2011) Chromatoid body and small RNAs in male germ cells. Reproduction 142: 195-209

150. Meikar O, Da Ros M, Liljenback H, Toppari J; Kotaja N (2010) Accumulation of piRNAs in the chromatoid bodies purified by a novel isolation protocol. Exp Cell Res 316: 1567-1575

151. Mette MF, Aufsatz W, van der Winden J, Matzke MA, Matzke AJ (2000) Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J19: 51945201

152. Mevel-Ninio M, Pelisson-A, Kinder J, Campos AR, Bucheton A (2007) The flamenco locus controls the gypsy and ZAM retroviruses and is required for Drosophila oogenesis. Genetics 175: 1615-1624

153. Miyoshi K, Tsukumo H, Nagami T, Siomi H, Siomi MC (2005) Slicer* function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev 19: 2837-2848

154. Moussa F, Oko R, Hermo L (1994) The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res 278: 363-378

155. Nagao A, Mituyama T, Huang H, Chen D, Siomi MC, Siomi H (2010) Biogenesis pathways of piRNAs loaded onto AG03 in the Drosophila testis. RNA 16: 2503-2515

156. Nakamura. A, Amikura R, Mukai M, Kobayashi S, Lasko PF (1996) Requirement for a noncoding RNA in Drosophila, polar- granules for germ cell establishment. Science 274: 2075-2079

157. Nantel F, Monaco L, Foulkes NS, Masquilier D, LeMeur M, Henriksen K, Dierich A, Parvinen M, Sassone-Corsi P (1996) Spermiogenesis deficiency and« germ-cell apoptosis in CREM-mutantmice. Nature 380: 159-162

158. Nishida KM, Okada TN, Kawamura T, Mituyama T, Kawamura *Y, Inagaki S, Huang H, Chen D, Kodama T, Siomi H, Siomi MC (2009) Functional involvement of Tudor and dPRMT5 in the piRNA processing pathway in Drosophila* germlines. EMBO J 28: 38203831

159. Nishida KM, Saito -K, Mori T, Kawamura Y, Nagami-OkadaiT, Inagaki S, Siomi H, Siomi MC (2007) Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. RNA 13: 1911-1922

160. Noce T, Okamoto-Ito S, Tsunekawa N (2001) Yasa homolog genes in mammalian germ cell development. Cell Struct Fund 26: 131-136

161. Ohara T, Sakaguchi Y, Suzuki T, Ueda H, Miyauchi K (2007) The 3' termini of mouse Piwi-interacting RNAs are 2'-0-methylated. Nat Struct Mol Biol 14: 349-350

162. Okamura K, Balla S, Martin R, Liu N, Lai EC (2008a) Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat Struct Mol Biol 15: 581-590

163. Okamura. K, Chung WJ, Ruby JG, Guo H, Bartel DP, Lai EC (2008b) The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 453: 803-806

164. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC (2007) The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130: 89-100

165. Oko R, Korley R, Murray MT, Hecht NB, Hermo L (1996) Germ cell-specific DNA and RNA binding proteins p48/52 are expressed at specific stages of male germ cell development and are present in the chromatoid body. Mol Reprod Dev 44: 1-13

166. Onohara Y, Fujiwara T, Yasukochi T, Himeno M, Yokota S (2010) Localization of mouse vasa homolog protein in chromatoid body and related nuage structures of mammalian spermatogenic cells during spermatogenesis. Histochem Cell Biol 133: 627-639

167. Pal-Bhadra M, Leibovitch BA, Gandhi SG, Rao M, Bhadra U, Birchler JA, Elgin SC (2004) Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303: 669-672

168. Pane A, Wehr K, Schupbach T (2007) zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell 12: 851-862

169. Paniagua R, Nistal M, Amat P, Rodriguez MC (1985) Presence of ribonucleoproteins and basic proteins in the nuage and intermitochondrial bars of human spermatogonia. J Anat 143: 201-206

170. Papp I, Mette MF, Aufsatz W, Daxinger L, Schauer SE, Ray A, van der Winden J, Matzke M, Matzke AJ (2003) Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol 132: 1382-1390

171. Parvinen M, Parvinen LM (1979) Active movements of the chromatoid body. A possible transport mechanism for haploid gene products. J Cell Biol 80: 621-628

172. Patil VS, Kai T (2010) Repression of Retroelements in Drosophila Germline via piRNA Pathway by the Tudor Domain Protein Tejas. Curr Biol 20: 724-730

173. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T (2004) Identification of virus-encoded microRNAs. Science 304: 734736

174. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309: 1573-1576

175. Pollack BP, Kotenko SV, He W, Izotova LS, Barnoski BL, Pestka S (1999) The human homologue of the yeast proteins Skbl and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem 274: 31531-31542

176. Prud'homme N, Gans M, Masson M, Terzian C, Bucheton A (1995) Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139: 697-711

177. Raff JW, Whitfield WG, Glover DM (1990) Two distinct mechanisms localise cyclin В transcripts in syncytial Drosophila embryos. Development 110: 1249-1261

178. Raz E (2000) The function and regulation of vasa-like genes in germ-cell development. Genome Biol 1: REVIEWS 1017

179. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16: 1616-1626

180. Ren J, Wang Y, Liang Y, Zhang Y, Bao S, Xu Z (2010) Methylation of ribosomal protein S10 by protein-arginine methyltransferase 5 regulates ribosome biogenesis. J Biol Chem 285: 12695-12705

181. Reuter M, Chuma S, Tanaka T, Franz T, Stark A, Pillai RS (2009) Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons andi alters the Mili-associated small RNA profile. Nat Struct Mol Biol 16: 639-646

182. Rhoades MW, Reinhart BJ, Lim LP, Bürge CB; Bartel B, Bartel DP (2002) Prediction, of plant microRNA targets. Cell 110: 513-520

183. Rongo C, Lehmann R (1996) Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet 12: 102-109

184. Rossi JJ (2005) RNAi and the P-body connection. Nat Cell Biol l: 643-644

185. Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448: 83-86

186. Russell L, Frank B'(1978) Ultrastructural characterization of nuage in spermatocytes of the rat testis. Anat Ree 190: 79-97

187. Saito K; Ishizuka A, Siomi-H, Siomi MG (2005) Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol 3: e235

188. Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20: 2214-2222

189. Saito K, Sakaguchi Y, Suzuki T, Siomi H, Siomi MC (2007) Pimet, the Drosophila homolog of HEN1, mediates 2'-0-methylation of Piwi- interacting RNAs at their 31 ends. Genes Dev' 21: 1603-1608

190. Sasaki T, Shiohama A, Minoshima S, Shimizu N (2003) Identification of eight members of the Argonaute family in the human genome small star, filled. Genomics 82: 323-330

191. Sassone-Corsi P (2002) Unique chromatin remodeling and transcriptional regulations in spermatogenesis. Science 296: 2176-2178

192. Savitsky M, Kwon D, Georgiev P, Kalmykova A, Gvozdev V (2006) Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline. Genes Dev 2 345-354

193. Scadden AD (2005) The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nat Struct Mol Biol 12: 489-496

194. Schulze SR, McAllister BF, Sinclair DA, Fitzpatrick KA, Marchetti M, Pimpinelli S, Honda BM (2006) Heterochromatic genes in Drosophila: a comparative analysis of two genes-Genetics 173: 1433-1445

195. Schupbach T, Wieschaus E (1986) Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113: 443-448

196. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208'

197. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin-R, Rajewsky N (2008)' Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63

198. Selenko P, Sprangers R, Stier G, Buhler D, Fischer U, Sattler M (2001) SMN tudor domain structure and' its interaction with the Sm proteins. Nat Struct Biol 8: 27-31

199. Sen GL, Blau HM (2005) Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat Cell Biol 7: 633-636

200. Sheth U, Parker R (2003) Decapping and decay of messenger RNA occur in cytoplasm0 processing bodies. Science 300: 805-808

201. Shibata N, Tsunekawa N, Okamoto-Ito S, Akasu R, Tokumasu A, Noce T (2004) IViouse RanBPM is a partner gene to a germline specific RNA helicase, mouse vasa homol°S protein: MolReprodDev 67:-1-7

202. Shoji M, Chuma S, Yoshida K, Morita T, Nakatsuji N (2005) RNA interference dixring spermatogenesis in mice. Dev Biol 282: 524-534

203. Shpiz S, Olovnikov I, Sergeeva A, Lavrov S, Abramov Y, Savitsky M, Kalmykova A (20ll) Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res

204. Singh SR, Hou SX (2008) Immunohistological techniques for studying the Drosophila male germline stem cell. Methods Mol Biol 450: 45-59

205. Siomi MC, Mannen T, Siomi H (2010) How does the royal family of Tudor rule the PlWI-interacting RNA pathway? Genes Dev 24: 636-646

206. Siomi MC, Sato K, Pezic D, Aravin AA (2011) PlWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258

207. Smith JL, Wilson JE, Macdonald PM (1992) Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos. Cell 70: 849-859

208. Smith JM, Bowles J, Wilson,M, Teasdale RD, Koopman P (2004) Expression of the tudor-related gene Tdrd5 during development of the male germline in mice. Gene Expr Patterns 4: 701-705

209. Snee MJ, Macdonald PM'(2004) Live imaging of nuage and polar granules: evidence against a precursor-product relationship4 and a novel role for Oskar in stabilization of polar granule components. JCellSci 117: 2109-2120

210. Soderstrom KO (1978) Formation of chromatoid body during rat spermatogenesis. Z Mikrosk Anat Forsch 92: 417-430

211. Soderstrom KO (1981) Labelling of the chromatid,body by 3H.uridine in.rat pachytene spermatocytes. Exp Cell Res 131: 488-491 ,

212. Soderstrom KO, Parvinen M (1976a) Incorporation of (3H)uridine by the chromatoid body during rat spermatogenesis. J Cell Biol 70: 239-246 '

213. Soderstrom KO, Parvinen M (1976b) RNA synthesis in different stages of rat, seminiferous epithelial'cycle. Mol Cell Endocrinol 5: 181-199

214. Soper SF, van der Heijden GW, Hardiman TC, Goodheart M, Martin SL, de-Boer P, Bortvin A (2008) Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15: 285-297

215. Specchia V, Piacentini L, Tritto P, Fanti L, D'Alessandro R, Palumbo G, Pimpinelli S, Bozzetti MP (2010) Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463: 662-665

216. Sprando RL, Russell LD (1987) Comparative study of cytoplasmic elimination in spermatids of selected mammalian species. Am J Anat 178: 72-80

217. St Johnston D, Beuchle D, Nusslein-Volhard C (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66: 51-63

218. Stapleton W, Das S, McKee BD (2001) A role of the Drosophila homeless gene in repression of Stellate in male meiosis. Chromosoma 110: 228-240

219. Stefani G, Slack FJ (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9: 219-230

220. Strome S, Lehmann R (2007) Germ versus soma decisions: lessons from flies and worms. Science 316: 392-393

221. Styhler S, Nakamura A, Swan A, Suter B, Lasko P (1998) vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125: 1569-1578

222. Susi FR, Clermont Y (1970) Fine structural modifications of the rat chromatoid body during spermiogenesis. Am JAnat 129: 177-191

223. Szakmary A, Reedy M, Qi H, Lin H (2009) The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J Cell Biol 185: 613-627

224. Talbot K, Miguel-Aliaga I, Mohaghegh P, Ponting CP, Davies KE (1998) Characterization* of a gene1 encoding survival motor neuron (SMN)-related protein, a constituent of the spliceosome complex. Hum Mol Genet 7: 2149-2156

225. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538

226. Tanaka H, Baba T (2005) Gene expression in spermiogenesis. Cell Mol Life Sci 62: 344-354

227. Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui* Y, Nakahara Y, Suzuki R, Yokoyama M, Noce T (2000) The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 14: 841-853

228. Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17: 49-63

229. Tang XM, Lalli MF, Clermont Y (1982) A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat. Am JAnat 163: 283-294

230. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R (2005) Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11: 371-382

231. Terry NA, Tulina N, Matunis E, DiNardo S (2006) Novel regulators revealed by profiling Drosophila testis stem cells within their niche. Dev Biol 294: 246-257

232. Thomson T, Lasko P (2004) Drosophila tudor is> essential for polar granule assembly and pole cell specification, but not for posterior patterning. Genesis 40: 164-170

233. Thomson T, Lasko P (2005) Tudor and its domains: germ cell formation from a Tudor perspective. Cell Res 15: 281-291

234. Thomson T, Lin H (2009) The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 25: 355-376

235. Thorne-Tjomsland G, Clermont Y, Hermo L (1988) Contribution of the Golgi apparatus components to the formation of the acrosomic system and chromatoid body in rat spermatids. Anat Rec 221: 591-598

236. Tinker R, Silver D, Montell DJ (1998) Requirement for the vasa RNA helicase in gurken mRNA localization. Dev Biol 199: 1-10

237. Tomancak P, Guichet A, Zavorszky P, Ephrussi A (1998) Oocyte polarity depends on regulation of gurken by Vasa. Development 125r 1723-1732

238. Toyooka Y, Tsunekawa-N, Takahashi Y, Matsui Y, Satoh M, Noce T (2000) Expression and», intracellular localization» of mouse Vasa-homologue protein during germ cell development: Mech Dev 93: 139-149

239. Tsai-Morris CH, Sheng Y, Lee E, Lei KJ, Dufau ML (2004) Gonadotropin-regulated' testicular. RNA. helicase (GRTH/Ddx25) is essential for spermatid, development and completion of spermatogenesis. Proc Natl Acad Sci USA 101: 6373-6378

240. Vagin VV, Hannon GJ, Aravin AA (2009a) Arginine methylation as a molecular signature of the Piwi small RNApathway. Cell Cycle 8: 4003-4004

241. Vagin W, Klenov MS, Kalmykova AI, Stolyarenko AD, Kotelnikov RN, Gvozdev VA (2004),The. RNA interference proteins and. vasa1 locus are involved in the silencing of retrotransposons in the female germline of Drosophila melanogaster. RNA Biol 1: 54-58

242. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD~(2006) A» distinct small RNA , pathway silences selfish genetic elements in the germline. Science 313: 320-324 •

243. Vasileva A, Tiedau. D, Firooznia A, Muller-Reichert T, Jessberger R (2009) Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation- of miRNA expression. Curr Biol 19: 630-639

244. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis-mRNAs. Mol Cell 16: 69-79

245. Vazquez J, Belmont AS, Sedat JW (2002) The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr Biol 12: 1473-1483

246. Ventela S, Toppari J, Parvinen M (2003) Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: mechanisms of haploid gene product sharing. Mol Biol Cell 14: 2768-2780

247. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676

248. Walt H, Armbruster BL (1984) Actin and RNA are components of the chromatoid bodies in spermatids of the rat. Cell Tissue Res 236: 487-490

249. Wang J, Saxe JP, Tanaka T, Chuma S, Lin H (2009) Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr Biol 19: 640-644

250. Wang Z, Lin H (2005) The division of Drosophila germline stem cells and their precursors requires a specific cyclin. Curr Biol 15: 328-333

251. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, Surani MA, Sakaki Y, Sasaki H (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543

252. Wawersik M (2006) Germ cell sex determination: piecing together a complex puzzle. Cell Cycle 5'. 1385-1390

253. Werner G, Werner K (1995) Immunocytochemical localization of histone H4 in the chromatoid body of rat'spermatids. J Submicrosc Cytol Pathol 27: 325-330'

254. White-Cooper H (2004) Spermatogenesis: analysis of meiosis and. morphogenesis. Methods Mol Biol 247: 45-75

255. White-Cooper H (2010) Molecular mechanisms of gene regulation i during- Drosophila* spermatogenesis. Reproduction 139: 11-21

256. Wightman B, Burglin TR, Gatto J, Arasu P, Ruvkun G (1991) Negative regulatory sequences in the lin-14 3'-untranslated region-are necessary to generate a temporal1 switch during Caenorhabditis elegans development. Genes Dev 5: 1813-1824

257. Wightman,B, Ha I, Ruvkun G (1993)-Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862

258. Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method" identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102: 9703-9708

259. Williams MA, Smith LD (1971) Ultrastructure of the "germinal plasm" during maturation and early cleavage in Rana pipiens. Dev Biol 25: 568-580'

260. Williamson A, Lehmann R (1996) Germ cell development in Drosophila. Annu Rev Cell Dev Biol 12: 365-391

261. Wilson JE, Connell JE, Macdonald PM (1996) aubergine enhances oskar translation in the Drosophila ovary. Development 122: 1631-1639

262. Wojcik C, DeMartino GN (2003) Intracellular localization of proteasomes. Int J Biochem Cell Biol 35: 579-589

263. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2: E104

264. Yamashita YM, Fuller MT, Jones DL (2005) Signaling in stem cell niches: lessons from the t Drosophila germline. J Cell Sci 118: 665-672

265. Yang N, Kazazian HH, Jr. (2006) LI retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct-Mol Biol 13: 763-771

266. Yekta S, Shih IH, Bartel DP (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304: 594-596

267. Yokota S (2008) Historical survey on chromatoid body research. Acta Histochem Cytochem 41: 65-82

268. Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124: 3157-3165

269. Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19: 2164-2175

270. Yu Z, Raabe T, Hecht NB (2005) MicroRNA Mirnl22a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol Reprod,13: 427-433

271. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101: 25-33

272. Zhou R, Hotta I, Denli AM, Hong P, Perrimon N, Hannon GJ (2008) Comparative analysis of argonaute-dependent small RNA pathways in Drosophila. Mol Cell 32: 592-599

273. Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719

Обратите внимание, представленные выше научные тексты размещены для ознакомления и получены посредством распознавания оригинальных текстов диссертаций (OCR). В связи с чем, в них могут содержаться ошибки, связанные с несовершенством алгоритмов распознавания. В PDF файлах диссертаций и авторефератов, которые мы доставляем, подобных ошибок нет.