Nuage morphogenesis becomes more complex: Two translocation pathways and two forms of nuage coexist in Drosophila germline syncytia

Cell and Tissue Research

Volumn 344, Issue 1, 2011, Pages 169-181

  Jaglarz, Mariusz K ^a   Kloc, Malgorzata ^b   Jankowska, Wladyslawa ^a   Szymanska, Beata ^a   Bilinski, Szczepan M ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

Drosophila melanogaster; Germ plasm; Nuage; Oogenesis; Sponge body

Indexed keywords

ARGONAUTE PROTEIN; RIBONUCLEOPROTEIN; SURVIVAL MOTOR NEURON PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL MATURATION; CELL MIGRATION; CELL ORGANELLE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CYTOPLASM; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; FEMALE; INTRACELLULAR TRANSPORT; LIFESPAN; MICROTUBULE; MICROTUBULE ORGANIZING CENTER; MORPHOGENESIS; NONHUMAN; NUAGE; OOCYTE DEVELOPMENT; OVARY; PRIORITY JOURNAL; SYNCYTIUM;

ANIMALS; DEAD-BOX RNA HELICASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; IMMUNOHISTOCHEMISTRY; MORPHOGENESIS; OOCYTES; OOGENESIS;

DROSOPHILA MELANOGASTER;

EID: 79953811217     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-011-1145-2     Document Type: Article

References (84)

1. Anne J, Mechler BM (2005) Valois, a component of the nuage and pole plasm, is involved in assembly of these structures, and binds to Tudor and the methyltransferase Capsuléen. Development 132:2167-2177 (Pubitemid 40744476)
2. Arkov AL, Ramos A (2010) Building RNA-protein granules: insight from the germline. Trends Cell Biol 20:482-490
3. Bardsley A, McDonald K, Boswell RE (1993) Distribution of Tudor protein in the Drosophila embryo suggests separation of functions based on site of localization. Development 119:207-219 (Pubitemid 23279140)
4. Bastock R, St Johnston D (2008) Drosophila oogenesis. Curr Biol 18:R1082-R1087
5. Battle DJ, Kasim M, Yong J, Lotti F, Lau CK, Mouaikel J, Zhang Z, Han K, Wan L, Dreyfuss G (2006) The SMN complex: an assembly machine for RNPs. Cold Spring Harb Symp Quant Biol 71:313-320
6. Becalska AN, Gavis ER (2009) Lighting up mRNA localization in Drosophila oogenesis. Development 136:2493-2503
7. Besse F, Ephrussi A (2008) Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat Rev Mol Cell Biol 9:971-980
8. Boswell RE, Mahowald AP (1985) tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43:97-104 (Pubitemid 16199699)
9. 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 (Pubitemid 26303873)
10. Brendza RP, Serbus LR, Duffy JB, Saxton WM (2000) A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289:2120-2122
11. Chang JS, Tan L, Schedl P (1999) The Drosophila CPEB homolog, Orb, is required for oskar protein expression in oocytes. Dev Biol 215:91-106 (Pubitemid 29519805)
12. Chang P, Torres J, Lewis RA, Mowry KL, Houliston E, King ML (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes by entrapment and association with endoplasmic reticulum. Mol Biol Cell 15:4669-4681 (Pubitemid 39299113)
13. Cohen RS (2005) The role of membranes and membrane trafficking in RNA localization. Biol Cell 97:5-18
14. Deshler JO, Highet MI, Schnapp BJ (1997) Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 276:1128-1131 (Pubitemid 27218124)
15. Du TG, Schmid M, Jansen RP (2007) Why cells move messages: the biological functions of mRNA localization. Semin Cell Dev Biol 18:171-177 (Pubitemid 46756367)
16. Du Y, Ferro-Novick S, Novick P (2004) Dynamics and inheritance of the endoplasmic reticulum. J Cell Sci 117:2871-2878 (Pubitemid 39117662)
17. Eddy EM (1975) Germ plasm and the differentiation of the germ line. Int Rev Cytol 43:229-281
18. English AR, Zurek N, Voeltz GK (2009) Peripheral ER structure and function. Curr Opin Cell Biol 21:596-602
19. Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358:387-392
20. 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 (Pubitemid 46012011)
21. Findley SD, Tamanaha M, Clegg NJ, Ruohola-Baker H (2003) Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130:859-871 (Pubitemid 36367507)
22. Fischer U, Liu Q, Dreyfuss G (1997) The SMN-Gemin2 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90:1023-1029
23. Gamberi C, Johnstone O, Lasko P (2006) Drosophila RNA binding proteins. Int Rev Cytol 248:43-139 (Pubitemid 43238170)
24. Gerst JE (2008) Message on the web: mRNA and ER co-trafficking. Trends Cell Biol 18:68-76
25. Gillespie DE, Berg CA (1995) Homeless is required for RNA localization in Drosophila oogenesis and encodes a new member of the DEH family of RNA-dependent ATPases. Genes Dev 9:2495-2508
26. Harris AN, Macdonald PM (2001) Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128:2823-2832 (Pubitemid 32701010)
27. Hay B, Jan LY, Jan YN (1988a) A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55:577-587
28. Hay B, Jan LY, Jan YN (1988b) Identification of a component of Drosophila polar granules. Development 103:635-640
29. Hay B, Jan LY, Jan YN (1990) Localization of Vasa, a component of Drosophila polar granules, in maternal effect mutants that alter embryonic anterioposterior polarity. Development 109:425-433 (Pubitemid 20205581)
30. Holt CE, Bullock SL (2009) Subcellular mRNA localization in animal cells and why it matters. Science 326:1212-1216
31. Kim-Ha J, Smith JL, Macdonald PM (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23-35 (Pubitemid 121001344)
32. 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
33. King ML, Messitt TJ, Mowry KL (2005) Putting RNAs in the right place at the right time: RNA localization in the frog oocyte. Biol Cell 97:19-33 (Pubitemid 40220710)
34. Kloc M, Etkin LD (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121:287-297
35. Kloc M, Etkin LD (1998) Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus. Mech Dev 73:95-106 (Pubitemid 28218546)
36. Kloc M, Etkin LD (2005) RNA localization mechanisms in oocytes. J Cell Sci 118:269-282 (Pubitemid 40277340)
37. Kloc M, Zearfoss NR, Etkin LD (2002) Mechanisms of subcellular mRNA localization. Cell 108:533-544 (Pubitemid 34260878)
38. Kloc M, Bilinski S, Etkin LD (2004) The Balbiani body and germ cell determinants: 150 years later. Curr Topics Dev Biol 59:1-36 (Pubitemid 39752349)
39. Lasko PF, Ashburner M (1990) Posterior localization of Vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev 4:905-921
40. Lee C, Chen L (1988) Dynamic behavior of endoplasmic reticulum in living cells. Cell 54:37-46
41. Lee L, Davies SE, Liu J-L (2009) The spinal muscular atrophy protein SMN affects Drosophila germline nuclear organization through the U body-P body pathway. Dev Biol 332:142-155
42. Lehmann R, Nusslein-Volhard C (1986) Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47:141-152
43. Liang L, Diehl-Jones W, Lasko P (1994) Localization of Vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120:1201-1211 (Pubitemid 24150045)
44. Lim AK, Kai T (2007) Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc Natl Acad Sci USA 104:6714-6719
45. Liu JL, Gall JG (2007) U bodies are cytoplasmic structures that contain uridine-rich small nuclear ribonucleoproteins and associate with P bodies. Proc Natl Acad Sci USA 104:11655-11659
46. Liu JL, Murphy C, Buszczak M, Clatterbuck S, Goodman R, Gall JG (2006) The Drosophila melanogaster Cajal body. J Cell Biol 172:875-884
47. Liu Q, Fischer U, Wang F, Dreyfuss G (1997) The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90:1013-1021 (Pubitemid 27408515)
48. Mahowald AP (1962) Fine structure of pole cells and polar granules in Drosophila melanogaster. J Exp Zool 151:201-215
49. Mahowald AP (2001) Assembly of the Drosophila germ plasm. Int Rev Cytol 203:187-213
50. Martin KC, Ephrussi A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136:719-730
51. Matova N, Mahajan-Miklos S, Mooseker MS, Cooley L (1999) Drosophila Quail, a villin-related protein, bundles actin filaments in apoptotic nurse cells. Development 126:5645-5657 (Pubitemid 30035013)
52. McCall K, Steller H (1998) Requirement for DCP-1 caspase during Drosophila oogenesis. Science 279:230-234 (Pubitemid 28103881)
53. Meignin C, Davis I (2010) Transmitting the message: intracellular mRNA localization. Curr Opin Cell Biol 22:112-119
54. Meister G, Fischer U (2002) Assisted RNP assembly: SMN and PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs. EMBO J 21:5853-5863 (Pubitemid 35315283)
55. Meister G, Buhler D, Pillai R, Lottspeich F, Fischer U (2001) A multiprotein complex mediates the ATP-dependent assembly of spliceosomal U snRNPs. Nat Cell Biol 3:945-949 (Pubitemid 34428738)
56. Meister G, Eggert C, Fischer U (2002) SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol 12:472-478 (Pubitemid 35346518)
57. Minakhina S, Steward R (2005) Axes formation and RNA localization. Curr Opin Gen Dev 15:416-421 (Pubitemid 40982093)
58. Nakamura A, Amikura R, Mukai M, Kobayashi S, Lasko PF (1996) Required for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science 274:2075-2079 (Pubitemid 27021527)
59. Nakamura A, Amikura R, Hanyu K, Kobayashi S (2001) Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development 128:3233-3242 (Pubitemid 32910376)
60. Nezis IP, Stravopodis DJ, Papassideri I, Robert-Nicoud M, Margaritis LH (2000) Stage-specific apoptotic patterns during Drosophila oogenesis. Eur J Cell Biol 79:610-620
61. Palacios IM (2007) How does an mRNA find its way? Intracellular localisation of transcripts. Semin Cell Dev Biol 18:163-170
62. Parker R, Seth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635-646 (Pubitemid 46341926)
63. 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
64. Paushkin S, Gubitz AK, Massenet S, Dreyfuss G (2002) The SMN complex, an assemblyosome of ribonucleoproteins. Curr Opin Cell Biol 14:305-312 (Pubitemid 34626968)
65. Pellizzoni L, Yong J, Dreyfuss G (2002) Essential role for the SMN complex in the specificity of snRNP assembly. Science 298:1775-1779 (Pubitemid 35404118)
66. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208-211
67. Rongo C, Lehmann R (1996) Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet 12:102-109 (Pubitemid 26094855)
68. Rongo C, Gavis ER, Lehmann R (1995) Localization of oskar RNA regulates oskar translation and requires Oskar protein. Development 121:2737-2746
69. Saffman EE, Lasko P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55:1141-1163 (Pubitemid 29361079)
70. Schupbach T, Wieschaus E (1986) Maternal-effect mutations altering the anteriorposterior pattern of the Drosophila embryo. Roux's Arch Dev Biol 195:302-317
71. Snee MJ, Macdonald PM (2004) 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 117:2109-2120 (Pubitemid 38745143)
72. Spradling AC (1993) Developmental genetics of oogenesis. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, vol 1. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp 1-70
73. St Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6:363-375
74. 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 (Pubitemid 28256725)
75. Terasaki M, Chen LB, Fujiwara K (1986) Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 103:1557-1568 (Pubitemid 17174178)
76. Theurkauf WE, Alberts BM, Jan YN, Jongens TA (1993) A central role for microtubules in the differentiation of Drosophila oocytes. Development 118:1169-1180 (Pubitemid 23252406)
77. Thomson T, Liua N, Arkov A, Lehmann R, Lasko P (2008) Isolation of new polar granule components in Drosophila reveals P body and ER associated proteins. Mech Dev 125:865-873
78. Tinker R, Silver D, Montell DJ (1998) Requirement for the vasa RNA helicase in gurken mRNA localization. Dev Biol 199:1-10 (Pubitemid 28317906)
79. Tomancak P, Guichet A, Zavorszky P, Ephrussi A (1998) Oocyte polarity depends on regulation of gurken by Vasa. Development 125:1723-1732 (Pubitemid 28256740)
80. Vedrenne C, Hauri H-P (2006) Morphogenesis of the endoplasmic reticulum: beyond active membrane expansion. Traffic 7:639-646 (Pubitemid 43676973)
81. Waterman-Storer C, Salmon E (1998) Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol 8:798-806 (Pubitemid 28324534)
82. Wilhelm JE, Mansfield J, Hom-Booher N, Wang S, Turck CW, Hazelrigg T, Vale RD (2000) Isolation of a ribonucleoprotein complex involved in mRNA localization in Drosophila oocytes. J Cell Biol 148:427-440
83. Wilsch-Brauninger M, Schwarz H, Nusslein-Volhard C (1997) A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis. J Cell Biol 139:817-829 (Pubitemid 27485845)
84. Zimyanin VL, Belaya K, Pecreaux J, Gilchrist MJ, Clark A, Davis I, St Johnston D (2008) In vivo imagining of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134:843-853