Translational Control of Germ Cell Decisions

  • Kumari Pushpa
  • Ganga Anil Kumar
  • Kuppuswamy Subramaniam
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 59)

Abstract

Germline poses unique challenges to gene expression control at the transcriptional level. While the embryonic germline maintains a global hold on new mRNA transcription, the female adult germline produces transcripts that are not translated into proteins until embryogenesis of subsequent generation. As a consequence, translational control plays a central role in governing various germ cell decisions including the formation of primordial germ cells, self-renewal/differentiation decisions in the adult germline, onset of gametogenesis and oocyte maturation. Mechanistically, several common themes such as asymmetric localization of mRNAs, conserved RNA-binding proteins that control translation by 3′ UTR binding, translational activation by the cytoplasmic elongation of the polyA tail and the assembly of mRNA-protein complexes called mRNPs have emerged from the studies on Caenorhabditis elegans, Xenopus and Drosophila. How mRNPs assemble, what influences their dynamics, and how a particular 3′ UTR-binding protein turns on the translation of certain mRNAs while turning off other mRNAs at the same time and space are key challenges for future work.

References

  1. Ariz M, Mainpal R, Subramaniam K (2009) C. elegans RNA-binding proteins PUF-8 and MEX-3 function redundantly to promote germline stem cell mitosis. Dev Biol 326:295–304PubMedPubMedCentralCrossRefGoogle Scholar
  2. Arumugam K, Macnicol MC, Macnicol AM (2012a) Autoregulation of Musashi1 mRNA translation during Xenopus oocyte maturation. Mol Reprod Dev 79:553–563PubMedCrossRefGoogle Scholar
  3. Arumugam K, MacNicol MC, Wang Y, Cragle CE, Tackett AJ, Hardy LL, MacNicol AM (2012b) Ringo/cyclin-dependent kinase and mitogen-activated protein kinase signaling pathways regulate the activity of the cell fate determinant Musashi to promote cell cycle re-entry in Xenopus oocytes. J Biol Chem 287:10639–10649PubMedPubMedCentralCrossRefGoogle Scholar
  4. Austin J, Kimble J (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51:589–599PubMedCrossRefGoogle Scholar
  5. Barnard DC, Ryan K, Manley JL, Richter JD (2004) Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 119:641–651PubMedCrossRefGoogle Scholar
  6. Barnard DC, Cao Q, Richter JD (2005) Differential phosphorylation controls Maskin association with eukaryotic translation initiation factor 4E and localization on the mitotic apparatus. Mol Cell Biol 25:7605–7615PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barrios F, Filipponi D, Pellegrini M, Paronetto MP, Di Siena S, Geremia R, Rossi P, De Felici M, Jannini EA, Dolci S (2010) Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J Cell Sci 123:871–880PubMedCrossRefGoogle Scholar
  8. Batchelder C, Dunn MA, Choy B, Suh Y, Cassie C, Shim EY, Shin TH, Mello C, Seydoux G, Blackwell TK (1999) Transcriptional repression by the Caenorhabditis elegans germ-line protein PIE-1. Genes Dev 13:202–212PubMedPubMedCentralCrossRefGoogle Scholar
  9. Biedermann B, Wright J, Senften M, Kalchhauser I, Sarathy G, Lee MH, Ciosk R (2009) Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 17:355–364PubMedCrossRefGoogle Scholar
  10. Bontems F, Stein A, Marlow F, Lyautey J, Gupta T, Mullins MC, Dosch R (2009) Bucky ball organizes germ plasm assembly in zebrafish. Curr Biol 19:414–422PubMedCrossRefGoogle Scholar
  11. Bowerman B, Draper BW, Mello CC, Priess JR (1993) The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74:443–452PubMedCrossRefGoogle Scholar
  12. Bowles J, Feng CW, Spiller C, Davidson TL, Jackson A, Koopman P (2010) FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev Cell 19:440–449PubMedCrossRefGoogle Scholar
  13. Cao Q, Richter JD (2002) Dissolution of the maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J 21:3852–3862PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cao Q, Kim JH, Richter JD (2006) CDK1 and calcineurin regulate Maskin association with eIF4E and translational control of cell cycle progression. Nat Struct Mol Biol 13:1128–1134PubMedCrossRefGoogle Scholar
  15. Cao Q, Padmanabhan K, Richter JD (2010) Pumilio 2 controls translation by competing with eIF4E for 7-methyl guanosine cap recognition. RNA 16:221–227PubMedPubMedCentralCrossRefGoogle Scholar
  16. Carreira-Rosario A, Bhargava V, Hillebrand J, Kollipara RK, Ramaswami M, Buszczak M (2016) Repression of Pumilio protein expression by Rbfox1 promotes germ cell differentiation. Dev Cell 36:562–571PubMedCrossRefGoogle Scholar
  17. Castagnetti S, Ephrussi A (2003) Orb and a long poly(A) tail are required for efficient oskar translation at the posterior pole of the Drosophila oocyte. Development 130:835–843PubMedCrossRefGoogle Scholar
  18. Chang JS, Tan L, Schedl P (1999) The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev Biol 215:91–106PubMedCrossRefGoogle Scholar
  19. Charlesworth A, Meijer HA, de Moor CH (2013) Specificity factors in cytoplasmic polyadenylation. Wiley Interdiscip Rev RNA 4:437–461PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chekulaeva M, Hentze MW, Ephrussi A (2006) Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles. Cell 124:521–533PubMedCrossRefGoogle Scholar
  21. Chen D, McKearin D (2003) Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol 13:1786–1791PubMedCrossRefGoogle Scholar
  22. Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P (2007) Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev Cell 13:691–704PubMedCrossRefGoogle Scholar
  23. Ciosk R, DePalma M, Priess JR (2006) Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science 311:851–853PubMedCrossRefGoogle Scholar
  24. Copeland PR, Wormington M (2001) The mechanism and regulation of deadenylation: identification and characterization of Xenopus PARN. RNA 7:875–886PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cragle C, MacNicol AM (2014) Musashi protein-directed translational activation of target mRNAs is mediated by the poly(A) polymerase, germ line development defective-2. J Biol Chem 289:14239–14251PubMedPubMedCentralCrossRefGoogle Scholar
  26. Crist CG, Montarras D, Buckingham M (2012) Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11:118–126PubMedCrossRefGoogle Scholar
  27. Crittenden SL, Troemel ER, Evans TC, Kimble J (1994) GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120:2901–2911PubMedGoogle Scholar
  28. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J (2002) A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417:660–663PubMedCrossRefGoogle Scholar
  29. Dahanukar A, Walker JA, Wharton RP (1999) Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol Cell 4:209–218PubMedCrossRefGoogle Scholar
  30. Detwiler MR, Reuben M, Li X, Rogers E, Lin R (2001) Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev Cell 1:187–199PubMedCrossRefGoogle Scholar
  31. Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR (1996) MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87:205–216PubMedCrossRefGoogle Scholar
  32. Eckmann CR, Kraemer B, Wickens M, Kimble J (2002) GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev Cell 3:697–710PubMedCrossRefGoogle Scholar
  33. Eckmann CR, Crittenden SL, Suh N, Kimble J (2004) GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168:147–160PubMedPubMedCentralCrossRefGoogle Scholar
  34. Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884PubMedCrossRefGoogle Scholar
  35. Forbes A, Lehmann R (1998) Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125:679–690PubMedGoogle Scholar
  36. Forrest KM, Gavis ER (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13:1159–1168PubMedCrossRefGoogle Scholar
  37. Fox PM, Vought VE, Hanazawa M, Lee MH, Maine EM, Schedl T (2011) Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline. Development 138:2223–2234PubMedPubMedCentralCrossRefGoogle Scholar
  38. Francis R, Barton MK, Kimble J, Schedl T (1995) gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139:579–606PubMedPubMedCentralGoogle Scholar
  39. Frise E, Hammonds AS, Celniker SE (2010) Systematic image-driven analysis of the spatial Drosophila embryonic expression landscape. Mol Syst Biol 6:345PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gallo CM, Wang JT, Motegi F, Seydoux G (2010) Cytoplasmic partitioning of P granule components is not required to specify the germline in C. elegans. Science 330:1685–1689PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gilboa L, Lehmann R (2004) How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males. Development 131:4895–4905PubMedCrossRefGoogle Scholar
  42. Govindan JA, Nadarajan S, Kim S, Starich TA, Greenstein D (2009) Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in C. elegans. Development 136:2211–2221PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gunkel N, Yano T, Markussen FH, Olsen LC, Ephrussi A (1998) Localization-dependent translation requires a functional interaction between the 5′ and 3′ ends of oskar mRNA. Genes Dev 12:1652–1664PubMedPubMedCentralCrossRefGoogle Scholar
  44. Guven-Ozkan T, Robertson SM, Nishi Y, Lin R (2010) zif-1 translational repression defines a second, mutually exclusive OMA function in germline transcriptional repression. Development 137:3373–3382PubMedPubMedCentralCrossRefGoogle Scholar
  45. Haccard O, Jessus C (2006) Redundant pathways for Cdc2 activation in Xenopus oocyte: either cyclin B or Mos synthesis. EMBO Rep 7:321–325PubMedCrossRefGoogle Scholar
  46. Hansen D, Wilson-Berry L, Dang T, Schedl T (2004) Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131:93–104PubMedCrossRefGoogle Scholar
  47. Hanyu-Nakamura K, Sonobe-Nojima H, Tanigawa A, Lasko P, Nakamura A (2008) Drosophila Pgc protein inhibits P-TEFb recruitment to chromatin in primordial germ cells. Nature 451:730–733PubMedPubMedCentralCrossRefGoogle Scholar
  48. Harris AN, Macdonald PM (2001) Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128:2823–2832PubMedGoogle Scholar
  49. Harris JE, Govindan JA, Yamamoto I, Schwartz J, Kaverina I, Greenstein D (2006) Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans. Dev Biol 299:105–121PubMedCrossRefGoogle Scholar
  50. Harris RE, Pargett M, Sutcliffe C, Umulis D, Ashe HL (2011) Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev Cell 20:72–83PubMedPubMedCentralCrossRefGoogle Scholar
  51. Henderson ST, Gao D, Lambie EJ, Kimble J (1994) lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120:2913–2924PubMedGoogle Scholar
  52. Hubstenberger A, Cameron C, Shtofman R, Gutman S, Evans TC (2012) A network of PUF proteins and Ras signaling promote mRNA repression and oogenesis in C. elegans. Dev Biol 366:218–231PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hunter CP, Kenyon C (1996) Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87:217–226PubMedCrossRefGoogle Scholar
  54. Jadhav S, Rana M, Subramaniam K (2008) Multiple maternal proteins coordinate to restrict the translation of C. elegans nanos-2 to primordial germ cells. Development 135:1803–1812PubMedPubMedCentralCrossRefGoogle Scholar
  55. Jambor H, Mueller S, Bullock SL, Ephrussi A (2014) A stem-loop structure directs oskar mRNA to microtubule minus ends. RNA 20:429–439PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jan E, Motzny CK, Graves LE, Goodwin EB (1999) The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J 18:258–269PubMedPubMedCentralCrossRefGoogle Scholar
  57. Jeong J, Verheyden JM, Kimble J (2011) Cyclin E and Cdk2 control GLD-1, the mitosis/meiosis decision, and germline stem cells in Caenorhabditis elegans. PLoS Genet 7:e1001348PubMedPubMedCentralCrossRefGoogle Scholar
  58. Joly W, Chartier A, Rojas-Rios P, Busseau I, Simonelig M (2013) The CCR4 deadenylase acts with Nanos and Pumilio in the fine-tuning of Mei-P26 expression to promote germline stem cell self-renewal. Stem Cell Rep 1:411–424CrossRefGoogle Scholar
  59. Kadyk LC, Kimble J (1998) Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125:1803–1813PubMedGoogle Scholar
  60. Kadyrova LY, Habara Y, Lee TH, Wharton RP (2007) Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. Development 134:1519–1527PubMedCrossRefGoogle Scholar
  61. Kalchhauser I, Farley BM, Pauli S, Ryder SP, Ciosk R (2011) FBF represses the Cip/Kip cell-cycle inhibitor CKI-2 to promote self-renewal of germline stem cells in C. elegans. EMBO J 30:3823–3829PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kalifa Y, Huang T, Rosen LN, Chatterjee S, Gavis ER (2006) Glorund, a Drosophila hnRNP F/H homolog, is an ovarian repressor of nanos translation. Dev Cell 10:291–301PubMedCrossRefGoogle Scholar
  63. Karaiskou A, Jessus C, Brassac T, Ozon R (1999) Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF auto-amplification. J Cell Sci 112(Pt 21):3747–3756PubMedGoogle Scholar
  64. Kaymak E, Ryder SP (2013) RNA recognition by the Caenorhabditis elegans oocyte maturation determinant OMA-1. J Biol Chem 288:30463–30472PubMedPubMedCentralCrossRefGoogle Scholar
  65. Keady BT, Kuo P, Martinez SE, Yuan L, Hake LE (2007) MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. J Cell Sci 120:1093–1103PubMedCrossRefGoogle Scholar
  66. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Orom UA et al (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131:1273–1286PubMedCrossRefGoogle Scholar
  67. Kim JH, Richter JD (2006) Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol Cell 24:173–183PubMedCrossRefGoogle Scholar
  68. Kim JH, Richter JD (2007) RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev 21:2571–2579PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kim KW, Wilson TL, Kimble J (2010) GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proc Natl Acad Sci USA 107:17445–17450PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kimble J (2011) Molecular regulation of the mitosis/meiosis decision in multicellular organisms. Cold Spring Harb Perspect Biol 3:a002683PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kim-Ha J, Smith JL, Macdonald PM (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66:23–35PubMedCrossRefGoogle Scholar
  72. Koprunner M, Thisse C, Thisse B, Raz E (2001) A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev 15:2877–2885PubMedPubMedCentralGoogle Scholar
  73. Korner CG, Wormington M, Muckenthaler M, Schneider S, Dehlin E, Wahle E (1998) The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J 17:5427–5437PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kugler JM, Lasko P (2009) Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly (Austin) 3:15–28CrossRefGoogle Scholar
  75. Lamont LB, Crittenden SL, Bernstein D, Wickens M, Kimble J (2004) FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev Cell 7:697–707PubMedCrossRefGoogle Scholar
  76. Leatherman JL, Levin L, Boero J, Jongens TA (2002) Germ cell-less acts to repress transcription during the establishment of the Drosophila germ cell lineage. Curr Biol 12:1681–1685PubMedCrossRefGoogle Scholar
  77. Lee MH, Schedl T (2001) Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev 15:2408–2420PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lehmann R (2012) Germline stem cells: origin and destiny. Cell Stem Cell 10:729–739PubMedPubMedCentralCrossRefGoogle Scholar
  79. Li Y, Minor NT, Park JK, McKearin DM, Maines JZ (2009) Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance. Proc Natl Acad Sci USA 106:9304–9309PubMedPubMedCentralCrossRefGoogle Scholar
  80. Li Y, Zhang Q, Carreira-Rosario A, Maines JZ, McKearin DM, Buszczak M (2013) Mei-p26 cooperates with Bam, Bgcn and Sxl to promote early germline development in the Drosophila ovary. PLoS One 8:e58301PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lin CL, Evans V, Shen S, Xing Y, Richter JD (2010) The nuclear experience of CPEB: implications for RNA processing and translational control. RNA 16:338–348PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lublin AL, Evans TC (2007) The RNA-binding proteins PUF-5, PUF-6, and PUF-7 reveal multiple systems for maternal mRNA regulation during C. elegans oogenesis. Dev Biol 303:635–649PubMedCrossRefGoogle Scholar
  83. Maduro MF, Meneghini MD, Bowerman B, Broitman-Maduro G, Rothman JH (2001) Restriction of mesendoderm to a single blastomere by the combined action of SKN-1 and a GSK-3beta homolog is mediated by MED-1 and -2 in C. elegans. Mol Cell 7:475–485PubMedCrossRefGoogle Scholar
  84. Mahowald AP (2001) Assembly of the Drosophila germ plasm. Int Rev Cytol 203:187–213PubMedCrossRefGoogle Scholar
  85. Marin VA, Evans TC (2003) Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130:2623–2632PubMedCrossRefGoogle Scholar
  86. Markussen FH, Michon AM, Breitwieser W, Ephrussi A (1995) Translational control of oskar generates short OSK, the isoform that induces pole plasma assembly. Development 121:3723–3732PubMedGoogle Scholar
  87. Markussen FH, Breitwieser W, Ephrussi A (1997) Efficient translation and phosphorylation of Oskar require Oskar protein and the RNA helicase Vasa. Cold Spring Harb Symp Quant Biol 62:13–17PubMedCrossRefGoogle Scholar
  88. McLaren A (1999) Signaling for germ cells. Genes Dev 13:373–376PubMedCrossRefGoogle Scholar
  89. Mello CC, Draper BW, Krause M, Weintraub H, Priess JR (1992) The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos. Cell 70:163–176PubMedCrossRefGoogle Scholar
  90. Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR (1996) The PIE-1 protein and germline specification in C. elegans embryos. Nature 382:710–712PubMedCrossRefGoogle Scholar
  91. Mendez R, Barnard D, Richter JD (2002) Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J 21:1833–1844PubMedPubMedCentralCrossRefGoogle Scholar
  92. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M et al (2000) Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489–1493PubMedCrossRefGoogle Scholar
  93. Merritt C, Seydoux G (2010) The Puf RNA-binding proteins FBF-1 and FBF-2 inhibit the expression of synaptonemal complex proteins in germline stem cells. Development 137:1787–1798PubMedPubMedCentralCrossRefGoogle Scholar
  94. Merritt C, Rasoloson D, Ko D, Seydoux G (2008) 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18:1476–1482PubMedPubMedCentralCrossRefGoogle Scholar
  95. Micklem DR, Adams J, Grunert S, St Johnston D (2000) Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J 19:1366–1377PubMedPubMedCentralCrossRefGoogle Scholar
  96. Millonigg S, Minasaki R, Nousch M, Eckmann CR (2014) GLD-4-mediated translational activation regulates the size of the proliferative germ cell pool in the adult C. elegans germ line. PLoS Genet 10:e1004647Google Scholar
  97. Mishima Y, Giraldez AJ, Takeda Y, Fujiwara T, Sakamoto H, Schier AF, Inoue K (2006) Differential regulation of germline mRNAs in soma and germ cells by zebrafish miR-430. Curr Biol 16:2135–2142PubMedPubMedCentralCrossRefGoogle Scholar
  98. Mootz D, Ho DM, Hunter CP (2004) The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1. Development 131:3263–3272PubMedCrossRefGoogle Scholar
  99. Nakamura A, Sato K, Hanyu-Nakamura K (2004) Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev Cell 6:69–78PubMedCrossRefGoogle Scholar
  100. Nelson MR, Leidal AM, Smibert CA (2004) Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. EMBO J 23:150–159PubMedCrossRefGoogle Scholar
  101. Newton FG, Harris RE, Sutcliffe C, Ashe HL (2015) Coordinate post-transcriptional repression of Dpp-dependent transcription factors attenuates signal range during development. Development 142:3362–3373PubMedPubMedCentralCrossRefGoogle Scholar
  102. Nie K, Gomez M, Landgraf P, Garcia JF, Liu Y, Tan LH, Chadburn A, Tuschl T, Knowles DM, Tam W (2008) MicroRNA-mediated down-regulation of PRDM1/Blimp-1 in Hodgkin/Reed-Sternberg cells: a potential pathogenetic lesion in Hodgkin lymphomas. Am J Pathol 173:242–252PubMedPubMedCentralCrossRefGoogle Scholar
  103. Ogura K, Kishimoto N, Mitani S, Gengyo-Ando K, Kohara Y (2003) Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans. Development 130:2495–2503PubMedCrossRefGoogle Scholar
  104. Oldenbroek M, Robertson SM, Guven-Ozkan T, Spike C, Greenstein D, Lin R (2013) Regulation of maternal Wnt mRNA translation in C. elegans embryos. Development 140:4614–4623PubMedPubMedCentralCrossRefGoogle Scholar
  105. Olivieri G, Olivieri A (1965) Autoradiographic study of nucleic acid synthesis during spermatogenesis in Drosophila melanogaster. Mutat Res 2:366–380PubMedCrossRefGoogle Scholar
  106. Padmanabhan K, Richter JD (2006) Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev 20:199–209PubMedPubMedCentralCrossRefGoogle Scholar
  107. Pagano JM, Farley BM, Essien KI, Ryder SP (2009) RNA recognition by the embryonic cell fate determinant and germline totipotency factor MEX-3. Proc Natl Acad Sci USA 106:20252–20257PubMedPubMedCentralCrossRefGoogle Scholar
  108. Posada J, Yew N, Ahn NG, Vande Woude GF, Cooper JA (1993) Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol Cell Biol 13:2546–2553PubMedPubMedCentralCrossRefGoogle Scholar
  109. Priti A, Subramaniam K (2015) PUF-8 functions redundantly with GLD-1 to promote the meiotic progression of spermatocytes in Caenorhabditis elegans. G3 (Bethesda)Google Scholar
  110. Rongo C, Gavis ER, Lehmann R (1995) Localization of oskar RNA regulates oskar translation and requires Oskar protein. Development 121:2737–2746PubMedGoogle Scholar
  111. Saffman EE, Styhler S, Rother K, Li W, Richard S, Lasko P (1998) Premature translation of oskar in oocytes lacking the RNA-binding protein bicaudal-C. Mol Cell Biol 18:4855–4862PubMedPubMedCentralCrossRefGoogle Scholar
  112. Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF (1988) Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335:519–525PubMedCrossRefGoogle Scholar
  113. Sassone-Corsi P (2002) Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296:2176–2178PubMedCrossRefGoogle Scholar
  114. Schafer M, Nayernia K, Engel W, Schafer U (1995) Translational control in spermatogenesis. Dev Biol 172:344–352PubMedCrossRefGoogle Scholar
  115. Schmid M, Kuchler B, Eckmann CR (2009) Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev 23:824–836PubMedPubMedCentralCrossRefGoogle Scholar
  116. Schumacher B, Hanazawa M, Lee MH, Nayak S, Volkmann K, Hofmann ER, Hengartner M, Schedl T, Gartner A (2005) Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 120:357–368PubMedCrossRefGoogle Scholar
  117. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, Smibert CA (2005) Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol 15:284–294PubMedCrossRefGoogle Scholar
  118. Seydoux G, Dunn MA (1997) Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 124:2191–2201PubMedGoogle Scholar
  119. Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A (1996) Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 382:713–716PubMedCrossRefGoogle Scholar
  120. Slaidina M, Lehmann R (2014) Translational control in germline stem cell development. J Cell Biol 207:13–21PubMedPubMedCentralCrossRefGoogle Scholar
  121. Smibert CA, Wilson JE, Kerr K, Macdonald PM (1996) smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev 10:2600–2609PubMedCrossRefGoogle Scholar
  122. Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, Xie T (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131:1353–1364PubMedCrossRefGoogle Scholar
  123. Spike CA, Coetzee D, Eichten C, Wang X, Hansen D, Greenstein D (2014a) The TRIM-NHL protein LIN-41 and the OMA RNA-binding proteins antagonistically control the prophase-to-metaphase transition and growth of Caenorhabditis elegans oocytes. Genetics 198:1535–1558PubMedPubMedCentralCrossRefGoogle Scholar
  124. Spike CA, Coetzee D, Nishi Y, Guven-Ozkan T, Oldenbroek M, Yamamoto I, Lin R, Greenstein D (2014b) Translational control of the oogenic program by components of OMA ribonucleoprotein particles in Caenorhabditis elegans. Genetics 198:1513–1533PubMedPubMedCentralCrossRefGoogle Scholar
  125. Strome S, Wood WB (1982) Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc Natl Acad Sci USA 79:1558–1562PubMedPubMedCentralCrossRefGoogle Scholar
  126. Subramaniam K, Seydoux G (1999) nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 126:4861–4871PubMedGoogle Scholar
  127. Suh N, Jedamzik B, Eckmann CR, Wickens M, Kimble J (2006) The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc Natl Acad Sci USA 103:15108–15112PubMedPubMedCentralCrossRefGoogle Scholar
  128. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119PubMedCrossRefGoogle Scholar
  129. Suzuki A, Saba R, Miyoshi K, Morita Y, Saga Y (2012) Interaction between NANOS2 and the CCR4-NOT deadenylation complex is essential for male germ cell development in mouse. PLoS One 7:e33558PubMedPubMedCentralCrossRefGoogle Scholar
  130. Suzuki A, Niimi Y, Shinmyozu K, Zhou Z, Kiso M, Saga Y (2016) Dead end1 is an essential partner of NANOS2 for selective binding of target RNAs in male germ cell development. EMBO Rep 17:37–46PubMedCrossRefGoogle Scholar
  131. Tabara H, Hill RJ, Mello CC, Priess JR, Kohara Y (1999) pos-1 encodes a cytoplasmic zinc-finger protein essential for germline specification in C. elegans. Development 126:1–11PubMedGoogle Scholar
  132. Tenenhaus C, Subramaniam K, Dunn MA, Seydoux G (2001) PIE-1 is a bifunctional protein that regulates maternal and zygotic gene expression in the embryonic germ line of Caenorhabditis elegans. Genes Dev 15:1031–1040PubMedPubMedCentralCrossRefGoogle Scholar
  133. Trcek T, Grosch M, York A, Shroff H, Lionnet T, Lehmann R (2015) Drosophila germ granules are structured and contain homotypic mRNA clusters. Nat Commun 6:7962PubMedPubMedCentralCrossRefGoogle Scholar
  134. Vaid S, Ariz M, Chaturbedi A, Kumar GA, Subramaniam K (2013) PUF-8 negatively regulates RAS/MAPK signalling to promote differentiation of C. elegans germ cells. Development 140:1645–1654PubMedPubMedCentralCrossRefGoogle Scholar
  135. Vourekas A, Alexiou P, Vrettos N, Maragkakis M, Mourelatos Z (2016) Sequence-dependent but not sequence-specific piRNA adhesion traps mRNAs to the germ plasm. Nature 531:390–394PubMedPubMedCentralCrossRefGoogle Scholar
  136. Walker AK, Boag PR, Blackwell TK (2007) Transcription reactivation steps stimulated by oocyte maturation in C. elegans. Dev Biol 304:382–393PubMedCrossRefGoogle Scholar
  137. Wang L, Eckmann CR, Kadyk LC, Wickens M, Kimble J (2002) A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419:312–316PubMedCrossRefGoogle Scholar
  138. Weidinger G, Stebler J, Slanchev K, Dumstrei K, Wise C, Lovell-Badge R, Thisse C, Thisse B, Raz E (2003) dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 13:1429–1434PubMedCrossRefGoogle Scholar
  139. West JA, Viswanathan SR, Yabuuchi A, Cunniff K, Takeuchi A, Park IH, Sero JE, Zhu H, Perez-Atayde A, Frazier AL et al (2009) A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460:909–913PubMedPubMedCentralGoogle Scholar
  140. Wharton KA, Thomsen GH, Gelbart WM (1991) Drosophila 60A gene, another transforming growth factor beta family member, is closely related to human bone morphogenetic proteins. Proc Natl Acad Sci USA 88:9214–9218PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wilson JE, Connell JE, Macdonald PM (1996) aubergine enhances oskar translation in the Drosophila ovary. Development 122:1631–1639PubMedGoogle Scholar
  142. Xie T, Spradling AC (1998) decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94:251–260PubMedCrossRefGoogle Scholar
  143. Yochem J, Greenwald I (1989) glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell 58:553–563PubMedCrossRefGoogle Scholar
  144. Youngren KK, Coveney D, Peng X, Bhattacharya C, Schmidt LS, Nickerson ML, Lamb BT, Deng JM, Behringer RR, Capel B et al (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435:360–364PubMedPubMedCentralCrossRefGoogle Scholar
  145. Zaessinger S, Busseau I, Simonelig M (2006) Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 133:4573–4583PubMedCrossRefGoogle Scholar
  146. Zhang F, Barboric M, Blackwell TK, Peterlin BM (2003) A model of repression: CTD analogs and PIE-1 inhibit transcriptional elongation by P-TEFb. Genes Dev 17:748–758PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zhou Z, Shirakawa T, Ohbo K, Sada A, Wu Q, Hasegawa K, Saba R, Saga Y (2015) RNA binding protein Nanos2 organizes post-transcriptional Buffering system to retain primitive state of mouse spermatogonial stem cells. Dev Cell 34:96–107PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Kumari Pushpa
    • 1
  • Ganga Anil Kumar
    • 2
    • 3
  • Kuppuswamy Subramaniam
    • 3
  1. 1.Regional Centre for BiotechnologyFaridabadIndia
  2. 2.Indian Institute of Technology-KanpurKanpurIndia
  3. 3.Indian Institute of Technology-MadrasChennaiIndia

Personalised recommendations