Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-23T13:34:37.082Z Has data issue: false hasContentIssue false
  • English
  • Français

Pumilio1 phosphorylation precedes translational activation of its target mRNA in zebrafish oocytes

Published online by Cambridge University Press:  05 October 2018

Atsushi Saitoh ,
Yuki Takada ,
Mayu Horie  and
Tomoya Kotani Open the ORCID record for Tomoya Kotani [Opens in a new window]
Atsushi Saitoh
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan
Yuki Takada
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan
Mayu Horie
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan
Tomoya Kotani*
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan.
*
*Author for correspondence: T Kotani. Department of Biological Sciences, Faculty of Science, Hokkaido University, North 10 West 8, Sapporo, Hokkaido 060-0810, Japan. Tel/Fax: +81 11 7064455. E-mail: tkotani@sci.hokudai.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

Translational regulation of mRNAs is crucial for promoting various cellular and developmental processes. Pumilio1 (Pum1) has been shown to play key roles in translational regulation of target mRNAs in many systems of diverse organisms. In zebrafish immature oocytes, Pum1 was shown to bind to cyclin B1 mRNA and promote the formation of cyclin B1 RNA granules. This Pum1-mediated RNA granule formation seemed critical to determine the timing of translational activation of cyclin B1 mRNA during oocyte maturation, leading to activation of maturation/M-phase-promoting factor (MPF) at the appropriate timing. Despite its fundamental importance, the mechanisms of translational regulation by Pum1 remain elusive. In this study, we examined the phosphorylation of Pum1 as a first step to understand the mechanisms of Pum1-mediated translation. SDS-PAGE analyses and phosphatase treatments showed that Pum1 was phosphorylated at multiple sites during oocyte maturation. This phosphorylation began in an early period after induction of oocyte maturation, which preceded the polyadenylation of cyclin B1 mRNA. Interestingly, depolymerization of actin filaments in immature oocytes caused phosphorylation of Pum1, disassembly of cyclin B1 RNA granules, and polyadenylation of cyclin B1 mRNA but not translational activation of the mRNA. Overexpression of the Pum1 N-terminus prevented the phosphorylation of Pum1, disassembly of cyclin B1 RNA granules, and translational activation of the mRNA even after induction of oocyte maturation. These results suggest that Pum1 phosphorylation in the early period of oocyte maturation is one of the key processes for promoting the disassembly of cyclin B1 RNA granules and translational activation of target mRNA.

Keywords

Cytoplasmic polyadenylationOocyte maturationRNA granuleTranslationVertebrate
Type
Research Article
Information
Zygote , Volume 26 , Issue 5 , October 2018 , pp. 372 - 380
Copyright
© Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asaoka-Taguchi, M, Yamada, M, Nakamura, A, Hanyu, K Kobayashi, S (1999) Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1, 431–437.Google Scholar
Barik, S (1993) Expression and biochemical properties of a protein serine/threonine phosphatase encoded by bacteriophage lambda. Proc Natl Acad Sci USA 90, 10633–10637.Google Scholar
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, 3852–3862.Google Scholar
Charlesworth, A, Cox, LL MacNicol, AM (2004) Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in Xenopus oocytes. J Biol Chem 279, 17650–176509.Google Scholar
Chen, D, Zheng, W, Lin, A, Uyhazi, K, Zhao, H Lin, H (2012) Pumilio 1 suppresses multiple activators of p53 to safeguard spermatogenesis. Curr Biol 22, 420–425.Google Scholar
Chen, J, Melton, C, Suh, N, Oh, JS, Horner, K, Xie, F, Sette, C, Blelloch, R Conti, M (2011) Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev 25, 755–766.Google Scholar
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, 660–663.Google Scholar
de Moor, CH Richter, JD (1999) Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J 18, 2294–2303.Google Scholar
Forbes, A Lehmann, R (1998) Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125, 679–690.Google Scholar
Gennarino, VA, Singh, RK, White, JJ, De Maio, A, Han, K, Kim, JY, Jafar-Nejad, P, di Ronza, A, Kang, H, Sayegh, LS, Cooper, TA, Orr, HT, Sillitoe, RV Zoghbi, HY (2015) Pumilio1 haploinsufficiency leads to SCA1-like neurodegeneration by increasing wild-type Ataxin1 levels. Cell 160, 1087–1098.Google Scholar
Hake, LE Richter, JD (1994) CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79, 617–627.Google Scholar
Han, SJ, Martins, JPS, Yang, Y, Kang, MK, Daldello, EM Conti, M (2017) The Translation of cyclin B1 and B2 is differentially regulated during mouse oocyte reentry into the meiotic cell cycle. Sci Rep 7, 14077.Google Scholar
Harvey, SA, Sealy, I, Kettleborough, R, Fenyes, F, White, R, Stemple, D Smith, JC (2013) Identification of the zebrafish maternal and paternal transcriptomes. Development 140, 2703–2710.Google Scholar
Horie, M Kotani, T (2016) Formation of mos RNA granules in the zebrafish oocyte that differ from cyclin B1 RNA granules in distribution, density and regulation. Eur J Cell Biol 95, 563–573.Google Scholar
Katsu, Y, Yamashita, M, Kajiura, H Nagahama, Y (1993) Behavior of the components of maturation-promoting factor, cdc2 kinase and cyclin B, during oocyte maturation of goldfish. Dev Biol 160, 99–107.Google Scholar
Kloc, M, Zearfoss, NR Etkin, LD (2002) Mechanisms of subcellular mRNA localization. Cell 108, 533–544.Google Scholar
Komrskova, P, Susor, A, Malik, R, Prochazkova, B, Liskova, L, Supolikova, J, Hladky, S Kubelka, M (2014) Aurora kinase A is not involved in CPEB1 phosphorylation and cyclin B1 mRNA polyadenylation during meiotic maturation of porcine oocytes. PLoS One 9, 7.Google Scholar
Kotani, T, Maehata, K Takei, N (2017) Regulation of translationally repressed mRNAs in zebrafish and mouse oocytes. Results Probl Cell Differ 63, 297–324.Google Scholar
Kotani, T, Yasuda, K, Ota, R Yamashita, M (2013) Cyclin B1 mRNA translation is temporally controlled through formation and disassembly of RNA granules. J Cell Biol 202, 1041–1055.Google Scholar
Kurisaki, I, Iwai, T, Yamashita, M, Kobayashi, M, Ito, E Matsuoka, I (2007) Identification and expression analysis of rainbow trout pumilio-1 and pumilio-2. Cell Tissue Res 327, 33–42.Google Scholar
Lee, JY, Lim, JM, Kim, DK, Zheng, YH, Moon, S, Han, BK, Song, KD, Kim, H Han, JY (2008) Identification and gene expression profiling of the Pum1 and Pum2 members of the Pumilio family in the chicken. Mol Reprod Dev 75, 184–190.Google Scholar
Lehmann, R Nussleinvolhard, C (1987) Involvement of the Pumilio gene in the transport of an abdominal signal in the Drosophila embryo. Nature 329, 167–170.Google Scholar
Lin, H Spradling, AC (1997) A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124, 2463–2476.Google Scholar
Mak, W, Fang, C, Holden, T, Dratver, MB Lin, H (2016) An important role of Pumilio 1 in regulating the development of the mammalian female germline. Biol Reprod 94, 134.Google Scholar
Martin, KC Ephrussi, A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136, 719–730.Google Scholar
Masui, Y Clarke, HJ (1979) Oocyte maturation. Int Rev Cytol 57, 185–282.Google Scholar
McGrew, LL, Dworkin-Rastl, E, Dworkin, MB Richter, JD (1989) Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev 3, 803–815.Google Scholar
Mendez, R, Barnard, D Richter, JD (2002) Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J 21, 1833–1844.Google Scholar
Murata, Y Wharton, RP (1995) Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80, 747–756.Google Scholar
Nakahata, S, Katsu, Y, Mita, K, Inoue, K, Nagahama, Y Yamashita, M (2001) Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J Biol Chem 276, 20945–20953.Google Scholar
Nakahata, S, Kotani, T, Mita, K, Kawasaki, T, Katsu, Y, Nagahama, Y Yamashita, M (2003) Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech Dev 120, 865–880.Google Scholar
Nukada, Y, Horie, M, Fukui, A, Kotani, T Yamashita, M (2015) Real-time imaging of actin filaments in the zebrafish oocyte and embryo. Cytoskeleton 72, 491–501.Google Scholar
Ota, R, Kotani, T Yamashita, M (2011a) Biochemical characterization of Pumilio1 and Pumilio2 in Xenopus oocytes. J Biol Chem 286, 2853–2863.Google Scholar
Ota, R, Kotani, T Yamashita, M (2011b) Possible involvement of Nemo-like kinase 1 in Xenopus oocyte maturation as a kinase responsible for Pumilio1, Pumilio2, and CPEB phosphorylation. Biochemistry 50, 5648–5659.Google Scholar
Padmanabhan, K Richter, JD (2006) Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev 20, 199–209.Google Scholar
Pique, M, Lopez, JM, Foissac, S, Guigo, R Mendez, R (2008) A combinatorial code for CPE-mediated translational control. Cell 132, 434–448.Google Scholar
Radford, HE, Meijer, HA de Moor, CH (2008) Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim Biophys Acta 1779, 217–229.Google Scholar
Salazar, AM, Silverman, EJ, Menon, KP Zinn, K (2010) Regulation of synaptic Pumilio function by an aggregation-prone domain. J Neurosci 30, 515–522.Google Scholar
Sheets, MD, Fox, CA, Hunt, T, Van de Woude, G Wickens, M (1994) The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev 8, 926–938.Google Scholar
Spassov, DS Jurecic, R (2002) Cloning and comparative sequence analysis of PUM1 and PUM2 genes, human members of the Pumilio family of RNA-binding proteins. Gene 299, 195–204.Google Scholar
Spassov, DS Jurecic, R (2003a) Mouse Pum1 and Pum2 genes, members of the Pumilio family of RNA-binding proteins, show differential expression in fetal and adult hematopoietic stem cells and progenitors. Blood Cells Mol Dis 30, 55–69.Google Scholar
Spassov, DS Jurecic, R (2003b) The PUF family of RNA-binding proteins: does evolutionarily conserved structure equal conserved function? IUBMB Life 55, 359–366.Google Scholar
Stutz, A, Conne, B, Huarte, J, Gubler, P, Volkel, V, Flandin, P Vassalli, JD (1998) Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes. Genes Dev 12, 2535–2548.Google Scholar
Takahashi, K, Kotani, T, Katsu, Y Yamashita, M (2014) Possible involvement of insulin-like growth factor 2 mRNA-binding protein 3 in zebrafish oocyte maturation as a novel cyclin B1 mRNA-binding protein that represses the translation in immature oocytes. Biochem Biophys Res Commun 448, 22–27.Google Scholar
Takei, N, Nakamura, T, Kawamura, S, Takada, Y, Satoh, Y, Kimura, AP Kotani, T (2018) High-sensitivity and high-resolution in situ hybridization of coding and long non-coding RNAs in vertebrate ovaries and testes. Biol Proceed Online 20, 6.Google Scholar
Tanaka, T Yamashita, M (1995) Pre-MPF is absent in immature oocytes of fishes and amphibians except Xenopus . Dev Growth Differ 37, 387–393.Google Scholar
Tay, J, Hodgman, R Richter, JD (2000) The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol 221, 1–9.Google Scholar
Vassalli, JD, Huarte, J, Belin, D, Gubler, P, Vassalli, A, O’Connell, ML, Parton, LA, Rickles, RJ Strickland, S (1989) Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev 3, 2163–2171.Google Scholar
Weill, L, Belloc, E, Bava, FA Mendez, R (2012) Translational control by changes in poly(A) tail length: recycling mRNAs. Nat Struct Mol Biol 19, 577–585.Google Scholar
White, EK, Moore-Jarrett, T Ruley, HE (2001) PUM2, a novel murine PUF protein, and its consensus RNA-binding site. RNA 7, 1855–1866.Google Scholar
Wickens, M, Bernstein, DS, Kimble, J Parker, R (2002) A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet 18, 150–157.Google Scholar
Yasuda, K, Kotani, T, Ota, R Yamashita, M (2010) Transgenic zebrafish reveals novel mechanisms of translational control of cyclin B1 mRNA in oocytes. Dev Biol 348, 76–86.Google Scholar
Zamore, PD, Williamson, JR Lehmann, R (1997) The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 3, 1421–1433.Google Scholar
Zhang, B, Gallegos, M, Puoti, A, Durkin, E, Fields, S, Kimble, J Wickens, MP (1997) A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390, 477–1384.Google Scholar
Zhang, M, Chen, D, Xia, J, Han, W, Cui, X, Neuenkirchen, N, Hermes, G, Sestan, N Lin, H (2017) Post-transcriptional regulation of mouse neurogenesis by Pumilio proteins. Genes Dev 31, 1–16.Google Scholar