Translational control of nanos mRNA by Smaug protein in Drosophila melanogaster[1][2]

Smaug is a RNA-binding protein in Drosophila that helps in maternal to zygotic transition (MZT).[3][4] The protein is named after the fictional character Smaug, the dragon in J.R.R. Tolkien's 1937 novel The Hobbit.[5] The MZT ends with the midblastula transition (MBT), which is defined as the first developmental event in Drosophila that depends on zygotic mRNA.[6] In Drosophila, the initial developmental events are controlled by maternal mRNAs like Hsp83, nanos, string, Pgc, and cyclin B mRNA.[7][8][9][1][10] Degradation of these mRNAs, which is expected to terminate maternal control and enable zygotic control of embryogenesis, happens at interphase of nuclear division cycle 14.[5][11] During this transition smaug protein targets the maternal mRNA for destruction using miRs. Thus activating the zygotic genes. Smaug is expected to play a role in expression of three miRNAs – miR-3, miR-6, miR-309 and miR-286 during MZT in Drosophila.[6] Among them smaug dependent expression of miR-309 is needed for destabilization of 410 maternal mRNAs.[12] In smaug mutants almost 85% of maternal mRNA is found to be stable. Smaug also binds to 3′ untranslated region (UTR) elements known as SMG response elements (SREs) on nanos mRNA[13][14] and represses its expression by recruiting a protein called Cup (an eIF4E-binding protein that blocks the binding of eIF4G to eIF4E).[15][16] There after it recruits deadenylation complex CCR4-Not on to the nanos mRNA which leads to deadenylation and subsequent decay of the mRNA.[17] It is also found to be involved in degradation and repression of maternal Hsp83 mRNA by recruiting CCR4/POP2/NOT deadenylase to the mRNA.[1] The human Smaug protein homologs are SAMD4A and SAMD4B.

References

  1. 1 2 3 Semotok, Jennifer L.; Cooperstock, Ramona L.; Pinder, Benjamin D.; Vari, Heli K.; Lipshitz, Howard D.; Smibert, Craig A. (2005-02-22). "Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo". Current Biology. 15 (4): 284–294. doi:10.1016/j.cub.2005.01.048. ISSN 0960-9822. PMID 15723788.
  2. ↑ Vardy, Leah; Orr-Weaver, Terry L. (2007). "Regulating translation of maternal messages: multiple repression mechanisms". Trends in Cell Biology. 17 (11): 547–554. doi:10.1016/j.tcb.2007.09.002. PMID 18029182.
  3. ↑ Schier, Alexander F. (2007-04-20). "The maternal-zygotic transition: death and birth of RNAs". Science. 316 (5823): 406–407. Bibcode:2007Sci...316..406S. doi:10.1126/science.1140693. ISSN 1095-9203. PMID 17446392. S2CID 36999389.
  4. ↑ Tadros, Wael; Westwood, J. Timothy; Lipshitz, Howard D. (June 2007). "The mother-to-child transition". Developmental Cell. 12 (6): 847–849. doi:10.1016/j.devcel.2007.05.009. ISSN 1534-5807. PMID 17543857.
  5. 1 2 Gilbert, Scott F. (2010). Developmental biology (9th ed.). Sunderland, Mass: Sinauer Associates. pp. 205–206. ISBN 9780878933846. OCLC 551199641.
  6. 1 2 Benoit, Beatrice; He, Chun Hua; Zhang, Fan; Votruba, Sarah M.; Tadros, Wael; Westwood, J. Timothy; Smibert, Craig A.; Lipshitz, Howard D.; Theurkauf, William E. (2009-03-15). "An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition". Development. 136 (6): 923–932. doi:10.1242/dev.031815. ISSN 0950-1991. PMC 2727558. PMID 19234062.
  7. ↑ Bashirullah, A.; Halsell, S. R.; Cooperstock, R. L.; Kloc, M.; Karaiskakis, A.; Fisher, W. W.; Fu, W.; Hamilton, J. K.; Etkin, L. D. (1999-05-04). "Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster". The EMBO Journal. 18 (9): 2610–2620. doi:10.1093/emboj/18.9.2610. ISSN 0261-4189. PMC 1171340. PMID 10228172.
  8. ↑ Bashirullah, A.; Cooperstock, R. L.; Lipshitz, H. D. (2001-06-19). "Spatial and temporal control of RNA stability". Proceedings of the National Academy of Sciences of the United States of America. 98 (13): 7025–7028. Bibcode:2001PNAS...98.7025B. doi:10.1073/pnas.111145698. ISSN 0027-8424. PMC 34617. PMID 11416182.
  9. ↑ Edgar, B. A.; Datar, S. A. (1996-08-01). "Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program". Genes & Development. 10 (15): 1966–1977. doi:10.1101/gad.10.15.1966. ISSN 0890-9369. PMID 8756353.
  10. ↑ Tadros, Wael; Houston, Simon A.; Bashirullah, Arash; Cooperstock, Ramona L.; Semotok, Jennifer L.; Reed, Bruce H.; Lipshitz, Howard D. (July 2003). "Regulation of maternal transcript destabilization during egg activation in Drosophila". Genetics. 164 (3): 989–1001. doi:10.1093/genetics/164.3.989. ISSN 0016-6731. PMC 1462612. PMID 12871909.
  11. ↑ Tadros, Wael; Goldman, Aaron L.; Babak, Tomas; Menzies, Fiona; Vardy, Leah; Orr-Weaver, Terry; Hughes, Timothy R.; Westwood, J. Timothy; Smibert, Craig A. (2007). "SMAUG Is a Major Regulator of Maternal mRNA Destabilization in Drosophila and Its Translation Is Activated by the PAN GU Kinase". Developmental Cell. 12 (1): 143–155. doi:10.1016/j.devcel.2006.10.005. PMID 17199047.
  12. ↑ Bushati, Natascha; Stark, Alexander; Brennecke, Julius; Cohen, Stephen M. (2008-04-08). "Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila". Current Biology. 18 (7): 501–506. doi:10.1016/j.cub.2008.02.081. ISSN 0960-9822. PMID 18394895.
  13. ↑ Smibert, C. A.; Lie, Y. S.; Shillinglaw, W.; Henzel, W. J.; Macdonald, P. M. (December 1999). "Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro". RNA. 5 (12): 1535–1547. doi:10.1017/S1355838299991392. ISSN 1355-8382. PMC 1369876. PMID 10606265.
  14. ↑ Dahanukar, A.; Walker, J. A.; Wharton, R. P. (August 1999). "Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila". Molecular Cell. 4 (2): 209–218. doi:10.1016/S1097-2765(00)80368-8. ISSN 1097-2765. PMID 10488336.
  15. ↑ Nelson, Meryl R.; Leidal, Andrew M.; Smibert, Craig A. (2004-01-14). "Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression". The EMBO Journal. 23 (1): 150–159. doi:10.1038/sj.emboj.7600026. ISSN 0261-4189. PMC 1271664. PMID 14685270.
  16. ↑ Nakamura, Akira; Sato, Keiji; Hanyu-Nakamura, Kazuko (January 2004). "Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis". Developmental Cell. 6 (1): 69–78. doi:10.1016/S1534-5807(03)00400-3. ISSN 1534-5807. PMID 14723848.
  17. ↑ Zaessinger, Sophie; Busseau, Isabelle; Simonelig, Martine (November 2006). "Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4". Development. 133 (22): 4573–4583. doi:10.1242/dev.02649. ISSN 0950-1991. PMID 17050620.
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