Literature DB >> 27256879

Nanos-mediated repression of hid protects larval sensory neurons after a global switch in sensitivity to apoptotic signals.

Balpreet Bhogal1, Amara Plaza-Jennings1, Elizabeth R Gavis2.   

Abstract

Dendritic arbor morphology is a key determinant of neuronal function. Once established, dendrite branching patterns must be maintained as the animal develops to ensure receptive field coverage. The translational repressors Nanos (Nos) and Pumilio (Pum) are required to maintain dendrite growth and branching of Drosophila larval class IV dendritic arborization (da) neurons, but their specific regulatory role remains unknown. We show that Nos-Pum-mediated repression of the pro-apoptotic gene head involution defective (hid) is required to maintain a balance of dendritic growth and retraction in class IV da neurons and that upregulation of hid results in decreased branching because of an increase in caspase activity. The temporal requirement for nos correlates with an ecdysone-triggered switch in sensitivity to apoptotic stimuli that occurs during the mid-L3 transition. We find that hid is required during pupariation for caspase-dependent pruning of class IV da neurons and that Nos and Pum delay pruning. Together, these results suggest that Nos and Pum provide a crucial neuroprotective regulatory layer to ensure that neurons behave appropriately in response to developmental cues.
© 2016. Published by The Company of Biologists Ltd.

Entities:  

Keywords:  Caspase; Drosophila; Non-apoptotic function; Nos; da neurons; hid

Mesh:

Substances:

Year:  2016        PMID: 27256879      PMCID: PMC4920170          DOI: 10.1242/dev.132415

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  61 in total

1.  Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons.

Authors:  Darren W Williams; James W Truman
Journal:  Development       Date:  2005-07-20       Impact factor: 6.868

2.  Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM.

Authors:  D Vucic; W J Kaiser; L K Miller
Journal:  Mol Cell Biol       Date:  1998-06       Impact factor: 4.272

3.  RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos.

Authors:  R P Wharton; G Struhl
Journal:  Cell       Date:  1991-11-29       Impact factor: 41.582

4.  Combinatorial use of translational co-factors for cell type-specific regulation during neuronal morphogenesis in Drosophila.

Authors:  Eugenia C Olesnicky; Balpreet Bhogal; Elizabeth R Gavis
Journal:  Dev Biol       Date:  2012-02-25       Impact factor: 3.582

5.  The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis.

Authors:  Rebecca Wilson; Lakshmi Goyal; Mark Ditzel; Anna Zachariou; David A Baker; Julie Agapite; Hermann Steller; Pascal Meier
Journal:  Nat Cell Biol       Date:  2002-06       Impact factor: 28.824

6.  Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons.

Authors:  Wesley B Grueber; Lily Y Jan; Yuh Nung Jan
Journal:  Cell       Date:  2003-03-21       Impact factor: 41.582

7.  Recognition and long-range interactions of a minimal nanos RNA localization signal element.

Authors:  S E Bergsten; T Huang; S Chatterjee; E R Gavis
Journal:  Development       Date:  2001-02       Impact factor: 6.868

8.  Expression of baculovirus P35 prevents cell death in Drosophila.

Authors:  B A Hay; T Wolff; G M Rubin
Journal:  Development       Date:  1994-08       Impact factor: 6.868

9.  Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes.

Authors:  Michele Markstein; Chrysoula Pitsouli; Christians Villalta; Susan E Celniker; Norbert Perrimon
Journal:  Nat Genet       Date:  2008-03-02       Impact factor: 38.330

10.  Tiling of the Drosophila epidermis by multidendritic sensory neurons.

Authors:  Wesley B Grueber; Lily Y Jan; Yuh Nung Jan
Journal:  Development       Date:  2002-06       Impact factor: 6.868

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  11 in total

1.  Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons.

Authors:  Conrad M Tenenbaum; Mala Misra; Rebecca A Alizzi; Elizabeth R Gavis
Journal:  Cell Rep       Date:  2017-09-26       Impact factor: 9.423

2.  Identification of diverse target RNAs that are functionally regulated by human Pumilio proteins.

Authors:  Jennifer A Bohn; Jamie L Van Etten; Trista L Schagat; Brittany M Bowman; Richard C McEachin; Peter L Freddolino; Aaron C Goldstrohm
Journal:  Nucleic Acids Res       Date:  2018-01-09       Impact factor: 16.971

Review 3.  Physiological functions of non-apoptotic caspase activity in the nervous system.

Authors:  Emilie Hollville; Mohanish Deshmukh
Journal:  Semin Cell Dev Biol       Date:  2017-12-07       Impact factor: 7.727

4.  Unique repression domains of Pumilio utilize deadenylation and decapping factors to accelerate destruction of target mRNAs.

Authors:  René M Arvola; Chung-Te Chang; Joseph P Buytendorp; Yevgen Levdansky; Eugene Valkov; Peter L Freddolino; Aaron C Goldstrohm
Journal:  Nucleic Acids Res       Date:  2020-02-28       Impact factor: 16.971

5.  Combinatorial control of messenger RNAs by Pumilio, Nanos and Brain Tumor Proteins.

Authors:  René M Arvola; Chase A Weidmann; Traci M Tanaka Hall; Aaron C Goldstrohm
Journal:  RNA Biol       Date:  2017-04-17       Impact factor: 4.652

Review 6.  Drosophila as a Model for Assessing the Function of RNA-Binding Proteins during Neurogenesis and Neurological Disease.

Authors:  Eugenia C Olesnicky; Ethan G Wright
Journal:  J Dev Biol       Date:  2018-08-18

Review 7.  Recent advances in branching mechanisms underlying neuronal morphogenesis.

Authors:  Shalini Menon; Stephanie Gupton
Journal:  F1000Res       Date:  2018-11-12

8.  The ELAV/Hu protein Found in neurons regulates cytoskeletal and ECM adhesion inputs for space-filling dendrite growth.

Authors:  Rebecca A Alizzi; Derek Xu; Conrad M Tenenbaum; Wei Wang; Elizabeth R Gavis
Journal:  PLoS Genet       Date:  2020-12-28       Impact factor: 5.917

9.  No significant regulation of bicoid mRNA by Pumilio or Nanos in the early Drosophila embryo.

Authors:  Tammy H Wharton; Krystle J Nomie; Robin P Wharton
Journal:  PLoS One       Date:  2018-03-30       Impact factor: 3.240

10.  Behavior of homing endonuclease gene drives targeting genes required for viability or female fertility with multiplexed guide RNAs.

Authors:  Georg Oberhofer; Tobin Ivy; Bruce A Hay
Journal:  Proc Natl Acad Sci U S A       Date:  2018-09-17       Impact factor: 11.205

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