Drosophila Valosin-Containing Protein is required for dendrite pruning through a regulatory role in mRNA metabolism

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 20, 2014, Pages 7331-7336

  Rumpf, Sebastian ^a,b,c,e   Bagley, Joshua A ^a,b,c   Thompson Peer, Katherine L ^a,b,c   Zhu, Sijun ^a,b,c,f   Gorczyca, David ^a,b,c   Beckstead, Robert B ^d   Jan, Lily Yeh ^a,b,c   Jan, Yuh Nung ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b Departments of Physiological Chemistry   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEASOME; RNA BINDING PROTEIN; TAR DNA BINDING PROTEIN; UBIQUITIN CONJUGATING ENZYME; VALOSIN CONTAINING PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITE; DENDRITE PRUNING; DOWN REGULATION; DROSOPHILA; ENZYME INHIBITION; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; HUMAN; IMMUNOFLUORESCENCE; METAMORPHOSIS; MOTONEURON; MUSHROOM BODY; NERVE CELL DEGENERATION; NONHUMAN; PERIKARYON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RNA METABOLISM; RNA SPLICING; UBIQUITINATION; UPREGULATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DENDRITES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ECDYSONE; GENE EXPRESSION REGULATION; MUTATION; NEURONS; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 84901036365     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406898111     Document Type: Article

References (41)

1. Luo L, OLeary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127-156.
2. Kuo CT, Jan LY, Jan YN (2005) Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc Natl Acad Sci USA 102(42):15230-15235.
3. Williams DW, Truman JW (2005) Cellular mechanisms of dendrite pruning in Drosophila: Insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 132(16):3631-3642.
4. Kirilly D, et al. (2009) A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat Neurosci 12(12):1497-1505.
5. Lee HH, Jan LY, Jan YN (2009) Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc Natl Acad Sci USA 106(15):6363-6368.
6. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9(10):1234-1236.
7. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51(3):283-290.
8. Watts RJ, Hoopfer ED, Luo L (2003) Axon pruning during Drosophila metamorphosis: Evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38(6):871-885.
9. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
10. Finley D (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477-513.
11. Rumpf S, Lee SB, Jan LY, Jan YN (2011) Neuronal remodeling and apoptosis require VCP-dependent degradation of the apoptosis inhibitor DIAP1. Development 138(6): 1153-1160.
12. Jentsch S, Rumpf S (2007) Cdc48 (p97): A molecular gearbox in the ubiquitin pathway? Trends Biochem Sci 32(1):6-11.
13. Watts GD, et al. (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat Genet 36(4):377-381.
14. Johnson JO, et al.; ITALSGEN Consortium (2010) Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68(5):857-864.
15. Neumann M, et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314(5796):130-133.
16. Kanamori T, et al. (2013) Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 340(6139):1475-1478.
17. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22(3):451-461.
18. Loncle N, Williams DW (2012) An interaction screen identifies headcase as a regulator of large-scale pruning. J Neurosci 32(48):17086-17096.
19. Parrish JZ, Xu P, Kim CC, Jan LY, Jan YN (2009) The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in drosophila sensory neurons. Neuron 63(6):788-802.
20. Terman JR, Mao T, Pasterkamp RJ, Yu HH, Kolodkin AL (2002) MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109(7):887-900.
21. Ritson GP, et al. (2010) TDP-43 mediates degeneration in a novel Drosophila model of disease caused by mutations in VCP/p97. J Neurosci 30(22):7729-7739.
22. Zhou HL, Geng C, Luo G, Lou H (2013) The p97-UBXD8 complex destabilizes mRNA by promoting release of ubiquitinated HuR from mRNP. Genes Dev 27(9):1046-1058.
23. Lisbin MJ, Qiu J, White K (2001) The neuron-specific RNA-binding protein ELAV regulates neuroglian alternative splicing in neurons and binds directly to its premRNA. Genes Dev 15(19):2546-2561.
24. Polymenidou M, et al. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 14(4):459-468.
25. Tollervey JR, et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14(4):452-458.
26. Lin MJ, Cheng CW, Shen CK (2011) Neuronal function and dysfunction of Drosophila dTDP. PLoS ONE 6(6):e20371.
27. Buchan JR, Kolaitis RM, Taylor JP, Parker R (2013) Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 153(7):1461-1474.
28. Lu Y, Ferris J, Gao FB (2009) Frontotemporal dementia and amyotrophic lateral sclerosis-Associated disease protein TDP-43 promotes dendritic branching. Mol Brain 2:30-39.
29. Chang YC, et al. (2011) Pathogenic VCP/TER94 alleles are dominant actives and contribute to neurodegeneration by altering cellular ATP level in a Drosophila IBMPFD model. PLoS Genet 7(2):e1001288.
30. Hoopfer ED, Penton A, Watts RJ, Luo L (2008) Genomic analysis of Drosophila neuronal remodeling: A role for the RNA-binding protein Boule as a negative regulator of axon pruning. J Neurosci 28(24):6092-6103.
31. Smyth KA, Belote JM (1999) The dominant temperature-sensitive lethal DTS7 of Drosophila melanogaster encodes an altered 20S proteasome beta-type subunit. Genetics 151(1):211-220.
32. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6(1):9-20.
33. Wong JJ, et al. (2013) A Cullin1-based SCF E3 ubiquitin ligase targets the InR/PI3K/TOR pathway to regulate neuronal pruning. PLoS Biol 11(9):e1001657.
34. Han C, et al. (2014) Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron 81(3):544-560.
35. Neumann M (2009) Molecular neuropathology of TDP-43 proteinopathies. Int J Mol Sci 10(1):232-246.
36. Grueber WB, et al. (2007) Projections of Drosophila multidendritic neurons in the central nervous system: Links with peripheral dendrite morphology. Development 134(1):55-64.
37. Grueber WB, Ye B, Moore AW, Jan LY, Jan YN (2003) Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr Biol 13(8):618-626.
38. Dietzl G, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448(7150):151-156.
39. Matsubara D, Horiuchi SY, Shimono K, Usui T, Uemura T (2011) The seven-pass transmembrane cadherin Flamingo controls dendritic self-Avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. Genes Dev 25(18): 1982-1996.
40. Ritter AR, Beckstead RB (2010) Sox14 is required for transcriptional and developmental responses to 20-hydroxyecdysone at the onset of drosophila metamorphosis. Dev Dyn 239(10):2685-2694.
41. Weaver TA, White RA (1995) headcase, an imaginal specific gene required for adult morphogenesis in Drosophila melanogaster. Development 121(12):4149-4160.