The Drosophila ortholog of the Zc3h14 RNA binding protein acts within neurons to pattern axon projection in the developing brain

Developmental Neurobiology

Volumn 76, Issue 1, 2016, Pages 93-106

  Kelly, Seth M ^a   Bienkowski, Rick ^b,c   Banerjee, Ayan ^b   Melicharek, David J ^d   Brewer, Zachariah A ^a   Marenda, Daniel R ^d   Corbett, Anita H ^b   Moberg, Kenneth H ^b  

^a 931 College Mall   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

dNab2; Drosophila; Mushroom body development; Polyadenosine RNA binding protein

Indexed keywords

DNAB2 PROTEIN; FASCICLIN II; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; ZC3H14 PROTEIN; DROSOPHILA PROTEIN; NAB2 PROTEIN, DROSOPHILA; RNA;

ADULT; ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; HOMOZYGOTE; KENYON CELL; LOSS OF FUNCTION MUTATION; MALE; MUSHROOM BODY; NERVE FIBER; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SHORT TERM MEMORY; ANIMAL; AXON; BRAIN; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL;

ANIMALS; AXONS; BRAIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; NEURONS; RNA; RNA-BINDING PROTEINS;

EID: 84949729859     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22301     Document Type: Article

References (48)

1. Armstrong JD, de Belle JS, Wang Z, Kaiser K. 1998. Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in drosophila. Learn Mem 5:102-114.
2. Aso Y, Grubel K, Busch S, Friedrich AB, Siwanowicz I, Tanimoto H. 2009. The mushroom body of adult drosophila characterized by gal4 drivers. J Neurogenet 23:156-172.
3. Banerjee A, Apponi LH, Pavlath GK, Corbett AH. 2013. Pabpn1: Molecular function and muscle disease. FEBS J 280:4230-4250.
4. Boyle M, Nighorn A, Thomas JB. 2006. Drosophila eph receptor guides specific axon branches of mushroom body neurons. Development 133:1845-1854.
5. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
6. Charlesworth A, Meijer HA, de Moor CH. 2013. Specificity factors in cytoplasmic polyadenylation. Wiley Interdiscip Rev RNA 4:437-461.
7. Chen E, Sharma MR, Shi X, Agrawal RK, Joseph S. 2014. Fragile X mental retardation protein regulates translation by binding directly to the ribosome. Mol Cell 54:407-417.
8. Cooper TA, Wan L, Dreyfuss G. 2009. RNA and disease. Cell 136:777-793.
9. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51.
10. Ejima A, Griffith LC. 2011. Assay for courtship suppression in drosophila. Cold Spring Harb Protoc 2011:pdb prot5575.
11. Fushima K, Tsujimura H. 2007. Precise control of fasciclin II expression is required for adult mushroom body development in drosophila. Dev Growth Differ 49:215-227.
12. Goossens T, Kang YY, Wuytens G, Zimmermann P, Callaerts-Vegh Z, Pollarolo G, Islam R, Hortsch M, Callaerts P. 2011. The drosophila L1CAM homolog neuroglian signals through distinct pathways to control different aspects of mushroom body axon development. Development 138:1595-1605.
13. Goss DJ, Kleiman FE. 2013. Poly(a) binding proteins: Are they all created equal?. Wiley Interdiscip Rev RNA 4:167-179.
14. Grenningloh G, Rehm EJ, Goodman CS. 1991. Genetic analysis of growth cone guidance in drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67:45-57.
15. Grillenzoni N, Flandre A, Lasbleiz C, Dura JM. 2007. Respective roles of the DRL receptor and its ligand wnt5 in drosophila mushroom body development. Development 134:3089-3097.
16. Guthrie CR, Greenup L, Leverenz JB, Kraemer BC. 2011. Msut2 is a determinant of susceptibility to tau neurotoxicity. Hum Mol Genet 20:1989-1999.
17. Guthrie CR, Schellenberg GD, Kraemer BC. 2009. SUT-2 potentiates tau-induced neurotoxicity in Caenorhabditis elegans. Hum. Mol. Genet 18:1825-1838.
18. Heisenberg M. 2003. Mushroom body memoir: From maps to models. Nat Rev Neurosci 4:266-275.
19. Ishimoto H, Wang Z, Rao Y, Wu CF, Kitamoto T. 2013. A novel role for ecdysone in drosophila conditioned behavior: Linking GPCR-mediated non-canonical steroid action to cAMP signaling in the adult brain. PLoS Genet 9:e1003843
20. Ishizuka A, Siomi MC, Siomi H. 2002. A drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev 16:2497-2508.
21. Keleman K, Vrontou E, Kruttner S, Yu JY, Kurtovic-Kozaric A, Dickson BJ. 2012. Dopamine neurons modulate pheromone responses in drosophila courtship learning. Nature 489:145-149.
22. Kelly S, Pak C, Garshasbi M, Kuss A, Corbett AH, Moberg K. 2012. New kid on the ID block: Neural functions of the Nab2/ZC3H14 class of Cys3His tandem zinc-finger polyadenosine RNA Binding Proteins. RNA Biol 9:555-562.
23. Kelly SM, Leung SW, Pak C, Banerjee A, Moberg KH, Corbett AH. 2014. A conserved role for the zinc finger polyadenosine RNA binding protein, ZC3H14, in control of poly(a) tail length. RNA. 20:681-688.
24. Kelly SM, Pabit SA, Kitchen CM, Guo P, Marfatia KA, Murphy TJ, Corbett AH, Berland KM. 2007. Recognition of polyadenosine RNA by zinc finger proteins. Proc Natl Acad Sci USA 104:12306-12311.
25. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U. 2001. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 10:329-338.
26. Lee T, Lee A, Luo L. 1999. Development of the drosophila mushroom bodies: Sequential generation of three distinct types of neurons from a neuroblast. Development. 126:4065-4076.
27. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
28. Lee T, Luo L. 2001. Mosaic analysis with a repressible cell marker (MARCM) for drosophila neural development. Trends Neurosci 24:251-254.
29. Leung SW, Apponi LH, Cornejo OE, Kitchen CM, Valentini SR, Pavlath GK, Dunham CM. 2009. Splice variants of the human zc3h14 gene generate multiple isoforms of a zinc finger polyadenosine RNA binding protein. Gene 439:71-78.
30. McKee AE, Silver PA. 2007. Systems perspectives on mRNA processing. Cell Res 17:581-590.
31. Michel CI, Kraft R, Restifo LL. 2004. Defective neuronal development in the mushroom bodies of drosophila fragile X mental retardation 1 mutants. J Neurosci 24:5798-5809.
32. Ng J. 2012. Wnt/PCP proteins regulate stereotyped axon branch extension in drosophila. Development 139:165-177.
33. Pak C, Garshasbi M, Kahrizi K, Gross C, Apponi LH, Noto JJ, Kelly SM. 2011. Mutation of the conserved polyadenosine RNA binding protein, zc3h14/dNab2, impairs neural function in drosophila and humans. Proc Natl Acad Sci USA 108:12390-12395.
34. Ropers HH. 2010. Genetics of early onset cognitive impairment. Annu Rev Genomics Hum Genet 11:161-187.
35. Santoro MR, Bray SM, Warren ST. 2012. Molecular mechanisms of fragile X syndrome: A twenty-year perspective. Annu Rev Pathol 7:219-245.
36. Shimizu K, Sato M, Tabata T. 2011. The wnt5/planar cell polarity pathway regulates axonal development of the drosophila mushroom body neuron. J Neurosci 31:4944-4954.
37. Shin JE, DiAntonio A. 2011. Highwire regulates guidance of sister axons in the drosophila mushroom body. J Neurosci 31:17689-17700.
38. Siegel RW, Hall JC. 1979. Conditioned responses in courtship behavior of normal and mutant drosophila. Proc Natl Acad Sci USA 76:3430-3434.
39. Wang J, Ma X, Yang JS, Zheng X, Zugates CT, Lee CH, Lee T. 2004. Transmembrane/juxtamembrane domain-dependent dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43:663-672.
40. Wang J, Zugates CT, Liang IH, Lee CH, Lee T. 2002. Drosophila dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33:559-571.
41. Wigington CP, Williams KR, Meers MP, Bassell GJ, Corbett AH. 2014. Poly(A) RNA-binding proteins and polyadenosine RNA: New members and novel functions. Wiley Interdiscip Rev RNA 5:601-622.
42. Wu JS, Luo L. 2006. A protocol for dissecting drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1:2110-2115.
43. Wu YC, Chen CH, Mercer A, Sokol NS. 2012. Let-7-complex microRNAs regulate the temporal identity of drosophila mushroom body neurons via chinmo. Dev Cell 23:202-209.
44. Yu HH, Chen CH, Shi L, Huang Y, Lee T. 2009. Twin-spot MARCM to reveal the developmental origin and identity of neurons. Nat Neurosci 12:947-953.
45. Zhan XL, Clemens JC, Neves G, Hattori D, Flanagan JJ, Hummel T, Vasconcelos ML, Chess A, Zipursky SL. 2004. Analysis of dscam diversity in regulating axon guidance in drosophila mushroom bodies. Neuron 43:673-686.
46. Zhang YQ, Bailey AM, Matthies HJ, Renden RB, Smith MA, Speese SD, Rubin GM, Broadie K. 2001. Drosophila fragile X-related gene regulates the MAP1B homolog futsch to control synaptic structure and function. Cell 107:591-603.
47. Zheng X, Zugates CT, Lu Z, Shi L, Bai JM, Lee T. 2006. Baboon/dSmad2 TGF-beta signaling is required during late larval stage for development of adult-specific neurons. EMBO J 25:615-627.
48. Zhu H, Luo L. 2004. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42:63-75.