Drosophila Hrp48 is required for mushroom body axon growth, branching and guidance

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Bruckert, Hélène ^a,b,c   Marchetti, Giovanni ^a,b,c   Ramialison, Mirana ^d   Besse, Florence ^a,b,c   Skoulakis, Efthimios M C ^e  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CENTRE DE BIOCHIMIE   (France)

^c INSERM   (France)

^d Monash University   (Australia)

^e BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

HRP48 PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HRP48 PROTEIN, DROSOPHILA;

ADULT; ANIMAL TISSUE; ARTICLE; AXON OVEREXTENSION; BRANCHING MORPHOGENESIS; CELL PROLIFERATION; DOWN REGULATION; DROSOPHILA MELANOGASTER; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE INACTIVATION; HRP48 GENE; IMMUNOLOCALIZATION; MALE; MUSHROOM BODY; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PENETRANCE; PERIKARYON; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEX DIFFERENCE; WESTERN BLOTTING; ANIMAL; AXON; CYTOLOGY; EMBRYOLOGY; GENETICS; METABOLISM; MUTATION; SEXUAL DEVELOPMENT;

ANIMALS; AXONS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; MALE; MUSHROOM BODIES; MUTATION; PENETRANCE; SEX CHARACTERISTICS;

EID: 84943311956     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0136610     Document Type: Article

References (37)

1. Loya CM, Van Vactor D, Fulga TA. Understanding neuronal connectivity through the post-transcriptional toolkit. Genes Dev. 2010; 24(7): 625-35. Epub 2010/04/03. doi: 10.1101/gad.1907710 PMID: 20360381; PubMed Central PMCID: PMC2849119.
2. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol. 2002; 3(3): 195-205. Epub 2002/05/08. doi: 10.1038/nrm760 PMID: 11994740.
3. Glisovic T, Bachorik JL, Yong J, Dreyfuss G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 2008; 582(14): 1977-86. Epub 2008/03/18. doi: 10.1016/j.febslet.2008.03.004 PMID: 18342629; PubMed Central PMCID: PMC2858862.
4. Muller-McNicoll M, Neugebauer KM. How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet. 2013; 14(4): 275-87. Epub 2013/03/13. doi: 10.1038/nrg3434 PMID: 23478349.
5. Bassell GJ, Kelic S. Binding proteins for mRNA localization and local translation, and their dysfunction in genetic neurological disease. Curr Opin Neurobiol. 2004; 14(5): 574-81. Epub 2004/10/07. doi: 10.1016/j.conb.2004.08.010 PMID: 15464890.
6. Lenzken SC, Achsel T, Carri MT, Barabino SM. Neuronal RNA-binding proteins in health and disease. Wiley Interdiscip Rev RNA. 2014; 5(4): 565-76. Epub 2014/04/02. doi: 10.1002/wrna.1231 PMID: 24687864.
7. Han SP, Tang YH, Smith R. Functional diversity of the hnRNPs: past, present and perspectives. Biochem J. 2010; 430(3): 379-92. Epub 2010/08/28. doi: 10.1042/BJ20100396 PMID: 20795951.
8. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 1993; 62: 289-321. Epub 1993/01/01. doi: 10.1146/annurev.bi.62.070193.001445 PMID: 8352591.
9. Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, Diaz Z, et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature. 2013; 495(7442): 467-73. Epub 2013/03/05. doi: 10.1038/nature11922 PMID: 23455423; PubMed Central PMCID: PMC3756911.
10. Jin P, Duan R, Qurashi A, Qin Y, Tian D, Rosser TC, et al. Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile Xtremor/ataxia syndrome. Neuron. 2007; 55(4): 556-64. Epub 2007/08/19. doi: 10.1016/j.neuron.2007.07.020 PMID: 17698009; PubMed Central PMCID: PMC1994817.
11. Sofola OA, Jin P, Qin Y, Duan R, Liu H, de Haro M, et al. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile XCGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron. 2007; 55(4): 565-71. Epub 2007/08/19. doi: 10.1016/j.neuron.2007.07.021 PMID: 17698010; PubMed Central PMCID: PMC2215388.
12. Matunis MJ, Matunis EL, Dreyfuss G. Isolation of hnRNP complexes from Drosophila melanogaster. J Cell Biol. 1992; 116(2): 245-55. Epub 1992/01/01. PMID: 1730753; PubMed Central PMCID: PMC2289285.
13. Heisenberg M. Mushroom body memoir: from maps to models. Nat Rev Neurosci. 2003; 4(4): 266-75. PMID: 12671643.
14. Lee T, Lee A, Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development. 1999; 126(18): 4065-76. PMID: 10457015.
15. Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, et al. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife. 2014; 3: e04577. doi: 10.7554/eLife.04577 PMID: 25535793; PubMed Central PMCID: PMC4273437.
16. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem. 1998; 5(1-2): 38-51. PMID: 10454371.
17. Yano T, Lopez de Quinto S, Matsui Y, Shevchenko A, Ephrussi A., Hrp48 a Drosophila hnRNPA/B homolog, binds and regulates translation of oskar mRNA. Dev Cell. 2004; 6(5): 637-48. Epub 2004/05/08. PMID: 15130489.
18. Huynh JR, Munro TP, Smith-Litiere K, Lepesant JA, St Johnston D. The Drosophila hnRNPA/B homolog, Hrp48, is specifically required for a distinct step in osk mRNA localization. Dev Cell. 2004; 6 (5): 625-35. Epub 2004/05/08. PMID: 15130488.
19. Marchetti G, Reichardt I, Knoblich JA, Besse F. The TRIM-NHL protein Brat promotes axon maintenance by repressing src64B expression. J Neurosci. 2014; 34(41): 13855-64. doi: 10.1523/JNEUROSCI.3285-13.2014 PMID: 25297111.
20. Wu JS, Luo L. A protocol for mosaic analysis with a repressible cell marker (MARCM) in Drosophila. Nat Protoc. 2006; 1(6): 2583-9. PMID: 17406512.
21. Hammond LE, Rudner DZ, Kanaar R, Rio DC. Mutations in the hrp48 gene, which encodes a Drosophila heterogeneous nuclear ribonucleoprotein particle protein, cause lethality and developmental defects and affect P-elementthird-intron splicing in vivo. Mol Cell Biol. 1997; 17(12): 7260-7. Epub 1997/12/31. PMID: 9372958; PubMed Central PMCID: PMC232583.
22. Ng J. Wnt/PCP proteins regulate stereotyped axon branch extension in Drosophila. Development. 2012; 139(1): 165-77. doi: 10.1242/dev.068668 PMID: 22147954; PubMed Central PMCID: PMC3231775.
23. Suissa Y, Kalifa Y, Dinur T, Graham P, Deshpande G, Schedl P, et al. Hrp48 attenuates Sxl expression to allow for proper notch expression and signaling in wing development. Proc Natl Acad Sci USA. 2010; 107(15): 6930-5. Epub 2010/03/31. doi: 10.1073/pnas.0910570107 PMID: 20351283; PubMed Central PMCID: PMC2872424.
24. Kosturko LD, Maggipinto MJ, Korza G, Lee JW, Carson JH, Barbarese E. Heterogeneous nuclear ribonucleoprotein (hnRNP) E1 binds to hnRNPA2and inhibits translation of A2 response element mRNAs. Mol Biol Cell. 2006; 17(8): 3521-33. Epub 2006/06/16. doi: 10.1091/mbc.E05-10-0946 PMID: 16775011; PubMed Central PMCID: PMC1525244.
25. Munro TP, Magee RJ, Kidd GJ, Carson JH, Barbarese E, Smith LM, et al. Mutational analysis of a heterogeneous nuclear ribonucleoprotein A2 response element for RNA trafficking. J Biol Chem. 1999; 274(48): 34389-95. Epub 1999/11/24. PMID: 10567417.
26. Muslimov IA, Patel MV, Rose A, Tiedge H. Spatial code recognition in neuronal RNA targeting: role of RNA-hnRNPA2 interactions. J Cell Biol. 2011; 194(3): 441-57. Epub 2011/08/03. doi: 10.1083/jcb.201010027 PMID: 21807882; PubMed Central PMCID: PMC3153643.
27. Shan J, Munro TP, Barbarese E, Carson JH, Smith R. A molecular mechanism for mRNA trafficking in neuronal dendrites. J Neurosci. 2003; 23(26): 8859-66. Epub 2003/10/03. PMID: 14523087.
28. Goodrich JS, Clouse KN, Schupbach T. Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development. 2004; 131(9): 1949-58. Epub 2004/04/02. doi: 10.1242/dev.01078 PMID: 15056611.
29. Blanchette M, Green RE, MacArthur S, Brooks AN, Brenner SE, Eisen MB, et al. Genome-wide analysis of alternative pre-mRNA splicing and RNA-binding specificities of the Drosophila hnRNP A/B family members. Mol Cell. 2009; 33(4): 438-49. Epub 2009/03/03. doi: 10.1016/j.molcel.2009.01.022 PMID: 19250905; PubMed Central PMCID: PMC2674966.
30. Ng J, Luo L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron. 2004; 44(5): 779-93. Epub 2004/12/02. doi: 10.1016/j.neuron.2004.11.014 PMID: 15572110.
31. Sanchez-Soriano N, Travis M, Dajas-Bailador F, Goncalves-Pimentel C, Whitmarsh AJ, Prokop A. Mouse ACF7 and drosophila short stop modulate filopodia formation and microtubule organisation during neuronal growth. J Cell Sci. 2009; 122(Pt 14): 2534-42. Epub 2009/07/03. doi: 10.1242/jcs.046268 PMID: 19571116; PubMed Central PMCID: PMC2704885.
32. Dickson BJ Molecular mechanisms of axon guidance. Science. 2002; 298(5600): 1959-64. Epub 2002/12/10. doi: 10.1126/science.1072165 PMID: 12471249.
33. Kolodkin AL, Tessier-Lavigne M. Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb Perspect Biol. 2011; 3(6). Epub 2010/12/03. doi: 10.1101/cshperspect.a001727 PMID: 21123392; PubMed Central PMCID: PMC3098670.
34. Goossens T, Kang YY, Wuytens G, Zimmermann P, Callaerts-Vegh Z, Pollarolo G, et al. The Drosophila L1CAM homolog Neuroglian signals through distinct pathways to control different aspects of mushroom body axon development. Development. 2011; 138(8): 1595-605. Epub 2011/03/11. doi: 10.1242/dev.052787 PMID: 21389050; PubMed Central PMCID: PMC3062427.
35. Wang J, Zugates CT, Liang IH, Lee CH, Lee T. Drosophila Dscamis required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron. 2002; 33(4): 559-71. Epub 2002/02/22. PMID: 11856530.
36. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, et al. The developmental tran-scriptome of Drosophila melanogaster. Nature. 2011; 471(7339): 473-9. Epub 2010/12/24. doi: 10.1038/nature09715 PMID: 21179090; PubMed Central PMCID: PMC3075879.
37. Hartmann B, Castelo R, Minana B, Peden E, Blanchette M, Rio DC, et al. Distinct regulatory programs establish widespread sex-specific alternative splicing in Drosophila melanogaster. Rna. 2011; 17 (3): 453-68. Epub 2011/01/15. doi: 10.1261/rna.2460411 PMID: 21233220; PubMed Central PMCID: PMC3039145.