Drosophila mutants of the autism candidate gene neurobeachin (rugose) exhibit neuro-developmental disorders, aberrant synaptic properties, altered locomotion, and impaired adult social behavior and activity patterns

References

• Abrahams, B. S., & Geschwind, D. H. (2008). Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet, 9, 341–355. doi: 10.1038/nrg2346
   PubMed Web of Science ®Google Scholar
• Banerjee, S., Riordan, M., & Bhat, M. A. (2014). Genetic aspects of autism spectrum disorders: insights from animal models. Front Cell Neurosci, 8, 58. doi: 10.3389/fncel.2014.00058
   PubMed Web of Science ®Google Scholar
• Berry-Kravis, E., & Ciurlionis, R. (1998). Overexpression of fragile X gene (FMR-1) transcripts increases cAMP production in neural cells. J Neurosci Res, 51, 41–48.
   PubMed Web of Science ®Google Scholar
• Broadie, K., & Bate, M. (1993). Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron, 11, 607–619.
   PubMed Web of Science ®Google Scholar
• Budnik, V., Zhong, Y., & Wu, C. F. (1990). Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurosci, 10, 3754–3768.
   PubMed Web of Science ®Google Scholar
• Burg, E. D., Langan, S. T., & Nash, H. A. (2013). Drosophila Social Clustering is Disrupted by Anesthetics and in narrow abdomen Ion Channel Mutants. Genes, Brain and Behavior, In Press. doi: 10.1111/gbb.12025
   PubMed Web of Science ®Google Scholar
• Castermans, D., Wilquet, V., Parthoens, E., Huysmans, C., Steyaert, J., Swinnen, L., et al. (2003). The neurobeachin gene is disrupted by a translocation in a patient with idiopathic autism. J Med Genet, 40, 352–356.
   PubMed Web of Science ®Google Scholar
• Dell’Acqua, M. L., Smith, K. E., Gorski, J. A., Horne, E. A., Gibson, E. S., & Gomez, L. L. (2006). Regulation of neuronal PKA signaling through AKAP targeting dynamics. Eur J Cell Biol, 85, 627–633. doi: 10.1016/j.ejcb.2006.01.010
   PubMed Web of Science ®Google Scholar
• Engel, J. E., & Wu, C. F. (1992). Interactions of membrane excitability mutations affecting potassium and sodium currents in the flight and giant fiber escape systems of Drosophila. J Comp Physiol A, 171, 93–104.
   PubMed Web of Science ®Google Scholar
• Engel, J. E., & Wu, C. F. (1996). Altered habituation of an identified escape circuit in Drosophila memory mutants. J Neurosci, 16, 3486–3499.
   PubMed Web of Science ®Google Scholar
• Engel, J.E., & Wu, C. F. (1998). Genetic dissection of functional contributions of specific potassium channel subunits in habituation of an escape circuit in Drosophila. J Neurosci, 18, 2254–2267.
   PubMed Web of Science ®Google Scholar
• Feng, Y., Ueda, A., & Wu, C. F. (2004). A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet, 18, 377–402. doi: 10.1080/01677060490894522
   PubMed Web of Science ®Google Scholar
• Fernandez, R. W., Nurilov, M., Feliciano, O., McDonald, I. S., & Simon, A. F. (2014). Straightforward Assay for Quantification of Social Avoidance in Drosophila melanogaster. J Vis Exp, (94). doi: 10.3791/52011
   PubMedGoogle Scholar
• Geschwind, D. H. (2009). Advances in autism. Annu Rev Med, 60, 367–380. doi: 10.1146/annurev.med.60.053107.121225
   PubMed Web of Science ®Google Scholar
• Han, J. D., Baker, N. E., & Rubin, C. S. (1997). Molecular characterization of a novel A kinase anchor protein from Drosophila melanogaster. J Biol Chem, 272, 26611–26619.
   PubMed Web of Science ®Google Scholar
• Jan, Y. N., Jan, L. Y., & Dennis, M. J. (1977). Two mutations of synaptic transmission in Drosophila. Proc R Soc Lond B Biol Sci, 198, 87–108.
   PubMed Web of Science ®Google Scholar
• Keshishian, H., & Kim, Y. S. (2004). Orchestrating development and function: retrograde BMP signaling in the Drosophila nervous system. Trends Neurosci, 27, 143–147. doi: 10.1016/j.tins.2004.01.004
   PubMed Web of Science ®Google Scholar
• Kidokoro, Y., & Nishikawa, K. (1994). Miniature endplate currents at the newly formed neuromuscular junction in Drosophila embryos and larvae. Neurosci Res, 19, 143–154.
   PubMed Web of Science ®Google Scholar
• Kuromi, H., Ueno, K., & Kidokoro, Y. (2010). Two types of Ca2 + channel linked to two endocytic pathways coordinately maintain synaptic transmission at the Drosophila synapse. Eur J Neurosci, 32, 335–346. doi: 10.1111/j.1460-9568.2010.07300.x
   PubMed Web of Science ®Google Scholar
• Levin, L. R., Han, P. L., Hwang, P. M., Feinstein, P. G., Davis, R. L., & Reed, R. R. (1992). The Drosophila learning and memory gene rutabaga encodes a Ca2+/Calmodulin-responsive adenylyl cyclase. Cell, 68, 479–489.
   PubMed Web of Science ®Google Scholar
• Medrihan, L., Rohlmann, A., Fairless, R., Andrae, J., Doring, M., Missler, M., et al. (2009). Neurobeachin, a protein implicated in membrane protein traffic and autism, is required for the formation and functioning of central synapses. J Physiol, 587, 5095–5106. doi: 10.1113/jphysiol.2009.178236
   PubMed Web of Science ®Google Scholar
• Michel, J. J., & Scott, J. D. (2002). AKAP mediated signal transduction. Annu Rev Pharmacol Toxicol, 42, 235–257. doi: 10.1146/annurev.pharmtox.42.083101.135801
   PubMed Web of Science ®Google Scholar
• Mogilner, A., Edelstein-Keshet, L., Bent, L., & Spiros, A. (2003). Mutual interactions, potentials, and individual distance in a social aggregation. J Math Biol, 47, 353–389. Epub 2003 May 2015.
   PubMed Web of Science ®Google Scholar
• Nagai, R., Hashimoto, R., & Yamaguchi, M. (2010). Drosophila Syntrophins are involved in locomotion and regulation of synaptic morphology. Exp Cell Res, 316, 2313–2321.
   PubMed Web of Science ®Google Scholar
• Nair, R., Lauks, J., Jung, S., Cooke, N. E., de Wit, H., Brose, N., et al. (2013). Neurobeachin regulates neurotransmitter receptor trafficking to synapses. J Cell Biol, 200, 61–80. doi: 10.1083/jcb.201207113
   PubMed Web of Science ®Google Scholar
• Niesmann, K., Breuer, D., Brockhaus, J., Born, G., Wolff, I., Reissner, C., et al. (2011). Dendritic spine formation and synaptic function require neurobeachin. Nat Commun, 2, 557. doi: 10.1038/ncomms1565
   PubMed Web of Science ®Google Scholar
• Nuytens, K., Tuand, K., Di Michele, M., Boonen, K., Waelkens, E., Freson, K., & Creemers, J. W. (2013). Platelets of mice heterozygous for neurobeachin, a candidate gene for autism spectrum disorder, display protein changes related to aberrant protein kinase A activity. Mol Autism, 4, 43. doi: 10.1186/2040-2392-4-43
   PubMedGoogle Scholar
• O’Neal, J., Gao, F., Hassan, A., Monahan, R., Barrios, S., Kilimann, M. W., et al (2009). Neurobeachin (NBEA) is a target of recurrent interstitial deletions at 13q13 in patients with MGUS and multiple myeloma. Exp Hematol, 37, 234–244. doi: 10.1016/j.exphem.2008.10.014
   PubMed Web of Science ®Google Scholar
• Ramaswami, M., Krishnan, K. S., & Kelly, R. B. (1994). Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron, 13, 363–375.
   PubMed Web of Science ®Google Scholar
• Rizo, J., & Sudhof, T. C. (2002). Snares and Munc18 in synaptic vesicle fusion. Nat Rev Neurosci, 3, 641–653. doi: 10.1038/nrn898
   PubMed Web of Science ®Google Scholar
• Savelyeva, L., Sagulenko, E., Schmitt, J. G., & Schwab, M. (2006). The neurobeachin gene spans the common fragile site FRA13A. Hum Genet, 118, 551–558. doi: 10.1007/s00439-005-0083-z
   PubMed Web of Science ®Google Scholar
• Shamloula, H. K., Mbogho, M. P., Pimentel, A. C., Chrzanowska-Lightowlers, Z. M., Hyatt, V., Okano, H., & Venkatesh, T. R. (2002). rugose (rg), a Drosophila A kinase anchor protein, is required for retinal pattern formation and interacts genetically with multiple signaling pathways. Genetics, 161, 693–710.
   PubMed Web of Science ®Google Scholar
• Sigrist, S. J., Reiff, D. F., Thiel, P. R., Steinert, J. R., & Schuster, C. M. (2003). Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci, 23, 6546–6556.
   PubMed Web of Science ®Google Scholar
• Simon, A. F., Chou, M.-T., Salazar, E. D., Nicholson, T., Saini, N., Metchev, S., & Krantz, D. E. (2012). A simple assay to study social behavior in Drosophila: measurement of social space within a group. Genes, Brain and Behavior, 11, 243–252. doi: 10.1111/j.1601-183X.2011.00740.x
   PubMed Web of Science ®Google Scholar
• Song, W., Ranjan, R., Dawson-Scully, K., Bronk, P., Marin, L., Seroude, L., et al. (2002). Presynaptic regulation of neurotransmission in Drosophila by the g protein-coupled receptor methuselah. Neuron, 36, 105–119.
   PubMed Web of Science ®Google Scholar
• Stewart, B. A., Atwood, H. L., Renger, J. J., Wang, J., & Wu, C. F. (1994). Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A, 175, 179–191.
   PubMed Web of Science ®Google Scholar
• Suh, G. S. B., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., et al. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature, 431, 854–859.
   PubMed Web of Science ®Google Scholar
• Thomas, J. B., & Wyman, R. J. (1984). Mutations altering synaptic connectivity between identified neurons in Drosophila. J Neurosci, 4, 530–538.
   PubMed Web of Science ®Google Scholar
• Ueda, A., & Wu, C. F. (2009). Role of rut adenylyl cyclase in the ensemble regulation of presynaptic terminal excitability: reduced synaptic strength and precision in a Drosophila memory mutant. J Neurogenet, 23, 185–199. doi: 10.1080/01677060802471726
   PubMed Web of Science ®Google Scholar
• Volders, K., Nuytens, K., & Creemers, J. W. (2011). The autism candidate gene Neurobeachin encodes a scaffolding protein implicated in membrane trafficking and signaling. Curr Mol Med, 11, 204–217.
   PubMed Web of Science ®Google Scholar
• Volders, K., Scholz, S., Slabbaert, J. R., Nagel, A. C., Verstreken, P., Creemers, J. W., et al. (2012). Drosophila rugose is a functional homolog of mammalian Neurobeachin and affects synaptic architecture, brain morphology, and associative learning. J Neurosci, 32, 15193–15204. doi: 10.1523/JNEUROSCI.6424-11.2012
   PubMed Web of Science ®Google Scholar
• Wu, C. F., Ganetzky, B., Jan, L. Y., Jan, Y. N., & Benzer, S. (1978). A Drosophila mutant with a temperature-sensitive block in nerve conduction. Proc Natl Acad Sci U S A, 75, 4047–4051.
   PubMed Web of Science ®Google Scholar
• Zhao, J., Lu, Y., Zhao, X., Yao, X., Shuai, Y., Huang, C., et al. (2013). Dissociation of rugose-dependent short-term memory component from memory consolidation in Drosophila. Genes Brain Behav, 12, 626–632. doi: 10.1111/gbb.12056
   PubMed Web of Science ®Google Scholar
• Zhong, Y., & Wu, C. F. (1991a). Alteration of four identified K+ currents in Drosophila muscle by mutations in eag. Science, 252, 1562–1564.
   PubMed Web of Science ®Google Scholar
• Zhong, Y., & Wu, C. F. (1991b). Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science, 251, 198–201.
   PubMed Web of Science ®Google Scholar