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Neuronal Genes and Developmental Neuronal Pathways in Drosophila Life Span Control

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Abstract

The nervous system has long been suggested as a key tissue that defines life span. The identity of neuronal cell types is established during development and maintained throughout adulthood due to the expression of specific neuronal genes coding for ion channels, neurotransmitters and neuropeptides, G-protein-coupled receptors, motor proteins, recognition and adhesion molecules. In this paper, we review data on the role of neuronal genes in Drosophila melanogaster life span control. Several pathways responsible for life span regulation are also important for the development of the nervous system. Genes involved in insulin-like, Target of Rapamycin, Janus Kinase/Signal Transducer and Activator of Transcription and cell polarity pathways, a number of global regulators and transcription factors play key roles both in aging and longevity control and in shaping the nervous system as a network of specialized neuronal cells in early development. Is their impact on life span related, at least partially, to their developmental functions or is it explained by other pleiotropic influences later in life? In this paper, we address this question based on the published data and our own findings.

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References

  • Alcedo J, Flatt T, Pasyukova EG (2013) Neuronal inputs and outputs of aging and longevity. Front Genet 4:71

    PubMed Central  PubMed  Google Scholar 

  • Alic N, Hoddinott MP, Vinti G, Partridge L (2011) Lifespan extension by increased expression of the Drosophila homologue of the IGFBP7 tumour suppressor. Aging Cell 10:137–147

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ashraf SI, Ip YT (2001) The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128:4757–4767

    CAS  PubMed  Google Scholar 

  • Ashraf SI, Hu X, Roote J, Ip YT (1999) The mesoderm determinant snail collaborates with related zinc-finger proteins to control Drosophila neurogenesis. EMBO J 18:6426–6638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Atwood SX, Prehoda KE (2009) aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr Biol 19:723–729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baines RA (2004) Synaptic strengthening mediated by bone morphogenetic protein-dependent retrograde signaling in the Drosophila CNS. J Neurosci 24:6904–6911

    Article  CAS  PubMed  Google Scholar 

  • Bauer JH, Chang C, Morris SN, Hozier S, Andersen S, Waitzman JS, Helfand SL (2005a) Expression of dominant-negative Dmp53 in the adult fly brain inhibits insulin signaling. Proc Natl Acad Sci USA 104:13355–13360

    Article  CAS  Google Scholar 

  • Bauer JH, Poon PC, Glatt-Deeley H, Abrams JM, Helfand SL (2005b) Neuronal expression of p53 dominant-negative proteins in adult Drosophila melanogaster extends life span. Curr Biol 15:2063–2068

    Article  CAS  PubMed  Google Scholar 

  • Bauer JH, Chang C, Morris SN, Hozier S, Andersen S, Waitzman JS, Helfand SL (2007) Expression of dominant-negative Dmp53 in the adult fly brain inhibits insulin signaling. Proc Natl Acad Sci USA 104:13355–13360

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bauer JH, Chang C, Bae G, Morris SN, Helfand SL (2010) Dominant-negative Dmp53 extends life span through the dTOR pathway in D. melanogaster. Mech Ageing Dev 131:193–201

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Betschinger J, Mechtler K, Knoblich JA (2003) The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422:326–330

    Article  CAS  PubMed  Google Scholar 

  • Biteau B, Karpac J, Supoyo S, Degennaro M, Lehmann R, Jasper H (2010) Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet 6:e1001159

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Blagosklonny MV (2009) Validation of anti-aging drugs by treating age-related diseases. Aging (Albany NY) 1:281–288

    CAS  Google Scholar 

  • Broughton S, Partridge L (2009) Insulin/IGF-like signalling, the central nervous system and aging. Biochem J 418:1–12

    Article  CAS  PubMed  Google Scholar 

  • Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, Driege Y, Martinez P, Hafen E, Withers DJ, Leevers SJ, Partridge L (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102:3105–3110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Broughton S, Alic N, Slack C, Bass T, Ikeya T, Vinti G, Tommasi AM, Driege Y, Hafen E, Partridge L (2008) Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS ONE 3:e3721

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Buchanan ME, Davis RL (2010) A distinct set of Drosophila brain neurons required for neurofibromatosis type 1-dependent learning and memory. J Neurosci 30:10135–10143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Buchanan ME, Guo HF, Tong J, Hannan F, Luo L, Zhong Y (2000) A neurofibromatosis-1-regulated pathway is required for learning in Drosophila. Nature 403:895–898

    Article  CAS  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

    CAS  PubMed  Google Scholar 

  • Byers D, Davis RL, Kiger JA Jr (1981) Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289:79–81

    Google Scholar 

  • Cai Y, Chia W, Yang XA (2001) A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. EMBO J 20:1704–1714

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cai Y, Yu F, Lin S, Chia W, Yang X (2003) Apical complex genes control mitotic spindle geometry and relative size of daughter cells in Drosophila neuroblast and pI asymmetric divisions. Cell 112(1):51–62

    Article  CAS  PubMed  Google Scholar 

  • Carbone MA, Jordan KW, Lyman RF, Harbison ST, Leips J, Morgan TJ, DeLuca M, Awadalla P, Mackay TF (2006) Phenotypic variation and natural selection at catsup, a pleiotropic quantitative trait gene in Drosophila. Curr Biol 16:912–919

    Article  CAS  PubMed  Google Scholar 

  • Certel SJ, Thor S (2004) Specification of Drosophila motoneuron identity by the combinatorial action of POU and LIM-HD factors. Development 131:5429–5439

    Article  CAS  PubMed  Google Scholar 

  • Chang KC, Garcia-Alvarez G, Somers G, Sousa-Nunes R, Rossi F, Lee YY, Soon SB, Gonzalez C, Chia W, Wang H (2010) Interplay between the transcription factor Zif and aPKC regulates neuroblast polarity and self-renewal. Dev Cell 19:778–785

    Article  CAS  PubMed  Google Scholar 

  • Colosimo PF, Liu X, Kaplan NA, Tolwinski NS (2010) GSK3beta affects apical-basal polarity and cell-cell adhesion by regulating aPKC levels. Dev Dyn 239:115–125

    CAS  PubMed  Google Scholar 

  • Connell-Crowley L, Le Gall M, Vo DJ, Giniger E (2000) The cyclin-dependent kinase Cdk5 controls multiple aspects of axon patterning in vivo. Curr Biol 10:599–602

    Article  CAS  PubMed  Google Scholar 

  • Connell-Crowley L, Vo D, Luke L, Giniger E (2007) Drosophila lacking the Cdk5 activator, p35, display defective axon guidance, age-dependent behavioral deficits and reduced lifespan. Mech Dev 124:341–349

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Copf T, Goguel V, Lampin-Saint-Amaux A, Scaplehorn N, Preat T (2011) Cytokine signaling through the JAK/STAT pathway is required for long-term memory in Drosophila. Proc Natl Acad Sci USA 108:8059–8064

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Luca M, Roshina NV, Geiger-Thornsberry GL, Lyman RF, Pasyukova EG, Mackay TFC (2003) Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nat Genet 34:429–433

    Article  PubMed  Google Scholar 

  • Demontis F, Perrimon N (2010) FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143:813–825

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dimitroff B, Howe K, Watson A, Campion B, Lee HG, Zhao N, O’Connor MB, Neufeld TP, Selleck S (2012) Diet and energy-sensing inputs affect TorC1-mediated axon misrouting but not TorC2-directed synapse growth in a Drosophila model of tuberous sclerosis. PLoS ONE 7:e30722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Drain P, Folkers E, Quinn WG (1991) cAMP-dependent protein kinase and the disruption of learning in transgenic flies. Neuron 6:71–82

    Article  CAS  PubMed  Google Scholar 

  • Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S (1976) dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci USA 73:1684–1688

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Enell LE, Kapan N, Söderberg JAE, Kahsai L, Nässel DR (2010) Insulin signaling, lifespan and stress resistance are modulated by metabotropic GABA receptors on insulin producing cells in the brain of Drosophila. PLoS ONE 5:e15780

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Feng Z (2010) p53 regulation of the IGF-1/AKT/mTOR pathways and the endosomal compartment. Cold Spring Harb Perspect Biol 2:a001057

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Flatt T, Min KJ, D’Alterio C, Villa-Cuesta E, Cumbers J, Lehmann R, Jones DL, Tatar M (2008) Drosophila germ-line modulation of insulin signaling and lifespan. Proc Natl Acad Sci USA 105:6368–6373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Franciscovich AL, Mortimer AD, Freeman AA, Gu J, Sanyal S (2008) Overexpression screen in Drosophila identifies neuronal roles of GSK-3 beta/shaggy as a regulator of AP-1-dependent developmental plasticity. Genetics 180:2057–2071

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Franco B, Bogdanik L, Bobinnec Y, Debec A, Bockaert J, Parmentier ML, Grau Y (2004) Shaggy, the homolog of glycogen synthase kinase 3, controls neuromuscular junction growth in Drosophila. J Neurosci 24:6573–6577

    Article  CAS  PubMed  Google Scholar 

  • Frankel S, Rogina B (2005) Drosophila longevity is not affected by heterochromatin-mediated gene silencing. Aging Cell 4:53–56

    Article  CAS  PubMed  Google Scholar 

  • Fridell Y-WC, Sanchez-Blanco A, Silvia BA, Helfand SL (2005) Targeted expression of the human uncoupling protein 2 (hUCP2) to adult neurons extends life span in the fly. Cell Metab 1:145–152

    Article  CAS  PubMed  Google Scholar 

  • Fridell YW, Hoh M, Kréneisz O, Hosier S, Chang C, Scantling D, Mulkey DK, Helfand SL (2009) Increased uncoupling protein (UCP) activity in Drosophila insulin-producing neurons attenuates insulin signaling and extends lifespan. Aging (Albany NY) 1:699–713

    Google Scholar 

  • Gervas N, Tchénio P, Preat T (2010) PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 65:516–529

    Article  CAS  Google Scholar 

  • Giannakou ME, Goss M, Jünger MA, Hafen E, Leevers SJ, Partridge L (2004) Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305:361

    Article  CAS  PubMed  Google Scholar 

  • Grönke S, Clarke DF, Broughton S, Andrews TD, Partridge L (2010) Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet 6:e1000857

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Haselton A, Sharmin E, Schrader J, Sah M, Poon P, Fridell YW (2010) Partial ablation of adult Drosophila insulin-producing neurons modulates glucose homeostasis and extends life span without insulin resistance. Cell Cycle 9:3063–3071

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hobert O (2011) Regulation of terminal differentiation programs in the nervous system. Annu Rev Cell Dev Biol 27:681–696

    Article  CAS  PubMed  Google Scholar 

  • Humphrey DM, Toivonen JM, Giannakou M, Partridge L, Brand MD (2009) Expression of human uncoupling protein-3 in Drosophila insulin-producing cells increases insulin-like peptide (DILP) levels and shortens lifespan. Exp Gerontol 44:316–327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hwangbo DS, Gershman B, Tu MP, Tatar M, Palmer M (2004) Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429:562–566

    Article  CAS  PubMed  Google Scholar 

  • Inoki K, Guan KL (2006) Complexity of the TOR signaling network. Trends Cell Biol 16:206–212

    Article  CAS  PubMed  Google Scholar 

  • Kanuka H, Kuranaga E, Takemoto K, Hiratou T, Okano H, Miura M (2005) Drosophila caspase transduces Shaggy/GSK-3beta kinase activity in neural precursor development. EMBO J 24:3793–3806

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S (2004) Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 14:885–890

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kapahi P, Chen D, Rogers AN, Katewa SD, Li PW, Thomas EL, Kockel L (2010) With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab 11:453–465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaplan NA, Colosimo PF, Liu X, Tolwinski NS (2011) Complex interactions between GSK3 and aPKC in Drosophila embryonic epithelial morphogenesis. PLoS ONE 6:e18616

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katewa SD, Kapahi P (2011) Role of TOR signaling in aging and related biological processes in Drosophila melanogaster. Exp Gerontol 46:382–390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kissler AE, Pettersson N, Frölich A, Sigrist SJ, Suter B (2009) Drosophila cdk5 is needed for locomotive behavior and NMJ elaboration, but seems dispensable for synaptic transmission. Dev Neurobiol 69:365–377

    Article  CAS  PubMed  Google Scholar 

  • Koike-Kumagai M, Yasunaga KI, Morikawa R, Kanamori T, Emoto K (2009) The target of rapamycin complex 2 controls dendritic tiling of Drosophila sensory neurons through the Tricornered kinase signalling pathway. EMBO J 28:3879–3892

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kraut R, Campos-Ortega JA (1996) Inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adaptor protein. Dev Biol 174:65–81

    Article  CAS  PubMed  Google Scholar 

  • Kraut R, Chia W, Jan LY, Jan YN, Knoblich JA (1996) Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383:50–55

    Article  CAS  PubMed  Google Scholar 

  • Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA 104:3574–3578

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Larson K, Yan SJ, Tsurumi A, Liu J, Zhou J, Gaur K, Guo D, Eickbush TH, Li WX (2012) Heterochromatin formation promotes longevity and represses ribosomal RNA synthesis. PLoS Genet 8:e1002473

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee KS, Iijima-Ando K, Iijima K, Lee WJ, Lee JH, Yu K, Lee DS (2009) JNK/FOXO-mediated neuronal expression of fly homologue of peroxiredoxin II reduces oxidative stress and extends life span. J Biol Chem 284:29454–29461

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li J, Li W, Calhoun HC, Xia F, Gao FB, Li W (2003) Patterns and functions of STAT activation during Drosophila embryogenesis. Mech Dev 120:1455–1468

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liao PC, Lin HY, Yuh CH, Yu LK, Wang HD (2008) The effect of neuronal expression of heat shock proteins 26 and 27 on lifespan, neurodegeneration, and apoptosis in Drosophila. Biochem Biophys Res Commun 376:637–641

    Article  CAS  PubMed  Google Scholar 

  • Libert S, Zwiener J, Chu X, Vanvoorhies W, Roman G, Pletcher SD (2007) Regulation of Drosophila life span by olfaction and food-derived odors. Science 315:1133–1137

    Article  CAS  PubMed  Google Scholar 

  • Lin YR, Kim K, Yang Y, Ivessa A, Sadoshima J, Park Y (2011a) Regulation of longevity by regulator of G-protein signaling protein, Loco. Aging Cell 10:438–447

    Article  CAS  PubMed  Google Scholar 

  • Lin YR, Parikh H, Park Y (2011b) Loco signaling pathway in longevity. Small GTPases 2:158–161

    Article  PubMed Central  PubMed  Google Scholar 

  • Livingstone MS, Tempel BL (1983) Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 303:67–70

    Article  CAS  PubMed  Google Scholar 

  • Loo LW, Secombe J, Little JT, Carlos LS, Yost C, Cheng PF, Flynn EM, Edgar BA, Eisenman RN (2005) The transcriptional repressor dMnt is a regulator of growth in Drosophila melanogaster. Mol Cell Biol 25:7078–7091

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Madeo F, Tavernarakis N, Kroemer G (2010) Can autophagy promote longevity? Nat Cell Biol 12:842–846

    Article  CAS  PubMed  Google Scholar 

  • Magwire MM, Yamamoto A, Carbone MA, Roshina NV, Symonenko AV, Pasyukova EG, Morozova TV, Mackay TFC (2010) Quantitative and molecular genetic analyses of mutations increasing Drosophila life span. PLoS Genet 6:e1001037

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martínez-Azorín F, Calleja M, Hernández-Sierra R, Farr CL, Kaguni LS, Garesse R (2008) Over-expression of the catalytic core of mitochondrial DNA (mtDNA) polymerase in the nervous system of Drosophila melanogaster reduces median life span by inducing mtDNA depletion. J Neurochem 105:165–176

    Article  PubMed  CAS  Google Scholar 

  • Martin-Pena A, Acebes A, Rodriguez JR, Sorribes A, de Polavieja GG, Fernandez-Funez P, Ferrus A (2006) Age-independent synaptogenesis by phosphoinositide 3 kinase. J Neurosci 26:10199–10208

    Article  CAS  PubMed  Google Scholar 

  • McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765–1768

    Article  CAS  PubMed  Google Scholar 

  • Min KJ, Yamamoto R, Buch S, Pankratz M, Tatar M (2008) Drosophila lifespan control by dietary restriction independent of insulin-like signaling. Aging Cell 7:199–206

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morrow G, Samson M, Michaud S, Tanguay RM (2004) Overexpression of the small mitochondrial Hsp22 extends Drosophila lifespan and increases resistance to oxidative stress. FASEB J 18:598–609

    CAS  PubMed  Google Scholar 

  • Mudher A, Shepherd D, Newman TA, Mildren P, Jukes JP, Squire A, Mears A, Drummond JA, Berg S, MacKay D, Asuni AA, Bhat R, Lovestone S (2004) GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol Psychiatry 9:522–530

    Article  CAS  PubMed  Google Scholar 

  • Mukunda L, Miazzi F, Kaltofen S, Hansson BS, Wicher D (2014) Calmodulin modulates insect odorant receptor function. Cell Calcium 55:191–199

    Article  CAS  PubMed  Google Scholar 

  • Nässel DR, Winther AM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104

    Article  PubMed  CAS  Google Scholar 

  • Nässel DR, Kubrak OI, Liu Y, Luo J, Lushchak OV (2013) Factors that regulate insulin producing cells and their output in Drosophila. Front Physiol 4:252

    Article  PubMed Central  PubMed  Google Scholar 

  • Natarajan R, Trivedi-Vyas D, Wairkar YP (2013) Tuberous sclerosis complex regulates Drosophila neuromuscular junction growth via the TORC2/Akt pathway. Hum Mol Genet 22:2010–2023

    Article  CAS  PubMed  Google Scholar 

  • Noble W, Hanger DP, Miller CC, Lovestone S (2013) The importance of tau phosphorylation for neurodegenerative diseases. Front Neurol 4:83

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nuzhdin SV, Pasyukova EG, Dilda CL, Zeng Z-B, Mackay TFC (1997) Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc Natl Acad Sci USA 94:9734–9739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Orr WC, Mockett RJ, Benes JJ, Sohal RS (2003) Effects of overexpression of copper-zinc and manganese superoxide dismutases, catalase, and thioredoxin reductase genes on longevity in Drosophila melanogaster. J Biol Chem 278:26418–26422

    Article  CAS  PubMed  Google Scholar 

  • Ouyang Y, Song Y, Lu B (2011) dp53 restrains ectopic neural stem cell formation in the Drosophila brain in a non-apoptotic mechanism involving Archipelago and cyclin E. PLoS ONE 6:e28098

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY (1987) Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237:749–753

    Article  CAS  PubMed  Google Scholar 

  • Parkes TL, Hilliker AJ, Phillips JP (1999) Motorneurons, reactive oxygen, and life span in Drosophila. Neurobiol Aging 20:531–535

    Article  CAS  PubMed  Google Scholar 

  • Parrish JZ, Kim MD, Jan LY, Jan YN (2006) Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev 20:820–835

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 63:788–802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Partridge L, Alic N, Bjedov I, Piper MD (2011) Ageing in Drosophila: the role of the insulin/Igf and TOR signalling network. Exp Gerontol 46:376–381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pasyukova EG, Vieira C, Mackay TFC (2000) Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156:1129–1146

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pasyukova EG, Roshina NV, Mackay TFC (2004) Shuttle craft: a candidate quantitative trait gene for Drosophila lifespan. Aging Cell 3:297–307

    Article  CAS  PubMed  Google Scholar 

  • Plyusnina EN, Shaposhnikov MV, Moskalev AA (2011) Increase of Drosophila melanogaster lifespan due to D-GADD45 overexpression in the nervous system. Biogerontology 12:211–226

    Article  CAS  PubMed  Google Scholar 

  • Poon PC, Kuo TH, Linford NJ, Roman G, Pletcher SD (2010) Carbon dioxide sensing modulates lifespan and physiology in Drosophila. PLoS Biol 8:e1000356

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Puig O, Mattila J (2011) Understanding Forkhead box class O function: lessons from Drosophila melanogaster. Antioxid Redox Signal 14:635–647

    Article  CAS  PubMed  Google Scholar 

  • Rana A, Rera M, Walker DW (2013) Parkin overexpression during aging reduces proteotoxicity, alters mitochondrial dynamics, and extends lifespan. Proc Natl Acad Sci USA 110:8638–8643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reenan RA, Rogina B (2008) Acquired temperature-sensitive paralysis as a biomarker of declining neuronal function in aging Drosophila. Aging Cell 7:179–186

    Article  CAS  PubMed  Google Scholar 

  • Reenan RA, Hanrahan CJ, Ganetzky B (2000) The mle (napts) RNA helicase mutation in Drosophila results in a splicing catastrophe of the para Na+ channel transcript in a region of RNA editing. Neuron 25:139–149

    Article  CAS  PubMed  Google Scholar 

  • Renger JJ, Ueda A, Atwood HL, Govind CK, Wu CF (2000) Role of cAMP cascade in synaptic stability and plasticity: ultrastructural and physiological analyses of individual synaptic boutons in Drosophila memory mutants. J Neurosci 20:3980–3992

    CAS  PubMed  Google Scholar 

  • Robinow S, White K (1988) The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev Biol 126:294–303

    Article  CAS  PubMed  Google Scholar 

  • Robinow S, White K (1991) Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J Neurobiol 22:443–461

    Article  CAS  PubMed  Google Scholar 

  • Rogina B, Helfand SL (1995) Regulation of gene expression is linked to life span in adult Drosophila. Genetics 141:1043–1048

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rogina B, Helfand SL, Frankel S (2002) Longevity regulation by Drosophila Rpd3 deacetylase and caloric restriction. Science 298:1745

    Article  CAS  PubMed  Google Scholar 

  • Root CM, Masuyama K, Green DS, Enell LE, Nässel DR, Lee CH, Wang JW (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311–321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roshina NV, Pasyukova EG (2007) Genes regulating the development and functioning of the nervous system determine life span in Drosophila melanogaster. Russ J Genet 43:356–362

    Article  CAS  Google Scholar 

  • Roshina NV, Symonenko AV, Krementsova AV, Trostnikov MV, Pasyukova EG (2014) Embryonic expression of shuttle craft, a Drosophila gene involved in neuron development, is associated with adult lifespan. Aging (Albany NY) 6:1076–1093

    Google Scholar 

  • Ruan H, Tang XD, Chen ML, Joiner ML, Sun G, Brot N, Weissbach H, Heinemann SH, Iverson L, Wu CF, Hoshi T (2002) High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA 99:2748–2753

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruiz-Canada C, Ashley J, Moeckel-Cole S, Drier E, Yin J, Budnik V (2004) New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 42:567–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rybina OY, Pasyukova EG (2010) A naturally occurring polymorphism at Drosophila melanogaster Lim3 locus, a homolog of human LHX3/4, affects Lim3 transcription and fly lifespan. PLoS ONE 5:e12621

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schaefer M, Shevchenko A, Shevchenko A, Knoblich JA (2000) A protein complex containing Inscuteable and the Galpha-binding protein pins orients asymmetric cell divisions in Drosophila. Curr Biol 10:353–362

    Article  CAS  PubMed  Google Scholar 

  • Seong KH, Matsuo T, Fuyama Y, Aigaki T (2001) Neural-specific overexpression of Drosophila plenty of SH3s (DPOSH) extends the longevity of adult flies. Biogerontology 2:271–281

    Article  CAS  PubMed  Google Scholar 

  • Sepp KJ, Hong P, Lizarraga SB, Liu JS, Mejia LA, Walsh CA, Perrimon N (2008) Identification of neural outgrowth genes using genome-wide RNAi. PLoS Genet 4:e1000111

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Siebold AP, Banerjee R, Tie F, Kiss DL, Moskowitz J, Harte PJ (2010) Polycomb repressive complex 2 and Trithorax modulate Drosophila longevity and stress resistance. Proc Natl Acad Sci USA 107:169–174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Simonsen A, Cumming RC, Brech A, Isakson P, Schubert DR, Finley KD (2008) Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4:176–184

    Article  CAS  PubMed  Google Scholar 

  • Skeath JB, Thor S (2003) Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol 13:8–15

    Article  CAS  PubMed  Google Scholar 

  • Skoulakis EM, Kalderon D, Davis RL (1993) Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11:197–208

    Article  CAS  PubMed  Google Scholar 

  • Smith CA, Lau KM, Rahmani Z, Dho SE, Brothers G, She YM, Berry DM, Bonneil E, Thibault P, Schweisguth F, Le Borgne R, McGlade CJ (2007) aPKC-mediated phosphorylation regulates asymmetric membrane localization of the cell fate determinant Numb. EMBO J 26:468–480

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Song Y, Ori-McKenney KM, Zheng Y, Han C, Jan LY, Jan YN (2012) Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. Genes Dev 26:612–1625

    Google Scholar 

  • Stathakis DG, Pentz ES, Freeman ME, Kullman J, Hankins GR, Pearlson NJ, Wright TR (1995) The genetic and molecular organization of the Dopa decarboxlyase gene cluster of Drosophila melanogaster. Genetics 141:629–655

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stathakis DG, Burton DY, McIvor WE, Krishnakumar S, Wright TR, O’Donnell JM (1999) The catecholamines up (Catsup) protein of Drosophila melanogaster functions as a negative regulator of tyrosine hydroxylase activity. Genetics 153:361–382

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stenesen D, Suh JM, Seo J, Yu K, Lee KS, Kim JS, Min KJ, Graff JM (2013) Adenosine nucleotide biosynthesis and AMPK regulate adult life span and mediate the longevity benefit of caloric restriction in flies. Cell Metab 17:101–112

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stoleru D, Nawathean P, Fernandez MP, Menet JS, Ceriani MF, Rosbash M (2007) The Drosophila circadian network is a seasonal timer. Cell 129:207–219

    Article  CAS  PubMed  Google Scholar 

  • Stroumbakis ND, Li Z, Tolias PP (1996) A homolog of human transcription factor NF-X1 encoded by the Drosophila shuttle craft gene is required in the embryonic central nervous system. Mol Cell Biol 16:192–201

    Google Scholar 

  • Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–110

    Article  CAS  PubMed  Google Scholar 

  • Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299:1346–1351

    Article  CAS  PubMed  Google Scholar 

  • Tea JS, Chihara T, Luo L (2010) Histone deacetylase Rpd3 regulates olfactory projection neuron Dendrite targeting via the transcription factor Prospero. J Neurosci 30:9939–9946

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thor S, Andersson SGE, Tomlinson A, Thomas JB (1999) A LIM-homodomain combinatorial code for motorneuron pathway selection. Nature 397:76–80

    Article  CAS  PubMed  Google Scholar 

  • Toba G, Yamamoto D, White K (2010) Life-span phenotypes of elav and Rbp9 in Drosophila suggest functional cooperation of the two ELAV-family protein genes. Arch Insect Biochem Physiol 74:261–265

    Article  CAS  PubMed  Google Scholar 

  • Tolias PP, Stroumbakis ND (1998) The Drosophila zygotic lethal gene shuttle craft is required maternally for proper embryonic development. Dev Genes Evol 208:274–282

    Article  CAS  PubMed  Google Scholar 

  • Tong JJ, Schriner SE, McCleary D, Day BJ, Wallace DC (2007) Life extension through neurofibromin mitochondrial regulation and antioxidant therapy for neurofibromatosis-1 in Drosophila melanogaster. Nat Genet 39:476–485

    Article  CAS  PubMed  Google Scholar 

  • Trostnikov MV, Roshina NV, Symonenko AV, Pasyukova EG (2014) GSK-3 beta affects survival and synaptic function in Drosophila melanogaster. In: Abstract book of the 3rd international conference “genetics of aging and longevity”, Russia, Sochi, 6–10 Apr, p 54

    Google Scholar 

  • Troulinaki K, Bano D (2012) Mitochondrial deficiency: a double-edged sword for aging and neurodegeneration. Front Genet 3:244

    Article  PubMed Central  PubMed  Google Scholar 

  • Trout WE, Kaplan WD (1970) A relation between longevity, metabolic rate, and activity in Shaker mutants of Drosophila melanogaster. Exp Gerontol 5:83–92

    Article  CAS  PubMed  Google Scholar 

  • Tsai PI, Wang M, Kao HH, Cheng YJ, Walker JA, Chen RH, Chien CT (2012) Neurofibromin mediates FAK signaling in confining synapse growth at Drosophila neuromuscular junctions. J Neurosci 32:16971–16981

    Article  CAS  PubMed  Google Scholar 

  • Udolph G, Rath P, Tio M, Toh J, Fang W, Pandey R, Technau GM, Chia W (2009) On the roles of Notch, Delta, kuzbanian, and inscuteable during the development of Drosophila embryonic neuroblast lineages. Dev Biol 336:156–168

    Article  CAS  PubMed  Google Scholar 

  • Ueda A, Wu CF (2006) Distinct frequency-dependent regulation of nerve terminal excitability and synaptic transmission by IA and IK potassium channels revealed by Drosophila Shaker and Shab mutations. J Neurosci 26:6238–6248

    Article  CAS  PubMed  Google Scholar 

  • van Dam TJ, Zwartkruis FJ, Bos JL, Snel B (2011) Evolution of the TOR pathway. J Mol Evol 73:209–220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Villeponteau B (1997) The heterochromatin loss model of aging. Exp Gerontol 32:383–394

    Article  CAS  PubMed  Google Scholar 

  • Wang MC, Bohmann D, Jasper H (2003) JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 5:811–816

    Article  CAS  PubMed  Google Scholar 

  • Wilson GF, Wang Z, Chouinard SW, Griffith LC, Ganetzky B (1998) Interaction of the K channel beta subunit, hyperkinetic, with eag family members. J Biol Chem 273:6389–6394

    Article  CAS  PubMed  Google Scholar 

  • Wodarz A, Ramrath A, Kuchinke U, Knust E (1999) Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402:544–547

    Article  CAS  PubMed  Google Scholar 

  • Wodarz A, Ramrath A, Grimm A, Knust E (2000) Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J Cell Biol 150:1361–1374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wong JJ, Li S, Lim EK, Wang Y, Wang C, Zhang H, Kirilly D, Wu C, Liou YC, Wang H, Yu F (2013) A Cullin1-based SCF E3 ubiquitin ligase targets the InR/PI3K/TOR pathway to regulate neuronal pruning. PLoS Biol 11:e1001657

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamazaki D, Horiuchi J, Nakagami Y, Nagano S, Tamura T, Saitoe M (2007) The Drosophila DCO mutation suppresses age-related memory impairment without affecting lifespan. Nat Neurosci 10:478–484

    CAS  PubMed  Google Scholar 

  • Yu F, Morin X, Cai Y, Yang X, Chia W (2000) Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100:399–409

    Article  CAS  PubMed  Google Scholar 

  • Yu F, Cai Y, Kaushik R, Yang X, Chia W (2003) Distinct roles of Galphai and Gbeta13F subunits of the heterotrimeric G protein complex in the mediation of Drosophila neuroblast asymmetric divisions. J Cell Biol 162:623–633

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu F, Wang H, Qian H, Kaushik R, Bownes M, Yang X, Chia W (2005) Locomotion defects, together with Pins, regulates heterotrimeric G-protein signaling during Drosophila neuroblast asymmetric divisions. Genes Dev 19:1341–1353

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zaitsev AA, Symonenko AV, Roshina NV, Pasyukova EG (2010) Involvement of the escargot gene of Drosophila melanogaster in lifespan control. Proc Tomsk State Univ 275:402–404

    Google Scholar 

  • Zhong Y, Wu CF (2004) Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J Neurosci 24:1439–1445

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zid BM, Rogers AN, Katewa SD, Vargas MA, Kolipinski MC, Lu TA, Benzer S, Kapahi P (2009) 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139:149–160

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

Authors are supported by the Presidium of the Russian Academy of Sciences Program “Biodiversity of natural systems” and the Russian Foundation for Basic Research grants #14-04-01464-a and #15-04-05797-a.

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Pasyukova, E., Symonenko, A., Roshina, N., Trostnikov, M., Veselkina, E., Rybina, O. (2015). Neuronal Genes and Developmental Neuronal Pathways in Drosophila Life Span Control. In: Vaiserman, A., Moskalev, A., Pasyukova, E. (eds) Life Extension. Healthy Ageing and Longevity, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-18326-8_1

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