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Neuronal Genes and Developmental Neuronal Pathways in Drosophila Life Span Control

  • Elena PasyukovaEmail author
  • Alexander Symonenko
  • Natalia Roshina
  • Mikhail Trostnikov
  • Ekaterina Veselkina
  • Olga Rybina
Chapter
Part of the Healthy Ageing and Longevity book series (HAL, volume 3)

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.

Keywords

Nervous system Neuronal genes Drosophila Life span Transcription factors 

Notes

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.

References

  1. Alcedo J, Flatt T, Pasyukova EG (2013) Neuronal inputs and outputs of aging and longevity. Front Genet 4:71PubMedCentralPubMedGoogle Scholar
  2. 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 10:137–147PubMedCentralPubMedCrossRefGoogle Scholar
  3. 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 128:4757–4767PubMedGoogle Scholar
  4. 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 18:6426–6638PubMedCentralPubMedCrossRefGoogle Scholar
  5. Atwood SX, Prehoda KE (2009) aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr Biol 19:723–729PubMedCentralPubMedCrossRefGoogle Scholar
  6. Baines RA (2004) Synaptic strengthening mediated by bone morphogenetic protein-dependent retrograde signaling in the Drosophila CNS. J Neurosci 24:6904–6911PubMedCrossRefGoogle Scholar
  7. 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 104:13355–13360CrossRefGoogle Scholar
  8. 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 15:2063–2068PubMedCrossRefGoogle Scholar
  9. 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 104:13355–13360PubMedCentralPubMedCrossRefGoogle Scholar
  10. 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 131:193–201PubMedCentralPubMedCrossRefGoogle Scholar
  11. Betschinger J, Mechtler K, Knoblich JA (2003) The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422:326–330PubMedCrossRefGoogle Scholar
  12. Biteau B, Karpac J, Supoyo S, Degennaro M, Lehmann R, Jasper H (2010) Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet 6:e1001159PubMedCentralPubMedCrossRefGoogle Scholar
  13. Blagosklonny MV (2009) Validation of anti-aging drugs by treating age-related diseases. Aging (Albany NY) 1:281–288Google Scholar
  14. Broughton S, Partridge L (2009) Insulin/IGF-like signalling, the central nervous system and aging. Biochem J 418:1–12PubMedCrossRefGoogle Scholar
  15. 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 102:3105–3110PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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:e3721PubMedCentralPubMedCrossRefGoogle Scholar
  17. Buchanan ME, Davis RL (2010) A distinct set of Drosophila brain neurons required for neurofibromatosis type 1-dependent learning and memory. J Neurosci 30:10135–10143PubMedCentralPubMedCrossRefGoogle Scholar
  18. 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 403:895–898CrossRefGoogle Scholar
  19. Budnik V, Zhong Y, Wu C-F (1990) Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurosci 10:3754–3768PubMedGoogle Scholar
  20. Byers D, Davis RL, Kiger JA Jr (1981) Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289:79–81Google Scholar
  21. 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 20:1704–1714PubMedCentralPubMedCrossRefGoogle Scholar
  22. 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):51–62PubMedCrossRefGoogle Scholar
  23. 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 16:912–919PubMedCrossRefGoogle Scholar
  24. Certel SJ, Thor S (2004) Specification of Drosophila motoneuron identity by the combinatorial action of POU and LIM-HD factors. Development 131:5429–5439PubMedCrossRefGoogle Scholar
  25. 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 19:778–785PubMedCrossRefGoogle Scholar
  26. Colosimo PF, Liu X, Kaplan NA, Tolwinski NS (2010) GSK3beta affects apical-basal polarity and cell-cell adhesion by regulating aPKC levels. Dev Dyn 239:115–125PubMedGoogle Scholar
  27. 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 10:599–602PubMedCrossRefGoogle Scholar
  28. 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 124:341–349PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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 108:8059–8064PubMedCentralPubMedCrossRefGoogle Scholar
  30. 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 34:429–433PubMedCrossRefGoogle Scholar
  31. Demontis F, Perrimon N (2010) FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143:813–825PubMedCentralPubMedCrossRefGoogle Scholar
  32. 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:e30722PubMedCentralPubMedCrossRefGoogle Scholar
  33. Drain P, Folkers E, Quinn WG (1991) cAMP-dependent protein kinase and the disruption of learning in transgenic flies. Neuron 6:71–82PubMedCrossRefGoogle Scholar
  34. Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S (1976) dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci USA 73:1684–1688PubMedCentralPubMedCrossRefGoogle Scholar
  35. 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:e15780PubMedCentralPubMedCrossRefGoogle Scholar
  36. Feng Z (2010) p53 regulation of the IGF-1/AKT/mTOR pathways and the endosomal compartment. Cold Spring Harb Perspect Biol 2:a001057PubMedCentralPubMedCrossRefGoogle Scholar
  37. 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 105:6368–6373PubMedCentralPubMedCrossRefGoogle Scholar
  38. 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 180:2057–2071PubMedCentralPubMedCrossRefGoogle Scholar
  39. 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 24:6573–6577PubMedCrossRefGoogle Scholar
  40. Frankel S, Rogina B (2005) Drosophila longevity is not affected by heterochromatin-mediated gene silencing. Aging Cell 4:53–56PubMedCrossRefGoogle Scholar
  41. 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 1:145–152PubMedCrossRefGoogle Scholar
  42. 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) 1:699–713Google Scholar
  43. 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 65:516–529CrossRefGoogle Scholar
  44. Giannakou ME, Goss M, Jünger MA, Hafen E, Leevers SJ, Partridge L (2004) Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305:361PubMedCrossRefGoogle Scholar
  45. Grönke S, Clarke DF, Broughton S, Andrews TD, Partridge L (2010) Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet 6:e1000857PubMedCentralPubMedCrossRefGoogle Scholar
  46. 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 9:3063–3071PubMedCentralPubMedCrossRefGoogle Scholar
  47. Hobert O (2011) Regulation of terminal differentiation programs in the nervous system. Annu Rev Cell Dev Biol 27:681–696PubMedCrossRefGoogle Scholar
  48. 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 44:316–327PubMedCentralPubMedCrossRefGoogle Scholar
  49. 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 429:562–566PubMedCrossRefGoogle Scholar
  50. Inoki K, Guan KL (2006) Complexity of the TOR signaling network. Trends Cell Biol 16:206–212PubMedCrossRefGoogle Scholar
  51. 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 24:3793–3806PubMedCentralPubMedCrossRefGoogle Scholar
  52. 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 14:885–890PubMedCentralPubMedCrossRefGoogle Scholar
  53. 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 11:453–465PubMedCentralPubMedCrossRefGoogle Scholar
  54. Kaplan NA, Colosimo PF, Liu X, Tolwinski NS (2011) Complex interactions between GSK3 and aPKC in Drosophila embryonic epithelial morphogenesis. PLoS ONE 6:e18616PubMedCentralPubMedCrossRefGoogle Scholar
  55. Katewa SD, Kapahi P (2011) Role of TOR signaling in aging and related biological processes in Drosophila melanogaster. Exp Gerontol 46:382–390PubMedCentralPubMedCrossRefGoogle Scholar
  56. 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 69:365–377PubMedCrossRefGoogle Scholar
  57. 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 28:3879–3892PubMedCentralPubMedCrossRefGoogle Scholar
  58. Kraut R, Campos-Ortega JA (1996) Inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adaptor protein. Dev Biol 174:65–81PubMedCrossRefGoogle Scholar
  59. Kraut R, Chia W, Jan LY, Jan YN, Knoblich JA (1996) Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383:50–55PubMedCrossRefGoogle Scholar
  60. Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA 104:3574–3578PubMedCentralPubMedCrossRefGoogle Scholar
  61. 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:e1002473PubMedCentralPubMedCrossRefGoogle Scholar
  62. 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 284:29454–29461PubMedCentralPubMedCrossRefGoogle Scholar
  63. Li J, Li W, Calhoun HC, Xia F, Gao FB, Li W (2003) Patterns and functions of STAT activation during Drosophila embryogenesis. Mech Dev 120:1455–1468PubMedCentralPubMedCrossRefGoogle Scholar
  64. 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 376:637–641PubMedCrossRefGoogle Scholar
  65. 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 315:1133–1137PubMedCrossRefGoogle Scholar
  66. 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 10:438–447PubMedCrossRefGoogle Scholar
  67. Lin YR, Parikh H, Park Y (2011b) Loco signaling pathway in longevity. Small GTPases 2:158–161PubMedCentralPubMedCrossRefGoogle Scholar
  68. Livingstone MS, Tempel BL (1983) Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 303:67–70PubMedCrossRefGoogle Scholar
  69. 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 25:7078–7091PubMedCentralPubMedCrossRefGoogle Scholar
  70. Madeo F, Tavernarakis N, Kroemer G (2010) Can autophagy promote longevity? Nat Cell Biol 12:842–846PubMedCrossRefGoogle Scholar
  71. 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:e1001037PubMedCentralPubMedCrossRefGoogle Scholar
  72. 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 105:165–176PubMedCrossRefGoogle Scholar
  73. 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 26:10199–10208PubMedCrossRefGoogle Scholar
  74. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765–1768PubMedCrossRefGoogle Scholar
  75. Min KJ, Yamamoto R, Buch S, Pankratz M, Tatar M (2008) Drosophila lifespan control by dietary restriction independent of insulin-like signaling. Aging Cell 7:199–206PubMedCentralPubMedCrossRefGoogle Scholar
  76. 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 18:598–609PubMedGoogle Scholar
  77. 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 9:522–530PubMedCrossRefGoogle Scholar
  78. Mukunda L, Miazzi F, Kaltofen S, Hansson BS, Wicher D (2014) Calmodulin modulates insect odorant receptor function. Cell Calcium 55:191–199PubMedCrossRefGoogle Scholar
  79. Nässel DR, Winther AM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104PubMedCrossRefGoogle Scholar
  80. Nässel DR, Kubrak OI, Liu Y, Luo J, Lushchak OV (2013) Factors that regulate insulin producing cells and their output in Drosophila. Front Physiol 4:252PubMedCentralPubMedCrossRefGoogle Scholar
  81. Natarajan R, Trivedi-Vyas D, Wairkar YP (2013) Tuberous sclerosis complex regulates Drosophila neuromuscular junction growth via the TORC2/Akt pathway. Hum Mol Genet 22:2010–2023PubMedCrossRefGoogle Scholar
  82. Noble W, Hanger DP, Miller CC, Lovestone S (2013) The importance of tau phosphorylation for neurodegenerative diseases. Front Neurol 4:83PubMedCentralPubMedCrossRefGoogle Scholar
  83. 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 94:9734–9739PubMedCentralPubMedCrossRefGoogle Scholar
  84. 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 278:26418–26422PubMedCrossRefGoogle Scholar
  85. 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:e28098PubMedCentralPubMedCrossRefGoogle Scholar
  86. 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 237:749–753PubMedCrossRefGoogle Scholar
  87. Parkes TL, Hilliker AJ, Phillips JP (1999) Motorneurons, reactive oxygen, and life span in Drosophila. Neurobiol Aging 20:531–535PubMedCrossRefGoogle Scholar
  88. 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 20:820–835PubMedCentralPubMedCrossRefGoogle Scholar
  89. 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 63:788–802PubMedCentralPubMedCrossRefGoogle Scholar
  90. Partridge L, Alic N, Bjedov I, Piper MD (2011) Ageing in Drosophila: the role of the insulin/Igf and TOR signalling network. Exp Gerontol 46:376–381PubMedCentralPubMedCrossRefGoogle Scholar
  91. Pasyukova EG, Vieira C, Mackay TFC (2000) Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156:1129–1146PubMedCentralPubMedGoogle Scholar
  92. Pasyukova EG, Roshina NV, Mackay TFC (2004) Shuttle craft: a candidate quantitative trait gene for Drosophila lifespan. Aging Cell 3:297–307PubMedCrossRefGoogle Scholar
  93. Plyusnina EN, Shaposhnikov MV, Moskalev AA (2011) Increase of Drosophila melanogaster lifespan due to D-GADD45 overexpression in the nervous system. Biogerontology 12:211–226PubMedCrossRefGoogle Scholar
  94. Poon PC, Kuo TH, Linford NJ, Roman G, Pletcher SD (2010) Carbon dioxide sensing modulates lifespan and physiology in Drosophila. PLoS Biol 8:e1000356PubMedCentralPubMedCrossRefGoogle Scholar
  95. Puig O, Mattila J (2011) Understanding Forkhead box class O function: lessons from Drosophila melanogaster. Antioxid Redox Signal 14:635–647PubMedCrossRefGoogle Scholar
  96. Rana A, Rera M, Walker DW (2013) Parkin overexpression during aging reduces proteotoxicity, alters mitochondrial dynamics, and extends lifespan. Proc Natl Acad Sci USA 110:8638–8643PubMedCentralPubMedCrossRefGoogle Scholar
  97. Reenan RA, Rogina B (2008) Acquired temperature-sensitive paralysis as a biomarker of declining neuronal function in aging Drosophila. Aging Cell 7:179–186PubMedCrossRefGoogle Scholar
  98. 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 25:139–149PubMedCrossRefGoogle Scholar
  99. 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 20:3980–3992PubMedGoogle Scholar
  100. Robinow S, White K (1988) The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev Biol 126:294–303PubMedCrossRefGoogle Scholar
  101. Robinow S, White K (1991) Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J Neurobiol 22:443–461PubMedCrossRefGoogle Scholar
  102. Rogina B, Helfand SL (1995) Regulation of gene expression is linked to life span in adult Drosophila. Genetics 141:1043–1048PubMedCentralPubMedGoogle Scholar
  103. Rogina B, Helfand SL, Frankel S (2002) Longevity regulation by Drosophila Rpd3 deacetylase and caloric restriction. Science 298:1745PubMedCrossRefGoogle Scholar
  104. 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 59:311–321PubMedCentralPubMedCrossRefGoogle Scholar
  105. Roshina NV, Pasyukova EG (2007) Genes regulating the development and functioning of the nervous system determine life span in Drosophila melanogaster. Russ J Genet 43:356–362CrossRefGoogle Scholar
  106. 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) 6:1076–1093Google Scholar
  107. 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 99:2748–2753PubMedCentralPubMedCrossRefGoogle Scholar
  108. 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 42:567–580PubMedPubMedCentralCrossRefGoogle Scholar
  109. 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:e12621PubMedCentralPubMedCrossRefGoogle Scholar
  110. 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 10:353–362PubMedCrossRefGoogle Scholar
  111. 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 2:271–281PubMedCrossRefGoogle Scholar
  112. 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:e1000111PubMedCentralPubMedCrossRefGoogle Scholar
  113. 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 107:169–174PubMedCentralPubMedCrossRefGoogle Scholar
  114. 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 4:176–184PubMedCrossRefGoogle Scholar
  115. Skeath JB, Thor S (2003) Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol 13:8–15PubMedCrossRefGoogle Scholar
  116. 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 11:197–208PubMedCrossRefGoogle Scholar
  117. 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 26:468–480PubMedCentralPubMedCrossRefGoogle Scholar
  118. 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 26:612–1625Google Scholar
  119. 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 141:629–655PubMedCentralPubMedGoogle Scholar
  120. 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 153:361–382PubMedCentralPubMedGoogle Scholar
  121. 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 17:101–112PubMedCentralPubMedCrossRefGoogle Scholar
  122. Stoleru D, Nawathean P, Fernandez MP, Menet JS, Ceriani MF, Rosbash M (2007) The Drosophila circadian network is a seasonal timer. Cell 129:207–219PubMedCrossRefGoogle Scholar
  123. 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 16:192–201Google Scholar
  124. 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 292:107–110PubMedCrossRefGoogle Scholar
  125. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299:1346–1351PubMedCrossRefGoogle Scholar
  126. Tea JS, Chihara T, Luo L (2010) Histone deacetylase Rpd3 regulates olfactory projection neuron Dendrite targeting via the transcription factor Prospero. J Neurosci 30:9939–9946PubMedCentralPubMedCrossRefGoogle Scholar
  127. Thor S, Andersson SGE, Tomlinson A, Thomas JB (1999) A LIM-homodomain combinatorial code for motorneuron pathway selection. Nature 397:76–80PubMedCrossRefGoogle Scholar
  128. 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 74:261–265PubMedCrossRefGoogle Scholar
  129. Tolias PP, Stroumbakis ND (1998) The Drosophila zygotic lethal gene shuttle craft is required maternally for proper embryonic development. Dev Genes Evol 208:274–282PubMedCrossRefGoogle Scholar
  130. 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 39:476–485PubMedCrossRefGoogle Scholar
  131. 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 54Google Scholar
  132. Troulinaki K, Bano D (2012) Mitochondrial deficiency: a double-edged sword for aging and neurodegeneration. Front Genet 3:244PubMedCentralPubMedCrossRefGoogle Scholar
  133. Trout WE, Kaplan WD (1970) A relation between longevity, metabolic rate, and activity in Shaker mutants of Drosophila melanogaster. Exp Gerontol 5:83–92PubMedCrossRefGoogle Scholar
  134. 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 32:16971–16981PubMedCrossRefGoogle Scholar
  135. 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 336:156–168PubMedCrossRefGoogle Scholar
  136. 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 26:6238–6248PubMedCrossRefGoogle Scholar
  137. van Dam TJ, Zwartkruis FJ, Bos JL, Snel B (2011) Evolution of the TOR pathway. J Mol Evol 73:209–220PubMedCentralPubMedCrossRefGoogle Scholar
  138. Villeponteau B (1997) The heterochromatin loss model of aging. Exp Gerontol 32:383–394PubMedCrossRefGoogle Scholar
  139. Wang MC, Bohmann D, Jasper H (2003) JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 5:811–816PubMedCrossRefGoogle Scholar
  140. 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 273:6389–6394PubMedCrossRefGoogle Scholar
  141. Wodarz A, Ramrath A, Kuchinke U, Knust E (1999) Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402:544–547PubMedCrossRefGoogle Scholar
  142. 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 150:1361–1374PubMedCentralPubMedCrossRefGoogle Scholar
  143. 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:e1001657PubMedCentralPubMedCrossRefGoogle Scholar
  144. 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 10:478–484PubMedGoogle Scholar
  145. 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 100:399–409PubMedCrossRefGoogle Scholar
  146. 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 162:623–633PubMedCentralPubMedCrossRefGoogle Scholar
  147. 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 19:1341–1353PubMedCentralPubMedCrossRefGoogle Scholar
  148. Zaitsev AA, Symonenko AV, Roshina NV, Pasyukova EG (2010) Involvement of the escargot gene of Drosophila melanogaster in lifespan control. Proc Tomsk State Univ 275:402–404Google Scholar
  149. Zhong Y, Wu CF (2004) Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J Neurosci 24:1439–1445PubMedCentralPubMedCrossRefGoogle Scholar
  150. 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 139:149–160PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Elena Pasyukova
    • 1
    Email author
  • Alexander Symonenko
    • 1
  • Natalia Roshina
    • 1
  • Mikhail Trostnikov
    • 1
  • Ekaterina Veselkina
    • 1
  • Olga Rybina
    • 1
  1. 1.Institute of Molecular Genetics of RASMoscowRussia

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