Caspase Inhibition in Select Olfactory Neurons Restores Innate Attraction Behavior in Aged

English version České info

The approaching era of an “aging society” is receiving considerable attention amongst biomedical researchers in advanced nations. In order to understand the molecular mechanisms underlying age-related alterations of neural circuitry, we focused on caspase-3, a cysteine protease that induces apoptotic cell death, using the fruit fly Drosophila melanogaster, a model often used to study aging due to a short lifespan of approximately 30–60 days. Here, we describe the spatiotemporal activation of caspase-3 in aged fly brains and show that caspase-3 is specifically activated in select olfactory neurons essential for innate odor attraction behavior. Furthermore, we discuss how inhibition of caspase-3 activation in those select olfactory neurons can rejuvenate the sensitivity of innate attraction behavior in aged flies. These findings suggest that caspase-3 plays an active role in producing age-related alterations to neuronal physiology and circuit function associated with animal behavior.

Vyšlo v časopise: Caspase Inhibition in Select Olfactory Neurons Restores Innate Attraction Behavior in Aged. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004437
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004437

Souhrn

Zdroje

1. ColmanRJ, AndersonRM, JohnsonSC, KastmanEK, KosmatkaKJ, et al. (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325: 201–204.

2. LibertS, ZwienerJ, ChuX, VanvoorhiesW, RomanG, et al. (2007) Regulation of Drosophila life span by olfaction and food-derived odors. Science 315: 1133–1137.

3. TonokiA, DavisRL (2012) Aging impairs intermediate-term behavioral memory by disrupting the dorsal paired medial neuron memory trace. Proc Natl Acad Sci U S A 109: 6319–6324.

4. KuranagaE, MiuraM (2007) Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 17: 135–144.

5. BergmannA, StellerH (2010) Apoptosis, stem cells, and tissue regeneration. Sci Signal 3: re8.

6. KuidaK, HaydarTF, KuanCY, GuY, TayaC, et al. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94: 325–337.

7. KuidaK, ZhengTS, NaS, KuanC, YangD, et al. (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384: 368–372.

8. HakemR, HakemA, DuncanGS, HendersonJT, WooM, et al. (1998) Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94: 339–352.

9. YoshidaH, KongYY, YoshidaR, EliaAJ, HakemA, et al. (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94: 739–750.

10. CecconiF, Alvarez-BoladoG, MeyerBI, RothKA, GrussP (1998) Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94: 727–737.

11. NonomuraK, YamaguchiY, HamachiM, KoikeM, UchiyamaY, et al. (2013) Local apoptosis modulates early mammalian brain development through the elimination of morphogen-producing cells. Dev Cell 27: 621–634.

12. D'AmelioM, CavallucciV, CecconiF (2009) Neuronal caspase-3 signaling: not only cell death. Cell Death Differ 17: 1104–1114.

13. WilliamsDW, KondoS, KrzyzanowskaA, HiromiY, TrumanJW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9: 1234–1236.

14. KuoCT, ZhuS, YoungerS, JanLY, JanYN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51: 283–290.

15. HuesmannGR, ClaytonDF (2006) Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron 52: 1061–1072.

16. ThompsonCK, BrenowitzEA (2008) Caspase inhibitor infusion protects an avian song control circuit from seasonal-like neurodegeneration. J Neurosci 28: 7130–7136.

17. LiZ, JoJ, JiaJM, LoSC, WhitcombDJ, et al. (2010) Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141: 859–871.

18. JiaoS, LiZ (2011) Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 70: 758–772.

19. OhsawaS, HamadaS, KuidaK, YoshidaH, IgakiT, et al. (2010) Maturation of the olfactory sensory neurons by Apaf-1/caspase-9-mediated caspase activity. Proc Natl Acad Sci U S A 107: 13366–13371.

20. D'AmelioM, CavallucciV, MiddeiS, MarchettiC, PacioniS, et al. (2011) Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 14: 69–76.

21. JoJ, WhitcombDJ, OlsenKM, KerriganTL, LoSC, et al. (2011) Abeta(1-42) inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3beta. Nat Neurosci 14: 545–547.

22. JefferisGS, HummelT (2006) Wiring specificity in the olfactory system. Semin Cell Dev Biol 17: 50–65.

23. WuCL, XiaS, FuTF, WangH, ChenYH, et al. (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10: 1578–1586.

24. OfstadTA, ZukerCS, ReiserMB (2011) Visual place learning in Drosophila melanogaster. Nature 474: 204–207.

25. SemmelhackJL, WangJW (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459: 218–223.

26. KatoK, AwasakiT, ItoK (2009) Neuronal programmed cell death induces glial cell division in the adult Drosophila brain. Development 136: 51–59.

27. QuinnLM, DorstynL, MillsK, ColussiPA, ChenP, et al. (2000) An essential role for the caspase dronc in developmentally programmed cell death in Drosophila. J Biol Chem 275: 40416–40424.

28. SiegristSE, HaqueNS, ChenCH, HayBA, HariharanIK (2010) Inactivation of both Foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr Biol 20: 643–648.

29. WangJW, WongAM, FloresJ, VosshallLB, AxelR (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271–282.

30. YamazakiD, HoriuchiJ, NakagamiY, NaganoS, TamuraT, et al. (2007) The Drosophila DCO mutation suppresses age-related memory impairment without affecting lifespan. Nat Neurosci 10: 478–484.

31. ChiangA, PriyaR, RamaswamiM, VijayraghavanK, RodriguesV (2009) Neuronal activity and Wnt signaling act through Gsk3-beta to regulate axonal integrity in mature Drosophila olfactory sensory neurons. Development 136: 1273–1282.

32. TonokiA, KuranagaE, ItoN, Nekooki-MachidaY, TanakaM, et al. (2011) Aging causes distinct characteristics of polyglutamine amyloids in vivo. Genes Cells 16: 557–564.

33. FlorentinA, AramaE (2012) Caspase levels and execution efficiencies determine the apoptotic potential of the cell. J Cell Biol 196: 513–527.

34. SchoenmannZ, Assa-KunikE, TiomnyS, MinisA, Haklai-TopperL, et al. (2010) Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J Neurosci 30: 6375–6386.

35. StoklJ, StrutzA, DafniA, SvatosA, DoubskyJ, et al. (2010) A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast. Curr Biol 20: 1846–1852.

36. RichardMB, TaylorSR, GreerCA (2010) Age-induced disruption of selective olfactory bulb synaptic circuits. Proc Natl Acad Sci U S A 107: 15613–15618.

37. OhsawaS, HamadaS, AsouH, KuidaK, UchiyamaY, et al. (2009) Caspase-9 activation revealed by semaphorin 7A cleavage is independent of apoptosis in the aged olfactory bulb. J Neurosci 29: 11385–11392.

38. SweeneyLB, CoutoA, ChouYH, BerdnikD, DicksonBJ, et al. (2007) Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 53: 185–200.

39. JefferisGS, MarinEC, StockerRF, LuoL (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414: 204–208.

40. ZhouL, SchnitzlerA, AgapiteJ, SchwartzLM, StellerH, et al. (1997) Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc Natl Acad Sci U S A 94: 5131–5136.

41. LeeT, LuoL (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461.

42. KotoA, KuranagaE, MiuraM (2009) Temporal regulation of Drosophila IAP1 determines caspase functions in sensory organ development. J Cell Biol 187: 219–231.

43. LaiSL, LeeT (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9: 703–709.

44. WuJS, LuoL (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1: 2110–2115.

45. RootCM, MasuyamaK, GreenDS, EnellLE, NasselDR, et al. (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59: 311–321.