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

PLoS Genetics

Volumn 10, Issue 6, 2014, Pages

  Chihara, Takahiro ^a,b   Kitabayashi, Aki ^a   Morimoto, Michie ^a   Takeuchi, Ken ichi ^a   Masuyama, Kaoru ^c   Tonoki, Ayako ^d,e   Davis, Ronald L ^d   Wang, Jing W ^c   Miura, Masayuki ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; PROTEIN P35; DROSOPHILA PROTEIN; OLFACTORY RECEPTOR; OR42B PROTEIN, DROSOPHILA; OR92A PROTEIN, DROSOPHILA;

ADULT; AGED; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL TISSUE; ANTENNA (ORGAN); APOPTOSIS; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; LIFESPAN; MALE; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY MEMORY; OLFACTORY RECEPTOR; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPATIOTEMPORAL ANALYSIS; AGING; ANIMAL; BIOSYNTHESIS; BRAIN MAPPING; CHEMOTAXIS; DENDRITE; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALUS; ODOR; OLFACTORY RECEPTOR NEURON; PHYSIOLOGY; SYNAPTIC TRANSMISSION; TRANSGENIC ANIMAL;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BEHAVIOR, ANIMAL; BRAIN MAPPING; CASPASE 3; CHEMOTAXIS; DENDRITES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MALUS; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; SMELL; SYNAPTIC TRANSMISSION;

EID: 84903451573     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004437     Document Type: Article

References (45)

1. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, et al. (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325: 201-204.
2. Libert S, Zwiener J, Chu X, Vanvoorhies W, Roman G, et al. (2007) Regulation of Drosophila life span by olfaction and food-derived odors. Science 315: 1133-1137.
3. Tonoki A, Davis RL, (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. Kuranaga E, Miura M, (2007) Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 17: 135-144.
5. Bergmann A, Steller H, (2010) Apoptosis, stem cells, and tissue regeneration. Sci Signal 3: re8.
6. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, et al. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94: 325-337.
7. Kuida K, Zheng TS, Na S, Kuan C, Yang D, et al. (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384: 368-372.
8. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, et al. (1998) Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94: 339-352.
9. Yoshida H, Kong YY, Yoshida R, Elia AJ, Hakem A, et al. (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94: 739-750.
10. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P, (1998) Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94: 727-737.
11. Nonomura K, Yamaguchi Y, Hamachi M, Koike M, Uchiyama Y, et al. (2013) Local apoptosis modulates early mammalian brain development through the elimination of morphogen-producing cells. Dev Cell 27: 621-634.
12. D'Amelio M, Cavallucci V, Cecconi F, (2009) Neuronal caspase-3 signaling: not only cell death. Cell Death Differ 17: 1104-1114.
13. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW, (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9: 1234-1236.
14. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN, (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51: 283-290.
15. Huesmann GR, Clayton DF, (2006) Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron 52: 1061-1072.
16. Thompson CK, Brenowitz EA, (2008) Caspase inhibitor infusion protects an avian song control circuit from seasonal-like neurodegeneration. J Neurosci 28: 7130-7136.
17. Li Z, Jo J, Jia JM, Lo SC, Whitcomb DJ, et al. (2010) Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141: 859-871.
18. Jiao S, Li Z, (2011) Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 70: 758-772.
19. Ohsawa S, Hamada S, Kuida K, Yoshida H, Igaki T, 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'Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, et al. (2011) Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 14: 69-76.
21. Jo J, Whitcomb DJ, Olsen KM, Kerrigan TL, Lo SC, 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. Jefferis GS, Hummel T, (2006) Wiring specificity in the olfactory system. Semin Cell Dev Biol 17: 50-65.
23. Wu CL, Xia S, Fu TF, Wang H, Chen YH, et al. (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10: 1578-1586.
24. Ofstad TA, Zuker CS, Reiser MB, (2011) Visual place learning in Drosophila melanogaster. Nature 474: 204-207.
25. Semmelhack JL, Wang JW, (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459: 218-223.
26. Kato K, Awasaki T, Ito K, (2009) Neuronal programmed cell death induces glial cell division in the adult Drosophila brain. Development 136: 51-59.
27. Quinn LM, Dorstyn L, Mills K, Colussi PA, Chen P, et al. (2000) An essential role for the caspase dronc in developmentally programmed cell death in Drosophila. J Biol Chem 275: 40416-40424.
28. Siegrist SE, Haque NS, Chen CH, Hay BA, Hariharan IK, (2010) Inactivation of both Foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr Biol 20: 643-648.
29. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R, (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271-282.
30. Yamazaki D, Horiuchi J, Nakagami Y, Nagano S, Tamura T, et al. (2007) The Drosophila DCO mutation suppresses age-related memory impairment without affecting lifespan. Nat Neurosci 10: 478-484.
31. Chiang A, Priya R, Ramaswami M, Vijayraghavan K, Rodrigues V, (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. Tonoki A, Kuranaga E, Ito N, Nekooki-Machida Y, Tanaka M, et al. (2011) Aging causes distinct characteristics of polyglutamine amyloids in vivo. Genes Cells 16: 557-564.
33. Florentin A, Arama E, (2012) Caspase levels and execution efficiencies determine the apoptotic potential of the cell. J Cell Biol 196: 513-527.
34. Schoenmann Z, Assa-Kunik E, Tiomny S, Minis A, Haklai-Topper L, 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. Stokl J, Strutz A, Dafni A, Svatos A, Doubsky J, et al. (2010) A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast. Curr Biol 20: 1846-1852.
36. Richard MB, Taylor SR, Greer CA, (2010) Age-induced disruption of selective olfactory bulb synaptic circuits. Proc Natl Acad Sci U S A 107: 15613-15618.
37. Ohsawa S, Hamada S, Asou H, Kuida K, Uchiyama Y, 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. Sweeney LB, Couto A, Chou YH, Berdnik D, Dickson BJ, et al. (2007) Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 53: 185-200.
39. Jefferis GS, Marin EC, Stocker RF, Luo L, (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414: 204-208.
40. Zhou L, Schnitzler A, Agapite J, Schwartz LM, Steller H, 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. Lee T, Luo L, (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461.
42. Koto A, Kuranaga E, Miura M, (2009) Temporal regulation of Drosophila IAP1 determines caspase functions in sensory organ development. J Cell Biol 187: 219-231.
43. Lai SL, Lee T, (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9: 703-709.
44. Wu JS, Luo L, (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1: 2110-2115.
45. Root CM, Masuyama K, Green DS, Enell LE, Nassel DR, et al. (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59: 311-321.