Drosophila tao controls mushroom body development and ethanol-stimulated behavior through par-1

Journal of Neuroscience

Volumn 31, Issue 3, 2011, Pages 1139-1148

  King, Ian ^a,e   Tsai, Linus T Y ^a,f   Pflanz, Ralf ^c   Voigt, Aaron ^c,g   Lee, Seongsoo ^d   Jäckle, Herbert ^c   Lu, Bingwei ^d   Heberlein, Ulrike ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

^f HARVARD UNIVERSITY   (United States)

^g UNIVERSITY OF AACHEN MEDICAL CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; COCAINE; DROSOPHILA PROTEIN; NICOTINE; PROTEIN TAO; PROTEINASE ACTIVATED RECEPTOR 1; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; DROSOPHILA; GENE FUNCTION; GENE MUTATION; GENOTYPE; LOCOMOTION; METAMORPHOSIS; MUSHROOM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYSICAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; DROSOPHILA; DROSOPHILA PROTEINS; ETHANOL; HYPERKINESIS; IMMUNOHISTOCHEMISTRY; METAMORPHOSIS, BIOLOGICAL; MOTOR ACTIVITY; MUSHROOM BODIES; NEURONS; PROTEIN-SERINE-THREONINE KINASES;

EID: 78751522556     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4416-10.2011     Document Type: Article

References (39)

1. Aso Y, Grübel K, Busch S, Friedrich AB, Siwanowicz I, Tanimoto H (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23:156-172.
2. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21:1523-1531.
3. Bainton RJ, Tsai LT, Singh CM, Moore MS, Neckameyer WS, Heberlein U (2000) Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10:187-194.
4. Biernat J, Wu YZ, Timm T, Zheng-Fischhöfer Q, Mandelkow E, Meijer L, Mandelkow EM (2002) Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity. Mol Biol Cell 13:4013-4028.
5. Bland ND, Robinson P, Thomas JE, Shirras AD, Turner AJ, Isaac RE (2009) Locomotor and geotactic behavior of Drosophila melanogaster overexpressing neprilysin 2. Peptides 30:571-574.
6. Chen Z, Hutchison M, Cobb MH (1999) Isolation of the protein kinase TAO2 and identification of its mitogen-activated protein kinase/extracellular signal-regulated kinase kinase binding domain. J Biol Chem 274:28803-28807.
7. Chen Z, Raman M, Chen L, Lee SF, Gilman AG, Cobb MH (2003) TAO (thousand-and-one amino acid) protein kinases mediate signaling from carbachol to p38 mitogen-activated protein kinase and ternary complex factors. J Biol Chem 278:22278-22283.
8. Dan I, Watanabe NM, Kusumi A (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11:220-230.
9. Devineni AV, Heberlein U (2009) Preferential ethanol consumption in Drosophila models features of addiction. Curr Biol 19:2126-2132.
10. Guarnieri DJ, Heberlein U (2003) Drosophila melanogaster, a genetic model system for alcohol research. Int Rev Neurobiol 54:199-228.
11. Hoskins RA, Nelson CR, Berman BP, Laverty TR, George RA, Ciesiolka L, Naeemuddin M, Arenson AD, Durbin J, David RG, Tabor PE, Bailey MR, DeShazo DR, Catanese J, Mammoser A, Osoegawa K, de Jong PJ, Celniker SE, Gibbs RA, Rubin GM, et al. (2000) A BAC-based physical map of the major autosomes of Drosophila melanogaster. Science 287:2271-2274.
12. Kong EC, Woo K, Li H, Lebestky T, Mayer N, Sniffen MR, Heberlein U, Bainton RJ, Hirsh J, Wolf FW (2010) A pair of dopamine neurons target the D1-like dopamine receptor DopR in the central complex to promote ethanol-stimulated locomotion in Drosophila. PLoS One 5:e9954.
13. Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-4076.
14. Lin DM, Goodman CS (1994) Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13:507-523.
15. McGuire SE, Mao Z, Davis RL (2004) Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004:pl6.
16. Moore MS, DeZazzo J, Luk AY, Tully T, Singh CM, Heberlein U (1998) Ethanol intoxication in Drosophila: genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93:997-1007.
17. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L (2002) Rac GTPases control axon growth, guidance and branching. Nature 416:442-447.
18. Nishimura I, Yang Y, Lu B (2004) PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116:671-682.
19. Phillips TJ, Shen EH (1996) Neurochemical bases of locomotion and ethanol stimulant effects. Int Rev Neurobiol 39:243-282.
20. Raman M, Earnest S, Zhang K, Zhao Y, Cobb MH (2007) TAO kinases mediate activation of p38 in response to DNA damage. EMBO J 26:2005-2014.
21. Reuter JE, Nardine TM, Penton A, Billuart P, Scott EK, Usui T, Uemura T, Luo L (2003) A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development 130:1203-1213.
22. Rodan AR, Kiger JA Jr, Heberlein U (2002) Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila. J Neurosci 22:9490-9501.
23. Rørth P (1996) A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci U S A 93:12418-12422.
24. Rothenfluh A, Threlkeld RJ, Bainton RJ, Tsai LT, Lasek AW, Heberlein U (2006) Distinct behavioral responses to ethanol are regulated by alternate RhoGAP18B isoforms. Cell 127:199-211.
25. Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348-353.
26. Sato K, Hayashi Y, Ninomiya Y, Shigenobu S, Arita K, Mukai M, Kobayashi S (2007) Maternal Nanos represses hid/skl-dependent apoptosis to maintain the germ line in Drosophila embryos. Proc Natl Acad Sci U S A 104:7455-7460.
27. Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28:261-271.
28. Sharma Y, Cheung U, Larsen EW, Eberl DF (2002) PPTGAL, a convenient Gal4 P-element vector for testing expression of enhancer fragments in Drosophila. Genesis 34:115-118.
29. Shulman JM, Feany MB (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165:1233-1242.
30. Shulman JM, Benton R, St Johnston D (2000) The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101:377-388.
31. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14:341-351.
32. Timm T, Li XY, Biernat J, Jiao J, Mandelkow E, Vandekerckhove J, Mandelkow EM (2003) MARKK, a Ste20-like kinase, activates the polarity-inducing kinase MARK/PAR-1. EMBO J 22:5090-5101.
33. Timm T, Matenia D, Li XY, Griesshaber B, Mandelkow EM (2006) Signaling from MARK to tau: regulation, cytoskeletal crosstalk, and pathological phosphorylation. Neurodegener Dis 3:207-217.
34. Tomancak P, Piano F, Riechmann V, Gunsalus KC, Kemphues KJ, Ephrussi A (2000) A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nat Cell Biol 2:458-460.
35. Truman JW (1990) Metamorphosis of the central nervous system of Drosophila. J Neurobiol 21:1072-1084.
36. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG (2000) The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805-813.
37. Wang JW, Imai Y, Lu B (2007) Activation of PAR-1 kinase and stimulation of tau phosphorylation by diverse signals require the tumor suppressor protein LKB1. J Neurosci 27:574-581.
38. Wolf FW, Rodan AR, Tsai LT, Heberlein U (2002) High-resolution analysis of ethanol-induced locomotor stimulation in Drosophila. J Neurosci 22:11035-11044.
39. Yasuda S, Tanaka H, Sugiura H, Okamura K, Sakaguchi T, Tran U, Takemiya T, Mizoguchi A, Yagita Y, Sakurai T, De Robertis EM, Yamagata K (2007) Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2beta and p38 MAP kinases. Neuron 56:456-471.