Drosophila MICAL regulates myofilament organization and synaptic structure

Mechanisms of Development

Volumn 124, Issue 5, 2007, Pages 390-406

  Beuchle, Dirk ^a   Schwarz, Heinz ^a   Langegger, Maria ^a   Koch, Iris ^a   Aberle, Hermann ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Actin; Drosophila; MICAL; Muscle filament; Myofibrillogenesis; Myosin; Neuromuscular junction; Sarcomere; Subsynaptic reticulum; Synapse; Synaptic growth; Titin

Indexed keywords

ACTIN; CONNECTIN; MUSCLE PROTEIN; MYOSIN; PROTEIN MICAL; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MICAL; EMBRYO; GENE EXPRESSION; GENETIC CONSERVATION; IMMUNOHISTOCHEMISTRY; MUTAGENESIS; MUTANT; MYOFILAMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; SARCOMERE; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; DNA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; MICROFILAMENTS; MOLECULAR SEQUENCE DATA; MUTATION; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; SYNAPSES;

EID: 33947698424     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2007.01.006     Document Type: Article

References (45)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhaes T.R., and Goodman C.S. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33 (2002) 545-558
2. Araujo S.J., and Tear G. Axon guidance mechanisms and molecules: lessons from invertebrates. Nat. Rev. Neurosci. 4 (2003) 910-922
3. Atwood H.L., Govind C.K., and Wu C.F. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J. Neurobiol. 24 (1993) 1008-1024
4. Beall C.J., Sepanski M.A., and Fyrberg E.A. Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. Genes Dev. 3 (1989) 131-140
5. Benzer S. Genetic dissection of behavior. Sci. Am. 229 (1973) 24-37
6. Beumer K.J., Rohrbough J., Prokop A., and Broadie K. A role for PS integrins in morphological growth and synaptic function at the postembryonic neuromuscular junction of Drosophila. Development 126 (1999) 5833-5846
7. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
8. Cooper S.T., Maxwell A.L., Kizana E., Ghoddusi M., Hardeman E.C., Alexander I.E., Allen D.G., and North K.N. C2C12 co-culture on a fibroblast substratum enables sustained survival of contractile, highly differentiated myotubes with peripheral nuclei and adult fast myosin expression. Cell Motil. Cytoskeleton 58 (2004) 200-211
9. de Jong S., Cavallo J.A., Rios C.D., Dworak H.A., and Sink H. Target recognition and synaptogenesis by motor axons: responses to the sidestep protein. Int. J. Dev. Neurosci. 23 (2005) 397-410
10. Dillon C., and Goda Y. The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28 (2005) 25-55
11. Dlugosz A.A., Antin P.B., Nachmias V.T., and Holtzer H. The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J. Cell Biol. 99 (1984) 2268-2278
12. Fischer J., Weide T., and Barnekow A. The MICAL proteins and rab1: a possible link to the cytoskeleton?. Biochem. Biophys. Res. Commun. 328 (2005) 415-423
13. Fischer M., Kaech S., Knutti D., and Matus A. Rapid actin-based plasticity in dendritic spines. Neuron 20 (1998) 847-854
14. Fischman D.A. The synthesis and assembly of myofibrils in embryonic muscle. Curr. Top. Dev. Biol. 5 (1970) 235-280
15. Fyrberg E., Fyrberg C.C., Beall C., and Saville D.L. Drosophila melanogaster troponin-T mutations engender three distinct syndromes of myofibrillar abnormalities. J. Mol. Biol. 216 (1990) 657-675
16. Goda Y., and Davis G.W. Mechanisms of synapse assembly and disassembly. Neuron 40 (2003) 243-264
17. Gregorio C.C., and Antin P.B. To the heart of myofibril assembly. Trends Cell Biol. 10 (2000) 355-362
18. Holtzer H., Sanger J.W., Ishikawa H., and Strahs K. Selected topics in skeletal myogenesis. Cold Spring Harbor Symp. Quant. Biol. 37 (1972) 549-566
19. Hummel T., Krukkert K., Roos J., Davis G., and Klambt C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26 (2000) 357-370
20. Jia X.X., Gorczyca M., and Budnik V. Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild type and mutants with increased excitability. J. Neurobiol. 24 (1993) 1025-1044
21. Lahey T., Gorczyca M., Jia X.X., and Budnik V. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13 (1994) 823-835
22. Lakey A., Labeit S., Gautel M., Ferguson C., Barlow D.P., Leonard K., and Bullard B. Kettin, a large modular protein in the Z-disc of insect muscles. EMBO J. 12 (1993) 2863-2871
23. Lamprecht R., and LeDoux J. Structural plasticity and memory. Nat. Rev. Neurosci. 5 (2004) 45-54
24. Lawton M.P., and Philpot R.M. Functional characterization of flavin-containing monooxygenase 1B1 expressed in Saccharomyces cerevisiae and Escherichia coli and analysis of proposed FAD- and membrane-binding domains. J. Biol. Chem. 268 (1993) 5728-5734
25. Li Z., and Sheng M. Some assembly required: the development of neuronal synapses. Nat. Rev. Mol. Cell Biol. 4 (2003) 833-841
26. Mahr A., and Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 6 (2006) 209-309
27. Marques G., Bao H., Haerry T.E., Shimell M.J., Duchek P., Zhang B., and O'Connor M.B. The Drosophila BMP type II receptor wishful thinking regulates neuromuscular synapse morphology and function. Neuron 33 (2002) 529-543
28. Matus A. Actin-based plasticity in dendritic spines. Science 290 (2000) 754-758
29. Meyer F., and Aberle H. At the next stop sign turn right: the metalloprotease Tolloid-related 1 controls the defasciculation of motor axons in Drosophila. Development 133 (2006) 4035-4044
30. Nadella M., Bianchet M.A., Gabelli S.B., Barrila J., and Amzel L.M. Structure and activity of the axon guidance protein MICAL. Proc. Natl. Acad. Sci. USA 102 (2005) 16830-16835
31. Parnas D., Haghighi A.P., Fetter R.D., Kim S.W., and Goodman C.S. Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 32 (2001) 415-424
32. Roos J., Hummel T., Ng N., Klambt C., and Davis G.W. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26 (2000) 371-382
33. Schuster C.M., Davis G.W., Fetter R.D., and Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17 (1996) 655-667
34. Siebold C., Berrow N., Walter T.S., Harlos K., Owens R.J., Stuart D.I., Terman J.R., Kolodkin A.L., Pasterkamp R.J., and Jones E.Y. High-resolution structure of the catalytic region of MICAL (molecule interacting with CasL), a multidomain flavoenzyme-signaling molecule. Proc. Natl. Acad. Sci. USA 102 (2005) 16836-16841
35. Sigrist S.J., Thiel P.R., Reiff D.F., Lachance P.E., Lasko P., and Schuster C.M. Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature 405 (2000) 1062-1065
36. Sink H., Rehm E.J., Richstone L., Bulls Y.M., and Goodman C.S. sidestep encodes a target-derived attractant essential for motor axon guidance in Drosophila. Cell 105 (2001) 57-67
37. Suzuki T., Nakamoto T., Ogawa S., Seo S., Matsumura T., Tachibana K., Morimoto C., and Hirai H. MICAL, a novel CasL interacting molecule, associates with vimentin. J. Biol. Chem. 277 (2002) 14933-14941
38. Terman J.R., Mao T., Pasterkamp R.J., Yu H.H., and Kolodkin A.L. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109 (2002) 887-900
39. Wagh D.A., Rasse T.M., Asan E., Hofbauer A., Schwenkert I., Dürrbeck H., Buchner S., Dabauvalle M.C., Schmidt M., Qin G., Wichmann C., Kittel R., Sigrist S.J., and Buchner E. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49 (2006) 833-844
40. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., and Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron 26 (2000) 313-329
41. Weide T., Teuber J., Bayer M., and Barnekow A. MICAL-1 isoforms, novel rab1 interacting proteins. Biochem. Biophys. Res. Commun. 306 (2003) 79-86
42. Wierenga R.K., Terpstra P., and Hol W.G. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187 (1986) 101-107
43. Yuste R., and Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24 (2001) 1071-1089
44. Ziegler D.M. Recent studies on the structure and function of multisubstrate flavin-containing monooxygenases. Annu. Rev. Pharmacol. Toxicol. 33 (1993) 179-199
45. Zito K., Parnas D., Fetter R.D., Isacoff E.Y., and Goodman C.S. Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 22 (1999) 719-729