The Drosophila receptor guanylyl cyclase Gyc76C is required for semaphorin-1a-plexin A-mediated axonal repulsion

Journal of Neuroscience

Volumn 24, Issue 30, 2004, Pages 6639-6649

  Ayoob, Joseph C ^a   Yu, Hung Hsiang ^a,b   Terman, Jonathan R ^a   Kolodkin, Alex L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Axon guidance; CGMP; Gyc76C; Plexin A; Receptor guanylyl cyclase; Semaphorin 1a

Indexed keywords

CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE; DROSOPHILA RECEPTOR GUANYLYL CYCLASE GYC76C; GUANYLATE CYCLASE; MEMBRANE PROTEIN; PLEXIN A; SEMAPHORIN 1A; UNCLASSIFIED DRUG;

ARTICLE; EMBRYO; ENZYME ACTIVE SITE; GENETIC ANALYSIS; GROWTH CONE; MALE; MOTOR NERVE; NERVE FIBER; NEUROMODULATION; NEUROMUSCULAR SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SECOND MESSENGER; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CYCLIC GMP; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GROWTH CONES; GUANYLATE CYCLASE; MALE; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; NERVE TISSUE PROTEINS; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SECOND MESSENGER SYSTEMS; SEMAPHORINS;

EID: 3343017377     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1104-04.2004     Document Type: Article

References (45)

1. Araujo SJ, Tear G (2003) Axon guidance mechanisms and molecules: lessons from invertebrates. Nat Rev Neurosci 4:910-922.
2. Artavanis-Tsakonas S, Matsuno K, Fortini M (1995) Notch signaling. Science 268:225-232.
3. Bellen HJ, Lewis RW, Liao G, He Y, Carlson JW, Tsang G, Evans-Holm M, Hiesinger PR, Schulze KL, Rubin GM, Hoskins RA, Spradling AC (2004) The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics, in press.
4. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
5. Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA (2003) A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23:1360-1371.
6. Chinkers M, Garbers DL (1989) The protein kinase domain of the ANP receptor is required for signaling. Science 245:1392-1394.
7. Dontchev VD, Letourneau PC (2002) Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility. J Neurosci 22:6659-6669.
8. Gibbs SM, Truman JW (1998) Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 20:83-93.
9. Gibbs SM, Becker A, Hardy RW, Truman JW (2001) Soluble guanylate cyclase is required during development for visual system function in Drosophila. J Neurosci 21:7705-7714.
10. Hallett MA, Delaat JL, Arikawa K, Schlamp CL, Kong F, Williams DS (1996) Distribution of guanylate cyclase within photoreceptor outer segments. J Cell Sci 109:1803-1812.
11. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509-563.
12. Kidd T, Bland KS, Goodman CS (1999) Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96:785-794.
13. Kuno T, Kamisaki Y, Waldman SA, Gariepy J, Schoolnik G, Murad F (1986) Characterization of the receptor for heat-stable enterotoxin from Escherichia coli in rat intestine. J Biol Chem 261:1470-1476.
14. Landgraf M, Bossing T, Technau GM, Bate M (1997) The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J Neurosci 17:9642-9655.
15. Li HS, Montell C (2000) TRP and the PDZ protein, INAD, form the core complex required for retention of the signalplex in Drosophila photoreceptor cells. J Cell Biol 150:1411-1422.
16. Liu W, Yoon J, Burg M, Chen L, Pak WL (1995) Molecular characterization of two Drosophila guanylate cyclases expressed in the nervous system. J Biol Chem 270:12418-12427.
17. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA (2000) Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52:375-414.
18. McNeil L, Chinkers M, Forte M (1995) Identification, characterization, and developmental regulation of a receptor guanylyl cyclase expressed during early stages of Drosophila development. J Biol Chem 270:7189-7196.
19. Ming G-L, Song H-J, Berninger S, Holt CE, Tessier-Lavigne M, Poo M-M (1997) cAMP-dependent growth cone guidance by netrin-1. Neuron 19:1225-1235.
20. Nishiyama M, Hoshino A, Tsai L, Henley JR, Goshima Y, Tessier-Lavigne M, Poo MM, Hong K (2003) Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 424:990-995.
21. Polleux F, Morrow T, Ghosh A (2000) Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404:567-573.
22. Pulido D, Campuzano S, Koda T, Modolell J, Barbacid M (1992) Dtrk, a Drosophila gene related to the trk family of neurotrophin receptors, encodes a novel class of neural cell adhesion molecule. EMBO J 11:391-404.
23. Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118:461-470.
24. Schmidt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, Rathjen FG (2002) cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. J Cell Biol 159:489-498.
25. Seeger M, Tear G, Ferres-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409-426.
26. Seidel C, Bicker G (2000) Nitric oxide and cGMP influence axonogenesis of antennal pioneer neurons. Development 127:4541-4549.
27. Song HJ, Poo MM (1999) Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol 9:355-363.
28. Song H-j, Ming G-I, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M-m (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281:1515-1518.
29. Suh PG, Hwang JI, Ryu SH, Donowitz M, Kim JH (2001) The roles of PDZ-containing proteins in PLC-beta-mediated signaling. Biochem Biophys Res Commun 288:1-7.
30. Tear G, Harris R, Sutaria S, Kilomanski K, Goodman CS, Seeger MA (1996) Commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16:501-514.
31. Terman JR, Kolodkin AL (2004) Nervy links protein kinase a to plexin-mediated semaphorin repulsion. Science 303:1204-1207.
32. Terman JR, Mao T, Pasterkamp RJ, Yu HH, Kolodkin AL (2002) MICALs, a family of conserved flavoprotein oxidoreductases, function in Plexin-mediated axonal repulsion. Cell 109:887-900.
33. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
34. Thompson DK, Garbers DL (1995) Dominant negative mutations of the guanylyl cyclase-A receptor. Extracellular domain deletion and catalytic domain point mutations. J Biol Chem 270:425-430.
35. Tomancak P, Beaton A, Weiszmann R, Kwan E, Shu S, Lewis SE, Richards S, AshburnerM, Hartenstein V, Celniker SE, Rubin GM (2002) Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol 3:0088.1-0088.14.
36. VanVactor D, Sink H, Fambrough D, Tsoo R, Goodman CS (1993) Genes that control neuromuscular specificity in Drosophila. Cell 73:1137-1153.
37. Waldman SA, Kuno T, Kamisaki Y, Chang LY, Gariepy J, O'Hanley P, Schoolnik G, Murad F (1986) Intestinal receptor for heat-stable enterotoxin of Escherichia coli is tightly coupled to a novel form of particulate guanylate cyclase. Infect Immun 51:320-326.
38. Wedel B, Garbers D (2001) The guanylyl cyclase family at Y2K. Annu Rev Physiol 63:215-233.
39. Wills Z, Bateman J, Korey CA, Comer A, Van Vactor D (1999) The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22:301-312.
40. Winberg ML, Noordermeer JN, Tamagnone L, Comoglio PM, Spriggs MK, Tessier-Lavigne M, Goodman CS (1998) Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95:903-916.
41. Winberg ML, Tamagnone L, Bai J, Comoglio PM, Montell D, Goodman CS (2001) The transmembrane protein Off-track associates with Plexins and functions downstream of semaphorin signaling during axon guidance. Neuron 32:53-62.
42. Yao KM, White K (1994) Neural specificity of elav expression: defining a Drosophila promoter for directing expression to the nervous system. J Neurochem 63:41-51.
43. Yu HH, Araj HH, Ralls SA, Kolodkin AL (1998) The transmembrane semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 20:207-220.
44. Yu HH, Huang AS, Kolodkin AL (2000) Semaphorin-1a acts in concert with the cell adhesion molecules fasciclin II and connectin to regulate axon fasciculation in Drosophila. Genetics 156:723-731.
45. Zhou L, Schnitzler A, Agapite J, Schwartz LM, Steller H, Nambu JR (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 USA 94:5131-5136.