Modulation of neurite outgrowth by activation of calcium-permeable kainate receptors expressed by rat nociceptive-like dorsal root ganglion neurons

Developmental Neurobiology

Volumn 71, Issue 10, 2011, Pages 818-835

  Joseph, Donald J ^a   Williams, Damian J ^a   MacDermott, Amy B ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Dorsal root ganglion; Growth cone; Microisland; Neurite outgrowth; RNA editing

Indexed keywords

4 METHYLGLUTAMIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR; CALCIUM; KAINIC ACID RECEPTOR; MESSENGER RNA; PHILANTHOTOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; CELL CULTURE; CONTROLLED STUDY; EMBRYO; NERVE FIBER GROWTH; NEURITE; NOCICEPTION; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; RNA EDITING; SPIDER; SPINAL GANGLION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ADENOSINE DEAMINASE; ANALYSIS OF VARIANCE; ANIMALS; CALCIUM; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; EXCITATORY AMINO ACID ANTAGONISTS; GANGLIA, SPINAL; GAP-43 PROTEIN; GENE EXPRESSION REGULATION; GLUTAMATES; GROWTH CONES; KAINIC ACID; MEMBRANE PROTEINS; NEURITES; NEUROMUSCULAR DEPOLARIZING AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; RNA EDITING; RNA, MESSENGER; SENSORY RECEPTOR CELLS; SPIDER VENOMS; SUBCELLULAR FRACTIONS;

EID: 80052639130     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20906     Document Type: Article

References (43)

1. Albuquerque C, Joseph DJ, Choudhury P, MacDermott AB. 2009a. Dissection, plating, and maintenance of cortical astrocyte cultures. CSH Protoc 2009:pdb prot5273.
2. Albuquerque C, Joseph DJ, Choudhury P, MacDermott AB. 2009b. Dissection, plating, and maintenance of dorsal horn neuron cultures. CSH Protoc 2009:pdb prot5274.
3. Albuquerque C, Joseph DJ, Choudhury P, MacDermott AB. 2009c. Dissection, plating, and maintenance of dorsal root ganglion neurons for monoculture and for coculture with dorsal horn neurons. CSH Protoc 2009:pdb prot5275.
4. Albuquerque C, Joseph DJ, Choudhury P, MacDermott AB. 2009d. Preparation of coverslips for neuronal cultures. CSH Protoc 2009:pdb prot5272.
5. Belcher S, Howe J. 1997. Characterization of RNA editing of the glutamate-receptor subunits GluR5 and GluR6 in granule cells during cerebellar development. Brain Res Mol Brain Res 52: 130-138.
6. Bernard A, Ferhat L, Dessi F, Charton G, Represa A, Ben-Ari Y, Khrestchatisky M. 1999. Q/R editing of the rat GluR5 and GluR6 kainate receptors in vivo and in vitro: evidence for independent developmental, pathological and cellular regulation. Eur J Neurosci 11: 604-616.
7. Catsicas M, Allcorn S, Mobbs P. 2001. Early activation of Ca(2+)-permeable AMPA receptors reduces neurite outgrowth in embryonic chick retinal neurons. J Neurobiol 49: 200-211.
8. Chang S, De Camilli P. 2001. Glutamate regulates actin-based motility in axonal filopodia. Nat Neurosci 4: 787-793.
9. Dickson BJ. 2002. Molecular mechanisms of axon guidance. Science 298: 1959-1964.
10. Dingledine R, Borges K, Bowie D, Traynelis SF. 1999. The glutamate receptor ion channels. Pharmacol Rev 51: 7-61.
11. Egebjerg J, Heinemann SF. 1993. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci USA 90: 755-759.
12. Fitzgerald M, Jennings E. 1999. The postnatal development of spinal sensory processing. Proc Natl Acad Sci USA 96: 7719-7722.
13. Gomez TM, Spitzer NC. 1999. In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397: 350-355.
14. Gomez TM, Zheng JQ. 2006. The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7: 115-125.
15. Henley J, Poo MM. 2004. Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 14: 320-330.
16. Huettner JE. 1990. Glutamate receptor channels in rat DRG neurons: Activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron 5: 255-266.
17. Ibarretxe G, Perrais D, Jaskolski F, Vimeney A, Mulle C. 2007. Fast regulation of axonal growth cone motility by electrical activity. J Neurosci 27: 7684-7695.
18. Jaskolski F, Coussen F, Nagarajan N, Normand E, Rosenmund C, Mulle C. 2004. Subunit composition and alternative splicing regulate membrane delivery of kainate receptors. J Neurosci 24: 2506-2515.
19. Joseph DJ, Choudhury P, Macdermott AB. 2010. An in vitro assay system for studying synapse formation between nociceptive dorsal root ganglion and dorsal horn neurons. J Neurosci Methods 189: 197-204.
20. Kerchner GA, Wilding TJ, Huettner JE, Zhuo M. 2002. Kainate receptor subunits underlying presynaptic regulation of transmitter release in the dorsal horn. J Neurosci 22: 8010-8017.
21. Kohler M, Burnashev N, Sakmann B, Seeburg PH. 1993. Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: Diversity by RNA editing. Neuron 10: 491-500.
22. Lee CJ, Kong H, Manzini MC, Albuquerque C, Chao MV, MacDermott AB. 2001. Kainate receptors expressed by a subpopulation of developing nociceptors rapidly switch from high to low Ca2+ permeability. J Neurosci 21: 4572-4581.
23. Lerma J, Paternain AV, Rodriguez-Moreno A, Lopez-Garcia JC. 2001. Molecular physiology of kainate receptors. Physiol Rev 81: 971-998.
24. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25: 402-408.
25. Mattson MP, Dou P, Kater SB. 1988. Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J Neurosci 8: 2087-2100.
26. Metzger F, Wiese S, Sendtner M. 1998. Effect of glutamate on dendritic growth in embryonic rat motoneurons. J Neurosci 18: 1735-1742.
27. Nishiyama M, von Schimmelmann MJ, Togashi K, Findley WM, Hong K. 2008. Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat Neurosci 11: 762-771.
28. Olsen DP, Dunlap K, Jacob MH. 2007. Kainate receptors and RNA editing in cholinergic neurons. J Neurochem 101: 327-341.
29. Partin KM, Patneau DK, Winters CA, Mayer ML, Buonanno A. 1993. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11: 1069-1082.
30. Paschen W, Dux E, Djuricic B. 1994. Developmental changes in the extent of RNA editing of glutamate receptor subunit GluR5 in rat brain. Neurosci Lett 174: 109-112.
31. Paschen W, Schmitt J, Dux E, Djuricic B. 1995. Temporal analysis of the upregulation of GluR5 mRNA editing with age: regional evaluation. Brain Res Dev Brain Res 86: 359-363.
32. Pinheiro P, Mulle C. 2006. Kainate receptors. Cell Tissue Res 326: 457-482.
33. Sato K, Kiyama H, Park HT, Tohyama M. 1993. AMPA, KA and NMDA receptors are expressed in the rat DRG neurones. Neuroreport 4: 1263-1265.
34. Schmauss C, Howe JR. 2002. RNA editing of neurotransmitter receptors in the mammalian brain. Sci STKE 2002:pe26.
35. Schmitz Y, Luccarelli J, Kim M, Wang M, Sulzer D. 2009. Glutamate controls growth rate and branching of dopaminergic axons. J Neurosci 29: 11973-11981.
36. Seeburg PH, Hartner J. 2003. Regulation of ion channel/neurotransmitter receptor function by RNA editing. Curr Opin Neurobiol 13: 279-283.
37. Sugiyama K, Muteki T. 1994. Local anesthetics depress the calcium current of rat sensory neurons in culture. Anesthesiology 80: 1369-1378.
38. Tashiro A, Dunaevsky A, Blazeski R, Mason CA, Yuste R. 2003. Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainate receptors: A two-step model of synaptogenesis. Neuron 38: 773-784.
39. Tessier-Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274: 1123-1133.
40. Tolle TR, Berthele A, Zieglgansberger W, Seeburg PH, Wisden W. 1993. The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray. J Neurosci 13: 5009-5028.
41. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, et al. 2010. Glutamate receptor ion channels: Structure, regulation, and function. Pharmacol Rev 62: 405-496.
42. Wilding TJ, Huettner JE. 1997. Activation and desensitization of hippocampal kainate receptors. J Neurosci 17: 2713-2721.
43. Zheng JQ, Wan JJ, Poo MM. 1996. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 16: 1140-1149.