An in vitro assay system for studying synapse formation between nociceptive dorsal root ganglion and dorsal horn neurons

Journal of Neuroscience Methods

Volumn 189, Issue 2, 2010, Pages 197-204

  Joseph, Donald J ^a   Choudhury, Papiya ^a   MacDermott, Amy B ^a  

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

Author keywords

Dorsal horn; Dorsal root ganglia; Electrophysiology; Immunocytochemistry; Microisland; Nociceptive; Synaptogenesis

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CELL MARKER; MICROTUBULE ASSOCIATED PROTEIN 2; PERIPHERIN; PROTEIN TYROSINE KINASE A; SUBSTANCE P; VANILLOID RECEPTOR 1; VESICULAR GLUTAMATE TRANSPORTER 2; COLLAGEN;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ASSAY; CELL LABELING; COCULTURE; COMPARATIVE ANATOMY; CONTROLLED STUDY; EMBRYO; FUNCTIONAL ANATOMY; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINAL GANGLION; SYNAPSE VESICLE; SYNAPTOGENESIS; SYNAPTOSOME; ANIMAL; CELL CULTURE; CYTOLOGY; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIAL; NERVE CELL; PAIN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; POSTERIOR HORN CELL; PROCEDURES; SPRAGUE DAWLEY RAT; SYNAPSE; TIME;

ANIMALS; ASTROCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; COLLAGEN; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; NEURONS; PAIN; PATCH-CLAMP TECHNIQUES; POSTERIOR HORN CELLS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TIME FACTORS;

EID: 77953551608     PISSN: 01650270     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2010.04.002     Document Type: Article

References (52)

1. 2+-permeable AMPA receptor. Eur J Neurosci 1999, 11:2758-2766.
2. Albuquerque C., Joseph D.J., Choudhury P., MacDermott A.B. Preparation of coverslips for neuronal cultures. CSH Protoc 2009, (August (8)). (pdb.prot5272).
3. Albuquerque C., Joseph D.J., Choudhury P., MacDermott A.B. Dissection, plating, and maintenance of cortical astrocyte cultures. CSH Protoc 2009, (August (8)). (pdb.prot5273).
4. Albuquerque C., Joseph D.J., Choudhury P., MacDermott A.B. Dissection, plating, and maintenance of dorsal horn neuron cultures. CSH Protoc 2009, (August (8)). (pdb.prot5274).
5. Albuquerque C., Joseph D.J., Choudhury P., MacDermott A.B. Dissection, Plating and maintenance of dissociated dorsal root ganglion (DRG) neurons for mono-culture and for co-culture with dorsal horn neurons. CSH Protoc 2009, (August (8)). (pdb.prot5275).
6. Alvarez F.J., Villalba R.M., Zerda R., Schneider S.P. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 2004, 472:257-280.
7. Amaral D.G., Dent J.A. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 1981, 195:51-86.
8. Averill S., McMahon S.B., Clary D.O., Reichardt L.F., Priestley J.V. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 1995, 7:1484-1494.
9. Bekkers J.M., Stevens C.F. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 1991, 88:7834-7838.
10. Belecky-Adams T., Wight D.C., Kopchick J.J., Parysek L.M. Intragenic sequences are required for cell type-specific and injury-induced expression of the rat peripherin gene. J Neurosci 1993, 13:5056-5065.
11. Bennett D.L., Averill S., Clary D.O., Priestley J.V., McMahon S.B. Postnatal changes in the expression of the trkA high-affinity NGF receptor in primary sensory neurons. Eur J Neurosci 1996, 8:2204-2208.
12. Bibel M., Barde Y.A. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 2000, 14:2919-2937.
13. Blue M.E., Parnavelas J.G. The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J Neurocytol 1983, 12:697-712.
14. Caceres A., Binder L.I., Payne M.R., Bender P., Rebhun L., Steward O. Differential subcellular localization of tubulin and the microtubule-associated protein MAP2 in brain tissue as revealed by immunocytochemistry with monoclonal hybridoma antibodies. J Neurosci 1984, 4:394-410.
15. Carlton S.M., Hargett G.L. Stereological analysis of Ca(2+)/calmodulin-dependent protein kinase II alpha -containing dorsal root ganglion neurons in the rat: colocalization with isolectin Griffonia simplicifolia, calcitonin gene-related peptide, or vanilloid receptor 1. J Comp Neurol 2002, 448:102-110.
16. Chen H.H., Frank E. Development and specification of muscle sensory neurons. Curr Opin Neurobiol 1999, 9:405-409.
17. Cohen-Cory S. The developing synapse: construction and modulation of synaptic structures and circuits. Science 2002, 298:770-776.
18. Craig A.M., Boudin H. Molecular heterogeneity of central synapses: afferent and target regulation. Nat Neurosci 2001, 4:569-578.
19. Davies A.M. The survival and growth of embryonic proprioceptive neurons is promoted by a factor present in skeletal muscle. Dev Biol 1986, 115:56-67.
20. Dyson S.E., Jones D.G. Quantitation of terminal parameters and their inter-relationships in maturing central synapses: a perspective for experimental studies. Brain Res 1980, 183:43-59.
21. Ernfors P. Local and target-derived actions of neurotrophins during peripheral nervous system development. Cell Mol Life Sci 2001, 58:1036-1044.
22. Goldstein M.E., Grant P., House S.B., Henken D.B., Gainer H. Developmental regulation of two distinct neuronal phenotypes in rat dorsal root ganglia. Neuroscience 1996, 71:243-258.
23. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
24. Gu J.G., MacDermott A.B. Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 1997, 389:749-753.
25. Guo A., Simone D.A., Stone L.S., Fairbanks C.A., Wang J., Elde R. Developmental shift of vanilloid receptor 1 (VR1) terminals into deeper regions of the superficial dorsal horn: correlation with a shift from TrkA to Ret expression by dorsal root ganglion neurons. Eur J Neurosci 2001, 14:293-304.
26. Harms K.J., Tovar K.R., Craig A.M. Synapse-specific regulation of AMPA receptor subunit composition by activity. J Neurosci 2005, 25:6379-6388.
27. Julius D., Basbaum A.I. Molecular mechanisms of nociception. Nature 2001, 413:203-210.
28. Juttner R., Rathjen F.G. Molecular analysis of axonal target specificity and synapse formation. Cell Mol Life Sci 2005, 62:2811-2827.
29. Lawson S.N., Crepps B.A., Perl E.R. Relationship of substance P to afferent characteristics of dorsal root ganglion neurones in guinea-pig. J Physiol 1997, 505(Pt 1):177-191.
30. Lee Y., Takami K., Kawai Y., Girgis S., Hillyard C.J., MacIntyre I., Emson P.C., Tohyama M. Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience 1985, 15:1227-1237.
31. Lee Y., Kawai Y., Shiosaka S., Takami K., Kiyama H., Hillyard C.J., Girgis S., MacIntyre I., Emson P.C., Tohyama M. Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: immunohistochemical analysis. Brain Res 1985, 330:194-196.
32. Lee C.J., Labrakakis C., Joseph D.J., Macdermott A.B. Functional similarities and differences of AMPA and kainate receptors expressed by cultured rat sensory neurons. Neuroscience 2004, 129:35-48.
33. Lipton S.A., Kater S.B. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 1989, 12:265-270.
34. Marmigere F., Ernfors P. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 2007, 8:114-127.
35. Matyash V, Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev. in press.
36. McAllister A.K. Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 2007, 30:425-450.
37. Michael G.J., Priestley J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 1999, 19:1844-1854.
38. Molliver D.C., Radeke M.J., Feinstein S.C., Snider W.D. Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J Comp Neurol 1995, 361:404-416.
39. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997, 19:849-861.
40. Prange O., Wong T.P., Gerrow K., Wang Y.T., El-Husseini A. A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc Natl Acad Sci USA 2004, 101:13915-13920.
41. Priestley J.V., Michael G.J., Averill S., Liu M., Willmott N. Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor. Can J Physiol Pharmacol 2002, 80:495-505.
42. Salt T.E., Morris R., Hill R.G. Distribution of substance P-responsive and nociceptive neurones in relation to substance P-immunoreactivity within the caudal trigeminal nucleus of the rat. Brain Res 1983, 273:217-228.
43. Scheiffele P. Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 2003, 26:485-508.
44. Segal M.M., Furshpan E.J. Epileptiform activity in microcultures containing small numbers of hippocampal neurons. J Neurophysiol 1990, 64:1390-1399.
45. Snider W.D., Silos-Santiago I. Dorsal root ganglion neurons require functional neurotrophin receptors for survival during development. Philos Trans R Soc Lond B Biol Sci 1996, 351:395-403.
46. Spitzer N.C. Electrical activity in early neuronal development. Nature 2006, 444:707-712.
47. Steinmetz C.C., Buard I., Claudepierre T., Nagler K., Pfrieger F.W. Regional variations in the glial influence on synapse development in the mouse CNS. J Physiol 2006, 577:249-261.
48. Todd A.J., Hughes D.I., Polgar E., Nagy G.G., Mackie M., Ottersen O.P., Maxwell D.J. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 2003, 17:13-27.
49. Traub R.J. The spinal contribution of substance P to the generation and maintenance of inflammatory hyperalgesia in the rat. Pain 1996, 67:151-161.
50. Vaughn J.E. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 1989, 3:255-285.
51. Woolf C.J., Ma Q. Nociceptors-noxious stimulus detectors. Neuron 2007, 55:353-364.
52. Zhang X., Bao L. The development and modulation of nociceptive circuitry. Curr Opin Neurobiol 2006, 16:460-466.