Immortalized human dorsal root ganglion cells differentiate into neurons with nociceptive properties

Journal of Neuroscience

Volumn 19, Issue 13, 1999, Pages 5420-5428

  Raymon, Heather K ^a,c   Thode, Silke ^a   Zhou, Jiuying ^a   Friedman, Glenn C ^a   Pardinas, Jose R ^a   Barrere, Christian ^a   Johnson, Randolph M ^b,d   Sah, Dinah W Y ^a,e  

^a Signal Pharmaceuticals   (United States)

^b ROCHE BIOSCIENCE   (United States)

^c CELGENE CORPORATION   (United States)

^d DURECT Corporation   (United States)

^e BIOGEN   (United States)

Author keywords

DRG; Human; Pain; PNS cell line; Precursor; Sensory neuron

Indexed keywords

CAPSAICIN; TETRACYCLINE; TRANSCRIPTION FACTOR;

ARTICLE; CELL IMMORTALIZATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NOCICEPTION; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; SCHWANN CELL; SENSORY NERVE; SMOOTH MUSCLE FIBER; SPINAL GANGLION; STEM CELL;

EID: 0033169103     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-13-05420.1999     Document Type: Article

References (51)

1. Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257-262.
2. Bevan S, Szolcsanyi J (1990) Sensory neuron-specific actions of capsaicin: mechanisms and applications. Trends Pharmacol Sci 11:330-333.
3. Bevan S, Yeats J (1991) Protons activate a cation conductance in a sub-population of rat dorsal root ganglion neurones. J Physiol (Lond) 433:145-161.
4. Bevan SJ, James IF, Rang HP, Winter J, Wood JN (1987) The mechanism of action of capsaicin - a sensory neurotoxin. In: Neurotoxins and their pharmacological implications (Jenner P, ed), pp 261-277. New York: Raven.
5. Boland LM, Dingledine R (1990) Multiple components of both transient and sustained barium currents in a rat dorsal root ganglion cell line. J Physiol (Lord) 420:223-245.
6. Bronner-Fraser M, Fraser SE (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335:161-164.
7. Caffrey JM, Eng DL, Black JA, Waxman SG, Kocsis JD (1992) Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 592:283-297.
8. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
9. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN (1995) A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377:428-431.
10. Collo G, North RA, Kawashima E, Merlo-Pich E, Neidhart S, Suprenant A, Buell G (1996) Cloning of P2×5 and P2×6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J Neurosci 16:2495-2507.
11. Duff RS, Langtimm CJ, Richardson MK, Sieber-Blum M (1991) In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail embryo. Dev Biol 147:451-459.
12. Elliott AA, Elliott JR (1993) Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol (Lond) 463:39-56.
13. Fitzgerald M (1983) Capsaicin and sensory neurones - a review. Pain 15:109-130.
14. Frank E, Sanes JR (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development 111:895-908.
15. Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739-768.
16. Hunt SP, Rossi J (1985) Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information. Philos Trans R Soc Lond [Biol] 308:283-289.
17. Kobrinsky EM, Pearson HA, Dolphin AC (1994) Low- and high-voltage-activated calcium channel currents and their modulation in the dorsal root ganglion cell line ND7-23. Neuroscience 58:539-552.
18. Kostyuk PG, Vcselovsky NS, Tsyndrenko AY (1981) Ionic currents in the somatic membrane of rat dorsal root ganglion neurons - I. Sodium currents. Neuroscience 6:2423-2430.
19. Kusano K, Gainer H (1993) Modulation of voltage-activated Ca currents by pain-inducing agents in a dorsal root ganglion neuronal line, F-11. J Neurosci Res 34:158-169.
20. Le Douarin NM, Xue ZG, Smith J (1985) In vivo and in vitro studies on the segregation of autonomie and sensory cell lineages. J Physiol (Lond) 80:255-261.
21. Lewis C, Neidhart S, Holy C, North RA, Buell G, Surprenant A (1995) Coexpression of P2×2 and P2×3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377:432-435.
22. Lo L, Anderson DJ (1995) Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 15:527-539.
23. Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ (1991) Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524-1537.
24. Matsumoto SG (1994) Neuronal differentiation in cultures of murine neural crest. II. Development of capsaicin-sensitive neurons. Brain Res Dev Brain Res 83:17-27.
25. Maxwell GD, Reid K, Elefanty A, Bartlett PF, Murphy M (1996) Glial cell line-derived neurotrophic factor promotes the development of adrenergic neurons in mouse neural crest cultures. Proc Natl Acad Sci USA 93:13274-13279.
26. Molliver DC, Radeke MJ, Feinstein SC, Snider WD (1995) Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J Comp Neurol 361:404-416.
27. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19:849-861.
28. Ogata N, Tatebayashi H (1993) Kinetic analysis of two types of Na+ channels in rat dorsal root ganglia. J Physiol (Lond) 466:9-37.
29. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84:309-320.
30. Platika D, Boulos MH, Baizer L, Fishman MC (1985) Neuronal traits of clonal cell lines derived by fusion of dorsal root ganglia neurons with neuroblastoma cells. Proc Natl Acad Sci USA 82:3499-3503.
31. Rao MS, Anderson DJ (1997) Immortalization and controlled in vitro differentiation of murine multipotent neural crest stem cells. J Neurobiol 32:722-746.
32. Roy ML, Narahashi T (1992) Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 12:2104-2111.
33. Sah DW, Ray J, Gage FH (1997) Bipotent progenitor cell lines from the human CNS. Nat Biotechnol 15:574-580.
34. Saito T, Greenwood A, Sun Q, Anderson DJ (1995) Identification by differential RT-PCR of a novel paired homeodomain protein specifically expressed in sensory neurons and a subset of their CNS targets. Mol Cell Neurosci 6:280-292.
35. Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, Herman RC (1996) Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 271:5953-5956.
36. Schweizer G, Ayer-Le Lievre C, Le Douarin NM (1983) Restrictions of developmental capacities in the dorsal root ganglia during the course of development. Cell Differ 13:191-200.
37. Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DJ (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77:349-360.
38. Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85:331-343.
39. Stemple DL, Anderson DJ (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:973-985.
40. Suburo AM, Wheatley SC, Horn DA, Gibson SJ, Jahn R, Fischer-Colbrie R, Wood JN, Latchman DS, Polak JM (1992) Intracellular redistribution of neuropeptides and secretory proteins during differentiation of neuronal cell lines. Neuroscience 46:881-889.
41. Sun Y, Maxwell GD (1994) Ciliary neurotrophic factor (CNTF) has a dose-dependent biphasic effect on the number of adrenergic cells which develop in avian trunk neural crest cultures. Neurosci Lett 165:1-4.
42. Szallasi A (1994) The vanilloid (capsaicin) receptor: receptor types and species differences. Gen Pharmacol 25:223-243.
43. Valera S, Hussy N, Evans RJ, Adami N, North RA, Suprenant A, Buell G (1994) A new class of ligand-gated ion channel defined by P2X receptor for extracellular ATP. Nature 371:516-519.
44. Varley JE, Maxwell GD (1996) BMP-2 and BMP-4, but not BMP-6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp Neurol 140:84-94.
45. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M (1997a) A proton-gated cation channel involved in acid-sensing. Nature 386:173-177.
46. Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M (1997b) Molecular cloning of a non-inactivating protongated Na+ channel specific for sensory neurons. J Biol Chem 272:20975-20978.
47. Wood JN, Winter J, James IF, Rang HP, Yeats J, Bevan S (1988) Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J Neurosci 8:3208-3220.
48. Wood JN, Bevan SJ, Coote PR, Dunn PM, Harmar A, Hogan P, Latchman DS, Morrison C, Rougon G, Theveniau M, Wheatley S (1990) Novel cell lines display properties of nociceptive sensory neurons. Proc R Soc Lond [Biol] 241:187-194.
49. Xue ZG, Le Douarin NM, Smith J (1988) Insulin and insulin-like growth factor-I can trigger the differentiation of catecholaminergic precursors in cultures of dorsal root ganglia. Cell Differ Dev 25:1-10.
50. Xue ZG, Xue XJ, Fauquet M, Smith J, Le Douarin N (1992) Expression of the gene encoding tyrosine hydroxylase in a subpopulation of quail dorsal root ganglion cells cultured in the presence of insulin or chick embryo extract. Brain Res Dev Brain Res 69:23-30.
51. Zeilhofer HU, Swandulla D, Reeh PW, Kress M (1996) Ca2+ permeability of the sustained proton-induced cation current in adult rat dorsal root ganglion neurons. J Neurophysiol 76:2834-2840.