Identification of Genes Differentially Expressed by Nerve Growth Factor- and Neurotrophin-3-dependent Sensory Neurons

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1997 Nov 14

PMID 9356508

Citations 16

Authors

R H Friedel

H Schnurch

J Stubbusch

Y A Barde

Affiliations

Soon will be listed here.

Abstract

The neurotrophins nerve growth factor (NGF) and neurotrophin-3 (NT3) support the survival of subpopulations of primary sensory neurons with defined and distinct physiological characteristics. Only a few genes have been identified as being differentially expressed in these subpopulations, and not much is known about the nature of the molecules involved in the processing of sensory information in NGF-dependent nociceptive neurons or NT3-dependent proprioceptive neurons. We devised a simple dorsal root ganglion (DRG) explant culture system, allowing the selection of neuronal populations preferentially responsive to NGF or NT3. The reliability of this assay was first monitored by the differential expression of the NGF and NT3 receptors trkA and trkC, as well as that of neuropeptides and calcium-binding proteins. We then identified four differentially expressed sodium channels, two enriched in the NGF population and two others in the NT3 population. Finally, using an optimized RNA fingerprinting protocol, we identified 20 additional genes, all differentially expressed in DRG explants cultured with NGF or NT3. This approach thus allows the identification of large number of genes expressed in subpopulations of primary sensory neurons and opens the possibility of studying the molecular mechanisms of nociception and proprioception.

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References

Satin J, KYLE J, Chen M, Bell P, Cribbs L, Fozzard H . A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties. Science. 1992; 256(5060):1202-5. DOI: 10.1126/science.256.5060.1202. View

Airaksinen M, Koltzenburg M, Lewin G, Masu Y, Helbig C, Wolf E . Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron. 1996; 16(2):287-95. DOI: 10.1016/s0896-6273(00)80047-1. View

Martin W, Hohmann A, Walker J . Suppression of noxious stimulus-evoked activity in the ventral posterolateral nucleus of the thalamus by a cannabinoid agonist: correlation between electrophysiological and antinociceptive effects. J Neurosci. 1996; 16(20):6601-11. PMC: 6578910. View

Chen C, Zhou X, Rush R . Neurotrophin-3 and trkC-immunoreactive neurons in rat dorsal root ganglia correlate by distribution and morphology. Neurochem Res. 1996; 21(7):809-14. DOI: 10.1007/BF02532304. View

Ernfors P, Lee K, Kucera J, Jaenisch R . Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell. 1994; 77(4):503-12. DOI: 10.1016/0092-8674(94)90213-5. View

Welsh J, Chada K, Dalal S, Cheng R, Ralph D, McClelland M . Arbitrarily primed PCR fingerprinting of RNA. Nucleic Acids Res. 1992; 20(19):4965-70. PMC: 334270. DOI: 10.1093/nar/20.19.4965. View

Baimbridge K, Celio M, Rogers J . Calcium-binding proteins in the nervous system. Trends Neurosci. 1992; 15(8):303-8. DOI: 10.1016/0166-2236(92)90081-i. View

Lenz S, Henschel Y, Zopf D, Voss B, Gundelfinger E . VILIP, a cognate protein of the retinal calcium binding proteins visinin and recoverin, is expressed in the developing chicken brain. Brain Res Mol Brain Res. 1992; 15(1-2):133-40. DOI: 10.1016/0169-328x(92)90160-d. View

Caffrey J, Eng D, Black J, Waxman S, Kocsis J . Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res. 1992; 592(1-2):283-97. DOI: 10.1016/0006-8993(92)91687-a. View

10.

De Koninck P, Carbonetto S, Cooper E . NGF induces neonatal rat sensory neurons to extend dendrites in culture after removal of satellite cells. J Neurosci. 1993; 13(2):577-85. PMC: 6576645. View

11.

Mu X, Silos-Santiago I, Carroll S, Snider W . Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J Neurosci. 1993; 13(9):4029-41. PMC: 6576438. View

12.

Crowley C, Spencer S, Nishimura M, Chen K, Armanini M, Ling L . Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 1994; 76(6):1001-11. DOI: 10.1016/0092-8674(94)90378-6. View

13.

Smeyne R, Klein R, Schnapp A, Long L, Bryant S, Lewin A . Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature. 1994; 368(6468):246-9. DOI: 10.1038/368246a0. View

14.

Klein R, Silos-Santiago I, Smeyne R, Lira S, Brambilla R, Bryant S . Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature. 1994; 368(6468):249-51. DOI: 10.1038/368249a0. View

15.

Snider W . Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell. 1994; 77(5):627-38. DOI: 10.1016/0092-8674(94)90048-5. View

16.

Farinas I, Jones K, Backus C, Wang X, Reichardt L . Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature. 1994; 369(6482):658-61. DOI: 10.1038/369658a0. View

17.

Gaese F, Kolbeck R, Barde Y . Sensory ganglia require neurotrophin-3 early in development. Development. 1994; 120(6):1613-9. DOI: 10.1242/dev.120.6.1613. View

18.

Goedert M, Otten U, Hunt S, Bond A, Chapman D, Schlumpf M . Biochemical and anatomical effects of antibodies against nerve growth factor on developing rat sensory ganglia. Proc Natl Acad Sci U S A. 1984; 81(5):1580-4. PMC: 344881. DOI: 10.1073/pnas.81.5.1580. View

19.

Petersen M, PIERAU F, Weyrich M . The influence of capsaicin on membrane currents in dorsal root ganglion neurones of guinea-pig and chicken. Pflugers Arch. 1987; 409(4-5):403-10. DOI: 10.1007/BF00583794. View

20.

Ernsberger U, Rohrer H . Neuronal precursor cells in chick dorsal root ganglia: differentiation and survival in vitro. Dev Biol. 1988; 126(2):420-32. DOI: 10.1016/0012-1606(88)90151-0. View