Overexpression of nerve growth factor in skin selectively affects the survival and functional properties of nociceptors

Journal of Neuroscience

Volumn 19, Issue 19, 1999, Pages 8509-8516

  Stucky, C L ^a   Koltzenburg, Martin ^a,d   Schneider, M ^a   Engle, M G ^b   Albers, K M ^c   Davis, B M ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Neurotrophin; P75; Pain; Programmed cell death; Sensory neuron; Trk

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE OVEREXPRESSION; HEAT SENSATION; HYPERALGESIA; MECHANICAL STIMULATION; MOUSE; MYELINATED NERVE; NERVE CONDUCTION; NOCICEPTIVE RECEPTOR; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SKIN NERVE; TRANSGENIC MOUSE;

EID: 0033216133     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-19-08509.1999     Document Type: Article

References (40)

1. Airaksinen MS, Koltzenburg M, Lewin GR, Masu Y, Helbig C, Wolf E, Brem G, Toyka KV, Thoenen H, Meyer M (1996) Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 16:287-295.
2. Albers KM, Wright DE, Davis BM (1994) Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14:1422-1432.
3. Arbuthnott ER, Boyd IA, Kalu KU (1980) Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. J Physiol (Lond) 308:125-157.
4. Baron R, Jänig W, Kollmann W (1988) Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat. J Comp Neurol 275:460-468.
5. 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.
6. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436-441.
7. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Phillips HS (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011.
8. Davies AM, Lumsden AGS (1984) Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion. J Comp Neurol 223:124-137.
9. Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353-358.
10. Davis BM, Lewin GR, Mendell LM, Jones ME, Albers KM (1993) Altered expression of nerve growth factor in the skin of transgenic mice leads to changes in response to mechanical stimuli. Neuroscience 56:789-792.
11. Davis BM, Albers KM, Seroogy KB, Katz DM (1994) Overexpression of NGF in transgenic mice induce sympathetic projections to primary sensory neurons. J Comp Neurol 349:464-474.
12. Davis BM, Wang H-S, Albers KM, Carlson SL, GoodnessTP, McKinnon D (1996) Effects of NGF overexpression on anatomical and physiological properties of sympathetic postganglionic neurons. Brain Res 724:47-54.
13. Davis BM, Fundin BT, Albers KM, Goodness TP, Cronk KM, Rice FL (1997) Overexpression of nerve growth factor in skin causes preferential increases among innervation to specific sensory targets. J Comp Neurol 387:489-506.
14. Forster C, Handwerker HO (1990) Automatic classification and analysis of microneurographic spike data using a PC/AT. J Neurosci Methods 31:109-118.
15. Goodness TP, Albers KM, Davis FE, Davis BM (1997) Overexpression of nerve growth factor in skin increases sensory neuron size and modulates trk receptor expression. Eur J Neurosci 9:1574-1585.
16. Gorin PD, Johnson EM (1980) Effects of long term nerve growth factor deprivation on the nervous system of the adult rat: an experimental autoimmune approach. Brain Res 198:27-42.
17. Hoffmeister B, Jänig W, Lisney SJW (1991) A proposed relationship between circumference and conduction velocity of unmyelinated axons from normal and regenerated cat hindlimb cutaneous nerves. Neuroscience 42:603-611.
18. Jhaveri S, Erzurumlu RS, Laywell ED, Steindler DA, Albers KM, Davis BM (1996) Excess nerve growth factor in the periphery does not obscure development of whisker-related patterns in the rodent brain. J Comp Neurol 374:41-51.
19. Johnson EM, Gorin PD, Brandeis LD, Pearson J (1980) Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor. Science 210:916-918.
20. Koltzenburg M, Stucky CL, Lewin GR (1997) Receptive properties of mouse sensory neurons innervating hairy skin. J Neurophysiol 78:1841-1850.
21. Koltzenburg M, Bennett DLH, Shelton DL, McMahon SB (1999) Neutralization of endogenous NGF prevents the sensitization of nociceptors supplying inflamed skin. Eur J Neurosci 11:1698-1704.
22. Kress M, Koltzenburg M, Reeh PW, Handwerker HO (1992) Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68:581-595.
23. Lawson SN (1992) Morphological and biochemical cell types of sensory neurons. In: Sensory neurons: diversity, development, and plasticity (Scott SA, ed), pp 27-59. New York: Oxford UP.
24. Lesser SS (1997) Neurotrophins differentially regulate voltage-gated ion channels. Mol Cell Neurosci 10:173-183.
25. Lewin GR, Barde Y-A (1996) Physiology of the neurotrophins. Annu Rev Neurosci 19:289-317.
26. Lewin GR, Mendell LM (1994) Regulation of cutaneous C-fiber heat nociceptors by nerve growth factor in the developing rat. J Neurophysiol 71:941-949.
27. Lewin GR, Ritter AM, Mendell LM (1993) Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13:2136-2148.
28. Mendelson B, Albers KM, Goodness TP, Davis BM (1996) Overexpression of nerve growth factor in epidermis of transgenic mice preserves excess sensory neurons but does not alter the somatotopic organization of cutaneous nerve projections. Neurosci Lett 211:68-72.
29. Olson L (1967) Outgrowth of sympathetic adrenergic neurons in mice treated with a nerve-growth factor (NGF). Z Zellforsch Mikrosk Anat 81:155-173.
30. Reeh PW (1986) Sensory receptors in mammalian skin in an in vitro preparation. Neurosci Lett 66:141-147.
31. Ritter AM, Lewin GR, Kremer NE, Mendell LM (1991) Requirement for nerve growth factor in the development of myelinated nociceptors in vivo. Nature 350:500-502.
32. Rueff A, Mendell LM (1996) Nerve growth factor and NT-5 induce increased thermal sensitivity of cutaneous nociceptors in vitro. J Neurophysiol 76:3593-3596.
33. Ruit KG, Osborne PA, Schmidt RE, Johnson EM, Snider WM (1990) Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse. J Neurosci 10:2413-2419.
34. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M (1994) Severe sensory deficits and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246-249.
35. Snider WD (1994) Functions of neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627-638.
36. Stucky CL, Koltzenburg M (1997) The low-affinity neurotrophin receptor p75 regulates the function but not the selective survival of specific subpopulations of sensory neurons. J Neurosci 17:4398-4405.
37. Stucky CL, DeChiara T, Lindsay RM, Yancopoulos GD, Koltzenburg M (1998) Neurotrophin 4 is required for the survival of a subclass of hair follicle receptors. J Neurosci 18:7040-7046.
38. Voyodic JT (1989) Target size regulates calibre and myelination of sympathetic axons. Nature 342:430-433.
39. Waxman SG (1980) Determinants of conduction velocity in myelinated nerve fibers. Muscle Nerve 3:141-150.
40. Waxman SG, Ritchie JM (1993) Molecular dissection of the myelinated axon. Ann Neurol 33:121-136.