Overexpression of brain-derived neurotrophic factor enhances sensory innervation and selectively increases neuron number

Journal of Neuroscience

Volumn 19, Issue 14, 1999, Pages 5919-5931

  LeMaster, Ann M ^a   Krimm, Robin F ^a   Davis, Brian M ^a   Noel, Teresa ^a   Forbes, Mary E ^b   Johnson, James E ^b   Albers, Kathryn M ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

BDNF; Meissner; Neurotrophin; Sensory; Transgenic; trkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 4;

ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL SURVIVAL; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE; SKIN NERVE; TRANSGENE;

EID: 0033565708     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-14-05919.1999     Document Type: Article

References (59)

1. Acheson A, Lindsay RM (1996) Non target-derived roles of the neurotrophins. Phil Trans R Soc Lond B Biol Sci 351:417-422.
2. 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.
3. 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.
4. Albers KM, Perrone TN, Goodness TP, Jones ME, Green MA, Davis B M (1996) Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J Cell Biol 134:487-497.
5. Barbacid M (1994) The Trk family of neurotrophin receptors. J Neurobiol 25:1386-1403.
6. Baxter GT, Radeke MJ, Kuo RC, Makrides V, Hinkle B, Hoang R, Medina-Selby A, Coit D, Valenzuela P, Feinstein SC (1997) Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J Neurosci 17:2683-2690.
7. Biffo S, Offenhauser N, Carter BD, Barde YA (1995) Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121:2461-2470.
8. Botchkarev VA, Botchkareva NV, Lommatzsch M, Peters EM, Lewin GR, Subramaniam A, Braun A, Renz H, Paus R (1998) BDNF overexpression induces differential increases among subsets of sympathetic innervation in murine back skin. Eur J Neurosci 10:3276-3283.
9. Buchman VL, Davies AM (1993) Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development 118:989-1001.
10. Carroll P, Lewin GR, Koltzenburg M, Toyka KV, Thoenen H (1998) A role for BDNF in mechanosensation. Nat Neurosci 1:42-46.
11. Conover JC, Erickson JT, Katz DM, Bianchi LM, Poueymirou WT, McClain J, Pan L, Helgren M, Ip NY, Boland P, Friedman B, Wiegand S, Vejsada R, Kato AC, DeChiara TM, Yancopoulos GD (1995) Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375:235-238.
12. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Philips 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.
13. 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.
14. 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.
15. Davis BM, Albers KM, Seroogy KB, Katz DM (1994) Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons. J Comp Neurol 349:464-474.
16. Davis BM, Wang HS, Albers KM, Carlson SL, Goodness TP, McKinnon D (1996) Effects of NGF overexpression on anatomical and physiological properties of sympathetic postganglionic neurons. Brain Res 724:47-54.
17. 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.
18. Eide FF, Vining ER, Eide BL, Zang K, Wang XY, Reichardt LF (1996) Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 16:3123-3129.
19. Erickson JT, Conover JC, Borday V, Champagnat J, Barbacid M, Yancopoulos G, Katz DM (1996) Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J Neurosci 16:5361-5371.
20. Ernfors P, Wetmore C, Olson L, Persson H (1990) Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5:511-526.
21. Ernfors P, Rosario CM, Merlio JP, Grant G, Aldskogius H, Persson H (1993) Expression of mRNAs for neurotrophin receptors in the dorsal root ganglion and spinal cord during development and following peripheral or central axotomy. Mol Brain Res 17:217-226.
22. Ernfors P, Lee KF, Jaenisch R (1994) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147-150.
23. Farinas I, Wilkinson GA, Backus C, Reichardt LF, Patapoutian A (1998) Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: direct NT-3 activation of TrkB neurons in vivo. Neuron 21:325-334.
24. Friedman B, Kleinfeld D, Ip NY, Verge VM, Moulton R, Boland P, Zlotchenko E, Lindsay RM, Liu L (1995) BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J Neurosci 15:1044-1056.
25. 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.
26. Jones KR, Farinas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
27. Klein R, Conway D, Parada LF, Barbacid M (1990a) The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61:647-656.
28. Klein R, Martin-Zanca D, Barbacid M, Parada LF (1990b) Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 109:845-850.
29. Liebl DJ, Tessarollo L, Palko ME, Parada LF (1997) Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J Neurosci 17:9113-9121.
30. LoPresti P, Scott SA (1994) Target specificity and size of avian sensory neurons supported in vitro by nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3. J Neurobiol 25:1613-1624.
31. Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD (1990) Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247:1446-1451.
32. Middlemas DS, Lindberg RA, Hunter T (1991) TrkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol 11:143-153.
33. Mills LR, Nurse CA, Diamond J (1989) The neural dependency of Merkel cell development in the rat: the touch domes and foot pads contrasted. Dev Biol 136:61-74.
34. Moll I, Kuhn C, Moll R (1995) Cytokeratin 20 is a general marker of cutaneous Merkel cells while certain neuronal proteins are absent. J Invest Dermatol 104:910-915.
35. Navarro X, Verdu E, Wendelschafer-Crabb G, Kennedy WR (1995) Innervation of cutaneous structures in the mouse hind paw: a confocal microscopy immunohistochemical study. J Neurosci Res 41:111-120.
36. Neuhuber WL (1987) Sensory vagal innervation of the rat esophagus and cardia: a light and electron microscopic anterograde tracing study. J Auton Nerv Syst 20:243-255.
37. Ninkina N, Adu J, Fischer A, Pinon LG, Buchman VL, Davies AM (1996) Expression and function of TrkB variants in developing sensory neurons. EMBO J 15:6385-6393.
38. Nurse CA, Farraway L (1988) Development of Merkel cell populations with contrasting sensitivities to neonatal deafferentation in the rat whisker pad. Somatosens Mot Res 6:141-162.
39. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
40. Paves H, Saarma M (1997) Neurotrophins as in vitro growth cone guidance molecules for embryonic sensory neurons. Cell Tissue Res 290:285-297.
41. Perl E (1992) Function of dorsal root ganglion neurons: an overview. In: Sensory neurons: diversity, development, and plasticity. (Scott SA, ed), pp 3-23. New York: Oxford UP.
42. Reichardt LF, Farinas I (1997) Neurotrophic factors and their receptors: roles in neuronal development and function. In: Molecular approaches to neural development. (Cowan MW, Jessell TM, Zipurski L, eds), pp 220-263. New York: Oxford UP.
43. Rice FL, Albers KM, Davis BM, Silos-Santiago I, Wilkinson GA, LeMaster AM, Ernfors P, Smeyne RJ, Aldskogius H, DeChiara TM, Philips HS, Reichardt LF, Barbacid M, Yancopoulos GD, Fundin BT (1998) Differential dependency of unmyelinated and Ad epidermal and upper dermal innervation on neurotrophins, trk receptors and p75 LNGFR. Dev Biol 198:57-81.
44. Robinson M, Buj-Bello A, Davies AM (1996) Paracrine interactions of BDNF involving NGF-dependent embryonic sensory neurons. Mol Cell Neurosci 7:143-151.
45. Rodriguez-Tebar A, Dechant G, Barde YA (1990) Binding of brain-derived neurotrophic factor to the nerve growth factor receptor. Neuron 4:487-492.
46. Rose RD, Rohrlich D (1987) Counting sectioned cells via mathematical reconstruction. J Comp Neurol 263:365-386.
47. Schecterson LC, Bothwell M (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
48. Silos-Santiago I, Fagan AM, Garber M, Fritzsch B, Barbacid M (1997) Severe sensory deficits but normal CNS development in newborn mice lacking trkB and trkC tyrosine protein kinase receptors. Eur J Neurosci 9:2045-2056.
49. Siuciak JA, Altar CA, Wiegand SJ, Lindsay RM (1994) Antinociceptive effect of brain-derived neurotrophic factor and neurotrophin-3. Brain Res 633:326-330.
50. Snider WD (1994) Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627-638.
51. Vassar R, Fuchs E (1991) Transgenic mice provide new insights into the role of TGF-a during epidermal development and differentiation. Genes Dev 5:714-727.
52. Vega JA, Haro JJ, Del Valle ME (1996) Immunohistochemistry of human cutaneous Meissner and pacinian corpuscles. Microsc Res Tech 34:351-361.
53. Wang X, Zinkel S, Polonsky K, Fuchs E (1997) Transgenic studies with a keratin promoter-driven growth hormone transgene; prospects for gene therapy. Proc Natl Acad Sci USA 94:219-226.
54. West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14:275-285.
55. Wheeler EF, Gong H, Grimes R, Benoit D, Vazquez L (1998a) p75NTR and Trk receptors are expressed in reciprocal patterns in a wide variety of non-neural tissues during rat embryonic development, indicating independent receptor functions. J Comp Neurol 391:407-428.
56. Wheeler EF, Naftel JP, Pan M, von Bartheld CS, Byers MR (1998b) Neurotrophin receptor expression is induced in a subpopulation of trigeminal neurons that label by retrograde transport of NGF or fluoro-gold following tooth injury. Brain Res Mol Brain Res 61:23-38.
57. Wright EM, Vogel KS, Davies AM (1992) Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival. Neuron 9:139-150.
58. Yancopoulos GD, Maisonpierre PC, Ip NY, Aldrich TH, Belluscio L, Boulton TG, Cobb MH, Squinto SP, Furth ME (1990) Neurotrophic factors, their receptors, and the signal transduction pathways they activate. Cold Spring Harbor Symp Quant Biol 55:371-379.
59. Zhou XF, Rush RA (1996) Endogenous brain-derived neurotrophic factor is anterogradely transported in primary sensory neurons. Neuroscience 74:945-953.