Home LiteratureArticle Details
PMID: 9547242 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Bcl-2 accelerates the maturation of early sensory neurons.

Middleton G, Piñón LG, Wyatt S, Davies AM

Abstract

Bcl-2 is a cytoplasmic protein that blocks apoptosis in a wide variety of cell types. Here we report a novel role for Bcl-2 in the early stages of neuronal development. Shortly after differentiating from progenitor cells, sensory neurons undergo a distinct morphological change; initially they have small, spindle-shaped, phase-dark cell bodies that become large, spherical, and phase-bright. Early sensory neurons cultured from the trigeminal ganglia of bcl-2-/- embryos at embryonic day 11 (E11) and E12 underwent this change more slowly than trigeminal neurons of wild-type embryos of the same ages. The delay was not attributable to the well documented role of Bcl-2 in preventing apoptosis, because Bcl-2-deficient early sensory neurons survived as well as wild-type neurons. Accordingly, there was a significantly smaller number of the more mature type of neuron in the early trigeminal ganglia of bcl-2-/- embryos, yet the number of neurons in the trigeminal ganglia of bcl-2-/- and wild-type embryos was similar. The absence of Bcl-2 did not cause a uniform delay in the developmental program of sensory neurons, because the time course of nerve growth factor receptor expression (both trkA and p75) was unaffected in the trigeminal neurons of bcl-2-/- embryos. These findings indicate that Bcl-2 expression is required for the normal progression of a particular early maturational change in embryonic sensory neurons.

MeSH Terms
Animals Cell Differentiation/physiology Cellular Senescence/physiology Embryonic and Fetal Development/physiology Mice Mice, Neurologic Mutants Neurons, Afferent/cytology Proto-Oncogene Proteins c-bcl-2/physiology Receptor, Nerve Growth Factor Receptor, trkA/analysis Receptors, Nerve Growth Factor/analysis Stem Cells/cytology Trigeminal Ganglion/cytology
Chemicals
Proto-Oncogene Proteins c-bcl-2 Receptor, Nerve Growth Factor Receptors, Nerve Growth Factor Receptor, trkA
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Middleton G
School of Biological and Medical Sciences, Bute Medical Buildings, University of St. Andrews, St. Andrews, Fife KY16 9AJ, Scotland.
Piñón L G
Wyatt S
Davies A M
References (40)
40 references, click to expand
  1. Regulation of nerve growth factor receptor gene expression in sympathetic neurons during development.
    J Cell Biol. 1995 Sep;130(6):1435-46 PMID: 7559764
  2. Bcl-2 promotes regeneration of severed axons in mammalian CNS.
    Nature. 1997 Jan 30;385(6615):434-9 PMID: 9009190
  3. Role of BCL-2 in the survival and function of developing and mature sympathetic neurons.
    Neuron. 1995 Sep;15(3):649-61 PMID: 7546744
  4. Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene.
    Science. 1992 Oct 9;258(5080):302-4 PMID: 1411528
  5. Bcl-2 affects survival but not neuronal differentiation of PC12 cells.
    J Neurosci. 1993 Oct;13(10):4422-8 PMID: 7692014
  6. The trk proto-oncogene encodes a receptor for nerve growth factor.
    Cell. 1991 Apr 5;65(1):189-97 PMID: 1849459
  7. NGF receptor expression in sensory neurons develops normally in embryos lacking NGF.
    Dev Biol. 1995 Oct;171(2):434-8 PMID: 7556925
  8. Fasciculation in the early mouse trigeminal nerve is not ordered in relation to the emerging pattern of whisker follicles.
    J Comp Neurol. 1986 Nov 1;253(1):13-24 PMID: 3793986
  9. Ectopic trkA expression mediates a NGF survival response in NGF-independent sensory neurons but not in parasympathetic neurons.
    J Cell Biol. 1993 Dec;123(6 Pt 1):1555-66 PMID: 8253850
  10. Regulation of expression of mRNAs encoding the nerve growth factor receptors p75 and trkA in developing sensory neurons.
    Development. 1993 Nov;119(3):635-48 PMID: 8187634
  11. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia.
    Neuron. 1994 Oct;13(4):1017-30 PMID: 7946326
  12. Deregulated Bcl-2-immunoglobulin transgene expands a resting but responsive immunoglobulin M and D-expressing B-cell population.
    Mol Cell Biol. 1990 May;10(5):1901-7 PMID: 2183011
  13. bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation.
    Cell. 1989 Apr 7;57(1):79-88 PMID: 2649247
  14. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair.
    Cell. 1993 Oct 22;75(2):229-40 PMID: 8402909
  15. Neurotrophin-3 is a survival factor in vivo for early mouse trigeminal neurons.
    J Neurosci. 1996 Dec 1;16(23):7661-9 PMID: 8922422
  16. Overexpression of Bcl-2 in a murine dopaminergic neuronal cell line leads to neurite outgrowth.
    Neurosci Lett. 1996 Jan 5;202(3):161-4 PMID: 8848256
  17. The growth rate of sensory nerve fibres in the mammalian embryo.
    Development. 1987 Jun;100(2):307-11 PMID: 3652972
  18. Bcl-2 is required for cranial sensory neuron survival at defined stages of embryonic development.
    Development. 1997 Oct;124(20):4173-8 PMID: 9374413
  19. p75-deficient trigeminal sensory neurons have an altered response to NGF but not to other neurotrophins.
    Neuron. 1993 Oct;11(4):565-74 PMID: 8398147
  20. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice.
    Science. 1993 Sep 17;261(5128):1584-8 PMID: 8372353
  21. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2.
    Cell. 1994 Feb 25;76(4):665-76 PMID: 7907274
  22. Inactivation of bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development.
    Neuron. 1996 Jul;17(1):75-89 PMID: 8755480
  23. Expression of the NGF receptor gene in sensory neurons and their cutaneous targets prior to and during innervation.
    Neuron. 1990 Mar;4(3):421-7 PMID: 2156540
  24. Bcl-2 gene is highly expressed during neurogenesis in the central nervous system.
    Biochem Biophys Res Commun. 1993 Mar 31;191(3):915-21 PMID: 8466531
  25. Functional interactions of neurotrophins and neurotrophin receptors.
    Annu Rev Neurosci. 1995;18:223-53 PMID: 7605062
  26. Bcl-2 influences axonal growth rate in embryonic sensory neurons.
    Curr Biol. 1997 Oct 1;7(10):798-800 PMID: 9368763
  27. Role of Bcl-2 in the brain-derived neurotrophic factor survival response.
    Eur J Neurosci. 1995 Jun 1;7(6):1266-72 PMID: 7582099
  28. Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival.
    Neuron. 1992 Jul;9(1):139-50 PMID: 1321644
  29. BCL2 regulates neural differentiation.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4504-8 PMID: 8633098
  30. Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons.
    Development. 1993 Jul;118(3):989-1001 PMID: 8076530
  31. Timing of neuronal death in trkA, trkB and trkC mutant embryos reveals developmental changes in sensory neuron dependence on Trk signalling.
    Development. 1996 Oct;122(10):3255-61 PMID: 8898237
  32. Trigeminal sensory neurons require extrinsic signals to switch neurotrophin dependence during the early stages of target field innervation.
    Dev Biol. 1995 Oct;171(2):590-605 PMID: 7556939
  33. The trk proto-oncogene product: a signal transducing receptor for nerve growth factor.
    Science. 1991 Apr 26;252(5005):554-8 PMID: 1850549
  34. Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion.
    J Comp Neurol. 1984 Feb 10;223(1):124-37 PMID: 6608534
  35. Neurotrophins: the yin and yang of nerve growth factor.
    Curr Biol. 1997 Jan 1;7(1):R38-40 PMID: 9072168
  36. Intrinsic differences in the growth rate of early nerve fibres related to target distance.
    Nature. 1989 Feb 9;337(6207):553-5 PMID: 2915705
  37. bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS.
    Development. 1994 Feb;120(2):301-11 PMID: 8149910
  38. Sympathetic neuron survival and TrkA expression in NT3-deficient mouse embryos.
    EMBO J. 1997 Jun 2;16(11):3115-23 PMID: 9214629
  39. Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia.
    Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3700-4 PMID: 8170972
  40. The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis.
    Cell. 1993 Apr 23;73(2):295-307 PMID: 8477446
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1998-05-01
Pages
3344-50
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6792656
Subset
IM
Grants
Wellcome Trust · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]