Home LiteratureArticle Details
PMID: 12451137 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Glia induce dendritic growth in cultured sympathetic neurons by modulating the balance between bone morphogenetic proteins (BMPs) and BMP antagonists.

Lein PJ, Beck HN, Chandrasekaran V, Gallagher PJ, Chen HL, Lin Y, Guo X, Kaplan PL, Tiedge H, Higgins D

Abstract

Dendritic growth in cultured sympathetic neurons requires specific trophic interactions. Previous studies have demonstrated that either coculture with glia or exposure to recombinant bone morphogenetic proteins (BMPs) is both necessary and sufficient to induce dendrite formation. These observations led us to test the hypothesis that BMPs mediate glial-induced dendritic growth. In situ hybridization and immunocytochemical studies indicate that the spatiotemporal expression of BMP5, -6, and -7 in rat superior cervical ganglia (SCG) is consistent with their proposed role in dendritogenesis. In vitro, both SCG glia and neurons were found to express BMP mRNA and protein when grown in the presence or absence of the other cell type. However, addition of ganglionic glia to cultured sympathetic neurons causes a marked increase in BMP proteins coincident with a significant decrease in follistatin and noggin. Functional assays indicate that glial-induced dendritic growth is significantly reduced by BMP7 antibodies and completely inhibited by exogenous noggin and follistatin. These data suggest that glia influence the rapid perinatal expansion of the dendritic arbor in sympathetic neurons by increasing BMP activity via modulation of the balance between BMPs and their antagonists.

MeSH Terms
Active Transport, Cell Nucleus/physiology Animals Antibodies/pharmacology Bone Morphogenetic Proteins/antagonists & inhibitors,genetics,metabolism Carrier Proteins Cell Division/physiology Cells, Cultured Coculture Techniques DNA-Binding Proteins/metabolism Dendrites/drug effects,physiology Down-Regulation/physiology Follistatin/genetics,metabolism Humans In Situ Hybridization Neuroglia/cytology,drug effects,physiology Neurons/cytology,drug effects,metabolism Proteins/genetics,metabolism RNA, Messenger/metabolism Rats Rats, Sprague-Dawley Signal Transduction/drug effects,physiology Smad Proteins Sympathetic Nervous System/cytology,drug effects,metabolism Trans-Activators/metabolism Up-Regulation/physiology
Chemicals
Antibodies Bone Morphogenetic Proteins Carrier Proteins DNA-Binding Proteins Follistatin Proteins RNA, Messenger Smad Proteins Trans-Activators noggin protein
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Lein Pamela J
Department of Environmental Health Sciences, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland 21205-2179, USA. plein@jhsph.edu
Beck Hiroko Nagasawa
Chandrasekaran Vidya
Gallagher Patrick J
Chen Hui-Ling
Lin Yuan
Guo Xin
Kaplan Paul L
Tiedge Henri
Higgins Dennis
References (46)
46 references, click to expand
  1. Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum.
    J Neurosci. 1999 Jun 15;19(12):4994-5004 PMID: 10366632
  2. A new role for glia: generation of neurons!
    Cell. 1999 Jun 11;97(6):667-70 PMID: 10380916
  3. Regulation of the onset of neural crest migration by coordinated activity of BMP4 and Noggin in the dorsal neural tube.
    Development. 1999 Nov;126(21):4749-62 PMID: 10518492
  4. OP-1 enhances dendritic growth from cerebral cortical neurons in vitro.
    Exp Neurol. 1999 Nov;160(1):151-63 PMID: 10630200
  5. Bone morphogenetic protein-7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons.
    Eur J Neurosci. 2000 Jan;12(1):106-16 PMID: 10651865
  6. Activin and bone morphogenetic proteins induce calcitonin gene-related peptide in embryonic sensory neurons in vitro.
    Mol Cell Neurosci. 1999 Dec;14(6):506-18 PMID: 10656256
  7. Noggin is a negative regulator of neuronal differentiation in developing neocortex.
    Dev Neurosci. 2000;22(1-2):68-73 PMID: 10657699
  8. Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration.
    Development. 2000 Nov;127(22):4845-54 PMID: 11044399
  9. Bone morphogenetic proteins induce gremlin, a protein that limits their activity in osteoblasts.
    Endocrinology. 2000 Dec;141(12):4558-63 PMID: 11108268
  10. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis.
    Neuron. 2000 Dec;28(3):713-26 PMID: 11163261
  11. Restricting Bmp-4 mediated apoptosis in hindbrain neural crest.
    Dev Dyn. 2001 Mar;220(3):276-83 PMID: 11241835
  12. Dendritic growth induced by BMP-7 requires Smad1 and proteasome activity.
    J Neurobiol. 2001 Aug;48(2):120-30 PMID: 11438941
  13. Bone morphogenetic protein-2, but not bone morphogenetic protein-7, promotes dendritic growth and calbindin phenotype in cultured rat striatal neurons.
    Neuroscience. 2001;104(3):783-90 PMID: 11440809
  14. Bone morphogenetic protein-5 (BMP-5) promotes dendritic growth in cultured sympathetic neurons.
    BMC Neurosci. 2001;2:12 PMID: 11580864
  15. Osteogenic protein-2. A new member of the transforming growth factor-beta superfamily expressed early in embryogenesis.
    J Biol Chem. 1992 Dec 15;267(35):25220-7 PMID: 1460021
  16. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain.
    Trends Neurosci. 1990 May;13(5):179-84 PMID: 1693236
  17. The use of UV light as a cross-linking agent for cells and tissue sections in in situ hybridization.
    DNA Cell Biol. 1991 Mar;10(2):143-7 PMID: 1706186
  18. Activin-binding protein from rat ovary is follistatin.
    Science. 1990 Feb 16;247(4944):836-8 PMID: 2106159
  19. Glial cells promote dendritic development in rat sympathetic neurons in vitro.
    Glia. 1988;1(6):380-92 PMID: 2976398
  20. Development of the rat superior cervical ganglion: ganglion cell maturation.
    J Neurosci. 1985 Mar;5(3):673-84 PMID: 2983044
  21. Morphological differentiation of embryonic rat sympathetic neurons in tissue culture. I. Conditions under which neurons form axons but not dendrites.
    Dev Biol. 1988 Aug;128(2):324-36 PMID: 3294060
  22. Development and regulation of dendrites in the rat superior cervical ganglion.
    J Neurosci. 1987 Mar;7(3):904-12 PMID: 3559715
  23. Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons.
    Neuron. 1995 Sep;15(3):597-605 PMID: 7546739
  24. glial cells missing: a genetic switch that controls glial versus neuronal fate.
    Cell. 1995 Sep 22;82(6):1013-23 PMID: 7553843
  25. Thrombin receptor activation protects neurons and astrocytes from cell death produced by environmental insults.
    J Neurosci. 1995 Jul;15(7 Pt 2):5389-401 PMID: 7623161
  26. Developmental alteration and neuron-specific expression of bone morphogenetic protein-6 (BMP-6) mRNA in rodent brain.
    Brain Res Mol Brain Res. 1995 Jan;28(1):122-8 PMID: 7707865
  27. Immunolocalization of vgr (BMP-6, DVR-6), a TGF-beta related cytokine, to Schwann cells of the rat peripheral nervous system: expression patterns are not modulated by autoimmune disease.
    Glia. 1995 Jan;13(1):75-8 PMID: 7751058
  28. Expression of BMP-6, a TGF-beta related morphogenetic cytokine, in rat radial glial cells.
    Glia. 1994 Oct;12(2):161-4 PMID: 7868189
  29. Neural induction by the secreted polypeptide noggin.
    Science. 1993 Oct 29;262(5134):713-8 PMID: 8235591
  30. Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: high affinity binding to basement membranes.
    Biochem Biophys Res Commun. 1994 Jan 28;198(2):693-700 PMID: 8297380
  31. Biosynthesis and in vivo localization of the decapentaplegic-Vg-related protein, DVR-6 (bone morphogenetic protein-6).
    J Cell Biol. 1993 Jan;120(2):493-502 PMID: 8421061
  32. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4.
    Cell. 1996 Aug 23;86(4):599-606 PMID: 8752214
  33. The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor.
    Cell. 1996 Aug 23;86(4):607-17 PMID: 8752215
  34. New views on synapse-glia interactions.
    Curr Opin Neurobiol. 1996 Oct;6(5):615-21 PMID: 8937825
  35. Cell division in the developing sympathetic nervous system.
    J Neurocytol. 1977 Jun;6(3):299-309 PMID: 903796
  36. The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4.
    Mech Dev. 1997 Apr;63(1):39-50 PMID: 9178255
  37. Bone morphogenetic proteins: neurotrophic roles for midbrain dopaminergic neurons and implications of astroglial cells.
    Eur J Neurosci. 1997 Aug;9(8):1699-709 PMID: 9283824
  38. Coexpression of the mRNAs encoding retinol dehydrogenase isozymes and cellular retinol-binding protein.
    J Cell Physiol. 1997 Oct;173(1):36-43 PMID: 9326447
  39. Mechanisms of neuronal polarity.
    Curr Opin Neurobiol. 1997 Oct;7(5):599-604 PMID: 9384542
  40. Bone morphogenetic protein-2 and retinoic acid induce neurotrophin-3 responsiveness in developing rat sympathetic neurons.
    Brain Res Mol Brain Res. 1998 Jan;53(1-2):206-17 PMID: 9473674
  41. Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating trkC expression.
    J Neurosci. 1998 May 1;18(9):3314-26 PMID: 9547239
  42. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite.
    Genes Dev. 1998 May 15;12(10):1438-52 PMID: 9585504
  43. Osteogenic protein-1 and related bone morphogenetic proteins regulate dendritic growth and the expression of microtubule-associated protein-2 in rat sympathetic neurons.
    Neurosci Lett. 1998 Apr 10;245(3):131-4 PMID: 9605473
  44. BMPs, Smads and metalloproteases: extracellular and intracellular modes of negative regulation.
    Curr Opin Genet Dev. 1998 Aug;8(4):443-9 PMID: 9729721
  45. Identification of a signaling pathway activated specifically in the somatodendritic compartment by a heparan sulfate that regulates dendrite growth.
    J Neurosci. 1998 Dec 1;18(23):9751-65 PMID: 9822735
  46. Bone morphogenetic proteins induce the expression of noggin, which limits their activity in cultured rat osteoblasts.
    J Clin Invest. 1998 Dec 15;102(12):2106-14 PMID: 9854046
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-12-01
Pages
10377-87
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6758753
Subset
IM
Grants
NIEHS NIH HHS · P30 ES003819 · United States
NINDS NIH HHS · 1 R15 NS/OD36401-01 · United States
NIEHS NIH HHS · 2 P30 ES03819-14 · United States
NINDS NIH HHS · R01 NS34158 · United States
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: product@genelibs.com