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PMID: 10493752 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Both the neuronal and inducible isoforms contribute to upregulation of retinal nitric oxide synthase activity by brain-derived neurotrophic factor.

Klöcker N, Kermer P, Gleichmann M, Weller M, Bähr M

Abstract

Although neurotrophins are best known for their trophic functions, growing evidence suggests that neurotrophins can also be neurotoxic, for instance by enhancing excitotoxic insults. We have shown recently that brain-derived neurotrophic factor (BDNF) limits its neuroprotective action on axotomized rat retinal ganglion cells (RGCs) by upregulating nitric oxide synthase (NOS) activity (Klöcker et al., 1998). The aim of the present study was to investigate this interaction of BDNF and NOS in the lesioned adult rat retina in more detail. We used NOS immunohistochemistry and NADPH-diaphorase (NADPH-d) reaction to characterize morphologically retinal NOS expression and activity. Using reverse transcription-PCR and Western blot analysis, we were able to identify the NOS isoforms being regulated. Six days after optic nerve lesion, we observed an increase in neuronal NOS (NOS-I) mRNA and protein expression in the inner retina. This did not lead to a marked increase in overall retinal NOS activity. Only RGC axons displayed strong de novo NADPH-d reactivity. In contrast, intraocular injection of BDNF resulted in a marked upregulation of NOS activity in NOS-I-immunoreactive structures, leaving the level of NOS-I expression unchanged. In addition, an induction of inducible NOS (NOS-II) was found after BDNF treatment. We identified microglial cells increasing in number and being activated by BDNF, which could serve as the cellular source of NOS-II. In summary, our data suggest that BDNF upregulates retinal NOS activity by both a post-translational regulation of NOS-I activity and an induction of NOS-II. These findings might be useful for developing pharmacological strategies to improve BDNF-mediated neuroprotection.

MeSH Terms
Animals Axotomy Brain-Derived Neurotrophic Factor/pharmacology Female Gene Expression Regulation, Enzymologic/drug effects,physiology Immunohistochemistry Memantine/pharmacology Nerve Fibers/enzymology,ultrastructure Nitric Oxide Synthase/analysis,genetics Nitric Oxide Synthase Type I Nitric Oxide Synthase Type II Optic Nerve/physiology RNA, Messenger/genetics Rats Rats, Inbred Strains Retina/cytology,enzymology Transcription, Genetic/drug effects
Chemicals
Brain-Derived Neurotrophic Factor RNA, Messenger Nitric Oxide Synthase Nitric Oxide Synthase Type I Nitric Oxide Synthase Type II Nos1 protein, rat Nos2 protein, rat Memantine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Klöcker N
Department of Neurology, University of Tübingen, 72076 Tübingen, Germany.
Kermer P
Gleichmann M
Weller M
Bähr M
References (67)
67 references, click to expand
  1. Nitric oxide as a secretory product of mammalian cells.
    FASEB J. 1992 Sep;6(12):3051-64 PMID: 1381691
  2. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function.
    J Neurosci. 1996 Apr 15;16(8):2508-21 PMID: 8786427
  3. BDNF-activated signal transduction in rat cortical glial cells.
    Eur J Neurosci. 1995 May 1;7(5):849-62 PMID: 7613622
  4. Synaptic signaling by nitric oxide.
    Curr Opin Neurobiol. 1997 Jun;7(3):374-8 PMID: 9232800
  5. Up-regulation of Bax protein in degenerating retinal ganglion cells precedes apoptotic cell death after optic nerve lesion in the rat.
    Eur J Neurosci. 1997 Aug;9(8):1763-72 PMID: 9283831
  6. PIN: an associated protein inhibitor of neuronal nitric oxide synthase.
    Science. 1996 Nov 1;274(5288):774-7 PMID: 8864115
  7. Inhibition of CPP32-like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo.
    J Neurosci. 1998 Jun 15;18(12):4656-62 PMID: 9614240
  8. Nitric oxide synthases: roles, tolls, and controls.
    Cell. 1994 Sep 23;78(6):915-8 PMID: 7522969
  9. Neurotrophins and their trk receptors in cultured cells of the glial lineage and in white matter of the central nervous system.
    J Mol Neurosci. 1995;6(4):237-48 PMID: 8860235
  10. Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons.
    J Neurophysiol. 1997 Nov;78(5):2363-71 PMID: 9356388
  11. Nitric oxide: pathophysiological mechanisms.
    Annu Rev Physiol. 1995;57:737-69 PMID: 7539995
  12. Neurobiology of nitric oxide.
    Crit Rev Neurobiol. 1996;10(3-4):291-316 PMID: 8978984
  13. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains.
    Cell. 1996 Mar 8;84(5):757-67 PMID: 8625413
  14. S-nitrosylation regulates apoptosis.
    Nature. 1997 Jul 31;388(6641):432-3 PMID: 9242400
  15. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats.
    J Neurosci. 1988 Jan;8(1):265-80 PMID: 2448429
  16. Lipopolysaccharide enhances synthesis of brain-derived neurotrophic factor in cultured rat microglia.
    J Neurosci Res. 1997 Dec 15;50(6):1023-9 PMID: 9452017
  17. Inhibition of inducible nitric oxide synthase by peroxisome proliferator-activated receptor agonists: correlation with induction of heme oxygenase 1.
    J Immunol. 1998 Jul 15;161(2):978-84 PMID: 9670978
  18. In vivo neurotrophic effects of GDNF on axotomized retinal ganglion cells.
    Neuroreport. 1997 Nov 10;8(16):3439-42 PMID: 9427303
  19. Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-D-aspartate receptor subunit 1.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8191-5 PMID: 9223337
  20. The localization of nitric oxide synthase in the rat eye and related cranial ganglia.
    Neuroscience. 1993 May;54(1):189-200 PMID: 7685860
  21. The role of neurotrophins in the developing nervous system.
    J Neurobiol. 1994 Nov;25(11):1334-48 PMID: 7852989
  22. Memantine reduces functional and morphological consequences induced by global ischemia in rats.
    Neurosci Lett. 1996 Apr 12;208(1):41-4 PMID: 8731170
  23. Differential activation of microglia after experimental spinal cord injury.
    J Neurotrauma. 1999 Mar;16(3):255-65 PMID: 10195473
  24. Bright and dark sides of nitric oxide in ischemic brain injury.
    Trends Neurosci. 1997 Mar;20(3):132-9 PMID: 9061868
  25. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein.
    Neuron. 1992 Nov;9(5):929-42 PMID: 1419001
  26. Nitric oxide inhibits CPP32-like activity under redox regulation.
    Biochem Biophys Res Commun. 1997 Jul 18;236(2):365-9 PMID: 9240442
  27. Factors affecting the survival of cat retinal ganglion cells after optic nerve injury.
    J Neurocytol. 1996 Jun;25(6):393-402 PMID: 8835787
  28. Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells In vivo.
    J Neurosci. 1998 Feb 1;18(3):1038-46 PMID: 9437024
  29. Nitric oxide synthase in motor neurons after axotomy.
    J Histochem Cytochem. 1994 Apr;42(4):451-7 PMID: 7510317
  30. Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies.
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11617-21 PMID: 1280832
  31. Neuroprotective effect of memantine demonstrated in vivo and in vitro.
    Eur J Pharmacol. 1990 Aug 21;185(1):19-24 PMID: 2226632
  32. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1632-6 PMID: 8127857
  33. Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats.
    J Neurobiol. 1993 Jan;24(1):23-36 PMID: 8419522
  34. Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase.
    J Neurosci. 1997 Jun 15;17(12):4633-41 PMID: 9169524
  35. Memantine is neuroprotective in a rat model of pressure-induced retinal ischemia.
    Invest Ophthalmol Vis Sci. 1998 May;39(6):1063-6 PMID: 9579489
  36. Phosphorylation and subcellular translocation of endothelial nitric oxide synthase.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6252-6 PMID: 7687064
  37. AII amacrine cells express functional NMDA receptors.
    Neuroreport. 1997 Mar 24;8(5):1219-23 PMID: 9175117
  38. Nitric oxide signaling in the central nervous system.
    Annu Rev Physiol. 1995;57:683-706 PMID: 7539993
  39. BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities.
    Brain Res Mol Brain Res. 1998 Mar 30;55(1):20-7 PMID: 9645956
  40. Axotomy-induced apoptotic cell death of neonatal rat facial motoneurons: time course analysis and relation to NADPH-diaphorase activity.
    Exp Neurol. 1996 Mar;138(1):33-44 PMID: 8593894
  41. Neurotrophic factors and their receptors.
    Curr Opin Cell Biol. 1995 Apr;7(2):148-55 PMID: 7612265
  42. Chronic low-dose glutamate is toxic to retinal ganglion cells. Toxicity blocked by memantine.
    Invest Ophthalmol Vis Sci. 1996 Jul;37(8):1618-24 PMID: 8675405
  43. BDNF potentiates spontaneous Ca2+ oscillations in cultured hippocampal neurons.
    Brain Res. 1997 Dec 19;778(2):318-28 PMID: 9459549
  44. MK-801 reduces retinal ganglion cell survival but improves visual performance after controlled optic nerve crush.
    J Neurotrauma. 1996 Dec;13(12):791-800 PMID: 9002064
  45. Expression of glutamate receptor genes in the mammalian retina: the localization of GluR1 through GluR7 mRNAs.
    J Neurosci. 1993 May;13(5):1888-98 PMID: 8478682
  46. Potentiated necrosis of cultured cortical neurons by neurotrophins.
    Science. 1995 Apr 28;268(5210):573-5 PMID: 7725105
  47. Expression of NMDA and high-affinity kainate receptor subunit mRNAs in the adult rat retina.
    Eur J Neurosci. 1994 Jul 1;6(7):1100-12 PMID: 7952290
  48. NADPH diaphorase expression in the rat retina after axotomy--a supportive role for nitric oxide.
    Eur J Neurosci. 1995 Nov 1;7(11):2226-39 PMID: 8563972
  49. Nitric oxide synthases: properties and catalytic mechanism.
    Annu Rev Physiol. 1995;57:707-36 PMID: 7539994
  50. Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells. A quantitative in vivo study.
    Invest Ophthalmol Vis Sci. 1996 Mar;37(4):489-500 PMID: 8595949
  51. Brain-derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex.
    J Physiol. 1997 Jan 1;498 ( Pt 1):153-64 PMID: 9023775
  52. Structure-function relationships in the neurotrophin family.
    J Neurobiol. 1994 Nov;25(11):1349-61 PMID: 7852990
  53. CREB: a major mediator of neuronal neurotrophin responses.
    Neuron. 1997 Nov;19(5):1031-47 PMID: 9390517
  54. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo.
    Brain Res. 1993 Feb 5;602(2):304-17 PMID: 8448673
  55. Apoptosis in adult retinal ganglion cells after axotomy.
    J Neurobiol. 1994 Apr;25(4):431-8 PMID: 8077968
  56. Nitric oxide inhibits c-Jun N-terminal kinase 2 (JNK2) via S-nitrosylation.
    Biochem Biophys Res Commun. 1998 Jun 29;247(3):809-13 PMID: 9647775
  57. Localization of NADPH-diaphorase/nitric oxide synthase in the rat retina: an electron microscopic study.
    Brain Res. 1995 Sep 4;690(2):231-5 PMID: 8535841
  58. Physiology of the neurotrophins.
    Annu Rev Neurosci. 1996;19:289-317 PMID: 8833445
  59. Nitric oxide synthase: aspects concerning structure and catalysis.
    Cell. 1994 Sep 23;78(6):927-30 PMID: 7522970
  60. Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-alpha/lipopolysaccharide.
    J Neurochem. 1998 Jul;71(1):88-94 PMID: 9648854
  61. The action of neurotrophins in the development and plasticity of the visual cortex.
    Prog Neurobiol. 1996 May;49(1):53-71 PMID: 8817698
  62. Induction of major histocompatibility class II antigen on microglial cells in postnatal and adult rats following intraperitoneal injections of lipopolysaccharide.
    Neurosci Res. 1997 Jun;28(2):111-8 PMID: 9220468
  63. Rat retinal ganglion cells express Ca(2+)-permeable non-NMDA glutamate receptors during the period of histogenetic cell death.
    Neurosci Lett. 1993 Apr 16;153(1):32-6 PMID: 8510821
  64. NO at work.
    Cell. 1994 Sep 23;78(6):919-25 PMID: 7923361
  65. Brain-derived neurotrophic factor modulates the development of the dopaminergic network in the rodent retina.
    J Neurosci. 1998 May 1;18(9):3351-62 PMID: 9547243
  66. Memantine reduces alterations to the mammalian retina, in situ, induced by ischemia.
    Vis Neurosci. 1999 Jan-Feb;16(1):45-52 PMID: 10022477
  67. Neurotrophic molecules.
    Ann Neurol. 1989 Oct;26(4):489-506 PMID: 2684002
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
1999-10-01
Pages
8517-27
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6783014
Subset
IM
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