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Nitric oxide targets oligodendrocytes and promotes their morphological differentiation.

Garthwaite G, Hampden-Smith K, Wilson GW, Goodwin DA, Garthwaite J - Glia (2014)

Bottom Line: This stimulation of oligodendrocyte growth could be replicated by low concentrations of 8-bromo-cGMP (maximum effect at 1 µM).It is concluded that oligodendrocytes are probably widespread targets for physiological NO (or natriuretic peptide) signals, with the resulting rise in cGMP serving to enhance their growth and maturation.NO might help coordinate the myelination of axons to the ongoing level of neuronal activity during development and could potentially contribute to adaptive changes in myelination in the adult.

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Affiliation: Wolfson Institute for Biomedical Research, University College London, London, WC1E 6BT, United Kingdom.

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Targeting of oligodendrocytes in slices of adult rat cerebellum by exogenous and endogenous NO. Slices were stimulated by (A) PAPA/NO (30 μM, 5 min), (B, C) BAY 41-2272 (3 μM, 5 min), (D) ANP (1 μM, 10 min) or (E) NMDA (30 μM, 2 min) all in the presence of IBMX (1 mM). L-nitroarginine (L-NNA, 100 μM) was present in C and D. Sections were stained for cGMP (green), CNPase (red) and DAPI (blue). Images are all overlays (red/green co-staining appears yellow) and are representative of six slices per condition in two experiments. Key: ml, molecular layer; P, Purkinje cell; Bg, Bergmann glia; gcl, granule cell layer, wm = white matter; arrows, oligodendrocytes; arrowheads, putative astrocytes. Scale bar (A) = 50 μm (applies to all panels). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]
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fig05: Targeting of oligodendrocytes in slices of adult rat cerebellum by exogenous and endogenous NO. Slices were stimulated by (A) PAPA/NO (30 μM, 5 min), (B, C) BAY 41-2272 (3 μM, 5 min), (D) ANP (1 μM, 10 min) or (E) NMDA (30 μM, 2 min) all in the presence of IBMX (1 mM). L-nitroarginine (L-NNA, 100 μM) was present in C and D. Sections were stained for cGMP (green), CNPase (red) and DAPI (blue). Images are all overlays (red/green co-staining appears yellow) and are representative of six slices per condition in two experiments. Key: ml, molecular layer; P, Purkinje cell; Bg, Bergmann glia; gcl, granule cell layer, wm = white matter; arrows, oligodendrocytes; arrowheads, putative astrocytes. Scale bar (A) = 50 μm (applies to all panels). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Mentions: The only previous study of this type had indicated that corpus callosal oligodendrocyte cGMP accumulation in response to NO is only transient during development, being most evident in the 2-week-old rat and declining thereafter (Tanaka et al., 1997). To examine the applicability of this result to the cerebellum, oligodendrocytes in slices from 3-week-old and adult (6-weeks-old) rats were tested for sensitivity to exogenous and endogenous NO, as well as to ANP. The adult tissue responded similarly to the slices from immature (8- to 10-day-old) animals described above. In brief, exposure to PAPA/NO caused cGMP immunostaining of oligodendrocytes located in the white matter and also within the internal granule cell layer (Fig. 5A). BAY 41-2272 generated a similar profile of cGMP immunostaining (Fig. 5B) that was abolished by L-nitroarginine (Fig. 5C). ANP (in the presence of L-nitroarginine) also evoked cGMP accumulation in oligodendrocytes in white and grey matter (Fig. 5D), as did NMDA (Fig. 5E). Strong cGMP immunoreactivity in Bergmann glia and other cells presumed to be astrocytes was also observed with PAPA/NO, BAY 41-2272 (without L-nitroarginine), ANP, and NMDA. Enlargements from Fig. 5 are in Supporting Information Fig. S1. The results using 3-week-old rat cerebellar slices subjected to PAPA/NO were closely comparable to those from the adult (not illustrated).


Nitric oxide targets oligodendrocytes and promotes their morphological differentiation.

Garthwaite G, Hampden-Smith K, Wilson GW, Goodwin DA, Garthwaite J - Glia (2014)

Targeting of oligodendrocytes in slices of adult rat cerebellum by exogenous and endogenous NO. Slices were stimulated by (A) PAPA/NO (30 μM, 5 min), (B, C) BAY 41-2272 (3 μM, 5 min), (D) ANP (1 μM, 10 min) or (E) NMDA (30 μM, 2 min) all in the presence of IBMX (1 mM). L-nitroarginine (L-NNA, 100 μM) was present in C and D. Sections were stained for cGMP (green), CNPase (red) and DAPI (blue). Images are all overlays (red/green co-staining appears yellow) and are representative of six slices per condition in two experiments. Key: ml, molecular layer; P, Purkinje cell; Bg, Bergmann glia; gcl, granule cell layer, wm = white matter; arrows, oligodendrocytes; arrowheads, putative astrocytes. Scale bar (A) = 50 μm (applies to all panels). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]
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fig05: Targeting of oligodendrocytes in slices of adult rat cerebellum by exogenous and endogenous NO. Slices were stimulated by (A) PAPA/NO (30 μM, 5 min), (B, C) BAY 41-2272 (3 μM, 5 min), (D) ANP (1 μM, 10 min) or (E) NMDA (30 μM, 2 min) all in the presence of IBMX (1 mM). L-nitroarginine (L-NNA, 100 μM) was present in C and D. Sections were stained for cGMP (green), CNPase (red) and DAPI (blue). Images are all overlays (red/green co-staining appears yellow) and are representative of six slices per condition in two experiments. Key: ml, molecular layer; P, Purkinje cell; Bg, Bergmann glia; gcl, granule cell layer, wm = white matter; arrows, oligodendrocytes; arrowheads, putative astrocytes. Scale bar (A) = 50 μm (applies to all panels). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]
Mentions: The only previous study of this type had indicated that corpus callosal oligodendrocyte cGMP accumulation in response to NO is only transient during development, being most evident in the 2-week-old rat and declining thereafter (Tanaka et al., 1997). To examine the applicability of this result to the cerebellum, oligodendrocytes in slices from 3-week-old and adult (6-weeks-old) rats were tested for sensitivity to exogenous and endogenous NO, as well as to ANP. The adult tissue responded similarly to the slices from immature (8- to 10-day-old) animals described above. In brief, exposure to PAPA/NO caused cGMP immunostaining of oligodendrocytes located in the white matter and also within the internal granule cell layer (Fig. 5A). BAY 41-2272 generated a similar profile of cGMP immunostaining (Fig. 5B) that was abolished by L-nitroarginine (Fig. 5C). ANP (in the presence of L-nitroarginine) also evoked cGMP accumulation in oligodendrocytes in white and grey matter (Fig. 5D), as did NMDA (Fig. 5E). Strong cGMP immunoreactivity in Bergmann glia and other cells presumed to be astrocytes was also observed with PAPA/NO, BAY 41-2272 (without L-nitroarginine), ANP, and NMDA. Enlargements from Fig. 5 are in Supporting Information Fig. S1. The results using 3-week-old rat cerebellar slices subjected to PAPA/NO were closely comparable to those from the adult (not illustrated).

Bottom Line: This stimulation of oligodendrocyte growth could be replicated by low concentrations of 8-bromo-cGMP (maximum effect at 1 µM).It is concluded that oligodendrocytes are probably widespread targets for physiological NO (or natriuretic peptide) signals, with the resulting rise in cGMP serving to enhance their growth and maturation.NO might help coordinate the myelination of axons to the ongoing level of neuronal activity during development and could potentially contribute to adaptive changes in myelination in the adult.

View Article: PubMed Central - PubMed

Affiliation: Wolfson Institute for Biomedical Research, University College London, London, WC1E 6BT, United Kingdom.

Show MeSH
Related in: MedlinePlus