Macrophages during avian optic nerve development: relationship to cell death and differentiation into microglia

Moujahid, Amale; Navascués, Julio; Marín‐Teva, José L.; Cuadros, Miguel A.

doi:10.1007/bf00214704

Cited by 39 publications

(49 citation statements)

References 46 publications

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“…The definitive characterization of cathepsin B/ D-expressing cells was confirmed by their histochemical labeling with TL that recognizes macrophage/microglial cells in the nervous system of rodents (Acarin et al, 1994;Santos et al, 2008). Furthermore, in most cases, cathepsin B/D-expressing cells were in chronotopographical coincidence with regions affected by extensive cell death during development, as has been shown for cell death and macrophage/microglial precursors in the nervous parenchyma (Hume et al, 1983;Navascues and MartinPartido, 1990;Martin-Partido et al, 1991;Perry et al, 1993;Moujahid et al, 1996;Rodriguez-Gallardo et al, 2005;Santos et al, 2008).…”

Section: Cathepsin B and D Expression In Macrophages And Microglial Pmentioning

confidence: 67%

“…This morphology is maintained at postnatal stages. These morphological changes have also been observed in the developing avian optic nerve (Moujahid et al, 1996). Those authors suggested that macrophages show different morphological features due to the changes in the cell environment during the optic stalk-optic nerve transition, passing from a neuroepithelial to a fibrous environment.…”

Section: Spatiotemporal Distribution Of Cathepsin B/d-expressing Macrmentioning

confidence: 71%

“…Only a few studies have dealt with the ontogeny of macrophages and microglial cells during development of the vertebrate optic pathways (Martin-Partido and Martin-Partido et al, 1991;Moujahid et al, 1996;Rodriguez-Gallardo et al, 2005). At early stages, cathepsin B/D-positive macrophages were observed in close relationship with areas of extensive cell death, such as the ventral optic nerve and the SONCs (see below), indicating that these cells phagocytose cell debris (Martin-Partido and Moujahid et al, 1996;Rodriguez-Gallardo et al, 2005).…”

Section: Spatiotemporal Distribution Of Cathepsin B/d-expressing Macrmentioning

confidence: 99%

“…At early stages, cathepsin B/D-positive macrophages were observed in close relationship with areas of extensive cell death, such as the ventral optic nerve and the SONCs (see below), indicating that these cells phagocytose cell debris (Martin-Partido and Moujahid et al, 1996;Rodriguez-Gallardo et al, 2005). However, TUNEL analysis revealed a weak cytoplasmic signal in neuroepithelial cells near the SONCs, indicating that they also engulf cell debris, as has previously been described in our laboratory MartinPartido and Navascues, 1990).…”

Section: Spatiotemporal Distribution Of Cathepsin B/d-expressing Macrmentioning

confidence: 99%

“…Cell death has been characterized in several vertebrate species in the developing retina (Glucksmann, 1951;Young, 1984;Cuadros and Rios, 1988;Martin-Partido et al, 1988;Cook et al, 1998;Diaz et al, 1999Diaz et al, , 2000Marin-Teva et al, 1999;Cusato et al, 2001;Mayordomo et al, 2003;Francisco-Morcillo et al, 2004;Candal et al, 2005;Rodriguez-Gallardo et al, 2005;Hidalgo-Sanchez et al, 2006;Valenciano et al, 2009;BejaranoEscobar et al, 2010) and optic pathways (Horsburgh and Sefton, 1986;Navascues et al, 1988;Moujahid et al, 1996;Rodriguez-Gallardo et al, 2005;Hidalgo-Sanchez et al, 2007). The three main phases of cell death that occur during development are denominated morphogenetic cell death, coinciding with the invagination of the optic vesicle, early neural cell death, associated with the differentiation of the first retinal neurons, and neurotrophic cell death, coinciding with the time of synaptogenesis of the retinal ganglion cells and their postsynaptic partners (for a review, see Valenciano et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Macrophage and microglia ontogeny in the mouse visual system can be traced by the expression of Cathepsins B and D

Bejarano-Escobar

Holguín-Arévalo

Montero

et al. 2011

Developmental Dynamics

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Here, we show a detailed chronotopographical analysis of cathepsin B and D expression during development of the mouse visual system. Both proteases were detected in large rounded/ameboid cells usually located in close relationship with prominent sites of extensive physiological cell death. In concordance with their morphological features and topographical distribution, we demonstrate that expressing cells corresponded with macrophages and microglial precursors. We found that as microglial precursors differentiated the expression of both cathepsins was down-regulated. Of interest, cathepsin B and D transcripts were never observed in degenerating cells. Our findings point to a role for cathepsin D and B in cell debris degradation after apoptotic processes rather than promoting cell death, as proposed for other developmental models. Additionally their pattern of expression suggests a role in the maturation of the microglial precursors.

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Section: Cathepsin B and D Expression In Macrophages And Microglial Pmentioning

confidence: 67%

Section: Spatiotemporal Distribution Of Cathepsin B/d-expressing Macrmentioning

confidence: 71%

Section: Spatiotemporal Distribution Of Cathepsin B/d-expressing Macrmentioning

confidence: 99%

Section: Spatiotemporal Distribution Of Cathepsin B/d-expressing Macrmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Macrophage and microglia ontogeny in the mouse visual system can be traced by the expression of Cathepsins B and D

Bejarano-Escobar

Holguín-Arévalo

Montero

et al. 2011

Developmental Dynamics

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Naturally occurring cell death and migration of microglial precursors in the quail retina during normal development

Marín‐Teva¹,

Cuadros

Calvente

et al. 1999

J. Comp. Neurol.

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We compared chronotopographical patterns of distribution of naturally occurring neuronal death in the ganglion cell layer (GCL) and the inner nuclear layer (INL) with patterns of tangential and radial migration of microglial precursors during quail retinal development. Apoptotic cells were identified by the terminal deoxynucleotidyl transferase‐mediated deoxyuridine triphosphate nick end labeling technique, and microglial precursors were identified by immunocytochemistry with an antibody recognizing quail microglial cells (QH1 antibody). Apoptotic cells were first detectable in the GCL at the seventh day of incubation (E7), were most abundant at E10, and were absent after E13. In the INL, apoptotic cells first appeared at E7, were most abundant at E12, and disappeared entirely after the third posthatching day (P3). In both retinal layers, cell death first appeared in a small central area of the retina and subsequently spread along three gradients: central‐to‐peripheral, temporal‐to‐nasal, and dorsal‐to‐ventral. The chronology of tangential (between E7 and E16) and radial migration (between E8 and P3) of microglial precursors was highly coincident with that of cell death in the GCL and INL. Comparison of the chronotopographical pattern of distribution of apoptotic nuclei in the GCL with the patterns of tangential and radial migration of microglial precursors neither supported nor refuted the hypothesis that ganglion cell death is the stimulus that triggers the entry and migration of microglial precursors in the developing retina. However, microglial cells in most of the retina traversed the INL only after cell death had ceased in this layer, suggesting that cell death in the INL does not attract microglial precursors migrating radially. Dead cell debris in this layer was phagocytosed by Müller cells, whereas migrating microglial cells were seen phagocytosing apoptotic bodies in the nerve fiber layer and GCL but not in the INL. J. Comp. Neurol. 412:255–275, 1999. © 1999 Wiley‐Liss, Inc.

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Development of microglia in the postnatal rat hippocampus

Dalmau

Finsen²,

Zimmer³

et al. 1998

Hippocampus

115

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During the prenatal development of the hippocampus, microglial cell precursors progressively occur in all subfields in accordance with known ontogenetic gradients of the region (Dalmau et al., J. Comp. Neurol. 1997a;377:70–84). The present study follows the regional distribution of these microglial cell precursors and their morphological differentiation in the rat hippocampus from birth to postnatal (P) day 18. The results demonstrate that the cellular differentiation and the subregional distribution of microglia follow the specific developmental gradients of the different parts of Ammon's horn and the dentate gyrus. Microglial cell distribution in the dentate gyrus is thus delayed compared with that in Ammon's horn. The appearance of microglia in the hippocampal subregions and differentiation of cell precursors into adult microglia occur earlier at temporal levels than at septal levels. Distribution of microglial cells follows an outside‐to‐inside pattern from the hippocampal fissure to the main cell layers in either Ammon's horn or the dentate gyrus. Meanwhile, the resident microglial cells located in the stratum oriens and dentate hilus at birth also increase in number and gradually disperse throughout the whole tissue of the two layers with age. In Ammon's horn, microglial differentiation occurs earlier in CA3 than in CA1. In the dentate gyrus, microglia appear earlier in relation to the external limb than to the internal limb, largely following a lateral‐to‐medial gradient. The differentiation and appearance of microglia in the various hippocampal and dentate subregions often correspond to the developmental stage of intrinsic and extrinsic afferent nerve fiber projections. Finally, in both Ammon's horn and the dentate gyrus, cells resembling reactive microglia are also observed and, in particular, in the perforant path projections from P9 to P18, suggesting their participation not only in phagocytosis of dead cells but also in axonal elimination and/or fiber reorganization. Hippocampus 1998;8:458–474. © 1998 Wiley‐Liss, Inc.

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Macrophages during avian optic nerve development: relationship to cell death and differentiation into microglia

Cited by 39 publications

References 46 publications

Macrophage and microglia ontogeny in the mouse visual system can be traced by the expression of Cathepsins B and D

Macrophage and microglia ontogeny in the mouse visual system can be traced by the expression of Cathepsins B and D

Naturally occurring cell death and migration of microglial precursors in the quail retina during normal development

Development of microglia in the postnatal rat hippocampus

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