Skip to main content
Journal of Anatomy logoLink to Journal of Anatomy
. 1991 Aug;177:145–158.

Haemopoietic phagocytes in the early differentiating avian retina.

M A Cuadros 1, M García-Martín 1, C Martin 1, A Ríos 1
PMCID: PMC1260422  PMID: 1769889

Abstract

The existence of specialised phagocytic cells is described in regions of the retinal neuroepithelium undergoing intense cell death during early differentiation of the avian embryo retina (2.5-5 days of incubation). These results were obtained using routine techniques for light microscopy, acid phosphatase histochemistry and immunocytochemical staining with antibodies MB-1 and QH-1, both specific for quail endothelial cells and all blood cells except mature erythrocytes. Specialised phagocytes were distinguishable from neuroepithelial cells on the basis of morphological criteria: in the former, the nucleus was not oval in shape and was not oriented perpendicular to basement membrane neuroepithelium. The cytoplasm of the specialised phagocytes was often filled with dead cell fragments. In contrast to neuroepithelial cells, the specialised phagocytes showed acid phosphatase activity and were labelled with both MB-1 and QH-1 antibodies in normal quail embryos and chick----quail yolk sac chimeras. Moreover, some acid phosphatase positive and MB-1/QH-1 positive cells also appeared in the presumptive vitreous body, at the edges of the optic cup and in the surrounding mesenchyme. As the vitreal cells and the specialised phagocytes of the neural retina were immunolabelled in chick----quail yolk sac chimeras, we conclude that they are derived from haemopoietic cells in the yolk sac. Some images suggest that these cells enter the vitreous body from the surrounding mesenchyme and traverse the basement membrane of the neuroepithelium in the optic disc region to give rise to the specialised phagocytes of the retinal neuroepithelium.

Full text

PDF
145

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashwell K. W., Holländer H., Streit W., Stone J. The appearance and distribution of microglia in the developing retina of the rat. Vis Neurosci. 1989;2(5):437–448. doi: 10.1017/s0952523800012335. [DOI] [PubMed] [Google Scholar]
  2. Chu-Wang I. W., Oppenheim R. W. Cell death of motoneurons in the chick embryo spinal cord. I. A light and electron microscopic study of naturally occurring and induced cell loss during development. J Comp Neurol. 1978 Jan 1;177(1):33–57. doi: 10.1002/cne.901770105. [DOI] [PubMed] [Google Scholar]
  3. Clarke P. G. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 1990;181(3):195–213. doi: 10.1007/BF00174615. [DOI] [PubMed] [Google Scholar]
  4. Cuadros M. A., Rios A. Spatial and temporal correlation between early nerve fiber growth and neuroepithelial cell death in the chick embryo retina. Anat Embryol (Berl) 1988;178(6):543–551. doi: 10.1007/BF00305042. [DOI] [PubMed] [Google Scholar]
  5. Fujimoto E., Miki A., Mizoguti H. Histochemical studies of the differentiation of microglial cells in the cerebral hemispheres of chick embryos and chicks. Histochemistry. 1987;87(3):209–216. doi: 10.1007/BF00492411. [DOI] [PubMed] [Google Scholar]
  6. García-Porrero J. A., Colvée E., Ojeda J. L. Cell death in the dorsal part of the chick optic cup. Evidence for a new necrotic area. J Embryol Exp Morphol. 1984 Apr;80:241–249. [PubMed] [Google Scholar]
  7. García-Porrero J. A., Colvée E., Ojeda J. L. The mechanisms of cell death and phagocytosis in the early chick lens morphogenesis: a scanning electron microscopy and cytochemical approach. Anat Rec. 1984 Jan;208(1):123–136. doi: 10.1002/ar.1092080113. [DOI] [PubMed] [Google Scholar]
  8. García-Porrero J. A., Ojeda J. L. Cell death and phagocytosis in the neuroepithelium of the developing retina. A TEM and SEM study. Experientia. 1979 Mar 15;35(3):375–376. doi: 10.1007/BF01964362. [DOI] [PubMed] [Google Scholar]
  9. HAMBURGER V. Regression versus peripheral control of differentiation in motor hypoplasia. Am J Anat. 1958 May;102(3):365–409. doi: 10.1002/aja.1001020303. [DOI] [PubMed] [Google Scholar]
  10. Hinds J. W., Hinds P. L. Early development of amacrine cells in the mouse retina: an electron microscopic, serial section analysis. J Comp Neurol. 1978 May 15;179(2):277–300. doi: 10.1002/cne.901790204. [DOI] [PubMed] [Google Scholar]
  11. Hinds J. W., Hinds P. L. Early ganglion cell differentiation in the mouse retina: an electron microscopic analysis utilizing serial sections. Dev Biol. 1974 Apr;37(2):381–416. doi: 10.1016/0012-1606(74)90156-0. [DOI] [PubMed] [Google Scholar]
  12. Horsburgh G. M., Sefton A. J. The early development of the optic nerve and chiasm in embryonic rat. J Comp Neurol. 1986 Jan 22;243(4):547–560. doi: 10.1002/cne.902430409. [DOI] [PubMed] [Google Scholar]
  13. Hume D. A., Perry V. H., Gordon S. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol. 1983 Jul;97(1):253–257. doi: 10.1083/jcb.97.1.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jordan F. L., Thomas W. E. Brain macrophages: questions of origin and interrelationship. Brain Res. 1988 Apr-Jun;472(2):165–178. doi: 10.1016/0165-0173(88)90019-7. [DOI] [PubMed] [Google Scholar]
  15. KALLEN B. Cell degeneration during normal ontogenesis of the rabbit brain. J Anat. 1955 Apr;89(2):153–161. [PMC free article] [PubMed] [Google Scholar]
  16. Kerr J. F., Wyllie A. H., Currie A. R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972 Aug;26(4):239–257. doi: 10.1038/bjc.1972.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kálmán M. Dead cells can be phagocytosed by any neighboring cell in early developing rat brain. Int J Neurosci. 1989 Jun;46(3-4):139–145. doi: 10.3109/00207458908986251. [DOI] [PubMed] [Google Scholar]
  18. Linden R., Cavalcante L. A., Barradas P. C. Mononuclear phagocytes in the retina of developing rats. Histochemistry. 1986;85(4):335–339. doi: 10.1007/BF00493486. [DOI] [PubMed] [Google Scholar]
  19. Martin C. Technique d'explanation in ovo de blastodermes d'embryons d'oiseaux. C R Seances Soc Biol Fil. 1972 Nov 9;166(2):283–285. [PubMed] [Google Scholar]
  20. Martín-Partido G., Navascués J. Macrophage-like cells in the presumptive optic pathways in the floor of the diencephalon of the chick embryo. J Neurocytol. 1990 Dec;19(6):820–832. doi: 10.1007/BF01186813. [DOI] [PubMed] [Google Scholar]
  21. Martín-Partido G., Rodríguez-Gallardo L., Alvarez I. S., Navascués J. Cell death in the ventral region of the neural retina during the early development of the chick embryo eye. Anat Rec. 1988 Nov;222(3):272–281. doi: 10.1002/ar.1092220308. [DOI] [PubMed] [Google Scholar]
  22. Matsumoto Y., Ikuta F. Appearance and distribution of fetal brain macrophages in mice. Immunohistochemical study with a monoclonal antibody. Cell Tissue Res. 1985;239(2):271–278. doi: 10.1007/BF00218004. [DOI] [PubMed] [Google Scholar]
  23. McMenamin P. G., Loeffler K. U. Cells resembling intraventricular macrophages are present in the subretinal space of human foetal eyes. Anat Rec. 1990 Jun;227(2):245–253. doi: 10.1002/ar.1092270213. [DOI] [PubMed] [Google Scholar]
  24. Meller K. Effects of concanavalin A on developing ganglion cells in the retina of chick embryos. J Embryol Exp Morphol. 1981 Oct;65:27–39. [PubMed] [Google Scholar]
  25. Murabe Y., Sano Y. Morphological studies on neuroglia. VII. Distribution of "brain macrophages" in brains of neonatal and adult rats, as determined by means of immunohistochemistry. Cell Tissue Res. 1983;229(1):85–95. doi: 10.1007/BF00217882. [DOI] [PubMed] [Google Scholar]
  26. Namba M., Dannenberg A. M., Jr, Tanaka F. Improvement in the histochemical demonstration of acid phosphatase, beta-galactosidase and nonspecific esterase in glycol methacrylate tissue sections by cold temperature embedding. Stain Technol. 1983 Jul;58(4):207–213. doi: 10.3109/10520298309066786. [DOI] [PubMed] [Google Scholar]
  27. Navascués J., Martín-Partido G., Alvarez I. S., Rodríguez-Gallardo L. Cell death in suboptic necrotic centers of chick embryo diencephalon and their topographic relationship with the earliest optic fiber fascicles. J Comp Neurol. 1988 Dec 1;278(1):34–46. doi: 10.1002/cne.902780103. [DOI] [PubMed] [Google Scholar]
  28. O'Connor T. M., Wyttenbach C. R. Cell death in the embryonic chick spinal cord. J Cell Biol. 1974 Feb;60(2):448–459. doi: 10.1083/jcb.60.2.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pardanaud L., Altmann C., Kitos P., Dieterlen-Lievre F., Buck C. A. Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development. 1987 Jun;100(2):339–349. doi: 10.1242/dev.100.2.339. [DOI] [PubMed] [Google Scholar]
  30. Peault B. M., Thiery J. P., Le Douarin N. M. Surface marker for hemopoietic and endothelial cell lineages in quail that is defined by a monoclonal antibody. Proc Natl Acad Sci U S A. 1983 May;80(10):2976–2980. doi: 10.1073/pnas.80.10.2976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schook P. Morphogenetic movements during the early development of the chick eye. An ultrastructural and spatial reconstructive study. B. Invagination of the optic vesicle and fusion of its walls. Acta Morphol Neerl Scand. 1980 Jun;18(23):159–180. [PubMed] [Google Scholar]
  32. Silver J., Hughes A. F. The relationship between morphogenetic cell death and the development of congenital anophthalmia. J Comp Neurol. 1974 Oct 1;157(3):281–301. doi: 10.1002/cne.901570303. [DOI] [PubMed] [Google Scholar]
  33. Silver J., Hughes A. F. The role of cell death during morphogenesis of the mammalian eye. J Morphol. 1973 Jun;140(2):159–170. doi: 10.1002/jmor.1051400204. [DOI] [PubMed] [Google Scholar]
  34. Silver J., Robb R. M. Studies on the development of the eye cup and optic nerve in normal mice and in mutants with congenital optic nerve aplasia. Dev Biol. 1979 Jan;68(1):175–190. doi: 10.1016/0012-1606(79)90252-5. [DOI] [PubMed] [Google Scholar]
  35. Theiler K., Varnum D. S., Nadeau J. H., Stevens L. C., Cagianut B. A new allele of ocular retardation: early development and morphogenetic cell death. Anat Embryol (Berl) 1976 Dec 22;150(1):85–97. doi: 10.1007/BF00346288. [DOI] [PubMed] [Google Scholar]
  36. Tseng C. Y., Ling E. A., Wong W. C. Light and electron microscopic and cytochemical identification of amoeboid microglial cells in the brain of prenatal rats. J Anat. 1983 Jun;136(Pt 4):837–849. [PMC free article] [PubMed] [Google Scholar]
  37. Ulshafer R. J., Clavert A. Cell death and optic fiber penetration in the optic stalk of the chick. J Morphol. 1979 Oct;162(1):67–76. doi: 10.1002/jmor.1051620105. [DOI] [PubMed] [Google Scholar]
  38. Young R. W. Cell death during differentiation of the retina in the mouse. J Comp Neurol. 1984 Nov 1;229(3):362–373. doi: 10.1002/cne.902290307. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES