{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T15:41:14Z","timestamp":1780414874545,"version":"3.54.1"},"reference-count":64,"publisher":"Wiley","issue":"3","license":[{"start":{"date-parts":[[2004,10,9]],"date-time":"2004-10-09T00:00:00Z","timestamp":1097280000000},"content-version":"vor","delay-in-days":5626,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J of Comparative Neurology"],"published-print":{"date-parts":[[1989,5,15]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>In an effort to understand naturally occurring neuronal death in the developing isthmo\u2010optic nucleus, we have accentuated one of its most probably causes, failure to receive adequate trophic maintenance from the axonal terminal zone in the retina, and have studied the dying neurons ultrastructurally. Retrograde trophic maintenance was blocked by means of intraocularly injected colchicine, which caused all the isthmo\u2010optic neurons to die by just one of the two or more kinds of cell death that they undergo during normal development. The present paper deals with the very prominent cytoplasmic aspects of this kind of cell death, notably the uptake of exogenous horseradish peroxidase and autophagy. There were also nuclear changes, which are dealt with mainly in the accompanying paper (Clarke and Hornung, <jats:italic>J. Comp. Neurol. 283<\/jats:italic>: 438\u2013449, '89).<\/jats:p><jats:p>Numerous cytoplasmic vacuoles occurred in both soma and dendrites, and they were of three main kinds, of which the smallest (less than 0.5 \u03bcm diameter) had unstructured contents, whereas the larger two (1\u20132 \u03bcm and 2\u20137 \u03bcm) were secondary lysosomes (mostly residual bodies).<\/jats:p><jats:p>Intravascularly injected horseradish peroxidase labeled all three kinds of vacuole but not the free cytoplasm, indicating that the uptake was by endocytosis rather than by leakage through holes in the membrane, as is confirmed by our failure to detect any such holes. We suspect that the smallest vacuoles are the primary endosomes, that these subsequently fuse with vacuoles of the intermediate kind, and that the largest vacuoles are formed by the fusion of these latter. The purpose of the endocytosis may be to channel the plasma membrane piecemeal into the lysosomes for destruction.<\/jats:p>","DOI":"10.1002\/cne.902830310","type":"journal-article","created":{"date-parts":[[2005,1,1]],"date-time":"2005-01-01T21:32:23Z","timestamp":1104615143000},"page":"425-437","source":"Crossref","is-referenced-by-count":57,"title":["Endocytosis and autophagy in dying neurons: An ultrastructural study in chick embryos"],"prefix":"10.1002","volume":"283","author":[{"given":"J. P.","family":"Hornung","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.","family":"Koppel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"P. G. H.","family":"Clarke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2004,10,9]]},"reference":[{"key":"e_1_2_1_2_1","doi-asserted-by":"publisher","DOI":"10.1159\/000112736"},{"key":"e_1_2_1_3_1","doi-asserted-by":"publisher","DOI":"10.1097\/00005072-197304000-00004"},{"key":"e_1_2_1_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0074-7696(08)61675-7"},{"key":"e_1_2_1_5_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01257989"},{"key":"e_1_2_1_6_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-94-011-6921-9_14"},{"key":"e_1_2_1_7_1","first-page":"237","article-title":"Ultrastructure of the preparative phase of cell death in the larval fat body of Drosophila melanogaster","volume":"16","author":"Butterworth F. M.","year":"1984","journal-title":"J. Insect Physiol."},{"key":"e_1_2_1_8_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902620406"},{"key":"e_1_2_1_9_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901770105"},{"key":"e_1_2_1_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/0005-2795(76)90186-0"},{"key":"e_1_2_1_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/0304-3940(82)90403-7"},{"key":"e_1_2_1_12_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00305575"},{"key":"e_1_2_1_13_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01003851"},{"key":"e_1_2_1_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/0166-2236(85)90120-1"},{"key":"e_1_2_1_15_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902340307"},{"key":"e_1_2_1_16_1","doi-asserted-by":"publisher","DOI":"10.1159\/000112284"},{"key":"e_1_2_1_17_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901670203"},{"key":"e_1_2_1_18_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00304692"},{"key":"e_1_2_1_19_1","first-page":"000","article-title":"Changes in the nuclei of dying neurons as studied with thymidine autoradiography","volume":"283","author":"Clarke P. G. H.","year":"1989","journal-title":"J. Comp. Neurol."},{"key":"e_1_2_1_20_1","doi-asserted-by":"publisher","DOI":"10.1016\/0309-1651(85)90074-8"},{"key":"e_1_2_1_21_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901670202"},{"key":"e_1_2_1_22_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901330205"},{"key":"e_1_2_1_23_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.61.3.599"},{"key":"e_1_2_1_24_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901800313"},{"key":"e_1_2_1_25_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ph.28.030166.002251"},{"key":"e_1_2_1_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4827(69)90030-5"},{"key":"e_1_2_1_27_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01005032"},{"key":"e_1_2_1_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0074-7696(08)61288-7"},{"key":"e_1_2_1_29_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-185X.1951.tb00774.x"},{"key":"e_1_2_1_30_1","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1242\/jcs.36.1.361","article-title":"Transport of glial cell acid phosphatase by endoplasmic reticulum into damaged axons","volume":"36","author":"Griffiths G. W.","year":"1979","journal-title":"J. Cell Sci."},{"key":"e_1_2_1_31_1","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1050880104"},{"key":"e_1_2_1_32_1","first-page":"192","volume-title":"Lysosomes in Biology and Pathology","author":"Holtzman E.","year":"1969"},{"key":"e_1_2_1_33_1","volume-title":"A Survey. Cell Biology Monographs","author":"Holtzman E.","year":"1976"},{"key":"e_1_2_1_34_1","first-page":"775","article-title":"Endocytic embryonic brain cells shown to be dying neurons","volume":"41","author":"Hornung J. P.","year":"1985","journal-title":"Experientia"},{"key":"e_1_2_1_35_1","first-page":"S349","article-title":"Endocytic dying neurons in the chick embryo isthmo\u2010optic nucleus: Ultrastructure and birthdates","volume":"22","author":"Hornung J. P.","year":"1985","journal-title":"Neurosci. Lett. [Suppl.]"},{"key":"e_1_2_1_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(79)91013-8"},{"key":"e_1_2_1_37_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-1281(78)80033-6"},{"key":"e_1_2_1_38_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902640105"},{"key":"e_1_2_1_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/0306-4522(78)90006-4"},{"key":"e_1_2_1_40_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.36.3.453"},{"key":"e_1_2_1_41_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2990.1986.tb00146.x"},{"key":"e_1_2_1_42_1","first-page":"493","article-title":"Morphological studies on neuroglia V. Microglial cells in the cerebral cortex of the rat, with special reference to their possible involvement in synaptic function","volume":"223","author":"Murabe Y.","year":"1982","journal-title":"Cell Tissue Res."},{"key":"e_1_2_1_43_1","first-page":"381","article-title":"Localization of endogenous peroxidases in animal tissues","volume":"12","author":"Novikoff A. B.","year":"1971","journal-title":"J. Microsc."},{"key":"e_1_2_1_44_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.47.6.802"},{"key":"e_1_2_1_45_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.902120407"},{"key":"e_1_2_1_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/0166-2236(85)90175-4"},{"key":"e_1_2_1_47_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00685365"},{"key":"e_1_2_1_48_1","doi-asserted-by":"publisher","DOI":"10.1038\/297683a0"},{"key":"e_1_2_1_49_1","first-page":"341","article-title":"Vascular permeability to horseradish peroxidase in the developing chick brain","volume":"163","author":"Peterson R. G.","year":"1969","journal-title":"Anat. Rec."},{"key":"e_1_2_1_50_1","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1083\/jcb.68.2.339","article-title":"Ultrastructural differences during embryonic cell death in normal and peripherally deprived ciliary ganglia","volume":"68","author":"Pilar G.","year":"1976","journal-title":"J. Cell Biol."},{"key":"e_1_2_1_51_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.901520202"},{"key":"e_1_2_1_52_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.17.1.208"},{"key":"e_1_2_1_53_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01262414"},{"key":"e_1_2_1_54_1","first-page":"383","article-title":"Peroxidaseverteilungs\u2010muster und Microphonpotentiale in der impulsbeschallten Meerschweinchen\u2010Cochlea","volume":"144","author":"Schmidt H.\u2010P.","year":"1978","journal-title":"Anat. Anz."},{"key":"e_1_2_1_55_1","doi-asserted-by":"publisher","DOI":"10.1002\/tera.1420070306"},{"key":"e_1_2_1_56_1","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/S0070-2161(08)60535-3","article-title":"Receptors for lysosomal enzymes and glycoproteins","volume":"18","author":"Shepherd V.","year":"1983","journal-title":"Curr. Top. Membr. Transport"},{"key":"e_1_2_1_57_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.68.3.665"},{"key":"e_1_2_1_58_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.96.1.1"},{"key":"e_1_2_1_59_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.20.3.497"},{"key":"e_1_2_1_60_1","doi-asserted-by":"publisher","DOI":"10.1177\/15.7.375"},{"key":"e_1_2_1_61_1","first-page":"55P","article-title":"A quantitative study of horseradish peroxidase uptake by boutons presynaptic to axotomized hypoglossal neurones","volume":"251","author":"Summer B. E. H.","year":"1975","journal-title":"J. Physiol. (Lond.)"},{"key":"e_1_2_1_62_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00216515"},{"key":"e_1_2_1_63_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4827(85)90239-3"},{"key":"e_1_2_1_64_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00236719"},{"key":"e_1_2_1_65_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-94-011-6921-9_2"}],"container-title":["Journal of Comparative Neurology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fcne.902830310","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/cne.902830310","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,22]],"date-time":"2023-10-22T15:27:48Z","timestamp":1697988468000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/cne.902830310"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1989,5,15]]},"references-count":64,"journal-issue":{"issue":"3","published-print":{"date-parts":[[1989,5,15]]}},"alternative-id":["10.1002\/cne.902830310"],"URL":"https:\/\/doi.org\/10.1002\/cne.902830310","archive":["Portico"],"relation":{},"ISSN":["0021-9967","1096-9861"],"issn-type":[{"value":"0021-9967","type":"print"},{"value":"1096-9861","type":"electronic"}],"subject":[],"published":{"date-parts":[[1989,5,15]]}}}