{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T06:21:19Z","timestamp":1767162079060,"version":"3.48.0"},"reference-count":80,"publisher":"The Royal Society","issue":"912","license":[{"start":{"date-parts":[[1975,7,17]],"date-time":"1975-07-17T00:00:00Z","timestamp":174787200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[1975,7,17]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The transport of immunoglobulins from mother to foetus and newly born mammal involves selective events which are independent of molecular size, related to immunoglobulin class, structure, and species of origin, and involve considerable protein degradation. Such events are briefly described as background information to a discussion of how selection of proteins might take place during transport across the cellular barriers concerned, namely the yolk sac splanchnopleur, chorio-allantoic placenta, and small intestine. Until recently the Brambell hypothesis has been the most favoured explanation. This implies that selection occurs intracellularly, within endodermal cells of the yolk sac splanchnopleur and small intestine, and within the syncytiotrophoblast of the chorio-allantoic placenta, of certain species. It also suggests that specific receptors are present which give attached proteins protection from degradation when the vesicles containing them fuse with lysosomes; such protected proteins are then liberated from the vesicle by exocytosis. This hypothesis is examined in the light of what is now known about the mechanism of uptake and transport of proteins by the endodermal cells and syncytiotrophoblast. It is suggested that rather than being an intracellular event, involving protection from proteolytic degradation, selection takes place at the cell surface. Evidence is presented, some direct and some circumstantial, that proteins may be selectively endocytosed by coated micropinocytotic vesicles, and non-selectively endocytosed through a complex apical canalicular system leading to macropinocytotic vesicle formation. In the small intestine of the suckling rat these two processes appear to be segregated, selective uptake occurring in the proximal half and non-selective uptake occurring in the distal half. In the endodermal cells of the rabbit yolk sac splanchnopleur, and by implication in the syncytiotrophoblast of man and monkey, it is suggested that both selective, and non-selective, uptake of protein occurs. Non-selective uptake into macropinocytotic vesicles is regarded as an event leading to complete degradation of all contained protein and functioning so as to supply the foetus and newly born mammal with essential amino acids. Selective uptake into coated micropinocytotic vesicles is regarded as an event leading to the transport of immunoglobulins across the cell without any contact with lysosomes, and functioning so as to supply the newly born mammal with protection against invasive organisms. Specific receptors are still required but only for the initial uptake and segregation of proteins into coated micropinocytotic vesicles. The role which the glycocalyx might have in such selective binding of proteins is considered and possible difficulties in characterization of specific receptors brought to light in view of the likely overwhelming need for non-specific binding to effect non-selective uptake.<\/jats:p>","DOI":"10.1098\/rstb.1975.0060","type":"journal-article","created":{"date-parts":[[2006,12,18]],"date-time":"2006-12-18T17:23:53Z","timestamp":1166462633000},"page":"395-410","source":"Crossref","is-referenced-by-count":31,"title":["Role of the cell surface in selection during transport of proteins from mother to foetus and newly born"],"prefix":"10.1098","volume":"271","author":[{"given":"A. E.","family":"Wild","sequence":"first","affiliation":[{"name":"Department of Biology, University of Southampton, Southampton SO9 3TU"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"175","reference":[{"key":"p_1","doi-asserted-by":"publisher","DOI":"10.1042\/bj0660579"},{"key":"p_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.2.4.99"},{"key":"p_3","doi-asserted-by":"publisher","DOI":"10.1007\/BF01248567"},{"key":"p_4","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(66)92190-8"},{"key":"p_5","unstructured":"Brambell F. W. R. 1970 The transmission of passive immunity from mother to young. Frontiers Biol. 18. Amsterdam: North-Holland."},{"key":"p_6","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1961.0013"},{"key":"p_7","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1958.0046"},{"key":"p_8","doi-asserted-by":"publisher","DOI":"10.1038\/2031352a0"},{"key":"p_9","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1959.0024"},{"key":"p_10","doi-asserted-by":"crossref","unstructured":"Brambell F. W. R. Hemmings W. A. Oakley C. L. & Porter R. R. i960 The relative transmission of the fractions of papain hydrolysed homologous y-globulin from the uterine cavity to the foetal circulation in the rabbit. Proc. R. Soc. Lond. B 151 478-482.","DOI":"10.1098\/rspb.1960.0011"},{"key":"p_11","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001250405"},{"key":"p_12","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1969.sp008902"},{"key":"p_13","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.35.2.357"},{"key":"p_14","unstructured":"Gitlin D. 1971 Development and metabolism of the immune globulins. In Immunological incompetence (ed. B. M. Kagan & E. R. Steihm) pp. 3-13. Chicago: Year Book Medical Publ."},{"key":"p_15","first-page":"289","article-title":"A new mouse immunoglobulin IgG3. J. exp","volume":"133","author":"Grey H. M .","year":"1971","journal-title":"Med."},{"key":"p_16","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.1971.0002"},{"key":"p_17","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1956.0026"},{"key":"p_18","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1958.0006"},{"key":"p_19","first-page":"96","article-title":"Protein transfer across foetal membranes. Br. med","volume":"17","author":"Hemmings W. A.","year":"1961","journal-title":"Bull."},{"key":"p_20","first-page":"165","article-title":"Transport of IgM antibody to the rabbit foetus","volume":"25","author":"Hemmings W. A.","year":"1973","journal-title":"Immunology"},{"key":"p_21","first-page":"645","article-title":"Transmission of IgA to the rabbit foetus and the suckling rat","volume":"25","author":"Hemmings W. A.","year":"1973","journal-title":"Immunology"},{"key":"p_22","unstructured":"Hemmings W. A. & Williams E. W. 1973 The attachment of IgG to components of the rabbit foetal yolk-sac endoderm cell. I.R.C.S. medical Sci. (73-10) 1-5-10."},{"key":"p_23","unstructured":"Jacques P. J. 1969 Endocytosis. In Lysosomes in biology andpathology 2 (ed. J. T. Dingle & H. B. Fell) pp. 395-420. Amsterdam: North-Holland."},{"key":"p_24","first-page":"541","article-title":"Ruthenium labelling of micropinocytotic activity in the rat visceral yolk sac placenta. J. ultrastruct","volume":"35","author":"Jollie W. P.","year":"1971","journal-title":"Res."},{"key":"p_25","first-page":"530","article-title":"Intestinal absorption and degradation of rat and bovine y-globulins in the suckling rat. Biochim. biophys","volume":"255","author":"Jones R. E.","year":"1972","journal-title":"Acta"},{"key":"p_26","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.42.1.202"},{"key":"p_27","first-page":"354","article-title":"Maternal-foetal transfer of human immune globulins and fragments in rabbits","volume":"8","author":"Kaplan K. C.","year":"1965","journal-title":"Immunology"},{"key":"p_28","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001290303"},{"key":"p_29","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001300404"},{"key":"p_30","doi-asserted-by":"crossref","unstructured":"Lagunoff D. & Curran D. E. 1972 Role of bristle-coated membrane in the uptake of ferritin by rat macrophages. Expl bell Res. 75 337-346.","DOI":"10.1016\/0014-4827(72)90438-7"},{"key":"p_31","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001180104"},{"key":"p_32","doi-asserted-by":"publisher","DOI":"10.1002\/ar.1091750104"},{"key":"p_33","first-page":"1","article-title":"Absorption of ferritin by rat kidney proximal tubule cells: Electron microscopic observations of the initial uptake phase in cells of microperfused single proximal tubules. J. ultrastruct","volume":"16","author":"Maunsbach A. B.","year":"1966","journal-title":"Res."},{"key":"p_34","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1963.0002"},{"key":"p_35","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1964.0040"},{"key":"p_36","unstructured":"Morris L G . 1968 Gamma globulin absorption in the new born. In Handbook of physiology - alimentary canal (ed. G. F. Code) sect. 6 vol. 3 pp. 1491-1512. Baltimore: American Physiol. Soc."},{"key":"p_37","first-page":"909","article-title":"Absorption of gamma globulin by small intestine","volume":"21","author":"Payne L. C.","year":"1962","journal-title":"Fedn Proc."},{"key":"p_38","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.45.3.635"},{"key":"p_39","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.58.1.189"},{"key":"p_40","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.20.2.313"},{"key":"p_41","first-page":"531","article-title":"An attempt to visualize protein transmission across the rabbit visceral yolk-sac","volume":"107","author":"Slade B. S.","year":"1970","journal-title":"J. Anat."},{"key":"p_42","first-page":"217","article-title":"Transmission of human y-globulin to rabbit foetus and its inhibition by conjugation with ferritin","volume":"2","author":"Slade B. S.","year":"1971","journal-title":"Immunology"},{"key":"p_43","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.4049\/jimmunol.108.5.1345","article-title":"Specificity of the in vitro-binding of IgG and rabbit serum albumin (RSA) to rabbit yolk sac membrane","volume":"108","author":"Sonoda S.","year":"1972","journal-title":"J. Immunol."},{"key":"p_44","unstructured":"Weston P. D. & Poole A. R. 1973 Antibodies to enzymes and their uses with specific reference to cathepsin D and other Iysosomal enzymes. In Lysosomes in biology and pathology (ed. J. T. Dingle) vol. 3 pp. 425-464. Amsterdam: North-Holland."},{"key":"p_45","first-page":"313","article-title":"Protein transmission across the rabbit foetal membranes. J. Embryol. exp","volume":"24","author":"Wild A. E.","year":"1970","journal-title":"Morph."},{"key":"p_46","unstructured":"Wild A. E. 1973 Transport of immunoglobulins and other proteins from mother to young. In Lysosomes in biology and pathology (ed. J. T. Dingle) vol. 3 pp. 169-215. Amsterdam: North-Holland."},{"key":"p_47","first-page":"521","article-title":"Protein transport across the placenta. In Transport at the cellular level (ed. M. A. Sleigh & Jennings)","author":"Wild A. E.","year":"1974","journal-title":"Soc. Exp. Biol. Symp. XXVIII0022"},{"key":"p_48","doi-asserted-by":"publisher","DOI":"10.1007\/BF02583471"},{"key":"p_49","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.39.3.564"},{"key":"p_50","unstructured":"J. B. L loyd {Biochemistry Research Unit Keele University Staffordshire). My colleagues and I at"},{"key":"p_51","unstructured":"Keele have recently made a quantitative study of pinocytosis in the rat yolk-sac maintained in"},{"key":"p_52","unstructured":"organ culture (Moore A. T. Williams K. E. & Lloyd J. B. Biochem. Soc. Trans. 1974 in the"},{"key":"p_53","unstructured":"Press). The anatomical relationships in the rat placenta are similar to those described by Dr"},{"key":"p_54","unstructured":"Wild for the rabbit and the 17 day rat yolk sac can easily be dissected free from other tissues;"},{"key":"p_55","unstructured":"it survives for many hours when cultured in a simple tissue culture medium (TC-199) con"},{"key":"p_56","unstructured":"taining 10 % calf serum. By adding radiolabelled macromolecular substrates to the culture"},{"key":"p_57","unstructured":"medium it has been possible to measure the rates of their pinocytic uptake. 1261-labelled poly"},{"key":"p_58","unstructured":"vinylpyrrolidone (PVP) and colloidal [198Au]gold are captured at approximately the same rate"},{"key":"p_59","unstructured":"whereas 1251-labelled bovine serum albumin or human fibrinogen are taken up at much higher"},{"key":"p_60","unstructured":"rates (up to 50 times the rate for 1251-labelled PVP). The rate of uptake of these proteins varies"},{"key":"p_61","unstructured":"considerably with changes in their conformational state presumably because such changes"},{"key":"p_62","unstructured":"expose or mask determinants on the molecule necessary for its uptake. These experiments are relevant at a number of points to the Brambell hypothesis and to the"},{"key":"p_63","unstructured":"alternative proposal by Wild. First the proteins we have used were fully degraded to amino"},{"key":"p_64","unstructured":"acids by the yolk-sac tissue after uptake. The kinetics revealed that endocytosis was the rate"},{"key":"p_65","unstructured":"determining step in the overall process of uptake digestion and release of digestion products."},{"key":"p_66","unstructured":"The catabolic machinery of this tissue is very great and its capacity much greater than demand."},{"key":"p_67","unstructured":"Secondly uptake that is followed by digestion although non-selective in Wild's sense (not"},{"key":"p_68","unstructured":"specific for y-globulins) is highly selective capturing some macromolecules much more effi"},{"key":"p_69","unstructured":"ciently than others. Thirdly it has been shown that this selectivity is not achieved by changes"},{"key":"p_70","unstructured":"in the rate of internalization of plasma membrane; hence it must reflect uptake of different"},{"key":"p_71","unstructured":"substrates within distinct types of vesicle or much more likely by differential adsorption of"},{"key":"p_72","unstructured":"substrates on plasma membrane `receptors'. Dr Wild you are suggesting that two distinct types of pinocytic vesicle are being formed from"},{"key":"p_73","unstructured":"the apical plasma membrane of yolk sac cells. Do you postulate a micro-heterogeneity of the"},{"key":"p_74","unstructured":"plasma membrane so that some regions can give rise to one type of vesicle and some to the"},{"key":"p_75","unstructured":"other? This seems a necessary corollary of your proposal but it sounds a difficult feat for a cell"},{"key":"p_76","unstructured":"to achieve particularly a cell in which internalization of membrane by pinocytosis is constantly"},{"key":"p_77","unstructured":"taking place."},{"key":"p_98","unstructured":"Hemmings W. A. & Williams E. W. 1974 Uptake of labelled ferritin and rat IgG from segments of the gut of the suckling rat. I.R.G.S. (Aliment; Biophys; Immunol) 2.1450."},{"key":"p_99","first-page":"381","article-title":"Direct deposition at high resolution of specific metals from solutions at radioactive sites in tissue sections","volume":"92","author":"Normandin D. K.","year":"1973","journal-title":"Soc."},{"key":"p_100","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.58.1.189"}],"container-title":["Philosophical Transactions of the Royal Society of London. B, Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rstb.1975.0060","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/rstb\/article-pdf\/271\/912\/395\/334991\/rstb.1975.0060.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/royalsocietypublishing.org\/rstb\/article-pdf\/271\/912\/395\/334991\/rstb.1975.0060.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T06:17:13Z","timestamp":1767161833000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/rstb\/article\/271\/912\/395\/54050\/Role-of-the-cell-surface-in-selection-during"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1975,7,17]]},"references-count":80,"journal-issue":{"issue":"912","published-print":{"date-parts":[[1975,7,17]]}},"URL":"https:\/\/doi.org\/10.1098\/rstb.1975.0060","relation":{},"ISSN":["0080-4622","2054-0280"],"issn-type":[{"type":"print","value":"0080-4622"},{"type":"electronic","value":"2054-0280"}],"subject":[],"published":{"date-parts":[[1975,7,17]]}}}