Abstract
In mammals, passive immunity is transferred from mother to offspring by transplacental passage or by intestinal absorption. The rabbit receives antibodies exclusively across the placenta, whereas intestinal absorption is the principal source of antibodies for the new-born pig. In the rat, passive immunity is transferred by both pathways. The role of the jejunal absorptive cells was investigated in these three species, by the use of specific immune globulins as tracers of protein absorption. Rabbit anti-peroxidase and anti-ferritin antibodies were injected into the jejunum of newborn pigs, rats, and rabbits, and absorption was studied over the first 2 hr. The specific antibodies were detected in glutaraldehyde-fixed tissues after in vitro treatment with the antigens, and in sera by immunological methods. Intact antibodies are transferred into the circulation of the pig and the rat, but not into that of the rabbit. In the three species, the jejunal absorptive cells take up antibodies by endocytosis. In the pig, the antibodies are transported across the epithelium in vacuoles. In the rabbit, the endocytosis of antibodies triggers a lysosomal response and all absorbed antibodies are trapped in lysosomes. In the rat, both situations are found; there is no evidence of transfer of antibody fragments into the circulation.
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- Anderson P. J. Purification and quantitation of glutaraldehyde and its effect on several enzyme activities in skeletal muscle. J Histochem Cytochem. 1967 Aug;15(11):652–661. doi: 10.1177/15.11.652. [DOI] [PubMed] [Google Scholar]
- BANGHAM D. R., TERRY R. J. The absorption of 131I-labelled homologous and heterologous serum proteins fed orally to young rats. Biochem J. 1957 Aug;66(4):579–583. doi: 10.1042/bj0660579. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BANGHAM D. R., TERRY R. J. The survival of globulins absorbed from the gut in suckling rats. Biochem J. 1957 Aug;66(4):584–587. doi: 10.1042/bj0660584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BATTY I., BRAMBELL F. W., HEMMINGS W. A., OAKLEY C. L. Selection of antitoxins by the foetal membranes of rabbits. Proc R Soc Lond B Biol Sci. 1954 Sep 27;142(909):452–471. doi: 10.1098/rspb.1954.0036. [DOI] [PubMed] [Google Scholar]
- BRAMBELL F. W., HALLIDAY R. The route by which passive immunity is transmitted from mother to foetus in the rat. Proc R Soc Lond B Biol Sci. 1956 May 29;145(919):170–178. doi: 10.1098/rspb.1956.0024. [DOI] [PubMed] [Google Scholar]
- CLARK S. L., Jr The ingestion of proteins and colloidal materials by columnar absorptive cells of the small intestine in suckling rats and mice. J Biophys Biochem Cytol. 1959 Jan 25;5(1):41–50. doi: 10.1083/jcb.5.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- COHEN S. G. The placental transmission of antibodies and serum gamma globulins. J Infect Dis. 1950 Nov-Dec;87(3):291–298. doi: 10.1093/infdis/87.3.291. [DOI] [PubMed] [Google Scholar]
- COMLINE R. S., ROBERTS H. E., TITCHEN D. A. Route of absorption of colostrum globulin in the newborn animal. Nature. 1951 Apr 7;167(4249):561–562. doi: 10.1038/167561a0. [DOI] [PubMed] [Google Scholar]
- DE PETRIS S., KARLSBAD G., PERNIS B. Localization of antibodies in plasma cells by electron microscopy. J Exp Med. 1963 May 1;117:849–862. doi: 10.1084/jem.117.5.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Duve C., Wattiaux R. Functions of lysosomes. Annu Rev Physiol. 1966;28:435–492. doi: 10.1146/annurev.ph.28.030166.002251. [DOI] [PubMed] [Google Scholar]
- FOSTER J. F., FRIEDELL R. W., CATRON D., DIECKMANN M. R. Electrophoretic studies on swine. III. Composition of baby pig plasma and sow's whey during lactation. Arch Biochem Biophys. 1951 Mar;31(1):104–112. doi: 10.1016/0003-9861(51)90189-0. [DOI] [PubMed] [Google Scholar]
- Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
- HALLIDAY R. The absorption of antibodies from immune sera by the gut of the young rat. Proc R Soc Lond B Biol Sci. 1955 Mar 15;143(912):408–413. doi: 10.1098/rspb.1955.0020. [DOI] [PubMed] [Google Scholar]
- HALLIDAY R. The absorption of antibody from immune sera and from mixtures of sera by the gut of the young rat. Proc R Soc Lond B Biol Sci. 1958 Jan 1;148(930):92–103. doi: 10.1098/rspb.1958.0008. [DOI] [PubMed] [Google Scholar]
- Holtzman E., Novikoff A. B., Villaverde H. Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum. J Cell Biol. 1967 May;33(2):419–435. doi: 10.1083/jcb.33.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isliker H., Jacot-Guillarmod H., Jaton J. C. The structure and biological activity of immunoglobulins and their subunits. Ergeb Physiol. 1965;56:67–113. [PubMed] [Google Scholar]
- Kekwick R. A. The serum proteins in multiple myelomatosis. Biochem J. 1940 Sep;34(8-9):1248–1257. doi: 10.1042/bj0341248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kraehenbuhl J. P., Gloor E., Blanc B. Morphologie comparée de la muqueuse intestinale de deux espèces animales aux possibilités d'absorption protéique néonatale différentes. Z Zellforsch Mikrosk Anat. 1966;70(2):209–219. [PubMed] [Google Scholar]
- Leduc E. H., Avrameas S., Bouteille M. Ultrastructural localization of antibody in differentiating plasma cells. J Exp Med. 1968 Jan 1;127(1):109–118. doi: 10.1084/jem.127.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MILLER F., PALADE G. E. LYTIC ACTIVITIES IN RENAL PROTEIN ABSORPTION DROPLETS. AN ELECTRON MICROSCOPICAL CYTOCHEMICAL STUDY. J Cell Biol. 1964 Dec;23:519–552. doi: 10.1083/jcb.23.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MORRIS I. G. The effects of heterologous sera on the uptake of rabbit antibody from the gut of young mice. Proc R Soc Lond B Biol Sci. 1958 Jan 1;148(930):84–91. doi: 10.1098/rspb.1958.0007. [DOI] [PubMed] [Google Scholar]
- MYERS W. L., SEGRE D. THE IMMUNOLOGIC BEHAVIOR OF BABY PIGS. III. TRANSPLACENTAL TRANSFER OF ANTIBODY GLOBULIN IN SWINE. J Immunol. 1963 Nov;91:697–700. [PubMed] [Google Scholar]
- Maack T. Changes in the activity of acid hydrolases during renal reabsorption of lysozyme. J Cell Biol. 1967 Oct;35(1):268–273. doi: 10.1083/jcb.35.1.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maunsbach A. B. Absorption of I-125-labeled homologous albumin by rat kidney proximal tubule cells. A study of microperfused single proximal tubules by electron microscopic autoradiography and histochemistry. J Ultrastruct Res. 1966 Jun;15(3):197–241. doi: 10.1016/s0022-5320(66)80108-9. [DOI] [PubMed] [Google Scholar]
- Maunsbach A. B. Albumin absorption by renal proximal tubule cells. Nature. 1966 Oct 29;212(5061):546–547. doi: 10.1038/212546a0. [DOI] [PubMed] [Google Scholar]
- NORDBRING F., OLSSON B. Electrophoretic and immunological studies on sera of young pigs. II. The effect of feeding bovine trypsin inhibitor with porcine colostrum on the absorption of antibodies and immune globulins. Acta Soc Med Ups. 1958;63(1-2):25–40. [PubMed] [Google Scholar]
- NORDBRING F., OLSSON B. Electrophoretic and immunological studies on sera of young pigs. III. Transfer of protein fractions and antibodies to the newborn pig by ingestion of porcine serum with a study of the effect of bovine trypsin inhibitor. Acta Soc Med Ups. 1958;63(1-2):41–52. [PubMed] [Google Scholar]
- NOVIKOFF A. B., ESSNER E., QUINTANA N. GOLGI APPARATUS AND LYSOSOMES. Fed Proc. 1964 Sep-Oct;23:1010–1022. [PubMed] [Google Scholar]
- Nakane P. K., Pierce G. B., Jr Enzyme-labeled antibodies for the light and electron microscopic localization of tissue antigens. J Cell Biol. 1967 May;33(2):307–318. doi: 10.1083/jcb.33.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novikoff A. B., Albala A., Biempica L. Ultrastructural and cytochemical observations on B-16 and Harding-Passey mouse melanomas. The origin of premelanosomes and compound melanosomes. J Histochem Cytochem. 1968 May;16(5):299–319. doi: 10.1177/16.5.299. [DOI] [PubMed] [Google Scholar]
- OUCHTERLONY O. Diffusion-in-gel methods for immunological analysis. Prog Allergy. 1958;5:1–78. [PubMed] [Google Scholar]
- PAYNE L. C., MARSH C. L. Gamma globulin absorption in the baby pig: the nonselective absorption of heterologous globulins and factors influencing absorption time. J Nutr. 1962 Feb;76:151–158. doi: 10.1093/jn/76.2.151. [DOI] [PubMed] [Google Scholar]
- PORTER R. R. The hydrolysis of rabbit y-globulin and antibodies with crystalline papain. Biochem J. 1959 Sep;73:119–126. doi: 10.1042/bj0730119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SCHEIDEGGER J. J. Une micro-méthode de l'immuno-electrophorèse. Int Arch Allergy Appl Immunol. 1955;7(2):103–110. [PubMed] [Google Scholar]
- STAVITSKY A. B., ARQUILLA E. R. Micromethods for the study of proteins and antibodies. III. Procedures and applications of hemagglutination and hemagglutination-inhibition reactions with bis-diazotized benzidine and protein-conjugated red blood cells. J Immunol. 1955 Apr;74(4):306–312. [PubMed] [Google Scholar]
- STRAUS W. CYTOCHEMICAL OBSERVATIONS ON THE RELATIONSHIP BETWEEN LYSOSOMES AND PHAGOSOMES IN KIDNEY AND LIVER BY COMBINED STAINING FOR ACID PHOSPHATASE AND INTRAVENOUSLY INJECTED HORSERADISH PEROXIDASE. J Cell Biol. 1964 Mar;20:497–507. doi: 10.1083/jcb.20.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- STRAUS W. Changes in droplet fractions from rat kidney cells after intraperitoneal injection of egg white. J Biophys Biochem Cytol. 1957 Nov 25;3(6):933–947. doi: 10.1083/jcb.3.6.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
- STRAUS W. Concentration of acid phosphatase, ribonuclease, desoxyribonuclease, beta-glucuronidase, and cathepsin in droplets isolated from the kidney cells of normal rats. J Biophys Biochem Cytol. 1956 Sep 25;2(5):513–521. doi: 10.1083/jcb.2.5.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
- STRAUS W. FACTORS AFFECTING THE STATE OF INJECTED HORSERADISH PEROXIDASE IN ANIMAL TISSUES AND PROCEDURES FOR THE STUDY OF PHAGOSOMES AND PHAGO-LYSOSOMES. J Histochem Cytochem. 1964 Jun;12:470–480. doi: 10.1177/12.6.470. [DOI] [PubMed] [Google Scholar]
- STRAUS W. OCCURRENCE OF PHAGOSOMES AND PHAGO-LYSOSOMES IN DIFFERENT SEGMENTS OF THE NEPHRON IN RELATION TO THE REABSORPTION, TRANSPORT, DIGESTION, AND EXTRUSION OF INTRAVENOUSLY INJECTED HORSERADISH PEROXIDASE. J Cell Biol. 1964 Jun;21:295–308. doi: 10.1083/jcb.21.3.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schneeberger-Keeley E. E., Karnovsky M. J. The ultrastructural basis of alveolar-capillary membrane permeability to peroxidase used as a tracer. J Cell Biol. 1968 Jun;37(3):781–793. doi: 10.1083/jcb.37.3.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scott G., Avrameas S., Bernhard W. Etude au microscope électronique de la formation d'anticorps à l'aide de la phosphatase alcaline utilisée comme antigène. C R Acad Sci Hebd Seances Acad Sci D. 1968 Feb 12;266(7):746–748. [PubMed] [Google Scholar]
- Sibalin M., Björkman N. On the fine structure and absorptive function of the porcine jejunal villi during the early suckling period. Exp Cell Res. 1966 Oct;44(1):165–174. doi: 10.1016/0014-4827(66)90423-x. [DOI] [PubMed] [Google Scholar]
- Sternberger L. A. Electron microscopic immunocytochemistry: a review. J Histochem Cytochem. 1967 Mar;15(3):139–159. doi: 10.1177/15.3.139. [DOI] [PubMed] [Google Scholar]
- Straus W. Cytochemical detection of sites of antibody to horseradish peroxidase in spleen and lymph nodes. J Histochem Cytochem. 1968 Apr;16(4):237–248. doi: 10.1177/16.4.237. [DOI] [PubMed] [Google Scholar]
- Straus W. Methods for the study of small phagosomes and their relationship to lysosomes with horseradish peroxidase as a "marker protein". J Histochem Cytochem. 1967 Jul;15(7):375–380. doi: 10.1177/15.7.375. [DOI] [PubMed] [Google Scholar]
- VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WEBB T., LAPRESLE C. Study of the adsorption on and desorption from polystyrene-human serum albumin conjugates of rabbit anti-human serum albumin antibodies having different specificities. J Exp Med. 1961 Jul 1;114:43–50. doi: 10.1084/jem.114.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WHIPPLE G. H., HILL R. B., Jr, TERRY R., LUCAS F. V., YUILE C. L. The placenta and protein metabolism; transfer studies using carbon 14-labeled proteins in dogs. J Exp Med. 1955 Jun 1;101(6):617–626. doi: 10.1084/jem.101.6.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de MURALT, GUGLER E., ROULET D. L. [The passage of immune globulins from the mother to the infant]. Bull Schweiz Akad Med Wiss. 1961 Oct;17:245–265. [PubMed] [Google Scholar]