Abstract
The intestine of the suckling rat has the uniquecapacity of absorbing immunoglobulins from maternalmilk. We investigated intestinal Fc receptor mRNAexpression and the absorption of orally administered antibodies to delineate the ontogeny and tissuespecificity of this transport system. Duodenalexpression of Fc receptor mRNA was at maximum levelsbetween 1 and 19 days of age, but was not detectableduring fetal life and in animals after weaning. Alongthe horizontal axis of the intestine, FcRn mRNAexpression was maximum in the proximal duodenum anddeclined gradually in distal bowel. Similarly,absorption of orally administered antibody was low shortlyafter birth, but reached maximum levels at 14 days ofage. By the time of weaning, antibody uptake had almostcompletely ceased. These data further delineate the temporal and spatial nature of theintestinal immunoglobulin transport system, andrepresent additional examples of how the intestinal Fcreceptor is transcriptionally regulated.
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REFERENCES
Henning SJ, Rubin DC, Shulman RJ: Ontogeny of the Intestinal Mucosa. In Physiology of the Gastrointestinal Tract. LR Johnson (ed). New York, Raven Press, 1994, pp 571-610
Appleby P, Catty D: Transmission of immunoglobulin to foetal and neonatal mice. J Reprod Immunol 5:203-213, 1983
Brambell FWR, Halliday R: The route by which passive immunity is transmitted from mother to foetus in the rat. Proc R Soc London (Biol) Ser B 145:1-11, 1956
Spooner RL, Metzger JJ, Halliday R, Larvor P: Synopsis of seminar on the role of the colostrum in relation to immunity and survival in the newborn ruminant and pig. Ann Rech Vet 9:177-179, 1978
Halliday R: Variation in immunoglobulin transfer from ewes to lambs. Ann Rech Vet 9:367-374, 1978
Halliday R, Russel AJ, Williams MR, Peart JN: Effects of energy intake during late pregnancy and of genotype on immunoglobulin transfer to calves in suckling herds. Res Vet Sci 24:26-31, 1978
Roberts DM, Guenthert M, Rodewald R: Isolation and characterization of the Fc receptor from the fetal yolk sac of the rat. J Cell Biol 111:1867-1876, 1990
Hasegawa H, Nakamura A, Watanabe K, Brown WR, Nagura H: Intestinal uptake of IgG in suckling rats. Distinction between jejunal and ileal epithelial cells demonstrated by simultaneous ultrastructural localization of IgG and acid phosphatase. Gastroenterology 92:186-191, 1987
Halliday R: Prenatal and postnatal transmission of passive immunity to young rats. Proc R Soc London (Biol) Ser B 144:427-430, 1955
Jones EA, Waldmann TA: The mechanism of intestinal uptake and transcellular transport of IgG in the neonatal rat. J Clin Invest 51:2916-2927, 1972
Martín MG, Wu SV, Ohning G, Wong H, Walsh JH: Parenterally or enterally administered anti-somatostatin antibody induces increased gastrin in suckling rats. Am J Physiol 266 (Gastrointest Liver Physiol):G417-G424, 1994
Berryman M, Rodewald R: β2-Microglobulin co-distributes with the heavy chain of the intestinal IgG-Fc receptor throughout the transepithelial transport pathway of the neonatal rat. J Cell Sci 108:2347-2360, 1995
Simister NE, Mostov KE: An Fc receptor structurally related to MHC class I antigens. Nature 337:184-187, 1989
Ahouse JJ, Hagerman CL, Mittal P, Gilbert DJ, Copeland NG, Jenkins NA, Simister NE: Mouse MHC class I-like Fc receptor encoded outside the MHC. J Immunol 151:6076-6088, 1993
Martín MG, Wu SV, Walsh JH: Hormonal control of intestinal Fc receptor gene expression and immunoglobulin transport in suckling rats. J Clin Invest 91:2844-2849, 1993
Rickard E, Sittampalam G, Clodfelter D: Protein assay for monoclonal antibodies. Bio Techniques 6:982-992, 1988
Chomczynski P, Sacci N: Single-step method of RNA isolation by acid guanidium thiocyanate-phenol extraction. Anal Biochem 162:156-159, 1987
Halliday R: The absorption of antibody from immune sera and from mixtures of sera by the gut of the young rat. Proc R Soc Med Sect B 148:92, 1966
Morphis LG, Gitlin D: Maturation of maternofoetal transport system for human IgG in the mouse. Nature 228:573, 1970
Adeniyi-Jones SCA, Ozato K: Transfer of antibodies directed to paternal major histocompatibility class I antigens from pregnant mice to the developing fetus. J Immunol 138:1408-1415, 1987
Bell SC, Billington WD: Humoral immune response in murine pregnancy. III. Relationship between anti-paternal alloantibody levels in maternal serum, placenta and fetus. J Reprod Immunol 5:299-310, 1983
Kandil E, Noguchi M, Ishibashi T, Kasahara M: Structural and phylogenetic analysis of the MHC class I-like Fc receptor gene. J Immunol 154:5907-5918, 1995
Nakamura K, Komuro T: A three-dimensional study of the embryonic development and postnatal maturation of duodenal villi. J Electron Microsc 32:4:338-347, 1983
Israel EJ, Simister N, Freiberg E, Caplan A, Walker WA: Immunoglobulin G binding sites on the human foetal intestine: A possible mechanism for the passive transfer of immunity from mother to infant. Immunology 79:77-81, 1993
Bangham DR: The transmission of homologous serum proteins to the fetus and to the amniotic fluid in the rhesus monkey. J Physiol (London) 153:265, 1960
Rodewald R: Intestinal transport of antibodies in the newborn rat. J Cell Biol 58:189-211, 1973
Clark SL: The ingestion of proteins and colloid materials by columnar absorptive cells of the small intestine in suckling rats and mice. J Biophys Biochem Cytol 5:411-448, 1959
Brambell FWR: The transmission of immunity from mother to young and the catabolism of immunoglobulins. Lancet 2:1087-1093, 1966
Graney DO: The uptake of ferritin by ileal absorptive cells in suckling rats. An electron microscope study. Am J Anat 123:227-254, 1968
Rodewald R: Selective antibody transport in the proximal small intestine of the neonatal rat. J Cell Biol 45:635-640, 1970
Mackenzie DDS: Selective uptake of immunoglobulins by the proximal intestine of suckling rats. Am J Physiol 223(6):1286-1295, 1972
Morris B, Morris R: The digestion and transmission of IgG by rat enterocytes. In Protein Transmission through Living Membranes. WA Hemmings (ed), Amsterdam, Elsevier/North-Holland Biomedical Press, 1979, pp 159-169
Morris B, Morris R: The digestion and transmission of labelled immunoglobulin G by enterocytes of the proximal distal regions of the small intestine of young rats. J Physiol (London) 273:427-442, 1977
Hasegawa H, Nakamura A, Watanabe K, Brown WR, Nagura H: Intestinal uptake of IgG in suckling rats. Distinction between jejunal and ileal epithelial cells demonstrated by simultaneous ultrastructural localization of IgG and acid phosphatase. Gastroenterology 92:186-191, 1987
Hobbs SM, Jackson LE, Peppard JV: Binding of subclasses of rat immunoglobulin G to detergent-isolated Fc receptor from neonatal rat intestine. J Biol Chem 262:8041-8046, 1987
Borthistle BK, Kubo RT, Brown WR, Grey HM: Studies on receptors for IgG on epithelial cells of the rat intestine. J Immunol 119:471-476, 1977
Israel EJ, Patel VK, Taylor SF, Marshak-Rothstein A, Simister NE: Requirement for a β2-microglobulin-associated Fc receptor for acquisition of maternal IgG by fetal and neonatal mice. J Immunol 154:6246-6251, 1995
Junghans RP, Anderson CL: The protection receptor for IgG catabolism is the β2-microglobulin-containing neonatal intestinal transport receptor. Proc Nat Acad Sci USA 93:5512-5516, 1996
Harada E, Hashimoto Y, Syuto B: Epidermal growth factor accelerates the intestinal cessation of macromolecular transmission in the suckling rat. Comp Biochem Physiol A: Comp Physiol 97A:201-204, 1990
Halliday R: The effect of steroid hormones on the absorption of antibody by the young rat. J Endocrinol 18:56-66, 1959
Daniels VG, Hardy RN, Malinowska KW: The effect of adrenalectomy or pharmacological inhibition of adrenocortical function on macromolecule uptake by the newborn rat intestine. J Physiol (London) 229:697-707, 1973
Harada E, Hashimoto Y, Syuto B: Precocious cessation of intestinal macromolecular transport and digestive enzymes development by prostaglandin E2 in suckling rats. Comp Biochem Physiol A 109:245-253, 1994
Solberg DH, Diamond JM: Comparison of different dietary sugars as inducers of intestinal sugar transporters. Am J Physiol 252:G574-G584, 1987
Yeh KY, Yeh M, Holt PR: Thyroxine and cortisone cooperate to modulate postnatal intestinal enzyme differentiation in the rat. Am J Physiol 260(23):G371-G378, 1991
Diamond JM, Karasov WH: Adaptive regulation of intestinal nutrient transporters. Proc Natl Acad Sci USA 84:2242-2245, 1987
Diamond JM: Hard-wired local triggering of intestinal enzyme expression. Nature 324:408, 1986
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Martin, M.G., Wu, S.V. & Walsh, J.H. Ontogenetic Development and Distribution of Antibody Transport and Fc Receptor mRNA Expression in Rat Intestine. Dig Dis Sci 42, 1062–1069 (1997). https://doi.org/10.1023/A:1018853506830
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DOI: https://doi.org/10.1023/A:1018853506830