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Medical Molecular Morphology

, Volume 40, Issue 1, pp 1–7 | Cite as

Molecular morphology of the digestive tract; macromolecules and food allergens are transferred intact across the intestinal absorptive cells during the neonatal-suckling period

  • Mamoru Fujita
  • Ryoko Baba
  • Mariko Shimamoto
  • Yoshiko Sakuma
  • Sunao Fujimoto
SPECIAL REVIEW SERIES: Molecular morphological approach for pathogenesis of hepatogastrointestinal diseases

Abstract

Food allergies represent an important medical problem throughout the developed world. The epithelium of the digestive tract is an important area of contact between the organism and its external environment. Accordingly, we must reconsider the transport of intestinal transepithelial macromolecules, including food allergens, in vivo. The intestinal epithelium of the neonatal-suckling rat is a useful model system for studies into endocytosis and transcytosis. Macromolecules and food allergens can be transferred intact with maternal immunoglobulins across the absorptive cells of duodenum and jejunum during the neonatal-suckling period. This review summarizes these observations as well as our recent molecular morphological studies.

Key words

Neonatal-suckling Small intestine Duodenum Jejunum Ileum Absorptive cells Endocytosis Transcytosis Macromolecule Food allergen 

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References

  1. 1.
    Cardell, RR,Jr, Badenhausen, S, Porter, KR 1967Intestinal triglyceride absorption in the rat. An electron microscopical studyJ Cell Biol34123155PubMedCrossRefGoogle Scholar
  2. 2.
    Walker, WA, Cornell, R, Davenport, LM, Isselbacher, KJ 1972Macromolecular absorption. Mechanism of horseradish peroxidase uptake and transport in adult and neonatal rat intestineJ Cell Biol54195205PubMedCrossRefGoogle Scholar
  3. 3.
    Koldovský, O, Dobiášovà, M, Hahn, P, Kolinská, J, Kraml, J, Pácha, J 1995Development of gastrointestinal functionsPhysiol Res44341348PubMedGoogle Scholar
  4. 4.
    Clark, SL 1959The ingestion of proteins and colloidal materials by columnar absorptive cells of the small intestine in suckling rats and miceJ Biophys Biochem Cytol54149PubMedGoogle Scholar
  5. 5.
    Bainter, K 1986Intestinal absorption of macromolecules and immune transmission from mother to youngCRC PressBoca RatonGoogle Scholar
  6. 6.
    Martin, MG, Wu, SV, Walsh, JH 1997Ontogenetic development and distribution of antibody transport and Fc receptor mRNA expression in rat intestineDig Dis Sci4210621069PubMedCrossRefGoogle Scholar
  7. 7.
    Jakoi, ER, Zampighi, G, Robertson, JD 1976Regular structures in unit membranes. II. Morphological and biochemical characterization of two water-soluble membrane proteins isolated from the suckling rat ileumJ Cell Biol7091111CrossRefGoogle Scholar
  8. 8.
    Robertson, JD, Knutton, S, Limbrick, AR, Jakoi, ER, Zampighi, G 1976Regular structures in unit membranes. III. Further observations on the particulate components of the suckling rat ileum endocytic membrane complexesJ Cell Biol70112122PubMedCrossRefGoogle Scholar
  9. 9.
    Fujita, M, Reinhart, F, Neutra, MR 1988Convergence of apical and basolateral endocytic pathways at the late endosome: double-tracer studies in ileal absorptive cells of suckling ratsJ Cell Biol107110aGoogle Scholar
  10. 10.
    Fujita, M, Reinhart, F, Neutra, MR 1990Convergence of apical and basolateral endocytic pathways at apical late endosomes in absorptive cells of suckling rat ileum in vivoJ Cell Sci97385394PubMedGoogle Scholar
  11. 11.
    Hirano, S, Kataoka, K 1986Histogenesis of the mouse jejunal mucosa, with special reference to proliferative cells and absorptive cellsArch Histol Jpn49333348PubMedGoogle Scholar
  12. 12.
    Ricardo, O, Castillo, MD, Arlyn, PRD, Arlyn, PMS, Francoise, CBS 1988Intestinal maturation in the rat: the role of enteral nutrientsJ Parenter Enteral Nutr12490495CrossRefGoogle Scholar
  13. 13.
    Miyamoto, K, Hase, K, Taketani, Y, Minami, H, Oka, T, Nakabou, Y, Hagihara, H 1992Developmental changes in intestinal glucose transporter mRNA levelsBiochem Biophys Res Commun183626631PubMedCrossRefGoogle Scholar
  14. 14.
    Matsumoto, K, Takao, Y, Akazawa, S, Yano, M, Uotani, S, Kawasaki, E, Takino, H, Yamasaki, H, Okuno, S, Yamaguchi, Y, Nagataki, S 1993Developmental change of facilitative glucose transporter expression in rat embryonal and fetal intestineBiochem Biophys Res19312751282CrossRefGoogle Scholar
  15. 15.
    David, ES, Cingari, DS, Ferraris, RP 1995Dietary induction of intestinal fructose absorption in weaning ratsPediatr Res37777782PubMedGoogle Scholar
  16. 16.
    Shu, R, David, ES, Ferraris, RP 1997Dietary fructose enhances intestinal fructose transport and GLUT5 expression in weaning ratsAm J Physiol Gastrointest Liver Physiol272G446G453Google Scholar
  17. 17.
    Shu, R, David, ES, Ferraris, RP 1998Luminal fructose modulates fructose transport and GLUT-5 expression in small intestine of weaning ratsAm J Physiol274G232G239PubMedGoogle Scholar
  18. 18.
    Jiang, L, David, ES, Espina, N, Ferraris, RP 2001GLUT-5 expression in neonatal rats: crypt-villus location and age-dependent regulationAm J Physiol Gastrointest Liver Physiol281G666G674PubMedGoogle Scholar
  19. 19.
    Baba, R, Yamami, M, Sakuma, Y, Fujita, M, Fujimoto, S 2005Relationship between glucose transporter and changes in the absorptive system in small intestinal absorptive cells during the weaning processMed Mol Morphol384753PubMedCrossRefGoogle Scholar
  20. 20.
    Kilshaw, P, Cant, A 1984The passage of maternal dietary proteins into human breast milkInt Arch Allergy Appl Immunol75815PubMedGoogle Scholar
  21. 21.
    Maeda, S 1993The concentration of bovine IgG in human breast milk measured using different methodsActa Paediatr8210121016PubMedGoogle Scholar
  22. 22.
    Jones, AC, Miles, EA, Warner, JO, Colwell, BM, Bryant, TN, Warner, JA 1996Fetal peripheral blood mononuclear cell proliferative responses to mitogenic and allergenic stimuli during gestationPediatr Allergy Immunol7109116PubMedGoogle Scholar
  23. 23.
    Lebovidge, JS, Stone, KD, Twarog, FJ, Raiselis, SW, Kalish, LA, Bailey, EP, Schneider, LC 2006Development of a preliminary questionnaire to assess parental response to children's food allergiesAnn Allergy Asthma Immunol96472477PubMedGoogle Scholar
  24. 24.
    Perr, HA 2006Novel foods to treat food allergy and gastrointestinal infectionCurr Allergy Asthma Rep6153159PubMedGoogle Scholar
  25. 25.
    Prates, S, Morais-Almeida, M, Matos, V, Loureiro, V, Rosado-Pinto, J 2006In vitro methods for specific IgE detection on cow's milk allergyAllergol Immunopathol (Madr)342731CrossRefGoogle Scholar
  26. 26.
    Sicherer, SH, Sampson, HA 2006Food allergyJ Allergy Clin Immunol117S470S475PubMedCrossRefGoogle Scholar
  27. 27.
    Juvonen, P 1996Allergy development and macromolecular absorption in infants with different feeding regimens during the first three days of life. A three-year prospective follow-upActa Paediatr8510471052PubMedGoogle Scholar
  28. 28.
    McClain, S, Bannon, GA 2006Animal models of food allergy: opportunities and barriersCurr Allergy Asthma Rep6141144PubMedGoogle Scholar
  29. 29.
    Baba, R, Fujita, M, Tein, CE, Miyoshi, M 2002Endocytosis by absorptive cells in the middle segment of the suckling rat small intestineAnat Sci Int77117123PubMedCrossRefGoogle Scholar
  30. 30.
    Rodewald, R 1970Selective antibody transport in the proximal small intestine of the neonatal ratJ Cell Biol45635640PubMedCrossRefGoogle Scholar
  31. 31.
    Rodewald, R 1972Intestinal transport of antibodies in the newborn ratJ Cell Biol58189211CrossRefGoogle Scholar
  32. 32.
    Rodewald, R 1973Intestinal transport antibodies in the newborn ratJ Cell Biol58189211PubMedCrossRefGoogle Scholar
  33. 33.
    Rodewald, R 1980Distribution of immunoglobulin G receptor in the small intestine of the young ratJ Cell Biol851832PubMedCrossRefGoogle Scholar
  34. 34.
    Abrahamson, DR, Rodewald, R 1981Evidence for the sorting of endocytic vesicle contents during receptor-mediated transport of IgG across newborn rat intestineJ Cell Biol91270280PubMedCrossRefGoogle Scholar
  35. 35.
    Geuze, HJ, Slot, JW, Strous, GJAM, Lodish, HF, Schwartz, AL 1983Intracellular site of asialoglycoprotein receptor-ligand uncoupling: double-label immunoelectron microscopy during receptor-mediated endocytosisCell32277287PubMedCrossRefGoogle Scholar
  36. 36.
    Rodewald, R, Kraehenbuhl, JP 1984Receptor-mediated transport of IgGJ Cell Biol99159164CrossRefGoogle Scholar
  37. 37.
    Harding, C, Levy, MA, Stahl, P 1985Morphological analysis of ligand uptake and processing: the role of multivesicular endosomes and CURL in receptor-ligand processingEur J Cell Biol36230238PubMedGoogle Scholar
  38. 38.
    Staley, TE, Bush, LJ 1985Receptor mechanism of the neonatal intestine and their relationship to immunoglobulin absorption and diseaseJ Dairy Sci68184205PubMedCrossRefGoogle Scholar
  39. 39.
    Graney, DO 1968The uptake of ferritin by ileal absorptive cells in suckling rats. An electron microscopic studyAm J Anat123227254PubMedCrossRefGoogle Scholar
  40. 40.
    Chase, CC, Munn, EA 1980Surface binding and uptake of polycationic ferritin by neonatal piglet intestinal epitheliumJ Cell Sci46235252PubMedGoogle Scholar
  41. 41.
    Gonnella, PA, Neutra, MR 1984Membrane-bound and fluid-phase macromolecules enter separate prelysosomal compartments in absorptive cells of suckling rat ileumJ Cell Biol99909917PubMedCrossRefGoogle Scholar
  42. 42.
    Gonatas, NK, Kim, SU, Stieber, A, Avrameas, S 1977Internalization of lectins in neuronal GERLJ Cell Biol73113PubMedCrossRefGoogle Scholar
  43. 43.
    Gonnella, PA, Neutra, MR 1985Glycoconjugate distribution and mobility on apical membranes of absorptive cells of suckling rat ileum in vivoAnat Rec213520528PubMedCrossRefGoogle Scholar
  44. 44.
    Hatae, T, Fujita, M, Okuyama, K 1988Study on the origin of apical tubules in ileal absorptive cells of suckling rats using concanavalin-A as a membrane-bound tracerCell Tissue Res251511521PubMedCrossRefGoogle Scholar
  45. 45.
    Oshikawa, T, Baba, R, Fujita, M 1996Apical endocytosis of lectins by the absorptive cells of the suckling rat jejunum in vivoOkajimas Folia Anat Jpn73229246PubMedGoogle Scholar
  46. 46.
    Wissing, SF, Graney, DO 1968Membrane modifications in the apical endocytic complex of ileal epithelia cellsJ Cell Biol39564579CrossRefGoogle Scholar
  47. 47.
    Ono, K 1975Absorption of horseradish peroxidase by the small intestinal epithelium in postnatal developing ratsZ Mikrosk-Anat Forsch89870883PubMedGoogle Scholar
  48. 48.
    Colony, PC, Neutra, MR 1985Macromolecular transport in the fetal rat intestineGastroenterology89294306PubMedGoogle Scholar
  49. 49.
    Wilson, JM, Whitney, JA, Neutra, MR 1987Identification of an endosomal antigen specific to absorptive cells of suckling rat ileumJ Cell Biol105691703PubMedCrossRefGoogle Scholar
  50. 50.
    Teichberg, S, Wapnir, RA, Moyse, J, Lifshitz, F 1992Development of the neonatal rat small intestinal barrier to nonspecific macromolecular absorption. II. Role of dietary corticosteronePediatr Res325057PubMedGoogle Scholar
  51. 51.
    Forssmann, WG, Metz, J, Heinrich, D 1975Gap junction in the hemotrichorial placenta of the ratJ Ultrastruct Res53374381PubMedCrossRefGoogle Scholar
  52. 52.
    Chaouet, G, Kolb, JP, Wegmann, TG 1983The murine placenta as an immunological barrier between the mother and the fetusImmunol Rev753160CrossRefGoogle Scholar
  53. 53.
    Suzuki, K, Kobayashi, M, Kobayashi, K 1997Structural and functional change of blood vessel labyrinth in maturing placenta of miceTrophoblast Res9155164Google Scholar
  54. 54.
    Georgiades, P, Ferguson-Smith, AC, Burton, GJ 2002Comparative developmental anatomy of the murine and human definitive placentaPlacenta2339PubMedCrossRefGoogle Scholar
  55. 55.
    Cross, JC, Baczyk, D, Dobric, N 2003Genes, development and evolution of the placentaPlacenta24123130PubMedCrossRefGoogle Scholar
  56. 56.
    Aoki, A, Forssmann, WG 1978Studies on the ultrastructure and permeability of the hemotrichrial placentaCell Tissue Res192409422PubMedCrossRefGoogle Scholar
  57. 57.
    Metz, J, Aoki, A, Forssmann, WG 1978Studies on the ultrastructure and permeability of the hemotrichrial placentaCell Tissue Res192391407PubMedCrossRefGoogle Scholar
  58. 58.
    Wegmann, TG, Singh, B, Carison, GA 1979Allogeneic placenta in a paternal strain antigen immunoabsorbentJ Immunol122270274PubMedGoogle Scholar
  59. 59.
    Falth-Magnusson, K, Kjellman, NI 1992Allergy prevention by maternal elimination diet during late pregnancy: a 5-year follow-up of a randomized studyJ Allergy Clin Immunol89709713PubMedCrossRefGoogle Scholar
  60. 60.
    Kurosumi, K, Kobayashi, Y 1968The fine structure of mammary glands of lactating rats, with special reference to the apocrine secretionExp Cell Res50177192PubMedCrossRefGoogle Scholar
  61. 61.
    Kimura, T 1969Electron microscopic study of the mechanism of secretion of milkNippon Sanka Fujinka Gakkaizassi21301308Google Scholar
  62. 62.
    Wooding, FBP 1970Theories of milk secretion: evidence from the electron microscopic examination of milkNature (Lond)226762764CrossRefGoogle Scholar
  63. 63.
    Lteif, AN, Schwenk, WF 1998Breast milkMayo Clin Proc73760763PubMedCrossRefGoogle Scholar
  64. 64.
    Van de Perre, P 2003Transfer of antibody via mother's milkVaccine2133743376PubMedCrossRefGoogle Scholar
  65. 65.
    Fukushima, Y 1997Consumption of cow milk and egg by lactating women and the presence of β-lactoglobulin and ovalbumin in breast milkAm J Clin Nutr653035PubMedGoogle Scholar

Copyright information

© The Japanese Society for Clinical Molecular Morphology 2007

Authors and Affiliations

  • Mamoru Fujita
    • 1
  • Ryoko Baba
    • 1
  • Mariko Shimamoto
    • 1
  • Yoshiko Sakuma
    • 1
  • Sunao Fujimoto
    • 1
  1. 1.Graduate School of Health and Nutrition SciencesNakamura Gakuen UniversityFukuokaJapan

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