Skip to main content
SpringerLink
Log in

Origin of the apical transcytic membrane system in jejunal absorptive cells of neonates

  • Original Paper
  • Published:
Medical Molecular Morphology Aims and scope Submit manuscript

Abstract

We investigated the origin of the apical transcytic membrane system in jejunal absorptive cells of neonatal rats using light, electron, and immunofluorescence microscopy. In rats just after birth, intraluminally injected horseradish peroxidase (HRP), used as a macromolecular tracer, was observed only in the apical endocytic membrane system including the lysosomes, of jejunal absorptive cells in vivo. No tracer, however, was found in the intercellular space between the jejunal absorptive cells and the submucosa. Immunoreactive neonatal Fc receptor (FcRn) was localized in the perinuclear region of these absorptive cells whereas immunoglobulin G (IgG) was not found in these absorptive cells. In contrast, in rats 2 h after breast-feeding, intraluminally injected HRP was observed in the apical endocytic membrane system and in the apical transcytic membrane system of the absorptive cells. Moreover, HRP was found in the intercellular space between the jejunal absorptive cells and the submucosa. Furthermore, FcRn and IgG were widely distributed throughout the absorptive cells, and IgG was detected in both the intercellular space and the submucosa. These data suggest that initiation of breast-feeding induces the transportation of membrane-incorporated FcRn from its perinuclear localization to the apical plasma membrane domain. This transportation is achieved through the membrane system, which mediates apical receptor-mediated transcytosis via the trans-Golgi network. Subsequently, the apical plasma membrane containing the FcRn binds to maternal IgG, is endocytosed into the absorptive cells, and is transported to the basolateral membrane domain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Fujita M, Baba R, Matsuguma M, Kai T, Nozaki S, Miyoshi M (1998) Apical and basolateral endocytic pathways in absorptive cells of suckling and adult rats small intestine in vivo. Digestion Absorption 20:113–118

    Google Scholar 

  2. Fujita M, Baba R, Tanaka R, Nozaki S, Miyoshi M (2000) Similarity and diversity of an apical endocytic membrane system in the absorptive cells of the rat small and large intestine. Digestion Absorption 22:9–14

    Google Scholar 

  3. Owen RL, Jones AL (1974) Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203

    PubMed  CAS  Google Scholar 

  4. Owen RL (1977) Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer’s patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 72:440–451

    PubMed  CAS  Google Scholar 

  5. Hatae T, Fujita M, Okuyama K (1988) Study on the origin of apical tubules in ileal absorptive cells of suckling rats using concanavalin-A as a membrane-bound tracer. Cell Tissue Res 251:511–521

    Article  PubMed  CAS  Google Scholar 

  6. Fujita M, Reinhart F, Neutra M (1990) Convergence of apical and basolateral endocytic pathways at apical late endosomes in absorptive cells of suckling rat ileum in vivo. J Cell Sci 97:385–394

    PubMed  Google Scholar 

  7. Fujita M, Mizutani A, Yamamoto T, Neutra M (1991) Apical and basolateral endocytosis of macromolecules in absorptive cells of suckling rat ileum. J Clin Electron Microsc 24:524–525

    Google Scholar 

  8. Fujita M, Matsukuma M (1992) Transepithelial transport of nonspecific macromolecules by absorptive cells of suckling rat jejunum. J Clin Electron Microsc 25:470–471

    Google Scholar 

  9. Oshikawa T, Baba R, Fujita M (1996) Apical endocytosis of lectins by the absorptive cells of the suckling rat jejunum in vivo. Okajimas Folia Anat Jpn 73:229–246

    PubMed  CAS  Google Scholar 

  10. Baba R, Matsuguma M, Fujita M, Kai T, Nozaki S, Miyoshi M (1999) Transcytic pathway of food allergen by the absorptive cells of the suckling rat small intestine in vivo. Digestion Absorption 21:81–84

    Google Scholar 

  11. Baba R, Tanaka R, Fujita M, Miyoshi M (1999) Cellular differentiation of absorptive cells in the neonatal rat colon: an electron microscopic study. Med Electron Microsc 32:105–113

    Article  PubMed  Google Scholar 

  12. Baba R, Fujita M, Tein CE, Miyoshi M (2002) Endocytosis by absorptive cells in the middle segment of the suckling rat small intestine. Anat Sci Int 77:117–123

    Article  PubMed  Google Scholar 

  13. Fujita M, Baba R, Shimamoto M, Sakuma Y, Fujimoto S (2007) Molecular morphology of the digestive tract; macromolecules and food allergens are transferred intact across the intestinal absorptive cells during the neonatal-suckling period. Med Mol Morphol 40:1–7

    Article  PubMed  CAS  Google Scholar 

  14. Rodewald R (1970) Selective antibody transport in the proximal small intestine of the neonatal rat. J Cell Biol 45:635–640

    Article  PubMed  CAS  Google Scholar 

  15. Rodewald R (1973) Intestinal transport of antibodies in the newborn rat. J Cell Biol 58:189–211

    Article  PubMed  CAS  Google Scholar 

  16. Rodewald R (1980) Distribution of immunoglobulin G receptors in the small intestine of the young rat. J Cell Biol 85:18–32

    Article  PubMed  CAS  Google Scholar 

  17. Abrahamson DR, Rodewald R (1981) Evidence for the sorting of endocytic vesicle contents during the receptor-mediated transport of IgG across the newborn rat intestine. J Cell Biol 91:270–280

    Article  PubMed  CAS  Google Scholar 

  18. Rodewald R, Abrahamson DR (1982) Receptor-mediated transport of IgG across the intestinal epithelium of the neonatal rat. Ciba Found Symp 92:209–232

    PubMed  CAS  Google Scholar 

  19. Rodewald R, Kraehenbuhl JP (1984) Receptor-mediated transport of IgG. J Cell Biol 99:159s–164s

    Article  PubMed  CAS  Google Scholar 

  20. Jakoi ER, Cambier J, Saslow S (1985) Transepithelial transport of maternal antibody: purification of IgG receptor from newborn rat intestine. J Immunol 135:3360–3364

    PubMed  CAS  Google Scholar 

  21. Mostov KE, Simister NE (1985) Transcytosis. Cell 43:389–390

    Article  PubMed  CAS  Google Scholar 

  22. Dickinson BL, Badizadegan K, Wu Z, Ahouse JC, Zhu X, Simister NE, Blumberg RS, Lencer WI (1999) Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J Clin Invest 104:903–911

    Article  PubMed  CAS  Google Scholar 

  23. Van de Perre P (2003) Transfer of antibody via mother’s milk. Vaccine 21:3374–3376

    Article  PubMed  Google Scholar 

  24. Simister NE, Mostov KE (1989) An Fc receptor structurally related to MHC class I antigen. Nature (Lond) 337:184–187

    Article  CAS  Google Scholar 

  25. Israel EJ, Simister N, Freiberg E, Caplan A, Walker WA (1993) 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

    PubMed  CAS  Google Scholar 

  26. Raghavan M, Gastinel LN, Bjorkman PJ (1993) The class I major histocompatibility complex related Fc receptor shows pH-dependent stability differences correlating with Immunoglobulin binding and release. Biochemistry 32:8654–8660

    Article  PubMed  CAS  Google Scholar 

  27. Burmeister WP, Huber AH, Bjorkman PJ (1994) Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature (Lond) 372:379–383

    Article  CAS  Google Scholar 

  28. Raghavan M, Bonagura VR, Morrison SL, Bjorkman PJ (1995) Analysis of the pH dependence of the neonatal Fc receptor/immunoglobulin G interaction using antibody and receptor variants. Biochemistry 34:14649–14657

    Article  PubMed  CAS  Google Scholar 

  29. Ghetie V, Ward ES (1997) FcRn: the MHC class I-related receptor that is more than an IgG transporter. Immunol Today 18:592–598

    Article  PubMed  CAS  Google Scholar 

  30. Israel EJ, Taylor S, Wu Z, Mizoguchi E, Blumberg RS, Bhan A, Simister NE (1997) Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 92:69–74

    Article  PubMed  CAS  Google Scholar 

  31. Borvak J, Richardson J, Medesan C, Antohe F, Radu C, Simionescu M, Ghetie V, Ward ES (1998) Functional expression of the MHC class I-related receptor, FcRn, in endothelial cells of mice. Int Immunol 10:1289–1298

    Article  PubMed  CAS  Google Scholar 

  32. Weng Z, Gulukota K, Vaughn DE, Bjorkman PJ, DeLisi C (1998) Computational determination of the structure of rat Fc bound to the neonatal Fc receptor. J Mol Biol 282:217–225

    Article  PubMed  CAS  Google Scholar 

  33. Praetor A, Ellinger I, Hunziker W (1999) Intracellular traffic of the MHC class I-like IgG Fc receptor, FcRn, expressed in epithelial MDCK cells. J Cell Sci 112:2291–2299

    PubMed  CAS  Google Scholar 

  34. Claypool SM, Dickinson BL, Yoshida M, Lencer WI, Blumberg RS (2002) Functional reconstitution of human FcRn in Madin-Darby canine kidney cells requires co-expressed human β2-microglobulin. J Biol Chem 277:28038–28050

    Article  PubMed  CAS  Google Scholar 

  35. Praetor A, Jones RM, Wong WL, Hunziker W (2002) Membraneanchored human FcRn can oligomerize in the absence of IgG. J Mol Biol 321:277–284

    Article  PubMed  CAS  Google Scholar 

  36. Takai T (2002) Roles of Fc receptors in autoimmunity. Nat Rev Immunol 2:580–592

    PubMed  CAS  Google Scholar 

  37. Shah U, Dickinson BL, Blumberg RS, Simister NE, Lencer WI, Walker WA (2003) Distribution of the IgG Fc receptor, FcRn, in the human fetal intestine. Pediatr Res 53:295–301

    PubMed  CAS  Google Scholar 

  38. Claypool SM, Dickinson BL, Wagner JS, Johansen FE, Venu N, Borawski JA, Lencer WI, Blumberg RS (2004) Bidirectional transepithelial IgG transport by a strongly polarized basolateral membrane FcΓ-receptor. Mol Biol Cell 15:1746–1759

    Article  PubMed  CAS  Google Scholar 

  39. Yoshida M, Claypool SM, Wagner JS, Mizoguchi E, Mizoguchi A, Roopenian DC, Lencer WI, Blumberg RS (2004) Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20:769–783

    Article  PubMed  CAS  Google Scholar 

  40. Tesar DB, Tiangco NE, Bjorkman PJ (2006) Ligand valency affects transcytosis, recycling and intracellular trafficking mediated by the neonatal Fc receptor. Traffic 7:1127–1142

    Article  PubMed  CAS  Google Scholar 

  41. Roopenian DC, Akilesh S (2007) FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 7:715–725

    Article  PubMed  CAS  Google Scholar 

  42. He W, Ladinsky MS, Huey-Tubman KE, Jensen GJ, Mclntosh JR, Björkman PJ (2008) FcRn-mediated antibody transport across epithelial cells revealed by electron tomography. Nature (Lond) 455:542–546

    Article  CAS  Google Scholar 

  43. Hirano S, Kataoka K (1986) Histogenesis of the mouse jejunal mucosa, with special reference to proliferative cells and absorptive cells. Arch Histol Jpn 49:333–348

    Article  PubMed  CAS  Google Scholar 

  44. Baba R, Yamami M, Sakuma Y, Fujita M, Fujimoto S (2005) Relationship between glucose transporter and changes in the absorptive system in small intestinal absorptive cells during the weaning process. Med Mol Morphol 38:47–53

    Article  PubMed  Google Scholar 

  45. Simons K, Wandinger-Ness A (1990) Polarized sorting in epithelia. Cell 62:207–210

    Article  PubMed  CAS  Google Scholar 

  46. Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759–803

    PubMed  CAS  Google Scholar 

  47. Hatae T, Fujita M, Sagara H (1984) Structural differentiation in the apical tubules of several absorptive epithelia. J Electron Microsc 33:292

    Google Scholar 

  48. Hatae T, Fujita M, Sagara H (1986) Helical structure in the apical tubules of several absorbing epithelia. Kidney proximal tubule, visceral yolk sac and ductuli efferentes. Cell Tissue Res 244:39–46

    Article  PubMed  CAS  Google Scholar 

  49. Hatae T, Fujita M, Sagara H, Okuyama K (1986) Formation of apical tubules from large endocytic vacuoles in kidney proximal tubule cells during absorption of horseradish peroxidase. Cell Tissue Res 246:271–278

    Article  PubMed  CAS  Google Scholar 

  50. Oliver C (1982) Endocytic pathways at the lateral and basal cell surfaces of exocrine acinar cells. J Cell Biol 95:154–161

    Article  PubMed  CAS  Google Scholar 

  51. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243–294

    Article  PubMed  CAS  Google Scholar 

  52. Apodaca G, Aroeti B, Tang K, Mostov KE (1993) Brefeldin-A inhibits the delivery of the polymeric immunoglobulin receptor to the basolateral surface of MDCK cells. J Biol Chem 268(27): 20380–20385

    PubMed  CAS  Google Scholar 

  53. Klumperman J (2000) Transport between ER and Golgi. Curr Opin Cell Biol 12:445–449

    Article  PubMed  CAS  Google Scholar 

  54. Ober RJ, Martinez C, Vaccaro C, Zhou J, Ward ES (2004) Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn. J Immunol 172:2021–2029

    PubMed  CAS  Google Scholar 

  55. Ober RJ, Martinez C, Lai X, Zhou J, Ward ES (2004) Exocytosis of IgG as mediated by the receptor, FcRn: an analysis at the singlemolecule level. Proc Natl Acad Sci U S A 101:11076–11081

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Health and Nutrition Sciences, Nakamura Gakuen University, 5-7-1 Befu, Jyonan-ku, Fukuoka, 814-0198, Japan

    Nana Kumagai, Yoshiko Sakuma, Kumi Arita, Miki Shinohara, Megumi Kourogi, Sunao Fujimoto & Mamoru Fujita

  2. Department of Anatomy, University of Occupational and Environmental Health, School of Medicine, Kitakyushu, Japan

    Ryoko Baba

  3. Fukuoka University School of Nursing, Fukuoka, Japan

    Yoshiko Sakuma & Kumi Arita

Authors
  1. Nana Kumagai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ryoko Baba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoshiko Sakuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kumi Arita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miki Shinohara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Megumi Kourogi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sunao Fujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mamoru Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mamoru Fujita.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumagai, N., Baba, R., Sakuma, Y. et al. Origin of the apical transcytic membrane system in jejunal absorptive cells of neonates. Med Mol Morphol 44, 71–78 (2011). https://doi.org/10.1007/s00795-010-0506-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00795-010-0506-3

Keywords

Search

Navigation