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J Cell Biol. Sep 1, 1983; 97(3): 607–617.
PMCID: PMC2112552

Transcytosis in thyroid follicle cells

Abstract

Inside-out follicles prepared from pig thyroid glands were used for studies on endocytosis. endocytosis. In this in vitro system, only the apical plasma membranes of follicle cells were exposed to tracers added to the culture medium. Cationized ferritin (CF) bound to the apical plasma membrane and was transferred first to endosomes and to lysosomes (within 5 min). Later, after approximately 30 min, CF was also found in stacked Golgi cisternae. In addition, a small fraction of endocytic vesicles carrying CF particles became inserted into the lateral (at approximately 11 min) and the basal (at approximately 16 min) plasma membranes. Morphometric evaluation of CF adhering to the basolateral cell surfaces showed that the vesicular transport across thyroid follicle cells (transcytosis) was temperature-sensitive; it ceased at 15 degrees C but increased about ninefold in follicles stimulated with thyrotropin (TSH). Thyroglobulin-gold conjugates and [3H]thyroglobulin (synthesized in separate follicle preparations in the presence of [3H]leucine) were absorbed to the apical plasma membrane and detected mainly in lysosomes. A small fraction was also transported to the basolateral cell surfaces where the thyroglobulin preparations detached and accumulated in the newly formed central cavity. As in the case of CF, transcytosis of thyroglobulin depended on the stimulation of follicles with TSH. The observations showed that a transepithelial vesicular transport operates in thyroid follicle cells. This transport is regulated by TSH and includes the transfer of thyroglobulin from the apical to the basolateral plasma membranes. Transcytosis of thyroglobulin could explain the occurrence of intact thyroglobulin in the circulation of man and several mammalian species.

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Selected References

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  • Berg G. The structure of human thyroglobulin. J Ultrastruct Res. 1975 Oct;53(1):113–118. [PubMed]
  • Björkman U, Ekholm R, Elmqvist LG, Ericson LE, Melander A, Smeds S. Induced unidirectional transport of protein into the thyroid follicular lumen. Endocrinology. 1974 Dec;95(6):1506–1517. [PubMed]
  • Böcker W, Lietz H. Demonstration of thyroglobulin in lymph vessels of TSH stimulated guinea pigs by the indirect immunofluorescence technique. Acta Endocrinol (Copenh) 1973 Dec;74(4):666–674. [PubMed]
  • Bonner WM, Laskey RA. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. [PubMed]
  • Brandtzaeg P. Mucosal and glandular distribution of immunoglobulin components: differential localization of free and bound SC in secretory epithelial cells. J Immunol. 1974 Apr;112(4):1553–1559. [PubMed]
  • Consiglio E, Salvatore G, Rall JE, Kohn LD. Thyroglobulin interactions with thyroid plasma membranes. The existence of specific receptors and their potential role. J Biol Chem. 1979 Jun 25;254(12):5065–5076. [PubMed]
  • Daniel PM, Pratt OE, Roitt IM, Torrigiani G. The release of thyroglobulin from the thyroid gland into thyroid lymphatics; the identification of thyroglobulin in the thyroid lymph and in the blood of monkeys by physical and immunological methods and its estimation by radioimmunoassay. Immunology. 1967 May;12(5):489–504. [PMC free article] [PubMed]
  • Denef JF, Ekholm R. Membrane labeling with cationized ferritin in isolated thyroid follicles. J Ultrastruct Res. 1980 May;71(2):203–221. [PubMed]
  • Ericson LE. Exocytosis and endocytosis in the thyroid follicle cell. Mol Cell Endocrinol. 1981 Apr;22(1):1–24. [PubMed]
  • Farquhar MG. Recovery of surface membrane in anterior pituitary cells. Variations in traffic detected with anionic and cationic ferritin. J Cell Biol. 1978 Jun;77(3):R35–R42. [PMC free article] [PubMed]
  • Farquhar MG. Membrane recycling in secretory cells: implications for traffic of products and specialized membranes within the Golgi complex. Methods Cell Biol. 1981;23:399–427. [PubMed]
  • Garbi C, Wollman SH. Ultrastructure and some other properties of inverted thyroid follicles in suspension culture. Exp Cell Res. 1982 Apr;138(2):343–353. [PubMed]
  • Herzog V, Farquhar MG. Luminal membrane retrieved after exocytosis reaches most golgi cisternae in secretory cells. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5073–5077. [PMC free article] [PubMed]
  • Herzog V, Miller F. Membrane retrieval in epithelial cells of isolated thyroid follicles. Eur J Cell Biol. 1979 Aug;19(3):203–215. [PubMed]
  • Herzog V, Miller F. Structural and functional polarity of inside-out follicles prepared from pig thyroid gland. Eur J Cell Biol. 1981 Apr;24(1):74–84. [PubMed]
  • Horisberger M. Agglutination of erythrocytes using lectin-labeled spacers. Experientia. 1978 Jun 15;34(6):721–722. [PubMed]
  • Ikekubo K, Kishihara M, Sanders J, Jutton J, Schneider AB. Differences between circulating and tissue thyroglobulin in rats. Endocrinology. 1981 Aug;109(2):427–432. [PubMed]
  • Laemmli UK, Favre M. Maturation of the head of bacteriophage T4. I. DNA packaging events. J Mol Biol. 1973 Nov 15;80(4):575–599. [PubMed]
  • LOWRY OH, ROSEBROUGH NJ, FARR AL, RANDALL RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed]
  • Luft JH. Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat Rec. 1971 Nov;171(3):369–415. [PubMed]
  • MOORE DH, RUSKA H. The fine structure of capillaries and small arteries. J Biophys Biochem Cytol. 1957 May 25;3(3):457–462. [PMC free article] [PubMed]
  • Mostov KE, Kraehenbuhl JP, Blobel G. Receptor-mediated transcellular transport of immunoglobulin: synthesis of secretory component as multiple and larger transmembrane forms. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7257–7261. [PMC free article] [PubMed]
  • NADLER NJ, YOUNG BA, LEBLOND CP, MITMAKER B. ELABORATION OF THYROGLOBULIN IN THE THYROID FOLLICLE. Endocrinology. 1964 Mar;74:333–354. [PubMed]
  • Nitsch L, Wollman SH. Ultrastructure of intermediate stages in polarity reversal of thyroid epithelium in follicles in suspension culture. J Cell Biol. 1980 Sep;86(3):875–880. [PMC free article] [PubMed]
  • Ottosen PD, Courtoy PJ, Farquhar MG. Pathways followed by membrane recovered from the surface of plasma cells and myeloma cells. J Exp Med. 1980 Jul 1;152(1):1–19. [PMC free article] [PubMed]
  • Renston RH, Jones AL, Christiansen WD, Hradek GT, Underdown BJ. Evidence for a vesicular transport mechanism in hepatocytes for biliary secretion of immunoglobulin A. Science. 1980 Jun 13;208(4449):1276–1278. [PubMed]
  • Rodewald R. Intestinal transport of antibodies in the newborn rat. J Cell Biol. 1973 Jul;58(1):189–211. [PMC free article] [PubMed]
  • Rodewald R. pH-dependent binding of immunoglobulins to intestinal cells of the neonatal rat. J Cell Biol. 1976 Nov;71(2):666–669. [PMC free article] [PubMed]
  • Roitt IM, Torrigiani G. Identification and estimation of undegraded thyroglobulin in human serum. Endocrinology. 1967 Sep;81(3):421–429. [PubMed]
  • Rolland M, Lissitzky S. Endogenous proteolytic activity and constituent polypeptide chains of sheep and pig 19 S thyroglobulin. Biochim Biophys Acta. 1976 Apr 14;427(2):696–707. [PubMed]
  • Russo RG, Liotta LA, Thorgeirsson U, Brundage R, Schiffmann E. Polymorphonuclear leukocyte migration through human amnion membrane. J Cell Biol. 1981 Nov;91(2 Pt 1):459–467. [PMC free article] [PubMed]
  • SALPETER MM, BACHMANN L. AUTORADIOGRAPHY WITH THE ELECTRON MICROSCOPE. A PROCEDURE FOR IMPROVING RESOLUTION, SENSITIVITY, AND CONTRAST. J Cell Biol. 1964 Aug;22:469–477. [PMC free article] [PubMed]
  • Seljelid R, Reith A, Nakken KF. The early phase of endocytosis in rat thyroid follicle cells. Lab Invest. 1970 Dec;23(6):595–605. [PubMed]
  • Tice LW, Wollman SH, Carter RC. Changes in tight junctions of thyroid epithelium with changes in thyroid activity. J Cell Biol. 1975 Sep;66(3):657–663. [PMC free article] [PubMed]
  • Uller RP, van Herle AJ, Chopra IJ. Thyroidal response to graded doses of bovine thyrotropin. J Clin Endocrinol Metab. 1977 Aug;45(2):312–318. [PubMed]
  • van den Hove MF, Couvreur M, de Visscher M, Salvatore G. A new mechanism for the reabsorption of thyroid iodoproteins: selective fluid pinocytosis. Eur J Biochem. 1982 Feb;122(2):415–422. [PubMed]
  • Van Deurs B, Von Bülow F, Møller M. Vesicular transport of cationized ferritin by the epithelium of the rat choroid plexus. J Cell Biol. 1981 Apr;89(1):131–139. [PMC free article] [PubMed]
  • Van Herle AJ, Vassart G, Dumont JE. Control of thyroglobulin synthesis and secretion (second of two parts). N Engl J Med. 1979 Aug 9;301(6):307–314. [PubMed]
  • Warchol JB, Brelińska R, Herbert DC. Analysis of colloidal gold methods for labelling proteins. Histochemistry. 1982;76(4):567–575. [PubMed]

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