An endoplasmic reticulum storage disease causing congenital goiter with hypothyroidism

Journal of Cell Biology

Volumn 133, Issue 3, 1996, Pages 517-527

  Kim, Paul S ^a   Kwon, O Yu ^a   Arvan, Peter ^a,b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; CHAPERONE; THYROGLOBULIN;

ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CONTROLLED STUDY; DIMERIZATION; ENDOPLASMIC RETICULUM; GOITER; HORMONE TRANSPORT; HYPOTHYROIDISM; INTRACELLULAR TRANSPORT; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; STORAGE DISEASE; THYROID GLAND; THYROID HORMONE SYNTHESIS;

ANIMALS; CYTOPLASMIC GRANULES; ENDOPLASMIC RETICULUM; FEMALE; GOITER; HYPOTHYROIDISM; MALE; METABOLISM, INBORN ERRORS; MICE; MICE, INBRED STRAINS; MOLECULAR CHAPERONES; MUTATION; PROTEIN FOLDING; SENSITIVITY AND SPECIFICITY; TEMPERATURE; THYROGLOBULIN; THYROID GLAND;

ANIMALIA;

EID: 0029941327     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.133.3.517     Document Type: Article

References (85)

1. Adkison, L.R., S. Taylor, and W.G. Beamer. 1990. Mutant gene-induced disorders of structure, function and thyroglobulin synthesis in congenital goitre (cog/cog) in mice. J. Endocrinol. 126:51-58.
2. Amara, J.F., S.H. Cheng, and A.E. Smith. 1992. Intracellular protein trafficking defects in human disease. Trends Cell Biol. 2:145-149.
3. Arima, T., M.J. Spiro, and R.G. Spiro. 1972. Studies on the carbohydrate units of thyroglobulin. J. Biol. Chem. 247:1825-1835.
4. Arvan, P., and J. Lee. 1991. Regulated and constitutive proteins targeting can be distinguished by secretory polarity in thyroid epithelial cells. J. Cell Biol. 112:365-376.
5. Basche, M., W.G. Beamer, and A.B. Schneider. 1989. Abnormal properties of thyroglobulin in mice with inherited congenital goiter (cog/cog). Endocrinology. 124:1822-1829.
6. Beamer, W.G., L.J. Maltais, M.H. DeBaets, and E.M. Eicher. 1987. Inherited congenital goiter in mice. Endocrinology. 120:838-840.
7. Bergeron, J.J.M., M.B. Brenner, D.Y. Thomas, and D.B. Williams. 1994. Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem. Sci. 19:124-128.
8. Bonadio, J., and P.M. Byers. 1985. Subtle structural alterations in the chains of type I procollagen produce osteogenesis imperfecta type II. Nature (Land.). 316:363-366.
9. Bonifacino, J.S., and J. Lippincott-Schwartz. 1991. Degradation of proteins within the endoplasmic reticulum. Curr. Opin. Cell Biol. 3:592-600.
10. Braakman. I., H. Hoover-Litty, K.R. Wagner, and A. Helenius. 1991. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell Biol. 114: 401-411.
11. Callea, F., M. Brisgotti, G. Fabbretti, F. Bonino, and V.J. Desmet. 1992. Hepatic endoplasmic reticulum storage diseases. Liver. 12:357-362.
12. Cavalieri, R.R., and G.L. Searle. 1967. Biosynthesis of thyroglobulin and subunits in the rat thyroid gland in vivo. Biochem. J. 102:25c-27c.
13. Chen, W., J. Helenius, I. Braakman, and A. Helenius. 1995. Cotranslational folding and calnexin binding during glycoprotein synthesis. Proc. Natl. Acad. Sci. USA. 92:6229-6233.
14. Cox, J.S., C.E. Shamu, and P. Walter. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell. 73:1197-1206.
15. Dorner, A.J., L.C. Wasley, P. Raney, S. Haugejorden, M. Green, and R.J. Kaufman. 1990. The stress response in Chinese hamster ovary cells. Regulation of ERp72 and protein disulfide isomerase expression and secretion. J. Biol. Chem. 265:22029-22034.
16. Dorner, A.J., L.C. Wasley, and R.J. Kaufman. 1992. Overexpression of GRP78 mitigates induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO (Eur. Mol. Biol. Organ.) J. 11:1563-1571.
17. Dumont, J.E., G. Vassart, and S. Refetoff. 1989. Thyroid disorders. In The Metabolic Basis of Inherited Disease. C.R. Scrier, A.L. Beaudet, W.L. Sly, and D. Valles, editors. McGraw-Hill Inc., New York. 1843-1883.
18. Dunn, J.T. 1992. Thyroglobulin: chemistry and biosynthesis. In Werner and Ingbar's: The Thyroid. L, Braverman and R. Utigers, editors. J.B. Lippincott Co., Philadelphia. 98-110.
19. Dunn, J.T., P.C. Anderson, J.W. Fox, C.A. Fassler, A.D. Dunn, L.A. Hite, and R.C. Moore. 1987. The sites of thyroid hormone formation in rabbit thyroglobulin. J. Biol. Chem. 262:16948-16952.
20. Fogelfeld, L., G. Harel, W.O. Beamer, and A.B. Schneider. 1992. Low-molecular weight iodoproteins in the congenital goiters of cog/cog mice. Thyroid. 2: 329-335.
21. Franc, J.L., A. Giraud, and J. Lanet. 1990. Effects of deoxymannojirimycin and castanospermine on the polarized secretion of thyroglobulin. Endocrinology. 126:1464-1470.
22. Freedman, R. B., T. R. Hirst, and M. F. Tuite. 1994, Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci. 19:331-336.
23. Ganan, S., J.J. Cazzulo, and A.J. Parodi. 1991. A major proportion of N-glycoproteins are transiently glucosylated in the endoplasmic reticulum. Biochemistry. 30:3098-3104.
24. Gentile, F., and G. Salvatore. 1993. Preferential sites of proteolytic cleavage of bovine, human, and rat thyroglobulin. The use of limited proteolysis to detect solvent exposed regions of the primary structure. Eur. J. Biochem. 218: 603-621.
25. Gentile, F., G. Palumbo, and G. Salvatore. 1992. The origin of the electrophoretic doublet of thyroglobulin. Biochem. Biophys. Res. Comm. 186:1185-1191.
26. Gibson, R., S. Schlesinger, and S. Kornfeld. 1979. The nonglycosylated glycoprotein of vesicular stomatitis virus is temperature-sensitive and undergoes intracellular aggregation at elevated temperatures. J. Biol. Chem. 254:3600-3607.
27. Gilmore, R. 1993. Protein translocation across the endoplasmic reticulum: a tunnel with toll booths at entry and exit. Cell. 75:589-592.
28. Hammond, C., and A. Helenius, 1994. Folding of VSV G protein: sequential interactions with BiP and calnexin. Science. (Wash. DC). 266:456-458.
29. Hammond, C., and A. Helenius. 1995. Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7:523-529.
30. Hebert, D.N., B. Foellmer, and A. Helenius. 1995. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell. 81:425-433.
31. Helenius, A. 1994. How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol. Biol. Cell. 5:253-265.
32. Hendershot, L.M. 1990. Immunoglobulin heavy chain and binding protein complexes are dissociated in vivo by light chain addition. J. Cell Biol. 111:829-837.
33. Kelleher, D.J., G. Kreibich, and R. Gilmore. 1992. Oligosaccharyltransferase activity is association with a protein complex composed of ribophorins I and II and a 48 kd protein. Cell. 69:55-65.
34. Kim, P.S., and P. Arvan. 1991. Folding and assembly of newly synthesized thryoglobulin occurs in a pre-Golgi compartment. J. Biol. Chem. 266:12412-12418.
35. Kim, P.S., and P. Arvan. 1993. Hormonal regulation of thyroglobulin export from the endoplasmic reticulum of cultured thyrocytes. J. Biol. Chem. 268: 4873-4879.
36. Kim, P.S., and P. Arvan. 1995. Calnexin and BiP act as sequential molecular chaperones during thyroglobulin folding in the endoplasmic reticulum. J. Cell. Biol. 128:29-38.
37. Kim, P.S., D. Bole, and P. Arvan. 1992. Transient aggregation of nascent thyroglobulin in the endoplasmic reticulum: relationship to the molecular chaperone, BiP. J. Cell Biol. 118:541-549.
38. Kim, P.S., K.-R. Kim, and P. Arvan. 1993. Disulfide-linked aggregation of thyroglobulin normally occurs during nascent protein folding. Am. J. Physiol. 265:C704-C711.
39. Kohno, K., K. Normington, J. Sambrook, M.J. Gething, and K. Mori. 1993. The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell. Biol. 13:877-890.
40. Kondo, Y., and Y. Kamiya. 1976. Purification and some properties of microsome-bound thyroglobulins. Biochim. Biophys. Acta. 427:268-284.
41. Kuliawat, R., and P. Arvan. 1994. lodination of thyroglobulin leads to thyroid hormone synthesis and basolateral secretion from filter-polarized thyroid epithelial cells. J. Biol. Chem. 269:4922-4927.
42. Kuznetsov, G., L.B. Chen, and S.K. Nigam. 1994. Several endoplasmic reticulum stress proteins, including ERp72, interact with thyroglobulin during its maturation. J. Biol. Chem. 269:22990-22995.
43. Lissitzky, S., M. Roques, J. Torresani, C. Simon, and S. Bouchilloux. 1964. Iodination and biosynthesis of rat thyroglobulin. Biochem. Biophys. Res. Comm. 16:249-253.
44. Lissitzky, S., J. Torresani, G.N. Burrow, S. Bouchilloux, and O. Chabaud. 1975. Defective thyroglobulin export as a cause of congenital goiter. Clin. Endocrinol. 4:363-392.
45. Lodish, H.F., N. Kong, and L. Wikstrom. 1992. Calcium is required for folding of newly made subunits of the asialoglycoprotein receptor within the endoplasmic reticulum. J. Biol. Chem. 267:12753-12760.
46. Macer, D.R., and G.L. Koch. 1988. Identification of a set of calcium-binding proteins in reticuloplasm, the luminal content of the endoplasmic reticulum. J. Cell Sci. 91:61-70.
47. Manchester, M., L. Everitt, D.D. Loeb, C.A. Hutchison III, R. Swanstrom, and C. A. Hutchison II. 1994. Identification of temperature-sensitive mutants of the human immunodeficiency virus type 1 protease through saturation mutagenesis. Amino acid side chain requirements for temperature sensitivity. J. Biol. Chem. 269:7689-7695.
48. Marquardt, T., D.N. Hebert, and A. Helenius. 1993. Post-translational folding of influenza hemagglutinin in isolated endoplasmic reticulum-derived microsomes. J. Biol. Chem. 268:19618-19625.
49. Mayerhofer, A., A.G. Amador, W.O. Beamer, and A. Bartke. 1988. Ultrastructural aspects of the goiter in cog/cog mice. J. Hered. 79:200-203.
50. McCauliffe, D.P., Y.S. Yang, J. Wilson, R.D. Sontheimer, and J.D. Capra. 1992. The 5′-flanking region of the human calreticulin gene shares homology with the human GRP78, GRP94, and protein disulfide isomerase promoters. J. Biol. Chem. 267:2557-2562.
51. Medeiros-Neto, G., and J.B. Stanbury. 1994. Inherited Disorders of the Thyroid System. CRC Press, Boca Raton, FL. 221 pp.
52. Medeiros-Neto, G., H.M. Targovnik, and G. Vassart. 1993. Defective thyroglobulin synthesis and secretion causing goiter and hypothyroidism. Endocr. Rev. 14:165-183.
53. Melnick, J., S. Aviel, and Y. Argon. 1992. The endoplasmic reticulum stress protein GRP94, in addition to BiP, associates with unassembled immunoglobulin chains. J. Biol. Chem. 267:21303-21306.
54. Melnick, J., J.L. Dul, and Y. Argon. 1994. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature (Land.). 370:373-375.
55. Michel-Bechel, M., G. Cotte, J.-L. Codaccioni, and A.-M. Athouel-Haon. 1969. Ultrastructure thyroidienne et perturbations biochimiques de l'hormonogenese. Acta Anal. 73:389-409.
56. Miura, O., and N. Aoki. 1990. Impaired secretion of mutant alpha 2-plasmin inhibitor (alpha 2 PI-Nara) from COS-7 and HepG2 cells: molecular and cellular basis for hereditary deficiency of alpha 2-plasmin inhibitor. Blood. 75: 1092-1096.
57. Miura, O., Y. Sugahara, and N. Aoki. 1993. Intracellular transport-deficient mutants causing hereditary deficiencies of factors in coagulation and fibrinolysis. Thromb. Haemostasis. 69:296-297.
58. Mori, K., W. Ma, M.J. Gething, and J. Sambrook. 1993. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell. 74:743-756.
59. Ohyama, Y., T. Hosoya, T. Kameya, N. Suzuki, S. Nakamura, K. Kazahari, K. Shibayama, Y. Yokota, and N. Matsura. 1994. Congenital euthyroid goitre with impaired thyroglobulin transport. Clin. Endocrinol. 41:129-135.
60. Otsu, M., R. Urade, M. Kito, F. Omura, and M. Kikuchi. 1995. A possible role of ER-60 protease in the degradation of misfolded proteins in the endoplasmic reticulum. J. Biol. Chem. 270:14958-14961.
61. Ou, W.-J., P.H. Cameron, D.Y. Thomas, and J.J.M. Bergeron. 1993. Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature (Lond.). 364:771-776.
62. Parodi, A.J., D.H. Mendelzon, and G.Z. Lederkremer. 1983. Transient glucosylation of protein-bound Man9GlcNAc2, Man8GlcNAc2, and Man7GlcNAc2 in calf thyroid cells. A possible recognition signal in the processing of glycoproteins. J. Biol. Chem. 258:8260-8265.
63. - channel is functional when retained in the endoplasmic reticulum of mammalian cells. J. Biol. Chem. 270:12347-12350.
64. Peterson, J.R., A. Ora, P.N. Van, and A. Helenius. 1995. Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol. Biol. Cell. 6:1173-1184.
65. Pind, S., J.R. Riordan, and D.B. Williams. 1994. Participation of the endoplasmic reticulum chaperone calnexin (p88, IP90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269:12784-12788.
66. Prockop, D.J., M.-L. Chu, W. De Wet, J.C. Myers, T. Pihlajaniemi, F. Ramirez, and M. Sippola. 1985. Mutations in osteogenesis imperfecta leading to the synthesis of abnormal type I procollagens. Ann. NY Acad. Sci. 460:289-297.
67. Rajasekaran, A.K., T. Morimoto, O.K. Hanzel, E. Rodriguez-Boulan, and G. Kreibich. 1993. Structural reorganization of the rough endoplasmic reticulum without size expansion accounts for dexamethasone-induced secretory activity in AR42J cells. J. Cell Sci. 105:333-345.
68. Rawitch, A.B., M.R. Litwer, J. Gregg, C.D. Turner, J.B. Rouse, and J.W. Hamilton. 1984. The isolation of identical thyroxine containing amino acid sequences from bovine, ovine and porcine thyroglobulins. Biochem. Biophys. Res. Comm. 118:423-429.
69. Schmale, H., U. Bahnsen, and D. Richter. 1993. Structure and expression of the vasopressin precursor gene in central diabetes insipidus. Ann. NY Acad. Sci. 689:74-82.
70. Seed, R.W., and I.H. Goldberg. 1965. lodination in relation to thyroglobulin maturation and subunit aggregation. Science (Wash. DC). 149:1380-1382.
71. Sifers, R.N., M.J. Finegold, and S.L. Woo. 1992. Molecular biology and genetics of alphal-antitrypsin deficiency. Semin. Liver Dis. 12:301-310.
72. Sousa, M.C., M.A. Ferrero-Garcia, and A.J. Parodi. 1992. Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Gl glycoprotein glucosyltransferase. Biochemistry. 31:97-105.
73. Srinivasan, M., N. Lenny, and M. Green. 1993. Identification of genomic sequences that mediate the induction of the endoplasmic reticulum stress protein, ERp72. by protein traffic. DNA Cell Biol. 12:807-822.
74. Sugisaki, T., W.G. Beamer, and T. Noguchi. 1992. Microcephalic cerebrum with hypomyelination in the congenital goiter mouse (cog). Neurochem. Res. 17: 1037-1040.
75. Taylor, B.A., and L. Rowe. 1987. The congenital goiter mutation is linked to the thyroglobulin gene in the mouse. Proc. Nat. Acad. Sci. USA. 84:1986-1990.
76. Tokunaga, F., S. Wakabayashi, and T. Koide. 1995. Warfarin causes the degradation of protein C precursor in the endoplasmic reticulum. Biochemistry. 34:1163-1170.
77. Urade, R., Y. Takenaka, and M. Kito. 1993. Protein degradation by ERp72 from rat and mouse liver endoplasmic reticulum. J. Biol. Chem. 268:22004-22009.
78. Van Herle, A.J., G. Vassarl, and J.E. Dumont. 1979. Control of thyroglobulin synthesis and secretion. N. Engl. J. Med 301:239-249 and 307-314.
79. Vecchio, G., G.M. Claar, and G. Salvatore. 1972. Biosynthesis of thyroid io-doproteins in vivo and in tissue slices. J. Biol. Chem. 247:4908-4913.
80. Wada, I., S. Imai, M. Kai, F. Sakane, and H. Kanoh. 1995. Chaperone function of calreticulin when expressed in the endoplasmic reticulum as the membrane-anchored and soluble forms. J. Biol. Chem. 270:20298-20304.
81. Wagar, G. 1974. Effect of actinomycin D on TSH-induced stimulation of thyroidal protein synthesis in the rat. Acta Endocrinol. 77:64-70.
82. Ware, F., A. Vassilakos, P. Peterson, M. Jackson, M. Lehrman, and D. Williams. 1995. The molecular chaperone calnexin binds Glc1Man9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J. Biol. Chem. 270:4697-4704.
83. Weissman, J.S., and P.S. Kim. 1993. Efficient catalysis of disulphide bond rearrangements by protein disulfide isomerase. Nature (Lond.). 365:185-188.
84. Wiest, D.L., J.K. Burkhardt, S. Hester, M. Hortsch, D.I. Meyer, and Y. Argon. 1990. Membrane biogenesis during B cell differentiation: most endoplasmic reticulum proteins are expressed coordinately. J. Cell Biol. 1101:1501-1511.
85. Yang, Y., S. Janich, J.A. Conn, and J.M. Wilson. 1993. The common variant of cystic fibrosis transmembrane conductance regulator is recognized by hsp 70 and degraded in a pre-Golgi nonlysosomal compartment. Proc. Natl. Acad. Sci. USA. 90:9480-9484.