Thyroglobulin from molecular and cellular biology to clinical endocrinology

Endocrine Reviews

Volumn 37, Issue 1, 2016, Pages 2-36

  Di Jeso, Bruno ^a   Arvan, Peter ^b  

^a UNIVERSITY OF SALENTO   (Italy)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINESTERASE; DIIODOTYROSINE; IODIDE; SECRETORY PROTEIN; THYROGLOBULIN; THYROID HORMONE; TYROSINE;

CONGENITAL HYPOTHYROIDISM; DIMERIZATION; DISULFIDE BOND; ENDOPLASMIC RETICULUM; FRAMESHIFT MUTATION; HORMONE SYNTHESIS; INTRACELLULAR TRANSPORT; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; REVIEW; THYROID FOLLICLE; VERTEBRATE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; ENDOPLASMIC RETICULUM STRESS; GENETIC PREDISPOSITION; GENETICS; HALOGENATION; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY; SECRETION (PROCESS); THYROID GLAND;

ANIMALS; CONGENITAL HYPOTHYROIDISM; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENETIC PREDISPOSITION TO DISEASE; HALOGENATION; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; THYROGLOBULIN; THYROID GLAND;

EID: 84957801406     PISSN: None     EISSN: 0163769X     Source Type: Journal    
DOI: 10.1210/er.2015-1090     Document Type: Review

References (284)

1. Pharoah PO, Buttfield IH, Hetzel BS. Neurological damage to the fetus resulting from severe iodine deficiency during pregnancy. Lancet. 1971;1:308-310.
2. Frati L, Bilstad J, Edelhoch H, Rall JE, Salvatore G. Biosynthesis of the 27 S thyroid iodoprotein. Arch Biochem Biophys. 1974;162:126-134.
3. Lee J, Di Jeso B, Arvan P. The cholinesterase-like domain of thyroglobulin functions as an intramolecular chaperone. J Clin Invest. 2008;118:2950-2958.
4. Novinec M, Kordis D, Turk V, Lenarcic B. Diversity and evolution of the thyroglobulin type-1 domain superfamily. Mol Biol Evol. 2006;23:744-755.
5. Takagi Y, Omura T, Go M. Evolutionary origin of thyroglobulin by duplication of esterase gene. FEBS Lett. 1991; 282:17-22.
6. Helenius A, Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem. 2004;73:1019-1049.
7. Hebert DN, Garman SC, Molinari M. The glycan code of the endoplasmic reticulum: asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol. 2005;15:364-370.
8. Malthièry Y, Marriq C, Bergé-Lefranc JL, et al. Thyroglobulin structure and function: recent advances. Biochimie. 1989;71:195-209.
9. Kim PS, Arvan P. Folding and assembly of newly synthesized thyroglobulin occurs in a pre-Golgi compartment. J Biol Chem. 1991;266:12412-12418.
10. Di Jeso B, Ulianich L, Pacifico F, et al. Folding of thyroglobulin in the calnexin/calreticulin pathway and its alteration by loss of Ca2+ from the endoplasmic reticulum. Biochem J. 2003;370:449-458.
11. Izumi M, Larsen PR. Triiodothyronine, thyroxine, and iodine in purified thyroglobulin from patients with Graves' disease. J Clin Invest. 1977;59:1105-1112.
12. Ogawara H, Bilstad JM, Cahnmann HJ. Iodoamino acid distribution in thyroglobulin iodinated in vivo and in vitro. Biochim Biophys Acta. 1972;257:339-349.
13. Rolland M, Montfort MF, Valenta L, Lissitzky S. Iodoamino acid composition of the thyroglobulin of normal and diseased thyroid glands. Comparison with in vitro iodinated thyroglobulin. Clin Chim Acta. 1972;39:95-108.
14. Paris M, Laudet V. The history of a developmental stage: metamorphosis in chordates. Genesis. 2008;46:657-672.
15. Fredriksson G, Öfverholm T, Ericson LE. Electron-microscopic studies of iodine-binding and peroxidase activity in the endostyle of the larval amphioxus (Branchiostoma lanceolatum). Cell Tissue Res. 1985;241:257-266.
16. Monaco F, Dominici R, Andreoli M, De Pirro R, Roche J. Thyroid hormone formation in thyroglobulin synthesized in the amphioxus (Branchiostoma lanceolatum pallas). Comp Biochem Physiol B. 1981;70:341-343.
17. Holland LZ, Albalat R, Azumi K, et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 2008;18:1100-1111.
18. Putnam NH, Butts T, Ferrier DE, et al. The amphioxus genome and the evolution of the chordate karyotype. Nature. 2008;453:1064-1071.
19. ParisM, Brunet F, MarkovGV, SchubertM, Laudet V. The amphioxus genome enlightens the evolution of the thyroid hormone signaling pathway. Dev Genes Evol. 2008;218: 667-680.
20. Paris M, Hillenweck A, Bertrand S. Active metabolism of thyroid hormone during metamorphosis of amphioxus. Integr Comp Biol. 2010;50:63-74.
21. Hodin J. Expanding networks: Signaling components in and a hypothesis for the evolution of metamorphosis. Integr Comp Biol. 2006;46:719-742.
22. Heyland A, Reitzel AM, Hodin J. Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea). Evol Dev. 2004;6:382-392.
23. Saito M, Seki M, Amemiya S, Yamasu K, Suyemitsu T, Ishihara K. Induction of metamorphosis in the sand dollar Peronella japonica by thyroid hormones. Dev Growth Differ. 1998;40:307-312.
24. Heyland A, Reitzel AM, Price DA, Moroz LL. Endogenous thyroid hormone synthesis in facultative planktotrophic larvae of the sand dollar Clypeaster rosaceus: implications for the evolutionary loss of larval feeding. Evol Dev. 2006;8: 568-579.
25. Eales JG. Iodine metabolism and thyroid-related functions in organisms lacking thyroid follicles: are thyroid hormones also vitamins? Proc Soc Exp Biol Med. 1997;214: 302-317.
26. Aloj S, Salvatore G, Roche J. Isolation and properties of a native subunit of lamprey thyroglobulin. J Biol Chem. 1967;242:3810-3814.
27. Borucinska JD, Tafur M. Comparison of histological features, and description of histopathological lesions in thyroid glands from three species of free-ranging sharks from the northwestern Atlantic, the blue shark, Prionace glauca (L.), the shortfin mako, Isurus oxyrhinchus Rafinesque, and the thresher, Alopias vulpinus (Bonnaterre). J Fish Dis. 2009;32:785-793.
28. Baas F, van Ommen GJ, Bikker H, Arnberg AC, de Vijlder JJ. The human thyroglobulin gene is over 300 kb long and contains introns of up to 64 kb. Nucleic Acids Res. 1986; 14:5171-5186.
29. Parma J, Christophe D, Pohl V, Vassart G. Structural organization of the 5' region of the thyroglobulin gene. Evidence for intron loss and "exonization" during evolution. J Mol Biol. 1987;196:769-779.
30. Mendive FM, Rivolta CM, Moya CM, Vassart G, Targovnik HM. Genomic organization of the human thyroglobulin gene: the complete intron-exon structure. Eur J Endocrinol. 2001;145:485-496.
31. Brocas H, Christophe D, Pohl V, Vassart G. Cloning of human thyroglobulin complementary DNA. FEBS Lett. 1982;137:189-192.
32. Malthiéry Y, Lissitzky S. Primary structure of human thyroglobulin deduced from the sequence of its 8448-base complementary DNA. Eur J Biochem. 1987;165:491-498.
33. van de Graaf SA, Ris-Stalpers C, Pauws E, Mendive FM, Targovnik HM, de Vijlder JJ. Up to date with human thyroglobulin. J Endocrinol. 2001;170:307-321.
34. Mercken L, Simons MJ, Swillens S, Massaer M, Vassart G. Primary structure of bovine thyroglobulin deduced from the sequence of its 8, 431-base complementary DNA. Nature. 1985;316:647-651.
35. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol. 1995;247: 536-540.
36. Molina F, Bouanani M, Pau B, Granier C. Characterization of the type-1 repeat from thyroglobulin, a cysteine-rich module found in proteins from different families. Eur J Biochem. 1996;240:125-133.
37. Lenarcic B, Bevec T. Thyropins-new structurally related proteinase inhibitors. Biol Chem. 1998;379:105-111.
38. Lenarcic B, Krishnan G, Borukhovich R, Ruck B, Turk V, Moczydlowski E. Saxiphilin, a saxitoxin-binding protein with two thyroglobulin type 1 domains, is an inhibitor of papain-like cysteine proteinases. J Biol Chem. 2000;275: 15572-15577.
39. Bevec T, Stoka V, Pungercic G, Dolenc I, Turk V. Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J Exp Med. 1996;183:1331-1338.
40. Lenarcic B, Turk V. Thyroglobulin type-1 domains in equistatin inhibit both papain-like cysteine proteinases and cathepsin D. J Biol Chem. 1999;274:563-566.
41. Meh P, Pavsic M, Turk V, Baici A, Lenarcic B. Dual concentration-dependent activity of thyroglobulin type-1 domain of testican: specific inhibitor and substrate of cathepsin L. Biol Chem. 2005;386:75-83.
42. Galesa K, Pain R, Jongsma MA, Turk V, Lenarcic B. Structural characterization of thyroglobulin type-1 domains of equistatin. FEBS Lett. 2003;539:120-124.
43. Yamashita M, Konagaya S. A novel cysteine protease inhibitor of the egg of chum salmon, containing a cysteinerich thyroglobulin-like motif. J Biol Chem. 1996;271: 1282-1284.
44. Bocock JP, Edgell CJ, Marr HS, Erickson AH. Human proteoglycan testican-1 inhibits the lysosomal cysteine protease cathepsin L. Eur J Biochem. 2003;270:4008-4015.
45. Durkin ME, Chakravarti S, Bartos BB, Liu SH, Friedman RL, Chung AE. Amino acid sequence and domain structure of entactin. Homology with epidermal growth factor precursor and low density lipoprotein receptor. J Cell Biol. 1988;107:2749-2756.
46. Headey SJ, Keizer DW, Yao S, et al. C-terminal domain of insulin-like growth factor (IGF) binding protein-6: structure and interaction with IGF-II. Mol Endocrinol. 2004; 18:2740-2750.
47. Stumptner-Cuvelette P, Benaroch P. Multiple roles of the invariant chain inMHCclass II function. Biochim Biophys Acta. 2002;1542:1-13.
48. Litvinov SV, Balzar M, Winter MJ, et al. Epithelial cell adhesion molecule (Ep-CAM) modulates cell-cell interactions mediated by classic cadherins. J Cell Biol. 1997;139: 1337-1348.
49. Guillemot JC, Naspetti M, Malergue F, Montcourrier P, Galland F, Naquet P. Ep-CAM transfection in thymic epithelial cell lines triggers the formation of dynamic actinrich protrusions involved in the organization of epithelial cell layers. Histochem Cell Biol. 2001;116:371-378.
50. Dunn JT, Dunn AD. The importance of thyroglobulin structure for thyroid hormone biosynthesis. Biochimie. 1999;81:505-509.
51. Lamas L, Anderson PC, Fox JW, Dunn JT. Consensus sequences for early iodination and hormonogenesis in humanthyroglobulin. J BiolChem. 1989;264:13541-13545.
52. Guncar G, Pungercic G, Klemencic I, Turk V, Turk D. Crystal structure of MHC class II-associated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsinsLand S.EMBOJ. 1999; 18:793-803.
53. Neumann GM, Bach LA. The N-terminal disulfide linkages ofhumaninsulin-like growth factor-binding protein-6 (hIGFBP-6) and hIGFBP-1 are different as determined by mass spectrometry. J Biol Chem. 1999;274:14587-14594.
54. Chong JM, Speicher DW. Determination of disulfide bond assignments and N-glycosylation sites of the human gastrointestinal carcinoma antigen GA733-2 (CO17-1A, EGP, KS1-4, KSA, and Ep-CAM). J Biol Chem. 2001;276:5804-5813.
55. Lee J, Di Jeso B, Arvan P. Maturation of thyroglobulin protein region I. J Biol Chem. 2011;286:33045-33052.
56. Lee J, Arvan P. Repeat motif-containing regions within thyroglobulin. J Biol Chem. 2011;286:26327-26333.
57. Südhof TC, Goldstein JL, Brown MS, Russell DW. The LDL receptor gene: a mosaic of exons shared with different proteins. Science. 1985;228:815-822.
58. Chiva C, Barthe P, Codina A, et al. Synthesis and NMR structure of p41icf, a potent inhibitor of human cathepsin L. J Am Chem Soc. 2003;125:1508-1517.
59. Dunn AD, Crutchfield HE, Dunn JT. Thyroglobulin processing by thyroidal proteases. Major sites of cleavage by cathepsins B, D, and L. J Biol Chem. 1991;266:20198-20204.
60. Gentile F, Salvatore G. 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. 1993;218:603-621.
61. Yang SX, Pollock HG, Rawitch AB. Glycosylation in human thyroglobulin: location of the N-linked oligosaccharide units and comparison with bovine thyroglobulin. Arch Biochem Biophys. 1996;327:61-70.
62. ConteM, Arcaro A, D'Angelo D, et al. Asingle chondroitin 6-sulfate oligosaccharide unit at Ser-2730 of human thyroglobulin enhances hormone formation and limits proteolytic accessibility at the carboxyl terminus: potential insights into thyroid homeostasis and autoimmunity. J Biol Chem. 2006;281:22200-22211.
63. Pungercic G, Dolenc I, Dolinar M, et al. Individual recombinant thyroglobulin type-1 domains are substrates for lysosomal cysteine proteinases. Biol Chem. 2002;383:1809-1812.
64. Dedieu A, Gaillard JC, Pourcher T, Darrouzet E, Armengaud J. Revisiting iodination sites in thyroglobulin with an organ-oriented shotgun strategy. J Biol Chem. 2011;286: 259-269.
65. Hall N, Pain A, BerrimanM, et al. Sequence of Plasmodium falciparum chromosomes 1, 3-9 and 13. Nature. 2002; 419:527-531.
66. Schumacher M, Camp S, Maulet Y, et al. Primary structure of Torpedo californica acetylcholinesterase deduced from its cDNA sequence. Nature. 1986;319:407-409.
67. Levitt M, Chothia C. Structural patterns in globular proteins. Nature. 1976;261:552-558.
68. Ollis DL, Cheah E, Cygler M, et al. Theα/β hydrolase fold. Protein Eng. 1992;5:197-211.
69. Cygler M, Schrag JD, Sussman JL, et al. Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases, and related proteins. Protein Sci. 1993;2:366-382.
70. Dvir H, Silman I, Harel M, Rosenberry TL, Sussman JL. Acetylcholinesterase: from 3D structure to function. Chem Biol Interact. 2010;187:10-22.
71. Sussman JL, Harel M, Frolow F, et al. Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science. 1991;253: 872-879.
72. Bourne Y, Taylor P, Marchot P. Acetylcholinesterase inhibition by fasciculin: crystal structure of the complex. Cell. 1995;83:503-512.
73. Morel N, Leroy J, Ayon A, Massoulié J, Bon S. AcetylcholinesteraseHand T dimers are associated through the same contact. Mutations at this interface interfere with the Cterminal T peptide, inducing degradation rather than secretion. J Biol Chem. 2001;276:37379-37389.
74. Lee J, Wang X, Di Jeso B, Arvan P. The cholinesterase-like domain, essential in thyroglobulin trafficking for thyroid hormone synthesis, is required for protein dimerization. J Biol Chem. 2009;284:12752-12761.
75. Gilbert MM, Auld VJ. Evolution of clams (cholinesteraselike adhesion molecules): structure and function during development. Front Biosci. 2005;10:2177-2192.
76. De Jaco A, Comoletti D, King CC, Taylor P. Trafficking of cholinesterases and neuroligins mutant proteins. An association with autism. Chem Biol Interact. 2008;175:349-351.
77. Lambert C, Léonard N, De Bolle X, Depiereux E. ESyPred3D: prediction of proteins 3D structures. Bioinformatics. 2002;18:1250-1256.
78. Wang X, Lee J, Di Jeso B, et al. Cis and trans actions of the Cholinesterase-Like domain within the thyroglobulin dimer. J Biol Chem. 2010;285:17564-17573.
79. MacPhee-Quigley K, Vedvick TS, Taylor P, Taylor SS. Profile of the disulfide bonds in acetylcholinesterase. J Biol Chem. 1986;261:13565-13570.
80. Richardson JS. The anatomy and taxonomy of protein structure. Adv Protein Chem. 1981;34:167-339.
81. Silman I, Sussman JL. Acetylcholinesterase: how is structure related to function? Chem Biol Interact. 2008;175: 3-10.
82. Park YN, Arvan P. The acetylcholinesterase homology region is essential for normal conformational maturation and secretion of thyroglobulin. J Biol Chem. 2004;279: 17085-17089.
83. Taurog A, Dorris ML, Doerge DR. Mechanism of simultaneous iodination and coupling catalyzed by thyroid peroxidase. Arch Biochem Biophys. 1996;330:24-32.
84. Dunn AD, Corsi CM, Myers HE, Dunn JT. Tyrosine 130 is an important outer ring donor for thyroxine formation in thyroglobulin. J Biol Chem. 1998;273:25223-25229.
85. Gavaret JM, Nunez J, Cahnmann HJ. Formation of dehydroalanine residues during thyroid hormone synthesis in thyroglobulin. J Biol Chem. 1980;255:5281-5285.
86. Gavaret JM, Cahnmann HJ, Nunez J. Thyroid hormone synthesis in thyroglobulin. The mechanism of the coupling reaction. J Biol Chem. 1981;256:9167-9173.
87. Gentile F, Ferranti P, Mamone G, Malorni A, Salvatore G. Identification of hormonogenic tyrosines in fragment 1218-1591 of bovine thyroglobulin by mass spectrometry. J Biol Chem. 1997;272:639-646.
88. Ohmiya Y, Hayashi H, Kondo T, Kondo Y. Location of dehydroalanine residues in the amino acid sequence of bovine thyroglobulin. Identification of "donor" tyrosine sites for hormonogenesis in thyroglobulin. J Biol Chem. 1990; 265:9066-9071.
89. Rolland M, Montfort MF, Lissitzky S. Efficiency of thyroglobulin as a thyroid hormone-forming protein. Biochim Biophys Acta. 1973;303:338-347.
90. Maurizis JC, Marriq C, Michelot J, Rolland M, Lissitzky S. Thyroid peroxidase-induced thyroid hormone synthesis in relation to thyroglobulin structure. FEBS Lett. 1979;102: 82-86.
91. Gavaret JM, Dème D, Nunez J, Salvatore G. Sequential reactivity of tyrosyl residues of thyroglobulin upon iodination catalyzed by thyroid peroxidase. J BiolChem. 1977; 252:3281-3285.
92. Van Zyl A, Edelhoch H. The properties of thyroglobulin. XV. The function of the protein in the control of diiodotyrosine synthesis. J Biol Chem. 1967;242:2423-2427.
93. de Vijlder JJ, den Hartog MT. Anionic iodotyrosine residues are required for iodothyronine synthesis. Eur J Endocrinol. 1998;138:227-231.
94. Lamas L, Taurog A, Salvatore G, Edelhoch H. Preferential synthesis of thyroxine from early iodinated tyrosyl residues in thyroglobulin. J Biol Chem. 1974;249:2732-2737.
95. Palumbo G, Gentile F, Condorelli GL, Salvatore G. The earliest site of iodination in thyroglobulin is residue number 5. J Biol Chem. 1990;265:8887-8892.
96. Dunn JT, Anderson PC, Fox JW, et al. The sites of thyroid hormone formation in rabbit thyroglobulin. J Biol Chem. 1987;262:16948-16952.
97. Cetrangolo GP, Arcaro A, Lepore A, et al. Hormonogenic donor Tyr2522 of bovine thyroglobulin. Insight into preferential T3 formation at thyroglobulin carboxyl terminus at low iodination level. Biochem Biophys Res Commun. 2014;450:488-493.
98. Sorimachi K, Ui N. Comparison of the iodoamino acid distribution in various preparations of hog thyroglobulin with different iodine content and subunit structure. Biochim Biophys Acta. 1974;342:30-40.
99. Fassler CA, Dunn JT, Anderson PC, et al. Thyrotropin alters the utilization of thyroglobulin's hormonogenic sites. J Biol Chem. 1988;263:17366-17371.
100. Di Jeso B, Liguoro D, Ferranti P, et al. Modulation of the carbohydrate moiety of thyroglobulin by thyrotropin and calcium in Fisher rat thyroid line-5 cells. J Biol Chem. 1992;267:1938-1944.
101. Larsen PR, Zavacki AM. The role of the iodothyronine deiodinases in the physiology and pathophysiology of thyroid hormone action. Eur Thyroid J. 2012;1:232-242.
102. Salvatore D, Tu H, Harney JW, Larsen PR. Type 2 iodothyronine deiodinase is highly expressed in human thyroid. J Clin Invest. 1996;98:962-968.
103. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev. 2002;23:38-89.
104. Nishikawa M, Toyoda N, Yonemoto T, et al. Quantitative measurements for type 1 deiodinase messenger ribonucleic acid in human peripheral blood mononuclear cells: mechanism of the preferential increase of T3 in hyperthyroid Graves' disease. Biochem Biophys Res Commun. 1998; 250:642-646.
105. Ishii H, Inada M, Tanaka K, et al. Triiodothyronine generation from thyroxine in human thyroid: enhanced conversion in Graves' thyroid tissue. J Clin Endocrinol Metab. 1981;52:1211-1217.
106. Toyoda N, Nishikawa M, Horimoto M, et al. Graves' immunoglobulinGstimulates iodothyronine 5'-deiodinating activity in FRTL-5 rat thyroid cells. J Clin Endocrinol Metab. 1990;70:1506-1511.
107. Palumbo G. Thyroid hormonogenesis. Identification of a sequence containing iodophenyl donor site(s) in calf thyroglobulin. J Biol Chem. 1987;262:17182-17188.
108. Cahnmann HJ, Pommier J, Nunez J. Spatial requirement for coupling of iodotyrosine residues to form thyroid hormones. Proc Natl Acad Sci USA. 1977;74:5333-5335.
109. Marriq C, Lejeune PJ, Venot N, Vinet L. Hormone formation in the isolated fragment 1-171 of human thyroglobulin involves the couple tyrosine 5 and tyrosine 130. Mol Cell Endocrinol. 1991;81:155-164.
110. Asunción M, Ingrassia R, Escribano J, et al. Efficient thyroid hormone formation by in vitro iodination of a segment of rat thyroglobulin fused to Staphylococcal protein A. FEBS Lett. 1992;297:266-270.
111. Dunn AD, Crutchfield HE, Dunn JT. Proteolytic processing of thyroglobulin by extracts of thyroid lysosomes. Endocrinology. 1991;128:3073-3080.
112. Tepel C, Brömme D, Herzog V, Brix K. Cathepsin K in thyroid epithelial cells: sequence, localization and possible function in extracellular proteolysis of thyroglobulin. J Cell Sci. 2000;113:4487-4498.
113. Jordans S, Jenko-Kokalj S, Kühl NM, et al. Monitoring compartment-specific substrate cleavage by cathepsins B, K, L, and S at physiologicalpHand redox conditions. BMC Biochem. 2009;10:23.
114. Rousset B, Selmi S, Bornet H, Bourgeat P, Rabilloud R, Munari-Silem Y. Thyroid hormone residues are released from thyroglobulin with only limited alteration of the thyroglobulin structure. J Biol Chem. 1989;264:12620-12626.
115. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 2001;106:157-169.
116. Jaiswal JK, Andrews NW, Simon SM. Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J Cell Biol. 2002;159:625-635.
117. Berndorfer U, Wilms H, Herzog V. Multimerization of thyroglobulin (TG) during extracellular storage: isolation of highly cross-linked TG from human thyroids. J Clin Endocrinol Metab. 1996;81:1918-1926.
118. Herzog V, Berndorfer U, Saber Y. Isolation of insoluble secretory product from bovine thyroid: extracellular storage of thyroglobulin in covalently cross-linked form. J Cell Biol. 1992;118:1071-1083.
119. Baudry N, Lejeune PJ, DelomF, Vinet L, Carayon P, Mallet B. Role of multimerized porcine thyroglobulin in iodine storage. Biochem Biophys Res Commun. 1998;242:292-296.
120. Dunn JT, Kim PS, Dunn AD. Favored sites for thyroid hormone formation on the peptide chains of human thyroglobulin. J Biol Chem. 1982;257:88-94.
121. Dunn JT, Kim PS, Dunn AD, Heppner DG Jr, Moore RC. The role of iodination in the formation of hormone-rich peptides from thyroglobulin. J Biol Chem. 1983;258: 9093-9099.
122. Berg G, Björkman U, Ekholm R. The structure of newly synthesized intracellular thyroglobulin molecules. Mol Cell Endocrinol. 1980;20:87-98.
123. Di Jeso B, Pereira R, Consiglio E, Formisano S, Satrustegui J, Sandoval IV. Demonstration of a Ca2+ requirement for thyroglobulin dimerization and export to the golgi complex. Eur J Biochem. 1998;252:583-590.
124. Di Jeso B, Park YN, Ulianich L, et al. Mixed-disulfide folding intermediates between thyroglobulin and endoplasmic reticulum resident oxidoreductases ERp57 and protein disulfide isomerase. Mol Cell Biol. 2005;25:9793-9805.
125. Reddy PS, Corley RB. Assembly, sorting, and exit of oligomeric proteins from the endoplasmic reticulum. BioEssays. 1998;20:546-554.
126. Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, Jones DT. Protein structure prediction servers at University College London. Nucleic Acids Res. 2005;33:W36-W38.
127. Kim PS, Ding M, Menon S, et al. A missense mutation G2320R in the thyroglobulin gene causes non-goitrous congenital primary hypothyroidism in the WIC-rdw rat. Mol Endocrinol. 2000;14:1944-1953.
128. Hishinuma A, Furudate S, Oh-Ishi M, Nagakubo N, Namatame T, Ieiri T. A novel missense mutation (G2320R) in thyroglobulin causes hypothyroidism in rdw rats. Endocrinology. 2000;141:4050-4055.
129. Kim PS, Hossain SA, Park YN, Lee I, Yoo SE, Arvan P. A single amino acid change in the acetylcholinesterase-like domain of thyroglobulin causes congenital goiter with hypothyroidism in the cog/cog mouse: a model of human endoplasmic reticulum storage diseases. Proc Natl Acad Sci USA. 1998;95:9909-9913.
130. Kim PS, Kwon OY, Arvan P. An endoplasmic reticulum storage disease causing congenital goiter with hypothyroidism. J Cell Biol. 1996;133:517-527.
131. Hishinuma A, Takamatsu J, Ohyama Y, et al. Two novel cysteine substitutions(C1263Rand C1995S) of thyroglobulin cause a defect in intracellular transport of thyroglobulin in patients with congenital goiter and the variant type of adenomatous goiter. J Clin Endocrinol Metab. 1999; 84:1438-1444.
132. Hishinuma A, Fukata S, Nishiyama S, et al. Haplotype analysis reveals founder effects of thyroglobulin gene mutations C1058R and C1977S in Japan. J Clin Endocrinol Metab. 2006;91:3100-3104.
133. D'Alessio C, Caramelo JJ, Parodi AJ. UDP-GlC:glycoprotein glucosyltransferase-glucosidase II, the ying-yang of the ER quality control. Semin Cell Dev Biol. 2010;21:491-499.
134. Imperiali B, O'Connor SE. Effect of N-linked glycosylation on glycopeptide and glycoprotein structure. Curr Opin Chem Biol. 1999;3:643-649.
135. Ferris SP, Jaber NS, Molinari M, Arvan P, Kaufman RJ. UDP-glucose:glycoprotein glucosyltransferase (UGGT1) promotes substrate solubility in the endoplasmic reticulum. Mol Biol Cell. 2013;24:2597-2608.
136. Flynn GC, Pohl J, Flocco MT, Rothman JE. Peptide-binding specificity of the molecular chaperone BiP. Nature. 1991;353:726-730.
137. Blond-Elguindi S, Cwirla SE, Dower WJ, et al. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell. 1993; 75:717-728.
138. Wang N, Daniels R, Hebert DN. The cotranslational maturation of the type Imembraneglycoprotein tyrosinase: the heat shock protein 70 system hands offto the lectin-based chaperone system. Mol Biol Cell. 2005;16:3740-3752.
139. Molinari M, Helenius A. Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science. 2000;288:331-333.
140. Hammond C, Helenius A. Folding of VSV G protein: sequential interaction with BiP and calnexin. Science. 1994; 266:456-458.
141. HebertDN, Foellmer B, Helenius A. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell. 1995;81:425-433.
142. Hebert DN, Foellmer B, Helenius A. Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes. EMBO J. 1996;15:2961-2968.
143. Ou WJ, Cameron PH, Thomas DY, Bergeron JJ. Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature. 1993;364:771-776.
144. Gidalevitz T, Stevens F, Argon Y. Orchestration of secretory protein folding by ER chaperones. Biochim Biophys Acta. 2013;1833:2410-2424.
145. Molinari M, Galli C, Vanoni O, Arnold SM, Kaufman RJ. Persistent glycoprotein misfolding activates the glucosidase II/UGT1-driven calnexin cycle to delay aggregation and loss of folding competence. Mol Cell. 2005;20:503-512.
146. Soldà T, Galli C, Kaufman RJ, Molinari M. Substratespecific requirements for UGT1-dependent release from calnexin. Mol Cell. 2007;27:238-249.
147. Pearse BR, Hebert DN. Lectin chaperones help direct the maturation of glycoproteins in the endoplasmic reticulum. Biochim Biophys Acta. 2010;1803:684-693.
148. Taylor SC, Thibault P, Tessier DC, Bergeron JJ, Thomas DY. Glycopeptide specificity of the secretory protein folding sensor UDP-glucose glycoprotein:glucosyltransferase. EMBO Rep. 2003;4:405-411.
149. Pearse BR, Gabriel L, Wang N, Hebert DN. A cell-based reglucosylation assay demonstrates the role of GT1 in the quality control of a maturing glycoprotein. J Cell Biol. 2008;181:309-320.
150. Caramelo JJ, Castro OA, Alonso LG, De Prat-Gay G, Parodi AJ. UDP-Glc:glycoprotein glucosyltransferase recognizes structured and solvent accessible hydrophobic patches in molten globule-like folding intermediates. Proc Natl Acad Sci USA. 2003;100:86-91.
151. Caramelo JJ, Castro OA, de Prat-Gay G, Parodi AJ. The endoplasmic reticulum glucosyltransferase recognizes nearly native glycoprotein folding intermediates. J Biol Chem. 2004;279:46280-46285.
152. Ritter C, Quirin K, Kowarik M, Helenius A. Minor folding defects trigger local modification of glycoproteins by the ER folding sensor GT. EMBO J. 2005;24:1730-1738.
153. Ritter C, Helenius A. Recognition of local glycoprotein misfolding by the ER folding sensor UDP-glucose:glycoprotein glucosyltransferase. Nat Struct Biol. 2000;7:278-280.
154. Peterson JR, Ora A, Van PN, Helenius A. Transient, lectinlike association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol Biol Cell. 1995;6: 1173-1184.
155. Spiro RG, Zhu Q, Bhoyroo V, Söling HD. Definition of the lectin-like properties of the molecular chaperone, calreticulin, and demonstration of its copurification with endomannosidase from rat liver Golgi. J Biol Chem. 1996;271: 11588-11594.
156. Vassilakos A, Michalak M, Lehrman MA, Williams DB. Oligosaccharide binding characteristics of the molecular chaperones calnexin and calreticulin. Biochemistry. 1998; 37:3480-3490.
157. Ware FE, Vassilakos A, Peterson PA, Jackson MR, Lehrman MA, Williams DB. The molecular chaperone calnexin binds Glc1Man9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J Biol Chem. 1995;270:4697-4704.
158. Wada I, Imai S, Kai M, Sakane F, Kanoh H. Chaperone function of calreticulin when expressed in the endoplasmic reticulum as the membrane-anchored and soluble forms. J Biol Chem. 1995;270:20298-20304.
159. Pieren M, Galli C, Denzel A, Molinari M. The use of calnexin and calreticulin by cellular and viral glycoproteins. J Biol Chem. 2005;280:28265-28271.
160. Schrag JD, Bergeron JJ, Li Y, et al. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell. 2001;8:633-644.
161. Baksh S, Michalak M. Expression of calreticulin in Escherichia coli and identification of its Ca2+ binding domains. J Biol Chem. 1991;266:21458-21465.
162. Daniels R, Kurowski B, Johnson AE, Hebert DN. N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell. 2003;11:79-90.
163. Hebert DN, Zhang JX, Chen W, Foellmer B, Helenius A. The number and location of glycans on influenza hemagglutinin determine folding and association with calnexin and calreticulin. J Cell Biol. 1997;139:613-623.
164. Danilczyk UG, Cohen-Doyle MF, Williams DB. Functional relationship between calreticulin, calnexin, and the endoplasmic reticulum luminal domain of calnexin. J Biol Chem. 2000;275:13089-13097.
165. Molinari M, Eriksson KK, Calanca V, et al. Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol Cell. 2004;13:125-135.
166. Oliver JD, van der Wal FJ, Bulleid NJ, High S. Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science. 1997;275:86-88.
167. Oliver JD, Roderick HL, Llewellyn DH, High S. ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol Biol Cell. 1999;10:2573-2582.
168. Zapun A, Darby NJ, Tessier DC, Michalak M, Bergeron JJ, Thomas DY. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J Biol Chem. 1998;273:6009-6012.
169. Frickel EM, Riek R, Jelesarov I, Helenius A, Wuthrich K, Ellgaard L. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc Natl Acad Sci USA. 2002;99:1954-1959.
170. Peaper DR, Wearsch PA, Cresswell P. Tapasin and ERp57 form a stable disulfide-linked dimer within theMHCclass I peptide-loading complex. EMBO J. 2005;24:3613-3623.
171. Peaper DR, Cresswell P. The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading. Proc Natl Acad Sci USA. 2008;105:10477-10482.
172. Peaper DR, Cresswell P. Regulation of MHC class I assembly and peptide binding. Annu Rev Cell Dev Biol. 2008;24:343-368.
173. Jessop CE, Tavender TJ, Watkins RH, Chambers JE, Bulleid NJ. Substrate specificity of the oxidoreductase ERp57 is determined primarily by its interaction with calnexin and calreticulin. J Biol Chem. 2009;284:2194-2202.
174. Denzel A, Molinari M, Trigueros C, et al. Early postnatal death and motor disorders in mice congenitally deficient in calnexin expression. Mol Cell Biol. 2002;22:7398-7404.
175. Mesaeli N, Nakamura K, Zvaritch E, et al. Calreticulin is essential for cardiac development. J Cell Biol. 1999;144: 857-868.
176. Soldà T, Garbi N, Hämmerling GJ, Molinari M. Consequences of ERp57 deletion on oxidative folding of obligate and facultative clients of the calnexin cycle. J Biol Chem. 2006;281:6219-6226.
177. Jessop CE, Chakravarthi S, Garbi N, Hämmerling GJ, Lovell S, Bulleid NJ. ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J. 2007;26:28-40.
178. Tadano-Aritomi K, Matsuda J, Fujimoto H, Suzuki K, Ishizuka I. Seminolipid and its precursor/degradative product, galactosylalkylacylglycerol, in the testis of saposin A-and prosaposin-deficient mice. J Lipid Res. 2003;44:1737-1743.
179. Kishimoto Y, Hiraiwa M, O'Brien JS. Saposins: structure, function, distribution, and molecular genetics. J Lipid Res. 1992;33:1255-1267.
180. Pearse BR, Tamura T, Sunryd JC, Grabowski GA, Kaufman RJ, Hebert DN. The role of UDP-Glc:glycoprotein glucosyltransferase 1 in the maturation of an obligate substrate prosaposin. J Cell Biol. 2010;189:829-841.
181. Moremen KW. Golgi alpha-mannosidase II deficiency in vertebrate systems: implications for asparagine-linked oligosaccharide processing in mammals. Biochim Biophys Acta. 2002;1573:225-235.
182. Ruddock LW, Molinari M. N-Glycan processing in ER quality control. J Cell Sci. 2006;119:4373-4380.
183. Sousa MC, Ferrero-Garcia MA, Parodi AJ. Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. Biochemistry. 1992;31:97-105.
184. Stigliano ID, Alculumbre SG, Labriola CA, Parodi AJ, D'Alessio C. Glucosidase II and N-glycan mannose content regulate the half-lives of monoglucosylated species in vivo. Mol Biol Cell. 2011;22:1810-1823.
185. Fagioli C, Sitia R. Glycoprotein quality control in the endoplasmic reticulum. Mannose trimming by endoplasmic reticulum mannosidase I times the proteasomal degradation of unassembled immunoglobulin subunits. J Biol Chem. 2001;276:12885-12892.
186. Suh K, Bergmann JE, Gabel CA. Selective retention of monoglucosylated high mannose oligosaccharides by a class of mutant vesicular stomatitis virus G proteins. J Cell Biol. 1989;108:811-819.
187. Trombetta ES, Parodi AJ. Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol. 2003;19:649-676.
188. Tokunaga F, Brostrom C, Koide T, Arvan P. Endoplasmic reticulum (ER)-associated degradation of misfolded N-linked glycoproteins is suppressed upon inhibition of ER mannosidase I. J Biol Chem. 2000;275:40757-40764.
189. Hoseki J, Ushioda R, Nagata K. Mechanism and components of endoplasmic reticulum-associated degradation. J Biochem. 2010;147:19-25.
190. Molinari M, Calanca V, Galli C, Lucca P, Paganetti P. Role ofEDEMin the release of misfolded glycoproteins from the calnexin cycle. Science. 2003;299:1397-1400.
191. Christianson JC, Shaler TA, Tyler RE, Kopito RR. OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat Cell Biol. 2008;10:272-282.
192. Hosokawa N, Kamiya Y, Kamiya D, Kato K, Nagata K. Human OS-9, a lectin required for glycoprotein endoplasmic reticulum-associated degradation, recognizes mannosetrimmed N-glycans. J Biol Chem. 2009;284:17061-17068.
193. Avezov E, Frenkel Z, Ehrlich M, Herscovics A, Lederkremer GZ. Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for N-glycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Mol Biol Cell. 2008;19:216-225.
194. Herscovics A, Romero PA, Tremblay LO. The specificity of the yeast and human class I ER α 1, 2-mannosidases involved in ER quality control is not as strict previously reported. Glycobiology. 2002;12:14G-15G.
195. Sevier CS, Kaiser CA. Formation and transfer of disulphide bonds in living cells. Nat Rev Mol Cell Biol. 2002;3:836-847.
196. Hatahet F, Ruddock LW. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal. 2009;11:2807-2850.
197. Appenzeller-Herzog C, Ellgaard L. The human PDI family: versatility packed into a single fold. Biochim Biophys Acta. 2008;1783:535-548.
198. Feige MJ, Hendershot LM. Disulfide bonds in ER protein folding and homeostasis. Curr Opin Cell Biol. 2011;23: 167-175.
199. Jessop CE, WatkinsRH, Simmons JJ, TasabM, Bulleid NJ. Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J Cell Sci. 2009;122:4287-4295.
200. Di Jeso B, Morishita Y, Treglia AS, et al. Transient covalent interactions of newly synthesized thyroglobulin with oxidoreductases of the endoplasmic reticulum. J Biol Chem. 2014;289:11488-11496.
201. Meunier L, Usherwood YK, Chung KT, Hendershot LM. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell. 2002;13:4456-4469.
202. Pirneskoski A, Klappa P, Lobell M, et al. Molecular characterization of the principal substrate binding site of the ubiquitous folding catalyst protein disulfide isomerase. J Biol Chem. 2004;279:10374-10381.
203. Netzer WJ, Hartl FU. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature. 1997;388:343-349.
204. Jaenicke R. Stability and folding of domain proteins. Prog Biophys Mol Biol. 1999;71:155-241.
205. Jansens A, van Duijn E, Braakman I. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science. 2002;2401-2403.
206. Kurniawan ND, Aliabadizadeh K, Brereton IM, Kroon PA, Smith R. NMR structure and backbone dynamics of a concatemer of epidermal growth factor homology modules of the human low-density lipoprotein receptor. J Mol Biol. 2001;311:341-356.
207. Oka OB, PringleMA, Schopp IM, Braakman I, Bulleid NJ. ERdj5 is the ER reductase that catalyzes the removal of non-native disulfides and correct folding of the LDL receptor. Mol Cell. 2013;50:793-804.
208. Dong M, Bridges JP, Apsley K, Xu Y, Weaver TE. ERdj4 and ERdj5 are required for endoplasmic reticulum-associated protein degradation of misfolded surfactant protein C. Mol Biol Cell. 2008;19:2620-2630.
209. Ushioda R, Hoseki J, Araki K, Jansen G, Thomas DY, Nagata K. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science. 2008; 321:569-572.
210. HagiwaraM, Maegawa K, SuzukiM, et al. Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol Cell. 2011;41:432-444.
211. Riemer J, Appenzeller-Herzog C, Johansson L, Bodenmiller B, Hartmann-Petersen R, Ellgaard L. A luminal flavoprotein in endoplasmic reticulum-associated degradation. Proc Natl Acad Sci USA. 2009;106:14831-14836.
212. Rastogi MV, LaFranchi SH. Congenital hypothyroidism. Orphanet J Rare Dis. 2010;5:17.
213. De Felice M, Di Lauro R. Minireview: intrinsic and extrinsic factors in thyroid gland development: an update. Endocrinology. 2011;152:2948-2956.
214. Portulano C, Paroder-Belenitsky M, Carrasco N. The Na+/I-symporter (NIS): mechanism and medical impact. Endocr Rev. 2014;35:106-149.
215. Bizhanova A, Kopp P. Genetics and phenomics of Pendred syndrome. Mol Cell Endocrinol. 2010;322:83-90.
216. Ris-Stalpers C, Bikker H. Genetics and phenomics of hypothyroidism and goiter due to TPO mutations. Mol Cell Endocrinol. 2010;322:38-43.
217. Grasberger H. Defects of thyroidal hydrogen peroxide generation in congenital hypothyroidism. Mol Cell Endocrinol. 2010;322:99-106.
218. MorenoJC, Visser TJ. Geneticsandphenomicsof hypothyroidism and goiter due to iodotyrosine deiodinase (DEHAL1) gene mutations. Mol Cell Endocrinol. 2010;322:91-98.
219. Targovnik HM, Esperante SA, Rivolta CM. Genetics and phenomics of hypothyroidism and goiter due to thyroglobulin mutations. Mol Cell Endocrinol. 2010;322:44-55.
220. Targovnik HM, Citterio CE, Rivolta CM. Thyroglobulin gene mutations in congenital hypothyroidism. Horm Res Paediatr. 2011;75:311-321.
221. Schell T, Kulozik AE, HentzeMW. Integration of splicing, transport and translation to achievemRNAquality control by the nonsense-mediated decay pathway. Genome Biol. 2002;3:REVIEWS1006.
222. Thermann R, Neu-Yilik G, Deters A, et al. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 1998;17:3484-3494.
223. Zhang J, Sun X, Qian Y, LaDuca JP, Maquat LE. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerasemRNA:a possible link between nuclear splicing and cytoplasmic translation. Mol Cell Biol. 1998;18:5272-5283.
224. Bhuvanagiri M, Schlitter AM, Hentze MW, Kulozik AE. NMD: RNA biology meets human genetic medicine. Biochem J. 2010;430:365-377.
225. DietzHC, ValleD, FrancomanoCA, KendziorRJJr, PyeritzRE, Cutting GR. The skipping of constitutive exons in vivo induced by nonsense mutations. Science. 1993;259:680-683.
226. González-Sarmiento R, Corral J, Mories MT, Corrales JJ, Miguel-Velado E, Miralles-Garcia JM. Monoallelic deletion in the 5' region of the thyroglobulin gene as a cause of sporadic nonendemic simple goiter. Thyroid. 2001;11:789-793.
227. Citterio CE, Rossetti LC, Souchon PF, et al. Novel mutational mechanism in the thyroglobulin gene: imperfect DNA inversion as a cause for hereditary hypothyroidism. Mol Cell Endocrinol. 2013;381:220-229.
228. van de Graaf SA, Ris-Stalpers C, Veenboer GJ, et al. A premature stopcodon in thyroglobulin messengerRNAresults in familial goiter and moderate hypothyroidism. J Clin Endocrinol Metab. 1999;84:2537-2542.
229. Pardo V, Vono-Toniolo J, Rubio IG, et al. The p. A2215D thyroglobulin gene mutation leads to deficient synthesis and secretion of the mutated protein and congenital hypothyroidism with wide phenotype variation. J Clin Endocrinol Metab. 2009;94:2938-2944.
230. Peteiro-Gonzalez D, Lee J, Rodriguez-Fontan J, et al. New insights into thyroglobulin pathophysiology revealed by the study of a family with congenital goiter. J Clin Endocrinol Metab. 2010;95:3522-3526.
231. de Vijlder JJ, van Voorthuizen WF, van Dijk JE, Rijnberk A, Tegelaers WH. Hereditary congenital goiter with thyroglobulin deficiency in a breed of goats. Endocrinology. 1978;102:1214-1222.
232. Niu DM, Hsu JH, Chong KW, et al. Six new mutations of the thyroglobulin gene discovered in Taiwanese children presenting with thyroid dyshormonogenesis. J Clin Endocrinol Metab. 2009;94:5045-5052.
233. Citterio CE, Coutant R, Rouleau S, et al. A new compound heterozygous for c.886C>T/c.2206C>T[p. R277X/p. Q717X] mutations in the thyroglobulin gene as a cause of foetal goitrous hypothyroidism. Clin Endocrinol (Oxf). 2011;74:533-535.
234. Citterio CE, Machiavelli GA, Miras MB, et al. New insights into thyroglobulin gene: molecular analysis of seven novel mutations associated with goiter and hypothyroidism. Mol Cell Endocrinol. 2013;365:277-291.
235. Targovnik HM, Medeiros-Neto G, Varela V, Cochaux P, Wajchenberg BL, Vassart G. A nonsense mutation causes human hereditary congenital goiter with preferential production of a 171-nucleotide-deleted thyroglobulin ribonucleic acid messenger. J Clin Endocrinol Metab. 1993;77: 210-215.
236. Mendive FM, Rivolta CM, González-Sarmiento R, Medeiros-Neto G, Targovnik HM. Nonsense-associated alternative splicing of the human thyroglobulin gene. Mol Diagn. 2005;9:143-149.
237. Machiavelli GA, Caputo M, Rivolta CM, et al. Molecular analysis of congenital goitres with hypothyroidism caused by defective thyroglobulin synthesis. Identification of a novel c.7006C > T[p. R2317X] mutation and expression of minigenes containing nonsense mutations in exon 7. Clin Endocrinol (Oxf). 2010;72:112-121.
238. Ieiri T, Cochaux P, Targovnik HM, et al. A 3' splice site mutation in the thyroglobulin gene responsible for congenital goiter with hypothyroidism. J Clin Invest. 1991; 88:1901-1905.
239. Targovnik HM, Vono J, Billerbeck AE, et al. A 138-nucleotide deletion in the thyroglobulin ribonucleic acid messenger in a congenital goiter with defective thyroglobulin synthesis. J Clin Endocrinol Metab. 1995;80:3356-3360.
240. Targovnik HM, Rivolta CM, Mendive FM, Moya CM, Vono J, Medeiros-Neto G. Congenital goiter with hypothyroidism caused by a 5' splice site mutation in the thyroglobulin gene. Thyroid. 2001;11:685-690.
241. Pardo V, Rubio IG, Knobel M, et al. Phenotypic variation among four family members with congenital hypothyroidism caused by two distinct thyroglobulin gene mutations. Thyroid. 2008;18:783-786.
242. Hermanns P, RefetoffS, Sriphrapradang C, et al. A clinically euthyroid child with a large goiter due to a thyroglobulin gene defect: clinical features and genetic studies. J Pediatr Endocrinol Metab. 2013;26:119-123.
243. Gutnisky VJ, Moya CM, Rivolta CM, et al. Two distinct compound heterozygous constellations (R277X/IVS34-1G>C and R277X/R1511X) in the thyroglobulin (TG) gene in affected individuals of a Brazilian kindred with congenital goiter and defective TG synthesis. J Clin Endocrinol Metab. 2004;89:646-657.
244. Rivolta CM, Targovnik HM. Molecular advances in thyroglobulin disorders. Clin Chim Acta. 2006;374:8-24.
245. Gass JN, Gifford NM, Brewer JW. Activation of an unfolded protein response during differentiation of antibodysecreting B cells. J Biol Chem. 2002;277:49047-49054.
246. Christis C, Fullaondo A, Schildknegt D, Mkrtchian S, Heck AJ, Braakman I. Regulated increase in folding capacity prevents unfolded protein stress in the ER. J Cell Sci. 2010; 123:787-794.
247. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011; 334:1081-1086.
248. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000;5:897-904.
249. Termine DJ, Moremen KW, Sifers RN. The mammalian UPR boosts glycoprotein ERAD by suppressing the proteolytic downregulation of ER mannosidase I. J Cell Sci. 2009;122:976-984.
250. Kouroku Y, Fujita E, Tanida I, et al. ER stress (PERK/eIF2α phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 2007;14:230-239.
251. Oyadomari S, Yun C, Fisher EA, et al. Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell. 2006;126:727-739.
252. Hollien J, Weissman JS. Decay of endoplasmic reticulumlocalized mRNAs during the unfolded protein response. Science. 2006;313:104-107.
253. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol. 2009;186:323-331.
254. Rutkowski DT, Arnold SM, Miller CN, et al. Adaptation to ER stress is mediated by differential stabilities of prosurvival and pro-apoptotic mRNAs and proteins. PLoS Biol. 2006;4:e374.
255. Lin JH, Li H, Yasumura D, et al. IRE1 signaling affects cell fate during the unfolded protein response. Science. 2007; 318:944-949.
256. Lin JH, Li H, Zhang Y, Ron D, Walter P. Divergent effects of PERK and IRE1 signaling on cell viability. PLoS One. 2009;4:e4170.
257. Han D, Lerner AG, Vande Walle L, et al. IRE1α kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell. 2009;138:562-575.
258. Tsang KY, Chan D, Bateman JF, Cheah KS. In vivo cellular adaptation to ER stress: survival strategies with doubleedged consequences. J Cell Sci. 2010;123:2145-2154.
259. Treglia AS, Turco S, Ulianich L, et al. Cell fate following ER stress: just a matter of "quo ante" recovery or death? Histol Histopathol. 2012;27:1-12.
260. Yang L, Carlson SG, McBurney D, Horton WE Jr. Multiple signals induce endoplasmic reticulum stress in both primary and immortalized chondrocytes resulting in loss of differentiation, impaired cell growth, and apoptosis. J Biol Chem. 2005;280:31156-31165.
261. HoMS, TsangKY, LoRL, etal. COL10A1nonsenseandframeshift mutations have a gain-of-function effect on the growth plate in human and mouse metaphyseal chondrodysplasia type Schmid. Hum Mol Genet. 2007;16:1201-1215.
262. Tsang KY, Chan D, Cheslett D, et al. Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol. 2007;5:e44.
263. Rajpar MH, McDermott B, Kung L, et al. Targeted induction of endoplasmic reticulum stress induces cartilage pathology. PLoS Genet. 2009;5:e1000691.
264. Firtina Z, Danysh BP, Bai X, Gould DB, Kobayashi T, Duncan MK. Abnormal expression of collagen IV in lens activates unfolded protein response resulting in cataract. J Biol Chem. 2009;284:35872-35884.
265. Ulianich L, Garbi C, Treglia AS, et al. ER stress is associated with dedifferentiation and an epithelial-to-mesenchymal transition-like phenotype inPCCl3 thyroid cells. J Cell Sci. 2008;121:477-486.
266. Kim PS, Arvan P. Endocrinopathies in the family of endoplasmic reticulum (ER) storage diseases: disorders of protein trafficking and the role of ER molecular chaperones. Endocr Rev. 1998;19:173-202.
267. Hebert DN, Molinari M. In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev. 2007;87:1377-1408.
268. Mayerhofer A, Amador AG, Beamer WG, Bartke A. Ultrastructural aspects of the goiter in cog/cog mice. J Hered. 1988;79:200-203.
269. Adkison LR, Taylor S, Beamer WG. Mutant gene-induced disorders of structure, function and thyroglobulin synthesis in congenital goitre (cog/cog) in mice. J Endocrinol. 1990;126:51-58.
270. Sakai Y, Yamashina S, Furudate SI. Missing secretory granules, dilated endoplasmic reticulum, and nuclear dislocation in the thyroid gland of rdw rats with hereditary dwarfism. Anat Rec. 2000;259:60-66.
271. Oh-Ishi M, Omori A, Kwon JY, Agui T, Maeda T, Furudate S. Detection and identification of proteins related to the hereditary dwarfism of the rdw rat. Endocrinology. 1998;139:1288-1299.
272. Umezu M, Fujimura T, Sugawara S, Kagabu S. Pituitary and serum levels of prolactin (PRL), thyroid stimulating hormone (TSH) and serum thyroxine (T4) in hereditary dwarf rats (rdw/rdw). Jikken Dobutsu. 1993;42:211-216.
273. Menon S, Lee J, Abplanalp WA, et al. Oxidoreductase interactions include a role for ERp72 engagement with mutant thyroglobulin from the rdw/rdw rat dwarf. J Biol Chem. 2007;282:6183-6191.
274. Baryshev M, Sargsyan E, Wallin G, et al. Unfolded protein response is involved in the pathology of human congenital hypothyroid goiter and rat non-goitrous congenital hypothyroidism. J Mol Endocrinol. 2004;32:903-920.
275. Kim PS, Lee J, Jongsamak P, et al. Defective protein folding and intracellular retention of thyroglobulin-R19K mutant as a cause of human congenital goiter. Mol Endocrinol. 2008;22:477-484.
276. Corral J, Martín C, Pérez R, et al. Thyroglobulin gene point mutation associated with non-endemic simple goitre. Lancet. 1993;341:462-464.
277. Pérez-Centeno C, González-Sarmiento R, Mories MT, Corrales JJ, Miralles-García JM. Thyroglobulin exon 10 gene point mutation in a patient with endemic goiter. Thyroid. 1996;6:423-427.
278. Vono-Toniolo J, Medeiros-Neto G, Kopp P. Three novel homozygous nucleotide substitutions in the TG gene in an inbred Brazilian kindred with congenital goiter and defective thyroglobulin synthesis. In: Proceedings from the Endocrine Society; June 19-22, 2002; San Francisco, CA; p 536 (Abstract P3-185).
279. Feldt-Rasmussen U, Hegedüs L, Perrild H, Rasmussen N, Hansen JM. Relationship between serum thyroglobulin, thyroid volume and serum TSH in healthy non-goitrous subjects and the relationship to seasonal variations in iodine intake. Thyroidology. 1989;1:115-118.
280. Izumi M, Larsen PR. Correlation of sequential changes in serum thyroglobulin, triiodothyronine, and thyroxine in patients with Graves' disease and subacute thyroiditis. Metabolism. 1978;27:449-460.
281. Hidaka Y, Nishi I, Tamaki H, et al. Differentiation of postpartum thyrotoxicosis by serum thyroglobulin: usefulness of a new multisite immunoradiometric assay. Thyroid. 1994;4:275-278.
282. Mazzaferri EL, Robbins RJ, Spencer CA, et al. Aconsensus report of the role of serum thyroglobulin as a monitoring method for low-risk patients with papillary thyroid carcinoma. J Clin Endocrinol Metab. 2003;88:1433-1441.
283. Targovnik HM, Edouard T, Varela V, et al. Two novel mutations in the thyroglobulin gene as cause of congenital hypothyroidism: identification a cryptic donor splice site in the exon 19. Mol Cell Endocrinol. 2012;348:313-321.
284. Citterio CE, MoralesCM, Bouhours-Nouet N, et al. Novel compound heterozygous thyroglobulin mutations c.745+1G>A/c.7036+2T>A associated with congenital goiter and hypothyroidism in a Vietnamese family: identification of a new cryptic 5 splice site in the exon 6. Mol Cell Endocrinol. 2015;404:102-112.