Disulfide bond formation and redox regulation in the Golgi apparatus.
Golgi
QSOX1
disulfide bonds
glycosyltransferases
mucins
redox regulation
secretory pathway
sialic acid
von Willebrand factor
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
06
09
2022
received:
06
08
2022
accepted:
24
09
2022
pubmed:
11
10
2022
medline:
30
11
2022
entrez:
10
10
2022
Statut:
ppublish
Résumé
Formation of disulfide bonds in secreted and cell-surface proteins involves numerous enzymes and chaperones abundant in the endoplasmic reticulum (ER), the first and main site for disulfide bonding in the secretory pathway. Although the Golgi apparatus is the major station after the ER, little is known about thiol-based redox activity in this compartment. QSOX1 and its paralog QSOX2 are the only known Golgi-resident enzymes catalyzing disulfide bonding. The localization of disulfide catalysts in an organelle downstream of the ER in the secretory pathway has long been puzzling. Recently, it has emerged that QSOX1 regulates particular glycosyltransferases, thereby influencing a central activity of the Golgi. Surprisingly, a few important disulfide-mediated multimerization events occurring in the Golgi were found to be independent of QSOX1. These multimerization events depend, however, on the low pH of the Golgi lumen and secretory granules. We compare and contrast disulfide-mediated multimerization in the ER vs. the Golgi to illustrate the variety of mechanisms controlling covalent supramolecular assembly of secreted proteins.
Identifiants
pubmed: 36214053
doi: 10.1002/1873-3468.14510
doi:
Substances chimiques
Proteins
0
Disulfides
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2859-2872Informations de copyright
© 2022 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Bulleid NJ, Ellgaard L. Multiple ways to make disulfides. Trends Biochem Sci. 2011;36:485-92. https://doi.org/10.1016/j.tibs.2011.05.004
Ellgaard L, McCaul N, Chatsisvili A, Braakman I. Co- and post-translational folding in the ER. Traffic. 2016;17:615-38. https://doi.org/10.1111/tra.12392
Hudson DA, Gannon SA, Thorpe C. Oxidative protein folding: from thiol-disulfide exchange reactions to the redox poise of the endoplasmic reticulum. Free Radic Biol Med. 2015;80:171-82. https://doi.org/10.1016/j.freeradbiomed.2014.07.037
Sevier CS, Qu H, Heldman N, Gross E, Fass D, Kaiser CA. Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell. 2007;129:333-44. https://doi.org/10.1016/j.cell.2007.02.039
Kim S, Sideris DP, Sevier CS, Kaiser CA. Balanced Ero1 activation and inactivation establishes ER redox homeostasis. J Cell Biol. 2012;196:713-25. https://doi.org/10.1083/jcb.201110090
Moilanen A, Ruddock LW. Non-native proteins inhibit the ER oxidoreductin 1 (Ero1)-protein disulfide-isomerase relay when protein folding capacity is exceeded. J Biol Chem. 2020;295:8647-55. https://doi.org/10.1074/jbc.RA119.011766
Moilanen A, Korhonen K, Saaranen MJ, Ruddock LW. Molecular analysis of human Ero1 reveals novel regulatory mechanisms for oxidative protein folding. Life Sci Alliance. 2018;1:e201800090. https://doi.org/10.26508/lsa.201800090
Appenzeller-Herzog C, Ellgaard L. The human PDI family: versatility packed into a single fold. Biochim Biophys Acta. 2008;1783:535-48. https://doi.org/10.1016/j.bbamcr.2007.11.010
Tempio T, Anelli T. The pivotal role of ERp44 in patrolling protein secretion. J Cell Sci. 2020;133:jcs240366. https://doi.org/10.1242/jcs.240366
Yim SH, Everley RA, Schildberg FA, Lee SG, Orsi A, Barbati ZR, et al. Role of Selenof as a gatekeeper of secreted disulfide-rich glycoproteins. Cell Rep. 2018;23:1387-98. https://doi.org/10.1016/j.celrep.2018.04.009
Watanabe S, Harayama M, Kanemura S, Sitia R, Inaba K. Structural basis of pH-dependent client binding by ERp44, a key regulator of protein secretion at the ER-Golgi interface. Proc Natl Acad Sci USA. 2017;114:E3224-32. https://doi.org/10.1073/pnas.1621426114
Vavassori S, Cortini M, Masui S, Sannino S, Anelli T, Caserta IR, et al. A pH-regulated quality control cycle for surveillance of secretory protein assembly. Mol Cell. 2013;50:783-92. https://doi.org/10.1016/j.molcel.2013.04.016
Chiu J, Passam F, Butera D, Hogg PJ. Protein disulfide isomerase in thrombosis. Semin Thromb Hemost. 2015;41:765-73. https://doi.org/10.1055/s-0035-1564047
Dihazi H, Dihazi GH, Bibi A, Eltoweissy M, Mueller CA, Asif AR, et al. Secretion of ERp57 is important for extracellular matrix accumulation and progression of renal fibrosis, and is an early sign of disease onset. J Cell Sci. 2013;126:3649-63. https://doi.org/10.1242/jcs.125088
Ilani T, Alon A, Grossman I, Horowitz B, Kartvelishvily E, Cohen SR, et al. A secreted disulfide catalyst controls extracellular matrix composition and function. Science. 2013;341:74-6. https://doi.org/10.1126/science.1238279
Wang TE, Li SH, Minabe S, Anderson AL, Dun MD, Maeda KI, et al. Mouse quiescin sulfhydryl oxidases exhibit distinct epididymal luminal distribution with segment-specific sperm surface associations. Biol Reprod. 2018;99:1022-33. https://doi.org/10.1093/biolre/ioy125
Alon A, Heckler EJ, Thorpe C, Fass D. QSOX contains a pseudo-dimer of functional and degenerate sulfhydryl oxidase domains. FEBS Lett. 2010;584:1521-5. https://doi.org/10.1016/j.febslet.2010.03.001
Alon A, Grossman I, Gat Y, Kodali VK, DiMaio F, Mehlman T, et al. The dynamic disulphide relay of quiescin sulfhydryl oxidase. Nature. 2012;488:414-8. https://doi.org/10.1038/nature11267
Gat Y, Vardi-Kilshtain A, Grossman I, Major DT, Fass D. Enzyme structure captures four cysteines aligned for disulfide relay. Protein Sci. 2014;23:1102-12. https://doi.org/10.1002/pro.2496
Grossman I, Aviram HY, Armony G, Horovitz A, Hofmann H, Haran G, et al. Single-molecule spectroscopy exposes hidden states in an enzymatic relay. Nat Commun. 2015;6:8624. https://doi.org/10.1038/ncomms9624
Ilani T, Reznik N, Yeshaya N, Feldman T, Vilela P, Lansky Z, et al. The QSOX1 disulfide catalyst maintains the colon mucosal barrier by regulating Golgi glycosyltransferases. EMBO J. 2022;in press. https://doi.org/10.15252/embj.2022111869
Antwi K, Hostetter G, Demeure MJ, Katchman BA, Decker GA, Ruiz Y, et al. Analysis of the plasma peptidome from pancreas cancer patients connects a peptide in plasma to overexpression of the parent protein in tumors. J Proteome Res. 2009;8:4722-31. https://doi.org/10.1021/pr900414f
Soloviev M, Esteves MP, Amiri F, Crompton MR, Rider CC. Elevated transcription of the gene QSOX1 encoding quiescin Q6 sulfhydryl oxidase 1 in breast cancer. PLoS One. 2013;8:e57327. https://doi.org/10.1371/journal.pone.0057327
Sung H-J, Ahn J-M, Yoon Y-H, Na S-S, Choi Y-J, Kim Y-I, et al. Quiescin sulfhydryl oxidase 1 (QSOX1) secreted by lung cancer cells promotes cancer metastasis. Int J Mol Sci. 2018;19:3213. https://doi.org/10.3390/ijms19103213
Knutsvik G, Collett K, Arnes J, Akslen LA, Stefansson IM. QSOX1 expression is associated with aggressive tumor features and reduced survival in breast carcinomas. Mod Pathol. 2016;29:1485-91. https://doi.org/10.1038/modpathol.2016.148
Nazempour N, Taleqani MH, Taheri N, Haji Ali Asgary Najafabadi AH, Shokrollahi A, Zamani A, et al. The role of cell surface proteins gene expression in diagnosis, prognosis, and drug resistance of colorectal cancer: in silico analysis and validation. Exp Mol Pathol. 2021;123:104688. https://doi.org/10.1016/j.yexmp.2021.104688
Jiang T, Zheng L, Li X, Liu J, Song H, Xu Y, et al. Quiescin sulfhydryl oxidase 2 overexpression predicts poor prognosis and tumor progression in patients with colorectal cancer: a study based on data mining and clinical verification. Front Cell Dev Biol. 2021;9:678770. https://doi.org/10.3389/fcell.2021.678770
Li Y, Liu M, Zhang Z, Deng L, Zhai Z, Liu H, et al. QSOX2 is an E2F1 target gene and a novel serum biomarker for monitoring tumor growth and predicting survival in advanced NSCLC. Front Cell Dev Biol. 2021;9:688798. https://doi.org/10.3389/fcell.2021.688798
Okalang U, Bar-Ner BM, Rajan KS, Friedman N, Aryal S, Egarmina K, et al. The spliced leader RNA silencing (SLS) pathway in Trypanosoma brucei is induced by perturbations of endoplasmic reticulum, Golgi complex, or mitochondrial protein factors: functional analysis of SLS-inducing kinase PK3. MBio. 2021;12:e0260221. https://doi.org/10.1128/mBio.02602-21
Rutkevich LA, Williams DB. Vitamin K epoxide reductase contributes to protein disulfide formation and redox homeostasis within the endoplasmic reticulum. Mol Biol Cell. 2012;23:2017-27. https://doi.org/10.1091/mbc.E12-02-0102
Horowitz B, Javitt G, Ilani T, Gat Y, Morgenstern D, Bard FA, et al. Quiescin sulfhydryl oxidase 1 (QSOX1) glycosite mutation perturbs secretion but not Golgi localization. Glycobiology. 2018;28:580-91. https://doi.org/10.1093/glycob/cwy044
Coppock DL, Kopman C, Scandalis S, Gilleran S. Preferential gene expression in quiescent human lung fibroblasts. Cell Growth Differ. 1993;4:483-93.
Coppock D, Kopman C, Cina-Poppe DA. Regulation of the quiescence-induced genes: quiescin Q6, decorin, and ribosomal protein S29. Biochem Biophys Res Commun. 2000;269:604-10. https://doi.org/10.1006/bbrc.2000.2324
Israel BA, Jiang L, Gannon SA, Thorpe C. Disulfide bond generation in mammalian blood serum: detection and purification of quiescin-sulfhydryl oxidase. Free Radic Biol Med. 2014;69:129-35. https://doi.org/10.1016/j.freeradbiomed.2014.01.020
Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in the colon is devoid of bacteria. Proc Natl Acad Sci USA. 2008;105:15064-9. https://doi.org/10.1073/pnas.0803124105
Wei Y-S, Lin W-Z, Wang T-E, Lee W-Y, Li S-H, Lin F-J, et al. Polarized epithelium-sperm co-culture system reveals stimulatory factors for the secretion of mouse epididymal quiescin sulfhydryl oxidase 1. J Reprod Dev. 2022;68:198-208. https://doi.org/10.1262/jrd.2021-128
Petris MJ, Strausak D, Mercer JF. The Menkes copper transporter is required for the activation of tyrosinase. Hum Mol Genet. 2000;9:2845-51. https://doi.org/10.1093/hmg/9.19.2845
Shanbhag V, Jasmer-McDonald K, Zhu S, Martin AL, Gudekar N, Khan A, et al. ATP7A delivers copper to the lysyl oxidase family of enzymes and promotes tumorigenesis and metastasis. Proc Natl Acad Sci USA. 2019;116:6836-41. https://doi.org/10.1073/pnas.1817473116
Nevitt T, Ohrvik H, Thiele DJ. Charging the travels of copper in eukaryotes from yeast to mammals. Biochim Biophys Acta. 2012;1823:1580-93. https://doi.org/10.1016/j.bbamcr.2012.02.011
Dong X, Springer TA. Disulfide exchange in multimerization of von Willebrand factor and gel-forming mucins. Blood. 2021;137:1263-7. https://doi.org/10.1182/blood.2020005989
Khoder-Agha F, Kietzmann T. The glycol-redox interplay: principles and consequences on the role of reactive oxygen species during protein glycosylation. Redox Biol. 2021;42:101888. https://doi.org/10.1016/j.redox.2021.101888
Tu BP, Weissman JS. The FAD- and O2-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell. 2002;10:983-94. https://doi.org/10.1016/s1097-2765(02)00696-2
Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, et al. Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc Natl Acad Sci USA. 2006;103:299-304. https://doi.org/10.1073/pnas.0506448103
Grossman-Haham I, Rosenblum G, Namani T, Hofmann H. Slow domain reconfiguration causes power-law kinetics in a two-state enzyme. Proc Natl Acad Sci USA. 2018;115:513-8. https://doi.org/10.1073/pnas.1714401115
Gross E, Kastner DB, Kaiser CA, Fass D. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell. 2004;117:601-10. https://doi.org/10.1016/s0092-8674(04)00418-0
Fass D. The Erv family of sulfhydryl oxidases. Biochim Biophys Acta. 2008;1783:557-66. https://doi.org/10.1016/j.bbamcr.2007.11.009
Raje S, Thorpe C. Inter-domain redox communication in flavoenzymes of the quiescin/sulfhydryl oxidase family: role of a thioredoxin domain in disulfide bond formation. Biochemistry. 2003;42:4560-8. https://doi.org/10.1021/bi030003z
Heckler EJ, Alon A, Fass D, Thorpe C. Human quiescin-sulfhydryl oxidase, QSOX1: probing internal redox steps by mutagenesis. Biochemistry. 2008;47:4955-63. https://doi.org/10.1021/bi702522q
Codding JA, Israel BA, Thorpe C. Protein substrate discrimination in the quiescin sulfhydryl oxidase (QSOX) family. Biochemistry. 2021;51:4226-35. https://doi.org/10.1021/bi300394w
Kodali VK, Thorpe C. Oxidative protein folding and the Quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid Redox Signal. 2010;13:1217-30. https://doi.org/10.1089/ars.2010.3098
Javitt G, Kinzel A, Reznik N, Fass D. Conformational switches and redox properties of the colon cancer-associated human lectin ZG16. FEBS J. 2021;288:6465-75. https://doi.org/10.1111/febs.16044
Lemons JMS, Feng X-J, Bennett BD, Legesse-Miller A, Johnson EL, Raitman I, et al. Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol. 2010;8:e1000514. https://doi.org/10.1371/journal.pbio.1000514
Feldman T, Grossman-Haham I, Elkis Y, Vilela P, Moskovits N, Barshack I, et al. Inhibition of fibroblast secreted QSOX1 perturbs extracellular matrix in the tumor microenvironment and decreases tumor growth and metastasis in murine cancer models. Oncotarget. 2020;11:386-98. https://doi.org/10.18632/oncotarget.27438
Kai F, Drain AP, Weaver VM. The extracellular matrix modulates the metastatic journey. Dev Cell. 2019;49:332-46. https://doi.org/10.1016/j.devcel.2019.03.026
Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med. 2008;14:518-27. https://doi.org/10.1038/nm1764
Araújo DGB, Nakao L, Gozzo P, Souza CDA, Balderrama V, Gugelmin ES, et al. Expression levels of quiescin sulfhydryl oxidase 1 (QSOX1) in neuroblastomas. Eur J Histochem. 2014;58:2228. https://doi.org/10.4081/ejh.2014.2228
Katchman BA, Antwi K, Hostetter G, Demeure MJ, Watanabe A, Decker GA, et al. Quiescin sulfhydryl oxidase 1 promotes invasion of pancreatic tumor cells mediated by matrix metalloproteinases. Mol Cancer Res. 2011;9:1621-31. https://doi.org/10.1158/1541-7786.MCR-11-0018
Katchman BA, Ocal IT, Cunliffe HE, Chang Y-H, Hostetter G, Watanabe A, et al. Expression of quiescin sulfhydryl oxidase 1 is associated with a highly invasive phenotype and correlates with a poor prognosis in Luminal B breast cancer. Breast Cancer Res. 2013;15:R28. https://doi.org/10.1186/bcr3407
Bergström JH, Birchenough GMH, Katona G, Schroeder BO, Schütte A, Ermund A, et al. Gram-positive bacteria are held at a distance in the colon mucus by the lectin-like protein ZG16. Proc Natl Acad Sci USA. 2016;113:13833-8. https://doi.org/10.1073/pnas.1611400113
Qian R, Chen C, Colley KJ. Location and mechanism of α2,6-sialyltransferase dimer formation. Role of cysteine residues in enzyme dimerization, localization, activity, and processing. J Biol Chem. 2001;276:28641-9. https://doi.org/10.1074/jbc.M103664200
Hirano Y, Suzuki T, Matsumoto T, Ishihara Y, Takaki Y, Kono M, et al. Disulphide linkage in mouse ST6Gal-I determination of linkage positions and mutant analysis. J Biochem. 2012;151:197-203. https://doi.org/10.1093/jb/mvr133
Hassinen A, Khoder-Agha F, Khosrowabadi E, Mennerich D, Harrus D, Noel M, et al. A Golgi-associated redox switch regulates catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I. Redox Biol. 2019;24:101182. https://doi.org/10.1016/j.redox.2019.101182
Caillard A, Sadoune M, Cescau A, Meddour M, Gandon M, Polidano E, et al. QSOX1, a novel actor of cardiac protection upon acute stress in mice. J Mol Cell Cardiol. 2018;119:75-86. https://doi.org/10.1016/j.yjmcc.2018.04.014
Borges BE, Appel MH, Cofré AR, Prado ML, Steclan CA, Esnard F, et al. The flavo-oxidase QSOX1 supports vascular smooth muscle cell migration and proliferation: evidence for a role in neointima growth. Biochim Biophys Acta. 2015;1852:1334-46. https://doi.org/10.1016/j.bbadis.2015.03.002
Nandakumar P, Lee D, Richard MA, Tekola-Ayele F, Tayo BO, Ware E, et al. Rare coding variants associated with blood pressure variation in 15 914 individuals of African ancestry. J Hypertens. 2017;35:1381-9. https://doi.org/10.1097/HJH.0000000000001319
Javitt G, Khmelnitsky L, Albert L, Bigman LS, Elad N, Morgenstern D, et al. Assembly mechanism of mucin and von Willebrand factor polymers. Cell. 2020;183:717-29. https://doi.org/10.1016/j.cell.2020.09.021
Dong X, Leksa NC, Chhabra ES, Arndt JW, Lu Q, Knockenhaur KE, et al. The von Willebrand factor D'D3 assembly and structural principles for factor VIII binding and concatemer biogenesis. Blood. 2019;133:1523-33. https://doi.org/10.1182/blood-2018-10-876300
Javitt G, Calvo MLG, Albert L, Reznik N, Ilani T, Diskin R, et al. Intestinal gel-forming mucins polymerize by disulfide-mediated dimerization of D3 domains. J Mol Biol. 2019;431:3740-52. https://doi.org/10.1016/j.jmb.2019.07.018
Javitt G, Fass D. Helical self-assembly of a mucin segment suggests an evolutionary origin for von Willebrand factor tubules. Proc Natl Acad Sci USA. 2022;119:e2116790119. https://doi.org/10.1073/pnas.2116790119
Anderson JR, Li J, Springer JA, Brown A. Structures of VWF tubules before and after concatemerization reveal a mechanism of disulfide bond exchange. Blood. 2022;140:1419-30. https://doi.org/10.1182/blood.2022016467
Wagner DD, Lawrence SO, Ohlsson-Wilhelm BM, Fay PJ, Marder VJ. Topology and order of formation of interchain disulfide bonds in von Willebrand factor. Blood. 1987;69:27-32.
Perez-Vilar J, Eckhardt AE, Hill RL. Porcine submaxillary mucin forms disulfide-bonded dimers between its carboxy-terminal domains. J Biol Chem. 1996;271:9845-50. https://doi.org/10.1074/jbc.271.16.9845
Lippok S, Kolšek K, Löf A, Eggert D, Vanderlinden W, Müller JP, et al. von Willebrand factor is dimerized by protein disulfide isomerase. Blood. 2016;127:1183-91. https://doi.org/10.1182/blood-2015-04-641902
Wagner DD, Marder VJ. Biosynthesis of von Willebrand protein by human endothelial cells: processing steps and their intracellular localization. J Cell Biol. 1984;99:2123-30. https://doi.org/10.1083/jcb.99.6.2123
Wagner DD, Mayadas T, Marder VJ. Initial glycosylation and acidic pH in the Golgi apparatus are required for multimerization of von Willebrand factor. J Cell Biol. 1986;102:1320-4. https://doi.org/10.1083/jcb.102.4.1320
Mayadas TN, Wagner DD. In vitro multimerization of von Willebrand factor is triggered by low pH. Importance of the propolypeptide and free sulfhydryls. J Biol Chem. 1989;264:13497-503.
Zeng J, Shu Z, Liang Q, Zhang J, Wu W, Wang X, et al. Structural basis of von Willebrand factor multimerization and tubular storage. Blood. 2022;139:3314-24. https://doi.org/10.1182/blood.2021014729
Zhou Y-F, Eng ET, Nishida N, Lu C, Walz T, Springer TA. A pH-regulated dimeric bouquet in the structure of von Willebrand factor. EMBO J. 2011;30:4098-111. https://doi.org/10.1038/emboj.2011.297
Mayadas TN, Wagner DD. Vicinal cysteines in the prosequence play a role in von Willebrand factor multimer assembly. Proc Natl Acad Sci USA. 1992;89:3531-5. https://doi.org/10.1073/pnas.89.8.3531
DiChiara AS, Li RC, Suen PH, Hosseini AS, Taylor RJ, Weickhardt AF, et al. A cysteine-based molecular code informs collagen C-propeptide assembly. Nat Commun. 2018;9:4206. https://doi.org/10.1038/s41467-018-06185-2
Bourhis J-M, Mariano N, Zhao Y, Harlos K, Exposito J-Y, Jones EY, et al. Structural basis of fibrillar collagen trimerization and related genetic disorders. Nat Struct Mol Biol. 2012;19:1031-6. https://doi.org/10.1038/nsmb.2389
Sharma U, Carrique L, Vadon-Le Goff S, Mariano N, Georges RN, Delolme F, et al. Structural basis of homo- and heterotrimerization of collagen I. Nat Commun. 2017;8:14671. https://doi.org/10.1038/ncomms14671
Sitia R, Neuberger M, Alberini C, Bet P, Fra A, Valetti C, et al. Developmental regulation of IgM secretion: the role of the carboxy-terminal cysteine. Cell. 1990;60:781-90. https://doi.org/10.1016/0092-8674(90)90092-s
Pasalic D, Weber B, Giannone C, Anelli T, Müller R, Fagioli C, et al. A peptide extension dictates IgM assembly. Proc Natl Acad Sci USA. 2017;114:E8575-84. https://doi.org/10.1073/pnas.1701797114
Li Y, Wang G, Li N, Wang Y, Zhu Q, Chu H, et al. Structural insights into immunoglobulin M. Science. 2020;367:1014-7. https://doi.org/10.1126/science.aaz5425
Giannone C, Chelazzi MR, Orsi A, Anelli T, Nguyen T, Buchner J, et al. Biogenesis of secretory immunoglobulin M requires intermediate non-native disulfide bonds and engagement of the protein disulfide isomerase ERp44. EMBO J. 2022;41:e108518. https://doi.org/10.15252/embj.2021108518
Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, et al. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell. 2005;121:1059-69. https://doi.org/10.1016/j.cell.2005.04.011
Frand AR, Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell. 1998;1:161-70. https://doi.org/10.1016/s1097-2765(00)80017-9
Pollard MG, Travers KJ, Weissman JS. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell. 1998;1:171-82. https://doi.org/10.1016/s1097-2765(00)80018-0
Hofmann S, Rothbauer U, Mühlenbein N, Baiker K, Hell K, Bauer MF. Functional and mutational characterization of human MIA40 acting during import into the mitochondrial intermembrane space. J Mol Biol. 2005;353:517-28. https://doi.org/10.1016/j.jmb.2005.08.064
Cabibbo A, Pagani M, Fabbri M, Rocchi M, Farmery MR, Bulleid NJ, et al. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J Biol Chem. 2000;275:4827-33. https://doi.org/10.1074/jbc.275.7.4827
Mesecke N, Spang A, Deponte M, Herrmann JM. A novel group of glutaredoxins in the cis-Golgi critical for oxidative stress resistance. Mol Biol Cell. 2008;19:2673-80. https://doi.org/10.1091/mbc.e07-09-0896
Izquierdo A, Casas C, Mühlenhoff U, Lillig CH, Herrero E. Saccharomyces cerevisiae Grx6 and Grx7 are monothiol glutaredoxins associated with the early secretory pathway. Eukaryot Cell. 2008;7:1415-26. https://doi.org/10.1128/EC.00133-08
Mesecke N, Mittler S, Eckers E, Herrmann JM, Deponte M. Two novel monothiol glutaredoxins from Saccharomyces cerevisiae provide further insight into iron-sulfur cluster binding, oligomerization, and enzymatic activity of glutaredoxins. Biochemistry. 2008;47:1452-63. https://doi.org/10.1021/bi7017865
Puigpinós J, Casas C, Herrero E. Altered intracellular calcium homeostasis and endoplasmic reticulum redox state in Saccharomyces cerevisiae cells lacking Grx6 glutaredoxin. Mol Biol Cell. 2015;26:104-16. https://doi.org/10.1091/mbc.E14-06-1137
Shu Z, Zeng J, Xia L, Cai H, Zhou A. Structural mechanism of VWF D'D3 dimer formation. Cell Discov. 2022;8:14. https://doi.org/10.1038/s41421-022-00378-2
Kellokumpu S. Golgi pH, ion and redox homeostasis: how much do they really matter? Front Cell Dev Biol. 2019;7:93. https://doi.org/10.3389/fcell.2019.00093
Hassinen A, Kellokumpu. Organizational interplay of Golgi N-glycosyltransferases involves organelle microenvironment-dependent transitions between enzyme homo- and heteromers. J Biol Chem. 2014;289:26937-48. https://doi.org/10.1074/jbc.M114.595058
Kitano M, Kizuka Y, Sobajima T, Nakano M, Nakajima K, Misaki R, et al. Rab11-mediated post-Golgi transport of the sialyltransferase ST3GAL4 suggests a new mechanism for regulating glycosylation. J Biol Chem. 2021;296:100354. https://doi.org/10.1016/j.jbc.2021.100354
Vattepu R, Sneed SL, Anthony RM. Sialylation as an important regulator of antibody function. Front Immunol. 2022;13:818736. https://doi.org/10.3389/fimmu.2022.818736
Steele H, Tague AJ, Skropeta D. The role of sialylation in respiratory viral infection and treatment. Curr Med Chem. 2021;28:5251-67. https://doi.org/10.2174/0929867328666210201153901
Pietrobono S, Stecca B. Aberrant sialylation in cancer: biomarker and potential target for therapeutic intervention. Cancer. 2021;13:2014. https://doi.org/10.3390/cancers13092014