A pH-Regulated Quality Control Cycle for Surveillance of Secretory Protein Assembly

Molecular Cell

Volumn 50, Issue 6, 2013, Pages 783-792

  Vavassori, Stefano ^a,b,c,d   Cortini, Margherita ^a,b,c,e   Masui, Shoji ^c,d,f   Sannino, Sara ^a,b   Anelli, Tiziana ^a,b   Caserta, Imma R ^a   Fagioli, Claudio ^a   Mossuto, Maria F ^a   Fornili, Arianna ^a,g   vanAnken, Eelco ^a,b   Degano, Massimo ^a   Inaba, Kenji ^c,f   Sitia, Roberto ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c KYUSHU UNIVERSITY   (Japan)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^f TOHOKU UNIVERSITY   (Japan)

^g KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; CALNEXIN; CALRETICULIN; CYSTEINE; ERP44 PROTEIN; IMMUNOGLOBULIN M; OLIGOMER; PROTEOME; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL CYCLE; DISULFIDE BOND; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PH; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEOMICS; QUALITY CONTROL; RNA INTERFERENCE; WESTERN BLOTTING;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; CELL CYCLE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HELA CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; OXIDOREDUCTASES; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SECRETORY PATHWAY;

EID: 84880809859     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.04.016     Document Type: Article

References (40)

1. Anelli T., Sitia R. Protein quality control in the early secretory pathway. EMBO J. 2008, 27:315-327.
2. Anelli T., Alessio M., Mezghrani A., Simmen T., Talamo F., Bachi A., Sitia R. ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family. EMBO J. 2002, 21:835-844.
3. Anelli T., Alessio M., Bachi A., Bergamelli L., Bertoli G., Camerini S., Mezghrani A., Ruffato E., Simmen T., Sitia R. Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J. 2003, 22:5015-5022.
4. Anelli T., Ceppi S., Bergamelli L., Cortini M., Masciarelli S., Valetti C., Sitia R. Sequential steps and checkpoints in the early exocytic compartment during secretory IgM biogenesis. EMBO J. 2007, 26:4177-4188.
5. Anelli T., Bergamelli L., Margittai E., Rimessi A., Fagioli C., Malgaroli A., Pinton P., Ripamonti M., Rizzuto R., Sitia R. Ero1α regulates Ca(2+) fluxes at the endoplasmic reticulum-mitochondria interface (MAM). Antioxid. Redox Signal. 2012, 16:1077-1087.
6. Appenzeller-Herzog C., Roche A.C., Nufer O., Hauri H.P. pH-induced conversion of the transport lectin ERGIC-53 triggers glycoprotein release. J.Biol. Chem. 2004, 279:12943-12950.
7. Cenci S., Mezghrani A., Cascio P., Bianchi G., Cerruti F., Fra A., Lelouard H., Masciarelli S., Mattioli L., Oliva L., et al. Progressively impaired proteasomal capacity during terminal plasma cell differentiation. EMBO J. 2006, 25:1104-1113.
8. Cortini M., Sitia R. From antibodies to adiponectin: role of ERp44 in sizing and timing protein secretion. Diabetes Obes. Metab. 2010, 12(Suppl 2):39-47.
9. Ellgaard L., Helenius A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 2003, 4:181-191.
10. Ellgaard L., Ruddock L.W. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005, 6:28-32.
11. Feige M.J., Groscurth S., Marcinowski M., Shimizu Y., Kessler H., Hendershot L.M., Buchner J. An unfolded CH1 domain controls the assembly and secretion of IgG antibodies. Mol. Cell 2009, 34:569-579.
12. Fra A.M., Fagioli C., Finazzi D., Sitia R., Alberini C.M. Quality control of ER synthesized proteins: an exposed thiol group as a three-way switch mediating assembly, retention and degradation. EMBO J. 1993, 12:4755-4761.
13. Fraldi A., Zito E., Annunziata F., Lombardi A., Cozzolino M., Monti M., Spampanato C., Ballabio A., Pucci P., Sitia R., Cosma M.P. Multistep, sequential control of the trafficking and function of the multiple sulfatase deficiency gene product, SUMF1 by PDI, ERGIC-53 and ERp44. Hum. Mol. Genet. 2008, 17:2610-2621.
14. Gilchrist A., Au C.E., Hiding J., Bell A.W., Fernandez-Rodriguez J., Lesimple S., Nagaya H., Roy L., Gosline S.J., Hallett M., et al. Quantitative proteomics analysis of the secretory pathway. Cell 2006, 127:1265-1281.
15. Haas I.G., Wabl M. Immunoglobulin heavy chain binding protein. Nature 1983, 306:387-389.
16. Hendershot L.M., Sitia R. Immunoglobulin assembly and secretion. Molecular Biology of B Cells 2005, 261-273. Elsevier Acad Press, Amsterdam. T.A.F. Honjo, M.S. Neuberger (Eds.).
17. Inaba K., Masui S., Iida H., Vavassori S., Sitia R., Suzuki M. Crystal structures of human Ero1α reveal the mechanisms of regulated and targeted oxidation of PDI. EMBO J. 2010, 29:3330-3343.
18. Lee Y.K., Brewer J.W., Hellman R., Hendershot L.M. BiP and immunoglobulin light chain cooperate to control the folding of heavy chain and ensure the fidelity of immunoglobulin assembly. Mol. Biol. Cell 1999, 10:2209-2219.
19. Li H., Robertson A.D., Jensen J.H. Very fast empirical prediction and rationalization of protein pKa values. Proteins 2005, 61:704-721.
20. Maeda Y., Ide T., Koike M., Uchiyama Y., Kinoshita T. GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus. Nat. Cell Biol. 2008, 10:1135-1145.
21. Makmura L., Hamann M., Areopagita A., Furuta S., Muñoz A., Momand J. Development of a sensitive assay to detect reversibly oxidized protein cysteine sulfhydryl groups. Antioxid. Redox Signal. 2001, 3:1105-1118.
22. Mariappan M., Radhakrishnan K., Dierks T., Schmidt B., von Figura K. ERp44 mediates a thiol-independent retention of formylglycine-generating enzyme in the endoplasmic reticulum. J.Biol. Chem. 2008, 283:6375-6383.
23. Masui S., Vavassori S., Fagioli C., Sitia R., Inaba K. Molecular bases of cyclic and specific disulfide interchange between human ERO1alpha protein and protein-disulfide isomerase (PDI). J.Biol. Chem. 2011, 286:16261-16271.
24. Mattioli L., Anelli T., Fagioli C., Tacchetti C., Sitia R., Valetti C. ER storage diseases: a role for ERGIC-53 in controlling the formation and shape of Russell bodies. J.Cell Sci. 2006, 119:2532-2541.
25. Miesenböck G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
26. Olsson M.H. Protein electrostatics and pKa blind predictions; contribution from empirical predictions of internal ionizable residues. Proteins 2011, 79:3333-3345.
27. Olsson M.H., Chresten R., Søndergaard M., Jensen J.H. PROPKA3: consistent treatment of internal and surface residues in empirical pKa predictions. J.Chem. Theory Comput. 2011, 7:525-537.
28. Otsu M., Bertoli G., Fagioli C., Guerini-Rocco E., Nerini-Molteni S., Ruffato E., Sitia R. Dynamic retention of Ero1alpha and Ero1beta in the endoplasmic reticulum by interactions with PDI and ERp44. Antioxid. Redox Signal. 2006, 8:274-282.
29. Paroutis P., Touret N., Grinstein S. The pH of the secretory pathway: measurement, determinants, and regulation. Physiology (Bethesda) 2004, 19:207-215.
30. Qiang L., Wang H., Farmer S.R. Adiponectin secretion is regulated by SIRT1 and the endoplasmic reticulum oxidoreductase Ero1-L alpha. Mol. Cell. Biol. 2007, 27:4698-4707.
31. Reddy P., Sparvoli A., Fagioli C., Fassina G., Sitia R. Formation of reversible disulfide bonds with the protein matrix of the endoplasmic reticulum correlates with the retention of unassembled Ig light chains. EMBO J. 1996, 15:2077-2085.
32. Ronzoni R., Anelli T., Brunati M., Cortini M., Fagioli C., Sitia R. Pathogenesis of ER storage disorders: modulating Russell body biogenesis by altering proximal and distal quality control. Traffic 2010, 11:947-957.
33. Schindler R., Itin C., Zerial M., Lottspeich F., Hauri H.P. ERGIC-53, a membrane protein of the ER-Golgi intermediate compartment, carries an ER retention motif. Eur. J. Cell Biol. 1993, 61:1-9.
34. Serve O., Kamiya Y., Maeno A., Nakano M., Murakami C., Sasakawa H., Yamaguchi Y., Harada T., Kurimoto E., Yagi-Utsumi M., et al. Redox-dependent domain rearrangement of protein disulfide isomerase coupled with exposure of its substrate-binding hydrophobic surface. J.Mol. Biol. 2010, 396:361-374.
35. Simmen T., Lynes E.M., Gesson K., Thomas G. Oxidative protein folding in the endoplasmic reticulum: tight links to the mitochondria-associated membrane (MAM). Biochim. Biophys. Acta 2010, 1798:1465-1473.
36. Sitia R., Neuberger M., Alberini C., Bet P., Fra A., Valetti C., Williams G., Milstein C. Developmental regulation of IgM secretion: the role of the carboxy-terminal cysteine. Cell 1990, 60:781-790.
37. van Anken E., Romijn E.P., Maggioni C., Mezghrani A., Sitia R., Braakman I., Heck A.J. Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion. Immunity 2003, 18:243-253.
38. Wang Z.V., Schraw T.D., Kim J.Y., Khan T., Rajala M.W., Follenzi A., Scherer P.E. Secretion of the adipocyte-specific secretory protein adiponectin critically depends on thiol-mediated protein retention. Mol. Cell. Biol. 2007, 27:3716-3731.
39. Wang L., Wang L., Vavassori S., Li S., Ke H., Anelli T., Degano M., Ronzoni R., Sitia R., Sun F., Wang C.C. Crystal structure of human ERp44 shows a dynamic functional modulation by its carboxy-terminal tail. EMBO Rep. 2008, 9:642-647.
40. Wilson D.W., Lewis M.J., Pelham H.R. pH-dependent binding of KDEL to its receptor invitro. J.Biol. Chem. 1993, 268:7465-7468.