C-terminal mutations destabilize SIL1/BAP and can cause Marinesco-Sjögren syndrome

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8552-8560

  Howes, Jennifer ^a,b   Shimizu, Yuichiro ^a,c   Feige, Matthias J ^a   Hendershot, Linda M ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c CHUGAI PHARMACEUTICAL CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPLASMIC RETICULUM; HOMOLOGY MODELING; IN-DEPTH ANALYSIS; LARGE AGGREGATES; MULTI SYSTEMS; MUTANT PROTEINS; NEURODEGENERATIVE; NUCLEOTIDE-EXCHANGE FACTOR; PHARMACOLOGICAL TREATMENT; POLYPEPTIDE CHAIN; PROTEASOMES; UNFOLDED PROTEINS;

AMINO ACIDS; CELL MEMBRANES; NEURODEGENERATIVE DISEASES; SATELLITES;

PROTEINS;

CHAPERONE; GLUCOSE REGULATED PROTEIN 78; SIL1 PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; ENDOPLASMIC RETICULUM; GENE; GENE MUTATION; GLYCOSYLATION; MARINESCO SJOGREN SYNDROME; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STABILITY; SIL1 GENE; STRUCTURAL HOMOLOGY;

AMINO ACID MOTIFS; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPLASMIC RETICULUM; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEAT-SHOCK PROTEINS; HEK293 CELLS; HUMANS; MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN STABILITY; PROTEOLYSIS; SPINOCEREBELLAR DEGENERATIONS;

EID: 84858025731     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.333286     Document Type: Article

References (44)

1. Hammond, C., and Helenius, A. (1995) Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7, 523-529
2. Ellgaard, L., and Helenius, A. (2001) ER quality control. Towards an understanding at the molecular level. Curr. Opin. Cell Biol. 13, 431-437 (Pubitemid 32709766)
3. Nishikawa, S. I., Fewell, S. W., Kato, Y., Brodsky, J. L., and Endo, T. (2001) Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J. Cell Biol. 153, 1061-1070
4. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049 (Pubitemid 39050393)
5. Moremen, K. W., and Molinari, M. (2006) N-Linked glycan recognition and processing. The molecular basis of endoplasmic reticulum quality control. Curr. Opin. Struct. Biol. 16, 592-599 (Pubitemid 44472609)
6. Michalak, M., Groenendyk, J., Szabo, E., Gold, L. I., and Opas, M. (2009) Calreticulin, a multiprocess calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 417, 651-666
7. Haas, I. G., and Wabl, M. (1983) Immunoglobulin heavy chain binding protein. Nature 306, 387-389 (Pubitemid 14242753)
8. Munro, S., and Pelham, H. R. (1986) An Hsp70-like protein in the ER. Identity with the 78-kDa glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291-300
9. Bole, D. G., Hendershot, L. M., and Kearney, J. F. (1986) Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol. 102, 1558-1566 (Pubitemid 16078740)
10. Hendershot, L., Bole, D., Köhler, G., and Kearney, J. F. (1987) Assembly and secretion of heavy chains that do not associate posttranslationally with immunoglobulin heavy chain-binding protein. J. Cell Biol. 104, 761-767 (Pubitemid 17024730)
11. Hamman, B. D., Hendershot, L. M., and Johnson, A. E. (1998) BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92, 747-758 (Pubitemid 28155314)
12. Skowronek, M. H., Hendershot, L. M., and Haas, I. G. (1998) The variable domain of nonassembled Ig light chains determines both their half-life and binding to the chaperone BiP. Proc. Natl. Acad. Sci. U.S.A. 95, 1574-1578 (Pubitemid 28103434)
13. Bertolotti, A., Zhang, Y., Hendershot, L. M., Harding, H. P., and Ron, D. (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2, 326-332
14. Shen, J., Chen, X., Hendershot, L., and Prywes, R. (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3, 99-111 (Pubitemid 34778399)
15. Lièvremont, J. P., Rizzuto, R., Hendershot, L., and Meldolesi, J. (1997) BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+. J. Biol. Chem. 272, 30873-30879 (Pubitemid 27527530)
16. Liberek, K., Skowyra, D., Zylicz, M., Johnson, C., and Georgopoulos, C. (1991) The Escherichia coli DnaK chaperone, the 70-kDa heat shock protein eukaryotic equivalent, changes conformation upon ATP hydrolysis, thus triggering its dissociation from a bound target protein. J. Biol. Chem. 266, 14491-14496 (Pubitemid 21907530)
17. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. U.S.A. 88, 2874-2878 (Pubitemid 21916522)
18. Cheetham, M. E., and Caplan, A. J. (1998) Structure, function and evolution of DnaJ. Conservation and adaptation of chaperone function. Cell Stress Chaperones 3, 28-36 (Pubitemid 28159676)
19. Chung, K. T., Shen, Y., and Hendershot, L. M. (2002) BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J. Biol. Chem. 277, 47557-47563 (Pubitemid 36159275)
20. Weitzmann, A., Volkmer, J., and Zimmermann, R. (2006) The nucleotide exchange factor activity of Grp170 may explain the non-lethal phenotype of loss of Sil1 function in man and mouse. FEBS Lett. 580, 5237-5240
21. Herczenik, E., and Gebbink, M. F. (2008) Molecular and cellular aspects of protein misfolding and disease. FASEB J. 22, 2115-2133 (Pubitemid 351948631)
22. Luo, S., Mao, C., Lee, B., and Lee, A. S. (2006) GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell Biol. 26, 5688-5697 (Pubitemid 44134326)
23. Paton, A. W., Beddoe, T., Thorpe, C. M., Whisstock, J. C., Wilce, M. C., Rossjohn, J., Talbot, U. M., and Paton, J. C. (2006) AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 443, 548-552 (Pubitemid 44527286)
24. Anttonen, A. K., Mahjneh, I., Hämäläinen, R. H., Lagier-Tourenne, C., Kopra, O., Waris, L., Anttonen, M., Joensuu, T., Kalimo, H., Paetau, A., Tranebjaerg, L., Chaigne, D., Koenig, M., Eeg-Olofsson, O., Udd, B., Somer, M., Somer, H., and Lehesjoki, A. E. (2005) The gene disrupted in Marinesco-Sjögren syndrome encodes SIL1, an HSPA5 cochaperone. Nat. Genet. 37, 1309-1311 (Pubitemid 41722182)
25. Senderek, J., Krieger, M., Stendel, C., Bergmann, C., Moser, M., Breitbach- Faller, N., Rudnik-Schöneborn, S., Blaschek, A., Wolf, N. I., Harting, I., North, K., Smith, J., Muntoni, F., Brockington, M., Quijano-Roy, S., Renault, F., Herrmann, R., Hendershot, L. M., Schröder, J. M., Lochmüller, H., Topaloglu, H., Voit, T., Weis, J., Ebinger, F., and Zerres, K. (2005) Mutations in SIL1 cause Marinesco-Sjögren syndrome, a cerebellar ataxia with cataract and myopathy. Nat. Genet. 37, 1312-1314 (Pubitemid 41722183)
26. Zhao, L., Longo-Guess, C., Harris, B. S., Lee, J. W., and Ackerman, S. L. (2005) Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat. Genet. 37, 974-979 (Pubitemid 43086155)
27. Karim, M. A., Parsian, A. J., Cleves, M. A., Bracey, J., Elsayed, M. S., Elsobky, E., and Parsian, A. (2006) A novel mutation in BAP/SIL1 gene causes Marinesco-Sjögren syndrome in an extended pedigree. Clin. Genet. 70, 420-423 (Pubitemid 44515646)
28. Anttonen, A. K., Siintola, E., Tranebjaerg, L., Iwata, N. K., Bijlsma, E. K., Meguro, H., Ichikawa, Y., Goto, J., Kopra, O., and Lehesjoki, A. E. (2008) Novel SIL1 mutations and exclusion of functional candidate genes in Marinesco-Sjögren syndrome. Eur. J. Hum. Genet. 16, 961-969
29. Eriguchi, M., Mizuta, H., Kurohara, K., Fujitake, J., and Kuroda, Y. (2008) Identification of a new homozygous frameshift insertion mutation in the SIL1 gene in 3 Japanese patients with Marinesco-Sjögren syndrome. J. Neurol. Sci. 270, 197-200
30. Munro, S., and Pelham, H. R. (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907
31. Raykhel, I., Alanen, H., Salo, K., Jurvansuu, J., Nguyen, V. D., Latva-Ranta, M., and Ruddock, L. (2007) A molecular specificity code for the three mammalian KDEL receptors. J. Cell Biol. 179, 1193-1204 (Pubitemid 350277738)
32. Sambrook, J. F., and Russell, D.W(2001) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
33. Konagurthu, A. S., Whisstock, J. C., Stuckey, P. J., and Lesk, A. M. (2006) MUSTANG. A multiple structural alignment algorithm. Proteins 64, 559-574 (Pubitemid 44100724)
34. Muñoz, V., and Serrano, L. (1997) Development of the multiple sequence approximation within the AGADIR model of α-helix formation. Comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 41, 495-509
35. Shomura, Y., Dragovic, Z., Chang, H. C., Tzvetkov, N., Young, J. C., Brodsky, J. L., Guerriero, V., Hartl, F. U., and Bracher, A. (2005) Regulation of Hsp70 function by HspBP1. Structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Mol. Cell 17, 367-379 (Pubitemid 40193308)
36. Yan, M., Li, J., and Sha, B. (2011) Structural analysis of the Sil1-Bip complex reveals the mechanism for Sil1 to function as a nucleotide-exchange factor. Biochem. J. 438, 447-455
37. Bu, G., Rennke, S., and Geuze, H. J. (1997) ERD2 proteins mediate ER retention of the HNEL signal of LRP's receptor-associated protein (RAP). J. Cell Sci. 110, 65-73 (Pubitemid 27057945)
38. Kabani, M., McLellan, C., Raynes, D. A., Guerriero, V., and Brodsky, J. L. (2002) HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Lett. 531, 339-342 (Pubitemid 35341220)
39. Titani, K., Kumar, S., Takio, K., Ericsson, L. H., Wade, R. D., Ashida, K., Walsh, K. A., Chopek, M. W., Sadler, J. E., and Fujikawa, K. (1986) Amino acid sequence of human von Willebrand factor. Biochemistry 25, 3171-3184 (Pubitemid 16056960)
40. Satomi, Y., Shimonishi, Y., and Takao, T. (2004)N-Glycosylation at Asn491 in the Asn-Xaa-Cys motif of human transferrin. FEBS Lett. 576, 51-56 (Pubitemid 39330456)
41. Fra, A. M., Fagioli, C., Finazzi, D., Sitia, R., and Alberini, C. M. (1993) Quality control of ER synthesized proteins. An exposed thiol group as a three-way switch mediating assembly, retention, and degradation. EMBO J. 12, 4755-4761 (Pubitemid 23330281)
42. Otero, J. H., Lizák, B., and Hendershot, L. M. (2010) Life and death of a BiP substrate. Semin. Cell Dev. Biol. 21, 472-478
43. Weitzmann, A., Baldes, C., Dudek, J., and Zimmermann, R. (2007) The heat shock protein 70 molecular chaperone network in the pancreatic endoplasmic reticulum. A quantitative approach. FEBS J. 274, 5175-5187 (Pubitemid 47485662)
44. Powers, E. T., Morimoto, R. I., Dillin, A., Kelly, J. W., and Balch, W. E. (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78, 959-991