AMPylation matches BiP activity to client protein load in the endoplasmic reticulum

eLife

Volumn 4, Issue DECEMBER2015, 2015, Pages

  Preissler, Steffen ^a   Rato, Cláudia ^a   Chen, Ruming ^a   Antrobus, Robin ^a   Ding, Shujing ^b   Fearnley, Ian M ^b   Ron, David ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; CARRIER PROTEIN; HEAT SHOCK PROTEIN; HYPE PROTEIN, HUMAN; MEMBRANE PROTEIN; MOLECULAR CHAPERONE GRP78;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE SEQUENCE; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; ISOELECTRIC FOCUSING; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PURIFICATION; RAT; REVERSE TRANSCRIPTION; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; ANIMAL; CELL LINE; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM; PROTEIN PROCESSING;

ANIMALS; CARRIER PROTEINS; CELL LINE; ENDOPLASMIC RETICULUM; GENE DELETION; HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84986577032     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12621     Document Type: Article

References (49)

1. Avezov E, Cross BCS, Kaminski Schierle GS, Winters M, Harding HP, Melo EP, Kaminski CF, Ron D. 2013. Lifetime imaging of a fluorescent protein sensor reveals surprising stability of ER thiol redox. The Journal of Cell Biology 201:337-349. doi: 10.1083/jcb.201211155
2. Balch WE, Morimoto RI, Dillin A, Kelly JW. 2008. Adapting proteostasis for disease intervention. Science 319: 916-919. doi: 10.1126/science.1141448
3. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nature Cell Biology 2:326-332. doi: 10.1038/35014014
4. Broncel M, Serwa RA, Bunney TD, Katan M, Tate EW. 2015. Global profiling of HYPE mediated AMPylation through a chemical proteomic approach. Molecular & Cellular Proteomics:mcp.115.054429. doi: 10.1074/mcp.O115.054429
5. Bunney TD, Cole AR, Broncel M, Esposito D, Tate EW, Katan M. 2014. Crystal structure of the human, FIC-domain containing protein HYPE and implications for its functions. Structure 22:1831-1843. doi: 10.1016/j.str.2014.10.007
6. Carlsson L, Lazarides E. 1983. ADP-ribosylation of the mr 83,000 stress-inducible and glucose-regulated protein in avian and mammalian cells: modulation by heat shock and glucose starvation. Proceedings of the National Academy of Sciences of the United States of America 80:4664-4668. doi: 10.1073/pnas.80.15.4664
7. Carroll J, Fearnley IM, Wang Q, Walker JE. 2009. Measurement of the molecular masses of hydrophilic and hydrophobic subunits of ATP synthase and complex i in a single experiment. Analytical Biochemistry 395:249-255. doi: 10.1016/j.ab.2009.08.006
8. Chambers JE, Petrova K, Tomba G, Vendruscolo M, Ron D. 2012. ADP ribosylation adapts an ER chaperone response to short-term fluctuations in unfolded protein load. The Journal of Cell Biology 198:371-385. doi: 10.1083/jcb.201202005
9. Chang SC, Erwin AE, Lee AS. 1989. Glucose-regulated protein (gRP94 and GRP78) genes share common regulatory domains and are coordinately regulated by common trans-acting factors. Molecular and Cellular Biology 9:2153-2162. doi: 10.1128/MCB.9.5.2153
10. De Los Rios P, Barducci A. 2014. Hsp70 chaperones are non-equilibrium machines that achieve ultra-affinity by energy consumption. eLife 3:e02218. doi: 10.7554/eLife.02218
11. Dorner AJ, Wasley LC, Kaufman RJ. 1992. Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in chinese hamster ovary cells. The EMBO Journal 11:1563-1571.
12. Engel P, Goepfert A, Stanger FV, Harms A, Schmidt A, Schirmer T, Dehio C. 2012. Adenylylation control by intra-or intermolecular active-site obstruction in fic proteins. Nature 482:107-110. doi: 10.1038/nature10729
13. Fernández-Sáiz V, Moro F, Arizmendi JM, Acebrón SP, Muga A. 2006. Ionic contacts at DnaK substrate binding domain involved in the allosteric regulation of lid dynamics. Journal of Biological Chemistry 281:7479-7488. doi: 10.1074/jbc.M512744200
14. Freiden PJ, Gaut JR, Hendershot LM. 1992. Interconversion of three differentially modified and assembled forms of BiP. The EMBO Journal 11:63-70.
15. Garcia-Pino A, Zenkin N, Loris R. 2014. The many faces of fic: structural and functional aspects of fic enzymes. Trends in Biochemical Sciences 39:121-129. doi: 10.1016/j.tibs.2014.01.001
16. Gaut JR, Hendershot LM. 1993. Mutations within the nucleotide binding site of immunoglobulin-binding protein inhibit ATPase activity and interfere with release of immunoglobulin heavy chain. The Journal of Biological Chemistry 268:7248-7255.
17. Gaut JR. 1997. In vivo threonine phosphorylation of immunoglobulin binding protein (biP) maps to its protein binding domain. Cell Stress & Chaperones 2:252-262. doi: 10.1379/1466-1268(1997)002<0252:IVTPOI>2.3.CO;2
18. Ham H, Woolery AR, Tracy C, Stenesen D, Kramer H, Orth K. 2014. Unfolded protein response-regulated drosophila fic (dFic) protein reversibly AMPylates BiP chaperone during endoplasmic reticulum homeostasis. Journal of Biological Chemistry 289:36059-36069. doi: 10.1074/jbc.M114.612515
19. Hendershot LM, Ting J, Lee AS. 1988. Identity of the immunoglobulin heavy-chain-binding protein with the 78, 000-dalton glucose-regulated protein and the role of posttranslational modifications in its binding function. Molecular and Cellular Biology 8:4250-4256. doi: 10.1128/MCB.8.10.4250
20. Kinch LN, Yarbrough ML, Orth K, Grishin NV, Kobe B. 2009. Fido, a novel AMPylation domain common to fic, doc, and AvrB. PLoS ONE 4:e5818. doi: 10.1371/journal.pone.0005818
21. Kityk R, Kopp J, Sinning I, Mayer MP. 2012. Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Molecular Cell 48:863-874. doi: 10.1016/j.molcel.2012.09.023
22. Klampf T, Gisslinger H, Harutyunyan AS, Nivarthi H, Rumi E, Milosevic JD, Them NCC, Berg T, Gisslinger B, Pietra D, Chen D, Vladimer GI, Bagienski K, Milanesi C, Casetti IC, Sant’Antonio E, Ferretti V, Elena C, Schischlik F, Cleary C, Six M, Schalling M, Schönegger A, Bock C, Malcovati L, Pascutto C, Superti-Furga G, Cazzola M, Kralovics R. 2013. Somatic mutations of calreticulin in myeloproliferative neoplasms. New England Journal of Medicine 369:2379-2390. doi: 10.1056/NEJMoa1311347
23. Kozutsumi Y, Segal M, Normington K, Gething M-J, Sambrook J. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332:462-464. doi: 10.1038/332462a0
24. Laitusis AL, Brostrom MA, Brostrom CO. 1999. The dynamic role of GRP78/BiP in the coordination of mRNA translation with protein processing. Journal of Biological Chemistry 274:486-493. doi: 10.1074/jbc.274.1.486
25. Laufen T, Mayer MP, Beisel C, Klostermeier D, Mogk A, Reinstein J, Bukau B. 1999. Mechanism of regulation of Hsp70 chaperones by DnaJ cochaperones. Proceedings of the National Academy of Sciences of the United States of America 96:5452-5457. doi: 10.1073/pnas.96.10.5452
26. LEDFORD BE, JACOBS DF. 1986. Translational control of ADP-ribosylation in eucaryotic cells. European Journal of Biochemistry 161:661-667. doi: 10.1111/j.1432-1033.1986.tb10491.x
27. LENO GH, LEDFORD BE. 1989. ADP-ribosylation of the 78-kDa glucose-regulated protein during nutritional stress. European Journal of Biochemistry 186:205-211. doi: 10.1111/j.1432-1033.1989.tb15196.x
28. Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M. 1991. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proceedings of the National Academy of Sciences of the United States of America 88:2874-2878. doi: 10.1073/pnas.88.7.2874
29. Logsdon CD. 1985. Glucocorticoids increase amylase mRNA levels, secretory organelles, and secretion in pancreatic acinar AR42J cells. The Journal of Cell Biology 100:1200-1208. doi: 10.1083/jcb.100.4.1200
30. Marcinowski M, Höller M, Feige MJ, Baerend D, Lamb DC, Buchner J. 2011. Substrate discrimination of the chaperone BiP by autonomous and cochaperone-regulated conformational transitions. Nature Structural & Molecular Biology 18:150-158. doi: 10.1038/nsmb.1970
31. Mayer MP. 2013. Hsp70 chaperone dynamics and molecular mechanism. Trends in Biochemical Sciences 38:507-514. doi: 10.1016/j.tibs.2013.08.001
32. Misselwitz B, Staeck O, Rapoport TA. 1998. J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences. Molecular Cell 2:593-603. doi: 10.1016/S1097-2765(00)80158-6
33. Novoa I, Zeng H, Harding HP, Ron D. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2. The Journal of Cell Biology 153:1011-1022. doi: 10.1083/jcb.153.5.1011
34. Paton AW, Beddoe T, Thorpe CM, Whisstock JC, Wilce MCJ, Rossjohn J, Talbot UM, Paton JC. 2006. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 443:548-552. doi: 10.1038/nature05124
35. Petrova K, Oyadomari S, Hendershot LM, Ron D. 2008. Regulated association of misfolded endoplasmic reticulum lumenal proteins with P58/DNAJc3. The EMBO Journal 27:2862-2872. doi: 10.1038/emboj.2008.199
36. Pincus D, Chevalier MW, Aragón T, van Anken E, Vidal SE, El-Samad H, Walter P, Kelly JW. 2010. BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biology 8: e1000415. doi: 10.1371/journal.pbio.1000415
37. Preissler S, Chambers JE, Crespillo-Casado A, Avezov E, Miranda E, Perez J, Hendershot LM, Harding HP, Ron D. 2015. Physiological modulation of BiP activity by trans -protomer engagement of the interdomain linker. eLife 4 e08961. doi: 10.7554/eLife.08961
38. Qi R, Sarbeng EB, Liu Q, Le KQ, Xu X, Xu H, Yang J, Wong JL, Vorvis C, Hendrickson WA, Zhou L, Liu Q. 2013. Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nature Structural & Molecular Biology 20:900-907. doi: 10.1038/nsmb.2583
39. Rahman M, Ham H, Liu X, Sugiura Y, Orth K, Kramer H. 2012. Visual neurotransmission in drosophila requires expression of fic in glial capitate projections. Nature Neuroscience 15:871-875. doi: 10.1038/nn.3102
40. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nature Protocols 8:2281-2308. doi: 10.1038/nprot.2013.143
41. Ronda C, Pedersen LE, Hansen HG, Kallehauge TB, Betenbaugh MJ, Nielsen AT, Kildegaard HF. 2014. Accelerating genome editing in CHO cells using CRISPR Cas9 and CRISPy, a web-based target finding tool. Biotechnology and Bioengineering 111:1604-1616. doi: 10.1002/bit.25233
42. Sanyal A, Chen AJ, Nakayasu ES, Lazar CS, Zbornik EA, Worby CA, Koller A, Mattoo S. 2015. A novel link between fic (filamentation induced by cAMP)-mediated Adenylylation/AMPylation and the unfolded protein response. Journal of Biological Chemistry 290:8482-8499. doi: 10.1074/jbc.M114.618348
43. Scorsone KA, Panniers R, Rowlands AG, Henshaw EC. 1987. Phosphorylation of eukaryotic initiation factor 2 during physiological stresses which affect protein synthesis. The Journal of Biological Chemistry 262:14538-14543.
44. Truttmann MC, Wu Q, Stiegeler S, Duarte JN, Ingram J, Ploegh HL. 2015. HypE-specific nanobodies as tools to modulate HypE-mediated target AMPylation. Journal of Biological Chemistry 290:9087-9100. doi: 10.1074/jbc.M114.634287
45. Tsunoda S, Avezov E, Zyryanova A, Konno T, Mendes-Silva L, Pinho Melo E, Harding HP, Ron D. 2014. Intact protein folding in the glutathione-depleted endoplasmic reticulum implicates alternative protein thiol reductants. eLife 3:e03421. doi: 10.7554/eLife.03421
46. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086. doi: 10.1126/science.1209038
47. Wei J, Gaut JR, Hendershot LM. 1995. In vitro dissociation of BiP-peptide complexes requires a conformational change in BiP after ATP binding but does not require ATP hydrolysis. Journal of Biological Chemistry 270: 26677-26682. doi: 10.1074/jbc.270.44.26677
48. Yang J, Nune M, Zong Y, Zhou L, Liu Q. 2015. Close and allosteric opening of the polypeptide-binding site in a human Hsp70 chaperone BiP. Structure 23:2191-2203. doi: 10.1016/j.str.2015.10.012
49. Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, Orth K. 2009. AMPylation of rho GTPases by vibrio VopS disrupts effector binding and downstream signaling. Science 323:269-272. doi: 10.1126/science.1166382