publication . Article . 2017

ER retention is imposed by COPII protein sorting and attenuated by 4-phenylbutyrate.

Wenfu Ma; Elena Goldberg; Jonathan Goldberg; Jonathan Goldberg;
Open Access
  • Published: 08 Jun 2017
  • Publisher: eLife Sciences Publications, Ltd
Abstract
Native cargo proteins exit the endoplasmic reticulum (ER) in COPII-coated vesicles, whereas resident and misfolded proteins are substantially excluded from vesicles by a retention mechanism that remains unresolved. We probed the ER retention process using the proteostasis regulator 4-phenylbutyrate (4-PBA), which we show targets COPII protein to reduce the stringency of retention. 4-PBA competes with p24 proteins to bind COPII. When p24 protein uptake is blocked, COPII vesicles package resident proteins and an ER-trapped mutant LDL receptor. We further show that 4-PBA triggers the secretion of a KDEL-tagged luminal resident, implying that a compromised retention...
Subjects
free text keywords: Research Article, Biophysics and Structural Biology, Cell Biology, COPII coat, vesicle transport, proteostasis, S. cerevisiae, Human, Transport protein, COPII, ER retention, Chemistry, Protein targeting, medicine.disease_cause, medicine, KDEL, Phenylbutyrate, Endoplasmic reticulum
Funded by
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| MOLECULAR GENETIC ANALYSIS OF THE DROSOPHILA 205K MAP
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F32GM012006-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
52 references, page 1 of 4

Adams, PD, Afonine, PV, Bunkóczi, G, Chen, VB, Davis, IW, Echols, N, Headd, JJ, Hung, LW, Kapral, GJ, Grosse-Kunstleve, RW, McCoy, AJ, Moriarty, NW, Oeffner, R, Read, RJ, Richardson, DC, Richardson, JS, Terwilliger, TC, Zwart, PH. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 213-221 [OpenAIRE] [PubMed] [DOI]

Adolf, F, Rhiel, M, Reckmann, I, Wieland, FT. Sec24C/D-isoform-specific sorting of the preassembled ER-Golgi Q-SNARE complex. Molecular Biology of the Cell. 2016; 27: 2697-2707 [OpenAIRE] [PubMed] [DOI]

Balch, WE, McCaffery, JM, Plutner, H, Farquhar, MG. Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell. 1994; 76: 841-852 [PubMed] [DOI]

Balch, WE, Morimoto, RI, Dillin, A, Kelly, JW. Adapting proteostasis for disease intervention. Science. 2008; 319: 916-919 [OpenAIRE] [PubMed] [DOI]

Barlowe, C, Orci, L, Yeung, T, Hosobuchi, M, Hamamoto, S, Salama, N, Rexach, MF, Ravazzola, M, Amherdt, M, Schekman, R. COPII: a membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell. 1994; 77: 895-907 [OpenAIRE] [PubMed] [DOI]

Barlowe, C, Helenius, A. Cargo Capture and Bulk flow in the early secretory pathway. Annual Review of Cell and Developmental Biology. 2016; 32: 197-222 [OpenAIRE] [PubMed] [DOI]

Beckers, CJ, Keller, DS, Balch, WE. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the golgi complex. Cell. 1987; 50: 523-534 [OpenAIRE] [PubMed] [DOI]

Belden, WJ, Barlowe, C. Deletion of yeast p24 genes activates the unfolded protein response. Molecular Biology of the Cell. 2001; 12: 957-969 [OpenAIRE] [PubMed] [DOI]

Bondulich, MK, Guo, T, Meehan, C, Manion, J, Rodriguez Martin, T, Mitchell, JC, Hortobagyi, T, Yankova, N, Stygelbout, V, Brion, JP, Noble, W, Hanger, DP. Tauopathy induced by low level expression of a human brain-derived tau fragment in mice is rescued by phenylbutyrate. Brain. 2016; 139: 2290-2306 [OpenAIRE] [PubMed] [DOI]

Bremser, M, Nickel, W, Schweikert, M, Ravazzola, M, Amherdt, M, Hughes, CA, Söllner, TH, Rothman, JE, Wieland, FT. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell. 1999; 96: 495-506 [OpenAIRE] [PubMed] [DOI]

Brusilow, SW. Phenylacetylglutamine may replace urea as a vehicle for waste nitrogen excretion. Pediatric Research. 1991; 29: 147-150 [OpenAIRE] [PubMed] [DOI]

Copic, A, Dorrington, M, Pagant, S, Barry, J, Lee, MC, Singh, I, Hartman, JL, Miller, EA. Genomewide analysis reveals novel pathways affecting endoplasmic reticulum homeostasis, protein modification and quality control. Genetics. 2009; 182: 757-769 [OpenAIRE] [PubMed] [DOI]

Copic, A, Latham, CF, Horlbeck, MA, D'Arcangelo, JG, Miller, EA. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science. 2012; 335: 1359-1362 [OpenAIRE] [PubMed] [DOI]

Dean, N, Pelham, HR. Recycling of proteins from the golgi compartment to the ER in yeast. The Journal of Cell Biology. 1990; 111: 369-377 [OpenAIRE] [PubMed] [DOI]

Elrod-Erickson, MJ, Kaiser, CA. Genes that control the fidelity of endoplasmic reticulum to golgi transport identified as suppressors of vesicle budding mutations. Molecular Biology of the Cell. 1996; 7: 1043-1058 [OpenAIRE] [PubMed] [DOI]

52 references, page 1 of 4
Abstract
Native cargo proteins exit the endoplasmic reticulum (ER) in COPII-coated vesicles, whereas resident and misfolded proteins are substantially excluded from vesicles by a retention mechanism that remains unresolved. We probed the ER retention process using the proteostasis regulator 4-phenylbutyrate (4-PBA), which we show targets COPII protein to reduce the stringency of retention. 4-PBA competes with p24 proteins to bind COPII. When p24 protein uptake is blocked, COPII vesicles package resident proteins and an ER-trapped mutant LDL receptor. We further show that 4-PBA triggers the secretion of a KDEL-tagged luminal resident, implying that a compromised retention...
Subjects
free text keywords: Research Article, Biophysics and Structural Biology, Cell Biology, COPII coat, vesicle transport, proteostasis, S. cerevisiae, Human, Transport protein, COPII, ER retention, Chemistry, Protein targeting, medicine.disease_cause, medicine, KDEL, Phenylbutyrate, Endoplasmic reticulum
Funded by
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| MOLECULAR GENETIC ANALYSIS OF THE DROSOPHILA 205K MAP
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F32GM012006-03
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
52 references, page 1 of 4

Adams, PD, Afonine, PV, Bunkóczi, G, Chen, VB, Davis, IW, Echols, N, Headd, JJ, Hung, LW, Kapral, GJ, Grosse-Kunstleve, RW, McCoy, AJ, Moriarty, NW, Oeffner, R, Read, RJ, Richardson, DC, Richardson, JS, Terwilliger, TC, Zwart, PH. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography. 2010; 66: 213-221 [OpenAIRE] [PubMed] [DOI]

Adolf, F, Rhiel, M, Reckmann, I, Wieland, FT. Sec24C/D-isoform-specific sorting of the preassembled ER-Golgi Q-SNARE complex. Molecular Biology of the Cell. 2016; 27: 2697-2707 [OpenAIRE] [PubMed] [DOI]

Balch, WE, McCaffery, JM, Plutner, H, Farquhar, MG. Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell. 1994; 76: 841-852 [PubMed] [DOI]

Balch, WE, Morimoto, RI, Dillin, A, Kelly, JW. Adapting proteostasis for disease intervention. Science. 2008; 319: 916-919 [OpenAIRE] [PubMed] [DOI]

Barlowe, C, Orci, L, Yeung, T, Hosobuchi, M, Hamamoto, S, Salama, N, Rexach, MF, Ravazzola, M, Amherdt, M, Schekman, R. COPII: a membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell. 1994; 77: 895-907 [OpenAIRE] [PubMed] [DOI]

Barlowe, C, Helenius, A. Cargo Capture and Bulk flow in the early secretory pathway. Annual Review of Cell and Developmental Biology. 2016; 32: 197-222 [OpenAIRE] [PubMed] [DOI]

Beckers, CJ, Keller, DS, Balch, WE. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the golgi complex. Cell. 1987; 50: 523-534 [OpenAIRE] [PubMed] [DOI]

Belden, WJ, Barlowe, C. Deletion of yeast p24 genes activates the unfolded protein response. Molecular Biology of the Cell. 2001; 12: 957-969 [OpenAIRE] [PubMed] [DOI]

Bondulich, MK, Guo, T, Meehan, C, Manion, J, Rodriguez Martin, T, Mitchell, JC, Hortobagyi, T, Yankova, N, Stygelbout, V, Brion, JP, Noble, W, Hanger, DP. Tauopathy induced by low level expression of a human brain-derived tau fragment in mice is rescued by phenylbutyrate. Brain. 2016; 139: 2290-2306 [OpenAIRE] [PubMed] [DOI]

Bremser, M, Nickel, W, Schweikert, M, Ravazzola, M, Amherdt, M, Hughes, CA, Söllner, TH, Rothman, JE, Wieland, FT. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell. 1999; 96: 495-506 [OpenAIRE] [PubMed] [DOI]

Brusilow, SW. Phenylacetylglutamine may replace urea as a vehicle for waste nitrogen excretion. Pediatric Research. 1991; 29: 147-150 [OpenAIRE] [PubMed] [DOI]

Copic, A, Dorrington, M, Pagant, S, Barry, J, Lee, MC, Singh, I, Hartman, JL, Miller, EA. Genomewide analysis reveals novel pathways affecting endoplasmic reticulum homeostasis, protein modification and quality control. Genetics. 2009; 182: 757-769 [OpenAIRE] [PubMed] [DOI]

Copic, A, Latham, CF, Horlbeck, MA, D'Arcangelo, JG, Miller, EA. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science. 2012; 335: 1359-1362 [OpenAIRE] [PubMed] [DOI]

Dean, N, Pelham, HR. Recycling of proteins from the golgi compartment to the ER in yeast. The Journal of Cell Biology. 1990; 111: 369-377 [OpenAIRE] [PubMed] [DOI]

Elrod-Erickson, MJ, Kaiser, CA. Genes that control the fidelity of endoplasmic reticulum to golgi transport identified as suppressors of vesicle budding mutations. Molecular Biology of the Cell. 1996; 7: 1043-1058 [OpenAIRE] [PubMed] [DOI]

52 references, page 1 of 4
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