A high-coverage shrna screen identifies TMEM129 as an E3 ligase involved in ER-associated protein degradation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Van De Weijer, Michael L ^a   Bassik, Michael C ^b,g   Luteijn, Rutger D ^a   Voorburg, Cornelia M ^a   Lohuis, Mirjam A M ^a   Kremmer, Elisabeth ^c   Hoeben, Rob C ^d   Leproust, Emily M ^e,h   Chen, Siyuan ^e,h   Hoelen, Hanneke ^a   Ressing, Maaike E ^a,d   Patena, Weronika ^b,f,i   Weissman, Jonathan S ^b   McManus, Michael T ^f   Wiertz, Emmanuel J H J ^a   Lebbink, Robert Jan ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e AGILENT TECHNOLOGIES   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g STANFORD UNIVERSITY   (United States)

^h Twist Bioscience   (United States)

ⁱ GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DERLIN 1 PROTEIN; DERLIN 2 PROTEIN; HLA ANTIGEN CLASS 1; PROTEIN P97; SHORT HAIRPIN RNA; TMEM129 PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UNCLASSIFIED DRUG; VIMP PROTEIN; ADENOSINE TRIPHOSPHATASE; DERL1 PROTEIN, HUMAN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; P97 ATPASE; PROTEIN; RNA BINDING PROTEIN; SEL1L PROTEIN, HUMAN; SELENOPROTEIN; SMALL INTERFERING RNA; TMEM129 PROTEIN, HUMAN; UBE2J2 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE; US11 PROTEIN, HERPESVIRUS; VIMP PROTEIN, HUMAN; VIRUS PROTEIN;

ENZYME ACTIVITY; GENOME; INFECTIOUS DISEASE; PROTEIN; PUBLIC HEALTH; SUBSTRATE; VIRUS;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; GENE LIBRARY; GENETIC ASSOCIATION; GENETIC SCREENING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; RAT; RNA LIBRARY; BIOSYNTHESIS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; ENDOPLASMIC RETICULUM; GENETICS; HEK293 CELL LINE; PATHOLOGY; PROTEIN FOLDING; RNA INTERFERENCE; TUMOR CELL LINE; U937 CELL LINE;

ADENOSINE TRIPHOSPHATASES; CELL LINE, TUMOR; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DOWN-REGULATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HEK293 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MEMBRANE PROTEINS; NUCLEAR PROTEINS; PROTEIN FOLDING; PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SELENOPROTEINS; U937 CELLS; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; VIRAL PROTEINS;

EID: 84900018251     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4832     Document Type: Article

References (53)

1. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M. & Hartl, F. U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355 (2013).
2. Hampton, R. Y. ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell Biol. 14, 476-482 (2002).
3. Amm, I., Sommer, T. & Wolf, D. H. Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim. Biophys. Acta 1843, 182-196 (2014).
4. Finley, D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513 (2009).
5. Merulla, J., Fasana, E., Soldà, T. & Molinari, M. Specificity and regulation of the endoplasmic reticulum-associated degradation machinery. Traffic 14, 767-777 (2013).
6. Needham, P. G. & Brodsky, J. L. How early studies on secreted and membrane protein quality control gave rise to the ER associated degradation (ERAD) pathway: the early history of ERAD. Biochim. Biophys. Acta 1833, 2447-2457 (2013).
7. Smith, M. H., Ploegh, H. L. & Weissman, J. S. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334, 1086-1090 (2011).
8. Christianson, J. C. et al. Defining human ERAD networks through an integrative mapping strategy. Nat. Cell Biol. 14, 93-105 (2011).
9. Hampton, R. Y. & Rine, J. Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J. Cell Biol. 125, 299-312 (1994).
10. Hampton, R. Y. & Bhakta, H. Ubiquitin-mediated regulation of 3-hydroxy-3-methylglutaryl-CoA reductase. Proc. Natl Acad. Sci. USA 94, 12944-12948 (1997).
11. Hansen, T. H. & Bouvier, M. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9, 503-513 (2009).
12. Pinto, A. K. & Hill, A. B. Viral interference with antigen presentation to CD8 T cells: lessons from cytomegalovirus. Viral Immunol. 18, 434-444 (2005).
13. Wiertz, E. J. et al. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779 (1996).
14. Lilley, B. N., Tortorella, D. & Ploegh, H. L. Dislocation of a type I membrane protein requires interactions between membrane-spanning segments within the lipid bilayer. Mol. Biol. Cell 14, 3690-3698 (2003).
15. Lilley, B. N. & Ploegh, H. L. A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429, 834-840 (2004).
16. Cho, S., Lee, M. & Jun, Y. Forced interaction of cell surface proteins with Derlin-1 in the endoplasmic reticulum is sufficient to induce their dislocation into the cytosol for degradation. Biochem. Biophys. Res. Commun. 430, 787-792 (2013).
17. Ye, Y., Shibata, Y., Yun, C., Ron, D. & Rapoport, T. a. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429, 841-847 (2004).
18. Ye, Y., Meyer, H. H. & Rapoport, T. A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656 (2001).
19. Lilley, B. N. & Ploegh, H. L. Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl Acad. Sci. USA 102, 14296-14301 (2005).
20. Kikkert, M. et al. Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of MHC class I molecules from the endoplasmic reticulum to the cytosol. Biochem. J. 358, 369-377 (2001).
21. Shamu, C. E., Flierman, D., Ploegh, H. L., Rapoport, T. A. & Chau, V. Polyubiquitination is required for US11-dependent movement of MHC class I heavy chain from endoplasmic reticulum into cytosol. Mol. Biol. Cell 12, 2546-2555 (2001).
22. Mueller, B., Lilley, B. N. & Ploegh, H. L. SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J. Cell Biol. 175, 261-270 (2006).
23. Claessen, J. H. L., Kundrat, L. & Ploegh, H. L. Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol. 22, 22-32 (2012).
24. Bays, N. W., Gardner, R. G., Seelig, L. P., Joazeiro, C. A. & Hampton, R. Y. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3, 24-29 (2001).
25. Swanson, R., Locher, M. & Hochstrasser, M. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation. Genes Dev. 15, 2660-2674 (2001).
26. Kikkert, M. et al. Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J. Biol. Chem. 279, 3525-3534 (2004).
27. Fang, S. et al. The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 98, 14422-14427 (2001).
28. Hassink, G. et al. TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum. Biochem. J. 388, 647-655 (2005).
29. Stagg, H. R. et al. The TRC8 E3 ligase ubiquitinates MHC class I molecules before dislocation from the ER. J. Cell Biol. 186, 685-692 (2009).
30. Deshaies, R. J. & Joazeiro, C. A. P. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434 (2009).
31. Chang, K., Elledge, S. J. & Hannon, G. J. Lessons from nature: microRNA-based shRNA libraries. Nat. Methods 3, 707-714 (2006).
32. Reynolds, A. et al. Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326-330 (2004).
33. Bassik, M. C. et al. Rapid creation and quantitative monitoring of high coverage shRNA libraries. Nat. Methods 6, 443-445 (2009).
34. Bassik, M. C. et al. A systematic mammalian genetic interaction map reveals pathways underlying ricin susceptibility. Cell 152, 909-922 (2013).
35. Silva, J. M. et al. Profiling essential genes in human mammary cells by multiplex RNAi screening. Science 319, 617-620 (2008).
36. Matheny, C. J. et al. Next-generation NAMPT inhibitors identified by sequential high-throughput phenotypic chemical and functional genomic screens. Chem. Biol. 20, 1352-1363 (2013).
37. Schekman, R. & Orci, L. Coat proteins and vesicle budding. Science 271, 1526-1533 (1996).
38. Ye, Y. & Rape, M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755-764 (2009).
39. Flierman, D., Coleman, C. S., Pickart, C. M., Rapoport, T. A. & Chau, V. E2-25K mediates US11-triggered retro-translocation of MHC class I heavy chains in a permeabilized cell system. Proc. Natl Acad. Sci. USA 103, 11589-11594 (2006).
40. Paulsson, K. M. et al. Association of tapasin and COPI provides a mechanism for the retrograde transport of major histocompatibility complex (MHC) class I molecules from the Golgi complex to the endoplasmic reticulum. J. Biol. Chem. 277, 18266-18271 (2002).
41. Hanzawa, H. et al. The structure of the C4C4 ring finger of human NOT4 reveals features distinct from those of C3HC4 RING fingers. J. Biol. Chem. 276, 10185-10190 (2001).
42. Burr, M. L. et al. HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. Proc. Natl Acad. Sci. USA 108, 2034-2039 (2011).
43. Mueller, B., Klemm, E. J., Spooner, E., Claessen, J. H. & Ploegh, H. L. SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc. Natl Acad. Sci. USA 105, 12325-12330 (2008).
44. Lenk, U. et al. A role for mammalian Ubc6 homologues in ER-associated protein degradation. J. Cell Sci. 115, 3007-3014 (2002).
45. Flierman, D., Ye, Y., Dai, M., Chau, V. & Rapoport, T. A. Polyubiquitin serves as a recognition signal, rather than a ratcheting molecule, during retrotranslocation of proteins across the endoplasmic reticulum membrane. J. Biol. Chem. 278, 34774-34782 (2003).
46. Christensen, D. E., Brzovic, P. S. & Klevit, R. E. E2-BRCA1 RING interactions dictate synthesis of mono-or specific polyubiquitin chain linkages. Nat. Struct. Mol. Biol. 14, 941-948 (2007).
47. Burr, M. L. et al. MHC class I molecules are preferentially ubiquitinated on endoplasmic reticulum luminal residues during HRD1 ubiquitin E3 ligase-mediated dislocation. Proc. Natl Acad. Sci. USA 110, 14290-14295 (2013).
48. Wiertz, E. J. et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438 (1996).
49. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
50. Paddison, P. J. et al. Cloning of short hairpin RNAs for gene knockdown in mammalian cells. Nat. Methods 1, 163-167 (2004).
51. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
52. Huang, D. W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
53. Huang, D. W., Sherman, B. T. & Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).