Genomewide analysis reveals novel pathways affecting endoplasmic eticulum homeostasis, protein modification and quality control

Genetics

Volumn 182, Issue 3, 2009, Pages 757-769

  Čopič, Alenka ^a   Dorrington, Mariana ^a   Pagant, Silvere ^a   Barry, Justine ^a   Lee, Marcus C S ^b   Singh, Indira ^c   Hartman IV, John L ^c   Miller, Elizabeth A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b University of Alabama ^*  (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; FUNGAL PROTEIN; GENE PRODUCT; GLYCOPHOSPHOLIPID; HISTONE; KAR2P PROTEIN; UNCLASSIFIED DRUG; ERD2 PROTEIN, S CEREVISIAE; HEAT SHOCK PROTEIN 70; HTZ1 PROTEIN, S CEREVISIAE; KAR2 PROTEIN, YEAST; RECEPTOR; SACCHAROMYCES CEREVISIAE PROTEIN;

ACETYLATION; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGAL GENE; FUNGAL STRAIN; FUNGUS IDENTIFICATION; FUNGUS MUTANT; GENE FUNCTION; GENE IDENTIFICATION; GENE INSERTION; GENETIC VARIABILITY; GENOME ANALYSIS; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; YEAST; BIOLOGICAL MODEL; CHEMISTRY; FUNGAL GENOME; GENETICS; GLYCOSYLATION; GOLGI COMPLEX; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE;

ACETYLATION; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GENOME, FUNGAL; GLYCOSYLATION; GOLGI APPARATUS; HISTONES; HOMEOSTASIS; HSP70 HEAT-SHOCK PROTEINS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MODELS, BIOLOGICAL; MUTATION; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, PEPTIDE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 70349318145     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.101105     Document Type: Article

References (56)

1. AGUILERA-ROMERO, A., J. KAMINSKA, A. SPANG, H. RIEZMAN and M. MUNIZ, 2008 The yeast p24 complex is required for the formation of COPI retrograde transport vesicles from the Golgi apparatus. J. Cell Biol. 180: 713-720.
2. ANELLI, T., and R. SITIA, 2008 Protein quality control in the early secretory pathway. EMBO J. 27: 315-327.
3. BABIARZ, J. E., J. E. HALLEY and J. RINE, 2006 Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev. 20: 700-710.
4. BARLOWE, C., 2003 Molecular recognition of cargo by the COPII complex: a most accommodating coat. Cell 114: 395-397.
5. BEH, C. T., and M. D. ROSE, 1995 Two redundant systems maintain levels of resident proteins within the yeast endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92: 9820-9823.
6. BELDEN, W. J., and C. BARLOWE, 1996 Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport. J. Biol. Chem. 271: 26939-26946.
7. BELDEN, W. J., and C. BARLOWE, 2001 Deletion of yeast p24 genes activates the unfolded protein response. Mol. Biol. Cell 12: 957-969.
8. BENNETT, M. K., 1995 SNAREs and the specificity of transport vesicle targeting. Curr. Opin. Cell Biol. 7: 581-586.
9. BONANGELINO, C. J., E. M. CHAVEZ and J. S. BONIFACINO, 2002 Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol. Biol. Cell 13: 2486-2501.
10. BOONE, C., H. BUSSEY and B. J. ANDREWS, 2007 Exploring genetic interactions and networks with yeast. Nat. Rev. 8: 437-449.
11. BREITKREUTZ, B. J., C. STARK and M. TYERS, 2003 Osprey: a network visualization system. Genome Biol. 4: R22.
12. BURRI, L., O. VARLAMOV, C. A. DOEGE, K. HOFMANN, T. BEILHARZ et al., 2003 A SNARE required for retrograde transport to the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 100: 9873-9877.
13. CALDWELL, S. R., K. J. HILL and A. A. COOPER, 2001 Degradation of endoplasmic reticulum (ER) quality control substrates requires transport between the ER and Golgi. J. Biol. Chem. 276: 23296-23303.
14. COLLINS, S. R., K. M. MILLER, N. L. MAAS, A. ROGUEV, J. FILLINGHAM et al., 2007 Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806-810.
15. CRAVEN, R. A., M. EGERTON and C. J. STIRLING, 1996 A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J. 15: 2640-2650.
16. DILCHER, M., B. VEITH, S. CHIDAMBARAM, E. HARTMANN, H. D. SCHMITT et al., 2003 Use1p is a yeast SNARE protein required for retrograde traffic to the ER. EMBO J. 22: 3664-3674.
17. ELLGAARD, L., and A. HELENIUS, 2003 Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 4: 181-191.
18. ELROD-ERICKSON, M. J., and C. A. KAISER, 1996 Genes that control the fidelity of endoplasmic reticulum to Golgi transport identified as suppressors of vesicle budding mutations. Mol. Biol. Cell 7: 1043-1058.
19. FLEISCHER, T. C., C. M. WEAVER, K. J. MCAFEE, J. L. JENNINGS and A. J. LINK, 2006 Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 20: 1294-1307.
20. GHAEMMAGHAMI, S., W. K. HUH, K. BOWER, R. W. HOWSON, A. BELLE et al., 2003 Global analysis of protein expression in yeast. Nature 425: 737-741. (Pubitemid 37314318)
21. GURKAN, C., S. M. STAGG, P. LAPOINTE and W. E. BALCH, 2006 The COPII cage: unifying principles of vesicle coat assembly. Nat. Rev. Mol. Cell. Biol. 7: 727-738.
22. HAASS, F. A., M. JONIKAS, P. WALTER, J. S. WEISSMAN, Y. N. JAN et al., 2007 Identification of yeast proteins necessary for cell-surface function of a potassium channel. Proc. Natl. Acad. Sci. USA 104: 18079-18084.
23. ITO, T., T. CHIBA, R. OZAWA, M. YOSHIDA, M. HATTORI et al., 2001 A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98: 4569-4574.
24. JONIKAS, M. C., S. R. COLLINS, V. DENIC, E. OH, E. M. QUAN et al., 2009 Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323: 1693-1697.
25. KAJIWARA, K., R. WATANABE, H. PICHLER, K. IHARA, S. MURAKAMI et al., 2008 Yeast ARV1 is required for efficient delivery of an early GPI intermediate to the first mannosyltransferase during GPI assembly and controls lipid flow from the endoplasmic reticulum. Mol. Biol. Cell 19: 2069-2082.
26. KEOGH, M. C., T. A. MENNELLA, C. SAWA, S. BERTHELET, N. J. KROGAN et al., 2006 The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev. 20: 660-665.
27. KINCAID, M. M., and A. A. COOPER, 2007 Misfolded proteins traffic from the endoplasmic reticulum (ER) due to ER export signals. Mol. Biol. Cell 18: 455-463.
28. KLUMPERMAN, J., 2000 Transport between ER and Golgi. Curr. Opin. Cell Biol. 12: 445-449.
29. KOBOR, M. S., S. VENKATASUBRAHMANYAM, M. D. MENEGHINI, J. W. GIN, J. L. JENNINGS et al., 2004 A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2: E131.
30. KROGAN, N. J., G. CAGNEY, H. YU, G. ZHONG, X. GUO et al., 2006 Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
31. LEE, M. C., E. A. MILLER, J. GOLDBERG, L. ORCI and R. SCHEKMAN, 2004 Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20: 87-123.
32. LEHLE, L., S. STRAHL and W. TANNER, 2006 Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. Engl. 45: 6802-6818.
33. LOCKSHON, D., L. E. SURFACE, E. O. KERR, M. KAEBERLEIN and B. K. KENNEDY, 2007 The sensitivity of yeast mutants to oleic acid implicates the peroxisome and other processes in membrane function. Genetics 175: 77-91.
34. MARZIOCH, M., D. C. HENTHORN, J. M. HERRMANN, R. WILSON, D. Y. THOMAS ET al., 1999 Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex. Mol. Biol. Cell 10: 1923-1938.
35. MENEGHINI, M. D., M. WU and H. D. MADHANI, 2003 Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725-736.
36. MEZZACASA, A., and A. HELENIUS, 2002 The transitional ER defines a boundary for quality control in the secretion of tsO45 VSV glycoprotein. Traffic 3: 833-849.
37. MUNIZ, M., C. NUOFFER, H. P. HAURI and H. RIEZMAN, 2000 The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles. J. Cell Biol. 148: 925-930.
38. NG, D. T., E. D. SPEAR and P. WALTER, 2000 The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J. Cell Biol. 150: 77-88.
39. ORLEAN, P., and A. K. MENON, 2007 Thematic review series: lipid posttranslational modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids. J. Lipid Res. 48: 993-1011.
40. OTTE, S., and C. BARLOWE, 2004 Sorting signals can direct receptor-mediated export of soluble proteins into COPII vesicles. Nat. Cell. Biol. 6: 1189-1194.
41. PAGANT, S., L. KUNG, M. DORRINGTON, M. C. LEE and E. A. MILLER, 2007 Inhibiting endoplasmic reticulum(ER)-associated degradation of misfolded Yor1p does not permit ER export despite the presence of a diacidic sorting signal. Mol. Biol. Cell 18: 3398-3413.
42. PELHAM, H. R., K. G. HARDWICK and M. J. LEWIS, 1988 Sorting of soluble ER proteins in yeast. EMBO J. 7: 1757-1762.
43. RON, D., 2002 Proteotoxicity in the endoplasmic reticulum: lessons from the Akita diabetic mouse. J. Clin. Invest. 109: 443-445.
44. SANTOS-ROSA, H., J. LEUNG, N. GRIMSEY, S. PEAK-CHEW and S. SINIOSSOGLOU, 2005 The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J. 24: 1931-1941.
45. SCHULDINER, M., S. R. COLLINS, N. J. THOMPSON, V. DENIC, A. BHAMIDIPATI et al., 2005 Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
46. SCHULDINER, M., J. METZ, V. SCHMID, V. DENIC, M. RAKWALSKA et al., 2008 The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134: 634-645.
47. SEMENZA, J. C., K. G. HARDWICK, N. DEAN and H. R. PELHAM, 1990 ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61: 1349-1357. (Pubitemid 20208838)
48. SINGH, I., R. PASS, S. O. TOGAY, J. W. RODGERS and J. L. HARTMAN, IV, 2009 Stringent mating-type-regulated auxotrophy increases the accuracy of systematic genetic interaction screens with Saccharomyces cerevisiae mutant arrays. Genetics 181: 289-300.
49. SPEAR, E. D., and D. T. NG, 2003 Stress tolerance of misfolded carboxypeptidase Y requires maintenance of protein trafficking and degradative pathways. Mol. Biol. Cell 14: 2756-2767.
50. TOWNSLEY, F. M., G. FRIGERIO and H. R. PELHAM, 1994 Retrieval of HDEL proteins is required for growth of yeast cells. J. Cell Biol. 127: 21-28.
51. TRAVERS, K. J., C. K. PATIL, L. WODICKA, D. J. LOCKHART, J. S. WEISSMAN et al., 2000 Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
52. VASHIST, S., W. KIM, W. J. BELDEN, E. D. SPEAR, C. BARLOWE et al., 2001 Distinct retrieval and retention mechanisms are required for the quality control of endoplasmic reticulum protein folding. J. Cell Biol. 155: 355-368.
53. WELCH, W. J., 2004 Role of quality control pathways in human diseases involving protein misfolding. Semin. Cell Dev. Biol. 15: 31-38.
54. WINZELER, E. A., D. D. SHOEMAKER, A. ASTROMOFF, H. LIANG, K. ANDERSON et al., 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906. (Pubitemid 29381993)
55. WRIGHT, R., M. L. PARRISH, E. CADERA, L. LARSON, C. K. MATSON et al., 2003 Parallel analysis of tagged deletion mutants efficiently identifies genes involved in endoplasmic reticulum biogenesis. Yeast 20: 881-892.
56. ZOU, Z., C. C. DIRUSSO, V. CTRNACTA and P. N. BLACK, 2002 Fatty acid transport in Saccharomyces cerevisiae. Directed mutagenesis of FAT1 distinguishes the biochemical activities associated with Fat1p. J. Biol. Chem. 277: 31062-31071.