Derlin-dependent accumulation of integral membrane proteins at cell surfaces

Journal of Cell Science

Volumn 122, Issue 13, 2009, Pages 2228-2239

  Schaheen, Basil ^a   Dang, Hope ^a   Fares, Hanna ^a  

^a University of Arizona   (United States)

Author keywords

Derlin; Membrane trafficking; Quality control

Indexed keywords

DERLIN PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MEMBRANE PROTEIN; PROTEASOME INHIBITOR; PROTEIN CUP 2; PROTEIN MCA 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CAENORHABDITIS ELEGANS; CELL MEMBRANE TRANSPORT; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENDOSOME; FEMALE; GENE IDENTIFICATION; LOSS OF FUNCTION MUTATION; MACROPHAGE; MALE; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; PHENOTYPE; PLASMA HALF LIFE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA INTERFERENCE;

ANIMALS; BASE SEQUENCE; BIOLOGICAL MARKERS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MEMBRANE; ENDOCYTOSIS; MACROPHAGES; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHYLOGENY; PROTEIN FOLDING; RECEPTORS, LDL; RECOMBINANT FUSION PROTEINS;

CAENORHABDITIS ELEGANS; EUKARYOTA;

EID: 69449085020     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.048892     Document Type: Article

References (77)

1. Altun-Gultekin, Z., Andachi, Y., Tsalik, E. L., Pilgrim, D., Kohara, Y. and Hobert, O. (2001). A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128, 1951-1969.
2. Bader, N., Jung, T. and Grune, T. (2007). The proteasome and its role in nuclear protein maintenance. Exp. Gerontol. 42, 864-870.
3. Bednarek, E. M., Schaheen, L., Gaubatz, J., Jorgensen, E. M. and Fares, H. (2007). The plasma membrane calcium ATPase MCA-3 is required for clathrin-mediated endocytosis in scavenger cells of Caenorhabditis elegans. Traffic 8, 543-553.
4. Benharouga, M., Haardt, M., Kartner, N. and Lukacs, G. L. (2001). COOH-terminal truncations promote proteasome-dependent degradation of mature cystic fibrosis transmembrane conductance regulator from post-Golgi compartments. J. Cell Biol. 153, 957-970.
5. Berthoud, V. M., Minogue, P. J., Laing, J. G. and Beyer, E. C. (2004). Pathways for degradation of connexins and gap junctions. Cardiovasc. Res. 62, 256-267.
6. 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.
7. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
8. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G. and Ron, D. (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
9. Cory, A. H., Owen, T. C., Barltrop, J. A. and Cory, J. G. (1991). Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 3, 207-212.
10. Cox, J. S. and Walter, P. (1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87, 391-404.
11. Cox, J. S., Shamu, C. E. and Walter, P. (1993). Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206.
12. Curry, H., Alvarez, G. R., Zwilling, B. S. and Lafuse, W. P. (2004). Toll-like receptor 2 stimulation decreases IFN-gamma receptor expression in mouse RAW264.7 macrophages. J. Interferon Cytokine Res. 24, 699-710.
13. Dang, H., Li, Z., Skolnik, E. Y. and Fares, H. (2004). Disease-related myotubularins function in endocytic traffic in Caenorhabditis elegans. Mol. Biol. Cell 15, 189-196.
14. Fares, H. and Greenwald, I. (2001a). Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159, 133-145.
15. Fares, H. and Greenwald, I. (2001b). Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat. Genet. 28, 64-68.
16. Frank, S., Upender, S., Hansen, S. H. and Casanova, J. E. (1998). ARNO is a guanine nucleotide exchange factor for ADP-ribosylation factor 6. J. Biol. Chem. 273, 23-27.
17. Goldberg, A. L. (2003). Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899.
18. Gong, X. and Chang, A. (2001). A mutant plasma membrane ATPase, Pma1-10, is defective in stability at the yeast cell surface. Proc. Natl. Acad. Sci. USA 98, 9104-9109.
19. Grant, B. and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
20. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H. and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579.
21. Greener, T., Grant, B., Zhang, Y., Wu, X., Greene, L. E., Hirsh, D. and Eisenberg, E. (2001). Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat. Cell Biol. 3, 215-219.
22. Hampton, R. Y. (2002). ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell Biol. 14, 476-482.
23. Harding, H. P., Zhang, Y. and Ron, D. (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274.
24. Haze, K., Yoshida, H., Yanagi, H., Yura, T. and Mori, K. (1999). Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10, 3787-3799.
25. Hitt, R. and Wolf, D. H. (2004). Der1p, a protein required for degradation of malfolded soluble proteins of the endoplasmic reticulum: topology and Der1-like proteins. FEMS Yeast Res. 4, 721-729.
26. Iwawaki, T., Hosoda, A., Okuda, T., Kamigori, Y., Nomura-Furuwatari, C., Kimata, Y., Tsuru, A. and Kohno, K. (2001). Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat. Cell Biol. 3, 158-164.
27. Jarosch, E., Lenk, U. and Sommer, T. (2003). Endoplasmic reticulum-associated protein degradation. Int. Rev. Cytol. 223, 39-81.
28. Kamath, R. S. and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
29. Kimata, Y., Oikawa, D., Shimizu, Y., Ishiwata-Kimata, Y. and Kohno, K. (2004). A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J. Cell Biol. 167, 445-456.
30. Knop, M., Finger, A., Braun, T., Hellmuth, K. and Wolf, D. H. (1996). Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J. 15, 753-763.
31. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H., Mori, K. and Kaufman, R. J. (2002). IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16, 452-466.
32. Lilley, B. N. and Ploegh, H. L. (2004). A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429, 834-840.
33. Lilley, B. N. and Ploegh, H. L. (2005). Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 102, 14296-14301.
34. Lin, S. X., Grant, B., Hirsh, D. and Maxfield, F. R. (2001). Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3, 567-572.
35. Ljunggren, H. G., Stam, N. J., Ohlen, C., Neefjes, J. J., Hoglund, P., Heemels, M. T., Bastin, J., Schumacher, T. N., Townsend, A., Karre, K. et al. (1990). Empty MHC class I molecules come out in the cold. Nature 346, 476-480.
36. Martin de Llano, J. J., Fuertes, G., Andreu, E. J., Puig, O., Chaves, F. J., Soutar, A. K., Armengod, M. E. and Knecht, E. (2006). A single point mutation in the low-density lipoprotein receptor switches the degradation of its mature protein from the proteasome to the lysosome. Int. J. Biochem. Cell Biol. 38, 1340-1351.
37. Matlack, K. E., Mothes, W. and Rapoport, T. A. (1998). Protein translocation: tunnel vision. Cell 92, 381-390.
38. Maxfield, F. R. and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell. Biol. 5, 121-132.
39. McCracken, A. A. and Brodsky, J. L. (2003). Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD). BioEssays 25, 868-877.
40. Meusser, B., Hirsch, C., Jarosch, E. and Sommer, T. (2005). ERAD: the long road to destruction. Nat. Cell Biol. 7, 766-772.
41. Miura, H., Tomoda, H., Miura, K., Takishima, K. and Omura, S. (1996). Lactacystin increases LDL receptor level on HepG2 cells. Biochem. Biophys. Res. Commun. 227, 684-687.
42. Mori, K., Ma, W., Gething, M. J. and Sambrook, J. (1993). A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756.
43. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
44. Oda, Y., Okada, T., Yoshida, H., Kaufman, R. J., Nagata, K. and Mori, K. (2006). Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J. Cell Biol. 172, 383-393.
45. Okamura, K., Kimata, Y., Higashio, H., Tsuru, A. and Kohno, K. (2000). Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun. 279, 445-450.
46. Patton, A., Knuth, S., Schaheen, B., Dang, H., Greenwald, I. and Fares, H. (2005). Endocytosis function of a ligand-gated ion channel homolog in Caenorhabditis elegans. Curr. Biol. 15, 1045-1050.
47. Pizzirusso, M. and Chang, A. (2004). Ubiquitin-mediated targeting of a mutant plasma membrane ATPase, Pma1-7, to the endosomal/vacuolar system in yeast. Mol. Biol. Cell 15, 2401-2409
48. Praitis, V., Casey, E., Collar, D. and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226.
49. Richly, H., Rape, M., Braun, S., Rumpf, S., Hoege, C. and Jentsch, S. (2005). A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120, 73-84.
50. Rolls, M. M., Hall, D. H., Victor, M., Stelzer, E. H. and Rapoport, T. A. (2002). Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol. Biol. Cell 13, 1778-1791.
51. Sambrook, J., Fritch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
52. Sato, M., Sato, K. and Nakano, A. (2002). Evidence for the intimate relationship between vesicle budding from the ER and the unfolded protein response. Biochem. Biophys. Res. Commun. 296, 560-567.
53. Sato, M., Sato, K., Fonarev, P., Huang, C. J., Liou, W. and Grant, B. D. (2005). Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat. Cell Biol. 7, 559-569.
54. Schekman, R. (2004). Cell biology: a channel for protein waste. Nature 429, 817-818.
55. Schroder, M. and Kaufman, R. J. (2005). ER stress and the unfolded protein response. Mutat. Res. 569, 29-63.
56. Schulze, A., Standera, S., Buerger, E., Kikkert, M., van Voorden, S., Wiertz, E., Koning, F., Kloetzel, P. M. and Seeger, M. (2005). The ubiquitin-domain Protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J. Mol. Biol. 354, 1021-1027.
57. Shaffer, A. L., Shapiro-Shelef, M., Iwakoshi, N. N., Lee, A. H., Qian, S. B., Zhao, H., Yu, X., Yang, L., Tan, B. K., Rosenwald, A. et al. (2004). XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21, 81-93.
58. Sharma, M., Pampinella, F., Nemes, C., Benharouga, M., So, J., Du, K., Bache, K. G., Papsin, B., Zerangue, N., Stenmark, H. et al. (2004). Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J. Cell Biol. 164, 923-933.
59. Shen, X., Ellis, R. E., Lee, K., Liu, C. Y., Yang, K., Solomon, A., Yoshida, H., Morimoto, R., Kurnit, D. M., Mori, K. et al. (2001). Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107, 893-903.
60. Sidrauski, C. and Walter, P. (1997). The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031-1039.
61. Sitia, R. and Braakman, I. (2003). Quality control in the endoplasmic reticulum protein factory. Nature 426, 891-894.
62. Sriburi, R., Jackowski, S., Mori, K. and Brewer, J. W. (2004). XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167, 35-41.
63. Taxis, C., Hitt, R., Park, S. H., Deak, P. M., Kostova, Z. and Wolf, D. H. (2003). Use of modular substrates demonstrates mechanistic diversity and reveals differences in chaperone requirement of ERAD. J. Biol. Chem. 278, 35903-35913.
64. Thompson, E. G., Schaheen, L., Dang, H. and Fares, H. (2007). Lysosomal trafficking functions of mucolipin-1 in murine macrophages. BMC Cell Biol. 8, 54.
65. Timmons, L. and Fire, A. (1998). Specific interference by ingested dsRNA. Nature 395, 854.
66. Treusch, S., Knuth, S., Slaugenhaupt, S. A., Goldin, E., Grant, B. D. and Fares, H. (2004). Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc. Natl. Acad. Sci. USA 101, 4483-4488.
67. Unkeless, J. C. (1979). Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J. Exp. Med. 150, 580-596.
68. van't Hof, W. and Resh, M. D. (1997). Rapid plasma membrane anchoring of newly synthesized p59fyn: selective requirement for NH2-terminal myristoylation and palmitoylation at cysteine-3. J. Cell Biol. 136, 1023-1035.
69. von Mikecz, A. (2006). The nuclear ubiquitin-proteasome system. J. Cell Sci. 119, 1977-1984.
70. Wilson, M. H., Highfield, H. A. and Limbird, L. E. (2001). The role of a conserved inter-transmembrane domain interface in regulating alpha(2a)-adrenergic receptor conformational stability and cell-surface turnover. Mol. Pharmacol. 59, 929-938.
71. Xue, Y., Fares, H., Grant, B., Li, Z., Rose, A. M., Clark, S. G. and Skolnik, E. Y. (2003). Genetic analysis of the myotubularin family of phosphatases in Caenorhabditis elegans. J. Biol. Chem. 278, 34380-34386.
72. Ye, Y., Shibata, Y., Yun, C., Ron, D. and Rapoport, T. A. (2004). A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429, 841-847.
73. Ye, Y., Shibata, Y., Kikkert, M., van Voorden, S., Wiertz, E. and Rapoport, T. A. (2005). Inaugural article: recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 102, 14132-14138.
74. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K. (2001). XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891.
75. Zaliauskiene, L., Kang, S., Brouillette, C. G., Lebowitz, J., Arani, R. B. and Collawn, J. F. (2000). Down-regulation of cell surface receptors is modulated by polar residues within the transmembrane domain. Mol. Biol. Cell 11, 2643-2655.
76. Zhang, D. W., Lagace, T. A., Garuti, R., Zhao, Z., McDonald, M., Horton, J. D., Cohen, J. C. and Hobbs, H. H. (2007). Binding of proprotein convertase subtilisin/kexin type 9 to epidermal growth factor-like repeat A of low density lipoprotein receptor decreases receptor recycling and increases degradation. J. Biol. Chem. 282, 18602-18612.
77. Zhang, Y., Grant, B. and Hirsh, D. (2001). RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol. Biol. Cell 12, 2011-2021.