BsdABsd2-dependent vacuolar turnover of a misfolded version of the UapA transporter along the secretory pathway: Prominent role of selective autophagy

Molecular Microbiology

Volumn 100, Issue 5, 2016, Pages 893-911

  Evangelinos, Minoas ^a   Martzoukou, Olga ^a   Chorozian, Koar ^a   Amillis, Sotiris ^a   Diallinas, George ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BSDABSD2 PROTEIN; HULARSP5 PROTEIN; MEMBRANE PROTEIN; UAPA PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; FUNGAL PROTEIN; UAPA PROTEIN, ASPERGILLUS NIDULANS;

ARTICLE; ASPERGILLUS NIDULANS; AUTOPHAGY; BIOACCUMULATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN UNFOLDING; SECRETORY PATHWAY; STEADY STATE; CELL VACUOLE; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN TRANSPORT;

ASPERGILLUS NIDULANS; AUTOPHAGY; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTATION; PROTEIN FOLDING; PROTEIN TRANSPORT; PROTEOLYSIS; SECRETORY PATHWAY; VACUOLES;

EID: 84962230423     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13358     Document Type: Article

References (72)

1. Abenza, J.F., Galindo, A., Pantazopoulou, A., Gil, C., de los Ríos, V., and Peñalva, M.A. (2010) Aspergillus RabB Rab5 integrates acquisition of degradative identity with the long distance movement of early endosomes. Mol Biol Cell 21: 2756-2769.
2. Abenza, J.F., Galindo, A., Pinar, M., Pantazopoulou, A., de los Ríos, V., and Peñalva, M.A. (2012) Endosomal maturation by Rab conversion in Aspergillus nidulans is coupled to dynein-mediated basipetal movement. Mol Biol Cell 23: 1889-1901.
3. Amillis, S., Cecchetto, G., Sophianopoulou, V., Koukaki, M., Scazzocchio, C., and Diallinas, G. (2004) Transcription of purine transporter genes is activated during the isotropic growth phase of Aspergillus nidulans conidia. Mol Microbiol 52: 205-216.
4. Amillis, S., Kosti, V., Pantazopoulou, A., Mikros, E., and Diallinas, G. (2011) Mutational analysis and modeling reveal functionally critical residues in transmembrane segments 1 and 3 of the UapA transporter. J Mol Biol 411: 567-580.
5. Apostolaki, A., Harispe, L., Calcagno-Pizarelli, A.M., Vangelatos, I., Sophianopoulou, V., Arst, H.N. Jr., et al. (2012) Aspergillus nidulans CkiA is an essential casein kinase I required for delivery of amino acid transporters to the plasma membrane. Mol Microbiol 84: 530-549.
6. Brodsky, J.L. (2012) Cleaning up: ER-associated degradation to the rescue. Cell 151: 1163-1167.
7. Chu, X.L., Feng, M.G., and Ying, S.H. (2016) Qualitative ubiquitome unveils the potential significances of protein lysine ubiquitination in hyphal growth of Aspergillus nidulans. Curr Genet 62: 191-201. doi:10.1007/s00294-015-0517-7
8. D'Arcangelo, J.G., Stahmer, K.R., and Miller, E.A. (2013) Vesicle-mediated export from the ER: COPII coat function and regulation. Biochim Biophys Acta 1833: 2464-2472.
9. Diallinas, G. (2014) Understanding transporter specificity and the discrete appearance of channel-like gating domains in transporters. Front Pharmacol 5: 207.
10. Diallinas, G., and Gournas, C. (2008) Structure-function relationships in the nucleobase-ascorbate transporter (NAT) family: lessons from model microbial genetic systems. Channels (Austin) 2: 363-372.
11. Ellgaard, L., and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191.
12. Felenbok, B. (1991) The ethanol utilization regulon of Aspergillus nidulans: the alcA-alcR system as a tool for the expression of recombinant proteins. J Biotechnol 17: 11-17.
13. Gardner, B.M., Pincus, D., Gotthardt, K., Gallagher, C.M., and Walter, P. (2013) Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5: a013169.
14. Gournas, C., Papageorgiou, I., and Diallinas, G. (2008) The nucleobase-ascorbate transporter (NAT) family: genomics, evolution, structure-function relationships and physiological role. Mol Biosyst 4: 404-416.
15. Gournas, C., Amillis, S., Vlanti, A., and Diallinas, G. (2010) Transport-dependent endocytosis and turnover of a uric acid-xanthine permease. Mol Microbiol 75: 246-260.
16. Gournas, C., Oestreicher, N., Amillis, S., Diallinas, G., and Scazzocchio, C. (2011) Completing the purine utilisation pathway of Aspergillus nidulans. Fungal Genet Biol 48: 840-848.
17. Haynes, C.M., Caldwell, S., and Cooper, A.A. (2002) An HRD/DER-independent ER quality control mechanism involves Rsp5p-dependent ubiquitination and ER-Golgi transport. J Cell Biol 158: 91-101.
18. Hegde, R.S., and Ploegh, H.L. (2010) Quality and quantity control at the endoplasmic reticulum. Curr Opin Cell Biol 22: 437-446.
19. Hettema, E.H., Valdez-Taubas, J., and Pelham, H.R. (2004) Bsd2 binds the ubiquitin ligase Rsp5 and mediates the ubiquitination of transmembrane proteins. EMBO J 23: 1279-1288.
20. Hollien, J., and Weissman, J.S. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313: 104-107.
21. Isasa, M., Suñer, C., Díaz, M., Puig-Sàrries, P., Zuin, A., Bichman, A., et al. (2016) Cold temperature induces the reprogramming of proteolytic pathways in yeast. J Biol Chem 291: 1664-1675.
22. Karachaliou, M., Amillis, S., Evangelinos, M., Kokotos, A.C., Yalelis, V., and Diallinas, G. (2013) The arrestin-like protein ArtA is essential for ubiquitination and endocytosis of the UapA transporter in response to both broad-range and specific signals. Mol Microbiol 88: 301-317.
23. Kawaguchi, S., Hsu, C.L., and Ng, D.T. (2010) Interplay of substrate retention and export signals in endoplasmic reticulum quality control. PLoS One 5: e15532.
24. Kimura, S., Maruyama, J., Kikuma, T., Arioka, M., and Kitamoto, K. (2011) Autophagy delivers misfolded secretory proteins accumulated in endoplasmic reticulum to vacuoles in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 406: 464-470.
25. Kincaid, M.M., and Cooper, A.A. (2007) Misfolded proteins traffic from the endoplasmic reticulum (ER) due to ER export signals. Mol Biol Cell 18: 455-463.
26. Kosti, V., Papageorgiou, I., and Diallinas, G. (2010) Dynamic elements at both cytoplasmically and extracellularly facing sides of the UapA transporter selectively control the accessibility of substrates to their translocation pathway. J Mol Biol 397: 1132-1134.
27. Koukaki, M., Giannoutsou, E., Karagouni, A., and Diallinas, G. (2003) A novel improved method for Aspergillus nidulans transformation. J Microbiol Methods 55: 687-695.
28. Koukaki, M., Vlanti, A., Goudela, S., Pantazopoulou, A., Gioule, H., Tournaviti, S., and Diallinas G. (2005) The nucleobase-ascorbate transporter (NAT) signature motif in UapA defines the function of the purine translocation pathway. J Mol Biol 350: 499-513.
29. Kruse, K.B., Brodsky, J.L., and McCracken, A.A. (2006) Autophagy: an ER protein quality control process. Autophagy 2: 135-137.
30. Lee, J.Y., and Yao, T.P. (2010) Quality control autophagy: a joint effort of ubiquitin, protein deacetylase and actin cytoskeleton. Autophagy 6: 555-557.
31. Lemus, L., and Goder, V. (2014) Regulation of endoplasmic reticulum-associated protein degradation (ERAD) by ubiquitin. Cells 3: 824-847.
32. Léon, S., Erpapazoglou, Z., and Haguenauer-Tsapis, R. (2008) Ear1p and Ssh4p are new adaptors of the ubiquitin ligase Rsp5p for cargo ubiquitylation and sorting at multivesicular bodies. Mol Biol Cell 19: 2379-2388.
33. Lewis, M.J., and Pelham, H.R. (2009) Inefficient quality control of thermosensitive proteins on the plasma membrane. PLoS One 4: e5038.
34. Lin, C.H., MacGurn, J.A., Chu, T., Stefan, C.J., and Emr, S.D. (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135: 714-722.
35. Liu, X.F., Supek, F., Nelson, N., and Culotta, V.C. (1997) Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J Biol Chem 272: 11763-11769.
36. Lukacs, G.L., and Verkman, A.S. (2012) CFTR: folding, misfolding and correcting the ΔF508 conformational defect. Trends Mol Med 18: 81-91.
37. Mari, M., and Reggiori, F. (2007) Atg9 trafficking in the yeast Saccharomyces cerevisiae. Autophagy 3: 145-148.
38. Martzoukou, O., Karachaliou, M., Yalelis, V., Leung, J., Byrne, B., Amillis, S., and Diallinas, G. (2015) Oligomerization of the UapA purine transporter is critical for ER-exit, plasma membrane localization and turnover. J Mol Biol 427: 2679-2696.
39. Meng, L., Mohan, R., Kwok, B.H., Elofsson, M., Sin, N., and Crews, C.M. (1999) Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci U S A 96: 10403-10408.
40. Mizushima, N., Levine, B., Cuervo, A.M., and Klionsky, D.J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075.
41. Nakatogawa, H., Ichimura, Y., and Ohsumi, Y. (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130: 165-78.
42. Nayak, T., Szewczyk, E., Oakley, C.E., Osmani, A., Ukil, L., Murray, S.L., et al. (2006). A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172: 1557-1566.
43. Nikko, E., and Pelham, H.R. (2009) Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10: 1856-1867.
44. Nyathi, Y., Wilkinson, B.M., and Pool, M.R. (2013) Co-translational targeting and translocation of proteins to the endoplasmic reticulum. Biochim Biophys Acta 1833: 2392-2402.
45. Pantazopoulou, A., and Diallinas, G. (2006) The first transmembrane segment (TMS1) of UapA contains determinants necessary for expression in the plasma membrane and purine transport. Mol Membr Biol 23: 337-348.
46. Pantazopoulou, A., and Peñalva, M.A. (2009) Organization and dynamics of the Aspergillus nidulans Golgi during apical extension and mitosis. Mol Biol Cell 20: 4335-4347.
47. Pantazopoulou, A., Lemuh, N.D., Hatzinikolaou, D.G., Drevet, C., Cecchetto, G., Scazzocchio, C., and Diallinas, G. (2007) Differential physiological and developmental expression of the UapA and AzgA purine transporters in Aspergillus nidulans. Fungal Genet Biol 44: 627-640.
48. Pantazopoulou, A., Pinar, M., Xiang, X., and Peñalva, M.A. (2014) Maturation of late Golgi cisternae into RabE (RAB11) exocytic post-Golgi carriers visualized in vivo. Mol Biol Cell 25: 2428-2443.
49. Papageorgiou, I., Gournas, C., Vlanti, A., Amillis, S., Pantazopoulou, A., and Diallinas, G. (2008) Specific interdomain synergy in the UapA transporter determines its unique specificity for uric acid among NAT carriers. J Mol Biol 382: 1121-1135.
50. Peñalva, M.A. (2005) Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet Biol 42: 963-975.
51. Peñalva, M.Á. (2010) Endocytosis in filamentous fungi: Cinderella gets her reward. Curr Opin Microbiol 13: 684-692.
52. Peñalva, M.A., Galindo, A., Abenza, J.F., Pinar, M., Calcagno-Pizarelli, A.M., Arst, H.N., and Pantazopoulou, A. (2012) Searching for gold beyond mitosis: mining intracellular membrane traffic in Aspergillus nidulans. Cell Logist 2: 2-14.
53. Pinar, M., Pantazopoulou, A., Arst, H.N. Jr, and Peñalva, M.A. (2013a) Acute inactivation of the Aspergillus nidulans Golgi membrane fusion machinery: correlation of apical extension arrest and tip swelling with cisternal disorganization. Mol Microbiol 89: 228-248.
54. Pinar, M., Pantazopoulou, A., and Peñalva, M.A. (2013b) Live-cell imaging of Aspergillus nidulans autophagy: RAB1 dependence, Golgi independence and ER involvement. Autophagy 9: 1024-1043.
55. Pinar, M., Arst, H.N. Jr., Pantazopoulou, A., Tagua, V.G., de Los Ríos, V., Rodríguez-Salarichs, J., et al. (2015) TRAPPII regulates exocytic Golgi exit by mediating nucleotide exchange on the Ypt31 ortholog RabERAB11. Proc Natl Acad Sci U S A 112: 4346-4351.
56. Rotin, D., and Staub, O. (2011) Role of the ubiquitin system in regulating ion transport. Pflugers Arch 461: 1-21.
57. Ruggiano, A., Foresti, O., and Carvalho, P. (2014) Quality control: ER-associated degradation: protein quality control and beyond. J Cell Biol 204: 869-879.
58. Sambrook, J., Fritsch, E., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
59. Sato, K., and Nakano, A. (2007) Mechanisms of COPII vesicle formation and protein sorting. FEBS Lett 581: 2076-2082.
60. Schubert, U., Anton, L.C., Gibbs, J., Norbury, C.C., Yewdell, J.W., and Bennink, J.R. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
61. Shintani, T., and Klionsky, D.J. (2004) Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem 279: 29889-29894.
62. Smith, M.H., Ploegh, H.L., and Weissman, J.S. (2011) Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086-1090.
63. Stanley, R.E., Ragusa, M.J., and Hurley, J.H. (2014) The beginning of the end: how scaffolds nucleate autophagosome biogenesis. Trends Cell Biol 24: 73-81.
64. Stimpson, H.E., Lewis, M.J., and Pelham, H.R. (2006) Transferrin receptor-like proteins control the degradation of a yeast metal transporter. EMBO J 25: 662-672.
65. Sullivan, J.A., Lewis, M.J., Nikko, E., and Pelham, H.R. (2007) Multiple interactions drive adaptor-mediated recruitment of the ubiquitin ligase rsp5 to membrane proteins in vivo and in vitro. Mol Biol Cell 18: 2429-2440.
66. Szewczyk, E., Nayak, T., Oakley, C.E., Edgerton, H., Xiong, Y., Taheri-Talesh, N., et al. (2006) Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1: 3111-3120.
67. Takeshita, N., Higashitsuji, Y., Konzack, S., and Fischer, R. (2008) Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 19: 339-351.
68. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., and Walter, P. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
69. Vlanti, A., Amillis, S., Koukaki, M., and Diallinas, G. (2006) A novel-type substrate-selectivity filter and ER-exit determinants in the UapA purine transporter. J Mol Biol 357: 808-819.
70. Walter, P., and Ron, D. (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086.
71. Wang, S., Thibault, G., and Ng, D.T. (2011) Routing misfolded proteins through the multivesicular body (MVB) pathway protects against proteotoxicity. J Biol Chem 286: 29376-29387.
72. Yao, T.P. (2010) The role of ubiquitin in autophagy-dependent protein aggregate processing. Genes Cancer 1: 779-786.