Cytosolic chaperones mediate quality control of higher-order septin assembly in budding yeast

Molecular Biology of the Cell

Volumn 26, Issue 7, 2015, Pages 1323-1344

  Johnson, Courtney R ^a   Weems, Andrew D ^a   Brewer, Jennifer M ^b,c   Thorner, Jeremy ^b   McMurray, Michael A ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UCSD MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHAPERONE YDJ1; HEAT SHOCK PROTEIN 104; SEPTIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 40; HSP104 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; YDJ1 PROTEIN, S CEREVISIAE;

ALLELE; ARTICLE; CELL PROLIFERATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOSOL; DIMERIZATION; DIPLOIDY; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; GENOTYPE; HAPLOIDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; YEAST CELL; CYTOSKELETON; GENETICS; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCETALES;

ALLELES; CYTOSKELETON; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; MUTATION; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEPTINS;

EID: 84926482977     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-11-1531     Document Type: Article

References (96)

1. Alpers JB, Paulus H (1971). Allosteric preconditioning: role of allosteric ligands in promoting the maturation of enzymes. Nature 233, 478-480.
2. Amberg D, Burke D, Strathern J (2005). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
3. Bertin A, McMurray MA, Grob P, Park S-S, Garcia G 3rd, Patanwala I, Ng H-L, Alber T, Thorner J, Nogales E (2008). Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc Natl Acad Sci USA 105, 8274-8279.
4. Betting J, Seufert W (1996). A yeast Ubc9 mutant protein with temperature-sensitive in vivo function is subject to conditional proteolysis by a ubiquitin- and proteasome-dependent pathway. J Biol Chem 271, 25790-25796.
5. Bordallo J, Plemper RK, Finger A, Wolf DH (1998). Der3p/Hrd1p is required for endoplasmic reticulum-associated degradation of misfolded lumenal and integral membrane proteins. Mol Biol Cell 9, 209-222.
6. Bridges AA, Zhang H, Mehta SB, Occhipinti P, Tani T, Gladfelter AS (2014). Septin assemblies form by diffusion-driven annealing on membranes. Proc Natl Acad Sci USA 111, 2146-2151.
7. Bösl B, Grimminger V, Walter S (2005). Substrate binding to the molecular chaperone Hsp104 and its regulation by nucleotides. J Biol Chem 280, 38170-38176.
8. Caplan AJ, Douglas MG (1991). Characterization of YDJ1: a yeast homologue of the bacterial dnaJ protein. J Cell Biol 114, 609-621.
9. Casamayor A, Snyder M (2003). Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol Cell Biol 23, 2762-2777.
10. Caviston JP, Longtine M, Pringle JR, Bi E (2003). The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol Biol Cell 14, 4051-4066.
11. Cid VJ, Adamíková L, Cenamor R, Molina M, Sánchez M, Nombela C (1998). Cell integrity and morphogenesis in a budding yeast septin mutant. Microbiology 144, 3463-3474.
12. Collie AMB, Landsverk ML, Ruzzo E, Mefford HC, Buysse K, Adkins JR, Knutzen DM, Barnett K, Brown RH Jr, Parry GJ, et al. (2010). Non-recurrent SEPT9 duplications cause hereditary neuralgic amyotrophy. J Med Genet 47, 601-607.
13. Connolly D, Hoang HG, Adler E, Tazearslan C, Simmons N, Bernard VV, Castaldi M, Oktay MH, Montagna C (2014). Septin 9 amplification and isoform-specific expression in peritumoral and tumor breast tissue. Biol Chem 395, 157-167.
14. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, et al. (2010). The genetic landscape of a cell. Science 327, 425-431.
15. Dekker C, Stirling PC, McCormack EA, Filmore H, Paul A, Brost RL, Costanzo M, Boone C, Leroux MR, Willison KR (2008). The interaction network of the chaperonin CCT. EMBO J 27, 1827-1839.
16. De Val N, McMurray MA, Lam LH, Hsiung CC-S, Bertin A, Nogales E, Thorner J (2013). Native cysteine residues are dispensable for the structure and function of all five yeast mitotic septins. Proteins 81, 1964-1979.
17. Dobbelaere J, Gentry MS, Hallberg RL, Barral Y (2003). Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev Cell 4, 345-357.
18. Dong Z, Ferger B, Paterna J-C, Vogel D, Furler S, Osinde M, Feldon J, Büeler H (2003). Dopamine-dependent neurodegeneration in rats induced by viral vector-mediated overexpression of the parkin target protein, CDCrel-1. Proc Natl Acad Sci USA 100, 12438-12443.
19. Downing KH, Nogales E (2010). Cryoelectron microscopy applications in the study of tubulin structure, microtubule architecture, dynamics and assemblies, and interaction of microtubules with motors. Methods Enzymol 483, 121-142.
20. Escusa-Toret S, Vonk WIM, Frydman J (2013). Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nat Cell Biol 15, 1231-1243.
21. Farkasovsky M, Herter P, Voss B, Wittinghofer A (2005). Nucleotide binding and filament assembly of recombinant yeast septin complexes. Biol Chem 386, 643-656.
22. Feldman DE, Thulasiraman V, Ferreyra RG, Frydman J (1999). Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol Cell 4, 1051-1061.
23. Frazier JA, Wong ML, Longtine MS, Pringle JR, Mann M, Mitchison TJ, Field C (1998). Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J Cell Biol 143, 737-749.
24. Garcia G 3rd, Bertin A, Li Z, Song Y, McMurray MA, Thorner J, Nogales E (2011). Subunit-dependent modulation of septin assembly: budding yeast septin Shs1 promotes ring and gauze formation. J Cell Biol 195, 993-1004.
25. Garcia W, de Araújo APU, Lara F, Foguel D, Tanaka M, Tanaka T, Garratt RC (2007). An intermediate structure in the thermal unfolding of the GTPase domain of human septin 4 (SEPT4/Bradeion-beta) forms amyloid-like filaments in vitro. Biochemistry 46, 11101-11109.
26. Gardner RG, Nelson ZW, Gottschling DE (2005). Degradation-mediated protein quality control in the nucleus. Cell 120, 803-815.
27. Gasper R, Meyer S, Gotthardt K, Sirajuddin M, Wittinghofer A (2009). It takes two to tango: regulation of G proteins by dimerization. Nat Rev Mol Cell Biol 10, 423-429.
28. Geiler-Samerotte KA, Dion MF, Budnik BA, Wang SM, Hartl DL, Drummond DA (2011). Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast. Proc Natl Acad Sci USA 108, 680-685.
29. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, Lopez- Hoyo N, Jiang L, Piccirillo S, Yu H, et al. (2005). Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19, 2816-2826.
30. Glover JR, Lindquist S (1998). Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82.
31. Gonzalez ME, Peterson EA, Privette LM, Loffreda-Wren JL, Kalikin LM, Petty EM (2007). High SEPT9-v1 expression in human breast cancer cells is associated with oncogenic phenotypes. Cancer Res 67, 8554-8564.
32. Guan J, Kinoshita M, Yuan L (2009). Spatiotemporal association of DNAJB13 with the annulus during mouse sperm flagellum development. BMC Dev Biol 9, 23.
33. Haarer BK, Pringle JR (1987). Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol Cell Biol 7, 3678-3687.
34. Hartwell LH (1971). Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res 69, 265-276.
35. Hartwell LH, Mortimer RK, Culotti J, Culotti M (1973). Genetic control of the cell division cycle in yeast: V. Genetic analysis of cdc mutants. Genetics 74, 267-286.
36. Horst R, Fenton WA, Englander SW, Wüthrich K, Horwich AL (2007). Folding trajectories of human dihydrofolate reductase inside the GroEL GroES chaperonin cavity and free in solution. Proc Natl Acad Sci USA 104, 20788-20792.
37. Hoyle HD, Turner FR, Brunick L, Raff EC (2001). Tubulin sorting during dimerization in vivo. Mol Biol Cell 12, 2185-2194.
38. Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
39. Hwang YW, Miller DL (1987). A mutation that alters the nucleotide specificity of elongation factor Tu, a GTP regulatory protein. J Biol Chem 262, 13081-13085.
40. Iwase M, Luo J, Nagaraj S, Longtine M, Kim HB, Haarer BK, Caruso C, Tong Z, Pringle JR, Bi E (2006). Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol Biol Cell 17, 1110-1125.
41. Jarosz DF, Taipale M, Lindquist S (2010). Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu Rev Genet 44, 189-216.
42. Jung AE, Fitzsimons HL, Bland RJ, During MJ, Young D (2008). HSP70 and constitutively active HSF1 mediate protection against CDCrel-1-mediated toxicity. Mol Ther 16, 1048-1055.
43. Kadota J, Yamamoto T, Yoshiuchi S, Bi E, Tanaka K (2004). Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae. Mol Biol Cell 15, 5329-5345.
44. Keppler A, Pick H, Arrivoli C, Vogel H, Johnsson K (2004). Labeling of fusion proteins with synthetic fluorophores in live cells. Proc Natl Acad Sci USA 101, 9955-9959.
45. Kim MS, Froese CD, Xie H, Trimble WS (2012). Uncovering principles that control septin-septin interactions. J Biol Chem 287, 30406-30413.
46. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU (2013). Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82, 323-355.
47. Kuhlenbäumer G, Hannibal MC, Nelis E, Schirmacher A, Verpoorten N, Meuleman J, Watts GD, De Vriendt E, Young P, Stögbauer F, et al. (2005). Mutations in SEPT9 cause hereditary neuralgic amyotrophy. Nat Genet 37, 1044-1046.
48. Kuo Y-C, Lin YH, Chen HI, Wang YY, Chiou YW, Lin HH, Pan HA, Wu CM, Su SM, Hsu CC, et al. (2012). SEPT12 mutations cause male infertility with defective sperm annulus. Hum Mutat 33, 710-719.
49. Lee DH, Sherman MY, Goldberg AL (1996). Involvement of the molecular chaperone Ydj1 in the ubiquitin-dependent degradation of short-lived and abnormal proteins in Saccharomyces cerevisiae. Mol Cell Biol 16, 4773-4781.
50. Longtine MS, Theesfeld CL, McMillan JN, Weaver E, Pringle JR, Lew DJ (2000). Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol Cell Biol 20, 4049-4061.
51. Lopez-Fanarraga M, Avila J, Guasch A, Coll M, Zabala JC (2001). Review: postchaperonin tubulin folding cofactors and their role in microtubule dynamics. J Struct Biol 135, 219-229.
52. Lundin VF, Leroux MR, Stirling PC (2010). Quality control of cytoskeletal proteins and human disease. Trends Biochem Sci 35, 288-297.
53. McCusker JH, Davis RW (1991). The use of proline as a nitrogen source causes hypersensitivity to, and allows more economical use of 5FOA in Saccharomyces cerevisiae. Yeast 7, 607-608.
54. McMurray M (2014). Lean forward: genetic analysis of temperature-sensitive mutants unfolds the secrets of oligomeric protein complex assembly. Bioessays 36, 836-846.
55. McMurray MA, Bertin A, Garcia G 3rd, Lam L, Nogales E, Thorner J (2011a). Septin filament formation is essential in budding yeast. Dev Cell 20, 540-549.
56. McMurray MA, Stefan CJ, Wemmer M, Odorizzi G, Emr SD, Thomer J (2011b). Genetic interactions with mutations affecting septin assembly reveal ESeRT functions in budding yeast cytokinesis. Biol Chem 392, 699-712.
57. McMurray MA, Thorner J (2008a). Biochemical properties and supramolecular architecture of septin hetero-oligomers and septin filaments. In: The Septins, ed. PA Hall, SE Russell, and JR Pringle, Hoboken, NJ: John Wiley & Sons, 49-100.
58. McMurray MA, Thorner J (2008b). Septin stability and recycling during dynamic structural transitions in cell division and development. Curr Biol 18, 1203-1208.
59. Moosavi B, Wongwigkarn J, Tuite MF (2010). Hsp70/Hsp90 co-chaperones are required for efficient Hsp104-mediated elimination of the yeast [PSI+] prion but not for prion propagation. Yeast 27, 167-179.
60. Nagai S (1963). diagnostic color differentiation plates for hereditary respiration deficiency in yeast. J Bacteriol 86, 299-302.
61. Nagaraj S, Rajendran A, Jackson CE, Longtine MS (2008). Role of nucleotide binding in septin-septin interactions and septin localization in Saccharomyces cerevisiae. Mol Cell Biol 28, 5120-5137.
62. Nogales E, Wolf SG, Downing KH (1998). Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391, 199-203.
63. Okada S, Leda M, Hanna J, Savage NS, Bi E, Goryachev AB (2013). Daughter cell identity emerges from the interplay of Cdc42, septins, and exocytosis. Dev Cell 26, 148-161.
64. Olzmann JA, Chin L-S (2008). Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 4, 85-87.
65. Pan F, Malmberg RL, Momany M (2007). Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol Biol 7, 103.
66. Park K-W, Hahn J-S, Fan Q, Thiele DJ, Li L (2006). De novo appearance and "strain" formation of yeast prion [PSI+] are regulated by the heat-shock transcription factor. Genetics 173, 35-47.
67. Parsell DA, Kowal AS, Lindquist S (1994). Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. J Biol Chem 269, 4480-4487.
68. Pissuti Damalio JC, Garcia W, Alves Macêdo JN, de Almeida Marques I, Andreu JM, Giraldo R, Garratt RC, Ulian Araújo AP (2012). Self assembly of human septin 2 into amyloid filaments. Biochimie 94, 628-636.
69. Sahi C, Kominek J, Ziegelhoffer T, Yu HY, Baranowski M, Marszalek J, Craig EA (2013). Sequential duplications of an ancient member of the DnaJ-family expanded the functional chaperone network in the eukaryotic cytosol. Mol Biol Evol 30, 985-998.
70. Sassanfar M, Samson L (1990). Identification and preliminary characterization of an O6-methylguanine DNA repair methyltransferase in the yeast Saccharomyces cerevisiae. J Biol Chem 265, 20-25.
71. Schaupp A, Marcinowski M, Grimminger V, Bösl B, Walter S (2007). Processing of proteins by the molecular chaperone Hsp104. J Mol Biol 370, 674-686.
72. Schirmer EC, Homann OR, Kowal AS, Lindquist S (2004). Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Mol Biol Cell 15, 2061-2072.
73. Sellin ME, Holmfeldt P, Stenmark S, Gullberg M (2011a). Microtubules support a disk-like septin arrangement at the plasma membrane of mammalian cells. Mol Biol Cell 22, 4588-4601.
74. Sellin ME, Sandblad L, Stenmark S, Gullberg M (2011b). Deciphering the rules governing assembly order of mammalian septin complexes. Mol Biol Cell 22, 3152-3164.
75. Shorter J, Lindquist S (2004). Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304, 1793-1797.
76. Sirajuddin M, Farkasovsky M, Hauer F, Kühlmann D, Macara IG, Weyand M, Stark H, Wittinghofer A (2007). Structural insight into filament formation by mammalian septins. Nature 449, 311-315.
77. Sirajuddin M, Farkasovsky M, Zent E, Wittinghofer A (2009). GTP-induced conformational changes in septins and implications for function. Proc Natl Acad Sci USA 106, 16592-16597.
78. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B (1998). Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9, 3273-3297.
79. Tian G, Bhamidipati A, Cowan NJ, Lewis SA (1999). Tubulin folding cofactors as GTPase-activating proteins. GTP hydrolysis and the assembly of the alpha/beta-tubulin heterodimer. J Biol Chem 274, 24054-24058.
80. Tian G, Lewis SA, Feierbach B, Stearns T, Rommelaere H, Ampe C, Cowan NJ (1997). Tubulin subunits exist in an activated conformational state generated and maintained by protein cofactors. J Cell Biol 138, 821-832.
81. Tian G, Vainberg IE, Tap WD, Lewis SA, Cowan NJ (1995). Quasi-native chaperonin-bound intermediates in facilitated protein folding. J Biol Chem 270, 23910-23913.
82. Vainberg IE, Lewis SA, Rommelaere H, Ampe C, Vandekerckhove J, Klein HL, Cowan NJ (1998). Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863-873.
83. Varadarajan R, Nagarajaram HA, Ramakrishnan C (1996). A procedure for the prediction of temperature-sensitive mutants of a globular protein based solely on the amino acid sequence. Proc Natl Acad Sci USA 93, 13908-13913.
84. Vergés E, Colomina N, Garí E, Gallego C, Aldea M (2007). Cyclin Cln3 is retained at the ER and released by the J chaperone Ydj1 in late G1 to trigger cell cycle entry. Mol Cell 26, 649-662.
85. Versele M, Gullbrand B, Shulewitz MJ, Cid VJ, Bahmanyar S, Chen RE, Barth P, Alber T, Thorner J (2004). Protein-protein interactions governing septin heteropentamer assembly and septin filament organization in Saccharomyces cerevisiae. Mol Biol Cell 15, 4568-4583.
86. Versele M, Thorner J (2004). Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J Cell Biol 164, 701-715.
87. Vrabioiu AM, Gerber SA, Gygi SP, Field CM, Mitchison TJ (2004). The majority of the Saccharomyces cerevisiae septin complexes do not exchange guanine nucleotides. J Biol Chem 279, 3111-3118.
88. Wang Y, Tian G, Cowan NJ, Cabral F (2006). Mutations affecting beta-tubulin folding and degradation. J Biol Chem 281, 13628-13635.
89. Weems AD, Johnson CR, Argueso JL, McMurray MA (2014). Higher-order septin assembly is driven by GTP-promoted conformational changes: evidence from unbiased mutational analysis in Saccharomyces cerevisiae. Genetics 196, 711-727.
90. Weissman JS, Kashi Y, Fenton WA, Horwich AL (1994). GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78, 693-702.
91. Wittinghofer A, Vetter IR (2011). Structure-function relationships of the G domain, a canonical switch motif. Annu Rev Biochem 80, 943-971.
92. Wu Y, Li J, Jin Z, Fu Z, Sha B (2005). The crystal structure of the C-terminal fragment of yeast Hsp40 Ydj1 reveals novel dimerization motif for Hsp40. J Mol Biol 346, 1005-1011.
93. Yam AY, Xia Y, Lin H-TJ, Burlingame A, Gerstein M, Frydman J (2008). Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat Struct Mol Biol 15, 1255-1262.
94. Zabala JC, Fontalba A, Avila J (1996). Tubulin folding is altered by mutations in a putative GTP binding motif. J Cell Sci 109, 1471-1478.
95. Zent E, Wittinghofer A (2014). Human septin isoforms and the GDP-GTP cycle. Biol Chem 395, 169-180.
96. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM (2000). Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci USA 97, 13354-13359.