The Yeast AAA⁺ Chaperone Hsp104 Is Part of a Network That Links the Actin Cytoskeleton with the Inheritance of Damaged Proteins

REFERENCES

• Abelson, J. N., C. Guthrie, and G. R. Fink. 2003. Guide to yeast genetics and molecular biology. Academic Press Inc., New York, NY.
   Google Scholar
• Adams, A. E., D. I. Johnson, R. M. Longnecker, B. F. Sloat, and J. R. Pringle. 1990. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111:131–142.
   PubMed Web of Science ®Google Scholar
• Aguilaniu, H., L. Gustafsson, M. Rigoulet, and T. Nystrom. 2003. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299:1751–1753.
   PubMed Web of Science ®Google Scholar
• Arsene, F., T. Tomoyasu, and B. Bukau. 2000. The heat shock response of Escherichia coli. Int. J. Food Microbiol. 55:3–9.
   PubMed Web of Science ®Google Scholar
• Belli, G., E. Gari, M. Aldea, and E. Herrero. 1998. Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14:1127–1138.
   PubMed Web of Science ®Google Scholar
• Belli, G., E. Gari, L. Piedrafita, M. Aldea, and E. Herrero. 1998. An activator/repressor dual system allows tight tetracycline-regulated gene expression in budding yeast. Nucleic Acids Res. 26:942–947.
   PubMedGoogle Scholar
• Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119–122.
   PubMed Web of Science ®Google Scholar
• Erjavec, N., L. Larsson, J. Grantham, and T. Nystrom. 2007. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev. 21:2410–2421.
   PubMed Web of Science ®Google Scholar
• Gehrung, S., and M. Snyder. 1990. The SPA2 gene of Saccharomyces cerevisiae is important for pheromone-induced morphogenesis and efficient mating. J. Cell Biol. 111:1451–1464.
   PubMedGoogle Scholar
• Ghaemmaghami, S., W. K. Huh, K. Bower, R. W. Howson, A. Belle, N. Dephoure, E. K. O'Shea, and J. S. Weissman. 2003. Global analysis of protein expression in yeast. Nature 425:737–741.
   PubMed Web of Science ®Google Scholar
• Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El-Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Guldener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C. Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391.
   PubMed Web of Science ®Google Scholar
• Guarente, L., G. Ruvkun, and R. Amasino. 1998. Aging, life span, and senescence. Proc. Natl. Acad. Sci. USA 95:11034–11036.
   PubMedGoogle Scholar
• Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
   Google Scholar
• Hartwell, L. H. 1971. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69:265–276.
   PubMed Web of Science ®Google Scholar
• Janke, C., M. M. Magiera, N. Rathfelder, C. Taxis, S. Reber, H. Maekawa, A. Moreno-Borchart, G. Doenges, E. Schwob, E. Schiebel, and M. Knop. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21:947–962.
   PubMed Web of Science ®Google Scholar
• Johnson, D. I., and J. R. Pringle. 1990. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111:143–152.
   PubMed Web of Science ®Google Scholar
• Kamei, T., K. Tanaka, T. Hihara, M. Umikawa, H. Imamura, M. Kikyo, K. Ozaki, and Y. Takai. 1998. Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J. Biol. Chem. 273:28341–28345.
   PubMed Web of Science ®Google Scholar
• Lippincott, J., and R. Li. 1998. Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J. Cell Biol. 143:1947–1960.
   PubMedGoogle Scholar
• Lum, R., M. Niggemann, and J. R. Glover. 2008. Peptide and protein binding in the axial channel of Hsp104. Insights into the mechanism of protein unfolding. J. Biol. Chem. 283:30139–30150.
   PubMedGoogle Scholar
• Maniatis, T., J. Sambrook, and E. F. Fritsch. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Martin, H., J. M. Rodriguez-Pachon, C. Ruiz, C. Nombela, and M. Molina. 2000. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275:1511–1519.
   PubMed Web of Science ®Google Scholar
• Moseley, J. B., and B. L. Goode. 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605–645.
   PubMed Web of Science ®Google Scholar
• Norden, C., D. Liakopoulos, and Y. Barral. 2004. Dissection of septin actin interactions using actin overexpression in Saccharomyces cerevisiae. Mol. Microbiol. 53:469–483.
   PubMedGoogle Scholar
• Pratt, W. B. 1998. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med. 217:420–434.
   PubMed Web of Science ®Google Scholar
• Pruyne, D., M. Evangelista, C. Yang, E. Bi, S. Zigmond, A. Bretscher, and C. Boone. 2002. Role of formins in actin assembly: nucleation and barbed-end association. Science 297:612–615.
   PubMed Web of Science ®Google Scholar
• Sagot, I., S. K. Klee, and D. Pellman. 2002. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4:42–50.
   PubMed Web of Science ®Google Scholar
• Sanchez, Y., and S. L. Lindquist. 1990. HSP104 required for induced thermotolerance. Science 248:1112–1115.
   PubMed Web of Science ®Google Scholar
• Schaupp, A., M. Marcinowski, V. Grimminger, B. Bosl, and S. Walter. 2007. Processing of proteins by the molecular chaperone hsp104. J. Mol. Biol. 370:674–686.
   PubMed Web of Science ®Google Scholar
• Schlieker, C., J. Weibezahn, H. Patzelt, P. Tessarz, C. Strub, K. Zeth, A. Erbse, J. Schneider-Mergener, J. W. Chin, P. G. Schultz, B. Bukau, and A. Mogk. 2004. Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 11:607–615.
   PubMed Web of Science ®Google Scholar
• Sheu, Y. J., B. Santos, N. Fortin, C. Costigan, and M. Snyder. 1998. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell. Biol. 18:4053–4069.
   PubMed Web of Science ®Google Scholar
• Shorter, J., and S. Lindquist. 2005. Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 6:435–450.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Tessarz, P., A. Mogk, and B. Bukau. 2008. Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol. Microbiol. 68:87–97.
   PubMed Web of Science ®Google Scholar
• Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364–2368.
   PubMed Web of Science ®Google Scholar
• Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G. F. Berriz, R. L. Brost, M. Chang, Y. Chen, X. Cheng, G. Chua, H. Friesen, D. S. Goldberg, J. Haynes, C. Humphries, G. He, S. Hussein, L. Ke, N. Krogan, Z. Li, J. N. Levinson, H. Lu, P. Menard, C. Munyana, A. B. Parsons, O. Ryan, R. Tonikian, T. Roberts, A. M. Sdicu, J. Shapiro, B. Sheikh, B. Suter, S. L. Wong, L. V. Zhang, H. Zhu, C. G. Burd, S. Munro, C. Sander, J. Rine, J. Greenblatt, M. Peter, A. Bretscher, G. Bell, F. P. Roth, G. W. Brown, B. Andrews, H. Bussey, and C. Boone. 2004. Global mapping of the yeast genetic interaction network. Science 303:808–813.
   PubMed Web of Science ®Google Scholar
• van Drogen, F., and M. Peter. 2002. Spa2p functions as a scaffold-like protein to recruit the Mpk1p MAP kinase module to sites of polarized growth. Curr. Biol. 12:1698–1703.
   PubMed Web of Science ®Google Scholar
• Weibezahn, J., C. Schlieker, B. Bukau, and A. Mogk. 2003. Characterization of a trap mutant of the AAA+ chaperone ClpB. J. Biol. Chem. 278:32608–32617.
   PubMed Web of Science ®Google Scholar
• Weibezahn, J., P. Tessarz, C. Schlieker, R. Zahn, Z. Maglica, S. Lee, H. Zentgraf, E. U. Weber-Ban, D. A. Dougan, F. T. Tsai, A. Mogk, and B. Bukau. 2004. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119:653–665.
   PubMed Web of Science ®Google Scholar
• Whitesell, L., and S. L. Lindquist. 2005. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer. 5:761–772.
   PubMed Web of Science ®Google Scholar
• Young, J. C., J. M. Barral, and F. U. Hartl. 2003. More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28:541–547.
   PubMed Web of Science ®Google Scholar