Cytosolic proteostasis through importing of misfolded proteins into mitochondria

Nature

Volumn 543, Issue 7645, 2017, Pages 443-446

  Ruan, Linhao ^a,b   Zhou, Chuankai ^c   Jin, Erli ^b   Kucharavy, Andrei ^a,b   Zhang, Ying ^c   Wen, Zhihui ^c   Florens, Laurence ^c   Li, Rong ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HEAT SHOCK PROTEIN 70; MITOCHONDRIAL PROTEIN; PROTEASOME; PROTEINASE; PEPTIDE HYDROLASE; PROTEIN; PROTEIN AGGREGATE;

CELLS AND CELL COMPONENTS; DEGRADATION; GENETIC ANALYSIS; MITOCHONDRION; NEUROLOGY; PROTEIN; YEAST;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN MISFOLDING; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; HEAT SHOCK RESPONSE; HOMEOSTASIS; METABOLISM; PHYSIOLOGY; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

CELL LINE; CYTOSOL; HEAT-SHOCK RESPONSE; HOMEOSTASIS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PEPTIDE HYDROLASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN AGGREGATES; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN TRANSPORT; PROTEINS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE;

EID: 85015714481     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature21695     Document Type: Article

References (47)

1. Lin, M. T. & Beal, M. F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795 (2006).
2. Balch, W. E., Morimoto, R. I., Dillin, A. & Kelly, J. W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008).
3. Hartl, F. U., Bracher, A. & Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332 (2011).
4. Schapira, A. H. Mitochondrial diseases. Lancet 379, 1825-1834 (2012).
5. López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M. & Kroemer, G. The hallmarks of aging. Cell 153, 1194-1217 (2013).
6. Hansson Petersen, C. A. et al. The amyloid β -peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc. Natl Acad. Sci. USA 105, 13145-13150 (2008).
7. Parsell, D. A., Kowal, A. S., Singer, M. A. & Lindquist, S. Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478 (1994).
8. Doyle, S. M., Genest, O. & Wickner, S. Protein rescue from aggregates by powerful molecular chaperone machines. Nat. Rev. Mol. Cell Biol. 14, 617-629 (2013).
9. Zhou, C. et al. Organelle-based aggregation and retention of damaged proteins in asymmetrically dividing cells. Cell 159, 530-542 (2014).
10. Miller, S. B., Mogk, A. & Bukau, B. Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J. Mol. Biol. 427, 1564-1574 (2015).
11. Gupta, R. et al. Firefly luciferase mutants as sensors of proteome stress. Nat. Methods 8, 879-884 (2011).
12. Wallace, E. W. et al. Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress. Cell 162, 1286-1298 (2015).
13. Neupert, W. & Herrmann, J. M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749 (2007).
14. Martin, J., Mahlke, K. & Pfanner, N. Role of an energized inner membrane in mitochondrial protein import. Δ Ψ drives the movement of presequences. J. Biol. Chem. 266, 18051-18057 (1991).
15. Serrano, R. Energy requirements for maltose transport in yeast. Eur. J. Biochem. 80, 97-102 (1977).
16. Stevens, H. C. & Nichols, J. W. The proton electrochemical gradient across the plasma membrane of yeast is necessary for phospholipid flip. J. Biol. Chem. 282, 17563-17567 (2007).
17. Pareek, G., Krishnamoorthy, V. & D'Silva, P. Molecular insights revealing interaction of Tim23 and channel subunits of presequence translocase. Mol. Cell. Biol. 33, 4641-4659 (2013).
18. Cabantous, S., Terwilliger, T. C. & Waldo, G. S. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23, 102-107 (2005).
19. Fehrenbacher, K. L., Yang, H. C., Gay, A. C., Huckaba, T. M. & Pon, L. A. Live cell imaging of mitochondrial movement along actin cables in budding yeast. Curr. Biol. 14, 1996-2004 (2004).
20. Lagier-Tourenne, C., Polymenidou, M. & Cleveland, D. W. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 19 (R1), R46-R64 (2010).
21. Becker, J., Walter, W., Yan, W. & Craig, E. A. Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol. Cell. Biol. 16, 4378-4386 (1996).
22. Kummer, E., Oguchi, Y., Seyffer, F., Bukau, B. & Mogk, A. Mechanism of Hsp104/ClpB inhibition by prion curing guanidinium hydrochloride. FEBS Lett. 587, 810-817 (2013).
23. Ryan, M. T., Voos, W. & Pfanner, N. Assaying protein import into mitochondria. Methods Cell Biol. 65, 189-215 (2001).
24. Devi, L., Raghavendran, V., Prabhu, B. M., Avadhani, N. G. & Anandatheerthavarada, H. K. Mitochondrial import and accumulation of α -synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J. Biol. Chem. 283, 9089-9100 (2008).
25. Baker, M. J., Tatsuta, T. & Langer, T. Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol. 3, a007559 (2011).
26. Rep, M. et al. Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science 274, 103-106 (1996).
27. Lee, D. H. & Goldberg, A. L. Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J. Biol. Chem. 271, 27280-27284 (1996).
28. Collins, G. A., Gomez, T. A., Deshaies, R. J. & Tansey, W. P. Combined chemical and genetic approach to inhibit proteolysis by the proteasome. Yeast 27, 965-974 (2010).
29. Knott, A. B., Perkins, G., Schwarzenbacher, R. & Bossy-Wetzel, E. Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 9, 505-518 (2008).
30. Tyedmers, J., Mogk, A. & Bukau, B. Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 11, 777-788 (2010).
31. Longtine, M. S. et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 (1998).
32. Mumberg, D., Müller, R. & Funk, M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119-122 (1995).
33. Huh, W. K. et al. Global analysis of protein localization in budding yeast. Nature 425, 686-691 (2003).
34. Tran, P. T., Paoletti, A. & Chang, F. Imaging green fluorescent protein fusions in living fission yeast cells. Methods 33, 220-225 (2004).
35. Zhou, C. et al. Motility and segregation of Hsp104-associated protein aggregates in budding yeast. Cell 147, 1186-1196 (2011).
36. Imamura, H. et al. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc. Natl Acad. Sci. USA 106, 15651-15656 (2009).
37. Florens, L. & Washburn, M. P. Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328, 159-175 (2006).
38. Washburn, M. P., Wolters, D. & Yates, J. R., III. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247 (2001).
39. Eng, J. K., McCormack, A. L. & Yates, J. R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989 (1994).
40. Tabb, D. L., McDonald, W. H. & Yates, J. R., III. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26 (2002).
41. Zhang, Y., Wen, Z., Washburn, M. P. & Florens, L. Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal. Chem. 82, 2272-2281 (2010).
42. Reinders, J., Zahedi, R. P., Pfanner, N., Meisinger, C. & Sickmann, A. Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J. Proteome Res. 5, 1543-1554 (2006).
43. Lam, S. S. et al. Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 12, 51-54 (2015).
44. Boldogh, I. R. & Pon, L. A. Purification and subfractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol. 80, 45-64 (2007).
45. Stojanovski, D., Pfanner, N. & Wiedemann, N. Import of proteins into mitochondria. Methods Cell Biol. 80, 783-806 (2007).
46. De Santis, M. E. et al. Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151, 778-793 (2012).
47. Fernández-Higuero, J. A. et al. Allosteric communication between the nucleotide binding domains of caseinolytic peptidase B. J. Biol. Chem. 286, 25547-25555 (2011).