The role of Djp1 in import of the mitochondrial protein mim1 demonstrates specificity between a cochaperone and its substrate protein

Molecular and Cellular Biology

Volumn 33, Issue 20, 2013, Pages 4083-4094

  Papic, Dažen ^a   Elbaz Alon, Yael ^b   Koerdt, Sophia Nina ^a   Leopold, Karoline ^a   Worm, Dennis ^a   Jung, Martin ^c   Schuldiner, Maya ^b   Rapaport, Doron ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CHAPERONE; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 40; MITOCHONDRIAL IMPORT RECEPTOR TOM70; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL PROTEIN MIM1; PROTEIN DJP1; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CYTOSOL; ENDOPLASMIC RETICULUM; GENE LOCUS; HIGH THROUGHPUT SCREENING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; YEAST;

CYTOSOL; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, FUNGAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84886896451     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00227-13     Document Type: Article

References (51)

1. Schmitt S, Prokisch H, Schlunck T, Camp DG, Jr, Ahting U, Waizenegger T, Scharfe C, Meitinger T, Imhof A, Neupert W, Oefner PJ, Rapaport D. 2006. Proteome analysis of mitochondrial outer membrane from Neurospora crassa. Proteomics 6:72-80.
2. Zahedi RP, Sickmann A, Boehm AM, Winkler C, Zufall N, Schonfisch B, Guiard B, Pfanner N, Meisinger C. 2006. Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol. Biol. Cell 17:1436-1450.
3. Lithgow T, Junne T, Suda K, Gratzer S, Schatz G. 1994. The mitochondrial outer membrane protein Mas22p is essential for protein import and viability of yeast. Proc. Natl. Acad. Sci. U. S. A. 91:11973-11977.
4. Ishikawa D, Yamamoto H, Tamura Y, Moritoh K, Endo T. 2004. Two novel proteins in the mitochondrial outer membrane mediate _-barrel protein assembly. J. Cell Biol. 166:621-627.
5. Waizenegger T, Schmitt S, Zivkovic J, Neupert W, Rapaport D. 2005. Mim1, a protein required for the assembly of the TOM complex of mitochondria. EMBO Rep. 6:57-62.
6. Okamoto K, Kondo-Okamoto N, Ohsumi Y. 2009. Mitochondriaanchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17:87-97.
7. Dimmer KS, Papic D, Schumann B, Sperl D, Krumpe K, Walther DM, Rapaport D. 2012. A crucial role for Mim2 in the biogenesis of mitochondrial outer membrane proteins. J. Cell Sci. 125:3464-3473.
8. Court DA, Nargang FE, Steiner H, Hodges RS, Neupert W, Lill R. 1996. Role of the intermembrane space domain of the preprotein receptor Tom22 in protein import into mitochondria. Mol. Cell. Biol. 16:4035-4042.
9. Thornton N, Stroud DA, Milenkovic D, Guiard B, Pfanner N, Becker T. 2010. Two modular forms of the mitochondrial sorting and assembly machinery are involved in biogenesis of alpha-helical outer membrane proteins. J. Mol. Biol. 396:540-549.
10. Popov-Celeketic J, Waizenegger T, Rapaport D. 2008. Mim1 functions in an oligomeric form to facilitate the integration of Tom20 into the mitochondrial outer membrane. J. Mol. Biol. 376:671-680.
11. Lueder F, Lithgow T. 2009. The three domains of the mitochondrial outer membrane protein Mim1 have discrete functions in assembly of theTOM complex. FEBS Lett. 583:1475-1480.
12. Beddoe T, Lithgow T. 2002. Delivery of nascent polypeptides to the mitochondrial surface. Biochim. Biophys. Acta 1592:35-39.
13. Hoogenraad NJ, Ward LA, Ryan MT. 2002. Import and assembly of proteins into mitochondria of mammalian cells. Biochim. Biophys. Acta 1592:97-105.
14. Endo T, Mitsui S, Nakai M, Roise D. 1996. Binding of mitochondrial presequences to yeast cytosolic heat shock protein 70 depends on the amphiphilicity of the presequence. J. Biol. Chem. 271:4161-4167.
15. Young JC, Hoogenraad NJ, Hartl F-U. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:41-50.
16. Caplan AJ, Cyr DM, Douglas MG. 1992. YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell 71:1143-1155.
17. Hettema EH, Ruigrok CC, Koerkamp MG, van den Berg M, Tabak HF, Distel B, Braakman I. 1998. The cytosolic DnaJ-like protein djp1p is involved specifically in peroxisomal protein import. J. Cell Biol. 142:421-434.
18. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
19. Breslow DK, Cameron DM, Collins SR, Schuldiner M, Stewart-Ornstein J, Newman HW, Braun S, Madhani HD, Krogan NJ, Weissman JS. 2008. A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat. Methods 5:711-718.
20. Shlevin L, Regev-Rudzki N, Karniely S, Pines O. 2007. Location-specific depletion of a dual-localized protein. Traffic 8:169-176.
21. Kondo-Okamoto N, Shaw JM, Okamoto K. 2008. Tetratricopeptide repeat proteins Tom70 and Tom71 mediate yeast mitochondrial morphogenesis. EMBO Rep. 9:63-69.
22. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
23. Habib SJ, Waizenegger T, Lech M, Neupert W, Rapaport D. 2005. Assembly of the TOB complex of mitochondria. J. Biol. Chem. 280:6434-6440.
24. Paschen SA, Waizenegger T, Stan T, Preuss M, CyrklaffM, Hell K, Rapaport D, Neupert W. 2003. Evolutionary conservation of biogenesis of _-barrel membrane proteins. Nature 426:862-866.
25. Tong AH, Boone C. 2006. Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313:171-192.
26. Tong AH, Drees B, Nardelli G, Bader GD, Brannetti B, Castagnoli L, Evangelista M, Ferracuti S, Nelson B, Paoluzi S, Quondam M, Zucconi A, Hogue CW, Fields S, Boone C, Cesareni G. 2002. A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295:321-324.
27. Cohen Y, Schuldiner M. 2011. Advanced methods for high-throughput microscopy screening of genetically modified yeast libraries. Methods Mol. Biol. 781:127-159.
28. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, AstromoffA, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
29. Frank R. 1992. Spot synthesis: an easy technique for the positionally addressable, parallel chemical synthesis on a membrane support. Tetrahedron 48:9217-9232.
30. Kramer A, Schneider-Mergener J. 1998. Synthesis and screening of peptide libraries on continuous cellulose membrane supports. Methods Mol. Biol. 87:25-39.
31. Daum G, Gasser S, Schatz G. 1982. Import of proteins into mitochondria: energy-dependent, two-step processing of the intermembrane space enzyme cytochrome b2 by isolated yeast mitochondria. J. Biol. Chem. 257:13075-13080.
32. Walther DM, Papic D, Bos MP, Tommassen J, Rapaport D. 2009. Signals in bacterial _-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proc. Natl. Acad. Sci. U. S. A. 106:2531-2536.
33. Schägger H, Cramer WA, von Jagow G. 1994. Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by twodimensional native electrophoresis. Anal. Biochem. 217:220-230.
34. Gilon T, Chomsky O, Kulka RG. 1998. Degradation signals for ubiquitin system proteolysis in Saccharomyces cerevisiae. EMBO J. 17:2759-2766.
35. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, Punna T, Ihmels J, Andrews B, Boone C, Greenblatt JF, Weissman JS, Krogan NJ. 2005. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123:507-519.
36. Papic D, Krumpe K, Dukanovic J, Dimmer KS, Rapaport D. 2011. Multispan mitochondrial outer membrane protein Ugo1 follows a unique Mim1-dependent import pathway. J. Cell Biol. 194:397-405.
37. Shiota T, Mabuchi H, Tanaka-Yamano S, Yamano K, Endo T. 2011. In vivo protein-interaction mapping of a mitochondrial translocator protein Tom22 at work. Proc. Natl. Acad. Sci. U. S. A. 108:15179-15183.
38. Stojanovski D, Guiard B, Kozjak-Pavlovic V, Pfanner N, Meisinger C. 2007. Alternative function for the mitochondrialSAMcomplex in biogenesis of _-helical TOM proteins. J. Cell Biol. 179:881-893.
39. Ulrich T, Gross LE, Sommer MS, SchleiffE, Rapaport D. 2012. Chloroplast beta-barrel proteins are assembled into the mitochondrial outer membrane in a process that depends on the TOM and TOB complexes. J. Biol. Chem. 287:27467-27479.
40. Walsh P, Bursac D, Law YC, Cyr D, Lithgow T. 2004. The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep. 5:567-571.
41. Keil P, Weinzierl A, Kiebler M, Dietmeier K, Söllner T, Pfanner N. 1993. Biogenesis of the mitochondrial receptor complex. Two receptors are required for binding of MOM38 to the outer membrane surface. J. Biol. Chem. 268:19177-19180.
42. Ramage L, Junne T, Hahne K, Lithgow T, Schatz G. 1993. Functional cooperation of mitochondrial protein import receptors in yeast. EMBO J. 12:4115-4123.
43. Sahi C, Craig EA. 2007. Network of general and specialty J protein chaperones of the yeast cytosol. Proc. Natl. Acad. Sci. U. S. A. 104:7163-7168.
44. Summers DW, Douglas PM, Ramos CH, Cyr DM. 2009. Polypeptide transfer from Hsp40 to Hsp70 molecular chaperones. Trends Biochem. Sci. 34:230-233.
45. Wiedemann N, Pfanner N, Ryan MT. 2001. The three modules of ADP/ATP carrier cooperate in receptor recruitment and translocation into mitochondria. EMBO J. 20:951-960.
46. Becker T, Wenz LS, Kruger V, Lehmann W, Muller JM, Goroncy L, Zufall N, Lithgow T, Guiard B, Chacinska A, Wagner R, Meisinger C, Pfanner N. 2011. The mitochondrial import protein Mim1 promotes biogenesis of multispanning outer membrane proteins. J. Cell Biol. 194: 387-395.
47. Deshaies RJ, Koch BD, Werner-Washburne M, Craig EA, Schekman R. 1988. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332:800-805.
48. Werner-Washburne M, Stone DE, Craig EA. 1987. Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 7:2568-2577.
49. Fan CY, Lee S, Ren HY, Cyr DM. 2004. Exchangeable chaperone modules contribute to specification of type I and type II Hsp40 cellular function. Mol. Biol. Cell 15:761-773.
50. Andrade-Navarro MA, Sanchez-Pulido L, McBride HM. 2009. Mitochondrial vesicles: an ancient process providing new links to peroxisomes. Curr. Opin. Cell Biol. 21:560-567.
51. Delille HK, Alves R, Schrader M. 2009. Biogenesis of peroxisomes and mitochondria: linked by division. Histochem. Cell Biol. 131:441-446.