Structure and mechanistic insights into novel iron-mediated moonlighting functions of human J-protein cochaperone, Dph4

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 13194-13205

  Thakur, Anushikha ^a   Chitoor, Balasubramanyam ^a   Goswami, Arvind V ^a   Pareek, Gautam ^a   Atreya, Hanudatta S ^a   D'Silva, Patrick ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-ASE ACTIVITY; CONFORMATIONAL FLEXIBILITY; DEPENDENT FUNCTIONS; ELECTRON CARRIER; INTRACELLULAR IRON; IRON BINDING; IRON SEQUESTRATION; IRON-STORAGE PROTEIN; METABOLIC REACTIONS; NMR STRUCTURES; ORTHOLOGS; PHYSIOLOGICAL FUNCTIONS; PROTEIN FUNCTIONS; SOLUTION STRUCTURES; SPECTRAL PROPERTIES; TETRAHEDRAL COORDINATION GEOMETRY; TWO DOMAINS; UV-VISIBLE;

AMINO ACIDS; BINDING ENERGY; BIOCHEMISTRY; BIOSYNTHESIS; ENZYME ACTIVITY; MAGNETIC RESONANCE; OLIGOMERIZATION; OLIGOMERS; PARAMAGNETISM; PHYSIOLOGY; PROTEINS; REDOX REACTIONS;

IRON;

AMIDE; CHAPERONE; DIPHTHAMIDE; HEAT SHOCK PROTEIN 70; PROTEIN DPH4; RUBREDOXIN; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; GENETIC CONSERVATION; HUMAN; IRON BALANCE; IRON BINDING CAPACITY; IRON STORAGE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; ULTRAVIOLET SPECTROSCOPY;

ADENOSINE TRIPHOSPHATASES; DIPHTHERIA TOXIN; EVOLUTION, MOLECULAR; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IRON; MOLECULAR CHAPERONES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; YEASTS; ZINC FINGERS;

EID: 84859779168     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.339655     Document Type: Article

References (49)

1. Craig, E. A., Huang, P., Aron, R., and Andrew, A. (2006) The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev. Physiol. Biochem. Pharmacol. 156, 1-21
2. Bukau, B., Weissman, J., and Horwich, A. (2006) Molecular chaperones and protein quality control. Cell 125, 443-451
3. Walsh, P., Bursać, D., Law, Y. C., Cyr, D., and Lithgow, T. (2004) The J-protein family. Modulating protein assembly, disassembly and translocation. EMBO Rep. 5, 567-571 (Pubitemid 39136416)
4. Mayer, M. P., Brehmer, D., Gässler, C. S., and Bukau, B. (2001) Hsp70 chaperone machines. Adv. Protein Chem. 59, 1-44 (Pubitemid 34169300)
5. Mayer, M. P., and Bukau, B. (2005) Hsp70 chaperones. Cellular functions and molecular mechanism. Cell Mol. Life Sci. 62, 670-684
6. Cheetham, M. E., and Caplan, A. J. (1998) Structure, function and evolution of DnaJ. Conservation and adaptation of chaperone function. Cell Stress Chaperones 3, 28-36 (Pubitemid 28159676)
7. Kampinga, H. H., and Craig, E. A. (2010) The HSP70 chaperone machinery. J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11, 579-592
8. Liu, S., Milne, G. T., Kuremsky, J. G., Fink, G. R., and Leppla, S. H. (2004) Identification of the proteins required for biosynthesis of diphthamide, the target of bacterial ADP-ribosylating toxins on translation elongation factor 2. Mol. Cell Biol. 24, 9487-9497 (Pubitemid 39391685)
9. Webb, T. R., Cross, S. H., McKie, L., Edgar, R., Vizor, L., Harrison, J., Peters, J., and Jackson, I. J. (2008) Diphthamide modification of eEF2 requires a J-domain protein and is essential for normal development. J. Cell Sci. 121, 3140-3145
10. Sahi, C., and Craig, E. A. (2007) Network of general and specialty J protein chaperones of the yeast cytosol. Proc. Natl. Acad. Sci. U.S.A. 104, 7163-7168 (Pubitemid 47186026)
11. Mattheakis, L. C., Shen, W. H., and Collier, R. J. (1992) DPH5, a methyltransferase gene required for diphthamide biosynthesis in Saccharomyces cerevisiae. Mol. Cell Biol. 12, 4026-4037
12. Kuo, C. F., and Fridovich, I. (1988) A stain for iron-containing proteins sensitive to nanogram levels of iron. Anal. Biochem. 170, 183-185
13. D'Silva, P. D., Schilke, B., Walter, W., Andrew, A., and Craig, E. A. (2003) J protein cochaperone of the mitochondrial inner membrane required for protein import into the mitochondrial matrix. Proc. Natl. Acad. Sci. U.S.A. 100, 13839-13844 (Pubitemid 37499153)
14. Pareek, G., Samaddar, M., and D'Silva, P. (2011) Primary sequence that determines the functional overlap between mitochondrial heat shock protein 70 Ssc1 and Ssc3 of Saccharomyces cerevisiae. J. Biol. Chem. 286, 19001-19013
15. Proudfoot, M. (2008) Biochemical and structural characterization of a novel family of cystathionine beta-synthase domain proteins fused to a zinc ribbon-like domain. J. Mol. Biol. 375, 301-315
16. Sun, J., Zhang, J., Wu, F., Xu, C., Li, S., Zhao, W., Wu, Z., Wu, J., Zhou, C. Z., Shi, Y. (2005) Solution structure of Kti11p from Saccharomyces cerevisiae reveals a novel zinc-binding module. Biochemistry 44, 8801-8809 (Pubitemid 40840445)
17. Rao, K. K., Evans, M. C., Cammack, R., Hall, D. O., Thompson, C. L., Jackson, P. J., and Johnson, C. E. (1972) Mössbauer effect in rubredoxin. Determination of the hyperfine field of the iron in a simple iron-sulfur protein. Biochem. J. 129, 1063-1070
18. Yoon, K. S., Hille, R., Hemann, C., and Tabita, F. R. (1999) Rubredoxin from the green sulfur bacterium Chlorobium tepidum functions as an electron acceptor for pyruvate ferredoxin oxidoreductase. J. Biol. Chem. 274, 29772-29778
19. Gething, M. J., and Sambrook, J. (1992) Protein folding in the cell. Nature 355, 33-45
20. Sadis, S., and Hightower, L. E. (1992) Unfolded proteins stimulate molecular chaperone Hsc70 ATPase by accelerating ADP/ATP exchange. Biochemistry 31, 9406-9412
21. Karzai, A. W., and McMacken, R. (1996) A bipartite signaling mechanism involved in DnaJ-mediated activation of the Escherichia coli DnaK protein. J. Biol. Chem. 271, 11236-11246 (Pubitemid 26155957)
22. Bertini, I., Turano, P., and Vila, A. J. (1993) Nuclear magnetic resonance of paramagnetic metalloproteins. Chem. Rev. 93, 2833-2932
23. Szyperski, T., Luginbühl, P., Otting, G., Güntert, P., and Wüthrich, K. (1993) Protein dynamics studied by rotating frame 15N spin relaxation times. J. Biomol. NMR 3, 151-164
24. Szyperski, T., Pellecchia, M., Wall, D., Georgopoulos, C., and Wüthrich, K. (1994) NMR structure determination of the Escherichia coli DnaJ molecular chaperone. Secondary structure and backbone fold of the N-terminal region (residues 2-108) containing the highly conserved J domain. Proc. Natl. Acad. Sci. U.S.A. 91, 11343-11347 (Pubitemid 24356340)
25. Wu, F., Zhang, J., Sun, J., Huang, H., Ji, P., Chu, W., Yu, M., Yang, F., Wu, Z., Wu, J., and Shi, Y. (2008) Solution structure of human DESR1, a CSL zinc-binding protein. Proteins 71, 514-518 (Pubitemid 351358630)
26. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley & Sons, Inc., New York
27. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+. A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
28. Bitto, E., Bingman, C. A., Bittova, L., Kondrashov, D. A., Bannen, R. M., Fox, B. G., Markley, J. L., and Phillips, G. N., Jr. (2008) Structure of human J-type co-chaperone HscB reveals a tetracysteine metal-binding domain. J. Biol. Chem. 283, 30184-30192
29. Clore, G. M., and Gronenborn, A. M. (1998) New methods of structure refinement for macromolecular structure determination by NMR. Proc. Natl. Acad. Sci. U.S.A. 95, 5891-5898 (Pubitemid 28248936)
30. Greene, M. K., Maskos, K., and Landry S. J. (1998) Role of the J-domain in the cooperation of Hsp40 with Hsp70. Proc. Natl. Acad. Sci. U.S.A. 95, 6108-6113 (Pubitemid 28248972)
31. Fewell, S. W., Pipas, J. M., and Brodsky, J. L. (2002) Mutagenesis of a functional chimeric gene in yeast identifies mutations in the simian virus 40 large T antigen J domain. Proc. Natl. Acad. Sci. U.S.A. 99, 2002-2007 (Pubitemid 34169004)
32. Garimella, R., Liu, X., Qiao, W., Liang, X., Zuiderweg, E. R., Riley, M. I., and Van Doren, S. R. (2006) Hsc70 contacts helix III of the J domain from polyomavirus T antigens. Addressing a dilemma in the chaperone hypothesis of how they release E2F from pRb. Biochemistry 45, 6917-6929
33. Whalen, K. A., de Jesus, R., Kean, J. A., and Schaffhausen, B. S. (2005) Genetic analysis of the polyomavirus DnaJ domain. J. Virology 79, 9982-9990 (Pubitemid 41022339)
34. Jiang, J., Maes, E. G., Taylor, A. B., Wang, L., Hinck, A. P., Lafer, E. M., and Sousa, R. (2007) Structural basis of J cochaperone binding and regulation of Hsp70. Mol. Cell 28, 422-433 (Pubitemid 350030560)
35. Yang, S. S., Ljungdahl, L. G., Dervartanian, D. V., and Watt, G. D. (1980) Isolation and characterization of two rubredoxins from Clostridium thermoaceticum. Biochim. Biophys. Acta 590, 24-33 (Pubitemid 10108810)
36. Petitdemange, H., Marczak, R., Blusson, H., and Gay, R. (1979) Isolation and properties of reduced nicotinamide adenine dinucleotiderubredoxin oxidoreductase of Clostridium acetobutylicum. Biochem. Biophys. Res. Commun. 91, 1258-1265 (Pubitemid 10143628)
37. Bär, C., Zabel, R., Liu, S., Stark, M. J., and Schaffrath, R. (2008) A versatile partner of eukaryotic protein complexes that is involved in multiple biological processes. Kti11/Dph3. Mol. Microbiol. 69, 1221-1233
38. Craig, E. A., and Marszalek, J. (2002) A specialized mitochondrial molecular chaperone system. A role in formation of Fe/S centers. Cell Mol. Life Sci. 59, 1658-1665 (Pubitemid 35346969)
39. Lill, R., and Mühlenhoff, U. (2008) Maturation of iron-sulfur proteins in eukaryotes. Mechanisms, connected processes, and diseases. Annu. Rev. Biochem. 77, 669-700
40. Sharma, A. K., Pallesen, L. J., Spang, R. J., and Walden, W. E. (2010) Cytosolic iron-sulfur cluster assembly (CIA) system. Factors, mechanism, and relevance to cellular iron regulation. J. Biol. Chem. 285, 26745-26751
41. Tong, W. H., and Rouault, T. (2000) Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J. 19, 5692-5700
42. Broderick, J. B. (2007) Assembling iron-sulfur clusters in the cytosol. Nat. Chem. Biol. 3, 243-244
43. Mühlenhoff, U., Richhardt, N., Ristow, M., Kispal, G., and Lill, R. (2002) The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11, 2025-2036 (Pubitemid 34919277)
44. Liu, X., and Theil, E. C. (2005) Ferritins. Dynamic management of biological iron and oxygen chemistry. Acc. Chem. Res. 38, 167-175 (Pubitemid 40388095)
45. Shi, H., Bencze, K. Z., Stemmler, T. L., and Philpott, C. C. (2008) A cytosolic iron chaperone that delivers iron to ferritin. Science 320, 1207-1210 (Pubitemid 351929507)
46. Yoon, T., and Cowan, J. A. (2003) Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J. Am. Chem. Soc. 125, 6078-6084 (Pubitemid 36582978)
47. Zhang, Y., Zhu, X., Torelli, A. T., Lee, M., Dzikovski, B., Koralewski, R. M., Wang, E., Freed, J., Krebs, C., Ealick, S. E., and Lin, H. (2010) Diphthamide biosynthesis requires an organic radical generated by an iron-sulfur enzyme. Nature 465, 891-896
48. Sahi, C., Lee, T., Inada, M., Pleiss, J. A., and Craig, E. A. (2010) Cwc23, an essential J protein critical for pre-mRNA splicing with a dispensable J domain. Mol. Cell Biol. 30, 33-42
49. Yang, C., Owen, H. A., and Yang, P. (2008) Dimeric heat shock protein 40 binds radial spokes for generating coupled power strokes and recovery strokes of 9 + 2 flagella. J. Cell Biol. 180, 403-415 (Pubitemid 351185924)