Use of cysteine-reactive cross-linkers to probe conformational flexibility of human DJ-1 demonstrates that Glu18 mutations are dimers

Journal of Neurochemistry

Volumn 130, Issue 6, 2014, Pages 839-853

  Prahlad, Janani ^a   Hauser, David N ^b,c   Milkovic, Nicole M ^a   Cookson, Mark R ^b   Wilson, Mark A ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

cysteine oxidation; DJ 1; PARK7; Parkinson disease; parkinsonism; structure

Indexed keywords

BIS MALEIMIDOETHANE; DIMER; DIMETHYL SULFOXIDE; DISUCCINIMIDYL SUBERATE; DJ 1 PROTEIN; MUTANT PROTEIN; THIOL DERIVATIVE; UNCLASSIFIED DRUG; CROSS LINKING REAGENT; CYSTEINE; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; GLUTAMIC ACID; NITROGEN; ONCOPROTEIN; PARK7 PROTEIN, HUMAN; RECOMBINANT PROTEIN; SIGNAL PEPTIDE; SOLVENT;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; HUMAN; IN VITRO STUDY; MOLECULAR WEIGHT; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; OXIDATION; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; SEDIMENTATION EQUILIBRIUM ULTRACENTRIFUGATION; THERMOSTABILITY; ULTRACENTRIFUGATION; WILD TYPE; X RAY CRYSTALLOGRAPHY; ALGORITHM; CHEMISTRY; CRYSTALLIZATION; CYSTEINE OXIDATION; DIMERIZATION; DJ-1; GENETICS; HEAT; HEK293 CELL LINE; ISOLATION AND PURIFICATION; OXIDATION REDUCTION REACTION; PARK7; PARKINSON DISEASE; PARKINSONISM; STRUCTURE;

CYSTEINE OXIDATION; DJ-1; PARK7; PARKINSON DISEASE; PARKINSONISM; STRUCTURE;

ALGORITHMS; CIRCULAR DICHROISM; CROSS-LINKING REAGENTS; CRYSTALLIZATION; CYSTEINE; DIMERIZATION; GLUTAMIC ACID; HEK293 CELLS; HOT TEMPERATURE; HUMANS; INDICATORS AND REAGENTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR WEIGHT; MUTATION; NITROGEN ISOTOPES; ONCOGENE PROTEINS; OXIDATION-REDUCTION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SOLVENTS; ULTRACENTRIFUGATION;

EID: 84908254530     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12763     Document Type: Article

References (61)

1. Afonine P. V., Grosse-Kunstleve R. W., Echols N., et al,. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367.
2. Aleyasin H., Rousseaux M. W. C., Phillips M., et al,. (2007) The Parkinson's disease gene DJ-1 is also a key regulator of stroke-induced damage. Proc. Natl Acad. Sci. USA 104, 18748-18753.
3. Billia F., Hauck L., Grothe D., Konecny F., Rao V., Kim R. H., and, Mak T. W., (2013) Parkinson-susceptibility gene DJ-1/PARK7 protects the murine heart from oxidative damage in vivo. Proc. Natl Acad. Sci. USA 110, 6085-6090.
4. Blackinton J., Lakshminarasimhan M., Thomas K. J., Ahmad R., Greggio E., Raza A. S., Cookson M. R., and, Wilson M. A., (2009) Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the parkinsonism protein DJ-1. J. Biol. Chem. 284, 6476-6485.
5. Bonifati V., Rizzu P., van Baren M. J., et al,. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299, 256-259.
6. Canet-Aviles R. M., Wilson M. A., Miller D. W., et al,. (2004) The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc. Natl Acad. Sci. USA 101, 9103-9108.
7. Cao J., Ying M., Xie N., et al,. (2014) The oxidation states of DJ-1 dictate the cell fate in response to oxidative stress triggered by 4-HPR: autophagy or apoptosis. Antioxid. Redox Signal. doi: 10.1089/ars.2013.5446 [Epub ahead of print].
8. Cookson M. R., and, Bandmann O., (2010) Parkinson's disease: insights from pathways. Hum. Mol. Genet. 19 (R1), R21-R27.
9. Delaglio F., Grzesiek S., Vuister G. W., Zhu G., Pfeifer J., and, Bax A., (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
10. Emsley P., and, Cowtan K., (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
11. Fenn T. D., Ringe D., and, Petsko G. A., (2003) POVScript+: a program for model and data visualization using persistence of vision ray-tracing. J. Appl. Crystallogr. 36, 944-947.
12. Giaime E., Yamaguchi H., Gautier C. A., Kitada T., and, Shen J., (2012) Loss of DJ-1 does not affect mitochondrial respiration but increases ROS production and mitochondrial permeability transition pore opening. PLoS ONE 7, e40501.
13. Green N. S., Reisler E., and, Houk K. N., (2001) Quantitative evaluation of the lengths of homobifunctional protein cross-linking reagents used as molecular rulers. Protein Sci. 10, 1293-1304.
14. Guzman J. N., Sanchez-Padilla J., Wokosin D., Kondapalli J., Ilijic E., Schumacker P. T., and, Surmeier D. J., (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468, 696-700.
15. Hao L. Y., Giasson B. I., and, Bonini N. M., (2010) DJ-1 is critical for mitochondrial function and rescues PINK1 loss of function. Proc. Natl Acad. Sci. USA 107, 9747-9752.
16. Hauser D. N., and, Hastings T. G., (2013) Mitochondrial dysfunction and oxidative stress in Parkinson's disease and monogenic parkinsonism. Neurobiol. Dis. 51, 35-42.
17. Hod Y., Pentyala S. N., Whyard T. C., and, El-Maghrabi M. R., (1999) Identification and characterization of a novel protein that regulates RNA-protein interaction. J. Cell. Biochem. 72, 435-444.
18. Holyoak T., Fenn T. D., Wilson M. A., Moulin A. G., Ringe D., and, Petsko G. A., (2003) Malonate: a versatile cryoprotectant and stabilizing solution for salt-grown macromolecular crystals. Acta Crystallogr. D Biol. Crystallogr. 59, 2356-2358.
19. Honbou K., Suzuki N. N., Horiuchi M., Niki T., Taira T., Ariga H., and, Inagaki F., (2003) The crystal structure of DJ-1, a protein related to male fertility and Parkinson's disease. J. Biol. Chem. 278, 31380-31384.
20. Huai Q., Sun Y., Wang H., Chin L. S., Li L., Robinson H., and, Ke H., (2003) Crystal structure of DJ-1/RS and implication on familial Parkinson's disease. FEBS Lett. 549, 171-175.
21. Hulleman J. D., Mirzaei H., Guigard E., Taylor K. L., Ray S. S., Kay C. M., Regnier F. E., and, Rochet J. C., (2007) Destabilization of DJ-1 by familial substitution and oxidative modifications: implications for Parkinson's disease. Biochemistry 46, 5776-5789.
22. Im J. Y., Lee K. W., Junn E., and, Mouradian M. M., (2010) DJ-1 protects against oxidative damage by regulating the thioredoxin/ASK1 complex. Neurosci. Res. 67, 203-208.
23. Imai Y., and, Lu B., (2011) Mitochondrial dynamics and mitophagy in Parkinson's disease: disordered cellular power plant becomes a big deal in a major movement disorder. Curr. Opin. Neurobiol. 21, 935-941.
24. Irrcher I., Aleyasin H., Seifert E. L., et al,. (2010) Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum. Mol. Genet. 19, 3734-3746.
25. Johnson B. A., (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352.
26. Joselin A. P., Hewitt S. J., Callaghan S. M., Kim R. H., Chung Y. H., Mak T. W., Shen J., Slack R. S., and, Park D. S., (2012) ROS-dependent regulation of Parkin and DJ-1 localization during oxidative stress in neurons. Hum. Mol. Genet. 21, 4888-4903.
27. Kahle P. J., Waak J., and, Gasser T., (2009) DJ-1 and prevention of oxidative stress in Parkinson's disease and other age-related disorders. Free Radic. Biol. Med. 47, 1354-1361.
28. Kato I., Maita H., Takahashi-Niki K., Saito Y., Noguchi N., Iguchi-Ariga S. M., and, Ariga H., (2013) Oxidized DJ-1 inhibits p53 by sequestering p53 from promoters in a DNA-binding affinity-dependent manner. Mol. Cell. Biol. 33, 340-359.
29. Kinumi T., Kimata J., Taira T., Ariga H., and, Niki E., (2004) Cysteine-106 of DJ-1 is the most sensitive cysteine residue to hydrogen peroxide-mediated oxidation in vivo in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 317, 722-728.
30. Krissinel E., and, Henrick K., (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
31. Lakshminarasimhan M., Maldonado M. T., Zhou W., Fink A. L., and, Wilson M. A., (2008) Structural impact of three Parkinsonism-associated missense mutations on human DJ-1. Biochemistry 47, 1381-1392.
32. Lakshminarasimhan M., Madzelan P., Nan R., Milkovic N. M., and, Wilson M. A., (2010) Evolution of new enzymatic function by structural modulation of cysteine reactivity in Pseudomonas fluorescens isocyanide hydratase. J. Biol. Chem. 285, 29651-29661.
33. Larsen N. J., Ambrosi G., Mullett S. J., Berman S. B., and, Hinkle D. A., (2011) DJ-1 knock-down impairs astrocyte mitochondrial function. Neuroscience 196, 251-264.
34. Laue T. M., Shah B. D., Ridgeway T. M., and, Pelletier S. L., (1992) Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science (, Harding S. E., Rowe A. J., and, Horton J. C., eds.), pp. 90-125. The Royal Society of Chemistry, Cambridge.
35. Lee S. J., Kim S. J., Kim I. K., et al,. (2003) Crystal structures of human DJ-1 and Escherichia coli Hsp31, which share an evolutionarily conserved domain. J. Biol. Chem. 278, 44552-44559.
36. Li H., Wells S. A., Jimenez-Roldan J. E., Romer R. A., Zhao Y., Sadler P. J., and, O'Connor P. B., (2012) Protein flexibility is key to cisplatin crosslinking in calmodulin. Protein Sci. 21, 1269-1279.
37. Lin J., Prahlad J., and, Wilson M. A., (2012) Conservation of oxidative protein stabilization in an insect homologue of parkinsonism-associated protein DJ-1. Biochemistry 51, 3799-3807.
38. Macedo M. G., Anar B., Bronner I. F., Cannella M., Squitieri F., Bonifati V., Hoogeveen A., Heutink P., and, Rizzu P., (2003) The DJ-1(L166P) mutant protein associated with early onset Parkinson's disease is unstable and forms higher-order protein complexes. Hum. Mol. Genet. 12, 2807-2816.
39. Maita C., Maita H., Iguchi-Ariga S. M., and, Ariga H., (2013) Monomer DJ-1 and its N-terminal sequence are necessary for mitochondrial localization of DJ-1 mutants. PLoS ONE 8, e54087.
40. Malgieri G., and, Eliezer D., (2008) Structural effects of Parkinson's disease linked DJ-1 mutations. Protein Sci. 17, 855-868.
41. Martinat C., Shendelman S., Jonason A., Leete T., Beal M. F., Yang L., Floss T., and, Abeliovich A., (2004) Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES- derived cell model of primary Parkinsonism. PLoS Biol. 2, e327.
42. Menzies F. M., Yenisetti S. C., and, Min K. T., (2005) Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Curr. Biol. 15, 1578-1582.
43. Meulener M., Whitworth A. J., Armstrong-Gold C. E., Rizzu P., Heutink P., Wes P. D., Pallanck L. J., and, Bonini N. M., (2005) Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Curr. Biol. 15, 1572-1577.
44. Meulener M. C., Xu K., Thomson L., Ischiropoulos H., and, Bonini N. M., (2006) Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging. Proc. Natl Acad. Sci. USA 103, 12517-12522.
45. Miller D. W., Ahmad R., Hague S., et al,. (2003) L166P mutant DJ-1, causative for recessive Parkinson's disease, is degraded through the ubiquitin-proteasome system. J. Biol. Chem. 278, 36588-36595.
46. Moore D. J., Zhang L., Dawson T. M., and, Dawson V. L., (2003) A missense mutation (L166P) in DJ-1, linked to familial Parkinson's disease, confers reduced protein stability and impairs homo-oligomerization. J. Neurochem. 87, 1558-1567.
47. Nagakubo D., Taira T., Kitaura H., Ikeda M., Tamai K., IguchiAriga S. M. M., and, Ariga H., (1997) DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem. Biophys. Res. Commun. 231, 509-513.
48. Oh K. J., Park Y. S., Lee K. A., Chung Y. J., and, Cho T. J., (2004) Molecular characterization of a thiJ-like gene in Chinese cabbage. J. Biochem. Mol. Biol. 37, 343-350.
49. Otwinowski Z., and, Minor W., (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
50. Pantoliano M. W., Petrella E. C., Kwasnoski J. D., et al,. (2001) High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screen. 6, 429-440.
51. Ramsey C. P., and, Giasson B. I., (2010) L10p and P158DEL DJ-1 mutations cause protein instability, aggregation, and dimerization impairments. J. Neurosci. Res. 88, 3111-3124.
52. Repici M., Straatman K. R., Balduccio N., Enguita F. J., Outeiro T. F., and, Giorgini F., (2013) Parkinson's disease-associated mutations in DJ-1 modulate its dimerization in living cells. J. Mol. Med. 91, 599-611.
53. Scopes R. K., (1974) Measurement of protein by spectrophotometry at 205 nm. Anal. Biochem. 59, 277-282.
54. Shadrach K. G., Rayborn M. E., Hollyfield J. G., and, Bonilha V. L., (2013) DJ-1-dependent regulation of oxidative stress in the retinal pigment epithelium (RPE). PLoS ONE 8, e67983.
55. Stefanatos R., Sriram A., Kiviranta E., Mohan A., Ayala V., Jacobs H. T., Pamplona R., and, Sanz A., (2012) dj-1beta regulates oxidative stress, insulin-like signaling and development in Drosophila melanogaster. Cell Cycle 11, 3876-3886.
56. Tao X., and, Tong L., (2003) Crystal structure of human DJ-1, a protein associated with early onset Parkinson's disease. J. Biol. Chem. 278, 31372-31379.
57. de Vries R. L., and, Przedborski S., (2013) Mitophagy and Parkinson's disease: be eaten to stay healthy. Mol. Cell. Neurosci. 55, 37-43.
58. Wagenfeld A., Gromoll J., and, Cooper T. G., (1998) Molecular cloning and expression of rat contraception associated protein 1 (CAP1), a protein putatively involved in fertilization. Biochem. Biophys. Res. Commun. 251, 545-549.
59. Wilson M. A., Collins J. L., Hod Y., Ringe D., and, Petsko G. A., (2003) The 1.1-A resolution crystal structure of DJ-1, the protein mutated in autosomal recessive early onset Parkinson's disease. Proc. Natl Acad. Sci. USA 100, 9256-9261.
60. Witt A. C., Lakshminarasimhan M., Remington B. C., Hasim S., Pozharski E., and, Wilson M. A., (2008) Cysteine pKa depression by a protonated glutamic acid in human DJ-1. Biochemistry 47, 7430-7440.
61. Yokota T., Sugawara K., Ito K., Takahashi R., Ariga H., and, Mizusawa H., (2003) Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochem. Biophys. Res. Commun. 312, 1342-1348.