High-fat diet induced isoform changes of the Parkinson's disease protein DJ-1

Journal of Proteome Research

Volumn 13, Issue 5, 2014, Pages 2339-2351

  Poschmann, Gereon ^a   Seyfarth, Katrin ^b   Besong Agbo, Daniela ^c   Klafki, Hans Wolfgang ^c   Rozman, Jan ^b   Wurst, Wolfgang ^b,d,e,f   Wiltfang, Jens ^c,i   Meyer, Helmut E ^g,h   Klingenspor, Martin ^b   Stühler, Kai ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^g RUHR UNIVERSITY BOCHUM   (Germany)

^h LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

ⁱ UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

DJ 1; high fat diet; obesity; oxidative thiol modification; protein isoforms

Indexed keywords

DJ 1 PROTEIN; DJ-1 PROTEIN, MOUSE; ISOPROTEIN; ONCOPROTEIN; PEROXIREDOXIN;

AKR MOUSE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY MASS; BRAIN REGION; BRAIN STEM; C57BL/6N MOUSE; CALORIC INTAKE; CEREBELLUM; CONTROLLED STUDY; FAT MASS; HYPOTHALAMUS; IMMUNODETECTION; ISOELECTRIC FOCUSING; LIPID DIET; LIVER; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; SKELETAL MUSCLE; SWISS WEBSTER MOUSE; WEIGHT GAIN; WESTERN BLOTTING; WHITE ADIPOSE TISSUE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CHEMISTRY; GENETICS; INBRED MOUSE STRAIN; ISOELECTRIC POINT; LIQUID CHROMATOGRAPHY; METABOLISM; OBESITY; OVERWEIGHT; PROCEDURES; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; DIET, HIGH-FAT; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HYPOTHALAMUS; ISOELECTRIC POINT; MALE; MASS SPECTROMETRY; MICE, INBRED AKR; MICE, INBRED C57BL; MICE, INBRED STRAINS; OBESITY; ONCOGENE PROTEINS; OVERWEIGHT; PARKINSON DISEASE; PEROXIREDOXINS; PROTEIN ISOFORMS; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY;

EID: 84899796114     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401157k     Document Type: Article

References (64)

1. James, W. P. The epidemiology of obesity: the size of the problem J. Intern. Med. 2008, 263 (4) 336-52
2. Prospective Studies Collaboration; Body-mass index and cause-specific mortality in 900000 adults: collaborative analyses of 57 prospective studies. Lancet 2009, 373, (9669), 1083-1096.
3. The InterAct Consortium; Long-Term Risk of Incident Type 2 Diabetes and Measures of Overall and Regional Obesity: The EPIC-InterAct Case-Cohort Study. PLoS Med. 2012, 9, (6), e1001230.
4. Hill, J. O.; Wyatt, H. R.; Peters, J. C. Energy balance and obesity Circulation 2012, 126 (1) 126-132
5. Chaput, J. P.; Klingenberg, L.; Astrup, A.; Sjodin, A. M. Modern sedentary activities promote overconsumption of food in our current obesogenic environment Obes. Rev. 2011, 12 (5) e12-20
6. Patrick, K.; Norman, G. J.; Calfas, K. J.; Sallis, J. F.; Zabinski, M. F.; Rupp, J.; Cella, J. Diet, physical activity, and sedentary behaviors as risk factors for overweight in adolescence Arch. Pediatr. Adolesc. Med. 2004, 158 (4) 385-390
7. Day, F. R.; Loos, R. J. Developments in obesity genetics in the era of genome-wide association studies J. Nutrigenet. Nutrigenomics 2011, 4 (4) 222-238
8. Segal, N. L.; Allison, D. B. Twins and virtual twins: bases of relative body weight revisited Int. J. Obes. Relat. Metab. Disord. 2002, 26 (4) 437-441
9. Reilly, J. J.; Armstrong, J.; Dorosty, A. R.; Emmett, P. M.; Ness, A.; Rogers, I.; Steer, C.; Sherriff, A. Avon Longitudinal Study of, P.; Children Study, T., Early life risk factors for obesity in childhood: cohort study BMJ 2005, 330 (7504) 1357
10. Dubois, L.; Girard, M.; Girard, A.; Tremblay, R.; Boivin, M.; Perusse, D. Genetic and environmental influences on body size in early childhood: a twin birth-cohort study Twin Res. Hum. Genet. 2007, 10 (3) 479-485
11. Speliotes, E. K.; Willer, C. J.; Berndt, S. I.; Monda, K. L.; Thorleifsson, G.; Jackson, A. U.; Lango Allen, H.; Lindgren, C. M.; Luan, J.; Magi, R.; Randall, J. C.; Vedantam, S.; Winkler, T. W.; Qi, L.; Workalemahu, T.; Heid, I. M.; Steinthorsdottir, V.; Stringham, H. M.; Weedon, M. N.; Wheeler, E.; Wood, A. R.; Ferreira, T.; Weyant, R. J.; Segre, A. V.; Estrada, K.; Liang, L.; Nemesh, J.; Park, J. H.; Gustafsson, S.; Kilpelainen, T. O.; Yang, J.; Bouatia-Naji, N.; Esko, T.; Feitosa, M. F.; Kutalik, Z.; Mangino, M.; Raychaudhuri, S.; Scherag, A.; Smith, A. V.; Welch, R.; Zhao, J. H.; Aben, K. K.; Absher, D. M.; Amin, N.; Dixon, A. L.; Fisher, E.; Glazer, N. L.; Goddard, M. E.; Heard-Costa, N. L.; Hoesel, V.; Hottenga, J. J.; Johansson, A.; Johnson, T.; Ketkar, S.; Lamina, C.; Li, S.; Moffatt, M. F.; Myers, R. H.; Narisu, N.; Perry, J. R.; Peters, M. J.; Preuss, M.; Ripatti, S.; Rivadeneira, F.; Sandholt, C.; Scott, L. J.; Timpson, N. J.; Tyrer, J. P.; van Wingerden, S.; Watanabe, R. M.; White, C. C.; Wiklund, F.; Barlassina, C.; Chasman, D. I.; Cooper, M. N.; Jansson, J. O.; Lawrence, R. W.; Pellikka, N.; Prokopenko, I.; Shi, J.; Thiering, E.; Alavere, H.; Alibrandi, M. T.; Almgren, P.; Arnold, A. M.; Aspelund, T.; Atwood, L. D.; Balkau, B.; Balmforth, A. J.; Bennett, A. J.; Ben-Shlomo, Y.; Bergman, R. N.; Bergmann, S.; Biebermann, H.; Blakemore, A. I.; Boes, T.; Bonnycastle, L. L.; Bornstein, S. R.; Brown, M. J.; Buchanan, T. A.; Busonero, F.; Campbell, H.; Cappuccio, F. P.; Cavalcanti-Proenca, C.; Chen, Y. D.; Chen, C. M.; Chines, P. S.; Clarke, R.; Coin, L.; Connell, J.; Day, I. N.; den Heijer, M.; Duan, J.; Ebrahim, S.; Elliott, P.; Elosua, R.; Eiriksdottir, G.; Erdos, M. R.; Eriksson, J. G.; Facheris, M. F.; Felix, S. B.; Fischer-Posovszky, P.; Folsom, A. R.; Friedrich, N.; Freimer, N. B.; Fu, M.; Gaget, S.; Gejman, P. V.; Geus, E. J.; Gieger, C.; Gjesing, A. P.; Goel, A.; Goyette, P.; Grallert, H.; Grassler, J.; Greenawalt, D. M.; Groves, C. J.; Gudnason, V.; Guiducci, C.; Hartikainen, A. L.; Hassanali, N.; Hall, A. S.; Havulinna, A. S.; Hayward, C.; Heath, A. C.; Hengstenberg, C.; Hicks, A. A.; Hinney, A.; Hofman, A.; Homuth, G.; Hui, J.; Igl, W.; Iribarren, C.; Isomaa, B.; Jacobs, K. B.; Jarick, I.; Jewell, E.; John, U.; Jorgensen, T.; Jousilahti, P.; Jula, A.; Kaakinen, M.; Kajantie, E.; Kaplan, L. M.; Kathiresan, S.; Kettunen, J.; Kinnunen, L.; Knowles, J. W.; Kolcic, I.; Konig, I. R.; Koskinen, S.; Kovacs, P.; Kuusisto, J.; Kraft, P.; Kvaloy, K.; Laitinen, J.; Lantieri, O.; Lanzani, C.; Launer, L. J.; Lecoeur, C.; Lehtimaki, T.; Lettre, G.; Liu, J.; Lokki, M. L.; Lorentzon, M.; Luben, R. N.; Ludwig, B.; Magic; Manunta, P.; Marek, D.; Marre, M.; Martin, N. G.; McArdle, W. L.; McCarthy, A.; McKnight, B.; Meitinger, T.; Melander, O.; Meyre, D.; Midthjell, K.; Montgomery, G. W.; Morken, M. A.; Morris, A. P.; Mulic, R.; Ngwa, J. S.; Nelis, M.; Neville, M. J.; Nyholt, D. R.; O'Donnell, C. J.; O'Rahilly, S.; Ong, K. K.; Oostra, B.; Pare, G.; Parker, A. N.; Perola, M.; Pichler, I.; Pietilainen, K. H.; Platou, C. G.; Polasek, O.; Pouta, A.; Rafelt, S.; Raitakari, O.; Rayner, N. W.; Ridderstrale, M.; Rief, W.; Ruokonen, A.; Robertson, N. R.; Rzehak, P.; Salomaa, V.; Sanders, A. R.; Sandhu, M. S.; Sanna, S.; Saramies, J.; Savolainen, M. J.; Scherag, S.; Schipf, S.; Schreiber, S.; Schunkert, H.; Silander, K.; Sinisalo, J.; Siscovick, D. S.; Smit, J. H.; Soranzo, N.; Sovio, U.; Stephens, J.; Surakka, I.; Swift, A. J.; Tammesoo, M. L.; Tardif, J. C.; Teder-Laving, M.; Teslovich, T. M.; Thompson, J. R.; Thomson, B.; Tonjes, A.; Tuomi, T.; van Meurs, J. B.; van Ommen, G. J.; Vatin, V.; Viikari, J.; Visvikis-Siest, S.; Vitart, V.; Vogel, C. I.; Voight, B. F.; Waite, L. L.; Wallaschofski, H.; Walters, G. B.; Widen, E.; Wiegand, S.; Wild, S. H.; Willemsen, G.; Witte, D. R.; Witteman, J. C.; Xu, J.; Zhang, Q.; Zgaga, L.; Ziegler, A.; Zitting, P.; Beilby, J. P.; Farooqi, I. S.; Hebebrand, J.; Huikuri, H. V.; James, A. L.; Kahonen, M.; Levinson, D. F.; Macciardi, F.; Nieminen, M. S.; Ohlsson, C.; Palmer, L. J.; Ridker, P. M.; Stumvoll, M.; Beckmann, J. S.; Boeing, H.; Boerwinkle, E.; Boomsma, D. I.; Caulfield, M. J.; Chanock, S. J.; Collins, F. S.; Cupples, L. A.; Smith, G. D.; Erdmann, J.; Froguel, P.; Gronberg, H.; Gyllensten, U.; Hall, P.; Hansen, T.; Harris, T. B.; Hattersley, A. T.; Hayes, R. B.; Heinrich, J.; Hu, F. B.; Hveem, K.; Illig, T.; Jarvelin, M. R.; Kaprio, J.; Karpe, F.; Khaw, K. T.; Kiemeney, L. A.; Krude, H.; Laakso, M.; Lawlor, D. A.; Metspalu, A.; et al. Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index Nat. Genet. 2010, 42 (11) 937-948
12. Godfrey, K. M.; Sheppard, A.; Gluckman, P. D.; Lillycrop, K. A.; Burdge, G. C.; McLean, C.; Rodford, J.; Slater-Jefferies, J. L.; Garratt, E.; Crozier, S. R.; Emerald, B. S.; Gale, C. R.; Inskip, H. M.; Cooper, C.; Hanson, M. A. Epigenetic gene promoter methylation at birth is associated with child's later adiposity Diabetes 2011, 60 (5) 1528-15234
13. Morton, G. J.; Cummings, D. E.; Baskin, D. G.; Barsh, G. S.; Schwartz, M. W. Central nervous system control of food intake and body weight Nature 2006, 443 (7109) 289-295
14. Ward, M. A.; Carlsson, C. M.; Trivedi, M. A.; Sager, M. A.; Johnson, S. C. The effect of body mass index on global brain volume in middle-aged adults: a cross sectional study BMC Neurol. 2005, 5, 23
15. Pannacciulli, N.; Del Parigi, A.; Chen, K.; Le, D. S.; Reiman, E. M.; Tataranni, P. A. Brain abnormalities in human obesity: a voxel-based morphometric study NeuroImage 2006, 31 (4) 1419-1425
16. Jeong, S. K.; Nam, H. S.; Son, M. H.; Son, E. J.; Cho, K. H. Interactive effect of obesity indexes on cognition Dementia Geriatr. Cognit. Disord. 2005, 19 (2-3) 91-96
17. Qiu, C.; De Ronchi, D.; Fratiglioni, L. The epidemiology of the dementias: an update Curr. Opin. Psychiatry 2007, 20 (4) 380-385
18. Kanaya, A. M.; Barrett-Connor, E.; Gildengorin, G.; Yaffe, K. Change in cognitive function by glucose tolerance status in older adults: a 4-year prospective study of the Rancho Bernardo study cohort Arch. Intern. Med. 2004, 164 (12) 1327-1333
19. Luchsinger, J. A.; Tang, M. X.; Shea, S.; Mayeux, R. Caloric intake and the risk of Alzheimer disease Arch. Neurol. 2002, 59 (8) 1258-1263
20. Wang, X.; Choi, J. W.; Joo, J. I.; Kim, D. H.; Oh, T. S.; Choi, D. K.; Yun, J. W. Differential expression of liver proteins between obesity-prone and obesity-resistant rats in response to a high-fat diet Br. J. Nutr. 2011, 106 (4) 612-626
21. Joo, J. I.; Oh, T. S.; Kim, D. H.; Choi, D. K.; Wang, X.; Choi, J. W.; Yun, J. W. Differential expression of adipose tissue proteins between obesity-susceptible and -resistant rats fed a high-fat diet Proteomics 2011, 11 (8) 1429-1448
22. Frese, C. K.; Boender, A. J.; Mohammed, S.; Heck, A. J.; Adan, R. A.; Altelaar, A. F. Profiling of Diet-Induced Neuropeptide Changes in Rat Brain by Quantitative Mass Spectrometry Anal. Chem. 2013, 85, 4594-4604
23. Klose, J.; Kobalz, U. Two-dimensional electrophoresis of proteins: an updated protocol and implications for a functional analysis of the genome Electrophoresis 1995, 16 (6) 1034-1059
24. Poschmann, G.; Sitek, B.; Sipos, B.; Stuhler, K. Application of saturation labeling in lung cancer proteomics Methods Mol. Biol. 2012, 854, 253-267
25. Schaefer, H.; Chamrad, D. C.; Marcus, K.; Reidegeld, K. A.; Bluggel, M.; Meyer, H. E. Tryptic transpeptidation products observed in proteome analysis by liquid chromatography-tandem mass spectrometry Proteomics 2005, 5 (4) 846-852
26. Hod, Y.; Pentyala, S. N.; Whyard, T. C.; El-Maghrabi, M. R. Identification and characterization of a novel protein that regulates RNA-protein interaction J. Cell. Biochem. 1999, 72 (3) 435-444
27. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20 (18) 3551-3567
28. Vizcaino, J. A.; Cote, R. G.; Csordas, A.; Dianes, J. A.; Fabregat, A.; Foster, J. M.; Griss, J.; Alpi, E.; Birim, M.; Contell, J.; O'Kelly, G.; Schoenegger, A.; Ovelleiro, D.; Perez-Riverol, Y.; Reisinger, F.; Rios, D.; Wang, R.; Hermjakob, H. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013 Nucleic Acids Res. 2013, 41, D1063-D1069
29. Besong Agbo, D.; Klafki, H.; Poschmann, G.; Seyfarth, K.; Genius, J.; Janssen, C.; Stuhler, K.; Wurst, W.; Meyer, H. E.; Klingenspor, M.; Wiltfang, J. Development of a capillary isoelectric focusing immunoassay to measure DJ-1 isoforms in biological samples Anal. Biochem. 2013, 443 (2) 197-204
30. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R. Stat. Soc. Ser. B 1995, 57 (1) 289-300
31. Canet-Aviles, R. M.; Wilson, M. A.; Miller, D. W.; Ahmad, R.; McLendon, C.; Bandyopadhyay, S.; Baptista, M. J.; Ringe, D.; Petsko, G. A.; Cookson, M. R. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (24) 9103-9108
32. Lin, X.; Cook, T. J.; Zabetian, C. P.; Leverenz, J. B.; Peskind, E. R.; Hu, S. C.; Cain, K. C.; Pan, C.; Edgar, J. S.; Goodlett, D. R.; Racette, B. A.; Checkoway, H.; Montine, T. J.; Shi, M.; Zhang, J. DJ-1 isoforms in whole blood as potential biomarkers of Parkinson disease Sci. Rep. 2012, 2, 954
33. Smith, B. K.; Andrews, P. K.; York, D. A.; West, D. B. Divergence in proportional fat intake in AKR/J and SWR/J mice endures across diet paradigms Am. J. Physiol. 1999, 277 (3 Pt 2) R776-R785
34. Prpic, V.; Watson, P. M.; Frampton, I. C.; Sabol, M. A.; Jezek, G. E.; Gettys, T. W. Adaptive changes in adipocyte gene expression differ in AKR/J and SWR/J mice during diet-induced obesity J. Nutr. 2002, 132 (11) 3325-3332
35. Lyons, J. A.; Haring, J. S.; Biga, P. R. Myostatin expression, lymphocyte population, and potential cytokine production correlate with predisposition to high-fat diet induced obesity in mice PloS One 2010, 5 (9) e12928
36. West, D. B.; Boozer, C. N.; Moody, D. L.; Atkinson, R. L. Dietary obesity in nine inbred mouse strains Am. J. Physiol. 1992, 262 (6 Pt 2) R1025-R1032
37. Hesse, D.; Dunn, M.; Heldmaier, G.; Klingenspor, M.; Rozman, J. Behavioural mechanisms affecting energy regulation in mice prone or resistant to diet-induced obesity Physiol. Behav. 2010, 99 (3) 370-380
38. Williams, L. M. Hypothalamic dysfunction in obesity Proc. Nutr. Soc. 2012, 71 (4) 521-533
39. Natale, M.; Bonino, D.; Consoli, P.; Alberio, T.; Ravid, R. G.; Fasano, M.; Bucci, E. M. A meta-analysis of two-dimensional electrophoresis pattern of the Parkinson's disease-related protein DJ-1 Bioinformatics 2010, 26 (7) 946-952
40. Elia, M., Organ and tissue contribution to metabolic rate. In Energy Metabolism: Tissue Determinants and Cellular Corollaries; Tucker, H. N.; Kinney, J. M., Eds.; Raven Press: New York, 1992.
41. Chari, M.; Lam, C. K. L.; Lam, T. K. T. Hypothalamic Fatty Acid Sensing in the Normal and Disease States. In Fat Detection: Taste, Texture, and Post Ingestive Effects; Montmayeur, J. P.; le Coutre, J., Eds.; CRC Press: Boca Raton, FL, 2010.
42. Meulener, M. C.; Xu, K.; Thomson, L.; Ischiropoulos, H.; Bonini, N. M. Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (33) 12517-12522
43. Frizzell, N.; Lima, M.; Baynes, J. W. Succination of proteins in diabetes Free Radical Res. 2011, 45 (1) 101-109
44. Frizzell, N.; Rajesh, M.; Jepson, M. J.; Nagai, R.; Carson, J. A.; Thorpe, S. R.; Baynes, J. W. Succination of thiol groups in adipose tissue proteins in diabetes: succination inhibits polymerization and secretion of adiponectin J. Biol. Chem. 2009, 284 (38) 25772-25781
45. Nagai, R.; Brock, J. W.; Blatnik, M.; Baatz, J. E.; Bethard, J.; Walla, M. D.; Thorpe, S. R.; Baynes, J. W.; Frizzell, N. Succination of protein thiols during adipocyte maturation: a biomarker of mitochondrial stress J. Biol. Chem. 2007, 282 (47) 34219-34228
46. Wilson, M. A. The Role of Cysteine Oxidation in DJ-1 Function and Dysfunction Antioxid. Redox Signaling 2011, 15 (1) 111-122
47. Kinumi, T.; Kimata, J.; Taira, T.; Ariga, H.; Niki, E. 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. 2004, 317 (3) 722-728
48. Blackinton, J.; Lakshminarasimhan, M.; Thomas, K. J.; Ahmad, R.; Greggio, E.; Raza, A. S.; Cookson, M. R.; Wilson, M. A. Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the parkinsonism protein DJ-1 J. Biol. Chem. 2009, 284 (10) 6476-6485
49. Witt, A. C.; Lakshminarasimhan, M.; Remington, B. C.; Hasim, S.; Pozharski, E.; Wilson, M. A. Cysteine pKa depression by a protonated glutamic acid in human DJ-1 Biochemistry 2008, 47 (28) 7430-7440
50. Choi, J.; Sullards, M. C.; Olzmann, J. A.; Rees, H. D.; Weintraub, S. T.; Bostwick, D. E.; Gearing, M.; Levey, A. I.; Chin, L. S.; Li, L. Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases J. Biol. Chem. 2006, 281 (16) 10816-10824
51. Madian, A. G.; Hindupur, J.; Hulleman, J. D.; Diaz-Maldonado, N.; Mishra, V. R.; Guigard, E.; Kay, C. M.; Rochet, J. C.; Regnier, F. E. Effect of single amino acid substitution on oxidative modifications of the Parkinson's disease-related protein, DJ-1 Mol. Cell. Proteomics 2012, 11 (2) M111 010892
52. Kahle, P. J.; Waak, J.; Gasser, T. DJ-1 and prevention of oxidative stress in Parkinson's disease and other age-related disorders Free Radical Biol. Med. 2009, 47 (10) 1354-1361
53. Giebelstein, J.; Poschmann, G.; Hojlund, K.; Schechinger, W.; Dietrich, J. W.; Levin, K.; Beck-Nielsen, H.; Podwojski, K.; Stuhler, K.; Meyer, H. E.; Klein, H. H. The proteomic signature of insulin-resistant human skeletal muscle reveals increased glycolytic and decreased mitochondrial enzymes Diabetologia 2012, 55 (4) 1114-1127
54. Inberg, A.; Linial, M. Protection of pancreatic beta-cells from various stress conditions is mediated by DJ-1 J. Biol. Chem. 2010, 285 (33) 25686-25698
55. Waanders, L. F.; Chwalek, K.; Monetti, M.; Kumar, C.; Lammert, E.; Mann, M. Quantitative proteomic analysis of single pancreatic islets Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (45) 18902-18907
56. Kim, Y. C.; Kitaura, H.; Taira, T.; Iguchi-Ariga, S. M.; Ariga, H. Oxidation of DJ-1-dependent cell transformation through direct binding of DJ-1 to PTEN Int. J. Oncol. 2009, 35 (6) 1331-1341
57. Kato, I.; Maita, H.; Takahashi-Niki, K.; Saito, Y.; Noguchi, N.; Iguchi-Ariga, S. M.; Ariga, H. Oxidized DJ-1 inhibits p53 by sequestering p53 from promoters in a DNA-binding affinity-dependent manner Mol. Cell. Biol. 2013, 33 (2) 340-359
58. Guzman, J. N.; Sanchez-Padilla, J.; Wokosin, D.; Kondapalli, J.; Ilijic, E.; Schumacker, P. T.; Surmeier, D. J. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1 Nature 2010, 468 (7324) 696-700
59. Polymeropoulos, M. H.; Lavedan, C.; Leroy, E.; Ide, S. E.; Dehejia, A.; Dutra, A.; Pike, B.; Root, H.; Rubenstein, J.; Boyer, R.; Stenroos, E. S.; Chandrasekharappa, S.; Athanassiadou, A.; Papapetropoulos, T.; Johnson, W. G.; Lazzarini, A. M.; Duvoisin, R. C.; Di Iorio, G.; Golbe, L. I.; Nussbaum, R. L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 1997, 276 (5321) 2045-2047
60. Chavarria, C.; Souza, J. M. Oxidation and nitration of alpha-synuclein and their implications in neurodegenerative diseases Arch. Biochem. Biophys. 2013, 533 (1-2) 25-32
61. Park, J. Y.; Lansbury, P. T., Jr. Beta-synuclein inhibits formation of alpha-synuclein protofibrils: a possible therapeutic strategy against Parkinson's disease Biochemistry 2003, 42 (13) 3696-3700
62. Papa, S.; De Rasmo, D. Complex I deficiencies in neurological disorders Trends Mol. Med. 2013, 19 (1) 61-69
63. Ferrer, I.; Perez, E.; Dalfo, E.; Barrachina, M. Abnormal levels of prohibitin and ATP synthase in the substantia nigra and frontal cortex in Parkinson's disease Neurosci. Lett. 2007, 415 (3) 205-209
64. Hayashi, T.; Ishimori, C.; Takahashi-Niki, K.; Taira, T.; Kim, Y. C.; Maita, H.; Maita, C.; Ariga, H.; Iguchi-Ariga, S. M. DJ-1 binds to mitochondrial complex I and maintains its activity Biochem. Biophys. Res. Commun. 2009, 390 (3) 667-672