Differential proteome of the striatum from hemiparkinsonian rats displays vivid structural remodeling processes

Journal of Proteome Research

Volumn 9, Issue 9, 2010, Pages 4671-4687

  Lessner, Grit ^a   Schmitt, Oliver ^a   Haas, Stefan J P ^a   Mikkat, Stefan ^b   Kreutzer, Michael ^b   Wree, Andreas ^a   Glocker, Michael O ^b  

^a Gertrudenstrasse 9 ^*  (Germany)

^b Proteome Center Rostock   (Germany)

Author keywords

6 OHDA; differential proteome analysis; MALDI TOF MS; Parkinson's disease; striatum

Indexed keywords

ACTIN RELATED PROTEIN 3; ALPHA INTERNEXIN; ALPHA TUBULIN; BETA TUBULIN; CALBINDIN; CALMODULIN; CALRETICULIN; CARRIER PROTEIN; CHAPERONE; CLATHRIN LIGHT CHAIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN; CYTOSKELETON PROTEIN; FASCIN; GLYCEROPHOSPHOINOSITOL INOSITOLPHOSPHODIESTERASE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 90; OXIDOPAMINE; PEROXIREDOXIN 3; PROTEIN DISULFIDE ISOMERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; STRUCTURAL PROTEIN; SUPEROXIDE DISMUTASE; SYNAPSIN II; SYNEXIN; TRANSCRIPTION FACTOR; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE; VIMENTIN; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; CORPUS STRIATUM; DOWN REGULATION; ENERGY METABOLISM; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; NERVE FIBER; NERVE FIBER REGENERATION; NONHUMAN; NUCLEIC ACID METABOLISM; PARKINSONISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; STRUCTURAL PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; MALE; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEOSTRIATUM; NEURONAL PLASTICITY; OXIDOPAMINE; PARKINSON DISEASE; PARKINSON DISEASE, SECONDARY; PROTEOME; PROTEOMICS; RATS; RATS, WISTAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ANIMALIA; RATTUS;

EID: 77956298563     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100389u     Document Type: Article

References (127)

1. Forno, L. S. Neuropathology of Parkinson's disease J. Neuropathol. Exp. Neurol. 1996, 55 (3) 259-72
2. Lang, A. E.; Lozano, A. M. Parkinson's disease. Second of two parts N. Engl. J. Med. 1998, 339 (16) 1130-43
3. Lang, A. E.; Lozano, A. M. Parkinson's disease. First of two parts N. Engl. J. Med. 1998, 339 (15) 1044-53
4. Blandini, F.; Nappi, G.; Tassorelli, C.; Martignoni, E. Functional changes of the basal ganglia circuitry in Parkinson's disease Prog. Neurobiol. 2000, 62 (1) 63-88
5. Nakano, I.; Fujimoto, K. [Rating scale and functional prognosis of Parkinson's disease] Nippon Rinsho. 2000, 58 (10) 2132-8
6. Cookson, M. R. Parkin's substrates and the pathways leading to neuronal damage Neuromol. Med. 2003, 3 (1) 1-13
7. Eriksen, J. L.; Wszolek, Z.; Petrucelli, L. Molecular pathogenesis of Parkinson disease Arch. Neurol. 2005, 62 (3) 353-7
8. Jeon, B. S.; Jackson-Lewis, V.; Burke, R. E. 6-Hydroxydopamine lesion of the rat substantia nigra: time course and morphology of cell death Neurodegeneration 1995, 4 (2) 131-7
9. Graeber, M. B.; Grasbon-Frodl, E.; Abell-Aleff, P.; Kosel, S. Nigral neurons are likely to die of a mechanism other than classical apoptosis in Parkinson's disease Parkinsonism Relat. Disord. 1999, 5 (4) 187-92
10. Bove, J.; Prou, D.; Perier, C.; Przedborski, S. Toxin-induced models of Parkinson's disease NeuroRx 2005, 2 (3) 484-94
11. Miller, R. L.; James-Kracke, M.; Sun, G. Y.; Sun, A. Y. Oxidative and inflammatory pathways in Parkinson's disease Neurochem. Res. 2009, 34 (1) 55-65
12. Faull, R. L.; Laverty, R. Changes in dopamine levels in the corpus striatum following lesions in the substantia nigra Exp. Neurol. 1969, 23 (3) 332-40
13. Deumens, R.; Blokland, A.; Prickaerts, J. Modeling Parkinson's disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway Exp. Neurol. 2002, 175 (2) 303-17
14. Sauer, H.; Oertel, W. H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat Neuroscience 1994, 59 (2) 401-15
15. Chin, M. H.; Qian, W. J.; Wang, H.; Petyuk, V. A.; Bloom, J. S.; Sforza, D. M.; Lacan, G.; Liu, D.; Khan, A. H.; Cantor, R. M.; Bigelow, D. J.; Melega, W. P.; Camp, D. G., 2nd; Smith, R. D.; Smith, D. J. Mitochondrial dysfunction, oxidative stress, and apoptosis revealed by proteomic and transcriptomic analyses of the striata in two mouse models of Parkinson's disease J. Proteome Res. 2008, 7 (2) 666-77
16. Zhang, X.; Zhou, J. Y.; Chin, M. H.; Schepmoes, A. A.; Petyuk, V. A.; Weitz, K. K.; Petritis, B. O.; Monroe, M. E.; Camp, D. G.; Wood, S. A.; Melega, W. P.; Bigelow, D. J.; Smith, D. J.; Qian, W. J.; Smith, R. D. Region-specific protein abundance changes in the brain of MPTP-induced Parkinson's disease mouse model J. Proteome Res. 2010, 9 (3) 1496-509
17. Sousa, V. L.; Bellani, S.; Giannandrea, M.; Yousuf, M.; Valtorta, F.; Meldolesi, J.; Chieregatti, E. {alpha}-synuclein and its A30P mutant affect actin cytoskeletal structure and dynamics Mol. Biol. Cell 2009, 20 (16) 3725-39
18. Huynh, D. P.; Scoles, D. R.; Ho, T. H.; Del Bigio, M. R.; Pulst, S. M. Parkin is associated with actin filaments in neuronal and nonneural cells Ann. Neurol. 2000, 48 (5) 737-44
19. McFarland, M. A.; Ellis, C. E.; Markey, S. P.; Nussbaum, R. L. Proteomics analysis identifies phosphorylation-dependent alpha-synuclein protein interactions Mol. Cell. Proteomics 2008, 7 (11) 2123-37
20. Tischfield, M. A.; Baris, H. N.; Wu, C.; Rudolph, G.; Van Maldergem, L.; He, W.; Chan, W.-M.; Andrews, C.; Demer, J. L.; Robertson, R. L.; Mackey, D. A.; Ruddle, J. B.; Bird, T. D.; Gottlob, I.; Pieh, C.; Traboulsi, E. I.; Pomeroy, S. L.; Hunter, D. G.; Soul, J. S.; Newlin, A.; Sabol, L. J.; Doherty, E. J.; de Uzcátegui, C. E.; de Uzcátegui, N.; Collins, M. L. Z.; Sener, E. C.; Wabbels, B.; Hellebrand, H.; Meitinger, T.; de Berardinis, T.; Magli, A.; Schiavi, C.; Pastore-Trossello, M.; Koc, F.; Wong, A. M.; Levin, A. V.; Geraghty, M. T.; Descartes, M.; Flaherty, M.; Jamieson, R. V.; Møller, H. U.; Meuthen, I.; Callen, D. F.; Kerwin, J.; Lindsay, S.; Meindl, A.; Guptasend, M. L.; Pellman, D.; Engle, E. C. Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance Cell 2010, 140 (1) 74-87
21. Yates, D. M.; Manser, C.; De Vos, K. J.; Shaw, C. E.; McLoughlin, D. M.; Miller, C. C. Neurofilament subunit (NFL) head domain phosphorylation regulates axonal transport of neurofilaments Eur. J. Cell Biol. 2009, 88 (4) 193-202
22. Petzold, A.; Altintas, A.; Andreoni, L.; Bartos, A.; Berthele, A.; Blankenstein, M. A.; Buee, L.; Castellazzi, M.; Cepok, S.; Comabella, M.; Constantinescu, C. S.; Deisenhammer, F.; Deniz, G.; Erten, G.; Espino, M.; Fainardi, E.; Franciotta, D.; Freedman, M. S.; Giedraitis, V.; Gilhus, N. E.; Giovannoni, G.; Glabinski, A.; Grieb, P.; Hartung, H. P.; Hemmer, B.; Herukka, S. K.; Hintzen, R.; Ingelsson, M.; Jackson, S.; Jacobsen, S.; Jafari, N.; Jalosinski, M.; Jarius, S.; Kapaki, E.; Kieseier, B. C.; Koel-Simmelink, M. J.; Kornhuber, J.; Kuhle, J.; Kurzepa, J.; Lalive, P. H.; Lannfelt, L.; Lehmensiek, V.; Lewczuk, P.; Livrea, P.; Marnetto, F.; Martino, D.; Menge, T.; Norgren, N.; Papuc, E.; Paraskevas, G. P.; Pirttila, T.; Rajda, C.; Rejdak, K.; Ricny, J.; Ripova, D.; Rosengren, L.; Ruggieri, M.; Schraen, S.; Shaw, G.; Sindic, C.; Siva, A.; Stigbrand, T.; Stonebridge, I.; Topcular, B.; Trojano, M.; Tumani, H.; Twaalfhoven, H. A.; Vecsei, L.; Van Pesch, V.; Vanderstichele, H.; Vedeler, C.; Verbeek, M. M.; Villar, L. M.; Weissert, R.; Wildemann, B.; Yang, C.; Yao, K.; Teunissen, C. E. Neurofilament ELISA validation J. Immunol. Methods 2009
23. Butkevich, E.; Hulsmann, S.; Wenzel, D.; Shirao, T.; Duden, R.; Majoul, I. Drebrin is a novel connexin-43 binding partner that links gap junctions to the submembrane cytoskeleton Curr. Biol. 2004, 14 (8) 650-8
24. Betarbet, R.; Sherer, T. B.; Greenamyre, J. T. Animal models of Parkinson's disease Bioessays 2002, 24 (4) 308-18
25. Schober, A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP Cell Tissue Res. 2004, 318 (1) 215-24
26. Somayajulu-Nitu, M.; Sandhu, J. K.; Cohen, J.; Sikorska, M.; Sridhar, T. S.; Matei, A.; Borowy-Borowski, H.; Pandey, S. Paraquat induces oxidative stress, neuronal loss in substantia nigra region and parkinsonism in adult rats: neuroprotection and amelioration of symptoms by water-soluble formulation of coenzyme Q10 BMC Neurosci. 2009, 10, 88
27. Xiong, N.; Huang, J.; Zhang, Z.; Zhang, Z.; Xiong, J.; Liu, X.; Jia, M.; Wang, F.; Chen, C.; Cao, X.; Liang, Z.; Sun, S.; Lin, Z.; Wang, T. Stereotaxical infusion of rotenone: a reliable rodent model for Parkinson's disease PLoS One 2009, 4 (11 e7878
28. Schmidt, W. J.; Alam, M. Controversies on new animal models of Parkinson's disease pro and con: the rotenone model of Parkinson's disease (PD) J. Neural Transm. Suppl. 2006, 70) 273-6
29. Hawlitschka, A.; Haas, S. J.; Schmitt, O.; Weiss, D. G.; Wree, A. Effects of systemic PSI administration on catecholaminergic cells in the brain, adrenal medulla and carotid body in Wistar rats Brain Res. 2007, 1173, 137-44
30. Isacson, O.; Kordower, J. H. Future of cell and gene therapies for Parkinson's disease Ann. Neurol. 2008, 64 (2) S122-38
31. Cai, J.; Donaldson, A.; Yang, M.; German, M. S.; Enikolopov, G.; Iacovitti, L. The role of Lmx1a in the differentiation of human embryonic stem cells into midbrain dopamine neurons in culture and after transplantation into a Parkinson's disease model Stem Cells 2009, 27 (1) 220-9
32. Hess, D. C.; Borlongan, C. V. Stem cells and neurological diseases Cell Prolif. 2008, 41, 94-114
33. Ebert, A. D.; Beres, A. J.; Barber, A. E.; Svendsen, C. N. Human neural progenitor cells over-expressing IGF-1 protect dopamine neurons and restore function in a rat model of Parkinson's disease Exp. Neurol. 2008, 209 (1) 213-23
34. Redmond, D. E., Jr.; Bjugstad, K. B.; Teng, Y. D.; Ourednik, V.; Ourednik, J.; Wakeman, D. R.; Parsons, X. H.; Gonzalez, R.; Blanchard, B. C.; Kim, S. U.; Gu, Z.; Lipton, S. A.; Markakis, E. A.; Roth, R. H.; Elsworth, J. D.; Sladek, J. R., Jr.; Sidman, R. L.; Snyder, E. Y. Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (29) 12175-80
35. Hovakimyan, M.; Haas, S. J.; Schmitt, O.; Gerber, B.; Wree, A.; Andressen, C. Mesencephalic human neural progenitor cells transplanted into the neonatal hemiparkinsonian rat striatum differentiate into neurons and improve motor behaviour J. Anat. 2006, 209 (6) 721-32
36. Fillmore, H. L.; Holloway, K. L.; Gillies, G. T. Cell replacement efforts to repair neuronal injury: a potential paradigm for the treatment of Parkinson's disease NeuroRehabilitation 2005, 20 (3) 233-42
37. Goldman, S. Stem and progenitor cell-based therapy of the human central nervous system Nat. Biotechnol. 2005, 23 (7) 862-71
38. Sun, F.; Cavalli, V. Neuroproteomics: towards understanding neuronal regeneration and degeneration Mol. Cell. Proteomics 2009
39. Fountoulakis, M.; Tsangaris, G. T.; Maris, A.; Lubec, G. The rat brain hippocampus proteome J. Chromatogr., B: Analyt. Technol. Biomed. Life Sci. 2005, 819 (1) 115-29
40. Kanehisa, M.; Goto, S. KEGG: Kyoto encyclopedia of genes and genomes Nucleic Acids Res. 2000, 28 (1) 27-30
41. Kanehisa, M.; Goto, S.; Furumichi, M.; Tanabe, M.; Hirakawa, M. KEGG for representation and analysis of molecular networks involving diseases and drugs Nucleic Acids Res. (n/a), 38 (Database issue) D355-60
42. Kanehisa, M.; Goto, S.; Hattori, M.; Aoki-Kinoshita, K. F.; Itoh, M.; Kawashima, S.; Katayama, T.; Araki, M.; Hirakawa, M. From genomics to chemical genomics: new developments in KEGG Nucleic Acids Res. 2006, 34 (Database issue) D354-7
43. Paxinos, G.; Watson, C. The rat brain in stereotaxic coordinates, 6 th ed.; Elsevier: Amsterdam, 2007.
44. Hefti, F.; Melamed, E.; Sahakian, B. J.; Wurtman, R. J. Circling behavior in rats with partial, unilateral nigro-striatal lesions: effect of amphetamine, apomorphine, and DOPA Pharmacol., Biochem. Behav. 1980, 12 (2) 185-8
45. Hefti, F.; Melamed, E.; Wurtman, R. J. Partial lesions of the dopaminergic nigrostriatal system in rat brain: biochemical characterization Brain Res. 1980, 195 (1) 123-37
46. Heikkila, R. E.; Shapiro, B. S.; Duvoisin, R. C. The relationship between loss of dopamine nerve terminals, striatal [3H]spiroperidol binding and rotational behavior in unilaterally 6-hydroxydopamine-lesioned rats Brain Res. 1981, 211 (2) 285-92
47. Casas, M.; Guix, T.; Prat, G.; Ferre, S.; Cadafalch, J.; Jane, F. Conditioning of rotational behavior after the administration of a single dose of apomorphine in rats with unilateral denervation of the dopaminergic nigrostriatal pathway: relevance to drug addiction Pharmacol., Biochem. Behav. 1988, 31 (3) 605-9
48. Carman, L. S.; Gage, F. H.; Shults, C. W. Partial lesion of the substantia nigra: relation between extent of lesion and rotational behavior Brain Res. 1991, 553 (2) 275-83
49. Hudson, J. L.; van Horne, C. G.; Stromberg, I.; Brock, S.; Clayton, J.; Masserano, J.; Hoffer, B. J.; Gerhardt, G. A. Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats Brain Res. 1993, 626 (1-2) 167-74
50. Moore, A. E.; Cicchetti, F.; Hennen, J.; Isacson, O. Parkinsonian motor deficits are reflected by proportional A9/A10 dopamine neuron degeneration in the rat Exp. Neurol. 2001, 172 (2) 363-76
51. Ungerstedt, U.; Arbuthnott, G. W. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system Brain Res. 1970, 24 (3) 485-93
52. Zetterstrom, T.; Herrera-Marschitz, M.; Ungerstedt, U. Simultaneous measurement of dopamine release and rotational behaviour in 6-hydroxydopamine denervated rats using intracerebral dialysis Brain Res. 1986, 376 (1) 1-7
53. Schmidt, R. H.; Ingvar, M.; Lindvall, O.; Stenevi, U.; Bjorklund, A. Functional activity of substantia nigra grafts reinnervating the striatum: neurotransmitter metabolism and [14C]2-deoxy-D-glucose autoradiography J. Neurochem. 1982, 38 (3) 737-48
54. Carta, M.; Lindgren, H. S.; Lundblad, M.; Stancampiano, R.; Fadda, F.; Cenci, M. A. Role of striatal L-DOPA in the production of dyskinesia in 6-hydroxydopamine lesioned rats J. Neurochem. 2006, 96 (6) 1718-27
55. Lorenz, P.; Bantscheff, M.; Ibrahim, S. M.; Thiesen, H. J.; Glocker, M. O. Proteome analysis of diseased joints from mice suffering from collagen-induced arthritis Clin. Chem. Lab. Med. 2003, 41 (12) 1622-32
56. Just, T.; Gafumbegete, E.; Gramberg, J.; Prufer, I.; Mikkat, S.; Ringel, B.; Pau, H. W.; Glocker, M. O. Differential proteome analysis of tonsils from children with chronic tonsillitis or with hyperplasia reveals disease-associated protein expression differences Anal. Bioanal. Chem. 2006, 384 (5) 1134-44
57. Rower, C.; Vissers, J. P.; Koy, C.; Kipping, M.; Hecker, M.; Reimer, T.; Gerber, B.; Thiesen, H. J.; Glocker, M. O. Towards a proteome signature for invasive ductal breast carcinoma derived from label-free nanoscale LC-MS protein expression profiling of tumorous and glandular tissue Anal. Bioanal. Chem. 2009, 395 (8) 2443-56
58. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-54
59. Goörg, A. P., W; Friedrich, C.; Kuick, R.; Strahler, J. R.; Hanash, S. M. Temperature-dependent spot positional variability in two-dimensional polypeptide patterns Electrophoresis 1991, 12, 653-658
60. Goörg, A. W. W.; Dunn, M. J. Current two-dimensional electrophoresis technology for proteomics Proteomics 2004, 4, 3665-3685
61. Westermeier, R. Sensitive, quantitative, and fast modifications for Coomassie Blue staining of polyacrylamide gels Proteomics 2006, 6 (2) 61-4
62. Bantscheff, M.; Ringel, B.; Madi, A.; Schnabel, R.; Glocker, M. O.; Thiesen, H. J. Differential proteome analysis and mass spectrometric characterization of germ line development-related proteins of Caenorhabditis elegans Proteomics 2004, 4 (8) 2283-95
63. Li, Z.; Kreutzer, M.; Mikkat, S.; Mise, N.; Glocker, M. O.; Putzer, B. M. Proteomic analysis of the E2F1 response in p53-negative cancer cells: new aspects in the regulation of cell survival and death Proteomics 2006, 6 (21) 5735-45
64. Fulda, S.; Mikkat, S.; Huang, F.; Huckauf, J.; Marin, K.; Norling, B.; Hagemann, M. Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803 Proteomics 2006, 6 (9) 2733-45
65. Nordhoff, E.; Schuörenberg, M.; Thiele, G.; Luöbbert, C.; Kloeppe, l. K.-D.; Theiss, D.; Lehrach, H.; Gobom, J. Sample preparation protocols for MALDI-MS of peptides and oligonucleotides using prestructured sample supports Int. J. Mass Spectrom. 2003, 226, 163-180
66. Mikkat, S.; Koy, C.; Ulbrich, M.; Ringel, B.; Glocker, M. O. Mass spectrometric protein structure characterization reveals cause of migration differences of haptoglobin alpha chains in two-dimensional gel electrophoresis Proteomics 2004, 4 (12) 3921-32
67. Heitner, J. C.; Koy, C.; Kreutzer, M.; Gerber, B.; Reimer, T.; Glocker, M. O. Differentiation of HELLP patients from healthy pregnant women by proteome analysis - on the way towards a clinical marker set J. Chromatogr., B: Analyt. Technol. Biomed. Life Sci. 2006, 840 (1) 10-9
68. Aminin, D. L.; Koy, C.; Dmitrenok, P. S.; Muller-Hilke, B.; Koczan, D.; Arbogast, B.; Silchenko, A. A.; Kalinin, V. I.; Avilov, S. A.; Stonik, V. A.; Collin, P. D.; Thiesen, H. J.; Deinzer, M. L.; Glocker, M. O. Immunomodulatory effects of holothurian triterpene glycosides on mammalian splenocytes determined by mass spectrometric proteome analysis J. Proteomics 2009, 72 (5) 886-906
69. Petrak, J.; Ivanek, R.; Toman, O.; Cmejla, R.; Cmejlova, J.; Vyoral, D.; Zivny, J.; Vulpe, C. D. Deja vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins Proteomics 2008, 8 (9) 1744-9
70. Wang, P.; Bouwman, F. G.; Mariman, E. C. Generally detected proteins in comparative proteomics - a matter of cellular stress response Proteomics 2009, 9 (11) 2955-66
71. Gerfen, C. R. Basal ganglia. In The Rat Nervous System, 3 rd ed.; Paxinos, G., Ed.; Elsevier Academic Press: Amsterdam, 2004; pp 455 - 508.
72. Jin, J.; Hulette, C.; Wang, Y.; Zhang, T.; Pan, C.; Wadhwa, R.; Zhang, J. Proteomic identification of a stress protein, mortalin/mthsp70/GRP75: relevance to Parkinson disease Mol. Cell. Proteomics 2006, 5 (7) 1193-204
73. Jimenez, C. R.; Stam, F. J.; Li, K. W.; Gouwenberg, Y.; Hornshaw, M. P.; De Winter, F.; Verhaagen, J.; Smit, A. B. Proteomics of the injured rat sciatic nerve reveals protein expression dynamics during regeneration Mol. Cell. Proteomics 2005, 4 (2) 120-32
74. Fukuda, T.; Oyamada, H.; Isshiki, T.; Maeda, M.; Kusakabe, T.; Hozumi, A.; Yamaguchi, T.; Igarashi, T.; Hasegawa, H.; Seidoh, T.; Suzuki, T. Distribution and variable expression of secretory pathway protein reticulocalbin in normal human organs and non-neoplastic pathological conditions J. Histochem. Cytochem. 2007, 55 (4) 335-45
75. Mizrak, S. C.; Bogerd, J.; Lopez-Casas, P. P.; Parraga, M.; Del Mazo, J.; de Rooij, D. G. Expression of stress inducible protein 1 (Stip1) in the mouse testis Mol. Reprod. Dev. 2006, 73 (11) 1361-6
76. Li, K. W.; Hornshaw, M. P.; Van Der Schors, R. C.; Watson, R.; Tate, S.; Casetta, B.; Jimenez, C. R.; Gouwenberg, Y.; Gundelfinger, E. D.; Smalla, K. H.; Smit, A. B. Proteomics analysis of rat brain postsynaptic density. Implications of the diverse protein functional groups for the integration of synaptic physiology J. Biol. Chem. 2004, 279 (2) 987-1002
77. Ding, Q.; Vaynman, S.; Souda, P.; Whitelegge, J. P.; Gomez-Pinilla, F. Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis Eur. J. Neurosci. 2006, 24 (5) 1265-76
78. Shi, M.; Bradner, J.; Bammler, T. K.; Eaton, D. L.; Zhang, J.; Ye, Z.; Wilson, A. M.; Montine, T. J.; Pan, C.; Zhang, J. Identification of glutathione S-transferase pi as a protein involved in Parkinson disease progression Am. J. Pathol. 2009, 175 (1) 54-65
79. Ritter, B.; Blondeau, F.; Denisov, A. Y.; Gehring, K.; McPherson, P. S. Molecular mechanisms in clathrin-mediated membrane budding revealed through subcellular proteomics Biochem. Soc. Trans. 2004, 32 (Pt 5) 769-73
80. Murshid, A.; Srivastava, A.; Kumar, R.; Presley, J. F. Characterization of the localization and function of NECAP 1 in neurons J. Neurochem. 2006, 98 (6) 1746-62
81. Conner, S. D.; Schmid, S. L. Regulated portals of entry into the cell Nature 2003, 422 (6927) 37-44
82. Hay, J. C.; Martin, T. F. Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca(2+)-activated secretion Nature 1993, 366 (6455) 572-5
83. Liscovitch, M.; Cantley, L. C. Signal transduction and membrane traffic: the PITP/phosphoinositide connection Cell 1995, 81 (5) 659-62
84. Smith, T. J.; Peterson, P. E.; Schmidt, T.; Fang, J.; Stanley, C. A. Structures of bovine glutamate dehydrogenase complexes elucidate the mechanism of purine regulation J. Mol. Biol. 2001, 307 (2) 707-20
85. Haberle, J.; Gorg, B.; Rutsch, F.; Schmidt, E.; Toutain, A.; Benoist, J. F.; Gelot, A.; Suc, A. L.; Hohne, W.; Schliess, F.; Haussinger, D.; Koch, H. G. Congenital glutamine deficiency with glutamine synthetase mutations N. Engl. J. Med. 2005, 353 (18) 1926-33
86. Fernandez, E.; Koek, W.; Ran, Q.; Gerhardt, G. A.; France, C. P.; Strong, R. Monoamine metabolism and behavioral responses to ethanol in mitochondrial aldehyde dehydrogenase knockout mice Alcohol.: Clin. Exp. Res. 2006, 30 (10) 1650-8
87. Gravel, M.; Peterson, J.; Yong, V. W.; Kottis, V.; Trapp, B.; Braun, P. E. Overexpression of 2′,3′-cyclic nucleotide 3′- phosphodiesterase in transgenic mice alters oligodendrocyte development and produces aberrant myelination Mol. Cell. Neurosci. 1996, 7 (6) 453-66
88. Riefler, G. M.; Balasingam, G.; Lucas, K. G.; Wang, S.; Hsu, S. C.; Firestein, B. L. Exocyst complex subunit sec8 binds to postsynaptic density protein-95 (PSD-95): a novel interaction regulated by cypin (cytosolic PSD-95 interactor) Biochem. J. 2003, 373 (Pt 1) 49-55
89. Firestein, B. L.; Firestein, B. L.; Brenman, J. E.; Aoki, C.; Sanchez-Perez, A. M.; El-Husseini, A. E.; Bredt, D. S. Cypin: a cytosolic regulator of PSD-95 postsynaptic targeting Neuron 1999, 24 (3) 659-72
90. Doran, J. F.; Jackson, P.; Kynoch, P. A.; Thompson, R. J. Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis J. Neurochem. 1983, 40 (6) 1542-7
91. Ardley, H. C.; Scott, G. B.; Rose, S. A.; Tan, N. G.; Robinson, P. A. UCH-L1 aggresome formation in response to proteasome impairment indicates a role in inclusion formation in Parkinson's disease J. Neurochem. 2004, 90 (2) 379-91
92. Lowe, J.; McDermott, H.; Landon, M.; Mayer, R. J.; Wilkinson, K. D. Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases J. Pathol. 1990, 161 (2) 153-60
93. Eom, C. Y.; Heo, W. D.; Craske, M. L.; Meyer, T.; Lehman, I. R. The neural F-box protein NFB42 mediates the nuclear export of the herpes simplex virus type 1 replication initiator protein (UL9 protein) after viral infection Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (12) 4036-40
94. Bai, C.; Sen, P.; Hofmann, K.; Ma, L.; Goebl, M.; Harper, J. W.; Elledge, S. J. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box Cell 1996, 86 (2) 263-74
95. Erhardt, J. A.; Hynicka, W.; DiBenedetto, A.; Shen, N.; Stone, N.; Paulson, H.; Pittman, R. N. A novel F box protein, NFB42, is highly enriched in neurons and induces growth arrest J. Biol. Chem. 1998, 273 (52) 35222-7
96. Dagda, R. K.; Zhu, J.; Kulich, S. M.; Chu, C. T. Mitochondrially localized ERK2 regulates mitophagy and autophagic cell stress: implications for Parkinson's disease Autophagy 2008, 4 (6) 770-82
97. Schmitt, O.; Eggers, R.; Haug, H. Topologic distribution of different types of neurons in the human putamen Anal. Quant. Cytol. Histol. 2000, 22 (2) 155-67
98. Zhang, J.; Goodlett, D. R. Proteomic approach to studying Parkinson's disease Mol. Neurobiol. 2004, 29 (3) 271-88
99. Fountoulakis, M.; Schuller, E.; Hardmeier, R.; Berndt, P.; Lubec, G. Rat brain proteins: two-dimensional protein database and variations in the expression level Electrophoresis 1999, 20 (18) 3572-9
100. Larbi, N. B.; Jefferies, C. 2D-DIGE: comparative proteomics of cellular signalling pathways Methods Mol. Biol. 2009, 517, 105-32
101. Pietrogrande, M. C.; Marchetti, N.; Dondi, F.; Righetti, P. G. Decoding 2D-PAGE complex maps: relevance to proteomics J. Chromatogr., B: Analyt. Technol. Biomed. Life Sci. 2006, 833 (1) 51-62
102. Zhang, X.; Fang, A.; Riley, C. P.; Wang, M.; Regnier, F. E.; Buck, C. Multi-dimensional liquid chromatography in proteomics - a review Anal. Chim. Acta (n/a), 664 (2) 101-13
103. Basso, M.; Giraudo, S.; Corpillo, D.; Bergamasco, B.; Lopiano, L.; Fasano, M. Proteome analysis of human substantia nigra in Parkinson's disease Proteomics 2004, 4 (12) 3943-52
104. Miyazaki, I.; Asanuma, M. Approaches to prevent dopamine quinone-induced neurotoxicity Neurochem. Res. 2009, 34 (4) 698-706
105. Van Laar, V. S.; Dukes, A. A.; Cascio, M.; Hastings, T. G. Proteomic analysis of rat brain mitochondria following exposure to dopamine quinone: implications for Parkinson disease Neurobiol. Dis. 2008, 29 (3) 477-89
106. Kaariainen, T. M.; Piltonen, M.; Ossola, B.; Kekki, H.; Lehtonen, S.; Nenonen, T.; Lecklin, A.; Raasmaja, A.; Mannisto, P. T. Lack of robust protective effect of quercetin in two types of 6-hydroxydopamine-induced parkinsonian models in rats and dopaminergic cell cultures Brain Res. 2008, 1203, 149-59
107. Jin, J.; Meredith, G. E.; Chen, L.; Zhou, Y.; Xu, J.; Shie, F. S.; Lockhart, P.; Zhang, J. Quantitative proteomic analysis of mitochondrial proteins: relevance to Lewy body formation and Parkinson's disease Brain Res. Mol. Brain Res. 2005, 134 (1) 119-38
108. Xun, Z.; Sowell, R. A.; Kaufman, T. C.; Clemmer, D. E. Protein expression in a Drosophila model of Parkinson's disease J. Proteome Res. 2007, 6 (1) 348-57
109. Ichibangase, T.; Saimaru, H.; Takamura, N.; Kuwahara, T.; Koyama, A.; Iwatsubo, T.; Imai, K. Proteomics of Caenorhabditis elegans over-expressing human alpha-synuclein analyzed by fluorogenic derivatization-liquid chromatography/tandem mass spectrometry: identification of actin and several ribosomal proteins as negative markers at early Parkinson's disease stages Biomed. Chromatogr. 2008, 22 (3) 232-4
110. Rodriguez, M.; Abdala, P.; Obeso, J. A. Excitatory responses in the 'direct' striatonigral pathway: effect of nigrostriatal lesion Mov. Disord. 2000, 15 (5) 795-803
111. Smith, A. D.; Amalric, M.; Koob, G. F.; Zigmond, M. J. Effect of bilateral 6-hydroxydopamine lesions of the medial forebrain bundle on reaction time Neuropsychopharmacology 2002, 26 (6) 756-64
112. Gonzalez-Hernandez, T.; Barroso-Chinea, P.; Rodriguez, M. Response of the GABAergic and dopaminergic mesostriatal projections to the lesion of the contralateral dopaminergic mesostriatal pathway in the rat Mov. Disord. 2004, 19 (9) 1029-1042
113. Soderstrom, K. E.; O'Malley, J. A.; Levine, N. D.; Sortwell, C. E.; Collier, T. J.; Steece-Collier, K., Impact of dendritic spine preservation in medium spiny neurons on dopamine graft efficacy and the expression of dyskinesias in parkinsonian rats. Eur. J. Neurosci.
114. Esposito, A.; Dohm, C. P.; Kermer, P.; Bahr, M.; Wouters, F. S. alpha-Synuclein and its disease-related mutants interact differentially with the microtubule protein tau and associate with the actin cytoskeleton Neurobiol. Dis. 2007, 26 (3) 521-31
115. Leverenz, J. B.; Umar, I.; Wang, Q.; Montine, T. J.; McMillan, P. J.; Tsuang, D. W.; Jin, J.; Pan, C.; Shin, J.; Zhu, D.; Zhang, J. Proteomic identification of novel proteins in cortical lewy bodies Brain Pathol. 2007, 17 (2) 139-45
116. Hong, Z.; Zhang, Q. Y.; Liu, J.; Wang, Z. Q.; Zhang, Y.; Xiao, Q.; Lu, J.; Zhou, H. Y.; Chen, S. D. Phosphoproteome study reveals Hsp27 as a novel signaling molecule involved in GDNF-induced neurite outgrowth J. Proteome Res. 2009, 8 (6) 2768-87
117. Zhou, Y.; Wang, Y.; Kovacs, M.; Jin, J.; Zhang, J. Microglial activation induced by neurodegeneration: a proteomic analysis Mol. Cell. Proteomics 2005, 4 (10) 1471-9
118. Periquet, M.; Corti, O.; Jacquier, S.; Brice, A. Proteomic analysis of parkin knockout mice: alterations in energy metabolism, protein handling and synaptic function J. Neurochem. 2005, 95 (5) 1259-76
119. Wooten, G. F.; Collins, R. C. Metabolic effects of unilateral lesion of the substantia nigra J. Neurosci. 1981, 1 (3) 285-91
120. Zhang, W.; Wang, T.; Pei, Z.; Miller, D. S.; Wu, X.; Block, M. L.; Wilson, B.; Zhang, W.; Zhou, Y.; Hong, J. S.; Zhang, J. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease Faseb J. 2005, 19 (6) 533-42
121. Reynolds, A. D.; Glanzer, J. G.; Kadiu, I.; Ricardo-Dukelow, M.; Chaudhuri, A.; Ciborowski, P.; Cerny, R.; Gelman, B.; Thomas, M. P.; Mosley, R. L.; Gendelman, H. E. Nitrated alpha-synuclein-activated microglial profiling for Parkinson's disease J. Neurochem. 2008, 104 (6) 1504-25
122. Beal, M. F. Mitochondria, oxidative damage, and inflammation in Parkinson's disease Ann. N.Y. Acad. Sci. 2003, 991, 120-31
123. Hald, A.; Lotharius, J. Oxidative stress and inflammation in Parkinson's disease: is there a causal link Exp. Neurol. 2005, 193 (2) 279-90
124. Rogers, J.; Mastroeni, D.; Leonard, B.; Joyce, J.; Grover, A. Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder Int. Rev. Neurobiol. 2007, 82, 235-46
125. Hald, A.; Van Beek, J.; Lotharius, J. Inflammation in Parkinson's disease: causative or epiphenomenal Subcell Biochem. 2007, 42, 249-79
126. Rojo, A. I.; Innamorato, N. G.; Martin-Moreno, A. M.; De Ceballos, M. L.; Yamamoto, M.; Cuadrado, A. Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease Glia 2009
127. Ghorayeb, I.; Puschban, Z.; Fernagut, P. O.; Scherfler, C.; Rouland, R.; Wenning, G. K.; Tison, F. Simultaneous intrastriatal 6-hydroxydopamine and quinolinic acid injection: a model of early-stage striatonigral degeneration Exp. Neurol. 2001, 167 (1) 133-47