Gene expression profiling in progressively MPTP-lesioned macaques reveals molecular pathways associated with sporadic Parkinson's disease

Brain Research

Volumn 1346, Issue , 2010, Pages 26-42

  Ohnuki, Tatsuya ^a,b   Nakamura, Atsushi ^a   Okuyama, Shigeru ^a   Nakamura, Shoji ^b  

^a TAISHO PHARMACEUTICAL CO LTD   (Japan)

^b YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Gene expression; Microarray; MPTP; Nonhuman primate; Parkinson's disease; Pathway analysis; Promoter analysis; Striatum; Substantia nigra

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 4 AMINOBUTYRIC ACID B RECEPTOR; ADENOSINE A2A RECEPTOR; ALPHA SYNUCLEIN; ANDROGEN RECEPTOR; AROMATIC LEVO AMINO ACID DECARBOXYLASE; BETA CATENIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CXCL13 CHEMOKINE; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; EPHRIN RECEPTOR A4; FIBROBLAST GROWTH FACTOR 1; HISTIDINE DECARBOXYLASE; INTERLEUKIN 11; KINESIN 2; KININOGEN; MICROTUBULE ASSOCIATED PROTEIN 5; N ETHYLMALEIMIDE SENSITIVE FACTOR; PROENKEPHALIN; PROTEASOME; PROTEIN BCL 10; SYNAPTOJANIN; TAU PROTEIN; TRANSCRIPTION FACTOR 7 LIKE 2; TUBULIN; TYROSINE 3 MONOOXYGENASE; UBIQUITIN; UNINDEXED DRUG; X LINKED INHIBITOR OF APOPTOSIS; COMPLEMENTARY DNA; WNT PROTEIN;

ANALYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEAVY CHAIN; HUMAN; MACACA; MALE; MICROARRAY ANALYSIS; MONKEY; NERVE DEGENERATION; NEUROFILAMENT; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; ANIMAL; ANIMAL LAMENESS; APOPTOSIS; BIOSYNTHESIS; CYTOSKELETON; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTOXICATION; LOCOMOTION; METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROMOTER REGION; PSYCHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; APOPTOSIS; CYTOSKELETON; DISEASE PROGRESSION; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LAMENESS, ANIMAL; LOCOMOTION; MACACA MULATTA; MALE; MICROARRAY ANALYSIS; MPTP POISONING; OXIDATIVE STRESS; PARKINSON DISEASE; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SYNAPSES; TYROSINE 3-MONOOXYGENASE; WNT PROTEINS;

MACACA; PRIMATES;

EID: 77955514552     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.05.066     Document Type: Article

References (80)

1. S. Alberi, B. Boda, P. Steiner, I. Nikonenko, H. Hirling, and D. Muller The endosomal protein NEEP21 regulates AMPA receptor-mediated synaptic transmission and plasticity in the hippocampus Mol. Cell. Neurosci. 29 2005 313 319
2. D.W. Anderson, K.A. Bradbury, and J.S. Schneider Neuroprotection in Parkinson models varies with toxin administration protocol Eur. J. Neurosci. 24 2006 3174 3182
3. F. Bassilana, N. MacE, Q. Li, J.M. Stutzmann, C.E. Gross, L. Pradier, J. Benavides, J. MeÍnager, and E. Bezard Unraveling substantia nigra sequential gene expression in a progressive MPTP-lesioned macaque model of Parkinson's disease Neurobiol. Dis. 20 2005 93 103
4. E. Bezard, S. Dovero, C. Prunier, P. Ravenscroft, S. Chalon, D. Guilloteau, A.R. Crossman, B. Bioulac, J.M. Brotchie, and C.E. Gross Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine- lesioned macaque model of Parkinson's disease J. Neurosci. 21 2001 6853 6861
5. H. Braak, C.M. Müller, U. Rüb, H. Ackermann, H. Bratzke, R.A. de Vos, and K. del Tredici Pathology associated with sporadic Parkinson's disease-where does it end? J. Neural. Transm. Suppl. 2006 89 97
6. I. Cantuti-Castelvetri, C. Keller-McGandy, B. Bouzou, G. Asteris, T.W. Clark, M.P. Frosch, and D.G. Standaert Effects of gender on nigral gene expression and parkinson disease Neurobiol. Dis. 26 2007 606 614
7. M.H. Chin, W.J. Qian, H. Wang, V.A. Petyuk, J.S. Bloom, D.M. Sforza, G. Lacan, D. Liu, A.H. Khan, R.M. Cantor, D.J. Bigelow, W.P. Melega, D.G. Camp II, R.D. Smith, and D.J. Smith 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. 7 2008 666 677
8. G. Christofori Changing neighbours, changing behaviour: cell adhesion molecule-mediated signalling during tumour progression EMBO. J. 22 2003 2318 2323
9. M. Clamp, D. Andrews, D. Barker, P. Bevan, G. Cameron, Y. Chen, L. Clark, T. Cox, J. Cuff, V. Curwen, T. Down, R. Durbin, E. Eyras, J. Gilbert, M. Hammond, T. Hubbard, A. Kasprzyk, D. Keefe, H. Lehvaslaiho, V. Iyer, C. Melsopp, E. Mongin, R. Pettett, S. Potter, A. Rust, E. Schmidt, S. Searle, G. Slater, J. Smith, W. Spooner, A. Stabenau, J. Stalker, E. Stupka, A. Ureta-Vidal, I. Vastrik, and E. Birney Ensembl 2002: accommodating comparative genomics Nucleic Acids Res. 31 2003 38 42
10. H. Clevers Wnt/β-catenin signaling in development and disease Cell 127 2006 469 480
11. E.K. de Jong, A.H. de Haas, N. Brouwer, H.R. van Weering, M. Hensens, I. Bechmann, P. Pratley, E. Wesseling, H.W. Boddeke, and K. Biber Expression of CXCL4 in microglia in vitro and in vivo and its possible signaling through CXCR3 J. Neurochem. 105 2008 1726 1736
12. D.C. Duke, L.B. Moran, M.E. Kalaitzakis, M. Deprez, D.T. Dexter, R.K. Pearce, and M.B. Graeber Transcriptome analysis reveals link between proteasomal and mitochondrial pathways in Parkinson's disease Neurogenetics 7 2006 139 148
13. O. Eberhardt, R.V. Coelln, S. Kugler, J. Lindenau, S. Rathke-Hartlieb, E. Gerhardt, S. Haid, S. Isenmann, C. Gravel, A. Srinivasan, M. Bahr, M. Weller, J. Dichgans, and J.B. Schulz Protection by synergistic effects of adenovirus-mediated X-chromosome-linked inhibitor of apoptosis and glial cell line-derived neurotrophic factor gene transfer in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine model of Parkinson's disease J. Neurosci. 20 2000 9126 9134
14. S. Ekins, A. Bugrim, L. Brovold, E. Kirillov, Y. Nikolsky, E. Rakhmatulin, S. Sorokina, A. Ryabov, T. Serebryiskaya, A. Melnikov, J. Metz, and T. Nikolskaya Algorithms for network analysis in systems-ADME/Tox using the MetaCore and MetaDrug platforms Xenobiotica 36 2006 877 901
15. J.R. Evans, and R.A. Barker Neurotrophic factors as a therapeutic target for Parkinson's disease Expert. Opin. Ther. Targets 12 2008 437 447
16. N. Gogolla, I. Galimberti, Y. Deguchi, and P. Caroni Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus Neuron 62 2009 510 525
17. R. Grondin, A.H. Tahar, V.D. Doan, P. Ladure, and P.J. Bédard Noradrenoceptor antagonism with idazoxan improves l-dopa-induced dyskinesias in MPTP monkeys Naunyn Schmiedebergs Arch. Pharmacol. 361 2000 181 186
18. E. Grunblatt, S. Mandel, G. Maor, and M.B. Youdim Gene expression analysis in N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mice model of Parkinson's disease using cDNA microarray: effect of R-apomorphine J. Neurochem. 78 2001 1 12
19. E. Grunblatt, S. Mandel, J. Jacob-Hirsch, S. Zeligson, N. Amariglo, G. Rechavi, J. Li, R. Ravid, W. Roggendorf, P. Riederer, and M.B. Youdim Gene expression profiling of parkinsonian substantia nigra pars compacta; alterations in ubiquitin-proteasome, heat shock protein, iron and oxidative stress regulated proteins, cell adhesion/cellular matrix and vesicle trafficking genes J. Neural. Transm. 111 2004 1543 1573
20. K. Gwinn-Hardy Genetics of parkinsonism Mov. Disord. 17 2002 645 656
21. A. Hartmann, S. Hunot, P.P. Michel, M.-P. Muriel, S. Vyas, B.A. Faucheux, A. Mouatt-Prigent, E. Turmel, A. Srinivasan, M. Ruberg, G.I. Evan, Y. Agid, and E.C. Hirsch Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease Proc. Natl Acad. Sci. 97 2000 2875 2880
22. M.A. Hauser, Y.J. Li, H. Xu, M.A. Noureddine, Y.S. Shao, S.R. Gullans, C.R. Scherzer, R.V. Jensen, A.C. McLaurin, J.R. Gibson, B.L. Scott, R.M. Jewett, J.E. Stenger, D.E. Schmechel, C.M. Hulette, and J.M. Vance Expression profiling of substantia nigra in Parkinson disease, progressive supranuclear palsy, and frontotemporal dementia with parkinsonism Arch. Neurol. 62 2005 917 921
23. H.M. Heerssen, M.F. Pazyra, and R.A. Segal Dynein motors transport activated Trks to promote survival of target-dependent neurons Nat. Neurosci. 7 2004 596 604
24. M.T. Herrero, I. Perez-Otano, C. Oset, A. Kastner, E.C. Hirsch, Y. Agid, M.R. Luquin, J.A. Obeso, and J. Del Rio GM-1 ganglioside promotes the recovery of surviving midbrain dopaminergic neurons in MPTP-treated monkeys Neuroscience 56 1993 965 972
25. S.J. Ho Sui, J.R. Mortimer, D.J. Arenillas, J. Brumm, C.J. Walsh, B.P. Kennedy, and W.W. Wasserman oPOSSUM: identification of over-represented transcription factor binding sites in co-expressed genes Nucleic Acids Res. 33 2005 3154 3164
26. J. Iczkiewicz, M.J. Jackson, L.A. Smith, S. Rose, and P. Jenner Osteopontin expression in substantia nigra in MPTP-treated primates and in Parkinson's disease Brain Res. 1118 2006 239 250
27. C. Imbert, E. Bezard, S. Guitraud, T. Boraud, and C.E. Gross Comparison between eight clinical rating scales used for the assessment of MPTP-induced Parkinsonism in the macaque monkey J. Neurosci. Methods 96 2000 71 76
28. C.A. Ingham, S.H. Hood, B. van Maldegem, A. Weenink, and G.W. Arbuthnott Morphological changes in the rat neostriatum after unilateral 6-hydroxydopamine injections into the nigrostriatal pathway Exp. Brain Res. 93 1993 17 27
29. C. Jaeger, A. Gonzalo Ruiz, and R. Llinas Organotypic slice cultures of dopaminergic neurons of substantia nigra Brain Res. Bull. 22 1989 981 991
30. V. Jackson-Lewis, M. Jakowec, R.E. Burke, and S. Przedborski Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine Neurodegeneration 4 1995 257 269
31. M.D. Kane, T.A. Jatkoe, C.R. Stumpf, J. Lu, J.D. Thomas, and S.J. Madore Assessment of the sensitivity and specificity of oligonucleotide (50mer) microarrays Nucleic Acids Res. 28 2000 4552 4557
32. M. Karin, and Y. Ben-Neriah Phosphorylation meets ubiquitination: the control of NF-κB activity Annu. Rev. Immunol. 18 2000 621 663
33. B. Kasper, S. Winoto-Morbach, J. Mittelstadt, E. Brandt, S. Schutze, and F. Petersen CXCL4-induced monocyte survival, cytokine expression, and oxygen radical formation is regulated by sphingosine kinase 1 Eur. J. Immunol. 40 2010 1162 1173
34. W. Le, O.M. Conneely, Y. He, J. Jankovic, and S.H. Appel Reduced Nurr1 expression increases the vulnerability of mesencephalic dopamine neurons to MPTP-induced injury J. Neurochem. 73 1999 2218 2221
35. C. Leranth, O. Petnehazy, and N.J. MacLusky Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats J. Neurosci. 23 2003 1588 1592
36. T.G. Lesnick, S. Papapetropoulos, D.C. Mash, J. Ffrench-Mullen, L. Shehadeh, M. de Andrade, J.R. Henley, W.A. Rocca, J.E. Ahlskog, and D.M. Maraganore A genomic pathway approach to a complex disease: axon guidance and Parkinson disease PLoS Genet. 3 2007 e98
37. L.A. Ligon, S. Karki, M. Tokito, and E.L. Holzbaur Dynein binds to β-catenin and may tether microtubules at adherens junctions Nat. Cell. Biol. 3 2001 913 917
38. D.A. Loeffler, D.M. Camp, and S.B. Conant Complement activation in the Parkinson's disease substantia nigra: an immunocytochemical study J. Neuroinflammation 3 2006 29
39. S. Mandel, E. Grunblatt, and M. Youdim cDNA microarray to study gene expression of dopaminergic neurodegeneration and neuroprotection in MPTP and 6-hydroxydopamine models: implications for idiopathic Parkinson's disease J. Neural. Transm. Suppl. 2000 117 124
40. S. Mandel, E. Grunblatt, P. Riederer, N. Amariglio, J. Jacob-Hirsch, G. Rechavi, and M.B. Youdim Gene expression profiling of sporadic Parkinson's disease substantia nigra pars compacta reveals impairment of ubiquitin-proteasome subunits, SKP1A, aldehyde dehydrogenase, and chaperone HSC-70 Ann. N. Y. Acad. Sci. 1053 2005 356 375
41. S.A. Mandel, T. Fishman-Jacob, and M.B. Youdim Modeling sporadic Parkinson's disease by silencing the ubiquitin E3 ligase component, SKP1A Parkinsonism. Relat. Disord. 15 Suppl 3 2009 S148 S151
42. M.P. Mattson, F.M. LaFerla, S.L. Chan, M.A. Leissring, P.N. Shepel, and J.D. Geiger Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders Trends. Neurosci. 23 2000 222 229
43. K.S. McNaught, and C.W. Olanow Protein aggregation in the pathogenesis of familial and sporadic Parkinson's disease Neurobiol. Aging 27 2006 530 545
44. R.M. Miller, L.M. Callahan, C. Casaceli, L. Chen, G.L. Kiser, B. Chui, T.M. Kaysser-Kranich, T.J. Sendera, C. Palaniappan, and H.J. Federoff Dysregulation of gene expression in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned mouse substantia nigra J. Neurosci. 24 2004 7445 7454
45. R.M. Miller, L.L. Chen, G.L. Kiser, T.L. Giesler, T.M. Kaysser-Kranich, C. Palaniappan, and H.J. Federoff Temporal evolution of mouse striatal gene expression following MPTP injury Neurobiol. Aging 26 2005 765 775
46. R.M. Miller, G.L. Kiser, T.M. Kaysser-Kranich, R.J. Lockner, C. Palaniappan, and H.J. Federoff Robust dysregulation of gene expression in substantia nigra and striatum in Parkinson's disease Neurobiol. Dis. 21 2006 305 313
47. E. Mitchell, D. Thomas, and R. Burnet Testosterone improves motor function in Parkinson's disease J. Clin. Neurosci. 13 2006 133 136
48. L.B. Moran, and M.B. Graeber Towards a pathway definition of Parkinson's disease: a complex disorder with links to cancer, diabetes and inflammation Neurogenetics 9 2008 1 13
49. L.B. Moran, D.C. Duke, M. Deprez, D.T. Dexter, R.K. Pearce, and M.B. Graeber Whole genome expression profiling of the medial and lateral substantia nigra in Parkinson's disease Neurogenetics 7 2006 1 11
50. L.B. Moran, E. Croisier, D.C. Duke, M.E. Kalaitzakis, F. Roncaroli, M. Deprez, D.T. Dexter, R.K. Pearce, and M.B. Graeber Analysis of alpha-synuclein, dopamine and parkin pathways in neuropathologically confirmed parkinsonian nigra Acta Neuropathol. 113 2007 253 263
51. T. Nagatsu, M. Mogi, H. Ichinose, and A. Togari Changes in cytokines and neurotrophins in Parkinson's disease J. Neural.Transm. Suppl. 2000 277 290
52. M.S. Okun, W.M. McDonald, and M.R. DeLong Refractory nonmotor symptoms in male patients with Parkinson disease due to testosterone deficiency: a common unrecognized comorbidity Arch. Neurol. 59 2002 807 811
53. M.J. O'Neill, T.K. Murray, M.P. Clay, T. Lindstrom, C.R. Yang, and E.S. Nisenbaum LY503430: pharmacology, pharmacokinetics, and effects in rodent models of Parkinson's disease CNS Drug. Rev. 11 2005 77 96
54. R. Pattarini, Y. Rong, C. Qu, and J.I. Morgan Distinct mechanisms of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyrimidine resistance revealed by transcriptome mapping in mouse striatum Neuroscience 155 2008 1174 1194
55. G. Ramesh, J.T. Borda, J. Dufour, D. Kaushal, R. Ramamoorthy, A.A. Lackner, and M.T. Philipp Interaction of the Lyme disease spirochete Borrelia burgdorferi with brain parenchyma elicits inflammatory mediators from glial cells as well as glial and neuronal apoptosis Am. J. Pathol. 173 2008 1415 1427
56. M.J. Reed, J.D. Hutton, P.M. Baxendale, V.H. James, H.S. Jacobs, and R.P. Fisher The conversion of androstenedione to oestrone and production of oestrone in women with endometrial cancer J. Steroid Biochem. 11 1979 905 911
57. D.M. Rocke, and B. Durbin A model for measurement error for gene expression arrays J. Comput. Biol. 8 2001 557 569
58. P. Samadi, P.J. Bédard, and C. Rouillard Opioids and motor complications in Parkinson's disease Trends Pharmacol. Sci. 27 2006 512 517
59. A. Sandelin, W. Alkema, P. Engström, W.W. Wasserman, and B. Lenhard JASPAR: an open-access database for eukaryotic transcription factor binding profiles Nucleic Acids Res. 32 2004 D91 D94
60. J.J. Savage, R.D. Mullen, K.W. Sloop, S.C. Colvin, S.A. Camper, C.L. Franklin, and S.J. Rhodes Transgenic mice expressing LHX3 transcription factor isoforms in the pituitary: effects on the gonadotrope axis and sex-specific reproductive disease J. Cell. Physiol. 212 2007 105 117
61. C.J. Schoenherr, A.J. Paquette, and D.J. Anderson Identification of potential target genes for the neuron-restrictive silencer factor Proc. Natl. Acad. Sci. U. S. A. 93 1996 9881 9886
62. A. Shimada, C.A. Morrison, and M.E. Mason TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells J. Neurosci. 18 1998 8559 8570
63. F. Simunovic, M. Yi, Y. Wang, L. Macey, L.T. Brown, A.M. Krichevsky, S.L. Andersen, R.M. Stephens, F.M. Benes, and K.C. Sonntag Gene expression profiling of substantia nigra dopamine neurons: further insights into Parkinson's disease pathology Brain 132 2009 1795 1809
64. F. Simunovic, M. Yi, Y. Wang, R. Stephens, and K.C. Sonntag Evidence for gender-specific transcriptional profiles of nigral dopamine neurons in Parkinson disease PLoS One 5 2010 e8856
65. P.K. Sonsalla, and R.E. Heikkila The influence of dose and dosing interval in MPTP-induced dopaminergic neurotoxicity in mice Eur. J. Pharmacol. 129 1986 339 345
66. G.T. Sutherland, N.A. Matigian, A.M. Chalk, M.J. Anderson, P.A. Silburn, A. Mackay-Sim, C.A. Wells, and G.D. Mellick A cross-study transcriptional analysis of Parkinson's disease PLoS One 4 2009 e4955
67. Y. Suzuki, Y. Nakabayashi, and R. Takahashi Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death Proc. Natl. Acad. Sci. U.S.A. 98 2001 8662 8667
68. R.M. Villalba, H. Lee, and Y. Smith Dopaminergic denervation and spine loss in the striatum of MPTP-treated monkeys Exp. Neurol. 215 2009 220 227
69. I.R. Vogt, A.J. Lees, B.O. Evert, T. Klockgether, M. Bonin, and U. Wullner Transcriptional changes in multiple system atrophy and Parkinson's disease putamen Exp. Neurol. 199 2006 465 478
70. H. Wang, N.C. McKnight, T. Zhang, M.L. Lu, S.P. Balk, and X. Yuan SOX9 is expressed in normal prostate basal cells and regulates androgen receptor expression in prostate cancer cells Cancer Res. 67 2007 528 536
71. T.F. Westbrook, G. Hu, X.L. Ang, P. Mulligan, N.N. Pavlova, A. Liang, Y. Leng, R. Maehr, Y. Shi, J.W. Harper, and S.J. Elledge SCFβ-TRCP controls oncogenic transformation and neural differentiation through REST degradation Nature 452 2008 370 374
72. P.S. Whitton Inflammation as a causative factor in the aetiology of Parkinson's disease Br. J. Pharmacol. 150 2007 963 976
73. A. Wood-Kaczmar, S. Gandhi, and N.W. Wood Understanding the molecular causes of Parkinson's disease Trends Mol. Med. 12 2006 521 528
74. T. Yamada, P.L. McGeer, and E.G. McGeer Lewy bodies in Parkinson's disease are recognized by antibodies to complement proteins Acta Neuropathol. 84 1992 100 104
75. M. Yankova, S.A. Hart, and C.S. Woolley Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study Proc. Natl. Acad. Sci. U.S.A. 98 2001 3525 3530
76. H. Yue, P.S. Eastman, B.B. Wang, J. Minor, M.H. Doctolero, R.L. Nuttall, R. Stack, J.W. Becker, J.R. Montgomery, M. Vainer, and R. Johnston An evaluation of the performance of cDNA microarrays for detecting changes in global mRNA expression Nucleic Acids Res. 29 2001 E41-1
77. S. Zaja-Milatovic, D. Milatovic, A.M. Schantz, J. Zhang, K. Montine, A. Sami, A.Y. Deutch, and T.J. Montine Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease Neurology 64 2005 545 547
78. Y. Zhang, M. James, F.A. Middleton, and R.L. Davis Transcriptional analysis of multiple brain regions in Parkinson's disease supports the involvement of specific protein processing, energy metabolism, and signaling pathways, and suggests novel disease mechanisms Am. J. Med. Genet. B. Neuropsychiatr. Genet. 137B 2005 5 16
79. J. Zou, S. Young, F. Zhu, F. Gheyas, S. Skeans, Y. Wan, L. Wang, W. Ding, M. Billah, T. McClanahan, R.L. Coffman, R. Egan, and S. Umland Microarray profile of differentially expressed genes in a monkey model of allergic asthma Genome Biol. 3 2002 research0020
80. C. Zuccato, M. Tartari, A. Crotti, D. Goffredo, M. Valenza, L. Conti, T. Cataudella, B.R. Leavitt, M.R. Hayden, T. Timmusk, D. Rigamonti, and E. Cattaneo Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes Nat. Genet. 35 2003 76 83