Expression analysis of dopaminergic neurons in Parkinson's disease and aging links transcriptional dysregulation of energy metabolism to cell death

Acta Neuropathologica

Volumn 122, Issue 1, 2011, Pages 75-86

  Elstner, Matthias ^a,b   Morris, Christopher M ^c   Heim, Katharina ^b   Bender, Andreas ^a   Mehta, Divya ^b   Jaros, Evelyn ^c   Klopstock, Thomas ^a   Meitinger, Thomas ^b,d   Turnbull, Douglass M ^c   Prokisch, Holger ^b,d  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Aging; Dopaminergic neuron; Energy metabolism; Gene expression; Glia; Hif 1 ; Mitochondria; mTOR; Parkinson's disease; Pathway analysis; PI3K Akt

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GROWTH FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR;

AGING; ARTICLE; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOPAMINERGIC NERVE CELL; DOWN REGULATION; ENERGY METABOLISM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; NERVE CELL PLASTICITY; NUTRITIONAL DEFICIENCY; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; RNA PROCESSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

AGED; AGED, 80 AND OVER; AGING; CASE-CONTROL STUDIES; CELL DEATH; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOPAMINE; ENERGY METABOLISM; GENE EXPRESSION PROFILING; HUMANS; NEURONAL PLASTICITY; NEURONS; PARKINSON DISEASE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; SYNAPSES; TRANSCRIPTION, GENETIC;

EID: 79959602140     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0828-9     Document Type: Article

References (69)

1. PM Abou-Sleiman MM Muqit NW Wood 2006 Expanding insights of mitochondrial dysfunction in Parkinson's disease Nat Rev Neurosci 7 207 219 16495942 1:CAS:528:DC%2BD28Xhs1Gqt70%3D 10.1038/nrn1868 (Pubitemid 43292466)
2. H Aleyasin MW Rousseaux PC Marcogliese, et al. 2010 DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway Proc Natl Acad Sci USA 107 3186 3191 20133695 1:CAS:528:DC%2BC3cXis1ChurY%3D 10.1073/pnas.0914876107
3. CA Altar MP Vawter SD Ginsberg 2009 Target identification for CNS diseases by transcriptional profiling Neuropsychopharmacology 34 18 54 18923405 1:CAS:528:DC%2BD1cXhsVyru73L 10.1038/npp.2008.172
4. M Atz D Walsh P Cartagena, et al. 2007 Methodological considerations for gene expression profiling of human brain J Neurosci Methods 163 295 309 17512057 1:CAS:528:DC%2BD2sXmtlSntrs%3D 10.1016/j.jneumeth.2007.03.022 (Pubitemid 46874608)
5. G Benard N Bellance C Jose S Melser K Nouette-Gaulain R Rossignol 2010 Multi-site control and regulation of mitochondrial energy production Biochim Biophys Acta 1797 698 709 20226160 1:CAS:528:DC%2BC3cXnvV2qs7Y%3D 10.1016/j.bbabio.2010.02.030
6. A Bender KJ Krishnan CM Morris, et al. 2006 High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease Nat Genet 38 515 517 16604074 1:CAS:528:DC%2BD28XjvVGksbs%3D 10.1038/ng1769
7. A Bender RM Schwarzkopf A McMillan, et al. 2008 Dopaminergic midbrain neurons are the prime target for mitochondrial DNA deletions J Neurol 255 1231 1235 18604467 10.1007/s00415-008-0892-9
8. R Betarbet RM Canet-Aviles TB Sherer, et al. 2006 Intersecting pathways to neurodegeneration in Parkinson's disease: effects of the pesticide rotenone on DJ-1, alpha-synuclein, and the ubiquitin-proteasome system Neurobiol Dis 22 404 420 16439141 1:CAS:528:DC%2BD28XktVyjs7g%3D 10.1016/j.nbd.2005.12.003 (Pubitemid 44294281)
9. NA Bishop T Lu BA Yankner 2010 Neural mechanisms of ageing and cognitive decline Nature 464 529 535 20336135 1:CAS:528:DC%2BC3cXjvVGlu7o%3D 10.1038/nature08983
10. K Bossers G Meerhoff R Balesar, et al. 2009 Analysis of gene expression in Parkinson's disease: possible involvement of neurotrophic support and axon guidance in dopaminergic cell death Brain Pathol 19 91 107 18462474 1:CAS:528:DC%2BD1MXitVWht78%3D 10.1111/j.1750-3639.2008.00171.x
11. H Braak K Del Tredici U Rüb RA de Vos EN Jansen Steur E Braak 2003 Staging of brain pathology related to sporadic Parkinson's disease Neurobiol Aging 24 197 211 12498954 10.1016/S0197-4580(02)00065-9 (Pubitemid 36007810)
12. C Buesa T Maes F Subirada M Barrachina I Ferrer 2004 DNA chip technology in brain banks: confronting a degrading world J Neuropathol Exp Neurol 63 1003 1014 15535128 1:CAS:528:DC%2BD2cXpslCrurY%3D (Pubitemid 39372585)
13. CR Cabello JJ Thune H Pakkenberg B Pakkenberg 2002 Ageing of substantia nigra in humans: cell loss may be compensated by hypertrophy Neuropathol Appl Neurobiol 28 283 291 12175340 1:STN:280:DC%2BD38vit1CnsA%3D%3D 10.1046/j.1365-2990.2002.00393.x (Pubitemid 34989290)
14. SE Calvano W Xiao DR Richards, et al. 2005 A network-based analysis of systemic inflammation in humans Nature 437 1032 1037 16136080 1:CAS:528:DC%2BD2MXhtV2ktrvI 10.1038/nature03985 (Pubitemid 41486985)
15. I Cantuti-Castelvetri C Keller-McGandy B Bouzou, et al. 2007 Effects of gender on nigral gene expression and Parkinson disease Neurobiol Dis 26 606 614 17412603 1:CAS:528:DC%2BD2sXlsFKnsbo%3D 10.1016/j.nbd.2007.02.009 (Pubitemid 46756328)
16. CS Chan JN Guzman E Ilijic, et al. 2007 'Rejuvenation' protects neurons in mouse models of Parkinson's disease Nature 447 1081 1086 17558391 1:CAS:528:DC%2BD2sXmvFKmurY%3D 10.1038/nature05865 (Pubitemid 47014425)
17. E Croisier MB Graeber 2006 Glial degeneration and reactive gliosis in alpha-synucleinopathies: the emerging concept of primary gliodegeneration Acta Neuropathol 112 517 530 16896905 10.1007/s00401-006-0119-z (Pubitemid 44550676)
18. W Dauer S Przedborski 2003 Parkinson's disease: mechanisms and models Neuron 39 889 909 12971891 1:CAS:528:DC%2BD3sXnsFait7o%3D 10.1016/S0896-6273(03) 00568-3 (Pubitemid 37130207)
19. AF Domingues DM Arduíno AR Esteves RH Swerdlow CR Oliveira SM Cardoso 2008 Mitochondria and ubiquitin-proteasomal system interplay: relevance to Parkinson's disease Free Radic Biol Med 45 820 825 18619530 1:CAS:528:DC%2BD1cXhtVylsbbK 10.1016/j.freeradbiomed.2008.06.007
20. DC Duke LB Moran ME Kalaitzakis, et al. 2006 Transcriptome analysis reveals link between proteasomal and mitochondrial pathways in Parkinson's disease Neurogenetics 7 139 148 16699787 1:CAS:528:DC%2BD28XhtVanu7%2FK 10.1007/s10048-006-0033-5 (Pubitemid 44078291)
21. A Elbaz F Moisan 2008 Update in the epidemiology of Parkinson's disease Curr Opin Neurol 21 454 460 18607207 10.1097/WCO.0b013e3283050461
22. M Elstner C Andreoli T Klopstock T Meitinger H Prokisch 2009 The mitochondrial proteome database: MitoP2 Methods Enzymol 457 3 20 19426859 1:CAS:528:DC%2BD1MXpsFejtb0%3D 10.1016/S0076-6879(09)05001-0
23. M Elstner CM Morris K Heim, et al. 2009 Single-cell expression profiling of dopaminergic neurons combined with association analysis identifies pyridoxal kinase as Parkinson's disease gene Ann Neurol 66 792 798 20035503 1:CAS:528:DC%2BC3cXhtlamsL8%3D 10.1002/ana.21780
24. MJ Farrer 2006 Genetics of Parkinson disease: paradigm shifts and future prospects Nat Rev Genet 7 306 318 16543934 1:CAS:528:DC%2BD28XisFWgtLk%3D 10.1038/nrg1831
25. JM Fearnley AJ Lees 1991 Ageing and Parkinson's disease: substantia nigra regional selectivity Brain 114 2283 2301 1933245 10.1093/brain/114.5.2283
26. T Fujino J Kondo M Ishikawa K Morikawa TT Yamamoto 2001 Acetyl-CoA synthetase 2, a mitochondrial matrix enzyme involved in the oxidation of acetate J Biol Chem 276 11420 11426 11150295 1:CAS:528:DC%2BD3MXjvFGjt7s%3D 10.1074/jbc.M008782200 (Pubitemid 38089336)
27. JJ Gagne MC Power 2010 Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis Neurology 74 995 1002 20308684 1:CAS:528: DC%2BC3cXjs1Ggsbs%3D 10.1212/WNL.0b013e3181d5a4a3
28. T Gasser 2009 Molecular pathogenesis of Parkinson disease: insights from genetic studies Expert Rev Mol Med 11 e22 19631006 10.1017/S1462399409001148
29. S Geisler KM Holmström D Skujat, et al. 2010 PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1 Nat Cell Biol 12 119 131 20098416 1:CAS:528:DC%2BC3cXhtlCqtbs%3D 10.1038/ncb2012
30. M Gerlach KL Double MB Youdim P Riederer 2000 Strategies for the protection of dopaminergic neurons against neurotoxicity Neurotox Res 2 99 114 16787835 1:CAS:528:DC%2BD3cXot1Cqsrk%3D 10.1007/BF03033788
31. MB Graeber 2008 Twenty-first century brain banking: at the crossroads Acta Neuropathol 115 493 496 18347804 10.1007/s00401-008-0363-5
32. E Grunblatt S Mandel J Jacob-Hirsch, et al. 2004 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 1543 1573 15455214 1:STN:280:DC%2BD2crptFGqsw%3D%3D 10.1007/s00702-004-0212-1 (Pubitemid 40068786)
33. JN Guzman J Sanchez-Padilla D Wokosin, et al. 2010 Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1 Nature 468 696 700 21068725 1:CAS:528:DC%2BC3cXhtl2rtb7F 10.1038/nature09536
34. MA Hauser YJ Li H Xu, et al. 2005 Expression profiling of substantia nigra in Parkinson disease, progressive supranuclear palsy, and frontotemporal dementia with parkinsonism Arch Neurol 62 917 921 15956162 10.1001/archneur.62. 6.917 (Pubitemid 40973453)
35. MB Hock A Kralli 2009 Transcriptional control of mitochondrial biogenesis and function Annu Rev Physiol 71 177 203 19575678 1:CAS:528: DC%2BD1MXjsValsb4%3D 10.1146/annurev.physiol.010908.163119
36. CM Klinge 2008 Estrogenic control of mitochondrial function and biogenesis J Cell Biochem 105 1342 1351 18846505 1:CAS:528:DC%2BD1cXhsFaks7fN 10.1002/jcb.21936
37. DW Lee S Rajagopalan A Siddiq, et al. 2009 Inhibition of prolyl hydroxylase protects against 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine- induced neurotoxicity: model for the potential involvement of the hypoxia-inducible factor pathway in Parkinson disease J Biol Chem 284 29065 29076 19679656 1:CAS:528:DC%2BD1MXht1Cmt7vP 10.1074/jbc.M109.000638
38. TG Lesnick S Papapetropoulos DC Mash, et al. 2007 A genomic pathway approach to a complex disease: axon guidance and Parkinson disease PLoS Genet 3 e98 17571925 10.1371/journal.pgen.0030098 (Pubitemid 47015858)
39. G López-Lluch PM Irusta P Navas R de Cabo 2008 Mitochondrial biogenesis and healthy aging Exp Gerontol 43 813 819 18662766 10.1016/j.exger.2008.06.014
40. T Lu Y Pan SY Kao, et al. 2004 Gene regulation and DNA damage in the ageing human brain Nature 429 883 891 15190254 1:CAS:528:DC%2BD2cXltVKltLY%3D 10.1038/nature02661 (Pubitemid 38843301)
41. C Malagelada ZH Jin V Jackson-Lewis S Przedborski LA Greene 2010 Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease J Neurosci 30 1166 1175 20089925 1:CAS:528: DC%2BC3cXhtlKlsr8%3D 10.1523/JNEUROSCI.3944-09.2010
42. IG McKeith DW Dickson J Lowe, et al. 2005 Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium Neurology 65 1863 1872 16237129 1:STN:280:DC%2BD2Mnpt1GqsQ%3D%3D 10.1212/01.wnl.0000187889.17253. b1 (Pubitemid 43970103)
43. RM Miller GL Kiser TM Kaysser-Kranich RJ Lockner C Palaniappan HJ Federoff 2006 Robust dysregulation of gene expression in substantia nigra and striatum in Parkinson's disease Neurobiol Dis 21 305 313 16143538 1:CAS:528:DC%2BD28XmsVGnsw%3D%3D 10.1016/j.nbd.2005.07.010 (Pubitemid 43099854)
44. K Mirnics J Pevsner 2004 Progress in the use of microarray technology to study the neurobiology of disease Nat Neurosci 7 434 439 15114354 1:CAS:528:DC%2BD2cXjsFKltrw%3D 10.1038/nn1230 (Pubitemid 38544572)
45. LB Moran DC Duke M Deprez DT Dexter RK Pearce MB Graeber 2006 Whole genome expression profiling of the medial and lateral substantia nigra in Parkinson's disease Neurogenetics 7 1 11 16344956 1:CAS:528:DC%2BD28XltVGnt7k%3D 10.1007/s10048-005-0020-2 (Pubitemid 43327678)
46. LB Moran MB Graeber 2008 Towards a pathway definition of Parkinson's disease: a complex disorder with links to cancer, diabetes and inflammation Neurogenetics 9 1 13 18196299 10.1007/s10048-007-0116-y
47. K Nakaso S Ito K Nakashima 2008 Caffeine activates the PI3K/Akt pathway and prevents apoptotic cell death in a Parkinson's disease model of SH-SY5Y cells Neurosci Lett 432 146 150 18201823 1:CAS:528:DC%2BD1cXitVegtbY%3D 10.1016/j.neulet.2007.12.034
48. DP Narendra SM Jin A Tanaka, et al. 2010 PINK1 is selectively stabilized on impaired mitochondria to activate Parkin PLoS Biol 8 e1000298 20126261 10.1371/journal.pbio.1000298
49. NB Nedelsky PK Todd JP Taylor 2008 Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection Biochim Biophys Acta 1782 691 699 18930136 1:CAS:528:DC%2BD1cXhsVCntb%2FN
50. T Pan S Kondo W Zhu W Xie J Jankovic W Le 2008 Neuroprotection of rapamycin in lactacystin-induced neurodegeneration via autophagy enhancement Neurobiol Dis 32 16 25 18640276 1:CAS:528:DC%2BD1cXhtFantbjF 10.1016/j.nbd.2008.06.003
51. P Riederer MB Youdim S Mandel M Gerlach E Grünblatt 2008 Genomic aspects of sporadic Parkinson's disease Parkinsonism Relat Disord 14 S88 S91 18585078 10.1016/j.parkreldis.2008.04.009
52. CD Rollo 2009 Dopamine and aging: intersecting facets Neurochem Res 34 601 629 18841466 1:CAS:528:DC%2BD1MXkvFygtQ%3D%3D 10.1007/s11064-008-9858-7
53. GW Ross H Petrovitch RD Abbott, et al. 2004 Parkinsonian signs and substantia nigra neuron density in decendents elders without PD Ann Neurol 56 532 539 15389895 10.1002/ana.20226 (Pubitemid 39319343)
54. G Rudow R O'Brien AV Savonenko, et al. 2008 Morphometry of the human substantia nigra in ageing and Parkinson's disease Acta Neuropathol 115 461 470 18297291 10.1007/s00401-008-0352-8
55. E Sekoguchi N Sato A Yasui, et al. 2003 A novel mitochondrial carnitine-acylcarnitine translocase induced by partial hepatectomy and fasting J Biol Chem 278 38796 38802 12882971 1:CAS:528:DC%2BD3sXnslWjsLk%3D 10.1074/jbc.M306372200 (Pubitemid 37221779)
56. F Simunovic M Yi Y Wang, et al. 2008 Gene expression profiling of substantia nigra dopamine neurons: further insights into Parkinson's disease pathology Brain 132 1795 1809 19052140 10.1093/brain/awn323
57. F Simunovic M Yi Y Wang R Stephens KC Sonntag 2010 Evidence for gender-specific transcriptional profiles of nigral dopamine neurons in Parkinson disease PLoS One 5 e8856 20111594 10.1371/journal.pone.0008856
58. AK Stark B Pakkenberg 2004 Histological changes of the dopaminergic nigrostriatal system in aging Cell Tissue Res 318 81 92 15365813 1:STN:280:DC%2BD2crjtVansA%3D%3D 10.1007/s00441-004-0972-9 (Pubitemid 39362629)
59. DJ Surmeier 2007 Calcium, ageing, and neuronal vulnerability in Parkinson's disease Lancet Neurol 6 933 938 17884683 1:CAS:528: DC%2BD2sXht1Krtr%2FN 10.1016/S1474-4422(07)70246-6 (Pubitemid 47405004)
60. GT Sutherland NA Matigian AM Chalk, et al. 2009 A cross-study transcriptional analysis of Parkinson's disease PLoS One 4 e4955 19305504 10.1371/journal.pone.0004955
61. LS Tain H Mortiboys RN Tao E Ziviani O Bandmann AJ Whitworth 2009 Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss Nat Neurosci 12 1129 1135 19684592 1:CAS:528:DC%2BD1MXpvFCrt7c%3D 10.1038/nn.2372
62. S Timmons MF Coakley AM Moloney C O' Neill 2009 Akt signal transduction dysfunction in Parkinson's disease Neurosci Lett 467 30 35 19800394 1:CAS:528:DC%2BD1MXhtlCnt7nI 10.1016/j.neulet.2009.09.055
63. TB Vanitallie 2008 Parkinson disease: primacy of age as a risk factor for mitochondrial dysfunction Metabolism 57 Suppl 2 S50 S55 18803967 1:CAS:528:DC%2BD1cXhtFektbnO 10.1016/j.metabol.2008.07.015
64. S Vasseur S Afzal J Tardivel-Lacombe DS Park JL Iovanna TW Mak 2009 DJ-1/PARK7 is an important mediator of hypoxia-induced cellular responses Proc Natl Acad Sci USA 106 1111 1116 19144925 1:CAS:528:DC%2BD1MXhsFyjurw%3D 10.1073/pnas.0812745106
65. MP Vawter H Tomita F Meng, et al. 2006 Mitochondrial-related gene expression changes are sensitive to agonal-pH state: implications for brain disorders Mol Psychiatry 11 663 679 1:CAS:528:DC%2BD28XmtFyrt7s%3D 10.1038/sj.mp.4001830 (Pubitemid 43989813)
66. IR Vogt AJ Lees BO Evert T Klockgether M Bonin U Wüllner 2006 Transcriptional changes in multiple system atrophy and Parkinson's disease putamen Exp Neurol 199 465 478 16626704 1:CAS:528:DC%2BD28XmtlGmt78%3D 10.1016/j.expneurol.2006.01.008 (Pubitemid 43928973)
67. DC Wright PC Geiger DH Han TE Jones JO Holloszy 2007 Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1 alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation J Biol Chem 282 18793 18799 17488713 1:CAS:528:DC%2BD2sXmvVarsLw%3D 10.1074/jbc.M611252200 (Pubitemid 47100154)
68. Y Zhang M James FA Middleton RL Davis 2005 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 137 5 16 (Pubitemid 41076605)
69. Zheng B, Liao Z, Locascio JJ, et al (2010) PGC-1α, a potential therapeutic target for early intervention in Parkinson's disease. Sci Transl Med 2:52ra73