Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection
Open accessAbstract
Molecular differences between dopamine (DA) neurons may explain why the mesostriatal DA neurons in the A9 region preferentially degenerate in Parkinson's disease (PD) and toxic models, whereas the adjacent A10 region mesolimbic and mesocortical DA neurons are relatively spared. To characterize innate physiological differences between A9 and A10 DA neurons, we determined gene expression profiles in these neurons in the adult mouse by laser capture microdissection, microarray analysis and real-time PCR. We found 42 genes relatively elevated in A9 DA neurons, whereas 61 genes were elevated in A10 DA neurons [> 2-fold; false discovery rate (FDR) < 1%]. Genes of interest for further functional analysis were selected by criteria of (i) fold differences in gene expression, (ii) real-time PCR validation and (iii) potential roles in neurotoxic or protective biochemical pathways. Three A9-elevated molecules [G-protein coupled inwardly rectifying K channel 2 (GIRK2), adenine nucleotide translocator 2 (ANT-2) and the growth factor IGF-1] and three A10-elevated peptides (GRP, CGRP and PACAP) were further examined in both alpha-synuclein overexpressing PC12 (PC12-alphaSyn) cells and rat primary ventral mesencephalic (VM) cultures exposed to MPP+ neurotoxicity. GIRK2-positive DA neurons were more vulnerable to MPP+ toxicity and overexpression of GIRK2 increased the vulnerability of PC12-alphaSyn cells to the toxin. Blocking of ANT decreased vulnerability to MPP+ in both cell culture systems. Exposing cells to IGF-1, GRP and PACAP decreased vulnerability of both cell types to MPP+, whereas CGRP protected PC12-alphaSyn cells but not primary VM DA neurons. These results indicate that certain differentially expressed molecules in A9 and A10 DA neurons may play key roles in their relative vulnerability to toxins and PD.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Bulk profiling experiments comparing substantia nigra pars compacta and ventral tegmental area neurons yielded gene expression differences but could not distinguish heterogeneous populations within each anatomical cluster.
“Bulk profiling experiments comparing SNc and VTA neurons did indeed yield some interesting gene expression differences [6–9], but suffered from the caveat that they could not distinguish heterogeneous populations within each anatomical cluster.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [7]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Mutation in the α-Synuclein Gene Identified in Families with Parkinson's Disease
Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., et al. (1997) · Science · doi:10.1126/science.276.5321.2045 · Cited by 8,240 · see citing works
Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism
Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., & Shimizu, N. (1998) · Nature · doi:10.1038/33416 · Cited by 5,227 · see citing works
α-Synuclein Locus Triplication Causes Parkinson's Disease
Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., et al. (2003) · Science · doi:10.1126/science.1090278 · Cited by 4,383 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
Chronic systemic pesticide exposure reproduces features of Parkinson's disease
Betarbet, R., Sherer, T., Mackenzie, G., Garcia-Osuna, M., Panov, A., & Greenamyre, J. (2000) · Nature Neuroscience · doi:10.1038/81834 · Cited by 3,797 · see citing works
AGEING AND PARKINSON'S DISEASE: SUBSTANTIA NIGRA REGIONAL SELECTIVITY
FEARNLEY, J. M., & LEES, A. J. (1991) · Brain · doi:10.1093/brain/114.5.2283 · Cited by 3,529 · see citing works
Hereditary Early-Onset Parkinson's Disease Caused by Mutations in <i>PINK1</i>
Valente, E. M., Abou-Sleiman, P. M., Caputo, V., Muqit, M. M. K., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A. R., Healy, D. G., et al. (2004) · Science · doi:10.1126/science.1096284 · Cited by 3,481 · see citing works
Mutations in the DJ-1 Gene Associated with Autosomal Recessive Early-Onset Parkinsonism
Bonifati, V., Rizzu, P., van Baren, M. J., Schaap, O., Breedveld, G. J., Krieger, E., Dekker, M. C. J., Squitieri, F., Ibáñez, P., Joosse, M., et al. (2003) · Science · doi:10.1126/science.1077209 · Cited by 2,800 · see citing works
Gene regulation and DNA damage in the ageing human brain
Lu, T., Pan, Y., Kao, S.-Y., Li, C., Kohane, I., Chan, J., & Yankner, B. A. (2004) · Nature · doi:10.1038/nature02661 · Cited by 1,874 · see citing works
Self-Inactivating Lentivirus Vector for Safe and Efficient In Vivo Gene Delivery
Zufferey, R., Dull, T., Mandel, R. J., Bukovsky, A., Quiroz, D., Naldini, L., & Trono, D. (1998) · Journal of Virology · doi:10.1128/jvi.72.12.9873-9880.1998 · Cited by 1,815 · see citing works
The substantia nigra of the human brain
Damier, P., Hirsch, É. C., Agid, Y., & Graybiel, A. M. (1999) · Brain · doi:10.1093/brain/122.8.1437 · Cited by 1,772 · see citing works
The ubiquitin pathway in Parkinson's disease
Leroy, E., Boyer, R., Auburger, G. W. J., Leube, B., Ulm, G., Mezey, É., Harta, G., Brownstein, M., Jonnalagada, S., Chernova, T., et al. (1998) · Nature · doi:10.1038/26652 · Cited by 1,572 · see citing works
Bombesin-like peptides can function as autocrine growth factors in human small-cell lung cancer
Cuttitta, F. F., Carney, D. N., Mulshine, J. L., Moody, T. W., FEDORKO, J., Fischler, A., & Minna, J. D. (1985) · Nature · doi:10.1038/316823a0 · Cited by 1,348 · see citing works
Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease
Hirsch, E., Graybiel, A. M., & Agid, Y. A. (1988) · Nature · doi:10.1038/334345a0 · Cited by 1,301 · see citing works
Bax and Adenine Nucleotide Translocator Cooperate in the Mitochondrial Control of Apoptosis
Marzo, I., Brenner, C., Zamzami, N., Jürgensmeier, J. M., Susin, S. A., Vieira, H. L. A., Prévost, M.-C., Xie, Z., Matsuyama, S., Reed, J. C., et al. (1998) · Science · doi:10.1126/science.281.5385.2027 · Cited by 1,168 · see citing works
Bim: a novel member of the Bcl‐2 family that promotes apoptosis
O’Connor, L., Strasser, A., O’Reilly, L. A., Hausmann, G., Adams, J. M., Cory, S., & Huang, D. C. S. (1998) · The EMBO Journal · doi:10.1093/emboj/17.2.384 · Cited by 1,163 · see citing works
Oxidative Pathways for Catecholamines in the Genesis of Neuromelanin and Cytotoxic Quinones
GRAHAM, D. G. (1978) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)13535-9 · Cited by 1,126 · cited 1× · see citing works
“Efficient DA sequestration into vesicles protects DA neurons from the deleterious effects of DA oxidation (82).”
BackgroundPituitary Adenylate Cyclase-Activating Polypeptide and Its Receptors: From Structure to Functions
Vaudry, D., Gonzalez, B. J., Basille, M., Yon, L., Fournier, A., & Vaudry, H. (2000) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01449-2 · Cited by 1,120 · see citing works
Mitochondrial Dysfunction and Oxidative Damage in parkin-deficient Mice
Palacino, J. J., Sagi, D., Goldberg, M. S., Krauss, S., Motz, C., Wacker, M., Klose, J., & Shen, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401135200 · Cited by 995 · see citing works
Tanner, C. M., Ottman, R., Goldman, S. M., Ellenberg, J., Chan, P., Mayeux, R. P., & Langston, J. W. (1999) · JAMA · doi:10.1001/jama.281.4.341 · Cited by 869 · see citing works
The mitochondrial transporter family (SLC25): physiological and pathological implications
Palmieri, F. (2004) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-003-1099-7 · Cited by 757 · see citing works
α-Synuclein Promotes Mitochondrial Deficit and Oxidative Stress
Hsu, L. J., Sagara, Y., Arroyo, A., Rockenstein, E. M., Sisk, A., Mallory, M. E., Wong, J., Takenouchi, T., Hashimoto, M., & Masliah, E. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64553-1 · Cited by 716 · see citing works
The substantia nigra of the human brain
Damier, P., Hirsch, É. C., Agid, Y., & Graybiel, A. M. (1999) · Brain · doi:10.1093/brain/122.8.1421 · Cited by 579 · see citing works
Drăghici, S., Khatri, P., Martins, R. P., Ostermeier, G. C., & Krawetz, S. A. (2003) · Genomics · doi:10.1016/s0888-7543(02)00021-6 · Cited by 578 · see citing works
Rate of cell death in parkinsonism indicates active neuropathological process
McGeer, P. L., Itagaki, S., Akiyama, H., & McGeer, E. G. (1988) · Annals of Neurology · doi:10.1002/ana.410240415 · Cited by 557 · see citing works
Arimura, A. (1998) · The Japanese Journal of Physiology · doi:10.2170/jjphysiol.48.301 · Cited by 512 · see citing works
Halestrap, A. P., & Brenner, C. (2003) · Current Medicinal Chemistry · doi:10.2174/0929867033457278 · Cited by 505 · see citing works
Tanaka, Y. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.9.919 · Cited by 497 · see citing works
Rab GTPases, intracellular traffic and disease
Seabra, M. C., Mules, E. H., & Hume, A. N. (2002) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(01)02227-4 · Cited by 468 · see citing works
Pituitary adenylate cyclase activating polypeptide (PACAP): discovery and current status of research
Arimura, A. (1992) · Regulatory Peptides · doi:10.1016/0167-0115(92)90621-z · Cited by 456 · see citing works
Karschin, C., Dißmann, E., Stühmer, W., & Karschin, A. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-11-03559.1996 · Cited by 449 · see citing works
Yamada, T., McGeer, P. L., Baimbridge, K. G., & McGeer, E. G. (1990) · Brain Research · doi:10.1016/0006-8993(90)91236-a · Cited by 448 · see citing works
Ion channel regulation by G proteins
Wickman, K., & Clapham, D. E. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.4.865 · Cited by 427 · see citing works
Yeast Genes That Enhance the Toxicity of a Mutant Huntingtin Fragment or α-Synuclein
Willingham, S., Outeiro, T. F., DeVit, M. J., Lindquist, S. L., & Muchowski, P. J. (2003) · Science · doi:10.1126/science.1090389 · Cited by 422 · see citing works
Is the mesocortical dopaminergic system involved in Parkinson disease?
Javoy-Agid, F., & Agid, Y. (1980) · Neurology · doi:10.1212/wnl.30.12.1326 · Cited by 417 · see citing works
Pakkenberg, B., Møller, A., Gundersen, H. J. G., Dam, A. M., & Pakkenberg, H. (1991) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.54.1.30 · Cited by 408 · see citing works
Neuhoff, H., Neu, A. D., Liss, B., & Roeper, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01290.2002 · Cited by 400 · see citing works
Midbrain dopaminergic cell loss in parkinson's disease: Computer visualization
German, D. C., Manaye, K. F., Smith, W. K., Woodward, D. J., & Saper, C. B. (1989) · Annals of Neurology · doi:10.1002/ana.410260403 · Cited by 396 · see citing works
Wolfart, J., Neuhoff, H., Franz, O., & Roeper, J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-03443.2001 · Cited by 345 · see citing works
Complex I and Parkinson's Disease
Greenamyre, J. T., Sherer, T., Betarbet, R. S., & Panov, A. V. (2001) · IUBMB Life · doi:10.1080/15216540152845939 · Cited by 335 · see citing works
German, D. C., Manaye, K. F., Sonsalla, P. K., & Brooks, B. A. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb24523.x · Cited by 319 · see citing works
Cassarino, D. S., Parks, J. K., Parker, W. D., & Bennett, J. P. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(98)00083-0 · Cited by 304 · see citing works
MPTP as a Mitochondrial Neurotoxic Model of Parkinson's Disease
Przedborski, S., Tieu, K., Perier, C., & Vila, M. (2004) · Journal of Bioenergetics and Biomembranes · doi:10.1023/b:jobb.0000041771.66775.d5 · Cited by 289 · see citing works
High levels of a retinoic acid-generating dehydrogenase in the meso-telencephalic dopamine system.
McCaffery, P., & Dräger, U. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.16.7772 · Cited by 266 · see citing works
Kermer, P., Klöcker, N., Labes, M., & Bähr, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-02-00722.2000 · Cited by 265 · see citing works
Functional Effects of the Mouse weaver Mutation on G Protein–Gated Inwardly Rectifying K+ Channels
Slesinger, P. A., Patil, N., Liao, Y. J., Jan, Y. N., Jan, L. Y., & Cox, D. (1996) · Neuron · doi:10.1016/s0896-6273(00)80050-1 · Cited by 262 · see citing works
Estradiol protects mesencephalic dopaminergic neurons from oxidative stress-induced neuronal death
Sawada, H., Ibi, M., Kihara, T., Urushitani, M., Akaike, A., & Shimohama, S. (1998) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19981201)54:5 · Cited by 246 · see citing works
Multiple risk factors for Parkinson's disease.
Gorell, J., Peterson, E., Rybicki, B., & Johnson, C. C. (2004) · Journal of Neurological Sciences · doi:10.1016/j.jns.2003.09.014 · Cited by 236 · see citing works
Ogi, K., Kimura, C., Onda, H., et al. (1990) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(05)80924-6 · Cited by 235 · see citing works
Any way you cut it: A new journal policy for the use of unbiased counting methods
Saper, C. B. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960101)364:1 · Cited by 226 · see citing works
Inanobe, A., Yoshimoto, Y., Horio, Y., Morishige, K., Hibino, H., Matsumoto, S., Tokunaga, Y., Maeda, T., Hata, Y., Takai, Y., et al. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-03-01006.1999 · Cited by 207 · see citing works
Calcitonin gene-related peptide: Novel neuropeptide
Goodman, E., & Iversen, L. L. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90568-0 · Cited by 207 · see citing works
German, D. C., Dubach, M. F., Askari, S., Speciale, S. G., & Bowden, D. M. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90320-x · Cited by 200 · see citing works
Haber, S. N., Ryoo, H., Cox, C., & Lu, W. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903620308 · Cited by 188 · see citing works
Generalized brain and skin proteasome inhibition in Huntington’s disease
Seo, H., Sonntag, K., & Isacson, O. (2004) · Annals of Neurology · doi:10.1002/ana.20207 · Cited by 188 · see citing works
Self-citationMeskenaïte, V. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970303)379:1 · Cited by 180 · see citing works
Bell, D., & McDermott, B. J. (1996) · Pharmacological Reviews · doi:10.1016/s0031-6997(25)06943-1 · Cited by 176 · see citing works
Delgado, M., & Ganea, D. (2003) · The FASEB Journal · doi:10.1096/fj.02-0799fje · Cited by 166 · see citing works
Dopamine transporter messenger RNA in Parkinson's disease and control substantia nigra neurons
Uhl, G. R., Walther, D. M., Mash, D. C., Faucheux, B. A., & Javoy-Agid, F. (1994) · Annals of Neurology · doi:10.1002/ana.410350421 · Cited by 151 · see citing works
Molecular basis for catecholaminergic neuron diversity
Grimm, J., Mueller, A., Hefti, F., & Rosenthal, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405340101 · Cited by 150 · see citing works
IGF-I prevents glutamate-induced motor neuron programmed cell death
Vincent, A. M., Mobley, B. C., Hiller, A., & Feldman, E. L. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.03.001 · Cited by 148 · see citing works
Quesada, A., & Micevych, P. E. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10833 · Cited by 147 · see citing works
Insulin-like growth factor-I, cognition and brain aging
van Dam, P. S., & Aleman, A. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.047 · Cited by 142 · see citing works
Seroogy, K. B., Dangaran, K., Lim, S., Haycock, J. W., & Fallon, J. H. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902790306 · Cited by 138 · see citing works
Specific A10 Dopaminergic Nuclei in the Midbrain Degenerate in Parkinson's Disease
McRitchie, D. A., Cartwright, H., & Halliday, G. M. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6418 · Cited by 135 · see citing works
Calcium-binding proteins in primate basal ganglia
Parent, A., Fortin, M., Côté, P., & Cicchetti, F. (1996) · Neuroscience Research · doi:10.1016/0168-0102(96)01065-6 · Cited by 127 · see citing works
Liang, C., Sinton, C. M., Sonsalla, P. K., & German, D. C. (1996) · Neurodegeneration · doi:10.1006/neur.1996.0042 · Cited by 116 · see citing works
Rodrı́guez, M., Barroso‐Chinea, P., Abdala, P., Obeso, J. A., & González‐Hernández, T. (2001) · Experimental Neurology · doi:10.1006/exnr.2000.7624 · Cited by 113 · see citing works
Passage of VIP / PACAP / Secretin Family Across the Blood-Brain Barrier: Therapeutic Effects
Doğrukol‐Ak, D., Töre, F., & Tunçel, N. (2004) · Current Pharmaceutical Design · doi:10.2174/1381612043384934 · Cited by 106 · see citing works
Hauser, E. R., Li, Y., Takeuchi, S., Walters, R., Noureddine, M., Maready, M., Darden, T. A., Hulette, C., Martin, E. R., Hauser, E. R., et al. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg070 · Cited by 103 · see citing works
Reglődi, D., Lubics, A., Tamás, A., et al. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.007 · Cited by 100 · see citing works
Schein, J. C., Hunter, D. D., & Roffler-Tarlov, S. K. (1998) · Developmental Biology · doi:10.1006/dbio.1998.9076 · Cited by 97 · see citing works
Graybiel, A. M., Ohta, K., & Roffler-Tarlov, S. K. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-03-00720.1990 · Cited by 95 · see citing works
Guan, J., Miller, O. T., Waugh, K. M., McCarthy, D. C., & Gluckman, P. D. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00145-2 · Cited by 81 · see citing works
Effects of bombesin on growth of human small cell lung carcinoma in vivo
Alexander, R. W. (1989) · Lung Cancer · doi:10.1016/0169-5002(89)90344-9 · Cited by 81 · see citing works
WANG, J., Hayashi, T., Zhang, W. R., Sakai, K., Shiro, Y., & Abe, K. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02008-4 · Cited by 78 · see citing works
Cell death in the midbrain of the murine mutation weaver
Roffler-Tarlov, S. K., Martin, B., Graybiel, A. M., & Kauer, J. S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01819.1996 · Cited by 75 · see citing works
Growth Factors Rescue Embryonic Dopamine Neurons from Programmed Cell Death
Zawada, W. M., Kirschman, D. L., Cohen, J., et al. (1996) · Experimental Neurology · doi:10.1006/exnr.1996.0115 · Cited by 73 · see citing works
Ole Isacson, A. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90104-t · Cited by 72 · see citing works
Liss, B., Neu, A. D., & Roeper, J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-08839.1999 · Cited by 62 · see citing works
Normal Values of Insulin-Like Growth Factor I and Their Clinical Utility in Adults
Strasburger, C. J., Bidlingmaier, M., Wu, Z., et al. (2001) · Hormone Research in Paediatrics · doi:10.1159/000063484 · Cited by 50 · see citing works
Poe, B., Linville, C., Riddle, D. R., Sonntag, W. E., & Brunso-Bechtold, J. K. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00341-4 · Cited by 49 · see citing works
N-terminal tripeptide of IGF-1 improves functional deficits after 6-OHDA lesion in rats
Krishnamurthi, R., Stott, S., Maingay, M., et al. (2004) · Neuroreport · doi:10.1097/01.wnr.0000127461.15985.07 · Cited by 46 · see citing works
Bombesin-like Peptides: Candidates as Diagnostic and Therapeutic Tools
Yeğen, B. Ç. (2003) · Current Pharmaceutical Design · doi:10.2174/1381612033455134 · Cited by 35 · see citing works
Shaik, S., Ren, J., & Ebadi, M. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01461-1 · Cited by 31 · see citing works
Sirinathsinghji, D. J. S., Kupsch, A. R., Mayer, E. J., et al. (1992) · Molecular Brain Research · doi:10.1016/0169-328x(92)90093-q · Cited by 28 · see citing works
Bayer, S. A., Triarhou, L. C., Thomas, J. C. S., et al. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06901.1994 · Cited by 23 · see citing works
Kiranadi, B., Bangham, J., & Smith, P. A. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)80561-g · Cited by 22 · see citing works
An immunohistochemical demonstration of gastrin-releasing peptide (GRP) in the rat substantia nigra.
Pj, L., Særmark, T., & Mikkelsen, J. D. (1990) · PubMed · Cited by 22 · see citing works
Commentary on “Alpha-synuclein and mitochondria: a tangled skein”
Beal, M. F. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2003.12.002 · Cited by 13 · see citing works
Bürvenich, S., Unsicker, K., & Krieglstein, K. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00038-4 · Cited by 10 · see citing works
Global Functional Profiling of Gene Expression Data
Drăghici, S., & Krawetz, S. A. (2005) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-47815-3_18 · Cited by 9 · see citing works
Ciliax (1999) · doi:10.1002/(sici)1096-9861(19990621)409:1
Flagged first, then by citations
Cited by
Sorted by citations
Tansey, M. G., & Goldberg, M. S. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.11.004 · Cited by 1,045 · see citing works
Human iPSC-based modeling of late-onset disease via progerin-induced aging
Miller, J. D., Ganat, Y. M., Kishinevsky, S., Bowman, R. L., Liu, B., Tu, E. Y., Mandal, P. K., Vera, E., Shim, J.-W., Kriks, S., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.11.006 · Cited by 777 · see citing works
Cooper, O., Seo, H., Andrabi, S., Guardia-Laguarta, C., Graziotto, J., Sundberg, M., McLean, J. R., Carrillo-Reid, L., Xie, Z., Osborn, T., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003985 · Cited by 508 · see citing works
Self-citationDefining midbrain dopaminergic neuron diversity by single-cell gene expression profiling
Poulin, J.-F., Zou, J., Drouin-Ouellet, J., Kim, K.-Y. A., Cicchetti, F., & Awatramani, R. B. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.008 · Cited by 352 · see citing works
Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches
Poulin, J.-F., Gaertner, Z., Moreno-Ramos, O. A., & Awatramani, R. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.01.004 · Cited by 238 · see citing works
Reglodi, D., Renaud, J., Tamas, A., Tizabi, Y., Socías, S. B., Del-Bel, E., & Raisman-Vozari, R. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.10.004 · Cited by 162 · see citing works
The problem of neuronal cell types: a physiological genomics approach
Nelson, S. B., Sugino, K., & Hempel, C. M. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.05.004 · Cited by 157 · see citing works
Panman, L., Papathanou, M., Laguna, A., Oosterveen, T., Volakakis, N., Acampora, D., Kurtsdotter, I., Yoshitake, T., Kehr, J., Joodmardi, E., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.016 · Cited by 143 · see citing works
Identification of neurodegenerative factors using translatome–regulatory network analysis
Brichta, L., Shin, W., Jackson-Lewis, V., Blesa, J., Yap, E.-L., Walker, Z., Zhang, J., Roussarie, J.-P., Alvarez, M. J., Califano, A., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4070 · Cited by 118 · see citing works
Development, wiring and function of dopamine neuron subtypes
Garritsen, O., van Battum, E. Y., Grossouw, L. M., & Pasterkamp, R. J. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00669-3 · Cited by 128 · see citing works
Di Salvio, M., Di Giovannantonio, L. G., Acampora, D., Prosperi, R., Omodei, D., Prakash, N., Wurst, W., & Simeone, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2661 · Cited by 118 · see citing works
Montgomery, S. L., Mastrangelo, M. A., Habib, D., Narrow, W. C., Knowlden, S. A., Wright, T. W., & Bowers, W. J. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2011.07.001 · Cited by 96 · see citing works
Endonuclease G mediates α‐synuclein cytotoxicity during Parkinson's disease
Büttner, S., Habernig, L., Broeskamp, F., Ruli, D., Vögtle, F. N., Vlachos, M., Macchi, F., Küttner, V., Carmona‐Gutierrez, D., Eisenberg, T., et al. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.228 · Cited by 87 · see citing works
Kramer, D. J., Risso, D., Kosillo, P., Ngai, J., & Bateup, H. S. (2018) · eNeuro · doi:10.1523/eneuro.0152-18.2018 · Cited by 70 · see citing works
Vulnerability of mesostriatal dopaminergic neurons in Parkinson’s disease
González-Hernández, T. (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00140 · Cited by 65 · see citing works
Viereckel, T., Dumas, S., Smith-Anttila, C. J. A., Vlcek, B., Bimpisidis, Z., Lagerström, M. C., Konradsson-Geuken, Å., & Wallén-Mackenzie, Å. (2016) · Scientific Reports · doi:10.1038/srep35203 · Cited by 45 · see citing works
Khan, S., Stott, S. R. W., Chabrat, A., Truckenbrodt, A. M., Spencer-Dene, B., Nave, K.-A., Guillemot, F., Levesque, M., & Ang, S.-L. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2414-16.2016 · Cited by 37 · see citing works
Bimpisidis, Z., König, N., Stagkourakis, S., Zell, V., Vlcek, B., Dumas, S., Giros, B., Broberger, C., Hnasko, T. S., & Wallén-Mackenzie, Å. (2019) · eNeuro · doi:10.1523/eneuro.0066-19.2019 · Cited by 36 · see citing works
Evolutionary development of neural systems in vertebrates and beyond
O’Connell, L. A. (2013) · Journal of Neurogenetics · doi:10.3109/01677063.2013.789511 · Cited by 17 · see citing works
- Authors
- Chung, C. Y., Seo, H., Sonntag, K. C., Brooks, A., Lin, L., & Isacson, O.
- Affiliations
- Harvard University (US)
- University of Rochester Medicine (US)
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-05-11
- Volume
- 14
- Issue
- 13
- Pages
- 1709-1725
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- PMC
- PMC2674782
- OpenAlex
- W2158662449
- Cited by
- 361
- References
- 94
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 13 · 2023: 17 · 2022: 14 · 2021: 10 · 2020: 17 · 2019: 21 · 2018: 11 · 2017: 23 · 2016: 16 · 2015: 17 · 2014: 24 · 2013: 14 · 2012: 19
- FWCI
- 12.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Molecular Genetics (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (P50NS039793)
- Medical Research and Materiel Command
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- midbrain dopaminergic neurons, Parkinson's disease, cell type-specific gene expression, MPP+ neurotoxicity, neuroprotection, GIRK2, insulin-like growth factor I, GRP, calcitonin gene-related peptide, PACAP, alpha-synuclein overexpression, PC12 cells, ventral mesencephalon, neuronal vulnerability
- MeSH terms
- Animals, Dopamine, Gene Expression Regulation, Herbicides, Mesencephalon, Neurons, Parkinson Disease, 1-Methyl-4-phenylpyridinium, PC12 Cells, MPTP Poisoning, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review