The DOI matches its Crossref record; 58 of the 59 references it cites were found in a registry or an index.
A Translational Profiling Approach for the Molecular Characterization of CNS Cell Types
Open accessAbstract
The cellular heterogeneity of the brain confounds efforts to elucidate the biological properties of distinct neuronal populations. Using bacterial artificial chromosome (BAC) transgenic mice that express EGFP-tagged ribosomal protein L10a in defined cell populations, we have developed a methodology for affinity purification of polysomal mRNAs from genetically defined cell populations in the brain. The utility of this approach is illustrated by the comparative analysis of four types of neurons, revealing hundreds of genes that distinguish these four cell populations. We find that even two morphologically indistinguishable, intermixed subclasses of medium spiny neurons display vastly different translational profiles and present examples of the physiological significance of such differences. This genetically targeted translating ribosome affinity purification (TRAP) methodology is a generalizable method useful for the identification of molecular changes in any genetically defined cell type in response to genetic alterations, disease, or pharmacological perturbations.
Overview
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
Verification
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Expression of markers associated with canonical SPNs suggests eSPNs have been molecularly “camouflaged,” including in studies using mice that have employed Drd1 and Adora2a driven–transgenes to label and manipulate dSPNs or iSPNs (Heiman et al., 2008; Kozorovitskiy et al., 2012; Kravitz et al., 2012).”
From Molecular diversity and specializations among the cells of the adult mouse brain (2018) · cites this paper as Heiman et al., 2008
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Crossing these mice to microglia-specific Cre mice allows for the isolation of ribosome-associated mRNAs in a cell-type-specific fashion using eGFP-based immunoaffinity purification28,91,93.”
From Lymphoid gene expression supports neuroprotective microglia function (2025) · cites this paper as [91]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“overexpression of an epitope-tagged ribosomal protein (referred to as ‘TRAP’ or ‘Ribo-tag’ methods) under the control of one such cell-type-specific promoter allows purification by immunoprecipitation of the transcripts bound by the polyribosome in the desired cells58”
From Decoding neuroproteomics: integrating the genome, translatome and functional anatomy (2014) · cites this paper as [58]
The cited source says what the claim attributes to it.
In the citing paper
“The TRAP approach91,92 relies on the genetic labelling of the ribosomal protein L10a with the enhanced green fluorescent protein (eGFP) using Eef1a1LSL.eGFPL10a/+ mice60.”
From Lymphoid gene expression supports neuroprotective microglia function (2025) · cites this paper as [91]
In the citing paper
“These neurons are defined by their transcriptional profiles, including dopamine receptor 1 (D1) vs. dopamine receptor 2 (D2) expression, substance P and enkephalin, and other enriched genes (16–18).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [18]
In the citing paper
“These fractions harbor complexes containing multiple ribosomes (Figure 7A) identified as such by immuno-EM on the same gradient fraction prepared from a transgenic mouse expressing the tagged ribosomal protein EGFP-rpL10a (Heiman et al., 2008; Doyle et al., 2008) (Figure 7B).”
From FMRP Stalls Ribosomal Translocation on mRNAs Linked to Synaptic Function and Autism (2011) · cites this paper as Heiman et al., 2008
In the citing paper
“No statistical methods were used to pre-determine sample sizes but our sample sizes are similar to those reported in previous publications19,31,95,99,108.”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [19]
In the citing paper
“The bacTRAP technology enabled us to assay AD-relevant neuronal cell types with genome-wide coverage, measure transcripts ex vivo (as opposed to postmortem), and specifically capture actively translated (rather than all transcribed) genes.”
From Selective Neuronal Vulnerability in Alzheimer’s Disease: A Network-Based Analysis (2020) · cites this paper as Heiman et al., 2008
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
Edgar, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.207 · Cited by 13,288
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572
Di Chiara, G., & Imperato, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.14.5274 · Cited by 4,733
Cocaine Receptors on Dopamine Transporters Are Related to Self-Administration of Cocaine
Ritz, M. C., Lamb, R. J., Goldberg, S. R., & Kuhar, M. J. (1987) · Science · doi:10.1126/science.2820058 · Cited by 2,180
A gene expression atlas of the central nervous system based on bacterial artificial chromosomes
Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., Nowak, N. J., Joyner, A., Leblanc, G., Hatten, M. E., et al. (2003) · Nature · doi:10.1038/nature02033 · Cited by 2,108
Self-citationThe neostriatal mosaic: multiple levels of compartmental organization
Gerfen, C. R. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90355-c · Cited by 1,471
Homer: a protein that selectively binds metabotropic glutamate receptors
Brakeman, P., Lanahan, A. A., O’Brien, R., Roche, K. W., Barnes, C. A., Huganir, R. L., & Worley, P. F. (1997) · Nature · doi:10.1038/386284a0 · Cited by 1,115
The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia
Gerfen, C. R. (1992) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.15.030192.001441 · Cited by 1,004
Application of a translational profiling approach for the comparative analysis of CNS cell types
Doyle, J. P., Dougherty, J. D., Heiman, M., Schmidt, E. F., Stevens, T. R., Ma, G., Bupp, S., Shrestha, P., Shah, R. D., Doughty, M. L., et al. (2008) · Cell · doi:10.1016/j.cell.2008.10.029 · Cited by 912
Self-citationDay, M., Wang, Z., Ding, J., An, X., Ingham, C. A., Shering, A. F., Wokosin, D., Ilijic, E., Sun, Z., Sampson, A. R., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1632 · Cited by 745
Self-citationDOUGLASS, J. O., McKinzie, A. A., & Couceyro, P. R. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02471.1995 · Cited by 665
Regulation of gene expression and cocaine reward by CREB and ΔFosB
McClung, C. A., & Nestler, E. J. (2003) · Nature Neuroscience · doi:10.1038/nn1143 · Cited by 625
Valjent, E., Pascoli, V., Svenningsson, P., Paul, S., Enslen, H., Corvol, J.-C., Stipanovich, A., Caboche, J., Lombroso, P. J., Nairn, A. C., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408305102 · Cited by 614
Self-citationCharacterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain
Ferland, R. J., Cherry, T. J., Preware, P. O., Morrisey, E. E., & Walsh, C. A. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10654 · Cited by 486
Hope, B. T., Kosofsky, B. E., Hyman, S. E., & Nestler, E. J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5764 · Cited by 474
Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans
Roy, P. J., Stuart, J. M., Lund, J., & Kim, S. K. (2002) · Nature · doi:10.1038/nature01012 · Cited by 439
GABAergic microcircuits in the neostriatum
Tepper, J. M., Koós, T. Z., & Wilson, C. J. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.08.007 · Cited by 436
Gold, S. J., Ni, Y. G., Dohlman, H. G., & Nestler, E. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-20-08024.1997 · Cited by 434
A database for post-genome analysis
Kanehisa, M. I. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01223-7 · Cited by 420
FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains
Lobo, M. K., Karsten, S. L., Gray, M., Geschwind, D. H., & Yang, X. W. (2006) · Nature Neuroscience · doi:10.1038/nn1654 · Cited by 411
Lee, K.-W., Kim, Y. D., Kim, A. M., Helmin, K. A., Nairn, A. C., & Greengard, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511244103 · Cited by 369
Self-citationKilman, V., van Rossum, M. C. W., & Turrigiano, G. G. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01328.2002 · Cited by 362
A Rap guanine nucleotide exchange factor enriched highly in the basal ganglia
Kawasaki, H., Springett, G. M., Toki, S., Canales, J. J., Harlan, P. C., Blumenstiel, J. P., Chen, E. J., Bany, I. A., Mochizuki, N., Ashbacher, A., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13278 · Cited by 353
Comparison of IPSCs Evoked by Spiny and Fast-Spiking Neurons in the Neostriatum
Koós, T. Z., Tepper, J. M., & Wilson, C. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2163-04.2004 · Cited by 309
Walaas, S. I., & Greengard, P. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-01-00084.1984 · Cited by 301
Self-citationPsychomotor stimulants and neuronal plasticity
Wolf, M. E., Sun, X., Mangiavacchi, S., & Chao, S. Z. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.006 · Cited by 288
Flores‐Hernández, J., Cepeda, C., Hernández, E., Calvert, C. R., Jokel, E. S., Fienberg, A. A., Greengard, P., & Levine, M. S. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00361.2002 · Cited by 270
Self-citationIsolation and characterization of a novel cardiac adenylylcyclase cDNA.
Ishikawa, Y., Katsushika, S., Chen, L., Halnon, N. J., Kawabe, J.-I., & Homcy, C. J. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42247-8 · Cited by 265
Hervé, D., Lévi‐Strauss, M., Marey‐Semper, I., Verney, C., Tassin, J., Glowinski, J., & Girault, J. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02237.1993 · Cited by 264
Immunopurification of Polyribosomal Complexes of Arabidopsis for Global Analysis of Gene Expression
Zanetti, M. E., Chang, I., Gong, F., Galbraith, D. W., & Bailey-Serres, J. N. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.059477 · Cited by 251
Differential expression of retinoid receptors in the adult mouse central nervous system
Krężel, W., Kastner, P., & Chambon, P. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00342-x · Cited by 238
Svenningsson, P., Hall, H., Sedvall, G., & Fredholm, B. B. (1997) · Synapse · doi:10.1002/(sici)1098-2396(199712)27:4 · Cited by 230
Magdaleno, S. M., Jensen, P., Brumwell, C. L., Seal, A., Lehman, K., Asbury, A., Cheung, T., Cornelius, T., Batten, D., Eden, C., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040086 · Cited by 222
Koninck, Y. D., & Módy, I. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.4.1318 · Cited by 220
Cloning and expression of an adenylyl cyclase localized to the corpus striatum
Glatt, C. E., & Snyder, S. H. (1993) · Nature · doi:10.1038/361536a0 · Cited by 211
Striatum‐ and testis‐specific phosphodiesterase PDE10A
Fujishige, K., Kotera, J., & Omori, K. (1999) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1999.00963.x · Cited by 188
Dependence of GABAergic Synaptic Areas on the Interneuron Type and Target Size
Kubota, Y., & Kawaguchi, Y. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00375.2000 · Cited by 170
Yuferov, V., Kroslak, T., Laforge, K. S., Zhou, Y., Ho, A., & Kreek, M. J. (2003) · Synapse · doi:10.1002/syn.10198 · Cited by 143
Oh, J. D., Woolf, N. J., Roghani, A., Edwards, R. H., & Butcher, L. L. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90031-v · Cited by 141
One-step affinity purification of the yeast ribosome and its associated proteins and mRNAs
Inada, T., Winstall, É., Tarun, S. Z., Yates, J. R., SCHIELTZ, D., & Sachs, A. B. (2002) · RNA · doi:10.1017/s1355838202026018 · Cited by 137
Castets, F., Bartoli, M., Barnier, J. V., Baillat, G., Salin, P., Moqrich, A., Bourgeois, J. P., Denizot, F., Rougon, G., Calothy, G., et al. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.134.4.1051 · Cited by 129
Nishi, A., Snyder, G. L., Nairn, A. C., & Greengard, P. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0722015.x · Cited by 120
Self-citationLombroso, P., Naegele, J. R., Sharma, E., & Lerner, M. R. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-07-03064.1993 · Cited by 119
Texture of the Nervous System of Man and the Vertebrates
y Cajal, S. R. (2002) · Springer eBooks · doi:10.1007/978-3-7091-6730-4 · Cited by 114
Oberdick, J., Levinthal, F., & Levinthal, C. (1988) · Neuron · doi:10.1016/0896-6273(88)90186-9 · Cited by 107
Genetic control of instrumental conditioning by striatopallidal neuron–specific S1P receptor Gpr6
Lobo, M. K., Cui, Y., Ostlund, S. B., Balleine, B. W., & Yang, X. W. (2007) · Nature Neuroscience · doi:10.1038/nn1987 · Cited by 100
A Novel G-Protein-Coupled Receptor Gene Expressed in Striatum
Mizushima, K., Miyamoto, Y., Tsukahara, F., Hirai, M., Sakaki, Y., & Ito, T. (2000) · Genomics · doi:10.1006/geno.2000.6340 · Cited by 95
Kunitomo, H., Uesugi, H., Kohara, Y., & Iino, Y. (2005) · Genome biology · doi:10.1186/gb-2005-6-2-r17 · Cited by 88
Ignatov, A., Lintzel, J., Kreienkamp, H., & Schaller, H. C. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.10.006 · Cited by 70
Ouimet, C., Hemmings, H., & Greengard, P. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-03-00865.1989 · Cited by 70
Self-citationMolecular cloning of DNA encoding a calmodulin-dependent phosphodiesterase enriched in striatum.
Polli, J. W., & Kincaid, R. L. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.22.11079 · Cited by 64
Chang, C.-W., Tsai, C.-W., Wang, H., Tsai, H., Chen, H.-Y., Tsai, T., Takahashi, H., Li, H.-Y., Fann, M., Yang, C.-W., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308645100 · Cited by 64
Girault, J., Horiuchi, A., Gustafson, E., Rosen, N. L., & Greengard, P. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01124.1990 · Cited by 63
Self-citationWatson, J. B., Coulter, P. M., Margulies, J. E., de Lecea, L., Danielson, P. E., Erlander, M. G., & Sutcliffe, J. G. (1994) · Journal of Neuroscience Research · doi:10.1002/jnr.490390113 · Cited by 57
Enhanced Sensitivity to Benzodiazepines in Active Cocaine-Abusing Subjects: A PET Study
Volkow, N. D., Wang, G., Fowler, J. S., HITZEMANN, R. J., Gatley, S. J., Dewey, S. L., & Pappas, N. R. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.2.200 · Cited by 55
Texture of the Nervous System of Man and the Vertebrates
y Cajal, S. R. (1999) · Springer eBooks · doi:10.1007/978-3-7091-6435-8 · Cited by 50
Cited by
Sorted by citations
Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling
Ingolia, N. T., Ghaemmaghami, S., Newman, J. R. S., & Weissman, J. S. (2009) · Science · doi:10.1126/science.1168978 · Cited by 3,853
The physiology, signaling, and pharmacology of dopamine receptors
Beaulieu, J.-M., & Gainetdinov, R. R. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.002642 · Cited by 2,763
The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain
Kriaucionis, S., & Heintz, N. (2009) · Science · doi:10.1126/science.1169786 · Cited by 2,700
Self-citationAdult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions
Ming, G.-L., & Song, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.001 · Cited by 2,651
Genomic analysis of reactive astrogliosis
Zamanian, J. L., Xu, L., Foo, L. C., Nouri, N., Zhou, L., Giffard, R. G., & Barres, B. A. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.6221-11.2012 · Cited by 2,404
Metadata
- Authors
- Heiman, M., Schaefer, A., Gong, S., Peterson, J. D., Day, M., Ramsey, K. E., Suárez-Fariñas, M., Schwarz, C., Stephan, D. A., Surmeier, D. J., Greengard, P., & Heintz, N.
- Affiliations
- Rockefeller University (US)
- Northwestern University (US)
- Translational Genomics Research Institute (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Heintz, Nathaniel
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2008-11
- Volume
- 135
- Issue
- 4
- Pages
- 738-748
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2696821
- OpenAlex
- W2150626351
- Cited by
- 1,134
- References
- 59
- Citations by year
- 2026: 28 · 2025: 61 · 2024: 57 · 2023: 65 · 2022: 55 · 2021: 60 · 2020: 79 · 2019: 76 · 2018: 93 · 2017: 76 · 2016: 70 · 2015: 70 · 2014: 97 · 2013: 70 · 2012: 55
- FWCI
- 16.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1755 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (1f32da021487-01)
- National Institute on Aging (AG09464, P01AG009464)
- National Institute of Mental Health (MH-074866, P50MH074866)
- National Institute on Drug Abuse (5F32DA021487, DA10044, P01DA010044, F32 DA021487)
- National Institute of Neurological Disorders and Stroke (NS 34696, R01NS034696, R37NS034696)
- National Center for Research Resources (UL1RR024143)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- translating ribosome affinity purification, polysomal mRNA, neuronal cell types, medium spiny neurons, translational profiling, BAC transgenic mice, cell type-specific gene expression
- MeSH terms
- Animals, Brain, Central Nervous System, Cocaine, Genetic Techniques, Immunohistochemistry, Mice, Transgenic, Models, Biological, Neurons, Ribosomes, Protein Biosynthesis, Dopamine Uptake Inhibitors, Chromosomes, Artificial, Bacterial, Green Fluorescent Proteins, Mice
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