Cell type–specific mRNA purification by translating ribosome affinity purification (TRAP)
Open accessAbstract
Cellular diversity and architectural complexity create barriers to understanding the function of the mammalian CNS at a molecular level. To address this problem, we have recently developed a methodology that provides the ability to profile the entire translated mRNA complement of any genetically defined cell population. This methodology, which we termed translating ribosome affinity purification, or TRAP, combines cell type-specific transgene expression with affinity purification of translating ribosomes. TRAP can be used to study the cell type-specific mRNA profiles of any genetically defined cell type, and it has been used in organisms ranging from Drosophila melanogaster to mice and human cultured cells. Unlike other methodologies that rely on microdissection, cell panning or cell sorting, the TRAP methodology bypasses the need for tissue fixation or single-cell suspensions (and the potential artifacts that these treatments introduce) and reports on mRNAs in the entire cell body. This protocol provides a step-by-step guide to implement the TRAP methodology, which takes 2 d to complete once all materials are in hand.
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The TRAP approach relies on the genetic labelling of the ribosomal protein L10a with the enhanced green fluorescent protein (eGFP) using Eef1a1LSL.eGFPL10a/+ mice.
“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 [92]
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A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · Journal of Pharmacology and Pharmacotherapeutics · doi:10.4103/0976-500x.72351 · Cited by 6,277 · see citing works
Cahoy, J. D., Emery, B., Kaushal, A., Foo, L. C., Zamanian, J. L., Christopherson, K. S., Xing, Y., Lubischer, J. L., Krieg, P. A., Krupenko, S. A., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4178-07.2008 · Cited by 3,129 · see citing works
Shizuya, H., Birren, B. W., Kim, U. J., Mancino, V., Slepak, T. I., Tachiiri, Y., & Simon, M. I. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.18.8794 · Cited by 1,672 · see citing works
Neuronal Subtype-Specific Genes that Control Corticospinal Motor Neuron Development In Vivo
Arlotta, P., Molyneaux, B. J., Chen, J., Inoue, J., Kominami, R., & Macklis, J. D. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.036 · Cited by 1,157 · see citing works
A translational profiling approach for the molecular characterization of CNS cell types
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., et al. (2008) · Cell · doi:10.1016/j.cell.2008.10.028 · Cited by 1,134 · see citing works
Self-citationGong, S., Doughty, M., Harbaugh, C. R., Cummins, A., Hatten, M. E., Heintz, N., & Gerfen, C. R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2707-07.2007 · Cited by 977 · see citing works
Self-citationMeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system
Mellén, M., Ayata, P., Dewell, S., Kriaucionis, S., & Heintz, N. (2012) · Cell · doi:10.1016/j.cell.2012.11.022 · Cited by 943 · see citing works
Self-citationApplication 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 · see citing works
Self-citationCoordinated Expression of Dopamine Receptors in Neostriatal Medium Spiny Neurons
Surmeier, D. J., Song, W., & Yan, Z. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-20-06579.1996 · Cited by 747 · see citing works
Gene expression profiles of laser-captured adjacent neuronal subtypes
Luo, L., Salunga, R. C., Guo, H., Bittner, A., Joy, K. C., Galindo, J. E., Xiao, H., Rogers, K. E., Wan, J. S., Jackson, M. R., et al. (1999) · Nature Medicine · doi:10.1038/4806 · Cited by 691 · see citing works
Molecular taxonomy of major neuronal classes in the adult mouse forebrain
Sugino, K., Hempel, C. M., Miller, M. N., Hattox, A. M., Shapiro, P., Wu, C., Huang, Z. J., & Nelson, S. B. (2006) · Nature Neuroscience · doi:10.1038/nn1618 · Cited by 521 · see citing works
Barres, B. A., Silverstein, B. E., Corey, D. P., & Chun, L. L. Y. (1988) · Neuron · doi:10.1016/0896-6273(88)90127-4 · Cited by 520 · see citing works
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 · see citing works
MeCP2 binds to 5hmc enriched within active genes and accessible chromatin in the nervous system
Mellén, M., Ayata, P., Dewell, S. B., Kriaučionis, S., & Heintz, N. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-s1-p52 · Cited by 345 · see citing works
Self-citationBac to the future: The use of bac transgenic mice for neuroscience research
Heintz, N. (2001) · Nature reviews. Neuroscience · doi:10.1038/35104049 · Cited by 333 · see citing works
Self-citationOkaty, B. W., Miller, M. N., Sugino, K., Hempel, C. M., & Nelson, S. B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0105-09.2009 · Cited by 309 · see citing works
Toledo-Rodriguez, M. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh092 · Cited by 241 · see citing works
Mustroph, A., Juntawong, P., & Bailey-Serres, J. N. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-563-7_6 · Cited by 171 · see citing works
A Versatile Method for Cell-Specific Profiling of Translated mRNAs in Drosophila
Thomas‐Wilson, A., Lee, P.-J., Dalton, J. E., Nomie, K. J., Stoica, L., Costa‐Mattioli, M., Chang, P. L., Nuzhdin, S. V., Arbeitman, M. N., & Dierick, H. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040276 · Cited by 129 · see citing works
SYNTHESIS OF NASCENT PROTEIN BY RIBOSOMES IN ESCHERICHIA COLI
McQuillen, K., Roberts, R. B., & Britten, R. J. (1959) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.45.9.1437 · Cited by 127 · see citing works
A manual method for the purification of fluorescently labeled neurons from the mammalian brain
Hempel, C. M., Sugino, K., & Nelson, S. B. (2007) · Nature Protocols · doi:10.1038/nprot.2007.416 · Cited by 124 · see citing works
Zhou, P., Zhang, Y., Ma, Q., Gu, F., Day, D. S., He, A., Zhou, B., Li, J., Stevens, S. M., Romo, D., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304124110 · Cited by 116 · see citing works
Profiling of Glucose-Sensing Neurons Reveals that GHRH Neurons Are Activated by Hypoglycemia
Stanley, S., Domingos, A. I., Kelly, L., Garfield, A., Damanpour, S., Heisler, L., & Friedman, J. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.09.002 · Cited by 110 · see citing works
Molecular adaptations of striatal spiny projection neurons during levodopa-induced dyskinesia
Heiman, M., Heilbut, A. M., Francardo, V., Kulicke, R., Fenster, R. J., Kolaczyk, E. D., Mesirov, J. P., Surmeier, D. J., Cenci, M. A., & Greengard, P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1401819111 · Cited by 106 · see citing works
Self-citationTomomura, M., Rice, D. S., Morgan, J. I., & Yuzaki, M. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01624.x · Cited by 86 · see citing works
The development and applications of the bacterial artificial chromosome cloning system.
Shizuya, H., & Kouros‐Mehr, H. (2001) · The Keio Journal of Medicine · doi:10.2302/kjm.50.26 · Cited by 81 · see citing works
Zomzely, C. E., Roberts, S., Gruber, C. P., & Brown, D. M. (1968) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)91962-9 · Cited by 70 · see citing works
Rapid bacterial artificial chromosome modification for large-scale mouse transgenesis
Gong, S., Kus, L., & Heintz, N. (2010) · Nature Protocols · doi:10.1038/nprot.2010.131 · Cited by 65 · see citing works
Self-citationReversal of RT-PCR Inhibition Observed in Heparinized Clinical Specimens
Jung, R., Lübcke, C., Wagener, C., & Neumaier, M. (1997) · BioTechniques · doi:10.2144/97231bm03 · Cited by 60 · see citing works
Evaluation of TRAP-sequencing technology with a versatile conditional mouse model
Hupe, M., Li, M. X., Gillner, K. G., Adams, R. H., & Stenman, J. M. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt995 · Cited by 54 · see citing works
Analysis and isolation of embryonic mammalian neurons by fluorescence- activated cell sorting
John, P. A. S., Kell, W., Mazzetta, J., Lange, G. D., & Barker, J. L. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-05-01492.1986 · Cited by 54 · see citing works
Development of translating ribosome affinity purification for zebrafish
Tryon, R. C., Pisat, N., Johnson, S. L., & Dougherty, J. D. (2012) · genesis · doi:10.1002/dvg.22363 · Cited by 40 · see citing works
Wang, S., Roy, N. S., Benraiss, A., & Goldman, S. A. (2000) · Developmental Neuroscience · doi:10.1159/000017437 · Cited by 39 · see citing works
Yao, F., Yu, F., Gong, L., Taube, D., Rao, D. D., & MacKenzie, R. G. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.09.023 · Cited by 36 · see citing works
FACS‐array gene expression analysis during early development of mouse telencephalic interneurons
Marsh, E. D., Minarcik, J., Campbell, K., Brooks‐Kayal, A. R., & Golden, J. A. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20602 · Cited by 34 · see citing works
Cell type–specific translational profiling in the Xenopus laevis retina
Watson, F. L., Mills, E. A., Wang, X., Guo, C., Chen, D. F., & Marsh-Armstrong, N. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23880 · Cited by 32 · see citing works
Neuwelt, E. A., Boguski, M. S., Frank, J. J., Procter-Appich, K., & Levy, C. C. (1978) · PubMed · Cited by 31 · see citing works
Efficacy of RNase inhibitors during brain polysome isolation
Gauthier, D., & Murthy, M. R. V. (1987) · Neurochemical Research · doi:10.1007/bf00993241 · Cited by 10 · see citing works
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Research works printed but not linked: 2
- Heiman M A translational profiling approach for the molecular characterization of CNS cell types Cell 135 738 748 10.1016/j.cell.2008.10.028 2008 19013281 PMC2696821 · DOI · Paper page
- Heiman M Molecular Adaptations of Striatal Spiny Projection Neurons During Levodopa-Induced Dyskinesia Proceedings of the National Academy of Sciences of the United States of America In Press 2014 PMC3970487 24599591
Cited by
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Normal aging induces A1-like astrocyte reactivity
Clarke, L. E., Liddelow, S. A., Chakraborty, C., Münch, A. E., Heiman, M., & Barres, B. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800165115 · Cited by 1,237 · see citing works
“RNAwas collected from hippocampi, striata, and cortex of Aldh1l1-eGFP-L10a mice based on published protocols (21, 22).”
MethodInfluentialSelf-citationSano, T., Huang, W., Hall, J. A., Yang, Y., Chen, A., Gavzy, S. J., Lee, J.-Y., Ziel, J. W., Miraldi, E. R., Domingos, A. I., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.061 · Cited by 547 · see citing works
“(legend continued on next page) 4 Cell 163, 1–13, October 8, 2015 ª2015 Elsevier Inc. (TRAP), which was developed to identify cell type-specific transcripts in tissues containing heterogeneous cell populations (Heiman et al., 2014).”
Disruption of mitochondrial complex I induces progressive parkinsonism
González‐Rodríguez, P., Zampese, E., Stout, K. A., Guzmán, J. N., Ilijić, E., Yang, B., Tkatch, T., Stavarache, M. A., Wokosin, D. L., Gao, L., et al. (2021) · Nature · doi:10.1038/s41586-021-04059-0 · Cited by 553 · see citing works
Ribosome profiling reveals the what, when, where and how of protein synthesis
Brar, G. A., & Weissman, J. S. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm4069 · Cited by 534 · see citing works
Mayr, C. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a034728 · Cited by 519 · see citing works
“…adds a tag to a ribosomal protein of the large ribosomal subunit in a cell type–specific manner by using either bac transgenics or the Cre-lox system in mice (Doyle et al. 2008; Heiman et al. 2014; Hupe et al. 2014), but can be applied to worms, flies, plants, and yeast (King and Gerber 2016).”
MethodRaj, B., & Blencowe, B. J. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.004 · Cited by 475 · see citing works
“…which mice are genetically engineered to produce a fluorescently tagged ribosomal protein in specialized cell types of interest (Doyle et al., 2008; Heiman et al., 2014; 2008), can additionally be used to determine the translation profile of individual cell types and detect cell-specific AS…”
BackgroundEpigenetic regulation of brain region-specific microglia clearance activity
Ayata, P., Badimon, A., Strasburger, H. J., Duff, M. K., Montgomery, S. E., Loh, Y.-H. E., Ebert, A., Pimenova, A. A., Ramirez, B. R., Chan, A. T., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0192-3 · Cited by 460 · see citing works
Brain circuit dysfunction in post-traumatic stress disorder: from mouse to man
Fenster, R. J., Lebois, L. A. M., Ressler, K. J., & Suh, J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0039-7 · Cited by 456 · see citing works
Self-citationMicrobiota modulate sympathetic neurons via a gut–brain circuit
Muller, P. A., Schneeberger, M., Matheis, F., Wang, P., Kerner, Z. J., Ilanges, A., Pellegrino, K., del Mármol, J. I., Castro, T. B. R., Furuichi, M., et al. (2020) · Nature · doi:10.1038/s41586-020-2474-7 · Cited by 449 · see citing works
Treatment resistant depression: A multi-scale, systems biology approach
Akil, H., Gordon, J. A., Hen, R., Javitch, J. A., Mayberg, H. S., McEwen, B. S., Meaney, M. J., & Nestler, E. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.08.019 · Cited by 443 · see citing works
“It is also now possible to use a variety of genetic reporter mice to study changes in gene expression in individual cell populations (e.g., Heiman et al., 2014).”
BackgroundWarm-Sensitive Neurons that Control Body Temperature
Tan, C. L., Cooke, E. K., Leib, D. E., Lin, Y.-C., Daly, G. E., Zimmerman, C. A., & Knight, Z. A. (2016) · Cell · doi:10.1016/j.cell.2016.08.028 · Cited by 402 · see citing works
The innate immunity protein IFITM3 modulates γ-secretase in Alzheimer’s disease
Hur, J.-Y., Frost, G. R., Wu, X., Crump, C., Pan, S. J., Wong, E., Barros, M., Li, T., Nie, P., Zhai, Y., et al. (2020) · Nature · doi:10.1038/s41586-020-2681-2 · Cited by 382 · see citing works
Self-citationTechnological Developments in lncRNA Biology
Jathar, S., Kumar, V., Srivastava, J. P., & Tripathi, V. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5203-3_10 · Cited by 348 · see citing works
Lee, H., Fenster, R. J., Pineda, S. S., Gibbs, W. S., Mohammadi, S., Davila-Velderrain, J., Garcia, F. J., Therrien, M., Novis, H. S., Gao, F., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.021 · Cited by 279 · see citing works
Self-citationAdrenergic Signaling in Muscularis Macrophages Limits Infection-Induced Neuronal Loss
Matheis, F., Muller, P. A., Graves, C. L., Gabanyi, I., Kerner, Z. J., Costa-Borges, D., Ahrends, T., Rosenstiel, P. C., & Mucida, D. (2020) · Cell · doi:10.1016/j.cell.2019.12.002 · Cited by 303 · see citing works
Er, E. E., Valiente, M., Ganesh, K., Zou, Y., Agrawal, S., Hu, J. Y., Griscom, B., Rosenblum, M. K., Boire, A. A., Brogi, E., et al. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0138-8 · Cited by 290 · see citing works
Codon-specific translation reprogramming promotes resistance to targeted therapy
Rapino, F., Delaunay, S., Rambow, F., Zhou, Z., Tharun, L., De Tullio, P., Sin, O., Shostak, K., Schmitz, S., Piepers, J., et al. (2018) · Nature · doi:10.1038/s41586-018-0243-7 · Cited by 271 · see citing works
Adipose tissue retains an epigenetic memory of obesity after weight loss
Hinte, L. C., Castellano‐Castillo, D., Ghosh, A., Melrose, K., Gasser, E., Noé, F., Massier, L., Dong, H., Sun, W., Hoffmann, A., et al. (2024) · Nature · doi:10.1038/s41586-024-08165-7 · Cited by 298 · see citing works
Injured adult neurons regress to an embryonic transcriptional growth state
Poplawski, G. H. D., Kawaguchi, R., Van Niekerk, E., Lu, P., Mehta, N., Canete, P., Lie, R., Dragatsis, I., Meves, J. M., Zheng, B., et al. (2020) · Nature · doi:10.1038/s41586-020-2200-5 · Cited by 247 · see citing works
Targeted Intron Retention and Excision for Rapid Gene Regulation in Response to Neuronal Activity
Mauger, O., Lemoine, F., & Scheiffele, P. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.032 · Cited by 228 · see citing works
Jiwaji, Z., Tiwari, S. S., Avilés-Reyes, R. X., Hooley, M., Hampton, D., Torvell, M., Johnson, D. A., McQueen, J., Baxter, P., Sabari-Sankar, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27702-w · Cited by 223 · see citing works
Jüttner, J., Szabo, A., Gross-Scherf, B., Morikawa, R. K., Rompani, S. B., Hantz, P., Szikra, T., Esposti, F., Cowan, C. S., Bharioke, A., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0431-2 · Cited by 218 · see citing works
“39 cycloheximide, RNasin and SUPERase-In RNase inhibitors, and Complete-EDTAfree protease inhibitors and then cleared by two-step centrifugation to isolate the polysome-containing cytoplasmic supernatant, as described previously (Heiman et al., 2014).”
MethodCSF‐1 Controls Cerebellar Microglia and Is Required for Motor Function and Social Interaction
Kana, V., Desland, F. A., Casanova-Acebes, M., Ayata, P., Badimon, A., Nabel, E., Yamamuro, K., Sneeboer, M., Tan, I.-L., Flanigan, M. E., et al. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20182037 · Cited by 220 · see citing works
Analysis of translation using polysome profiling
Chassé, H., Boulben, S., Costache, V., Cormier, P., & Morales, J. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw907 · Cited by 202 · see citing works
“Tagged ribosomes are affinity-purified and associated mRNAs are identified by microarray or deep-sequencing (10).”
BackgroundTranslation in astrocyte distal processes sets molecular heterogeneity at the gliovascular interface
Boulay, A. C., Saubaméa, B., Adam, N., Chasseigneaux, S., Mazaré, N., Gilbert, A., Bahin, M., Bastianelli, L., Blugeon, C., Perrin, S., et al. (2017) · Cell Discovery · doi:10.1038/celldisc.2017.5 · Cited by 179 · see citing works
Zawistowski, J. S., Bevill, S. M., Goulet, D. R., Stuhlmiller, T. J., Beltran, A. S., Olivares-Quintero, J. F., Singh, D., Sciaky, N., Parker, J. S., Rashid, N. U., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0653 · Cited by 180 · see citing works
“Tumors were processed as described (56) with minor modifications.”
MethodGraves, S. M., Xie, Z., Stout, K. A., Zampese, E., Burbulla, L. F., Shih, J. C., Kondapalli, J., Patriarchi, T., Tian, L., Brichta, L., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0556-3 · Cited by 185 · see citing works
Self-citationAstrocyte-oligodendrocyte interaction regulates central nervous system regeneration
Molina-Gonzalez, I., Holloway, R. K., Jiwaji, Z., Dando, O., Kent, S. A., Emelianova, K., Lloyd, A. F., Forbes, L. H., Mahmood, A., Skripuletz, T., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39046-8 · Cited by 176 · see citing works
Immediate and deferred epigenomic signatures of in vivo neuronal activation in mouse hippocampus
Fernandez-Albert, J., Lipinski, M., Lopez-Cascales, M. T., Rowley, M. J., Martin-Gonzalez, A. M., del Blanco, B., Corces, V. G., & Barco, A. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0476-2 · Cited by 166 · see citing works
Microbiota-modulated CART <sup>+</sup> enteric neurons autonomously regulate blood glucose
Muller, P. A., Matheis, F., Schneeberger, M., Kerner, Z., Jové, V., & Mucida, D. (2020) · Science · doi:10.1126/science.abd6176 · Cited by 154 · see citing works
Astrocytes and microglia: Models and tools
Guttenplan, K. A., & Liddelow, S. A. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180200 · Cited by 156 · see citing works
A Central Extended Amygdala Circuit That Modulates Anxiety
Ahrens, S., Wu, M. V., Furlan, A., Hwang, G., Paik, R., Li, H., Penzo, M. A., Tollkühn, J., & Li, B. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0705-18.2018 · Cited by 150 · see citing works
“Both the CeA and the BNST are complex structures that contain heterogeneous neuronal populations, which likely form discrete neural circuits subserving distinct functions (Duvarci and Pare, 2014; Herry and Johansen, 2014; Stamatakis et al., 2014; Kash et al., 2015; Gungor and Paré, 2016).”
BackgroundAbernathy, D. G., Kim, W. K., McCoy, M. J., Lake, A. M., Ouwenga, R., Lee, S. W., Xing, X., Li, D., Lee, H. J., Heuckeroth, R. O., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.08.002 · Cited by 145 · see citing works
Urs, N. M., Gee, S. M., Pack, T. F., McCorvy, J. D., Evron, T., Snyder, J. C., Yang, X., Rodriguiz, R. M., Borrelli, E., Wetsel, W. C., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1614347113 · Cited by 142 · see citing works
Floriou‐Servou, A., von Ziegler, L., Stalder, L., Sturman, O., Privitera, M., Rassi, A., Cremonesi, A., Thöny, B., & Bohacek, J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.02.003 · Cited by 126 · 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
Self-citationFurlanis, E., Traunmüller, L., Fucile, G., & Scheiffele, P. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0465-5 · Cited by 136 · see citing works
PNOCARC Neurons Promote Hyperphagia and Obesity upon High-Fat-Diet Feeding
Jais, A., Paeger, L., Sotelo-Hitschfeld, T., Bremser, S., Prinzensteiner, M., Klemm, P., Mykytiuk, V., Widdershooven, P. J. M., Vesting, A. J., Grzelka, K., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.022 · Cited by 129 · see citing works
Megat, S., Ray, P. R., Moy, J. K., Lou, T., Barragán‐Iglesias, P., Li, Y., Pradhan, G., Wangzhou, A., Ahmad, A., Burton, M. D., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2661-18.2018 · Cited by 128 · see citing works
“8 using mRNAs isolated with immunoprecipitation of translating ribosomes (Heiman et al., 2014).”
MethodTranslational Control Mechanisms in Persistent Pain
Khoutorsky, A., & Price, T. J. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.11.006 · Cited by 127 · see citing works
Translatomics: The Global View of Translation
Zhao, J., Qin, B., Nikolay, R., Spahn, C. M. T., & Zhang, G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20010212 · Cited by 129 · see citing works
“This is time-consuming, costly and is not applicable to species, for which no stable transformation method has been established [27,29].”
BackgroundMethodTranslatome profiling: methods for genome-scale analysis of mRNA translation
King, H. A., & Gerber, A. P. (2014) · Briefings in Functional Genomics · doi:10.1093/bfgp/elu045 · Cited by 125 · see citing works
“[71].”
Chromatin remodeling inactivates activity genes and regulates neural coding
Yang, Y., Yamada, T., Hill, K. K., Hemberg, M., Reddy, N. C., Cho, H. Y., Guthrie, A. N., Oldenborg, A., Heiney, S. A., Ohmae, S., et al. (2016) · Science · doi:10.1126/science.aad4225 · Cited by 123 · see citing works
“mCherry-positive cerebella were selected under a stereomicroscope (Olympus SZX16) and subjected to TRAP analyses as described with modifications (25).”
MethodKorb, E., Herre, M., Zucker-Scharff, I., Gresack, J. E., Allis, C. D., & Darnell, R. B. (2017) · Cell · doi:10.1016/j.cell.2017.07.033 · Cited by 122 · see citing works
“We next examinedwhether these robust changes also occur in neurons in vivo using the bacTrap system (Heiman et al., 2014) (Figure 2D).”
Zhou, W., Pal, A. S., Hsu, A. Y.-H., Gurol, T., Zhu, X., Wirbisky-Hershberger, S. E., Freeman, J. L., Kasinski, A. L., & Deng, Q. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.058 · Cited by 117 · see citing works
“We have optimized the published protocol (Heiman et al., 2014) that no contamination from the phagocytes were detected (Figure 5H).”
MethodCo-translational assembly of mammalian nuclear multisubunit complexes
Kamenova, I., Mukherjee, P., Conic, S., Mueller, F., El-Saafin, F., Bardot, P., Garnier, J., Dembélé, D., Capponi, S., Timmers, H. T. M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09749-y · Cited by 120 · see citing works
Megat, S., Ray, P. R., Tavares‐Ferreira, D., Moy, J. K., Sankaranarayanan, I., Wangzhou, A., Lou, T. F., Barragán‐Iglesias, P., Campbell, Z. T., Dussor, G. O., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2663-18.2019 · Cited by 118 · see citing works
“A second technique is translating ribosome affinity purification (TRAP), which relies on genetic tagging of ribosomal proteins for cell-specific pulldown of translating ribosomes bound to mRNAs for RNA-seq (Doyle et al., 2008; Heiman et al., 2008, 2014).”
MethodThe bone microenvironment increases phenotypic plasticity of ER+ breast cancer cells
Bado, I. L., Zhang, W., Hu, J., Xu, Z., Wang, H., Sarkar, P., Li, L., Wan, Y., Liu, J., Wu, W., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.03.008 · Cited by 117 · see citing works
“Translating Ribosome Affinity Purification (TRAP) sequencing (TRAP-seq)— TRAP assay was adopted from previous studies (Heiman et al., 2014).”
Amygdala NPY Circuits Promote the Development of Accelerated Obesity under Chronic Stress Conditions
Ip, C. K., Zhang, L., Farzi, A., Qi, Y., Clarke, I. M., Reed, F. M., Shi, Y., Enriquez, R. F., Dayas, C. V., Graham, B. A., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.04.001 · Cited by 112 · see citing works
Ribosomal biogenesis as an emerging target of neurodevelopmental pathologies
Hetman, M., & Słomnicki, Ł. P. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14576 · Cited by 110 · see citing works
“…neural cell type-specific analysis of individual mRNA translation efficiency across the entire transcriptome could be determined in relevant cell culture- or animal models using such technologies as Ribo-Tag or the translating ribosome affinity purification (Sanz et al. 2009; Heiman et al. 2014).”
MethodForbes, T. A., Goldstein, E. Z., Dupree, J. L., Jablonska, B., Scafidi, J., Adams, K. L., Kawasawa, Y. I., Hashimoto‐Torii, K., & Gallo, V. (2020) · Nature Communications · doi:10.1038/s41467-020-14762-7 · Cited by 109 · see citing works
Astroglial Calcium Signaling Encodes Sleep Need in Drosophila
Blum, I. D., Keleş, M. F., Baz, E., Han, E., Park, K. H., Luu, S., Issa, H. A., Brown, M. P., Ho, M. C. W., Tabuchi, M., et al. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.012 · Cited by 109 · see citing works
Activity-dependent modulation of synapse-regulating genes in astrocytes
Farhy-Tselnicker, I., Boisvert, M., Liu, H., Dowling, C. C., Erikson, G. A., Blanco‐Suárez, E., Farhy, C., Shokhirev, M. N., Ecker, J. R., & Allen, N. J. (2021) · eLife · doi:10.7554/elife.70514 · Cited by 106 · see citing works
Porniece, M., Cremer, A. L., Klemm, P., Steuernagel, L., Sundaram, S. M., Jaïs, A., Hausen, A. C., Tao, J., Secher, A., Pedersen, T. Å., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00499-0 · Cited by 107 · see citing works
Rannals, M. D., Hamersky, G. R., Page, S. C., Campbell, M. N., Briley, A., Gallo, R. A., Phan, B. N., Hyde, T. M., Kleinman, J. E., Shin, J. H., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.021 · Cited by 106 · see citing works
Serotonin receptor 4 in the hippocampus modulates mood and anxiety
Karayol, R., Medrihan, L., Warner‐Schmidt, J. L., Fait, B. W., Rao, M. N., Holzner, E. B., Greengard, P., Heintz, N., & Schmidt, E. F. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00994-y · Cited by 103 · see citing works
Self-citationWilliams, E. S., Manning, C. E., Eagle, A. L., Swift-Gallant, A., Duque-Wilckens, N., Chinnusamy, S., Moeser, A., Jordan, C., Leinninger, G., & Robison, A. J. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.08.006 · Cited by 101 · see citing works
“(B) Only female mice displayed reduced sucrose preference after SCVS. (C) Schematic depicting retrograde Cre viral vector strategy and electrophysiology time course (left) and L10-GFP vHPC stained with anti-GFP demonstrating vHPC-NAc projections (right).”
MethodInfluentialExtensive cryptic splicing upon loss of RBM17 and TDP43 in neurodegeneration models
Tan, Q., Yalamanchili, H. K., Park, J., Maio, A. D., Lu, H., Wan, Y., White, J. J., Bondar, V. V., Sayegh, L. S., Liu, X., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw337 · Cited by 96 · see citing works
A neurodegenerative cellular stress response linked to dark microglia and toxic lipid secretion
Flury, A. G., Aljayousi, L., Park, H.-J., Khakpour, M., Mechler, J., Aziz, S., McGrath, J. D., Deme, P., Sandberg, C., Ibáñez, F. G., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.11.018 · Cited by 98 · see citing works
Sleep Regulation by Neurotensinergic Neurons in a Thalamo-Amygdala Circuit
Ma, C., Zhong, P., Liu, D., Barger, Z., Zhou, L., Chang, W.-C., Kim, B., & Dan, Y. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.015 · Cited by 94 · see citing works
Omomyc Reveals New Mechanisms To Inhibit the MYC Oncogene
Demma, M. J., Mapelli, C., Sun, A., Bodea, S., Ruprecht, B., Javaid, S., Wiswell, D., Muise, E., Chen, S., Zelina, J., et al. (2019) · Molecular and Cellular Biology · doi:10.1128/mcb.00248-19 · Cited by 92 · see citing works
Rapid Molecular Profiling of Defined Cell Types Using Viral TRAP
Nectow, A. R., Moya, M. V., Ekstrand, M. I., Mousa, A., McGuire, K. L., Sferrazza, C. E., Field, B. C., Rabinowitz, G. S., Sawicka, K., Liang, Y., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.048 · Cited by 92 · see citing works
“By directing the expression of an EGFP-tagged ribosome protein L10a (EGFPL10a) to defined cell populations, TRAP enables the isolation of cell-type-specific polysome-bound mRNAs from whole-tissue homogenates, avoiding potential adaptations and RNA degradation that can result from lengthier cellular isolation methods (…”
BackgroundMethodInfluentialSelf-citationCa 2+ channels couple spiking to mitochondrial metabolism in substantia nigra dopaminergic neurons
Zampese, E., Wokosin, D. L., González‐Rodríguez, P., Guzmán, J. N., Tkatch, T., Kondapalli, J., Surmeier, W. C., D’Alessandro, K. B., Stefani, D. D., Rizzuto, R., et al. (2022) · Science Advances · doi:10.1126/sciadv.abp8701 · Cited by 91 · see citing works
Mazaré, N., Oudart, M., Moulard, J., Cheung, G. T. Y., Tortuyaux, R., Mailly, P., Mazaud, D., Bemelmans, A., Boulay, A.-C., Blugeon, C., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108076 · Cited by 90 · see citing works
“Tg(Aldh1l1-eGFP/Rpl10a) JD130Htz (MGI: 5496674) (Aldh1l1:L10a-eGFP) mice were obtained from Nathaniel Heintz’s laboratory (Rockefeller University, New York City, NY) and kept under pathogen-free conditions (Heiman et al., 2014).”
Sudmant, P. H., Lee, H., Dominguez, D., Heiman, M., & Burge, C. B. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.094 · Cited by 83 · see citing works
Self-citationBassoon proteinopathy drives neurodegeneration in multiple sclerosis
Schattling, B., Engler, J. B., Volkmann, C., Rothammer, N., Woo, M. S., Petersen, M., Winkler, I., Kaufmann, M., Rosenkranz, S. C., Fejtová, A., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0385-4 · Cited by 83 · see citing works
Signatures of sex: Sex differences in gene expression in the vertebrate brain
Gegenhuber, B., & Tollkühn, J. (2019) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.348 · Cited by 85 · see citing works
Hall, H., Medina, P., Cooper, D. A., Escobedo, S. E., Rounds, J., Brennan, K., Vincent, C., Miura, P., Doerge, R. W., & Weake, V. M. (2017) · BMC Genomics · doi:10.1186/s12864-017-4304-3 · Cited by 82 · see citing works
“Complementary cell type-specific data on the ribosome-bound pool of mRNAs destined for translation could be obtained using the translating ribosome affinity purification (TRAP) technique, based on cell-specific expression of an EGFP-tagged ribosomal subunit [119, 120].”
MethodLoss of eIF4E Phosphorylation Engenders Depression-like Behaviors via Selective mRNA Translation
Amorim, I. S., Kedia, S., Kouloulia, S., Simbriger, K., Gantois, I., Jafarnejad, S. M., Li, Y., Kampaite, A., Pooters, T., Romanò, N., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2673-17.2018 · Cited by 82 · see citing works
“3C), it would be imperative to perform cell-type-specific profiling of translation in neuronal and non-neuronal cells (e.g., microglia) using methodologies, such as TRAP (Heiman et al., 2014).”
MethodMicroglia-astrocyte crosstalk regulates synapse remodeling via Wnt signaling
Faust, T. E., Lee, Y., O’Connor, C. D., Boyle, M. A., Gunner, G., Durán‐Laforet, V., Ferrari, L. L., Murphy, R. E., Badimon, A., Sakers, K., et al. (2025) · Cell · doi:10.1016/j.cell.2025.08.023 · Cited by 81 · see citing works
An Excitatory Circuit in the Perioculomotor Midbrain for Non-REM Sleep Control
Zhang, Z., Zhong, P., Hu, F., Barger, Z., Ren, Y., Ding, X., Li, S., Weber, F., Chung, S., Palmiter, R. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.041 · Cited by 79 · see citing works
Localization of transcripts, translation, and degradation for spatiotemporal sarcomere maintenance
Lewis, Y. E., Moskovitz, A., Mutlak, M., Heineke, J., Caspi, L. H., & Kehat, I. (2018) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2018.01.012 · Cited by 74 · see citing works
Nguyen, T.-M., Schreiner, D., Xiao, L., Traunmüller, L., Bornmann, C., & Scheiffele, P. (2016) · eLife · doi:10.7554/elife.22757 · Cited by 79 · see citing works
“For Ribotag purifications the procedure of Heiman and colleagues for affinity-purification of polysomes (Heiman et al., 2014) was modified as follows: Brains of mice between (postnatal day 24 to 28) were dissected in ice-cold PBS and four hippocampi (two animals per condition) were lysed in 500 mL…”
MethodInfluentialSaito, Y., Yuan, Y., Zucker-Scharff, I., Fak, J. J., Jereb, S., Tajima, Y., Licatalosi, D. D., & Darnell, R. B. (2019) · Neuron · doi:10.1016/j.neuron.2018.12.019 · Cited by 77 · see citing works
Efficient analysis of mammalian polysomes in cells and tissues using Ribo Mega-SEC
Yoshikawa, H., Larance, M., Harney, D., Sundaramoorthy, R., Ly, T., Owen‐Hughes, T., & Lamond, A. I. (2018) · eLife · doi:10.7554/elife.36530 · Cited by 75 · see citing works
“This suggests that eS10 is one of the RPs released from ribosomal subunits after EDTA treatment, as reported previously for the 5S RNP (Blobel, 1971; Steitz et al., 1988).”
MethodInfluentialHwang, H.-W., Saito, Y., Park, C. Y., Blachère, N. E., Tajima, Y., Fak, J. J., Zucker-Scharff, I., & Darnell, R. B. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.024 · Cited by 74 · see citing works
eIF4E-Dependent Translational Control: A Central Mechanism for Regulation of Pain Plasticity
Uttam, S., Wong, C., Price, T. J., & Khoutorsky, A. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00470 · Cited by 74 · see citing works
Lee, K., Chan, J. Y., Liang, C., Ip, C. K., Shi, Y., Herzog, H., Hughes, W. E., Bensellam, M., Delghingaro‐Augusto, V., Koina, M. E., et al. (2022) · Diabetologia · doi:10.1007/s00125-022-05669-7 · Cited by 70 · see citing works
“Translating ribosome affinity purification Translating ribosome affinity purification (TRAP) was performed based on the previously published protocol [30, 31].”
Marrocco, J., Petty, G. H., Ríos, M. B., Gray, J. D., Kogan, J. F., Waters, E. M., Schmidt, E. F., Lee, F. S., & McEwen, B. S. (2017) · Nature Communications · doi:10.1038/s41467-017-01014-4 · Cited by 69 · see citing works
Multiomic profiling of the acute stress response in the mouse hippocampus
von Ziegler, L., Floriou‐Servou, A., Waag, R., Gupta, R. R. D., Sturman, O., Gapp, K., Maat, C. A., Kockmann, T., Lin, H.-Y., Duss, S. N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29367-5 · Cited by 68 · see citing works
Plant translational reprogramming for stress resilience
Son, S.-M., & Park, S. R. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1151587 · Cited by 58 · see citing works
“Numerous global translatome profiling technologies, such as polysome profiling, ribosome profiling, translating ribosome affinity purification, and 3′ ribosome-profiling sequencing, have been developed and utilized to study plant translation (Ingolia et al., 2009; Heiman et al., 2014; Mazzoni-Putman and Stepanova, 201…”
BackgroundPiol, D., Robberechts, T., & Cruz, S. D. (2023) · Neuron · doi:10.1016/j.neuron.2023.02.028 · Cited by 65 · see citing works
Rodrigues, D. C., Mufteev, M., Weatheritt, R. J., Djuric, U., Ha, K., Ross, P. J., Wei, W., Piekna, A., Sartori, M. A., Byres, L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2020.02.107 · Cited by 67 · see citing works
Diet-induced adaptive thermogenesis requires neuropeptide FF receptor-2 signalling
Zhang, L., Ip, C. K., Lee, I.-C. J., Qi, Y., Reed, F. M., Karl, T., Low, J. K., Enriquez, R. F., Lee, N. J., Baldock, P. A. J., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06462-0 · Cited by 66 · see citing works
Regulation of gene expression via translational buffering
Kusnadi, E. P., Timpone, C., Topisirović, I., Larsson, O. S., & Furic, L. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2021.119140 · Cited by 60 · see citing works
Mapping Gene Expression in Excitatory Neurons during Hippocampal Late-Phase Long-Term Potentiation
Chen, P. B., Kawaguchi, R., Blum, C., Achiro, J. M., Coppola, G., O’Dell, T. J., & Martin, K. C. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00039 · Cited by 61 · see citing works
“These include the promoter-dependent tagging of ribosomal proteins with a small protein tag (Heiman et al., 2014), which allows for downstream purification of the ribosome-associated RNA population within a genetically defined cell population from tissue composed of multiple cell types.”
BackgroundNeuroinflammation Plays a Critical Role in Cerebral Cavernous Malformation Disease
Lai, C. C., Nelsen, B., Frías-Anaya, E., Gallego-Gutiérrez, H., Orecchioni, M., Herrera, V., Ortiz, E., Sun, H., Mesarwi, O. A., Ley, K. F., et al. (2022) · Circulation Research · doi:10.1161/circresaha.122.321129 · Cited by 65 · see citing works
Kocabas, A. M., Duarte, T. T., Kumar, S. S., & Hynes, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.048 · Cited by 64 · see citing works
Chen, X., & Dickman, D. K. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1007117 · Cited by 59 · see citing works
Scheckel, C., Imeri, M., Schwarz, P., & Aguzzi, A. (2020) · eLife · doi:10.7554/elife.62911 · Cited by 57 · see citing works
The Future of Cross-Linking and Immunoprecipitation (CLIP)Preprint
Ule, J., Hwang, H., & Darnell, R. B. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032243 · Cited by 63 · see citing works
“Second, the utilization of a mix of high-affinity GFP antibodies (Heiman et al. 2014) allows cTag-CLIP analysis to be performed with a standardized and optimized highstringency protocol for different RBPs (Hwang et al.”
Autophagy coupled to translation is required for long-term memory
Pandey, K. R., Yu, X., Steinmetz, A. B., & Alberini, C. M. (2020) · Autophagy · doi:10.1080/15548627.2020.1775393 · Cited by 61 · see citing works
“Three weeks after infection, rats were euthanized, and immunoprecipitations were performed using monoclonal EGFP antibodies clone 19C8 and 19F7 antibody (purchased from Memorial Sloan Kettering, NY, core antibody facility) as previously described [43].”
MethodInfluentialAbles, J. L., Görlich, A., Antolin‐Fontes, B., Wang, C., Lipford, S. M., Riad, M. H., Ren, J., Hu, F., Luo, M., Kenny, P. J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717506114 · Cited by 61 · see citing works
“Heiman M, Kulicke R, Fenster RJ, Greengard P, Heintz N (2014) Cell type-specific mRNA purification by translating ribosome affinity purification (TRAP).”
MethodInfluentialSelf-citationFunctional Micropeptides Encoded by Long Non-Coding RNAs: A Comprehensive Review
Pan, J., Wang, R., Shang, F., Ma, R., Rong, Y., & Zhang, Y. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.817517 · Cited by 60 · see citing works
A cortico-amygdala neural substrate for endocannabinoid modulation of fear extinction
Gunduz‐Cinar, O., Castillo, L. I., Xia, M. Y., Leer, E. V., Brockway, E. T., Pollack, G. A., Yasmin, F., Bukalo, O., Limoges, A., Oreizi-Esfahani, S., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.023 · Cited by 59 · see citing works
The Dominantly Inherited Alzheimer Network (DIAN), Li, Z., Del-Aguila, J. L., Dube, U., Budde, J., Martinez, R., Black, K., Xiao, Q., Cairns, N. J., Dougherty, J. D., et al. (2018) · Genome Medicine · doi:10.1186/s13073-018-0551-4 · Cited by 56 · see citing works
“Purification of cell-type-specific messenger RNA (mRNA) by TRAP was described previously [45] with modifications.”
MethodAn amygdala circuit that suppresses social engagement
Kwon, J.-T., Ryu, C., Lee, H., Sheffield, A., Fan, J., Cho, D. H., Bigler, S., Sullivan, H. A., Choe, H. K., Wickersham, I. R., et al. (2021) · Nature · doi:10.1038/s41586-021-03413-6 · Cited by 61 · see citing works
Self-citationβ-Catenin maintains lung epithelial progenitors after lung specification
Ostrin, E. J., Little, D. R., Gerner-Mauro, K. N., Sumner, E. A., Ríos-Corzo, R., Ambrosio, E. M., Holt, S. E., Forcioli-Conti, N., Akiyama, H., Hanash, S., et al. (2018) · Development · doi:10.1242/dev.160788 · Cited by 55 · see citing works
“To further validate our progenitor gene list, we adapted the translating ribosome affinity purification (TRAP) method, where a Cre-dependent tagged ribosomal protein is expressed in cell types of interest allowing affinity purification of the associated translating mRNAs, which are considered representative of the tot…”
MethodInfluentialSödersten, E., Toskas, K., Rraklli, V., Tiklová, K., Björklund, Å. K., Ringnér, M., Perlmann, T., & Holmberg, J. (2018) · Nature Communications · doi:10.1038/s41467-018-03538-9 · Cited by 52 · see citing works
Circuit-specific hippocampal ΔFosB underlies resilience to stress-induced social avoidance
Eagle, A. L., Manning, C., WILLIAMS, E. S., Bastle, R. M., Gajewski, P. A., Garrison, A., Wirtz, A. J., Akguen, S., Brandel-Ankrapp, K. L., Endege, W. O., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17825-x · Cited by 54 · see citing works
- Authors
- Heiman, M., Kulicke, R., Fenster, R. J., Greengard, P., & Heintz, N.
- Affiliations
- Broad Institute (US)
- Rockefeller University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Heiman, Myriam
- Venue
- Nature Protocols
- Published
- 2014-05-08
- Volume
- 9
- Issue
- 6
- Pages
- 1282-1291
- ISSN
- 1750-2799 (ISSN-L)
- 1754-2189
- PMC
- PMC4102313
- OpenAlex
- W1993981485
- Cited by
- 498
- References
- 39
- Citations by year
- 2026: 36 · 2025: 49 · 2024: 54 · 2023: 52 · 2022: 54 · 2021: 44 · 2020: 49 · 2019: 48 · 2018: 45 · 2017: 30 · 2016: 21 · 2015: 12 · 2014: 4
- FWCI
- 9.16
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Nature Protocols (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- PMC
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (P50MH090963, MH090963)
- National Institute of General Medical Sciences (T32GM007739)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- translating ribosome affinity purification, central nervous system, cell type-specific gene expression
- MeSH terms
- Animals, Cells, Cultured, Humans, Polyribosomes, Ribosomes, RNA, Messenger, Gene Expression Profiling, Mice, Single-Cell Analysis
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