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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 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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“Tagged ribosomes are affinity-purified and associated mRNAs are identified by microarray or deep-sequencing (10).”
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“8 using mRNAs isolated with immunoprecipitation of translating ribosomes (Heiman et al., 2014).”
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BackgroundMethodTranslatome profiling: methods for genome-scale analysis of mRNA translation
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“mCherry-positive cerebella were selected under a stereomicroscope (Olympus SZX16) and subjected to TRAP analyses as described with modifications (25).”
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“We next examinedwhether these robust changes also occur in neurons in vivo using the bacTrap system (Heiman et al., 2014) (Figure 2D).”
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“We have optimized the published protocol (Heiman et al., 2014) that no contamination from the phagocytes were detected (Figure 5H).”
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“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).”
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“Translating Ribosome Affinity Purification (TRAP) sequencing (TRAP-seq)— TRAP assay was adopted from previous studies (Heiman et al., 2014).”
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“…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).”
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Serotonin receptor 4 in the hippocampus modulates mood and anxiety
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“(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).”
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Sleep Regulation by Neurotensinergic Neurons in a Thalamo-Amygdala Circuit
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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
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 94
“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 96
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
“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 85
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., Fejtova, A., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0385-4 · Cited by 86
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 91
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 80
“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 80
“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 93
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 81
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 77
Nguyen, T.-M., Schreiner, D., Xiao, L., Traunmüller, L., Bornmann, C., & Scheiffele, P. (2016) · eLife · doi:10.7554/elife.22757 · Cited by 82
“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
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 71
“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
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 79
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 66
“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
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
Plant translational reprogramming for stress resilience
Son, S., & Park, S. R. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1151587 · Cited by 68
“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 68
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 72
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
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 66
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 63
“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
Kocabas, A. M., Duarte, T. T., Kumar, S. S., & Hynes, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.048 · Cited by 62
Chen, X., & Dickman, D. K. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1007117 · Cited by 61
Scheckel, C., Imeri, M., Schwarz, P., & Aguzzi, A. (2020) · eLife · doi:10.7554/elife.62911 · Cited by 57
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 65
“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
“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 63
“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 63
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 64
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
“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
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 48
“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 55
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 58
Metadata
- 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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