Cited by 501RNA and protein synthesis mechanismsRNA Research and SplicingSingle-cell and spatial transcriptomics

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Cell type–specific mRNA purification by translating ribosome affinity purification (TRAP)

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Heiman, Myriam, Kulicke, Ruth, Fenster, Robert J, Greengard, Paul, Heintz, Nathaniel·2014·Nature Protocols

DOI 10.1038/nprot.2014.085PMC PMC4102313

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Abstract

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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Retracted
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Method
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Method
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Method
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Method
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Method
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MethodInfluential
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Self-citation
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Self-citation
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Background
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Method
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Kreher, C., Favret, J., Weinstock, N. I., Maulik, M., Hong, X., Gelb, M. H., Wrabetz, L. G., Feltri, M. L., & Shin, D. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001661 · Cited by 14
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Method
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Method
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MethodInfluential
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Background
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Fridy, P. C., Farrell, R. J., Molloy, K. R., Keegan, S., Wang, J., Jacobs, E. Y., Li, Y., Trivedi, J. M., Sehgal, V. S., Fenyö, D., et al. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107623 · Cited by 14
Local protein synthesis at neuromuscular synapses is required for motor functions
Tu, W.-Y., Xu, W., Bai, L., Liu, J., Han, Y., Luo, B., Wang, B., Zhang, K., & Shen, C. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114661 · Cited by 12
A journey to uncharted territory: new technical frontiers in studying tumor–stromal cell interactions
Guldner, I. H., & Zhang, S. (2014) · Integrative Biology · doi:10.1039/c4ib00192c · Cited by 12
Getting Down to Specifics
McClure, C. D., & Southall, T. D. (2015) · Advances in genetics · doi:10.1016/bs.adgen.2015.06.003 · Cited by 12
“However, optimisation of the method’s protocol have been reported to improve these caveats (Heiman et al., 2014).”
Method
A High-Content Screen Identifies MicroRNAs That Regulate Liver Repopulation After Injury in Mice
Zahm, A. M., Wang, A. W., Wang, Y. J., Schug, J., Wangensteen, K. J., & Kaestner, K. H. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.11.025 · Cited by 12
RISC-mediated control of selected chromatin regulators stabilizes ground state pluripotency of mouse embryonic stem cells
Pandolfini, L., Luzi, E., Bressan, D., Ucciferri, N., Bertacchi, M., Brandi, R., Rocchiccioli, S., D’Onofrio, M., & Cremisi, F. (2016) · Genome biology · doi:10.1186/s13059-016-0952-x · Cited by 12
“of polysome profiling [26, 27] (see “Methods”; Additional file 1: Figure S2a, b), adapting the translating ribosome affinity purification (TRAP) protocol for our purposes.”
Method
Integrating single-cell omic techniques to resolve the spatio-temporal complexity of arbuscular mycorrhizal symbiosis
Ferreras-Garrucho, G., Chancellor, T., & Paszkowski, U. (2025) · Journal of Experimental Botany · doi:10.1093/jxb/eraf404 · Cited by 12
Non-conventional peptides in plants: From gene regulation to crop improvement
Chen, H., Yu, J., & Li, W. (2022) · The Crop Journal · doi:10.1016/j.cj.2022.10.006 · Cited by 11
Large-scale gene expression changes in APP/PSEN1 and GFAP mutation models exhibit high congruence with Alzheimer’s disease
Gammie, S. C., Messing, A., Hill, M. A., Kelm‐Nelson, C. A., & Hagemann, T. L. (2024) · PLoS ONE · doi:10.1371/journal.pone.0291995 · Cited by 11
Single-Nuclei Sequencing Reveals a Robust Corticospinal Response to Nearby Axotomy But Overall Insensitivity to Spinal Injury
Wang, Z., Kumaran, M., Batsel, E., Testor-Cabrera, S., Beine, Z., Ribelles, A. A., Tsoulfas, P., Venkatesh, I., & Blackmore, M. G. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1508-24.2024 · Cited by 21
Persistent changes in the dorsal root ganglion nociceptor translatome governs hyperalgesic priming in mice: roles of GPR88 and Meteorin
Sankaranarayanan, I., Kume, M., Mohammed, A., Mwirigi, J. M., Inturi, N. N., Munro, G., Petersen, K. A., Tavares‐Ferreira, D., & Price, T. J. (2025) · Pain · doi:10.1097/j.pain.0000000000003523 · Cited by 11
Immunoprecipitation of Ribosome-Bound mRNAs from Astrocytic Perisynaptic Processes of the Mouse Hippocampus
Mazaré, N., Oudart, M., Cheung, G. T. Y., Boulay, A.-C., & Cohen‐Salmon, M. (2020) · STAR Protocols · doi:10.1016/j.xpro.2020.100198 · Cited by 11
“Figure 2B shows that compared with the first supernatant obtained from hippocampal homogenate (S1), the synaptogliosome fraction (P3) contains low levels of GFAP, high levels of the postsynaptic protein PSD95 and the cytosolic PAP protein Ezrin.”
Background
The Cranial Neural Crest in a Multiomics Era
Chong-Morrison, V., & Sauka‐Spengler, T. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.634440 · Cited by 11
“Isolating polysomes using recently-developed TRAP method (Heiman et al., 2014) and their associated mRNAs in the zebrafish migratory NC at 16–18 ss informed us of both known and novel NC markers forming the translatome at this developmental window (Chong, 2017).”
Method
Inherently Emissive Puromycin Analogues for Live Cell Labelling
Hadidi, K., Steinbuch, K. B., Dozier, L. E., Patrick, G. N., & Tor, Y. (2023) · Angewandte Chemie International Edition · doi:10.1002/anie.202216784 · Cited by 11
Innovations advancing our understanding of microglia in Alzheimer's disease: From in vitro to in vivo models
Maksour, S., & Ooi, L. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15885 · Cited by 12
Regulation of the hippocampal translatome by Apoer2-ICD release
Wasser, C. R., Werthmann, G. C., Hall, E. M., Kuhbandner, K., Wong, C. H. Y., Durakoglugil, M. S., & Herz, J. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00652-1 · Cited by 11
“The matrix was prepared as described in [34].”
BackgroundMethodInfluential
Age- and sex- divergent translatomic responses of the mouse retinal pigmented epithelium
Chucair‐Elliott, A. J., Ocañas, S. R., Pham, K. D., Machalinski, A. H., Plafker, S. M., Stout, M. B., Elliott, M. H., & Freeman, W. M. (2024) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2024.04.012 · Cited by 11
“…(Deal and Henikoff, 2011) isolates biotin tagged nuclei, and thus cell type-specific gDNA, while Translating Ribosome Affinity Purification (TRAP) (Heiman et al., 2014) isolates cell-type specific EGFP + ribosome-bound RNA for genomic/epigenomic and transcriptomic/translatomic analyses,…”
Background
DNA methylation and hydroxymethylation characterize the identity of D1 and D2 striatal projection neurons
Marion‐Poll, L., Roussarie, J.-P., Taing, L., Dard-Dascot, C., Servant, N., Jaszczyszyn, Y., Jordi, E., Mulugeta, E., Hervé, D., Bourc’his, D., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-04269-w · Cited by 11
Self-citation
Novel insights into small open reading frame-encoded micropeptides in hepatocellular carcinoma: A potential breakthrough
Zhang, Q., & Liu, L. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.216691 · Cited by 10
CPEB2-activated axonal translation of VGLUT2 mRNA promotes glutamatergic transmission and presynaptic plasticity
Lu, W.-H., Chang, T.-T., Chang, Y., Liu, Y.-H., Lin, C.-H., Suen, C., Hwang, M., & Huang, Y. (2024) · Journal of Biomedical Science · doi:10.1186/s12929-024-01061-2 · Cited by 11
“From 2 independent RIP experiments, 3,309 transcripts with raw signal > 1,000 were enriched more used the TRAP method [56] to isolate ribosome-associ-ated transcripts (i.e., translatome) in axons and somas of auditory cortical TE3 neurons before and after cued fear conditioning [20].”
Method
Common and divergent pathways in early stages of glutamate and tau-mediated toxicities in neurodegeneration
Chongtham, A., Sharma, A., Nath, B., Murtha, K., Gorbachev, K., Ramakrishnan, A., Schmidt, E. F., Shen, L., & Pereira, A. C. (2024) · Experimental Neurology · doi:10.1016/j.expneurol.2024.114967 · Cited by 10
Differential Protein Expression in Striatal D1- and D2-Dopamine Receptor-Expressing Medium Spiny Neurons
Mansuri, M. S., Peng, G., Wilson, R. S., Lam, T. T., Zhao, H., Williams, K. R., & Nairn, A. C. (2020) · Proteomes · doi:10.3390/proteomes8040027 · Cited by 9
“These include Translating Ribosome Affinity Purification (TRAP) lines that were designed to profile mRNA translation in defined cell types [21,22] and that allow isolation of nuclei from specific cell types using FANS [18].”
Method
Structural and molecular characterization of paraventricular thalamic glucokinase‐expressing neuronal circuits in the mouse
Gaspari, S., Quenneville, S., Sánchez-Archidona, A. R., Thorens, B., & Croizier, S. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25312 · Cited by 10
sncRiboTag-Seq: Cell-type-specific RiboTag-Seq for cells in low abundance in mouse brain tissue
Gao, Y., & Zhao, X. (2020) · STAR Protocols · doi:10.1016/j.xpro.2020.100231 · Cited by 11
Simultaneous measurement of nascent transcriptome and translatome using 4-thiouridine metabolic RNA labeling and translating ribosome affinity purification
Imai, H., Utsumi, D., Torihara, H., Takahashi, K., Kuroyanagi, H., & Yamashita, A. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad545 · Cited by 9
RPL-4 and RPL-9 Mediated Ribosome Purifications Facilitate the Efficient Analysis of Gene Expression in Caenorhabditis elegans Germ Cells
Nousch, M. (2020) · G3 Genes Genomes Genetics · doi:10.1534/g3.120.401644 · Cited by 9
A transient brain endothelial translatome response to endotoxin is associated with mild cognitive changes post-shock in young mice
Lu, S., Portela, I. D. J., Martino, N., Ramos, R. B., Salinero, A. E., Smith, R. M., Zuloaga, K. L., & Adam, A. P. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.07.041 · Cited by 8
Chronic treatment with fluoxetine regulates mitochondrial features and plasticity-associated transcriptomic pathways in parvalbumin-positive interneurons of prefrontal cortex
Jetsonen, E., Didio, G., Suleymanova, I., Teino, I., Ċastrén, E., & Umemori, J. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02219-8 · Cited by 11
Cell Type-specific mRNA Purification in Caenorhabditis elegans via Translating Ribosome Affinity Purification
McLachlan, I. G., & Flavell, S. W. (2019) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3328 · Cited by 9
“Translating Ribosome Affinity Purification (TRAP), or ribotagging, is a method to purify polysomal RNA from genetically-defined cell types (Heiman et al., 2008; Sanz et al., 2009; Heiman et al., 2014).”
Method
Gene Expression at the Tripartite Synapse: Bridging the Gap Between Neurons and Astrocytes
Imrie, G., Gray, M. B., Raghuraman, V., & Farhy-Tselnicker, I. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-64839-7_5 · Cited by 8
Prenatal Androgenization Alters the Development of GnRH Neuron and Preoptic Area RNA Transcripts in Female Mice
Burger, L. L., Wagenmaker, E. R., Phumsatitpong, C., Olson, D. P., & Moenter, S. M. (2020) · Endocrinology · doi:10.1210/endocr/bqaa166 · Cited by 10
Recognition memory-induced gene expression in the perirhinal cortex: A transcriptomic analysis
Scott, H., Rogers, M. F., Scott, H. L., Campbell, C., Warburton, E. C., & Uney, J. B. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.04.007 · Cited by 9
“New more selective techniques, such as translating ribosome affinity purification (TRAP) [61], could be used to refine which transcripts are analysed, firstly by examining only those transcripts that at that instant are being translated, and secondly by targeting specific cell types within a tissue.”
Glial immune-related pathways as mediators of closed head TBI effects on behavior in DrosophilaPreprint
van Alphen, B., Stewart, S., Iwanaszko, M., Xu, F., Bang, E., Rozenfeld, S., Ramakrishnan, A., Itoh, T. Q., Braun, R., & Allada, R. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/422535 · Cited by 9
Long-read subcellular fractionation and sequencing reveals the translational fate of full-length mRNA isoforms during neuronal differentiationPreprint
Ritter, A. J., Draper, J. M., Vollmers, C., & Sanford, J. R. (2024) · Genome Research · doi:10.1101/gr.279170.124 · Cited by 9
“Frac-seq, which our proposed method builds on, isolates actively translating ribosomes and assesses translation efficiency by stratifying transcripts by the number of ribosomes with which they are associated (Sterne-Weiler et al. 2013).”
Rules and impacts of nonsense‐mediated mRNA decay in the degradation of long noncoding RNAs
Singh, A. K. (2024) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1853 · Cited by 8
High-throughput translational profiling with riboPLATE-seq
Metz, J. B., Hornstein, N. J., Sharma, S. D., Worley, J., Gonzalez, C., & Sims, P. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-09638-3 · Cited by 8
Molecular signatures of regional vulnerability to tauopathy in excitatory cortical neurons
Broekaart, D. W. M., Sharma, A., Ramakrishnan, A., Chongtham, A., Günther, D. M., Subramaniyan, S., Wang, M., Patel, V., Zhang, B., Grinberg, L. T., et al. (2025) · Acta Neuropathologica · doi:10.1007/s00401-025-02879-2 · Cited by 7
“…we used the viral Translating Ribosome Affinity Purification (vTRAP) methodology, which allows the generation of regional and cell type-specific transcriptome data from polysomal RNA [37, 82] of vulnerable and resistant cell types in brain regions of interest in the PS19 (P301S) mouse model.”
Next generation sequencing technologies to address aberrant mRNA translation in cancer
Román, Á., Benitez, D. A., Díaz-Pizarro, A., Pino, N. D. V.-D., Olivera-Gómez, M., Cumplido-Laso, G., Carvajal-González, J. M., & Mulero‐Navarro, S. (2024) · NAR Cancer · doi:10.1093/narcan/zcae024 · Cited by 8
“A notable advantage of this technique lies in the utilization of specific promoters that control the expression of the tagged gene, enabling a cell type-specific measure of translation in tissues or complex co-cultures ( 34–36 ).”
Background
Changes in nucleus accumbens core translatome accompanying incubation of cocaine craving
Kawa, A. B., Hashimoto, J. G., Beutler, M. M., Guizzetti, M., & Wolf, M. E. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02112-4 · Cited by 7
Mega-enhancers compartmentalize transcriptionally active long genes in the brain
Zhao, Z., Parra, O. A. P., Fujita, S.-I., Musella, F., Alvarado, N. J. S., Alber, F., Yang, Y., & Yamada, T. (2026) · Nature Cell Biology · doi:10.1038/s41556-026-02043-2 · Cited by 7
“TRAP from synchronously developing granule neurons (sync-TRAP) 31,73,74 was performed by electroporating the cerebellum of P6 mouse pups with the pCAG–Rpl10a–GFP and pCAG–mCherry plasmids together with a vector encoding U6-sgRNA targeting the indicated gene or a control sequence at day 4, 8 or 28…”
Discovery of the hidden coding information in cancers: Mechanisms and biological functions
Zhou, X., Wu, X.-H., Lai, K., Zhou, R.-Y., Chen, Z., Yang, Z.-G., & Gao, X.-W. (2022) · International Journal of Cancer · doi:10.1002/ijc.34360 · Cited by 8
“However, TRAP-Seq requires more effort to generate transgenic samples.(62) The advantages and disadvantages were summarized in Table 1.”
Background
Decoding the molecular crosstalk between grafted stem cells and the stroke-injured brain
Azevedo-Pereira, R. L., Manley, N. C., Dong, C., Zhang, Y., Lee, A. G., Zatulovskaia, Y. A., Gupta, V., Vu, J. T., Han, S. S., Berry, J. E., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112353 · Cited by 7
Experience-dependent translational state defined by cell type-specific ribosome profilingPreprint
Eacker, S. M., Crawford, K., Brichta, L., Rießland, M., Ingolia, N. T., Greengard, P., Dawson, T. M., & Dawson, V. L. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/169425 · Cited by 7
“TRAP was performed as previously described using all the suppliers of reagents specified in the previous description (Kulicke et al. 2014).”
MethodSelf-citation
Injury distance limits the transcriptional response to spinal injuryPreprint
Wang, Z., Kumaran, M., Batsel, E., Testor-Cabrera, S., Beine, Z., Ribelles, A. A., Tsoulfas, P., Venkatesh, I., & Blackmore, M. G. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.27.596075 · Cited by 7
“Technical differences between the studies might contribute to the discrepancy, such as the ten-day post-injury timepoint in the previous study compared to seven days in our study and, crucially, the use of a TRAP approach 50 versus our single-nuclei analysis centered approach.”
Method
RAD23B acquires a copper metalloadaptor function in amphibian-to-reptile evolution to increase metabolism and regulate genomic integrity
Xiao, T., He, D., Liu, D., Jia, S., Chen, Q., Silverman, D., Maitra, N., Huang, A. Y., Pezacki, A. T., Nguyen, T. T., et al. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.08.024 · Cited by 6
Activity-dependent protein synthesis in neurons requires microglial-metabolic coupling
Adler, D. I., Martín‐Ávila, A., Cheng, E., Oliveira, M. M., Zhang, M., Evans, H. T., Yuan, D., Sam, R., Zhang, N., Sellés, M. C., et al. (2026) · Cell Metabolism · doi:10.1016/j.cmet.2026.05.006 · Cited by 7
Low Dopamine D2 Receptor Expression Drives Gene Networks Related to GABA, cAMP, Growth and Neuroinflammation in Striatal Indirect Pathway Neurons
Guerri, L., Dobbs, L. K., Silva, D. A. D. S. E., Meyers, A., Ge, A., Lecaj, L., Djakuduel, C., Islek, D., Hipolito, D., Badillo-Martinez, A., et al. (2022) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2022.08.010 · Cited by 9
“Translating Ribosome Affinity Purification (TRAP) TRAP isolation of ribosome-bound mRNA from iMSNs in mouse was performed as described (39) with the following differences: Matrix per whole mouse striatum: 150μl Streptavidin MyOne T1 Dynabeads (Invitrogen, #65601) and 60μl Biotinylated protein L recombinant purified (T…”
Method
Calling Cards: A Customizable Platform to Longitudinally Record Protein‐DNA Interactions Over Time in Cells and Tissues
Yen, A., Mateusiak, C., Sarafinovska, S., Gachechiladze, M. A., Guo, J., Chen, X., Moudgil, A., Cammack, A. J., Hoisington‐Lopez, J., Crosby, M., et al. (2023) · Current Protocols · doi:10.1002/cpz1.883 · Cited by 5
Translational control in the spinal cord regulates gene expression and pain hypersensitivity in the chronic phase of neuropathic pain
Lister, K. C., Wong, C., Uttam, S., Parisien, M., Stecum, P., Brown, N., Cai, W., Ho-Tieng, D., Hooshmandi, M., Gu, N., et al. (2026) · eLife · doi:10.7554/elife.100451.3 · Cited by 6

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
ORCID: Heiman, Myriam
Kulicke, Ruth
Fenster, Robert J
Greengard, Paul
Heintz, Nathaniel
Venue: Nature Protocols
Publisher: Springer Science and Business Media LLC
Published: 2014-05-08
Volume: 9
Issue: 6
Pages: 1282-1291
ISSN: 1750-2799 (ISSN-L)
1754-2189
DOI: 10.1038/nprot.2014.085
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
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
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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Cell type–specific mRNA purification by translating ribosome affinity purification (TRAP)

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