The DOI matches its Crossref record; 70 of the 70 references it cites were found in a registry or an index.
A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing
Open accessAbstract
MicroRNAs (miRNAs) are small noncoding regulatory RNAs that reduce stability and/or translation of fully or partially sequence-complementary target mRNAs. In order to identify miRNAs and to assess their expression patterns, we sequenced over 250 small RNA libraries from 26 different organ systems and cell types of human and rodents that were enriched in neuronal as well as normal and malignant hematopoietic cells and tissues. We present expression profiles derived from clone count data and provide computational tools for their analysis. Unexpectedly, a relatively small set of miRNAs, many of which are ubiquitously expressed, account for most of the differences in miRNA profiles between cell lineages and tissues. This broad survey also provides detailed and accurate information about mature sequences, precursors, genome locations, maturation processes, inferred transcriptional units, and conservation patterns. We also propose a subclassification scheme for miRNAs for assisting future experimental and computational functional analyses.
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In the citing paper
“miR-27a/b are expressed in SN of human midbrain (Additional file 2a) [34–36]”
From miR-27a and miR-27b regulate autophagic clearance of damaged mitochondria by targeting PTEN-induced putative kinase 1 (PINK1) (2016) · cites this paper as [34]
In the citing paper
“Several previous studies showed that miR-27a/b are expressed in human midbrain [34–36].”
From miR-27a and miR-27b regulate autophagic clearance of damaged mitochondria by targeting PTEN-induced putative kinase 1 (PINK1) (2016) · cites this paper as [34]
In the citing paper
“Previous studies have shown that only a small population of miRNAs accounts for a majority of miRNA pool in the brain (Shin et al. 2010, Hu et al. 2011, Landgraf et al. 2007, Berezikov et al. 2006).”
From miR‐186 is decreased in aged brain and suppresses BACE 1 expression (2016) · cites this paper as Landgraf et al. 2007
In the citing paper
“miRNAs often show strong cell typeand tissue-specific regulation of their targets (Landgraf et al., 2007;Jovic ˇic ´et al., 2013).”
From microRNA-33 Regulates ApoE Lipidation and Amyloid-β Metabolism in the Brain (2015) · cites this paper as Landgraf et al., 2007
In the citing paper
“Importantly, miRNAs quite often show cell-type, tissue, and species-specific regulation of their target genes due to the differences in their expression levels and the complexity of interaction with their targets in different cellular contexts (Landgraf et al., 2007;Jovic ˇic ´et al., 2013).”
From microRNA-33 Regulates ApoE Lipidation and Amyloid-β Metabolism in the Brain (2015) · cites this paper as Landgraf et al., 2007
In the citing paper
“Substantial data indicate that microRNA 21 (miR-21) is significantly elevated in glioblastoma (GBM) and in many other tumors of various origins.”
From MicroRNA 21 Promotes Glioma Invasion by Targeting Matrix Metalloproteinase Regulators (2008) · cites this paper as [33]
In the citing paper
“We also found 20 miRNAs that are up-regulated more than 2 fold during differentiation and some were previously identified from rat brain tissues: miR-21, miR-152, miR-142-5p and -3p, miR-338, miR-339 and miR-378 (Landgraf et al., 2007).”
From Identification of Dynamically Regulated MicroRNA and mRNA Networks in Developing Oligodendrocytes (2008) · cites this paper as Landgraf et al., 2007
In the citing paper
“Notably, these included hsa-miR-219a and hsa-miR-338, both known to promote myelin repair 54 , and hsa-miR-23, which enhances oligodendrocyte differentiation and myelin synthesis 55 .”
From Human brain microRNAs exhibit cell-type specificity and age dependence (2026) · cites this paper as [54]
In the citing paper
“both known to promote myelin repair 54 , and hsa-miR-23, which enhances oligodendrocyte differentiation and myelin synthesis 55”
From Human brain microRNAs exhibit cell-type specificity and age dependence (2026) · cites this paper as [54]
In the citing paper
“miR-375, miR-141, and miR-200a in the pituitary (Landgraf et al. 2007);”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Landgraf et al. 2007
In the citing paper
“with some being shown to be expressed in a tissue- (16), cell type- (17), or even cell state-specific manner (18)”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [16]
In the citing paper
“Recent efforts in profiling of the most studied types of small ncRNA, miRNA, across cells and tissues demonstrated the existence of tissue- and cell type-specific short noncoding transcripts (16, 24, 25, 33).”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [16]
In the citing paper
“We identified both well-described brain-specific miRNAs, such as mir-9, mir-124, mir-219, mir-338 (16, 24, 33), as well as those which are missing from existing catalogs, such as mir-666, mir-878, mir-433, etc.”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [16]
In the citing paper
“Consistent with previous reports, we observed that a group of miRNAs known to be brain specific, such as miR-124, miR-29b and miR-9, were highly enriched in all the samples. (Bak et al., 2008, Landgraf et al., 2007).”
From Cell-Type-Based Analysis of MicroRNA Profiles in the Mouse Brain (2012) · cites this paper as Landgraf et al., 2007
In the citing paper
“The most thorough of these microRNA localization projects performed small RNA library sequencing (RNA-seq) on over 250 libraries from 26 organ systems. However, this nascent effort sequenced only ∼1200 reads per library (Landgraf et al. 2007).”
From Toward the human cellular microRNAome (2017) · cites this paper as Landgraf et al. 2007
In the citing paper
“a previous study showed that miR-155 expression was highly specific to cells of hematopoietic origin 51 .”
From Identification of a protective microglial state mediated by miR-155 and interferon-γ signaling in a mouse model of Alzheimer’s disease (2023) · cites this paper as [51]
In the citing paper
“The first and as of now most comprehensive analysis of miRNA abundance in different tissues has been reported by Landgraf et al. in 2007 (3).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“For canonical miRNAs they found a high concordance of tissue-specific expression in humans and rodents.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“This sequencing-based study reported 340 miRNAs in 26 organs.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“Amongst others, Landgraf et al. detected tissue-specific expression of miR-122 in liver, of miR-9, miR-124 and miR 128a/b in brain, of miR-7, miR-375, miR-141 and miR-200a in pituitary gland and of miR-142, miR-144, miR-150, miR-155 and miR-223 in hematopoietic cells.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“The, as of now, most comprehensive study on tissue-specific miRNAs in humans was published by Landgraf et al. in 2007 (3).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“They identified 340 mature human miRNAs including 33 novel miRNAs not listed in the miRBase version 9.1, which was the current version at the time of the study (17).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“MiR-124 (miR-124–3p) was identified as the third most specific miRNA in the nervous system by Landgraf et al.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“They sequenced 256 small RNA libraries from 26 different organ systems and cell types of humans and rodents, with ∼1000 clone each.”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“MiR-514a-3p belongs to the miR-506 family; the mouse orthologue of miR-506, mmu-201, has been shown to be specifically expressed in reproductive tissues (3).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [3]
In the citing paper
“Loss-of-function of the abundant neuronal miRNAs let-7 and miR-124, and of the less abundant miR-125 and miR-132 (Landgraf et al., 2007), caused a marked pruning of the dendritic arbor, as quantified by Sholl analysis (Figure 4A, E).”
From Regulation of Synaptic Structure and Function by FMRP-Associated MicroRNAs miR-125b and miR-132 (2010) · cites this paper as Landgraf et al., 2007
In the citing paper
“The second is that early publications of general miRNA expression focused on tissues, which comprise numerous cell types, and the localization of miRNAs, whether cell specific or ubiquitous, has not been established [8, 9].”
From A curated human cellular microRNAome based on 196 primary cell types (2022) · cites this paper as [9]
In the citing paper
“Notably, five of the top 25 upregulated miRNAs in IS patients were brain-specific or enriched, including hsa-miR-9-3p, hsa-miR-124-3p, hsa-miR-143-3p, hsa-miR-98-5p, and hsa-miR-93-5p.”
From Acute Cerebral Ischemia Increases a Set of Brain-Specific miRNAs in Serum Small Extracellular Vesicles (2022) · cites this paper as Landgraf et al., 2007
In the citing paper
“Likewise, 9 out of the 20 upregulated miRNAs in tMCAO mice are brain-specific or preferentially expressed in brain tissues, including mmu-miR-124-3p, mmu-miR-9-3p, mmu-miR-9-5p, mmu-miR-323-3p, mmu-miR-219b-5p, mmu-miR-129b-3p, mmu-miR-129-5p, mmu-miR-433-3p, and mmu-miR-128-3p (Table 3).”
From Acute Cerebral Ischemia Increases a Set of Brain-Specific miRNAs in Serum Small Extracellular Vesicles (2022) · cites this paper as Landgraf et al., 2007
In the citing paper
“Previous reports have shown that miR-138-5p is highly expressed in the CNS, particularly among brain neurons [45,46,47].”
From MicroRNA-138-5p Targets Pro-Apoptotic Factors and Favors Neural Cell Survival: Analysis in the Injured Spinal Cord (2022) · cites this paper as [45]
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Metadata
- Authors
- Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M., Lin, C., Socci, N. D., Hermida, L., Fulci, V., Chiaretti, S., Foà, R., Schliwka, J., Fuchs, U., Novosel, A., Müller, R.-U., Schermer, B., Bissels, U., Inman, J., Phan, Q., Chien, M., Weir, D. B., Choksi, R., De Vita, G., Frezzetti, D., Trompeter, H.-I., Hornung, V., Teng, G., Hartmann, G., Palkovits, M., Di Lauro, R., Wernet, P., Macino, G., Rogler, C. E., Nagle, J. W., Ju, J., Papavasiliou, F. N., Benzing, T., Lichter, P., Tam, W., Brownstein, M. J., Bosio, A., Borkhardt, A., Russo, J. J., Sander, C., Zavolan, M., & Tuschl, T.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Basel (CH)
- Memorial Sloan Kettering Cancer Center (US)
- SIB Swiss Institute of Bioinformatics (CH)
- Sapienza University of Rome (IT)
- German Cancer Research Center (DE)
- Ludwig-Maximilians-Universität München (DE)
- University Medical Center Freiburg (DE)
- Miltenyi Biotec (Germany) (DE)
- J. Craig Venter Institute (US)
- Columbia University (US)
- University of Naples Federico II (IT)
- Düsseldorf University Hospital (DE)
- Rockefeller University (US)
- University of Bonn (DE)
- Albert Einstein College of Medicine (US)
- National Institutes of Health (US)
- Cornell University (US)
- Corresponding author
- Zavolan, Mihaela
- Tuschl, Thomas
- ORCID
- Landgraf, Pablo
- Rusu, Mirabela
- Iovino, Nicola
- Aravin, Alexei
- Pfeffer, Sébastien
- Kamphorst, Alice O.
- Landthaler, Markus
- Lin, Carolina
- Socci, Nicholas D.
- Hermida, Leandro
- Fulci, Valerio
- Chiaretti, Sabina
- Foà, Robin
- Müller, Roman-Ulrich
- Schermer, Bernhard
- Inman, Jason
- Frezzetti, Daniela
- Trompeter, Hans-Ingo
- Hornung, Veit
- Hartmann, Gunther
- Papavasiliou, F. Nina
- Benzing, Thomas
- Tam, Wayne
- Bosio, Andreas
- Borkhardt, Arndt
- Russo, James J.
- Sander, Chris
- Zavolan, Mihaela
- Tuschl, Thomas
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-06
- Volume
- 129
- Issue
- 7
- Pages
- 1401-1414
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2681231
- OpenAlex
- W2149146453
- Cited by
- 3,626
- References
- 70
- Citations by year
- 2026: 42 · 2025: 73 · 2024: 87 · 2023: 104 · 2022: 131 · 2021: 160 · 2020: 152 · 2019: 167 · 2018: 205 · 2017: 185 · 2016: 221 · 2015: 238 · 2014: 275 · 2013: 310 · 2012: 283
- FWCI
- 84.13
- 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, 2274 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)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- HAL (submittedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (105945, 205321)
- National Institute of General Medical Sciences (P01GM073047)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- microRNA, small RNA sequencing, microRNA precursors, microRNA maturation, miRNA conservation, microRNA target regulation, hematopoietic cells, neurons, cell lineage, miRNA expression profiling
- MeSH terms
- Animals, Base Sequence, Gene Expression Regulation, Hematopoietic Stem Cells, Humans, Molecular Sequence Data, Phylogeny, RNA, Messenger, Sequence Homology, Nucleic Acid, Gene Library, Conserved Sequence, Cell Lineage, Hematologic Neoplasms, Gene Expression Profiling, MicroRNAs, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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