Evidence map›Paper›PMID 24153179›Full record

ArticleNature2013

Differential L1 regulation in pluripotent stem cells of humans and apes.

Maria C N Marchetto, Iñigo Narvaiza, Ahmet M Denli, Christopher Benner, Thomas A Lazzarini, Jason L Nathanson, Apuã C M Paquola, Keval N Desai, Roberto H Herai, Matthew D Weitzman and 3 more

Abstract readComparative Study
In one paragraph

Article in Nature, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 139 papers.

0numbers the graph read from it
0cells of the map it votes in
139citing papers in PubMed
42.5field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

139 citing papers in PubMed, 240 citations in OpenAlex.

  1. A Role for Astrocyte Metabolism in Species-Specific Neuronal Development.bioRxiv : the preprint server for biology · 2026
    Article
  2. LINE-1 Retrotransposons and Amyotrophic Lateral Sclerosis.International journal of molecular sciences · 2026
    Review
  3. Article
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  8. The modern human aryl hydrocarbon receptor is more active when ancestralized by genome editing.Proceedings of the National Academy of Sciences of the United States of America · 2024
    Article
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  15. Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2023
    Review
  16. Review
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  18. Article
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79 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

13 authors at 5 institutions in 1 country.

Maria C N Marchetto *Laboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Iñigo Narvaiza *Laboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Ahmet M DenliLaboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Christopher BennerLaboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Thomas A LazzariniLaboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Jason L NathansonUniversity of California San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, Institute for Genomic Medicine. Sanford Consortium for Regenerative Medicine. 2880 Torrey Pines Scenic Dr. Room 3805, La Jolla, CA 92037.
Apuã C M PaquolaLaboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Keval N DesaiUniversity of California San Diego, Division of Biological Sciences. 9500 Gilman Dr. La Jolla, CA 92093.
Roberto H HeraiUniversity of California San Diego, School of Medicine, Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program, 2880 Torrey Pines Scenic Road - Sanford Consortium, La Jolla, CA 92093, MC 0695, USA.
Matthew D WeitzmanDepartment of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine and Center for Cellular and Molecular Therapeutics, The Children's Hospital of Philadelphia, Philadelphia, PA 19104-4318.
Gene W YeoUniversity of California San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, Institute for Genomic Medicine. Sanford Consortium for Regenerative Medicine. 2880 Torrey Pines Scenic Dr. Room 3805, La Jolla, CA 92037.
Alysson R MuotriUniversity of California San Diego, School of Medicine, Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program, 2880 Torrey Pines Scenic Road - Sanford Consortium, La Jolla, CA 92093, MC 0695, USA.
Fred H GageLaboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Salk Institute for Biological Studies · USRady Children's Hospital-San Diego · USSanford Consortium for Regenerative Medicine · USChildren's Hospital of Philadelphia · USUniversity of California, San Diego · US

Funding

Viral Vector Core (VVC)P30CA014195 · NCI · SALK INSTITUTE FOR BIOLOGICAL STUDIES · PI Ye Zheng · 1985 to 2026
$82.8M
Functional RNA elements in the human genomeR01HG004659 · NHGRI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI Kevin Daniel Corbett, Eugene Wei-Ming Yeo · 2008 to 2026
$12.4M
Single-Cell Approaches to Reveal How Jumping Genes Individualize Neural CircuitsR01MH095741 · NIMH · SALK INSTITUTE FOR BIOLOGICAL STUDIES · PI GAGE, FRED H · 2011 to 2015
$6.5M
Defining the messenger RNP code in the brainR01NS075449 · NINDS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI YEO, EUGENE WEI-MING · 2012 to 2016
$3.0M
Mechanisms of APOBEC3A InhibitionR01AI074967 · NIAID · SALK INSTITUTE FOR BIOLOGICAL STUDIES · PI WEITZMAN, MATTHEW D. · 2009 to 2013
$2.3M
The Impact of L1retrotransposition in the nervous systemR01MH094753 · NIMH · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI MUOTRI, ALYSSON R. · 2011 to 2015
$1.9M
Genomic Measurement of Alternative SplicingR01GM084317 · NIGMS · UNIVERSITY OF CALIFORNIA SANTA CRUZ · PI ARES, MANUEL, YEO, EUGENE WEI-MING · 2009 to 2012
$1.8M
L1 Retrotransposon and Neural DiversityR01MH088485 · NIMH · SALK INSTITUTE FOR BIOLOGICAL STUDIES · PI GAGE, FRED H · 2009 to 2012
$1.5M
NCI NIH HHS P30 CA014195NHGRI NIH HHS HG004659NHGRI NIH HHS R01 HG004659NIAID NIH HHS AI074967NIAID NIH HHS R01 AI074967NIGMS NIH HHS GM084317NIGMS NIH HHS R01 GM084317NIMH NIH HHS MH08848NIMH NIH HHS MH094753NIMH NIH HHS R01 MH088485NIMH NIH HHS R01 MH094753NIMH NIH HHS R01 MH095741NINDS NIH HHS NS075449NINDS NIH HHS R01 NS075449
6 · The paper itself

Abstract

Identifying cellular and molecular differences between human and non-human primates (NHPs) is essential to the basic understanding of the evolution and diversity of our own species. Until now, preserved tissues have been the main source for most comparative studies between humans, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). However, these tissue samples do not fairly represent the distinctive traits of live cell behaviour and are not amenable to genetic manipulation. We propose that induced pluripotent stem (iPS) cells could be a unique biological resource to determine relevant phenotypical differences between human and NHPs, and that those differences could have potential adaptation and speciation value. Here we describe the generation and initial characterization of iPS cells from chimpanzees and bonobos as new tools to explore factors that may have contributed to great ape evolution. Comparative gene expression analysis of human and NHP iPS cells revealed differences in the regulation of long interspersed element-1 (L1, also known as LINE-1) transposons. A force of change in mammalian evolution, L1 elements are retrotransposons that have remained active during primate evolution. Decreased levels of L1-restricting factors APOBEC3B (also known as A3B) and PIWIL2 (ref. 7) in NHP iPS cells correlated with increased L1 mobility and endogenous L1 messenger RNA levels. Moreover, results from the manipulation of A3B and PIWIL2 levels in iPS cells supported a causal inverse relationship between levels of these proteins and L1 retrotransposition. Finally, we found increased copy numbers of species-specific L1 elements in the genome of chimpanzees compared to humans, supporting the idea that increased L1 mobility in NHPs is not limited to iPS cells in culture and may have also occurred in the germ line or embryonic cells developmentally upstream to germline specification during primate evolution. We propose that differences in L1 mobility may have differentially shaped the genomes of humans and NHPs and could have continuing adaptive significance.

Indexed as

AnimalsArgonaute ProteinsCell LineCell ShapeCytidine DeaminaseEvolution, MolecularGenome, HumanHigh-Throughput Nucleotide SequencingHumansKaryotypingLong Interspersed Nucleotide ElementsMice, NudeMinor Histocompatibility AntigensPan paniscusPan troglodytesPluripotent Stem CellsAPOBEC3B protein, humanArgonaute ProteinsCytidine DeaminaseMinor Histocompatibility AntigensPIWIL2 protein, humanRNA, Messenger

Identifiers

PMID24153179
PMCPMC4064720
OpenAlexW2037794677

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.