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The Human LINE-1 Retrotransposon Creates DNA Double-strand Breaks
Open accessAbstract
Long interspersed element-1 (L1) is an autonomous retroelement that is active in the human genome. The proposed mechanism of insertion for L1 suggests that cleavage of both strands of genomic DNA is required. We demonstrate that L1 expression leads to a high level of double-strand break (DSB) formation in DNA using immunolocalization of gamma-H2AX foci and the COMET assay. Similar to its role in mediating DSB repair in response to radiation, ATM is required for L1-induced gamma-H2AX foci and for L1 retrotransposition. This is the first characterization of a DNA repair response from expression of a non-long terminal repeat (non-LTR) retrotransposon in mammalian cells as well as the first demonstration that a host DNA repair gene is required for successful integration. Notably, the number of L1-induced DSBs is greater than the predicted numbers of successful insertions, suggesting a significant degree of inefficiency during the integration process. This result suggests that the endonuclease activity of endogenously expressed L1 elements could contribute to DSB formation in germ-line and somatic tissues.
Checked 2026-10-06 · 2 references not checked yet
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TL;DR
L1 expression induces DNA double-strand breaks (DSBs) in mammalian cells, detected by γ-H2AX foci and neutral COMET, and this requires L1 endonuclease activity. ATM is required for L1-induced γ-H2AX foci and for L1 retrotransposition.
Key findings
- L1.3 transfection in HeLa produced γ-H2AX foci in 60–70% of cells, with 20–200 foci per focus-positive cell (mean 68), similar to 6 Gy ionizing radiation (mean 86); an endonuclease mutant (EN–) essentially abolished foci.
- Neutral COMET showed pronounced tail moments at 24 h after L1.3, with no tails at 48 h; L1-induced foci were largely repaired by 48 h.
- L1.3 cotransfection reduced neoR colony yield by 60%; EN– showed no significant toxicity, while RT– showed toxicity similar to wild-type L1.3. L1.3 reduced the mitotic index, whereas empty vector or EN– did not induce checkpoint responses.
- In ATM+ YZ-5 cells, synL1_optORF1_neo produced 62±6 and 24±10 L1 colonies; in ATM– EBS-7 cells, 0 colonies, while neoR plasmid controls were 207±38, 133±10, 115±12, and 91±4.7. L1-induced DSBs exceed insertions; the paper estimates conservatively tenfold more DSBs than insertions, with 100-fold within reason.
Methods
- Transient transfections of L1.3, L1 EN–, L1 RT–, ORF2, and synL1_optORF1_neo into HeLa, mouse 3T3, MCF7, and isogenic YZ-5 (ATM+) / EBS-7 (ATM–) cells.
- DSBs assessed by anti-γ-H2AX immunofluorescence and neutral single-cell gel electrophoresis (COMET); retrotransposition by G418 colony formation; toxicity by cotransfected neoR colony yield; cell-cycle by mitotic index; apoptosis by annexin V FACS/TUNEL.
- Main comparisons were between wild-type L1 and endonuclease/reverse transcriptase mutants, empty vector, and ATM+ versus ATM– cells; colony counts reported with SD.
Limitations
- Stated: the mechanism of second-strand cleavage is unresolved; whether ORF2 makes both breaks, uses another enzyme, or homes to existing nicks remains to be determined.
- Stated: poor understanding of L1 RNA/protein nuclear transport; overexpression may skew the DSB:insertion ratio by titrating repair factors or producing ORF2 activity unrelated to integration; a quantitative assay of L1 integration intermediates without selectable cassettes is needed.
- Stated/evident: fixed-cell γ-H2AX counts underestimate total breaks (the paper says slightly underestimate expected by about two- to threefold) and do not integrate frequency over time; most experiments use transformed cell lines and overexpressed L1, so relevance to endogenous L1 in normal tissues is not directly established (evident).
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Similar to its role in mediating DSB repair in response to radiation, ATM is required for L1-induced γ-H2AX foci and for L1 retrotransposition.”
- Also stated in: § Results · plain
“As shown in Table 1, synL1_optORF1_neo produced colonies efficiently in ATM+ cells. No colonies were detected in ATM– cells.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Results · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Similar to its role in mediating DSB repair in response to radiation, ATM is required for L1-induced γ-H2AX foci and for L1 retrotransposition.”
- Also stated in: § Results · plain
“L1.3 expression induced γ-H2AX foci in ATMC but not in ATMK cells with exposure times normalized to observation of IR-induced foci in ATM+ (Figure 5).”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Results · plain
None of the sources cited for this claim have been checked yet.
In the paper
“Notably, the number of L1-induced DSBs is greater than the predicted numbers of successful insertions, suggesting a significant degree of inefficiency during the integration process.”
- Also stated in: § Results · hedged
“Therefore, it is conservative to estimate that tenfold more L1-induced DSBs are produced than insertions, although a 100-fold difference is within reason (our γ-H2AX counts slightly underestimate the expected by about twoto threefold39,40).”
What the sources say
- Not checked yetcites [39] Rothkamm, 2003, Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses, Proc. Natl Acad. Sci. USA source
- Not checked yetcites [40] Sedelnikova, 2002, Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody, Radiat. Res. source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Also stated in: § Results · hedged
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The L1-induced foci are largely repaired by 48 h post transfection, as evidenced by the decreasing percentage of cells with γ-H2AX foci and the decreasing number of γ-H2AX foci per cell (Figure 2(b)).”
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIn the paper
“Mutations in the endonuclease domain of the L1 ORF2 resulted in essentially complete loss of the γ-H2AX foci in HeLa cells (Figure 2(a)), consistent with the inability of the endonuclease mutant of L1 to support retrotransposition.44”
What the sources say
- Not checked yetcites [44] Moran, 1996, High frequency retrotransposition in cultured mammalian cells, Cell source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“L1.3 RT– produced fewer foci than observed with wild-type L1.3, suggesting that high levels of focus formation may depend on the presence of the first L1 cDNA strand.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The observation that MCF7 cells show the same induction of γ-H2AX foci following wild-type L1 transfections suggests that the response is not likely due to apoptosis (Figure 2(d)).”
Load-bearingStrength:hedged· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Transient inhibition of ATM with kinase inhibitors or a dominant negative plasmid in HeLa cells (data not shown) also demonstrate the involvement of ATM in promoting retrotransposition.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“At 24 h post L1.3 transfection, 3T3 cells have high numbers of distinct foci as observed for HeLa cells (Figure 2(c)).”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Over-expression of ORF2 alone resulted in the formation of only modest numbers of foci 24 h post transfection (Figure 2(c)).”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- It may state two separate claims as one. 9
- Probably not a substantial claim. 6
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We demonstrate that L1 expression leads to a high level of double-strand break (DSB) formation in DNA using immunolocalization of γ-H2AX foci and the COMET assay.”
- Also stated in: § Results · plain
“γ-H2AX foci were present in L1.3-transfected HeLa cells in high numbers and high focus intensity 24 h after transfection (Figure 2(a)).”
- Also stated in: § Results · plain
“Transfection with L1.3 produced pronounced tail-moments at 24 h post transfection in the majority of cells (Figure 3).”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Also stated in: § Results · plain
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“L1 EN– showed no significant toxicity, while L1.3 RT– showed toxicity levels similar to that of the wild-type L1.3.”
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“Although most full-length L1 elements in the human genome are defective, our data suggest that more may be capable of causing genomic damage than the limited number capable of active retro-transposition.78”
What the sources say
- Not checked yetcites [78] Brouha, 2003, Hot L1s account for the bulk of retrotransposition in the human population, Proc. Natl Acad. Sci. USA source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Notably, a modified toxicity assay shows no L1-induced toxicity in the ATM– cell line (data not shown), suggesting that ATM is specifically required for retrotransposition and not the survival of cells after L1 expression.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, ORF2 expression alone is sufficient for generating DSBs, but it is probably facilitated by the presence of ORF1.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“On the basis of in vitro analysis of the R2 element from the silkworm Bombyx mori (R2Bm), the current model for non-long terminal repeat (non-LTR) element insertion is target-primed reverse transcription (TPRT) (Figure 1).6,7”
What the sources say
- Not checked yetcites [6] Luan, 1993, Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition, Cell source
- Not checked yetcites [7] Luan, 1995, RNA template requirements for target DNA-primed reverse transcription by the R2 retrotransposable element, Mol. Cell. Biol. source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This last report and our results demonstrate that non-LTR retrotransposons encode protein machinery that initiates insertion into DNA but largely requires host factors for many of the subsequent steps.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The ATM requirement for L1 integration could have potential consequences for human health in ATM-compromised individuals.”
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This work demonstrates that the L1 integration process produces DSBs and requires a DSB-repair protein.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Because non-LTR insertion proceeds through a different integration mechanism in which cDNA synthesis precedes endonuclease activity, this dependence represents a novel understanding of the L1 life cycle.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
In the paper
“The COMET assay is based on the method outlined by Singh et al.53”
What the sources say
- Not checked yetcites Singh et al.53 Singh, 1988, A simple technique for quantitation of low levels of DNA damage in individual cells, Expt. Cell Res. source
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“L1 utilizes an APE-like endonuclease to insert into the target DNA.5”
What the sources say
- Not checked yetcites [5] Feng, 1996, Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition, Cell source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In these models of TPRT, cleavage of both strands of genomic DNA is required, which implies that an intermediate equivalent to a DSB is present during the integration process.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, the L1 endonuclease may be responsible for insertion of the dispersed sites of homology, as well as creating the DSBs adjacent to them that facilitate the instability.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
The paper relies on this without support.
The DSB formation observed from transfected L1 expression reflects the behavior of endogenously expressed L1 elements.
“This result suggests that the endonuclease activity of endogenously expressed L1 elements could contribute to DSB formation in germ-line and somatic tissues.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“DNA lesions, in particular dsDNA breaks (DSB), can arise as ‘collateral damage’ associated with retrotransposition19, 20, 102.”
From The role of retrotransposable elements in ageing and age-associated diseases (2021) · cites this paper as [102]
The cited source says what the claim attributes to it.
In the citing paper
“Since ectopic retrotransposon activation has been associated with DNA damage and genomic instability (87, 90)”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [90]
The cited source says what the claim attributes to it.
In the citing paper
“Long interspersed element 1 (L1) retrotransposon activity, in particular, has been linked to DNA damage5, mutagenesis6,7, and deregulation of host gene transcription8.”
From SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age (2014) · cites this paper as [5]
In the citing paper
“In addition, locus-specific DNA hypermethylation has been associated with ageing blood and tissues 52,53 and appears to be conserved between mice, monkeys and humans 54 .”
From The roles of DNA, RNA and histone methylation in ageing and cancer (2019) · cites this paper as [54]
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Metadata
- Authors
- Gasior, S. L., Wakeman, T. P., Xu, B., & Deininger, P. L.
- Affiliations
- Tulane University (US)
- Louisiana State University (US)
- Corresponding author
- Deininger, Prescott L.
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2006-04
- Volume
- 357
- Issue
- 5
- Pages
- 1383-1393
- ISSN
- 0022-2836 (ISSN-L)
- PMC
- PMC4136747
- OpenAlex
- W1987332588
- Semantic Scholar
- 0eebb3ad93ef9c873e76a6294c3d89270c042f53
- Cited by
- 519
- References
- 90
- Citations by year
- 2026: 26 · 2025: 31 · 2024: 33 · 2023: 30 · 2022: 35 · 2021: 35 · 2020: 28 · 2019: 21 · 2018: 26 · 2017: 20 · 2016: 22 · 2015: 27 · 2014: 27 · 2013: 30 · 2012: 26
- FWCI
- 25.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation (EPS-0346411)
- U.S. Public Health Service (R01GM45668)
- National Institutes of Health
- U.S. Department of Defense (DAM 17-03-1-0709)
- American Cancer Society
- Brown Foundation
- Louisiana Board of Regents (P20RR020152-01, R03ES013301-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Keywords
- LINE-1 retrotransposons, DNA double-strand breaks, retrotransposition, ATM, γH2AX foci, DNA repair, endonuclease activity, non-LTR retrotransposons, human genome
- MeSH terms
- Animals, Cell Cycle, DNA, DNA Damage, DNA Repair, DNA-Binding Proteins, HeLa Cells, Histones, Humans, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Long Interspersed Nucleotide Elements, Comet Assay, Tumor Suppressor Proteins, DNA Fragmentation, Ataxia Telangiectasia Mutated Proteins
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