Horizontal transfer of oncogenes by uptake of apoptotic bodies
Open accessAbstract
Tumor formation involves the accumulation of a series of genetic alterations that are required for malignant growth. In most malignancies, genetic changes can be observed at the chromosomal level as losses or gains of whole or large portions of chromosomes . Here we provide evidence that tumor DNA may be horizontally transferred by the uptake of apoptotic bodies. Phagocytosis of apoptotic bodies derived from H-ras V12 - and human c-myc-transfected rat fibroblasts resulted in loss of contact inhibition in vitro and a tumorigenic phenotype in vivo . Fluorescence in situ hybridization analysis revealed the presence of rat chromosomes or of rat and mouse fusion chromosomes in the nuclei of the recipient murine cells. The transferred DNA was propagated, provided that the transferred DNA conferred a selective advantage to the cell and that the phagocytotic host cell was p53-negative. These results suggest that lateral transfer of DNA between eukaryotic cells may result in aneuploidy and the accumulation of genetic changes that are necessary for tumor formation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Genetic information can also be transferred by uptake of apoptotic bodies.
“These results suggest that genetic information can also be transferred by uptake of apoptotic bodies.”
From Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies (2013) · cites this paper as [114]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
The citation lists haven’t been fetched yet
References 31 · Cited by 550
Research works printed but not linked: 29
- [1]Kerr J F, Wyllie A H, Currie A R. Br J Cancer. 1972;26:239–257. doi: 10.1038/bjc.1972.33. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [2]Wyllie A H, Kerr J F, Currie A R. Int Rev Cytol. 1980;68:251–306. doi: 10.1016/s0074-7696(08)62312-8. [DOI] [PubMed] [Google Scholar] · DOI
- [3]Bursch W, Paffe S, Putz B, Barthel G, Schulte-Hermann R. Carcinogenesis. 1990;11:847–853. doi: 10.1093/carcin/11.5.847. [DOI] [PubMed] [Google Scholar] · DOI
- [4]Bursch W, Taper H S, Lauer B, Schulte-Hermann R. Virchows Arch B Cell Pathol Incl Mol Pathol. 1985;50:153–166. doi: 10.1007/BF02889898. [DOI] [PubMed] [Google Scholar] · DOI
- [5]Barres B A, Hart I K, Coles H S, Burne J F, Voyvodic J T, Richardson W D, Raff M C. Cell. 1992;70:31–46. doi: 10.1016/0092-8674(92)90531-g. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- [6]Holmgren L, O'Reilly M S, Folkman J. Nat Med. 1995;1:149–153. doi: 10.1038/nm0295-149. [DOI] [PubMed] [Google Scholar] · DOI
- [7]Rao L, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S, White E. Proc Natl Acad Sci USA. 1992;89:7742–7746. doi: 10.1073/pnas.89.16.7742. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [8]Evan G I, Wyllie A H, Gilbert C S, Littlewood T D, Land H, Brooks M, Waters C M, Penn L Z, Hancock D C. Cell. 1992;69:119–128. doi: 10.1016/0092-8674(92)90123-t. [DOI] [PubMed] [Google Scholar] · DOI
- [9]Lowe S W, Lin A W. Carcinogenesis. 2000;21:485–495. doi: 10.1093/carcin/21.3.485. [DOI] [PubMed] [Google Scholar] · DOI
- [10]Christofori G, Naik P, Hanahan D. Nature (London) 1994;369:414–418. doi: 10.1038/369414a0. [DOI] [PubMed] [Google Scholar] · DOI
- [11]Lake J A, Jain R, Rivera M C. Science. 1999;283:2027–2028. doi: 10.1126/science.283.5410.2027. [DOI] [PubMed] [Google Scholar] · DOI
- [12]Ochman H, Lawrence J G, Groisman E A. Nature (London) 2000;405:299–304. doi: 10.1038/35012500. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- [13]Holmgren L, Szeles A, Rajnavölgyi E, Klein G, Folkman J, Ernebrg I, Falk K. Blood. 1999;93:3956–3963. [PubMed] [Google Scholar]
- [14]Spetz A, Patterson B K, Lore K, Andersson J, Holmgren L. J Immunol. 1999;163:736–742. [PubMed] [Google Scholar]
- [15]de la Taille A, Chen M W, Burchardt M, Chopin D K, Buttyan R. Cancer Res. 1999;59:5461–5463. [PubMed] [Google Scholar]
- [16]Donehower L A, Harvey M, Slagle B L, McArthur M J, Montgomery C A J, Butel J S, Bradley A. Nature (London) 1992;356:215–221. doi: 10.1038/356215a0. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- [17]Spector D L, Goldman R D, Leinwand L A. Cells: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Lab. Press; 1997. [Google Scholar]
- [18]Shih C, Shilo B Z, Goldfarb M P, Dannenberg A, Weinberg R A. Proc Natl Acad Sci USA. 1979;11:5714–5718. doi: 10.1073/pnas.76.11.5714. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [19]Henriksson M, Bakardjiev A, Klein G, Lüscher B. Oncogene. 1993;8:3199–3209. [PubMed] [Google Scholar]
- [20]Szeles A, Bajalica-Lagercrantz S, Lindblom A, Lushnikova T, Kashuba V I, Imreh S, Nordenskjold M, Klein G, Zabarovsky E. Chromosome Res. 1996;4:310–313. doi: 10.1007/BF02263683. [DOI] [PubMed] [Google Scholar] · DOI
- [21]Pinkel D, Straume T, Gray J W. Proc Natl Acad Sci USA. 1986;83:2934–2938. doi: 10.1073/pnas.83.9.2934. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [22]Cheng L, Fu J, Tsukumoto A, Hawley R G. Nat Biotechnol. 1996;14:606–609. doi: 10.1038/nbt0596-606. [DOI] [PubMed] [Google Scholar] · DOI
- [24]Levine A J. Cell. 1997;88:323–331. doi: 10.1016/s0092-8674(00)81871-1. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- [26]Harvey M, Sands A T, Weiss R S, Hegi M E, Wiseman R W, Pantazis P, Giovanella B C, Tainsky M A, Bradley A, Donehower L A. Oncogene. 1993;8:2457–2467. [PubMed] [Google Scholar]
- [27]Oberhammer F, Fritsch G, Schmied M, Pavelka M, Printz D, Purchio T, Lassmann H, Schulte-Hermann R. J Cell Sci. 1993;104:317–326. doi: 10.1242/jcs.104.2.317. [DOI] [PubMed] [Google Scholar] · DOI
- [28]Nagata S. Exp Cell Res. 2000;256:12–18. doi: 10.1006/excr.2000.4834. [DOI] [PubMed] [Google Scholar] · DOI
- [29]Bishop J M. Cell. 1991;64:235–248. doi: 10.1016/0092-8674(91)90636-d. [DOI] [PubMed] [Google Scholar] · DOI
- [30]Hanahan D, Weinberg R A. Cell. 2000;100:57–70. doi: 10.1016/s0092-8674(00)81683-9. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- [31]Jackson A L, Loeb L A. Semin Cancer Biol. 1998;8:421–429. doi: 10.1006/scbi.1998.0113. [DOI] [PubMed] [Google Scholar] · DOI
- Authors
- Bergsmedh, A., Szeles, A., Henriksson, M., Bratt, A., Folkman, M. J., Spetz, A.-L., & Holmgren, L.
- Affiliations
- Karolinska Institutet (SE)
- Cancer Center Karolinska Hospital R8:03, SE 17176, Stockholm, Sweden; Microbiology and Tumor Biology Center, Karolinska Institutet, S-171 77 Stockholm, Sweden; Surgical Research Laboratory, Children's Hospital, Boston, Ma 02115; Center for Infectious Diseases, Department of Medicine, Karolinska Institutet, Huddinge University Hospital, S-141 86, Huddinge, Sweden
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-05-15
- Volume
- 98
- Issue
- 11
- Pages
- 6407-6411
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC33481
- OpenAlex
- W1991293757
- Cited by
- 550
- References
- 31
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 31 · 2023: 37 · 2022: 34 · 2021: 42 · 2020: 29 · 2019: 29 · 2018: 21 · 2017: 22 · 2016: 37 · 2015: 15 · 2014: 20 · 2013: 21 · 2012: 18
- FWCI
- 5.93
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- horizontal gene transfer, apoptotic bodies, phagocytosis, oncogenes, H-Ras V12, c-Myc, tumor formation, contact inhibition, chromosome fusion, aneuploidy, tumor DNA
- MeSH terms
- Animals, Cell Transformation, Neoplastic, Cells, Cultured, DNA, Neoplasm, Fibroblasts, Humans, Genes, ras, Genes, myc, Mice, SCID, Apoptosis, 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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review