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DNA topoisomerase II in therapy-related acute promyelocytic leukemia

DNA topoisomerase II in therapy-related acute promyelocytic leukemia
DNA topoisomerase II in therapy-related acute promyelocytic leukemia
Background: Chromosomal translocations leading to chimeric oncoproteins are important in leukemogenesis, but how they form is unclear. We studied acute promyelocytic leukemia (APL) with the t(15;17) translocation that developed after treatment of breast or laryngeal cancer with chemotherapeutic agents that poison topoisomerase II.
Methods: We used long-range polymerase chain reaction and sequence analysis to characterize t(15;17) genomic breakpoints in therapy-related APL. To determine whether topoisomerase II was directly involved in mediating breaks of double-stranded DNA at the observed translocation breakpoints, we used a functional in vitro assay to examine topoisomerase II–mediated cleavage in the normal homologues of the PML and RARA breakpoints.
Results: Translocation breakpoints in APL that developed after exposure to mitoxantrone, a topoisomerase II poison, were tightly clustered in an 8-bp region within PML intron 6. In functional assays, this "hot spot" and the corresponding RARA breakpoints were common sites of mitoxantrone-induced cleavage by topoisomerase II. Etoposide and doxorubicin also induced cleavage by topoisomerase II at the translocation breakpoints in APL arising after exposure to these agents. Short, homologous sequences in PML and RARA suggested the occurrence of DNA repair by means of the nonhomologous end-joining pathway.
Conclusions: Drug-induced cleavage of DNA by topoisomerase II mediates the formation of chromosomal translocation breakpoints in mitoxantrone-related APL and in APL that occurs after therapy with other topoisomerase II poisons.
1529-1538
Mistry, Anita R.
3ba510ad-7e95-4d3d-8fa3-ea55bad24a4c
Felix, Carolyn A.
facbe9f3-411a-49a0-8e84-4b95ef87c053
Whitmarsh, Ryan J.
f654c2a1-0673-4856-b80a-0ee33cf13a47
Mason, Annabel
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Reiter, Andreas
ffa23e84-4a13-4cb5-aaf0-3fafe25dbede
Cassinat, Bruno
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Parry, Anne
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Walz, Christoph
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Wiemels, Joseph L.
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Segal, Mark R.
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Adès, Lionel
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Blair, Ian A.
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Osheroff, Neil
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Peniket, Andrew J.
a134984d-8b9c-4de8-b44e-635579f56ce9
Lafage-Pochitaloff, Marina
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Cross, Nicholas C.P.
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Chomienne, Christine
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Solomon, Ellen
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Fenaux, Pierre
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Grimwade, David
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Mistry, Anita R.
3ba510ad-7e95-4d3d-8fa3-ea55bad24a4c
Felix, Carolyn A.
facbe9f3-411a-49a0-8e84-4b95ef87c053
Whitmarsh, Ryan J.
f654c2a1-0673-4856-b80a-0ee33cf13a47
Mason, Annabel
c7b56e10-05ee-413d-962f-9e2a2c4e614d
Reiter, Andreas
ffa23e84-4a13-4cb5-aaf0-3fafe25dbede
Cassinat, Bruno
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Parry, Anne
65bb8b31-6dc0-40f9-9726-455cd8813e1c
Walz, Christoph
b8d235ac-2a38-41e7-a22f-e0bb78719b19
Wiemels, Joseph L.
894da244-7cf2-46bf-aebd-a2c7254d4ddb
Segal, Mark R.
3e615f10-d77b-4612-bd9d-afc73b53e992
Adès, Lionel
849fce6a-f294-4631-97c0-7f25ec01be20
Blair, Ian A.
a79ba3fe-8e88-4a89-8e31-d546942c1059
Osheroff, Neil
70ad1cc4-b71b-4b51-b30a-14621edf8cd9
Peniket, Andrew J.
a134984d-8b9c-4de8-b44e-635579f56ce9
Lafage-Pochitaloff, Marina
26af43da-edb3-4318-bc1a-4810a59fc039
Cross, Nicholas C.P.
f87650da-b908-4a34-b31b-d62c5f186fe4
Chomienne, Christine
adf9025f-fd73-4750-9d40-cb6a1301e41f
Solomon, Ellen
40fc664b-304f-4f6d-bbb5-e9fb3a738351
Fenaux, Pierre
b8c41c87-5626-4726-b298-95b71d172bfb
Grimwade, David
9f299c71-1e4c-42b1-9b39-d1e1ddc1dc26

Mistry, Anita R., Felix, Carolyn A., Whitmarsh, Ryan J., Mason, Annabel, Reiter, Andreas, Cassinat, Bruno, Parry, Anne, Walz, Christoph, Wiemels, Joseph L., Segal, Mark R., Adès, Lionel, Blair, Ian A., Osheroff, Neil, Peniket, Andrew J., Lafage-Pochitaloff, Marina, Cross, Nicholas C.P., Chomienne, Christine, Solomon, Ellen, Fenaux, Pierre and Grimwade, David (2005) DNA topoisomerase II in therapy-related acute promyelocytic leukemia. New England Journal of Medicine, 352 (15), 1529-1538.

Record type: Article

Abstract

Background: Chromosomal translocations leading to chimeric oncoproteins are important in leukemogenesis, but how they form is unclear. We studied acute promyelocytic leukemia (APL) with the t(15;17) translocation that developed after treatment of breast or laryngeal cancer with chemotherapeutic agents that poison topoisomerase II.
Methods: We used long-range polymerase chain reaction and sequence analysis to characterize t(15;17) genomic breakpoints in therapy-related APL. To determine whether topoisomerase II was directly involved in mediating breaks of double-stranded DNA at the observed translocation breakpoints, we used a functional in vitro assay to examine topoisomerase II–mediated cleavage in the normal homologues of the PML and RARA breakpoints.
Results: Translocation breakpoints in APL that developed after exposure to mitoxantrone, a topoisomerase II poison, were tightly clustered in an 8-bp region within PML intron 6. In functional assays, this "hot spot" and the corresponding RARA breakpoints were common sites of mitoxantrone-induced cleavage by topoisomerase II. Etoposide and doxorubicin also induced cleavage by topoisomerase II at the translocation breakpoints in APL arising after exposure to these agents. Short, homologous sequences in PML and RARA suggested the occurrence of DNA repair by means of the nonhomologous end-joining pathway.
Conclusions: Drug-induced cleavage of DNA by topoisomerase II mediates the formation of chromosomal translocation breakpoints in mitoxantrone-related APL and in APL that occurs after therapy with other topoisomerase II poisons.

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Published date: 2005

Identifiers

Local EPrints ID: 24868
URI: http://eprints.soton.ac.uk/id/eprint/24868
PURE UUID: 09a39f6f-6853-4e86-9cb9-5e41c7631da8
ORCID for Nicholas C.P. Cross: ORCID iD orcid.org/0000-0001-5481-2555

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Date deposited: 03 Apr 2006
Last modified: 23 Jul 2022 01:49

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Contributors

Author: Anita R. Mistry
Author: Carolyn A. Felix
Author: Ryan J. Whitmarsh
Author: Annabel Mason
Author: Andreas Reiter
Author: Bruno Cassinat
Author: Anne Parry
Author: Christoph Walz
Author: Joseph L. Wiemels
Author: Mark R. Segal
Author: Lionel Adès
Author: Ian A. Blair
Author: Neil Osheroff
Author: Andrew J. Peniket
Author: Marina Lafage-Pochitaloff
Author: Christine Chomienne
Author: Ellen Solomon
Author: Pierre Fenaux
Author: David Grimwade

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