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A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome

A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome
A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome
BACKGROUND: Idiopathic hypereosinophilic syndrome involves a prolonged state of eosinophilia associated with organ dysfunction. It is of unknown cause. Recent reports of responses to imatinib in patients with the syndrome suggested that an activated kinase such as ABL, platelet-derived growth factor receptor (PDGFR), or KIT, all of which are inhibited by imatinib, might be the cause. METHODS: We treated 11 patients with the hypereosinophilic syndrome with imatinib and identified the molecular basis for the response. RESULTS: Nine of the 11 patients treated with imatinib had responses lasting more than three months in which the eosinophil count returned to normal. One such patient had a complex chromosomal abnormality, leading to the identification of a fusion of the Fip1-like 1 (FIP1L1) gene to the PDGFRalpha (PDGFRA) gene generated by an interstitial deletion on chromosome 4q12. FIP1L1-PDGFRalpha is a constitutively activated tyrosine kinase that transforms hematopoietic cells and is inhibited by imatinib (50 percent inhibitory concentration, 3.2 nM). The FIP1L1-PDGFRA fusion gene was subsequently detected in 9 of 16 patients with the syndrome and in 5 of the 9 patients with responses to imatinib that lasted more than three months. Relapse in one patient correlated with the appearance of a T674I mutation in PDGFRA that confers resistance to imatinib. CONCLUSIONS: The hypereosinophilic syndrome may result from a novel fusion tyrosine kinase - FIP1L1-PDGFRalpha - that is a consequence of an interstitial chromosomal deletion. The acquisition of a T674I resistance mutation at the time of relapse demonstrates that FIP1L1-PDGFRalpha is the target of imatinib. Our data indicate that the deletion of genetic material may result in gain-of-function fusion proteins
research support, male, platelet-derived growth factor, mutation, pyrimidines, pair 4, u.s.gov't, remission induction, chromosome deletion, piperazines, middle aged, tyrosine, eosinophilia, genes, abnormalities, report, non-u.s.gov't, human, female, drug therapy, p.h.s., proteins, base sequence, antagonists & inhibitors, patients, genetic, protein, time, humans, evaluation studies, adult, protein-tyrosine kinase, enzyme inhibitors, growth, chromosomes, methods, hypereosinophilic syndrome, syndrome, recombination, molecular sequence data, genetics, therapeutic use
1201-1214
Cools, Jan
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DeAngelo, Daniel J.
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Gotlib, Jason
b9586ecc-826a-48aa-9a0d-32e871da28dd
Stover, Elizabeth H.
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Legare, Robert D.
7e536f02-9e5a-4473-8aae-1a1cec777d09
Cortes, Jorges
e97eb50f-4948-4682-bb2c-4546fa5a7fc0
Kutok, Jeffrey
6526ad3d-cb09-4882-acd5-22b875b153e2
Clark, Jennifer
3b5cd533-55d2-46b9-bfe3-f1a657af83ca
Galinsky, Ilene
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Griffin, James D.
8c209ae1-acb8-40e7-99a0-64cf4c4cd447
Cross, Nicholas C. P.
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Tefferi, Ayalew
772fe8d4-f061-4e7c-af13-91959ea634e5
Malone, James
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Alam, Rafeul
f9df0664-1b34-4c66-9abc-fffbe793be3b
Schrier, Stanley L.
e10d3f75-d204-4451-978f-8fdf85c0ae6b
Schmid, Janet
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Rose, Michal
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Vandenberghe, Peter
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Verhoef, Gregor
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Boogaerts, Marc
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Wlodarska, Iwona
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Kantarjian, Hagop
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Marynen, Peter
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Coutre, Steven E.
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Stone, Richard
eca33fd7-4fe8-4d5a-9983-8cb824134f34
Gilliland, D. Gary
eb6d954f-0e6e-411b-ac75-7c7dab6de745
Cools, Jan
5d132bb4-5780-44ae-8157-6eb412e9599d
DeAngelo, Daniel J.
4d5d5496-b850-4ab5-a57d-b13f3842582d
Gotlib, Jason
b9586ecc-826a-48aa-9a0d-32e871da28dd
Stover, Elizabeth H.
57a3512b-f84a-4bf6-8b36-cd6a0a93ae97
Legare, Robert D.
7e536f02-9e5a-4473-8aae-1a1cec777d09
Cortes, Jorges
e97eb50f-4948-4682-bb2c-4546fa5a7fc0
Kutok, Jeffrey
6526ad3d-cb09-4882-acd5-22b875b153e2
Clark, Jennifer
3b5cd533-55d2-46b9-bfe3-f1a657af83ca
Galinsky, Ilene
80a66c2d-6f31-4b7a-90fa-5c8040c565e5
Griffin, James D.
8c209ae1-acb8-40e7-99a0-64cf4c4cd447
Cross, Nicholas C. P.
f87650da-b908-4a34-b31b-d62c5f186fe4
Tefferi, Ayalew
772fe8d4-f061-4e7c-af13-91959ea634e5
Malone, James
3a5689e4-3c10-4b65-8d79-d379426d1676
Alam, Rafeul
f9df0664-1b34-4c66-9abc-fffbe793be3b
Schrier, Stanley L.
e10d3f75-d204-4451-978f-8fdf85c0ae6b
Schmid, Janet
e4678a1b-0499-40b1-9c24-102bd82735d3
Rose, Michal
05cf3a13-66c8-4050-96a8-7d19bb1c6189
Vandenberghe, Peter
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Verhoef, Gregor
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Boogaerts, Marc
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Wlodarska, Iwona
43a4d401-64a8-476a-8ff9-416363712f2e
Kantarjian, Hagop
644b92bc-918c-4fda-9ef8-739853934b4c
Marynen, Peter
0ce534df-3258-482a-9db8-54ced20ca12e
Coutre, Steven E.
ac43a40d-114a-4adb-bb5d-00d7356435be
Stone, Richard
eca33fd7-4fe8-4d5a-9983-8cb824134f34
Gilliland, D. Gary
eb6d954f-0e6e-411b-ac75-7c7dab6de745

Cools, Jan, DeAngelo, Daniel J., Gotlib, Jason, Stover, Elizabeth H., Legare, Robert D., Cortes, Jorges, Kutok, Jeffrey, Clark, Jennifer, Galinsky, Ilene, Griffin, James D., Cross, Nicholas C. P., Tefferi, Ayalew, Malone, James, Alam, Rafeul, Schrier, Stanley L., Schmid, Janet, Rose, Michal, Vandenberghe, Peter, Verhoef, Gregor, Boogaerts, Marc, Wlodarska, Iwona, Kantarjian, Hagop, Marynen, Peter, Coutre, Steven E., Stone, Richard and Gilliland, D. Gary (2003) A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome. New England Journal of Medicine, 348 (13), 1201-1214.

Record type: Article

Abstract

BACKGROUND: Idiopathic hypereosinophilic syndrome involves a prolonged state of eosinophilia associated with organ dysfunction. It is of unknown cause. Recent reports of responses to imatinib in patients with the syndrome suggested that an activated kinase such as ABL, platelet-derived growth factor receptor (PDGFR), or KIT, all of which are inhibited by imatinib, might be the cause. METHODS: We treated 11 patients with the hypereosinophilic syndrome with imatinib and identified the molecular basis for the response. RESULTS: Nine of the 11 patients treated with imatinib had responses lasting more than three months in which the eosinophil count returned to normal. One such patient had a complex chromosomal abnormality, leading to the identification of a fusion of the Fip1-like 1 (FIP1L1) gene to the PDGFRalpha (PDGFRA) gene generated by an interstitial deletion on chromosome 4q12. FIP1L1-PDGFRalpha is a constitutively activated tyrosine kinase that transforms hematopoietic cells and is inhibited by imatinib (50 percent inhibitory concentration, 3.2 nM). The FIP1L1-PDGFRA fusion gene was subsequently detected in 9 of 16 patients with the syndrome and in 5 of the 9 patients with responses to imatinib that lasted more than three months. Relapse in one patient correlated with the appearance of a T674I mutation in PDGFRA that confers resistance to imatinib. CONCLUSIONS: The hypereosinophilic syndrome may result from a novel fusion tyrosine kinase - FIP1L1-PDGFRalpha - that is a consequence of an interstitial chromosomal deletion. The acquisition of a T674I resistance mutation at the time of relapse demonstrates that FIP1L1-PDGFRalpha is the target of imatinib. Our data indicate that the deletion of genetic material may result in gain-of-function fusion proteins

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More information

Published date: 27 March 2003
Keywords: research support, male, platelet-derived growth factor, mutation, pyrimidines, pair 4, u.s.gov't, remission induction, chromosome deletion, piperazines, middle aged, tyrosine, eosinophilia, genes, abnormalities, report, non-u.s.gov't, human, female, drug therapy, p.h.s., proteins, base sequence, antagonists & inhibitors, patients, genetic, protein, time, humans, evaluation studies, adult, protein-tyrosine kinase, enzyme inhibitors, growth, chromosomes, methods, hypereosinophilic syndrome, syndrome, recombination, molecular sequence data, genetics, therapeutic use

Identifiers

Local EPrints ID: 59601
URI: http://eprints.soton.ac.uk/id/eprint/59601
PURE UUID: 3cbceea6-9d2e-4705-986a-9f8347d962e4
ORCID for Nicholas C. P. Cross: ORCID iD orcid.org/0000-0001-5481-2555

Catalogue record

Date deposited: 04 Sep 2008
Last modified: 23 Jul 2022 01:49

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Contributors

Author: Jan Cools
Author: Daniel J. DeAngelo
Author: Jason Gotlib
Author: Elizabeth H. Stover
Author: Robert D. Legare
Author: Jorges Cortes
Author: Jeffrey Kutok
Author: Jennifer Clark
Author: Ilene Galinsky
Author: James D. Griffin
Author: Ayalew Tefferi
Author: James Malone
Author: Rafeul Alam
Author: Stanley L. Schrier
Author: Janet Schmid
Author: Michal Rose
Author: Peter Vandenberghe
Author: Gregor Verhoef
Author: Marc Boogaerts
Author: Iwona Wlodarska
Author: Hagop Kantarjian
Author: Peter Marynen
Author: Steven E. Coutre
Author: Richard Stone
Author: D. Gary Gilliland

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