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Erschienen in: International Journal of Hematology 3/2018

21.05.2018 | Original Article

Copy number abnormality of acute lymphoblastic leukemia cell lines based on their genetic subtypes

verfasst von: Chihiro Tomoyasu, Toshihiko Imamura, Toshihiro Tomii, Mio Yano, Daisuke Asai, Hiroaki Goto, Akira Shimada, Masashi Sanada, Shotaro Iwamoto, Junko Takita, Masayoshi Minegishi, Takeshi Inukai, Kanji Sugita, Hajime Hosoi

Erschienen in: International Journal of Hematology | Ausgabe 3/2018

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Abstract

In this study, we performed genetic analysis of 83 B cell precursor acute lymphoblastic leukemia (B-ALL) cell lines. First, we performed multiplex ligation-dependent probe amplification analysis to identify copy number abnormalities (CNAs) in eight genes associated with B-ALL according to genetic subtype. In Ph+ B-ALL cell lines, the frequencies of IKZF1, CDKN2A/2B, BTG1, and PAX5 deletion were significantly higher than those in Ph B-ALL cell lines. The frequency of CDKN2A/2B deletion in KMT2A rearranged cell lines was significantly lower than that in non-KMT2A rearranged cell lines. These findings suggest that CNAs are correlated with genetic subtype in B-ALL cell lines. In addition, we determined that three B-other ALL cell lines had IKZF1 deletions (YCUB-5, KOPN49, and KOPN75); we therefore performed comprehensive genetic analysis of these cell lines. YCUB-5, KOPN49, and KOPN75 had P2RY8-CRLF2, IgH-CRLF2, and PAX5-ETV6 fusions, respectively. Moreover, targeted capture sequencing revealed that YCUB-5 had JAK2 R683I and KRAS G12D, and KOPN49 had JAK2 R683G and KRAS G13D mutations. These data may contribute to progress in the field of leukemia research.
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Literatur
1.
Zurück zum Zitat Liem NL, Papa RA, Milross CG, Schmid MA, Tajbakhsh M, Choi S, et al. Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood. 2004;103(10):3905–14.CrossRefPubMed Liem NL, Papa RA, Milross CG, Schmid MA, Tajbakhsh M, Choi S, et al. Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood. 2004;103(10):3905–14.CrossRefPubMed
2.
Zurück zum Zitat McCormack E, Bruserud O, Gjertsen BT. Animal models of acute myelogenous leukaemia—development, application and future perspectives. Leukemia. 2005;19(5):687–706.CrossRefPubMed McCormack E, Bruserud O, Gjertsen BT. Animal models of acute myelogenous leukaemia—development, application and future perspectives. Leukemia. 2005;19(5):687–706.CrossRefPubMed
3.
Zurück zum Zitat Maude SL, Tasian SK, Vincent T, Hall JW, Sheen C, Roberts KG, et al. Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 2012;120(17):3510–8.CrossRefPubMedPubMedCentral Maude SL, Tasian SK, Vincent T, Hall JW, Sheen C, Roberts KG, et al. Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 2012;120(17):3510–8.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST, et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 2009;10(2):125–34.CrossRef Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST, et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 2009;10(2):125–34.CrossRef
5.
Zurück zum Zitat Roberts KG, Li Y, Payne-Turner D, Harvey RC, Yang YL, Pei D, McCastlain K, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. New Engl J of Med. 2014;371:1005–15.CrossRef Roberts KG, Li Y, Payne-Turner D, Harvey RC, Yang YL, Pei D, McCastlain K, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. New Engl J of Med. 2014;371:1005–15.CrossRef
6.
Zurück zum Zitat Hirose M, Minato K, Tobinai K, Ohira M, Ise T, Watanabe S, Shimoyama M, Taniwaki M, Abe T. A novel pre-T cell line derived from acute lymphoblastic leukemia. Gan. 1982;73(4):600–5.PubMed Hirose M, Minato K, Tobinai K, Ohira M, Ise T, Watanabe S, Shimoyama M, Taniwaki M, Abe T. A novel pre-T cell line derived from acute lymphoblastic leukemia. Gan. 1982;73(4):600–5.PubMed
7.
Zurück zum Zitat Minegishi M, Tsuchiya S, Minegishi N, Konno T. Establishment of five human malignant non-T lymphoid cell lines and mixed lymphocyte-tumor reaction. Tohoku J Exp Med. 1987;151:283–92.CrossRefPubMed Minegishi M, Tsuchiya S, Minegishi N, Konno T. Establishment of five human malignant non-T lymphoid cell lines and mixed lymphocyte-tumor reaction. Tohoku J Exp Med. 1987;151:283–92.CrossRefPubMed
8.
Zurück zum Zitat Kawamura M, Kikuchi A, Kobayashi S, Hanada R, Yamamoto K, Horibe K, et al. Mutations of the p53 and ras genes in childhood t(1;19)-acute lymphoblastic leukemia. Blood. 1995;85(9):2546–52.PubMed Kawamura M, Kikuchi A, Kobayashi S, Hanada R, Yamamoto K, Horibe K, et al. Mutations of the p53 and ras genes in childhood t(1;19)-acute lymphoblastic leukemia. Blood. 1995;85(9):2546–52.PubMed
9.
Zurück zum Zitat Ariyasu T, Matsuo Y, Harashima A, Nakamura S, Takaba S, Tsubota T, et al. Establishment and characterization of “biphenotypic” acute leukemia cell lines with a variant Ph translocation t(9;22;10) (q34;q11;q22). Hum Cell. 1998;11(1):43–50.PubMed Ariyasu T, Matsuo Y, Harashima A, Nakamura S, Takaba S, Tsubota T, et al. Establishment and characterization of “biphenotypic” acute leukemia cell lines with a variant Ph translocation t(9;22;10) (q34;q11;q22). Hum Cell. 1998;11(1):43–50.PubMed
10.
Zurück zum Zitat Kang J, Kisenge RR, Toyoda H, Tanaka S, Bu J, Azuma E, et al. Chemical sensitization and regulation of TRAIL-induced apoptosis in a panel of B-lymphocytic leukaemia cell lines. Br J Haematol. 2003;123:921–32.CrossRefPubMed Kang J, Kisenge RR, Toyoda H, Tanaka S, Bu J, Azuma E, et al. Chemical sensitization and regulation of TRAIL-induced apoptosis in a panel of B-lymphocytic leukaemia cell lines. Br J Haematol. 2003;123:921–32.CrossRefPubMed
11.
Zurück zum Zitat Goto H, Naruto T, Tanoshima R, Kato H, Yokosuka T, Yanagimachi M, et al. Chemo-sensitivity in a panel of B-cell precursor acute lymphoblastic leukemia cell lines, YCUB series, derived from children. Leu Res. 2009;33:1386–91.CrossRef Goto H, Naruto T, Tanoshima R, Kato H, Yokosuka T, Yanagimachi M, et al. Chemo-sensitivity in a panel of B-cell precursor acute lymphoblastic leukemia cell lines, YCUB series, derived from children. Leu Res. 2009;33:1386–91.CrossRef
12.
Zurück zum Zitat Hirase C, Maeda Y, Takai S, Kanamaru A. Hypersensitivity of Ph-positive lymphoid cell lines to rapamycin: possible clinical application of mTOR inhibitor. Leuk Res. 2009;33:450–9.CrossRefPubMed Hirase C, Maeda Y, Takai S, Kanamaru A. Hypersensitivity of Ph-positive lymphoid cell lines to rapamycin: possible clinical application of mTOR inhibitor. Leuk Res. 2009;33:450–9.CrossRefPubMed
13.
Zurück zum Zitat Shiotsu Y, Kiyoi H, Ishikawa Y, Tanizaki R, Shimizu M, Umehara H, et al. KW-2449, a novel multikinase inhibitor, suppresses the growth of leukemia cells with FLT3 mutations or T315I-mutated BCR/ABL translocation. Blood. 2009;114:1607–17.CrossRefPubMed Shiotsu Y, Kiyoi H, Ishikawa Y, Tanizaki R, Shimizu M, Umehara H, et al. KW-2449, a novel multikinase inhibitor, suppresses the growth of leukemia cells with FLT3 mutations or T315I-mutated BCR/ABL translocation. Blood. 2009;114:1607–17.CrossRefPubMed
14.
Zurück zum Zitat Hirose K, Inukai T, Kikuchi J, Furukawa Y, Ikawa T, Kawamoto H, et al. Aberrant induction of LMO2 by the E2A-HLF chimeric transcription factor and its implication in leukemogenesis of B-precursor ALL with t(17;19). Blood 2010;116:962–70.CrossRef Hirose K, Inukai T, Kikuchi J, Furukawa Y, Ikawa T, Kawamoto H, et al. Aberrant induction of LMO2 by the E2A-HLF chimeric transcription factor and its implication in leukemogenesis of B-precursor ALL with t(17;19). Blood 2010;116:962–70.CrossRef
15.
Zurück zum Zitat Okabe S, Tauchi T, Ohyashiki K. Establishment of a new Philadelphia chromosome-positive acute lymphoblastic leukemia cell line (SK-9) with T315I mutation. Exp Hematol. 2010;38:765–72.CrossRefPubMed Okabe S, Tauchi T, Ohyashiki K. Establishment of a new Philadelphia chromosome-positive acute lymphoblastic leukemia cell line (SK-9) with T315I mutation. Exp Hematol. 2010;38:765–72.CrossRefPubMed
16.
Zurück zum Zitat Akbari Moqadam F, Boer JM, Lange-Turenhout EA, Pieters R, den Boer ML. Altered expression of miR-24, miR-126 and miR-365 does not affect viability of childhood TCF3-rearranged leukemia cells. Leukemia. 2014;28(5):1008–14.CrossRefPubMed Akbari Moqadam F, Boer JM, Lange-Turenhout EA, Pieters R, den Boer ML. Altered expression of miR-24, miR-126 and miR-365 does not affect viability of childhood TCF3-rearranged leukemia cells. Leukemia. 2014;28(5):1008–14.CrossRefPubMed
17.
Zurück zum Zitat Asai D, Imamura T, Suenobu S, Saito A, Hasegawa D, Deguchi T, et al. IKZF1 deletion is associated with a poor outcome in pediatric B-cell precursor acute lymphoblastic leukemia in Japan. Cancer Med. 2013;2:412–9.CrossRefPubMedPubMedCentral Asai D, Imamura T, Suenobu S, Saito A, Hasegawa D, Deguchi T, et al. IKZF1 deletion is associated with a poor outcome in pediatric B-cell precursor acute lymphoblastic leukemia in Japan. Cancer Med. 2013;2:412–9.CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Roberts KG, Morin RD, Zhang J, Hirst M, Zhao Y, Su X, et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell. 2012;22(2):153–66.CrossRefPubMedPubMedCentral Roberts KG, Morin RD, Zhang J, Hirst M, Zhao Y, Su X, et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell. 2012;22(2):153–66.CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Ishida H, Kanamitsu K, Washio K, Muraoka M, Sakakibara K, Matsubara T, et al. Relapsed infant MLL-rearranged acute lymphoblastic leukemia with additional genetic alterations. Pediatr Blood Cancer. 2016;63(11):2059–60.CrossRefPubMed Ishida H, Kanamitsu K, Washio K, Muraoka M, Sakakibara K, Matsubara T, et al. Relapsed infant MLL-rearranged acute lymphoblastic leukemia with additional genetic alterations. Pediatr Blood Cancer. 2016;63(11):2059–60.CrossRefPubMed
20.
Zurück zum Zitat Schwab CJ, Chilton L, Morrison H, Jones L, Al-Shehhi H, Erhorn A, et al. Genes commonly deleted in childhood B-cell precursor acute lymphoblastic leukemia: association with cytogenetics and clinical features. Haematologica. 2013;98(7):1081–8.CrossRefPubMedPubMedCentral Schwab CJ, Chilton L, Morrison H, Jones L, Al-Shehhi H, Erhorn A, et al. Genes commonly deleted in childhood B-cell precursor acute lymphoblastic leukemia: association with cytogenetics and clinical features. Haematologica. 2013;98(7):1081–8.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Imamura T, Kiyokawa N, Kato M, Imai C, Okamoto Y, Yano M, et al. Characterization of pediatric Philadelphia-negative B-cell precursor acute lymphoblastic leukemia with kinase fusions in Japan. Blood Cancer J. 2016;6:e419.CrossRefPubMedPubMedCentral Imamura T, Kiyokawa N, Kato M, Imai C, Okamoto Y, Yano M, et al. Characterization of pediatric Philadelphia-negative B-cell precursor acute lymphoblastic leukemia with kinase fusions in Japan. Blood Cancer J. 2016;6:e419.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Reshmi SC, Harvey RC, Roberts KG, Stonerock E, Smith A, Jenkins H, et al. Targetable kinase gene fusions in high-risk B-ALL: a study from the Children’s Oncology Group. Blood. 2017;129(25):3352–61.PubMedPubMedCentral Reshmi SC, Harvey RC, Roberts KG, Stonerock E, Smith A, Jenkins H, et al. Targetable kinase gene fusions in high-risk B-ALL: a study from the Children’s Oncology Group. Blood. 2017;129(25):3352–61.PubMedPubMedCentral
23.
Zurück zum Zitat Kim WY, Sharpless NE. The regulation of INK4/ARF in cancer and aging. Cell. 2006;127(2):265–75.CrossRefPubMed Kim WY, Sharpless NE. The regulation of INK4/ARF in cancer and aging. Cell. 2006;127(2):265–75.CrossRefPubMed
24.
Zurück zum Zitat van Zutven LJ, van Drunen E, de Bont JM, Wattel MM, Den Boer ML, Pieters R, et al. CDKN2 deletions have no prognostic value in childhood precursor-B acute lymphoblastic leukaemia. Leukemia. 2005;19(7):1281–4.CrossRefPubMed van Zutven LJ, van Drunen E, de Bont JM, Wattel MM, Den Boer ML, Pieters R, et al. CDKN2 deletions have no prognostic value in childhood precursor-B acute lymphoblastic leukaemia. Leukemia. 2005;19(7):1281–4.CrossRefPubMed
25.
Zurück zum Zitat Braun M, Pastorczak A, Fendler W, Madzio J, Tomasik B, Taha J, et al. Biallelic loss of CDKN2A is associated with poor response to treatment in pediatric acute lymphoblastic leukemia. Leuk Lymphoma. 2017;58(5):1162–71.CrossRefPubMed Braun M, Pastorczak A, Fendler W, Madzio J, Tomasik B, Taha J, et al. Biallelic loss of CDKN2A is associated with poor response to treatment in pediatric acute lymphoblastic leukemia. Leuk Lymphoma. 2017;58(5):1162–71.CrossRefPubMed
26.
Zurück zum Zitat Churchman ML, Low J, Qu C, Paietta EM, Kasper LH, Chang Y, et al. Efficacy of retinoids in IKZF1-mutated BCR-ABL1 acute lymphoblastic leukemia. Cancer Cell. 2015;28(3):343–56.CrossRefPubMedPubMedCentral Churchman ML, Low J, Qu C, Paietta EM, Kasper LH, Chang Y, et al. Efficacy of retinoids in IKZF1-mutated BCR-ABL1 acute lymphoblastic leukemia. Cancer Cell. 2015;28(3):343–56.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Rouault JP, Rimokh R, Tessa C, Paranhos G, Ffrench M, Duret L, et al. BTG1, a member of a new family of antiproliferative genes. EMBO J. 1992;11(4):1663–70.PubMedPubMedCentralCrossRef Rouault JP, Rimokh R, Tessa C, Paranhos G, Ffrench M, Duret L, et al. BTG1, a member of a new family of antiproliferative genes. EMBO J. 1992;11(4):1663–70.PubMedPubMedCentralCrossRef
28.
Zurück zum Zitat Scheijen B, Boer JM, Marke R, Tijchon E, van Ingen Schenau D, Waanders E, et al. Tumor suppressors BTG1 and IKZF1 cooperate during mouse leukemia development and increase relapse risk in B-cell precursor acute lymphoblastic leukemia patients. Haematologica. 2017;102(3):541–51.CrossRefPubMedPubMedCentral Scheijen B, Boer JM, Marke R, Tijchon E, van Ingen Schenau D, Waanders E, et al. Tumor suppressors BTG1 and IKZF1 cooperate during mouse leukemia development and increase relapse risk in B-cell precursor acute lymphoblastic leukemia patients. Haematologica. 2017;102(3):541–51.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Cazzaniga G, Daniotti M, Tosi S, Giudici G, Aloisi A, Pogliani E, et al. The paired box domain gene PAX5 is fused to ETV6/TEL in an acute lymphoblastic leukemia case. Cancer Res. 2001;61(12):4666–70.PubMed Cazzaniga G, Daniotti M, Tosi S, Giudici G, Aloisi A, Pogliani E, et al. The paired box domain gene PAX5 is fused to ETV6/TEL in an acute lymphoblastic leukemia case. Cancer Res. 2001;61(12):4666–70.PubMed
30.
Zurück zum Zitat Strehl S, König M, Dworzak MN, Kalwak K, Haas OA. PAX5/ETV6 fusion defines cytogenetic entity dic(9;12)(p13;p13). Leukemia. 2003;17(6):1121–3.CrossRefPubMed Strehl S, König M, Dworzak MN, Kalwak K, Haas OA. PAX5/ETV6 fusion defines cytogenetic entity dic(9;12)(p13;p13). Leukemia. 2003;17(6):1121–3.CrossRefPubMed
31.
Zurück zum Zitat Fazio G, Cazzaniga V, Palmi C, Galbiati M, Giordan M, te Kronnie G, et al. PAX5/ETV6 alters the gene expression profile of precursor B cells with opposite dominant effect on endogenous PAX5. Leukemia. 2013;27(4):992–5.CrossRefPubMed Fazio G, Cazzaniga V, Palmi C, Galbiati M, Giordan M, te Kronnie G, et al. PAX5/ETV6 alters the gene expression profile of precursor B cells with opposite dominant effect on endogenous PAX5. Leukemia. 2013;27(4):992–5.CrossRefPubMed
32.
Zurück zum Zitat Chen IM, Harvey RC, Mullighan CG, Gastier-Foster J, Wharton W, Kang H, et al. Outcome modeling with CRLF2, IKZF1, JAK, and minimal residual disease in pediatric acute lymphoblastic leukemia: a Children’s Oncology Group study. Blood. 2012;119(15):3512–22.CrossRefPubMedPubMedCentral Chen IM, Harvey RC, Mullighan CG, Gastier-Foster J, Wharton W, Kang H, et al. Outcome modeling with CRLF2, IKZF1, JAK, and minimal residual disease in pediatric acute lymphoblastic leukemia: a Children’s Oncology Group study. Blood. 2012;119(15):3512–22.CrossRefPubMedPubMedCentral
Metadaten
Titel
Copy number abnormality of acute lymphoblastic leukemia cell lines based on their genetic subtypes
verfasst von
Chihiro Tomoyasu
Toshihiko Imamura
Toshihiro Tomii
Mio Yano
Daisuke Asai
Hiroaki Goto
Akira Shimada
Masashi Sanada
Shotaro Iwamoto
Junko Takita
Masayoshi Minegishi
Takeshi Inukai
Kanji Sugita
Hajime Hosoi
Publikationsdatum
21.05.2018
Verlag
Springer Japan
Erschienen in
International Journal of Hematology / Ausgabe 3/2018
Print ISSN: 0925-5710
Elektronische ISSN: 1865-3774
DOI
https://doi.org/10.1007/s12185-018-2474-7

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