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Erschienen in: International Journal of Hematology 3/2018

17.10.2017 | Original Article

MAGI-1 expression is decreased in several types of human T-cell leukemia cell lines, including adult T-cell leukemia

verfasst von: Takashi Kozakai, Masahiko Takahashi, Masaya Higuchi, Toshifumi Hara, Kousuke Saito, Yuetsu Tanaka, Masayoshi Masuko, Jun Takizawa, Hirohito Sone, Masahiro Fujii

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

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Abstract

Membrane-associated guanylate kinase with inverted orientation protein 1 (MAGI-1) is a cytoplasmic scaffold protein that interacts with various signaling molecules; it negatively controls the cell growth of various types of cells and positively controls cell–cell interaction. In T cells, MAGI-1 has been shown to inhibit Akt activity through its interaction with PTEN and MEK1. In this study we found that MAGI-1 expression is decreased in multiple (9 out of 15) human T-cell leukemia cell lines, including adult T-cell leukemia (ATL), T-cell acute lymphoblastic leukemia and chronic T-cell lymphocytic leukemia. The overexpression of MAGI-1 protein in a MAGI-1-low ATL cell line reduced cellular growth. While the overexpression of MAGI-1 protein in a MAGI-1-low ATL cell line reduced the Akt and MEK activities, the knockdown of MAGI-1 in a MAGI-1-high ATL cell line augmented the Akt and MEK activities. Collectively, the findings of the present study suggest that the decreased expression of MAGI-1 in human T cells contributes to the development of several types of T-cell leukemia, partly through the stimulation of the Akt and MEK pathways.
Literatur
1.
Zurück zum Zitat Dobrosotskaya I, Guy RK, James GL. MAGI-1, a membrane-associated guanylate kinase with a unique arrangement of protein–protein interaction domains. J Biol Chem. 1997;272(50):31589–97.CrossRefPubMed Dobrosotskaya I, Guy RK, James GL. MAGI-1, a membrane-associated guanylate kinase with a unique arrangement of protein–protein interaction domains. J Biol Chem. 1997;272(50):31589–97.CrossRefPubMed
2.
Zurück zum Zitat Valiente M, Andres-Pons A, Gomar B, Torres J, Gil A, Tapparel C, et al. Binding of PTEN to specific PDZ domains contributes to PTEN protein stability and phosphorylation by microtubule-associated serine/threonine kinases. J Biol Chem. 2005;280(32):28936–43.CrossRefPubMed Valiente M, Andres-Pons A, Gomar B, Torres J, Gil A, Tapparel C, et al. Binding of PTEN to specific PDZ domains contributes to PTEN protein stability and phosphorylation by microtubule-associated serine/threonine kinases. J Biol Chem. 2005;280(32):28936–43.CrossRefPubMed
3.
Zurück zum Zitat Zmajkovicova K, Jesenberger V, Catalanotti F, Baumgartner C, Reyes G, Baccarini M. MEK1 is required for PTEN membrane recruitment, AKT regulation, and the maintenance of peripheral tolerance. Mol Cell. 2013;50(1):43–55.CrossRefPubMedPubMedCentral Zmajkovicova K, Jesenberger V, Catalanotti F, Baumgartner C, Reyes G, Baccarini M. MEK1 is required for PTEN membrane recruitment, AKT regulation, and the maintenance of peripheral tolerance. Mol Cell. 2013;50(1):43–55.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Latorre IJ, Roh MH, Frese KK, Weiss RS, Margolis B, Javier RT. Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J Cell Sci. 2005;118(Pt 18):4283–93.CrossRefPubMedPubMedCentral Latorre IJ, Roh MH, Frese KK, Weiss RS, Margolis B, Javier RT. Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J Cell Sci. 2005;118(Pt 18):4283–93.CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Yasunaga J, Matsuoka M. Leukemogenesis of adult T-cell leukemia. Int J Hematol. 2003;78(4):312–20.CrossRefPubMed Yasunaga J, Matsuoka M. Leukemogenesis of adult T-cell leukemia. Int J Hematol. 2003;78(4):312–20.CrossRefPubMed
7.
Zurück zum Zitat Matsuoka M, Yasunaga J. Human T-cell leukemia virus type 1: replication, proliferation and propagation by Tax and HTLV-1 bZIP factor. Curr Opin Virol. 2013;3(6):684–91.CrossRefPubMed Matsuoka M, Yasunaga J. Human T-cell leukemia virus type 1: replication, proliferation and propagation by Tax and HTLV-1 bZIP factor. Curr Opin Virol. 2013;3(6):684–91.CrossRefPubMed
8.
Zurück zum Zitat Akagi T, Ono H, Nyunoya H, Shimotohno K. Characterization of peripheral blood T-lymphocytes transduced with HTLV-I Tax mutants with different trans-activating phenotypes. Oncogene. 1997;14(17):2071–8.CrossRefPubMed Akagi T, Ono H, Nyunoya H, Shimotohno K. Characterization of peripheral blood T-lymphocytes transduced with HTLV-I Tax mutants with different trans-activating phenotypes. Oncogene. 1997;14(17):2071–8.CrossRefPubMed
9.
10.
Zurück zum Zitat Currer R, Van Duyne R, Jaworski E, Guendel I, Sampey G, Das R, et al. HTLV tax: a fascinating multifunctional co-regulator of viral and cellular pathways. Front Microbiol. 2012;3:406.CrossRefPubMedPubMedCentral Currer R, Van Duyne R, Jaworski E, Guendel I, Sampey G, Das R, et al. HTLV tax: a fascinating multifunctional co-regulator of viral and cellular pathways. Front Microbiol. 2012;3:406.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Makokha GN, Takahashi M, Higuchi M, Saito S, Tanaka Y, Fujii M. Human T-cell leukemia virus type 1 Tax protein interacts with and mislocalizes the PDZ domain protein MAGI-1. Cancer Sci. 2013;104(3):313–20.CrossRefPubMed Makokha GN, Takahashi M, Higuchi M, Saito S, Tanaka Y, Fujii M. Human T-cell leukemia virus type 1 Tax protein interacts with and mislocalizes the PDZ domain protein MAGI-1. Cancer Sci. 2013;104(3):313–20.CrossRefPubMed
12.
Zurück zum Zitat Iwanaga Y, Tsukahara T, Ohashi T, Tanaka Y, Arai M, Nakamura M, et al. Human T-cell leukemia virus type 1 tax protein abrogates interleukin-2 dependence in a mouse T-cell line. J Virol. 1999;73(2):1271–7.PubMedPubMedCentral Iwanaga Y, Tsukahara T, Ohashi T, Tanaka Y, Arai M, Nakamura M, et al. Human T-cell leukemia virus type 1 tax protein abrogates interleukin-2 dependence in a mouse T-cell line. J Virol. 1999;73(2):1271–7.PubMedPubMedCentral
13.
Zurück zum Zitat Tsubata C, Higuchi M, Takahashi M, Oie M, Tanaka Y, Gejyo F, et al. PDZ domain-binding motif of human T-cell leukemia virus type 1 Tax oncoprotein is essential for the interleukin 2 independent growth induction of a T-cell line. Retrovirology. 2005;2:46.CrossRefPubMedPubMedCentral Tsubata C, Higuchi M, Takahashi M, Oie M, Tanaka Y, Gejyo F, et al. PDZ domain-binding motif of human T-cell leukemia virus type 1 Tax oncoprotein is essential for the interleukin 2 independent growth induction of a T-cell line. Retrovirology. 2005;2:46.CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Yamada Y, Sugahara K, Tsuruda K, Nohda K, Hata T, Maeda T, et al. Fas-resistance in ATL cell lines not associated with HTLV-I or FAP-1 production. Cancer Lett. 1999;147(1–2):215–9.CrossRefPubMed Yamada Y, Sugahara K, Tsuruda K, Nohda K, Hata T, Maeda T, et al. Fas-resistance in ATL cell lines not associated with HTLV-I or FAP-1 production. Cancer Lett. 1999;147(1–2):215–9.CrossRefPubMed
15.
Zurück zum Zitat Hori T, Uchiyama T, Tsudo M, Umadome H, Ohno H, Fukuhara S, et al. Establishment of an interleukin 2-dependent human T cell line from a patient with T cell chronic lymphocytic leukemia who is not infected with human T cell leukemia/lymphoma virus. Blood. 1987;70(4):1069–72.PubMed Hori T, Uchiyama T, Tsudo M, Umadome H, Ohno H, Fukuhara S, et al. Establishment of an interleukin 2-dependent human T cell line from a patient with T cell chronic lymphocytic leukemia who is not infected with human T cell leukemia/lymphoma virus. Blood. 1987;70(4):1069–72.PubMed
16.
Zurück zum Zitat Higuchi M, Tsubata C, Kondo R, Yoshida S, Takahashi M, Oie M, et al. Cooperation of NF-kappaB2/p100 activation and the PDZ domain binding motif signal in human T-cell leukemia virus type 1 (HTLV-1) Tax1 but not HTLV-2 Tax2 is crucial for interleukin-2-independent growth transformation of a T-cell line. J Virol. 2007;81(21):11900–7.CrossRefPubMedPubMedCentral Higuchi M, Tsubata C, Kondo R, Yoshida S, Takahashi M, Oie M, et al. Cooperation of NF-kappaB2/p100 activation and the PDZ domain binding motif signal in human T-cell leukemia virus type 1 (HTLV-1) Tax1 but not HTLV-2 Tax2 is crucial for interleukin-2-independent growth transformation of a T-cell line. J Virol. 2007;81(21):11900–7.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Yasunaga J, Matsuoka M. Leukaemogenic mechanism of human T-cell leukaemia virus type I. Rev Med Virol. 2007;17(5):301–11.CrossRefPubMed Yasunaga J, Matsuoka M. Leukaemogenic mechanism of human T-cell leukaemia virus type I. Rev Med Virol. 2007;17(5):301–11.CrossRefPubMed
18.
Zurück zum Zitat Zaric J, Joseph JM, Tercier S, Sengstag T, Ponsonnet L, Delorenzi M, et al. Identification of MAGI1 as a tumor-suppressor protein induced by cyclooxygenase-2 inhibitors in colorectal cancer cells. Oncogene. 2012;31(1):48–59.CrossRefPubMed Zaric J, Joseph JM, Tercier S, Sengstag T, Ponsonnet L, Delorenzi M, et al. Identification of MAGI1 as a tumor-suppressor protein induced by cyclooxygenase-2 inhibitors in colorectal cancer cells. Oncogene. 2012;31(1):48–59.CrossRefPubMed
19.
Zurück zum Zitat Freeburn RW, Wright KL, Burgess SJ, Astoul E, Cantrell DA, Ward SG. Evidence that SHIP-1 contributes to phosphatidylinositol 3,4,5-trisphosphate metabolism in T lymphocytes and can regulate novel phosphoinositide 3-kinase effectors. J Immunol. 2002;169(10):5441–50.CrossRefPubMed Freeburn RW, Wright KL, Burgess SJ, Astoul E, Cantrell DA, Ward SG. Evidence that SHIP-1 contributes to phosphatidylinositol 3,4,5-trisphosphate metabolism in T lymphocytes and can regulate novel phosphoinositide 3-kinase effectors. J Immunol. 2002;169(10):5441–50.CrossRefPubMed
20.
Zurück zum Zitat Yoshita M, Higuchi M, Takahashi M, Oie M, Tanaka Y, Fujii M. Activation of mTOR by human T-cell leukemia virus type 1 Tax is important for the transformation of mouse T cells to interleukin-2-independent growth. Cancer Sci. 2012;103(2):369–74.CrossRefPubMed Yoshita M, Higuchi M, Takahashi M, Oie M, Tanaka Y, Fujii M. Activation of mTOR by human T-cell leukemia virus type 1 Tax is important for the transformation of mouse T cells to interleukin-2-independent growth. Cancer Sci. 2012;103(2):369–74.CrossRefPubMed
21.
Zurück zum Zitat Higuchi M, Takahashi M, Tanaka Y, Fujii M. Downregulation of proapoptotic Bim augments IL-2-independent T-cell transformation by human T-cell leukemia virus type-1 Tax. Cancer Med. 2014;3(6):1605–14.CrossRefPubMedPubMedCentral Higuchi M, Takahashi M, Tanaka Y, Fujii M. Downregulation of proapoptotic Bim augments IL-2-independent T-cell transformation by human T-cell leukemia virus type-1 Tax. Cancer Med. 2014;3(6):1605–14.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Feng X, Jia S, Martin TA, Jiang WG. Regulation and involvement in cancer and pathological conditions of MAGI1, a tight junction protein. Anticancer Res. 2014;34(7):3251–6.PubMed Feng X, Jia S, Martin TA, Jiang WG. Regulation and involvement in cancer and pathological conditions of MAGI1, a tight junction protein. Anticancer Res. 2014;34(7):3251–6.PubMed
23.
Zurück zum Zitat Kranjec C, Massimi P, Banks L. Restoration of MAGI-1 expression in human papillomavirus-positive tumor cells induces cell growth arrest and apoptosis. J Virol. 2014;88(13):7155–69.CrossRefPubMedPubMedCentral Kranjec C, Massimi P, Banks L. Restoration of MAGI-1 expression in human papillomavirus-positive tumor cells induces cell growth arrest and apoptosis. J Virol. 2014;88(13):7155–69.CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Zhang G, Liu T, Wang Z. Downregulation of MAGI1 associates with poor prognosis of hepatocellular carcinoma. J Investig Surg. 2012;25(2):93–9.CrossRef Zhang G, Liu T, Wang Z. Downregulation of MAGI1 associates with poor prognosis of hepatocellular carcinoma. J Investig Surg. 2012;25(2):93–9.CrossRef
25.
Zurück zum Zitat Zhang G, Wang Z. MAGI1 inhibits cancer cell migration and invasion of hepatocellular carcinoma via regulating PTEN. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2011;36(5):381–5.PubMed Zhang G, Wang Z. MAGI1 inhibits cancer cell migration and invasion of hepatocellular carcinoma via regulating PTEN. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2011;36(5):381–5.PubMed
26.
Zurück zum Zitat Nakahata S, Ichikawa T, Maneesaay P, Saito Y, Nagai K, Tamura T, et al. Loss of NDRG2 expression activates PI3K–AKT signalling via PTEN phosphorylation in ATLL and other cancers. Nat Commun. 2014;5:3393.CrossRefPubMedPubMedCentral Nakahata S, Ichikawa T, Maneesaay P, Saito Y, Nagai K, Tamura T, et al. Loss of NDRG2 expression activates PI3K–AKT signalling via PTEN phosphorylation in ATLL and other cancers. Nat Commun. 2014;5:3393.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Kataoka K, Nagata Y, Kitanaka A, Shiraishi Y, Shimamura T, Yasunaga J, et al. Integrated molecular analysis of adult T cell leukemia/lymphoma. Nat Genet. 2015;47(11):1304–15.CrossRefPubMed Kataoka K, Nagata Y, Kitanaka A, Shiraishi Y, Shimamura T, Yasunaga J, et al. Integrated molecular analysis of adult T cell leukemia/lymphoma. Nat Genet. 2015;47(11):1304–15.CrossRefPubMed
28.
Zurück zum Zitat Kotelevets L, Van Hengel J, Bruyneel E, Mareel M, Van Roy F, Chastre E. Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J. 2005;19(1):115–7.CrossRefPubMed Kotelevets L, Van Hengel J, Bruyneel E, Mareel M, Van Roy F, Chastre E. Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J. 2005;19(1):115–7.CrossRefPubMed
29.
Zurück zum Zitat Humbert P, Russell S, Richardson H. Dlg, Scribble and Lgl in cell polarity, cell proliferation and cancer. Bioessays: News Rev Mol Cell Dev Biol. 2003;25(6):542–53.CrossRef Humbert P, Russell S, Richardson H. Dlg, Scribble and Lgl in cell polarity, cell proliferation and cancer. Bioessays: News Rev Mol Cell Dev Biol. 2003;25(6):542–53.CrossRef
30.
Zurück zum Zitat Frese KK, Latorre IJ, Chung SH, Caruana G, Bernstein A, Jones SN, et al. Oncogenic function for the Dlg1 mammalian homolog of the Drosophila discs-large tumor suppressor. EMBO J. 2006;25(6):1406–17.CrossRefPubMedPubMedCentral Frese KK, Latorre IJ, Chung SH, Caruana G, Bernstein A, Jones SN, et al. Oncogenic function for the Dlg1 mammalian homolog of the Drosophila discs-large tumor suppressor. EMBO J. 2006;25(6):1406–17.CrossRefPubMedPubMedCentral
Metadaten
Titel
MAGI-1 expression is decreased in several types of human T-cell leukemia cell lines, including adult T-cell leukemia
verfasst von
Takashi Kozakai
Masahiko Takahashi
Masaya Higuchi
Toshifumi Hara
Kousuke Saito
Yuetsu Tanaka
Masayoshi Masuko
Jun Takizawa
Hirohito Sone
Masahiro Fujii
Publikationsdatum
17.10.2017
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/s12185-017-2359-1

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