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A Modeled Hydrophobic Domain on the TCL1 Oncoprotein Mediates Association with AKT at the Cytoplasmic Membrane

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    A Modeled Hydrophobic Domain on the TCL1 Oncoprotein Mediates Association with AKT at the Cytoplasmic Membrane†
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    Department of Pathology and Laboratory Medicine, Microbiology and Immunology, UCLA-DOE Laboratory of Structural Biology and Molecular Medicine, Molecular Biology Institute and UCLA AIDS Institute, UCLA School of Medicine, Los Angeles, California 90095−1732
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    Biochemistry

    Cite this: Biochemistry 2002, 41, 20, 6376–6382
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    https://doi.org/10.1021/bi016068o
    Published April 17, 2002
    Copyright © 2002 American Chemical Society
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    Abstract

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    AKT has a critical role in relaying cell survival and proliferation signals initiated by ligand binding to surface receptors in mammalian cells. Induction of AKT serine/threonine kinase activity is augmented by the T-cell leukemia-1 (TCL1) oncoprotein through a physical association requiring the AKT pleckstrin homology domain. Here, we used molecular modeling and identified an exposed hydrophobic patch composed of two discontinuous amino acid stretches near one end of the TCL1 β-barrel that was required for a TCL1−AKT association. Site-directed mutations of this region did not affect TCL1 secondary structure, yet they disrupted interactions with AKT. This region was found in other members of the TCL1 oncoprotein family, such as TCL1b and MTCP1, and suggested a conserved, novel AKT binding domain. Interestingly, TCL1 and AKT co-localize in multiple cell compartments, but only extracts from the plasma membrane stimulate optimal complex formation in vitro. Identification of an AKT binding domain on TCL1 is an important step in deciphering the complex interactions that regulate AKT kinase activity in lymphocyte development and neoplasia within the immune system.

    Copyright © 2002 American Chemical Society

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    †

     This work was supported by an Amgen/UC BioStar Award (S98-35 to M.A.T.), a UCLA CFAR Award (S.W.F. and M.A.T.), the Lymphoma Research Foundation of America (M.A.T.), a PHSNS Award (T32-CA09056 to C.S.M.), and the National Institutes of Health (GM40185 to P.M. and CA74929 to M.A.T.).

    ‡

     Department of Pathology and Laboratory Medicine.

    §

     Microbiology and Immunology.

    ‖

     UCLA-DOE Laboratory of Structural Biology and Molecular Medicine.

    *

     To whom correspondence should be addressed:  Department of Pathology and Laboratory Medicine, UCLA School of Medicine, MacDonald Research Laboratories, Room 4-760, 675 Charles E. Young Drive South, Los Angeles, CA 90095-1732. Telephone:  310-206-6754. Fax:  310-267-0382. E-mail:  [email protected].

    #

     Molecular Biology Institute.

    ⊥

     UCLA AIDS Institute.

    Cited By

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    This article is cited by 28 publications.

    1. Siyu Sun, Wenjia Fang. Current understandings on T-cell prolymphocytic leukemia and its association with TCL1 proto-oncogene. Biomedicine & Pharmacotherapy 2020, 126 , 110107. https://doi.org/10.1016/j.biopha.2020.110107
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    6. Marco Herling, Kaushali A. Patel, Michael A. Teitell, Marina Konopleva, Farhad Ravandi, Ryuji Kobayashi, Dan Jones. High TCL1 expression and intact T-cell receptor signaling define a hyperproliferative subset of T-cell prolymphocytic leukemia. Blood 2008, 111 (1) , 328-337. https://doi.org/10.1182/blood-2007-07-101519
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    8. Masayuki Noguchi, Virginie Ropars, Christian Roumestand, Futoshi Suizu. Proto‐oncogene TCL1: more than just a coactivator for Akt. The FASEB Journal 2007, 21 (10) , 2273-2284. https://doi.org/10.1096/fj.06-7684com
    9. Samuel W. French, David W. Dawson, Hsiao-Wen Chen, Robert N. Rainey, Stuart A. Sievers, Cynthia E. Balatoni, Larry Wong, Joshua J. Troke, Mai T.N. Nguyen, Carla M. Koehler, Michael A. Teitell. The TCL1 oncoprotein binds the RNase PH domains of the PNPase exoribonuclease without affecting its RNA degrading activity. Cancer Letters 2007, 248 (2) , 198-210. https://doi.org/10.1016/j.canlet.2006.07.006
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    14. Makoto Hiromura, Futoshi Okada, Toshiyuki Obata, Daniel Auguin, Takeshi Shibata, Christian Roumestand, Masayuki Noguchi. Inhibition of Akt Kinase Activity by a Peptide Spanning the βA Strand of the Proto-oncogene TCL1. Journal of Biological Chemistry 2004, 279 (51) , 53407-53418. https://doi.org/10.1074/jbc.M403775200
    15. Michael A. Teitell, Pier Paolo Pandolfi. Lymphoid Malignancies. 2004https://doi.org/10.1002/0471675067.mmc014
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    17. Motoyasu Saji, Matthew D Ringel. Akt signaling in thyroid neoplasia. Current Opinion in Endocrinology & Diabetes 2004, 11 (4) , 197-204. https://doi.org/10.1097/01.med.0000137757.50167.ec
    18. Tony Petrella, Rein Willemze, Rein Willemze, Rein Willemze, Chris J.L.M. Meijer, Sophie Dalac, Rein Willemze, Rein Willemze, Tony Petrella. TCL1 and CLA Expression in Agranular CD4/CD56 Hematodermic Neoplasms (Blastic NK-Cell Lymphomas) and Leukemia Cutis. American Journal of Clinical Pathology 2004, 122 (2) , 307-313. https://doi.org/10.1309/0QPPAVTUPCV9UCLV
    19. Tony Petrella, Chris J.L.M. Meijer, Sophie Dalac, Rein Willemze, Marc Maynadié, Laurent Machet, Olivier Casasnovas, Béatrice Vergier, Michael A. Teitell. TCL1 and CLA Expression in Agranular CD4/CD56 Hematodermic Neoplasms (Blastic NK-Cell Lymphomas) and Leukemia Cutis. American Journal of Clinical Pathology 2004, 122 (2) , 307-313. https://doi.org/10.1309/0QPPAVTUPCV9UCLV
    20. Daniel Auguin, Philippe Barthe, Catherine Royer, Marc-Henri Stern, Masayuki Noguchi, Stefan T. Arold, Christian Roumestand. Structural Basis for the Co-activation of Protein Kinase B by T-cell Leukemia-1 (TCL1) Family Proto-oncoproteins. Journal of Biological Chemistry 2004, 279 (34) , 35890-35902. https://doi.org/10.1074/jbc.M400364200
    21. Jee-Yin Ahn, Rong Rong, Todd G. Kroll, Erwin G. Van Meir, Solomon H. Snyder, Keqiang Ye. PIKE (Phosphatidylinositol 3-Kinase Enhancer)-A GTPase Stimulates Akt Activity and Mediates Cellular Invasion. Journal of Biological Chemistry 2004, 279 (16) , 16441-16451. https://doi.org/10.1074/jbc.M312175200
    22. Richard B. Lock. TCL1: a new drug target in lymphoid and germ-cell malignancies?. The International Journal of Biochemistry & Cell Biology 2003, 35 (12) , 1614-1618. https://doi.org/10.1016/S1357-2725(03)00146-8
    23. Marco Herling, Michael A. Teitell, Rhine R. Shen, L. Jeffrey Medeiros, Dan Jones. TCL1 expression in plasmacytoid dendritic cells (DC2s) and the related CD4+ CD56+ blastic tumors of skin. Blood 2003, 101 (12) , 5007-5009. https://doi.org/10.1182/blood-2002-10-3297
    24. Michael R. Gold. Akt is TCL-ish: implications for B-cell lymphoma. Trends in Immunology 2003, 24 (3) , 104-108. https://doi.org/10.1016/S1471-4906(03)00022-X
    25. Yuri Pekarsky, Cora Hallas, Carlo M. Croce. Targeting Mature T Cell Leukemia. American Journal of PharmacoGenomics 2003, 3 (1) , 31-36. https://doi.org/10.2165/00129785-200303010-00005
    26. Samuel W. French, Cindy S. Malone, Rhine R. Shen, Mathilde Renard, Sarah E. Henson, Maurine D. Miner, Randolph Wall, Michael A. Teitell. Sp1 Transactivation of the TCL1 Oncogene. Journal of Biological Chemistry 2003, 278 (2) , 948-955. https://doi.org/10.1074/jbc.M207166200
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    28. Katrina K. Hoyer, Samuel W. French, Devin E. Turner, Mai T. N. Nguyen, Mathilde Renard, Cindy S. Malone, Sonja Knoetig, Chen-Feng Qi, Thomas T. Su, Hilde Cheroutre, Randolph Wall, David J. Rawlings, Herbert C. Morse, Michael A. Teitell. Dysregulated TCL1 promotes multiple classes of mature B cell lymphoma. Proceedings of the National Academy of Sciences 2002, 99 (22) , 14392-14397. https://doi.org/10.1073/pnas.212410199
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    Biochemistry

    Cite this: Biochemistry 2002, 41, 20, 6376–6382
    Click to copy citationCitation copied!
    https://doi.org/10.1021/bi016068o
    Published April 17, 2002
    Copyright © 2002 American Chemical Society
    Request reuse permissions

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