Cancer Letters
Volume 248, Issue 2 , Pages 198-210 , 18 April 2007

The TCL1 oncoprotein binds the RNase PH domains of the PNPase exoribonuclease without affecting its RNA degrading activity

  • Samuel W. French

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • David W. Dawson

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • Hsiao-Wen Chen

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • Robert N. Rainey

      Affiliations

    • Department of Chemistry and Biochemistry, UCLA, Los Angeles, CA 90095-1569, USA
    • ,
  • Stuart A. Sievers

      Affiliations

    • Department of Chemistry and Biochemistry, UCLA, Los Angeles, CA 90095-1569, USA
    • ,
  • Cynthia E. Balatoni

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • Larry Wong

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • Joshua J. Troke

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • Mai T.N. Nguyen

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • ,
  • Carla M. Koehler

      Affiliations

    • Department of Chemistry and Biochemistry, UCLA, Los Angeles, CA 90095-1569, USA
    • Molecular Biology Institute and Jonsson Comprehensive Cancer Center, UCLA, Los Angeles, CA 90095, USA
    • ,
  • Michael A. Teitell

      Affiliations

    • Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095-1732, USA
    • Molecular Biology Institute and Jonsson Comprehensive Cancer Center, UCLA, Los Angeles, CA 90095, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 310 206 6754; fax: +1 310 267 0382.

Received 12 April 2006 ,Accepted 13 July 2006.

References 

  1. Teitell MA. The TCL1 family of oncoproteins: co-activators of transformation. Nat. Rev. Cancer. 2005;5:640
  2. Auguin D, Barthe P, Royer C, Stern MH, Noguchi M, Arold ST, et al. Structural basis for the co-activation of protein kinase B by T-cell leukemia-1 (TCL1) family proto-oncoproteins. J. Biol. Chem. 2004;279:35890
  3. Hoyer KK, French SW, Turner DE, Nguyen MT, Renard M, Malone CS, et al. Dysregulated TCL1 promotes multiple classes of mature B cell lymphoma. Proc. Natl. Acad. Sci. USA. 2002;99:14392
  4. Laine J, Kunstle G, Obata T, Sha M, Noguchi M. The protooncogene TCL1 is an Akt kinase coactivator. Mol. Cell. 2000;6:395
  5. Pekarsky Y, Koval A, Hallas C, Bichi R, Tresini M, Malstrom S, et al. Tcl1 enhances Akt kinase activity and mediates its nuclear translocation. Proc. Natl. Acad. Sci. USA. 2000;97:3028
  6. Leszczyniecka M, Su ZZ, Kang DC, Sarkar D, Fisher PB. Expression regulation and genomic organization of human polynucleotide phosphorylase, hPNPase(old-35), a Type I interferon inducible early response gene. Gene. 2003;316:143
  7. Leszczyniecka M, Kang DC, Sarkar D, Su ZZ, Holmes M, Valerie K, et al. Identification and cloning of human polynucleotide phosphorylase, hPNPase old-35, in the context of terminal differentiation and cellular senescence. Proc. Natl. Acad. Sci. USA. 2002;99:16636
  8. Teitell M, Damore MA, Sulur GG, Turner DE, Stern MH, Said JW, et al. TCL1 oncogene expression in AIDS-related lymphomas and lymphoid tissues. Proc. Natl. Acad. Sci. USA. 1999;96:9809
  9. Said JW, Hoyer KK, French SW, Rosenfelt L, Garcia-Lloret M, Koh PJ, et al. TCL1 oncogene expression in B cell subsets from lymphoid hyperplasia and distinct classes of B cell lymphoma. Lab Invest. 2001;81:555
  10. French SW, Shen RR, Koh PJ, Malone CS, Mallick P, Teitell MA. A modeled hydrophobic domain on the TCL1 oncoprotein mediates association with AKT at the cytoplasmic membrane. Biochemistry. 2002;41:6376
  11. Chen CY, Gherzi R, Andersen JS, Gaietta G, Jurchott K, Royer HD, et al. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 2000;14:1236
  12. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, et al. UniProt: the Universal Protein knowledgebase. Nucleic Acids Res. 2004;32:D115
  13. Bairoch A, Apweiler R, Wu CH, Barker WC, Boeckmann B, Ferro S, et al. The Universal Protein Resource (UniProt). Nucleic Acids Res. 2005;33:D154
  14. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, et al. The Protein Data Bank. Nucleic Acids Res. 2000;28:235
  15. Symmons MF, Jones GH, Luisi BF. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure Fold Des. 2000;8:1215
  16. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403
  17. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673
  18. Kelley LA, MacCallum RM, Sternberg MJ. Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 2000;299:499
  19. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993;234:779
  20. Fiser A, Do RK, Sali A. Modeling of loops in protein structures. Protein Sci. 2000;9:1753
  21. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 2000;29:291
  22. Laskowski RA, Moss DS, Thornton JM. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 1993;231:1049
  23. Vriend G. WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 1990;8:52
  24. Rodriguez R, Chinea G, Lopez N, Pons T, Vriend G. Homology modeling, model and software evaluation: three related resources. Bioinformatics. 1998;14:523
  25. Kleywegt GJ. Use of non-crystallographic symmetry in protein structure refinement. Acta. Crystallogr. D. Biol. Crystallogr. 1996;52:842
  26. Hoh F, Yang YS, Guignard L, Padilla A, Stern MH, Lhoste JM, et al. Crystal structure of p14TCL1, an oncogene product involved in T-cell prolymphocytic leukemia, reveals a novel beta-barrel topology. Structure. 1998;6:147
  27. Gabb HA, Jackson RM, Sternberg MJ. Modelling protein docking using shape complementarity, electrostatics and biochemical information. J. Mol. Biol. 1997;272:106
  28. Moont G, Gabb HA, Sternberg MJ. Use of pair potentials across protein interfaces in screening predicted docked complexes. Proteins. 1999;35:364
  29. Jackson RM, Gabb HA, Sternberg MJ. Rapid refinement of protein interfaces incorporating solvation: application to the docking problem. J. Mol. Biol. 1998;276:265
  30. Narducci MG, Pescarmona E, Lazzeri C, Signoretti S, Lavinia AM, Remotti D, et al. Regulation of TCL1 expression in B- and T-cell lymphomas and reactive lymphoid tissues. Cancer Res. 2000;60:2095
  31. Raijmakers R, Egberts WV, van Venrooij WJ, Pruijn GJ. Protein-protein interactions between human exosome components support the assembly of RNase PH-type subunits into a six-membered PNPase-like ring. J. Mol. Biol. 2002;323:653
  32. Baginsky S, Shteiman-Kotler A, Liveanu V, Yehudai-Resheff S, Bellaoui M, Settlage RE, et al. Chloroplast PNPase exists as a homo-multimer enzyme complex that is distinct from the Escherichia coli degradosome. RNA. 2001;7:1464
  33. Symmons MF, Williams MG, Luisi BF, Jones GH, Carpousis AJ. Running rings around RNA: a superfamily of phosphate-dependent RNases. Trends Biochem. Sci. 2002;27:11
  34. Lisitsky I, Kotler A, Schuster G. The mechanism of preferential degradation of polyadenylated RNA in the chloroplast. The exoribonuclease 100RNP/polynucleotide phosphorylase displays high binding affinity for poly(A) sequence. J. Biol. Chem. 1997;272:17648
  35. Yehudai-Resheff S, Portnoy V, Yogev S, Adir N, Schuster G. Domain analysis of the chloroplast polynucleotide phosphorylase reveals discrete functions in RNA degradation, polyadenylation, and sequence homology with exosome proteins. Plant Cell. 2003;15:2003
  36. Sarkar D, Park ES, Emdad L, Randolph A, Valerie K, Fisher PB. Defining the domains of human polynucleotide phosphorylase (hPNPaseOLD-35) mediating cellular senescence. Mol. Cell. Biol. 2005;25:7333
  37. Sarkar D, Park ES, Fisher PB. Defining the mechanism by which IFN-beta dowregulates c-myc expression in human melanoma cells: pivotal role for human polynucleotide phosphorylase (hPNPase(old-35)). Cell Death Differ. 2006;
  38. Nagaike T, Suzuki T, Katoh T, Ueda T. Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem. 2005;280:19721
  39. Kang SM, Narducci MG, Lazzeri C, Mongiovi AM, Caprini E, Bresin A, et al. Impaired T- and B-cell development in Tcl1-deficient mice. Blood. 2005;105:1288
  40. Suzuki A, Kaisho T, Ohishi M, Tsukio-Yamaguchi M, Tsubata T, Koni PA, et al. Critical roles of Pten in B cell homeostasis and immunoglobulin class switch recombination. J. Exp. Med. 2003;197:657
  41. Miyauchi H, Minamino T, Tateno K, Kunieda T, Toko H, Komuro I. Akt negatively regulates the in vitro lifespan of human endothelial cells via a p53/p21-dependent pathway. Embo J. 2004;23:212
  42. Carpousis AJ. The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes. Biochem. Soc. Trans. 2002;30:150
  43. Blum E, Py B, Carpousis AJ, Higgins CF. Polyphosphate kinase is a component of the Escherichia coli RNA degradosome. Mol. Microbiol. 1997;26:387
  44. Miczak A, Kaberdin VR, Wei CL, Lin-Chao S. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. USA. 1996;93:3865
  45. Py B, Higgins CF, Krisch HM, Carpousis AJ. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature. 1996;381:169
  46. Baginsky S, Gruissem W. Endonucleolytic activation directs dark-induced chloroplast mRNA degradation. Nucleic Acids Res. 2002;30:4527
  47. Li QS, Gupta JD, Hunt AG. Polynucleotide phosphorylase is a component of a novel plant poly(A) polymerase. J. Biol. Chem. 1998;273:17539
  48. Yehudai-Resheff S, Hirsh M, Schuster G. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell. Biol. 2001;21:5408
  49. Mendez R, Leplae R, Lensink MF, Wodak SJ. Assessment of CAPRI predictions in rounds 3-5 shows progress in docking procedures. Proteins. 2005;60:150
  50. Mendez R, Leplae R, De Maria L, Wodak SJ. Assessment of blind predictions of protein-protein interactions: current status of docking methods. Proteins. 2003;52:51
  51. Kunstle G, Laine J, Pierron G, Kagami Si S, Nakajima H, Hoh F, et al. Identification of Akt association and oligomerization domains of the Akt kinase coactivator TCL1. Mol. Cell Biol. 2002;22:1513
  52. Venclovas C, Zemla A, Fidelis K, Moult J. Assessment of progress over the CASP experiments. Proteins. 2003;53(Suppl. 6):585
  53. Sarkar D, Leszczyniecka M, Kang DC, Lebedeva IV, Valerie K, Dhar S, et al. Down-regulation of Myc as a potential target for growth arrest induced by human polynucleotide phosphorylase (hPNPaseold-35) in human melanoma cells. J. Biol. Chem. 2003;278:24542
  54. Chen CY, Shyu AB. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 1995;20:465
  55. Gewartowski K, Tomecki R, Muchowski L, Dmochow Ska A, Dzwonek A, Malecki M, et al. Up-regulation of human PNPase mRNA by beta-interferon has no effect on protein level in melanoma cell lines. Acta. Biochim. Pol. 2006;53:179
  56. Hoyer KK, Herling M, Bagrintseva K, Dawson DW, French SW, Renard M, et al. T cell leukemia-1 modulates TCR signal strength and IFN-gamma levels through phosphatidylinositol 3-kinase and protein kinase C pathway activation. J. Immunol. 2005;175:864
  57. Lee B, Richards FM. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 1971;55:379

PII: S0304-3835(06)00430-7

doi: 10.1016/j.canlet.2006.07.006

Cancer Letters
Volume 248, Issue 2 , Pages 198-210 , 18 April 2007

Article Tools

* Image Usage & Resolution