PML protein association with specific nucleolar structures differs in normal, tumor and senescent human cells

Journal of Structural Biology

Volumn 159, Issue 1, 2007, Pages 56-70

  Janderová Rossmeislová, Lenka ^a,b   Nováková, Zora ^a,b   Vlasáková, Jana ^a,b   Philimonenko, Vlada ^a,b   Hozák, Pavel ^a,b   Hodný, Zdeněk ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Actinomycin D; Nucleolus; PML; PML nuclear bodies; Senescence; Stem cells

Indexed keywords

DACTINOMYCIN; PROMYELOCYTIC LEUKEMIA PROTEIN; RIBOSOME RNA;

ARTICLE; CELL ACTIVITY; CELL CYCLE REGULATION; CELL GROWTH; CELL IMMORTALIZATION; CELL STRUCTURE; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE SYNTHESIS; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MESENCHYMAL STEM CELL; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN BINDING; SKIN FIBROBLAST;

CELL AGING; CELL LINE; CELL LINE, TUMOR; CELL NUCLEOLUS; FIBROBLASTS; HELA CELLS; HUMANS; MESENCHYMAL STEM CELLS; MICROSCOPY, FLUORESCENCE; NEOPLASM PROTEINS; NEOPLASMS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 34249938802     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.02.008     Document Type: Article

References (60)

1. Ascoli C.A., and Maul G.G. Identification of a novel nuclear domain. J. Cell Biol. 112 (1991) 785-795
2. Bernardi R., Scaglioni P.P., Bergmann S., Horn H.F., Vousden K.H., and Pandolfi P.P. PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat Cell Biol 6 (2004) 665-672
3. Bhat K.P., Itahana K., Jin A., and Zhang Y. Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. Embo J. 23 (2004) 2402-2412
4. Bischof O., Kirsh O., Pearson M., Itahana K., Pelicci P.G., and Dejean A. Deconstructing PML-induced premature senescence. Embo J. 21 (2002) 3358-3369
5. Carbone R., Pearson M., Minucci S., and Pelicci P.G. PML NBs associate with the hMre11 complex and p53 at sites of irradiation induced DNA damage. Oncogene 21 (2002) 1633-1640
6. Carmo-Fonseca M., Mendes-Soares L., and Campos I. To be or not to be in the nucleolus. Nat Cell Biol. 2 (2000) E107-E112
7. Craig C., Kim M., Ohri E., Wersto R., Katayose D., Li Z., Choi Y.H., Mudahar B., Srivastava S., Seth P., and Cowan K. Effects of adenovirus-mediated p16INK4A expression on cell cycle arrest are determined by endogenous p16 and Rb status in human cancer cells. Oncogene 16 (1998) 265-272
8. David-Pfeuty T., and Nouvian-Dooghe Y. Human p14(Arf): an exquisite sensor of morphological changes and of short-lived perturbations in cell cycle and in nucleolar function. Oncogene 21 (2002) 6779-6790
9. de Stanchina E., Querido E., Narita M., Davuluri R.V., Pandolfi P.P., Ferbeyre G., and Lowe S.W. PML is a direct p53 target that modulates p53 effector functions. Mol Cell 13 (2004) 523-535
10. Dellaire G., and Bazett-Jones D.P. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioassays 26 (2004) 963-977
11. Dundr M., Hoffmann-Rohrer U., Hu Q., Grummt I., Rothblum L.I., Phair R.D., and Misteli T. A kinetic framework for a mammalian RNA polymerase in vivo. Science 298 (2002) 1623-1626
12. Duprez E., Saurin A.J., Desterro J.M., Lallemand-Breitenbach V., Howe K., Boddy M.N., Solomon E., de The H., Hay R.T., and Freemont P.S. SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J. Cell Sci. 112 Pt 3 (1999) 381-393
13. Eskiw C.H., Dellaire G., Mymryk J.S., and Bazett-Jones D.P. Size, position and dynamic behavior of PML nuclear bodies following cell stress as a paradigm for supramolecular trafficking and assembly. J. Cell Sci. 116 (2003) 4455-4466
14. Ferbeyre G., de Stanchina E., Querido E., Baptiste N., Prives C., and Lowe S.W. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 14 (2000) 2015-2027
15. Flenghi L., Fagioli M., Tomassoni L., Pileri S., Gambacorta M., Pacini R., Grignani F., Casini T., Ferrucci P.F., Martelli M.F., et al. Characterization of a new monoclonal antibody (PG-M3) directed against the aminoterminal portion of the PML gene product: immunocytochemical evidence for high expression of PML proteins on activated macrophages, endothelial cells, and epithelia. Blood 85 (1995) 1871-1880
16. Fromont-Racine M., Senger B., Saveanu C., and Fasiolo F. Ribosome assembly in eukaryotes. Gene 313 (2003) 17-42
17. Fuchsova B., and Hozak P. The localization of nuclear DNA helicase II in different nuclear compartments is linked to transcription. Exp Cell Res 279 (2002) 260-270
18. Gambacorta M., Flenghi L., Fagioli M., Pileri S., Leoncini L., Bigerna B., Pacini R., Tanci L.N., Pasqualucci L., Ascani S., Mencarelli A., Liso A., Pelicci P.G., and Falini B. Heterogeneous nuclear expression of the promyelocytic leukemia (PML) protein in normal and neoplastic human tissues. Am J. Pathol. 149 (1996) 2023-2035
19. Grisendi S., Mecucci C., Falini B., and Pandolfi P.P. Nucleophosmin and cancer. Nat Rev Cancer 6 (2006) 493-505
20. Grummt I. Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Prog. Nucleic Acid Res. Mol Biol. 62 (1999) 109-154
21. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17 (2003) 1691-1702
22. Gurrieri C., Capodieci P., Bernardi R., Scaglioni P.P., Nafa K., Rush L.J., Verbel D.A., Cordon-Cardo C., and Pandolfi P.P. Loss of the tumor suppressor PML in human cancers of multiple histologic origins. J. Natl. Cancer Inst 96 (2004) 269-279
23. Hannan K.M., Brandenburger Y., Jenkins A., Sharkey K., Cavanaugh A., Rothblum L., Moss T., Poortinga G., McArthur G.A., Pearson R.B., and Hannan R.D. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 23 (2003) 8862-8877
24. Hozak P., Cook P.R., Schofer C., Mosgoller W., and Wachtler F. Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. J. Cell Sci. 107 Pt 2 (1994) 639-648
25. Iapalucci-Espinoza S., and Franze-Fernandez M.T. Effect of protein synthesis inhibitors and low concentrations of actinomycin D on ribosomal RNA synthesis. FEBS Lett 107 (1979) 281-284
26. Ishov A.M., Sotnikov A.G., Negorev D., Vladimirova O.V., Neff N., Kamitani T., Yeh E.T., Strauss III J.F., and Maul G.G. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147 (1999) 221-234
27. Janderova L., McNeil M., Murrell A.N., Mynatt R.L., and Smith S.R. Human mesenchymal stem cells as an in vitro model for human adipogenesis. Obes Res 11 (2003) 65-74
28. Jin A., Itahana K., O'Keefe K., and Zhang Y. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol. 24 (2004) 7669-7680
29. Kataoka M., Wiehle S., Spitz F., Schumacher G., Roth J.A., and Cristiano R.J. Down-regulation of bcl-2 is associated with p16INK4-mediated apoptosis in non-small cell lung cancer cells. Oncogene 19 (2000) 1589-1595
30. Lavau C., Marchio A., Fagioli M., Jansen J., Falini B., Lebon P., Grosveld F., Pandolfi P.P., Pelicci P.G., and Dejean A. The acute promyelocytic leukaemia-associated PML gene is induced by interferon. Oncogene 11 (1995) 871-876
31. Lu W., Lin J., and Chen J. Expression of p14ARF overcomes tumor resistance to p53. Cancer Res 62 (2002) 1305-1310
32. Mallette F.A., Goumard S., Gaumont-Leclerc M.F., Moiseeva O., and Ferbeyre G. Human fibroblasts require the Rb family of tumor suppressors, but not p53, for PML-induced senescence. Oncogene 23 (2004) 91-99
33. Mattsson K., Pokrovskaja K., Kiss C., Klein G., and Szekely L. Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation. Proc. Natl. Acad. Sci. U.S.A 98 (2001) 1012-1017
34. Maul G.G., Negorev D., Bell P., and Ishov A.M. Review: properties and assembly mechanisms of ND10, PML bodies, or PODs. J. Struct. Biol. 129 (2000) 278-287
35. Mayer C., Zhao J., Yuan X., and Grummt I. mTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev 18 (2004) 423-434
36. Michishita E., Nakabayashi K., Suzuki T., Kaul S.C., Ogino H., Fujii M., Mitsui Y., and Ayusawa D. 5-Bromodeoxyuridine induces senescence-like phenomena in mammalian cells regardless of cell type or species. J. Biochem. (Tokyo) 126 (1999) 1052-1059
37. Olson M.O. The Nucleolus Landes Biosciences (2004), Kluwer Academic
38. Olson M.O., and Dundr M. The moving parts of the nucleolus. Histochem. Cell Biol. 123 (2005) 203-216
39. Park Y.B., Park M.J., Kimura K., Shimizu K., Lee S.H., and Yokota J. Alterations in the INK4a/ARF locus and their effects on the growth of human osteosarcoma cell lines. Cancer Genet Cytogenet 133 (2002) 105-111
40. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., and Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-147
41. Regad T., and Chelbi-Alix M.K. Role and fate of PML nuclear bodies in response to interferon and viral infections. Oncogene 20 (2001) 7274-7286
42. Rohde J., Heitman J., and Cardenas M.E. The TOR kinases link nutrient sensing to cell growth. J. Biol. Chem. 276 (2001) 9583-9586
43. Rubbi C.P., and Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. Embo J. 22 (2003) 6068-6077
44. Ruggero D., and Pandolfi P.P. Does the ribosome translate cancer?. Nat Rev Cancer 3 (2003) 179-192
45. Russell J., and Zomerdijk J.C. RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem. Sci. 30 (2005) 87-96
46. Salomoni P., and Pandolfi P.P. The role of PML in tumor suppression. Cell 108 (2002) 165-170
47. Sedelnikova O.A., Horikawa I., Zimonjic D.B., Popescu N.C., Bonner W.M., and Barrett J.C. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat Cell Biol 6 (2004) 168-170
48. Seker H., Rubbi C., Linke S.P., Bowman E.D., Garfield S., Hansen L., Borden K.L., Milner J., and Harris C.C. UV-C-induced DNA damage leads to p53-dependent nuclear trafficking of PML. Oncogene 22 (2003) 1620-1628
49. Serrano M., Lin A.W., McCurrach M.E., Beach D., and Lowe S.W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88 (1997) 593-602
50. Shav-Tal Y., Blechman J., Darzacq X., Montagna C., Dye B.T., Patton J.G., Singer R.H., and Zipori D. Dynamic Sorting of Nuclear Components into Distinct Nucleolar Caps during Transcriptional Inhibition. Mol Biol Cell 16 (2005) 2395-2413
51. Stadler M., Chelbi-Alix M.K., Koken M.H., Venturini L., Lee C., Saib A., Quignon F., Pelicano L., Guillemin M.C., Schindler C., et al. Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element. Oncogene 11 (1995) 2565-2573
52. Sternsdorf T., Grotzinger T., Jensen K., and Will H. Nuclear dots: actors on many stages. Immunobiology 198 (1997) 307-331
53. Stuurman N., de Graaf A., Floore A., Josso A., Humbel B., de Jong L., and van Driel R. A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies. J. Cell Sci. 101 Pt 4 (1992) 773-784
54. Suzuki T., Michishita E., Ogino H., Fujii M., and Ayusawa D. Synergistic induction of the senescence-associated genes by 5-bromodeoxyuridine and AT-binding ligands in HeLa cells. Exp Cell Res 276 (2002) 174-184
55. Wang Z.G., Ruggero D., Ronchetti S., Zhong S., Gaboli M., Rivi R., and Pandolfi P.P. PML is essential for multiple apoptotic pathways. Nat Genet 20 (1998) 266-272
56. Weber J.D., Taylor L.J., Roussel M.F., Sherr C.J., and Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat Cell Biol 1 (1999) 20-26
57. Wesierska-Gadek J., Schloffer D., Kotala V., and Horky M. Escape of p53 protein from E6-mediated degradation in HeLa cells after cisplatin therapy. Int. J. Cancer 101 (2002) 128-136
58. White R.J. RNA polymerases I and III, growth control and cancer. Nat Rev Mol Cell Biol. 6 (2005) 69-78
59. Wojcik C., and DeMartino G.N. Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35 (2003) 579-589
60. Zhang Y., Wolf G.W., Bhat K., Jin A., Allio T., Burkhart W.A., and Xiong Y. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol. 23 (2003) 8902-8912