PML promotes MHC class II gene expression by stabilizing the class II transactivator

Journal of Cell Biology

Volumn 199, Issue 1, 2012, Pages 49-63

  Ulbricht, Tobias ^a   Alzrigat, Mohammad ^a   Horch, Almut ^b   Reuter, Nina ^c   Von Mikecz, Anna ^d   Steimle, Viktor ^e   Schmitt, Eberhard ^f,g   Krämer, Oliver H ^h   Stamminger, Thomas ^c   Hemmerich, Peter ^a  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b CARL ZEISS SMT AG   (Germany)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^e UNIVERSITÉ DE SHERBROOKE   (Canada)

^f UNIVERSITY OF GÖTTINGEN   (Germany)

^g UNIVERSITY OF HEIDELBERG   (Germany)

^h FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS II TRANSACTIVATOR; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN DEGRADATION;

CELLS, CULTURED; GENE EXPRESSION PROFILING; GENES, MHC CLASS II; HUMANS; INTERFERON-GAMMA; NUCLEAR PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84869231649     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201112015     Document Type: Article

References (75)

1. Aoto, T., N. Saitoh, T. Ichimura, H. Niwa, and M. Nakao. 2006. Nuclear and chromatin reorganization in the MHC-Oct3/4 locus at developmental phases of embryonic stem cell differentiation. Dev. Biol. 298:354-367. http://dx.doi.org/10.1016/j.ydbio.2006.04.450
2. Ascoli, C.A., and G.G. Maul. 1991. Identification of a novel nuclear domain. J. Cell Biol. 112:785-795. http://dx.doi.org/10.1083/jcb.112.5.785
3. Bernardi, R., and P.P. Pandolfi. 2007. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 8:1006-1016. http://dx.doi.org/10.1038/nrm2277
4. Bernardi, R., P.P. Scaglioni, S. Bergmann, H.F. Horn, K.H. Vousden, and P.P. Pandolfi. 2004. PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat. Cell Biol. 6:665-672. http://dx.doi.org/10.1038/ncb1147
5. Bernassola, F., P. Salomoni, A. Oberst, C.J. Di Como, M. Pagano, G. Melino, and P.P. Pandolfi. 2004. Ubiquitin-dependent degradation of p73 is inhibited by PML. J. Exp. Med. 199:1545-1557. http://dx.doi.org/10.1084/jem.20031943
6. Boisvert, F.M., M.J. Hendzel, and D.P. Bazett-Jones. 2000. Promyelocytic leukemia (PML) nuclear bodies are protein structures that do not accumulate RNA. J. Cell Biol. 148:283-292. http://dx.doi.org/10.1083/jcb.148.2.283
7. Boisvert, F.M., M.J. Kruhlak, A.K. Box, M.J. Hendzel, and D.P. Bazett-Jones. 2001. The transcription coactivator CBP is a dynamic component of the promyelocytic leukemia nuclear body. J. Cell Biol. 152:1099-1106. http://dx.doi.org/10.1083/jcb.152.5.1099
8. Bontron, S., C. Ucla, B. Mach, and V. Steimle. 1997. Efficient repression of endogenous major histocompatibility complex class II expression through dominant negative CIITA mutants isolated by a functional selection strategy. Mol. Cell. Biol. 17:4249-4258.
9. Branco, M.R., and A. Pombo. 2006. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol. 4:e138. http://dx.doi.org/10.1371/journal.pbio.0040138
10. Brand, P., T. Lenser, and P. Hemmerich. 2010. Assembly dynamics of PML nuclear bodies in living cells. PMC Biophys. 3:3. http://dx.doi.org/10.1186/1757-5036-3-3
11. Camacho-Carvajal, M.M., S. Klingler, F. Schnappauf, S.B. Hake, and V. Steimle. 2004. Importance of class II transactivator leucine-rich repeats for dominant-negative function and nucleo-cytoplasmic transport. Int. Immunol. 16:65-75. http://dx.doi.org/10.1093/intimm/dxh010
12. Chen, M., L. Singer, A. Scharf, and A. von Mikecz. 2008. Nuclear polyglutamine-containing protein aggregates as active proteolytic centers. J. Cell Biol. 180:697-704. http://dx.doi.org/10.1083/jcb.200708131
13. Ching, R.W., G. Dellaire, C.H. Eskiw, and D.P. Bazett-Jones. 2005. PML bodies: a meeting place for genomic loci? J. Cell Sci. 118:847-854. http://dx.doi.org/10.1242/jcs.01700
14. Cho, Y., I. Lee, G.G. Maul, and E. Yu. 1998. A novel nuclear substructure, ND10: distribution in normal and neoplastic human tissues. Int. J. Mol. Med. 1:717-724.
15. Choi, N.M., P. Majumder, and J.M. Boss. 2011. Regulation of major histocompatibility complex class II genes. Curr. Opin. Immunol. 23:81-87. http://dx.doi.org/10.1016/j.coi.2010.09.007
16. Christova, R., T. Jones, P.J. Wu, A. Bolzer, A.P. Costa-Pereira, D. Watling, I.M. Kerr, and D. Sheer. 2007. P-STAT1 mediates higher-order chromatin remodelling of the human MHC in response to IFNgamma. J. Cell Sci. 120:3262-3270. http://dx.doi.org/10.1242/jcs.012328
17. Collins, T., A.J. Korman, C.T. Wake, J.M. Boss, D.J. Kappes, W. Fiers, K.A. Ault, M.A.J. Gimbrone Jr., J.L. Strominger, and J.S. Pober. 1984. Immune interferon activates multiple class II major histocompatibility complex genes and the associated invariant chain gene in human endothelial cells and dermal fibroblasts. Proc. Natl. Acad. Sci. USA. 81:4917-4921. http://dx.doi.org/10.1073/pnas.81.15.4917
18. Condemine, W., Y. Takahashi, J. Zhu, F. Puvion-Dutilleul, S. Guegan, A. Janin, and H. de Thé. 2006. Characterization of endogenous human promyelocytic leukemia isoforms. Cancer Res. 66:6192-6198. http://dx.doi.org/10.1158/0008-5472.CAN-05-3792
19. De Thé, H., M. Riviere, W. Bernhard, and W. Bernhard. 1960. [Examination by electron microscope of the VX2 tumor of the domestic rabbit derived from the Shope papilloma]. Bull. Assoc. Fr. Etud. Cancer. 47:570-584.
20. Dong, Y., W.M. Rohn, and E.N. Benveniste. 1999. IFN-gamma regulation of the type IV class II transactivator promoter in astrocytes. J. Immunol. 162:4731-4739.
21. El Bougrini, J., L. Dianoux, and M.K. Chelbi-Alix. 2011. PML positively regulates interferon gamma signaling. Biochimie. 93:389-398. http://dx.doi.org/10.1016/j.biochi.2010.11.005
22. Everett, R.D., W.C. Earnshaw, A.F. Pluta, T. Sternsdorf, A.M. Ainsztein, M. Carmena, S. Ruchaud, W.L. Hsu, and A. Orr. 1999. A dynamic connection between centromeres and ND10 proteins. J. Cell Sci. 112:3443-3454.
23. Everett, R.D., S. Rechter, P. Papior, N. Tavalai, T. Stamminger, and A. Orr. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80:7995-8005. http://dx.doi.org/10.1128/JVI.00734-06
24. Fabunmi, R.P., W.C. Wigley, P.J. Thomas, and G.N. DeMartino. 2001. Interferon gamma regulates accumulation of the proteasome activator PA28 and immunoproteasomes at nuclear PML bodies. J. Cell Sci. 114:29-36.
25. Fagioli, M., M. Alcalay, P.P. Pandolfi, L. Venturini, A. Mencarelli, A. Simeone, D. Acampora, F. Grignani, and P.G. Pelicci. 1992. Alternative splicing of PML transcripts predicts coexpression of several carboxy-terminally different protein isoforms. Oncogene. 7:1083-1091.
26. Fuchsová, B., P. Novák, J. Kafková, and P. Hozák. 2002. Nuclear DNA helicase II is recruited to IFN-α-activated transcription sites at PML nuclear bodies. J. Cell Biol. 158:463-473. http://dx.doi.org/10.1083/jcb.200202035
27. Gambacorta, M., L. Flenghi, M. Fagioli, S. Pileri, L. Leoncini, B. Bigerna, R. Pacini, L.N. Tanci, L. Pasqualucci, S. Ascani, et al. 1996. Heterogeneous nuclear expression of the promyelocytic leukemia (PML) protein in normal and neoplastic human tissues. Am. J. Pathol. 149:2023-2035.
28. Gialitakis, M., P. Arampatzi, T. Makatounakis, and J. Papamatheakis. 2010. Gamma interferon-dependent transcriptional memory via relocalization of a gene locus to PML nuclear bodies. Mol. Cell. Biol. 30:2046-2056. http://dx.doi.org/10.1128/MCB.00906-09
29. Grande, M.A., I. van der Kraan, B. van Steensel, W. Schul, H. de Thé, H.T. van der Voort, L. de Jong, and R. van Driel. 1996. PML-containing nuclear bodies: their spatial distribution in relation to other nuclear components. J. Cell. Biochem. 63:280-291. http://dx.doi.org/10.1002/(SICI)1097-4644(19961201)63:3<280::AID-JCB3 >3.0.CO;2-T
30. Guillot, P.V., S.Q. Xie, M. Hollinshead, and A. Pombo. 2004. Fixationinduced redistribution of hyperphosphorylated RNA polymerase II in the nucleus of human cells. Exp. Cell Res. 295:460-468. http://dx.doi.org/10.1016/j.yexcr.2004.01.020
31. Hager, G.L., J.G. McNally, and T. Misteli. 2009. Transcription dynamics. Mol. Cell. 35:741-753. http://dx.doi.org/10.1016/j.molcel.2009.09.005
32. Hake, S.B., K. Masternak, C. Kammerbauer, C. Janzen, W. Reith, and V. Steimle. 2000. CIITA leucine-rich repeats control nuclear localization, in vivo recruitment to the major histocompatibility complex (MHC) class II enhanceosome, and MHC class II gene transactivation. Mol. Cell. Biol. 20:7716-7725. http://dx.doi.org/10.1128/MCB.20.20.7716-7725.2000
33. Hemmerich, P., S. Weidtkamp-Peters, C. Hoischen, L. Schmiedeberg, I. Erliandri, and S. Diekmann. 2008. Dynamics of inner kinetochore assembly and maintenance in living cells. J. Cell Biol. 180:1101-1114. http://dx.doi.org/10.1083/jcb.200710052
34. Hemmerich, P., L. Schmiedeberg, and S. Diekmann. 2011. Dynamic as well as stable protein interactions contribute to genome function and maintenance. Chromosome Res. 19:131-151. http://dx.doi.org/10.1007/s10577-010-9161-8
35. Jensen, K., C. Shiels, and P.S. Freemont. 2001. PML protein isoforms and the RBCC/TRIM motif. Oncogene. 20:7223-7233. http://dx.doi.org/10.1038/sj.onc.1204765
36. Kießlich, A., A. von Mikecz, and P. Hemmerich. 2002. Cell cycle-dependent association of PML bodies with sites of active transcription in nuclei of mammalian cells. J. Struct. Biol. 140:167-179. http://dx.doi.org/10.1016/S1047-8477(02)00571-3
37. Kumar, P.P., O. Bischof, P.K. Purbey, D. Notani, H. Urlaub, A. Dejean, and S. Galande. 2007. Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat. Cell Biol. 9:45-56. http://dx.doi.org/10.1038/ncb1516
38. 3induced PML or PML/retinoic acid receptor α degradation. J. Exp. Med. 193:1361-1371. http://dx.doi.org/10.1084/jem.193.12.1361
39. Londhe, P., B. Zhu, J. Abraham, C. Keller, and J. Davie. 2012. CIITA is silenced by epigenetic mechanisms that prevent the recruitment of transactivating factors in rhabdomyosarcoma cells. Int. J. Cancer. 131:E437-E448. http://dx.doi.org/10.1002/ijc.26478
40. Louria-Hayon, I., T. Grossman, R.V. Sionov, O. Alsheich, P.P. Pandolfi, and Y. Haupt. 2003. The promyelocytic leukemia protein protects p53 from Mdm2-mediated inhibition and degradation. J. Biol. Chem. 278:33134-33141. http://dx.doi.org/10.1074/jbc.M301264200
41. MacPherson, M.J., L.G. Beatty, W. Zhou, M. Du, and P.D. Sadowski. 2009. The CTCF insulator protein is posttranslationally modified by SUMO. Mol. Cell. Biol. 29:714-725. http://dx.doi.org/10.1128/MCB.00825-08
42. Majumder, P., and J.M. Boss. 2010. CTCF controls expression and chromatin architecture of the human major histocompatibility complex class II locus. Mol. Cell. Biol. 30:4211-4223. http://dx.doi.org/10.1128/MCB.00327-10
43. Majumder, P., J.A. Gomez, B.P. Chadwick, and J.M. Boss. 2008. The insulator factor CTCF controls MHC class II gene expression and is required for the formation of long-distance chromatin interactions. J. Exp. Med. 205:785-798. http://dx.doi.org/10.1084/jem.20071843
44. Milovic-Holm, K., E. Krieghoff, K. Jensen, H. Will, and T.G. Hofmann. 2007. FLASH links the CD95 signaling pathway to the cell nucleus and nuclear bodies. EMBO J. 26:391-401. http://dx.doi.org/10.1038/sj.emboj.7601504
45. Müller, W.G., D. Rieder, G. Kreth, C. Cremer, Z. Trajanoski, and J.G. McNally. 2004. Generic features of tertiary chromatin structure as detected in natural chromosomes. Mol. Cell. Biol. 24:9359-9370. http://dx.doi.org/10.1128/MCB.24.21.9359-9370.2004
46. Negorev, D., and G.G. Maul. 2001. Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene. 20:7234-7242. http://dx.doi.org/10.1038/sj.onc.1204764
47. Otten, L.A., V. Steimle, S. Bontron, and B. Mach. 1998. Quantitative control of MHC class II expression by the transactivator CIITA. Eur. J. Immunol. 28:473-478. http://dx.doi.org/10.1002/(SICI)1521-4141(199802)28:02<473::AID-IMMU4 73>3.0.CO;2-E
48. Reith, W., S. LeibundGut-Landmann, and J.M. Waldburger. 2005. Regulation of MHC class II gene expression by the class II transactivator. Nat. Rev. Immunol. 5:793-806. http://dx.doi.org/10.1038/nri1708
49. Rockel, T.D., D. Stuhlmann, and A. von Mikecz. 2005. Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J. Cell Sci. 118:5231-5242. http://dx.doi.org/10.1242/jcs.02642
50. Saitoh, N., Y. Uchimura, T. Tachibana, S. Sugahara, H. Saitoh, and M. Nakao. 2006. In situ SUMOylation analysis reveals a modulatory role of RanBP2 in the nuclear rim and PML bodies. Exp. Cell Res. 312:1418-1430. http://dx.doi.org/10.1016/j.yexcr.2006.01.013
51. Scharf, A., T.D. Rockel, and A. von Mikecz. 2007. Localization of proteasomes and proteasomal proteolysis in the mammalian interphase cell nucleus by systematic application of immunocytochemistry. Histochem. Cell Biol. 127:591-601. http://dx.doi.org/10.1007/s00418-006-0266-2
52. Schnappauf, F., S.B. Hake, M.M. Camacho Carvajal, S. Bontron, B. Lisowska-Grospierre, and V. Steimle. 2003. N-terminal destruction signals lead to rapid degradation of the major histocompatibility complex class II transactivator CIITA. Eur. J. Immunol. 33:2337-2347. http://dx.doi.org/10.1002/eji.200323490
53. Sharma, P., R. Murillas, H. Zhang, and M.R. Kuehn. 2010. N4BP1 is a newly identified nucleolar protein that undergoes SUMO-regulated polyubiquitylation and proteasomal turnover at promyelocytic leukemia nuclear bodies. J. Cell Sci. 123:1227-1234. http://dx.doi.org/10.1242/jcs.060160
54. Shiels, C., S.A. Islam, R. Vatcheva, P. Sasieni, M.J. Sternberg, P.S. Freemont, and D. Sheer. 2001. PML bodies associate specifically with the MHC gene cluster in interphase nuclei. J. Cell Sci. 114:3705-3716.
55. Spilianakis, C., J. Papamatheakis, and A. Kretsovali. 2000. Acetylation by PCAF enhances CIITA nuclear accumulation and transactivation of major histocompatibility complex class II genes. Mol. Cell. Biol. 20:8489-8498. http://dx.doi.org/10.1128/MCB.20.22.8489-8498.2000
56. Sprague, B.L., R.L. Pego, D.A. Stavreva, and J.G. McNally. 2004. Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys. J. 86:3473-3495. http://dx.doi.org/10.1529/biophysj.103.026765
57. Steimle, V., L.A. Otten, M. Zufferey, and B. Mach. 1993. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell. 75:135-146.
58. Steimle, V., C.A. Siegrist, A. Mottet, B. Lisowska-Grospierre, and B. Mach. 1994. Regulation of MHC class II expression by interferon-gamma mediated by the transactivator gene CIITA. Science. 265:106-109. http://dx.doi.org/10.1126/science.8016643
59. Sternsdorf, T., T. Grötzinger, K. Jensen, and H. Will. 1997. Nuclear dots: actors on many stages. Immunobiology. 198:307-331. http://dx.doi.org/10.1016/S0171-2985(97)80051-4
60. Sun, Y., L.K. Durrin, and T.G. Krontiris. 2003. Specific interaction of PML bodies with the TP53 locus in Jurkat interphase nuclei. Genomics. 82:250-252. http://dx.doi.org/10.1016/S0888-7543(03)00075-2
61. Suter, D.M., N. Molina, D. Gatfield, K. Schneider, U. Schibler, and F. Naef. 2011. Mammalian genes are transcribed with widely different bursting kinetics. Science. 332:472-474. http://dx.doi.org/10.1126/science.1198817
62. Tavalai, N., and T. Stamminger. 2008. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta. 1783: 2207-2221. http://dx.doi.org/10.1016/j.bbamcr.2008.08.004
63. Tavalai, N., P. Papior, S. Rechter, M. Leis, and T. Stamminger. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 80:8006-8018. http://dx.doi.org/10.1128/JVI.00743-06
64. Terris, B., V. Baldin, S. Dubois, C. Degott, J.F. Flejou, D. Hénin, and A. Dejean. 1995. PML nuclear bodies are general targets for inflammation and cell proliferation. Cancer Res. 55:1590-1597.
65. Van Damme, E., K. Laukens, T.H. Dang, and X. Van Ostade. 2010. A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. Int. J. Biol. Sci. 6:51-67. http://dx.doi.org/10.7150/ijbs.6.51
66. Volpi, E.V., E. Chevret, T. Jones, R. Vatcheva, J. Williamson, S. Beck, R.D. Campbell, M. Goldsworthy, S.H. Powis, J. Ragoussis, et al. 2000. Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J. Cell Sci. 113:1565-1576.
67. von Mikecz, A., S. Zhang, M. Montminy, E.M. Tan, and P. Hemmerich. 2000. CREB-binding protein (CBP)/p300 and RNA polymerase II colocalize in transcriptionally active domains in the nucleus. J. Cell Biol. 150:265-273. http://dx.doi.org/10.1083/jcb.150.1.265
68. Wang, J., C. Shiels, P. Sasieni, P.J. Wu, S.A. Islam, P.S. Freemont, and D. Sheer. 2004. Promyelocytic leukemia nuclear bodies associate with transcriptionally active genomic regions. J. Cell Biol. 164:515-526. http://dx.doi.org/10.1083/jcb.200305142
69. Weidtkamp-Peters, S., T. Lenser, D. Negorev, N. Gerstner, T.G. Hofmann, G. Schwanitz, C. Hoischen, G. Maul, P. Dittrich, and P. Hemmerich. 2008. Dynamics of component exchange at PML nuclear bodies. J. Cell Sci. 121:2731-2743. http://dx.doi.org/10.1242/jcs.031922
70. Wiesmeijer, K., C. Molenaar, I.M. Bekeer, H.J. Tanke, and R.W. Dirks. 2002. Mobile foci of Sp100 do not contain PML: PML bodies are immobile but PML and Sp100 proteins are not. J. Struct. Biol. 140:180-188. http://dx.doi.org/10.1016/S1047-8477(02)00529-4
71. Wright, K.L., K.C. Chin, M. Linhoff, C. Skinner, J.A. Brown, J.M. Boss, G.R. Stark, and J.P. Ting. 1998. CIITA stimulation of transcription factor binding to major histocompatibility complex class II and associated promoters in vivo. Proc. Natl. Acad. Sci. USA. 95:6267-6272. http://dx.doi.org/10.1073/pnas.95.11.6267
72. Wu, X., X. Kong, L. Luchsinger, B.D. Smith, and Y. Xu. 2009. Regulating the activity of class II transactivator by posttranslational modifications: exploring the possibilities. Mol. Cell. Biol. 29:5639-5644. http://dx.doi.org/10.1128/MCB.00661-09
73. Xie, S.Q., and A. Pombo. 2006. Distribution of different phosphorylated forms of RNA polymerase II in relation to Cajal and PML bodies in human cells: an ultrastructural study. Histochem. Cell Biol. 125:21-31. http://dx.doi.org/10.1007/s00418-005-0064-2
74. Xu, Z.X., A. Timanova-Atanasova, R.X. Zhao, and K.S. Chang. 2003. PML colocalizes with and stabilizes the DNA damage response protein TopBP1. Mol. Cell. Biol. 23:4247-4256. http://dx.doi.org/10.1128/MCB.23.12.4247-4256.2003
75. Zhong, S., P. Salomoni, and P.P. Pandolfi. 2000. The transcriptional role of PML and the nuclear body. Nat. Cell Biol. 2:E85-E90. http://dx.doi.org/10.1038/35010583