Of mice, flies, and man: The emerging role of polycomb-group genes in human malignant lymphomas

International Journal of Hematology

Volumn 81, Issue 4, 2005, Pages 281-287

  Raaphorst, Frank M ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Chromatin; Epigenetics; Gene regulation; Lymphoma; Polycomb

Indexed keywords

EMBRYONIC ECTODERM DEVELOPMENT PROTEIN; HISTONE DEACETYLASE; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE; POLYCOMB GROUP PROTEINS; REPRESSOR PROTEIN;

B CELL LYMPHOMA; CELL CYCLE; DISEASE SEVERITY; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; LYMPHOMA; LYMPHOPOIESIS; REVIEW; T CELL LYMPHOMA; ANIMAL; APOPTOSIS; FLY; GENETICS; MOUSE;

ANIMALS; APOPTOSIS; CELL CYCLE; DIPTERA; EMBRYONIC DEVELOPMENT; GENE SILENCING; HUMANS; LYMPHOMA, B-CELL; LYMPHOMA, T-CELL; MICE; REPRESSOR PROTEINS;

EID: 22844446351     PISSN: 09255710     EISSN: None     Source Type: Journal    
DOI: 10.1532/IJH97.05023     Document Type: Review

References (82)

1. Lund AH, van Lohuizen M. Polycomb complexes and silencing mechanisms. Curr Opin Cell Biol. 2004;16:239-246.
2. Otte AP, Kwaks TH. Gene repression by Polycomb group protein complexes: a distinct complex for every occasion? Curr Opin Genet Dev. 2003;13:448-454.
3. Sewalt RG, Kwaks TH, Hamer K, Otte AP. Biochemical analysis of mammalian polycomb group protein complexes and the identification of genetic elements that block polycomb-mediated gene repression. Methods Enzymol. 2004;377:282-296.
4. Jacobs JJ, van Lohuizen M. Polycomb repression: from cellular memory to cellular proliferation and cancer. Biochim Biophys Acta. 2002;1602:151-161.
5. Lessard J, Sauvageau G. Polycomb group genes as epigenetic regulators of normal and leukemic hemopoiesis. Exp Hematol. 2003;31: 567-585.
6. Attwooll C, Oddi S, Cartwright P, et al. A novel repressive E2F6 complex containing the polycomb group protein, EPC1, that interacts with EZH2 in a proliferation-specific manner. J Biol Chem. 2005;280:1199-1208.
7. Gunster MJ, Raaphorst FM, Hamer KM, et al. Differential expression of human Polycomb group proteins in various tissues and cell types. J Cell Biochem. 2001;36(suppl):129-143.
8. van Galen JC, Dukers DF, Giroth C, et al. Distinct expression patterns of polycomb oncoproteins and their binding partners during the germinal center reaction. Eur J Immunol. 2004;34:1870-1881.
9. Akasaka T, Takahashi N, Suzuki M, Koseki H, Bodmer R, Koga H. MBLR, a new RING finger protein resembling mammalian Polycomb gene products, is regulated by cell cycle-dependent phosphorylation. Genes Cells. 2002;7:835-850.
10. Kuzmichev A, Margueron R, Vaquero A, et al. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A. 2005;102: 1859-1864.
11. Kuzmichev A, Jenuwein T, Tempst P, Reinberg D. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell. 2004;14:183-193.
12. Voncken JW, Niessen H, Neufeld B, et al. MAPKAP kinase 3pK phosphorylates and regulates chromatin association of the Polycomb group protein Bmi1. J Biol Chem. 2005;280:5178-5187.
13. Breiling A, Turner BM, Bianchi ME, Orlando V. General transcription factors bind promoters repressed by Polycomb group proteins. Nature. 2001;412:651-655.
14. Garcia-Cuellar MP, Zilles O, Schreiner SA, Birke M, Winkler TH, Slany RK. The ENL moiety of the childhood leukemia-associated MLL-ENL oncoprotein recruits human Polycomb 3. Oncogene. 2001;20:411-419.
15. Sewalt RG, Gunster MJ, van der Vlag J, Satijn DP, Otte AP. C-terminal binding protein is a transcriptional repressor that interacts with a specific class of vertebrate Polycomb proteins. Mol Cell Biol. 1999;19:777-787.
16. Trimarchi JM, Fairchild B, Wen J, Lees JA. The E2F6 transcription factor is a component of the mammalian Bmi1-containing polycomb complex. Proc Natl Acad Sci U S A. 2001;98:1519-1524.
17. Qin H, Wang J, Liang Y, Taniguchi Y, Tanigaki K, Han H. RING1 inhibits transactivation of RBP-J by Notch through interaction with LIM protein KyoT2. Nucleic Acids Res. 2004;32:1492-1501.
18. Garcia E, Marcos-Gutierrez C, del Mar LM, Moreno JC, Vidal M. RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1. EMBO J. 1999;18:3404-3418.
19. Soulez M, Saurin AJ, Freemont PS, Knight JC. SSX and the synovial-sarcoma-specific chimaeric protein SYT-SSX co-localize with the human Polycomb group complex. Oncogene. 1999;18: 2739-2746.
20. Hobert O, Jallal B, Ullrich A. Interaction of Vav with ENX-1, a putative transcriptional regulator of homeobox gene expression. Mol Cell Biol. 1996;16:3066-3073.
21. Schwendemann A, Lehmann M. Pipsqueak and GAGA factor act in concert as partners at homeotic and many other loci. Proc Natl Acad Sci U S A. 2002;99:12883-12888.
22. Spitz F, Gonzalez F, Duboule D. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell. 2003;113:405-417.
23. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403:41-45.
24. van der Vlag J, Otte AP. Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat Genet. 1999;23:474-478.
25. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298:1039-1043.
26. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 2002;16:2893-2905.
27. Kagey MH, Melhuish TA, Powers SE, Wotton D. Multiple activities contribute to Pc2 E3 function. EMBO J. 2005;24:108-119.
28. Sewalt RG, Lachner M, Vargas M, et al. Selective interactions between vertebrate Polycomb homologs and the SUV39H1 histone lysine methyltransferase suggest that histone H3-K9 methylation contributes to chromosomal targeting of Polycomb group proteins. Mol Cell Biol. 2002;22:5539-5553.
29. Fang J, Chen T, Chadwick B, Li E, Zhang Y. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem. 2004;279: 52812-52815.
30. Wang H, Wang L, Erdjument-Bromage H, et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature. 2004;431: 873-878.
31. Kirmizis A, Bartley SM, Kuzmichev A, et al. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev. 2004;18:1592-1605.
32. Breiling A, O'Neill LP, D'Eliseo D, Turner BM, Orlando V. Epigenome changes in active and inactive Polycomb-group-controlled regions. EMBO Rep. 2004;5:976-982.
33. Ringrose L, Ehret H, Paro R. Distinct contributions of histone H3 lysine 9 and 27 methylation to locus-specific stability of Polycomb complexes. Mol Cell. 2004;16:641-653.
34. Pasini D, Bracken AP, Jensen MR, Denchi EL, Helin K. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J. 2004;23:4061-4071.
35. Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS. Hierarchical recruitment of Polycomb group silencing complexes. Mol Cell. 2004;14:637-646.
36. Poux S, Melfi R, Pirrotta V. Establishment of Polycomb silencing requires a transient interaction between PC and ESC. Genes Dev. 2001;15:2509-2514.
37. Shaffer AL, Rosenwald A, Staudt LM. Lymphoid malignancies: the dark side of B-cell differentiation. Nat Rev Immunol. 2002;2: 920-932.
38. Claus R, Lubbert M. Epigenetic targets in hematopoietic malignancies. Oncogene. 2003;22:6489-6496.
39. Seto M. Genetic and epigenetic factors involved in B-cell lymphomagenesis. Cancer Sci. 2004;95:704-710.
40. van der Lugt NM, Domen J, Linders K, et al. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 1994;8:757-769.
41. Akasaka T, van Lohuizen M, van der Lugt N, et al. Mice doubly deficient for the Polycomb Group genes Mel18 and Bmi1 reveal synergy and requirement for maintenance but not initiation of Hox gene expression. Development. 2001;128:1587-1597.
42. Akasaka T, Tsuji K, Kawahira H, et al. The role of mel-18, a mammalian Polycomb group gene, during IL-7-dependent proliferation of lymphocyte precursors. Immunity. 1997;7:135-146.
43. Akasaka T, Kanno M, Balling R, Mieza MA, Taniguchi M, Koseki H. A role for mel-18, a Polycomb group-related vertebrate gene, during the anteroposterior specification of the axial skeleton. Development. 1996;122:1513-1522.
44. Core N, Bel S, Gaunt SJ, et al. Altered cellular proliferation and mesoderm patterning in Polycomb-M33-deficient mice. Development. 1997;124:721-729.
45. Takihara Y, Tomotsune D, Shirai M, et al. Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development. 1997;124:3673-3682.
46. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature. 1999; 397:164-168.
47. Haupt Y, Bath ML, Harris AW, Adams JM. bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. Oncogene. 1993;8:3161-3164.
48. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell. 1991;65: 737-752.
49. Haupt Y, Alexander WS, Barri G, Klinken SP, Adams JM. Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in E mu-myc transgenic mice. Cell. 1991;65:753-763.
50. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev. 1999;13:2678-2690.
51. Alkema MJ, Jacobs H, van Lohuizen M, Berns A. Perturbation of B and T cell development and predisposition to lymphomagenesis in Eμ Bmi1 transgenic mice require the Bmi1 RING finger. Oncogene. 1997;15:899-910.
52. Dimri GP, Martinez JL, Jacobs JJ, et al. The Bmi-1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res. 2002;62:4736-4745.
53. Itahana K, Zou Y, Itahana Y, et al. Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol Cell Biol. 2003;23:389-401.
54. Kim JH, Yoon SY, Kim CN, et al. The Bmi-1 oncoprotein is overexpressed in human colorectal cancer and correlates with the reduced p16INK4a/p14ARF proteins. Cancer Lett. 2004;203: 217-224.
55. Vonlanthen S, Heighway J, Altermatt HJ, et al. The bmi-1 oncoprotein is differentially expressed in non-small cell lung cancer and correlates with INK4A-ARF locus expression. Br J Cancer. 2001; 84:1372-1376.
56. INK4A/cyclin D/Rb pathway in penile carcinoma, one of which is mediated by high-risk human papillomavirus. J Pathol. 2003;201:109-118.
57. Raaphorst FM, Otte AP, van Kemenade FJ, et al. Distinct bmi-1 and ezh2 expression patterns in thymocytes and mature T cells suggest a role for Polycomb genes in human T cell differentiation. J Immunol. 2001;166:5925-5934.
58. Raaphorst FM, van Kemenade FJ, Fieret E, et al. Cutting edge: polycomb gene expression patterns reflect distinct B cell differentiation stages in human germinal centers. J Immunol. 2000;164:1-4.
59. Tarte K, Zhan F, De Vos J, Klein B, Shaughnessy J Jr. Gene expression profiling of plasma cells and plasmablasts: toward a better understanding of the late stages of B-cell differentiation. Blood. 2003;102:592-600.
60. Lessard J, Schumacher A, Thorsteinsdottir U, van Lohuizen M, Magnuson T, Sauvageau G. Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation. Genes Dev. 1999;13:2691-2703.
61. Lessard J, Baban S, Sauvageau G. Stage-specific expression of Polycomb group genes in human bone marrow cells. Blood. 1998;91: 1216-1224.
62. van Kemenade FJ, Raaphorst FM, Blokzijl T, et al. Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood. 2001;97:3896-3901.
63. Raaphorst FM, Vermeer M, Fieret E, et al. Site-specific expression of polycomb-group genes encoding the HPC-HPH/PRC1 complex in clinically defined primary nodal and cutaneous large B-cell lymphomas. Am J Pathol. 2004;164:533-542.
64. Visser HP, Gunster MJ, Kluin-Nelemans HC, et al. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol. 2001;112:950-958.
65. Bea S, Tort F, Pinyol M, et al. BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphomas. Cancer Res. 2001;61:2409-2412.
66. Dukers DF, van Galen JC, Giroth C, et al. Unique Polycomb gene expression pattern in Hodgkin's lymphoma and Hodgkin's lymphoma-derived cell lines. Am J Pathol. 2004;164:873-881.
67. Raaphorst FM, van Kemenade FJ, Blokzijl T, et al. Coexpression of BMI-1 and EZH2 polycomb group genes in Reed-Sternberg cells of Hodgkin's disease. Am J Pathol. 2000;157:709-715.
68. Sanchez-Beato M, Sanchez E, Garcia JF, et al. Abnormal PcG protein expression in Hodgkin's lymphoma: relation with E2F6 and NFκB transcription factors. J Pathol. 2004;204:528-537.
69. Raaphorst FM, Otte AP, Meijer CJ. Polycomb-group genes as regulators of mammalian lymphopoiesis. Trends Immunol. 2001;22: 682-690.
70. Grange F, Bekkenk MW, Wechsler J, et al. Prognostic factors in primary cutaneous large B-cell lymphomas: a European multicenter study. J Clin Oncol. 2001;19:3602-3610.
71. Rijlaarsdam JU, Toonstra J, Meijer OW, Noordijk EM, Willemze R. Treatment of primary cutaneous B-cell lymphomas of follicle center cell origin: a clinical follow-up study of 55 patients treated with radiotherapy or polychemotherapy. J Clin Oncol. 1996;14:549-555.
72. Pandolfino TL, Siegel RS, Kuzel TM, Rosen ST, Guitart J. Primary cutaneous B-cell lymphoma: review and current concepts. J Clin Oncol. 2000;18:2152-2168.
73. Vermeer MH, Geelen FA, van Haselen CW, et al. Primary cutaneous large B-cell lymphomas of the legs: a distinct type of cutaneous B-cell lymphoma with an intermediate prognosis. Dutch Cutaneous Lymphoma Working Group. Arch Dermatol. 1996;132: 1304-1308.
74. de Boer WP, Oudejans JJ, Meijer CJ, Lankelma J. Analysing gene expressions with GRANK. BioInformatics. 2003;19:2000-2001.
75. Taniguchi T, Chikatsu N, Takahashi S, et al. Expression of p16INK4A and p14ARF in hematological malignancies. Leukemia. 1999;13:1760-1769.
76. Berns K, Hijmans EM, Mullenders J, et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature. 2004;428:431-437.
77. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 2003;22:5323-5335.
78. Lessard J, Sauvageau G. Bmi-1 determines proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423:255-260.
79. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M. Stem cells and cancer: the Polycomb connection. Cell. 2004;118:409-418.
80. Varambally S, Dhanasekaran SM, Zhou M, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature. 2002;419:624-629.
81. Ruter B, Wijermans PW, Lubbert M. DNA methylation as a therapeutic target in hematologic disorders: recent results in older patients with myelodysplasia and acute myeloid leukemia. Int J Hematol. 2004;80:128-135.
82. Villar-Garea A, Esteller M. Histone deacetylase inhibitors: understanding a new wave of anticancer agents. Int J Cancer. 2004;112: 171-178.