The role of PRDMs in cancer: One family, two sides

Current Opinion in Genetics and Development

Volumn 36, Issue , 2016, Pages 83-91

  Mzoughi, Slim ^a,b   Tan, Ying Xim ^a   Low, Diana ^a   Guccione, Ernesto ^a,b,c  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DIVISION OF MEDICAL ONCOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; NUCLEIC ACID BINDING PROTEIN; PROTEIN PRDM; PROTEIN PRDM10; PROTEIN PRDM11; PROTEIN PRDM12; PROTEIN PRDM13; PROTEIN PRDM14; PROTEIN PRDM15; PROTEIN PRDM16; PROTEIN PRDM17; PROTEIN PRDM2; PROTEIN PRDM3; PROTEIN PRDM4; PROTEIN PRDM5; PROTEIN PRDM6; PROTEIN PRDM7; PROTEIN PRDM8; PROTEIN PRDM9; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN;

CARCINOGENESIS; CARCINOGENICITY; DISEASE ASSOCIATION; GENE FUNCTION; GENE MUTATION; HEMATOLOGIC MALIGNANCY; HUMAN; LARGE CELL LYMPHOMA; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRDM GENE; PRDM14 GENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; STRUCTURE ACTIVITY RELATION; TUMOR SUPPRESSOR GENE; ZINC FINGER MOTIF; GENE EXPRESSION REGULATION; GENETICS; MULTIGENE FAMILY; NEOPLASM; PROTEIN PROTEIN INTERACTION; RNA-BINDING DOMAIN;

DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MULTIGENE FAMILY; NEOPLASMS; PROTEIN INTERACTION MAPS; REPRESSOR PROTEINS; RNA-BINDING MOTIFS;

EID: 84968649895     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2016.03.009     Document Type: Review

References (75)

1. Fumasoni I., Meani N., Rambaldi D., Scafetta G., Alcalay M., Ciccarelli F.D. Family expansion and gene rearrangements contributed to the functional specialization of PRDM genes in vertebrates. BMC Evol Biol 2007, 7:187.
2. Clifton M.K., Westman B.J., Thong S.Y., O'Connell M.R., Webster M.W., Shepherd N.E., Quinlan K.G., Crossley M., Blobel G.A., Mackay J.P. The identification and structure of an N-terminal PR domain show that FOG1 is a member of the prdm family of proteins. PLOS ONE 2014, 9.
3. Ma Z.Y., Swigut T., Valouev A., Rada-Iglesias A., Wysocka J. Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat Struct Mol Biol 2011, 18:120-U175.
4. Yamaji M., Ueda J., Hayashi K., Ohta H., Yabuta Y., Kurimoto K., Nakato R., Yamada Y., Shirahige K., Saitou M. PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 2013, 12:368-382.
5. Huang S., Shao G., Liu L. The PR domain of the Rb-binding zinc finger protein RIZ1 is a protein binding interface and is related to the SET domain functioning in chromatin-mediated gene expression. J Biol Chem 1998, 273:15933-15939.
6. Wu H., Min J., Lunin V.V., Antoshenko T., Dombrovski L., Zeng H., Allali-Hassani A., Campagna-Slater V., Vedadi M., Arrowsmith C.H., et al. Structural biology of human H3K9 methyltransferases. PLoS ONE 2010, 5:e8570.
7. Hayashi K., Yoshida K., Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 2005, 438:374-378.
8. Koh-Stenta X., Joy J., Poulsen A., Li R., Tan Y., Shim Y., Min J.H., Wu L.L., Ngo A., Peng J.H., et al. Characterization of the histone methyltransferase PRDM9 using biochemical, biophysical and chemical biology techniques. Biochem J 2014, 461:323-334.
9. Eram M.S., Bustos S.P., Lima-Fernandes E., Siarheyeva A., Senisterra G., Hajian T., Chau I., Duan S., Wu H., Dombrovski L., et al. Trimethylation of histone H3 lysine 36 by human methyltransferase PRDM9 protein. J Biol Chem 2014, 289:12177-12188.
10. Derunes C., Briknarova K., Geng L., Li S., Gessner C.R., Hewitt K., Wu S., Huang S., Woods V.I., Ely K.R. Characterization of the PR domain of RIZ1 histone methyltransferase. Biochem Biophys Res Commun 2005, 333:925-934.
11. Pinheiro I., Margueron R., Shukeir N., Eisold M., Fritzsch C., Richter F.M., Mittler G., Genoud C., Goyama S., Kurokawa M., et al. Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 2012, 150:948-960.
12. Eom G.H., Kim K., Kim S.M., Kee H.J., Kim J.Y., Jin H.M., Kim J.R., Kim J.H., Choe N., Kim K.B., et al. Histone methyltransferase PRDM8 regulates mouse testis steroidogenesis. Biochem Biophys Res Commun 2009, 388:131-136.
13. Hohenauer T., Moore A.W. The Prdm family: expanding roles in stem cells and development. Development 2012, 139:2267-2282.
14. Fog C.K., Galli G.G., Lund A.H. PRDM proteins: important players in differentiation and disease. BioEssays 2012, 34:50-60.
15. Huang S. The retinoblastoma protein-interacting zinc finger gene RIZ in 1p36-linked cancers. Front Biosci 1999, 4:D528-D532.
16. Mock B.A., Coleman M.P., Huang S. Riz maps to distal chromosome 4 near genes involved in tumorigenesis and nerve degeneration. Mamm Genome 1996, 7:637.
17. Buyse I.M., Takahashi E., Huang S. Physical mapping of the retinoblastoma interacting zinc finger gene RIZ to D1S228 on chromosome 1p36. Genomics 1996, 34:119-121.
18. Mock B.A., Liu L., LePaslier D., Huang S. The B-lymphocyte maturation promoting transcription factor BLIMP1/PRDI-BF1 maps to D6S447 on human chromosome 6q21-q22.1 and the syntenic region of mouse chromosome 10. Genomics 1996, 37:24-28.
19. Yang X.H., Huang S. PFM1 (PRDM4), a new member of the PR-domain family, maps to a tumor suppressor locus on human chromosome 12q23-q24.1. Genomics 1999, 61:319-325.
20. Pasqualucci L., Compagno M., Houldsworth J., Monti S., Grunn A., Nandula S.V., Aster J.C., Murty V.V., Shipp M.A., Dalla-Favera R. Inactivation of the PRDM1/BLIMP1 gene in diffuse large B cell lymphoma. J Exp Med 2006, 203:311-317.
21. Nie K., Gomez M.F., Landgraf P., Garcia J.F., Liu Y., Tan L.H.C., Chadbum A., Tuschl T., Knowles D.M., Tam W. MicroRNA-mediated translation repression of PRDM1 in Hodgkin/Reed Sternberg cells - a potential pathogenetic lesion in Hodgkin lymphoma. Blood 2006, 108:185a-186a.
22. Nie K., Zhang T.T., Allawi H., Gomez M., Liu Y.F., Chadburn A., Wang Y.L., Knowles D.M., Tam W. Epigenetic down-regulation of the tumor suppressor gene PRDM1/Blimp-1 in diffuse large B cell lymphomas a potential role of the microRNA Let-7. Am J Pathol 2010, 177:1470-1479.
23. Tam W., Gomez M., Chadburn A., Lee J.W., Chan W.C., Knowles D.M. Mutational analysis of PRDM1 indicates a tumor-suppressor role in diffuse large B-cell lymphomas. Blood 2006, 107:4090-4100.
24. Mandelbaum J., Bhagat G., Tang H.Y., Mo T.W., Brahmachary M., Shen Q.O., Chadburn A., Rajewsky K., Tarakhovsky A., Pasqualucci L., et al. BLIMP1 is a tumor suppressor gene frequently disrupted in activated B cell-like diffuse large B cell lymphoma. Cancer Cell 2010, 18:568-579.
25. Calado D.P., Zhang B., Srinivasan L., Sasaki Y., Seagal J., Unitt C., Rodig S., Kutok J., Tarakhovsky A., Schmidt-Supprian M., et al. Constitutive canonical NF-kappaB activation cooperates with disruption of BLIMP1 in the pathogenesis of activated B cell-like diffuse large cell lymphoma. Cancer Cell 2010, 18:580-589.
26. Yu J., Angelin-Duclos C., Greenwood J., Liao J., Calame K. Transcriptional repression by Blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol Cell Biol 2000, 20:2592-2603.
27. Gyory I., Wu J., Fejer G., Seto E., Wright K.L. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat Immunol 2004, 5:299-308.
28. Koh C.M.B.M., Guccione E. The where and the how of PRMT5. Curr Mol Biol Rep 2015, 1:19-28.
29. Ancelin K., Lange U.C., Hajkova P., Schneider R., Bannister A.J., Kouzarides T., Surani M.A. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 2006, 8:623-630.
30. Koh C.M., Bezzi M., Low D.H., Ang W.X., Teo S.X., Gay F.P., Al-Haddawi M., Tan S.Y., Osato M., Sabo A., et al. MYC regulates the core pre-mRNA splicing machinery as an essential step in lymphomagenesis. Nature 2015, 523:96-100.
31. Gu Z., Li Y., Lee P., Liu T., Wan C., Wang Z. Protein arginine methyltransferase 5 functions in opposite ways in the cytoplasm and nucleus of prostate cancer cells. PLoS ONE 2012, 7:e44033.
32. Du Y., Carling T., Fang W., Piao Z., Shen J.C., Huang S. Hypermethylation in human cancers of the RIZ1 tumor suppressor gene, a member of a histone/protein methyltransferase superfamily. Cancer Res 2001, 61:8094-8099.
33. Piao Z., Fang W., Malkhosyan S., Kim H., Horii A., Perucho M., Huang S. Frequent frameshift mutations of RIZ in sporadic gastrointestinal and endometrial carcinomas with microsatellite instability. Cancer Res 2000, 60:4701-4704.
34. Liu Z.Y., Wang J.Y., Liu H.H., Ma X.M., Wang C.L., Zhang X.P., Tao Y.Q., Lu Y.C., Liao J.C., Hu G.H. Retinoblastoma protein-interacting zinc-finger gene 1 (RIZ1) dysregulation in human malignant meningiomas. Oncogene 2013, 32:1216-1222.
35. Zhang C.J., Li H.M., Wang Y., Liu W.J., Zhang Q.H., Zhang T.G., Zhang X.Y., Han B., Zhou G.Y. Epigenetic inactivation of the tumor suppressor gene RIZ1 in hepatocellular carcinoma involves both DNA methylation and histone modifications. J Hepatol 2010, 53:889-895.
36. Kim K.C., Geng L.Q., Huang S. Inactivation of a histone methyltransferase by mutations in human cancers. Cancer Res 2003, 63:7619-7623.
37. Steele-Perkins G., Fang W., Yang X.H., Van Gele M., Carling T., Gu J., Buyse I.M., Fletcher J.A., Liu J.S., Bronson R., et al. Tumor formation and inactivation of RIZ1, an Rb-binding member of a nuclear protein-methyltransferase superfamily. Genes Dev 2001, 15:2250-2262.
38. Abu Shadat N.M., Koide N., Khuda I.I.E., Dagvadorj J., Tumurkhuu G., Naiki Y., Komatsu T., Yoshida T., Yokochi T. Retinoblastoma protein-interacting zinc finger 1 (RIZ1) regulates the proliferation of monocytic leukemia cells via activation of p53. Cancer Investig 2010, 28:806-812.
39. Pastural E., Takahashi N., Dong W.F., Bainbridge M., Hull A., Pearson D., Huang S., Lowsky R., DeCoteau J.F., Geyer C.R. RIZ1 repression is associated with insulin-like growth factor-1 signaling activation in chronic myeloid leukemia cell lines. Oncogene 2007, 26:1586-1594.
40. Abbondanza C., Medici N., Nigro V., Rossi V., Gallo L., Piluso G., Belsito A., Roscigno A., Bontempo P., Puca A.A., et al. The retinoblastoma-interacting zinc-finger protein RIZ is a downstream effector of estrogen action. Proc Natl Acad Sci U S A 2000, 97:3130-3135.
41. Gazzerro P., Abbondanza C., D'Arcangelo A., Rossi M., Medici N., Moncharmont B., Puca G.A. Modulation of RIZ gene expression is associated to estradiol control of MCF-7 breast cancer cell proliferation. Exp Cell Res 2006, 312:340-349.
42. Deng Q.D., Huang S. PRDM5 is silenced in human cancers and has growth suppressive activities. Oncogene 2004, 23:4903-4910.
43. Duan Z., Person R.E., Lee H.H., Huang S., Donadieu J., Badolato R., Grimes H.L., Papayannopoulou T., Horwitz M.S. Epigenetic regulation of protein-coding and MicroRNA genes by the gfi 1-interacting tumor suppressor PRDM5. Mol Cell Biol 2007, 27:6889-6902.
44. Hofvander J., Tayebwa J., Nilsson J., Magnusson L., Brosjo O., Larsson O., Vult von Steyern F., Mandahl N., Fletcher C.D., Mertens F. Recurrent PRDM10 gene fusions in undifferentiated pleomorphic sarcoma. Clin Cancer Res 2015, 21:864-869.
45. Reid A.G., Nacheva E.P. A potential role for PRDM12 in the pathogenesis of chronic myeloid leukaemia with derivative chromosome 9 deletion. Leukemia 2004, 18:178-180.
46. Yang C.M., Shinkai Y. Prdm12 is induced by retinoic acid and exhibits anti-proliferative properties through the cell cycle modulation of P19 embryonic carcinoma cells. Cell Struct Funct 2013, 38:197-206.
47. Hussin J., Sinnett D., Casals F., Idaghdour Y., Bruat V., Saillour V., Healy J., Grenier J.C., de Malliard T., Busche S., et al. Rare allelic forms of PRDM9 associated with childhood leukemogenesis. Genome Res 2013, 23:419-430.
48. Woodward E.L., Olsson M.L., Johansson B., Paulsson K. Allelic variants of PRDM9 associated with high hyperdiploid childhood acute lymphoblastic leukaemia. Br J Haematol 2014, 166:947-949.
49. Fog C.K., Asmar F., Come C., Jensen K.T., Johansen J.V., Kheir T.B., Jacobsen L., Friis C., Louw A., Rosgaard L., et al. Loss of PRDM11 promotes MYC-driven lymphomagenesis. Blood 2015, 125:1272-1281.
50. Fears S., Mathieu C., ZeleznikLe N., Huang S., Rowley J.D., Nucifora G. Intergenic splicing of MDS1 and EVI1 occurs in normal tissues as well as in myeloid leukemia and produces a new member of the PR domain family. Proc Natl Acad Sci U S A 1996, 93:1642-1647.
51. Morishita K., Parganas E., Willman C.L., Whittaker M.H., Drabkin H., Oval J., Taetle R., Valentine M.B., Ihle J.N. Activation of evi1 gene-expression in human acute myelogenous leukemias by translocations spanning 300-400 kilobases on chromosome band-3q26. Proc Natl Acad Sci U S A 1992, 89:3937-3941.
52. Arai S., Yoshimi A., Shimabe M., Ichikawa M., Nakagawa M., Imai Y., Goyama S., Kurokawa M. Evi-1 is a transcriptional target of mixed-lineage leukemia oncoproteins in hematopoietic stem cells. Blood 2011, 117:6304-6314.
53. Buonamici S., Li D.L., Chi Y.Q., Zhao R., Wang X.R., Brace L., Ni H.Y., Saunthararajah Y., Nucifora G. EVI1 induces myelodysplastic syndrome in mice. J Clin Investig 2004, 114:713-719.
54. Jin G.A., Yamazaki Y., Takuwa M., Takahara T., Kaneko K., Kuwata T., Miyata S., Nakamura T: Trib1 Evi1 cooperate with Hoxa and Meis1 in myeloid leukemogenesis. Blood 2007, 109:3998-4005.
55. Kustikova O.S., Schwarzer A., Stahlhut M., Brugman M.H., Neumann T., Yang M., Li Z., Schambach A., Heinz N., Gerdes S., et al. Activation of Evi1 inhibits cell cycle progression and differentiation of hematopoietic progenitor cells. Leukemia 2013, 27:1127-1138.
56. Louz D., van den Broek M., Verbakel S., Vankan Y., van Lom K., Joosten M., Meijer D., Lowenberg B., Delwel R. Erythroid defects and increased retrovirally-induced tumor formation in Evi1 transgenic mice. Leukemia 2000, 14:1876-1884.
57. Yoshimi A., Goyama S., Watanabe-Okochi N., Yoshiki Y., Nannya Y., Nitta E., Arai S., Sato T., Shimabe M., Nakagawa M., et al. Evi1 represses PTEN expression and activates PI3K/AKT/mTOR via interactions with polycomb proteins. Blood 2011, 117:3617-3628.
58. Du Y., Jenkins N.A., Copeland N.G. Insertional mutagenesis identifies genes that promote the immortalization of primary bone marrow progenitor cells. Blood 2005, 106:3932-3939.
59. Nishikata I., Sasaki H., Iga M., Tateno Y., Imayoshi S., Asou N., Nakamura T., Morishita K. A novel EVIl gene family, MEL1 lacking a PR domain (MELlS) is expressed mainly in t(1;3)(p36;q21)-positive AML and blocks G-CSF-induced myeloid differentiation. Blood 2003, 102:3323-3332.
60. Shing D.C., Trubia M., Marchesi F., Radaelli E., Belloni E., Tapinassi C., Scanziani E., Mecucci C., Crescenzi B., Lahortiga I., et al. Overexpression of sPRDM16 coupled with loss of p53 induces myeloid leukemias in mice. J Clin Invest 2007, 117:3696-3707.
61. Yoshida M., Nosaka K., Yasunaga J., Nishikata I., Morishita K., Matsuoka M. Aberrant expression of the MEL1S gene identified in association with hypomethylation in adult T-cell leukemia cells. Blood 2004, 103:2753-2760.
62. Gyory I., Fejer G., Ghosh N., Seto E., Wright K.L. Identification of a functionally impaired positive regulatory domain I binding factor 1 transcription repressor in myeloma cell lines. J Immunol 2003, 170:3125-3133.
63. Zhang Y.W., Xie H.Q., Chen Y., Jiao B., Shen Z.X., Chen S.J., Zhao W.L. Loss of promoter methylation contributes to the expression of functionally impaired PRDM1 beta isoform in diffuse large B-cell lymphoma. Int J Hematol 2010, 92:439-444.
64. Abbondanza C., De Rosa C., D'Arcangelo A., Pacifico M., Spizuoco C., Piluso G., Di Zazzo E., Gazzerro P., Medici N., Moncharmont B., et al. Identification of a functional estrogen-responsive enhancer element in the promoter 2 of PRDM2 gene in breast cancer cell lines. J Cell Physiol 2012, 227:964-975.
65. Wu Y., Ferguson J.E., Wang H., Kelley R., Ren R., McDonough H., Meeker J., Charles P.C., Wang H., Patterson C. PRDM6 is enriched in vascular precursors during development and inhibits endothelial cell proliferation, survival, and differentiation. J Mol Cell Cardiol 2008, 44:47-58.
66. Davis C.A., Haberland M., Arnold M.A., Sutherland L.B., McDonald O.G., Richardson J.A., Childs G., Harris T.M., Owens G.K., Olson E.N. PRISM/PRDM6, a transcriptional repressor that promotes the proliferative gene program in smooth muscle cells. Circ Res 2006, 99:E21.
67. Dettman E.J., Justice M.J. The zinc finger SET domain gene Prdm14 is overexpressed in lymphoblastic lymphomas with retroviral insertions at Evi32. PLoS ONE 2008, 3.
68. Dettman E.J., Simko S.J., Ayanga B., Carofino B.L., Margolin J.F., Morse H.C., Justice M.J. Prdm14 initiates lymphoblastic leukemia after expanding a population of cells resembling common lymphoid progenitors. Oncogene 2011, 30:2859-2873.
69. Nishikawa N., Toyota M., Suzuki H., Honma T., Fujikane T., Ohmura T., Nishidate T., Ohe-Toyota M., Maruyama R., Sonoda T., et al. Gene amplification and overexpression of PRDM14 in breast cancers. Cancer Res 2007, 67:9649-9657.
70. Carofino B.L., Ayanga B., Justice M.J. A mouse model for inducible overexpression of Prdm14 results in rapid-onset and highly penetrant T-cell acute lymphoblastic leukemia (T-ALL). Dis Models Mech 2013, 6:1494-1506.
71. Bi H.X., Shi H.B., Zhang T., Cui G. PRDM14 promotes the migration of human non-small cell lung cancer through extracellular matrix degradation in vitro. Chin Med J 2015, 128:373-377.
72. Snellenberg S., Cillessen S.A., Van Criekinge W., Bosch L., Meijer C.J., Snijders P.J., Steenbergen R.D. Methylation-mediated repression of PRDM14 contributes to apoptosis evasion in HPV-positive cancers. Carcinogenesis 2014, 35:2611-2618.
73. Hsu C.H., Peng K.L., Jhang H.C., Lin C.H., Wu S.Y., Chiang C.M., Lee S.C., Yu W.C., Juan L.J. The HPV E6 oncoprotein targets histone methyltransferases for modulating specific gene transcription. Oncogene 2012, 31:2335-2349.
74. Chan Y.S., Goke J., Lu X.Y., Venkatesan N., Feng B., Su I.H., Ng H.H. A PRC2-dependent repressive role of PRDM14 in human embryonic stem cells and induced pluripotent stem cell reprogramming. Stem Cells 2013, 31:682-692.
75. Rea S., Eisenhaber F., O'Carroll N., Strahl B.D., Sun Z.W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000, 406:593-599.