PHD fingers in human diseases: Disorders arising from misinterpreting epigenetic marks

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 647, Issue 1-2, 2008, Pages 3-12

  Baker, Lindsey A ^a   Allis, C David ^a   Wang, Gang G ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Epigenetics; H3K4 methylation; ING; NSD1; Plant Homeodomain (PHD) finger; RAG2

Indexed keywords

ALPHA THALASSEMIA X LINKED MENTAL RETARDATION PROTEIN; AUTOIMMUNE REGULATOR PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HISTONE; HISTONE H3 LYSINE 4; HOMEODOMAIN PROTEIN; INHIBITOR OF GROWTH PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; NUCLEAR RECEPTOR BINDING SET DOMAIN CONTAINING 1 PROTEIN; PHD FINGER PROTEIN 6; PLANT HOMEODOMAIN FINGER PROTEIN; RAG2 PROTEIN; UNCLASSIFIED DRUG;

CARCINOGENESIS; CHROMOSOME TRANSLOCATION; COVALENT BOND; DNA DAMAGE; DNA TEMPLATE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC CONSERVATION; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNE DEFICIENCY; IMMUNOPATHOLOGY; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NEOPLASM; NEUROLOGIC DISEASE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; SOMATIC MUTATION;

AUTOIMMUNITY; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HUMANS; MODELS, GENETIC; MODELS, MOLECULAR; MUTATION; NEOPLASMS; NERVOUS SYSTEM DISEASES; SYNDROME; TRANSCRIPTION FACTORS;

EID: 55949118684     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2008.07.004     Document Type: Review

References (112)

1. Kornberg R.D., and Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98 (1999) 285-294
2. Bernstein B.E., Meissner A., and Lander E.S. The mammalian epigenome. Cell 128 (2007) 669-681
3. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
4. Shahbazian M.D., and Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76 (2007) 75-100
5. Ruthenburg A.J., Allis C.D., and Wysocka J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25 (2007) 15-30
6. Kouzarides T. SnapShot: histone-modifying enzymes. Cell 131 (2007) 822
7. Ruthenburg A.J., Li H., Patel D.J., and Allis C.D. Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell Biol. 8 (2007) 983-994
8. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., and Patel D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14 (2007) 1025-1040
9. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., Wu C., and Allis C.D. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442 (2006) 86-90
10. Shi X., Hong T., Walter K.L., Ewalt M., Michishita E., Hung T., Carney D., Pena P., Lan F., Kaadige M.R., Lacoste N., Cayrou C., Davrazou F., Saha A., Cairns B.R., Ayer D.E., Kutateladze T.G., Shi Y., Cote J., Chua K.F., and Gozani O. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442 (2006) 96-99
11. Li H., Ilin S., Wang W., Duncan E.M., Wysocka J., Allis C.D., and Patel D.J. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442 (2006) 91-95
12. Li H., Fischle W., Wang W., Duncan E.M., Liang L., Murakami-Ishibe S., Allis C.D., and Patel D.J. Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger. Mol. Cell 28 (2007) 677-691
13. Pena P.V., Davrazou F., Shi X., Walter K.L., Verkhusha V.V., Gozani O., Zhao R., and Kutateladze T.G. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442 (2006) 100-103
14. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., Erdjument-Bromage H., Tempst P., Lin S.P., Allis C.D., Cheng X., and Bestor T.H. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448 (2007) 714-717
15. Lan F., Collins R.E., De Cegli R., Alpatov R., Horton J.R., Shi X., Gozani O., Cheng X., and Shi Y. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448 (2007) 718-722
16. Zhang K., Mosch K., Fischle W., and Grewal S.I. Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat. Struct. Mol. Biol. 15 (2008) 381-388
17. Strahl B.D., and Allis C.D. The language of covalent histone modifications. Nature 403 (2000) 41-45
18. Jones P.A., and Baylin S.B. The epigenomics of cancer. Cell 128 (2007) 683-692
19. Wang G.G., Allis C.D., and Chi P. Chromatin remodeling and cancer. Part I: Covalent histone modifications. Trends Mol. Med. 13 (2007) 363-372
20. Wang G.G., Allis C.D., and Chi P. Chromatin remodeling and cancer. Part II: ATP-dependent chromatin remodeling. Trends Mol. Med. 13 (2007) 373-380
21. Bienvenu T., and Chelly J. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 7 (2006) 415-426
22. Bienz M. The PHD finger, a nuclear protein-interaction domain. Trends Biochem. Sci. 31 (2006) 35-40
23. Matthews A.G., Kuo A.J., Ramon-Maiques S., Han S., Champagne K.S., Ivanov D., Gallardo M., Carney D., Cheung P., Ciccone D.N., Walter K.L., Utz P.J., Shi Y., Kutateladze T.G., Yang W., Gozani O., and Oettinger M.A. RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450 (2007) 1106-1110
24. Ramon-Maiques S., Kuo A.J., Carney D., Matthews A.G., Oettinger M.A., Gozani O., and Yang W. The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 18993-18998
25. Schindler U., Beckmann H., and Cashmore A.R. HAT3.1, a novel Arabidopsis homeodomain protein containing a conserved cysteine-rich region. Plant J. 4 (1993) 137-150
26. Palacios A., Munoz I.G., Pantoja-Uceda D., Marcaida M.J., Torres D., Martin-Garcia J.M., Luque I., Montoya G., and Blanco F.J. Molecular basis of histone H3K4ME3 recognition by ING4. J. Biol. Chem. (2008)
27. Taverna S.D., Ilin S., Rogers R.S., Tanny J.C., Lavender H., Li H., Baker L., Boyle J., Blair L.P., Chait B.T., Patel D.J., Aitchison J.D., Tackett A.J., and Allis C.D. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 24 (2006) 785-796
28. Iberg A.N., Espejo A., Cheng D., Kim D., Michaud-Levesque J., Richard S., and Bedford M.T. Arginine methylation of the histone H3 tail impedes effector binding. J. Biol. Chem. 283 (2008) 3006-3010
29. Kirmizis A., Santos-Rosa H., Penkett C.J., Singer M.A., Vermeulen M., Mann M., Bahler J., Green R.D., and Kouzarides T. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature (2007)
30. Org T., Chignola F., Hetenyi C., Gaetani M., Rebane A., Liiv I., Maran U., Mollica L., Bottomley M.J., Musco G., and Peterson P. The autoimmune regulator PHD finger binds to non-methylated histone H3K4 to activate gene expression. EMBO Rep. 9 (2008) 370-376
31. Iwase S., Lan F., Bayliss P., de la Torre-Ubieta L., Huarte M., Qi H.H., Whetstine J.R., Bonni A., Roberts T.M., and Shi Y. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128 (2007) 1077-1088
32. Karagianni P., Amazit L., Qin J., and Wong J. ICBP90, a novel methyl K9 H3 binding protein linking protein ubiquitination with heterochromatin formation. Mol. Cell Biol. 28 (2008) 705-717
33. Shi X., Kachirskaia I., Walter K.L., Kuo J.H., Lake A., Davrazou F., Chan S.M., Martin D.G., Fingerman I.M., Briggs S.D., Howe L., Utz P.J., Kutateladze T.G., Lugovskoy A.A., Bedford M.T., and Gozani O. Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36. J. Biol. Chem. 282 (2007) 2450-2455
34. Jung D., and Alt F.W. Unraveling V(D)J recombination; insights into gene regulation. Cell 116 (2004) 299-311
35. Oettinger M.A. How to keep V(D)J recombination under control. Immunol. Rev. 200 (2004) 165-181
36. Fugmann S.D., Lee A.I., Shockett P.E., Villey I.J., and Schatz D.G. The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu. Rev. Immunol. 18 (2000) 495-527
37. Shinkai Y., Rathbun G., Lam K.P., Oltz E.M., Stewart V., Mendelsohn M., Charron J., Datta M., Young F., Stall A.M., et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68 (1992) 855-867
38. Schwarz K., Gauss G.H., Ludwig L., Pannicke U., Li Z., Lindner D., Friedrich W., Seger R.A., Hansen-Hagge T.E., Desiderio S., Lieber M.R., and Bartram C.R. RAG mutations in human B cell-negative SCID. Science 274 (1996) 97-99
39. Marrella V., Poliani P.L., Sobacchi C., Grassi F., and Villa A. Of Omenn and mice. Trends Immunol. 29 (2008) 133-140
40. Sobacchi C., Marrella V., Rucci F., Vezzoni P., and Villa A. RAG-dependent primary immunodeficiencies. Hum. Mutat. 27 (2006) 1174-1184
41. Omenn G.S. Familial reticuloendotheliosis with eosinophilia. N. Engl. J. Med. 273 (1965) 427-432
42. Goldmit M., Ji Y., Skok J., Roldan E., Jung S., Cedar H., and Bergman Y. Epigenetic ontogeny of the Igk locus during B cell development. Nat. Immunol. 6 (2005) 198-203
43. Morshead K.B., Ciccone D.N., Taverna S.D., Allis C.D., and Oettinger M.A. Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 11577-11582
44. Sleckman B.P., Gorman J.R., and Alt F.W. Accessibility control of antigen-receptor variable-region gene assembly: role of cis-acting elements. Annu. Rev. Immunol. 14 (1996) 459-481
45. Krangel M.S. Gene segment selection in V(D)J recombination: accessibility and beyond. Nat. Immunol. 4 (2003) 624-630
46. Liu Y., Subrahmanyam R., Chakraborty T., Sen R., and Desiderio S. A plant homeodomain in RAG-2 that binds Hypermethylated lysine 4 of histone H3 is necessary for efficient antigen-receptor-gene rearrangement. Immunity 27 (2007) 561-571
47. Elkin S.K., Ivanov D., Ewalt M., Ferguson C.G., Hyberts S.G., Sun Z.Y., Prestwich G.D., Yuan J., Wagner G., Oettinger M.A., and Gozani O.P. A PHD finger motif in the C terminus of RAG2 modulates recombination activity. J. Biol. Chem. 280 (2005) 28701-28710
48. Gomez C.A., Ptaszek L.M., Villa A., Bozzi F., Sobacchi C., Brooks E.G., Notarangelo L.D., Spanopoulou E., Pan Z.Q., Vezzoni P., Cortes P., and Santagata S. Mutations in conserved regions of the predicted RAG2 kelch repeats block initiation of V(D)J recombination and result in primary immunodeficiencies. Mol. Cell Biol. 20 (2000) 5653-5664
49. Noordzij J.G., de Bruin-Versteeg S., Verkaik N.S., Vossen J.M., de Groot R., Bernatowska E., Langerak A.W., van Gent D.C., and van Dongen J.J. The immunophenotypic and immunogenotypic B-cell differentiation arrest in bone marrow of RAG-deficient SCID patients corresponds to residual recombination activities of mutated RAG proteins. Blood 100 (2002) 2145-2152
50. Villa A., Sobacchi C., Notarangelo L.D., Bozzi F., Abinun M., Abrahamsen T.G., Arkwright P.D., Baniyash M., Brooks E.G., Conley M.E., Cortes P., Duse M., Fasth A., Filipovich A.M., Infante A.J., Jones A., Mazzolari E., Muller S.M., Pasic S., Rechavi G., Sacco M.G., Santagata S., Schroeder M.L., Seger R., Strina D., Ugazio A., Valiaho J., Vihinen M., Vogler L.B., Ochs H., Vezzoni P., Friedrich W., and Schwarz K. V(D)J recombination defects in lymphocytes due to RAG mutations: severe immunodeficiency with a spectrum of clinical presentations. Blood 97 (2001) 81-88
51. Finnish-German APECED Consortium. An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Nat. Genet. 17 (1997) 399-403
52. Nagamine K., Peterson P., Scott H.S., Kudoh J., Minoshima S., Heino M., Krohn K.J., Lalioti M.D., Mullis P.E., Antonarakis S.E., Kawasaki K., Asakawa S., Ito F., and Shimizu N. Positional cloning of the APECED gene. Nat. Genet. 17 (1997) 393-398
53. Cheng M.H., Shum A.K., and Anderson M.S. What's new in the Aire?. Trends Immunol. 28 (2007) 321-327
54. Anderson M.S., Venanzi E.S., Klein L., Chen Z., Berzins S.P., Turley S.J., von Boehmer H., Bronson R., Dierich A., Benoist C., and Mathis D. Projection of an immunological self shadow within the thymus by the aire protein. Science 298 (2002) 1395-1401
55. Derbinski J., Gabler J., Brors B., Tierling S., Jonnakuty S., Hergenhahn M., Peltonen L., Walter J., and Kyewski B. Promiscuous gene expression in thymic epithelial cells is regulated at multiple levels. J. Exp. Med. 202 (2005) 33-45
56. Pitkanen J., Doucas V., Sternsdorf T., Nakajima T., Aratani S., Jensen K., Will H., Vahamurto P., Ollila J., Vihinen M., Scott H.S., Antonarakis S.E., Kudoh J., Shimizu N., Krohn K., and Peterson P. The autoimmune regulator protein has transcriptional transactivating properties and interacts with the common coactivator CREB-binding protein. J. Biol. Chem. 275 (2000) 16802-16809
57. Bjorses P., Halonen M., Palvimo J.J., Kolmer M., Aaltonen J., Ellonen P., Perheentupa J., Ulmanen I., and Peltonen L. Mutations in the AIRE gene: effects on subcellular location and transactivation function of the autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy protein. Am. J. Hum. Genet. 66 (2000) 378-392
58. Ruan Q.G., and She J.X. Autoimmune polyglandular syndrome type 1 and the autoimmune regulator. Clin. Lab. Med. 24 (2004) 305-317
59. Saugier-Veber P., Drouot N., Wolf L.M., Kuhn J.M., Frebourg T., and Lefebvre H. Identification of a novel mutation in the autoimmune regulator (AIRE-1) gene in a French family with autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy. Eur. J. Endocrinol. 144 (2001) 347-351
60. Soderbergh A., Rorsman F., Halonen M., Ekwall O., Bjorses P., Kampe O., and Husebye E.S. Autoantibodies against aromatic l-amino acid decarboxylase identifies a subgroup of patients with Addison's disease. J. Clin. Endocrinol. Metab. 85 (2000) 460-463
61. Stolarski B., Pronicka E., Korniszewski L., Pollak A., Kostrzewa G., Rowinska E., Wlodarski P., Skorka A., Gremida M., Krajewski P., and Ploski R. Molecular background of polyendocrinopathy-candidiasis-ectodermal dystrophy syndrome in a Polish population: novel AIRE mutations and an estimate of disease prevalence. Clin. Genet. 70 (2006) 348-354
62. Wolff A.S., Erichsen M.M., Meager A., Magitta N.F., Myhre A.G., Bollerslev J., Fougner K.J., Lima K., Knappskog P.M., and Husebye E.S. Autoimmune polyendocrine syndrome type 1 in Norway: phenotypic variation, autoantibodies, and novel mutations in the autoimmune regulator gene. J. Clin. Endocrinol. Metab. 92 (2007) 595-603
63. Peterson P., Pitkanen J., Sillanpaa N., and Krohn K. Autoimmune polyendocrinopathy candidiasis ectodermal dystrophy (APECED): a model disease to study molecular aspects of endocrine autoimmunity. Clin. Exp. Immunol. 135 (2004) 348-357
64. Bottomley M.J., Stier G., Pennacchini D., Legube G., Simon B., Akhtar A., Sattler M., and Musco G. NMR structure of the first PHD finger of autoimmune regulator protein (AIRE1). Insights into autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) disease. J. Biol. Chem. 280 (2005) 11505-11512
65. Garkavtsev I., Kazarov A., Gudkov A., and Riabowol K. Suppression of the novel growth inhibitor p33ING1 promotes neoplastic transformation. Nat. Genet. 14 (1996) 415-420
66. Kichina J.V., Zeremski M., Aris L., Gurova K.V., Walker E., Franks R., Nikitin A.Y., Kiyokawa H., and Gudkov A.V. Targeted disruption of the mouse ing1 locus results in reduced body size, hypersensitivity to radiation and elevated incidence of lymphomas. Oncogene 25 (2006) 857-866
67. Campos E.I., Chin M.Y., Kuo W.H., and Li G. Biological functions of the ING family tumor suppressors. Cell Mol. Life Sci. 61 (2004) 2597-2613
68. Shi X., and Gozani O. The fellowships of the INGs. J. Cell Biochem. 96 (2005) 1127-1136
69. Soliman M.A., and Riabowol K. After a decade of study-ING, a PHD for a versatile family of proteins. Trends Biochem. Sci. 32 (2007) 509-519
70. Doyon Y., Cayrou C., Ullah M., Landry A.J., Cote V., Selleck W., Lane W.S., Tan S., Yang X.J., and Cote J. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 21 (2006) 51-64
71. Doyon Y., Selleck W., Lane W.S., Tan S., and Cote J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell Biol. 24 (2004) 1884-1896
72. Campos E.I., Martinka M., Mitchell D.L., Dai D.L., and Li G. Mutations of the ING1 tumor suppressor gene detected in human melanoma abrogate nucleotide excision repair. Int. J. Oncol. 25 (2004) 73-80
73. Chen L., Matsubara N., Yoshino T., Nagasaka T., Hoshizima N., Shirakawa Y., Naomoto Y., Isozaki H., Riabowol K., and Tanaka N. Genetic alterations of candidate tumor suppressor ING1 in human esophageal squamous cell cancer. Cancer Res. 61 (2001) 4345-4349
74. Chen B., Campos E.I., Crawford R., Martinka M., and Li G. Analyses of the tumour suppressor ING1 expression and gene mutation in human basal cell carcinoma. Int. J. Oncol. 22 (2003) 927-931
75. Gong W., Suzuki K., Russell M., and Riabowol K. Function of the ING family of PHD proteins in cancer. Int. J. Biochem. Cell Biol. 37 (2005) 1054-1065
76. Kuzmichev A., Zhang Y., Erdjument-Bromage H., Tempst P., and Reinberg D. Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1). Mol. Cell Biol. 22 (2002) 835-848
77. Garate M., Campos E.I., Bush J.A., Xiao H., and Li G. Phosphorylation of the tumor suppressor p33(ING1b) at Ser-126 influences its protein stability and proliferation of melanoma cells. FASEB J. 21 (2007) 3705-3716
78. Takahashi M., Seki N., Ozaki T., Kato M., Kuno T., Nakagawa T., Watanabe K., Miyazaki K., Ohira M., Hayashi S., Hosoda M., Tokita H., Mizuguchi H., Hayakawa T., Todo S., and Nakagawara A. Identification of the p33(ING1)-regulated genes that include cyclin B1 and proto-oncogene DEK by using cDNA microarray in a mouse mammary epithelial cell line NMuMG. Cancer Res. 62 (2002) 2203-2209
79. Moore M.A., Chung K.Y., Plasilova M., Schuringa J.J., Shieh J.H., Zhou P., and Morrone G. NUP98 dysregulation in myeloid leukemogenesis. Ann. N.Y. Acad. Sci. 1106 (2007) 114-142
80. Griffis E.R., Altan N., Lippincott-Schwartz J., and Powers M.A. Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol. Biol. Cell 13 (2002) 1282-1297
81. Kasper L.H., Brindle P.K., Schnabel C.A., Pritchard C.E., Cleary M.L., and van Deursen J.M. CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol. Cell Biol. 19 (1999) 764-776
82. van Zutven L.J., Onen E., Velthuizen S.C., van Drunen E., von Bergh A.R., van den Heuvel-Eibrink M.M., Veronese A., Mecucci C., Negrini M., de Greef G.E., and Beverloo H.B. Identification of NUP98 abnormalities in acute leukemia: JARID1A (12p13) as a new partner gene. Genes Chromosomes Cancer 45 (2006) 437-446
83. Reader J.C., Meekins J.S., Gojo I., and Ning Y. A novel NUP98-PHF23 fusion resulting from a cryptic translocation t(11;17)(p15;p13) in acute myeloid leukemia. Leukemia 21 (2007) 842-844
84. Klose R.J., Yan Q., Tothova Z., Yamane K., Erdjument-Bromage H., Tempst P., Gilliland D.G., Zhang Y., and Kaelin Jr. W.G. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 128 (2007) 889-900
85. Cerveira N., Correia C., Doria S., Bizarro S., Rocha P., Gomes P., Torres L., Norton L., Borges B.S., Castedo S., and Teixeira M.R. Frequency of NUP98-NSD1 fusion transcript in childhood acute myeloid leukaemia. Leukemia 17 (2003) 2244-2247
86. Rosati R., La Starza R., Veronese A., Aventin A., Schwienbacher C., Vallespi T., Negrini M., Martelli M.F., and Mecucci C. NUP98 is fused to the NSD3 gene in acute myeloid leukemia associated with t(8;11)(p11.2;p15). Blood 99 (2002) 3857-3860
87. Huang N., vom Baur E., Garnier J.M., Lerouge T., Vonesch J.L., Lutz Y., Chambon P., and Losson R. Two distinct nuclear receptor interaction domains in NSD1, a novel SET protein that exhibits characteristics of both corepressors and coactivators. EMBO J. 17 (1998) 3398-3412
88. Tatton-Brown K., Douglas J., Coleman K., Baujat G., Cole T.R., Das S., Horn D., Hughes H.E., Temple I.K., Faravelli F., Waggoner D., Turkmen S., Cormier-Daire V., Irrthum A., and Rahman N. Genotype-phenotype associations in Sotos syndrome: an analysis of 266 individuals with NSD1 aberrations. Am. J. Hum. Genet. 77 (2005) 193-204
89. Keats J.J., Maxwell C.A., Taylor B.J., Hendzel M.J., Chesi M., Bergsagel P.L., Larratt L.M., Mant M.J., Reiman T., Belch A.R., and Pilarski L.M. Overexpression of transcripts originating from the MMSET locus characterizes all t(4;14)(p16;q32)-positive multiple myeloma patients. Blood 105 (2005) 4060-4069
90. Wang G.G., Cai L., Pasillas M.P., and Kamps M.P. NUP98-NSD1 links H3K36 methylation to Hox-A gene activation and leukaemogenesis. Nat. Cell Biol. 9 (2007) 804-812
91. Ayton P.M., and Cleary M.L. Molecular mechanisms of leukemogenesis mediated by MLL fusion proteins. Oncogene 20 (2001) 5695-5707
92. Lochner K., Siegler G., Fuhrer M., Greil J., Beck J.D., Fey G.H., and Marschalek R. A specific deletion in the breakpoint cluster region of the ALL-1 gene is associated with acute lymphoblastic T-cell leukemias. Cancer Res. 56 (1996) 2171-2177
93. Micci F., Panagopoulos I., Bjerkehagen B., and Heim S. Consistent rearrangement of chromosomal band 6p21 with generation of fusion genes JAZF1/PHF1 and EPC1/PHF1 in endometrial stromal sarcoma. Cancer Res. 66 (2006) 107-112
94. Sarma K., Margueron R., Ivanov A., Pirrotta V., and Reinberg D. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol. Cell Biol. 28 (2008) 2718-2731
95. Kurotaki N., Imaizumi K., Harada N., Masuno M., Kondoh T., Nagai T., Ohashi H., Naritomi K., Tsukahara M., Makita Y., Sugimoto T., Sonoda T., Hasegawa T., Chinen Y., Tomita Ha H.A., Kinoshita A., Mizuguchi T., Yoshiura Ki K., Ohta T., Kishino T., Fukushima Y., Niikawa N., and Matsumoto N. Haploinsufficiency of NSD1 causes Sotos syndrome. Nat. Genet. 30 (2002) 365-366
96. Douglas J., Hanks S., Temple I.K., Davies S., Murray A., Upadhyaya M., Tomkins S., Hughes H.E., Cole T.R., and Rahman N. NSD1 mutations are the major cause of Sotos syndrome and occur in some cases of Weaver syndrome but are rare in other overgrowth phenotypes. Am. J. Hum. Genet. 72 (2003) 132-143
97. Rayasam G.V., Wendling O., Angrand P.O., Mark M., Niederreither K., Song L., Lerouge T., Hager G.L., Chambon P., and Losson R. NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J. 22 (2003) 3153-3163
98. Gibbons R. Alpha thalassaemia-mental retardation, X linked. Orphanet J. Rare Dis. 1 (2006) 15
99. Raymond F.L. X linked mental retardation: a clinical guide. J. Med. Genet. 43 (2006) 193-200
100. Gibbons R.J., Picketts D.J., Villard L., and Higgs D.R. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell 80 (1995) 837-845
101. Berube N.G., Mangelsdorf M., Jagla M., Vanderluit J., Garrick D., Gibbons R.J., Higgs D.R., Slack R.S., and Picketts D.J. The chromatin-remodeling protein ATRX is critical for neuronal survival during corticogenesis. J. Clin. Invest. 115 (2005) 258-267
102. Argentaro A., Yang J.C., Chapman L., Kowalczyk M.S., Gibbons R.J., Higgs D.R., Neuhaus D., and Rhodes D. Structural consequences of disease-causing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 11939-11944
103. Stayton C.L., Dabovic B., Gulisano M., Gecz J., Broccoli V., Giovanazzi S., Bossolasco M., Monaco L., Rastan S., Boncinelli E., et al. Cloning and characterization of a new human Xq13 gene, encoding a putative helicase. Hum. Mol. Genet. 3 (1994) 1957-1964
104. Cardoso C., Timsit S., Villard L., Khrestchatisky M., Fontes M., and Colleaux L. Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum. Mol. Genet. 7 (1998) 679-684
105. Le Douarin B., Nielsen A.L., Garnier J.M., Ichinose H., Jeanmougin F., Losson R., and Chambon P. A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J. 15 (1996) 6701-6715
106. Berube N.G., Smeenk C.A., and Picketts D.J. Cell cycle-dependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum. Mol. Genet. 9 (2000) 539-547
107. Nan X., Hou J., Maclean A., Nasir J., Lafuente M.J., Shu X., Kriaucionis S., and Bird A. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 2709-2714
108. Petrij F., Giles R.H., Dauwerse H.G., Saris J.J., Hennekam R.C., Masuno M., Tommerup N., van Ommen G.J., Goodman R.H., Peters D.J., et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 376 (1995) 348-351
109. Kalkhoven E., Roelfsema J.H., Teunissen H., den Boer A., Ariyurek Y., Zantema A., Breuning M.H., Hennekam R.C., and Peters D.J. Loss of CBP acetyltransferase activity by PHD finger mutations in Rubinstein-Taybi syndrome. Hum. Mol. Genet. 12 (2003) 441-450
110. Lower K.M., Turner G., Kerr B.A., Mathews K.D., Shaw M.A., Gedeon A.K., Schelley S., Hoyme H.E., White S.M., Delatycki M.B., Lampe A.K., Clayton-Smith J., Stewart H., van Ravenswaay C.M., de Vries B.B., Cox B., Grompe M., Ross S., Thomas P., Mulley J.C., and Gecz J. Mutations in PHF6 are associated with Borjeson-Forssman-Lehmann syndrome. Nat. Genet. 32 (2002) 661-665
111. Voss A.K., Gamble R., Collin C., Shoubridge C., Corbett M., Gecz J., and Thomas T. Protein and gene expression analysis of Phf6, the gene mutated in the Borjeson-Forssman-Lehmann Syndrome of intellectual disability and obesity. Gene. Expr. Patterns 7 (2007) 858-871
112. Lee J., Hagerty S., Cormier K.A., Ferrante R.J., Kung A.L., and Ryu H. Monoallele deletion of CBP leads to pericentromeric heterochromatin condensation through ESET expression and histone H3 (K9) methylation. Hum. Mol. Genet. (2008)