Epigenetics and Chromatin Biology Group, Gupta Lab., Cancer Research Institute, Advanced Centre for Treatment, Research and Education in Cancer, Tata Memorial Centre, Navi Mumbai, India
,
Epigenetics and Chromatin Biology Group, Gupta Lab., Cancer Research Institute, Advanced Centre for Treatment, Research and Education in Cancer, Tata Memorial Centre, Navi Mumbai, India
,
Epigenetics and Chromatin Biology Group, Gupta Lab., Cancer Research Institute, Advanced Centre for Treatment, Research and Education in Cancer, Tata Memorial Centre, Navi Mumbai, India
1 Epigenetics and Chromatin Biology Group, Gupta Lab., Cancer Research Institute, Advanced Centre for Treatment, Research and Education in Cancer, Tata Memorial Centre, Navi Mumbai, India
2 Epigenetics and Chromatin Biology Group, Gupta Lab., Cancer Research Institute, Advanced Centre for Treatment, Research and Education in Cancer, Tata Memorial Centre, Navi Mumbai, India
3 Epigenetics and Chromatin Biology Group, Gupta Lab., Cancer Research Institute, Advanced Centre for Treatment, Research and Education in Cancer, Tata Memorial Centre, Navi Mumbai, India
Histones, the structural unit of chromatin, must be assembled/dissembled to preserve or change chromatin organization in accordance to cellular needs. Initially, function of histone chaperones was thought to be only “histone carriers/vehicles”, but now with accumulating evidences they are known to be the key actors of histone metabolism. With this outburst of knowledge, histone chaperones are now placed at the center of gene regulation, having roles to play in DNA replication, repair and transcription. This review will focus on the current knowledge we have about the role of histone chaperones in regulating cellular processes and their relation to disease. In addition, we discuss the potential of histone chaperones as a therapeutic target.
KeywordsHistonesChromatinCancerTherapeutic Target
Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. and Richmond, T.J. (1997) Crystal Structure of the Nucleosome Core Particle at 2.8 A Resolution. Nature, 389, 251-260. http://dx.doi.org/10.1038/38444
Smith, S. and Stillman, B. (1991) Stepwise Assembly of Chromatin during DNA Replication in Vitro. EMBO Journal, 10, 971-980.
Thoma, F., Koller, T. and Klug, A. (1979) Involvement of Histone H1 in the Organization of the Nucleosome and of the Salt-Dependent Superstructures of Chromatin. Journal of Cell Biology, 83, 403-427. http://dx.doi.org/10.1083/jcb.83.2.403
Panetta, G., Buttinelli, M., Flaus, A., Richmond, T.J. and Rhodes, D. (1998) Differential Nucleosome Positioning on Xenopus Oocyte and Somatic 5 S RNA Genes Determines Both TFIIIA and H1 Binding: A Mechanism for Selective H1 Repression. Journal of Cell Biology, 282, 683-697.
Lowary, P.T. and Widom, J. (1998) New DNA Sequence Rules for High Affinity Binding to Histone Octamer and Sequence-Directed Nucleosome Positioning. Journal of Cell Biology, 276, 19-42.
Verreault, A. (2000) De Novo Nucleosome Assembly: New Pieces in an Old Puzzle. Genes & Development, 14, 1430-1438.
Orphanides, G., LeRoy, G., Chang, C.H., Luse, D.S. and Reinberg, D. (1998) FACT, a Factor That Facilitates Transcript Elongation through Nucleosomes. Cell, 92, 105-116. http://dx.doi.org/10.1016/S0092-8674(00)80903-4
Orphanides, G. and Reinberg, D. (2000) RNA Polymerase II Elongation through Chromatin. Nature, 407, 471-475. http://dx.doi.org/10.1038/35035000
Smith, S. and Stillman, B. (1989) Purification and Characterization of CAF-I, a Human Cell Factor Required for Chromatin Assembly during DNA Replication in Vitro. Cell, 58, 15-25. http://dx.doi.org/10.1016/0092-8674(89)90398-X
De Robertis, E.M., Longthorne, R.F. and Gurdon, J.B. (1978) Intracellular Migration of Nuclear Proteins in Xenopus Oocytes. Nature, 272, 254-256. http://dx.doi.org/10.1038/272254a0
Tagami, H., Ray-Gallet, D., Almouzni, G. and Nakatani, Y. (2004) Histone H3.1 and H3.3 Complexes Mediate Nucleosome Assembly Pathways Dependent or Independent of DNA Synthesis. Cell, 116, 51-61. http://dx.doi.org/10.1016/S0092-8674(03)01064-X
Luk, E., Vu, N.D., Patteson, K., Mizuguchi, G., Wu, W.H., Ranjan, A., Backus, J., Sen, S., Lewis, M., Bai, Y. and Wu, C. (2007) Chz1, a Nuclear Chaperone for Histone H2AZ. Molecular Cell, 25, 357-368. http://dx.doi.org/10.1016/j.molcel.2006.12.015
Obri, A., Ouararhni, K., Papin, C., Diebold, M.L., Padmanabhan, K., Marek, M., Stoll, I., Roy, L., Reilly, P.T., Mak, T.W., Dimitrov, S., Romier, C. and Hamiche, A. (2014) ANP32E Is a Histone Chaperone That Removes H2A.Z from Chromatin. Nature, 505, 648-653. http://dx.doi.org/10.1016/j.molcel.2006.12.015
Goldberg, A.D., Banaszynski, L.A., Noh, K.M., Lewis, P.W., Elsaesser, S.J., Stadler, S., Dewell, S., Law, M., Guo, X., Li, X., Wen, D., Chapgier, A., DeKelver, R.C., Miller, J.C., Lee, Y.L., Boydston, E.A., Holmes, M.C., Gregory, P.D., Greally, J.M., Rafii, S., Yang, C., Scambler, P.J., Garrick, D., Gibbons, R.J., Higgs, D.R., Cristea, I.M., Urnov, F.D., Zheng, D. and Allis, C.D. (2010) Distinct Factors Control Histone Variant H3.3 Localization at Specific Genomic Regions. Cell, 140, 678-691. http://dx.doi.org/10.1016/j.cell.2010.01.003
Shintomi, K., Iwabuchi, M., Saeki, H., Ura, K., Kishimoto, T. and Ohsumi, K. (2005) Nucleosome Assembly Protein-1 Is a Linker Histone Chaperone in Xenopus Eggs. Proceedings of the National Academy of Sciences of the United States of America, 102, 8210-8215. http://dx.doi.org/10.1073/pnas.0500822102
Wade, P.A. and Kikyo, N. (2002) Chromatin Remodeling in Nuclear Cloning. European Journal of Biochemistry, 269, 2284-2287. http://dx.doi.org/10.1046/j.1432-1033.2002.02887.x
Gadad, S.S., Senapati, P., Syed, S.H., Rajan, R.E., Shandilya, J., Swaminathan, V., Chatterjee, S., Colombo, E., Dimitrov, S., Pelicci, P.G., Ranga, U. and Kundu, T.K. (2011) The Multifunctional Protein Nucleophosmin (NPM1) Is a Human Linker Histone H1 Chaperone. Biochemistry, 50, 2780-2789. http://dx.doi.org/10.1021/bi101835j
Angelov, D., Bondarenko, V.A., Almagro, S., Menoni, H., Mongelard, F., Hans, F., Mietton, F., Studitsky, V.M., Hamiche, A., Dimitrov, S. and Bouvet, P. (2006) Nucleolin Is a Histone Chaperone with FACT-Like Activity and Assists Remodeling of Nucleosomes. EMBO Journal, 25, 1669-1679. http://dx.doi.org/10.1038/sj.emboj.7601046
Park, Y.J. and Luger, K. (2006) The Structure of Nucleosome Assembly Protein 1. Proceedings of the National Academy of Sciences of the United States of America, 103, 1248-1253. http://dx.doi.org/10.1073/pnas.0508002103
van Dijk, J., Miro, J., Strub, J.M., Lacroix, B., van Dorsselaer, A., Edde, B. and Janke, C. (2008) Polyglutamylation Is a Post-Translational Modification with a Broad Range of Substrates. Journal of Biological Chemistry, 283, 3915-3922. http://dx.doi.org/10.1074/jbc.M705813200
Daganzo, S.M., Erzberger, J.P., Lam, W.M., Skordalakes, E., Zhang, R., Franco, A.A., Brill, S.J., Adams, P.D., Berger, J.M. and Kaufman, P.D. (2003) Structure and Function of the Conserved Core of Histone Deposition Protein Asf1. Current Biology, 13, 2148-2158. http://dx.doi.org/10.1016/j.cub.2003.11.027
DeSilva, H., Lee, K. and Osley, M.A. (1998) Functional Dissection of Yeast Hir1p, a WD Repeat-Containing Transcriptional Corepressor. Genetics, 148, 657-667.
Kaufman, P.D., Kobayashi, R., Kessler, N. and Stillman, B. (1995) The p150 and p60 Subunits of Chromatin Assembly Factor I: A Molecular Link between Newly Synthesized Histones and DNA Replication. Cell, 81, 1105-1114. http://dx.doi.org/10.1016/S0092-8674(05)80015-7
Muto, S., Senda, M., Akai, Y., Sato, L., Suzuki, T., Nagai, R., Senda, T. and Horikoshi, M. (2007) Relationship between the Structure of SET/TAF-Iβ/INHAT and Its Histone Chaperone Activity. Proceedings of the National Academy of Sciences of the United States of America, 104, 4285-4290. http://dx.doi.org/10.1073/pnas.0603762104
Park, Y.J. and Luger, K. (2008) Histone Chaperones in Nucleosome Eviction and Histone Exchange. Current Opinion in Structural Biology, 18, 282-289. http://dx.doi.org/10.1016/j.sbi.2008.04.003
Gambus, A., Jones, R.C., Sanchez-Diaz, A., Kanemaki, M., van Deursen, F., Edmondson, R.D. and Labib, K. (2006) GINS Maintains Association of Cdc45 with MCM in Replisome Progression Complexes at Eukaryotic DNA Replication Forks. Nature Cell Biology, 8, 358-366.
Groth, A., Corpet, A., Cook, A.J., Roche, D., Bartek, J., Lukas, J. and Almouzni, G. (2007) Regulation of Replication Fork Progression through Histone Supply and Demand. Science, 318, 1928-1931. http://dx.doi.org/10.1126/science.1148992
Tan, B.C., Chien, C.T., Hirose, S. and Lee, S.C. (2006) Functional Cooperation between FACT and MCM Helicase Facilitates Initiation of Chromatin DNA Replication. EMBO Journal, 25, 3975-3985. http://dx.doi.org/10.1038/sj.emboj.7601271
Jasencakova, Z., Scharf, A.N., Ask, K., Corpet, A., Imhof, A., Almouzni, G. and Groth, A. (2010) Replication Stress Interferes with Histone Recycling and Predeposition Marking of New Histones. Molecular Cell, 37, 736-743. http://dx.doi.org/10.1016/j.molcel.2010.01.033
Adkins, M.W., Carson, J.J., English, C.M., Ramey, C.J. and Tyler, J.K. (2007) The Histone Chaperone Anti-Silencing Function 1 Stimulates the Acetylation of Newly Synthesized Histone H3 in S-Phase. Journal of Biological Chemistry, 282, 1334-1340. http://dx.doi.org/10.1074/jbc.M608025200
Rolef Ben-Shahar, T., Castillo, A.G., Osborne, M.J., Borden, K.L., Kornblatt, J. and Verreault, A. (2009) Two Fundamentally Distinct PCNA Interaction Peptides Contribute to Chromatin Assembly Factor 1 Function. Molecular and Cellular Biology, 29, 6353-6365. http://dx.doi.org/10.1128/MCB.01051-09
Mello, J.A., Sillje, H.H., Roche, D.M., Kirschner, D.B., Nigg, E.A. and Almouzni, G. (2002) Human Asf1 and CAF-1 Interact and Synergize in a Repair-Coupled Nucleosome Assembly Pathway. EMBO Reports, 3, 329-334. http://dx.doi.org/10.1093/embo-reports/kvf068
Lee, C.K., Shibata, Y., Rao, B., Strahl, B.D. and Lieb, J.D. (2004) Evidence for Nucleosome Depletion at Active Regulatory Regions Genome-Wide. Nature Genetics, 36, 900-905. http://dx.doi.org/10.1038/ng1400
Selth, L.A., Sigurdsson, S. and Svejstrup, J.Q. (2010) Transcript Elongation by RNA Polymerase II. Annual Review of Biochemistry, 79, 271-293. http://dx.doi.org/10.1146/annurev.biochem.78.062807.091425
Cho, E.J., Kobor, M.S., Kim, M., Greenblatt, J. and Buratowski, S. (2001) Opposing Effects of Ctk1 Kinase and Fcp1 Phosphatase at Ser 2 of the RNA Polymerase II C-Terminal Domain. Genes & Development, 15, 3319-3329. http://dx.doi.org/10.1101/gad.935901
Lee, J.S. and Shilatifard, A. (2007) A Site to Remember: H3K36 Methylation a Mark for Histone Deacetylation. Mutation Research, 618, 130-134. http://dx.doi.org/10.1016/j.mrfmmm.2006.08.014
Xue, Y.M., Kowalska, A.K., Grabowska, K., Przybyt, K., Cichewicz, M.A., Del Rosario, B.C. and Pemberton, L.F. (2013) Histone Chaperones Nap1 and Vps75 Regulate Histone Acetylation during Transcription Elongation. Molecular and Cellular Biology, 33, 1645-1656. http://dx.doi.org/10.1128/MCB.01121-12
Duina, A.A., Rufiange, A., Bracey, J., Hall, J., Nourani, A. and Winston, F. (2007) Evidence That the Localization of the Elongation Factor Spt16 across Transcribed Genes Is Dependent upon Histone H3 Integrity in Saccharomyces cerevisiae. Genetics, 177, 101-112. http://dx.doi.org/10.1534/genetics.106.067140
Aguilera, A. and Garcia-Muse, T. (2012) R Loops: From Transcription Byproducts to Threats to Genome Stability. Molecular Cell, 46, 115-124. http://dx.doi.org/10.1016/j.molcel.2012.04.009
Ahmad, K. and Henikoff, S. (2002) The Histone Variant H3.3 Marks Active Chromatin by Replication-Independent Nucleosome Assembly. Molecular Cell, 9, 1191-1200. http://dx.doi.org/10.1016/S1097-2765(02)00542-7
Schwabish, M.A. and Struhl, K. (2006) Asf1 Mediates Histone Eviction and Deposition during Elongation by RNA Polymerase II. Molecular Cell, 22, 415-422. http://dx.doi.org/10.1016/j.molcel.2006.03.014
Jenuwein, T. and Allis, C.D. (2001) Translating the Histone Code. Science, 293, 1074-1080. http://dx.doi.org/10.1126/science.1063127
Yang, J.H., Choi, J.H., Jang, H., Park, J.Y., Han, J.W., Youn, H.D. and Cho, E.J. (2011) Histone Chaperones Cooperate to Mediate Mef2-Targeted Transcriptional Regulation during Skeletal Myogenesis. Biochemical and Biophysical Research Communications, 407, 541-547. http://dx.doi.org/10.1016/j.bbrc.2011.03.055
Yang, J.H., Song, Y., Seol, J.H., Park, J.Y., Yang, Y.J., Han, J.W., Youn, H.D. and Cho, E.J. (2011) Myogenic Transcriptional Activation of MyoD Mediated by Replication-Independent Histone Deposition. Proceedings of the National Academy of Sciences of the United States of America, 108, 85-90. http://dx.doi.org/10.1073/pnas.1009830108
Black, B.L. and Olson, E.N. (1998) Transcriptional Control of Muscle Development by Myocyte Enhancer Factor-2 (MEF2) Proteins. Annual Review of Cell and Developmental Biology, 14, 167-196. http://dx.doi.org/10.1146/annurev.cellbio.14.1.167
Roberts, C., Sutherland, H.F., Farmer, H., Kimber, W., Halford, S., Carey, A., Brickman, J.M., Wynshaw-Boris, A. and Scambler, P.J. (2002) Targeted Mutagenesis of the Hira Gene Results in Gastrulation Defects and Patterning Abnormalities of Mesoendodermal Derivatives Prior to Early Embryonic Lethality. Molecular and Cellular Biology, 22, 2318-2328. http://dx.doi.org/10.1128/MCB.22.7.2318-2328.2002
Song, T.Y., Yang, J.H., Park, J.Y., Song, Y., Han, J.W., Youn, H.D. and Cho, E.J. (2012) The Role of Histone Chaperones in Osteoblastic Differentiation of C2C12 Myoblasts. Biochemical and Biophysical Research Communications, 423, 726-732. http://dx.doi.org/10.1016/j.bbrc.2012.06.026
Dutta, D., Ray, S., Home, P., Saha, B., Wang, S., Sheibani, N., Tawfik, O., Cheng, N. and Paul, S. (2010) Regulation of Angiogenesis by Histone Chaperone HIRA-Mediated Incorporation of Lysine 56-Acetylated Histone H3.3 at Chromatin Domains of Endothelial Genes. Journal of Biological Chemistry, 285, 41567-41577. http://dx.doi.org/10.1074/jbc.M110.190025
Drane, P., Ouararhni, K., Depaux, A., Shuaib, M. and Hamiche, A. (2010) The Death-Associated Protein DAXX Is a Novel Histone Chaperone Involved in the Replication-Independent Deposition of H3.3. Genes & Development, 24, 1253-1265. http://dx.doi.org/10.1101/gad.566910
Wong, L.H., McGhie, J.D., Sim, M., Anderson, M.A., Ahn, S., Hannan, R.D., George, A.J., Morgan, K.A., Mann, J.R. and Choo, K.H. (2010) ATRX Interacts with H3.3 in Maintaining Telomere Structural Integrity in Pluripotent Embryonic Stem Cells. Genome Research, 20, 351-360. http://dx.doi.org/10.1101/gr.101477.109
Kappes, F., Waldmann, T., Mathew, V., Yu, J., Zhang, L., Khodadoust, M.S., Chinnaiyan, A.M., Luger, K., Erhardt, S., Schneider, R. and Markovitz, D.M. (2011) The DEK Oncoprotein Is a Su(var) that Is Essential to Heterochromatin Integrity. Genes & Development, 25, 673-678. http://dx.doi.org/10.1101/gad.2036411
Corpet, A., De Koning, L., Toedling, J., Savignoni, A., Berger, F., Lemaitre, C., O’Sullivan, R.J., Karlseder, J., Barillot, E., Asselain, B., Sastre-Garau, X. and Almouzni, G. (2011) Asf1b, the Necessary Asf1 Isoform for Proliferation, Is Predictive of Outcome in Breast Cancer. EMBO Journal, 30, 480-493. http://dx.doi.org/10.1038/emboj.2010.335
Staibano, S., Mascolo, M., Mancini, F.P., Kisslinger, A., Salvatore, G., Di Benedetto, M., Chieffi, P., Altieri, V., Prezioso, D., Ilardi, G., De Rosa, G. and Tramontano, D. (2009) Overexpression of Chromatin Assembly Factor-1 (CAF-1) p60 Is Predictive of Adverse Behaviour of Prostatic Cancer. Histopathology, 54, 580-589. http://dx.doi.org/10.1111/j.1365-2559.2009.03266.x
Polo, S.E., Theocharis, S.E., Grandin, L., Gambotti, L., Antoni, G., Savignoni, A., Asselain, B., Patsouris, E. and Almouzni, G. (2010) Clinical Significance and Prognostic Value of Chromatin Assembly Factor-1 Overexpression in Human Solid Tumours. Histopathology, 57, 716-724. http://dx.doi.org/10.1111/j.1365-2559.2010.03681.x
Alekseev, O.M., Richardson, R.T., Tsuruta, J.K. and O’Rand, M.G. (2011) Depletion of the Histone Chaperone tNASP Inhibits Proliferation and Induces Apoptosis in Prostate Cancer PC-3 Cells. Reproductive Biology and Endocrinology, 9, 50. http://dx.doi.org/10.1186/1477-7827-9-50
Gasparian, A.V., Burkhart, C.A., Purmal, A.A., Brodsky, L., Pal, M., Saranadasa, M., Bosykh, D.A., Commane, M., Guryanova, O.A., Pal, S., Safina, A., Sviridov, S., Koman, I.E., Veith, J., Komar, A.A., Gudkov, A.V. and Gurova, K.V. (2011) Curaxins: Anticancer Compounds that Simultaneously Suppress NF-κB and Activate p53 by Targeting FACT. Science Translational Medicine, 3, 95ra74. http://dx.doi.org/10.1126/scitranslmed.3002530
Koman, I.E., Commane, M., Paszkiewicz, G., Hoonjan, B., Pal, S., Safina, A., Toshkov, I., Purmal, A.A., Wang, D., Liu, S., Morrison, C., Gudkov, A.V. and Gurova, K.V. (2012) Targeting FACT Complex Suppresses Mammary Tumorigenesis in Her2/neu Transgenic Mice. Cancer Prevention Research, 5, 1025-1035. http://dx.doi.org/10.1158/1940-6207.CAPR-11-0529
Garcia, H., Miecznikowski, J.C., Safina, A., Commane, M., Ruusulehto, A., Kilpinen, S., Leach, R.W., Attwood, K., Li, Y., Degan, S., Omilian, A.R., Guryanova, O., Papantonopoulou, O., Wang, J., Buck, M., Liu, S., Morrison, C. and Gurova, K.V. (2013) Facilitates Chromatin Transcription Complex Is an “Accelerator” of Tumor Transformation and Potential Marker and Target of Aggressive Cancers. Cell Reports, 4, 159-173. http://dx.doi.org/10.1016/j.celrep.2013.06.013
Kurki, S., Peltonen, K., Latonen, L., Kiviharju, T.M., Ojala, P.M., Meek, D. and Laiho, M. (2004) Nucleolar Protein NPM Interacts with HDM2 and Protects Tumor Suppressor Protein p53 from HDM2-Mediated Degradation. Cancer Cell, 5, 465-475. http://dx.doi.org/10.1016/S1535-6108(04)00110-2
Grisendi, S., Mecucci, C., Falini, B. and Pandolfi, P.P. (2006) Nucleophosmin and Cancer. Nature Reviews Cancer, 6, 493-505. http://dx.doi.org/10.1038/nrc1885
Haferlach, C., Mecucci, C., Schnittger, S., Kohlmann, A., Mancini, M., Cuneo, A., Testoni, N., Rege-Cambrin, G., Santucci, A., Vignetti, M., Fazi, P., Martelli, M.P., Haferlach, T. and Falini, B. (2009) AML with Mutated NPM1 Carrying a Normal or Aberrant Karyotype Show Overlapping Biologic, Pathologic, Immunophenotypic, and Prognostic Features. Blood, 114, 3024-3032. http://dx.doi.org/10.1182/blood-2009-01-197871
Yang, Y.F., Zhang, X.Y., Yang, M., He, Z.H., Peng, N.F., Xie, S.R. and Xie, Y.F. (2014) Prognostic Role of Nucleophosmin in Colorectal Carcinomas. Asian Pacific Journal of Cancer Prevention, 15, 2021-2026.
Wise-Draper, T.M., Morreale, R.J., Morris, T.A., Mintz-Cole, R.A., Hoskins, E.E., Balsitis, S.J., Husseinzadeh, N., Witte, D.P., Wikenheiser-Brokamp, K.A., Lambert, P.F. and Wells, S.I. (2009) DEK Proto-Oncogene Expression Interferes with the Normal Epithelial Differentiation Program. American Journal of Pathology, 174, 71-81. http://dx.doi.org/10.2353/ajpath.2009.080330
Wise-Draper, T.M., Mintz-Cole, R.A., Morris, T.A., Simpson, D.S., Wikenheiser-Brokamp, K.A., Currier, M.A., Cripe, T.P., Grosveld, G.C. and Wells, S.I. (2009) Overexpression of the Cellular DEK Protein Promotes Epithelial Transformation in Vitro and in Vivo. Cancer Research, 69, 1792-1799. http://dx.doi.org/10.1158/0008-5472.CAN-08-2304
Soekarman, D., von Lindern, M., Daenen, S., de Jong, B., Fonatsch, C., Heinze, B., Bartram, C., Hagemeijer, A. and Grosveld, G. (1992) The Translocation (6;9) (p23;q34) Shows Consistent Rearrangement of Two Genes and Defines a Myeloproliferative Disorder with Specific Clinical Features. Blood, 79, 2990-2997.
Riveiro-Falkenbach, E. and Soengas, M.S. (2010) Control of Tumorigenesis and Chemoresistance by the DEK Oncogene. Clinical Cancer Research, 16, 2932-2938. http://dx.doi.org/10.1158/1078-0432.CCR-09-2330
Jiao, Y., Shi, C., Edil, B.H., de Wilde, R.F., Klimstra, D.S., Maitra, A., Schulick, R.D., Tang, L.H., Wolfgang, C.L., Choti, M.A., Velculescu, V.E., Diaz Jr., L.A., Vogelstein, B., Kinzler, K.W., Hruban, R.H. and Papadopoulos, N. (2011) DAXX/ATRX, MEN1, and mTOR Pathway Genes Are Frequently Altered in Pancreatic Neuroendocrine Tumors. Science, 331, 1199-1203. http://dx.doi.org/10.1126/science.1200609
Schwartzentruber, J., Korshunov, A., Liu, X.Y., Jones, D.T., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A.M., Quang, D.A., Tonjes, M., Hovestadt, V., Albrecht, S., Kool, M., Nantel, A., Konermann, C., Lindroth, A., Jager, N., Rausch, T., Ryzhova, M., Korbel, J.O., Hielscher, T., Hauser, P., Garami, M., Klekner, A., Bognar, L., Ebinger, M., Schuhmann, M.U., Scheurlen, W., Pekrun, A., Fruhwald, M.C., Roggendorf, W., Kramm, C., Durken, M., Atkinson, J., Lepage, P., Montpetit, A., Zakrzewska, M., Zakrzewski, K., Liberski, P.P., Dong, Z., Siegel, P., Kulozik, A.E., Zapatka, M., Guha, A., Malkin, D., Felsberg, J., Reifenberger, G., von Deimling, A., Ichimura, K., Collins, V.P., Witt, H., Milde, T., Witt, O., Zhang, C., Castelo-Branco, P., Lichter, P., Faury, D., Tabori, U., Plass, C., Majewski, J., Pfister, S.M. and Jabado, N. (2012) Driver Mutations in Histone H3.3 and Chromatin Remodelling Genes in Paediatric Glioblastoma. Nature, 482, 226-231. http://dx.doi.org/10.1038/nature10833
Lorain, S., Demczuk, S., Lamour, V., Toth, S., Aurias, A., Roe, B.A. and Lipinski, M. (1996) Structural Organization of the WD Repeat Protein-Encoding Gene HIRA in the DiGeorge Syndrome Critical Region of Human Chromosome 22. Genome Research, 6, 43-50. http://dx.doi.org/10.1101/gr.6.1.43
Farrell, M.J., Stadt, H., Wallis, K.T., Scambler, P., Hixon, R.L., Wolfe, R., Leatherbury, L. and Kirby, M.L. (1999) HIRA, a DiGeorge Syndrome Candidate Gene, Is Required for Cardiac Outflow Tract Septation. Circulation Research, 84, 127-135. http://dx.doi.org/10.1161/01.RES.84.2.127