Human cytomegalovirus (HCMV) gene expression during infection is characterized as a sequential process including immediate-early (IE), early (E), and late (L)-stage gene expression. The most abundantly expressed gene at the IE stage of infection is the major IE (MIE) gene that produces IE1 and IE2. IE1 has been the focus of study because it is an important protein, not only for viral gene expression but also for viral replication. It is believed that IE1 plays important roles in viral gene regulation by interacting with cellular proteins. In the current study, we performed protein array assays and identified 83 cellular proteins that interact with IE1. Among them, seven are RNA-binding proteins that are important in RNA processing; more than half are nuclear proteins that are involved in gene regulations. Tumorigenesis-related proteins are also found to interact with IE1, implying that the role of IE1 in tumorigenesis might need to be reevaluated. Unexpectedly, cytoplasmic proteins, such as Golgi autoantigen and GGA1 (both related to the Golgi trafficking protein), are also found to be associated with IE1. We also employed a coimmunoprecipitation assay to test the interactions of IE1 and some of the proteins identified in the protein array assays and confirmed that the results from the protein array assays are reliable. Many of the proteins identified by the protein array assay have not been previously reported. Therefore, the functions of the IE1-protein interactions need to be further explored in the future.
References
[1]
Sweet, C. The pathogenicity of cytomegalovirus. FEMS Microbiol. Rev. 1999, 23, 457–482, doi:10.1111/j.1574-6976.1999.tb00408.x.
[2]
Landolfo, S.; Gariglio, M.; Gribaudo, G.; Lembo, D. The human cytomegalovirus. Pharmacol. Ther. 2003, 98, 269–297, doi:10.1016/S0163-7258(03)00034-2.
[3]
Mocarski, E.S., Jr.; Shenk, T.; Pass, R.F. Cytomegaloviruses, 5th ed. ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2006.
[4]
Tang, Q.; Li, L.; Maul, G.G. Mouse cytomegalovirus early M112/113 proteins control the repressive effect of IE3 on the major immediate-early promoter. J. Virol. 2005, 79, 257–263, doi:10.1128/JVI.79.1.257-263.2005.
[5]
Tang, Q.; Maul, G. Immediate early interactions and epigenetic defense mechanisms. In In Cytomegaloviruses: Molecular Biology and Immunology; Reddehase, M.J., Ed.; Hethersett, Horizon Scientific Press: Norwich, UK, 2005.
[6]
Hagemeier, C.; Walker, S.M.; Sissons, P.J.; Sinclair, J.H. The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently trans-activate the c-Fos, c-Myc and hsp70 promoters via basal promoter elements. J. Gen. Virol. 1992, 73, 2385–2393, doi:10.1099/0022-1317-73-9-2385.
[7]
Liu, B.; Hermiston, T.W.; Stinski, M.F. A cis-acting element in the major immediate-early (IE) promoter of human cytomegalovirus is required for negative regulation by IE2. J. Virol. 1991, 65, 897–903.
[8]
Scully, A.L.; Sommer, M.H.; Schwartz, R.; Spector, D.H. The human cytomegalovirus IE2 86-kilodalton protein interacts with an early gene promoter via site-specific DNA binding and protein-protein associations. J. Virol. 1995, 69, 6533–6540.
[9]
Awasthi, S.; Isler, J.A.; Alwine, J.C. Analysis of splice variants of the immediate-early 1 region of human cytomegalovirus. J. Virol. 2004, 78, 8191–8200, doi:10.1128/JVI.78.15.8191-8200.2004.
[10]
Sadanari, H.; Yamada, R.; Yamagoshi, T.; Ohnishi, K.; Matsubara, K.; Fukuda, S.; Tanaka, J. The major immediate-early genes of human cytomegalovirus induce two novel proteins with molecular weights of 91 and 102 kilodaltons. Arch. Virol. 2000, 145, 1257–1266, doi:10.1007/s007050070125.
[11]
Ahn, J.H.; Hayward, G.S. The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells. J. Virol. 1997, 71, 4599–4613.
[12]
Meier, J.L.; Stinski, M.F. Effect of a modulator deletion on transcription of the human cytomegalovirus major immediate-early genes in infected undifferentiated and differentiated cells. J. Virol. 1997, 71, 1246–1255.
[13]
Stenberg, R.M. The human cytomegalovirus major immediate-early gene. Intervirology 1996, 39, 343–349.
[14]
Stenberg, R.M.; Thomsen, D.R.; Stinski, M.F. Structural analysis of the major immediate early gene of human cytomegalovirus. J. Virol. 1984, 49, 190–199.
[15]
Tang, Q.; Maul, G.G. Mouse cytomegalovirus immediate-early protein 1 binds with host cell repressors to relieve suppressive effects on viral transcription and replication during lytic infection. J. Virol. 2003, 77, 1357–1367, doi:10.1128/JVI.77.2.1357-1367.2003.
[16]
Lee, H.R.; Kim, D.J.; Lee, J.M.; Choi, C.Y.; Ahn, B.Y.; Hayward, G.S.; Ahn, J.H. Ability of the human cytomegalovirus IE1 protein to modulate sumoylation of PML correlates with its functional activities in transcriptional regulation and infectivity in cultured fibroblast cells. J. Virol. 2004, 78, 6527–6542.
[17]
Nevels, M.; Paulus, C.; Shenk, T. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. USA 2004, 101, 17234–17239, doi:10.1073/pnas.0407933101.
[18]
Ahn, J.H.; Hayward, G.S. Disruption of PML-associated nuclear bodies by IE1 correlates with efficient early stages of viral gene expression and DNA replication in human cytomegalovirus infection. Virology 2000, 274, 39–55, doi:10.1006/viro.2000.0448.
[19]
Ishov, A.M.; Stenberg, R.M.; Maul, G.G. Human cytomegalovirus immediate early interaction with host nuclear structures: Definition of an immediate transcript environment. J. Cell Biol. 1997, 138, 5–16, doi:10.1083/jcb.138.1.5.
[20]
Lee, H.R.; Huh, Y.H.; Kim, Y.E.; Lee, K.; Kim, S.; Ahn, J.H. N-Terminal determinants of human cytomegalovirus IE1 protein in nuclear targeting and disrupting PML-associated subnuclear structures. Biochem. Biophys. Res. Commun. 2007, 356, 499–504, doi:10.1016/j.bbrc.2007.03.007.
[21]
Maul, G.G.; Negorev, D.; Bell, P.; Ishov, A.M. Review: Properties and assembly mechanisms of ND10, PML bodies, or PODs. J. Struct. Biol. 2000, 129, 278–287, doi:10.1006/jsbi.2000.4239.
[22]
Paulus, C.; Krauss, S.; Nevels, M. A human cytomegalovirus antagonist of type I IFN-dependent signal transducer and activator of transcription signaling. Proc. Natl. Acad. Sci. USA 2006, 103, 3840–3845, doi:10.1073/pnas.0600007103.
[23]
Huh, Y.H.; Kim, Y.E.; Kim, E.T.; Park, J.J.; Song, M.J.; Zhu, H.; Hayward, G.S.; Ahn, J.H. Binding STAT2 by the acidic domain of human cytomegalovirus IE1 promotes viral growth and is negatively regulated by SUMO. J. Virol. 2008, 82, 10444–10454, doi:10.1128/JVI.00833-08.
[24]
Krauss, S.; Kaps, J.; Czech, N.; Paulus, C.; Nevels, M. Physical requirements and functional consequences of complex formation between the cytomegalovirus IE1 protein and human STAT2. J. Virol. 2009, 83, 12854–12870, doi:10.1128/JVI.01164-09.
[25]
Knoblach, T.; Grandel, B.; Seiler, J.; Nevels, M.; Paulus, C. Human cytomegalovirus IE1 protein elicits a type II interferon-like host cell response that depends on activated STAT1 but not interferon-gamma. PLoS Pathog. 2011, 7, e1002016, doi:10.1371/journal.ppat.1002016.
[26]
Zhang, Z.; Huong, S.M.; Wang, X.; Huang, D.Y.; Huang, E.S. Interactions between human cytomegalovirus IE1-72 and cellular p107: Functional domains and mechanisms of up-regulation of cyclin E/cdk2 kinase activity. J. Virol. 2003, 77, 12660–12670, doi:10.1128/JVI.77.23.12660-12670.2003.
[27]
Castillo, J.P.; Frame, F.M.; Rogoff, H.A.; Pickering, M.T.; Yurochko, A.D.; Kowalik, T.F. Human cytomegalovirus IE1-72 activates ataxia telangiectasia mutated kinase and a p53/p21-mediated growth arrest response. J. Virol. 2005, 79, 11467–11475, doi:10.1128/JVI.79.17.11467-11475.2005.
[28]
Hu, S.; Xie, Z.; Onishi, A.; Yu, X.; Jiang, L.; Lin, J.; Rho, H.S.; Woodard, C.; Wang, H.; Jeong, J.S.; et al. Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling. Cell 2009, 139, 610–622, doi:10.1016/j.cell.2009.08.037.
[29]
Tang, Q.; Maul, G.G. Mouse cytomegalovirus crosses the species barrier with help from a few human cytomegalovirus proteins. J. Virol. 2006, 80, 7510–7521, doi:10.1128/JVI.00684-06.
[30]
Reeves, M.; Woodhall, D.; Compton, T.; Sinclair, J. Human cytomegalovirus IE72 protein interacts with the transcriptional repressor hDaxx to regulate LUNA gene expression during lytic infection. J. Virol. 2010, 84, 7185–7194, doi:10.1128/JVI.02231-09.
[31]
Gaspar, M.; Shenk, T. Human cytomegalovirus inhibits a DNA damage response by mislocalizing checkpoint proteins. Proc. Natl. Acad. Sci. USA 2006, 103, 2821–2826, doi:10.1073/pnas.0511148103.
[32]
Xuan, B.; Qian, Z.; Torigoi, E.; Yu, D. Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J. Virol. 2009, 83, 3463–3474, doi:10.1128/JVI.02307-08.
[33]
Andoniou, C.E.; Andrews, D.M.; Manzur, M.; Ricciardi-Castagnoli, P.; Degli-Esposti, M.A. A novelcheckpoint in the Bcl-2-regulated apoptotic pathway revealed by murine cytomegalovirus infection of dendritic cells. J. Cell Biol. 2004, 166, 827–837, doi:10.1083/jcb.200403010.
[34]
Tower, C.; Fu, L.; Gill, R.; Prichard, M.; Lesort, M.; Sztul, E. Human cytomegalovirus UL97 kinase prevents the deposition of mutant protein aggregates in cellular models of Huntington’s disease and ataxia. Neurobiol. Dis. 2011, 41, 11–22, doi:10.1016/j.nbd.2010.08.013.
[35]
Mak, G.W.; Lai, W.L.; Zhou, Y.; Li, M.; Ng, I.O.; Ching, Y.P. CDK5RAP3 is a novel repressor of p14ARF in hepatocellular carcinoma cells. PLoS One 2012, 7, e42210.
[36]
Tsukahara, F.; Hattori, M.; Muraki, T.; Sakaki, Y. Identification and cloning of a novel cDNA belonging to tetratricopeptide repeat gene family from Down syndrome-critical region 21q22.2. J. Biochem. 1996, 120, 820–827, doi:10.1093/oxfordjournals.jbchem.a021485.
[37]
Munro, S. The golgin coiled-coil proteins of the Golgi apparatus. Cold Spring Harb. Perspect. Biol. 2011, 3, doi:10.1101/cshperspect.a005256.
[38]
Hennig, L.; Derkacheva, M. Diversity of Polycomb group complexes in plants: Same rules, different players? Trends Genet. 2009, 25, 414–423, doi:10.1016/j.tig.2009.07.002.
[39]
Sutherland, L.C.; Rintala-Maki, N.D.; White, R.D.; Morin, C.D. RNA binding motif (RBM) proteins: A novel family of apoptosis modulators? J. Cell Biochem. 2005, 94, 5–24, doi:10.1002/jcb.20204.
[40]
Seldin, L.; Poulson, N.D.; Foote, H.P.; Lechler, T. NuMA localization, stability and function in spindle orientation involves 4.1 and Cdk1 interactions. Mol. Biol. Cell 2013, 24, 3651–3662, doi:10.1091/mbc.E13-05-0277.
[41]
Kuo, P.C.; Tsao, Y.P.; Chang, H.W.; Chen, P.H.; Huang, C.W.; Lin, S.T.; Weng, Y.T.; Tsai, T.C.; Shieh, S.Y.; Chen, S.L. Breast cancer amplified sequence 2, a novel negative regulator of the p53 tumor suppressor. Cancer Res. 2009, 69, 8877–8885, doi:10.1158/0008-5472.CAN-09-2023.
[42]
Huang, Y.C.; Schmitt, M.; Yang, Z.; Que, L.G.; Stewart, J.C.; Frampton, M.W.; Devlin, R.B. Gene expression profile in circulating mononuclear cells after exposure to ultrafine carbon particles. Inhal. Toxicol. 2010, 22, 835–846, doi:10.3109/08958378.2010.486419.
[43]
Tategu, M.; Nakagawa, H.; Hayashi, R.; Yoshida, K. Transcriptional co-factor CDCA4 participates in the regulation of JUN oncogene expression. Biochimie 2008, 90, 1515–1522, doi:10.1016/j.biochi.2008.05.014.
[44]
Shen, T.; Huang, S. The role of Cdc25A in the regulation of cell proliferation and apoptosis. Anticancer Agents Med. Chem. 2012, 12, 631–639, doi:10.2174/187152012800617678.
[45]
Trub, T.; Frantz, J.D.; Miyazaki, M.; Band, H.; Shoelson, S.E. The role of a lymphoid-restricted, Grb2-like SH3-SH2-SH3 protein in T cell receptor signaling. J. Biol. Chem. 1997, 272, 894–902, doi:10.1074/jbc.272.2.894.
[46]
Matsuki, H.; Takahashi, M.; Higuchi, M.; Makokha, G.N.; Oie, M.; Fujii, M. Both G3BP1 and G3BP2 contribute to stress granule formation. Genes Cells 2013, 18, 135–146, doi:10.1111/gtc.12023.
[47]
Salomoni, P.; Khelifi, A.F. DAXX: Death or survival protein? Trends Cell Biol. 2006, 16, 97–104, doi:10.1016/j.tcb.2005.12.002.
[48]
Kamimura, J.; Wakui, K.; Kadowaki, H.; Watanabe, Y.; Miyake, K.; Harada, N.; Sakamoto, M.; Kinoshita, A.; Yoshiura, K.; Ohta, T.; et al. The IHPK1 gene is disrupted at the 3p21.31 breakpoint of t(3;9) in a family with type 2 diabetes mellitus. J. Hum. Genet. 2004, 49, 360–365.
[49]
Song, C.; Zhu, S.; Wu, C.; Kang, J. Histone Deacetylase (HDAC) 10 suppresses cervical cancer metastasis through inhibition of matrix metalloproteinase (MMP) 2 and 9 Expression. J. Biol. Chem. 2013, 288, 28021–28033, doi:10.1074/jbc.M113.498758.
[50]
Al-Kandari, W.; Jambunathan, S.; Navalgund, V.; Koneni, R.; Freer, M.; Parimi, N.; Mudhasani, R.; Fontes, J.D. ZXDC, a novel zinc finger protein that binds CIITA and activates MHC gene transcription. Mol. Immunol. 2007, 44, 311–321, doi:10.1016/j.molimm.2006.02.029.
[51]
Machesky, L.M.; Johnston, S.A. MIM: A multifunctional scaffold protein. J. Mol. Med. 2007, 85, 569–576, doi:10.1007/s00109-007-0207-0.
[52]
Else, T.; Trovato, A.; Kim, A.C.; Wu, Y.; Ferguson, D.O.; Kuick, R.D.; Lucas, P.C.; Hammer, G.D. Genetic p53 deficiency partially rescues the adrenocortical dysplasia phenotype at the expense of increased tumorigenesis. Cancer Cell 2009, 15, 465–476, doi:10.1016/j.ccr.2009.04.011.
[53]
Boman, A.L.; Zhang, C.; Zhu, X.; Kahn, R.A. A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol. Biol. Cell 2000, 11, 1241–1255, doi:10.1091/mbc.11.4.1241.
[54]
Nakamura, T.; Jenkins, N.A.; Copeland, N.G. Identification of a new family of Pbx-related homeobox genes. Oncogene 1996, 13, 2235–2242.
[55]
Wong, M.H.; Hermiston, M.L.; Syder, A.J.; Gordon, J.I. Forced expression of the tumor suppressor adenomatosis polyposis coli protein induces disordered cell migration in the intestinal epithelium. Proc. Natl. Acad. Sci. USA 1996, 93, 9588–9593, doi:10.1073/pnas.93.18.9588.
[56]
Katoh, M. Identification and characterization of mouse Ppfia1 gene in silico. Int. J. Mol. Med. 2003, 12, 263–267.
[57]
Narkis, G.; Ofir, R.; Landau, D.; Manor, E.; Volokita, M.; Hershkowitz, R.; Elbedour, K.; Birk, O.S. Lethal contractural syndrome type 3 (LCCS3) is caused by a mutation in PIP5K1C, which encodes PIPKI gamma of the phophatidylinsitol pathway. Am. J. Hum. Genet. 2007, 81, 530–539, doi:10.1086/520771.
[58]
Miki, T.; Takano, K.; Yoneda, Y. The role of mammalian Staufen on mRNA traffic: A view from its nucleocytoplasmic shuttling function. Cell Struct. Funct. 2005, 30, 51–56, doi:10.1247/csf.30.51.
[59]
Geetha, T.; Vishwaprakash, N.; Sycheva, M.; Babu, J.R. Sequestosome 1/p62: Across diseases. Biomarkers 2012, 17, 99–103, doi:10.3109/1354750X.2011.653986.
[60]
Rigden, D.J.; Liu, H.; Hayes, S.D.; Urbe, S.; Clague, M.J. Ab initio protein modelling reveals novel human MIT domains. FEBS Lett. 2009, 583, 872–878, doi:10.1016/j.febslet.2009.02.012.
[61]
Huang, K.; Nair, A.K.; Muller, Y.L.; Piaggi, P.; Bian, L.; del Rosario, M.; Knowler, W.C.; Kobes, S.; Hanson, R.L.; Bogardus, C.; et al. Whole exome sequencing identifies variation in CYB5A and RNF10 associated with adiposity and type 2 diabetes. Obesity 2013, doi:10.1002/oby.20647.
[62]
Kuang, Z.; Yao, S.; Xu, Y.; Lewis, R.S.; Low, A.; Masters, S.L.; Willson, T.A.; Kolesnik, T.B.; Nicholson, S.E.; Garrett, T.J.; et al. SPRY domain-containing SOCS box protein 2: Crystal structure and residues critical for protein binding. J. Mol. Biol. 2009, 386, 662–674, doi:10.1016/j.jmb.2008.12.078.
[63]
Svotelis, A.; Bianco, S.; Madore, J.; Huppe, G.; Nordell-Markovits, A.; Mes-Masson, A.M.; Gevry, N. H3K27 demethylation by JMJD3 at a poised enhancer of anti-apoptotic gene BCL2 determines ERalpha ligand dependency. EMBO J. 2011, 30, 3947–3961, doi:10.1038/emboj.2011.284.
[64]
Privalsky, M.L. Regulation of SMRT and N-CoR corepressor function. Curr. Top. Microbiol. Immunol. 2001, 254, 117–136.
[65]
Marangos, P.J.; Schmechel, D. The neurobiology of the brain enolases. Essays Neurochem. Neuropharmacol. 1980, 4, 211–247.
[66]
Topfer-Petersen, E.; Cechova, D.; Henschen, A.; Steinberger, M.; Friess, A.E.; Zucker, A. Cell biology of acrosomal proteins. Andrologia 1990, 22, 110–121.
[67]
Kramer, B.F.; Schoor, O.; Kruger, T.; Reichle, C.; Muller, M.; Weinschenk, T.; Hennenlotter, J.; Stenzl, A.; Rammensee, H.G.; Stevanovic, S. MAGED4-expression in renal cell carcinoma and identification of an HLA-A*25-restricted MHC class I ligand from solid tumor tissue. Cancer Biol. Ther. 2005, 4, 943–948, doi:10.4161/cbt.4.9.1907.
[68]
Kuwahara, K.; Takano, M.; Nakao, K. Pathophysiological significance of T-type Ca2+ channels: Transcriptional regulation of T-type Ca2+ channel—Regulation of CACNA1H by neuron-restrictive silencer factor. J. Pharmacol. Sci. 2005, 99, 211–213, doi:10.1254/jphs.FMJ05002X4.
[69]
Shahbazian, D.; Parsyan, A.; Petroulakis, E.; Hershey, J.; Sonenberg, N. eIF4B controls survival and proliferation and is regulated by proto-oncogenic signaling pathways. Cell Cycle 2010, 9, 4106–4109, doi:10.4161/cc.9.20.13630.
[70]
Bonini, N.M.; Gitler, A.D. Model organisms reveal insight into human neurodegenerative disease:Ataxin-2 intermediate-length polyglutamine expansions are a risk factor for ALS. J. Mol. Neurosci. 2011, 45, 676–683, doi:10.1007/s12031-011-9548-9.
[71]
Rutkowski, D.T.; Kaufman, R.J. All roads lead to ATF4. Dev. Cell 2003, 4, 442–444, doi:10.1016/S1534-5807(03)00100-X.
[72]
Bernier, F.; Soucy, P.; Luu-The, V. Human phenol sulfotransferase gene contains two alternative promoters: Structure and expression of the gene. DNA Cell Biol. 1996, 15, 367–375, doi:10.1089/dna.1996.15.367.
[73]
Bosley, T.M.; Salih, M.A.; Jen, J.C.; Lin, D.D.; Oystreck, D.; Abu-Amero, K.K.; MacDonald, D.B.; al Zayed, Z.; al Dhalaan, H.; Kansu, T.; et al. Neurologic features of horizontal gaze palsy and progressive scoliosis with mutations in ROBO3. Neurology 2005, 64, 1196–1203.
[74]
Du, P.; Ye, L.; Li, H.; Yang, Y.; Jiang, W.G. The tumour suppressive role of metastasis suppressor-1, MTSS1, in human kidney cancer, a possible connection with the SHH pathway. J. Exp. Ther. Oncol. 2012, 10, 91–99.
[75]
Lu, P.; Hankel, I.L.; Hostager, B.S.; Swartzendruber, J.A.; Friedman, A.D.; Brenton, J.L.; Rothman, P.B.; Colgan, J.D. The developmental regulator protein Gon4l associates with protein YY1, co-repressor Sin3a, and histone deacetylase 1 and mediates transcriptional repression. J. Biol. Chem. 2011, 286, 18311–18319, doi:10.1074/jbc.M110.133603.
[76]
McPherson, J.P.; Sarras, H.; Lemmers, B.; Tamblyn, L.; Migon, E.; Matysiak-Zablocki, E.; Hakem, A.; Azami, S.A.; Cardoso, R.; Fish, J.; et al. Essential role for Bclaf1 in lung development and immune system function. Cell Death Differ. 2009, 16, 331–339, doi:10.1038/cdd.2008.167.
[77]
Yi, F.; Pereira, L.; Merrill, B.J. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 2008, 26, 1951–1960, doi:10.1634/stemcells.2008-0229.
[78]
Fong, N.M.; Jensen, T.C.; Shah, A.S.; Parekh, N.N.; Saltiel, A.R.; Brady, M.J. Identification of binding sites on protein targeting to glycogen for enzymes of glycogen metabolism. J. Biol. Chem. 2000, 275, 35034–35039.
[79]
Ross, S.E.; McCord, A.E.; Jung, C.; Atan, D.; Mok, S.I.; Hemberg, M.; Kim, T.K.; Salogiannis, J.; Hu, L.; Cohen, S.; et al. Bhlhb5 and Prdm8 form a repressor complex involved in neuronal circuit assembly. Neuron 2012, 73, 292–303, doi:10.1016/j.neuron.2011.09.035.
[80]
Honore, B.; Rasmussen, H.H.; Vorum, H.; Dejgaard, K.; Liu, X.; Gromov, P.; Madsen, P.; Gesser, B.; Tommerup, N.; Celis, J.E. Heterogeneous nuclear ribonucleoproteins H, H’, and F are members of a ubiquitously expressed subfamily of related but distinct proteins encoded by genes mapping to different chromosomes. J. Biol. Chem. 1995, 270, 28780–28789, doi:10.1074/jbc.270.48.28780.
[81]
Keegan, K.; Johnson, D.E.; Williams, L.T.; Hayman, M.J. Isolation of an additional member of the fibroblast growth factor receptor family, FGFR-3. Proc. Natl. Acad. Sci. USA 1991, 88, 1095–1099, doi:10.1073/pnas.88.4.1095.
[82]
Jaiswal, B.S.; Kljavin, N.M.; Stawiski, E.W.; Chan, E.; Parikh, C.; Durinck, S.; Chaudhuri, S.; Pujara, K.; Guillory, J.; Edgar, K.A.; et al. Oncogenic ERBB3 mutations in human cancers. Cancer Cell 2013, 23, 603–617, doi:10.1016/j.ccr.2013.04.012.
[83]
Mishima, Y.; Miyagi, S.; Saraya, A.; Negishi, M.; Endoh, M.; Endo, T.A.; Toyoda, T.; Shinga, J.; Katsumoto, T.; Chiba, T.; et al. The Hbo1-Brd1/Brpf2 complex is responsible for global acetylation of H3K14 and required for fetal liver erythropoiesis. Blood 2011, 118, 2443–2453, doi:10.1182/blood-2011-01-331892.
[84]
Hatakeyama, S. TRIM proteins and cancer. Nat. Rev. Cancer 2011, 11, 792–804, doi:10.1038/nrc3139.
[85]
Wiemann, S.; Weil, B.; Wellenreuther, R.; Gassenhuber, J.; Glassl, S.; Ansorge, W.; Bocher, M.; Blocker, H.; Bauersachs, S.; Blum, H.; et al. Toward a catalog of human genes and proteins: Sequencing and analysis of 500 novel complete protein coding human cDNAs. Genome Res. 2001, 11, 422–435, doi:10.1101/gr.GR1547R.
[86]
Maciejewski, J.P.; Padgett, R.A. Defects in spliceosomal machinery: A new pathway of leukaemogenesis. Br. J. Haematol. 2012, 158, 165–173, doi:10.1111/j.1365-2141.2012.09158.x.
[87]
Sauve, F.; McBroom, L.D.; Gallant, J.; Moraitis, A.N.; Labrie, F.; Giguere, V. CIA, a novel estrogen receptor coactivator with a bifunctional nuclear receptor interacting determinant. Mol. Cell Biol. 2001, 21, 343–353, doi:10.1128/MCB.21.1.343-353.2001.
[88]
Lo, S.H.; Weisberg, E.; Chen, L.B. Tensin: A potential link between the cytoskeleton and signal transduction. Bioessays 1994, 16, 817–823, doi:10.1002/bies.950161108.
[89]
Roubin, R.; Acquaviva, C.; Chevrier, V.; Sedjai, F.; Zyss, D.; Birnbaum, D.; Rosnet, O. Myomegalin is necessary for the formation of centrosomal and Golgi-derived microtubules. Biol. Open 2013, 2, 238–250, doi:10.1242/bio.20123392.
[90]
Ishov, A.M.; Vladimirova, O.V.; Maul, G.G. Daxx-mediated accumulation of human cytomegalovirus tegument protein pp71 at ND10 facilitates initiation of viral infection at these nuclear domains. J. Virol. 2002, 76, 7705–7712, doi:10.1128/JVI.76.15.7705-7712.2002.
[91]
Morin, R.D.; Mendez-Lago, M.; Mungall, A.J.; Goya, R.; Mungall, K.L.; Corbett, R.D.; Johnson, N.A.; Severson, T.M.; Chiu, R.; Field, M.; et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 2011, 476, 298–303, doi:10.1038/nature10351.
[92]
Seimiya, H.; Smith, S. The telomeric poly(ADP-ribose) polymerase, tankyrase 1, contains multiple binding sites for telomeric repeat binding factor 1 (TRF1) and a novel acceptor, 182-kDa tankyrase-binding protein (TAB182). J. Biol. Chem. 2002, 277, 14116–14126, doi:10.1074/jbc.M112266200.
[93]
Kuuselo, R.; Savinainen, K.; Azorsa, D.O.; Basu, G.D.; Karhu, R.; Tuzmen, S.; Mousses, S.; Kallioniemi, A. Intersex-like (IXL) is a cell survival regulator in pancreatic cancer with 19q13 amplification. Cancer Res. 2007, 67, 1943–1949, doi:10.1158/0008-5472.CAN-06-3387.
[94]
Geiman, D.E.; Ton-That, H.; Johnson, J.M.; Yang, V.W. Transactivation and growth suppression by the gut-enriched Kruppel-like factor (Kruppel-like factor 4) are dependent on acidic amino acid residues and protein-protein interaction. Nucleic Acids Res. 2000, 28, 1106–1113, doi:10.1093/nar/28.5.1106.
Revello, M.G.; Gerna, G. Diagnosis and management of human cytomegalovirus infection in the mother, fetus, and newborn infant. Clin. Microbiol. Rev. 2002, 15, 80–715.
[102]
Revello, M.G.; Zavattoni, M.; Furione, M.; Lilleri, D.; Gorini, G.; Gerna, G. Diagnosis and outcomeof preconceptional and periconceptional primary human cytomegalovirus infections. J. Infect. Dis. 2002, 186, 553–557, doi:10.1086/341831.
Chou, S.; Marousek, G.; Guentzel, S.; Follansbee, S.E.; Poscher, M.E.; Lalezari, J.P.; Miner, R.C.; Drew, W.L. Evolution of mutations conferring multidrug resistance during prophylaxis and therapy for cytomegalovirus disease. J. Infect. Dis. 1997, 176, 786–789, doi:10.1086/517302.
[105]
Anderson, K.P.; Fox, M.C.; Brown-Driver, V.; Martin, M.J.; Azad, R.F. Inhibition of human cytomegalovirus immediate-early gene expression by an antisense oligonucleotide complementary to immediate-early RNA. Antimicrob. Agents Chemother. 1996, 40, 2004–2011.
[106]
Smith, J.A.; Pari, G.S. Expression of human cytomegalovirus UL36 and UL37 genes is required for viral DNA replication. J. Virol. 1995, 69, 1925–1931.
[107]
Munch, K.; Messerle, M.; Plachter, B.; Koszinowski, U.H. An acidic region of the 89K murine cytomegalovirus immediate early protein interacts with DNA. J. Gen. Virol. 1992, 73, 499–506, doi:10.1099/0022-1317-73-3-499.
