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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front. Biol.    2016, Vol. 11 Issue (2) : 85-95    https://doi.org/10.1007/s11515-016-1398-y
REVIEW
The epigenetics of CHARGE syndrome
Nina K. Latcheva1,2,Rupa Ghosh1,Daniel R. Marenda1,3,*()
1. Department of Biology, Drexel University, Philadelphia, PA 19104, USA
2. Program in Molecular and Cellular Biology and Genetics, Drexel University College of Medicine, Philadelphia, PA 19129, USA
3. Department of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA 19129, USA
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Abstract

In biology, we continue to appreciate the fact that the DNA sequence alone falls short when attempting to explain the intricate inheritance patterns for complex traits. This is particularly true for human disorders that appear to have simple genetic causes. The study of epigenetics, and the increased access to the epigenetic profiles of different tissues has begun to shed light on the genetic complexity of many basic biological processes, both physiological and pathological. Epigenetics refers to heritable changes in gene expression that are not due to alterations in the DNA sequence. Various mechanisms of epigenetic regulation exist, including DNA methylation and histone modification. The identification, and increased understanding of key players and mechanisms of epigenetic regulation have begun to provide significant insight into the underlying origins of various human genetic disorders. One such disorder is CHARGE syndrome (OMIM 214800), which is a leading cause of deaf-blindness worldwide. A majority of CHARGE syndrome cases are caused by haploinsufficiency for the CHD7 gene, which encodes an ATP-dependent chromatin remodeling protein involved in the epigenetic regulation of gene expression. The CHD7 protein has been highly conserved throughout evolution, and research into the function of CHD7 homologs in multiple model systems has increased our understanding of this family of proteins, and epigenetic mechanisms in general. Here we provide a review of CHARGE syndrome, and discuss the epigenetic functions of CHD7 in humans and CHD7 homologs in model organisms.

Keywords Drosophila      Kismet      CHD7      CHARGE syndrome      chromatin remodeling     
Corresponding Author(s): Daniel R. Marenda   
Just Accepted Date: 25 April 2016   Online First Date: 09 May 2016    Issue Date: 17 May 2016
 Cite this article:   
Nina K. Latcheva,Rupa Ghosh,Daniel R. Marenda. The epigenetics of CHARGE syndrome[J]. Front. Biol., 2016, 11(2): 85-95.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-016-1398-y
https://academic.hep.com.cn/fib/EN/Y2016/V11/I2/85
Fig.1  Homology between Chd7 proteins in model organisms. Schematic representation of conserved Chd7 proteins in model organisms used to study CHARGE syndrome. Percent value indicates homology to human CHD7. Green is chromodomain; blue is ATPase domain; purple is Switching-defective protein 3, Adaptor 2, Nuclear receptor co-repressor, Transcription factor (TF)IIIB (SANT)-Slide domain; dark gray is Brahma and Kismet (BRK) domain; yellow is DEAD-like helicase (DEXDc) domain; red is helicase superfamily C-terminal (HELICc) domain.
1 Aalfs J D, Kingston R E (2000). What does ʻchromatin remodelingʼ mean? Trends Biochem Sci, 25(11): 548–555
https://doi.org/10.1016/S0968-0004(00)01689-3
2 Allen M D, Religa T L, Freund S M, Bycroft M (2007). Solution structure of the BRK domains from CHD7. J Mol Biol, 371(5): 1135–1140
https://doi.org/10.1016/j.jmb.2007.06.007
3 Allis C D, Berger S L, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007). New nomenclature for chromatin-modifying enzymes. Cell, 131(4): 633–636
https://doi.org/10.1016/j.cell.2007.10.039
4 Bajpai R, Chen D A, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang C P, Zhao Y, Swigut T, Wysocka J (2010). CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature, 463(7283): 958–962
https://doi.org/10.1038/nature08733
5 Balasubramanian D, Akhtar-Zaidi B, Song L, Bartels C F, Veigl M, Beard L, Myeroff L, Guda K, Lutterbaugh J, Willis J, Crawford G E, Markowitz S D, Scacheri P C (2012). H3K4me3 inversely correlates with DNA methylation at a large class of non-CpG-island-containing start sites. Genome Med, 4(5): 47
https://doi.org/10.1186/gm346
6 Balow S A, Pierce L X, Zentner G E, Conrad P A, Davis S, Sabaawy H E, McDermott B MJr, Scacheri P C (2013). Knockdown of fbxl10/kdm2bb rescues chd7 morphant phenotype in a zebrafish model of CHARGE syndrome. Dev Biol, 382(1): 57–69
https://doi.org/10.1016/j.ydbio.2013.07.026
7 Basson M A, van Ravenswaaij-Arts C (2015). Functional Insights into Chromatin remodelling from studies on CHARGE syndrome. Trends Genet, 31(10): 600–611
https://doi.org/10.1016/j.tig.2015.05.009
8 Blake K D, Hartshorne T S, Lawand C, Dailor A N, Thelin J W (2008). Cranial nerve manifestations in CHARGE syndrome. Am J Med Genet A, 146A(5): 585–592
https://doi.org/10.1002/ajmg.a.32179
9 Blake K D, Prasad C (2006). CHARGE syndrome. Orphanet J Rare Dis, 1(1): 34
https://doi.org/10.1186/1750-1172-1-34
10 Bosman E A, Penn A C, Ambrose J C, Kettleborough R, Stemple D L, Steel K P (2005). Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum Mol Genet, 14(22): 3463–3476
https://doi.org/10.1093/hmg/ddi375
11 Bouazoune K, Kingston R E (2012). Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc Natl Acad Sci USA, 109(47): 19238–19243
https://doi.org/10.1073/pnas.1213825109
12 Boyer L A, Latek R R, Peterson C L (2004). The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol, 5(2): 158–163
https://doi.org/10.1038/nrm1314
13 Cavalli G, Paro R (1999). Epigenetic inheritance of active chromatin after removal of the main transactivator. Science, 286(5441): 955–958
https://doi.org/10.1126/science.286.5441.955
14 Daubresse G, Deuring R, Moore L, Papoulas O, Zakrajsek I, Waldrip W R, Scott M P, Kennison J A, Tamkun J W (1999). The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development, 126(6): 1175–1187
15 de Lonlay-Debeney P, Cormier-Daire V, Amiel J, Abadie V, Odent S, Paupe A, Couderc S, Tellier A L, Bonnet D, Prieur M, Vekemans M, Munnich A, Lyonnet S (1997). Features of DiGeorge syndrome and CHARGE association in five patients. J Med Genet, 34(12): 986–989
https://doi.org/10.1136/jmg.34.12.986
16 Dorighi K M, Tamkun J W (2013). The trithorax group proteins Kismet and ASH1 promote H3K36 dimethylation to counteract Polycomb group repression in Drosophila. Development, 140(20): 4182–4192
https://doi.org/10.1242/dev.095786
17 Engelen E, Akinci U, Bryne J C, Hou J, Gontan C, Moen M, Szumska D, Kockx C, van Ijcken W, Dekkers D H, Demmers J, Rijkers E J, Bhattacharya S, Philipsen S, Pevny L H, Grosveld F G, Rottier R J, Lenhard B, Poot R A (2011). Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat Genet, 43(6): 607–611
https://doi.org/10.1038/ng.825
18 Fasulo B, Deuring R, Murawska M, Gause M, Dorighi K M, Schaaf C A, Dorsett D, Brehm A, Tamkun J W (2012). The Drosophila MI-2 chromatin-remodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet, 8(8): e1002878
https://doi.org/10.1371/journal.pgen.1002878
19 Feng W, Khan M A, Bellvis P, Zhu Z, Bernhardt O, Herold-Mende C, Liu H K (2013). The chromatin remodeler CHD7 regulates adult neurogenesis via activation of SoxC transcription factors. Cell Stem Cell, 13(1): 62–72
https://doi.org/10.1016/j.stem.2013.05.002
20 Feng W, Liu H K (2013). Epigenetic regulation of neuronal fate determination: the role of CHD7. Cell Cycle, 12(24): 3707–3708
https://doi.org/10.4161/cc.26876
21 Fraga M F, Ballestar E, Paz M F, Ropero S, Setien F, Ballestar M L, Heine-Suner D, Cigudosa J C, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector T D, Wu Y Z, Plass C, Esteller M (2005). Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA, 102(30): 10604–10609
https://doi.org/10.1073/pnas.0500398102
22 Gangaraju V K, Bartholomew B (2007). Mechanisms of ATP dependent chromatin remodeling. Mutat Res, 618(1–2): 3–17
https://doi.org/10.1016/j.mrfmmm.2006.08.015
23 Gao X, Gordon D, Zhang D, Browne R, Helms C, Gillum J, Weber S, Devroy S, Swaney S, Dobbs M, Morcuende J, Sheffield V, Lovett M, Bowcock A, Herring J, Wise C (2007). CHD7 gene polymorphisms are associated with susceptibility to idiopathic scoliosis. Am J Hum Genet, 80(5): 957–965
https://doi.org/10.1086/513571
24 Ghosh R, Vegesna S, Safi R, Bao H, Zhang B, Marenda D R, Liebl F L (2014). Kismet positively regulates glutamate receptor localization and synaptic transmission at the Drosophila neuromuscular junction. PLoS ONE, 9(11): e113494
https://doi.org/10.1371/journal.pone.0113494
25 Gregory L C, Gevers E F, Baker J, Kasia T, Chong K, Josifova D J, Caimari M, Bilan F, McCabe M J, Dattani M T (2013). Structural pituitary abnormalities associated with CHARGE syndrome. J Clin Endocrinol Metab, 98(4): E737–E743
https://doi.org/10.1210/jc.2012-3467
26 He D, Marie C, Zhao C, Kim B, Wang J, Deng Y, Clavairoly A, Frah M, Wang H, He X, Hmidan H, Jones B V, Witte D, Zalc B, Zhou X, Choo D I, Martin D M, Parras C, Lu Q R (2016). Chd7 cooperates with Sox10 and regulates the onset of CNS myelination and remyelination. Nat Neurosci, doi: 10.1038/nn.4258
27 Hurd E A, Adams M E, Layman W S, Swiderski D L, Beyer L A, Halsey K E, Benson J M, Gong T W, Dolan D F, Raphael Y, Martin D M (2011). Mature middle and inner ears express Chd7 and exhibit distinctive pathologies in a mouse model of CHARGE syndrome. Hear Res, 282(1–2): 184–195
https://doi.org/10.1016/j.heares.2011.08.005
28 Hurd E A, Capers P L, Blauwkamp M N, Adams M E, Raphael Y, Poucher H K, Martin D M (2007). Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm Genome, 18(2): 94–104
https://doi.org/10.1007/s00335-006-0107-6
29 Hurd E A, Micucci J A, Reamer E N, Martin D M (2012). Delayed fusion and altered gene expression contribute to semicircular canal defects in Chd7 deficient mice. Mech Dev, 129(9–12): 308–323
https://doi.org/10.1016/j.mod.2012.06.002
30 Hurd E A, Poucher H K, Cheng K, Raphael Y, Martin D M (2010). The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear. Development, 137(18): 3139–3150
https://doi.org/10.1242/dev.047894
31 Jacobs-McDaniels N L, Albertson R C (2011). Chd7 plays a critical role in controlling left-right symmetry during zebrafish somitogenesis. Dev Dyn, 240(10): 2272–2280
https://doi.org/10.1002/dvdy.22722
32 Janssen N, Bergman J E, Swertz M A, Tranebjaerg L, Lodahl M, Schoots J, Hofstra R M, van Ravenswaaij-Arts C M, Hoefsloot L H (2012). Mutation update on the CHD7 gene involved in CHARGE syndrome. Hum Mutat, 33(8): 1149–1160
https://doi.org/10.1002/humu.22086
33 Jongmans M C, Admiraal R J, van der Donk K P, Vissers L E, Baas A F, Kapusta L, van Hagen J M, Donnai D, de Ravel T J, Veltman J A, Geurts van Kessel A, De Vries B B, Brunner H G, Hoefsloot L H, van Ravenswaaij C M (2006). CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene. J Med Genet, 43(4): 306–314
https://doi.org/10.1136/jmg.2005.036061
34 Jongmans M C, Hoefsloot L H, van der Donk K P, Admiraal R J, Magee A, van de Laar I, Hendriks Y, Verheij J B, Walpole I, Brunner H G, van Ravenswaaij C M (2008). Familial CHARGE syndrome and the CHD7 gene: a recurrent missense mutation, intrafamilial recurrence and variability. Am J Med Genet A, 146A(1): 43–50
https://doi.org/10.1002/ajmg.a.31921
35 Kaminsky Z A, Tang T, Wang S C, Ptak C, Oh G H, Wong A H, Feldcamp L A, Virtanen C, Halfvarson J, Tysk C, McRae A F, Visscher P M, Montgomery G W, Gottesman I I, Martin N G, Petronis A (2009). DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet, 41(2): 240–245
https://doi.org/10.1038/ng.286
36 Kim K H, Roberts C W (2013). CHD7 in charge of neurogenesis. Cell Stem Cell, 13(1): 1–2
https://doi.org/10.1016/j.stem.2013.06.010
37 Kirmizis A, Santos-Rosa H, Penkett C J, Singer M A, Vermeulen M, Mann M, Bahler J, Green R D, Kouzarides T (2007). Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature, 449(7164): 928–932
https://doi.org/10.1038/nature06160
38 Kita Y, Nishiyama M, Nakayama K I (2012). Identification of CHD7S as a novel splicing variant of CHD7 with functions similar and antagonistic to those of the full-length CHD7L. Genes Cells, 17(7): 536–547
https://doi.org/10.1111/j.1365-2443.2012.01606.x
39 Kornberg R D, Lorch Y (1999). Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell, 98(3): 285–294
https://doi.org/10.1016/S0092-8674(00)81958-3
40 Kosaki K (2011). Role of rare cases in deciphering the mechanisms of congenital anomalies: CHARGE syndrome research. Congenit Anom (Kyoto), 51(1): 12–15
https://doi.org/10.1111/j.1741-4520.2010.00309.x
41 Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693–705
https://doi.org/10.1016/j.cell.2007.02.005
42 Kouzarides T (2007). SnapShot: Histone-modifying enzymes. Cell, 131(4): 822–822.e1
https://doi.org/10.1016/j.cell.2007.11.005
43 Kouzarides T (2007). SnapShot: Histone-modifying enzymes. Cell, 128(4): 802
https://doi.org/10.1016/j.cell.2007.02.018
44 Lalani S R, Safiullah A M, Fernbach S D, Harutyunyan K G, Thaller C, Peterson L E, McPherson J D, Gibbs R A, White L D, Hefner M, Davenport S L, Graham J MJr, Bacino C A, Glass N L, Towbin J A, Craigen W J, Neish S R, Lin A E, Belmont J W (2006). Spectrum of CHD7 mutations in 110 individuals with CHARGE syndrome and genotype-phenotype correlation. Am J Hum Genet, 78(2): 303–314
https://doi.org/10.1086/500273
45 Layman W S, Hurd E A, Martin D M (2011). Reproductive dysfunction and decreased GnRH neurogenesis in a mouse model of CHARGE syndrome. Hum Mol Genet, 20(16): 3138–3150
https://doi.org/10.1093/hmg/ddr216
46 Layman W S, McEwen D P, Beyer L A, Lalani S R, Fernbach S D, Oh E, Swaroop A, Hegg C C, Raphael Y, Martens J R, Martin D M (2009). Defects in neural stem cell proliferation and olfaction in Chd7 deficient mice indicate a mechanism for hyposmia in human CHARGE syndrome. Hum Mol Genet, 18(11): 1909–1923
https://doi.org/10.1093/hmg/ddp112
47 Melicharek D, Shah A, DiStefano G, Gangemi A J, Orapallo A, Vrailas-Mortimer A D, Marenda D R (2008). Identification of novel regulators of atonal expression in the developing Drosophila retina. Genetics, 180(4): 2095–2110
https://doi.org/10.1534/genetics.108.093302
48 Melicharek D J, Ramirez L C, Singh S, Thompson R, Marenda D R (2010). Kismet/CHD7 regulates axon morphology, memory and locomotion in a Drosophila model of CHARGE syndrome. Hum Mol Genet, 19(21): 4253–4264
https://doi.org/10.1093/hmg/ddq348
49 Micucci J A, Layman W S, Hurd E A, Sperry E D, Frank S F, Durham M A, Swiderski D L, Skidmore J M, Scacheri P C, Raphael Y, Martin D M (2014). CHD7 and retinoic acid signaling cooperate to regulate neural stem cell and inner ear development in mouse models of CHARGE syndrome. Hum Mol Genet, 23(2): 434–448
https://doi.org/10.1093/hmg/ddt435
50 Mueller-Planitz F, Klinker H, Ludwigsen J, Becker P B (2013). The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat Struct Mol Biol, 20(1): 82–89
https://doi.org/10.1038/nsmb.2457
51 Papp B, Muller J (2006). Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev, 20(15): 2041–2054
https://doi.org/10.1101/gad.388706
52 Paro R, Strutt H, Cavalli G (1998). Heritable chromatin states induced by the Polycomb and trithorax group genes. Novartis Found Symp, 214: 51–61; discussion 61–56, 104–113
53 Patten S A, Jacobs-McDaniels N L, Zaouter C, Drapeau P, Albertson R C, Moldovan F (2012). Role of Chd7 in zebrafish: a model for CHARGE syndrome. PLoS ONE, 7(2): e31650
https://doi.org/10.1371/journal.pone.0031650
54 Petruk S, Sedkov Y, Johnston D M, Hodgson J W, Black K L, Kovermann S K, Beck S, Canaani E, Brock H W, Mazo A (2012). TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell, 150(5): 922–933
https://doi.org/10.1016/j.cell.2012.06.046
55 Pinto G, Abadie V, Mesnage R, Blustajn J, Cabrol S, Amiel J, Hertz-Pannier L, Bertrand A M, Lyonnet S, Rappaport R, Netchine I (2005). CHARGE syndrome includes hypogonadotropic hypogonadism and abnormal olfactory bulb development. J Clin Endocrinol Metab, 90(10): 5621–5626
https://doi.org/10.1210/jc.2004-2474
56 Reisman D, Glaros S, Thompson E A (2009). The SWI/SNF complex and cancer. Oncogene, 28(14): 1653–1668
https://doi.org/10.1038/onc.2009.4
57 Richmond T J, Davey C A (2003). The structure of DNA in the nucleosome core. Nature, 423(6936): 145–150
https://doi.org/10.1038/nature01595
58 Sanlaville D, Verloes A (2007). CHARGE syndrome: an update. Eur J Hum Genet, 15(4): 389–399
https://doi.org/10.1038/sj.ejhg.5201778
59 Santoro R, Li J, Grummt I (2002). The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet, 32(3): 393–396
https://doi.org/10.1038/ng1010
60 Schnetz M P, Bartels C F, Shastri K, Balasubramanian D, Zentner G E, Balaji R, Zhang X, Song L, Wang Z, Laframboise T, Crawford G E, Scacheri P C (2009). Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res, 19(4): 590–601
https://doi.org/10.1101/gr.086983.108
61 Schnetz M P, Handoko L, Akhtar-Zaidi B, Bartels C F, Pereira C F, Fisher A G, Adams D J, Flicek P, Crawford G E, Laframboise T, Tesar P, Wei C L, Scacheri P C (2010). CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet, 6(7): e1001023
https://doi.org/10.1371/journal.pgen.1001023
62 Souriau J, Gimenes M, Blouin C, Benbrik I, Benbrik E, Churakowskyi A, Churakowskyi B (2005). CHARGE syndrome: developmental and behavioral data. Am J Med Genet A, 133A(3): 278–281
https://doi.org/10.1002/ajmg.a.30549
63 Srinivasan S, Armstrong J A, Deuring R, Dahlsveen I K, McNeill H, Tamkun J W (2005). The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development, 132(7): 1623–1635
https://doi.org/10.1242/dev.01713
64 Srinivasan S, Dorighi K M, Tamkun J W (2008). Drosophila Kismet regulates histone H3 lysine 27 methylation and early elongation by RNA polymerase II. PLoS Genet, 4(10): e1000217
https://doi.org/10.1371/journal.pgen.1000217
65 Tellier A L, Cormier-Daire V, Abadie V, Amiel J, Sigaudy S, Bonnet D, de Lonlay-Debeney P, Morrisseau-Durand M P, Hubert P, Michel J L, Jan D, Dollfus H, Baumann C, Labrune P, Lacombe D, Philip N, LeMerrer M, Briard M L, Munnich A, Lyonnet S (1998). CHARGE syndrome: report of 47 cases and review. Am J Med Genet, 76(5): 402–409
https://doi.org/10.1002/(SICI)1096-8628(19980413)76:5<402::AID-AJMG7>3.0.CO;2-O
66 Terriente-Felix A, Molnar C, Gomez-Skarmeta J L, de Celis J F (2011). A conserved function of the chromatin ATPase Kismet in the regulation of hedgehog expression. Dev Biol, 350(2): 382–392
https://doi.org/10.1016/j.ydbio.2010.12.003
67 Therrien M, Morrison D K, Wong A M, Rubin G M (2000). A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics, 156(3): 1231–1242
68 Torres-Padilla M E, Parfitt D E, Kouzarides T, Zernicka-Goetz M (2007). Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature, 445(7124): 214–218
https://doi.org/10.1038/nature05458
69 Vissers L E, van Ravenswaaij C M, Admiraal R, Hurst J A, de Vries B B, Janssen I M, van der Vliet W A, Huys E H, de Jong P J, Hamel B C, Schoenmakers E F, Brunner H G, Veltman J A, van Kessel A G (2004). Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet, 36(9): 955–957
https://doi.org/10.1038/ng1407
70 Workman J L (2006). Nucleosome displacement in transcription. Genes Dev, 20(15): 2009–2017
https://doi.org/10.1101/gad.1435706
71 Zentner G E, Hurd E A, Schnetz M P, Handoko L, Wang C, Wang Z, Wei C, Tesar P J, Hatzoglou M, Martin D M, Scacheri P C (2010a). CHD7 functions in the nucleolus as a positive regulator of ribosomal RNA biogenesis. Hum Mol Genet, 19(18): 3491–3501
https://doi.org/10.1093/hmg/ddq265
72 Zentner G E, Layman W S, Martin D M, Scacheri P C (2010b). Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A, 152A(3): 674–686
https://doi.org/10.1002/ajmg.a.33323
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