RNA expression analysis of MSL complex components in <i>Drosophila</i> aneuploid embryogenesis

QI Haizhu; TIAN Yu; ZHANG Shuai; SUN Lin

doi:10.12202/j.0476-0301.2020373

Journal of Beijing Normal University(Natural Science) > 2021 > 57(3): 329-336. > DOI: 10.12202/j.0476-0301.2020373

QI Haizhu, TIAN Yu, ZHANG Shuai, SUN Lin. RNA expression analysis of MSL complex components in Drosophila aneuploid embryogenesis[J]. Journal of Beijing Normal University(Natural Science), 2021, 57(3): 329-336. DOI: 10.12202/j.0476-0301.2020373

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RNA expression analysis of MSL complex components in Drosophila aneuploid embryogenesis

College of Life Sciences, Beijing Key Laboratory of Gene Resource and Molecular Development, Beijing Normal University, 100875, Beijing, China

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Received Date: November 02, 2020
Available Online: January 20, 2021

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Abstract

Abstract

Unbalanced gene dosage of aneuploidy usually results in some detrimental consequences in development, or even in death．The male specific lethal (MSL) complex, which is thought to play a fundamental role in regulating dosage compensation in Drosophila , also has great impact on gene expression in aneuploidy．To explore the molecular mechanism in embryogenesis, gene expression of MSL complex components was compared between normal diploid and autosomal trisomy embryos．TSA-FISH (tyramide signal amplification-fluorescence in situ hybridization) technology was used to detect changes in subcellular localization of transcripts. In early stage of aneuploid embryo development or maternal expression stage when no MSL complex is assembled, most complex component genes already showed differences at the transcript level．Such differences mainly derived from maternal non-haploid gametes．As embryo development proceeds, gene dosage imbalance due to increased chromosome fragmentation produced inverse dosage effect leading to differential expression of the MSL complex components．Consequently, it will continue to affect subsequent development of aneuploid embryos at later stages．
- aneuploidy,
- MSL complex,
- TSA-FISH,
- inverse dosage effect

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References

[1]	GOGENDEAU D,SIUDEJA K,GAMBAROTTO D,et al. Aneuploidy causes premature differentiation of neural and intestinal stem cells[J]. Nature Communications,2015,6:8894 doi: 10.1038/ncomms9894
[2]	DE GRAAF G,BUCKLEY F,SKOTKO B G. Estimates of the live births,natural losses,and elective terminations with Down syndrome in the United States[J]. American Journal of Medical Genetics Part A,2015,167A(4):756 doi: 10.1002/ajmg.a.37001
[3]	KAJII T. Predicted prevalence of Down syndrome live births in Japan,1970-2006[J]. American Journal of Medical Genetics Part A,2008,146A(11):1387 doi: 10.1002/ajmg.a.32323
[4]	WILSON L R,VATANSEVER D,ANNUS T,et al. Differential effects of Down’s syndrome and Alzheimer’s neuropathology on default mode connectivity[J]. Human Brain Mapping,2019,40(15):4551 doi: 10.1002/hbm.24720
[5]	WEAVER B A,CLEVELAND D W. Does aneuploidy cause cancer?[J]. Current Opinion in Cell Biology,2006,18(6):658 doi: 10.1016/j.ceb.2006.10.002
[6]	HERBERT M,KALLEAS D,COONEY D,et al. Meiosis and maternal aging:insights from aneuploid oocytes and trisomy births[J]. Cold Spring Harbor Perspectives in Biology,2015,7(4):a017970 doi: 10.1101/cshperspect.a017970
[7]	PAULSSON K,JOHANSSON B. Trisomy 8 as the sole chromosomal aberration in acute myeloid leukemia and myelodysplastic syndromes[J]. Pathologie Biologie,2007,55(1):37 doi: 10.1016/j.patbio.2006.04.007
[8]	WENZEL E S,SINGH A T K. Cell-cycle checkpoints and aneuploidy on the path to cancer[J]. In Vivo (Athens,Greece),2018,32(1):1
[9]	GEORGIEV P,CHLAMYDAS S,AKHTAR A. Drosophila dosage compensation:males are from Mars,females are from Venus[J]. Fly,2011,5(2):147 doi: 10.4161/fly.5.2.14934
[10]	BAI X Y,ALEKSEYENKO A A,KURODA M I. Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes[J]. The EMBO Journal,2004,23(14):2853 doi: 10.1038/sj.emboj.7600299
[11]	KOYA S K,MELLER V H. Modulation of heterochromatin by male specific lethal proteins and roX RNA in Drosophila melanogaster males[J]. PLoS One,2015,10(10):e0140259 doi: 10.1371/journal.pone.0140259
[12]	LI F,PARRY D A D,SCOTT M J. The amino-terminal region of Drosophila MSL1 contains basic,glycine-rich,and leucine zipper-like motifs that promote X chromosome binding,self-association,and MSL2 binding,respectively[J]. Molecular and Cellular Biology,2005,25(20):8913 doi: 10.1128/MCB.25.20.8913-8924.2005
[13]	KADLEC J,HALLACLI E,LIPP M,et al. Structural basis for MOF and MSL3 recruitment into the dosage compensation complex by MSL1[J]. Nature Structural & Molecular Biology,2011,18(2):142
[14]	VILLA R,FORNÉ I,MÜLLER M,et al. MSL2 combines sensor and effector functions in homeostatic control of the Drosophila dosage compensation machinery[J]. Molecular Cell,2012,48(4):647 doi: 10.1016/j.molcel.2012.09.012
[15]	GU W,SZAUTER P,LUCCHESI J C. Targeting of MOF,a putative histone acetyl transferase,to the X chromosome of Drosophila melanogaster[J]. Developmental Genetics,1998,22(1):56
[16]	SU J M,WANG F,CAI Y,et al. The functional analysis of histone acetyltransferase MOF in tumorigenesis[J]. International Journal of Molecular Sciences,2016,17(1):99 doi: 10.3390/ijms17010099
[17]	COPUR Ö,GORCHAKOV A,FINKL K,et al. Sex-specific phenotypes of histone H4 point mutants establish dosage compensation as the critical function of H4K16 acetylation in Drosophila[J]. Proceedings of the National Academy of Sciences of the United States of America,2018,115(52):13336 doi: 10.1073/pnas.1817274115
[18]	IZZO A,REGNARD C,MORALES V,et al. Structure-function analysis of the RNA helicase maleless[J]. Nucleic Acids Research,2008,36(3):950 doi: 10.1093/nar/gkm1108
[19]	CUGUSI S,KALLAPPAGOUDAR S,LING H P,et al. The Drosophila helicase maleless (MLE) is implicated in functions distinct from its role in dosage compensation[J]. Molecular & Cellular Proteomics,2015,14(6):1478 doi: 10.1074/mcp.M114.040667
[20]	MORRA R,SMITH E R,YOKOYAMA R,et al. The MLE subunit of the Drosophila MSL complex uses its ATPase activity for dosage compensation and its helicase activity for targeting[J]. Molecular & Cellular Biology,2008,28(3):958
[21]	MELLER V H,RATTNER B P. The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex[J]. The EMBO Journal,2002,21(5):1084 doi: 10.1093/emboj/21.5.1084
[22]	KELLEY R L,MELLER V H,GORDADZE P R,et al. Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin[J]. Cell,1999,98(4):513 doi: 10.1016/S0092-8674(00)81979-0
[23]	JOHNSON A F,HOU J,YANG H,et al. Magnitude of modulation of gene expression in aneuploid maize depends on the extent of genomic imbalance[J]. Journal of Genetics and Genomics,2020,47(2):93 doi: 10.1016/j.jgg.2020.02.002
[24]	GUO M,DAVIS D,BIRCHLER J A. Dosage effects on gene expression in a maize ploidy series[J]. Genetics,1996,142(4):1349
[25]	BHADRA U,GANDHI S G,PALAPARTHI R,et al. Drosophila maleless gene counteracts X global aneuploid effects in males[J]. The FEBS Journal,2016,283(18):3457 doi: 10.1111/febs.13818
[26]	SCHÖNHUBER W,FUCHS B,JURETSCHKO S,et al. Improved sensitivity of whole-cell hybridization by the combination of horseradish peroxidase-labeled oligonucleotides and tyramide signal amplification[J]. Applied and Environmental Microbiology,1997,63(8):3268 doi: 10.1128/AEM.63.8.3268-3273.1997
[27]	EICKHORST T,TIPPKÖTTER R. Improved detection of soil microorganisms using fluorescence in situ hybridization (FISH) and catalyzed reporter deposition (CARD-FISH)[J]. Soil Biology and Biochemistry,2008,40(7):1883
[28]	LAUTER G, SÖLL I,HAUPTMANN G. Sensitive multiplexed fluorescent in situ hybridization using enhanced tyramide signal amplification and its combination with immunofluorescent protein visualization in zebrafish[J]. Methods in Molecular Biology,2020,2047:397
[29]	SUN L,JOHNSON A F,LI J,et al. Differential effect of aneuploidy on the X chromosome and genes with sex-biased expression in Drosophila[J]. Proceedings of the National Academy of Sciences of the United States of America,2013,110(41):16514 doi: 10.1073/pnas.1316041110
[30]	ZIMMERMAN S G,PETERS N C,ALTARAS A E,et al. Optimized RNA ISH,RNA FISH and protein-RNA double labeling (IF/FISH) in Drosophila ovaries[J]. Nature Protocols,2013,8(11):2158 doi: 10.1038/nprot.2013.136

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RNA expression analysis of MSL complex components in Drosophila aneuploid embryogenesis

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