males absent on the first


DEVELOPMENTAL BIOLOGY

Effects of Mutation or Deletion

In Drosophila, dosage compensation is controlled by the male-specific lethal (MSL) complex consisting of MSL proteins and roX RNAs. The MSL complex is specifically localized on the male X chromosome where it acts to increase its expression ~2-fold. A model for the targeted assembly of the MSL complex has been proposed in which initial binding occurs at ~35 dispersed chromatin entry sites, followed by spreading in cis into flanking regions. Here, one of the chromatin entry sites, the roX1 gene, was analyzed to determine which sequences are sufficient to recruit the MSL complex. Association and spreading of the MSL complex from roX1 transgenes was found in the absence of detectable roX1 RNA synthesis from the transgene. The recruitment activity was mapped to a 217 bp roX1 fragment that shows male-specific DNase hypersensitivity and can be preferentially cross-linked in vivo to the MSL complex. When inserted on autosomes, this small roX1 segment is sufficient to produce an ectopic chromatin entry site that can nucleate binding and spreading of the MSL complex hundreds of kilobases into neighboring regions (Kageymama, 2001).

MSL1 and MSL2 are thought to form a core complex that binds to chromatin entry sites, while MLE and other components including roX RNAs may be added sequentially. To assess whether all the MSL components are required to bind to the roX1 exons, MSL1 localization on the roX1c3.4 transgene was analyzed in msl mutant animals. Since msl mutant males show poor morphology of polytene chromosomes, females carrying a Hsp83-MSL2 transgene were analyzed. Females normally lack MSL2 and can not form MSL complexes, but when MSL2 is constitutively expressed in females, the complex forms and is localized to both X chromosomes. The roX1c3.4 transgene recruits the MSL complex in the absence of functional mof as well as in cells lacking msl3, as expected for an authentic chromatin entry site. Thus, functional msl3 and mof are not required for MSL binding to chromatin entry sites including roX1, but in their absence the complex fails to associate with the additional hundreds of sites seen in its wild-type pattern on the X chromosome. This has been interpreted as an inability of the complex to spread between chromatin entry sites in the absence of either MSL3 or MOF. To test this hypothesis at the level of an individual entry site, a strain was examined in which MSL1 showed frequent spreading from a roX1 transgene (roX1c3.4-51A). It was found that lack of functional msl3 or mof prevents spreading, as it does on the endogenous X chromosome. Taken together, the MLE helicase protein is essential for the MSL complex to bind to the roX1 transgene, while the MSL3 chromodomain protein and MOF histone acetyltransferase are required only for spreading (Kageymama, 2001).

Mutations in Drosophila ISWI, a member of the SWI2/SNF2 family of chromatin remodeling ATPases, alter the global architecture of the male X chromosome. The transcription of genes on this chromosome is increased 2-fold relative to females due to dosage compensation, a process involving the acetylation of histone H4 at lysine 16 (H4K16). Blocking H4K16 acetylation suppresses the X chromosome defects resulting from loss of ISWI function in males. In contrast, the forced acetylation of H4K16 in ISWI mutant females causes X chromosome defects indistinguishable from those seen in ISWI mutant males. Increased expression of MOF, the histone acetyltransferase that acetylates H4K16, strongly enhances phenotypes resulting from the partial loss of ISWI function. Peptide competition assays have revealed that H4K16 acetylation reduces the ability of ISWI to interact productively with its substrate. These findings suggest that H4K16 acetylation directly counteracts chromatin compaction mediated by the ISWI ATPase (Corona, 2002).

A functional dosage compensation complex required for male killing in Drosophila

Bacteria that selectively kill males ('male-killers') were first characterized more than 50 years ago in Drosophila and have proved to be common in insects. However, the mechanism by which sex specificity of virulence is achieved has remained unknown. This study tested the ability of Spiroplasma poulsonii to kill Drosophila melanogaster males carrying mutations in genes that encode the dosage compensation complex. The bacterium failed to kill males lacking any of the five protein components of the complex (Veneti, 2005).

Certain isofemale lines of Drosophila only give rise to daughters following the death of male embryos. Male death is due to the presence of intracellular bacteria that pass from a female to her progeny and that selectively kill males during embryogenesis. These male-killing bacteria are found in a wide range of other insect species, and many different bacteria have evolved male-killing phenotypes. In some host species, male-killers drive the host population sex ratio to levels as high as 100 females per male and alter the pattern of mate competition. However, the underlying processes that produce male-limited mortality are unclear. This study examined the interaction between the male-killing bacterium Spiroplasma poulsonii and the sex determination pathway of D. melanogaster (Veneti, 2005).

The primary signal of sex in Drosophila is the X-to-autosome ratio. This signal is permanently established in expression of Sex-lethal (Sxl) in females and its absence in males. This, in turn, effects three processes: germline sexual identity, somatic sexual differentiation, and dosage compensation, the process by which the gene expression titer on the X chromosome is equalized between two sexes despite their difference in X chromosome number. Mutations in the gene tra that convert XX individuals to male somatic sex do not induce female death. These observations indicate germline formation and migration happen correctly in male embryos and that dying male embryos do not express Sxl. Therefore, the requirement of the Spiroplasma for genes within the system of dosage compensation was examined (Veneti, 2005).

In Drosophila, the single X of males is hypertranscribed. This process of hypertranscription requires the formation of the dosage compensation complex (DCC) and its binding to (and modification of) the X chromosome. SXL in female Drosophila inhibits the production of MSL-2 protein, which is thus only present in male Drosophila. MSL-2 forms a complex with four other proteins, MSL-1, MSL-3, MLE, and MOF, which collectively form the DCC. MSL-1, MSL-3, MLE, and MOF are constitutively present in both males and females and are also supplied maternally. The complete DCC binds, with JIL-1, to the male X chromosome at various entry points, and, with the products of two noncoding RNAs, RoX1 and RoX2, it affects the modification of the single X chromosome and its hypertranscription (Veneti, 2005).

The effect was examined of mutations within the host DCC on the ability of the male-killer to function. The survival of male progeny beyond embryogenesis to L2/L3 (and in one case adult) was scored in the presence of different loss-of-function mutations within the dosage compensation system (normal male-killing occurs during embryogenesis), in the presence and absence of infection. Because many genes within this group additionally show strong maternal effects, the effect of mutations was in each case tested by using both mothers that were heterozygous for the loss-of-function mutation and mothers homozygous for it (Veneti, 2005).

Uninfected males homozygous for loss-of-function mutations within the dosage compensation system generally survive to the third larval instar. Survival to the third larval instar was studied for loss-of-function alleles of msl-1 (alleles msl-11 and msl-1b), msl-2 (msl-2g227 and msl-2g134), msl-3 (msl-3132), mle (mle9, mle1), and mof (mof1), and survival to adult for mle1/mle6 transheterozygotes. In the case of all alleles of msl-1, msl-3, mle, and mof, a similar pattern is observed: Males homozygous or hemizygous for the loss-of-function mutation have appreciable survival in the presence of infection when their mother is also homozygous for the loss-of-function mutation. In contrast, heterozygous male embryos that were siblings of the above (that will have a wild-type DCC) were always killed, as were all male embryos in the case where the mother was heterozygous (where maternal supply of these proteins enables dosage compensation to be initiated, although not maintained). In the case of mle1/mle6 transheterozygotes, male survival to adult was observed. For the case of mof, male-killing was restored to full efficiency when 18H1, a transgenic copy of mof, was added to the mof1 loss-of-function background. Within the above crosses, three observations make sure the observation that Spiroplasma was fully operational. First, crosses involving heterozygous mothers, where male-killing was complete, were conducted concurrently with those using homozygous mothers, and the females in these crosses were siblings from the same vials. Second, in each cross and vial where homozygous males survived, heterozygous males (with wild-type function) still died. Finally, F1 females derived from these crosses, when mated to wild-type males, produced a full, female-biased sex ratio (Veneti, 2005).

In the case of msl-2, where there is no maternal supply of MSL-2, survival of homozygous sons was observed for both homozygous and heterozygous mothers for the case of the mutation msl-2g134. For the case of msl-2 g227, no male progeny were observed from infected females (table S5). This mutation does not rescue males in the assay, probably because the two mutations have different effects on msl-2 expression. The msl-2g134 allele prevents formation of MSL-2 protein, whereas msl-2 g227 potentially encodes the RING-finger element of a truncated MSL-2 protein (Veneti, 2005).

Thus, absence or reduced function of any of the proteins of the DCC can reduce the efficiency of male killing, and a functional DCC is required for male killing by S. poulsonii. The fact that the genes mediating this process in Drosophila have been well studied can be exploited to yield further insights into the mechanism of male killing (Veneti, 2005).


REFERENCES

Akhtar, A. and Becker, P. B. (2000a). Activation of transcription through histone H4 acetylation by Mof, an acetyltransferase essential for dosage compensation in Drosophila. Molec. Cell 5: 367-375. PubMed Citation: 10882077

Akhtar, A., Zink, D. and Becker, P. B. (2000b). Chromodomains are protein-RNA interaction modules. Nature 407: 405-409. PubMed Citation: 11014199

Bhadra, U., Pal-Bhadra, M. and Birchler, J. A. (2000). Histone acetylation and gene expression analysis of Sex lethal mutants in Drosophila. Genetics 155: 753-763. PubMed Citation: 10835396

Bone, J. R., Lavender, J., Richman, R., Palmer, M. J., Turner, B. M. and Kuroda, M. I. (1994). Acetylated histone H4 on the male X-chromosome is associated with dosage compensation in Drosophila. Genes Dev. 8: 96-104. PubMed Citation: 8288132

Borrow, J. J. et. al. (1996). The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nature Genet. 14: 33-41. PubMed Citation: 8782817

Brady, M. E., et al. (1999). Tip60 is a nuclear hormone receptor coactivator. J. Biol. Chem. 274(25): 17599-604. PubMed Citation: 10364196

Buscaino, A., et al. (2003). MOF-regulated acetylation of MSL-3 in the Drosophila dosage compensation complex. Molec. Cell 11: 1265-1277. 12769850

Cai, Y., et al. (2010). Subunit composition and substrate specificity of a MOF-containing histone acetyltransferase distinct from the male-specific lethal (MSL) complex. J. Biol. Chem. 285: 4268-4272. PubMed Citation: 20018852

Carapeti, M., et al. (1998). A novel fusion between MOZ and the nuclear receptor coactivator TIF2 in acute myeloid leukemia. Blood 91(9): 3127-33

Champagne, N., et al. (1999). Identification of a human histone acetyltransferase related to monocytic leukemia zinc finger protein. J. Biol. Chem. 274: 28528-28536

Chelmicki, T., Dundar, F., Turley, M. J., Khanam, T., Aktas, T., Ramirez, F., Gendrel, A. V., Wright, P. R., Videm, P., Backofen, R., Heard, E., Manke, T. and Akhtar, A. (2014). MOF-associated complexes ensure stem cell identity and Xist repression. Elife 3: e02024. PubMed ID: 24842875

Chen, Z. H., Zhu, M., Yang, J., Liang, H., He, J., He, S., Wang, P., Kang, X., McNutt, M. A., Yin, Y. and Shen, W. H. (2014). PTEN interacts with histone H1 and controls chromatin condensation. Cell Rep 8: 2003-2014. PubMed ID: 25199838

Clarke, A. S., et al. (1999). Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell. Biol. 19(4): 2515-26

Copur, O., Gorchakov, A., Finkl, K., Kuroda, M. I. and Muller, J. (2018). Sex-specific phenotypes of histone H4 point mutants establish dosage compensation as the critical function of H4K16 acetylation in Drosophila. Proc Natl Acad Sci U S A. PubMed ID: 30530664

Copps, K., Richman, R., Lyman, L.M., Chang, K.A., Rampersad-Ammons, J., and Kuroda, M.I. (1998). Complex formation by the Drosophila MSL proteins: role of the Msl2 RING finger in protein complex assembly. EMBO J. 17: 5409-5417

Corona, D. F., et al. (2002). Modulation of ISWI function by site-specific histone acetylation. EMBO Rep. 3(3): 242-7. 11882543

Creaven M., et al. (1999). Control of the histone-acetyltransferase activity of Tip60 by the HIV-1 transactivator protein, Tat. Biochemistry 38(27): 8826-30

Dahlsveen, I. K., Gilfillan, G. D., Shelest, V. I., Lamm, R. and Becker, P. B. (2006). Targeting determinants of dosage compensation in Drosophila. PLoS Genet. 2(2): e5. 16462942

Dou, Y., et al. (2005). Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121: 873-885. 15960975

Eddy, S. (1999). Noncoding RNA genes. Curr. Opin. Genet. Dev. 9: 695-699

Ehrenhofer-Murray, A. E., Rivier. D. H. and Rine, J. (1997). The role of Sas2, an acetyltransferase homologue of Saccharomyces cerevisiae, in silencing and ORC function. Genetics 145(4): 923-34

Feller, C., Prestel, M., Hartmann, H., Straub, T., Soding, J. and Becker, P. B. (2012). The MOF-containing NSL complex associates globally with housekeeping genes, but activates only a defined subset. Nucleic Acids Res 40: 1509-1522. PubMed ID: 22039099

Hochheimer, A., Zhou, S., Zheng, S., Holmes, M. C. and Tjian, R. (2002). TRF2 associates with DREF and directs promoter-selective gene expression in Drosophila. Nature 420: 439-445. PubMed ID: 12459787

Gavaravarapu, S. and Kamine J. (2000). Tip60 inhibits activation of CREB protein by protein kinase A. Biochem. Biophys. Res. Commun. 269(3): 758-66

Gu, W., Szauter, P. and Lucchesi, J.C. (1998) Targeting of Mof, a putative histone acetyl transferase to the X chromosome of Drosophila melanogaster. Dev. Genet. 22: 56-64

Gu, W., et al. (2000). Targeting the chromatin-remodeling MSL complex of Drosophila to its sites of action on the X chromosome requires both acetyl transferase and ATPase activities. EMBO J. 19: 5202-5211

Haberle, V., Arnold, C. D., Pagani, M., Rath, M., Schernhuber, K. and Stark, A. (2019). Transcriptional cofactors display specificity for distinct types of core promoters. Nature 570(7759):122-126. PubMed ID: 31092928

Heseding, C., Saumweber, H., Rathke, C. and Ehrenhofer-Murray, A. E. (2016). Widespread colocalization of the Drosophila histone acetyltransferase homolog MYST5 with DREF and insulator proteins at active genes. Chromosoma [Epub ahead of print]. PubMed ID: 26894919

Hilfiker, A., Yang, Y., Hayes, D. H., Beard, C. A., Manning, J. E. and Lucchesi, J. C. (1994). Dosage compensation in Drosophila: the X-chromosomal binding of MSL-1 and Mle is dependent on Sxl activity. EMBO J. 13: 3542-3550

Hilfiker, A., Hilfiker-Kleiner, D., Pannuti, A. and Lucchesi, J. C. (1997). mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J.16: 2054-2060

Hochheimer, A., Zhou, S., Zheng, S., Holmes, M. C. and Tjian, R. (2002). TRF2 associates with DREF and directs promoter-selective gene expression in Drosophila. Nature 420: 439-445. PubMed Citation: 12459787

Hug, C. B., Grimaldi, A. G., Kruse, K. and Vaquerizas, J. M. (2017). Chromatin architecture emerges during zygotic genome activation independent of transcription. Cell 169(2): 216-228 e219. PubMed ID: 28388407

Iizuka, M. and Stillman, B. (1999). Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J. Biol. Chem. 274(33): 23027-34

Ikeda, K., Steger, D. J., Eberharter, A., and Workman, J. L. (1999). Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes. Mol. Cell. Biol. 19: 855-863

Ivanova, A. V., Bonaduce, M. J., Ivanov, S. V. and Klar, A. J. (1998.) The chromo and SET domains of the Clr4 protein are essential for silencing in fission yeast. Nature Genet. 19: 192-195

Jiang, N., Emberly, E., Cuvier, O. and Hart, C. M. (2009). Genome-wide mapping of boundary element-associated factor (BEAF) binding sites in Drosophila melanogaster links BEAF to transcription. Mol Cell Biol 29: 3556-3568. Pubmed: 19380483

Kageyama, Y., et al. (2001). Association and spreading of the Drosophila dosage compensation complex from a discrete roX1 chromatin entry site. EMBO J. 20: 2236-2245. 11331589

Kamine, J., et al. (1996). Identification of a cellular protein that specifically interacts with the essential cysteine region of the HIV-1 Tat transactivator. Virology 216(2): 357-66

Kelley, R. L., Meller, V. H., Gordadze, P. R., Roman, G., Davis, R. L. and Kuroda, M. I. (1999). Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell 98: 513-522

Kimura, A. and Horikoshi, M. (1998). Tip60 acetylates six lysines of a specific class in core histones in vitro. Genes Cells 3(12): 789-800

Kind, J. and Akhtar, A. (2007). Cotranscriptional recruitment of the dosage compensation complex to X-linked target genes. Genes Dev. 21: 2030-2040. PubMed Citation: 17699750

Kind, J., et al. (2008) Genome-wide analysis reveals MOF as a key regulator of dosage compensation and gene expression in Drosophila. Cell 133: 813-828. PubMed Citation: 18510926

Lam, K. C., Muhlpfordt, F., Vaquerizas, J. M., Raja, S. J., Holz, H., Luscombe, N. M., Manke, T. and Akhtar, A. (2012). The NSL complex regulates housekeeping genes in Drosophila. PLoS Genet 8: e1002736. PubMed ID: 22723752

Laverty, C., Li, F., Belikoff, E. J. and Scott, M. J. (2011). Abnormal dosage compensation of reporter genes driven by the Drosophila glass multiple reporter (GMR) enhancer-promoter. PLoS One 6: e20455. Pubmed: 21655213

Lu, L. , Berkey, K. A. and Casero, R. A., Jr. (1996). RGFGIGS is an amino acid sequence required for acetyl coenzyme A binding and activity of human spermidine/spermine N1-acetyltransferase. J. Biol. Chem. 271: 18920-18924

Mendjan. S., et al. (2006). Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell 21: 811-823. 16543150

Mendjan S, et al. (2006), Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell. 21: 811-823. PubMed Citation: 16543150

Morales, V., Straub, T., Neumann, M. F., Mengus, G., Akhtar, A. and Becker, P. B. (2004). Functional integration of the histone acetyltransferase MOF into the dosage compensation complex. EMBO J. 23(11): 2258-68. 15141166

Morales, V., Regnard, C., Izzo, A., Vetter, I. and Becker, P. B. (2005). The MRG domain mediates the functional integration of MSL3 into the dosage compensation complex. Mol Cell Biol. 25(14): 5947-54. 15988010

Neal, K. C., et al. (2000). A new human member of the MYST family of histone acetyl transferases with high sequence similarity to Drosophila Mof. Biochim. Biophys. Acta. 1490(1-2): 170-4. PubMed Citation: 10786633

Pessoa Rodrigues, C., Herman, J. S., Herquel, B., Valsecchi, C. I. K., Stehle, T., Grun, D. and Akhtar, A. (2020). Temporal expression of MOF acetyltransferase primes transcription factor networks for erythroid fate. Sci Adv 6(21): eaaz4815. PubMed ID: 32671208

Philip, P., Pettersson, F. and Stenberg, P. (2012). Sequence signatures involved in targeting the Male-Specific Lethal complex to X-chromosomal genes in Drosophila melanogaster. BMC Genomics 13: 97. Pubmed: 22424303

Prestel, M., Feller, C., Straub, T., Mitlohner, H. and Becker, P. B. (2010), The activation potential of MOF is constrained for dosage compensation. Mol. Cell 38: 815-826. PubMed Citation: 20620953

Raja, S. J., et al. (2010). The nonspecific lethal complex is a transcriptional regulator in Drosophila. Mol. Cell. 38: 827-841. PubMed Citation: 20620954

Ravens, S., Fournier, M., Ye, T., Stierle, M., Dembele, D., Chavant, V. and Tora, L. (2014). MOF-associated complexes have overlapping and unique roles in regulating pluripotency in embryonic stem cells and during differentiation. Elife: e02104. PubMed ID: 24898753

Reifsnyder, C., et al. (1996). Yeast SAS silencing genes and human genes associated with AML and HIV-1 Tat interactions are homologous with acetyltransferases. Nat. Genet. 14(1): 42-9. PubMed Citation: 8782818

Samata, M., Alexiadis, A., Richard, G., Georgiev, P., Nuebler, J., Kulkarni, T., Renschler, G., Basilicata, M. F., Zenk, F. L., Shvedunova, M., Semplicio, G., Mirny, L., Iovino, N. and Akhtar, A. (2020). Intergenerationally maintained histone H4 lysine 16 acetylation is instructive for future gene activation. Cell. PubMed ID: 32502394

Scott, M. J., et al. (2000). Msl1 plays a central role in assembly of the MSL complex, essential for dosage compensation in Drosophila. EMBO J. 19: 144-155. PubMed Citation: 10619853

Sheikh, B. N., Bechtel-Walz, W., Lucci, J., Karpiuk, O., Hild, I., Hartleben, B., Vornweg, J., Helmstadter, M., Sahyoun, A. H., Bhardwaj, V., Stehle, T., Diehl, S., Kretz, O., Voss, A. K., Thomas, T., Manke, T., Huber, T. B. and Akhtar, A. (2015). MOF maintains transcriptional programs regulating cellular stress response. Oncogene [Epub ahead of print]. PubMed ID: 26387537

Sliva, D., et al. (1999). Tip60 interacts with human interleukin-9 receptor alpha-chain. Biochem. Biophys. Res. Commun. 263(1): 149-55. PubMed Citation: 10486269

Smith E. R., et al. (1998). ESA1 is a histone acetyltransferase that is essential for growth in yeast. Proc. Natl. Acad. Sci. 95(7): 3561-5. PubMed Citation: 9520405

Smith, E. R., et al. (2000). The Drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Molec. Cell. Biol. 20: 312-318. PubMed Citation: 10594033

Smith, E. R., Cayrou, C., Huang, R., Lane, W. S., Cote, J. and Lucchesi, J. C. (2005). A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Mol. Cell. Biol. 25(21): 9175-88. 16227571

Steinemann, M., Steinemann, S. and Turner, B. M. (1996). Evolution of dosage compensation. Chromosome Res. 4: 185-190. PubMed Citation: 8793201

Takechi, S. and Nakayama, T. (1999). Sas3 is a histone acetyltransferase and requires a zinc finger motif. Biochem. Biophys. Res. Commun. 266(2): 405-10. PubMed Citation: 10600516

Taipale, M., Rea, S., Richter, K., Vilar, A., Lichter, P., Imhof, A. and Akhtar, A. (2005). hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol. Cell. Biol. 25(15):6798-810. 16024812

Vanyai, H. K., Garnham, A., May, R. E., McRae, H. M., Collin, C., Wilcox, S., Smyth, G. K., Thomas, T. and Voss, A. K. (2019). MOZ directs the distal-less homeobox gene expression program during craniofacial development. Development 146(14). PubMed ID: 31340933

Veneti, Z., Bentley, J. K., Koana, T., Braig, H. R. and Hurst, G. D. (2005). A functional dosage compensation complex required for male killing in Drosophila. Science 307(5714): 1461-3. 15746426

Wei, T., Liu, H., Zhu, H., Chen, W., Wu, T., Bai, Y., Zhang, X., Miao, Y., Wang, F., Cai, Y. and Jin, J. (2022). Two distinct males absent on the first (MOF)-containing histone acetyltransferases are involved in the epithelial-mesenchymal transition in different ways in human cells. Cell Mol Life Sci 79(5): 238. PubMed ID: 35416545

Yamamoto, T. and Horikoshi, M. (1997). Novel substrate specificity of the histone acetyltransferase activity of HIV-1-Tat interactive protein Tip60. J. Biol. Chem. 272(49): 30595-8. PubMed Citation: 9388189

Zhao, X., Su, J., Wang, F., Liu, D., Ding, J., Yang, Y., Conaway, J. W., Conaway, R. C., Cao, L., Wu, D., Wu, M., Cai, Y. and Jin, J. (2013). Crosstalk between NSL histone acetyltransferase and MLL/SET complexes: NSL complex functions in promoting histone H3K4 di-methylation activity by MLL/SET complexes. PLoS Genet 9: e1003940. PubMed ID: 24244196

Zippo, A., et al. (2009). Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138(6): 1122-36. PubMed Citation: 19766566


males absent on the first: Biological Overview | Evolutionary Homologs | Regulation | Developmental Biology

date revised: 15 December 2020

Home page: The Interactive Fly © 1997 Thomas B. Brody, Ph.D.

The Interactive Fly resides on the
Society for Developmental Biology's Web server.