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Gene Review

HO  -  Hop

Saccharomyces cerevisiae S288c

Synonyms: Ho endonuclease, Homothallic switching endonuclease, YDL227C
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Disease relevance of HO


High impact information on HO

  • The INO80 complex is recruited to a HO endonuclease-induced DSB through a specific interaction with the DNA damage-induced phosphorylated histone H2A (gamma-H2AX) [3].
  • Swi5p remains at HO for only 5 min [4].
  • Using CHIP, we measured recruitment of Swi/Snf, SAGA, the repressor Ash1p, and transcription factors Swi5p and SBF to the HO endonuclease promoter as cells progress through the yeast cell cycle [4].
  • We describe the identification of five genes, called SHE1-SHE5, that encode cytoplasmic proteins required for mother-specific HO expression [5].
  • Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins [5].

Biological context of HO

  • Cell cycle-specific expression of the SWI4 transcription factor is required for the cell cycle regulation of HO transcription [6].
  • Transcription of the HO gene is start-dependent and restricted to the late G1/early S phase of haploid mother cells [6].
  • For HO and the DNA replication genes, cell cycle stage-specific expression has been shown to be dependent on the Cdc28 kinase and passage through START [7].
  • SWI5 encodes a zinc-finger protein required for expression of the yeast HO gene [8].
  • In addition, rfa1-44 shows a reduced ability to undergo sporulation and HO-induced gene conversion [9].

Anatomical context of HO

  • She proteins might be required for the transport of factors that promote HO repression from the mother cell into its bud [5].
  • Ash1p, which only accumulates in daughter cell nuclei, binds to HO soon after Swi5p and aborts recruitment of Swi/Snf, SAGA, and SBF [4].
  • Physical monitoring of DNA showed that SPO13: : HO induced gene conversions both in Rad+ and in rad50 delta cells that cannot initiate normal meiotic DSBs [10].

Associations of HO with chemical compounds

  • Here, we show that cells released from cdc28ts arrest in the presence of cycloheximide show wild-type levels of induction for HO, CLN1, and CDC9 (DNA ligase) [7].
  • Multiple DSBs were created either by expressing the HO endonuclease in strains containing several HO cut sites embedded within randomly dispersed Ty1 elements or by phleomycin treatment [11].
  • SCE frequencies were measured after cells were exposed to UV, X-rays, 4-nitroquinoline 1-oxide (4-NQO) and methyl methanesulfonate (MMS), or when an HO endonuclease-induced DSB was introduced at his3-Delta3'::HOcs [12].
  • This mutation, cdc1-100, completely eliminated HO-induced Ura+ recombination yet maintained both spontaneous preinduced recombination levels and cell viability, cdc1-100 mutants were moderately sensitive to killing by methyl methanesulfonate and gamma irradiation [13].
  • Experiments examining the kinetics of binding show that Mediator binds to HO promoter elements 1.5 kb upstream of the transcription start site in early G1, but this binding occurs without RNA Pol II [14].

Physical interactions of HO

  • There are two Swi5p binding sites in the HO promoter, site A at -1800 and site B at -1300 [15].
  • SIN1 interacts with a protein that binds the URS1 region of the yeast HO gene [16].
  • We also find that inactivation of the Sin3p/Rpd3p deacetylase complex leads to a high level of acetylation at the HO locus throughout the cell cycle [17].
  • Assembly and disassembly of Rad51 and Rad52 complexes were monitored by immunofluorescence during homologous recombination initiated by an HO endonuclease-induced double-strand break (DSB) at the MAT locus [18].
  • Studies using a three-hybrid assay for RNA binding indicate that Mpt5 binds to the 3'-UTR of HO mRNA containing a UUGU sequence but not a UACU sequence [19].

Enzymatic interactions of HO

  • Studies in which an HO endonuclease cut was introduced between the two leu2 copies indicate that the rfa1-D228Y mutation partially suppresses the rad52 defect in recovering recombination products [20].
  • We constructed strains containing two ura3 segments on one side of the HO cut site and one ura3 region on the other side to characterize how flanking repeats find each other [21].
  • In these blocked cells, the HO-cut ends of MATa remained stable for at least 3 h [22].
  • Mitotic recombination was initiated by HO endonuclease-induced DSBs at the HO cut site (HOcs) located at his3-delta 3'::HOcs, and His+ recombinants were selected [23].

Regulatory relationships of HO


Other interactions of HO

  • Transcription of HO also requires SNF5 and SNF6 [28].
  • Constitutive synthesis of SWI4 mRNA leads to constitutive synthesis of HO mRNA [6].
  • The HO promoter contains 10 copies of a cell cycle-regulated upstream activation sequence, which is activated by SWI4 and SWI6 [6].
  • SWI5 is a transcriptional activator of the HO endonuclease gene, whereas ACE2 is not [24].
  • In Saccharomyces cerevisiae, the genes encoding the HO endonuclease, G1-specific cyclins CLN1 and CLN2, as well as most proteins involved in DNA synthesis, are periodically transcribed with maximal levels reached in late G1 [7].

Analytical, diagnostic and therapeutic context of HO

  • Chromatin immunoprecipitation experiments revealed that the Ddc1 protein associates with a region near the MAT locus after HO expression [29].
  • In vivo analysis of the Saccharomyces cerevisiae HO nuclease recognition site by site-directed mutagenesis [30].
  • We aimed to understand the molecular basis of this behaviour in a flor autochthonous strain, verifying the MAT locus status by a PCR-based HO gene disruption and sequencing of the Y region of the HML, HMR and MAT loci, after nested PCR [31].
  • The presence of the ho::neo and HO alleles in the heterothallic and homothallic progeny was confirmed by Southern-blot analysis [32].
  • We termed this novel type of life cycle "delayed homothallism". The results of complementation tests with standard ho strains and introduction of a wild type HO gene showed that delayed homothallism was caused by a defective HO gene [33].


  1. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Rudin, N., Haber, J.E. Mol. Cell. Biol. (1988) [Pubmed]
  2. In situ detection of specific DNA double strand breaks using rolling circle amplification. Li, J., Young, C.S., Lizardi, P.M., Stern, D.F. Cell Cycle (2005) [Pubmed]
  3. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Morrison, A.J., Highland, J., Krogan, N.J., Arbel-Eden, A., Greenblatt, J.F., Haber, J.E., Shen, X. Cell (2004) [Pubmed]
  4. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cosma, M.P., Tanaka, T., Nasmyth, K. Cell (1999) [Pubmed]
  5. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins. Jansen, R.P., Dowzer, C., Michaelis, C., Galova, M., Nasmyth, K. Cell (1996) [Pubmed]
  6. Cell cycle-specific expression of the SWI4 transcription factor is required for the cell cycle regulation of HO transcription. Breeden, L., Mikesell, G.E. Genes Dev. (1991) [Pubmed]
  7. Direct induction of G1-specific transcripts following reactivation of the Cdc28 kinase in the absence of de novo protein synthesis. Marini, N.J., Reed, S.I. Genes Dev. (1992) [Pubmed]
  8. The Swi5 zinc-finger and Grf10 homeodomain proteins bind DNA cooperatively at the yeast HO promoter. Brazas, R.M., Stillman, D.J. Proc. Natl. Acad. Sci. U.S.A. (1993) [Pubmed]
  9. A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52. Firmenich, A.A., Elias-Arnanz, M., Berg, P. Mol. Cell. Biol. (1995) [Pubmed]
  10. Meiotic recombination initiated by a double-strand break in rad50 delta yeast cells otherwise unable to initiate meiotic recombination. Malkova, A., Ross, L., Dawson, D., Hoekstra, M.F., Haber, J.E. Genetics (1996) [Pubmed]
  11. The Mre11 nuclease is not required for 5' to 3' resection at multiple HO-induced double-strand breaks. Llorente, B., Symington, L.S. Mol. Cell. Biol. (2004) [Pubmed]
  12. Multiple recombination pathways for sister chromatid exchange in Saccharomyces cerevisiae: role of RAD1 and the RAD52 epistasis group genes. Dong, Z., Fasullo, M. Nucleic Acids Res. (2003) [Pubmed]
  13. Mutations in the Saccharomyces cerevisiae CDC1 gene affect double-strand-break-induced intrachromosomal recombination. Halbrook, J., Hoekstra, M.F. Mol. Cell. Biol. (1994) [Pubmed]
  14. The Swi5 activator recruits the Mediator complex to the HO promoter without RNA polymerase II. Bhoite, L.T., Yu, Y., Stillman, D.J. Genes Dev. (2001) [Pubmed]
  15. Long-range interactions at the HO promoter. McBride, H.J., Brazas, R.M., Yu, Y., Nasmyth, K., Stillman, D.J. Mol. Cell. Biol. (1997) [Pubmed]
  16. SIN1 interacts with a protein that binds the URS1 region of the yeast HO gene. Katcoff, D.J., Yona, E., Hershkovits, G., Friedman, H., Cohen, Y., Dgany, O. Nucleic Acids Res. (1993) [Pubmed]
  17. Cell cycle-regulated histone acetylation required for expression of the yeast HO gene. Krebs, J.E., Kuo, M.H., Allis, C.D., Peterson, C.L. Genes Dev. (1999) [Pubmed]
  18. In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. Miyazaki, T., Bressan, D.A., Shinohara, M., Haber, J.E., Shinohara, A. EMBO J. (2004) [Pubmed]
  19. Post-transcriptional regulation through the HO 3'-UTR by Mpt5, a yeast homolog of Pumilio and FBF. Tadauchi, T., Matsumoto, K., Herskowitz, I., Irie, K. EMBO J. (2001) [Pubmed]
  20. An allele of RFA1 suppresses RAD52-dependent double-strand break repair in Saccharomyces cerevisiae. Smith, J., Rothstein, R. Genetics (1999) [Pubmed]
  21. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Sugawara, N., Haber, J.E. Mol. Cell. Biol. (1992) [Pubmed]
  22. Physical monitoring of mating type switching in Saccharomyces cerevisiae. Connolly, B., White, C.I., Haber, J.E. Mol. Cell. Biol. (1988) [Pubmed]
  23. Expression of Saccharomyces cerevisiae MATa and MAT alpha enhances the HO endonuclease-stimulation of chromosomal rearrangements directed by his3 recombinational substrates. Fasullo, M., Bennett, T., Dave, P. Mutat. Res. (1999) [Pubmed]
  24. Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase. Dohrmann, P.R., Butler, G., Tamai, K., Dorland, S., Greene, J.R., Thiele, D.J., Stillman, D.J. Genes Dev. (1992) [Pubmed]
  25. Genetic interactions between mediator and the late G1-specific transcription factor Swi6 in Saccharomyces cerevisiae. Li, L., Quinton, T., Miles, S., Breeden, L.L. Genetics (2005) [Pubmed]
  26. HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events. Malkova, A., Klein, F., Leung, W.Y., Haber, J.E. Proc. Natl. Acad. Sci. U.S.A. (2000) [Pubmed]
  27. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Ira, G., Pellicioli, A., Balijja, A., Wang, X., Fiorani, S., Carotenuto, W., Liberi, G., Bressan, D., Wan, L., Hollingsworth, N.M., Haber, J.E., Foiani, M. Nature (2004) [Pubmed]
  28. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Peterson, C.L., Herskowitz, I. Cell (1992) [Pubmed]
  29. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K., Sugimoto, K. Science (2001) [Pubmed]
  30. In vivo analysis of the Saccharomyces cerevisiae HO nuclease recognition site by site-directed mutagenesis. Nickoloff, J.A., Singer, J.D., Heffron, F. Mol. Cell. Biol. (1990) [Pubmed]
  31. Diversity of Y region at HML locus in a Saccharomyces cerevisiae strain isolated from a Sardinian wine. Pirino, G., Zara, S., Pinna, G., Farris, G.A., Budroni, M. Antonie Van Leeuwenhoek (2004) [Pubmed]
  32. Conversion of homothallic yeast to heterothallism through HO gene disruption. van Zyl, W.H., Lodolo, E.J., Gericke, M. Curr. Genet. (1993) [Pubmed]
  33. A novel type of life cycle "delayed homothallism" in Saccharomyces cerevisiae wy2 showed slow interconversion of mating-type. Tani, Y., Kurokui, T., Masaki, C., Hayakawa, M., Ekino, K., Tomohiro, Y., Miyata, A., Furukawa, K., Hayashida, S. Biosci. Biotechnol. Biochem. (1994) [Pubmed]
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