Skip to main content
SpringerLink
Log in

Chriz, a chromodomain protein specific for the interbands of Drosophila melanogaster polytene chromosomes

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Polytene interphase chromosomes are compacted into a series of bands and interbands reflecting their organization into independent chromosomal domains. In order to understand chromosomal organization, we set out to study the role of proteins that are selective for interbands. Here we describe the Drosophila melanogaster chromodomain protein Chriz that is coimmunoprecipitated with the zinc finger protein Z4. Both proteins colocalize exclusively to the interbands on Drosophila polytene chromosomes. Like Z4, Chriz is ubiquitously expressed throughout development and is associated with chromatin in all interphase nuclei. Following dissociation from chromatin, early in mitosis Chriz binds to the centrosomes and to the mitotic spindle. Newly induced amorphic Chriz alleles are early lethal, and ubiquitous overexpression of Chriz is lethal as well. Available Chriz hypomorphs which survive until pupal stage have a normal chromosomal phenotype. Reducing Z4 protein does not affect Chriz binding to polytene chromosomes and vice versa. Z4 is still chromosomally bound when Chriz protein is depleted by RNA interference.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Akhtar A (2003) Dosage compensation: an intertwined world of RNA and chromatin remodelling. Curr Opin Genet Dev 13:161–169

    Google Scholar 

  • Akhtar A, Zink D, Becker PB (2000) Chromodomains are protein–RNA interaction modules. Nature 407:405–409

    Google Scholar 

  • Altschul M, Simpson KW, Dykes NL, Mauldin EA, Reubi JC, Cummings JF (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  Google Scholar 

  • Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270–2275

    Google Scholar 

  • Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, Scott MP, Tamkun JW (2002) The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J 21:5245–5254

    Google Scholar 

  • Beermann W (1972) Chromomeres and genes. In: Beermann W, Reiner J, Ursprium H (eds) Results and problems in cell differentiation, vol 4. Springer, Berlin Heidelberg New York, pp 1–33

    Google Scholar 

  • Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, Tsang G, Evans-Holm M, Hiesinger PR, Schulze KL, Rubin GM, Hoskins RA, Spradling AC (2004) The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167:761–781

    Article  CAS  PubMed  Google Scholar 

  • Benyajati C, Worcel A (1976) Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster. Cell 9:393–407

    Google Scholar 

  • Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3:1273–1287

    CAS  PubMed  Google Scholar 

  • Bouazoune K, Mitterweger A, Langst G, Imhof A, Akhtar A, Becker PB, Brehm A (2002) The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. EMBO J 21:2430–2440

    Google Scholar 

  • Brand AH, Perrimon N (1993) Target gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    CAS  PubMed  Google Scholar 

  • Byrd NK, Shearn A (2003) ASH1, a Drosophila trithorax group protein, is required for methylation of lysine 4 residues on histone H3. Proc Natl Acad Sci U S A 100:11535–11540

    Google Scholar 

  • Callan HG (1987) Lampbrush chromosomes as seen in historical perspective. In: Hennig W (ed) Results and problems in cell differentiation, vol 14. Structure and function of eukaryotic chromosomes. Springer, Berlin Heidelberg New York, pp 5–26

    Google Scholar 

  • Cherbas L, Hu X, Zhimulev I, Belyaeva E, Cherbas P (2002) EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130:271–284

    Google Scholar 

  • Clegg NJ, Frost DM, Larkin MK, Subrahmanyan L, Bryant Z, Ruohola-Baker H (1997) Maelstrom is required for an early step in the establishment of Drosophila oocyte polarity: posterior localization of grk mRNA. Development 124:4661–4671

    Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16(22):10881–10890

    CAS  PubMed  Google Scholar 

  • Cuvier O, Hart CM, Laemmli UK (1998) Identification of a class of chromatin boundary elements. Mol Cell Biol 18:7478–7486

    Google Scholar 

  • Czermin B, Melfi R, McCabe D, Steitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185–196

    Google Scholar 

  • Ebert A, Schotta G, Lein S, Kubicek S, Krauss V, Jenuwein T, Reuter G (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18:2973–2983

    Google Scholar 

  • Eggert H, Gortchakov A, Saumweber H (2004) Identification of the Drosophila interband-specific protein Z4 as a DNA-binding zinc-finger protein determining chromosomal structure. J Cell Sci 117:4253–4264

    Google Scholar 

  • Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17:1870–1881

    Article  CAS  PubMed  Google Scholar 

  • Frasch M, Glover DM, Saumweber H (1986) Nuclear antigens follow different pathways into daughter nuclei during mitosis in early Drosophila embryos. J Cell Sci 82:155–172

    Google Scholar 

  • Gerber M, Ma J, Dean K, Eissenberg JC, Shilatifard A (2001) Drosophila ELL is associated with actively elongating RNA polymerasse II on transcriptionally active sites in vivo. EMBO J 20:6104–6114

    Google Scholar 

  • Hart CM, Zhao K, Laemmli UK (1997) The scs′ boundary element: characterization of boundary element-associated factors. Mol Cell Biol 17(2):999–1009

    Google Scholar 

  • Hoskins RA, Nelson CR, Berman BP, Laverty TR, George RA, Ciesiolka L, Naeemuddin M, Arenson AD, Durbin J, David RG, Tabor PE, Bailey MR, DeShazo DR, Catanese J, Mammoser A, Osoegawa K, de Jong PJ, Celniker SE, Gibbs RA, Rubin GM, Scherer SE (2000) A BAC-based physical map of the major autosomes of Drosophila melanogaster. Science 287:2271–2274

    Google Scholar 

  • Hovemann BT, Reim I, Werner S, Katz S, Saumweber H (2000) The protein Hrb57A of Drosophila melanogaster closely related to hnRNP K from vertebrates is present at sites active in transcription and coprecipitates with four RNA-binding proteins. Gene 245:127–137

    Google Scholar 

  • Igo-Kemenes T, Zachau HG (1978) Domains in chromatin structure. Cold Spring Harb Symp Quant Biol 42:109–118

    Google Scholar 

  • Ito K, Sass H, Urban J, Hofbauer A, Schneuwly S (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290:1–10

    Google Scholar 

  • Jin Y, Wang Y, Walker DL, Dong H, Conley C, Johansen J, Johansen KM (1999) JIL-1: a novel chromosomal tandem kinase implicated in transcriptional regulation in Drosophila. Mol Cell 4:129–135

    Google Scholar 

  • Jin Y, Wang Y, Johansen J, Johansen KM (2000) JIL-1, a chromosomal kinase implicated in the regulation of chromatin structure, associates with the male specific lethal (MSL) dosage compensation complex. J Cell Biol 149:1005–1010

    Google Scholar 

  • Kellum R, Schedl P (1991) A position-effect assay for boundaries of higher order chromosomal domains. Cell 64:941–950

    Google Scholar 

  • Kellum R, Schedl P (1992) A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol Cell Biol 12:2424–2431

    Google Scholar 

  • Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. Academic, San Diego

    Google Scholar 

  • Mohrmann L, Langenberg K, Krijgsveld J, Kal AJ, Heck AJ, Verrijzer CP (2004) Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes. Mol Cell Biol 24:3077–3088

    Google Scholar 

  • Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV, Laue ED (2002) Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416:403–407

    Google Scholar 

  • O’Connell PO, Rosbash M (1984) Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res 12:5495–5513

    Google Scholar 

  • Oh SW, Kingsley T, Shin HH, Zheng Z, Chen HW, Chen X, Wang H, Ruan P, Moody M, Hou SX (2003) A P-element insertion screen identified mutations in 455 novel essential genes in Drosophila. Genetics 163:195–201

    Google Scholar 

  • Paddy MR, Saumweber H, Agard DA, Sedat JW (1996) Time-resolved, in vivo studies of mitotic spindle formation and nuclear lamina breakdown in Drosophila early embryos. J Cell Sci 109:591–607

    Google Scholar 

  • Paro R, Hogness DS (1991) The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A 88:263–267

    Google Scholar 

  • Paulson JR, Laemmli UK (1977) The structure of histone-depleted metaphase chromosomes. Cell 12:817–828

    Google Scholar 

  • Plagens U, Greenleaf AL, Bautz EKF (1976) Distribution of RNA Polymerase on Drosophila polytene chromosomes studied by indirect immunofluorescence. Chromosoma 59:157–165

    Google Scholar 

  • Rath U, Wang D, Ding Y, Xu YZ, Qi H, Blacketer MJ, Girton J, Johansen J, Johansen K (2004) Chromator, a novel and essential chromodomain protein interacts directly with the putative spindle matrix protein Skeletor. J Cell Biochem 93(5):1033–1047

    Google Scholar 

  • Reim I, Mattow J, Saumweber H (1999) The RRM protein NonA from Drosophila forms a complex with the RRM proteins Hrb87F and S5 and the Zn finger protein PEP on hnRNA. Exp Cell Res 253:573–586

    Google Scholar 

  • Ringrose L, Ehret H, Paro R (2004) Distinct contributions of histone H3 Lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Mol Cell 16:641–653

    Google Scholar 

  • Roseman RR, Johnson EA, Rodesch CK, Bjerke M, Nagoshi RN, Geyer PK (1995) A P-element containing suppressor of hairy-wing binding regions has novel properties for mutagenesis in Drosophila melanogaster. Genetics 141:1061–1074

    Google Scholar 

  • Rubin GM, Yandell MD, Wortman JR, Gabor Miklos GL, Nelson CR, Hariharan IK, Fortini ME, Li PW, Apweiler R, Fleischmann W, Cherry JM, Henikoff S, Skupski MP, Misra S, Ashburner M, Birney E, Boguski MS, Brody T, Brokstein P, Celniker SE, Chervitz SA, Coates D, Cravchik A, Gabrielian A, Galle RF, Gelbart WM, George RA, Goldstein LS, Gong F, Guan P, Harris NL, Hay BA, Hoskins RA, Li J, Li Z, Hynes RO, Jones SJ, Kuehl PM, Lemaitre B, Littleton JT, Morrison DK, Mungall C, O’Farrell PH, Pickeral OK, Shue C, Vosshall LB, Zhang J, Zhao Q, Zheng XH, Lewis S (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215

    Article  CAS  PubMed  Google Scholar 

  • Rykowski MC, Parmelee SJ, Agard DA, Sedat JW (1988) Precise determination of the molecular limits of a polytene chromosome band: regulatory sequences for the Notch gene are in the interband. Cell 54:461–472

    Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NCT, Schreiber SL, Mellor JU, Kouzarides T (2002) Active genes are trimethylated at K4 of histone H3. Nature 419:407–411

    Google Scholar 

  • Sass H (1982) RNA polymerase B in polytene chromosomes: immunofluorescent and autoradiographic analysis during stimulated and repressed RNA synthesis. Cell 28:269–278

    Google Scholar 

  • Sass H, Bautz EKF (1982) Interbands of polytene chromosomes: binding sites and start points for RNA polymerase. Chromosoma 86:77–93

    Google Scholar 

  • Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H3-K20 trimethylation at constitutive heterochromatin. Genes Dev 18:1251–1262

    Google Scholar 

  • Semeshin VF, Zhimulev IF, Belyaeva ES (1979) Electron microscope autoradiographic study on transcriptional activity of Drosophila melanogaster polytene chromosomes. Chromosoma 73:163–177

    Google Scholar 

  • Smoller D, Friedel C, Schmid A, Bettler D, Lam L, Yedvobnick B (1990) The Drosophila neurogenic locus mastermind encodes a protein unusually rich in aminoacid homopolymers. Genes Dev 4:1688–1700

    Google Scholar 

  • The FlyBase Consortium (2003) The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res 31:172–175. (http://www.flybase.net/)

    Google Scholar 

  • Udvardy A, Maine E, Schedl P (1985) The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains. J Mol Biol 20:341–358

    Google Scholar 

  • Vazquez J, Schedl P (2000) Deletion of an insulator element by the mutation facet-strawberry in Drosophila melanogaster. Genetics 155:1297–1311

    Google Scholar 

  • Weeks JR, Hardin SE, Shen J, Lee JM, Greenleaf AL (1993) Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activity and transcript processing. Genes Dev 7:2329–2344

    Google Scholar 

  • Wilder EL, Perrimon N (1995) Dual functions of wingless in the Drosophila leg imaginal disc. Development 121:477–488

    Google Scholar 

  • Wodarz A, Hinz U, Engelbert M, Knust E (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82:67–76

    Article  CAS  PubMed  Google Scholar 

  • Zhao K, Hart CM, Laemmli UK (1995) Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81:879–889

    Google Scholar 

  • Zhimulev IF (1996) Morphology and structure of polytene chromosomes. Adv Genet 34:1–497

    Google Scholar 

  • Zhimulev IF, Belyaeva ES (1975) 3H-uridine labeling patterns in the Drososphila melanogaster salivary gland chromosomes X, 2R and 3L. Chromosoma 49:219–231

    Google Scholar 

Download references

Acknowledgements

The authors thank I. Passow and R. Gienapp for excellent technical assistance. We acknowledge the help of K. Matthews from Bloomington Stock Center for provision of fly stocks and A. Carpenter for her kind gift of the transposase donor stock. I.F.Z. and A.A.G. were supported by a short-term DAAD Scholarship, by Programs for Molecular and Cellular Biology 10.1 and N70/2004, Program for Scientific Schools 918.2003, and by a grant Frontiers in Genetics 2-04. H.E. and H.S. were supported by a grant from DFG Sa338/9-1 Schwerpunkt Epigenetics.

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

    A. A. Gortchakov & I. F. Zhimulev

  2. Cytogenetics Division, Institute of Biology, Humboldt University, Berlin, Germany

    H. Eggert, M. Gan & H. Saumweber

  3. Max Planck Institute for Infection Biology, Berlin, Germany

    J. Mattow

Authors
  1. A. A. Gortchakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Eggert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Mattow
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. F. Zhimulev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. Saumweber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. Saumweber.

Additional information

Communicated by H. Jäckle

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gortchakov, A.A., Eggert, H., Gan, M. et al. Chriz, a chromodomain protein specific for the interbands of Drosophila melanogaster polytene chromosomes. Chromosoma 114, 54–66 (2005). https://doi.org/10.1007/s00412-005-0339-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-005-0339-3

Keywords

Search

Navigation