Chromosoma

, Volume 114, Issue 1, pp 54–66 | Cite as

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

  • A. A. Gortchakov
  • H. Eggert
  • M. Gan
  • J. Mattow
  • I. F. Zhimulev
  • H. Saumweber
Research Article

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.

References

  1. Akhtar A (2003) Dosage compensation: an intertwined world of RNA and chromatin remodelling. Curr Opin Genet Dev 13:161–169Google Scholar
  2. Akhtar A, Zink D, Becker PB (2000) Chromodomains are protein–RNA interaction modules. Nature 407:405–409Google Scholar
  3. 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 25:3389–3402PubMedGoogle Scholar
  4. 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 297:2270–2275Google Scholar
  5. 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 21:5245–5254Google Scholar
  6. 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 1–33Google Scholar
  7. 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 167:761–781CrossRefPubMedGoogle Scholar
  8. Benyajati C, Worcel A (1976) Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster. Cell 9:393–407Google Scholar
  9. 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 3:1273–1287PubMedGoogle Scholar
  10. 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 21:2430–2440Google Scholar
  11. Brand AH, Perrimon N (1993) Target gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415PubMedGoogle Scholar
  12. 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 100:11535–11540Google Scholar
  13. 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 5–26Google Scholar
  14. 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 130:271–284Google Scholar
  15. 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 124:4661–4671Google Scholar
  16. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16(22):10881–10890PubMedGoogle Scholar
  17. Cuvier O, Hart CM, Laemmli UK (1998) Identification of a class of chromatin boundary elements. Mol Cell Biol 18:7478–7486Google Scholar
  18. 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 111:185–196Google Scholar
  19. 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 18:2973–2983Google Scholar
  20. 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 117:4253–4264Google Scholar
  21. 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 17:1870–1881CrossRefPubMedGoogle Scholar
  22. Frasch M, Glover DM, Saumweber H (1986) Nuclear antigens follow different pathways into daughter nuclei during mitosis in early Drosophila embryos. J Cell Sci 82:155–172Google Scholar
  23. 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 20:6104–6114Google Scholar
  24. Hart CM, Zhao K, Laemmli UK (1997) The scs′ boundary element: characterization of boundary element-associated factors. Mol Cell Biol 17(2):999–1009Google Scholar
  25. 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 287:2271–2274Google Scholar
  26. 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 245:127–137Google Scholar
  27. Igo-Kemenes T, Zachau HG (1978) Domains in chromatin structure. Cold Spring Harb Symp Quant Biol 42:109–118Google Scholar
  28. 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 290:1–10Google Scholar
  29. 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 4:129–135Google Scholar
  30. 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 149:1005–1010Google Scholar
  31. Kellum R, Schedl P (1991) A position-effect assay for boundaries of higher order chromosomal domains. Cell 64:941–950Google Scholar
  32. Kellum R, Schedl P (1992) A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol Cell Biol 12:2424–2431Google Scholar
  33. Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. Academic, San DiegoGoogle Scholar
  34. 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 24:3077–3088Google Scholar
  35. 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 416:403–407Google Scholar
  36. O’Connell PO, Rosbash M (1984) Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res 12:5495–5513Google Scholar
  37. 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 163:195–201Google Scholar
  38. 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 109:591–607Google Scholar
  39. 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 88:263–267Google Scholar
  40. Paulson JR, Laemmli UK (1977) The structure of histone-depleted metaphase chromosomes. Cell 12:817–828Google Scholar
  41. Plagens U, Greenleaf AL, Bautz EKF (1976) Distribution of RNA Polymerase on Drosophila polytene chromosomes studied by indirect immunofluorescence. Chromosoma 59:157–165Google Scholar
  42. 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):1033–1047Google Scholar
  43. 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 253:573–586Google Scholar
  44. 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 16:641–653Google Scholar
  45. 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 141:1061–1074Google Scholar
  46. 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 287:2204–2215CrossRefPubMedGoogle Scholar
  47. 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 54:461–472Google Scholar
  48. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  49. 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 419:407–411Google Scholar
  50. Sass H (1982) RNA polymerase B in polytene chromosomes: immunofluorescent and autoradiographic analysis during stimulated and repressed RNA synthesis. Cell 28:269–278Google Scholar
  51. Sass H, Bautz EKF (1982) Interbands of polytene chromosomes: binding sites and start points for RNA polymerase. Chromosoma 86:77–93Google Scholar
  52. 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 18:1251–1262Google Scholar
  53. Semeshin VF, Zhimulev IF, Belyaeva ES (1979) Electron microscope autoradiographic study on transcriptional activity of Drosophila melanogaster polytene chromosomes. Chromosoma 73:163–177Google Scholar
  54. 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 4:1688–1700Google Scholar
  55. 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
  56. 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 20:341–358Google Scholar
  57. Vazquez J, Schedl P (2000) Deletion of an insulator element by the mutation facet-strawberry in Drosophila melanogaster. Genetics 155:1297–1311Google Scholar
  58. 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 7:2329–2344Google Scholar
  59. Wilder EL, Perrimon N (1995) Dual functions of wingless in the Drosophila leg imaginal disc. Development 121:477–488Google Scholar
  60. 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 82:67–76CrossRefPubMedGoogle Scholar
  61. Zhao K, Hart CM, Laemmli UK (1995) Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81:879–889Google Scholar
  62. Zhimulev IF (1996) Morphology and structure of polytene chromosomes. Adv Genet 34:1–497Google Scholar
  63. Zhimulev IF, Belyaeva ES (1975) 3H-uridine labeling patterns in the Drososphila melanogaster salivary gland chromosomes X, 2R and 3L. Chromosoma 49:219–231Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • A. A. Gortchakov
    • 1
  • H. Eggert
    • 2
  • M. Gan
    • 2
  • J. Mattow
    • 3
  • I. F. Zhimulev
    • 1
  • H. Saumweber
    • 2
  1. 1.Institute of Cytology and GeneticsSiberian Branch of Russian Academy of SciencesNovosibirskRussia
  2. 2.Cytogenetics Division, Institute of BiologyHumboldt UniversityBerlinGermany
  3. 3.Max Planck Institute for Infection BiologyBerlinGermany

Personalised recommendations