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Molecular and Cellular Biology, April 2006, p. 2637-2647, Vol. 26, No. 7
0270-7306/06/$08.00+0     doi:10.1128/MCB.26.7.2637-2647.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Alternative ESC and ESC-Like Subunits of a Polycomb Group Histone Methyltransferase Complex Are Differentially Deployed during Drosophila Development

Liangjun Wang,1 Neal Jahren,2 Marcus L. Vargas,2 Erica F. Andersen,2 Judith Benes,1 Junyu Zhang,1 Ellen L. Miller,2 Richard S. Jones,1* and Jeffrey A. Simon2*

Department of Biological Sciences, Southern Methodist University, Dallas, Texas 75275,1 Department of Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, Minnesota 554552

Received 15 November 2005/ Returned for modification 13 December 2005/ Accepted 24 December 2005

The Extra sex combs (ESC) protein is a Polycomb group (PcG) repressor that is a key noncatalytic subunit in the ESC-Enhancer of zeste [E(Z)] histone methyltransferase complex. Survival of esc homozygotes to adulthood based solely on maternal product and peak ESC expression during embryonic stages indicate that ESC is most critical during early development. In contrast, two other PcG repressors in the same complex, E(Z) and Suppressor of zeste-12 [SU(Z)12], are required throughout development for viability and Hox gene repression. Here we describe a novel fly PcG repressor, called ESC-Like (ESCL), whose biochemical, molecular, and genetic properties can explain the long-standing paradox of ESC dispensability during postembryonic times. Developmental Western blots show that ESCL, which is 60% identical to ESC, is expressed with peak abundance during postembryonic stages. Recombinant complexes containing ESCL in place of ESC can methylate histone H3 with activity levels, and lysine specificity for K27, similar to that of the ESC-containing complex. Coimmunoprecipitations show that ESCL associates with E(Z) in postembryonic cells and chromatin immunoprecipitations show that ESCL tracks closely with E(Z) on Ubx regulatory DNA in wing discs. Furthermore, reduced escl+ dosage enhances esc loss-of-function phenotypes and double RNA interference knockdown of ESC/ESCL in wing disc-derived cells causes Ubx derepression. These results suggest that ESCL and ESC have similar functions in E(Z) methyltransferase complexes but are differentially deployed as development proceeds.

* Corresponding author. Mailing address for Jeffrey A. Simon: 321 Church St. SE, Minneapolis, MN 55455. Phone: (612) 626-5097. Fax: (612) 626-6140. E-mail: simon{at}cbs.umn.edu. Mailing address for Richard S. Jones: 6501 Airline, Dallas, TX 75275. Phone: (214) 768-3810. Fax: (214) 768-3955. E-mail: rjones{at}mail.smu.edu.

Molecular and Cellular Biology, April 2006, p. 2637-2647, Vol. 26, No. 7
0022-538X/06/$08.00+0     doi:10.1128/MCB.26.7.2637-2647.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Emmons, R. B., Genetti, H., Filandrinos, S., Lokere, J., Wu, C.-t. (2009). Molecular Genetic Analysis of Suppressor 2 of zeste Identifies Key Functional Domains. Genetics 182: 999-1013 [Abstract] [Full Text]  
  • Lo, S. M., Ahuja, N. K., Francis, N. J. (2009). Polycomb Group Protein Suppressor 2 of Zeste Is a Functional Homolog of Posterior Sex Combs. Mol. Cell. Biol. 29: 515-525 [Abstract] [Full Text]  
  • de Ayala Alonso, A. G., Gutierrez, L., Fritsch, C., Papp, B., Beuchle, D., Muller, J. (2007). A Genetic Screen Identifies Novel Polycomb Group Genes in Drosophila. Genetics 176: 2099-2108 [Abstract] [Full Text]  
  • Tie, F., Stratton, C. A., Kurzhals, R. L., Harte, P. J. (2007). The N Terminus of Drosophila ESC Binds Directly to Histone H3 and Is Required for E(Z)-Dependent Trimethylation of H3 Lysine 27. Mol. Cell. Biol. 27: 2014-2026 [Abstract] [Full Text]  


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