Journal of Cell Science, Vol 111, Issue 18 2753-2761, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

Dynamics of the sub-nuclear distribution of Modulo and the regulation of position-effect variegation by nucleolus in Drosophila

L Perrin, O Demakova, L Fanti, S Kallenbach, S Saingery, NI Mal'ceva, S Pimpinelli, I Zhimulev and J Pradel
Laboratoire de Genetique et de Physiologie du Developpement, Institut de Biologie du Developpement de Marseille, CNRS/INSERM/Universite de la Mediterranee/AP de Marseille, Campus de Luminy Case 907. 13288 Marseille cedex 9, France.

modulo belongs to the class of Drosophila genes named 'suppressor of position-effect variegation', suggesting the involvement of the encoded protein in chromatin compaction/relaxation processes. Using complementary procedures of cell fractionation, immunolocalisation on mitotic and polytene chromosomes and cross-linking/immunoprecipitation of genomic DNA targets, we have analysed the sub-nuclear distribution of Modulo. While actually associated to condensed chromatin and heterochromatin sites, the protein is also abundantly found at nucleolus. From a comparison of Modulo pattern on chromosomes of different cell types and mutant lines, we propose a model in which the nucleolus balances the Modulo protein available for chromatin compaction and PEV modification. At a molecular level, repetitive elements instead of rDNA constitute Modulo DNA targets, indicating that the protein directly contacts DNA in heterochromatin but not at the nucleolus. Consistent with a role for Modulo in nucleolus activity and protein synthesis capacity, somatic clones homozygous for a null mutation express a cell-autonomous phenotype consisting of growth alteration and short slender bristles, characteristic traits of Minute mutations, which are known to affect ribosome biogenesis. The results provide evidence suggesting that Modulo participates in distinct molecular networks in the nucleolus and heterochromatin and has distinct functions in the two compartments.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				S. Paredes and K. A. Maggert Ribosomal DNA contributes to global chromatin regulation PNAS, October 20, 2009; 106(42): 17829 - 17834. [Abstract] [Full Text] [PDF]

				S. Paredes and K. A. Maggert Expression of I-CreI Endonuclease Generates Deletions Within the rDNA of Drosophila Genetics, April 1, 2009; 181(4): 1661 - 1671. [Abstract] [Full Text] [PDF]

				Z. Cui and P. J. DiMario RNAi Knockdown of Nopp140 Induces Minute-like Phenotypes in Drosophila Mol. Biol. Cell, June 1, 2007; 18(6): 2179 - 2191. [Abstract] [Full Text] [PDF]

				L. M. Mikhaylova, A. M. Boutanaev, and D. I. Nurminsky Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line PNAS, August 8, 2006; 103(32): 11975 - 11980. [Abstract] [Full Text] [PDF]

				M. K. Sjoberg, E. Shestakova, Z. Mansuroglu, R. B. Maccioni, and E. Bonnefoy Tau protein binds to pericentromeric DNA: a putative role for nuclear tau in nucleolar organization J. Cell Sci., May 15, 2006; 119(10): 2025 - 2034. [Abstract] [Full Text] [PDF]

				F. Bantignies, R. H. Goodman, and S. M. Smolik The interaction between the coactivator dCBP and Modulo, a chromatin-associated factor, affects segmentation and melanotic tumor formation in Drosophila PNAS, February 14, 2002; (2002) 52509799. [Abstract] [Full Text] [PDF]

				S. Kuhfittig, J. Szabad, G. Schotta, J. Hoffmann, E. Máthé, and G. Reuter pitkinD, a Novel Gain-of-Function Enhancer of Position-Effect Variegation, Affects Chromatin Regulation During Oogenesis and Early Embryogenesis in Drosophila Genetics, March 1, 2001; 157(3): 1227 - 1244. [Abstract] [Full Text]

				G. Roman, J. He, and R. L. Davis kurtz, a Novel Nonvisual Arrestin, Is an Essential Neural Gene in Drosophila Genetics, July 1, 2000; 155(3): 1281 - 1295. [Abstract] [Full Text]

				F. Vernì, R. Gandhi, M. L. Goldberg, and M. Gatti Genetic and Molecular Analysis of wings apart-like (wapl), a Gene Controlling Heterochromatin Organization in Drosophila melanogaster Genetics, April 1, 2000; 154(4): 1693 - 1710. [Abstract] [Full Text]

				Z. Huang, B. Philippin, E. O'Leary, J. V. Bonventre, W. Kriz, and R. Witzgall Expression of the Transcriptional Repressor Protein Kid-1 Leads to the Disintegration of the Nucleolus J. Biol. Chem., March 19, 1999; 274(12): 7640 - 7648. [Abstract] [Full Text] [PDF]

				L. Perrin, P. Romby, P. Laurenti, H. Berenger, S. Kallenbach, H.-M. Bourbon, and J. Pradel The Drosophila Modifier of Variegation modulo Gene Product Binds Specific RNA Sequences at the Nucleolus and Interacts with DNA and Chromatin in a Phosphorylation-dependent Manner J. Biol. Chem., March 5, 1999; 274(10): 6315 - 6323. [Abstract] [Full Text] [PDF]

				F. Bantignies, R. H. Goodman, and S. M. Smolik The interaction between the coactivator dCBP and Modulo, a chromatin-associated factor, affects segmentation and melanotic tumor formation in Drosophila PNAS, March 5, 2002; 99(5): 2895 - 2900. [Abstract] [Full Text] [PDF]