Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster.

Abstract

Abstract. Using a computer-based system for model building and analysis, three-dimensional models of 24Drosophila melanogaster salivary gland nuclei have been constructed from optically or physically sectioned glands, allowing several generalizations about chromosome folding and packaging in these nuclei. First and most surprising, the prominent coiling of the chromosomes is strongly chiral, with fight-handed gyres predominating. Second, high frequency appositions between certain loci and the nuclear envelope appear almost exclusively at positions of intercalary heterochromatin; in addition, the chromocenter is always apposed to the envelope. Third, chromosomes are invariably separated into mutually exclusive spatial domains while usually extending across the nucleus in a polarized (Rabl) orientation. Fourth, the arms of each autosome are almost always juxtaposed, but no other relative arm positions are strongly favored. Finally, despite these nonrandom structural features, each chromosome is found to fold into a wide variety of different configurations. In addition, a set of nuclei has been analyzed in which the normally aggregrated centromeric regions of the chromosomes are located far apart from one another. These nuclei have the same architectural motifs seen in normal nuclei. This implies that such characteristics as separate chromosome domains and specific chromosomenuclear envelope contacts are largely independent of the relative placement of the different chromosomes within the nucleus.E UKARYOTIC cells contain enormous lengths of DNA that must undergo considerable packing to fit inside the interphase nucleus. The packing is accomplished through multiple foldings of the DNA molecule within each chromosome and the folding of the chromosomes themselves inside the nucleus. This hierarchy of foldings is under several general constraints. First, the DNA must be available to regulatory factors and transcriptional machinery in such a way that readout of the genome can be precisely controlled. Second, the resident copies of DNA must be faithfully duplicated and repackaged with histones and other proteins; in dividing cells, the daughter helices must also be topologically resolved. Finally, nuclear division depends on a number of tightly orchestrated events: condensation of chromatin into compact chromosomes, dissolution of the nuclear envelope, movement of chromosomes to a central plate with subsequent splitting of daughter chromatids toward opposite poles, decondensation of daughter chromosomes, and reassembly of the nuclear envelope around them.Despite the interest in elucidating the means by which cells accommodate these constraints and package their genomes, only a meager sketch of higher order structures can currently be claimed. Beyond the level of the 10-nm nucleosomal fiber, little.consensus has been reached. This is particularly true of the highest level of chromosome organization, the threedimensional arrangement of chromosomes in the interphase nucleus. For reviews, see references 13 and 21.The giant ...

Human telomeres are attached to the nuclear matrix.

“…locates telomeric loci near the surface of mammalian interphase nuclei (van Dekken et al, 1989). These and similar observations in other systems suggest that the ends of eukaryotic chromosomes are located close to the nuclear envelope (Agard and Sedat, 1983;Mathog et al, 1984;Foe and Alberts, 1985;Hochstrasser et al, 1986;Mathog and Sedat, 1989;Chung et al, 1990;Rawlins et al, 1991). This positioning throughout interphase in organisms as diverse as flies, trypanosomes, plants and mammals is likely to be a consequence of specific anchorage of telomeric DNA at the nuclear periphery.…”

“…Rabl (1885) (Sperling and Ludtke, 1981;Cremer et al, 1982;Foe and Alberts, 1985). Furthermore, direct analysis of chromosome topography by three-dimensional microscopy indicates that the ends of interphase chromosomes are close to the nuclear envelope in a wide variety of eukaryotes (Agard and Sedat, 1983;Mathog et al, 1984;Hochstrasser et al, 1986;Mathog and Sedat, 1989;van Dekken et al, 1989;Chung et al, 1990;Rawlins et al, 1991). These cytological data suggest that telomeres could be attached to the nuclear envelope.…”

Three distinct chromatin domains in telomere ends of polytene chromosomes inDrosophila melanogaster Telmutants

“…They compensate for incomplete DNA replication and contribute to the stability of chromosomes and karyotype (Muller, 1932;Pardue and Debaryshe, 1999;Biessmann and Mason, 2003). Telomeres also participate in nuclear architecture maintenance, and are known to associate with nuclear lamina (Hochstrasser et al, 1986;Marshall et al, 1996;Hari et al, 2001) or with nuclear matrix (de Lange, 1992;Luderus et al, 1996). However, the factors that underlie these phenomena, as well as the mechanisms of telomere functioning, remain poorly understood in Drosophila melanogaster.…”

Developing bioimaging and quantitative methods to study 3D genome

“…It is first described in nuclei of salamander larvae by Karl Rabl [16]. Rabl-like configuration also exists in other eukaryotic cells, such as Sacharomyces cerevisae [17], in the embryonic cells of Ascaris [18], in Drosophila melanogaster [19], in spermatocytes of the mosquito Aedes aegypti [20], fibroblasts of the treeshrew (Tupaia belangeri), the lymphocytes of the Indian muntjac, Chinese hamster fibroblasts [21], and some plants [22]. However, it was reported that chromosome alignment in Rabl configuration might not be important to control gene expression [23].…”