Evidence for a Relatively Random Array of Human Chromosomes on the Mitotic Ring

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1999 Apr 6

PMID 10189364

Citations 19

Authors

D C Allison

A L Nestor

Affiliations

Soon will be listed here.

Abstract

We used fluorescence in situ hybridization (FISH) to study the positions of human chromosomes on the mitotic rings of cultured human lymphocytes, MRC-5 fibroblasts, and CCD-34Lu fibroblasts. The homologous chromosomes of all three cell types had relatively random positions with respect to each other on the mitotic rings of prometaphase rosettes and anaphase cells. Also, the positions of the X and Y chromosomes, colocalized with the somatic homologues in male cells, were highly variable from one mitotic ring to another. Although random chromosomal positions were found in different pairs of CCD-34Lu and MRC-5 late-anaphases, the separations between the same homologous chromosomes in paired late-anaphase and telophase chromosomal masses were highly correlated. Thus, although some loose spatial associations of chromosomes secondary to interphase positioning may exist on the mitotic rings of some cells, a fixed order of human chromosomes and/or a rigorous separation of homologous chromosomes on the mitotic ring are not necessary for normal mitosis. Furthermore, the relative chromosomal positions on each individual metaphase plate are most likely carried through anaphase into telophase.

Citing Articles

Mitotic Antipairing of Homologous Chromosomes.

Hua L, Casas C, Mikawa T Results Probl Cell Differ. 2022; 70:191-220.

PMID: 36348108 PMC: 9731508. DOI: 10.1007/978-3-031-06573-6_6.

Plant 3D Chromatin Organization: Important Insights from Chromosome Conformation Capture Analyses of the Last 10 Years.

Zhang X, Wang T Plant Cell Physiol. 2021; 62(11):1648-1661.

PMID: 34486654 PMC: 8664644. DOI: 10.1093/pcp/pcab134.

Ultra-Structural Imaging Provides 3D Organization of 46 Chromosomes of a Human Lymphocyte Prophase Nucleus.

Sajid A, Lalani E, Chen B, Hashimoto T, Griffin D, Bhartiya A Int J Mol Sci. 2021; 22(11).

PMID: 34206020 PMC: 8198510. DOI: 10.3390/ijms22115987.

Impaired CENP-E Function Renders Large Chromosomes More Vulnerable to Congression Failure.

Tovini L, McClelland S Biomolecules. 2019; 9(2).

PMID: 30691136 PMC: 6406671. DOI: 10.3390/biom9020044.

Mitotic antipairing of homologous and sex chromosomes via spatial restriction of two haploid sets.

Hua L, Mikawa T Proc Natl Acad Sci U S A. 2018; 115(52):E12235-E12244.

PMID: 30530674 PMC: 6310853. DOI: 10.1073/pnas.1809583115.

References

Feldman M, Mello-Sampayo T, SEARS E . Somatic association in Triticum aestivum. Proc Natl Acad Sci U S A. 1966; 56(4):1192-9. PMC: 220038. DOI: 10.1073/pnas.56.4.1192. View

Barr M, BERTRAM E . A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature. 1949; 163(4148):676. DOI: 10.1038/163676a0. View

Juricek D . Non-random chromosome distribution in radial metaphases from the chinese hamster. I. Uncultured cells. Chromosoma. 1975; 50(3):313-26. DOI: 10.1007/BF00283474. View

Hens L . Chromosome distribution in a23 Chinese hamster fibroblasts. Chromosoma. 1976; 57(3):205-17. DOI: 10.1007/BF00295207. View

Korf B, DIACUMAKOS E . Random arrangement of mitotic chromosomes in radial metaphases of the Indian muntjac. Cytogenet Cell Genet. 1977; 19(6):335-43. DOI: 10.1159/000130827. View

Zorn C, Cremer C, Cremer T, Zimmer J . Unscheduled DNA synthesis after partial UV irradiation of the cell nucleus. Distribution in interphase and metaphase. Exp Cell Res. 1979; 124(1):111-9. DOI: 10.1016/0014-4827(79)90261-1. View

Korf B, DIACUMAKOS E . Absence of true interchromosomal connectives in microsurgically isolated chromosomes. Exp Cell Res. 1980; 130(2):377-85. DOI: 10.1016/0014-4827(80)90015-4. View

Vogel F, Kruger J . Is there a general relationship between estimated chromosome distances in interphase and location of genes with related functions?. Hum Genet. 1983; 63(4):362-8. DOI: 10.1007/BF00274763. View

Manuelidis L . Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences. Proc Natl Acad Sci U S A. 1984; 81(10):3123-7. PMC: 345233. DOI: 10.1073/pnas.81.10.3123. View

10.

Heslop-Harrison J, Bennett M . Chromosome order--possible implications for development. J Embryol Exp Morphol. 1984; 83 Suppl:51-73. View

11.

Hubert J, Bourgeois C . The nuclear skeleton and the spatial arrangement of chromosomes in the interphase nucleus of vertebrate somatic cells. Hum Genet. 1986; 74(1):1-15. DOI: 10.1007/BF00278778. View

12.

Borden J, Manuelidis L . Movement of the X chromosome in epilepsy. Science. 1988; 242(4886):1687-91. DOI: 10.1126/science.3201257. View

13.

Chaly N, Brown D . The prometaphase configuration and chromosome order in early mitosis. J Cell Sci. 1988; 91 ( Pt 3):325-35. DOI: 10.1242/jcs.91.3.325. View

14.

Hiraoka Y, Agard D, Sedat J . Temporal and spatial coordination of chromosome movement, spindle formation, and nuclear envelope breakdown during prometaphase in Drosophila melanogaster embryos. J Cell Biol. 1990; 111(6 Pt 2):2815-28. PMC: 2116368. DOI: 10.1083/jcb.111.6.2815. View

15.

Holowacz T, De Boni U . Arrangement of kinetochore proteins and satellite DNA in neuronal interphase nuclei: changes induced by gamma-aminobutyric acid (GABA). Exp Cell Res. 1991; 197(1):36-42. DOI: 10.1016/0014-4827(91)90476-b. View

16.

Ferguson M, Ward D . Cell cycle dependent chromosomal movement in pre-mitotic human T-lymphocyte nuclei. Chromosoma. 1992; 101(9):557-65. DOI: 10.1007/BF00660315. View

17.

Park P, De Boni U . Spatial rearrangement and enhanced clustering of kinetochores in interphase nuclei of dorsal root ganglion neurons in vitro: association with nucleolar fusion. Exp Cell Res. 1992; 203(1):222-9. DOI: 10.1016/0014-4827(92)90058-g. View

18.

Hiraoka Y, Dernburg A, Parmelee S, Rykowski M, Agard D, Sedat J . The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J Cell Biol. 1993; 120(3):591-600. PMC: 2119536. DOI: 10.1083/jcb.120.3.591. View

19.

Spector D . Macromolecular domains within the cell nucleus. Annu Rev Cell Biol. 1993; 9:265-315. DOI: 10.1146/annurev.cb.09.110193.001405. View

20.

Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E . Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harb Symp Quant Biol. 1993; 58:777-92. DOI: 10.1101/sqb.1993.058.01.085. View