The 3D positioning of ANT2 and ANT3 genes within female X chromosome territories correlates with gene activity

Experimental Cell Research

Volumn 252, Issue 2, 1999, Pages 363-375

  Dietzel, Steffen ^a   Schiebel, Katrin ^a   Little, Graham ^a   Edelmann, Peter ^a   Rappold, Gudrun A ^a   Eils, Roland ^a   Cremer, Christoph ^a   Cremer, Thomas ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

ANT genes; Chromosome structure; Chromosome territories; Confocal microscopy; Fluorescence in situ hybridization; Nuclear organization; X chromosome inactivation

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE;

ARTICLE; CONFOCAL LASER MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ACTIVITY; GENE INACTIVATION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THREE DIMENSIONAL IMAGING; X CHROMOSOME;

EID: 0033231484     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4635     Document Type: Article

References (67)

1. Barr M. L., Bertram E. G. A morphological distinction between neurons of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature. 163:1949;676-677.
2. Lyon M. F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 190:1961;372-373.
3. Grant S. G., Chapman V. M. Mechanism of X-chromosome regulation. Annu. Rev. Genet. 22:1988;199-233.
4. Clemson C. M., McNeil J. A., Willard H. F., Lawrence J. B. XIST RNA paints the inactive X chromosome at interphase: Evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132:1996;259-275.
5. Heard E., Clerc P., Avner P. X-chromosome inactivation in mammals. Annu. Rev. Genet. 31:1997;571-610.
6. Brown C. J., Ballabio A., Rupert J. L., Lafreniere R. G., Grompe M., Tonlorenzi R., Willard H. F. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature. 349:1991;38-44.
7. Borsani G., Tonlorenzi R., Simmler M. C., Dandolo L., Arnaud D., Capra V., Grompe M., Pizzuti A., Muzny D., Lawrence C. Characterization of a murine gene expressed from the inactive X chromosome. Nature. 351:1991;325-329.
8. Rastan S. X chromosome inactivation and the Xist gene. Curr. Opin. Genet. Dev. 4:1994;292-297.
9. Kay G. F., Barton S. C., Surani M. A., Rastan S. Imprinting and X chromosome counting mechanisms determine Xist expression in early mouse development. Cell. 77:1994;639-650.
10. Penny G. D., Kay G. F., Sheardown S. A., Rastan S., Brockdorff N. Requirement for Xist in X chromosome inactivation. Nature. 379:1996;131-137.
11. Brown C. J., Hendrich B. D., Rupert J. L., Lafreniere R. G., Xing Y., Lawrence J., Willard H. F. The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell. 71:1992;527-542.
12. Cremer T., Kurz A., Zirbel R., Dietzel S., Rinke B., Schröck E., Speicher M. R., Mathieu U., Jauch A., Emmerich P., Scherthan H., Ried T., Cremer C., Lichter P. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harb. Symp. Quant. Biol. 58:1993;777-792.
13. Lamond A. I., Earnshaw W. C. Structure and function in the nucleus. Science. 280:1998;547-553.
14. Lewin B. Genes V. 1994;Oxford Univ. Press, Oxford.
15. Eils R., Dietzel S., Bertin E., Schröck E., Speicher M. R., Ried T., Robert-Nicoud M., Cremer C., Cremer T. Three-dimensional reconstruction of painted human interphase chromosomes: Active and inactive X-chromosome territories have similar volumes but differ in shape and surface structure. J. Cell Biol. 135:1996;1427-1440.
16. Visser A. E., Eils R., Jauch A., Little G., Bakker P. J. M., Cremer T., Aten J. A. Spatial distributions of early and late replicating chromatin in interphase chromosome territories. Exp. Cell Res. 243:1998;398-407.
17. Schultheiss H. P., Klingenberg M. Immunoelectrophoretic characterization of the ADP/ATP carrier from heart, kidney and liver. Arch. Biochem. Biophys. 239:1985;273-279.
18. Schiebel K., Weiss B., Wöhrle D., Rappold G. A human pseudoautosomal gene, ADP/ATP translocase, escapes X-inactivation whereas a homologue on Xq is subject to X-inactivation. Nature Genet. 3:1993;82-87.
19. Slim R., Levilliers J., Lüdecke H. J., Claussen U., Nguyen V. C., Gough N. M., Horsthemke B., Petit C. A human pseudoautosomal gene encodes the ANT3 ADP/ATP translocase and escapes X-inactivation. Genomics. 16:1993;26-33.
20. Boggs B. A., Chinault A. C. Analysis of replication timing properties of human X-chromosomal loci by fluorescence in situ hybridization. Proc. Natl. Acad. Sci. USA. 91:1994;6083-6087.
21. Lunardi J., Attardi G. Differential regulation of expression of the multiple ADP/ATP translocase genes in human cells. J. Biol. Chem. 266:1991;16534-16540.
22. Stepien G., Torroni A., Chung A. B., Hodge J. A., Wallace D. C. Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. J. Biol. Chem. 267:1992;14592-14597.
23. Schiebel K., Mertz A., Winkelmann M., Nagaraja R., Rappold G. Localization of the adenine nucleotide translocase gene ANT2 to chromosome Xq24-q25 with tight linkage to DXS425. Genomics. 24:1994;605-606.
24. Bornfleth H., Sätzler K., Eils R., Cremer C. High precision distance measurements and volume-conserving segmentation of objects near and below the resolution limit in three-dimensional confocal fluorescence microscopy. J. Microsc. 189:1998;118-136.
25. Dietzel S., Eils R., Sätzler K., Bornfleth H., Jauch A., Cremer C., Cremer T. Evidence against a looped structure of the inactive human X-chromosome territory. Exp. Cell Res. 240:1998;187-196.
26. Ku D.-H., Kagan J., Chen S.-T., Chang C.-D., Baserga R., Wurzel J. The human fibroblast adenine translocator gene. J. Biol. Chem. 265:1990;16060-16063.
27. Cozens A.-L., Runswick M. J., Walker J. E. DNA sequence of two expressed nuclear genes for human mitochondrial ADP/ATP translocase. J. Mol. Biol. 206:1989;261-280.
28. Herrmann B. G., Barlow D. P., Lehrach H. A large inverted duplication allows homologous recombination between chromosomes heterozygous for the proximal t-complex inversion. Cell. 48:1987;813-825.
29. Dietzel S., Jauch A., Kienle D., Qu G., Holtgreve-Grez H., Eils R., Münkel C., Bittner M., Meltzer P., Trent J. M., Cremer T. Separate and variably shaped chromosome arm domains are disclosed by chromosome arm painting in human cell nuclei. Chromosome Res. 6:1998;25-33.
30. Toder R., Rappold G. A., Schiebel K., Schempp W. ANT3 and STS are autosomal in prosimian lemurs: Implication for the evolution of the pseudoautosomal region. Hum. Genet. 95:1995;22-28.
31. Ried K., Rao E., Schiebel K., Rappold G. A. Gene duplications as a recurrent theme in the evolution of the human pseudoautosomal region 1: Isolation of the gene ASMTL. Hum. Mol. Genet. 7:1998;1771-1778.
32. Lichter P., Cremer T. Chromosome analysis by non-isotopic in situ hybridization. Rooney D. E., Czepulkowski B. H. Human Cytogenetics - A Practical Approach. 1992;IRL Press, Oxford.
33. Johnson G. D., Nogueira Araujo G. M. A simple method of reducing the fading of immunofluorescence during microscopy. J. Immunol. Methods. 43:1981;349-350.
34. Konstantinides K., Rasure J. The Khoros software development environment for image and signal processing. IEEE Trans. Image Proc. 3:1994;243-252.
35. Eils R., Bertin E., Saracoglu K., Rinke B., Schröck E., Parazza F., Usson Y., Robert Nicoud M., Stelzer E. H., Chassery J. M., Cremer T., Cremer C. Application of confocal laser microscopy and three-dimensional Voronoi diagrams for volume and surface estimates of interphase chromosomes. J. Microsc. 177:1995;150-161.
36. Eils R., Saracoglu K., Münkel C., Imhoff J., Sätzler K., Bertin E., Dietzel S., Schröck E., Ried T., Cremer T., Cremer C. Three dimensional imaging approaches and Monte Carlo simulations: Development of tools to study the morphology and distribution of chromosome territories and subchromosomal targets in human cell nuclei. Zool. Stud. 34:1995;7-10.
37. Bischoff A., Albers J., Kharboush I., Stelzer E., Cremer T., Cremer C. Differences of size and shape of active and inactive X-chromosome domains in human amniotic fluid cell nuclei. Microsc. Res. Tech. 25:1993;68-77.
38. Rinke B., Bischoff A., Meffert M. C., Scharschmidt R., Hausmann M., Stelzer E. H. K., Cremer T., Cremer C. Volume ratios of painted chromosome territories 5, 7 and X in female human cell nuclei studied with confocal laser microscopy and the Cavalieri estimator. Bioimaging. 3:1995;1-11.
39. Young I. T. Proof without prejudice: use of the Kolmogorov-Smirnov test for the analysis of histograms from flow systems and other sources. J. Histochem. Cytochem. 25:1977;935-941.
40. Yen P. H., Patel P., Chinault A. C., Mohandas T., Shapiro L. J. Differential methylation of hypoxanthin phosphoribosyltransferase genes on active and inactive human X chromosomes. Proc. Natl. Acad. Sci. USA. 81:1984;1759-1763.
41. Keith D. H., Singer-Sam J. S., Riggs A. D. Active X chromosome DNA is unmethylated at eight CCGG sites clustered in a guanine-plus-cytosine-rich island at the 5′end of the gene for phosphoglycerate kinase. Mol. Cell Biol. 6:1986;4122-4125.
42. Toniolo D., Martini G., Migeon B. R., Dono R. Expression of the G6PD locus on the human X chromosome is associated with demethylation of three CpG islands within 100 kb of DNA. EMBO J. 7:1988;401-406.
43. Goodfellow P. J., Mondello C., Darling S. M., Pym B., Little P., Goodfellow P. N. Absence of methylation of a CpG-rich region at the 5′end of the MIC2 gene on the active X, the inactive X and the Y chromosome. Proc. Natl. Acad. Sci. USA. 85:1988;5605-5609.
44. Mondello C., Goodfellow P. J., Goodfellow P. N. Analysis of methylation of a human X located gene which escape X-inactivation. Nucleic Acids Res. 16:1988;6813-6824.
45. Spector D. L. Nuclear organization and gene expression. Exp. Cell Res. 229:1996;189-197.
46. Zirbel R. M., Mathieu U. R., Kurz A., Cremer T., Lichter P. Evidence for a nuclear compartment of transcription and splicing located at chromosome domain boundaries. Chromosome Res. 1:1993;93-106.
47. Xing Y. G., Johnson C. V., Moen P. T., McNeil J. A., Lawrence J. B. Nonrandom gene organization: Structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J. Cell Biol. 131:1995;1635-1647.
48. Smith K. P., Moen P. T., Wydner K. L., Coleman J. R., Lawrence J. B. Processing of endogenous pre-mRNAs in association with SC-35 domains is gene specific. J. Cell Biol. 144:1999;617-629.
49. Park P. C., De Boni U. A specific conformation of the territory of chromosome 17 locates ERBB-2 sequences to a DNase-hypersensitive domain at the nuclear periphery. Chromosoma. 107:1998;87-95.
50. Kurz A., Lampel S., Nickolenko J. E., Bradl J., Benner A., Zirbel R. M., Cremer T., Lichter P. Active and inactive genes localize preferentially in the periphery of chromosome territories. J. Cell Biol. 135:1996;1195-1205.
51. Abranches R., Beven A. F., Aragón-Alcaide L., Shaw P. J. Transcription sites are not correlated with chromosome territories in wheat nuclei. J. Cell Biol. 143:1998;5-12.
52. Berezney R., Ma H., Meng C. L., Samarabandu J., Cheng P. C. Connecting genomic architecture and DNA replication in three dimensions. Zool. Stud. 34:1995;29-32.
53. Ferreira J., Paolella G., Ramos C., Lamond A. I. Spatial organization of large-scale chromatin domains in the nucleus: A magnified view of single chromosome territories. J. Cell Biol. 139:1997;1597-1610.
54. Zink D., Cremer T., Saffrich R., Fischer R., Trendelenburg M. F., Ansorge W., Stelzer E. H. Structure and dynamics of human interphase chromosome territories in vivo. Hum. Genet. 102:1998;241-251.
55. Jackson D. A., Pombo A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140:1998;1285-1295.
56. Zink D., Bornfleth H., Visser A., Cremer C., Cremer T. Organization of early and late replicating DNA in human chromosome territories. Exp. Cell Res. 247:1999;176-188.
57. Cremer T., Dietzel S., Eils R., Lichter P., Cremer C. Chromosome territories, nuclear matrix filaments and interchromatin channels: A topological view on nuclear architecture and function. Brandham P. E., Bennett M. D. Kew Chromosome Conference IV. 1995;Royal Botanic Gardens, Kew.
58. Cremer C., Münkel C., Granzow M., Jauch A., Dietzel S., Eils R., Guan X.-Y., Meltzer P. S., Trent J. M., Langowski J., Cremer T. Nuclear architecture and the induction of chromosomal aberrations. Mutat. Res. 366:1996;97-116.
59. Zachar Z., Kramer J., Mims I. P., Bingham P. M. Evidence for channeled diffusion of pre-mRNAs during nuclear RNA transport in metazoans. J. Cell Biol. 121:1993;729-742.
60. Cmarko D., Verschure P. J., Martin T. E., Dahmus M. E., Krause S., Fu X. D., van Driel R., Fakan S. Ultrastructural analysis of transcription and splicing in the cell nucleus after bromo-UTP microinjection. Mol. Biol. Cell. 10:1999;211-223.
61. Hell S., Lindek S., Cremer C., Stelzer E. H. K. Measurement of the 4Pi-confocal point spread function proves 75 nm axial resolution. Appl. Phys. Lett. 64:1994;1335-1337.
62. Lindek S., Stelzer E. H. K. Confocal theta microscopy and a 4Pi-confocal theta microscope. Proc. SPIE. 2184:1994;188-194.
63. Robinett C. C., Straight A., Li G., Willhelm C., Sudlow G., Murray A., Belmont A. S. In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J. Cell Biol. 135:1996;1685-1700.
64. Buchenau P., Saumweber H., Arndt-Jovin D. J. The dynamic nuclear redistribution of an hnRNP K-homologous protein during Drosophila embryo development and heat shock: Flexibility of transcription sites in vivo. J. Cell Biol. 137:1997;291-303.
65. Marshall W. F., Straight A., Marko J. F., Swedlow J., Dernburg A., Belmont A., Murray A. W., Agard D. A., Sedat J. W. Interphase chromosomes undergo constrained diffusional motion in living cells. Curr. Biol. 7:1997;930-939.
66. Misteli T., Caceres J. F., Spector D. L. The dynamics of a pre-mRNA splicing factor in living cells. Nature. 387:1997;523-527.
67. Zink D., Cremer T. Cell nucleus: Chromosome dynamics in nuclei of living cells. Curr. Biol. 8:1998;R321-324.