Abstract
Interphase chromosomes form distinct spatial domains called chromosome territories (CTs). The position of CTs is known not to be at random and is related to chromosome size and gene density. To elucidate how CTs are arranged in primate proliferating fibroblasts and whether the radial position of CTs has been conserved during primate evolution, several specific CTs corresponding to conserved chromosomes since the Simiiformes (human 6, 12, 13, and 17 homologous CTs) have been studied in 3D preserved interphase nuclei from proliferant cells of two New World monkey species (Lagothrix lagothricha, Saimiri sciureus) and in human by three-dimensional fluorescent in situ hybridization (3D-FISH). Our results indicate that both gene-density and chromosome size influence chromosome territory arrangement in the nucleus. This influence is greater for chromosome-size than for gene-density in the three species studied. A comparison of the radial position of a given CT and its homolog in the species analyzed suggests similar CT distributions for homologous chromosomes. Our statistical analysis using the logit model shows that such homologous positionings cannot, however, be considered identical.
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References
Agresti A (2002) Categorical data analysis, 2nd edn. Wiley.
Aten JA, Stap J, Krawczyk PM, van Oven CH, Hoebe RA, Essers J, Kanaar R (2004) Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303:92–95
Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Müller S, Eils R, Cremer C, Speicher MR, Cremer T (2005) Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 3:e157
Boquest AC, Day BN, Prather RS (1999) Flow-cytometric cell analysis of cultured porcine fetal fibroblasts cells. Biol Reprod 60:1013–1019
Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet 10:211–219
Bridger JM, Boyle S, Kill IR, Bickmore WA (2000) Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr Biol 10(3):149–152
Cornforth MN, Greulich-Bode KM, Loucas BD, Arsuaga J, Vazquez M, Sachs RK, Bruckner M, Molls M, Hahnfeldt P, Hlatky L, Brenner DJ (2002) Chromosomes are predominantly located randomly with respect to each other in interphase human cells. J Cell Biol 159:237–244
Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2:292–301
Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E, Speicher MR, Mathieu U, Jauch A, Emmerich P et al (1993) Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harbor Symp Quant Biol 58:777–792
Cremer M, von Hase J, Volm T, Brero A, Kreth G, Walter J, Fischer C, Solovei I, Cremer C, Cremer T (2001) Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res 9:541–567
Cremer M, Kupper K, Wagler B, Wizelman L, von Hase J, Weiland Y, Kreja L, Diebold J, Speicher MR, Cremer T (2003) Inheritance of gene density-related higher order chromatin arrangements in normal and tumor cell nuclei. J Cell Biol 162:809–820
Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119–1131
Foster HA, Bridger JM (2005). The genome and the nucleus: a marriage made by evolution. Genome organisation and nuclear architecture. Chromosoma 114(4):212–229
Garcia M, Miró R, Estop A, Ponsà M, Egozcue J (1983) Constitutive heterochromatin polymorphism in Lagothrix lagothricha cana, Cebus apella, and Cebus capucinus. Am J Primatol 4:117–126
Garcia M, Borrell A, Mudry M, Egozcue J, Ponsà M (1995) Prometaphase karyotype and restriction-enzime banding in squirrel monkeys, Saimiri boliviensis boliviensis (Primates: Platyrrhini). J Mammal 76(2):497–503
Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I (2001) Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res 9:569–584
Kill IR, Faragher RGA, Lawrence K, Shall S (1994) The expression of proliferation-dependent antigens during the lifespan of normal and progeroid human fibroblasts in culture. J Cell Sci 107:571–579
Kozubek S, Lukasova E, Mareckova A, Skalnikova M, Kozubek M, Bartova E, Kroha V, Krahulcova E, Slotova J (1999) The topological organization of chromosomes 9 and 22 in cell nuclei has a determinative role in the induction of t(9,22) translocations and in the pathogenesis of t(9,22) leukemias. Chromosoma 108:426–435
Kozubek S, Lukasova E, Jirsova P, Koutna I, Kozubek M, Ganova A, Bartova E, Falk M, Pasekova R (2002) 3D Structure of the human genome: order in randomness. Chromosoma 111:321–331
Kreth G, Finsterle J, von Hase J, Cremer M, Cremer C (2004) Radial arrangement of chromosome territories in human cell nuclei: a computer model approach based on gene density indicates a probabilistic global positioning code. Biophys J 86(5):2803–2812
Lukasova E, Kozubek S, Kozubek M, Kjeronska J, Ryznar L, Horakova J, Krahulcova E, Horneck G (1997) Localisation and distance between ABL and BCR genes in interphase nuclei of bone marrow cells of control donors and patients with chronic myeloid leukaemia. Hum Genet 100:525–535
Mahy NL, Perry PE, Bickmore WA (2002) Gene density and transcription influence the localization of chromatin outside of chromosome territories detectable by FISH. J Cell Biol 159:753–763
Mayer R, Brero A, von Hase J, Schroeder T, Cremer T, Dietzel S (2005) Common themes and cell types specific variations of higher order chromatin arrangements in the mouse. BMC Cell Biol 6:44
Misteli T (2005) Concepts in nuclear architecture. Bioessays 27(5):477–487
Neves H, Ramos C, da Silva MG, Parreira A, Parreira L (1999) The nuclear topography of ABL, BCR, PML, and RAR genes: evidence for gene proximity in specific phases of the cell cycle and stages of hematopoietic differentiation. Blood 93:1197–1207
Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE (2000) Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290:138–141
Parada L, Misteli T (2002) Chromosome positioning in the interphase nucleus. Trends Cell Biol 12:425–432
Parada LA, Roix JJ, Misteli T (2003) An uncertainty principle in chromosome positioning. Trends Cell Biol 13:393–396
Parada LA, McQueen PG, Misteli T (2004) Tissue-specific spatial organization of genomes. Genome Biol 5(7):R44
Rens W, O’Brien PC, Graves JA, Ferguson-Smith MA (2003) Localization of chromosome regions in potoroo nuclei (Potorous tridactylus. Marsupialia: Potoroinae). Chromosoma 112:66–76
Roix JJ, McQueen PG, Munson PJ, Parada LA, Misteli T (2003) Spatial proximity of translocation-prone gene loci in human lymphomas. Nat Genet 34(3):287–291
Ruiz-Herrera A, Garcia F, Mora L, Egozcue J, Ponsa M, Garcia M (2005) Evolutionary conserved chromosomal segments in the human karyotype are bounded by unstable chromosome bands. Cytogenet Genome Res 108:161–174
Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, Cmarko D, Cremer C, Fakan S, Cremer T (2002) Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 276:10–23
Sun HB, Shen J, Yokota H (2000) Size-dependent positioning of human chromosomes in interphase nuclei. Biophys J 79:184–190
Tanabe H, Müller S, Neusser M, von Hase J, Calcagno E, Cremer M, Solovei I, Cremer C, Cremer T (2002a) Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci U S A 99:4424–4429
Tanabe H, Habermann FA, Solovei I, Cremer M, Cremer T (2002b) Non-random radial arrangements of interphase chromosome territories: evolutionary considerations and functional implications. Mutat Res 504:37–45
Tanabe H, Kupper K, Ishida T, Neusser M, Mizusawa H (2005) Inter- and intra-specific gene-density-correlated radial chromosome territory arrangements are conserved in Old World monkeys. Cytogenet Genome Res 108:255–261
Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J, Beck S, Campbell RD, Goldsworthy M, Powis SH, Ragoussis J, Trowsdale J, Sheer D (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113 (Pt 9):1565–1576
Acknowledgements
The authors would like to thank Dr. Miguel Martin for his help in the statistical discussion of the paper, Dr. S. Müller’s and Dr. S. Kozubek’s groups for the development of the methodology, Marta Farré for the karyotype control analysis, Dr. Marc Isamat for reviewing the English manuscript, the Servei de Microscòpia, the Servei de Citometria and Servei de Cultius of the Universitat Autònoma de Barcelona. Financial support was received from the Ministerio de Educación y Ciencia (BFU2004-03422) and from the Universitat Autònoma de Barcelona (grant to L. Mora).
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Communicated by T. Misteli
This paper is dedicated to the memory of Prof. Josep Egozcue, our enthusiast teacher and a good friend.
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Results of logit model. Association coefficients (ORs) between expressed situation odds (peripheral/central positions) and the basal one (PDF 65 kb)
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Mora, L., Sánchez, I., Garcia, M. et al. Chromosome territory positioning of conserved homologous chromosomes in different primate species. Chromosoma 115, 367–375 (2006). https://doi.org/10.1007/s00412-006-0064-6
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DOI: https://doi.org/10.1007/s00412-006-0064-6