Abstract
Chromosomal rearrangements in humans are largely related to pathological conditions, and phenotypic effects are also linked to alterations in the expression profile following nuclear relocation of genes between functionally different compartments, generally occupying the periphery or the inner part of the cell nuclei. On the other hand, during evolution, chromosomal rearrangements may occur apparently without damaging phenotypic effects and are visible in currently phylogenetically related species. To increase our insight into chromosomal reorganisation in the cell nucleus, we analysed 18 chromosomal regions endowed with different genomic properties in cell lines derived from eight primate species covering the entire evolutionary tree. We show that homologous loci, in spite of their evolutionary relocation along the chromosomes, generally remain localised to the same functional compartment of the cell nuclei. We conclude that evolutionarily successful chromosomal rearrangements are those that leave the nuclear position of the regions involved unchanged. On the contrary, in pathological situations, the effect typically observed is on gene structure alteration or gene nuclear reposition. Moreover, our data indicate that new centromere formation could potentially occur everywhere in the chromosomes, but only those emerging in very GC-poor/gene-poor regions, generally located in the nuclear periphery, have a high probability of being retained through evolution. This suggests that, in the cell nucleus of related species, evolutionary chromosomal reshufflings or new centromere formation does not alter the functionality of the regions involved or the interactions between different loci, thus preserving the expression pattern of orthologous genes.
Similar content being viewed by others
Abbreviations
- 3C:
-
Chromosome conformation capture
- 4C:
-
Chromosome conformation capture-on-chip
- 5C:
-
Chromosome conformation capture carbon copy
- AC:
-
Ancestral centromere
- BAC:
-
Bacterial artificial chromosome
- Cae :
-
Cercopithecus aethiops
- Cja :
-
Callithrix jacchus
- Cmo :
-
Callicebus moloch
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- ENC:
-
Evolutionary new centromere
- FISH:
-
Fluorescence in situ hybridisation
- Ggo :
-
Gorilla gorilla
- HCN:
-
Human constitutional new centromeres
- Hi-C:
-
High-throughput chromosome capture
- Hsa :
-
Homo sapiens
- LAD:
-
Lamina associated domain
- Lca :
-
Lemur catta
- Mmu :
-
Macaca mulatta
- PHA:
-
Phytohaemagglutinin
- Ptr :
-
Pan troglodytes
- RNL:
-
Radial nuclear location
- SSC:
-
Saline sodium citrate buffer
- TAD:
-
Topologically associated domain
References
Amor DJ, Choo KH (2002) Neocentromeres: role in human disease, evolution, and centromere study. Am J Hum Genet 71:695–714
Ballabio E, Cantarella CD, Federico C, Di Mare P, Hall G et al (2009) Ectopic expression of the HLXB9 gene is associated with an altered nuclear position in t(7;12) leukaemias. Leukemia 23:1179–1182
Bernà L, Chaurasia A, Angelini C, Federico C, Saccone S et al (2012) The footprint of metabolism in the organization of mammalian genomes. BMC Genomics 13:174–186
Bernardi G (2015) Chromosome architecture and genome organization. PLoS One 10(11):e0143739. doi:10.1371/journal.pone.0143739
Bickmore WA, van der Maarel SM (2003) Perturbations of chromatin structure in human genetic disease: recent advances. Hum Mol Genet 12:207–213
Bickmore WA, van Steensel B (2013) Genome architecture: domain organization of interphase chromosomes. Cell 152:1270–1284
Bridger JM, Boyle S, Kill IR, Bickmore WA (2000) Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr Biol 10:149–152
Costantini M, Clay O, Federico C, Saccone S, Auletta F et al (2007) Human chromosomal bands: nested structure, high definition map and molecular basis. Chromosoma 116:36–49
Cremer T, Cremer M, Hübner B, Strickfaden H, Smeets D et al (2015) The 4D nucleome: evidence for a dynamic nuclear landscape based on co-aligned active and inactive nuclear compartments. FEBS Lett 589(20 Pt A):2931–2943
Croft JA, Bridger JM, Boyle S, Perry P, Teague P et al (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119–1131
Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295:1306–1311
Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL et al (2006) Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res 6:1299–1309
Eder V, Ventura M, Ianigro M, Teti M, Rocchi M et al (2003) Chromosome 6 phylogeny in primates and centromere repositioning. Mol Biol Evol 20:1506–1512
Federico C, Cantarella CD, Di Mare P, Tosi S, Saccone S (2008) The radial arrangement of the human chromosome 7 in the lymphocyte cell nucleus is associated with chromosomal band gene density. Chromosoma 117:399–410
Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E et al (2008) Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4(3):e1000039. doi:10.1371/journal.pgen.1000039
Foster HA, Bridger JM (2005) The genome and the nucleus: a marriage made by evolution. Genome organization and nuclear architecture. Chromosoma 114:212–229
Fraser J, Williamson I, Bickmore WA, Dostie J (2015) An overview of genome organization and how we got there: from FISH to Hi-C. Microbiol Mol Biol Rev 79:347–372
Gilbert N, Boyle S, Fiegler H, Woodfine K, Carter NP et al (2004) Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers. Cell 118:555–566
Grasser F, Neusser M, Fiegler H, Thormeyer T, Cremer MP et al (2008) Replication-timing-correlated spatial chromatin arrangements in cancer and in primate interphase nuclei. J Cell Sci 121:1876–1886
Hepperger C, Otten S, von Hase J, Dietzel S (2007) Preservation of large-scale chromatin structure in FISH experiments. Chromosoma 116:117–133
Jabbari K, Bernardi G (2017) An isochore framework underlies chromatin architecture. PLoS One 12(1):e0168023. doi:10.1371/journal.pone.0168023
Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries SS et al (2013) Single-cell dynamics of genome-nuclear lamina interactions. Cell 153:178–192
Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM et al (2002) Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296:158–162
Kupper K, Kolbl A, Biener D, Dittrich S, von Hase J et al (2007) Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma 116:285–306
Leotta CG, Federico C, Brundo MV, Tosi S, Saccone S (2014) HLXB9 gene expression, and nuclear location during in vitro neuronal differentiation in the SK-N-BE neuroblastoma cell line. PLoS One 9(8):e105481. doi:10.1371/journal.pone.0105481
Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293
Marshall OJ, Chueh AC, Wong LH, Choo KH (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282. doi:10.1016/j.ajhg.2007.11.009
Montefalcone G, Tempesta S, Rocchi M, Archidiacono N (1999) Centromere repositioning. Genome Res 9:1184–1188
Mora L, Sánchez I, Garcia M, Ponsà M (2006) Chromosome territory positioning of conserved homologous chromosomes in different primate species. Chromosoma 115:367–375
Müller S, Stanyon R, O’Brien PCM, Ferguson-Smith MA, Plesker R et al (1999) Defining the ancestral karyotype of all primates by multidirectional chromosome painting between tree shrews, lemurs and humans. Chromosoma 108:393–400
Muller S, Finelli P, Neusser M, Wienberg J (2004) The evolutionary history of human chromosome 7. Genomics 84:458–467
Neusser M, Schubel V, Koch A, Cremer T, Müller S (2007) Evolutionary conserved, cell type and species-specific higher order chromatin arrangements in interphase nuclei of primates. Chromosoma 116:307–320
Ono A, Kono K, Ikebe D, Muto A, Sun J et al (2007) Nuclear positioning of the BACH2 gene in BCR-ABL positive leukemic cells. Genes Chromosom Cancer 46:67–74
Purgato S, Belloni E, Piras FM, Zoli M, Badiale C et al (2015) Centromere sliding on a mammalian chromosome. Chromosoma 124:277–287. doi:10.1007/s00412-014-0493-6
Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665–1680
Saccone S, Federico C, Bernardi G (2002) Localization of the gene-richest and the gene-poorest isochores in the interphase nuclei of mammals and birds. Gene 300:169–178
Sadoni N, Langer S, Fauth C, Bernardi G, Cremer T et al (1999) Nuclear organization of mammalian genomes: polar chromosome territories build up functionally distinct higher order compartments. J Cell Biol 146:1211–1226
Seuànez HN (1979) The phylogeny of human chromosomes. Springer, Berlin
Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R et al (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 38:1348–1354
Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C et al (2002) Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 276:10–23
Stanyon R, Rocchi M, Capozzi O, Roberto R, Misceo D et al (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosom Res 16:17–39
Stevens TJ, Lando D, Basu S, Atkinson LP, Cao Y et al (2017) 3D structures of individual mammalian genomes studied by single-cell Hi-C. Nature 544:59–64. doi:10.1038/nature21429
Szczerbal I, Foster HA, Bridger JM (2009) The spatial repositioning of adipogenesis genes is correlated with their expression status in a porcine mesenchymal stem cell adipogenesis model system. Chromosoma 118:647–663
Tanabe H, Muller S, Neusser M, von Hase J, Calcagno E et al (2002) Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci U S A 99:4424–4429
Tolomeo D, Capozzi O, Stanyon RR, Archidiacono N, D'Addabbo P et al (2017) Epigenetic origin of evolutionary novel centromeres. Sci Rep 3:41980. doi:10.1038/srep41980
Tosi S, Mostafa Kamel Y, Owoka T, Federico C, Truong TH et al (2015) Paediatric acute myeloid leukaemia with the t(7;12)(q36;p13) rearrangement: a review of the biological and clinical management aspects. Biomark Res 3:21. doi:10.1186/s40364-015-0041-4
Tsend-Ayush E, Grutzner F, Yue Y, Grossmann B, Hansel U et al (2004) Plasticity of human chromosome 3 during primate evolution. Genomics 83:193–202
Ventura M, Archidiacono N, Rocchi M (2001) Centromere emergence in evolution. Genome Res 11:595–599
Ventura M, Weigl S, Carbone L, Cardone MF, Misceo D et al (2004) Recurrent sites for new centromere seeding. Genome Res 14:1696–1703
Ventura M, Antonacci F, Cardone MF, Stanyon R, D’Addabbo P et al (2007) Evolutionary formation of new centromeres in macaque. Science 316:243–246
Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J et al (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 113:1565–1576
Wang S, Su JH, Beliveau BJ, Bintu B, Moffitt JR et al (2016) Spatial organization of chromatin domains and compartments in single chromosomes. Science 353:598–602
Watanabe Y, Maekawa M (2013) R/G-band boundaries: genomic instability and human disease. Clin Chim Acta 419:108–112. doi:10.1016/j.cca.2013.02.011
Williamson I, Berlivet S, Eskeland R, Boyle S, Illingworth RS et al (2014) Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev 28:2778–2791
Woodfine K, Fiegler H, Beare DM, Collina JE, McCann OT et al (2004) Replication timing of the human genome. Hum Mol Genet 13:191–202
Zink D (2006) The temporal program of DNA replication: new insights into old questions. Chromosoma 115:273–287
Acknowledgements
The authors wish to thank the anonymous reviewers for constructive comments. This work was supported by P.R.A. to SS and F.I.R. to VF from the University of Catania.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Rachel O’Neill
Rights and permissions
About this article
Cite this article
Federico, C., Pappalardo, A.M., Ferrito, V. et al. Genomic properties of chromosomal bands are linked to evolutionary rearrangements and new centromere formation in primates. Chromosome Res 25, 261–276 (2017). https://doi.org/10.1007/s10577-017-9560-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-017-9560-1