Parental genomes mix in mule and human cell nuclei.
Abstract: Whether chromosome sets inherited from father and mother occupy separate spaces in the cell nucleus is a question first asked over 110 years ago. Recently, the nuclear organization of the genome has come increasingly into focus as an important level of epigenetic regulation. In this context, it is indispensable to know whether or not parental genomes are spatially separated. Genome separation had been demonstrated for plant hybrids and for the early mammalian embryo. Conclusive studies for somatic mammalian cell nuclei are lacking because homologous chromosomes from the two parents cannot be distinguished within a species. We circumvented this problem by investigating the three-dimensional distribution of chromosomes in mule lymphocytes and fibroblasts. Genomic DNA of horse and donkey was used as probes in fluorescence in situ hybridization under conditions where only tandem repetitive sequences were detected. We thus could determine the distribution of maternal and paternal chromosome sets in structurally preserved interphase nuclei for the first time. In addition, we investigated the distribution of several pairs of chromosomes in human bilobed granulocytes. Qualitative and quantitative image evaluation did not reveal any evidence for the separation of parental genomes. On the contrary, we observed mixing of maternal and paternal chromosome sets.
Publication Date: 2009-02-07 PubMed ID: 19198867DOI: 10.1007/s00412-008-0200-6Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article is about a study on the spatial organisation of genomes inherited from the mother and father in the cell nucleus. The researchers used mule lymphocytes and fibroblasts, along with human bilobed granulocytes, to observe and conclude that the parental genomes are not separated and, instead, they mix.
Objective and Background
- The study aims to address a long-standing question in biology about whether the genetic material inherited from each parent occupies separate spaces within a cell nucleus.
- This study was undertaken due to a rediscovered interest in the organization of the genome within the nucleu. This structure is now thought to play a crucial role in epigenetic regulation, the process where gene expression is controlled without changes to the DNA sequence.
- Previously, somatic cells in mammals could not be conclusively studied due to the inability to distinguish homologous chromosomes from each parent within a species.
Methodology
- To get around the difficulty in distinguishing between chromosomes from each parent, the research team used mule lymphocytes and fibroblasts that contained genetic material from a horse and a donkey—two different species.
- The researchers used fluorescent in situ hybridization with the genomic DNA of a horse and a donkey to study the three-dimensional distribution of chromosomes. Special conditions were set up to ensure that only tandem repetitive sequences were detected.
- Additionally, the researchers studied the distribution of several pairs of chromosomes in human bilobed granulocytes.
Findings
- The image evaluation did not uncover any evidence to support the notion of genome separation from each parent.
- Instead, the evaluation revealed that the chromosomes inherited from the mother and the father do not occupy separate regions within the cell nucleus, but mix.
- This was the first time the distribution of maternal and paternal chromosome sets in structurally preserved interphase nuclei was observed and documented.
Implications
- These findings contradict previous beliefs about genome separation and have significant implications for understanding genetic inheritance and regulation.
- The study’s methodology could be adopted in future research on genetic material organisation and its role in epigenetic regulation.
Cite This Article
APA
Hepperger C, Mayer A, Merz J, Vanderwall DK, Dietzel S.
(2009).
Parental genomes mix in mule and human cell nuclei.
Chromosoma, 118(3), 335-347.
https://doi.org/10.1007/s00412-008-0200-6 Publication
Researcher Affiliations
- Department Biologie II, Ludwig-Maximilians-Universität München, Grosshaderner Str. 2, 82152 Planegg-Martinsried, Germany.
MeSH Terms
- Animals
- Cell Nucleus / genetics
- Centromere / genetics
- Chimera / genetics
- Chromosomes, Mammalian / genetics
- Equidae / genetics
- Fibroblasts / ultrastructure
- Genome
- Granulocytes
- Horses / genetics
- Humans
- Lymphocytes / ultrastructure
References
This article includes 47 references
- Mayer W, Smith A, Fundele R, Haaf T. Spatial separation of parental genomes in preimplantation mouse embryos.. J Cell Biol 2000 Feb 21;148(4):629-34.
- Mayer R, Brero A, von Hase J, Schroeder T, Cremer T, Dietzel S. Common themes and cell type specific variations of higher order chromatin arrangements in the mouse.. BMC Cell Biol 2005 Dec 7;6:44.
- Gadi IK, Ryder OA. Molecular cytogenetics of the equidae. II. purification and cytological localization of a (G + C)-rich satellite DNA from Equus hemionus onager and cross-species hybridization to E. asinus chromosomes.. Cytogenet Cell Genet 1983;35(2):124-30.
- Allison DC, Nestor AL. Evidence for a relatively random array of human chromosomes on the mitotic ring.. J Cell Biol 1999 Apr 5;145(1):1-14.
- Foster HA, Bridger JM. The genome and the nucleus: a marriage made by evolution. Genome organisation and nuclear architecture.. Chromosoma 2005 Sep;114(4):212-29.
- Stöck M, Lamatsch DK, Steinlein C, Epplen JT, Grosse WR, Hock R, Klapperstück T, Lampert KP, Scheer U, Schmid M, Schartl M. A bisexually reproducing all-triploid vertebrate.. Nat Genet 2002 Mar;30(3):325-8.
- GLASS E. [Identification of chromosomes in karyotype of rat liver].. Chromosoma 1956;7(8):655-69.
- Woods GL, White KL, Vanderwall DK, Li GP, Aston KI, Bunch TD, Meerdo LN, Pate BJ. A mule cloned from fetal cells by nuclear transfer.. Science 2003 Aug 22;301(5636):1063.
- Lanctôt C, Cheutin T, Cremer M, Cavalli G, Cremer T. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions.. Nat Rev Genet 2007 Feb;8(2):104-15.
- Misteli T. Beyond the sequence: cellular organization of genome function.. Cell 2007 Feb 23;128(4):787-800.
- Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Müller S, Eils R, Cremer C, Speicher MR, Cremer T. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes.. PLoS Biol 2005 May;3(5):e157.
- Albiez H, Cremer M, Tiberi C, Vecchio L, Schermelleh L, Dittrich S, Küpper K, Joffe B, Thormeyer T, von Hase J, Yang S, Rohr K, Leonhardt H, Solovei I, Cremer C, Fakan S, Cremer T. Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks.. Chromosome Res 2006;14(7):707-33.
- Cremer T, Cremer M, Dietzel S, Müller S, Solovei I, Fakan S. Chromosome territories--a functional nuclear landscape.. Curr Opin Cell Biol 2006 Jun;18(3):307-16.
- Spolsky C, Uzzell T. Natural interspecies transfer of mitochondrial DNA in amphibians.. Proc Natl Acad Sci U S A 1984 Sep;81(18):5802-5.
- Wienberg J. Fluorescence in situ hybridization to chromosomes as a tool to understand human and primate genome evolution.. Cytogenet Genome Res 2005;108(1-3):139-60.
- Tanious FA, Veal JM, Buczak H, Ratmeyer LS, Wilson WD. DAPI (4',6-diamidino-2-phenylindole) binds differently to DNA and RNA: minor-groove binding at AT sites and intercalation at AU sites.. Biochemistry 1992 Mar 31;31(12):3103-12.
- Guerrini F, Bucci S, Ragghianti M, Mancino G, Hotz H, Uzzell T, Berger L. Genomes of two water frog species resist germ line exclusion in interspecies hybrids.. J Exp Zool 1997 Oct 1;279(2):163-76.
- Brandriff BF, Gordon LA, Segraves R, Pinkel D. The male-derived genome after sperm-egg fusion: spatial distribution of chromosomal DNA and paternal-maternal genomic association.. Chromosoma 1991 May;100(4):262-6.
- Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I. Arrangements of macro- and microchromosomes in chicken cells.. Chromosome Res 2001;9(7):569-84.
- Kikuchi S, Tanaka H, Wako T, Tsujimoto H. Centromere separation and association in the nuclei of an interspecific hybrid between Torenia fournieri and T. baillonii (Scrophulariaceae) during mitosis and meiosis.. Genes Genet Syst 2007 Oct;82(5):369-75.
- Young IT. Proof without prejudice: use of the Kolmogorov-Smirnov test for the analysis of histograms from flow systems and other sources.. J Histochem Cytochem 1977 Jul;25(7):935-41.
- Ryder OA, Hansen SK. Molecular cytogenetics of the Equidae. I. Purification and cytological localization of a (G + C)-rich satellite DNA from Equus przewalskii.. Chromosoma 1979 Apr 30;72(2):115-29.
- Nagele RG, Freeman T, Fazekas J, Lee KM, Thomson Z, Lee HY. Chromosome spatial order in human cells: evidence for early origin and faithful propagation.. Chromosoma 1998 Nov;107(5):330-8.
- Pera F, Rainer B. Studies of multipolar mitoses in euploid tissue cultures. I. Somatic reduction to exactly haploid and triploid chromosome sets.. Chromosoma 1973 May 14;42(1):71-86.
- Hepperger C, Otten S, von Hase J, Dietzel S. Preservation of large-scale chromatin structure in FISH experiments.. Chromosoma 2007 Apr;116(2):117-33.
- Fung JC, Marshall WF, Dernburg A, Agard DA, Sedat JW. Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations.. J Cell Biol 1998 Apr 6;141(1):5-20.
- Kosak ST, Groudine M. Gene order and dynamic domains.. Science 2004 Oct 22;306(5696):644-7.
- Lasken RS, Egholm M. Whole genome amplification: abundant supplies of DNA from precious samples or clinical specimens.. Trends Biotechnol 2003 Dec;21(12):531-5.
- Bártová E, Kozubek S, Jirsová P, Kozubek M, Lukásová E, Skalníková M, Cafourková A, Koutná I, Paseková R. Higher-order chromatin structure of human granulocytes.. Chromosoma 2001 Sep;110(5):360-70.
- Quattro JM, Avise JC, Vrijenhoek RC. Molecular evidence for multiple origins of hybridogenetic fish clones (Poeciliidae:Poeciliopsis).. Genetics 1991 Feb;127(2):391-8.
- Bridge JA, Nelson M, McComb E, McGuire MH, Rosenthal H, Vergara G, Maale GE, Spanier S, Neff JR. Cytogenetic findings in 73 osteosarcoma specimens and a review of the literature.. Cancer Genet Cytogenet 1997 May;95(1):74-87.
- Chaudhuri JP, Walther JU. Separation of parental genomes in human blood and bone marrow cells and its implications.. Int J Oncol 2003 Nov;23(5):1257-62.
- Hsu TC, Cooper JE, Mace ML Jr, Brinkley BR. Arrangement of centromeres in mouse cells.. Chromosoma 1971;34(1):73-87.
- Tanabe H, Müller S, Neusser M, von Hase J, Calcagno E, Cremer M, Solovei I, Cremer C, Cremer T. Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates.. Proc Natl Acad Sci U S A 2002 Apr 2;99(7):4424-9.
- Haaf T. The battle of the sexes after fertilization: behaviour of paternal and maternal chromosomes in the early mammalian embryo.. Chromosome Res 2001;9(4):263-71.
- Nagele RG, Freeman T, McMorrow L, Thomson Z, Kitson-Wind K, Lee Hy. Chromosomes exhibit preferential positioning in nuclei of quiescent human cells.. J Cell Sci 1999 Feb;112 ( Pt 4):525-35.
- Yang F, Fu B, O'Brien PC, Nie W, Ryder OA, Ferguson-Smith MA. Refined genome-wide comparative map of the domestic horse, donkey and human based on cross-species chromosome painting: insight into the occasional fertility of mules.. Chromosome Res 2004;12(1):65-76.
- Cornforth MN, Greulich-Bode KM, Loucas BD, Arsuaga J, Vázquez M, Sachs RK, Brückner M, Molls M, Hahnfeldt P, Hlatky L, Brenner DJ. Chromosomes are predominantly located randomly with respect to each other in interphase human cells.. J Cell Biol 2002 Oct 28;159(2):237-44.
- GLASS E. [The problem of genome separation in mitosis of untreated rat liver].. Chromosoma 1957;8(5):468-92.
- Mayer W, Fundele R, Haaf T. Spatial separation of parental genomes during mouse interspecific (Mus musculus x M. spretus) spermiogenesis.. Chromosome Res 2000;8(6):555-8.
- Raudsepp T, Chowdhary BP. Construction of chromosome-specific paints for meta- and submetacentric autosomes and the sex chromosomes in the horse and their use to detect homologous chromosomal segments in the donkey.. Chromosome Res 1999;7(2):103-14.
- Wijers ER, Zijlstra C, Lenstra JA. Rapid evolution of horse satellite DNA.. Genomics 1993 Oct;18(1):113-7.
- Deng W, Tsao SW, Lucas JN, Leung CS, Cheung AL. A new method for improving metaphase chromosome spreading.. Cytometry A 2003 Jan;51(1):46-51.
- Nagele R, Freeman T, McMorrow L, Lee HY. Precise spatial positioning of chromosomes during prometaphase: evidence for chromosomal order.. Science 1995 Dec 15;270(5243):1831-5.
- Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. Differences in the localization and morphology of chromosomes in the human nucleus.. J Cell Biol 1999 Jun 14;145(6):1119-31.
- Chaudhuri JP, Kasprzycki E, Battaglia M, McGill JR, Brøgger A, Walther JU, Reith A. Biphasic chromatin structure and FISH signals in reflect intranuclear order.. Cell Oncol 2005;27(5-6):327-34.
- Odartchenko N, Keneklis T. Localization of paternal DNA in interphase nuclei of mouse eggs during early cleavage.. Nature 1973 Feb 23;241(5391):528-9.
Citations
This article has been cited 4 times.- Hua LL, Casas CJ, Mikawa T. Mitotic Antipairing of Homologous Chromosomes.. Results Probl Cell Differ 2022;70:191-220.
- Keenan CR, Mlodzianoski MJ, Coughlan HD, Bediaga NG, Naselli G, Lucas EC, Wang Q, de Graaf CA, Hilton DJ, Harrison LC, Smyth GK, Rogers KL, Boudier T, Allan RS, Johanson TM. Chromosomes distribute randomly to, but not within, human neutrophil nuclear lobes.. iScience 2021 Mar 19;24(3):102161.
- Solinhac R, Mompart F, Martin P, Robelin D, Pinton P, Iannuccelli E, Lahbib-Mansais Y, Oswald IP, Yerle-Bouissou M. Transcriptomic and nuclear architecture of immune cells after LPS activation.. Chromosoma 2011 Oct;120(5):501-20.
- Yerle-Bouissou M, Mompart F, Iannuccelli E, Robelin D, Jauneau A, Lahbib-Mansais Y, Delcros C, Oswald IP, Gellin J. Nuclear architecture of resting and LPS-stimulated porcine neutrophils by 3D FISH.. Chromosome Res 2009;17(7):847-62.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists