Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T10:29:38.477Z Has data issue: false hasContentIssue false

Spatial Distribution of Heterochromatin Bodies in the Nuclei of Triatoma infestans (Klug)

Published online by Cambridge University Press:  12 May 2020

Carlos Henrique L. Imperador
Affiliation:
Department of Structural and Functional Biology, Institute of Biology, University of Campinas (Unicamp), Rua Monteiro Lobato 255, 13083-862Campinas, SP, Brazil
Vanessa B. Bardella
Affiliation:
Department of Biology, Institute of Biosciences, State University of São Paulo (Unesp), Avenida 24-A, 1515, 13506-900Rio Claro, SP, Brazil
Eli Heber M. dos Anjos
Affiliation:
Department of Structural and Functional Biology, Institute of Biology, University of Campinas (Unicamp), Rua Monteiro Lobato 255, 13083-862Campinas, SP, Brazil
Vera L.C.C. Rodrigues
Affiliation:
Superintendence for Control of Endemic Diseases (SUCEN), Rua Afonso Pessini, 86, 13845-206Mogi-Guaçu, SP, Brazil
Diogo C. Cabral-de-Mello
Affiliation:
Department of Biology, Institute of Biosciences, State University of São Paulo (Unesp), Avenida 24-A, 1515, 13506-900Rio Claro, SP, Brazil
Maria Luiza S. Mello*
Affiliation:
Department of Structural and Functional Biology, Institute of Biology, University of Campinas (Unicamp), Rua Monteiro Lobato 255, 13083-862Campinas, SP, Brazil
*
*Author for correspondence: Maria Luiza S. Mello, E-mail: [email protected]
Get access

Abstract

Constitutive heterochromatin typically exhibits low gene density and is commonly found adjacent or close to the nuclear periphery, in contrast to transcriptionally active genes concentrated in the innermost nuclear region. In Triatoma infestans cells, conspicuous constitutive heterochromatin forms deeply stained structures named chromocenters. However, to the best of our knowledge, no information exists regarding whether these chromocenters acquire a precise topology in the cell nuclei or whether their 18S rDNA, which is important for ribosome function, faces the nuclear center preferentially. In this work, the spatial distribution of fluorescent Feulgen-stained chromocenters and the distribution of their 18S rDNA was analyzed in Malpighian tubule cells of T. infestans using confocal microscopy. The chromocenters were shown to be spatially positioned relatively close to the nuclear periphery, though not adjacent to it. The variable distance between the chromocenters and the nuclear periphery suggests mobility of these bodies within the cell nuclei. The distribution of 18S rDNA at the edge of the chromocenters was not found to face the nuclear interior exclusively. Because the genome regions containing 18S rDNA in the chromocenters also face the nuclear periphery, the proximity of the chromocenters to this nuclear region is not assumed to be associated with overall gene silencing.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alladin, N, Moskovtsev, SI, Russel, H, Kenigsberg, S, Lulat, AGM & Librach, CL (2013). The three-dimensional image analysis of the chromocenter in motile and immotile human sperm. Systems Biol Reprod Med 59, 146152. doi:10.3109/19396368.2013.772679CrossRefGoogle ScholarPubMed
Allshire, RC & Madhani, HD (2018). Ten principles of heterochromatin formation and function. Nat Rev 19, 229244. doi:10.1038/nrm.2017.119CrossRefGoogle ScholarPubMed
Alvarenga, EM, Imperador, CHL, Bardella, VB, Rodrigues, VLCC, Mondin, M, Cabral-de-Mello, DC, Moraes, AS & Mello, MLS (2018). Histone acetylation and methylation marks in chromatin of Panstrongylus megistus (Hemiptera, Reduviidae). Acta Histochem 120, 572577. doi:10.1016/j.acthis.2018.07.002Google Scholar
Alvarenga, EM, Mondin, M, Martins, JA, Rodrigues, VLCC, Vidal, BC, Rincones, J, Carazzolle, MF, Andrade, LM & Mello, MLS (2011). Spatial distribution of AT- and GC-rich DNA within interphase cell nuclei of Triatoma infestans Klug. Micron 42, 568578. doi:10.1016/j.micron.2011.02.002CrossRefGoogle ScholarPubMed
Alvarenga, EM, Rodrigues, VLCC, Moraes, AS, Naves, LS, Mondin, M, Felisbino, MB & Mello, MLS (2016). Histone epigenetic marks in heterochromatin and euchromatin of the Chagas’ disease vector, Triatoma infestans. Acta Histochem 118, 401412. doi:10.1016/j.acthis.2016.04.002CrossRefGoogle Scholar
Bártova, E, Krejci, J, Harnicarová, A, Galiová, G & Kozubek, S (2008). Histone modifications and nuclear architecture: A review. J Histochem Cytochem 56, 711721. doi:10.1369/jhc.2008.951251CrossRefGoogle ScholarPubMed
Berr, A & Schubert, I (2007). Interphase chromosome arrangement in Arabidopsis thaliana is similar in differentiated and meristematic tissues and shows a transient mirror symmetry after nuclear division. Genetics 176, 853863. doi:10.1534/genetics.107.073270CrossRefGoogle Scholar
Bickmore, WA (2013). The spatial organization of the human genome. Ann Rev Genomics Human Genet 14, 6784. doi:10.1146/annurev-genom-091212-153515CrossRefGoogle ScholarPubMed
Boyle, S, Rodesch, MJ, Halvensleben, HA, Jeddeloh, JA & Bickmore, WA (2011). Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res 19, 901909. doi:10.1007/s10577-011-9245-0CrossRefGoogle ScholarPubMed
Cabral-de-Mello, DC, Moura, RC & Martins, C (2010). Chromosomal mapping of repetitive DNAs in the beetle Dichotomius geminatus provides the first evidence for an association of 5S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and a complement. Heredity 104, 393400. doi:10.1038/hdy.2009.126CrossRefGoogle Scholar
Campos, SGP, Rodrigues, VLCC & Mello, MLS (2002). Changes in nuclear phenotype frequencies following sequential cold shocks in Triatoma infestans (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz 97, 857864.CrossRefGoogle Scholar
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, 541567. doi:10.1023/A:1012495201697CrossRefGoogle ScholarPubMed
Cremer, T & Cremer, C (2001). Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2, 292301. doi:10.1038/35066075CrossRefGoogle ScholarPubMed
Cremer, T & Cremer, C (2010). Chromosome territories. Cold Spring Harb Perspect Biol, 123. doi: 10.1101/cshperspect.a003889.Google ScholarPubMed
Cremer, T, Kreth, G, Koester, H, Fink, RH, Heintzmann, R, Cremer, M, Solovei, I, Zink, D & Cremer, C (2000). Chromosome territories, interchromatin domain compartment, and nuclear matrix: An integrated view of the functional nuclear architecture. Crit Rev Eukaryot Gene Expr 10, 179212. doi:10.1615/CritRevEukarGeneExpr.v10.i2.60CrossRefGoogle ScholarPubMed
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, 11191131. doi:10.1083/jcb.145.6.1119CrossRefGoogle ScholarPubMed
Cryderman, DE, Morris, EJ, Biessmann, H, Elgin, SCR & Wallrath, LL (1999). Silencing at Drosophila telomeres: Nuclear organization and chromatin structure play critical roles. EMBO J 18, 37243735. doi:10.1093/emboj/18.13.3724CrossRefGoogle ScholarPubMed
Deniaud, E & Bickmore, WA (2009). Transcription and the nuclear periphery: Edge of darkness? Curr Opin Genet Dev 19, 187191. doi:10.1016/j.gde.2009.01.005CrossRefGoogle ScholarPubMed
De Nooijer, S, Wellink, J, Mulder, B & Bisseling, T (2009). Non-specific interactions are sufficient to explain the position of heterochromatic chromocenters and nucleoli in interphase nuclei. Nucleic Acids Res 37, 35583568. doi:10.1093/nar/gkp219CrossRefGoogle ScholarPubMed
Dieudonné, M, Maiuri, P, Biancotto, C, Knezevich, A, Kula, A, Lusic, M & Marcello, A (2009). Transcriptional competence of the integrated HIC-1 provirus at the nuclear periphery. EMBO J 28, 22312243. doi:10.1038/emboj.2009.141CrossRefGoogle Scholar
Ellison, JR & Howard, GC (1981). Non-random position of the AT-rich DNA sequences in early embryos of Drosophila virilis. Chromosoma 83, 555561. doi:10.1007/BF00328279CrossRefGoogle Scholar
Fang, Y & Spector, D (2005). Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell 16, 57105718. doi:10.1091/mbc.e05-08-0706CrossRefGoogle ScholarPubMed
Finlan, LE, Sproul, D, Thomson, I, Boyle, S, Kerr, E, Perry, P, Ylstra, B, Chubb, JR & Bickmore, WA (2008). Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4, e1000039. doi:10.1371/journal.pgen.1000039CrossRefGoogle ScholarPubMed
Fransz, P, De Jong, J, Lysak, M, Castiglione, MR & Schubert, I (2002). Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci USA 99, 1458414589. doi:10.1073/pnas.212325299CrossRefGoogle ScholarPubMed
Fritz, A, Baructu, AR, Martin-Buley, L, van Wijnen, AJ, Zaidi, SK, Imbalzano, AN, Lian, JB, Stein, JL & Stein, GS (2016). Chromosomes at work: Organization of chromosome territories in the interphase nucleus. J Cell Biochem 117, 919. doi:10.1002/jcb.25280CrossRefGoogle ScholarPubMed
Harnicarova, A, Kozubek, S, Pachernik, J, Krejci, J & Bártova, E (2006). Distinct nuclear arrangement of active and inactive c-myc genes in control and differentiated colon carcinoma cells. Expt Cell Res 312, 40194035. doi:10.1016/j.yexcr.2006.09.007CrossRefGoogle ScholarPubMed
Hochstrasser, M, Mathog, D, Gruenbaum, Y, Saumweber, H & Sedat, JW (1986). Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster. J Cell Biol 102, 112123. doi:10.1083/jcb.102.1.112CrossRefGoogle ScholarPubMed
Ioannou, D & Griffin, DK (2011). Male infertility, chromosome abnormalities, and nuclear organization. Cytogenet Genome Res 133, 269279. doi:10.1159/000322060CrossRefGoogle ScholarPubMed
Jost, KL, Bertulat, B, Rapp, A, Brero, A, Hardt, T, Domaing, P, Gösele, C, Schulz, H, Hübner, N & Cardoso, MC (2015). Gene repositioning within the cell nucleus is not random and is determined by its genomic neighborhood. Epigenet Chromatin 8, 36. doi:10.1186/s13072-015-0025-5CrossRefGoogle Scholar
Küpper, K, Kölbl, A, Biener, D, Dittrich, S, von Hase, J, Thormeyer, T, Fiegler, H, Carter, NP, Speicher, MR, Cremer, T & Cremer, M (2007). Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma 116, 285306. doi:10.1007/s00412-007-0098-4CrossRefGoogle Scholar
Kurz, A, Lampel, S, Nickolenko, JE, Bradl, J, Benner, A, Zirbel, RM, Cremer, T & Lichter, P (1996). Active and inactive genes localize preferentially in the periphery of chromosome territories. J Cell Biol 135, 11951205. doi:10.1083/jcb.135.5.1195CrossRefGoogle ScholarPubMed
Meister, P & Taddei, A (2013). Building silent compartments at the nuclear periphery: A recurrent theme. Curr Opin Genet Dev 23, 96103. doi:10.1016/j.gde.2012.12.001CrossRefGoogle ScholarPubMed
Mello, MLS (1971). Nuclear behavior in the Malpighian tubes of Triatoma infestans. Cytologia (Tokyo) 36, 4249. doi:10.1508/cytologia.36.42CrossRefGoogle Scholar
Mello, MLS (1972). Micro-interferometry of insect polyploidy nuclei. Cytologia (Tokyo) 37, 261270. doi:10.1508/cytologia.37.261CrossRefGoogle ScholarPubMed
Mello, MLS (1975). Feulgen-DNA values and ploidy degrees in the Malpighian tubes of some triatomids. Rev Brasil Pesq Méd Biol 8, 101107.Google ScholarPubMed
Mello, MLS (1978). Computer analysis of stained chromatin in Malpighian tubes of Triatoma infestans (Klug) (Hemiptera, Reduviidae). Mikroskopie (Wien) 34, 285299.Google Scholar
Mello, MLS (1989). Nuclear fusion and change in chromatin packing state in response to starvation in Triatoma infestans. Rev Brasil Genét 12, 485498.Google Scholar
Mello, MLS (2013). Spatial distribution of heterochromatin bodies in vectors of Chagas disease as studied by confocal microscopy. Proceedings – Life Sciences (LS), Microscopy Conference MC2013 at Regensburg – August 25–30, 2013, pp. 131132.Google Scholar
Mello, MLS & Dolder, H (1977). Fine structure of the Malpighian tubes in the blood-sucking insect, Triatoma infestans Klug. Protoplasma 93, 275288. doi:10.1007/BF01275659CrossRefGoogle Scholar
Mello, MLS, Dolder, H & Dias, CA (1990). Nuclear ultrastructure of Malpighian tubule cells in Triatoma infestans (Hemiptera, Reduviidae) under conditions of full nourishment and starvation. Rev Brasil Genét 13, 517.Google Scholar
Mello, MLS, Kubrusly, FS, Randi, MAF, Rodrigues, VLCC & Ferraz-Filho, NA (1995). Effects of heavy metals on chromatin supraorganization, nuclear phenotypes, and survival of Triatoma infestans. Entomol Exp Appl 74, 209218. doi:10.1111/j.1570-7458.1995.tb01893.xCrossRefGoogle Scholar
Mello, MLS, Tavares, MCH, Dantas, MM, Rodrigues, VLCC, Maria, SS, Campos, SP & Garcia, NL (2001). Cell death and survival alterations in Malpighian tubules of Triatoma infestans following heat shock. Biochem Cell Biol 79, 709717. doi:10.1139/o01-136CrossRefGoogle ScholarPubMed
Mello, MLS & Vidal, BC (2017). The Feulgen reaction: A brief review and new perspectives. Acta Histochem 119, 603609. doi:10.1016/j.acthis.2017.07.002CrossRefGoogle ScholarPubMed
Olszewska, M, Wiland, E & Kurpisz, M (2008). Positioning of chromosome 15, 18, X and Y centromeres in sperm cells of fertile individuals and infertile patients with increased level of aneuploidy. Chromosome Res 16, 875890. doi:10.1007/s10577-008-1246-2CrossRefGoogle Scholar
Panzera, Y, Pita, S, Ferreiro, MJ, Ferrandis, I, Lages, C, Pérez, R, Silva, AE, Guerra, M & Panzera, F (2012). High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138, 5667. doi:10.1159/000341888CrossRefGoogle Scholar
Pinkel, D, Straume, T & Gray, JW (1986). Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83, 29342938. doi:10.1073/pnas.83.9.2934CrossRefGoogle ScholarPubMed
Pita, S, Panzera, F, Mora, P, Vela, J, Cuadrado, Á, Sánchez, A, Palomegue, T & Lorite, P (2017). Comparative repeatome analysis on Triatoma infestans Andean and non-Andean lineages, main vector of Chagas disease. PLoS ONE 12, e0181635. doi:10.1371/journal.pone.0181635CrossRefGoogle ScholarPubMed
Ruault, M, Dubarry, M & Taddei, A (2008). Re-positioning genes in the nuclear envelope in mammalian cells: Impact on transcription. Trends Genet 24, 574581. doi:10.1016/j.tig.2008.08.008CrossRefGoogle ScholarPubMed
Schreiber, G, Bogliolo, AR & Pinto, AC (1972). Cytogenetics of Triatominae: Caryotype, DNA content, nuclear size and heteropyknosis of autosomes. Brazil J Biol 32, 255263.Google Scholar
Solari, J (1979). Autosomal synaptonemal complexes and sex chromosomes without axes in Triatoma infestans (Reduviidae: Hemiptera). Chromosoma 72, 225240. doi:10.10007/BF00293236CrossRefGoogle Scholar
Solovei, I, Kreysing, M, Lanctôt, C, Kösem, S, Peichl, L, Cremer, T, Gick, J & Joffe, B (2009). Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137, 356368. doi:10.1016/j.cell.2009.01.052CrossRefGoogle ScholarPubMed
Sterner, DE & Berger, SL (2000). Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64, 435459. doi:10.1128/MMBR.64.2.435-459.2000CrossRefGoogle ScholarPubMed
Talasz, H, Lindner, HH, Sarg, B & Helliger, W (2005). Histone H4-lysine 20 monomethylation is increased in promoter and coding regions of active genes and correlates with hyperacetylation. J Biol Chem 280, 3881438822. doi:10.1074/jbc.M505563200CrossRefGoogle ScholarPubMed
Towbin, BD, Gonzales-Sandoval, A & Gasser, SM (2013). Mechanisms of heterochromatin subnuclear localization. Trends Biochem Sci 38, 356363. doi:10.1016/j.tibs.2013.04.004CrossRefGoogle ScholarPubMed
Towbin, BD, Meister, P & Gasser, SM (2009). The nuclear envelope – a scaffold for silencing? Curr Opin Genet Dev 19, 180186. doi:10.1016/j.gde.2009.01.006CrossRefGoogle ScholarPubMed
Vidal, BC, Schlüter, G & Moore, GW (1973). Cell nucleus pattern recognition: Influence of staining. Acta Cytol 17, 510521.Google Scholar
Wigglesworth, VB (1984). Insect Physiology, 8th ed.London: Chapman and Hall.Google Scholar
Wu, R, Terry, AV, Singh, PB & Gilbert, DM (2005). Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol Biol Cell 16, 28722881. doi:10.1091/mbc.e04-11-0997CrossRefGoogle ScholarPubMed
Zalenskaya, IA & Zalensky, AO (2004). Non-random positioning of chromosomes in human sperm nuclei. Chromosome Res 12, 163173. doi:10.1023/B:CHRO.0000013166.04629.97Google ScholarPubMed
Supplementary material: File

Imperador et al. supplementary material

Imperador et al. supplementary material

Download Imperador et al. supplementary material(File)
File 14.3 MB