Aging Process in Chromatin of Animals

Maciej Wnuk, Monika Bugno-Poniewierska, Anna Lewińska 4 , Bernadetta Oklejewicz, Tomasz Ząbek 3 ,  and Ewa Słota
  • 1 Department of Genetics, University of Rzeszow, Rejtana 16C, 35-959 Rzeszów, Poland
  • 2 Centre of Applied Biotechnology and Basic Sciences, University of Rzeszow, Sokołowska 26, 36-100 Kolbuszowa, Poland
  • 3 Laboratory of Genomics, National Research Institute of Animal Production, 32-083 Balice n. Kraków, Poland
  • 4 Department of Biochemistry and Cell Biology, University of Rzeszow, Rejtana 16C, 35-959 Rzeszów, Poland

Aging Process in Chromatin of Animals

The aging process is a variable, stochastic and pleiotropic phenomenon which is regulated by different environmental and genetic factors. The age-associated changes, which occur at the molecular and cellular levels and disturb biological homeostasis, may directly or indirectly contribute to aging, causing apoptosis or cellular senescence and consequently leading to the death of the organism. In this context, it is particularly interesting to observe changes in somatic cell chromatin. In the present paper, we summarized the knowledge on the biological aspects of aging with special consideration of age-related changes in chromatin like DNA damage, shortening telomeres or age-related changes in methylation of DNA.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Allsopp R. C., Vaziri H., Patterson C., Goldstein S., Younglai E. V., Futcher A. B., Greider C. W., Harley C. B. (1992). Telomere length predicts replicative capacity of human fibroblasts. Proc. Natl. Acad. Sci. U. S. A., 9: 10114-10118.

  • Altieri F., Grillo C., Maceroni M., Chichiarelli S. (2008). DNA damage and repair: from molecular mechanisms to health implications. Antioxid Redox Signal, 10: 891-937.

  • Argyle D., Ellsmore V., Gault E. A., Munro A. F., Nasir L. (2003). Equine telomeres and telomerase in cellular immortalisation and ageing. Mech. Ageing Dev., 124: 759-764.

  • Benetti R., Garcia-Cao M., Blasco M. A. (2007). Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet., 39: 243-250.

  • Berletch J. B., Andrews L. G., Tollefsbol T. O. (2007). A method to detect DNA methyltransferase I gene transcription in vitro in aging systems. Methods Mol. Biol., 371: 73-80.

  • Blackburn E. H. (1991). Structure and function of telomeres. Nature, 350: 569-573.

  • Blackburn E. H. (2005). Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett., 579: 859-862.

  • Bolzan A. D., Bianchi M. S. (2006). Telomeres, interstitial telomeric repeat sequences, and chromosomal aberrations. Mutat. Res., 612: 189-214.

  • Brock G. J., Bird A. (1997). Mosaic methylation of the repeat unit of the human ribosomal RNA genes. Hum. Mol. Genet., 6: 451-456.

  • Burhans W. C., Weinberger M. (2007). DNA replication stress, genome instability and aging. Nucleic Acids Res., 35: 7545-7556.

  • Buys C. H., Osinga J., Anders G. J. (1979). Age-dependent variability of ribosomal RNA-gene activity in man as determined from frequencies of silver staining nucleolus organizing regions on metaphase chromosomes of lymphocytes and fibroblasts. Mech. Ageing Dev., 11: 55-75.

  • Das B. C., Rani R., Mitra A. B., Luthra U. K. (1986). The number of silver-staining NORs (rDNA) in lymphocytes of newborns and its relationship to human development. Mech. Ageing Dev., 36: 117-123.

  • Denton T. E., Liem S. L., Cheng K. M., Barrett J. V. (1981). The relationship between aging and ribosomal gene activity in humans as evidenced by silver staining. Mech. Ageing Dev., 15: 1-7.

  • Derjusheva S. E., Loginova J. A., Parada R., Chiriaeva O. G., Smirnov A. F., Jaszczak K. (1998). The comparative analysis of NOR polymorphism detected by FISH and Ag-staining on horse chromosomes. Caryologica, 51: 1-11.

  • Flores M., Morales L., Gonzaga-Jauregui C., Dominguez-Vidana R., Zepeda C., Yanez O., Gutierrez M., Lemus T., Valle D., Avila M. C., Blanco D., Medina-Ruiz S., Meza K., Ayala E., Garcia D., Bustos P., Gonzalez V., Girard L., Tusie-Luna T., Davila G., Palacios R. (2007). Recurrent DNA inversion rearrangements in the human genome. Proc. Natl. Acad. Sci. U. S. A., 104: 6099-6106.

  • Fraga M. F., Esteller M. (2007). Epigenetics and aging: the targets and the marks. Trends Genet., 23: 413-418.

  • Frenck R. W. Jr., Blackburn E. H., Shannon K. M. (1998). The rate of telomere sequence loss in human leukocytes varies with age. Proc. Natl. Acad. Sci. U. S. A., 95: 5607-5610.

  • Funayama R., Ishikawa F. (2007). Cellular senescence and chromatin structure. Chromosoma, 116: 431-440.

  • Funayama R., Saito M., Tanobe H., Ishikawa F. (2006). Loss of linker histone H1 in cellular senescence. J. Cell Biol., 175: 869-880.

  • Gaudet F., Hodgson J. G., Eden A., Jackson-Grusby L., Dausman J., Gray J. W., Leonhardt H., Jaenisch R. (2003). Induction of tumors in mice by genomic hypomethylation. Science., 300: 489-492.

  • Gilley D., Herbert B. S., Huda N., Tanaka H., Reed T. (2008). Factors impacting human telomere homeostasis and age-related disease. Mech. Ageing Dev., 129: 27-34.

  • Goodpasture C., Bloom S. E. (1975). Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma, 53: 37-50.

  • Gorbunova V., Seluanov A., Mao Z., Hine C. (2007). Changes in DNA repair during aging. Nucleic Acids Res., 35: 7466-7474.

  • Gruber J., Schaffer S., Halliwell B. (2008). The mitochondrial free radical theory of ageing - where do we stand? Front Biosci., 13: 6554-6579.

  • Gruenbaum Y., Stein R., Cedar H., Razin A. (1981). Methylation of CpG sequences in eukaryotic DNA. FEBS Lett., 124: 67-71.

  • Guarente L. (1997). Chromatin and ageing in yeast and in mammals. Ciba Found. Symp., 211: 104-111.

  • Guillen A. K., Hirai Y., Tanoue T., Hirai H. (2004). Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chromosome Res., 12: 225-237.

  • Hayflick L. (1998). A brief history of the mortality and immortality of cultured cells. Keio J. Med., 47: 174-182.

  • Herbig U., Ferreira M., Condel L., Carey D., Sedivy J. M. (2006). Cellular senescence in aging primates. Science, 311, p. 1257.

  • Hines W. C., Fajardo AM., Joste N. E., Bisoffi M., Griffith J. K. (2005). Quantitative and spatial measurements of telomerase reverse transcriptase expression within normal and malignant human breast tissues. Mol. Cancer Res., 3: 503-509.

  • Hodes R. J., Hathcock K. S., Weng N. P. (2002). Telomeres in T and B cells. Nat. Rev. Immunol., 2: 699-706.

  • Hubbell H. R. (1985). Silver staining as an indicator of active ribosomal genes. Stain Technol., 60: 285-294.

  • Huda N., Tanaka H., Herbert B. S., Reed T., Gilley D. (2007). Shared environmental factors associated with telomere length maintenance in elderly male twins. Aging Cell., 6: 709-713.

  • Johnson T. E., Henderson S., Murakami S., de Castro E., de Castro S. H., Cypser J., Rikke B., Tedesco P., Link C. (2002). Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease. J. Inherit. Metab. Dis., 25: 197-206.

  • Johnson L. K., Johnson R., Strehler B. L. (1975). Cardiac hypertrophy, aging and changes in cardiac ribosomal RNA gene dosage in man. J. Mol. Cell Cardiol., 7: 125-133.

  • Kappei D., Londono-Vallejo J. A. (2008). Telomere length inheritance and aging. Mech. Ageing Dev., 129: 17-26.

  • Kosciolek B. A., Rowley P. T. (1998). Human lymphocyte telomerase is genetically regulated. Genes Chromosomes Cancer, 21: 124-130.

  • Leach N. T., Rehder C., Jensen K., Holt S., Jackson-Cook C. (2004). Human chromosomes with shorter telomeres and large heterochromatin regions have a higher frequency of acquired somatic cell aneuploidy. Mech. Ageing Dev., 125: 563-573.

  • Levy M. Z., Allsopp R. C., Futcher A. B., Greider C. W., Harley C. B. (1992). Telomere end-replication problem and cell aging. J. Mol. Biol., 225: 951-960.

  • Lezhava T. (2001). Chromosome and aging: genetic conception of aging. Biogerontology, 2: 253-260.

  • Li H., Mitchell J. R., Hasty P. (2008). DNA double-strand breaks: a potential causative factor for mammalian aging? Mech. Ageing Dev., 129: 416-424.

  • Li Y., Santoro R., Grummt I. (2005). The chromatin remodeling complex NoRC controls replication timing of ribosomal RNA genes. EMBO J., 24: 120-127.

  • Liu L., Wylie R. C., Andrews L. G., Tollefsbol T. O. (2003). Aging, cancer and nutrition: the DNA methylation connection. Mech. Ageing Dev., 124: 989-998.

  • Matsubara Y., Murata M., Yoshida T., Watanabe K., Saito I., Miyaki K., Omae K., Ikeda Y. (2006). Telomere length of normal leukocytes is affected by a functional polymorphism of hTERT. Biochem. Biophys. Res. Commun., 341: 128-131.

  • Mays-Hoopes L. L. (1989). DNA methylation in aging and cancer. J. Gerontol., 44: 35-36.

  • McStay B., Grummt I. (2008). The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol., 24: 131-157.

  • Nakatani K., Qu W. M., Zhang M. C., Fujii H., Furukawa H., Miyazaki T., Iwano M., Saito Y., Nose M., Ono M. (2007). A genetic locus controlling aging-sensitive regression of B lymphopoiesis in an autoimmune-prone MRL/lpr strain of mice. Scand. J. Immunol., 66: 654-661.

  • Narita M., Nunez S., Heard E., Narita M., Lin A. W., Hearn S. A., Spector D. L., Hannon G. J., Lowe S. W. (2003). Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell, 113: 703-716.

  • Nordfjall K., Osterman P., Melander O., Nilsson P., Roos G. (2007). hTERT (-1327)T/C polymorphism is not associated with age-related telomere attrition in peripheral blood. Biochem. Biophys. Res. Commun., 358: 215-218.

  • Nussenzweig A. (2007). Causes and consequences of the DNA damage response. Cell Cycle, 6: 2339-2340.

  • Sander M., Avlund K., Lauritzen M., Gottlieb T., Halliwell B., Stevnsner T., Wewer U., Bohr V. A. (2008). Aging - from molecules to populations. Mech. Ageing Dev., 129: 614-623.

  • Sedelnikova O. A., Horikawa I., Zimonjic D. B., Popescu N. C., Bonner W. M., Barrett J. C. (2004). Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol., 6: 168-170.

  • Słota E., Wnuk M., Bugno M., Pienkowska-Schelling A., Schelling C., Bratus A., Kotylak Z. (2007). The mechanisms determining the nucleolar-organizing regions inactivation of domestic horse chromosomes. J. Anim. Breed. Genet., 124: 163-171.

  • Smogorzewska A., de Lange T. (2004). Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem., 73: 177-208.

  • Stancheva I., Lucchini R., Koller T., Sogo J. M. (1997). Chromatin structure and methylation of rat rRNA genes studied by formaldehyde fixation and psoralen cross-linking. Nucleic Acids Res., 25: 1727-1735.

  • Strohner R., Németh A., Nightingale K. P., Grummt I., Becker P. B., Längst G. (2004). Recruitment of the nucleolar remodeling complex NoRC establishes ribosomal DNA silencing in chromatin. Mol. Cell. Biol., 24: 1791-1798.

  • Swisshelm K., Disteche C. M., Thorvaldsen J., Nelson A., Salk D. (1990). Age-related increase in methylation of ribosomal genes and inactivation of chromosome-specific rRNA gene clusters in mouse. Mutat. Res., 237: 131-146.

  • Świtoński M., Marcolla P., Pieńkowska A., Cholewiński G. (1994). Preliminary investigation on inter-individual variation of the nucleolar organizer regions (AgNORs) in the horse karyotype. Anim. Sci. Pap. Rep., 12: 15-19.

  • Thomas S., Mukherjee A. B. (1996). A longitudinal study of human age-related ribosomal RNA gene activity as detected by silver-stained NORs. Mech. Ageing Dev., 92: 101-109.

  • Um J. H., Kim S. J., Kim D. W., Ha M. Y., Jang J. H., Kim D. W., Chung B. S., Kang C. D., Kim S. H. (2003). Tissue-specific changes of DNA repair protein Ku and mtHSP70 in aging rats and their retardation by caloric restriction. Mech. Ageing Dev., 124: 967-975.

  • Weng N. P., Levine B. L., June C. H., Hodes R. J. (1995). Human naive and memory T lymphocytes differ in telomeric length and replicative potential. Proc. Natl. Acad. Sci. U. S. A., 92: 11091-11094.

  • Wilson D. M., Sofinowski T. M., McNeill D. R. (2003). Repair mechanisms for oxidative DNA damage. Front. Biosci., 8: 963-981.

  • Wnuk M., Bugno-Poniewierska M., Lewinska A., Oklejewicz B., Zabek T., Bartosz G., Słota E. (2011). Age-related changes in genomic stability of horses. Mech. Ageing Dev., 132: 257-268.

  • Zhang R., Chen W., Adams P. D. (2007). Molecular dissection of formation of senescence-associated heterochromatin foci. Mol. Cell Biol., 27: 2343-2358.

OPEN ACCESS

Journal + Issues

Search