Telomere Maintenance and Telomerase Activity Are Differentially Regulated in Asexual and Sexual Worms

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2012 Feb 29

PMID 22371573

Citations 41

Authors

Thomas C J Tan

Ruman Rahman

Farah Jaber-Hijazi

Daniel A Felix

Chen Chen

Edward J Louis

Aziz Aboobaker

Affiliations

Soon will be listed here.

Abstract

In most sexually reproducing animals, replication and maintenance of telomeres occurs in the germ line and during early development in embryogenesis through the use of telomerase. Somatic cells generally do not maintain telomere sequences, and these cells become senescent in adults as telomeres shorten to a critical length. Some animals reproduce clonally and must therefore require adult somatic mechanisms for maintaining their chromosome ends. Here we study the telomere biology of planarian flatworms with apparently limitless regenerative capacity fueled by a population of highly proliferative adult stem cells. We show that somatic telomere maintenance is different in asexual and sexual animals. Asexual animals maintain telomere length somatically during reproduction by fission or when regeneration is induced by amputation, whereas sexual animals only achieve telomere elongation through sexual reproduction. We demonstrate that this difference is reflected in the expression and alternate splicing of the protein subunit of the telomerase enzyme. Asexual adult planarian stem cells appear to maintain telomere length over evolutionary timescales without passage through a germ-line stage. The adaptations we observe demonstrate indefinite somatic telomerase activity in proliferating stem cells during regeneration or reproduction by fission, and establish planarians as a pertinent model for studying telomere structure, function, and maintenance.

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References

Flores I, Blasco M . The role of telomeres and telomerase in stem cell aging. FEBS Lett. 2010; 584(17):3826-30. DOI: 10.1016/j.febslet.2010.07.042. View

Reddien P, Oviedo N, Jennings J, Jenkin J, Sanchez Alvarado A . SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science. 2005; 310(5752):1327-30. DOI: 10.1126/science.1116110. View

Aboobaker A . Planarian stem cells: a simple paradigm for regeneration. Trends Cell Biol. 2011; 21(5):304-11. DOI: 10.1016/j.tcb.2011.01.005. View

Partridge L, Gems D . Benchmarks for ageing studies. Nature. 2007; 450(7167):165-7. DOI: 10.1038/450165a. View

Gomes N, Shay J, Wright W . Telomere biology in Metazoa. FEBS Lett. 2010; 584(17):3741-51. PMC: 2928394. DOI: 10.1016/j.febslet.2010.07.031. View

Olovnikov A . A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol. 1973; 41(1):181-90. DOI: 10.1016/0022-5193(73)90198-7. View

Henson J, Neumann A, Yeager T, Reddel R . Alternative lengthening of telomeres in mammalian cells. Oncogene. 2002; 21(4):598-610. DOI: 10.1038/sj.onc.1205058. View

Skold H, Asplund M, Wood C, Bishop J . Telomerase deficiency in a colonial ascidian after prolonged asexual propagation. J Exp Zool B Mol Dev Evol. 2011; 316(4):276-83. DOI: 10.1002/jez.b.21399. View

Fitzgerald M, Riha K, Gao F, Ren S, McKnight T, Shippen D . Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc Natl Acad Sci U S A. 1999; 96(26):14813-8. PMC: 24730. DOI: 10.1073/pnas.96.26.14813. View

10.

Skold H, Obst M . Potential for clonal animals in longevity and ageing studies. Biogerontology. 2011; 12(5):387-96. DOI: 10.1007/s10522-011-9333-8. View

11.

Gonzalez-Estevez C, Arseni V, Thambyrajah R, Felix D, Aboobaker A . Diverse miRNA spatial expression patterns suggest important roles in homeostasis and regeneration in planarians. Int J Dev Biol. 2009; 53(4):493-505. DOI: 10.1387/ijdb.082825cg. View

12.

Lauzon R, Rinkevich B, Patton C, Weissman I . A morphological study of nonrandom senescence in a colonial urochordate. Biol Bull. 2000; 198(3):367-78. DOI: 10.2307/1542692. View

13.

Laird D, Weissman I . Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate Botryllus schlosseri. Dev Biol. 2004; 273(2):185-94. DOI: 10.1016/j.ydbio.2004.05.029. View

14.

Meier B, Clejan I, Liu Y, Lowden M, Gartner A, Hodgkin J . trt-1 is the Caenorhabditis elegans catalytic subunit of telomerase. PLoS Genet. 2006; 2(2):e18. PMC: 1361356. DOI: 10.1371/journal.pgen.0020018. View

15.

McEachern M, Haber J . Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem. 2006; 75:111-35. DOI: 10.1146/annurev.biochem.74.082803.133234. View

16.

Riha K, McKnight T, Griffing L, Shippen D . Living with genome instability: plant responses to telomere dysfunction. Science. 2001; 291(5509):1797-800. DOI: 10.1126/science.1057110. View

17.

Kilian A, Bowtell D, Abud H, Hime G, Venter D, Keese P . Isolation of a candidate human telomerase catalytic subunit gene, which reveals complex splicing patterns in different cell types. Hum Mol Genet. 1997; 6(12):2011-9. DOI: 10.1093/hmg/6.12.2011. View

18.

Joffee B, Solovei I, MACGREGOR H . Ends of Chromosomes in Polycelis tenuis (Platyhelminthes) have telomere repeat TTAGGG. Chromosome Res. 1996; 4(4):323-4. DOI: 10.1007/BF02263686. View

19.

Bosch T . Hydra and the evolution of stem cells. Bioessays. 2009; 31(4):478-86. DOI: 10.1002/bies.200800183. View

20.

Blackburn E, Challoner P . Identification of a telomeric DNA sequence in Trypanosoma brucei. Cell. 1984; 36(2):447-57. DOI: 10.1016/0092-8674(84)90238-1. View