Telomere maintenance and telomerase activity are differentially regulated in asexual and sexual worms

Thomas C. J. Tan, Ruman Rahman, Farah Jaber-Hijazi, Daniel A. Felix, Chen Chen, Edward J. Louis, and Aziz Aboobaker
PNAS published ahead of print February 27, 2012 https://doi.org/10.1073/pnas.1118885109

  1. Edited* by James E. Haber, Brandeis University, Waltham, MA, and approved February 6, 2012 (received for review November 16, 2011)

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.

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: aziz.aboobaker{at}nottingham.ac.uk.

  • Author contributions: T.C.J.T., E.J.L., and A.A. designed research; T.C.J.T., R.R., F.J.-H., D.A.F., and C.C. performed research; R.R., E.J.L., and A.A. contributed new reagents/analytic tools; T.C.J.T., E.J.L., and A.A. analyzed data; and T.C.J.T., E.J.L., and A.A. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. JF693290–JF693293).

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1118885109/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Telomere biology of immortal worms
Thomas C. J. Tan, Ruman Rahman, Farah Jaber-Hijazi, Daniel A. Felix, Chen Chen, Edward J. Louis, Aziz Aboobaker
Proceedings of the National Academy of Sciences Feb 2012, 201118885; DOI: 10.1073/pnas.1118885109
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