Skip to main content
Log in

Telomere elongation and telomerase expression in regenerating arms of the starfish Luidia clathrata (Asteroidea: Echinodermata)

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Regeneration in echinoderms has been extensively characterized physiologically, but fewer studies have addressed the genetic mechanisms underlying the process. Telomeres, genetic sequences on the ends of chromosomes that shorten with cell division, are associated with cell senescence, and thus genetic age after cell growth. Relative telomere lengths in the starfish Luidia clathrata were measured in arms of juveniles, adults prior to injury, and adults after injury during initial regeneration. Additionally, relative telomerase expression was measured in arms of adults prior to injury, at wound closure, and during initial regeneration. Telomeres were longer in juveniles than uninjured adults, indicating genetic aging. Telomeres elongated in adults after injury. Telomerase was detected before and after injury. The combination of genetic aging and telomerase expression both before and after injury suggests possible post-transcriptional regulation of telomerase. Additionally, as previous studies did not detect elongated telomeres in regenerated arms, it is possible that telomere elongation occurs early in the regenerative process as a mechanism to permit cellular division for growth without aging the final regenerated arm.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bakaysa SL, Mucci LA, Slagboom PE et al (2007) Telomere length predicts survival independent of genetic influences. Aging Cell 6:769–774. doi:10.1111/j.1474-9726.2007.00340.x

    Article  CAS  Google Scholar 

  • Blackburn EH (2001) Switching and signaling at the telomere. Cell 106:661–673

    Article  CAS  Google Scholar 

  • Blasco MA (2005) Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6:611–622. doi:10.1038/nrg1656

    Article  CAS  Google Scholar 

  • Bosch TCG (2009) Hydra and the evolution of stem cells. BioEssays: news and reviews in molecular. Cell Dev Biol 31:478–486. doi:10.1002/bies.200800183

    Google Scholar 

  • Carnevali MC (2006) Regeneration in echinoderms: repair, regrowth, cloning. Invertebr Surviv J 3:64–76

    Google Scholar 

  • Ebert TA, Russell MP, Gamba G, Bodnar A (2008) Growth, survival, and longevity estimates for the rock-boring sea urchin Echinometra lucunter lucunter (Echinodermata, Echinoidea) in Bermuda. Bull Mar Sci 82:381–403

    Google Scholar 

  • Edmondson CH (1935) Autotomy and regeneration in Hawaiian starfishes. Bernice P. Bishop Museum Occasional Papers, vol 11, issue 8. The Museum, Honolulu, Hawaii, pp 3–20

  • Elmore LW, Norris MW, Sircar S et al (2008) Upregulation of telomerase function during tissue regeneration. Exp Biol Med (Maywood, N.J.) 233:958–967. doi:10.3181/0712-RM-345

    Article  CAS  Google Scholar 

  • Emson RH, Wilkie I (1980) Fission and autotomy in echinoderms. Oceanogr Mar Biol Annu Rev 18:155–250

    Google Scholar 

  • Farzaneh-Far R, Cawthon RM, Na B et al (2008) Prognostic value of leukocyte telomere length in patients with stable coronary artery disease: data from the heart and soul study. Arterioscler Thromb Vasc Biol 28:1379–1384

    Article  CAS  Google Scholar 

  • Francis N, Gregg T, Owen R et al (2006) Lack of age-associated telomere shortening in long- and short-lived species of sea urchins. FEBS Lett 580:4713–4717. doi:10.1016/j.febslet.2006.07.049

    Article  CAS  Google Scholar 

  • Gandellini P, Folini M, Bandiera R et al (2007) Down-regulation of human telomerase reverse transcriptase through specific activation of RNAi pathway quickly results in cancer cell growth impairment. Biochem Pharmacol 73:1703–1714

    Article  CAS  Google Scholar 

  • Garcia-Cisneros A, Pérez-Portela R, Almroth BC et al (2015) Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina. Heredity 115:437–443

    Article  CAS  Google Scholar 

  • Herbig U, Jobling WA, Chen BP et al (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21 CIP1, but not p16 INK4a. Mol Cell 14:501–513

    Article  CAS  Google Scholar 

  • Hernroth B, Farahani F, Brunborg G, Dupont S, Dejmek A, Nilsson Sköld H (2010) Possibility of mixed progenitor cells in sea star arm regeneration. J Exp Zool (Molecular and Developmental Evolution) 314B:457–468

    Article  CAS  Google Scholar 

  • Kaack KE, Pomory CM (2011) Salinity effects on arm regeneration in Luidia clathrata (Echinodermata: Asteroidea). Mar Freshw Behav Physiol 44:359–374. doi:10.1080/10236244.2011.634060

    Article  Google Scholar 

  • Lawrence JM (1992) Arm loss and regeneration in Asteroidea (Echinodermata). In: Scalera-Liaci L, Canicatti C (eds) Echinoderm research 1991. Baklema, Rotterdam, pp 39–52

    Google Scholar 

  • Lawrence JM (2010) Energetic costs of loss and regeneration of arms in stellate echinoderms. Integr Comp Biol 50:506–514

    Article  Google Scholar 

  • Lawrence JM, Klinger TS, McClintock JB et al (1986) Allocation of nutrient resources to body components by regenerating Luidia clathrata (Say) (Echinodermata: Asteroidea). J Exp Mar Biol Ecol 102:47–53. doi:10.1016/0022-0981(86)90125-5

    Article  Google Scholar 

  • Mah CL, Blake DB (2012) Global diversity and phylogeny of the Asteroidea (Echinodermata). PLoS One 7:e35644. doi:10.1371/journal.pone.0035644

    Article  CAS  Google Scholar 

  • Marrs J, Wilkie IC, Sköld M, Maclaren WM, McKenzie JD (2000) Size-related aspects of arm damage, tissue mechanics, and autotomy in the starfish Asterias rubens. Mar Biol 137:59–70

    Article  Google Scholar 

  • Ohunchida K, Mizumoto K, Ogura Y, Ishikawa N, Nagai E, Yamaguchi K, Tanaka M (2005) Quantitative assessment of telomerase activity and human telomerase reverse transcriptase messenger RNA levels in pancreatic juice samples for the diagnosis of pancreatic cancer. Clin Cancer Res 11:2285–2292

    Article  Google Scholar 

  • Ojimi MC, Isomura N, Hidaka M (2009) Telomerase activity is not related to life history stage in the jellyfish Cassiopea sp. Comp Biochem Physiol A Mol Integr Physiol 152:240–244. doi:10.1016/j.cbpa.2008.10.008

    Article  Google Scholar 

  • Olovnikov AM (1973) A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol 41:181–190. doi:10.1016/0022-5193(73)90198-7

    Article  CAS  Google Scholar 

  • Pomory CM, Lares MT (2000) Rate of regeneration of two arms in the field and its effect on body components in Luidia clathrata (Echinodermata: Asteroidea). J Exp Mar Biol Ecol 254:211–220

    Article  CAS  Google Scholar 

  • Schaetzlein S, Lucas-Hahn A, Lemme E et al (2004) Telomere length is reset during early mammalian embryogenesis. Proc Natl Acad Sci USA 101:8034–8038. doi:10.1073/pnas.0402400101

    Article  CAS  Google Scholar 

  • Schram JB, McClintock JB, Angus RA, Lawrence JM (2011) Regenerative capacity and biochemical composition of the sea star Luidia clathrata (Say) (Echinodermata: Asteroidea) under conditions of near-future ocean acidification. J Exp Mar Biol Ecol 407:266–274

    Article  CAS  Google Scholar 

  • Tan TCJ, Rahman R, Jaber-Hijazi F et al (2012) Telomere maintenance and telomerase activity are differentially regulated in asexual and sexual worms. Proc Natl Acad Sci USA 109:4209–4214. doi:10.1073/pnas.1118885109

    Article  CAS  Google Scholar 

  • Zielke S, Bodnar A (2010) Telomeres and telomerase activity in scleractinian corals and Symbiodinium spp. The Biological Bulletin 218:113–121. doi:10.1086/BBLv218n2p113

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Colton Seals for starfish husbandry assistance, and Stacy Cecil and Katie Vaccaro for assistance with field work and collections. This study was funded by a Grant from the University of West Florida Scholarly and Creative Activities Committee (Grant No. 164317).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexis M. Janosik.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Additional information

Responsible Editor: T. Reusch.

Reviewed by Undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Varney, R.M., Pomory, C.M. & Janosik, A.M. Telomere elongation and telomerase expression in regenerating arms of the starfish Luidia clathrata (Asteroidea: Echinodermata). Mar Biol 164, 195 (2017). https://doi.org/10.1007/s00227-017-3230-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3230-x

Navigation