Skip to main content
Log in

Homeobox Genes Expressed During Echinoderm Arm Regeneration

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Regeneration in echinoderms has proved to be more amenable to study in the laboratory than the more classical vertebrate models, since the smaller genome size and the absence of multiple orthologs for different genes in echinoderms simplify the analysis of gene function during regeneration. In order to understand the role of homeobox-containing genes during arm regeneration in echinoderms, we isolated the complement of genes belonging to the Hox class that are expressed during this process in two major echinoderm groups: asteroids (Echinaster sepositus and Asterias rubens) and ophiuroids (Amphiura filiformis), both of which show an extraordinary capacity for regeneration. By exploiting the sequence conservation of the homeobox, putative orthologs of several Hox genes belonging to the anterior, medial, and posterior groups were isolated. We also report the isolation of a few Hox-like genes expressed in the same systems.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arenas-Mena C, Martinez P, Cameron RA, Davidson EH (1998) Expression of the Hox gene complex in the indirect development of a sea urchin. Proc Natl Acad Sci USA 95:13062–13067

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arnone MI, Rizzo F, Annunciata R, Cameron RA, Peterson KJ, Martinez P (2006) Genetic organization and embryonic expression of the ParaHox genes in the sea urchin (Strongulocentrotus purpuratus): insights into the relationship between clustering and colinearity. Dev Biol 300:63–73

    Article  CAS  PubMed  Google Scholar 

  • Bannister R, McGonnell IM, Graham A, Thorndyke MC, Beesley PW (2005) Afuni, a novel transforming growth factor-β gene is involved in arm regeneration by the brittle star (Amphiura filiformis). Dev Genes Evol 215:393–401

    Article  CAS  PubMed  Google Scholar 

  • Bayascas JR, Castillo E, Munoz-Marmo AM, Salo E (1997) Planarian Hox gene: novel patterns of expression during regeneration. Development 124:144–148

    Google Scholar 

  • Bayascas JR, Castillo E, Munoz-Marmol AM, Baguna J, Salo E (1998a) Synchronous and early activation of planarian Hox genes and the re-specification of body axes during regneration in Dugesia (G.) tigrina (Turbellaria; Tricladida). Hydrobiologia 383:125–130

    Article  Google Scholar 

  • Bayascas JR, Castillo E, Salo E (1998b) Platyhelminthes have a hox code differentially activated during regeneration, with genes closely related to those of spiralian protostomes. Dev Genes Evol 208:467–473

    Article  CAS  PubMed  Google Scholar 

  • Bouillet P, Chazaud C, Oulad-Abdelghani M, Dolle P, Chambon P (1995) Sequence and expression pattern of the Stra7 (Gbx-2) homeobox-containing gene induced by retinoic acid in P19 embryonal carcinoma cells. Dev Dyn 204:372–382

    Article  CAS  PubMed  Google Scholar 

  • Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346

    CAS  PubMed  Google Scholar 

  • Cameron RA, Rowen L, Nesbitt R, Bloom S, Rast JP, Berney K, Arenas-Mena C, Martinez P, Lucas S, Richardson PM, Davidson EH, Peterson KJ, Hood L (2006) Unusual gene order and organization of the sea urchin hox cluster. J Exp Zool B Mol Dev Evol 306:45–58

    Article  PubMed  Google Scholar 

  • Candia Carnavali MD (2006) Regeneration in echinoderms: repair, regrowth, cloning. ISJ 3:64–76

    Google Scholar 

  • Candia Carnevali MD, Bonasoro F (2001a) Introduction to the biology of regeneration in echinoderms. Microsc Res Tech 55:365–368

    Article  CAS  PubMed  Google Scholar 

  • Candia Carnevali MD, Bonasoro F (2001b) Microscopic overview of crinoids regeneration. Microsc Res Tech 55:403–426

    Article  CAS  PubMed  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC (1998) Cellular and molecular mechanisms of arm regeneration in crinoid echinoderms: the potential of arm explants. Dev Genes Evol 208:421–430

    Article  CAS  PubMed  Google Scholar 

  • Candia AF, Wright CV (1996) Differential localization of Mox-1 and Mox-2 proteins indicates distinct roles during development. Int J Dev Biol 40:1179–1184

    CAS  PubMed  Google Scholar 

  • Carlson MR, Komine Y, Bryant SV, Gardiner DM (2001) Expression of Hoxb13 and Hoxc10 in developing and regenerating Axolotl limbs and tails. Dev Biol 229:396–406

    Article  CAS  PubMed  Google Scholar 

  • Cisternas P, Byrne M (2009) Expression of Hox4 during development of the pentamerous juvenile sea star Parvulastra exigua. Dev Genes Evol 219:613–618

    Article  CAS  PubMed  Google Scholar 

  • Dollé P, Izpisúa-Belmonte JC, Falkenstein H, Renucci A, Duboule D (1989) Coordinate expression of the murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature 342:767–772

    Article  PubMed  Google Scholar 

  • Dolmatov YuI (1999) Regeneration in echinoderms. Russ J Mar Biol 25:225–233

    Google Scholar 

  • Dupont S, Thorndyke M (2006) Growth or differentiation? Adaptive regeneration in the brittlestar (Amphiura filiformis). J Exp Biol 209:3873–3881

    Article  PubMed  Google Scholar 

  • Ferrier DEK, Minguillon C, Holland PWH, Garcia-Fernandez J (2000) The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol Dev 2:284–293

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Fernàndez J, Holland PWH (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563–566

    Article  PubMed  Google Scholar 

  • Gardiner DM, Blumberg B, Komine Y, Bryant SV (1995) Regulation of HoxA expression in developing and regenerating axolotl limbs. Development 121(6):1731–1741

    CAS  PubMed  Google Scholar 

  • Gehring WJ, Kloter U, Suga H (2009) Evolution of the Hox gene complex from an evolutionary ground state. Curr Top Dev Biol 88:35–61

    Article  CAS  PubMed  Google Scholar 

  • Goss RJ (1969) Principles of regeneration. Academic Press, New York

    Google Scholar 

  • Heberlein U, Penton A, Falsafi S, Hackett D, Rubin GM (1994) The C-terminus of the homeodomain is required for functional specificity of the Drosophila rough gene. Mech Dev 48:35–49

    Article  CAS  PubMed  Google Scholar 

  • Hernroth B, Farahani F, Brunborg G, Dupont S, Dejmek A, Sköld HN (2010) Possibility of mixed progenitor cells in sea star arm regeneration. J Exp Zool B Mol Dev Evol 314:457–468

    Article  PubMed  Google Scholar 

  • Izpisúa-Belmonte JC, Falkenstein H, Dollé P, Renucci A, Duboule D (1991) Muringe genes related to the Drosophila AbdB hometic gene are sequentially expressed during development of the posterior part of the body. EMBO J 10:2279–2289

    PubMed Central  PubMed  Google Scholar 

  • Long S, Byrne M (2001) Evolution of the echinoderm Hox gene cluster. Evol Dev 3:302–311

    Article  CAS  PubMed  Google Scholar 

  • Long S, Martinez P, Chen WC, Thorndyke M, Byrne M (2003) Evolution of echinoderms may not have required modification of the ancestral deuterostome HOX gene cluster: first report of PG4 and PG5 Hox orthologues in echinoderms. Dev Genes Evol 213:573–576

    Article  CAS  PubMed  Google Scholar 

  • Lowe CJ, Wray GA (1997) Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718–721

    Article  CAS  PubMed  Google Scholar 

  • Martinez P, Lee JC, Davidson EH (1997) Complete sequence of SpHox8 and its linkage in the single Hox gene cluster of Strongylocentrotus purpuratus. J Mol Evol 44:371–377

    Article  CAS  PubMed  Google Scholar 

  • Martinez P, Rast JP, Arenas-Mena C, Davidson EH (1999) Organization of an echinoderm Hox gene cluster. Proc Natl Acad Sci USA 96:1469–1474

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mattson P (1976) Regeneration. Bobbs-Merrill, Indianapolis 178 pp

    Google Scholar 

  • Mito T, Endo K (2000) PCR survey of Hox genes in the crinoid and ophiuroid: evidence for anterior conservation and posterior expansion in the echinoderm Hox gene cluster. Mol Phylogenet Evol 14:375–388

    Article  CAS  PubMed  Google Scholar 

  • Nohno T, Noji S, Koyama E, Ohyama K, Myokai F, Kuroiwa A, Saito T, Taniguchi S (1991) Involvement of the chox-4 homeobox genes in determination of anteroposterior axial polarity during limb development. Cell 64:1197–1205

    Article  CAS  PubMed  Google Scholar 

  • Nye HL, Cameron JA, Chernoff EA, Stocum DL (2003) Regeneration of the urodele limb: a review. Dev Dyn 226:280–294

    Article  PubMed  Google Scholar 

  • Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV (1996) PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122:983–1095

    CAS  PubMed  Google Scholar 

  • Orii H, Kato K, Umesono Y, Sakurai T, Agata K, Watanabe K (1999) The planarian HOM/HOX homeobox genes (Plox) expressed along the anteroposterior axis. Dev Biol 210:456–468

    Article  CAS  PubMed  Google Scholar 

  • Patruno M, Smertenko A, Candia Carnevali MD, Bonasoro F, Beesley PW, Thorndyke MC (2002) Expression of transforming growth factor β-like molecules in normal and regeneration arms of the crinoid Antedon mediterranea: immunocytochemical and biochemical evidence. Proc R Soc Lond B Biol Sci 269:1741–1747

    Article  CAS  Google Scholar 

  • Patruno M, McGonnell I, Graham A, Beesley P, Candia Carnevali MD, Thorndyke M (2003) Anbmp2/4 is a new member of the transforming growth factor-β superfamily isolated from a crinoid and involved in regeneration. Proc R Soc Lond B Biol Sci 270:1341–1347

    Article  CAS  Google Scholar 

  • Pendleton JW, Nagai BK, Murtha MT, Ruddle FH (1993) Expansion of the Hox gene family and the evolution of chordates. Proc Natl Acad Sci USA 90:6300–6304

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peterson KJ (2004) Isolation of Hox and Parahox genes in the hemichordate Ptychodera flava and the evolution of deuterostome Hox genes. Mol Phylogenet Evol 31:1208–1215

    Article  CAS  PubMed  Google Scholar 

  • Sánchez Alvarado A, Tsonis PA (2006) Bridging the regeneration gap: genetic insight from diverse animal models. Nature Rev Genet 7:873–883

    Article  PubMed  Google Scholar 

  • Savard P, Gates PB, Brockes JP (1988) Position dependent expression of a homeobox gene transcript in relation to amphibian limb regeneration. EMBO J 7:4275–4282

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sea Urchin Genome Sequencing Consortium (2006) The genome of the sea urchin (Strongylocentrotus purpuratus). Science 413:941–952

    Article  Google Scholar 

  • Suàrez-Castillo EC, Medina-Ortiz WE, Roig-Lòpez JL, Garcia-Arraras JE (2004) Ependymin, a gene involved in regeneration and neuroplasticity in vertebrates, is over expressed during regeneration in the echinoderm Holothuria glaberrima. Gene 334:133–143

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21:172–185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thorndyke MC, Chen W, Beesley PW, Patruno M (2001) Molecular approach to echinoderm regeneration. Microsc Res Tech 55:474–485

    Article  CAS  PubMed  Google Scholar 

  • Torok MA, Gardiner DM, Shubin NH, Bryant SV (1998) Expression of HoxD genes in developing and regenerating axolotl limbs. Dev Biol 200:225–233

    Article  CAS  PubMed  Google Scholar 

  • Tsonis PA (2000) Review: regeneration in vertebrates. Dev Biol 221:273–284

    Article  CAS  PubMed  Google Scholar 

  • Veraksa A, Campo MD, McGinnis W (2000) Developmental patterning genes and their conserved functions: from model organisms to humans. Mol Gen Metab 69:85–100

    Article  CAS  Google Scholar 

  • Vickery MS, McClintock JB (1998) Regeneration in metazoan larvae. Nature 394:140

    Article  CAS  Google Scholar 

  • Zhang J, Nei M (1996) Evolution of Antennapedia-class homeobox genes. Genetics 142:295–330

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the help of the personnel at the Kristineberg Marine Station and at the National Institute of Marine Sciences and Technologies (Monastir). We thank Olga Ortega-Martinez (Kristineberg) for the picture of an Amphiura regenerating tip.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yousra Ben Khadra or Pedro Martinez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ben Khadra, Y., Said, K., Thorndyke, M. et al. Homeobox Genes Expressed During Echinoderm Arm Regeneration. Biochem Genet 52, 166–180 (2014). https://doi.org/10.1007/s10528-013-9637-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-013-9637-2

Keywords

Navigation