Skip to main content

Advertisement

SpringerLink
Log in

Extracellular matrix gene expression during arm regeneration in Amphiura filiformis

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Extracellular matrix (ECM) plays a dynamic role during tissue development and re-growth. Body part regeneration efficiency relies also on effective ECM remodelling and deposition. Among invertebrates, echinoderms are well known for their striking regenerative abilities since they can rapidly regenerate functioning complex structures. To gather insights on the involvement of ECM during arm regeneration, the brittle star Amphiura filiformis was chosen as experimental model. Eight ECM genes were identified and cloned, and their spatio-temporal and quantitative expression patterns were analysed by means of whole mount in situ hybridisation and quantitative PCR on early and advanced regenerative stages. Our results show that almost none of the selected ECM genes are expressed at early stages of regeneration, suggesting a delay in their activation that may be responsible for the high regeneration efficiency of these animals, as described for other echinoderms and in contrast to most vertebrates. Moreover, at advanced stages, these genes are spatially and temporally differentially expressed, suggesting that the molecular regulation of ECM deposition/remodelling varies throughout the regenerative process. Phylogenetic analyses of the identified collagen-like genes reveal complex evolutionary dynamics with many rounds of duplications and losses and pinpointed their homologues in selected vertebrates. The study of other ECM genes will allow a better understanding of ECM contribution to brittle star arm regeneration.

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

Access this article

Log in via an institution

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, Ath edn. Garland Science, New York, pp 1065–1125

    Google Scholar 

  • Altenhoff AM, Glover NM, Train C-M, Kaleb K, Vesztrocy AW, Dylus D, de Farias TM, Zile K, Stevenson C, Long J, Redestig H, Gonnet GH, Dessimoz C (2018) The OMA orthology database in 2018: retrieving evolutionary relationships among all domains of life through richer web and programmatic interfaces. Nucleic Acids Res 46:D477–D485

    CAS  PubMed  Google Scholar 

  • Arpino V, Brock M, Gill SE (2015) The role of TIMPs in regulation of extracellular matrix proteolysis. Matrix Biol 44-46:247–254

    CAS  PubMed  Google Scholar 

  • Barros CS, Franco SJ, Müller U (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3:a005108

    PubMed  PubMed Central  Google Scholar 

  • Bely AE, Nyberg KG (2009) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25:161–170

    PubMed  Google Scholar 

  • Ben Amar M, Bianca C (2016) Towards a unified approach in the modeling of fibrosis: a review with research perspectives. Phys Life Rev 17:61–85

    PubMed  Google Scholar 

  • Ben Khadra Y, Ferrario C, Di Benedetto C, Said K, Bonasoro F, Candia Carnevali MD, Sugni M (2015a) Wound repair during arm regeneration in the red starfish Echinaster sepositus. Wound Repair Regen 23:611–622

    PubMed  Google Scholar 

  • Ben Khadra Y, Ferrario C, Di Benedetto C, Said K, Bonasoro F, Candia Carnevali MD, Sugni M (2015b) Re-growth, morphogenesis, and differentiation during starfish arm regeneration. Wound Repair Regen 23:623–634

    PubMed  Google Scholar 

  • Ben Khadra Y, Sugni M, Ferrario C, Bonasoro F, Oliveri P, Martinez P, Candia Carnevali MD (2018) Regeneration in stellate echinoderms: Crinoidea, Asteroidea and Ophiuroidea. In: Kloc M, Kubiak JZ (eds) Marine organisms as model systems in biology and medicine ©Springer International Publishing AG, part of Springer Nature 2018, vol Chapter 14. https://doi.org/10.1007/978-3-319-92486-1_14

    Chapter  Google Scholar 

  • Biressi ACM, Zou T, Dupont S, Di Benedetto C, Bonasoro F, Thorndyke MC, Candia Carnevali MD (2010) Wound healing and arm regeneration in Ophioderma longicaudum and Amphiura filiformis (Ophiuroidea, Echinodermata): comparative morphogenesis and histogenesis. Zoomorphology 129:1–19

    Google Scholar 

  • Blankenship J, Benson S (1984) Collagen metabolism and spicule formation in sea urchin micromere. Exp Cell Res 152:98–104

    CAS  PubMed  Google Scholar 

  • Bock O, Mrowietz U (2002) Keloids. A fibroproliferative disorder of unknown etiology. Hautarzt 53:515

    CAS  PubMed  Google Scholar 

  • Bonnans C, Chou J, Werb Z (2014) Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 15(12):786–801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bosch TCG (2007) Why polyps regenerate and we don't: towards a cellular and molecular framework for Hydra regeneration. Dev Biol 303:421–433

    CAS  PubMed  Google Scholar 

  • Brockes JP, Kumar A (2002) Plasticity and reprogramming of differentiated cells in amphibian regeneration. Mol Cell Biol 3:566–574

    CAS  Google Scholar 

  • Brockes JP, Kumar A (2008) Comparative aspects of animal regeneration. Ann Rev Cell Develop Biol 24:525–549

    CAS  Google Scholar 

  • Burns G, Ortega-Martinez O, Thorndyke MC, Peck LS, Dupont S, Clark MS (2011) Dynamic gene expression profiles during arm regeneration in the brittle star Amphiura filiformis. J Exp Mar Biol Ecol 407:315–322

    CAS  Google Scholar 

  • Byrne M (1994) Ophiuroidea. In: Microscopic anatomy of invertebrates, vol 14. Echinodermata, pp 247–343

  • Cabrera-Serrano A, García-Arrarás JE (2004) RGD-containing peptides inhibit intestinal regeneration in the sea cucumber Holothuria glaberrima. Dev Dyn 231:171–178

    CAS  PubMed  Google Scholar 

  • Cameron RA, Samanta M, Yuan A, He D, Davidson E (2009) SpBase: the sea urchin database and web site. Nucleic Acids Res D:750–754

  • Candia Carnevali MD (2006) Regeneration in echinoderms: repair, regrowth and cloning. Invert Surv J:364–376

  • Chia F-S, Xing J (1996) Echinoderm coelomocytes. Zool Stud 35:231–254

    Google Scholar 

  • Clouse RM, Linchangco GV Jr, Kerr AM, Reid RW, Janies DA (2015) Phylotranscriptomic analysis uncovers a wealth of tissue inhibitor of metalloproteinases variants in echinoderms. R Soc Open Sci 2:150377

    PubMed  PubMed Central  Google Scholar 

  • Czarkwiani A, Dylus DV, Oliveri P (2013) Expression of skeletogenic genes during arm regeneration in the brittle star Amphiura filiformis. Gene Expr Patterns 13:464–472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Czarkwiani A, Ferrario C, Dylus DV, Sugni M, Oliveri P (2016) Skeletal regeneration in the brittle star Amphiura filiformis. Front Zool 13:18

    PubMed  PubMed Central  Google Scholar 

  • Delroisse J, Ullrich-Lüter E, Ortega-Martinez O, Dupont S, Arnone MI, Mallefet J, Flammang P (2014) High opsin diversity in a non-visual infaunal brittle star. BMC Genomics 15:1035

    PubMed  PubMed Central  Google Scholar 

  • Diegelmann RF, Evans MC (2004) Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci 9:283–289

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Dylus DV, Blowes LM, Czarkwiani A, Elphick MR, Oliveri P (2018) Developmental transcriptome of the brittle star Amphiura filiformis reveals gene regulatory network rewiring in echinoderm larval skeleton evolution. Genome Biology 19:26

  • Erickson JR, Echeverri K (2018) Learning from regeneration research organisms: the circuitous road to scar free wound healing. Dev Biol 433(2):144–154

    CAS  PubMed  Google Scholar 

  • Exposito J, Valcourt U, Cluzel C, Lethias C (2010) The fibrillar collagen family. IJMS 11(2):407–426

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrario C, Ben Khadra Y, Czarkwiani A, Zakrzewski A, Martinez P, Colombo G, Bonasoro F, Candia Carnevali MD, Oliveri P, Sugni M (2018) Fundamental aspects of arm repair phase in two echinoderm models. Dev Biol Spec Issue Regen 433(2):297–309

    CAS  Google Scholar 

  • Geer LY, Domrachev M, Lipman DJ, Bryant SH (2002) CDART: protein homology by domain architecture. Genome Res 12(10):1619–1623

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gelse K, Pöschl E, Aigner T (2003) Collagens-structure, function, and biosynthesis. Adv Drug Deliv Rev 55:1531–1546

    CAS  PubMed  Google Scholar 

  • Gemberling M, Bailey TJ, Hyde DR, Poss KD (2013) The zebrafish as a model for complex tissue regeneration. Trends Genet 29:611-620

  • Godwin J, Kuraitis D, Rosenthal N (2014) Extracellular matrix considerations for scar-free repair and regeneration: insights from regenerative diversity among vertebrates. Int J Biochem Cell Biol 56:47–55

    CAS  PubMed  Google Scholar 

  • González-Rosa JM, Martín V, Peralta M, Torres M, Mercader N (2011) Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 138:1663–1674

    PubMed  Google Scholar 

  • Govindan J, Iovine MK (2015) Dynamic remodeling of the extra cellular matrix during zebrafish fin regeneration. Gene Expr Patterns 19(1–2):21–29

    CAS  PubMed  Google Scholar 

  • Hernroth B, Farahani F, Brunborg G, Dupont S, Gejmek A, Sköld HN (2010) Possibility of mixed progenitor in sea star arm regeneration. J Exp Zool B Mol Dev Evol 314B:1–12

    Google Scholar 

  • Hyman LH (1955) The invertebrates. Vol. 4. Echinodermata. Mc Graw Hill Book Company Inc. New York, Toronto, London 34-131, 245–412

  • Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326:1216–1219

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iorio V, Troughton LD, Hamill KJ (2015) Laminins: roles and utility in wound repair. Adv Wound Care (New Rochelle) 4(4):250–263

    Google Scholar 

  • Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong S-Y, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics. DOI:https://doi.org/10.1093/bioinformatics/btu031

  • Karp RD, Coffaro KA (1982) Cellular defense systems of the Echinodermata. Phylogeny and Ontogeny 257–282

  • Keane TJ, Horejs C-M, Stevens MM (2018) Scarring vs. functional healing: matrix-based strategies to regulate tissue repair. Adv Drug Deliv Rev 129:407–419

  • King RS, Newmark PA (2012) The cell biology of regeneration JCB: review. J Cell Biol 196:553–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kishore U, Reid KB (2000) C1q: structure, function, and receptors. Immunopharmacology 49(1–2):159–170

    CAS  PubMed  Google Scholar 

  • Kudtarkar P, Cameron RA (2017) Echinobase: an expanding resource for echinoderm genomic information. Database 2017 DOI: https://doi.org/10.1093/database/bax074

  • Liesi P, Kaakkola S, Dahl D, Vaheri A (1984) Laminin is induced in astrocytes of adult brain by injury. EMBO J 3:683–686

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu P, Takai K, Weaver VM, Werb Z (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 3(12):a005058

    PubMed  PubMed Central  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2014) Transcriptomic changes during regeneration of the central nervous system in an echinoderm. BMC Genomics 15:357

    PubMed  PubMed Central  Google Scholar 

  • Mescher AL, Neff AW (2005) Regenerative capacity and the developing immune system. Adv Biochem Eng Biotechnol 93:39–66

    CAS  PubMed  Google Scholar 

  • Miao T, Zixuan W, Sun L, Li X, Xing L, Bai Y, Wang F, Yang H (2017) Extracellular matrix remodeling and matrix metalloproteinases (ajMMP-2 like and ajMMP-16 like) characterization during intestine regeneration of sea cucumber Apostichopus japonicus. Comp Biochem Physiol B: Biochem Mol Biol 212:12–23

    CAS  Google Scholar 

  • Milligan M (1946) Trichrome stain for formalin-fixed tissue. Am J Clin Pathol 10:184

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Okazaki K, Inoué S (1976) Crystal property of the larval sea urchin spicule. Develop Growth Differ 18:413–434

    Google Scholar 

  • Ortiz-Pineda PA, Ramírez-Gómez F, Pérez-Ortiz J, González-Díaz S, Santiago-De Jesús F, Hernández-Pasos J, Del Valle-Avila C, Rojas-Cartagena C, Suárez-Castillo EC, Tossas K, Méndez-Merced AT, Roig-López JL, Ortiz-Zuazaga H, García-Arrarás JE (2009) Gene expression profiling of intestinal regeneration in the sea cucumber. BMC Genomics 10:262. DOI:https://doi.org/10.1186/1471-2164-10-262

  • Purushothaman S, Saxena S, Meghah V, Brahmendra Swamy CV, Ortega-Martinez O, Dupont S, Idris M (2015) Transcriptomic and proteomic analyses of Amphiura filiformis arm tissue-undergoing regeneration. J Proteome 112:113–124

    CAS  Google Scholar 

  • Quiñones JL, Rosa R, Ruiz DL, García-Arrarás JE (2002) Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol 250:181–197

    PubMed  Google Scholar 

  • Rahban SR, Garner WL (2003) Fibroproliferative scars. Clin Plast Surg 30:77

    PubMed  Google Scholar 

  • Rousselle P, Montmasson M, Garnier C (2018) Extracellular matrix contribution to skin wound re-epithelialization. Matrix Biol 75-76:12-26

  • Saló E, Abril JF, Adell T, Cebrià F, Eckelt K, Fernàndez-Taboada E, Handberg-Thorager M, Iglesias M, Molina MD, Rodrìguea-Esteban G (2009) Planarian regeneration: achievements and future directions after 20 years of research. Int J Dev Biol 53:1317–1327. https://doi.org/10.1387/ijdb.072414es

  • Satoh A, Hirata A, Makanae A (2012) Collagen reconstitution is inversely correlated with induction of limb regeneration in Ambystoma mexicanum. Zool Sci 29:191–197

    CAS  Google Scholar 

  • Sheehy EJ, Cunniffe GM, O’Brien FJ (2018) Collagen-based biomaterials for tissue regeneration and repair. Peptides and proteins as biomaterials for tissue regeneration and repair 127-150 DOI:https://doi.org/10.1016/B978-0-08-100803-4.00005-X

  • Smith VJ (1981) The echinoderms. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells. Academic Press, London, pp 513–562

    Google Scholar 

  • Stevenson TJ, Vinarsky V, Atkinson DL, Keating MT, Odelberg SJ (2006) Tissue inhibitor of metalloproteinase 1 regulates matrix metalloproteinase activity during newt limb regeneration. Dev Dyn 235(3):606–616

    CAS  PubMed  Google Scholar 

  • Sun L, Chen M, Yang H, Wang T, Liu B, Shu C, Gardiner DM (2011) Large scale gene expression profiling during intestine and body wall regeneration in the sea cucumber Apostichopus japonicus. Comp Biochem Physiol D. DOI:https://doi.org/10.1016/j.cbd.2011.03.002

  • Swinehart IT, Badylak SF (2016) Extracellular matrix bioscaffolds in tissue remodeling and morphogenesis. Dev Dyn 245:351–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tassava RA, Nace JD, Wei Y (1996) Extracellular matrix protein turnover during salamander limb regeneration. Wound Repair Regen 4(1):75–81

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Whittaker CA, Bergeron KF, Whittle J, Brandhorst BP, Burke RD, Hynes RO (2006) The echinoderm adhesome. Dev Biol 300:252–266

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yi S, Ding F, Gong L, Gu X (2017) Extracellular matrix scaffolds for tissue engineering and regenerative medicine. Curr Stem Cell Res Ther 12(3):233–246

    CAS  PubMed  Google Scholar 

  • Yun S (2014) The role of extracellular matrix in planarian regeneration. PhD thesis (University of Hong Kong)

  • Zhao A, Qin H, Fu X (2016) What determines the regenerative capacity in animals? BioScience 66(9):735–746

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Sven Lovén Centre for Marine Sciences in Kristineberg (Sweden) for help during the collection of experimental animals. We thank Wendy Hart (University College London) and Fraser Simpson (University College London) for help with gene cloning. We are grateful to Iain C. Wilkie for his suggestions for improving the manuscript. This work was partly funded by the KVA fund SL2015-0048 from the Royal Swedish Academy of Science. CF and LP were funded by an Erasmus Placement fellowship. AC was funded by a Wellcome Trust PhD studentship (099745/Z/12/Z). MS was funded by a Young Researcher Grant of the University of Milan.

Funding

This work was partly funded by the KVA fund SL2015-0048 from the Royal Swedish Academy of Science. CF and LP were funded by an Erasmus Placement fellowship. AC was funded by a Wellcome Trust PhD studentship (099745/Z/12/Z). MS was funded by a Young Researcher Grant of the University of Milan.

Author information

Author notes

  1. Anna Czarkwiani

    Present address: Center for Regenerative Therapies Dresden, Fetscherstraße 105, 01307, Dresden, Germany

Authors and Affiliations

  1. Department of Environmental Science and Policy, University of Milan, via Celoria, 2, 20133, Milan, Italy

    Cinzia Ferrario, Laura Piovani, Maria Daniela Candia Carnevali & Michela Sugni

  2. Center for Complexity and Biosystems, Department of Physics, University of Milan, via Celoria, 16, 20133, Milan, Italy

    Cinzia Ferrario & Michela Sugni

  3. Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT,, UK

    Anna Czarkwiani, Laura Piovani & Paola Oliveri

  4. Department of Computational Biology, University Lausanne, Genopode, 1015, Lausanne, Switzerland

    David Viktor Dylus

  5. Swiss Institute of Bioinformatics, Genopode, 1015, Lausanne, Switzerland

    David Viktor Dylus

  6. GAIA 2050 Center, Department of Environmental Science and Policy, University of Milan, via Celoria, 2, 20133, Milan, Italy

    Maria Daniela Candia Carnevali & Michela Sugni

Authors
  1. Cinzia Ferrario
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Czarkwiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Viktor Dylus
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura Piovani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Daniela Candia Carnevali
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michela Sugni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paola Oliveri
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CF, MS and PO conceived the study and wrote the manuscript. CF and AC carried out the molecular experiments and the histological sections. AC provided the experimental animal images. LP helped with in situ hybridisation experiments and performed Q-PCR with PO. DVD performed phylogenetic analysis. CF, AC, DVD, MS, PO and MDCC analysed the data. All authors contributed to and approved the final manuscript.

Corresponding authors

Correspondence to Michela Sugni or Paola Oliveri.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 14.9 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferrario, C., Czarkwiani, A., Dylus, D.V. et al. Extracellular matrix gene expression during arm regeneration in Amphiura filiformis. Cell Tissue Res 381, 411–426 (2020). https://doi.org/10.1007/s00441-020-03201-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-020-03201-0

Keywords

Search

Navigation