in

Wounding response in Porifera (sponges) activates ancestral signaling cascades involved in animal healing, regeneration, and cancer

  • 1.

    Eming, S. A., Martin, P. & Tomic-Canic, M. Wound repair and regeneration: Mechanisms, signaling, and translation. Sci. Transl. Med. 6, 265sr6–265sr6 (2014).

  • 2.

    Wilkinson, H. N. & Hardman, M. J. Wound healing: Cellular mechanisms and pathological outcomes. Open Biol. 10, 20023 (2020).

    Google Scholar 

  • 3.

    Dvorak, H. F. Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650–1659 (1986).

    CAS 
    PubMed 

    Google Scholar 

  • 4.

    Dvorak, H. F. Tumors: Wounds that do not heal–Redux. Cancer Immunol. Res. 3, 1–11 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 5.

    Schäfer, M. & Werner, S. Cancer as an overhealing wound: An old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9, 628–638 (2008).

    PubMed 

    Google Scholar 

  • 6.

    MacCarthy-Morrogh, L. & Martin, P. The hallmarks of cancer are also the hallmarks of wound healing. Sci. Signal. 13, eaay8690 (2020).

  • 7.

    Trigos, A. S., Pearson, R. B., Papenfuss, A. T. & Goode, D. L. How the evolution of multicellularity set the stage for cancer. Br. J. Cancer 118, 145–152 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 8.

    Bely, A. E. & Nyberg, K. G. Evolution of animal regeneration: Re-emergence of a field. Trends Ecol. Evol. 25, 161–170 (2010).

    PubMed 

    Google Scholar 

  • 9.

    Bosch, T. C. G. Why polyps regenerate and we don’t: Towards a cellular and molecular framework for Hydra regeneration. Dev. Biol. 303, 421–433 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • 10.

    Gurtner, G. C., Werner, S., Barrandon, Y. & Longaker, M. T. Wound repair and regeneration. Nature 453, 314–321 (2008).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 11.

    Slack, J. M. Animal regeneration: Ancestral character or evolutionary novelty?. EMBO Rep. 18, 1497–1508 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    Wenger, Y., Buzgariu, W., Reiter, S. & Galliot, B. Injury-induced immune responses in Hydra. Semin. Immunol. 26, 277–294 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • 13.

    Poss, K. D., Wilson, L. G. & Keating, M. T. Heart regeneration in zebrafish. Science (80-. ). 298, 2188–2190 (2002).

  • 14.

    Kao, D., Felix, D. & Aboobaker, A. The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios. BMC Genomics 14, 1–17 (2013).

    Google Scholar 

  • 15.

    Gehrke, A. R. et al. Acoel genome reveals the regulatory landscape of whole-body regeneration. Science (80-. ). 363 (2019).

  • 16.

    DuBuc, T. Q., Traylor-Knowles, N. & Martindale, M. Q. Initiating a regenerative response; cellular and molecular features of wound healing in the cnidarian Nematostella vectensis. BMC Biol. 12, 24 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Cary, G. A., Wolff, A., Zueva, O., Pattinato, J. & Hinman, V. F. Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa. BMC Biol. 17, 16 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 18.

    Owlarn, S. et al. Generic wound signals initiate regeneration in missing-tissue contexts. Nat. Commun. 8, 1–13 (2017).

    CAS 

    Google Scholar 

  • 19.

    Ramon-Mateu, J., Ellison, S. T., Angelini, T. E. & Martindale, M. Q. Regeneration in the ctenophore Mnemiopsis leidyi occurs in the absence of a blastema, requires cell division, and is temporally separable from wound healing. BMC Biol. 17, 80 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 20.

    Pawlik, J. R. & Deignan, L. K. Cowries graze Verongid sponges on Caribbean reefs. Coral Reefs 34, 663 (2015).

    ADS 

    Google Scholar 

  • 21.

    Rice, M. M., Ezzat, L. & Burkepile, D. E. Corallivory in the anthropocene: Interactive effects of anthropogenic stressors and corallivory on coral reefs. Front. Mar. Sci. 5, 1–14 (2019).

    Google Scholar 

  • 22.

    Pawlik, J. R., Loh, T.-L., McMurray, S. E. & Finelli, C. M. Sponge communities on Caribbean coral reefs are structured by factors that are top-down, not bottom-up. PLoS One 8, e62573 (2013).

  • 23.

    Mortimer, C., Dunn, M., Haris, A., Jompa, J. & Bell, J. Estimates of sponge consumption rates on an Indo-Pacific reef. Mar. Ecol. Prog. Ser. 672, 123–140 (2021).

    ADS 
    CAS 

    Google Scholar 

  • 24.

    de Goeij, J. M. et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science (80-. ). 342, 108–10 (2013).

  • 25.

    Rix, L. et al. Differential recycling of coral and algal dissolved organic matter via the sponge loop. Funct. Ecol. 31, 778–789 (2016).

    Google Scholar 

  • 26.

    Maldonado, M. et al. Sponge grounds as key marine habitats: A synthetic review of types, structure, functional roles and conservation concerns. Mar. Animal Forests https://doi.org/10.1007/978-3-319-17001-5 (2015).

    Article 

    Google Scholar 

  • 27.

    Soubigou, A., Ross, E. G., Touhami, Y., Chrismas, N. & Modepalli, V. Regeneration in sponge Sycon ciliatum partly mimics postlarval development. Development https://doi.org/10.1242/dev.193714 (2020).

    Article 
    PubMed 

    Google Scholar 

  • 28.

    Telford, M. J., Moroz, L. L. & Halanych, K. M. A sisterly dispute. Nature 529, 286–287 (2016).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 29.

    Feuda, R. et al. Improved modeling of compositional heterogeneity supports sponges as sister to all other animals. Curr. Biol. https://doi.org/10.1016/j.cub.2017.11.008 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 30.

    Dunn, C. W., Leys, S. P. & Haddock, S. H. D. The hidden biology of sponges and ctenophores. Trends Ecol. Evol. 30, 282–291 (2015).

    PubMed 

    Google Scholar 

  • 31.

    Borisenko, I. E., Adamska, M., Tokina, D. B. & Ereskovsky, A. V. Transdifferentiation is a driving force of regeneration in Halisarca dujardini (Demospongiae, Porifera). PeerJ 3, e1211 (2015).

  • 32.

    Lavrov, A. I., Bolshakov, F. V., Tokina, D. B. & Ereskovsky, A. V. Sewing up the wounds: The epithelial morphogenesis as a central mechanism of calcaronean sponge regeneration. J. Exp. Zool. Part B Mol. Dev. Evol. 330, 351–371 (2018).

  • 33.

    Ereskovsky, A. V. et al. Transdifferentiation and mesenchymal‐to‐epithelial transition during regeneration in Demospongiae (Porifera). J. Exp. Zool. Part B Mol. Dev. Evol. 334, 37–58 (2020).

  • 34.

    Alexander, B. E. et al. Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage? PeerJ 3, e820 (2015).

  • 35.

    Pozzolini, M. et al. Insights into the evolution of metazoan regenerative mechanisms: TGF superfamily member roles in tissue regeneration of the marine sponge Chondrosia reniformis Nardo, 1847. J. Exp. Biol. 222, jeb207894 (2019).

  • 36.

    Kenny, N. J. et al. Towards the identification of ancestrally shared regenerative mechanisms across the Metazoa: A transcriptomic case study in the demosponge Halisarca caerulea. Mar. Genomics 37, 135–147 (2018).

    PubMed 

    Google Scholar 

  • 37.

    Pawlik, J. R. Handbook of marine natural products. in Handbook of Marine Natural Products (eds. Fattorusso, E., Gerwick, W. H. & Taglialatela-Scafati, O.) 677–705 (Springer, New York, 2012). https://doi.org/10.1007/978-90-481-3834-0

  • 38.

    Walters, K. D. & Pawlik, J. R. Is there a trade-off between wound-healing and chemical defenses among Caribbean reef sponges?. Integr. Comp. Biol. 45, 352–358 (2005).

    PubMed 

    Google Scholar 

  • 39.

    Becerro, M. A., Turon, X., Uriz, M. J. & Templado, J. Can a sponge feeder be a herbivore? Tylodina perversa (Gastropoda) feeding on Aplysina aerophoba (Demospongiae). Biol. J. Linn. Soc. 78, 429–438 (2003).

    Google Scholar 

  • 40.

    Wu, Y.-C. et al. Opisthobranch grazing results in mobilisation of spherulous cells and re-allocation of secondary metabolites in the sponge Aplysina aerophoba. Sci. Rep. 10, 21934 (2020).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 41.

    Pita, L., Hoeppner, M. P., Ribes, M. & Hentschel, U. Differential expression of immune receptors in two marine sponges upon exposure to microbial-associated molecular patterns. Sci. Rep. 8, 16081 (2018).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Stewart, F. J., Ottesen, E. A. & Delong, E. F. Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics. ISME J. 4, 896–907 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • 43.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible read trimming tool for Illumina NGS data. Bioinformatics btu170 (2014).

  • 44.

    Menzel, P. & Krogh, A. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat. Commun. 7, 11257 (2015).

    ADS 

    Google Scholar 

  • 45.

    Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat. Protoc. 8, 1494 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 46.

    Smith-Unna, R., Boursnell, C., Patro, R., Hibberd, J. M. & Kelly, S. TransRate: Reference free quality assessment of de-novo transcriptome assemblies. Genome Res. 26, 1134–1144 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. Genome analysis BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 48.

    Bryant, D. M. et al. A tissue-mapped axolotl de novo transcriptome enables identification of limb regeneration factors. Cell Rep. 18, 762–776 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 49.

    Kanehisa, M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Conesa, A. et al. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • 51.

    Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6, e21800 (2011).

  • 52.

    Wickham, H. ggplot2: Elegant graphics for data analysis. (Springer, Berlin, 2016).

  • 53.

    Team, R. C. R: A language and environment for statistical computing. (2019).

  • 54.

    Team, Rs. RStudio: Integrated Development for R. (2015).

  • 55.

    Szklarczyk, D. et al. STRING v11: Protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • 56.

    Pritchard, L., Jones, S. & Cock, P. IBioIC Introd. Bioinform. Train. Course https://doi.org/10.5281/zenodo.1184095 (2018).

  • 57.

    Forbes, S. A. et al. The catalogue of somatic mutations in cancer (COSMIC). Curr. Protoc. Hum. Genet. 57 (2008).

  • 58.

    Trigos, A. S., Pearson, R. B., Papenfuss, A. T. & Goode, D. L. Somatic mutations in early metazoan genes disrupt regulatory links between unicellular and multicellular genes in cancer. Elife 8, 1–28 (2019).

    Google Scholar 

  • 59.

    Cerenius, L. & Söderhäll, K. Coagulation in invertebrates. J. Innate Immun. 3, 3–8 (2011).

    PubMed 

    Google Scholar 

  • 60.

    Davie, E. W., Fujikawa, K. & Kisiel, W. The coagulation cascade: Initiation, maintenance, and regulation. Biochemistry 30, 10363–10370 (1991).

    CAS 
    PubMed 

    Google Scholar 

  • 61.

    Richardson, V. R., Cordell, P., Standeven, K. F. & Carter, A. M. Substrates of factor XIII-A: Roles in thrombosis and wound healing. Clin. Sci. 124, 123–137 (2013).

    CAS 

    Google Scholar 

  • 62.

    Domazet-Lošo, T. & Tautz, D. Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa. BMC Biol. 8, 1–10 (2010).

    Google Scholar 

  • 63.

    Trigos, A. S., Pearson, R. B., Papenfuss, A. T. & Goode, D. L. Altered interactions between unicellular and multicellular genes drive hallmarks of transformation in a diverse range of solid tumors. Proc. Natl. Acad. Sci. USA 114, 6406–6411 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Rohani, M. G. & Parks, W. C. Matrix remodeling by MMPs during wound repair. Matrix Biol. 44–46, 113–121 (2015).

    PubMed 

    Google Scholar 

  • 65.

    Grose, R. et al. A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 129, 2303–2315 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • 66.

    Sebé-Pedrós, A. et al. Early metazoan cell type diversity and the evolution of multicellular gene regulation. Nat. Ecol. Evol. 2, 1176–1188 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Paps, J. & Holland, P. W. H. Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty. Nat. Commun. 9, 1730 (2018).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 68.

    Sharrocks, A. D. The ETS-domain transcription factor family. Nat. Rev. Mol. Cell Biol. 2, 827–837 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • 69.

    Larroux, C. et al. Developmental expression of transcription factor genes in a demosponge: Insights into the origin of metazoan multicellularity. Evol. Dev. 8, 150–173 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 70.

    Petersen, H. O. et al. A comprehensive transcriptomic and proteomic analysis of Hydra head regeneration. Mol. Biol. Evol. 32, 1928–1947 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 71.

    Cardozo, M. J., Mysiak, K. S., Becker, T. & Becker, C. G. Reduce, reuse, recycle—Developmental signals in spinal cord regeneration. Dev. Biol. 432, 53–62 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 72.

    Adamska, M. et al. Wnt and TGF-β expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2, e1031 (2007).

  • 73.

    Stewart, Z. K. et al. Transcriptomic investigation of wound healing and regeneration in the cnidarian Calliactis polypus. Sci. Rep. 7, 41458 (2017).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 74.

    Chablais, F. & Jazwinska, A. The regenerative capacity of the zebrafish heart is dependent on TGF signaling. Development 139, 1921–1930 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • 75.

    Chen, H., Lin, F., Xing, K. & He, X. The reverse evolution from multicellularity to unicellularity during carcinogenesis. Nat. Commun. 6, 1–10 (2015).

    ADS 

    Google Scholar 

  • 76.

    Srivastava, M. et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720–726 (2010).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 77.

    Ćetković, H., Halasz, M. & Herak Bosnar, M. Sponges: A reservoir of genes implicated in human cancer. Mar. Drugs 16, 20 (2018).

    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    3 Questions: Anuradha Annaswamy on building smart infrastructures

    Calculating dissolved marine oxygen values based on an enhanced Benthic Foraminifera Oxygen Index