Oscarella lobularis (Homoscleromorpha, Porifera) Regeneration: Epithelial Morphogenesis and Metaplasia

Abstract

Sponges are known to possess remarkable reconstitutive and regenerative abilities ranging from common wounding or body part regeneration to more impressive re-building of a functional body from dissociated cells. Among the four sponge classes, Homoscleromorpha is notably the only sponge group to possess morphologically distinct basement membrane and specialized cell-junctions, and is therefore considered to possess true epithelia. The consequence of this peculiar organization is the predominance of epithelial morphogenesis during ontogenesis of these sponges. In this work we reveal the underlying cellular mechanisms used during morphogenesis accompanying ectosome regeneration in the homoscleromorph sponge model: Oscarella lobularis. We identified three main sources of novel exopinacoderm during the processes of its regeneration and the restoration of functional peripheral parts of the aquiferous system in O. lobularis: (1) intact exopinacoderm surrounding the wound surface, (2) the endopinacoderm from peripheral exhalant and inhalant canals, and (3) the intact choanoderm found on the wound surface. The basic morphogenetic processes during regeneration are the spreading and fusion of epithelial sheets that merge into one continuous epithelium. Transdifferentiation of choanocytes into exopinacocytes is also present. Epithelial-mesenchymal transition is absent during regeneration. Moreover, we cannot reveal any other morphologically distinct pluripotent cells. In Oscarella, neither blastema formation nor local dedifferentiation and proliferation have been detected, which is probably due to the high morphogenetic plasticity of the tissue. Regeneration in O. lobularis goes through cell transdifferentiation and through the processes, when lost body parts are replaced by the remodeling of the remaining tissue. Morphogenesis during ectosome regeneration in O. lobularis is correlated with its true epithelial organization. Knowledge of the morphological basis of morphogenesis during Oscarella regeneration could have important implications for our understanding of the diversity and evolution of regeneration mechanisms in metazoans, and is a strong basis for future investigations with molecular-biological approaches.

The biology of choanocytes and choanocyte chambers and their role in the sponge stem cell system

“…queenslandica, it has been reported in a number of other species (Alexander et al, 2015;Borisenko et al, 2015;Ereskovsky et al, 2015) and could be occurring in A. queenslandica as well. If this was the case, genes involved in these processes would not be identified as differentially expressed (e.g.…”

“…Pinacocytes have also been observed to transdifferentiate in response to wounds as well as having the capacity to proliferate, although proliferation in pinacocytes is possibly a rare event (Alexander et al, 2015;Borisenko et al, 2015;Ereskovsky et al, 2015). To investigate the full capacity and potential behavior of sponge cell types through transcriptomes, the quartile expression analysis applied here shows all of the genes that are expressed (in contrast with differentially expressed) in each cell type.…”

“…As choanocytes are involved in regeneration in many sponge species as well (Alexander et al, 2015;Borisenko et al, 2015;Ereskovsky et al, 2015), they may have an analogous role in the sponge body as quiescent stem cell populations of some tissues found in other animals (Li and Clevers, 2010;Buczacki et al, 2013), that respond to tissue damage with proliferation and transdifferentiation. I propose that in A. queenslandica and potentially other species, choanocytes are a crucial part of the stem cell system, forming a differentiationdedifferentiation cycle with archeocytes and assisting in the growth of the sponge as well as increasing and maintaining the stem cell population.…”

“…However, regeneration in many sponge species involves reorganization and transdifferentiation of the cells in close proximity to the wound, without a marked increase in proliferation (Harrison, 1972;Boury-Esnault, 1976;Simpson, 1984;Smith and Hildemann, 1986;Louden et al, 2007;Borisenko et al, 2015;Ereskovsky et al, 2015). In fact, a recent study on Halisarca caerulea showed that proliferation rates in close proximity to the wound decrease during regeneration (Alexander et al, 2015), most likely due to the energy cost of regeneration (Koopmans et al, 2011).…”

“…Archeocytes are multifunctional, amoebocytic cells that are pluripotent and capable of self-renewal; they are likely the predominant stem cell in sponges (De Sutter and Van de Vyver, 1977;Müller et al, 2006;Funayama, 2008Funayama, , 2010Okamoto et al, 2012). Choanocytes are also highly proliferative and can transdifferentiate into somatic and germ cells in a range of contexts including tissue regeneration, juvenile growth and remodeling, and sexual reproduction (Simpson, 1984;Paulus and Weissenfels, 1986;Leys and Ereskovsky, 2006;Funayama, 2010;Alexander et al, 2014;Nakanishi et al, 2014;Borisenko et al, 2015;Ereskovsky et al, 2015). Unlike many other metazoan stem cells, both archeocytes and choanocytes have additional specializations and physiological functions, including the capture of food by choanocytes and transportation of nutrients by archeocytes (Simpson, 1984;Funayama et al, 2005).…”