Multipotent epithelial cells in the process of regeneration and asexual reproduction in colonial tunicates

Abstract

The cellular and molecular features of multipotent epithelial cells during regeneration and asexual reproduction in colonial tunicates are described in the present study. The epicardium has been regarded as the endodermal tissue-forming epithelium in the order Enterogona, because only body fragments having the epicardium exhibit the regenerative potential. Epicardial cells in Polycitor proliferus have two peculiar features; they always accompany coelomic undifferentiated cells, and they contain various kinds of organelles in the cytoplasm. During strobilation a large amount of organelles are discarded in the lumen, and then, each tissue-forming cell takes an undifferentiated configuration. Septum cells in the stolon are also multipotent in Enterogona. Free cells with a similar configuration to the septum inhabit the hemocoel. They may provide a pool for epithelial septum cells. At the distal tip of the stolon, septum cells are columnar in shape and apparently undifferentiated. They are the precursor of the stolonial bud. In Pleurogona, the atrial epithelium of endodermal origin is multipotent. In Polyandrocarpa misakiensis, it consists of pigmented squamous cells. The cells have ultrastructurally fine granules in the cytoplasm. During budding, coelomic cells with similar morphology become associated with the atrial epithelium. Then, cells of organ placodes undergo dedifferentiation, enter a cell division cycle, and commence morphogenesis. Retinoic acid-related molecules are involved in this dedifferentiation process of multipotent cells. We conclude that in colonial tunicates two systems support the flexibility of tissue remodeling during regeneration and asexual reproduction; dedifferentiation of epithelial cells and epithelial transformation of coelomic free cells.

Cell proliferation dynamics of somatic and germline tissues during zooidal life span in the colonial tunicateBotryllus primigenus

“…The reserve cells are also known as stem cells, which include the multipotent adult progenitor cells (MAPCs) in mammals (Jiang et al, 2002) and the crypt cells in the vertebrate small intestine (Potten and Loeffler, 1987;Ishizuya-Oka, 2007). Another example of formative tissue is multipotent epithelium such as the peritoneum in bryozoans (Brien, 1968), the coelomic epithelium in sea cucumbers (Mashanov et al, 2005), and certain types of mesodermal and endodermal epithelia in colonial tunicates (Kawamura et al, 2008). These epithelial cells change the cell fate directly without cell dissociation or blastema formation.…”

“…The inner vesicle plays a key role in renewing and remodeling the body architecture ( Fig. 1; for reviews, Berrill, 1950a;Manni et al, 2007;Kawamura et al, 2008). In Poly-androcarpa misakiensis, the cell proliferation kinetics of the multipotent epithelium has been examined only at the early stages of bud development (Kawamura and Nakauchi, 1986b;Kawamura et al, 1988).…”

Germline cell formation and gonad regeneration in solitary and colonial ascidians

“…In the order Enterogona, this mesenchymal space is situated in the abdomen and delimited by the epicardium and the epidermis (see Fig. 1a,b in Kawamura et al, 2008a). In Ciona, the epicardium develops into the perivisceral epithelium to encircle the digestive tract, so that the mesenchymal space is mainly confined to the perivisceral region.…”

“…In ascidians, the gonads are located in the major mesenchymal space of the adult zooid (Kawamura et al, 2008a). In the order Enterogona, this mesenchymal space is situated in the abdomen and delimited by the epicardium and the epidermis (see Fig.…”

“…The ascidian embryo is a typical example of determinative or mosaic development (Satoh, 1994). However, after metamorphosis somatic cells in some species show the remarkable developmental flexibility such as regeneration (Brien, 1968, Carnevali andBurighel, 2010) and asexual development (Manni et al, 2007, Kawamura et al, 2008a. Due to their phylogenetic position and well characterized embryonic development, ascidians represent excellent models to study the germline segregation from soma.…”