Table of Contents:

Wound Healing

In annelids, w'ound healing is elicited by nonlethal amputation across the main body axis. It consists of an initial fast wound-sealing response followed by a slower reepi- thelialization process.

Wound sealing is achieved by rapid contraction of the circular muscles proximal to the amputation plane, which brings together the edge of the wound while closing off the exchange between the external and internal environments (Bely 2014). Sealing of the w'ound is sometimes aided by extrusion of the gut tissues. This initial muscular response is complemented by the migration of coelomic cells to the wound site to form a mass knowm as a w'ound plug (Stein and Cooper 1983).

Wound sealing is followed by reepithelialization: the severed edges of the epidermis fuse together over the wound, forming a continuous epithelial sheet. Internally, the severed gut edges also fuse, forming a blind end. In some cases, the edges of the gut and body wall might fuse instead, sealing the wound and restoring the gut outlet in the same step—as seen during posterior “open regeneration” in nereids (Kostyuchenko et al. 2019). The newly formed outer epithelial layer is usually called wound epithelium and is different in histological and ultrastructural details, including a lack of basement membrane and a modified extracellular matrix that may play key roles in triggering cell dedifferentiation and proliferation in adjacent tissues (Bely 2014). Although more studies specifically addressing the role of the w'ound- healing process in enabling the regenerative response in annelids are needed, it is likely that the wound epithelium and wound extracellular matrix play a pivotal function in regeneration, as found in many other phyla (Brockes and Kumar 2008).

Cell Migration

Wound healing and regeneration are achieved through changes in cell behavior, as cells are the main effectors of all developmental processes required to rebuild the lost structures. While many such processes are studied at the tissue or organ levels, two aspects of regeneration are best approached by looking at the cell level: cell migration (this section) and cell proliferation (next section).

Traditionally, cell migration during annelid regeneration has been studied through indirect observation of individuals fixed at different time points along the regenerative process. These provided static snapshots upon which cell dynamics were statistically inferred based on changes in spatial distribution of specific cell types; direct observation and quantification of cell migration through live imaging have only recently been reported (Zattara, Turlington, and Bely 2016).

Extensive cell migration can be seen within minutes to hours after injury in many annelids; this increased cell activity lasts for about 1 day after amputation and then subsides (Bely 2014). In vivo observations of cell migration during the first day of regeneration using time-lapse photomicrography in the clitellate Pristina leidyi found a suite of cell morphotypes showing distinctive sets of directional behaviors during the first day of regeneration, and in noninjured control animals (Zattara, Turlington, and Bely 2016). These morphotypes match reports from histological observations of other species, but despite several attempts to classify them, terminology and homology are still unclear, both between and within species (Herlant-Meewis 1964; Stein and Cooper 1983; Baskin 1974; Cornec et al. 1987; Vetvicka and Sima 2009; Bely 2014). A simple classification based on morphology and behavior is given in Table 10.1. These morphotypes may however only reflect transient behavioral states rather than differentiated cell types, as in vivo observations often show the presence of intermediate types, or a dynamic switch among morphologies.

Amoebocytes (Figure 10.3A-B) are amoeboid cells that move by extending pseudopodia along and between the surface of tissues like the gut, inner lining of the coelomic cavity, or between muscle and connective layers. They range in size from small (5-8 pm) to quite large (up to 30 pm). They may contain a variable number of cytoplasmic granules and are sometimes classified into granular (or granulocyte; Figure 10.3A) and hyaline (Figure Ю.ЗВ) amoebocytes. Amoebocytes most likely play a role in immune responses and in phagocytosis of pathogen invaders, foreign particles, and damaged cells.

Eleocytes (Figure 10.3C) are large (up to 40-60 pm), round cells containing vesicles or granules, similar to those found in the chloragogen cells that line the peritoneal surface of the gut in many annelids. They are present in nearly all annelids (Stein and Cooper 1983). They are believed to play roles in nutrition, excretion, and osmotic balance (Vetvicka and Sima 2009), although functions in immunity and regeneration have also been proposed (Liebmann 1942; Stein and Cooper 1983). Though typically found freely in the peritoneal cavity or clinging to septal or peritoneal tissues, eleocytes can attach to the epithelial linings, adopt a more amoeboid shape, and crawl over that substrate (Figure Ю.ЗС, lower panel).

Sarcolytes (Figure 10.3D) are small- to medium-sized (5-15 pm) hyaline cells that vary from spherical to rod-shaped and are free floating or attached to the peritoneal lining of the body wall. They derive from autolysis of muscle fibers near the wound site (Cornec et al. 1987; Zattara, Turlington, and Bely 2016), and are eventually phagocytized by amoebocytes.

Neoblasts ordissepimentary cells (Figure 10.3E) are small- to medium-sized (5-15 pm) spindle-shaped cells usually found sliding over the ventral nerve cord or along the peritoneal lining. Their role has been long debated (Randolph 1891; Krecker 1923; Stone 1932; Stephan-Dubois 1954; Bilello and Potswald 1974; Cornec et al. 1987; Tadokoro et al. 2006; Myohara 2012; Sugio et al. 2012; Zattara, Turlington, and Bely 2016). These cells are normally found on segmental septa and are characterized as spherical in shape with a large nucleus-to-cytoplasm ratio, suggesting they might not be fully differentiated. After amputation, they are thought to enlarge, adopt a spindle

TABLE 10.1

Cell Morphotypes Observed during Wound Healing and Regeneration

Cell Type

Size

Range

Features

Putative Function

Found in

Reference

Amoebocytes,

granular/granulocyte

5-30 pm

Small to large, irregular but often amoeboid in shape: few to many granular inclusions

Cellular immunity, phagocytosis

Polychaetes, Clitellates

Baskin 1974; Vetvicka and Sima 2009: Zattara, Turlington, and Bely 2016

Amoebocytes,

hyaline

5-30 pm

Small to large, irregular but often amoeboid in shape: no granules

Cellular immunity, phagocytosis

Polychaetes, Clitellates

Baskin 1974: Stein and Cooper 1983: Vetvicka and Sima 2009; Zattara. Turlington, and Bely 2016

Eleocytes

10^60

pm

Large, round, with numerous granular inclusions

Trophic, recycling of phagocy tized sarcolytes

Polychaetes, clitellates

Baskin 1974; Vetvicka and Sima 2009; Zattara, Turlington, and Bely 2016

Sarcolytes

5-15 pm

Small to medium, round or ovoid, hyaline; free or clinging from body wall

Free muscle cells, originated from body wall, usually phagocy tized by amoebocytes

Polychaetes, clitellates

Baskin 1974; Zattara, Turlington, and Bely 2016

Dissepimentary

cells/"neoblasts”

5-15 pm

Small to medium, spindle shaped, no granules: move by sliding over substrate

Progenitors of certain mesodermal structures (which ones is contested)

Clitellates

Randolph 1892: Krcckcr 1923: Cornec et al. 1987: Zattara, Turlington, and Bely 2016

Free coelornic cell types observed during wound healing and regeneration. The top row shows schematic depictions; middle and bottom row show examples from the cli- tellate Pristina leidyi. Scale bars

FIGURE 10.3 Free coelornic cell types observed during wound healing and regeneration. The top row shows schematic depictions; middle and bottom row show examples from the cli- tellate Pristina leidyi. Scale bars: 20 pm. Modified after Zattara, Turlington, and Bely 2016.

shape, and move to the dorsal surface of the ventral nerve cord, migrating toward the wound site, and accumulating there. Proposed functions vary from a relatively minor role as the source cells for new peritoneal lining to as far as claiming that they proliferate and differentiate in all kinds of mesodermal, ectodermal, and even endodermal tissue in the regenerate. These inferences are based mostly on static snapshots from histological sections; to date, in vivo imaging studies in a single clitellate species have supported presence and directional migration of neoblast-like cells, but gave no information on their origin or eventual fate. In non-clitellate annelids, migration of these cell types has been reported only for short distances, or not at all, indicating that any potential major role of neoblasts in regeneration would be an evolutionary innovation of clitellates, and not an ancestral annelid feature (Hill 1970; Potswald 1972; Paulus and Muller 2006; Bely 2014). Such a scenario is supported by the recent finding that cell migration to the wound site contributes materials to the regenerating tissues on the capitellid Capitella teleta, member of a lineage close to the base of the clitellates (Jong and Seaver 2017).

Current data strongly suggest that cell morphotypes are driven by their current function rather than by their cell lineage. Additional in vivo studies that combine time-lapse microscopy, cell ablation, and use of drugs inhibiting cell migration, performed across a wider range of species, are needed to better characterize cell types, their behavior, and their roles in wound healing, immunity, and regeneration in annelids.

 
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