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Invertebrate and vertebrate species have many unusual cellular structures, such as long- or short-lived cell-in-cell structures and coenocytes. Coenocytes (often incorrectly described as syncytia) are multinuclear cells derived, unlike syncytia, not from the fusion of multiple cells but from multiple nuclear divisions without cytokinesis. An example of a somatic coenocyte is the coenocytic blastoderm in Drosophila. An astonishing property of coenocytes is the ability to differentiate the nuclei sharing a common cytoplasm into different subpopulations with different fate trajectories. An example of a germline coenocyte is the oogenic precursor of appendicularian tunicates, which shares many features with the somatic coenocyte of Drosophila. The germline coenocyte (coenocyst) is quite an unexpected structure because in most animals, including Drosophila, Xenopus, and mice, oogenesis proceeds within a group (cyst, nest) of sibling cells (cystocytes) connected by the intercellular bridges (ring canals, RCs) derived from multiple divisions with incomplete cytokinesis of a progenitor cell called the cystoblast. Here, I discuss the differences and similarities between cystocyte-based and coenocyst-based oogenesis, and the resemblance of coenocystic oogenesis to coenocytic somatic blastoderm in Drosophila. I also describe cell-in-cell structures that although not mechanistically, cytologically, or molecularly connected to somatic or germline coenocytes, are both unorthodox and intriguing cytological phenomena rarely covered by scientific literature.
Fig. 1. Cell-in-cell structures.
Cell-in-cell structures can be short-lived (A, B) or longer-lasting (C). (A) Leukocyte passage through the endothelium when the engulfed leukocyte remains in the endothelial cell for a short time before being released on the other side of the endothelial barrier. (B) A T cell ingested by a melanoma cell. After a short time, the T cell is digested through the lysosome pathway, and released nutrients nourish the host cell. (C) A longer-lasting cell-in-cell structure when thymocytes are engulfed by the thymic nurse cell that not only nourishes them, but also performs negative/positive selection releasing mature, antigen-specific, self-tolerant T cells. Thymic nurse cells are epithelial cells that express MHC Class I and MHC Class II antigens. The interaction of these antigens with the developing thymocytes determines whether the thymocyte undergoes positive or negative selection. Thymocytes expressing T cell receptors (TCR) with affinity to MHC class I and II molecules are positively selected while those expressing potentially harmful TCR are deactivated and destroyed (negative selection) by the lysosomal pathway.
Fig. 2. Drosophila coenocytic (syncytial) blastoderm.
(A) After egg fertilization, the zygotic nucleus divides producing a population of nuclei within the common eggcytoplasm forming the coenocytic (syncytial) blastoderm. In the next step, some of the nuclei migrate to the eggposterior pole where the pole plasm containing germ cell determinants is located. These nuclei will eventually form the pole cells, which are the precursor of future germline. Most somatic nuclei move to the cell cortex where they eventually cellularize. Some of the somatic nuclei remain in the yolky center part of the egg as the yolk nuclei, which become polyploid, but their exact function remains unknown. (B) Blastoderm cellularization starts from the nucleus moving to the cortical, yolkless layer of cytoplasm. Once there, nucleus and its associated centrosomes induce the formation of under-membrane actin cup, which is followed by the elongation of aster microtubules, invagination of cellular membrane, and redistribution of actin along the membrane. Eventually, the cellular membrane completely encloses the nucleus and separates cell at the blastoderm surface.
Fig. 3. Germline cysts.
(A) The linear cysts form during development of the telotrophic ovaries in the rove beetle Creophilus maxillosus. The first division of the cystoblast produces two cystocytes connected by a ring canal (RC; marked by a black rectangle): the pro-oocyte, always remaining in contact with the somatic cell, and the pro-nurse cell. Next, several synchronous divisions produce a chain of cells connected by RCs. In each chain of sibling cells, the pro-oocyte is always located at the top of somatic cells. The, so far, unidentified signal emanating from somatic cells induces ribosomal DNA amplification, resulting in a large rDNA body (marked by a blue sphere) in the pro-oocytenucleus. The pro-oocyte becomes the oocyte and the remaining cystocytes undergo endoreplication and become the nurse cells. At each division, the rDNA body always segregates to the pro-oocyte. For a detailed description of Creophilus oogenesis see Kloc (2019). (B) The branched cystocyst in Drosophila. In the 16-cell cyst, only the two oldest cystocytes have four RCs each. One of these cystocytes becomes the oocyte, while the remaining cystocytes endoreplicate and become nurse cells. (C) In the annelid worm Enchytraeus albidus, a female germline cyst contains 15 nurse cells and one oocyte, all connected by individual RCs to the anuclear island of cytoplasm, the cytophore. (D) In some arachnids, the germline cyst contains the growing oocytes connected by the individual RCs to a centrally located large nurse cell with a large and branched nucleus. (E) The RCs are stabilized intercellular bridges derived from incomplete cytokinesis of cystocytes. Drosophila RCs contain various proteins such as actin, Hts, and Kelch, and their size is regulated by the Msn kinase.
Fig. 4. Coenocystic oogenesis in appendicularian tunicates.
(A) Existing model of appendicularian oogenesis according to Ganot et al. (2007a, 2007b). Phase 1. The coenocyst, which is positive for germline marker Vasa protein, contains many nuclei embedded in a common cytoplasm. It originates from nuclear divisions without cytokinesis. Phase 2. Nuclei segregate and differentiate into two distinct subpopulations: smaller pro-oocyte nuclei and larger (endoreplicating) pro-nurse cell nuclei. Phase 3. Pro-oocytes become separated from the common cytoplasm but remain connected to it by ring canals (RCs). Phase 4. Some of the pro-oocytes are selected as the future oocytes. They grow using nutrients from a common cytoplasm and become the oocytes, while the nuclei of non-selected pro-oocytes return to the common cytoplasm and eventually, like the pro-nurse nuclei, endoreplicate their DNA. Phase 5. Oocytes connected to the coenocyst by RCs grow further, while the remaining nuclei degrade. (B) Proposed modified model. The coenocyst progenitor (an equivalent of the cystoblast), the coenoblast, undergoes nuclear divisions without cytokinesis, producing a multinuclear coenocyst. After nuclear segregation into pro-oocytes and pro-nurse cell fate, the pro-oocytes become sequestered by the invagination of coenocyst membrane underlined by actin (red) in the process reminiscent of cellularization of coenocytic blastoderm in Drosophila. However, in contrast to the Drosophila blastoderm, the cellularization of pro-oocytes is incomplete and leaves RC-like intercellular connections between the pro-oocyte and coenocyst cytoplasm. These RC-like bridges serve to transport nutrients from the common cytoplasm to the growing oocytes.
