Region-specific regulation of stem cell-driven regeneration in tapeworms

Abstract

Tapeworms grow at rates rivaling the fastest-growing metazoan tissues. To propagate they shed large parts of their body; to replace these lost tissues they regenerate proglottids (segments) as part of normal homeostasis. Their remarkable growth and regeneration are fueled by adult somatic stem cells that have yet to be characterized molecularly. Using the rat intestinal tapeworm, Hymenolepis diminuta, we find that regenerative potential is regionally limited to the neck, where head-dependent extrinsic signals create a permissive microenvironment for stem cell-driven regeneration. Using transcriptomic analyses and RNA interference, we characterize and functionally validate regulators of tapeworm growth and regeneration. We find no evidence that stem cells are restricted to the regeneration-competent neck. Instead, lethally irradiated tapeworms can be rescued when cells from either regeneration-competent or regeneration-incompetent regions are transplanted into the neck. Together, the head and neck tissues provide extrinsic cues that regulate stem cells, enabling region-specific regeneration in this parasite.

The esophageal gland mediates host immune evasion by the human parasiteSchistosoma mansoni

“…In flatworms, differentiated cells do not proliferate; thus, genes regulated in a cell cycle-dependent manner, such as histone 2b ( h2b ), can be used as generic stem cell markers ( 6 , 15 – 17 ). Using h2b as a marker of these cells in cercariae ( Fig.…”

Articulating the “stem cell niche” paradigm through the lens of non-model aquatic invertebrates

“…Several species of Platyhelminthes and Acoelomorpha (acoel flatworms) exhibit extensive regenerative capacities, up to whole-body regeneration [110][111][112][113][114]. This capacity requires a group of ASCs called neoblasts [115][116][117] that are located within the parenchymal tissue of many freeliving (e.g., [111,118]) and parasitic flatworms [119].…”

“…In well-studied species, such as Schmidtea mediterranea, the neoblasts constitute up to one-third of the animal's cells [120] and are known to be the only proliferating cells in the adult body. Regeneration properties have been thoroughly examined in a few species: the Platyhelminthes S. mediterranea [111,121], Dugesia japonica [122], the tapeworm Hymenolepis diminuta [114], and the acoels Isodiametra pulchra [26] and Hofstenia miamia [123,124]. Early experiments demonstrated that all new somatic cells emerging during tissue maintenance, as well as during regeneration, originated from neoblasts [111,125].…”

Screwed up: Spirality of segments and other iterated structures suggest an underlying principle of seriality in bilaterians

“…For instance, proglottids lack the set of characters that has been used to define segments (see Scholtz, 2002Scholtz, , 2010Scholtz, , 2020c. Furthermore, proglottids do not form by a combination of a pre-anal proliferation zone and an anteroposterior differentiation of segments, but rather by stem cells that form a growth zone in the neck area behind the anterior scolex; the differentiation follows a posteroanterior gradient (Koziol et al, 2016;Olson, 2008;Rozario et al, 2019). Likewise, the formation of the cuticular annuli in nematodes follows a different pathway compared with annelids and arthropods.…”