Abstract
BackgroundFor animal cells, ciliation and mitosis appear to be mutually exclusive. While uniciliated cells can resorb their cilium to undergo mitosis, multiciliated cells apparently can never divide again. Nevertheless, many multiciliated epithelia in animals must grow or undergo renewal. The larval epidermis in a number of marine invertebrate larvae, such as those of annelids, mollusks and nemerteans, consists wholly or in part of multiciliated epithelial cells, generally organized into a swimming and feeding apparatus. Many of these larvae must grow substantially to reach metamorphosis. Do individual epithelial cells simply expand to accommodate an increase in body size, or are there dividing cells amongst them? If some cells divide, where are they located?ResultsWe show that the nemertean pilidium larva, which is almost entirely composed of multiciliated cells, retains pockets of proliferative cells in certain regions of the body. Most of these are found near the larval ciliated band in the recesses between the larval lobes and lappets, which we refer to as axils. Cells in the axils contribute both to the growing larval body and to the imaginal discs that form the juvenile worm inside the pilidium.ConclusionsOur findings not only explain how the almost-entirely multiciliated pilidium can grow, but also demonstrate direct coupling of larval and juvenile growth in a maximally-indirect life history.
Highlights
For animal cells, ciliation and mitosis appear to be mutually exclusive
Growth of the nemertean pilidium larva is largely due to cell division in the axils Our first indication that cell proliferation, rather than changes in cell shape, is responsible for larval growth in the pilidium came from experiments in which we injected zygotes of the heteronemertean Micrura alaskensis with mRNA encoding a fluorescent protein fusion to the microtubule binding domain of Ensconsin (EMTB-3xGFP)
We suggest that the BrdU-positive cells in the axils and their progeny are responsible for the majority of the growth in the pilidium larva, and produce the dark regions shown in Figures 1 and 2
Summary
Ciliation and mitosis appear to be mutually exclusive. While uniciliated cells can resorb their cilium to undergo mitosis, multiciliated cells apparently can never divide again. The larval epidermis in a number of marine invertebrate larvae, such as those of annelids, mollusks and nemerteans, consists wholly or in part of multiciliated epithelial cells, generally organized into a swimming and feeding apparatus. An obvious example is the vertebrate airway epithelium, which is lined by cells bearing multiple cilia, but must retain the ability to replace damaged cells [8,9] Another example is the planktonic larvae of benthic marine invertebrates, many of which swim and feed using ciliated organs, and, at the same time, dramatically increase in size over the course of larval life [10]. Larval epithelia of deuterostomes, such as sea urchins, are typically composed of uniciliated cells that can divide after temporarily resorbing the cilium [5] Such larvae require very many cells to swim and feed efficiently. Larvae of annelids and mollusks that swim using multiciliated cells typically have non-ciliated regions, which could be responsible for the growth of the ciliated organs [10,11,12]
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