Adult neurogenesis in crayfish: Origin, expansion, and migration of neural progenitor lineages in a pseudostratified neuroepithelium

Abstract

Two decades after the discovery of adult-born neurons in the brains of decapod crustaceans, the deutocerebral proliferative system (DPS) producing these neural lineages has become a model of adult neurogenesis in invertebrates. Studies on crayfish have provided substantial insights into the anatomy, cellular dynamics, and regulation of the DPS. Contrary to traditional thinking, recent evidence suggests that the neurogenic niche in the crayfish DPS lacks self-renewing stem cells, its cell pool being instead sustained via integration of hemocytes generated by the innate immune system. Here, we investigated the origin, division and migration patterns of the adultborn neural progenitor (NP) lineages in detail. We show that the niche cell pool is not only replenished by hemocyte integration but also by limited numbers of symmetric cell divisions with some characteristics reminiscent of interkinetic nuclear migration.Once specified in the niche, first generation NPs act as transit-amplifying intermediate NPs that eventually exit and produce multicellular clones as they move along migratory streams toward target brain areas. Different clones may migrate simultaneously in the streams but occupy separate tracks and show spatio-temporally flexible division patterns. Based on this, we propose an extended DPS model that emphasizes structural similarities to pseudostratified neuroepithelia in other arthropods and vertebrates. This model includes hemocyte integration and intrinsic cell proliferation to synergistically counteract niche cell pool depletion during the animal's lifespan. Further, we discuss parallels to recent findings on mammalian adult neurogenesis, as both systems seem to exhibit a similar decoupling of proliferative replenishment divisions and consuming neurogenic divisions.

A New Protocol of Computer-Assisted Image Analysis Highlights the Presence of Hemocytes in the Regenerating Cephalic Tentacles of Adult Pomacea canaliculata

“…In the leech H. medicinalis , the neural cells synthesize immune-related factors that seem fundamental for microglial recruitment and the neural cord regeneration [ 44 , 45 ]. On the basis of the existing literature [ 9 , 10 , 12 , 31 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 ], it is tempting to speculate that the role of hemocytes in regenerating cephalic tentacle of P. canaliculata is not only that of scavenger cells removing the cell debris immediately after the amputation, but also to play an active role in the regrowth of neural and other tissue components. Further studies are necessary for gaining an in-depth comprehension of the roles played by hemocytes in the adult regeneration of P. canaliculata .…”

The Crustacean Antennule: A Complex Organ Adapted for Lifelong Function in Diverse Environments and Lifestyles

“…Loss of a portion of the antennule can modulate the rate of neurogenesis in the proliferation zone and speed the repair and recovery of the antennules (Harrison et al, 2001a(Harrison et al, , 2003(Harrison et al, , 2004. Coincident with this lifelong neurogenesis in the antennule is lifelong neurogenesis of interneurons in the brain regions receiving the OSN projections-the olfactory lobes (Sandeman et al, 2011;Schmidt, 2014;Brenneis and Beltz, 2020).…”

Methods to study organogenesis in decapod crustacean larvae II: analysing cells and tissues

“…17). The thymidine analogon 5-bromo-2-deoxyuridine (BrdU) is a wellknown S phase-specific marker to analyse neurogenesis in adult crustacean brains [139,140,[140][141][142][143]. This marker was also applied to study aspects of neurogenesis in late crustacean embryos and larvae such as the development of the ventral nerve cord [144][145][146], the brain [147][148][149] and the compound eyes [150][151][152].…”

“…BrdU-labelling has turned out a robust technique which can be used as a tool to analyse cell proliferation from crustacean embryos (review [1,2]) across the larvae to adult animals [139,140,[140][141][142][143]. However, when interpreting the results of the method presented here it has to be borne in mind that this technique labels DNA synthesis which is not necessarily equivalent to mitosis considering that cells may replicate their DNA without cell division to become polyploid.…”