First‐generation neuronal precursors in the crayfish brain are not self‐renewing

Abstract

Adult-born neurons in crayfish (Procambarus clarkii) are the progeny of 1st-generation precursor cells (functionally analogous to neuronal stem cells in vertebrates) that are located in a neurogenic niche on the ventral surface of the brain. The daughters of these precursor cells migrate along the processes of bipolar niche cells to proliferation zones in the cell clusters where the somata of the olfactory interneurons reside. Here they divide again, producing offspring that differentiate into olfactory local and projection neurons. The features of this neuronal assembly line, and the fact that it continues to function when the brain is isolated and perfused or maintained in organotypic culture, provide opportunities unavailable in other organisms to explore the sequence of cellular and molecular events leading to the production of new neurons in adult brains. Further, we have determined that the 1st-generation precursor cells are not a self-renewing population, and that the niche is, nevertheless, not depleted as the animals grow and age. We conclude, therefore, that the niche is not a closed system and that there must be an extrinsic source of neuronal stem cells. Based on in vitro studies demonstrating that cells extracted from the hemolymph are attracted to the niche, as well as the intimate relationship between the niche and vasculature, we hypothesize that the hematopoietic system is a likely source of these cells.

Adult Neurogenesis: Lessons from Crayfish and the Elephant in the Room

“…Niche cells, including the 1st-generation neural precursors, are distinctive because they label for glutamine synthetase. The 1st-generation precursors divide in the niche, producing 2nd-generation precursors that migrate along fibrous streams formed by the processes of bipolar niche cells, until they reach proliferation zones in cell cluster 9 or 10 [Benton et al, , 2013 ( fig. 1 ).…”

“Crustacea”: Decapoda – Astacida

“…In a follow-up study, Chaves da Silva et al ( 2012 showed that the anterior proliferation centre is located within the cor frontale , an accessory heart which pumps hemolymph to the brain via the cerebral artery, thus providing a direct link to the neurogenetic niche. In a remarkable cell culture experiment, Benton et al ( 2013 ) succeeded in co-culturing freshly dissected crayfi sh brains with hematocytes that were previously labelled with a vital dye (CellTracker). In the majority of their experiments, labelled hematocytes were taken up in the neurogenetic niche after 6 h of co-cultivation.…”

“…In the majority of their experiments, labelled hematocytes were taken up in the neurogenetic niche after 6 h of co-cultivation. In summary, Benton et al ( 2013 ) suggested that their experimental evidence shows that the pool of cells within the crayfi sh niche is not selfrenewing but that multipotent stem cells from the hematopoietic tissue are the source replenishing the niche cell pool. In this view, the niche is a system that transforms multipotent blood stem cells into the fi rst-generation neuron precursor cells (review in Sandeman et al 2015 ).…”

Evolutionary Developmental Biology of Invertebrates 4

“…Beginning with studies by Harzsch and Dawirs ( 1996b ) and Schmidt ( 1997 ), it is now well known that a life-long generation of new olfactory interneurons that is driven by a persisting neurogenic niche is a characteristic feature of the decapod crustacean central olfactory pathway, and today, this is without question the hottest topic in crayfi sh developmental biology (Beltz and Sandeman 2003 ;Schmidt 2007aSchmidt , b , 2014Sullivan et al 2007a , b ;Beltz et al 2011 ;Sandeman et al 2011Sandeman et al , 2014Benton et al 2013 ). In vivo application of the S-phase-specifi c proliferation marker BrdU showed continuous mitotic activity within a proliferation zone (the lateral proliferation zone) associated with a cluster of olfactory interneurons (cluster 10; terminology of Sandeman et al 1992 ) that persisted from larval into juvenile stages of the brachyuran crab Hyas araneus (Harzsch and Dawirs 1996b ).…”

“…Noonin et al ( 2012 ) found a specialised region within crayfi sh hematopoietic tissue, the "anterior proliferation centre (APC)", which is located close to the brain and contains multipotent stem cells. In a remarkable cell culture experiment, Benton et al ( 2013 ) succeeded in co-culturing freshly dissected crayfi sh brains with hematocytes that were previously labelled with a vital dye (CellTracker). In a remarkable cell culture experiment, Benton et al ( 2013 ) succeeded in co-culturing freshly dissected crayfi sh brains with hematocytes that were previously labelled with a vital dye (CellTracker).…”