Cells from the Immune System Generate Adult-Born Neurons in Crayfish

Benton, Jeanne L.; Kery, Rachel; Li, Jingjing; Noonin, Chadanat; Söderhäll, Irene; Beltz, Barbara S.

doi:10.1016/j.devcel.2014.06.016

Cited by 61 publications

(114 citation statements)

References 39 publications

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“…Evidence to support this hypothesis is shown in Figure 3, where in situ hybridization for CHF mRNA clearly shows cells with and without CHF expression (a marker for SGCs) (Figure 3). Recent studies have also shown a link between the immune system and adult neurogenesis in crayfish; therefore, cells within the APC and/or HPT likely give rise to neuronal precursors (Beltz et al, 2015(Beltz et al, , 2011Benton et al, 2014). However, to obtain a clear picture of how commitment and differentiation are regulated in this tissue, it is absolutely necessary to identify additional markers for the different stages of development into different mature hemocyte types, as illustrated in Figure 3.…”

Section: Hemocyte Lineages and Releasementioning

confidence: 99%

Crustacean hematopoiesis

Söderhäll

2016

Developmental & Comparative Immunology

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Crustacean hemocytes are important mediators of immune reactions, and the regulation of hemocyte homeostasis is of utmost importance for the health of these animals. This review discusses the current knowledge on the lineages, synthesis and differentiation of hemocytes in crustaceans. Hematopoietic tissues, their origins, and the regulation of hematopoiesis during molting, seasonal variation and infection are discussed. Furthermore, studies concerning the molecular regulation of hemocyte formation in crustaceans are also described, and the different lineages and their molecular markers are discussed and compared with several insect species. Signaling pathways and the regulation of hematopoiesis by transcription factors are typically conserved among these arthropods, whereas cytokines and growth factors are more variable and species specific. However, considering the great diversity among the crustaceans, one should be cautious in drawing general conclusions from studies of only a few species.2

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Section: Hemocyte Lineages and Releasementioning

confidence: 99%

Crustacean hematopoiesis

Söderhäll

2016

Developmental & Comparative Immunology

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138

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“…Moreover, increasing description of the nervous regulation of hematopoietic function, together with the putative importance of the relationship between SVZ vasculature and NSCs, seems to be the dawn of an interpenetration of both systems. Likewise, recent findings demonstrating that crayfish neurons are generated from the immune system is another example of this crisscross (Benton et al, 2014). We therefore suggest that in mammals, the interpenetration of both systems relies, at least partly, on neural crest derivatives present in bone marrow.…”

Section: Discussionmentioning

confidence: 87%

Are neural crest stem cells the missing link between hematopoietic and neurogenic niches?

Coste

Neirinckx

Gothot

et al. 2015

Front. Cell. Neurosci.

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Hematopoietic niches are defined as cellular and molecular microenvironments that regulate hematopoietic stem cell (HSC) function together with stem cell autonomous mechanisms. Many different cell types have been characterized as contributors to the formation of HSC niches, such as osteoblasts, endothelial cells, Schwann cells, and mesenchymal progenitors. These mesenchymal progenitors have themselves been classified as CXC chemokine ligand (CXCL) 12-abundant reticular (CAR) cells, stem cell factor expressing cells, or nestin-positive mesenchymal stem cells (MSCs), which have been recently identified as neural crest-derived cells (NCSCs). Together, these cells are spatially associated with HSCs and believed to provide appropriate microenvironments for HSC self-renewal, differentiation, mobilization and hibernation both by cell-cell contact and soluble factors. Interestingly, it appears that regulatory pathways governing the hematopoietic niche homeostasis are operating in the neurogenic niche as well. Therefore, this review paper aims to compare both the regulation of hematopoietic and neurogenic niches, in order to highlight the role of NCSCs and nervous system components in the development and the regulation of the hematopoietic system.

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“…However, between days 8 and 14 after injection, BrdU + cells were once again observed in the niche. Adapted from Benton et al [2014].…”

Section: The Innate Immune System Of Crayfishmentioning

confidence: 99%

“…One of these concerns the functional relationships between adult neurogenesis and the immune system. The immune system plays critical roles in combating disease, in neural physiology and development, and in regulating neural stem cell (NSC) niches in both vertebrate and invertebrate species [Perry et al, 1993[Perry et al, , 2010Gonzalez-Perez et al, 2010Paolicelli et al, 2011;Benton et al, 2014]. However, while immunological mechanisms involved in adult neurogenesis are of potential broad importance to our understanding of how the normal brain is maintained throughout life, the contributions of the immune system to adult neurogenesis remain largely unknown.…”

Section: Introductionmentioning

confidence: 99%

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

Beltz

Brenneis²,

Benton³

2016

Brain Behav Evol

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The 1st-generation neural precursors in the crustacean brain are functionally analogous to neural stem cells in mammals. Their slow cycling, migration of their progeny, and differentiation of their descendants into neurons over several weeks are features of the neural precursor lineage in crayfish that also characterize adult neurogenesis in mammals. However, the 1st-generation precursors in crayfish do not self-renew, contrasting with conventional wisdom that proposes the long-term self-renewal of adult neural stem cells. Nevertheless, the crayfish neurogenic niche, which contains a total of 200-300 cells, is never exhausted and neurons continue to be produced in the brain throughout the animal's life. The pool of neural precursors in the niche therefore cannot be a closed system, and must be replenished from an extrinsic source. Our in vitro and in vivo data show that cells originating in the innate immune system (but not other cell types) are attracted to and incorporated into the neurogenic niche, and that they express a niche-specific marker, glutamine synthetase. Further, labeled hemocytes that undergo adoptive transfer to recipient crayfish generate cells in neuronal clusters in the olfactory pathway of the adult brain. These hemocyte descendants express appropriate neurotransmitters and project to target areas typical of neurons in these regions. These studies indicate that under natural conditions, the immune system provides neural precursors supporting adult neurogenesis in the crayfish brain, challenging the canonical view that ectodermal tissues generating the embryonic nervous system are the sole source of neurons in the adult brain. However, these are not the first studies that directly implicate the immune system as a source of neural precursor cells. Several types of data in mammals, including adoptive transfers of bone marrow or stem cells as well as the presence of fetal microchimerism, suggest that there must be a population of cells that are able to access the brain and generate new neurons in these species.

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Cells from the Immune System Generate Adult-Born Neurons in Crayfish

Cited by 61 publications

References 39 publications

Crustacean hematopoiesis

Crustacean hematopoiesis

Are neural crest stem cells the missing link between hematopoietic and neurogenic niches?

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

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