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Invertebrate hematopoiesis: an anterior proliferation centre as a link between the hematopoietic tissue and the brain
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
Aquatic Molecular Genetics and Biotechnology Laboratory, National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Bangkok.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
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2012 (English)In: Stem Cells and Development, ISSN 1547-3287, E-ISSN 1557-8534, Vol. 21, no 17, 3173-3186 p.Article in journal (Refereed) Published
Abstract [en]

During evolution, the innate and adaptive immune systems developed to protect organisms from nonself substances. The innate immune system is phylogenetically more ancient and is present in most multicellular organisms, whereas adaptive responses are restricted to vertebrates. Arthropods, lack the blood cells of the lymphoid lineage, and oxygen-carrying erythrocytes, making them suitable model animals to study the regulation of the blood cells of the innate immune system. Many crustaceans have a long life span and need to continuously synthesize blood cells, in contrast to many insects. The hematopoietic tissue (HPT) of Pacifastacus leniusculus provides a simple model to study hematopoiesis because the tissue can be isolated and the proliferation of stem cells and their differentiation can be studied both in vivo and in vitro. Here we demonstrate new findings of a physical link between the HPT and the brain. Actively proliferating cells were localized to an anterior proliferation centre (APC) in the anterior part of the tissue near the area linking the HPT to the brain, whereas more differentiated cells were detected in the posterior part. The central areas of HPT expand in response to lipopolysaccharide-induced blood loss. Cells isolated from the APC divide rapidly and form cell clusters in vitro; conversely, the cells from the remaining HPT form monolayers, and they can be induced to differentiate in vitro. Our findings offer an opportunity to learn more about invertebrate hematopoiesis and its connection to the central nervous system and thereby to obtain new information about the evolution of different blood and nerve cell lineages.

Place, publisher, year, edition, pages
2012. Vol. 21, no 17, 3173-3186 p.
National Category
Research subject
URN: urn:nbn:se:uu:diva-174038DOI: 10.1089/scd.2012.0077ISI: 000310840500011PubMedID: 22564088OAI: oai:DiVA.org:uu-174038DiVA: diva2:565204
Swedish Research Council, 621-2011-4797; 621-2009-5715; 319-2010-6250Formas, 223.2011-606
Available from: 2012-11-06 Created: 2012-05-10 Last updated: 2013-11-06Bibliographically approved
In thesis
1. Melanization and Hemocyte Homeostasis  in the Freshwater Crayfish, Pacifastacus leniusculus
Open this publication in new window or tab >>Melanization and Hemocyte Homeostasis  in the Freshwater Crayfish, Pacifastacus leniusculus
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Blood cells or hemocytes play important roles in immunity. They are a major source of many immune-related molecules such as antibodies in adaptive immunity of vertebrates and prophenoloxidase (proPO) in invertebrates. In the crayfish Pacifastacus leniusculus, the proPO-system has been reported to be an important component of immune responses against microorganisms. In this study, several mutant strains of Aeromonas hydrophila were used to reveal that LPS (lipopolysaccharide) is an important factor for the pathogenicity of A. hydrophila, strongly inducing the proPO system and melanization. This proPO activating system is a multistep process, which has to be tightly controlled to avoid the harmful side effects of toxic intermediates. Many regulating factors have been reported to fine-tune the proPO-system. In this study, the cleavage of caspase-1-like activity was shown to be a novel negative regulator of PO activity in crayfish. Moreover, the fragments obtained by cleavage of proPO by the proPO-activating enzyme and caspase-1-like protein increased bacterial clearance. Thus, the peptides generated also have important biological functions.

In addition to being a source of immune proteins, hemocytes also participate in phagocytosis, encapsulation, and nodulation. An infection normally causes a reduction of hemocyte numbers. Consequently, hemocyte homeostasis is important for maintaining appropriate hemocyte numbers in the circulation of the animal. This study shows that the reactive oxygen species level in the anterior proliferation center of crayfish hematopoietic tissue (HPT), together with cell proliferation, was increased during infection. Pl-β-thymosins were proposed to be involved in hemocyte homeostasis by increasing stem cell migration and thus increasing the circulating hemocyte number. Crayfish hemocyte numbers, as well astakine (Ast1 and Ast2) expression in hemocytes and HPT, were previously shown to be under circadian regulation. Here, we show that Ast1, Ast2, and proPO exhibit rhythmic expression in the crayfish brain similarly to their orthologs, prokineticin 1, prokineticin 2 and tyrosinase, respectively, in the zebrafish brain. Tyrosinase expression was detected in zebrafish brain cells while PO-positive cells were identified as hemocytes that had infiltrated into the crayfish brain. Therefore, this information suggests a close relationship between crayfish hemocytes and the crayfish brain as well as vertebrate neurons.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. 48 p.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1086
melanization, prophenoloxidase, caspase, hematopoiesis, thymosin, astakine, circadian rhythm, reactive oxygen species, tyrosinase, prokineticin
National Category
urn:nbn:se:uu:diva-209209 (URN)978-91-554-8774-4 (ISBN)
Public defence
2013-11-28, Lindahlssalen, EBC, Norbyvägen 18A, Uppsala, 10:00 (English)
Available from: 2013-11-06 Created: 2013-10-15 Last updated: 2016-05-09

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Noonin, ChadanatLin, XionghuiSöderhäll, KennethSöderhäll, Irene
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