Transcriptome Analysis of the White Body of the Squid Euprymna tasmanica with Emphasis on Immune and Hematopoietic Gene Discovery

Salazar, Karla A.; Joffe, Nina R.; Dinguirard, Nathalie; Houde, Peter; Castillo, Maria G.

doi:10.1371/journal.pone.0119949

Cited by 29 publications

(41 citation statements)

References 104 publications

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“…The white body is a multi-lobed organ that wraps around the optic bundle [22, 31]. Haematopoietic development in the white body was first described in the common octopus O. vulgaris by Cowden (1972) [98], who identified primary, secondary and tertiary leukoblasts in histological sections.…”

Section: Cephalopod Haematopoiesis and Haemocyte Functionmentioning

confidence: 99%

“…The larger cells were more phagocytic and produced a more intense respiratory burst than the smaller cells [26]. However, a similar study found three haemocyte types in O. vulgaris , which were described as hyalinocytes, granulocytes, and haemoblast-like cells [22]. Such discrepancies demonstrate a need for a standardized characterization of the haemocyte populations in cephalopods.…”

Section: Cephalopod Haematopoiesis and Haemocyte Functionmentioning

confidence: 99%

“…Haematopoiesis in molluscs is not a well-understood process; however, progress is being made in this area to define the networks of signalling pathways important for haemocyte development, as well as the endogenous factors that regulate haemocyte numbers [19–22]. Evidence so far indicates that major differences exist among the various molluscan classes in terms of haemocyte lineages and haematopoietic sites.…”

Section: Introductionmentioning

confidence: 99%

“…Other reported pericardial sites of gastropod haemocyte production include the external surface of the ctenidial/pulmonary and renal veins in the pericardial cavity [30]. In cephalopods, haemocytes are thought to originate from the white body, which is a multi-lobed organ that wraps around the optic bundle [22, 31], while in the bivalves, the irregularly folded structure (IFS) of the gills has been proposed as the site of haemocyte formation [21]. In many members of these molluscan groups, a haematopoietic site is yet to be described, and it is possible that more than one primary haematopoietic site exists within each of these groups.…”

Section: Introductionmentioning

confidence: 99%

“…Numerous cytokines, growth factors, receptors, intracellular signalling components, and homologs of transcription factors known to be involved in vertebrate haematopoiesis have been identified as part of genomic or transcriptional studies [19, 22, 32], or are assumed to be present in various molluscan groups [33]. These assumptions are based on sequence identity or immunoreactivity with antibodies raised against their vertebrate counterparts and sometimes a demonstration that they perform similar functions [16, 34].…”

Section: Introductionmentioning

confidence: 99%

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Haematopoiesis in molluscs: A review of haemocyte development and function in gastropods, cephalopods and bivalves

Pila

Sullivan

et al. 2016

Developmental & Comparative Immunology

110

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Haematopoiesis is a process that is responsible for generating sufficient numbers of blood cells in the circulation and in tissues. It is central to maintenance of homeostasis within an animal, and is critical for defense against infection. While haematopoiesis is common to all animals possessing a circulatory system, the specific mechanisms and ultimate products of haematopoietic events vary greatly. Our understanding of this process in non-vertebrate organisms is primarily derived from those species that serve as developmental and immunological models, with sparse investigations having been carried out in other organisms spanning the metazoa. As research into the regulation of immune and blood cell development advances, we have begun to gain insight into haematopoietic events in a wider array of animals, including the molluscs. What began in the early 1900’s as observational studies on the morphological characteristics of circulating immune cells has now advanced to mechanistic investigations of the cytokines, growth factors, receptors, signalling pathways, and patterns of gene expression that regulate molluscan haemocyte development. Emerging is a picture of an incredible diversity of developmental processes and outcomes that parallels the biological diversity observed within the different classes of the phylum Mollusca. However, our understanding of haematopoiesis in molluscs stems primarily from the three most-studied classes, the Gastropoda, Cephalopoda and Bivalvia. While these represent perhaps the molluscs of greatest economic and medical importance, the fact that our information is limited to only 3 of the 9 extant classes in the phylum highlights the need for further investigation in this area. In this review, we summarize the existing literature that defines haematopoiesis and its products in gastropods, cephalopods and bivalves.

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Section: Cephalopod Haematopoiesis and Haemocyte Functionmentioning

confidence: 99%

Section: Cephalopod Haematopoiesis and Haemocyte Functionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Haematopoiesis in molluscs: A review of haemocyte development and function in gastropods, cephalopods and bivalves

Pila

Sullivan

et al. 2016

Developmental & Comparative Immunology

110

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Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes/Vibrio fischeri symbiosis

2019

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The binary association between the squid, Euprymna scolopes, and its symbiont, Vibrio fischeri, serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, to V. fischeri is altered if the symbiont is removed from the light organ, suggesting that host colonization alters hemocyte recognition of V. fischeri. To investigate the influence of symbiosis on immune maturation during development, we characterized hemocyte binding and phagocytosis of V. fischeri and nonsymbiotic Vibrio harveyi from symbiotic (sym) and aposymbiotic (apo) juveniles, and wild‐caught and laboratory‐raised sym and apo adults. Our results demonstrate that while light organ colonization by V. fischeri did not alter juvenile hemocyte response, these cells bound a similar number of V. fischeri and V. harveyi yet phagocytosed only V. harveyi. Our results also indicate that long‐term colonization altered the adult hemocyte response to V. fischeri but not V. harveyi. All hemocytes from adult squid, regardless of apo or sym state, both bound and phagocytosed a similar number of V. harveyi while hemocytes from both wild‐caught and sym‐raised adults bound significantly fewer V. fischeri, although more V. fischeri were phagocytosed by hemocytes from wild‐caught animals. In contrast, hemocytes from apo‐raised squid bound similar numbers of both V. fischeri and V. harveyi, although more V. harveyi cells were engulfed, suggesting that blood cells from apo‐raised adults behaved similarly to juvenile hosts. Taken together, these data suggest that persistent colonization by the light organ symbiont is required for hemocytes to differentially bind and phagocytose V. fischeri. The cellular immune system of E. scolopes likely possesses multiple mechanisms at different developmental stages to promote a specific and life‐long interaction with the symbiont.

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Immunity in Molluscs: Recognition and Effector Mechanisms, with a Focus on Bivalvia

Gerdol

Gomez‐Chiarri

Castillo

et al. 2018

Advances in Comparative Immunology

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The study of molluscan immune systems, and in particular those of bivalve molluscs (clams, oysters, scallops, mussels, etc.) has experienced great growth in recent decades, mainly due to the needs of a rapidly growing aquaculture industry to manage the impacts of disease and the application of -omic tools to this diverse group of invertebrate organisms. Several unique aspects of molluscan immune systems highlighted in this chapter include the importance of feeding behavior and mucosal immunity, the discovery of unique levels of diversity in immune genes, and experimental indication of transgenerational immune priming. The development of comparative functional studies using natural and selectively bred disease-resistant strains, together with the potential but yet to be fully developed application of gene-editing technologies, should provide exciting insights into the functional relevance of immune gene family expansion and molecular diversification in bivalves. Other areas of bivalve immunity that deserve further study include elucidation of the process of hematopoiesis, the molecular characterization of hemocyte subpopulations, and the genetic and molecular mechanisms underlying immune priming. While the most important aspects of the immune system of the largest group of molluscs, gastropods (e.g., snails and slugs), are discussed in detail in Chap. 12, we also briefly outline the most distinctive features of the immune system of another fascinating group of marine molluscs, cephalopods, which include invertebrate animals with extraordinary morphological and behavioral complexity.

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Transcriptome Analysis of the White Body of the Squid Euprymna tasmanica with Emphasis on Immune and Hematopoietic Gene Discovery

Cited by 29 publications

References 104 publications

Haematopoiesis in molluscs: A review of haemocyte development and function in gastropods, cephalopods and bivalves

Haematopoiesis in molluscs: A review of haemocyte development and function in gastropods, cephalopods and bivalves

Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes/Vibrio fischeri symbiosis

Immunity in Molluscs: Recognition and Effector Mechanisms, with a Focus on Bivalvia

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