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The First Morphologic and Functional Characterization of Hemocytes In Fish and Shellfish Immunology 81 (2018) 423–429 Contents lists available at ScienceDirect Fish and Shellfish Immunology journal homepage: www.elsevier.com/locate/fsi Short communication The first morphologic and functional characterization of hemocytes in Hong Kong oyster, Crassostrea hongkongensis T Jun Lia,b,1, Yuehuan Zhanga,b,1, Fan Maoa,b, Yue Lina,b, Shu Xiaoa,b, Zhiming Xianga,b, ∗∗ ∗ Haitao Maa,b, Yang Zhanga,b, , Ziniu Yua,b, a CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, PR China b South China Sea Bio-Resource Exploitation and Utilization Collaborative Innovation Center, PR China ARTICLE INFO ABSTRACT Keywords: Hemocytes are the first line of defence of the innate immune system of molluscs. For the first time hemocytes of Crassostrea hongkongensis Crassostrea hongkongensis were morphologically and functionally characterized, identifying circulating cell types Hemocytes and studying their involvement in immune responses. In the present study, two main populations, hyalinocytes ROS and granulocytes, were characterized based on the presence or absence of cytoplasmic granules, using light and Phagocytosis electron microscopy (TEM), and flow cytometry analyses. Granulocytes are 7–13 μm in diameter and present Antibacterial activity evident cytoplasmic granules, and hyalinocytes, 6–15 μm in diameter, with a few or no granules. The mean number of circulating hemocytes in the hemolymph was 2.52 × 106 cells/mL. Flow cytometry indicated that both granulocytes and hyalinocytes showed cell phagocytosis and reactive oxygen species (ROS) production. However, phagocytosis and spontaneous production of reactive oxygen species (ROS) in granulocytes are much more active compared with hyalinocytes, which demonstrated that the granulocytes are the main hemocytes involved in the immune response of Hong Kong oyster. Moreover, the cell-free hemolymph showed antibacterial activity against Vibrio alginolyticus. Our results provide the basic information of hemocytes population of Hong Kong oyster for further investigations associated with innate immunity. 1. Introduction Although there is controversy concerning morphological descrip- tions of hemocytes types, two main hemocytes types, granulocytes and It is generally accepted that invertebrates lack an acquired immune hyalinocytes (agranulocytes), are generally recognized in bivalves system, but they do possess innate immunity, which consists of both based on the presence or absence of cytoplasmic granules [13,14]. cellular and humoral components of the circulatory system [1]. The Hyalinocytes contain few or no granules, and a round well-centred invertebrate innate immune system is the first line of defense against nucleus, whereas granulocytes, which contain granules and an ec- infection by a variety of pathogens [2]. The circulating hemocytes play centric, round to ovoid nucleus [15]. From a functional point of view, a central role in innate immunity. They are involved in recognition of both hyalinocytes and granulocytes can form pseudopodia, aggregate, invading foreign substances, encapsulation responses, phagocytosis, phagocyte particles and produce reactive oxygen species. However, production of reactive oxygen intermediates and secretion of in- granulocytes show higher phagocytic and higher levels of ROS flammatory cytokines [3–7]. In addition to their role in host defense, [7,16–18]. On the contrary, some authors have suggested the presence invertebrate hemocytes also perform various important physiological of only one cell type in mollusk hemolymph. Ottaviani et al. found only functions, including nutrient digestion, transportation, and distribution, one cell type in two different stages is present in Mytilus gallopro- digestion, wound healing, detoxification processes, shell mineralization vincialis, consistently with the Mix's one-cell-type model [19]. In Mac- and excretion [8–12]. Therefore, it is fundamentally important to rocallista nimbosa, flow cytometrically characterized hemocytes ap- characterize the circulating hemocytes in order to further understand peared as a unique population, both in terms of morphology and its role in oysters. intracellular parameters, but displayed high inter-individual variability ∗ Corresponding author. South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou, 510301, PR China. ∗∗ Corresponding author. South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou, 510301, PR China. E-mail addresses: [email protected] (Y. Zhang), [email protected] (Z. Yu). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.fsi.2018.05.062 Received 16 February 2018; Received in revised form 26 May 2018; Accepted 31 May 2018 Available online 01 June 2018 1050-4648/ © 2018 Elsevier Ltd. All rights reserved. J. Li et al. Fish and Shellfish Immunology 81 (2018) 423–429 [20]. In C. rhizophorae, the different subpopulations of hemocytes may 2.3. Light microscopy in reality be different stages of one type of cell, which accumulates granules and loses complexity as it degranulates in response to en- Immediately after withdrawal from C. hongkongensis,30μl whole vironmental stress [21]. On the other hand, even the existence of three hemolymph were loaded onto acid alcohol cleaned micro-scope slides. types of hemocytes has been hypothesized. Hemocytes of the sub- After adhesion to slides, hemocytes were fixed for 20 min in 4% par- tropical oysters Saccostrea kegaki, Ostrea circumpicta, C. ariakensis and aformaldehyde dissolved in PBS and then air-dried, mounted and ob- Hyotissa hyotis were classified into three main types: granulocytes, served under Olympus BH-2 microscope equipped with a video camera hyalinocytes and blast-like cells [22,23]. In addition, three populations (JVC 3-CCD) and ImageNT and Microimage software. of hemocytes (granulocytes, hyalinocytes and intermediate cells) and (hyalinocytes, granulocytes and serous cells) were observed in C. vir- 2.4. Subpopulations analysis of hemocytes ginica and Pinctada imbricate, respectively [24,25]. C.hongkongensis, is an endemic oyster species along the coastal of Flow cytometry analysis was performed as previously described the South China, with a cultivation history of a couple of centuries [29]. After withdrawal, hemolymph was diluted 1:1 in anti-clotting [26,27]. It is found in low-salinity estuaries from the Fujian to Guangxi solution and analyzed by a “FACSCalibur” flow cytometer (Becton provinces, with populations centered in the Guangdong province. Dickinson Biosciences, USA), equipped with a laser providing excitation However, another oyster, Crassostrea gigas is a eurythermal and eur- at 488 nm. Hemocytes populations were defined based on their forward yhaline species which widely distributes around the world and adapted scatter (FSC, correlated to size) and the side scatter (SSC, correlated to to the low-temperate and high-salinity waters of northern China. Due to internal complexity) properties. A total of 10,000 events were acquired its high economic and ecological value, C. hongkongensis aquaculture for each hemolymph sample. The analysis was identically repeated on 5 has been one of the largest coastal industries in this area, and the an- adult oysters. Data were processed using Cell Quest Software” (Becton nual production has recently reached almost one million tons. To pre- Dickinson Immunocytometry Systems, USA) and were displayed as dot vent disease associated mortality and subsequent management of the plot. Hong Kong oyster farming, understanding the immune system of C. hongkongensis is crucial. Hemocytes are thought to play a central role in 2.5. Phagocytic capability of hemocytes the recognition and elimination of foreign pathogens. The character- ization of hemocytes is essential to understand its immune system of C. Flow cytometry was used to measure the phagocytic activity of hongkongensis as well as its resistance to pathogenic infection. hemocytes of the Hongkong oyster as described previously [29]. To our knowledge, despite the availability of studies on the mor- Briefly, the collected hemolymph was incubated with fluorescent (FITC) phology and function of hemocytes in other molluscan species, no latex beads (1 μm, sigma, USA) for 1 h at 20 °C. After incubation, excess systematic information concerning circulating hemocytes morphology, of particles were removed by gently washing twice with PBS. Cell as- function and their involvement in immune response in the C. hon- sociated fluorescence was measured using flow cytometry (BD FACS- gkongensis has previously been reported. With the aim of providing the Calibur) at 530 nm (FL1). Hemocytes cell populations were defined first description of hemocytes from this oyster species, we characterized based on their size (FSC) and granularity (SSC) properties, and a total of C. hongkongensis hemocytes on the basis of their morphology and 10,000 events were acquired for each sample. The mean fluorescent functions, particularly potential immunological activities including the intensity in different populations was determined using the Cell Quest production of ROS, phagocytosis ability and antibacterial activity. Software. 2. Materials and methods 2.6. ROS production of hemocytes 2.1. Animals and hemolymph collection ROS were measured with the non-fluorescent probe 2′,7 ′- di- chlorofluorescein diacetate (DCFH-DA)
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