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Enhanced Cellular Immunity in Shrimp (Litopenaeus Vannamei) After ‘Vaccination’

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Enhanced Cellular Immunity in Shrimp (Litopenaeus Vannamei) After ‘Vaccination’ Enhanced Cellular Immunity in Shrimp (Litopenaeus vannamei) after ‘Vaccination’ Edward C. Pope1., Adam Powell1., Emily C. Roberts1, Robin J. Shields1, Robin Wardle2, Andrew F. Rowley1* 1 Centre for Sustainable Aquatic Research, Department of Biosciences, College of Science, Swansea University, Swansea, United Kingdom, 2 Intervet/Schering – Plough Animal Health (Aquaculture), Aquaculture Centre, Saffron Walden, United Kingdom Abstract It has long been viewed that invertebrates rely exclusively upon a wide variety of innate mechanisms for protection from disease and parasite invasion and lack any specific acquired immune mechanisms comparable to those of vertebrates. Recent findings, however, suggest certain invertebrates may be able to mount some form of specific immunity, termed ‘specific immune priming’, although the mechanism of this is not fully understood (see Textbox S1). In our initial experiments, either formalin-inactivated Vibrio harveyi or sterile saline were injected into the main body cavity (haemocoel) of juvenile shrimp (Litopenaeus vannamei). Haemocytes (blood cells) from V. harveyi-injected shrimp were collected 7 days later and incubated with a 1:1 mix of V. harveyi and an unrelated Gram positive bacterium, Bacillus subtilis. Haemocytes from ‘vaccinated’ shrimp showed elevated levels of phagocytosis of V. harveyi, but not B. subtilis, compared with those from saline-injected (non-immunised) animals. The increased phagocytic activity was characterised by a significant increase in the percentage of phagocytic cells. When shrimp were injected with B. subtilis rather than vibrio, there was no significant increase in the phagocytic activity of haemocytes from these animals in comparison to the non-immunised (saline injected) controls. Whole haemolymph (blood) from either ‘immunised’ or non-immunised’ shrimp was shown to display innate humoral antibacterial activity against V. harveyi that was absent against B. subtilis. However, there was no difference in the potency of antibacterial activity between V. harveyi-injected shrimp and control (saline injected) animals showing that ‘vaccination’ has no effect on this component of the shrimp’s immune system. These results imply that the cellular immune system of shrimp, particularly phagocytosis, is capable of a degree of specificity and shows the phenomenon of ‘immune priming’ reported by other workers. However, in agreement with other studies, this phenomenon is not universal to all potential pathogens. Citation: Pope EC, Powell A, Roberts EC, Shields RJ, Wardle R, et al. (2011) Enhanced Cellular Immunity in Shrimp (Litopenaeus vannamei) after ‘Vaccination’. PLoS ONE 6(6): e20960. doi:10.1371/journal.pone.0020960 Editor: Sebastian D. Fugmann, National Institute on Aging, United States of America Received January 25, 2011; Accepted May 17, 2011; Published June 16, 2011 Copyright: ß 2011 Pope et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was partially supported by a pilot project grant from Intervet/Schering-Plough Animal Health (http://www.intervet.com) to A.F.R. and R.J.S. The funders contributed to the design of the study but had no role in data collection and analysis or preparation of the manuscript. Competing Interests: Intervet/Schering-Plough Animal Health currently manufacture and sell a vaccine (AquaVacTM VibromaxTM) for farmed shrimp that contains inactivated forms of several Vibrio species, including the Vibrio harveyi strain used in this study. The studies reported in this manuscript did not use this vaccine, however, and were not designed to support it. This does not alter the authors’ adherence to all the PLoS ONE policies on sharing data and materials. * E-mail: [email protected] . These authors contributed equally to this work. Introduction however, that some of these reports have attracted criticism (e.g. [7]) principally because they are largely based on phenomenolog- Invertebrates do not possess a specific, adaptive immune system ical observations (e.g. increased resistance/survival following based on the clonal expansion of activated lymphocytes, such as is secondary challenge) and often lack mechanistic explanations for found in vertebrates. In the absence of ‘true’ lymphocytes and how the immune system accomplishes such heightened resistance functional antibody, they have been traditionally thought to rely to infection. instead entirely on innate (non-specific) immunity for internal The studies of Watson et al. [8] have identified a potential defence against parasites and pathogens [1]. It has been argued mechanism for ‘specific immune priming’ in invertebrates. These that the cost limitation of a resource hungry, specific immune workers found a homologue of the Down syndrome cell adhesion system may reduce other fitness related traits in invertebrates [2] molecule (Dscam) in fruit flies (Drosophila) that is expressed in key and that the innate immune system is therefore the most ‘cost- phagocytic cell types in this insect’s immune system. They also effective’ method to defend these animals against disease. Recent conclusively demonstrated that suppression of Dscam gene reports, however, have suggested the existence of some form of expression in flies by RNA interference, results in a marked immune memory in invertebrates that is referred to by some reduction in the phagocytic activity of blood cells. Finally, they authors as ‘immune priming’ or ‘specific immune priming’ (e.g. estimated that 18,000 isoforms of Dscam could be formed by [3], see Textbox S1). In certain cases, this enhanced resistance to sequence variation in the three immunoglobulin-like domains of infection appears to be passed from parents to progeny (so called this molecule and that these probably allowed Dscam to show ‘trans-generational immune priming’; [4–6]). It should be noted differential binding to foreign agents in an analogous way to how PLoS ONE | www.plosone.org 1 June 2011 | Volume 6 | Issue 6 | e20960 Enhanced Immunity in Shrimp after ‘Vaccination’ vertebrate antibody binds different antigens. In a related Animal Health and is known to be pathogenic to shrimp. invertebrate (the mosquito) further experimentation has revealed Experimental groups were assigned randomly across 661500L the production of different Dscam-like molecules with varying tanks (12–14 animals tank21, 3 tanks treatment21) and monitored pathogen interaction specificities following challenge with different for moulting and mortality twice daily, with all moults and dead pathogens [9], again analogous to the clonal selection mechanism animals removed. Animals were sacrificed for the phagocytosis of vertebrate immunity. In turn, this modulated the phagocytic assay and antibacterial assay 7 and 8 d post-injection (post- activities of the mosquito’s haemocytes to enhance host survival vaccination) respectively. The sterility of the formalin-inactivated following challenge. Such studies imply that following challenge V. harveyi and saline was verified by plating on tryptic soy agar (+2% with pathogens or parasites, variants of Dscam will be formed that NaCl) and incubating at 25uC for 48 h. Whole haemolymph enhance the clearance and destruction by phagocytic haemocytes (plasma and blood cells) for the antibacterial assay was obtained by of those invaders upon re-exposure. These Dscam homologues act bleeding from the ventral blood vessel of anaesthetised (30 s on ice) as specific pattern recognition molecules that selectively bind animals using a sterile 21G needle and immediately stored at microbes to the phagocytic blood cells. Hence Dscam is one of a 280uC. Previous work in our laboratory has shown that freezing number of candidates to explain the phenomenon of specific does not impair antibacterial potency when compared to prelim- immune priming, at least in insects. inary experiments using fresh tissue (data not shown). Little attention has been paid to the development of putative Experiment 2 used the same methodology as the first trial except ‘vaccines’ aimed to boost growth and welfare in invertebrates juvenile shrimp (11.561.4 g, mean 61 S.D., N = 41) were injected because of their perceived lack of a specific immune system. Such with formalin-inactivated B. subtilis (108 bacteria animal21)orthe approaches are, however, urgently needed for the aquaculture- same volume of sterile 3% NaCl solution, with a second injection of based production of economically beneficial invertebrates such as the same treatment 7 d later. Animals were sacrificed for the shrimp and other decapods crustaceans. Over the last few years, phagocytosis assay 7 d after the second injection (i,e, Day 14). global aquaculture has regularly produced over 2.4 million tonnes of cultured shrimp per annum, worth approximately $11 billion Phagocytosis Studies [10] and these values will probably increase with the projected rise Preparation of target bacteria. Bacillus subtilis (NCIMB in global population and associated increase in demand for protein 1048; originally isolated from the marine environment) and V. [11]. Unfortunately, viral and bacterial disease pandemics, harveyi (VIB 645 CZV-STL-1) were each grown overnight in TSB including vibriosis, have resulted in widespread shrimp mortality (+2% NaCl) with constant agitation, centrifuged (4500 g,4uC, and significant economic loss over the past few decades
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