How Do Invertebrates And Animals Without A Specific Immune System Defend Against Invaders
Invertebrate Immune Systems–Specific, Quasi-Specific, or Nonspecific?
Abstract
Until recently, it was widely accustomed that invertebrates fail to prove a loftier caste of specificity and memory in their immune strategies. Recent reports accept challenged this view such that our understanding of the capabilities of the invertebrate immune systems needs to exist reassessed. This account critically reviews the available show that suggests the beingness of a high degree of memory and specificity in some invertebrates and seeks mechanistic explanations of such observations. It is postulated that elevated levels of phagocytosis may be a fractional explanation for this phenomenon.
One of the fundamental hallmarks of the mammalian immune system is the ability to generate clones of lymphocytes, each with its own unique ability to recognize and proliferate in the presence of a specific Ag. Hence, this immune organisation is said to accept both retention (the power to reply rapidly upon re-exposure to a particular Ag) and specificity. This feature of the allowed system probably first evolved >500 one thousand thousand years ago with the evolution of the start jawed (gnathostomate) vertebrates (1). Despite some initial indications >30 years ago that invertebrates also accept a specific (adaptive) immune system based on the clonal expansion of activated lymphocytes, it has become the central dogma of evolutionary immunologists that invertebrates, in the absence of "true" lymphocytes and functional Ab, rely entirely on innate immunity every bit their chief mechanism of defense against parasites and pathogens. More recently, our noesis of these innate defenses has flourished to the stage that nosotros now take a detailed appreciation of both the cellular and humoral mechanisms in many invertebrates, but particularly in insects such as the dipteran fly Drosophila (2, 3, four) and in crustaceans such as shrimp, Penaeus/Litopenaeus spp. (5). With the global aquaculture production of shrimp currently exceeding 2.4 meg tons per annum (6) and an estimated loss of up to 25% of this production as a result of affliction, there is a slap-up need to understand the immune defenses of these commercially important animals. Reports on the potential development of vaccines to combat a major viral pathogen of shrimp chosen white spot syndrome virus (WSSV)2 (vii, 8), together with studies that suggest the existence of specific or "primed" immunity in insects and crustaceans that in some instances can plainly be transferred from parent to offspring (ix, 10, 11), have challenged this central dogma. These largely phenomenological studies offer niggling in terms of potential mechanisms to explain their novel observations. Most recently, however, detailed investigations into the action of a homologue of Down syndrome cell adhesion molecule (Dscam) in Drosophila (12) and the musquito Anopheles gambiae (xiii) provide compelling explanations for how such specificity might be achieved at least in these invertebrates. This review aims to provide a critical overview of the findings to appointment and seeks potential mechanisms to explain these observations based on recent advances in our understanding of the mechanisms controlling the allowed defenses of invertebrates.
The allowed defenses of invertebrates-a brief guide to the mechanisms
It must be remembered that considering of the tremendous diversity of body patterns, life histories, and ecological niches inside the 1.iii million-plus species of living invertebrates, at that place is besides a similar potential for diversity in their immune strategies. Hence, the allowed strategy of a relatively long-lived aquatic crustacean such as the edible crab Cancer pagurus, which may survive for several years, may be very different from that in shorter-lived, terrestrial, social insects such as bees or wasps. Indeed, information technology could exist argued that only long-lived animals would gain any evolutionary advantage from the development of an adaptive immune organisation capable of showing "memory." The following section of this review concentrates on the arthropods (insects, crustaceans, and related forms), a highly successful group of protostomate invertebrates of which a great bargain is known of their immune systems and diseases. Wherever possible, ii model animals are referenced: the fruit wing Drosophila melanogaster and the shrimp Penaeus/Litopenaeus spp.
Arthropods in general employ a range of cellular and humoral defenses to protect themselves from disease agents that manage to gain admission to their internal tissues by penetrating the exoskeleton/cuticle or alimentary canal. The cells principally involved are the circulating and sessile blood cells (correctly termed he-mocytes) and various other jail cell types, including those in the fatty body of insects and the hepatopancreas and gills in crustaceans. These hemocytes are morphologically distinct from vertebrate leukocytes, and although they share names such as "granulocytes" this does non necessarily imply any evolutionary or functional relationships. Hemocytes perform a number of cardinal actions, including the initiation of wound repair/blood coagulation to prevent pathogen ingress into the main trunk cavity termed the hemocoel. If this barrier is breached, the claret cells present in the hemocoel tin can phagocytose and digest small invaders such as protozoans, bacteria, fungi, and viruses and ensheath multicellular parasites in a thick wall of hemocytes, a process termed encapsulation (Fig. 1⇓; Refs. 2, 3, 4 , xiv , and fifteen). In the last cellular defense mechanism, termed nodule formation or nodulation, microorganisms are cleared from the hemocoel and become enmeshed in a fundamental core of melanized hemocytes surrounded by a wall of flattened hemocytes, hence isolating such particles from the rest of the host (xv). These cellular defenses are highly efficient, and early pioneering immunologists including Elie Metchnikoff and Serge Metalnikov marveled at their potential to clear and kill extremely large numbers of pathogenic bacteria that would accept proved fatal to more circuitous animals such as humans.
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FIGURE 1.
Schematic of the defense strategies of arthropods to parasites and pathogens. Such organisms are recognized by a diversity of blueprint recognition molecules either gratuitous in the plasma or associated with various cell types. The cellular events consist of phagocytosis by specialist "professional" phagocytes while nodule formation removes big numbers of microorganisms from the hemocoel such that they become walled off by a sheath of cells. Encapsulation occurs when larger invaders or damaged cocky-tissues are recognized and become surrounded past a multilayer of hemocytes. Bacteria and fungi are also killed by AMPs or by intermediates of the prophenoloxidase cascade. Lectins and complement-like factors may act equally recognition molecules and aid in the emptying of invading organisms.
In terms of humoral mechanisms, the antimicrobial peptides (AMPs) are central effectors in the elimination and destruction of bacteria and fungi in invertebrates (Fig. 1⇑). In insects such equally Drosophila several distinct forms are synthesized by the fat body (the functional equivalent of the liver in insects), while in shrimp these AMPs are largely synthesized within the hemocytes (v). Examples of Drosophila AMPs include diptericins, drosomycins, Metchnikowins, defensins, attacins, cecropins, and drosocins (2, 3), whereas shrimp produce penaeidins, crustins, and hemocyanin-derived peptides (5, sixteen). As well as AMPs, both insects and crustaceans utilise a variety of antimicrobial enzymes such as lysozyme. Lectins, either gratis in the blood (hemolymph) or associated with the hemocytes, may deed as both recognizers and effectors of amnesty. The prophenoloxidase cascade is thought to generate cytotoxic and opsonic factors together with melanin that is evident during the host response to strange invaders (Fig. 1⇑). In Drosophila at least, recent studies have shown that the activation of this system does not appear to accept a major influence on the power of these animals to survive microbial claiming (17), mayhap suggesting that this enzymatic cascade is of less overall importance than previously considered.
The importance of cellular (phagocytosis) vs humoral (AMP) defenses has been comprehensively reassessed in Drosophila (18). Information technology was shown that double mutants of Drosophila larvae containing few or no circulating hemocytes but still with the ability to generate AMPs largely intact did not survive opportunistic bacterial or fungal infections (18), the implication being that greater emphasis needs to be placed on a molecular understanding of the cellular defenses such as phagocytosis and nodule formation.
The case for specific immunity in invertebrates
Even though the invertebrate immune organization lacks lymphocytes and functional Igs, this should not dominion out the potential for the being of a unique form of an adaptive allowed system that might have been discarded with the evolution of the first vertebrates. This section critically reviews the evidence for such specificity. Pioneers in evolutionary immunology such as Edwin Cooper and Bill Hildemann made employ of the graft rejection models widely used by mammalian immunologists at the time to examine whether invertebrates also show a loftier degree of self-nonself recognition as seen in mammals and also whether second ready grafts showed accelerated graft rejection (taken equally a authentication of memory). Cooper's work (nineteen) showed that earthworms could recognize and reject grafts from other earthworms and that they possessed the apparent ability to bear witness faster rejection upon secondary exposure. To appointment, at that place is no tested mechanistic caption for these important findings. A further interesting graft rejection model comes from colonial animals such as sponges and tunicates. In the case of the tunicate Botryllus schlosseri, the colonies are formed by a budding procedure to produce zooids that are genetically identical and share a common vascular system. When adjacent colonies of B. schlosseri grow close together, finger-like processes called ampullae from the zooids either fuse, leading to the commutation of blood cells, or are rejected postfusion, resulting in an inflammatory reaction and prison cell destruction. Our insight into this process has recently been strongly enhanced past the observations of Nyholm et al. (20), who identified the first invertebrate allorecognition receptor. Somatic diversification of this receptor can occur by culling splicing, resulting in individual-specific forms inside all tissues of the zooid. Interestingly, although potential homologues were found with other vertebrate immune arrangement receptors, one interpretation of this work by Litman (21) highlighted that it may non be possible to explicate the observation in this invertebrate in terms of what nosotros know about allorecognition in mammals. Substantially, if invertebrates do show specificity and memory in their immune reactivity, it is probably a error to await for explanations centered on the mammalian immune organisation.
In the final few years, several groups of researchers have claimed to show the presence of some form of acquired (specific) immunity in invertebrates (Tabular array I⇓). Kurtz and Franz (22) infected copepods (a crustacean) with two strains of its natural tapeworm parasite, Schistocephalus solidus. Four days subsequently they exposed these copepods to identical numbers of either the aforementioned or dissimilar strains of the parasite and subsequently on twenty-four hour period half-dozen screened these to assess the reinfection rates. They found a significant reduction in the reinfection rate in those copepods previously exposed to the same strain of parasite. Their interpretation was that the immune arrangement of the copepod was specifically "primed" by prior exposure to the parasite. Although this is an interesting observation, the short time scale of the experiment is of concern because the parasites remaining from the kickoff exposure only four days later might have had some role in reinfection totally independent of the host defenses.
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Table I.
Recent examples of reported acquired (specific) immunity in arthropodsa
And then-called "trans-generational immunological priming" has been reported in insects including mealworms (eleven) and bumblebees (10) and also in a crustacean, Daphnia (9). In the case of the report past Sadd et al. (10), Bombus terrestris queens were exposed to either the bacterium Arthrobacter globiformis or sterile saline. At a later time the progeny (offspring workers) from these queens were stimulated past LPS injection and 24 h later the antibacterial and phenoloxidase activities in the claret were measured. Although no meaning differences were constitute in phenoloxidase levels, the antibacterial activity in the worker bees was significantly college in those descendants from the queens that had been challenged with bacteria compared with those from the saline-challenged group. Unfortunately, the nature of the test amanuensis (A. globiformis) used in the antibacterial assay was not revealed, so the possibility of the specificity of this reaction remains untested. Although like results were also noted with mealworms, in that the antibacterial activity was significantly higher in the progeny from the adults previously exposed to LPS and the phenoloxidase levels were unaltered, the assay used to achieve these conclusions was not strictly quantitative (11). More conclusive data were obtained by Little et al. (9) in their studies with the h2o flea Daphia magna. H2o fleas were artificially infected with either the pathogenic bacterium Pasteuria ramosa strain A or the P. ramosa strain Yard. The progeny of these two groups of animals were afterwards exposed to either strain A or G and their reproductive fecundity and survival postchallenge were determined. In both cases, exposure to homologous combinations (i.due east., strain A followed by strain A or strain G followed by strain 1000) increased survival after the second challenge and increased reproductive fecundity. No mechanistic explanation of these observations was attempted.
More than convincing show for a specific element in the allowed response of whatsoever invertebrate comes from experiments with bumblebees (B. terrestris) where groups of these insects were initially exposed to the Gram-negative bacterium Pseudomonas fluorescens, ii closely related Gram-positive leaner, Paenibacillus alvei and Paenibacillus larvae, or saline (23). Either 8 or 22 days later the insects were given a secondary homologous or heterologous exposure, and their survival and ability to clear the iii dissimilar species of bacteria from the blood was adamant. This approach convincingly demonstrated that insects in the homologous re-exposure grouping (e.k., P. fluorescens injected at day 0 and either day 8 or 22) showed significantly higher survival rates than those given either saline or heterologous claiming. The authors found no evidence that this apparent specific protection involved AMPs; instead, they suggested (but did not test their hypothesis) that the homologue of Dscam formed by an alternatively spliced, hypervariable Ig domain-encoding gene recently elucidated in insects (12, 13) could be responsible for this specificity. If key humoral factors such every bit AMPs are non involved in this specific "immune priming," the caption of the specificity may be in the cellular reactivity of the hemocytes (e.chiliad., phagocytosis or nodule formation) toward these leaner. Finally, a recent written report has shown that the immune system of Drosophila can be "primed" by exposure to a sublethal dose of Streptococcus pneumoniae that has some level of specificity and connected for "the life of the fly" (24). Although such specific protection could also be found for other pathogens such as the entomopathogenic mucus Beauveria bassiana, rather surprisingly (and mayhap worryingly) the other bacteria tested yielded no enhancement in protection against subsequently claiming (24).
Mechanistic explanations for specific or quasi-specific immunity
This section seeks to explore potential mechanisms that could account for the heightened and apparently specific protection observed in some of the recent studies already discussed. As previously described, cellular defense reactions are primal players in protecting both insects and crustaceans from invading pathogens. Therefore, this is an appropriate starting point to wait for mechanistic explanations of such changes. It is oftentimes forgotten that we have had evidence from studies performed over two decades ago (e.g., Ref. 25) for heightened phagocytic activity in the hemocytes of some invertebrates following previous exposure to strange material. More recently, greater insight into such activities has been gained from elegant but elementary approaches using a range of challenge regimes in the lobster Homarus americanus (26). What these authors establish was that the injection of LPS into lobsters but acted every bit a nonspecific stimulator of phagocytic activity but that the challenge of these animals with whole, live pathogenic leaner (Aerococcus viridans var. homari) induced marked increases in the in vitro phagocytic activity of lobster hemocytes, particularly against this challenge bacterium. Hence, there is evidence in the literature of enhanced phagocytic activeness in "vaccinated" animals that shows some caste of specificity. Our noesis of the recognition of microbial invaders past both insect and crustacean phagocytic hemocytes is surprisingly limited compared with that of the Imd (immune deficiency)/TLR pathways of AMP synthesis (see Refs. 2 and three for detailed reviews). What is clear is that the phagocytic hemocytes have both specific and nonspecific mechanisms of recognizing cocky from nonself (27, 28, 29, thirty). The nature of the pattern recognition proteins (PRPs) either in the plasma or directly associated with the phagocytic hemocytes that can specifically react with pathogen-associated molecular patterns (PAMPs) including peptidoglycan, LPS, dsRNA, and β-ane,3-glucans is incompletely understood, although several PRPs accept been identified in both insects and crustaceans (e.g., 29, xxx), some of which involve plasma-derived lectins that bind to hemocytes via lectin receptors. Whether these PRPs concord a clue to the heightened phagocytic activity reported in "immunized" lobsters is uncertain, but a model that could explicate this with some degree of specificity (as shown in the lobster studies) is illustrated in Fig. 2⇓. The work of Watson et al. (12) on the behavior of the Dscam homologue in Drosophila has profound bearing on this discussion in that some of the predicted 18,000 isoforms of this molecule can bind leaner (Escherichia coli), and the uptake of this bacterium past the phagocytic hemocytes is partially dependent on the presence of Dscam. An additional insight into the potential importance of Dscam variants in developing an explanation of how the innate organization of invertebrates could prove specificity emerges from work with the equivalent Dscam cistron (AgDscam) in the musquito A. gambiae (13). This factor is capable of producing in backlog of 31,000 alternative splice forms to yield proteins with a variable range of binding capabilities to nonself cloth. The claiming of a mosquito-derived, hemocyte-like jail cell line with a range of unlike Gram-positive and Gram-negative bacteria, LPS, peptidoglycan, or 2 species of Plasmodium (Plasmodium berghei and Plasmodium falciparum) quickly yielded dissimilar spliced forms of AgDscam such that their products were idea to have variable binding properties to these challenge agents. Both in vitro and in vivo challenge experimental approaches also revealed that exposure of mosquitoes to the 2 related parasites (P. berghei and P. falciparum) yielded dissimilar AgDscam variants, indicating a possible specificity in the way in which the mosquito immune system could deal with these closely related parasites. When AgDscam gene silencing experiments were conducted, Dong et al. (13) found articulate damage of the immune defenses of mosquitoes such that they became susceptible to infections by opportunistic bacteria. Finally, these authors reported convincing evidence that the nature of the claiming pathogen was reflected in the resulting AgDscam splice form variants. These experiments with mosquitoes and fruit flies provide a plausible explanation of how bumblebees can bear witness heightened specific responses following the second challenge with bacteria (23). The alternative splicing of Dscam produces a serial of recognition elements (PRPs) in insects that could also yield sufficient specificity to explain the phagocytic stimulation seem in lobster hemocytes; yet, whether all arthropods possess this gene remains to be elucidated. Further insight will be gained by a detailed exam of the nature of binding between Dscam variants and different closely related microorganisms or parasites.
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FIGURE 2.
A mechanistic caption of how phagocytic hemocytes could bear witness specific or quasi-specific acme in their rates of uptake upon secondary exposure to the homologous microorganism based on the existence of PRPs either free in the blood or associated with the jail cell membrane as pattern recognition receptors that can directly bind particular microbes. Although the model is simplistic and hypothetical, contempo experimental evidence has shown the being of hypervariable PRPs in insects (12 ,thirteen ) with the ability to differently bind and recognize a range of microorganisms, microbial products, and multicellular parasites.
It is besides worth briefly evaluating whether the differential expression of AMPs following microbial claiming could lead to quasi-specificity in immune reactivity upon the second encounter. At that place is some bear witness from studies with Drosophila that the consecration and expression of AMPs is related to the nature of the challenging infectious amanuensis. Thus, Lemaitre et al. (31) reported that the challenge of fruit flies with a fungal amanuensis resulted in the biosynthesis of anti-fungal AMPs, whereas an infection past a Gram-negative bacterium resulted in an increment in the levels of AMPs appropriate for the devastation of such bacteria. Unfortunately, this finding does not appear to be universal for other invertebrates and other pathogens. For example, recent studies have either failed to observe an upwards-regulation of gene expression for AMPs following microbial challenge (32) or found that the nature of the challenge agent has no direct bearing on the resulting AMP profile (33).
The current model for the induction of AMP biosynthesis in Drosophila shows two distinct pathways, 1 using TLR(due south) and a further one using Imd. Gram-positive leaner and fungi principally stimulate the Toll pathway while Gram-negative bacteria mainly stimulate the Imd pathway (2, 3, 31). Despite the carve up nature of these two pathways, some AMP genes such every bit those for defensin and Metchnikowin depend on both pathways. It seems unlikely that selective AMP gene upward-regulation could provide a mechanistic model that could go anywhere toward explaining the specificity of protection claimed to be present in some insects. Therefore, selective consecration of AMP biosynthesis on its own does not seem to be a promising artery to explore in the search for a mechanistic explanation of acquired amnesty in invertebrates. As in the mammalian immune organisation, there is evidence of coaction between cellular and humoral events in invertebrates. It has long been thought that there may be a link betwixt phagocytic hemocytes and the fat trunk cells that are responsible for AMP biosynthesis. A recent report past Brennan et al. (34) identified a factor, psidin, that codes for a protein found in the lysosomes in the hemocytes of Drosophila. In psidin mutants the induction of defensin is severely hampered, suggesting the importance of hemocytes in controlling or stimulating AMP biosynthesis. Ane implication of this could be that hemocytes deed in an analogous mode to that of vertebrate APCs in that they either produce signals (cytokines?) that command the fat torso or they digest circuitous Ags in lysosomes in such a fashion as to present components of these to the AMP-producing cells (35). If, as already discussed, the principal explanation for the observed "specific immunity" in invertebrates is an top of phagocytic activities of the hemocytes, a knock-on effect of this could involve the modulation of AMP biosynthesis.
The future potential for vaccine development for invertebrates
It may come as a surprise to immunologists who piece of work with mammals that there is a need to develop vaccines to protect the wellness of invertebrates. Clearly there is no requirement to develop vaccines for the vast bulk of invertebrates, particularly begetting in mind that some of these are pests to our agricultural crops or vectors of disease. Invertebrates of do good to humankind include honeybees that play a vital office in pollination and those animals bailiwick to aquacultural development. In the example of shrimp aquaculture, which has been already highlighted in this review, during their larval development shrimp are highly susceptible to nonspecific vibrio infections while later on the adults are subject to serious acute viral diseases (36). To our knowledge, at that place is only one commercially available "vaccine" for invertebrates, namely AquaVac Vibromax, a multivalent vaccine from Schering-Plough Animal Wellness designed to give protection to shrimp larvae from a range of pathogenic vibrios. Although this vaccine appears to provide a demonstrable improvement in the survival and the "health status" of larvae, its manner of activeness is unknown, as is its specificity. Commercially available vaccines for protection of shrimp confronting WSSV are likely to announced in the very nigh future judging from contempo encouraging reports of credible enhanced survival of WSSV vaccine-treated shrimp (east.thousand., Ref. eight).
Likewise as these "vaccines," several types of potential immunostimulants take been investigated in a variety of crustaceans of importance to the growing aquaculture industry. These include bacterial products (e.one thousand., LPS and peptidoglycans), animal-, establish-, alga-, and yeast-derived complex carbohydrates (diverse glucans, Ergosan, and chitin), and "probiotic" bacteria (e.grand., Lactobacillus plantarum) (e.yard., Refs. 37, 38, 39). By definition, immunostimulants human action to nonspecifically stimulate immune potential, for instance by enhancing the total number or killing potential of hemocytes and/or stimulating the expression of AMPs (Fig. 1⇑). Although some contempo reports provide good show of such events in crustaceans following the dietary application of bacterial peptidoglycan as an immunostimulant (twoscore), a recent key review of the immunostimulants used in crustacean aquaculture has questioned the evidence of articulate health benefits from their delivery and has suggested that some factors could even over-stimulate the immune arrangement to the detriment of the host (37).
Overall, consistent testify that putative vaccines requite enhanced and specific protection to invertebrates is currently defective.
Endmost remarks
There is mounting evidence that at least some invertebrates testify a high level of specificity in their immune response to different pathogens such that subsequent re-exposure results in enhanced protection. Whether these observations prove the existence of an coordinating adaptive allowed organisation with levels of specificity and memory with equivalent status to that in jawed vertebrates is notwithstanding very much unanswered. Also, there is a large gap between the phenomenological observations made in some animals such as honeybees and Daphnia and the rapid advances in our understanding of potential molecular mechanisms exemplified by the important observations in Drosophila and Anopheles (12, thirteen). What is surely needed is the ability to unequivocally evidence the existence of allowed mechanisms in selected invertebrates that both yield a retentiveness component and take specificity in their mode of action. Furthermore, a bulldoze to reconcile phenomena with the machinery in ane or 2 model species is wanting. Perhaps the offset stage in a determined quest to prove the being of some form of acquired immunity in invertebrates is to find appropriate model animals. Inside the protostomate invertebrates, either shrimp of Drosophila would appear to be good candidates for such approaches as they both have well-divers immune systems. Likewise, because there are ii principal evolutionary lineages within the creature kingdom, namely the deuterostomes and the protostomes, it would also exist advisable to examine such events in a deuterstomate model organism. The recent genome analyses of 2 deuterostome invertebrates, the sea squirt Ciona intestinalis and the purple sea urchin Strongylocentrotus purpuratus, and the initial interpretations of these studies regarding allowed genes (41, 42, 43) would brand them ideal for such goals. Chiefly, both of these animals are relatively abundant in the aquatic environs, have big numbers of blood cells, and are fairly hands maintained under aquarium conditions, hence permitting long-term primary and secondary challenge experiments. One time suitable model species have been identified, greater emphasis on experimental design is needed. For example the time scale and the putative specificity of the response need to exist carefully examined. Some studies reviewed have used very brusk periods betwixt primary and secondary challenge such that a simple tiptop in hemocyte numbers, as occurs post-obit wounding, could explain their findings. The nature of the immunogen used also requires careful selection where information technology is important to choose appropriate microbial and macrobial agents that are naturally establish in the surround with the particular fauna nether study. Finally, care is needed to ensure that the specificity of the putative changes in immune reactivity is fully addressed by secondary challenge with a wide range of related and unrelated pathogens or parasites. If, as suggested by several studies, elevated phagocytosis may provide a mechanistic explanation for the specificity of immune reactivity (xiii, 25, 26), it would be very easy to assess this in a systematic manner in an appropriate animal model. To engagement this is still lacking.
Disclosures
The authors have no fiscal disharmonize of involvement.
Footnotes
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The costs of publication of this article were defrayed in part by the payment of folio charges. This commodity must therefore be hereby marked ad in accordance with 18 U.S.C. Department 1734 solely to indicate this fact.
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↵one Address correspondence and reprint requests to Prof. Andrew F. Rowley, Section of Biological Sciences, Swansea University, Singleton Park, Swansea SA2 8PP, U.Chiliad. E-mail accost: a.f.rowley{at}swansea.ac.uk
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↵2 Abbreviations used in this newspaper: WSSV, white spot syndrome virus; AMP, antimicrobial peptide; Dscam, Down's syndrome cell adhesion molecule; Imd, immune deficiency; PRP, pattern recognition poly peptide.
- Received September iv, 2007.
- Accepted October 10, 2007.
- Copyright © 2007 by The American Association of Immunologists
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Source: https://www.jimmunol.org/content/179/11/7209
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