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Immunological and Therapeutic Strategies Against Salmonid Cryptobiosis Hindawi Publishing Corporation Journal of Biomedicine and Biotechnology Volume 2010, Article ID 341783, 9 pages doi:10.1155/2010/341783 Review Article Immunological and Therapeutic Strategies against Salmonid Cryptobiosis Patrick T. K. Woo Department of Integrative Biology, University of Guelph, Guelph, ON, Canada N1G 2W1 Correspondence should be addressed to Patrick T. K. Woo, [email protected] Received 1 August 2009; Accepted 18 September 2009 Academic Editor: Luis I. Terrazas Copyright © 2010 Patrick T. K. Woo. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Salmonid cryptobiosis is caused by the haemoflagellate, Cryptobia salmositica. Clinical signs of the disease in salmon (Oncorhynchus spp.) include exophthalmia, general oedema, abdominal distension with ascites, anaemia, and anorexia. The disease-causing factor is a metalloprotease and the monoclonal antibody (mAb-001) against it is therapeutic. MAb-001 does not fix complement but agglutinates the parasite. Some brook charr, Salvelinus fontinalis cannot be infected (Cryptobia-resistant); this resistance is controlled by a dominant Mendelian locus and is inherited. In Cryptobia-resistant charr the pathogen is lysed via the Alternative Pathway of Complement Activation. However, some charr can be infected and they have high parasitaemias with no disease (Cryptobia-tolerant). In infected Cryptobia-tolerant charr the metalloprotease is neutralized by a natural antiprotease, α2 macroglobulin. Two vaccines have been developed. A single dose of the attenuated vaccine protects 100% of salmonids (juveniles and adults) for at least 24 months. Complement fixing antibody production and cell-mediated response in vaccinated fish rise significantly after challenge. Fish injected with the DNA vaccine initially have slight anaemias but they recover and have agglutinating antibodies. On challenge, DNA-vaccinated fish have lower parasitaemias, delayed peak parasitaemias and faster recoveries. Isometamidium chloride is therapeutic against the pathogen and its effectiveness is increased after conjugation to antibodies. 1. Introduction and reproduction. In some areas fish are no longer suitable for human consumption because of the high levels of Fish has been and will continue to be one of the major accumulated pollutants, and no new fishing grounds have sources of animal protein for humans. It will likely become been discovered. According to the Food and Agriculture more important as the population heads towards 8 billion in Organization, aquaculture continues to be the fastest food about 20 years as food production (e.g., growing of crops, producing sector with about a 10% annual increase. It would breeding of domestic animals) has and will continue to be higher if not for disease outbreaks [1]. Intensive culture compete with other human activities (e.g., transportation, of freshwater and marine fishes in cages is well developed in housing, industry) for the limited usable/inhabitable land. many countries, especially in those that have large numbers Besides being a more affordable animal protein many species of rivers and lakes and/or long coastlines (e.g., China, Chile, of marine fishes have beneficial health components which Norway). However, disease outbreaks become more frequent include the polyunsaturated fatty acids (e.g., Omega 3). as intensive fish culture tends to facilitate the transmission However, the capture-fishery is either stagnant or has been of parasites between fish in cages and the acquisition of in decline as natural fish stocks in many parts of the world pathogens from feral fishes that are attracted to the uneaten have been reduced significantly because of over and/or food in cages [2]. indiscriminate fishing and/or the destruction of spawning The piscine immune system is well developed, and in grounds. Many undesirable discharges (e.g., organophos- many ways it is similar to that in mammals (e.g., [3]) phates, heavy metals) into the aquatic environments, espe- which include a comparable set of immunocompetent cells cially from industries, are known to reduce fish survival [4]. In general, the adaptive immune response is slower to 2 Journal of Biomedicine and Biotechnology Figure 2: Exophthalmia in rainbow trout with an acute experimen- Figure 1: Cryptobia salmositica with red cell from an experimentally tal cryptobiosis (reproduced from Woo [5]). infected rainbow trout (reproduced from Woo [5]). develop in fish than in mammals, and this is in part due to its lower body temperature. However, the innate immunity infishisaswelldevelopedandisasresponsiveasthat in mammals. The present discussion is in two parts; the first part (Section 2) is a brief review on Cryptobia and the pathobiology in cryptobiosis—information which are relevant to the discussion on the development of strategies against the pathogen and disease (Section 3). 2. Cryptobia salmositica and Cryptobiosis Figure 3: Positive antiglobulin reaction; red blood cells from an 2.1. The Parasite. Cryptobia is a parasitic flagellate that has experimentally infected rainbow trout (reproduced from Woo [5]). worldwide distribution, and a few species are known to cause disease in marine and freshwater fishes. This extracellular parasite is elongated and is a little larger than a fish red blood cell. Its nucleus is close to the kinetoplast which is protein, and glucose are reduced along with depletion located at the anterior end. The parasite has an anterior of liver glycogen [14]. The metabolism and swimming flagellum and a recurrent flagellum that attaches to the performance of infected rainbow trout are also significantly body and exit as a free flagellum at the posterior end reduced [15], and the bioenergetic cost of the disease in [5]. juvenile fish is considerable. These are contributing factors Salmonid cryptobiosis is caused by the haemoflagellate to the retarded growth as there are significant reductions in food consumption, dry weight and energy gained, Cryptobia (Trypanoplasma) salmositica (Figure 1). The ffi pathogen has been reported in all species of Pacific salmon, energy concentration, and gross conversion e ciency. Oncorhynchus spp., along the west coast of North America However, the attenuated vaccine strain (Section 3.3.1) [5], and outbreaks of cryptobiosis with high fish mortalities has no detectable bioenergetic cost to juvenile fish have occurred in both freshwater hatcheries and in sea [16]. cage cultures [6]. The parasite multiplies by binary fission, and the parasitaemia peaks at about 4-5 weeks after 2.2. A Cysteine Protease and a Metalloprotease. Two proteases infection (e.g., [7–9]). The severity of the disease (e.g., have been identified in the pathogen [17]. The cysteine the anaemia) is directly related to the parasitaemia and protease consisting of four polypeptide bands (49, 60, 66, clinical signs include exophthalmia (Figure 2), general and 97 kDa) is a metabolic enzyme while the metalloprotease oedema, abdominal distension with ascites, a microcytic (200 kDa) is a histolytic enzyme. The metalloprotease has and hypochromic anaemia, positive antiglobulin reaction been isolated and purified (Figure 4). Its proteolytic activity (or positive Coombs’ test) of red cells (Figure 3), and is inhibited by excess of zinc ions [17–19]. The purified anorexia [7, 10, 11]. Anorexia is a double-edged sword—it enzyme lyses red blood cells [20] by digesting erythrocyte is beneficial to the host in that it reduces the severity of the membranes [18]. Consequently, it is an important contribut- disease by lowering plasma proteins and subsequently the ing factor to the anaemia which is a very consistent clinical parasitaemia but it is also detrimental to the fish in that it sign of the disease. Also, the purified metalloprotease readily contributes to the immunodepression [11, 12]. During acute degrades types I, IV, and V collagens (Figure 5) and laminin disease the haemolytic activity of complement is significantly [18]. It is secreted by the parasite in fish [21] and in culture lowered [13]. In addition, plasma thyroxine (T3 and T4), [19], and it contributes significantly to the development Journal of Biomedicine and Biotechnology 3 AB CDM ABCDE F M 215 200 200 116 116 110 97 97.4 97.4 66 66 45 45 Figure 5: In vitro proteolytic degradation of collagen type V by purified metalloprotease from Cryptobia salmositica. Lanes A–E: Figure 4: Purification of cysteine protease and metalloprotease collagen incubated with metalloprotease for 0, 2, 4, 6, and 8 hours from Cryptobia salmositica. Lane A: crude cell lysate; lane B: respectively; lane F: collagen incubated under same conditions partially purified cysteine protease from a DEAE-agarose column; as lanes A–E, but without metalloprotease (control); lane M: lane C: partially purified metalloprotease from a DEAE-agarose molecular markers (reproduced from Zuo and Woo [18]). column; lane D: a single band of purified metalloprotease from a Sephacryl S-300 column; lane M: molecular markers (kDa) ABC (reproduced from Zuo & Woo [18]). 200 of the disease and histopathogical lesions in infected fish 116 97 4 [22]. Briefly, metalloprotease activities can be neutralized by 66 either a monoclonal antibody (Section 3.1)oranatural antiprotease (Section 3.2.2) or the antibody against the DNA vaccine (Section 3.3.2); this neutralization essentially “dis- 45 arms” the pathogen so that the host immune system can more readily control the infection. 3. Strategies against
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