Characterization of mucosal immunity in rainbow trout Oncorhynchus mykiss challenged with infectious hematopoietic necrosis virus:identification of antiviral activity

Cain, Kenneth D.; LaPatra, Scott E.; Baldwin, Thomas J.; Shewmaker, Bill; Jones, Jerry W.; Ristow, Sandra S.

doi:10.3354/dao027161

Cited by 29 publications

(16 citation statements)

References 22 publications

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“…Likewise, we compared injection and immersion challenges to independently assess the within-host replication and viral entry traits. Our assumption was that injection bypassed the host entry stage of the virus by skirting skin mucosal defenses, an important component of the fish immune system (12). This assumption is supported by findings that injection challenges typically induce higher levels of mortality than immersion challenges in rainbow trout (12,35,45,48).…”

Section: Discussionmentioning

confidence: 69%

“…Our assumption was that injection bypassed the host entry stage of the virus by skirting skin mucosal defenses, an important component of the fish immune system (12). This assumption is supported by findings that injection challenges typically induce higher levels of mortality than immersion challenges in rainbow trout (12,35,45,48). However, the work presented here did not examine cellular entry, which is a completely separate phenomenon based largely on viral receptors.…”

Section: Discussionmentioning

confidence: 76%

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In Vivo Fitness Associated with High Virulence in a Vertebrate Virus Is a Complex Trait Regulated by Host Entry, Replication, and Shedding

Wargo

Kurath

2011

J Virol

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The relationship between pathogen fitness and virulence is typically examined by quantifying only one or two pathogen fitness traits. More specifically, it is regularly assumed that within-host replication, as a precursor to transmission, is the driving force behind virulence. In reality, many traits contribute to pathogen fitness, and each trait could drive the evolution of virulence in different ways. Here, we independently quantified four viral infection cycle traits, namely, host entry, within-host replication, within-host coinfection fitness, and shedding, in vivo, in the vertebrate virus Infectious hematopoietic necrosis virus (IHNV). We examined how each of these stages of the viral infection cycle contributes to the fitness of IHNV genotypes that differ in virulence in rainbow trout. This enabled us to determine how infection cycle fitness traits are independently associated with virulence. We found that viral fitness was independently regulated by each of the traits examined, with the largest impact on fitness being provided by within-host replication. Furthermore, the more virulent of the two genotypes of IHNV we used had advantages in all of the traits quantified. Our results are thus congruent with the assumption that virulence and within-host replication are correlated but suggest that infection cycle fitness is complex and that replication is not the only trait associated with virulence.Despite a recent surge in research, the evolution of viral virulence remains a controversial issue (1,7,10,18,22,37,50,60). Some studies have suggested a positive link between viral fitness and virulence (6, 13, 17, 39, 42, 49, 52-54, 58, 59), whereas others found no evidence of such an association (20,24,27) or even indicated that the converse, that virulence is negatively associated with viral fitness, is true (36, 43). Despite the fact that these studies span a wide range of virus and host taxa, a limitation of many of these studies is that viral fitness was typically estimated from only one or two virus traits, at one stage of the viral infection cycle. In reality, viral fitness is likely shaped by multiple traits at each of the viral infection stages, i.e., entry into the host, replication in the host, and shedding from the host, all of which could differentially impact selection for virulence (5).Most estimates of viral fitness come from examinations of the within-host replication stage of the viral infection cycle. For a few systems, researchers have made an effort to provide a detailed assessment of the importance of within-host dynamics on fitness, by separately quantifying replication in single-genotype infections and the relative abilities of virus genotypes to produce infectious progeny in a coinfection environment, herein referred to as coinfection fitness (15,39,59). However, the connection between within-host fitness and transmission remains elusive (20, 24, 42, 52), partly due to an incomplete understanding of virus investment into shedding and entry (8,45). These limitations are compounded in verteb...

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Section: Discussionmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 76%

In Vivo Fitness Associated with High Virulence in a Vertebrate Virus Is a Complex Trait Regulated by Host Entry, Replication, and Shedding

Wargo

Kurath

2011

J Virol

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“…Cain (Cain et al, 1996) was able to detect low anti-IHNV (infectious hematopoietic necrosis virus) activity in gut mucus of juvenile rainbow trout following immersion with this virus. Interestingly, neutralising activity was also present in gut mucus following injection challenge but titers were lower than in the waterborne challenge.…”

Section: Mucosal Immune Responsesmentioning

confidence: 99%

Mucosal immunoglobulins and B cells of teleost fish

Salinas

Zhang

Sunyer

2011

Developmental & Comparative Immunology

518

350

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As physical barriers that separate teleost fish from the external environment, mucosae are also active immunological sites that protect them against exposure to microbes and stressors. In mammals, the sites where antigens are sampled from mucosal surfaces and where stimulation of naive T and B lymphocytes occurs are known as inductive sites and are constituted by mucosa-associated lymphoid tissue (MALT). According to anatomical location, the MALT in teleost fish is subdivided into gut-associated lymphoid tissue (GALT), skin-associated lymphoid tissue (SALT), and gill-associated lymphoid tissue (GIALT). All MALT contain a variety of leukocytes, including, but not limited to, T cells, B cells, plasma cells, macrophages and granulocytes. Secretory immunoglobulins are produced mainly by plasmablasts and plasma cells, and play key roles in the maintenance of mucosal homeostasis. Until recently, teleost fish B cells were thought to express only two classes of immunoglobulins, IgM and IgD, in which IgM was thought to be the only one responding to pathogens both in systemic and mucosal compartments. However, a third teleost immunoglobulin class, IgT/IgZ, was discovered in 2005, and it has recently been shown to behave as the prevalent immunoglobulin in gut mucosal immune responses. The purpose of this review is to summarise the current knowledge of mucosal immunoglobulins and B cells of fish MALT. Moreover, we attempt to integrate the existing knowledge on both basic and applied research findings on fish mucosal immune responses, with the goal to provide new directions that may facilitate the development of novel vaccination strategies that stimulate not only systemic, but also mucosal immunity.

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“…One of these studies examined mucosal responses after infection with infectious hematopoietic necrosis virus (IHNV). The authors observed that mucosal Igs were not important for the protection of the animal, as neutralizing antibodies were not detected in the skin, or gut mucus, while IgM neutralizing antibodies were observed in serum (Cain et al, 1996). On the other hand, innate functions of B cells, such as phagocytosis (Li et al, 2006; Zhang et al, 2010) and cytokine production (Takizawa et al, 2013), has not yet been studied during viral infection in teleosts.…”

Section: Mucosal B Cell Responses In Gutmentioning

confidence: 99%

B cells and their role in the teleost gut

Parra

Korytář

Takizawa

et al. 2016

Developmental & Comparative Immunology

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Mucosal surfaces are the main route of entry for pathogens in all living organisms. In the case of teleost fish, mucosal surfaces cover the vast majority of the animal. As these surfaces are in constant contact with the environment, fish are perpetually exposed to a vast number of pathogens. Despite the potential prevalence and variety of pathogens, mucosal surfaces are primarily populated by commensal non-pathogenic bacteria. Indeed, a fine balance between these two populations of microorganisms is crucial for animal survival. This equilibrium, controlled by the mucosal immune system, maintains homeostasis at mucosal tissues. Teleost fish possess a diffuse mucosa-associated immune system in the intestine, with B cells being one of the main responders. Immunoglobulins produced by these lymphocytes are a critical line of defense against pathogens and also prevent the entrance of commensal bacteria into the epithelium. In this review we will summarize recent literature regarding the role of B-lymphocytes and immunoglobulins in gut immunity in teleost fish, with specific focus on immunoglobulin isotypes and the microorganisms, pathogenic and non-pathogenic that interact with the immune system.

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Characterization of mucosal immunity in rainbow trout Oncorhynchus mykiss challenged with infectious hematopoietic necrosis virus:identification of antiviral activity

Cited by 29 publications

References 22 publications

In Vivo Fitness Associated with High Virulence in a Vertebrate Virus Is a Complex Trait Regulated by Host Entry, Replication, and Shedding

In Vivo Fitness Associated with High Virulence in a Vertebrate Virus Is a Complex Trait Regulated by Host Entry, Replication, and Shedding

Mucosal immunoglobulins and B cells of teleost fish

B cells and their role in the teleost gut

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