Gut Immune System and the Implications of Oral-Administered Immunoprophylaxis in Finfish Aquaculture

Abstract

The gastrointestinal immune system plays an important role in immune homeostasis regulation. It regulates the symbiotic host-microbiome interactions by training and developing the host’s innate and adaptive immunity. This interaction plays a vital role in host defence mechanisms and at the same time, balancing the endogenous perturbations of the host immune homeostasis. The fish gastrointestinal immune system is armed with intricate diffused gut-associated lymphoid tissues (GALTs) that establish tolerance toward the enormous commensal gut microbiome while preserving immune responses against the intrusion of enteric pathogens. A comprehensive understanding of the intestinal immune system is a prerequisite for developing an oral vaccine and immunostimulants in aquaculture, particularly in cultured fish species. In this review, we outline the remarkable features of gut immunity and the essential components of gut-associated lymphoid tissue. The mechanistic principles underlying the antigen absorption and uptake through the intestinal epithelial, and the subsequent immune activation through a series of molecular events are reviewed. The emphasis is on the significance of gut immunity in oral administration of immunoprophylactics, and the different potential adjuvants that circumvent intestinal immune tolerance. Comprehension of the intestinal immune system is pivotal for developing effective fish vaccines that can be delivered orally, which is less labour-intensive and could improve fish health and facilitate disease management in the aquaculture industry.

Oral vaccination of fish against vibriosis using spore-display technology

“…In humans, oral immunization stimulates an immune response that is effective against both mucosal and systemic infections ( 100 ). In fish, oral immunization is thought to preferably induce a mucosal immune response accompanied by secretion of immunoglobulins IgM, IgD, and IgT/Z ( 13 , 14 ). The fish intestinal mucosa is one of the main routes for pathogens translocation into the body to cause disease; thus, inducing a “frontline” mucosal immunity (via bath or oral vaccination) is of utmost importance.…”

“…Another explanation is the occurrence of oral tolerance to our spore-based vaccine, due to prolonged/repetitive exposure to the OmpK antigen. Oral tolerance is a phenomenon of systemic immunity suppression (with the generation of regulatory T-cells) that occurs to avoid unnecessary immune responses against normal gut commensals and certain food-derived antigens while maintaining an active reaction against enteric pathogens ( 14 ). Previous studies in fish described the occurrence of oral tolerances, inferred by gradual down-regulation of immunity genes expression or suppression of antibody production ( 14 ).…”

“…Oral tolerance is a phenomenon of systemic immunity suppression (with the generation of regulatory T-cells) that occurs to avoid unnecessary immune responses against normal gut commensals and certain food-derived antigens while maintaining an active reaction against enteric pathogens ( 14 ). Previous studies in fish described the occurrence of oral tolerances, inferred by gradual down-regulation of immunity genes expression or suppression of antibody production ( 14 ). Such mechanism is however unlikely to have occurred in our study since OmpK-vaccinated European seabass juveniles showed significantly lower mortality when challenged with V. anguillarum than did non-vaccinated fish.…”

“…The few available are commercialized as boosts to previous injection vaccination strategies and are not intended to be used on their own ( 5 , 6 , 11 , 12 ). This is mainly because i) many aspects of fish immunology are still unknown; ii) mucosal vaccination is still in the early steps of development, including for humans and terrestrial animals and, iii) oral vaccine success in fish is highly dependent on the correct antigen-adjuvant combination, with previous attempts failing to elicit an effective immune response and protection upon a bacterial challenge ( 5 , 6 , 11 – 14 ).…”

Dietary Supplementation of a Commercial Prebiotic, Probiotic and Their Combination Affected Growth Performance and Transient Intestinal Microbiota of Red Drum (Sciaenops ocellatus L.)

“…The manipulation of immune responses through dietary treatments is a prophylactic management strategy of interest for aquaculture to ultimately reduce the incidence of diseases and prevent economic losses [ 42 ]. The concept of providing beneficial probiotic bacteria along with complex carbohydrates to serve as their nourishment could produce a synbiotic effect and benefit the intestinal immune system [ 3 ].…”