Fish immune system. A crossroads between ... - …

1 Inmunologia 64pag 26/9/03 12:25 P gina 277. Revisi n Inmunolog a Vol. 22 / N m 3/ Julio-Septiembre 2003:277-286. Fish immune system . a crossroads between innate and adaptive responses L. Tort, Balasch, S. Mackenzie Department of Cell Biology, Physiology and Immunology, Universitat Aut noma de Barcelona, Bellaterra, Spain EL SISTEMA INMUNITARIO DE LOS PECES. UNA ENCRUCIJADA ENTRE LAS. RESPUESTAS INMUNITARIAS INNATAS Y ADAPTATIVAS. RESUMEN. Considerados como la base evolutiva vertebrada tras su radia- ABSTRACT. ci n adaptativa en el Dev nico, los peces constituyen en la actua- Fish, as the first vertebrate group appearing in evolution after adap- lidad el grupo m s exitoso y diversificado de vertebrados.

2 Como tive radiation during the Devonic period, still represent the most suc- grupo, este conjunto heterog neo de organismos representa una cessful and diverse group of vertebrates. This heterogeneous group of aparente encrucijada entre la respuesta inmunitaria innata y la organisms occupy an apparent crossroads between the innate immune aparici n de una respuesta inmunitaria adaptativa. La mayor a response and the appearance of the adaptive immune response. Impor- de rganos inmunitarios de los mam feros tienen sus hom logos tantly, immune organs homologues to those of the mammalian immu- en los peces. Sin embargo, su eventual menor complejidad estruc- ne system are present in fish.

3 However, their structural complexity is tural podr a potencialmente limitar la capacidad para generar una less, potentially limiting the capability to generate fully functional adap- respuesta inmunitaria completamente funcional frente a la inva- tive immune responses against pathogen invasion. The ability of fish to si n de pat genos. Se discute aqu la capacidad de los peces para mount successful immune responses with apparently more robust inna- generar respuestas inmunitarias exitosas, teniendo en cuenta la te responses than that observed in higher vertebrates is discussed. robustez aparente de la respuesta innata de los peces, en com- paraci n con la observada en vertebrados superiores.

4 KEY WORDS: innate immunity / adaptive immunity / Vertebrates /. Fish / Evolution. PALABRAS CLAVE: Inmunidad innata / Inmunidad adaptati- va / Vertebrados / Peces / Evoluci n. INTRODUCTION The adaptation of autocatalytic functions is a coevolutionary A recent estimation assumes that about 1029 prokaryotic process, which in case of the immune system involves cells exist in oceans(1), which are mainly responsible for the competition related to the number of microorganisms and marine biomass. The aquatic media not only allows transport their pathogenicity. Although most effector mechanisms of but also the growth of microorganisms. Thus, a number of allorecognition in invertebrates are not known, recent studies trophic chains are less productive due to the ubiquity of in comparative immunology stress two general patterns: (a).

5 Heterotrophic bacteria which utilize 70% of the marine conservation of the defensive signal pathways that are relevant biogenic carbon(2) and viruses that may account for 1010 to nonspecific immunity, and (b) restriction of adaptive cells/L in aquatic habitats(3). immunity to vertebrates (Fig. 1). 277. Inmunologia 64pag 26/9/03 12:25 P gina 278. FISH immune system . a crossroads between innate AND adaptive RESPONSES VOL. 22 NUM. 3/ 2003. Figure 1. Evolutive emergence of immune mechanisms through the animal kingdom. It is known that evolutive mechanisms act on the existing their virulence depends on environmental factors such as material and are restricted to the limitations of both biotic thermic, ionic and osmotic changes, iron and oxygen and abiotic resources available in the environment.

6 Animals availability, pollutants, eutrophia, etc. In fish, evolved from small bodies to bigger bodies, from less immunocompetence depends more on fish weight rather isolation from environment to higher degree of isolation, than on age, mainly due to the need of a minimum number from higher dependency of the environmental conditions of immunocompetent cells. Thus, it is known that some fish to higher degree of self-regulation systems. Therefore, a larvae have the ability to process antigens, even when they progressively richer internal medium is increasingly found. are still dependent on yolk resources(5). The immune system of fishes is conditioned by the particular environment, but also by their poikilothermic condition.

7 Most pathogenic bacteria are opportunistic microorganisms THE innate immune system . normally present in the aquatic microflora. The obligatory Over 98% of pluricellular organisms are able to maintain pathogens Renibacterium y Mycobacterium(4) are scarce, but their integrity thanks to an innate immune system based on 278. Inmunologia 64pag 26/9/03 12:25 P gina 279. INMUNOLOG A L. TORT, BALASCH, S. MACKENZIE. TABLE I. Relevant immune differences between jawed fishes and mammals Jawed Fishes Mammals Biotic constrictions Temperature range -2 to 35 C to C. Primary environment Water Air Metabolism Poikilothermia Homeothermia Endothermia (eg. bluefin tuna and some pelagic fishes).

8 External interfaces Mucous skin, gills Respiratory tree Humoral diversity Ig isotypes IgM, IgD? (Teleostei) IgM, IgA, IgD, IgE, IgG. IgM, IgX/IgR, IgW, NAR(C) (Chondrichthyes). IgM redox forms Ig gene rearrangement Multicluster (Chondrichthyes and some Teleostei) Translocon Non-specific diversity Several C3 isoforms (Teleostei) No C3 isoforms Overall performance Antibody affinity Low High Antibody response Slow Fast Memory response Weak Strong Affinity maturation Low or absent High Low temperatures High dependence, immunosuppressive response Low dependence (only in poikilothermic fish). Lymphoid organs Haematopoietic tissue Head kidney (Teleostei) Bone marrow Epigonal and Leydig organs, meningeal tissue, orbital and subcranial hematopoietic tissue (Chondrichthyes).

9 Thymus Involution species-dependent, influenced by seasonal Involution with age changes and hormonal cycles Lymphoid nodes Absent Present Gut-associated lymphoid tissues Not organized, lymphoid aggregates Organized, Peyer patches Leydig organ and spiral valve (Chondrichthyes). Germinal centres Absent (melanomacrophage centres?), Present dendritic cells probably present cell phagocytosis and secretion of soluble antimicrobial The innate response is the basis of immune defence of molecules. Thus, the innate responses of insects and mammals invertebrates and lower vertebrates. Its relevance may be involve antibacterial peptides and homologous receptors assessed by taking into account the evolutive success of (Toll in insects and their TLR homologues in mammals) which some invertebrates such as the arthropods, which are the use similar pathways of regulation and transcription(6-8).

10 Major group of animals. Similarly, 40% of the species of The innate system is the earliest immune mechanism vertebrates belong to fishes. Therefore their immune system and it is characterised by being non-specific and therefore should display a number of features that allow them to not depending upon previous recognition of the surface successfully maintain such a diversity, and their adaptation structures of the invader. It has also the advantage of being to a variety of environments, from deep sea to rivers or inducible by external molecules but at the same time is lakes of all climates and even environments combining dry constitutive and reacts within a very short time scale.