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The scope of the crustacean immune system for disease control

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Abstract

The culture or wild capture of marine and freshwater shellfish, including crustaceans, is without doubt a key source of protein for a burgeoning world population. Historically the expansion of aquaculture has, however, been accompanied by the increased incidence of economically significant diseases, most notably of viral and bacterial origin. Since the late 1970s great progress has been made in our understanding of the generalized protostome innate immune system. Distinct pathways, pathogen receptor proteins and effector molecules have since been identified that are not ancestral or homologous to those of the deuterostomes, including vertebrates. Within the past decade progress has accelerated with the rapid characterisation of new classes of recognition proteins, immune effectors and regulatory pathways. This paper provides a broad overview of our current understanding of invertebrate immunology, taking the crustacean decapod immune system as its focus. Recent developments in the field are described briefly and their implications and potential considered. These advances offer fundamental new insights in our efforts to understand disease in cultured populations and also to develop knowledge of environmental effects on host/pathogen interactions within a fishery context. Of course, challenges do remain, including the lack of an immortal cell line and the limited publically-available genomic resources. These are considered in this review as priorities for future research effort. With the continued application of more insightful technologies, coupled with associated investment, it is expected that the speed at which some of these issues are resolved will accelerate.

Highlights

► Recent advances in our understanding of decapod immunity are summarised. ► Five avenues offer promise for mitigating disease, including studies of gut immunity. ► The potential of diverse pattern recognition and antimicrobial peptides are considered. ► Challenges to progress are identified, including the lack of cell lines and genomic data.

Introduction

For future generations, and in response to the increasing global population, the reliance on crustacean shellfish as a source of animal protein is set to increase. Inevitably this will lead to an increase in demand from wild fishery stocks and expansion of aquaculture (Subasinghe et al., 2009, Stentiford et al., 2012). However, the expansion of fishery effort in wild species and the increase in aquaculture across new species and new countries are not without significant issue, including the potential for habitat destruction, socioeconomic challenges, an increased prevalence or geographic spread of existing diseases and the potential for new diseases to arise.

Pathogens of commercial significance to the global crustacean shellfish industry (fisheries and aquaculture) have been reviewed in detail by other contributions to this volume. As described, significant economic global impacts are caused by viruses (e.g. White Spot Syndrome Virus (WSSV) and Infectious Hypodermal and Haematopoietic Necrosis Virus (IHHNV)), Gram-negative bacteria (e.g. Vibrio harveyi, Vibrio penaecidia, and opportunistic vibrios) and protozoa (e.g. Hematodinium spp.). Regionally, other pathogens are also commercially significant, including the Gram-positive bacterium, Aerococcus viridans var homari, which detrimentally affects wild-caught lobsters Homarus americanus in Canada and the United States.

The intention of this review is to provide a brief but broad overview of our current understanding of the crustacean innate immune system, with special reference to the Decapoda, and to identify avenues for future focus as part of a suite of solutions to ensure global food security using farmed and wild caught crustacean shellfish.

Section snippets

Current knowledge of the crustacean immune mechanism – an overview

The immune system of decapods is comprised of both cellular and non-cellular (humoral) components. Whilst this classification is operationally useful it is an artificial distinction. There is considerable integration of the cellular and humoral compartments to produce a single coordinated system. Cellular responses are triggered or enhanced by factors present within the plasma and humoral elements are often produced in, and secreted from, circulating and fixed haemocytes. Components and

Existing prophylactic treatments of crustacean disease based on current knowledge

In the preceding discussion a brief overview of current knowledge of the immune response in commercially important crustaceans has been provided. Whilst the details of many pathways, and how they inter-relate, are still unknown these limited data have provided a basis from which attempts have been made to combat disease within crustacean aquaculture by prophylaxis. The intention here has been to augment the innate immune response prior to actual pathogen exposure. Efforts have focussed on

Directions for future research

Current approaches to the prophylactic treatment of disease within crustacean aquaculture should be superseded by new strategies that are based on a more complete understanding of the complexity of the immune response within the Decapoda. The goal should be to manipulate the immune system in a calculated way so as to avoid triggering localised and/or systemic haemocyte degranulation or the inappropriate activation of cascades leading to the release of toxic but non-specific immune effectors.

Practical challenges to future study

From the above discussion it is fair to conclude that very significant advances have been made recently in our understanding of crustacean immunology. However, impediments to progress do exist. From a research standpoint the lack of an immortal crustacean cell line represents a significant impediment to progress. Research in crustacean immunity, and in particular host/virus interactions, has always trailed that of advances in our understanding of insect immunology. In part this is attributable

Summary

This is undoubtedly an exciting time in the field of invertebrate immunology. New discoveries of PRPs, immune effectors and regulatory pathways are offering fundamental new insights in our efforts to understand disease in cultured populations and also to develop knowledge of environmental effects on host/pathogen interactions within a fishery context. The pace at which new discoveries are reported has increased in the past ten years and the number of research groups around the world with

Acknowledgment

The author would like to acknowledge the generous financial support of the OECD in presenting this manuscript.

References (132)

  • P.-H. Chou et al.

    Penaeus monodon Dscam (PmDscam) has a highly diverse cytoplasmic tail and is the first membrane-bound shrimp Dscam to be reported

    Fish and Shellfish Immunology

    (2011)
  • B.M. Christensen et al.

    Melanization immune responses in mosquito vectors

    TRENDS in Parasitology

    (2005)
  • C.N. Cole et al.

    Defective interfering particles of poliovirus. 3. interference and enrichment

    Journal of Molecular Biology

    (1973)
  • B.J. Cuthbertson et al.

    Diversity in penaeidin antimicrobial peptide form and function

    Developmental and Comparative Immunology

    (2008)
  • E. de la Vega et al.

    Anti-lipopolysaccharide factor in Litopenaeus vannamei (LvALF): a broad spectrum antimicrobial peptide essential for shrimp immunity against bacterial and fungal infection

    Molecular Immunology

    (2008)
  • J. de Lorgeril et al.

    A relationship between antimicrobial peptide gene expression and capacity of a selected shrimp line to survive a Vibrio infection

    Molecular Immunology

    (2008)
  • T.W. Flegel et al.

    Presence of multiple viruses in non-diseased cultivated shrimp at harvest

    Aquaculture

    (2004)
  • L. Fortun-Lamothe et al.

    A review on the interactions between gut microflora and digestive mucosal immunity. Possible ways to improve the health of rabbits

    Livestock Science

    (2007)
  • S.A. Frank

    Within-host spatial dynamics of viruses and defective interfering particles

    Journal of Theoretical Biology

    (2000)
  • K. Fukatsu et al.

    Nutrition and gut immunity

    The Surgical Clinics of North America

    (2011)
  • J.C. Garcia et al.

    Differential gene expression in White Spot Syndrome Virus (WSSV)-infected naive and previously challenged Pacific white shrimp Penaeus (Litopenaeus) vannamei

    Aquaculture

    (2009)
  • J.A. Hammond et al.

    Lipopolysaccharide induces DNA-synthesis in a sub-population of hemocytes from the swimming crab, Liocarcinus depurator

    Developmental and Comparative Immunology

    (2002)
  • K.C. Han-Ching Wang et al.

    RNAi knock-down of the Litopenaeus vannamei Toll gene (LvToll) significantly increases mortality and reduces bacterial clearance after challenge with Vibrio harveyi

    Developmental and Comparative Immunology

    (2010)
  • C. Hauton et al.

    In vivo effects of immunostimulants on gene expression and disease resistance in lobster (Homarus gammarus) post-larval stage VI (PLVI) juveniles

    Molecular Immunology

    (2007)
  • T. Itami et al.

    Enhancement of disease resistance of kuruma shrimp, Penaeus japonicus, after oral administration of peptidoglycan derived from Biifidobacterium thermophilium

    Aquaculture

    (1998)
  • G. Jiang et al.

    Studies on nitric oxide synthase activity in haemocytes of shrimps Fenneropenaeus chinensis and Marsupenaeus japonicus after white spot syndrome virus infection

    Nitric oxide

    (2006)
  • P. Jiravanichpaisal et al.

    Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonisation

    Immunobiology

    (2006)
  • M.W. Johansson et al.

    Crustacean haemocytes and haematopoiesis

    Aquaculture

    (2000)
  • M.W. Johansson et al.

    Peroxinectin, a novel cell adhesion protein from crayfish blood

    Biochemical and Biophysical Research Communications

    (1995)
  • C.J. Kang et al.

    Characterization and expression of a new subfamily member of penaeidin antimicrobial peptides (penaeidin 5) from Fenneropenaeus chinensis

    Molecular Immunology

    (2007)
  • N. Kanthong et al.

    Mosquito cells accommodate balanced, persistent co-infections with a densovirus and Dengue virus

    Developmental and Comparative Immunology

    (2008)
  • S.L. Lee et al.

    Processing of an antibacterial peptide from hemocyanin of the freshwater crayfish Pacifastacus leniusculus

    The Journal of Biological Chemistry

    (2003)
  • S.Y. Lee et al.

    A lipopolysaccharide- and beta-1,3-glucan-binding protein from hemocytes of the freshwater crayfish Pacifastacus leniusculus – Purification, characterization, and cDNA cloning

    Journal of Biological Chemistry

    (2000)
  • F. Li et al.

    A Dorsal homolog (FcDorsal) in the Chinese shrimp Fenneropenaeus chinensis is responsive to both bacteria and WSSV challenge

    Developmental and Comparative Immunology

    (2010)
  • C.Y. Li et al.

    Tiger shrimp (Penaeus monodon) penaeidin possesses cytokine features to promote integrin-mediated granulocyte and semi-granulocyte adhesion

    Fish and Shellfish Immunology

    (2010)
  • X. Lin et al.

    Crustacean hematopoeisis and the astakine cytokines

    Blood

    (2011)
  • H. Liu et al.

    Antiviral immunity in crustaceans

    Fish and Shellfish Immunology

    (2009)
  • H. Liu et al.

    Peptidoglycan activation of the proPO-system without a peptidoglycan receptor protein (PGRP)?

    Developmental and Comparative Immunology

    (2011)
  • S.E. Lofgren et al.

    Trypanocidal and leishmanicidal activities of different antimicrobial peptides (AMPS) isolated from aquatic animals

    Experimental Parasitology

    (2008)
  • S. Lorenzon et al.

    Effects of LPS on circulating haemocytes in crustaceans in vivo

    Fish and Shellfish Immunology

    (1999)
  • T. Luo et al.

    Purification, characterization and cDNA cloning of a novel lipopolysaccharide-binding lectin from the shrimp Penaeus monodon

    Developmental and Comparative Immunology

    (2006)
  • T. Luo et al.

    PmAV, a novel gene involved in virus resistance of shrimp Penaeus monodon

    FEBS Letters

    (2003)
  • T.H.T. Ma et al.

    Molecular cloning of a C-type lectin (LvLT) from the shrimp Litopenaeus vannamei: Early gene down-regulation after WSSV infection

    Fish and Shellfish Immunology

    (2007)
  • T. Mekata et al.

    Identification of cDNA encoding Toll receptor, MjToll gene from kuruma shrimp, Marsupenaeus japonicus

    Fish and Shellfish Immunology

    (2008)
  • A. Prapavorarat et al.

    Identification of genes expressed in response to yellow head virus infection in the black tiger shrimp, Penaeus monodon, by suppression subtractive hybridization

    Developmental and Comparative Immunology

    (2010)
  • T. Rodríguez-Ramos et al.

    An inducible nitric oxide synthase (NOS) is expressed in haemocytes of the spiny lobster Panulirus argus: cloning, characterization and expression analysis

    Fish and Shellfish Immunology

    (2010)
  • C. Roulston et al.

    Isolation and in vitro characterisation of prohaemocytes from the spider crab, Hyas araneus (L.)

    Developmental and Comparative Immunology

    (2011)
  • D. Schmucker et al.

    Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity

    Cell

    (2000)
  • T. Sequeira et al.

    Evidence for circulating hemocyte proliferation in the shrimp, Penaeus japonicus

    Developmental and Comparative Immunology

    (1996)
  • X.-Z. Shi et al.

    Identification and molecular characterization of a Spätzle-like protein from Chinese shrimp (Fenneropenaeus chinensis)

    Fish and Shellfish Immunology

    (2009)
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