Ontogeny of humoral immune parameters in fish

doi:10.1016/j.fsi.2005.03.010

Fish & Shellfish Immunology

Volume 19, Issue 5, November 2005, Pages 429-439

https://doi.org/10.1016/j.fsi.2005.03.010 Get rights and content

Abstract

The first appearance of IgM in lymphocytes varies considerably among fish species. Generally, the first appearance of B-lymphocytes and immunoglobulins is late in marine species compared to fresh water species, and larvae have reached about 20–30 mm in length when IgM is first expressed. Rainbow trout and channel catfish show the first appearances of surface IgM at about 1 week after hatching. Marine species like the sea bass, spotted wolffish and cod show IgM positive lymphocytes 1–10 weeks after hatching. Transfer of maternal antibody to eggs and embryos has been demonstrated in several species. Examples are plaice, tilapia, carp, sea bass and salmon, but not cod. The ontogeny of complement component C3 has been studied in Atlantic halibut (Hippoglossus hippoglossus L.), Atlantic cod (Gadus morhua L.) and the spotted wolffish (Anarhichas minor O.). By Western blotting experiments C3 was found in unfertilised eggs in the spotted wolffish indicating a maternal transfer. RT-PCR analysis revealed C3 mRNA transcripts from 290 d° in spotted wolffish eggs. Using immunohistochemistry and in situ hybridisation, C3 was found in liver, brain, kidney and muscle of cod larvae 2 days post-hatching and in intestines, pancreas, heart and gills at different stages of larval development. Also, C3 was detectable in halibut larvae in yolk sac, muscle, liver, brain, chondrocytes, spinal chord, eye, heart, intestines and kidney. These studies suggest that complement may play a role in generation of different organs, not only in the defence against invading pathogens. Lysozyme is a bactericidal enzyme present in mucus, lymphoid tissue and serum of most fish species, but not in cod and wolffish. The enzyme has been detected in oocytes, fertilised eggs and larval stages of fish species like coho salmon, sea bass and tilapia. The activity of other enzymes like the cathepsins has been described in eggs and larvae of sea bass, cod and salmonids. Cathepsins may have a bactericidal role in the skin of fish. Lectins are carbohydrate-binding proteins that interact with pathogenic surface structures that result in opsonization, phagocytosis or activation of complement. Lectins have been isolated from the eggs of various fish species.

Section snippets

Autologous and maternal IgM

Immunoglobulins are the primary humoral component of the acquired immune system. The first appearance of cytoplasmic and surface IgM in lymphocytes varies considerably in different fish species. Comparison of published data is, however, complicated by the fact that different methods for IgM detection have been used like immuno- or in situ histology, flow cytometry, ELISA or Western blotting of tissue homogenates. In general, the first appearance of B-lymphocytes and immunoglobulins is late in

Complement

The complement system is a multicomponent defence system of vertebrate species involving 20–30 plasma proteins and several receptors. When activated, inactive complement components are turned into active serine proteases that split other inactive complement components in a sequential manner. The main results of the activation are opsonization (removal of foreign antigens coated with complement components by phagocytic cells); lysis of invading microorganisms and infected cells; and inflammation

Lysozyme and other enzymes involved in innate defence

Lysozyme is an important innate defence parameter and is widely distributed in invertebrates and vertebrates. Lysozyme is a bactericidal enzyme, involved in the hydrolysis (and lysis) of the β-(1,4) linked glycoside bonds of bacterial cell wall peptidoglycans. Although primarily associated with defence against Gram positive bacteria, lysozyme is also involved in defence against Gram negative bacteria, parasites and viruses [57], [58], [59]. Lysozyme is present in mucus, lymphoid tissue, serum

Lectins

Lectins, like C-type lectins and pentraxins are carbohydrate-binding proteins that interact with non-self and pathogenic surface structures and result in opsonization, phagocytosis or activation of the complement cascade. Various lectins have been isolated from the eggs of different fish species. For example, fucose binding lectin was isolated from sea bass ova [82], galactose-specific lectin from the eggs of coho salmon [83], and rhamnose binding lectin was demonstrated in oocytes, fertilised

Other innate parameters

Protease inhibitors can be involved in the defence against pathogens, which secrete proteolytic enzymes [89]. Most widely studied is the α-2-macroglobulin (α-2-M), which has a broad specificity involving the physical encapsulation of the protease [90]. Proteinase inhibitors, mainly cysteine protease inhibitors, have been described in the eggs of a few fish species [91], [92], [93], but their role in innate defence is unknown. Bacterial growth inhibitors, like iron-binding proteins, have been

Acknowledgements

The authors acknowledge the financial support through the EU project “FISHAID” (contract no. QLK2-CT-2000-01076) and the members of the FISHAID project for valuable comments.

References (96)

C. Chantanachookhin et al.
Comparative study of the ontogeny of the lymphoid organs in three species of marine fish
Aquaculture
(1991)
G. Breuil et al.
Ontogeny of IgM-bearing cells and changes in the immunoglobulin M-like protein level (IgM) during larval stages in sea bass (Dicentrarchus labrax)
Fish Shellfish Immunol
(1997)
N.M.S. Dos Santos et al.
Ontogeny of B and T cells in sea bass (Dicentrarchus labrax L.)
Fish Shellfish Immunol
(2000)
R.N. Gröntvedt et al.
Immunoglobulin producing cells in the spotted wolfish (Anarhichas minor Olafsen)
Dev Comp Immunol
(2003)
M.B. Schrøder et al.
Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod (Gadus morhua L.)
Dev Comp Immunol
(1998)
J.C.E. Koumans-Van Diepen et al.
Immunocytochemical and flow cytometric analysis of B-cells and plasma cells in carp (Cyprinus carpio L.): an ontogenetic study
Fish Shellfish Immunol
(1994)
A. Castillo et al.
Ontogeny of IgM and IgM bearing cells in rainbow trout
Dev Comp Immunol
(1993)
L. Petrie-Hanson et al.
Ontogeny of channel catfish lymphoid organs
Vet Immunol Immunopathol
(2001)
J.E. Bly et al.
Transfer of passive immunity from mother to young in a teleost fish: haemagglutinating activity in the serum and eggs of plaice, Pleuronectes platessa L.
Comp Biochem Physiol A
(1986)
A. Takemura
Changes in an immunoglobulin M (IgM)-like protein during larval stages in tilapia, Oreochromis mossambicus
Aquaculture
(1993)

Y.A. Olsen et al.

Degradation kinetics of immunoglobulin in the egg, alevin and fry of Atlantic salmon, Salmo salar L., and the localisation of immunoglobulin in the egg

Fish Shellfish Immunol

(1997)

B. Magnadóttir et al.

The ontogenic development of innate immune parameters of cod (Gadus morhua L.)

Comp Biochem Biophys

(2004)

A. Takemura et al.

Transfer of maternally-derived immunoglobulin (IgM) to larvae in tilapia, Oreochromis mossambicus

Fish Shellfish Immunol

(1997)

A. Lillehaug et al.

Passive transfer of specific maternal immunity does not protect Atlantic salmon (Salmo salar L.) fry against yersiniosis

Fish Shellfish Immunol

(1996)

J.R. Hayman et al.

Immunoglobulin in the eggs of the channel catfish (Ictalurus punctatus)

Dev Comp Immunol

(1993)

H. Fuda et al.

A peculiar immunoglobulin M (IgM) identified in eggs of chum salmon (Oncorhynchus keta)

Dev Comp Immunol

(1992)

M.C.H. Holland et al.

The complement system in teleosts

Fish Shellfish Immunol

(2002)

K. Ikeda et al.

Serum lectin with known structure activates complement through the classical pathway

J Biol Chem

(1987)

M. Matsushita et al.

Cleavage of the third component of complement (C3) by mannose-binding protein associated serine protease (MASP) with subsequent complement activation

Immunobiology

(1995)

D. Mastellos et al.

Complement: more than a “guard” against invading pathogens?

Trends Immunol

(2002)

S.R. Lange et al.

The ontogeny of complement component C3 in Atlantic cod (Gadus morhua L.) – an immunohistochemical study

Fish Shellfish Immunol

(2004)

S.R. Lange et al.

An immunohistochemical study on complement component C3 in juvenile Atlantic halibut (Hippoglosus hippoglossus L.)

Dev Comp Immunol

(2004)

I.K. Zarkadis et al.

Molecular cloning of the seventh component of complement in rainbow trout

Dev Comp Immunol

(2005)

A. Kazantzi et al.

Molecular cloning of the beta subunit of complement component eight of rainbow trout

Dev Comp Immunol

(2003)

S.R. Lange et al.

Isolation and characterization of complement component C3 from Atlantic cod (Gadus morhua L.) and Atlantic halibut (Hippoglossus hippoglossus L.)

Fish Shellfish Immunol

(2004)

T.K. Abelseth et al.

The spotted wolffish (Anarhichas minor Olafsen) complement component C3: isolation, characterisation and tissue distribution

Fish Shellfish Immunol

(2003)

M. Shah et al.

The gene encoding the sea urchin complement protein, SpC3, is expressed in embryos and can be upregulated by bacteria

Dev Comp Immunol

(2003)

T. Ellingsen et al.

The ontogeny of complement component C3 in the spotted wolffish (Anarhichas minor Olafsen)

Fish Shellfish Immunol

(2005)

A. Hanif et al.

Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae

Fish Shellfish Immunol

(2004)

P. Gasque et al.

Complement components of the innate immune system in health and disease in the CNS

Immunopharmacology

(2000)

J.A. Andrades et al.

Complement proteins are present in developing endochondral bone and may mediate cartilage cell death and vascularization

Exp Cell Res

(1996)

B.P. Morgan et al.

Expression of complement in the brain: role in health and disease

Immunol Today

(1996)

J.B. Alexander et al.

Noncellular nonspecific defense mechanisms of fish

Annu Rev Fish Dis

(1992)

B. Grinde et al.

Species and individual variation in lysozyme activity in fish of interest in aquaculture

Aquaculture

(1988)

A. Takemura

Immunohistochemical localization of lysozyme in the prelarvae of tilapia, Oreochromis mossambicus

Fish Shellfish Immunol

(1996)

O. Carnevali et al.

Changes of lysosomal enzyme activities in sea bass (Dicentrarchus labrax) eggs and developing embryos

Aquaculture

(2001)

S. Brooks et al.

Molecular characterisation of ovarian cathepsin D in the rainbow trout, Oncorhynchus mykiss

Gene

(1997)

J.H. Cho et al.

Matrix metalloproteinase 2 is involved in the regulation of the antimicrobial peptide parasin I production in catfish skin mucosa

FEBS Lett

(2002)

H. Tateno et al.

Immunohistochemical localization of rhamnose-binding lectins in the steelhead trout (Oncorhynchus mykiss)

Dev Comp Immunol

(2002)

C.J. Bayne et al.

The acute phase response and innate immunity of fish

Dev Comp Immunol

(2001)

P.B. Armstrong et al.

α-2-Macroglobulin: an evolutionarily conserved arm of the innate immune system

Dev Comp Immunol

(1999)

M. Yamashita et al.

A novel cysteine protease inhibitor of the egg of chum salmon, containing a cysteine rich thyroglobulin-like motif

J Biochem

(1996)

D.J. Macey et al.

Iron levels and major iron-binding proteins in the plasma of ammocoetes and adults of the Southern Hemisphere lamprey Geotria australis Gray

Comp Biochem Physiol A

(1982)

B. Sheid et al.

A tumor growth inhibitory factor and a tumor growth promoting factor isolated from unfertilised ova of shad (Alosa sapidissima)

Biochem Biophys Res Commun

(1989)

J.H.W.M. Rombout et al.

Phylogeny and ontogeny of fish leucocytes

Fish Shellfish Immunol

(2005)

L. Petrie-Hanson et al.

Humoral immune responses of channel catfish (Ictalurus punctatus) fry and fingerlings exposed to Edwardsiella ictaluri

Fish Shellfish Immunol

(1999)

A.G. Zapata et al.

Immunity in fish larvae

(1997)

A. Mor et al.

Evidence of transfer of immunity from mother to eggs in tilapias

Isr J Aquacult/Bamidgeh

(1988)

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Ontogeny of humoral immune parameters in fish

Abstract

Section snippets

Autologous and maternal IgM

Complement

Lysozyme and other enzymes involved in innate defence

Lectins

Other innate parameters

Acknowledgements

Aquaculture

Fish Shellfish Immunol

Fish Shellfish Immunol

Dev Comp Immunol

Dev Comp Immunol

Fish Shellfish Immunol

Dev Comp Immunol

Vet Immunol Immunopathol

Comp Biochem Physiol A

Aquaculture

Fish Shellfish Immunol

Comp Biochem Biophys

Fish Shellfish Immunol

Fish Shellfish Immunol

Dev Comp Immunol

Dev Comp Immunol

Fish Shellfish Immunol

J Biol Chem

Immunobiology

Trends Immunol

Fish Shellfish Immunol

Dev Comp Immunol

Dev Comp Immunol

Dev Comp Immunol

Fish Shellfish Immunol

Fish Shellfish Immunol

Dev Comp Immunol

Fish Shellfish Immunol

Fish Shellfish Immunol

Immunopharmacology

Exp Cell Res

Immunol Today

Annu Rev Fish Dis

Aquaculture

Fish Shellfish Immunol

Aquaculture

Gene

FEBS Lett

Dev Comp Immunol

Dev Comp Immunol

Dev Comp Immunol

J Biochem

Comp Biochem Physiol A

Biochem Biophys Res Commun

Fish Shellfish Immunol

Humoral immune responses of channel catfish (Ictalurus punctatus) fry and fingerlings exposed to Edwardsiella ictaluri

Fish Shellfish Immunol

Immunity in fish larvae

Evidence of transfer of immunity from mother to eggs in tilapias

Isr J Aquacult/Bamidgeh