This document discusses maternal immunity transfer in teleost fish. It describes how various immune factors like immunoglobulins, complement components, lysozymes, lectins, and yolk proteins are transferred from mother to offspring to provide protection. This transfer is critical because fish eggs have closed systems and offspring rely on maternal immunity before developing their own immune systems. The document outlines the modes of transfer and factors that can influence it, as well as potential applications for improving fish culture through maternal immunity priming.
2. Maternal Immunity
Maternal immunity refers to
the immunity transferred
across the placenta, colostrum,
milk or eggs from mother to
offspring, which is supposed to
play a key role to protect the
vulnerable offspring against
pathogenic attacks.
Maternal transfer of
immunity is defined as the
immunity transferred from
mother to offspring, which is
supposed to play a key role in
protecting the vulnerable
offspring against pathogenic
attacks at early stages of life
(Yue et al., 2013).
3. Maternal Immunity
These maternally-transferred factors include,
IgM
lysozymes
lectin
complement
components
cathelicidin
yolk proteins - phosvitin
and lipovitellin
1
5
2
4
6
3
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C
LC
CA
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4. Fish eggs are in most cases cleidoic, i.e. closed free-living
system following fertilization.
They are therefore supposed to depend upon these maternal
immunity for protection against invading pathogens before
full maturation of immunological systems.
Both innate and adaptive type of immunity are transferred
of from mother to offspring in fishes.
Mouth bearers can transfer some immunity to larvae
through the mucus secreted from mouth cavity.
5. Delayed maturation of lymphoid organs and immuno-
competence in fish.
The concept of maternal transfer of immunity is more than
100 years old
Maternally derived immunity is essential
Little or only limited ability of developing fish embryos
and larvae to synthesize specific antibodies after certain
weeks of hatching.
8. Transfer of maternally-derived
immune factors
Previous studies on several fish species have shown that
maternal IgM is able to be transferred from mother to
offspring
Likewise, maternal transfer of the innate immune factors to
offspring has also been reported in different teleost species.
Moreover, immunization of parents results in a significant
increase in IgM levels and lysozyme activities in the eggs
compared to control.
9. Vg-derived proteins
Vg is an egg yolk precursor protein, present in the females of all
oviparous species including fish, amphibians, reptiles, birds, most
invertebrates and the platypus.
Usually synthesized extraovarianly and transported by the
circulation system to the ovary.
Where it is internalized into growing oocytes and proteolytically
cleaved to generate yolk proteins, phosvitin (Pv) and lipovitellin
(Lv).
These are later used as the nutrients by developing embryos.
10. Initially regarded as a female-specific protein.
However its synthesis, albeit in smaller quantities, has been
shown to occur in male and sexually immature animals.
Vg may, in addition to being involved in yolk protein formation,
play a role independent of gender.
Recently, Vg has been shown to be an immune-relevant molecule
involved in the defense of host against the microbes including
bacterium and virus.
Pv and Lv, that both are proteolytically cleaved products of Vg,
are naturally transferred from mother to eggs in fish.
11. Traditionally considered as the yolk reserves of nutrients
essential for growth and development.
Pv and Lv, may also play an immunological role in
developing embryos and larvae.
Pv was proven to possess an antimicrobial activity in
zebrafish embryos and larvae.
Chicken egg yolk Pv was also shown to be able to inhibit the
growth of the Gram-negative bacterium Escherichia coli .
12. Fish native Lv was associated with the immune defense of
rosy barb embryos and larvae.
Pv and Lv are maternally-transferred proteins involved in
both nutritional supply and immune defense in embryos and
larvae in fishes.
13. Complement components
Consists of 35 soluble and membrane proteins
Part of first line of defense mechanism
Contains components as C1, C2, C3, C4, C5, C6, C7, C8,
C9, factor B, H, I, D, E
Activated by 3 pathways
14. ACP- triggered by the certain structures on microbial surface in
an antibody-independent manner.
CCP - initiated by binding of antibody to the C1 complex.
MBLP - activated by binding of microbial polysaccharides to
circulating lectins, such as mannose binding lectin (MBL).
Different complement components (C3, C4, C5, C6, C7, Bf & Df)
have been demonstrated to be transmitted from mother to
offspring in rainbow trout, carp, spotted wolf fish and Atlantic
salmon.
First evidence is from the zebrafish embryo (C3 & Bf).
15. It is associated with the early defense against pathogens in
developing embryos and larvae.
Maternal immunization caused a remarkable increase in
C3 and Bf in the mother and a corresponding increase in
the offspring.
The embryos derived from immunized D. rerio were
significantly more tolerant to the pathogenic bacterium
Aeromonas hydrophila than those from unimmunized
mother.
16. Mode of action of maternally-
derived immune factors
Maternally-transferred immunity can not only protect fish
embryos and larvae but also prevent them from vertical transfer
from mother to offspring.
Both Pv and Lv were able to bind to the microbial conserved
components(PAMPs), including LPS (G – ve) PGN (G – ve and +
ve ) and lipoteichoic acid (LTA) of G + ve bacteria.
Pv is an effector molecule capable of killing bacteria directly.
Lv is an opsonin capable of enhancing macrophage phagocytosis.
17. Immune factor Function
Lysozymes
catalyze hydrolysis of 1,4-beta-linkages of bacterial cell walls,
thereby causing bacterial lysis
Lectins
interact with pathogenic surface carbohydrates leading to
opsonization, phagocytosis or activation of complement
Cathelicidin
an inhibitory effect on bacterial growth via degrading into
small peptides or stimulating the release of cytokines enabling
a more effective response to invading pathogens
Immunoglobulins such as IgM
opsonize bacteria, resulting in their degradation and
eradication by phagocytic cells.
Maternally-transferred complement components in fish eggs
operate via the AP, protecting embryos and larvae against
pathogenic attack.
18. Mode of maternally-derived
immune factor transfer
Whole the mode of maternally-derived immune factor transfer
remains largely unknown.
Mode of IgM and yolk protein transfer – reported in fish.
Maternal IgM is transferred from mother to offspring through
yolk in birds, reptiles and fishes.
In oviparous fishes, maternal IgM is initially transferred via
yolk to immature oocytes during vitellogenesis and then to eggs
and yolk sac larvae in a sequential manner.
19. In viviparous fishes, IgM is secreted from the epithelia of
the ovigerous lamellae of pregnant females into ovarian
cavity fluid and absorbed by enterocytes of the
hypertrophied hindgut in foetus.
Maternal IgM is transferred to piscine eggs by the
transcytosis across follicle cells.
In the entire IgM transfer process, follicular cells probably
play an active role because of the presence of IgM within
thecal and granulosa cells (and in the interposed basement
membrane) of pre-vitellogenic and vitellogenic follicles.
Maternal IgM can also be incorporated into fish oocytes
together with Vg.
20. Autogenous IgM synthesis and/or transfer of IgM mRNA
are also possible because a significant level of IgM gene
transcription has been observed in teleost oocytes.
In case of teleosts, maternally derived IgM usually persists
for limited duration, which gets exhausted within the
completion of yolk absorption process and completely
disappear during larval stages.
The persistence of maternal Ig - depending upon body size
and metabolic rate.
21. Yolk proteins
Transfer of Vg into piscine growing oocytes is dependent upon
their plasma membrane receptor for Vg.
Vg receptors have eight-repeat ligand-binding domain as key
structural elements and these multiple ovarian Vg receptors are
responsible for interaction with different types of Vg proteins.
It has been found that the lipovitellin domain of teleost Vg
mediates its binding to the oocyte receptor.
Interestingly, Vg receptor can be recycled to the oocyte surface
during the vitellogenic growth phase.
23. Transfer is particularly sensitive to the availability of
specific nutrients or minerals that are required as materials
or precursors for the synthetic process of immune factors.
Availability of nutrients such as protein, vitamins, fat and
fatty acid all affects the growth, maturation, reproductive
performances (including the process of vitellogenesis,
fertilization and hatchability) and immunity of brood,
and then impairs embryonic development and larval health
The pathogenic environment experienced by brood fish
during vitellogenesis affects the quality and quantity of the
immune factors transferred to offspring.
24. Possible applications in fish culture
Maternal immunity can therefore be used as an alternative
strategy to promote the immunity of fish larvae, thus
increasing their survival rate.
Practically, this can be easily achieved by feeding brood
fish with specific nutrients like vitamins or immunizing
brood fish with vaccines like inactivated pathogens.
25. Famous findings….
The administration of 0.2% β-glucan to rainbow trout fry only instead of
feeding both brood fish and fry could have the same positive effects in
promoting the immunity of fry and resistance to Y. ruckeri (Ghaedi G et al.,
2015).
Transfer of maternal immune factors from mother to offspring is particularly
sensitive to the availability of specific nutrients or minerals that are needed
as materials or precursors for the synthetic process of immune factors
(Zhang et al., 2013).
26. The protein extracts of scallop eggs exhibited
remarkable agglutination activity and
bactericidal effect against gram-negative
bacteria Escherichia coli and Vibro anguillarum,
and fungi Pichia pastoris. The results indicated
that scallop eggs or embryos received maternal
derived immune competence to defense against
the invading pathogens. (Yue F et al., 2013)
It therefore seems that a maternally
transmitted disease resistance induced by
glucan, protected the larvae against a
WSSV infection. (Huang C-C et al., 1999)
27. The physiological condition of parents has
a profound effect on their offspring fitness
by providing non-genetic factors, such as
hormones and nutrients (Groothuis et al.,
2005; Vijendravarma et al., 2010).
The maternal transferred immunity
from mother with immune experience
has positive impact on the offspring
immunity or disease resistance, which
is termed as trans-generational
immune priming (TGIP) (Sadd et al.,
2005).
In invertebrate, trans-generational effect of immunity
has been first demonstrated in shrimp Penaeus monodon
that offspring derived from glucan-injected mothers have
significantly higher survival rates than the control group
against WSSV infection (Huang and Song 1999).
28. Conclusion
Alternative strategy to promote the immunity of
fish larvae
Criteria for selective breeding programmes and/or
large scale brood stock immunization programmes.
Further studies has to initiate to examine the
degree of immunity transferred (species-wise) and
relationship between egg size and the efficiency of
maternal immunity.
29. References
Zhang S, Wang Z, Wang H (2013). Review - Maternal immunity in fish, Developmental
and Comparative Immunology 39; 72–78
Ghaedi G, Keyvanshokooh S, Azarma H M, Akhlaghi M (2015). Effects of dietary β-
glucan on maternal immunity and fry quality of rainbow trout (Oncorhynchus mykiss),
Aquaculture 441; 78–83
Huang C-C and Song Y-L (1999). Maternal transmission of immunity to white spot
syndrome associated virus (WSSV) in shrimp (Penaeus monodon ), Dev. and Comp.
Immunology 23; 545 – 552
Wang H, Ji D, Shao J, Zhang S (2012). Maternal transfer and protective role of
antibodies in zebrafish Danio rerio, Molecular Immunology 51; 332– 336
Mulero I, García-Ayala A, Meseguer J, Mulero V (2007). Maternal transfer of
immunity and ontogeny of autologous immunocompetence of fish: A minireview,
Aquaculture 268; 244–250
Swain P. and Nayak S.K. (2009). Review - Role of maternally derived immunity in
fish, Fish & Shellfish Immunology 27; 89–99
Mingming H, FuHong D, Zhen M, Jilin L (2014). The effect of vaccinating turbot
broodstocks on the maternal immunity transfer to offspring immunity, Fish & Shellfish
Immunology 39; 118-124
Editor's Notes
Cathelicidin-related antimicrobial peptides are a family of polypeptides found in lysosomes of macrophages andpolymorphonuclear leukocytes (PMNs)
Vitellogenin (VTG or less popularly known as VG) (from latin vitellus, yolk, and gener, to produce) is a synonymous term for the gene and the expressed protein. The protein molecule is classified as a glycolipoprotein, having properties of a sugar, fat and protein. It belongs to a family of several lipid transport proteins.