Transferencia Maternal

Developmental and Comparative Immunology 39 (2013) 72–78

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Developmental and Comparative Immunology

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Review

Maternal immunity in fish

Shicui Zhang a,⇑, Zhiping Wang b, Hongmiao Wang a

a Institute of Evolution and Marine Biodiversity and Department of Marine Biology, Ocean University of China, Qingdao 266003, Chinab Department of Life Science, Weinan Teachers University, Weinan 714000, China

a r t i c l e i n f o

Article history:Available online 28 February 2012

Keywords:FishMaternal immunityMaternal transferEggYolk proteins

0145-305X/$ - see front matter � 2012 Elsevier Ltd.doi:10.1016/j.dci.2012.02.009

Abbreviations: Vg, vitellogenin; Pv, phosvitin; Lpathway; AP, alternative pathway; LP, lectin pathwlectin; PAMPs, pathogen-associated molecular patteLTA, lipoteichoic acid; PGN, peptidoglycan.⇑ Corresponding author. Address: Room 205, Ke Xue

University of China, Qingdao 266003, China. Tel.: +86E-mail address: [email protected] (S. Zhang).

a b s t r a c t

Both innate and adaptive immune-relevant factors are transferred from mother to offspring in fishes.These maternally-transferred factors include IgM, lysozymes, lectin, cathelicidin and complementcomponents. Recently, yolk proteins, phosvitin and lipovitellin, have been shown to be maternally-transferred factors, functioning in the defense of teleost larvae against pathogens. Among these factors,the mode of action of complement components and yolk proteins has been explored, whereas that ofall the other factors remains elusive. At present, the transfer mechanisms of maternally-derived immunefactors are largely unknown although those of IgM and yolk protein transmission from mother to off-spring have been reported in some fishes. Maternal transfer of immunity is affected by many elements,including biological factors, such as age and maturation, and environmental conditions experienced bybrood fish, such as pathogens and nutritional supply. Practically, the manipulation of maternal immunitytransfer can be used to enhance the survival rate of fish larvae.

� 2012 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 722. Transfer of maternally-derived immune factors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73

2.1. Vg-derived proteins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 732.2. Complement components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73

3. Mode of action of maternally-derived immune factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 744. Mode of maternally-derived immune factor transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74

4.1. IgM . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 754.2. Yolk proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75

5. Factors affecting maternal immunity transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
5.1. Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 755.2. Pathogens. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
6. Possible applications in fish culture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76

1. Introduction

Maternal immunity refers to the immunity transferred acrossthe placenta, colostrum, milk or eggs from mother to offspring,which is supposed to play a key role to protect the vulnerable

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v, lipovitellin; CP, classicalay; MBL, mannose-binding

rns; LPS, lipopolysaccharide;

Guan, 5 Yushan Road, Ocean532 82032787.

offspring against pathogenic attacks. Maternal immunity was ini-tially described in mammals and birds more than 100 years ago(Ehrlich, 1892; Klemperer, 1893), and has now been documentedamong different vertebrates such as mammals (Leach et al., 1990;Dardillat et al., 1978; Gustafsson et al., 1994; Sadeharju et al.,2007), birds (Kissling et al., 1954; reviewed in Brambell, 1970;Heller et al., 1990; Bencina et al., 2005; Hamal et al., 2006), reptiles(Schumacher et al., 1999), amphibians (Poorten and Kuhn, 2009)and fishes (reviewed in Zapata et al., 2006; reviewed in Swainand Nayak, 2009) as well as in invertebrates including insect(Moret and Schmid-Hempel, 2001; Zanchi et al., 2011), shrimp(Huang and Song, 1999) and amphioxus (Liang et al., 2009).

Fig. 1. A diagram showing the transfer and persistence of maternal immunity with respect to acquisition of immunocompetence at the different stages of development. Bothinnate and adaptive immune-relevant factors are transferred from mother to offspring, which play a critical role to protect the vulnerable offspring against pathogenic attacksbefore full development and maturation of immune system in fish.

S. Zhang et al. / Developmental and Comparative Immunology 39 (2013) 72–78 73

Fish eggs are in most cases cleidoic, i.e. closed free-living systemfollowing fertilization; they are therefore supposed to dependupon the maternal provision of immune-relevant molecules forprotection against invading pathogens before full maturation ofimmunological systems (Fig. 1). In the past two decades, the mas-sive increase in aquaculture has put a greater emphasis on studiesof the immune system and defense mechanisms against diseasesassociated with fish. As a result, a great stride has been made inrecent years on the defense roles of maternally-derived factors inembryos and larvae in fishes, and our knowledge as such hasdramatically increased. Below we will discuss the transfer ofmaternally-derived immune factors, mode of action of mater-nally-derived factors, mode of maternally-derived factor transfer,factors affecting maternal immunity transfer and possibleapplication in fish culture, with a special emphasis on vitellogenin(Vg)-derived proteins and complement.

2. Transfer of maternally-derived immune factors

Previous studies on several fish species have shown that mater-nal IgM is able to be transferred from mother to offspring(Van Loon et al., 1981; Bly et al., 1986; Mor and Avtalion, 1990;Fuda et al., 1992; Castillo et al., 1993; Breuil et al., 1997; Olsenand Press, 1997; Hanif et al., 2004; Picchietti et al., 2004, 2006;Swain et al., 2006). Likewise, maternal transfer of the innate im-mune factors including the complement component C3 (Ellingsenet al., 2005; Huttenhuis et al., 2006; Løvoll et al., 2007; Wanget al., 2008, 2009), lectins (Bildfell et al., 1992; Tateno et al.,2002; Jung et al., 2003; Dong et al., 2004; Hasan et al., 2009),lysozymes (Yousif et al., 1991, 1994; Wang and Zhang, 2010) andcathelicidin (Seppola et al., 2009) to offspring has also beenreported in different teleost species. Moreover, immunization ofparents results in a significant increase in IgM levels (Mor andAvtalion, 1990; Sin et al., 1994; Oshima et al., 1996; Hanif et al.,2004) and lysozyme activities (Hanif et al., 2004) in the eggscompared to control. These maternally-derived immune factorshave been elegantly reviewed by Mulero et al. (reviewed in Muleroet al., 2007) and Swain and Nayak (reviewed in Swain and Nayak,2009). Here we will only describe the transfer of Vg-derivedproteins and complement components because their immunologi-cal function in fish embryos and larvae has been experimentallytested.

2.1. Vg-derived proteins

Vg is an egg yolk precursor protein, present in the females of alloviparous species including fish, amphibians, reptiles, birds, mostinvertebrates and the platypus. Vg is usually synthesized extra-ovarianly and transported by the circulation system to the ovary,where it is internalized into growing oocytes and proteolyticallycleaved to generate yolk proteins, phosvitin (Pv) and lipovitellin(Lv), that are later used as the nutrients by developing embryos(Arukwe and Goksøyr, 2003; reviewed in Finn and Fyhn, 2010).Vg was initially regarded as a female-specific protein (Pan et al.,1969); however its synthesis, albeit in smaller quantities, has beenshown to occur in male and sexually immature animals (reviewedin Engelmann, 1978; Piulacks et al., 2003). These suggest that Vgmay, in addition to being involved in yolk protein formation, playa role independent of gender. Recently, Vg has been shown to bean immune-relevant molecule involved in the defense of hostagainst the microbes including bacterium (Zhang et al., 2005; Shiet al., 2006; Li et al., 2008, 2009; Liu et al., 2009; Tong et al.,2010; reviewed in Zhang et al., 2011) and virus (Garcia et al., 2010).

Pv and Lv, that both are proteolytically cleaved products of Vg,are naturally transferred from mother to eggs in fish. They are tra-ditionally considered as the yolk reserves of nutrients essential forgrowth and development (reviewed in Finn and Fyhn, 2010). As Vghas been demonstrated to be an immune-relevant molecule, wethus hypothesize that its derived proteins, Pv and Lv, may also playan immunological role in developing embryos and larvae. Asexpected, Pv was proven to possess an antimicrobial activity inzebrafish embryos and larvae (Wang et al., 2011). In line with this,chicken egg yolk Pv was also shown to be able to inhibit thegrowth of the Gram-negative bacterium Escherichia coli (SattarKhan et al., 2000). Similarly, fish native Lv was associated withthe immune defense of rosy barb embryos and larvae (Zhang andZhang, 2011). All these demonstrate that Pv and Lv arematernally-transferred proteins involved in both nutritionalsupply and immune defense in embryos and larvae in fishes(Fig. 1).

2.2. Complement components

Complement system consisting of approximately 35 plasma andmembrane-bound proteins comprises one of the first lines of

74 S. Zhang et al. / Developmental and Comparative Immunology 39 (2013) 72–78

defense against pathogenic infection by alerting host the presenceof potential pathogens as well as clearing pathogens. There arethree pathways by which the complement system can be acti-vated: the classical pathway (CP), alternative pathway (AP) andlectin pathway (LP). The CP activation is initiated by binding ofantibody to the C1 complex, formed by C1q and two serine prote-ases (C1r and C1s), or by direct binding of the C1q component tothe pathogen surface, and requires both Ca2+ and Mg2+ (reviewedin Ruddy, 1974; reviewed in Robertson, 1998; Kishore and Reid,2000; reviewed in Trouw and Daha, 2011). The AP is mainlytriggered by the certain structures on microbial surface in anantibody-independent manner, and requires Mg2+ alone (reviewedin Yano, 1996; Zhang et al., 2003). The LP is activated by binding ofmicrobial polysaccharides to circulating lectins, such as mannose-binding lectin (MBL), and requires Ca2+ (reviewed in Morgan, 1995;reviewed in Turner, 1996; Thiel et al., 1997; reviewed in Willmentand Brown, 2008). These three pathways merge at a commonamplification step involving the formation of unstable proteasecomplexes, named C3-convertases (C3bBb in alternative pathwayand C4b2a in classical/lectin pathways), and the cleavage of C3to generate C3b and proceed through a terminal pathway that ini-tiates the assembly of a membrane attack complex, which leads tocomplement-mediated lysis. Different complement componentssuch as C3, C4, C5, C6, C7, factor B (Bf) and factor D have been dem-onstrated to be transmitted from mother to offspring in rainbowtrout (Løvoll et al., 2006), carp (Huttenhuis et al., 2006; Shenet al., 2011), spotted wolffish (Ellingsen et al., 2005) and Atlanticsalmon (Løvoll et al., 2007). Recently, we have found that bothC3 and Bf, the key factors functioning in the AP, are present inthe newly fertilized eggs of Danio rerio, providing the first evidencefor a maternal transfer of the complement proteins in zebrafish(Wang et al., 2008, 2009).

Maternal complement components in fish eggs have been pro-posed to be associated with the early defense against pathogensin developing embryos and larvae. However, firm evidence to sup-port this is rather limited. We showed for the first time that theGram-negative bacterium E. coli is sensitive to lysis by the cytosolprepared from the fertilized eggs of zebrafish, and the bacteriolyticactivity was abolished by pre-incubation of anti-C3 antibody withthe egg cytosol, a process that would cause the precipitation of thecentral component of all known complement pathways, C3. More-over, the lytic activity was depleted by heating at 45 �C, a temper-ature known to inactivate fish complement (reviewed in Zarkadiset al., 2001). Furthermore, maternal immunization caused aremarkable increase in C3 and Bf in the mother and a correspond-ing increase in the offspring, and accordingly, the embryos derivedfrom immunized D. rerio were significantly more tolerant to thepathogenic bacterium Aeromonas hydrophila than those fromunimmunized mother (Wang et al., 2009). These data show thatcomplement factors are indeed transferred from mother to eggs,and these maternally-transferred complement factors clearlyparticipate in the immune response protecting the developingembryos from pathogenic attacks.

3. Mode of action of maternally-derived immune factors

Eggs of most fish are released and fertilized externally, and theresulting embryos and larvae are therefore exposed to an aquaticenvironment full of potential pathogens (reviewed in Zapataet al., 2006). Maternally-transferred immunity can not only protectfish embryos and larvae against pathogenic agents present in theenvironment but also prevent them from vertical transfer frommother to offspring. Although the exact mode of action of mater-nally-transferred immune factors in the early stages of fish re-mains to be studied, different factors appear to function indifferent fashions. For example, maternally-transferred lysozymes

may catalyze hydrolysis of 1,4-beta-linkages of bacterial cell walls,thereby causing bacterial lysis (Huttenhuis et al., 2006); mater-nally-transferred lectins may interact with pathogenic surface car-bohydrates leading to opsonization, phagocytosis or activation ofcomplement (reviewed in Alexander and Ingram, 1992; Yousifet al., 1994; Tateno et al., 1998); and maternally-transferred cath-elicidin may exert an inhibitory effect on bacterial growth viadegrading into small peptides (Broekman et al., 2011; Lu et al.,2011) or stimulating the release of cytokines enabling a moreeffective response to invading pathogens (Bridle et al., 2011).Immunoglobulins such as IgM can opsonize bacteria, resulting intheir degradation and eradication by phagocytic cells. Mater-nally-transferred IgM in eggs and embryos may also act as anopsonin, facilitating the phagocytosis of opsonized bacteria byphagocytes (reviewed in Holland and Lambris, 2002).

To explore the underlying mechanisms how Vg-derived yolkproteins are involved in immune defense, we performed the pro-tein-microbe interaction analysis and enzyme-linked immuno-sorbent assay. It was found that both Pv and Lv were able tobind to the Gram-negative bacterium E. coli and the Gram-posi-tive bacterium Staphylococcus aureus. In agreement, they werealso able to bind to the microbial conserved components, calledpathogen-associated molecular patterns (PAMPs), including lipo-polysaccharide (LPS) of Gram-negative bacteria, peptidoglycan(PGN) of both Gram-negative and positive bacteria and lipotei-choic acid (LTA) of Gram-positive bacteria (Wang et al., 2011;Zhang and Zhang, 2011). These indicate that Pv and Lv are bothmultivalent pattern recognition receptors (PRR) capable of recog-nizing Gram-negative as well as positive bacteria via interactionwith PAMPs. In addition, we showed by scanning electronmicroscopy that Pv was able to cause lysis of both E. coli andS. aureus (Wang et al., 2011), and by phagocytosis test that coat-ing of E. coli and S. aureus with Lv facilitated the phagocytosis ofthese bacteria by macrophages (Zhang and Zhang, 2011). Thesedenote that Pv is an effector molecule capable of killing bacteriadirectly, whereas Lv is an opsonin capable of enhancing macro-phage phagocytosis.

To determine how maternally-transferred complement factorsfunction in the early stages of zebrafish, the antibodies againstC1q (a key component of CP), C4 (a key component of both CPand LP) and Bf (a key component of AP) were utilized to blockthe CP, LP or AP, respectively. It was found that precipitation ofC1q and C4 caused little loss of the bacteriolytic activity of theegg cytosol, whereas precipitation of Bf resulted in a significantreduction of the lytic activity. Furthermore, addition of EGTA toremove Ca2+ from the egg cytosol, which can inhibit both CPand LP, induced little decrease in the bacteriolytic activity. Incontrast, pre-incubation of EDTA with the egg cytosol led to asubstantial reduction of the bacteriolytic activity, and saturationof the chelator with Mg2+ was capable of restoring the lytic activ-ity, but not by addition of Ca2+. Moreover, selective inhibition ofthe AP by zymosan A induced a marked loss of bacteriolyticactivity, while addition of L-lysine, an inactivator of the CP, wasnot inhibitory. All these clearly indicate that maternally-trans-ferred complement components in fish eggs operate via the AP,protecting embryos and larvae against pathogenic attack (Wanget al., 2008).

4. Mode of maternally-derived immune factor transfer

The mode of IgM and yolk protein transfer from mother to off-spring has been reported in some fish, but as a whole the mode ofmaternally-derived immune factor transfer remains largely un-known. Here our discussion will focus on the mode of IgM and yolkproteins in fish.


4.1. IgM

In mammals, maternal immunoglobulin G (IgG) is transportedacross the placenta from mother to fetus. IgG from breast milk inmany mammalian species (rodents, bovines, cats, ferrets, etc.) isalso transported across the intestinal epithelium into the neonatalcirculation. In contrast, maternal IgM is transferred from mother tooffspring through yolk in birds, reptiles and fishes. Maternal trans-fer of IgM has been demonstrated in different fishes. In oviparousfishes, maternal IgM is initially transferred via yolk to immatureoocytes during vitellogenesis and then to eggs and yolk sac larvaein a sequential manner (Kanlis et al., 1995). In viviparous fishessuch as Neoditrema ransonneti (Embiotocidae), IgM is secreted fromthe epithelia of the ovigerous lamellae of pregnant females intoovarian cavity fluid and absorbed by enterocytes of the hypertro-phied hindgut in fetus (Nakamura et al., 2006).

The transplacental transfer of mammalian IgG involves an Fcreceptor-mediated transcytosis of IgG across the syncytiotropho-blast barrier and a transcellular pathway through the endotheliumof fetal capillaries (reviewed in Simister, 2003; Fuchs and Ellinger,2004). Analogously, maternal IgM is also transferred to piscineeggs by the transcytosis across follicle cells (Picchietti et al.,2006). In the entire IgM transfer process, follicular cells probablyplay an active role because of the presence of IgM within thecaland granulosa cells (and in the interposed basement membrane)of pre-vitellogenic and vitellogenic follicles. Further studies shouldbe performed to define if Fc receptors are present in the oocytesand involved in the process of IgM transfer to the oocytes.

Maternal IgM can also be incorporated into fish oocytestogether with Vg. This is supported by the facts that IgM concen-tration in Pagrus major oocytes was increased throughout vitello-genesis (Kanlis et al., 1995) and detection of IgM was limited tothe mature ovary of Cyprinus carpio (Suzuki et al., 1994). However,autogenous IgM synthesis and/or transfer of IgM mRNA are alsopossible because a significant level of IgM gene transcription hasbeen observed in teleost oocytes (Picchietti et al., 2006). Therefore,a detailed study is needed to establish the mode of maternal IgMtransfer in different fish species.

4.2. Yolk proteins

During oogenesis in the chicken, Vg is taken up into the growingoocytes via a member of the low density lipoprotein receptor genefamily termed LR8 (Bujo et al., 1994). This ligand-receptor medi-ated endocytosis of Vg is accompanied by degradation of the yolkprecursor protein by cathepsin D, generating Pv and Lv depositedin yolk granules (Barber et al., 1991; Schneider, 1996). The receptorexists in two isoforms that differ by a so-called O-linked sugar do-main; the shorter form (LR8�) is present exclusively in the oocytesproper, and the longer protein (LR8+) predominates in somatic cells(Hermann et al., 2000). Vg receptor is localized in coated pits onthe surface of growing oocytes and is of vital importance to egg-laying hen. Similarly, transfer of Vg into piscine growing oocytesis also dependent upon their plasma membrane receptor for Vg.Vg receptors from white perch, tilapia, salmon and rainbow troutwere shown to share key structural elements (e.g. an eight-repeatligand-binding domain) with Vg receptors from chicken (Stifaniet al., 1990; Hiramatsu et al., 2004a). Multiple ovarian Vg receptorshave been reported in white perch and rainbow trout (Tyler andLubberink, 1996; Hiramatsu et al., 2002; Reading et al., 2011), thatmay be responsible for interaction with different types of Vg pro-teins. It has been found that the lipovitellin domain of teleost Vgmediates its binding to the oocyte receptor (Stifani et al., 1990;Hiramatsu et al., 2002, 2004b). Interestingly, Vg receptor can berecycled to the oocyte surface during the vitellogenic growth phase(Perazzolo et al., 1999; Hiramatsu et al., 2004a).

5. Factors affecting maternal immunity transfer

Many factors affect the immunity of brood fish, thereby exert-ing an influence on the transfer of maternal immunity to offspring,especially when fishes are experienced a pathogenic conditionprior to the egg production period. These factors include water pol-lution (reviewed in Schwedler et al., 1985), adverse environmentalconditions (Miller and Clen, 1984; reviewed in Zapata et al., 1992;Swain et al., 2007; reviewed in Bowden et al., 2007; Valenzuelaet al., 2007) and stress conditions like handling (Ellsaesser andClem, 1986) and crowding (Klinger et al., 1983; Ortuno et al.,2001) as well as some biological factors such as age, maturationand reproduction (Slater and Schreck, 1993; Suzuki et al., 1996,1997; reviewed in Harris and Bird, 2000). Here we only briefly dis-cuss the effects of nutrients and pathogens on brood fish immunityand its transfer from mother to offspring.

5.1. Nutrients

Role of nutrition and its effect on immunity and disease resis-tance have been established in fish as well as in other aquaticanimals (reviewed in Blazer, 1992; reviewed in Lall and Olivier,1993). Thus, transfer of maternal immune factors from mother tooffspring is particularly sensitive to the availability of specificnutrients or minerals that are required as materials or precursorsfor the synthetic process of immune factors. Poor nutrient supplyor unreasonable proportioning of supplied nutrients will depressthe maternal synthesis of immune factors, and hence decrease theirquality and quantity transferred to offspring. Previous studies haveshown that availability of nutrients such as protein, vitamins, fat andfatty acid all affects the growth, maturation, reproductive perfor-mances (including the process of vitellogenesis, fertilization andhatchability) and immunity of brood fish (reviewed in Swain andNayak, 2009), and then impairs embryonic development and larvalhealth. For example, L-ascorbic acid supplementation in broodstockdiet has been correlated with lysozyme activity in sea bass embryosand larvae (Cecchini et al., 2000). It is clear that the nutrients for fe-male fish exert a profound influence on the synthesis and verticaltransfer of maternal immune factors, and hence on the egg qualityand health status of offspring at early stages. However, informationas such is rather limited, and needs further study.

5.2. Pathogens

The environment experienced by brood fish during vitellogene-sis affects the quality and quantity of the immune factors trans-ferred to offspring. The females that have not been exposed toparticular pathogens will not synthesize antibody specific to thosepathogens and their immune responses remain at low levels, lead-ing to the limited transfer of maternal immunity, therefore, theiroffspring are susceptible to infection. In contrast, the mothers ex-posed to particular pathogens will synthesize more immune factorsincluding both adaptive and innate immune components, these fac-tors can then be transferred to offspring, helping them to mount ra-pid and efficient immune responses when challenged with the samepathogen. For example, immunization of female fishes with differ-ent pathogens not only enhanced the vertical transfer of mater-nally-derived immune factors but also improved the survivabilityof their offspring (Mor and Avtalion, 1990; Sin et al., 1994; Oshimaet al., 1996; Hanif et al., 2004; Swain et al., 2006; Wang et al., 2009).

6. Possible applications in fish culture

Significant mortality is routinely recorded at larval and postlarval stages of fishes over the world, and how to enhance the


survival rate of fish larvae is a problem of practical importance.Moreover, fish larvae have no or only limited immune responseability before the maturation of their immune system, thus directimmunization on them can not improve their immunity. As mater-nally-transferred immune factors have been proven to be able totransfer from mother to offspring and enhance the immunity offish larvae, maternal immunity can therefore be used as analternative strategy to promote the immunity of fish larvae, thusincreasing their survival rate. Practically, this can be easilyachieved by feeding brood fish with specific nutrients like vitaminsor immunizing brood fish with vaccines like inactivated pathogens.

Acknowledgements

This work was supported by Grants of Ministry of Science andTechnology of China (2012CB114404) and Natural Science Founda-tion of China (30972274) to SCZ.

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