Long‐term maternal imprinting of the specific B cell repertoire by maternal antibodies

Fink, Katja; Zellweger, Raphaël M.; Weber, Jacqueline; Manjarrez‐Orduño, Nataly; Holdener, Martin; Senn, Beatrice M.; Hengartner, Hans; Zinkernagel, Rolf M.

doi:10.1002/eji.200737872

Cited by 32 publications

(20 citation statements)

References 54 publications

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“…This could be especially the case for long-lived colonial birds such as Procellariiformes, which can breed in aggregates of thousands of pairs. In addition to protective effects against pathogens, maternal antibodies have been suggested to be responsible for an educational effect by acting on the ongoing process of lymphocytes maturation to select clones that display a higher reaction to selected parasites [50]. Maternal antibodies could also allow the occurrence of a 'natural vaccination' by attenuating the effects of an infection by a parasite, thus producing optimal conditions for the immunization of the newborn [51], a mechanism that might be particularly valuable in longlived species.…”

Section: Discussionmentioning

confidence: 99%

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

et al. 2011

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The evolution of different life-history strategies has been suggested as a major force constraining physiological mechanisms such as immunity. In some long-lived oviparous species, a prolonged persistence of maternal antibodies in offspring could thus be expected in order to protect them over their long growth period. Here, using an intergenerational vaccination design, we show that specific maternal antibodies can display an estimated half-life of 25 days post-hatching in the nestlings of a long-lived bird. This temporal persistence is much longer than previously known for birds and it suggests specific properties in the regulation of IgY immunoglobulin catabolism in such a species. We also show that maternal antibodies in the considered procellariiform species are functional as late as 20 days of age. Using a modelling approach, we highlight that the potential impact of such effects on population viability could be important, notably when using vaccination for conservation. These results have broad implications, from comparative immunology to evolutionary eco-epidemiology and conservation biology.

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Section: Discussionmentioning

confidence: 99%

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

et al. 2011

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“…However, some evidence also supports a positive effect via immunological imprinting (Gasparini et al 2006;Grindstaff et al 2006;Reid et al 2006). The exact mechanism is unclear, but the B-cell repertoire may somehow model itself after antibodies in circulation (Fink et al 2008).…”

Section: Discussionmentioning

confidence: 99%

Ecological and life-history factors influencing the evolution of maternal antibody allocation: a phylogenetic comparison

et al. 2009

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Maternally derived yolk antibodies provide neonates with immune protection in early life at negligible cost to mothers. However, developmental effects on the neonate's future immunity are potentially costly and thus could limit yolk antibody deposition. The benefits to neonatal immunity must be balanced against costs, which may depend on neonate vulnerability to pathogens, developmental trajectories and the immunological strategies best suited to a species' pace of life. We measured yolk antibodies and life-history features of 23 species of small Neotropical birds and assessed the evidence for each of several hypotheses for life history and ecological effects on the evolution of yolk antibody levels. Developmental period and yolk antibodies are negatively related, which possibly reflect the importance of humoral immune priming through antigen exposure, and selection to avoid autoimmunity, in species with a slower pace of life. There is also a strong relationship between body size and yolk antibody concentration, suggesting that larger species are architecturally equipped to produce and transfer higher concentrations of antibodies. These results suggest that developmental effects of maternally derived antibodies, such as imprinting effects on B-cell diversity or autoimmune effects, are important and deserve more consideration in future research.

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“…Therefore, maternal antibody plays an essential role in shaping the specific antibody repertoire and peripheral B cell development in the neonate long after the maternal antibodies themselves become undetectable (16,17).…”

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confidence: 99%

Protective Role of Passively Transferred Maternal Cytokines against Bordetella pertussis Infection in Newborn Piglets

et al. 2017

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Maternal vaccination represents a potential strategy to protect both the mother and the offspring against life-threatening infections. This protective role has mainly been associated with antibodies, but the role of cell-mediated immunity, in particular passively transferred cytokines, is not well understood. Here, using a pertussis model, we have demonstrated that immunization of pregnant sows with heat-inactivated bacteria leads to induction of a wide range of cytokines (e.g., tumor necrosis factor alpha [TNF-␣], gamma interferon [IFN-␥], interleukin-6 [IL-6], IL-8, and IL-12/IL-23p40) in addition to pertussis-specific antibodies. These cytokines can be detected in the sera and colostrum/milk of vaccinated sows and subsequently were detected at significant levels in the serum and bronchoalveolar lavage fluid of piglets born to vaccinated sows together with pertussis-specific antibodies. In contrast, active vaccination of newborn piglets with heat-inactivated bacteria induced high levels of specific IgG and IgA but no cytokines. Although the levels of antibodies in vaccinated piglets were comparable to those of passively transferred antibodies, no protection against Bordetella pertussis infection was observed. Thus, our results demonstrate that a combination of passively transferred cytokines and antibodies is crucial for disease protection. The presence of passively transferred cytokines/antibodies influences the cytokine secretion ability of splenocytes in the neonate, which provides novel evidence that maternal immunization can influence the newborn's cytokine milieu and may impact immune cell differentiation (e.g., Th1/Th2 phenotype). Therefore, these maternally derived cytokines may play an essential role both as mediators of early defense against infections and possibly as modulators of the immune repertoire of the offspring.

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Long‐term maternal imprinting of the specific B cell repertoire by maternal antibodies

Cited by 32 publications

References 54 publications

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

Ecological and life-history factors influencing the evolution of maternal antibody allocation: a phylogenetic comparison

Protective Role of Passively Transferred Maternal Cytokines against Bordetella pertussis Infection in Newborn Piglets

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