Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity

Grindstaff, Jennifer L.; Hasselquist, Dennis; Nilsson, Jan‐Åke; Sandell, Maria I.; Smith, Henrik G.; Stjernman, Martin

doi:10.1098/rspb.2006.3608

Cited by 131 publications

(180 citation statements)

References 38 publications

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“…Queen bumblebees (Bombus terrestris) injected with bacteria produce workers that show higher levels of antibacterial activity [65]. Immunized pied flycatchers (F. hypoleuca) produce offspring with elevated endogenous antibody production [66]. Offspring from mice infected with an intestinal nematode when pregnant are more likely to clear infection as adults [20,67].…”

Section: Discussionmentioning

confidence: 99%

“…A third group of mechanisms involves epigenetic effects, whereby maternal experience affects DNA expression, but not sequences, in offspring [24]. This may be achieved by the modulation of DNA methylation via changes in the exposure of offspring to androgens and other hormones [19,25,26], or through other biochemical mechanisms [27].…”

Section: Introductionmentioning

confidence: 99%

“…Maternal exposure to pathogens or antigens (e.g. bacterial polysaccharides) promotes offspring immunocompetence in species ranging from insects to birds and mammals [19][20][21]. The mechanisms that bring about TGIP are varied [9].…”

Section: Introductionmentioning

confidence: 99%

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Infection before pregnancy affects immunity and response to social challenge in the next generation

Curno

Reader

McElligott

et al. 2011

Phil. Trans. R. Soc. B

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Natural selection should favour parents that are able to adjust their offspring's life-history strategy and resource allocation in response to changing environmental and social conditions. Pathogens impose particularly strong and variable selective pressure on host life histories, and parental genes will benefit if offspring are appropriately primed to meet the immunological challenges ahead. Here, we investigated transgenerational immune priming by examining reproductive resource allocation by female mice in response to direct infection with Babesia microti prior to pregnancy. Female mice previously infected with B. microti gained more weight over pregnancy, and spent more time nursing their offspring. These offspring generated an accelerated response to B. microti as adults, clearing the infection sooner and losing less weight as a result of infection. They also showed an altered hormonal response to novel social environments, decreasing instead of increasing testosterone production upon social housing. These results suggest that a dominance-resistance trade-off can be mediated by cues from the previous generation. We suggest that strategic maternal investment in response to an infection leads to increased disease resistance in the following generation. Offspring from previously infected mothers downregulate investment in acquisition of social dominance, which in natural systems would reduce access to mating opportunities. In doing so, however, they avoid the reduced disease resistance associated with increased testosterone and dominance. The benefits of accelerated clearance of infection and reduced weight loss during infection may outweigh costs associated with reduced social dominance in an environment where the risk of disease is high.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Infection before pregnancy affects immunity and response to social challenge in the next generation

Curno

Reader

McElligott

et al. 2011

Phil. Trans. R. Soc. B

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“…Behavioural, endocrine and epigenetic correlates of maternal experiences are thought to prime the offspring to elevate resilience and enhance survival under adverse environmental conditions [124,125]). For example, mouse offspring exposed to maternal stress develop some resilience to social stress when adult [120].…”

Section: Transgenerational Programming Of Stress Resiliencementioning

confidence: 99%

Section: Transgenerational Programming Of Stress Resiliencementioning

confidence: 99%

Non-genetic Inheritance of Behaviour and Stress Resilience

Hao¹,

Metz²

2013

Non-Genetic Inheritance

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IntroductionResearch in the past 15 years has provided groundbreaking new insights into the determinants of brain function and behavioural traits across generations. Aside from genetic inheritance and environmental experiences, we have learned that individual differences in behaviour appear to be programmed by transgenerational epigenetic mechanisms. These insights represent milestones in the identification of the origins of neurological and psychiatric diseases. The incidence of these conditions, including Parkinson's disease, multiple sclerosis, depression, and schizophrenia, has risen sharply over the past decades. The origins of these conditions in most cases remain unknown, however, striking evidence suggests that the onset and severity of these conditions of the brain are influenced by adverse experiences, such as stress [1][2][3]. Stress may program behaviour and physiology of subsequent generations to facilitate adaptive responses to a stressful environment, however, it may also alter the offspring's health trajectories [4][5][6][7][8][9]. So far three main mechanisms were suggested to mediate transgenerational inheritance of phenotype and health status, including epigenetic regulation of gene expression [10], alterations in parental behaviour (e.g., licking and grooming) and physiological programming by means of an altered stress response [8]. The unifying feature of these non-genomic routes of transmission is that they operate in the absence of changes in the DNA sequence. In this review we propose that the risk of behavioural changes, neurological and psychiatric diseases is critically determined by individual stress vulnerability and resilience, which is programmed across generations through non-genomic mechanisms.It is well established that stress represents a striking influence on mental health [11,12]. For example, a series of studies investigating the response of pregnant women to the World Trade Centre attacks on September 11, 2001 revealed an elevated incidence of post-traumatic stress disorder (PTSD) among these women and propagation of the associated physiological responses to their children [13,14]. Consequently, these mothers as well as their infants showed greater stress responses to novel situations [13]. Understanding the neurological roots of both stress vulnerability and resilience in these and other cases may provide new means of prevention and treatment for psychiatric disease and stress-related neurological disorders [15,16]. The following will discuss possible behavioural, endocrine and epigenetic correlates of non-genomic programming. Abstract Recent research has shown that brain function and behaviour can be influenced by experience and environmental conditions of previous generations. Studies of the mechanisms of transgenerational programming may provide milestones in the identification of the origins of mental illness and neurological disorders. The origins of neurological conditions in most cases remain unknown, however, striking evidence suggests that onset and severity are i...

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Estrogen‐dependent sex difference in microglia in the developing brain of Japanese quail (Coturnix japonica)

Delage

Cornil

2020

Developmental Neurobiology

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Although they are usually viewed as the first line of defense in response to injury, inflammation, or disease (Nayak et al., 2014), microglia, the brain immunocompetent cells, have emerged as major contributors of brain development as well as homeostasis throughout life (Cuadros et al., 1994; Lenz & McCarthy, 2014). Microglia are myeloid cells originating from the yolk sac that start colonizing the developing brain around embryonic day 9.5-10.5 in rodents (Ginhoux et al., 2010) and as early as 4.5 gestational weeks in humans (Verney et al., 2010). They enter the brain via the ventricles, meninges, and developing blood vessels under an immature ameboid form (Thion & Garel, 2017). They migrate and proliferate through the nervous system parenchyma (Nikodemova et al., 2015; Tay et al., 2016), then progressively transition to ramified microglia as they reach their final location (Lannes et al., 2017; Thion et al., 2018). After the formation of the blood-brain barrier, microglia proliferate by self-renewal throughout life (Ajami et al.,

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Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity

Cited by 131 publications

References 38 publications

Infection before pregnancy affects immunity and response to social challenge in the next generation

Infection before pregnancy affects immunity and response to social challenge in the next generation

Non-genetic Inheritance of Behaviour and Stress Resilience

Estrogen‐dependent sex difference in microglia in the developing brain of Japanese quail (Coturnix japonica)

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