A Common Language: How Neuroimmunological Cross Talk Regulates Adult Hippocampal Neurogenesis

Leiter, Odette; Kempermann, Gerd; Walker, Tara L.

doi:10.1155/2016/1681590

Cited by 25 publications

(18 citation statements)

References 166 publications

(188 reference statements)

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“…Peripheral immune cells and the factors they secrete can influence adult neurogenesis, not only in the context of disease but also under baseline conditions 1 – 5 . Mast cells (MC), widely known for their role in allergy and histaminergic responses 6 , 7 , are derived from hematopoietic stem cells and reside in small numbers within the brain from birth.…”

Section: Introductionmentioning

confidence: 99%

Mast cells increase adult neural precursor proliferation and differentiation but this potential is not realized in vivo under physiological conditions

Wasielewska

Grönnert

Rund

et al. 2017

Sci Rep

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There is growing evidence that both peripheral and resident immune cells play an important part in regulating adult neural stem cell proliferation and neurogenesis, although the contribution of the various immune cell types is still unclear. Mast cells, a population of immune cells known for their role in the allergic response, have been implicated in the regulation of adult hippocampal neurogenesis. Mast cell-deficient c-kitW-sh/W-sh mice have previously been shown to exhibit significantly decreased adult hippocampal neurogenesis and associated learning and memory deficits. However, given that numerous other cell types also express high levels of c-kit, the utility of these mice as a reliable model of mast cell-specific depletion is questionable. We show here, using a different model of mast cell deficiency (Mcpt5CreR26DTA/DTA), that precursor proliferation and adult neurogenesis are not influenced by mast cells in vivo. Interestingly, when applied at supraphysiological doses, mast cells can activate latent hippocampal precursor cells and increase subventricular zone precursor proliferation in vitro, an effect that can be blocked with specific histamine-receptor antagonists. Thus, we conclude that while both mast cells and their major chemical mediator histamine have the potential to affect neural precursor proliferation and neurogenesis, this is unlikely to occur under physiological conditions.

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Section: Introductionmentioning

confidence: 99%

Mast cells increase adult neural precursor proliferation and differentiation but this potential is not realized in vivo under physiological conditions

Wasielewska

Grönnert

Rund

et al. 2017

Sci Rep

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“…Indeed, exposure to young and old blood modulates transcriptional hallmarks of CP aging (Baruch et al 2014 ) that may in turn affect the CP secretome, shown to modulate neurogenesis in an age-dependent manner. At the neurogenic niche level, aging results in altered vasculature, microgliosis and astrogliosis, all of which can in turn regulate neurogenesis (Leiter et al 2016 ). While exposure to young blood has been shown to increase vasculature in the aged mouse SVZ (Katsimpardi et al 2014 ), the extent to which the aging systemic environment alters the neurogenic niche is not fully understood.…”

Section: Discussionmentioning

confidence: 99%

“…The neurogenic niche is complex, comprised of many different cell types that influence NSC function (reviewed by Aimone et al 2014 ). Vasculature, microglia, and astrocytes have all been shown support adult neurogenesis under basal conditions; however, this homeostatic relationship can be disrupted, particularly in the context of inflammation (Leiter et al 2016 ). Thus, it has been postulated that age-related changes to the neurogenic niche—which include astrogliosis, microgliosis and vasculature deterioration—may contribute to the age-related decline in adult neurogenesis (Leiter et al 2016 ).…”

Section: Neurogenic Niche: Mediator Of the Aging Systemic Environmentmentioning

confidence: 99%

“…Vasculature, microglia, and astrocytes have all been shown support adult neurogenesis under basal conditions; however, this homeostatic relationship can be disrupted, particularly in the context of inflammation (Leiter et al 2016 ). Thus, it has been postulated that age-related changes to the neurogenic niche—which include astrogliosis, microgliosis and vasculature deterioration—may contribute to the age-related decline in adult neurogenesis (Leiter et al 2016 ). Given the inflammatory remodeling that occurs in blood during aging, it is possible that the age-related changes in the neurogenic niche at least partially reflect blood aging, thereby providing an additional mechanism by which blood aging could regulates neurogenesis.…”

Section: Neurogenic Niche: Mediator Of the Aging Systemic Environmentmentioning

confidence: 99%

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The systemic environment: at the interface of aging and adult neurogenesis

2017

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Aging results in impaired neurogenesis in the two neurogenic niches of the adult mammalian brain, the dentate gyrus of the hippocampus and the subventricular zone of the lateral ventricle. While significant work has characterized intrinsic cellular changes that contribute to this decline, it is increasingly apparent that the systemic environment also represents a critical driver of brain aging. Indeed, emerging studies utilizing the model of heterochronic parabiosis have revealed that immune-related molecular and cellular changes in the aging systemic environment negatively regulate adult neurogenesis. Interestingly, these studies have also demonstrated that age-related decline in neurogenesis can be ameliorated by exposure to the young systemic environment. While this burgeoning field of research is increasingly garnering interest, as yet, the precise mechanisms driving either the pro-aging effects of aged blood or the rejuvenating effects of young blood remain to be thoroughly defined. Here, we review how age-related changes in blood, blood-borne factors, and peripheral immune cells contribute to the age-related decline in adult neurogenesis in the mammalian brain, and posit both direct neural stem cell and indirect neurogenic niche-mediated mechanisms.

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“…There is also an indirect effect of T cells likely to be mediated via interaction with monocyte-derived macrophages or astrocytes (Garg et al, 2009;Walsh et al, 2014). Increasing evidence suggests that peripheral immune cells coming to the brain via the blood stream positively influence adult neurogenesis in the rodent hippocampus (recently reviewed by (Leiter et al, 2016)). As discussed above, monocyte-derived macrophages and microglia have functionally different subtypes.…”

Section: T Lymphocytesmentioning

confidence: 99%

Role of the immune response in initiating central nervous system regeneration in vertebrates: learning from the fish

Bosak¹,

Murata²,

Bludau³

et al. 2018

Int. J. Dev. Biol.

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The mammalian central nervous system is not able to regenerate neurons lost upon injury. In contrast, anamniote vertebrates show a remarkable regenerative capacity and are able to replace damaged cells and restore function. Recent studies have shown that in naturally regenerating vertebrates, such as zebrafish, inflammation is a key processes required for the initiation of regeneration. These findings are in contrast to many studies in mammals, where the central nervous system has long been viewed as an immune-privileged organ with inflammation considered one of the key negative factors causing lack of neuronal regeneration. In this review, we discuss similarities and differences between naturally regenerating vertebrates, and those with very limited to non-existing regenerative capacity. We will introduce neural stem and progenitor cells in different species and explain how they differ in their reaction to acute injury of the central nervous system. Next, we illustrate how different organisms respond to injuries by activation of their immune system. Important immune cell types will be discussed in relation to their effects on neural stem cell behavior. Finally, we will give an overview on key inflammatory mediators secreted upon injury that have been linked to activation of neural stem cells and regeneration. Overall, understanding how species with regenerative potential couple inflammation and successful regeneration will help to identify potential targets to stimulate proliferation of neural stem cells and subsequent neurogenesis in mammals and may provide targets for therapeutic intervention strategies for neurodegenerative diseases.

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A Common Language: How Neuroimmunological Cross Talk Regulates Adult Hippocampal Neurogenesis

Cited by 25 publications

References 166 publications

Mast cells increase adult neural precursor proliferation and differentiation but this potential is not realized in vivo under physiological conditions

Mast cells increase adult neural precursor proliferation and differentiation but this potential is not realized in vivo under physiological conditions

The systemic environment: at the interface of aging and adult neurogenesis

Role of the immune response in initiating central nervous system regeneration in vertebrates: learning from the fish

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