Activity‐Dependent Notch Signalling in the Hypothalamic‐Neurohypophysial System of Adult Mouse Brains

Mannari, Tetsuya; Miyata, Seiji

doi:10.1111/jne.12172

Cited by 5 publications

(8 citation statements)

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“…For example, Notch signaling or the cleavage of Notch1 is activated by an increase in synaptic activity and plays a role in synaptic plasticity in the hippocampal CA1 region ( 126 ). DLL4 and Notch3 were found to be expressed at OXT-containing axonal terminals and pituicytes in the NH, respectively [( 41 ); Figures 10 A,A’]. Similarly, the strong expression of DLL4 was observed at axonal terminals and vascular pericytes in the ME [( 42 ); Figures 10 B,B’,C,C’].…”

Section: Notch Signaling and The Extracellular Microenvironmentmentioning

confidence: 99%

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Advances in Understanding of Structural Reorganization in the Hypothalamic Neurosecretory System

Miyata

2017

Front. Endocrinol.

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The hypothalamic neurosecretory system synthesizes neuropeptides in hypothalamic nuclei and releases them from axonal terminals into the circulation in the neurohypophysis (NH) and median eminence (ME). This system plays a crucial role in regulating body fluid homeostasis and social behaviors as well as reproduction, growth, metabolism, and stress responses, and activity-dependent structural reorganization has been reported. Current knowledge on dynamic structural reorganization in the NH and ME, in which the axonal terminals of neurosecretory neurons directly contact the basement membrane (BM) of a fenestrated vasculature, is discussed herein. Glial cells, pituicytes in the NH and tanycytes in the ME, engulf axonal terminals and interpose their cellular processes between axonal terminals and the BM when hormonal demands are low. Increasing demands for neurosecretion result in the retraction of the cellular processes of glial cells from axonal terminals and the BM, permitting increased neurovascular contact. The shape conversion of pituicytes and tanycytes is mediated by neurotransmitters and sex steroid hormones, respectively. The NH and ME have a rough vascular BM profile of wide perivascular spaces and specialized extension structures called "perivascular protrusions." Perivascular protrusions, the insides of which are occupied by the cellular processes of vascular mural cells pericytes, contribute to increasing neurovascular contact and, thus, the efficient diffusion of hypothalamic neuropeptides. A chronic physiological stimulation has been shown to increase perivascular protrusions via the shape conversion of pericytes and the profile of the vascular surface. Continuous angiogenesis occurs in the NH and ME of healthy normal adult rodents depending on the signaling of vascular endothelial growth factor (VEGF). The inhibition of VEGF signaling suppresses the proliferation of endothelial cells (ECs) and promotes their apoptosis, which results in decreases in the population of ECs and axonal terminals. Pituicytes and tanycytes are continuously replaced by the proliferation and differentiation of stem/progenitor cells, which may be regulated by matching those of ECs and axonal terminals. In conclusion, structural reorganization in the NH and ME is caused by the activity-dependent shape conversion of glial cells and vascular mural cells as well as the proliferation of endothelial and glial cells by angiogenesis and gliogenesis, respectively.

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Section: Notch Signaling and The Extracellular Microenvironmentmentioning

confidence: 99%

“…Scale bars represent 50 μm (A) , 10 μm (D) , and 1 μm (E) . Micrographs are rearranged with courtesy from BioScientifica [ (A) ( 40 )] and permission from Springer [ (C) ( 41 )] and John Wiley & Sons [ (B) ( 42 )]; [ (D,E) ( 23 )].…”

Section: Size-limited Vascular Permeabilitymentioning

confidence: 99%

Advances in Understanding of Structural Reorganization in the Hypothalamic Neurosecretory System

Miyata

2017

Front. Endocrinol.

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“…This neuroglial and neurovascular reconstruction was previously attributed to the shape conversion of pituicytes via β‐adrenergic receptor signalling . Moreover, several molecules are proposed to play roles in the neuroglial and neurovascular contacts resulting in this structural reconstruction, such as cell adhesion molecules , tenascin‐C , chondroitin sulphate proteoglycans , DLL4 and extracellular matrix‐degrading enzymes . Thus, the structural reconstruction of neuroglial and neurovascular contacts during dehydration and lactation is responsible for accelerating neuropeptide release by increasing the contact area between the axonal terminals and vascular surface .…”

mentioning

confidence: 93%

“…The NH has been shown to undergo marked activity‐dependent structural reconstruction during a chronic physiological stimulation, such as dehydration and lactation . Neurohypophysial resident glial cells, or pituicytes, surround the axonal terminals of magnocellular neurones under normal conditions, whereas a chronic physiological stimulation increases the direct contact of axonal terminals with the outer basement membrane or vascular surface . This neuroglial and neurovascular reconstruction was previously attributed to the shape conversion of pituicytes via β‐adrenergic receptor signalling .…”

mentioning

confidence: 99%

Structural Reconstruction of the Perivascular Space in the Adult Mouse Neurohypophysis During an Osmotic Stimulation

Nishikawa

Furube

Morita

et al. 2017

J Neuroendocrinology

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Oxytocin (OXT) and arginine vasopressin (AVP) neuropeptides in the neurohypophysis (NH) control lactation and body fluid homeostasis, respectively. Hypothalamic neurosecretory neurones project their axons from the supraoptic and paraventricular nuclei to the NH to make contact with the vascular surface and release OXT and AVP. The neurohypophysial vascular structure is unique because it has a wide perivascular space between the inner and outer basement membranes. However, the significance of this unique vascular structure remains unclear; therefore, we aimed to determine the functional significance of the perivascular space and its activity-dependent changes during salt loading in adult mice. The results obtained revealed that pericytes were the main resident cells and defined the profile of the perivascular space. Moreover, pericytes sometimes extended their cellular processes or 'perivascular protrusions' into neurohypophysial parenchyma between axonal terminals. The vascular permeability of low-molecular-weight (LMW) molecules was higher at perivascular protrusions than at the smooth vascular surface. Axonal terminals containing OXT and AVP were more likely to localise at perivascular protrusions than at the smooth vascular surface. Chronic salt loading with 2% NaCl significantly induced prominent changes in the shape of pericytes and also increased the number of perivascular protrusions and the surface area of the perivascular space together with elevations in the vascular permeability of LMW molecules. Collectively, these results indicate that the perivascular space of the NH acts as the main diffusion route for OXT and AVP and, in addition, changes in the shape of pericytes and perivascular reconstruction occur in response to an increased demand for neuropeptide release.

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“…The axonal terminals of hypothalamic neurons have been shown to exhibit neurovascular and neuroglial structural plasticity in the ME during the estrous cycle (Prevot, 2002 ; Ojeda et al, 2008 ) and the NH during dehydration and lactation (Miyata et al, 2001 ; Miyata and Hatton, 2002 ). In the NH, Notch signaling has been associated with neurovascular and neuroglial plasticity (Miyata et al, 2004 , 2005 ; Mannari and Miyata, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

New aspects in fenestrated capillary and tissue dynamics in the sensory circumventricular organs of adult brains

2015

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The blood–brain barrier (BBB) generally consists of endothelial tight junction barriers that prevent the free entry of blood-derived substances, thereby maintaining the extracellular environment of the brain. However, the circumventricular organs (CVOs), which are located along the midlines of the brain ventricles, lack these endothelial barriers and have fenestrated capillaries; therefore, they have a number of essential functions, including the transduction of information between the blood circulation and brain. Previous studies have demonstrated the extensive contribution of the CVOs to body fluid and thermal homeostasis, energy balance, the chemoreception of blood-derived substances, and neuroinflammation. In this review, recent advances have been discussed in fenestrated capillary characterization and dynamic tissue reconstruction accompanied by angiogenesis and neurogliogenesis in the sensory CVOs of adult brains. The sensory CVOs, including the organum vasculosum of the lamina terminalis (OVLT), subfornical organ (SFO), and area postrema (AP), have size-selective and heterogeneous vascular permeabilities. Astrocyte-/tanycyte-like neural stem cells (NSCs) sense blood- and cerebrospinal fluid-derived information through the transient receptor potential vanilloid 1, a mechanical/osmotic receptor, Toll-like receptor 4, a lipopolysaccharide receptor, and Nax, a Na-sensing Na channel. They also express tight junction proteins and densely and tightly surround mature neurons to protect them from blood-derived neurotoxic substances, indicating that the NSCs of the CVOs perform BBB functions while maintaining the capacity to differentiate into new neurons and glial cells. In addition to neurogliogenesis, the density of fenestrated capillaries is regulated by angiogenesis, which is accompanied by the active proliferation and sprouting of endothelial cells. Vascular endothelial growth factor (VEGF) signaling may be involved in angiogenesis and neurogliogenesis, both of which affect vascular permeability. Thus, recent findings advocate novel concepts for the CVOs, which have the dynamic features of vascular and parenchymal tissues.

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Activity‐Dependent Notch Signalling in the Hypothalamic‐Neurohypophysial System of Adult Mouse Brains

Cited by 5 publications

References 60 publications

Advances in Understanding of Structural Reorganization in the Hypothalamic Neurosecretory System

Advances in Understanding of Structural Reorganization in the Hypothalamic Neurosecretory System

Structural Reconstruction of the Perivascular Space in the Adult Mouse Neurohypophysis During an Osmotic Stimulation

New aspects in fenestrated capillary and tissue dynamics in the sensory circumventricular organs of adult brains

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