Neuronal porosome – The secretory portal at the nerve terminal: Its structure–function, composition, and reconstitution

Jena, Bhanu P.

doi:10.1016/j.molstruc.2014.04.055

Cited by 5 publications

(5 citation statements)

References 97 publications

(153 reference statements)

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“…[ 26 27 ] Since both control and chronic HIWN-exposed animals demonstrate the decreased size of docked synaptic vesicles compared to undocked vesicles, the fractional discharge of vesicular content via porosome-mediated kiss-and-run mechanism of synaptic vesicle fusion and neurotransmitter release at large axon terminal is interfered. [ 17 18 ] This observation is consistent with our earlier findings, demonstrating that the exposure of cats to chronic noise alters the main structural parameters of porosome complex, i.e. its diameter and depth.…”

Section: Discussionsupporting

confidence: 92%

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Electron Microscopy Demonstrating Noise Exposure Alters Synaptic Vesicle Size in the Inferior Colliculus of Cat

et al. 2021

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Context: White noise is known to have detrimental effects on different brain regions, especially auditory regions, including inferior colliculus. Although the basis for such alterations has been hypothesized to result from abnormalities in neurotransmitter release, the mechanism is unclear. The final step in neurotransmission is the docking and transient fusion of synaptic vesicles at the base of cup-shaped lipoprotein structures called porosomes at the presynaptic membrane and the consequent release of neurotransmitters. Earlier studies in cat brain document altered morphology of the secretory portal the porosome at nerve terminals in the inferior colliculus following white noise exposure. The current study was performed to test the hypothesis of possible changes to synaptic vesicle size in the colliculus, following white noise exposure. Material and Methods: Electron microscopic morphometry of synaptic vesicles size in axo-dendritic synapses at the colliculus region of the cat brain was performed. Results: We report, for first time, decreased size of both docked and undocked vesicles in high-intensity white noise-exposed animals. In both control and experimental animals, docked vesicles are demonstrated to be smaller than undocked vesicles, suggesting fractional discharge of vesicular contents via porosome-mediated kiss-and-run mechanism. Conclusion: These studies advance our understanding of neurotransmitter release and the impact of white noise on brain function.

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Section: Discussionsupporting

confidence: 92%

“…The final steps in neurotransmission are the docking and fusion of synaptic vesicles at the presynaptic membrane, including the “kiss-and-run” mechanism mediated by the 15 nm cup-shaped lipoprotein porosome structures [ Figure 1 ]. [ 17 18 ]…”

Section: Introductionmentioning

confidence: 99%

Electron Microscopy Demonstrating Noise Exposure Alters Synaptic Vesicle Size in the Inferior Colliculus of Cat

et al. 2021

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“…Despite detailed analysis, we did not observe significant changes in the fine morphology of porosome complexsecretory machinery of cell, directly related to the neurotransmission (Cho et al, 2004;Jena, 2015). Therefore, we do not exclude that fine alterations take place before synaptic vesicles dock with the synaptic membrane.…”

Section: Discussionmentioning

confidence: 65%

“…For this purpose, the images of the axon terminals were enlarged onto the computer screen and each vesicle and cristae were sequentially marked, using the brush tool. For the measurement of opening diameter and the depth of porosome complex-secretory machinery of cell (Cho et al, 2004;Jena, 2015), totally 201 synaptic profiles were observed: n = 101 in PPA-treated brain and n = 100-in PBS-treated brain. Quantitative data were analysed using the Minitab software.…”

Section: Quantitative Analysismentioning

confidence: 99%

Behavioural and brain ultrastructural changes following the systemic administration of propionic acid in adolescent male rats. Further development of a rodent model of autism

Lobzhanidze

Japaridze²,

Lordkipanidze

et al. 2020

Intl J of Devlp Neuroscience

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Short chain fatty acids, produced as gut microbiome metabolites but also present in the diet, exert broad effects in host physiology. Propionic acid (PPA), along with butyrate and acetate, plays a growing role in health, but also in neurological conditions. Increased PPA exposure in humans, animal models and cell lines elicit diverse behavioural and biochemical changes consistent with organic acidurias, mitochondrial disorders and autism spectrum disorders (ASD). ASD is considered a disorder of synaptic dysfunction and cell signalling, but also neuroinflammatory and neurometabolic components. We examined behaviour (Morris water and radial arm mazes) and the ultrastructure of the hippocampus and medial prefrontal cortex (electron microscopy) following a single intraperitoneal (i.p.) injection of PPA (175 mg/kg) in male adolescent rats. PPA treatment showed altered social and locomotor behaviour without changes in learning and memory. Both transient and enduring ultrastructural alterations in synapses, astro‐ and microglia were detected in the CA1 hippocampal area. Electron microscopic analysis showed the PPA treatment significantly decreased the total number of synaptic vesicles, presynaptic mitochondria and synapses with a symmetric active zone. Thus, brief systemic administration of this dietary and enteric short chain fatty acid produced behavioural and dynamic brain ultrastructural changes, providing further validation of the PPA model of ASD.

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“…Results from this study provide critical insights into the aetiology of CF disease and for potential therapies. Similarly, recent studies using mass spectrometry provide some understanding of the lipidome of the neuronal porosome complex , and the role of Hsp90 in porosome assembly and function , enabling further understanding of the porosome structure–function . Currently, for further understand porosome structure–function, the major focus of our laboratory is to determine the distribution and interaction of proteins and lipids within the porosome complex using chemical crosslinking followed by mass spectrometry, and molecular modelling.…”

Section: Discovery Of the ‘Porosome’mentioning

confidence: 99%

‘Porosome’ discovered nearly 20 years ago provides molecular insights into the kiss‐and‐run mechanism of cell secretion

Jena

2015

J Cellular Molecular Medi

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Secretion is a fundamental cellular process in living organisms, from yeast to cells in humans. Since the 1950s, it was believed that secretory vesicles completely merged with the cell plasma membrane during secretion. While this may occur, the observation of partially empty vesicles in cells following secretion suggests the presence of an additional mechanism that allows partial discharge of intra-vesicular contents during secretion. This proposed mechanism requires the involvement of a plasma membrane structure called ‘porosome’, which serves to prevent the collapse of secretory vesicles, and to transiently fuse with the plasma membrane (Kiss-and-run), expel a portion of its contents and disengage. Porosomes are cup-shaped supramolecular lipoprotein structures at the cell plasma membrane ranging in size from 15 nm in neurons and astrocytes to 100–180 nm in endocrine and exocrine cells. Neuronal porosomes are composed of nearly 40 proteins. In comparison, the 120 nm nuclear pore complex is composed of >500 protein molecules. Elucidation of the porosome structure, its chemical composition and functional reconstitution into artificial lipid membrane, and the molecular assembly of membrane-associated t-SNARE and v-SNARE proteins in a ring or rosette complex resulting in the establishment of membrane continuity to form a fusion pore at the porosome base, has been demonstrated. Additionally, the molecular mechanism of secretory vesicle swelling, and its requirement for intra-vesicular content release during cell secretion has also been elucidated. Collectively, these observations provide a molecular understanding of cell secretion, resulting in a paradigm shift in our understanding of the secretory process.

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Neuronal porosome – The secretory portal at the nerve terminal: Its structure–function, composition, and reconstitution

Cited by 5 publications

References 97 publications

Electron Microscopy Demonstrating Noise Exposure Alters Synaptic Vesicle Size in the Inferior Colliculus of Cat

Electron Microscopy Demonstrating Noise Exposure Alters Synaptic Vesicle Size in the Inferior Colliculus of Cat

Behavioural and brain ultrastructural changes following the systemic administration of propionic acid in adolescent male rats. Further development of a rodent model of autism

‘Porosome’ discovered nearly 20 years ago provides molecular insights into the kiss‐and‐run mechanism of cell secretion

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