Identification and mechanosensitivity of viscerofugal neurons

Hibberd, Timothy J.; Zagorodnyuk, Vladimir; Spencer, Nick J.; Brookes, Simon Jonathan

doi:10.1016/j.neuroscience.2012.08.040

Cited by 38 publications

(29 citation statements)

References 39 publications

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“…Several studies have reported distinct mechanosensitive responses in enteric neurons to tensile stress (stretch), compressive stress (volume injection, glass probe, or von Frey hair), shear stress, and cell swelling (hypoosmotic solutions) (Dong, Jiang, Dong, & Mittal, 2014; Hibberd, Zagorodnyuk, Spencer, & Brookes, 2012; Kugler et al, 2015; Kunze et al, 1999; Kunze, Clerc, Furness, & Gola, 2000; Kunze et al, 1998; Mayer & Wood, 1975; Mazzuoli & Schemann, 2009, 2012; Spencer & Smith, 2004). While these studies suggest roles in mechanosen-sitivity sensing and control of muscle activity, as well as a servo-feedback loop (Mazzuoli-Weber & Schemann, 2015), the identities of the mechano-sensitive ion channels responsible for mechanotransduction are largely unknown.…”

Section: Mechanosensitive Ion Channelsmentioning

confidence: 99%

Mechanosensitive Piezo Channels in the Gastrointestinal Tract

Alcaino

Farrugia

Beyder

2017

Current Topics in Membranes

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Sensation of mechanical forces is critical for normal function of the gastrointestinal (GI) tract and abnormalities in mechanosensation are linked to GI pathologies. In the GI tract there are several mechanosensitive cell types—epithelial enterochromaffin cells, intrinsic and extrinsic enteric neurons, smooth muscle cells and interstitial cells of Cajal. These cells use mechanosensitive ion channels that respond to mechanical forces by altering transmembrane ionic currents in a process called mechanoelectrical coupling. Several mechanosensitive ionic conductances have been identified in the mechano-sensory GI cells, ranging from mechanosensitive voltage-gated sodium and calcium channels to the mechanogated ion channels, such as the two-pore domain potassium channels K2P (TREK-1) and nonselective cation channels from the transient receptor potential family. The recently discovered Piezo channels are increasingly recognized as significant contributors to cellular mechanosensitivity. Piezo1 and Piezo2 are nonselective cationic ion channels that are directly activated by mechanical forces and have well-defined biophysical and pharmacologic properties. The role of Piezo channels in the GI epithelium is currently under investigation and their role in the smooth muscle syncytium and enteric neurons is still not known. In this review, we outline the current state of knowledge on mechanosensitive ion channels in the GI tract, with a focus on the known and potential functions of the Piezo channels.

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Section: Mechanosensitive Ion Channelsmentioning

confidence: 99%

Mechanosensitive Piezo Channels in the Gastrointestinal Tract

Alcaino

Farrugia

Beyder

2017

Current Topics in Membranes

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“…134 At least some of these neurons in the distal bowel project directly to the spinal cord. [136][137][138] Viscerofugal neurons have been shown to be directly mecha-nosensitive 139,140 but are also synaptically activated by enteric circuitry. 140,141 Their axons project in mesenteric nerves, pelvic nerves and possibly splanchnic nerves and contribute to recorded action potential discharge in colonic nerves.…”

Section: Viscerofugal Enteric Primary Afferentsmentioning

confidence: 99%

“…140,141 Their axons project in mesenteric nerves, pelvic nerves and possibly splanchnic nerves and contribute to recorded action potential discharge in colonic nerves. 140 …”

Section: Viscerofugal Enteric Primary Afferentsmentioning

confidence: 99%

Extrinsic primary afferent signalling in the gut

Brookes

Spencer

Costa

et al. 2013

Nat Rev Gastroenterol Hepatol

240

216

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Visceral sensory neurons activate reflex pathways that control gut function and also give rise to important sensations, such as fullness, bloating, nausea, discomfort, urgency and pain. Sensory neurons are organised into three distinct anatomical pathways to the central nervous system (vagal, thoracolumbar and lumbosacral). Although remarkable progress has been made in characterizing the roles of many ion channels, receptors, and second messengers in visceral sensory neurons, the basic aim of understanding how many classes there are, and how they differ, has proven difficult to achieve. We suggest that there are just five structurally distinct types of sensory endings in the gut wall that account for essentially all of the primary afferent neurons in the three pathways. Each of these five major structural types of endings seems to show distinctive combinations of physiological responses. These types are: 'intraganglionic laminar' endings in myenteric ganglia; 'mucosal' endings located in the subepithelial layer; 'muscular mucosal' afferents, with mechanosensitive endings close to the muscularis mucosae; 'intramuscular' endings, with endings within the smooth muscle layers; and 'vascular' afferents, with sensitive endings primarily on blood vessels. 'Silent' afferents might be a subset of inexcitable 'vascular' afferents, which can be switched on by inflammatory mediators.Extrinsic sensory neurons comprise an attractive focus for targeted therapeutic intervention in a range of gastrointestinal disorders.2

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“…Whether VGLUT 2 -IR nonpeptidergic DRG neurons are both the origin of the MPG baskets, as well as of the neuropil surrounding myenteric plexus neurons in the mouse colorectum (see Section 3.4), and participate in sensory-motor coupling remains to be demonstrated. Finally, one additional source could be viscerofugal neurons projecting towards the MPG, found in rat [196], guinea pig [197], and mouse [198]. Interestingly, we recently showed a small subpopulation of myenteric neurons expressing VGLUT 2 mRNA in the mouse colorectum [61] (see below).…”

Section: Expression Of Vgluts In Autonomic Gangliamentioning

confidence: 99%

VGLUTs in Peripheral Neurons and the Spinal Cord: Time for a Review

Brumovsky

2013

ISRN Neurology

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Vesicular glutamate transporters (VGLUTs) are key molecules for the incorporation of glutamate in synaptic vesicles across the nervous system, and since their discovery in the early 1990s, research on these transporters has been intense and productive. This review will focus on several aspects of VGLUTs research on neurons in the periphery and the spinal cord. Firstly, it will begin with a historical account on the evolution of the morphological analysis of glutamatergic systems and the pivotal role played by the discovery of VGLUTs. Secondly, and in order to provide an appropriate framework, there will be a synthetic description of the neuroanatomy and neurochemistry of peripheral neurons and the spinal cord. This will be followed by a succinct description of the current knowledge on the expression of VGLUTs in peripheral sensory and autonomic neurons and neurons in the spinal cord. Finally, this review will address the modulation of VGLUTs expression after nerve and tissue insult, their physiological relevance in relation to sensation, pain, and neuroprotection, and their potential pharmacological usefulness.

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Identification and mechanosensitivity of viscerofugal neurons

Cited by 38 publications

References 39 publications

Mechanosensitive Piezo Channels in the Gastrointestinal Tract

Mechanosensitive Piezo Channels in the Gastrointestinal Tract

Extrinsic primary afferent signalling in the gut

VGLUTs in Peripheral Neurons and the Spinal Cord: Time for a Review

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