Differential localization of Ca2+ channel ?1 subunits in the enteric nervous system: Presence of ?1B channel-like immunoreactivity in intrinsic primary afferent neurons

Kirchgessner, Annette L.; Liu, M.-T.

doi:10.1002/(sici)1096-9861(19990621)409:1<85::aid-cne7>3.0.co;2-x

Cited by 35 publications

(45 citation statements)

References 72 publications

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“…In the adult ENS, N-, P/Q-, L-and R-type Ca 2ϩ currents have been recorded, mostly from guinea pig myenteric neurons (Kirchgessner and Liu, 1999;Starodub and Wood, 1999;Reis et al, 2000;Bian and Galligan, 2007 (Talavera et al, 2008). Several TRP channels are expressed in the mature ENS (Boesmans et al, 2011) and also in parts of the developing mammalian nervous system that are also of neural crest origin, including embryonic dorsal root ganglion neurons (Tamura et al, 2005;Elg et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Early Emergence of Neural Activity in the Developing Mouse Enteric Nervous System

Hao¹,

Boesmans²,

Abbeel³

et al. 2011

J. Neurosci.

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Neurons of the enteric nervous system (ENS) arise from neural crest cells that migrate into and along the developing gastrointestinal tract. A subpopulation of these neural-crest derived cells express pan-neuronal markers early in development, shortly after they first enter the gut. However, it is unknown whether these early enteric "neurons" are electrically active. In this study we used live Ca 2ϩ imaging to examine the activity of enteric neurons from mice at embryonic day 11.5 (E11.5), E12.5, E15.5, and E18.5 that were dissociated and cultured overnight. PGP9.5-immunoreactive neurons from E11.5 gut cultures responded to electrical field stimulation with fast [Ca 2ϩ ] i transients that were sensitive to TTX and -conotoxin GVIA, suggesting roles for voltage-gated Na ϩ channels and N-type voltage-gated Ca 2ϩ channels. E11.5 neurons were also responsive to the nicotinic cholinergic agonist, dimethylphenylpiperazinium, and to ATP. In addition, spontaneous [Ca 2ϩ ] i transients were present. Similar responses were observed in neurons from older embryonic gut. Wholecell patch-clamp recordings performed on E12.5 enteric neurons after 2-10 h in culture revealed that these neurons fired both spontaneous and evoked action potentials. Together, our results show that enteric neurons exhibit mature forms of activity at early stages of ENS development. This is the first investigation to directly examine the presence of neural activity during enteric neuron development. Along with the spinal cord and hindbrain, the ENS appears to be one of the earliest parts of the nervous system to exhibit electrical activity.

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Section: Discussionmentioning

confidence: 99%

Early Emergence of Neural Activity in the Developing Mouse Enteric Nervous System

Hao¹,

Boesmans²,

Abbeel³

et al. 2011

J. Neurosci.

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“…Consistent with this idea, pheromone stimulation of the vomeronasal organ, distention of the colon, seizure activity in the cerebellum or forskolin treatment of spinal cord neurons give rise to N-channel-dependent increases in pCREB and ⁄ or c-fos (Ha et al, 1997;Campbell & Hess, 1998;Kirchgessner & Liu, 1999;Takasaki et al, 2005;Murakami et al, 2006). However, in some of these studies, whether N-channels directly initiate transcriptional events or act indirectly by controlling release of neurotransmitter, which stimulates downstream signal transduction cascades, is unclear (Campbell & Hess, 1998;Takasaki et al, 2005;Murakami et al, 2006).…”

Section: Introductionmentioning

confidence: 92%

“…However, in some of these studies, whether N-channels directly initiate transcriptional events or act indirectly by controlling release of neurotransmitter, which stimulates downstream signal transduction cascades, is unclear (Campbell & Hess, 1998;Takasaki et al, 2005;Murakami et al, 2006). In other cases, the firing frequency that initiated N-channel activity was not measured (Ha et al, 1997;Kirchgessner & Liu, 1999). However, in the case of fetal petrosal ganglia neurons, N-channel activity during phasic (5 Hz) membrane depolarization stimulates gene expression (Brosenitsch & Katz, 2001).…”

Section: Introductionmentioning

confidence: 99%

Ca²⁺ influx through both L‐ and N‐type Ca²⁺ channels increases c‐fos expression by electrical stimulation of sympathetic neurons

Zhao

Liu

Rittenhouse

2007

Eur J of Neuroscience

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During direct membrane depolarization, Ca2+ influx primarily through L-type Ca2+ (L-) channels initiates activity-dependent gene transcription. This is surprising given that in most neurons a minority of the total Ca2+ current arises from L-channel activity. However, many studies have stimulated Ca2+ influx with unphysiological stimuli such as chronic membrane depolarization using high K+ medium. Few studies have tested whether other Ca2+ channels stimulate gene transcription in adult neurons as a consequence of direct electrical stimulation. Therefore, we evaluated the role of L- and N-type Ca2+ (N-) channel activity in regulating mRNA levels of c-fos, an activity-dependent transcription factor, in adult rat superior cervical ganglion (SCG) neurons as the majority of Ca2+ channels are N-type, while only a minority are L-type. Changes in c-fos mRNA levels were measured using semi-quantitative and single-cell RT-PCR. Phosphorylation of CREB (pCREB) and changes in c-Fos levels were visualized in dissociated cells by immunocytochemistry. Increases in pCREB, c-fos mRNA and c-Fos protein with either K+ or electrical depolarization required Ca2+ influx. These results support previous findings that elevated c-fos levels result from pCREB stimulating c-fos transcription. Elevation of pCREB, c-fos and c-Fos with K+ depolarization depended on L-channel activity. By contrast, antagonizing either channel at 10-Hz stimulation minimized these increases despite unequal numbers of the two channel types. Transition to exclusive L-channel involvement occurred with increasing frequency of stimulation (from 10 to 20 to 50 Hz). Our results demonstrate that N- and L-channel participation in regulating c-fos expression is encoded in the pattern of electrical stimulation.

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“…These L-, P/Q-, N-, R-, and T-types are now designated Ca v 1.1-1.4, Ca v 2.1-2.3, and Ca v 3.1-3.3 (Ertel et al 2000;Hille 2001). On the other hand, by using immunohistochemistry at least three (P/Q-type, N-type, L-type) Ca 2+ channel α 1 subunits have been identified in the ENS of the rat and guinea pig intestine (Kirchgessner and Liu 1999). Further, the Ca 2+ entry pathway including L-type Ca 2+ channel exists in the mammalian colonic epithelia (Lindqvist et al 1998;Harvey et al 2002).…”

confidence: 99%

L-Type Ca2+ Channels in the Enteric Nervous System Mediate Oscillatory Cl- Secretion in Guinea Pig Colon

Nishikitani

Yasuoka

Kawada

et al. 2007

Tohoku J. Exp. Med.

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Differential localization of Ca2+ channel ?1 subunits in the enteric nervous system: Presence of ?1B channel-like immunoreactivity in intrinsic primary afferent neurons

Cited by 35 publications

References 72 publications

Early Emergence of Neural Activity in the Developing Mouse Enteric Nervous System

Early Emergence of Neural Activity in the Developing Mouse Enteric Nervous System

Ca²⁺ influx through both L‐ and N‐type Ca²⁺ channels increases c‐fos expression by electrical stimulation of sympathetic neurons

L-Type Ca2+ Channels in the Enteric Nervous System Mediate Oscillatory Cl- Secretion in Guinea Pig Colon

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Differential localization of Ca2+ channel ?1 subunits in the enteric nervous system: Presence of ?1B channel-like immunoreactivity in intrinsic primary afferent neurons

Cited by 35 publications

References 72 publications

Early Emergence of Neural Activity in the Developing Mouse Enteric Nervous System

Early Emergence of Neural Activity in the Developing Mouse Enteric Nervous System

Ca2+ influx through both L‐ and N‐type Ca2+ channels increases c‐fos expression by electrical stimulation of sympathetic neurons

L-Type Ca2+ Channels in the Enteric Nervous System Mediate Oscillatory Cl- Secretion in Guinea Pig Colon

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Ca²⁺ influx through both L‐ and N‐type Ca²⁺ channels increases c‐fos expression by electrical stimulation of sympathetic neurons