Acquisition of cholinergic and peptidergic properties by sympathetic innervation of rat sweat glands requires interaction with normal target

Schotzinger, Robert J.; Landis, Story C.

doi:10.1016/0896-6273(90)90037-g

Cited by 129 publications

(62 citation statements)

References 60 publications

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“…Nevertheless, our data clearly show that expression of CHT increases dramatically following initial target contact. These data are consistent with previous studies suggesting that the innervation lacks cholinergic markers before and during initial plexus development (Schotzinger and Landis, 1990a;Stevens and Landis, 1988).…”

Section: Discussionsupporting

confidence: 83%

“…The suppression of noradrenergic properties involves decreasing the catecholamine synthesizing enzymes TH and dopamine-β-hydroxylase (DBH) , along with the TH cofactor BH4 (Habecker et al, 2002). The loss of catecholamines is accompanied by a coordinated increase in ChAT and VAChT, and the expression of acetylcholinesterase, VIP and calcitonin-gene related peptide (CGRP) (Landis, 1990;Landis and Keefe, 1983;Schotzinger and Landis, 1990a). Despite our detailed knowledge of many aspects of this developmental switch in neurotransmitter phenotype, until recently the tools were not available to examine the expression of CHT, which controls the rate-limiting step in ACh production.…”

Section: Discussionmentioning

confidence: 99%

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Developmental expression of the high affinity choline transporter in cholinergic sympathetic neurons

Guidry

Willison

Blakely

et al. 2005

Autonomic Neuroscience

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Choline uptake by the high affinity choline transporter (CHT) is the rate-limiting step in acetylcholine synthesis. Induction of CHT is therefore a critical step in cholinergic differentiation, and we examined the developmental expression of CHT in cholinergic sympathetic neurons that innervate rodent sweat glands. During postnatal development the earliest sympathetic axons in the rear footpads are noradrenergic, containing intense tyrosine hydroxylase immunoreactivity and lacking CHTimmunoreactivity (CHT-IR). By postnatal day 7 (P7) in mouse, and P10 in rat, weak CHT-IR appeared in axons associated with the sweat gland anlagen. CHT staining intensity increased during the following weeks in conjunction with plexus arborization and gland maturation. The pattern of CHT-immunoreactivity (CHT-IR) in the sweat gland innervation was similar to staining for the vesicular acetylcholine transporter and vasoactive intestinal peptide. Immunoblots of tissue from sympathectomized rats confirmed that most of the CHT in footpad was contained in sympathetic neurons. Although CHT expression has been reported in noradrenergic sympathetic neurons of the superior cervical ganglion, these data indicate that in the sympathetic neurons projecting to sweat glands CHT is present at detectable levels only after association with the glands.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

Developmental expression of the high affinity choline transporter in cholinergic sympathetic neurons

Guidry

Willison

Blakely

et al. 2005

Autonomic Neuroscience

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“…In addition to cholinergic markers, the mature sweat gland innervation contains immunoreactivity for two neuropeptides, VIP and CGRP. VIP is induced in sympathetic neurons by cholinergic differentiation factors in vitro (Nawa et al, 1991;Rao and Landis, 1993) and by sweat glands in vivo (Schotzinger and Landis, 1990;Schotzinger et al, 1994).…”

Section: Catecholamines Are Not Required For the Appearance Of Cholinmentioning

confidence: 99%

Catecholamines Are Required for the Acquisition of Secretory Responsiveness by Sweat Glands

et al. 2000

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The sympathetic innervation of sweat glands undergoes a developmental change in transmitter phenotype from catecholaminergic to cholinergic. Acetylcholine elicits sweating and is necessary for development and maintenance of secretory responsiveness, the ability of glands to produce sweat after nerve stimulation or agonist administration. To determine whether catecholamines play a role in the development or function of this system, we examined the onset of secretory responsiveness in two transgenic mouse lines, one albino and the other pigmented, that lack tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholamine synthesis. Although both lines lack TH, their catecholamine levels differ because tyrosinase in pigmented mice serves as an alternative source for catecholamine synthesis (Rios et al., 1999). At postnatal day 21 (P21), 28 glands on average are active in interdigital hind footpads of albino TH wild-type mice. In contrast, fewer than one gland is active in albino TH null mice, which lack catecholamines in gland innervation. Treatment of albino TH null mice with DOPA, a catecholamine precursor, from P11 to P21 increases the number of active glands to 14. Pigmented TH null mice, which have faint catecholamine fluorescence in the developing gland innervation, possess 12 active glands at P21, indicating that catecholamines made via tyrosinase, albeit reduced from wild-type levels, support development of responsiveness. Gland formation and the appearance of cholinergic markers occur normally in albino TH null mice, suggesting that catecholamines act directly on gland cells to trigger their final differentiation and to induce responsiveness. Thus, catecholamines, like acetylcholine, are essential for the development of secretory responsiveness.

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“…Because of signals derived from this target, adrenergic traits such as catecholamine production are downregulated, whereas the induction of cholinergic features, like choline acetyl transferase (ChAT), vesicular acetylcholine transporter (VAChT) and the co-expressed neuropeptide vasoactive intestinal peptide (VIP), leads to a functionally cholinergic sweat gland innervation. The importance of the target tissue for this transmitter phenotype switch to occur has been firmly established by sweat gland transplantation, by replacement by parotid gland (Schotzinger and Landis, 1990) and by analysis of the tabby mouse mutant, which is devoid of sweat glands (Guidry and Landis, 1995). Cholinergic sympathetic neurons innervate, as additional target tissues, the skeletal muscle vasculature and the periosteum, the connective tissue covering the bone.…”

Section: Introductionmentioning

confidence: 99%

Target-dependent specification of the neurotransmitter phenotype:cholinergic differentiation of sympathetic neurons is mediated in vivo by gp130 signaling

et al. 2006

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Sympathetic neurons are generated through a succession of differentiation steps that initially lead to noradrenergic neurons innervating different peripheral target tissues. Specific targets, like sweat glands in rodent footpads, induce a change from noradrenergic to cholinergic transmitter phenotype. Here, we show that cytokines acting through the gp130 receptor are present in sweat glands. Selective elimination of the gp130 receptor in sympathetic neurons prevents the acquisition of cholinergic and peptidergic features (VAChT, ChT1, VIP) without affecting other properties of sweat gland innervation. The vast majority of cholinergic neurons in the stellate ganglion, generated postnatally, are absent in gp130-deficient mice. These results demonstrate an essential role of gp130-signaling in the target-dependent specification of the cholinergic neurotransmitter phenotype.

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Acquisition of cholinergic and peptidergic properties by sympathetic innervation of rat sweat glands requires interaction with normal target

Cited by 129 publications

References 60 publications

Developmental expression of the high affinity choline transporter in cholinergic sympathetic neurons

Developmental expression of the high affinity choline transporter in cholinergic sympathetic neurons

Catecholamines Are Required for the Acquisition of Secretory Responsiveness by Sweat Glands

Target-dependent specification of the neurotransmitter phenotype:cholinergic differentiation of sympathetic neurons is mediated in vivo by gp130 signaling

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