Guinea-pig sympathetic postganglionic neurones contain haem oxygenase-2

Vollerthun, R; Höhler, Brigitte; Kummer, Wolfgang

doi:10.1097/00001756-199512290-00042

Cited by 19 publications

(10 citation statements)

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“…The viability of the in-vitro preparations used for this experiment and the efficiency of axonal transport in this model were demonstrated by the accumulation of SP immunoreactivity at the crush, and the efficiency of HO-2 immunohistochemistry was verified by positive labelling of neuronal cell bodies in the same preparation. In contrast to the findings obtained for the central processes of sensory neurons in this study, we have found HO-2 immunoreactivity in a small number of noradrenergic sympathetic axons following crushing of the guinea-pig sciatic nerve (Vollerthun et al 1995), and a few thick HO-2-immunoreactive nerve trunks have been reported in the feline oesophagus (Ny et al 1995) and in some perivascular axons in rat (Zakhary et al 1996). Thus, HO-2 is not completely excluded from axons in all types of peripheral neurons, but its amount appears to be low in this compartment.…”

Section: Discussioncontrasting

confidence: 99%

Heme oxygenase-2 in primary afferent neurons of the guinea-pig

Vollerthun

Höhler

Kummer

1996

Histochem Cell Biol

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Sensory ganglia (trigeminal, jugular, nodose, cervical and lumbar dorsal root ganglia) of the guinea-pig were investigated for the presence of a constitutive carbon monoxide-generating enzyme, heme oxygenase-2 (HO-2). A 36-kDa HO-2 immunoreactive protein was identified by Western blotting in protein extracts from dorsal root ganglia and localized by immunohistochemistry to all neuronal perikarya, including both substance P-positive and substance P-negative neurons, in all ganglia investigated. This ubiquitous distribution points to a general requirement for HO-2 in primary afferent neurons rather than to an association with a specific functionally defined subpopulation. Neither the axons of the sensory neurons nor their peripheral terminals in the skin and around visceral arteries were HO-2 immunoreactive. Explants of dorsal root ganglia with crushes placed on the dorsal roots showed accumulation of the neuropeptide, substance P, at the ganglionic side of the crush, but these axons were non-reactive to HO-2, indicating that there is no substantial transport of HO-2 towards the central ending of these sensory neurons. Collectively, the findings suggest that HO-2 exerts it major effects within the sensory ganglia themselves.

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Section: Discussioncontrasting

confidence: 99%

Heme oxygenase-2 in primary afferent neurons of the guinea-pig

Vollerthun

Höhler

Kummer

1996

Histochem Cell Biol

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“…4). Peripheral autonomic ganglion neurons express HO-2 (25,26). Membrane potential was measured in superior mesenteric ganglion neurons of mice to determine whether CO acts as a hyperpolarizing factor in these postganglionic sympathetic neurons.…”

Section: Resultsmentioning

confidence: 99%

A major role for carbon monoxide as an endogenous hyperpolarizing factor in the gastrointestinal tract

Farrugia

Sha

Lü

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

106

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Carbon monoxide (CO) is proposed as a physiological messenger. CO activates cGMP and has a direct effect on potassium channels. Both actions of CO lead to hyperpolarization of a cell's resting membrane potential, suggesting that CO may function as a hyperpolarizing factor, although direct evidence is still lacking. Here we take advantage of the known membrane potential gradient that exists in the muscle layers of the gastrointestinal tract to determine whether CO is an endogenous hyperpolarizing factor. We find that heme oxygenase-2-null mice have depolarized smooth muscle cells and that the membrane potential gradient in the gut is abolished. Exogenous CO hyperpolarizes the membrane potential. Regions of the canine gastrointestinal tract that are more hyperpolarized generate more CO and have higher heme oxygenase activity than more depolarized regions. Our results suggest that CO is a critical hyperpolarizing factor required for the maintenance of intestinal smooth muscle membrane potential and gradient.A role for carbon monoxide (CO) is proposed in cell signaling and neurotransmission (1, 2), hormone release (3, 4), as a cytoprotective agent (5), and in regulation of vascular tone (6, 7). The major source of CO is from the breakdown of heme by heme oxygenase (HO); the absence of HO-2, the constitutive HO isoform, significantly impairs the production of CO in gut and other tissues (8). HO-2 is widely expressed in tissues containing smooth muscle, including blood vessels (6), the pulmonary system (9), and the gastrointestinal tract (10), suggesting that CO is continually produced in these tissues. Multiple mechanisms of action for CO have been proposed, including activation of guanylyl cyclase and direct activation of K ϩ channels (11). Both mechanisms can result in membrane hyperpolarization, raising the possibility that CO can act as an endogenous hyperpolarizing factor. To determine whether CO is an endogenous hyperpolarizing factor, we took advantage of the known membrane potential gradients that exist in the muscle layers of the gastrointestinal tract. We chose the gastrointestinal tract as our model because our previous studies in the HO-2-null mouse demonstrate that intestinal smooth muscle is depolarized in the HO-2-null mouse (2), and because of the presence of a measurable smooth muscle membrane potential gradient that has not been reported in vascular smooth muscle. We hypothesized that if CO acts as a physiologically relevant hyperpolarizing factor, then CO production should mirror the membrane potential gradient along the long axis of the stomach as well as across the gut wall and that these resting membrane potential gradients would be diminished or abolished in HO-2-null mice. In the gastrointestinal tract of all species studied, there is a large gradient (Ϸ30 mV) in membrane potential along the long axis of the stomach from the fundus (proximal stomach) to the pylorus (distal stomach) (12). There is also a membrane potential gradient across the thickness of circular muscle layer (12, 13). In the ...

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“…There seems to be a specific differential distribution of the enzymes HO2 and NO synthase in autonomic ganglia. In these ganglia, the enzyme HO2 exists in the perikarya and dendrites of principal neurons but not in axons or presynaptic nerve terminals (Vollerthun et al, 1995(Vollerthun et al, , 1996Zakhary et al, 1996;Magnusson et al, 2000). In contrast, NO synthase exists in sympathetic preganglionic neurons (Blottner and Baumgarten, 1992;Dun et al, 1992;Valtschanoff et al, 1992) and has been localized mainly within preganglionic nerve terminals in sympathetic ganglia (Dun et al, 1993;Morris et al, 1993;Saito et al, 1994;Anderson et al, 1995;Okamura et al, 1995;Klimaschewski et al, 1996b).…”

Section: Discussionmentioning

confidence: 99%

“…It is produced by the enzyme heme oxygenase-2 (HO2) when it transforms heme to biliverdin. In sympathetic ganglia, HO2 is reported to be present only in cell bodies and some dendrites of postganglionic principal neurons, but none was found in preganglionic nerve terminals (Vollerthun et al, 1995). Because CO is, in many ways, similar to NO, we examined the possibility of involvement of CO in the induction and maintenance of LTP in the SCG of the rat.…”

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confidence: 99%

Retrograde Carbon Monoxide Is Required for Induction of Long-Term Potentiation in Rat Superior Cervical Ganglion

et al. 2001

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Carbon monoxide (CO), produced in the body by the enzyme heme oxygenase (HO), has been suggested as a retrograde synaptic messenger with a prominent role in the long-term potentiation (LTP) of certain areas of the brain. LTP of sympathetic ganglia is 5-HT 3 receptor-dependent and has been shown to require nitric oxide for the maintenance, but not for the induction, phase. We investigated the possibility of CO being required for the induction of ganglionic LTP. Pretreatment of rat isolated superior cervical ganglia with oxyhemoglobin (25-100 M) completely blocked LTP. In the same ganglia, prolonged washout of oxyhemoglobin did not uncover any potentiation of the compound action potential. Oxyhemoglobin had no significant effect on the maintenance phase in ganglia with established LTP. Pretreatment of ganglia with the HO inhibitor zinc protoporphyrin-IX (ZnPP) (10 M) completely and irreversibly prevented the expression of tetanus-evoked LTP. However, in the same ganglia, after superfusion of CO in the presence of ZnPP, tetanic stimulation readily evoked LTP. No effect was seen on the maintenance phase when ZnPP was superfused on ganglia with established LTP. Pretreatment of ganglia with the 5-HT 3 receptor antagonist ondansetron (0.4 M) alone completely and irreversibly blocked LTP. However, in the presence of CO, ondansetron did not block LTP. These results suggest that activation of 5-HT 3 receptors may be involved in the production of CO. The results also suggest that CO, probably originating outside the presynaptic nerve terminal, is involved in the induction of LTP.

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Guinea-pig sympathetic postganglionic neurones contain haem oxygenase-2

Cited by 19 publications

References 0 publications

Heme oxygenase-2 in primary afferent neurons of the guinea-pig

Heme oxygenase-2 in primary afferent neurons of the guinea-pig

A major role for carbon monoxide as an endogenous hyperpolarizing factor in the gastrointestinal tract

Retrograde Carbon Monoxide Is Required for Induction of Long-Term Potentiation in Rat Superior Cervical Ganglion

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