Differential distribution and regulation of galanin receptors- 1 and -2 in the rat lumbar spinal cord

doi:10.1016/j.brainres.2006.02.088

Brain Research

Volume 1085, Issue 1, 26 April 2006, Pages 111-120

https://doi.org/10.1016/j.brainres.2006.02.088 Get rights and content

Abstract

The expression of the galanin receptor-1 and -2 (Gal₁ and Gal₂) messenger ribonucleic acids (mRNAs) was studied in the lower spinal cord of rat by means of in situ hybridization, using ribonucleic acid probes (riboprobes). Naïve rats as well as rats with unilateral axotomy of the sciatic nerve or unilateral inflammation of the hindpaw were analyzed. In naïve rats, numerous Gal₁ mRNA-positive (+) neurons were detected in lamina (L) I–III. In addition, several Gal₁ mRNA⁺ neurons were seen in deeper layers, including the ventral horns, area X, and the lateral spinal nucleus. In contrast, few and comparatively weakly labeled Gal₂ mRNA⁺ neurons were observed, mostly in the ventral horns and in area X, with fewer in the dorsal horn and in the sympathetic and parasympathetic intermediate lateral cell columns. Axotomy induced a strong increase in intensity and number of Gal₂ mRNA⁺ motoneurons ipsilateral to the lesion. In contrast, nerve cut or hindpaw inflammation did not alter the expression of Gal₁ or Gal₂ in the dorsal horn. The present (and previous) results suggest that galanin, acting through Gal₁ and Gal₂ receptors, has a modulatory role on spinal excitability, not only via interneurons in superficial dorsal horn, but also on neurons in deep layers and area X, as well as on the sympathetic and parasympathetic outflow. Furthermore, the nerve injury-induced Gal₂ upregulation in motor neurons suggests a role for galanin in survival/regeneration mechanisms.

Introduction

The 29 amino acid (30 in humans) galanin peptide (Tatemoto et al., 1983) has a wide distribution in the nervous system, and there is evidence for involvement in a wide variety of neuronal functions (see Bartfai et al., 1993, Counts et al., 2003, Crawley, 1995, Fuxe et al., 1998, Hökfelt et al., 2005, Merchenthaler et al., 1993, Ögren et al., 1998, Robinson, 2004, Vrontakis, 2002). So far three galanin receptors have been cloned, the first one (Gal₁) from a human melanoma cell line by Habert-Ortoli et al. (1994) and subsequently also the corresponding rat receptor (Burgevin et al., 1995, Gustafson et al., 1996, Parker et al., 1995). Soon after Gal₂ and Gal₃ were identified (see Branchek et al., 1998, Branchek et al., 2000, Iismaa and Shine, 1999). The cellular localization of these receptors have so far mainly been demonstrated with in situ hybridization, whereby Gal₁ and Gal₂ mRNAs appear to have a more widespread distribution in the rat brain than Gal₃ mRNA (Gustafson et al., 1996, Mennicken et al., 2002, O'Donnell et al., 1999, O'Donnell et al., 2003, Parker et al., 1995). In situ hybridization has also provided evidence for presence of Gal₁ and Gal₂ mRNA in dorsal root ganglia (DRGs) and spinal cord (Gustafson et al., 1996, Kerekes et al., 2003, O'Donnell et al., 1999, Parker et al., 1995, Shi et al., 1997, Xu et al., 1996a, Xu et al., 1996b, Zhang et al., 1998). Using RT-PCR, Waters and Krause (2000) have analyzed all three receptors in various central and peripheral tissues and identified Gal_1–3 in DRGs and spinal cord. Finally, there are immunohistochemical studies reporting on the distribution of Gal₁ and Gal₂ in the nervous system (Anselmi et al., 2005, Jimenez-Andrade et al., 2004, Landry et al., submitted for publication, Larm et al., 2003, Pham et al., 2002, Suzuki and Dickenson, 2000).

In the spinal cord, in situ hybridization has so far mainly shown presence of numerous small Gal₁ mRNA-positive (+) neurons in the superficial layers of the dorsal horn, although the study by O'Donnell et al. (1999), focusing on Gal₂, also reported a wide distribution of Gal₁ in the lumbar spinal cord. More recently, Gal₁ protein was observed with immunohistochemistry in local dorsal horn neurons in lamina (L) II with a dense plexus of processes surrounding the cell bodies, as well as some larger neurons in deeper layers (Landry et al., submitted for publication). Interestingly, while undetectable in the facial motor nucleus under normal conditions, Gal₂ mRNA has been shown to be upregulated 3 and 7 days after facial nerve crush or axotomy (Burazin and Gundlach, 1998). However, no studies have analyzed this situation at the spinal cord level. Here, we reinvestigate the distribution of Gal₁ and Gal₂ mRNA in the rat lower spinal cord using in situ hybridization based on riboprobes, including analyses of the effect of unilateral peripheral axotomy and inflammation.

Section snippets

Animals

The experiments were performed on eighteen male Sprague–Dawley rats (body weight: 250–300 g; B and K, Stockholm, Sweden). The animals were maintained under standard conditions on a 12-h day/night cycle (light on 07:00 a.m.), with water and food ad libitum.

The procedures and lesions were approved by the local ethical committee (Stockholms Norra Djurförsöksetiska Nämnd; #249/01, 335/01, 219/03, 130/02) and are in accordance with the policy of the Society of Neuroscience on the use of animals in

Naïve rats

Numerous Gal₁ mRNA⁺ neurons were observed in the dorsal horn of the thoraco-lumbar (Fig. 1a), lumbar (Fig. 1c), and the lumbo-sacral (Fig. 1e) spinal cord, with a few cells in the lateral spinal nucleus (Fig. 1c). Their distribution varied between different layers, with the highest density of Gal₁ mRNA⁺ neurons in LI–III (Fig. 1, Fig. 2, Fig. 3). However, many Gal₁ mRNA⁺ neurons could also be observed in LIV and deeper, in particular at the lumbo-sacral level (Fig. 1, Fig. 2, Fig. 3). In

Discussion

The present study extends earlier in situ hybridization analyses of the distribution of Gal₁ and Gal₂ in the rat spinal cord (Gustafson et al., 1996, O'Donnell et al., 1999, Parker et al., 1995, Zhang et al., 1998) and provide a detailed account of these two receptors at the lower spinal level. Thus, Gal₁ mRNA⁺ neurons are present in all dorsal horn layers, with some neurons in the lateral spinal nucleus. Particularly at the lumbo-sacral level, several GalR₁ mRNA⁺ neurons extend into the dorsal

Conclusions

In this study, we re-visit the expression of galanin receptors in the rat spinal cord and show that Gal₂, but not Gal₁, is dramatically upregulated in motor neurons after peripheral nerve axotomy. Gal₂ receptors could be targets for somatodendritically released galanin upregulated in the motoneurons after peripheral nerve injury, representing attempts to survive and to promote regeneration. The extensive distribution of Gal₁ in the dorsal horn provides multiple sites for involvement of galanin

Acknowledgments

This study was supported by the Swedish Research Council (04X-2887), the Marianne and Marcus Wallenberg Foundation, and the Knut and Alice Wallenberg Foundation. PB was supported by a Carrillo Oñativia Grant, Austral University, and the Karolinska Institutet.

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In the spinal nervous system, the expression of galanin (GAL) and galanin receptors (GALRs) that play important roles in the transmission and modulation of nociceptive information can be affected by nerve injury. However, in the trigeminal nervous system, the effects of trigeminal nerve injury on the expression of GAL are controversy in the previous studies. Besides, little is known about the effects of trigeminal nerve injury on the expression of GALRs. In the present study, the effects of trigeminal nerve injury on the expression of GAL and GALRs in the rat trigeminal ganglion (TG) were investigated by using quantitative real-time reverse transcription-polymerase chain reaction and immunohistochemistry. To identify the nerve-injured and nerve-uninjured TG neurons, activating transcription factor 3 (ATF3, the nerve-injured neuron marker) was stained by immunofluorescence. The levels of GAL mRNA in the rostral half and caudal half of the TG dramatically increased after transection of infraorbital nerve (ION) and inferior alveolar nerve (IAN), respectively. Immunohistochemical labeling of GAL and ATF3 revealed that GAL level was elevated in both injured and adjacent uninjured small and medium-sized TG neurons after ION/IAN transection. In addition, the levels of GAL₂R-like immunoreactivity were reduced in both injured and adjacent uninjured TG neurons after ION/IAN transection, while levels of GAL₁R and GAL₃R-like immunoreactivity remained unchanged. Furthermore, the number of small to medium-sized TG neurons co-expressing GAL- and GAL₁R/GAL₂R/GAL₃R-like immunoreactivity was significantly increased after ION/IAN transection. In line with previous studies in other spinal neuron systems, these results suggest that GAL and GALRs play functional roles in orofacial neuropathic pain and trigeminal nerve regeneration after trigeminal nerve injury.
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Diabetic peripheral neuropathic pain (DPNP) is a distal spontaneous pain, caused by lesion of sensory neurons and accompanied by depression and anxiety frequently, which reduce life quality of patients and increase society expenditure. To date, antidepressants, serotonin-noradrenaline reuptake inhibitors and anticonvulsants are addressed as first-line therapy to DPNP, alone or jointly. It is urgently necessary to develop novel agents to treat DPNP and its complications. Evidences indicate that neuropeptide galanin can regulate multiple physiologic and pathophysiological processes. Pain, depression and anxiety may upregulate galanin expression. In return, galanin can modulate depression, anxiety, pain threshold and pain behaviors. This article provides a new insight into regulative effects of galanin and its subtype receptors on antidepressant, antianxiety and against DPNP. Through activating GALR1, galanin reinforces depression-like and anxiogenic-like behaviors, but exerts antinociceptive roles. While via activating GALR2, galanin is referred to as anti-depressive and anti-anxiotropic compounds, and at low and high concentration facilitates and inhibits nociceptor activity, respectively. The mechanism of the galanin roles is relative to increase in K⁺ currents and decrease in Ca²⁺ currents, as well as neurotrophic and neuroprotective roles. These data are helpful to develop novel drugs to treat DPNP and its complications.
A preliminary study on DRGs and spinal cord of a galanin receptor 2-EGFP transgenic mouse
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Therefore, the main bulk of information on galanin receptors (Gal1–3-R) stems from studies on their transcripts. Thus, as shown with in situ hybridization (ISH), qPCR and/or single cell analysis, transcripts for Gal1-R and Gal2-R are found at substantial levels in neurons in DRGs (Chiu et al., 2014; Costigan et al., 2002; Hobson et al., 2006; Kerekes et al., 2003; Sten Shi et al., 1997; Usoskin et al., 2015; Xiao et al., 2002; Xu et al., 1996) and in the spinal cord (2008; Brumovsky et al., 2006; Haring et al., 2018; O'Donnell et al., 1999; Serafin et al., 2019). This said, Jimenz-Andrade et al. used anti-receptor antibodies and demonstrated, in rat, presence of Gal2-R-like immunoreactivity (LI) both in many DRG neuron cell bodies and peripheral digital nerve axons (Jimenez-Andrade et al., 2004).
The neuropeptide galanin functions via three G-protein coupled receptors, Gal₁_–₃-R. Both Gal₁-R and ₂-R are involved in pain signaling at the spinal level. Here a Gal₂-R-EGFP transgenic (TG) mouse was generated and studied in pain tests and by characterizing Gal₂-R expression in both sensory ganglia and spinal cord. After peripheral spared nerve injury, mechanical allodynia developed and was ipsilaterally similar between wild type (WT) and TG mice. A Gal₂-R-EGFP-positive signal was primarily observed in small and medium-sized dorsal root ganglion (DRG) neurons and in spinal interneurons and processes. No significant difference in size distribution of DRG neuronal profiles was found between TG and WT mice. Both percentage and fluorescence intensity of Gal₂-R-EGFP-positive neuronal profiles were overall significantly upregulated in ipsilateral DRGs as compared to contralateral DRGs. There was an ipsilateral reduction in substance P-positive and calcitonin gene-related peptide (CGRP)-positive neuronal profiles, and this reduction was more pronounced in TG as compared to WT mice. Moreover, Gal₂-R-EGFP partly co-localized with three pain-related neuropeptides, CGRP, neuropeptide Y and galanin, both in intact and injured DRGs, and with galanin also in local neurons in the superficial dorsal horn. Taken together, the present results provide novel information on the localization and phenotype of DRG and spinal neurons expressing the second galanin receptor, Gal₂-R, and on phenotypic changes following peripheral nerve injury. Gal2-R may also be involved in autoreceptor signaling.
Spinal neuropeptide expression and neuropathic behavior in the acute and chronic phases after spinal cord injury: Effects of progesterone administration
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At the dorsal horn, profuse galanin [16,17] and NPY [18,19] immunoreactive neuropils can be detected, corresponding to both primary afferent endings and local interneurons, the latter mainly located in laminae I–III. Regarding galanin and NPY receptors, GalR1 is expressed by numerous dorsal horn interneurons [20], while Y1R is found both in local interneurons and projection neurons [21]. In contrast, GalR2 and Y2R show a more restricted distribution, respectively confined to a small subpopulation of dorsal horn neurons [20] and primary afferent endings [22,23].
Patients with spinal cord injury (SCI) develop chronic pain that severely compromises their quality of life. We have previously reported that progesterone (PG), a neuroprotective steroid, could offer a promising therapeutic strategy for neuropathic pain. In the present study, we explored temporal changes in the expression of the neuropeptides galanin and tyrosine (NPY) and their receptors (GalR1 and GalR2; Y1R and Y2R, respectively) in the injured spinal cord and evaluated the impact of PG administration on both neuropeptide systems and neuropathic behavior. Male rats were subjected to spinal cord hemisection at T13 level, received daily subcutaneous injections of PG or vehicle, and were evaluated for signs of mechanical and thermal allodynia. Real time PCR was used to determine relative mRNA levels of neuropeptides and receptors, both in the acute (1 day) and chronic (28 days) phases after injury. A significant increase in Y1R and Y2R expression, as well as a significant downregulation in GalR2 mRNA levels, was observed 1 day after SCI. Interestingly, PG early treatment prevented Y1R upregulation and resulted in lower NPY, Y2R and GalR1 mRNA levels. In the chronic phase, injured rats showed well-established mechanical and cold allodynia and significant increases in galanin, NPY, GalR1 and Y1R mRNAs, while maintaining reduced GalR2 expression. Animals receiving PG treatment showed basal expression levels of galanin, NPY, GalR1 and Y1R, and reduced Y2R mRNA levels. Also, and in line with previously published observations, PG-treated animals did not develop mechanical allodynia and showed reduced sensitivity to cold stimulation. Altogether, we show that SCI leads to considerable changes in the spinal expression of galanin, NPY and their associated receptors, and that early and sustained PG administration prevents them. Moreover, our data suggest the participation of galaninergic and NPYergic systems in the plastic changes associated with SCI-induced neuropathic pain, and further supports the therapeutic potential of PG- or neuropeptide-based therapies to prevent and/or treat chronic pain after central injuries.
UVB irradiation induces rapid changes in galanin, substance P and c-fos immunoreactivity in rat dorsal root ganglia and spinal cord
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The individual cell diameters were calculated from the neuronal profile cross-sectional areas, in the individual profiles containing a visible nucleus, under the assumption that the neurons imaged were spherical (using NIS-Elements 3.00 software (Nikon Instruments, Japan)). Neuronal profiles which had a diameter of <35 μm were defined as small-sized, whereas neurons with a diameter of ≥35 μm were classified as medium- to large-sized [7,17]. The number of galanin or SP immunopositive neuronal profiles with a visible nucleus were determined and classified as small-sized or medium- to large-sized neurons.
Recent studies have shown that UVB irradiation induces primary and secondary hyperalgesia in rats and humans peaking about 24 h after UVB exposure. In the present study we investigated the changes in galanin, substance P and c-fos immunoreactivity in rat DRG and spinal cord at the L5 level 2–96 h after UVB irradiation. UVB irradiation of the heel area in rats almost increased the skin blood flow two-fold 24 h after irradiation as measured by laser Doppler technique. UVB irradiation induced a significant reduction of the proportion of galanin positive DRG neurons for all time points, except at 12 h. In the spinal cord, UVB irradiation induced increased immunoreactivity for galanin in the dorsal horn, the area around the central canal and interestingly also in the lateral spinal nucleus 12–96 h after exposure. For substance P the proportion of substance P positive neurons was unchanged but UVB irradiation induced increased substance P immunoreactivity in the dorsal part of the spinal cord 48 h after irradiation. UVB irradiation also induced c-fos immunoreactivity in the dorsal horn and the area around the central canal 24 and 48 h after exposure. This translational model of UVB irradiation will induce rapid changes of neuropeptides implicated in nociceptive signaling in areas known to be of importance for nociception in a time frame, about 24 h after exposure, where also neurophysiological alteration have been described in humans and rats.
The generation of knock-in mice expressing fluorescently tagged galanin receptors 1 and 2
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In mouse spinal cord expression of Gal1 mRNA has previously been detected by northern blot and RT-PCR (Jacoby et al., 2002; Wang et al., 1997), and by ISH was reported as enriched in the dorsal horn (Table 1 of Guo et al., 2012). We detected dense Gal1-mCherry immunofluorescence in the superficial dorsal horn laminae I–II with lesser levels in the lateral spinal nucleus and lamina X, similar to previous rat Gal1 mRNA ISH studies (Brumovsky et al., 2006b; O'Donnell et al., 1999). It will be of interest to determine the expression of other neurochemical markers within intrinsic neurons highly expressing Gal1-mCherry.
The neuropeptide galanin has diverse roles in the central and peripheral nervous systems, by activating the G protein-coupled receptors Gal₁, Gal₂ and the less studied Gal₃ (GalR1–3 gene products). There is a wealth of data on expression of Gal_1–3 at the mRNA level, but not at the protein level due to the lack of specificity of currently available antibodies. Here we report the generation of knock-in mice expressing Gal₁ or Gal₂ receptor fluorescently tagged at the C-terminus with, respectively, mCherry or hrGFP (humanized Renilla green fluorescent protein). In dorsal root ganglia (DRG) neurons expressing the highest levels of Gal₁-mCherry, localization to the somatic cell membrane was detected by live-cell fluorescence and immunohistochemistry, and that fluorescence decreased upon addition of galanin. In spinal cord, abundant Gal₁-mCherry immunoreactive processes were detected in the superficial layers of the dorsal horn, and highly expressing intrinsic neurons of the lamina III/IV border showed both somatic cell membrane localization and outward transport of receptor from the cell body, detected as puncta within cell processes. In brain, high levels of Gal₁-mCherry immunofluorescence were detected within thalamus, hypothalamus and amygdala, with a high density of nerve endings in the external zone of the median eminence, and regions with lesser immunoreactivity included the dorsal raphe nucleus. Gal₂-hrGFP mRNA was detected in DRG, but live-cell fluorescence was at the limits of detection, drawing attention to both the much lower mRNA expression than to Gal₁ in mice and the previously unrecognized potential for translational control by upstream open reading frames (uORFs).

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Research ReportDifferential distribution and regulation of galanin receptors- 1 and -2 in the rat lumbar spinal cord

Abstract

Introduction

Section snippets

Animals

Naïve rats

Discussion

Conclusions

Acknowledgments

Neuropeptides

Neuroscience

Regul. Pept.

Pain

Neuroscience

Neuropeptides

Neurosci. Lett.

Neuropeptides

Pain

Neuroscience

Neuroscience

Exp. Neurol.

Trends Pharmacol. Sci.

J. Chem. Neuroanat.

Prog. Neurobiol.

Neurosci. Lett.

Brain Res. Mol. Brain Res.

Prog. Brain Res.

Peptides

FEBS Lett.

Neuroscience

Eur. J. Pharmacol.

Neuropeptides

Distribution of 125I-galanin binding sites, immunoreactive galanin, and its coexistence with 5-hydroxytryptamine in the cat spinal cord: biochemical, histochemical, and experimental studies at the light and electron microscopic level

J. Comp. Neurol.

Galanin—A neuroendocrine peptide

Curr. Rev. Neurobiol.

Molecular biology and pharmacology of galanin receptors

Ann. N. Y. Acad. Sci.

Galanin receptor subtypes

TiPS

Inducible galanin and GalR2 receptor system in motor neuron injury and regeneration

J. Neurochem.

Cloning, pharmacological characterization, and anatomical distribution of a rat cDNA encoding for a galanin receptor

J. Mol. Neurosci.

Research Report
Differential distribution and regulation of galanin receptors- 1 and -2 in the rat lumbar spinal cord