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J Dent Res 82(9): 677-681, 2003
© 2003 International and American Associations for Dental Research

RESEARCH REPORT
Biomaterials & Bioengineering

Galanin-immunoreactive Nerve Fibers in the Periodontal Ligament during Experimental Tooth Movement

T. Deguchi, N. Takeshita, T.A. Balam, Y. Fujiyoshi, and T. Takano-Yamamoto*

Department of Orthodontics, Okayama University Graduate School of Medicine and Dentistry, 2-5-1, Shikata-cho, Okayama, 700, Japan;

* corresponding author, t_yamamo{at}md.okayama-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Neuropeptides have been suggested to play a role in pain transmission during orthodontic tooth movement. We examined this hypothesis by examining the effect of orthodontic tooth movement on the expression of galanin (GAL)-immunoreactive (ir) nerve fibers in the periodontal ligament (PDL) of one mesial root (MR) and two distal roots (DRs) of the rat maxillary first molar. In control rats, GAL-ir fibers were very rare in the PDL. One day after the insertion of the elastic band, the number of GAL-ir fibers increased, becoming most numerous at 3 days. From 5 to 28 days, GAL-ir fibers tended to decrease. Electron microscopic observation showed that all of the GAL-ir fibers were unmyelinated. These findings suggest that GAL-containing nerve fibers in the PDL may play an important role in the response of the tissue to experimental tooth movement.

KEY WORDS: galanin • tooth movement • periodontal ligament • rat


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Orthodontic tooth movement causes various histological changes in the periodontal ligament (PDL) (Rygh, 1973; Takano-Yamamoto et al., 1992). In one of those histological changes, periodontal nerves have been considered to respond to orthodontic force (Ohtake, 1982). Orthodontic tooth movement may initiate pain by stimulating peripheral nerves to release mediators, such as neuropeptides. Clinically, after the orthodontic force has been applied, patients feel pain from 1 to 2 days, continuing until 3 to 7 days, and gradually diminishing day by day (Ngan et al., 1989). There have been some reports indicating that the number of nerve fibers containing neuropeptides such as calcitonin gene-related peptide (CGRP) and substance P (SP) in the PDL increased during experimental tooth movement (Kvinnsland and Kvinnsland, 1990; Saito et al., 1991).

Galanin (GAL) is a 29-amino-acid peptide originally isolated from porcine intestine (Tatemoto et al., 1983). It has been shown to occur in the small neurons in the sensory ganglia, which suggests that GAL may play a role in the transmission of nociceptive information (Ch’ng et al., 1985; Skofitsch and Jacobowitz, 1985a; Matsuda et al., 1990; Wakisaka et al., 1996). Following nerve injury, GAL is known to increase within the dorsal root ganglion neurons and in the corresponding primary afferent terminals in the superficial dorsal horn of the spinal cord (Hökfelt et al., 1987; Villar et al., 1989). Furthermore, GAL is down-regulated in primary afferent neurons following inflammation (Ji et al., 1995).

In the present study, GAL-containing nerve fibers in the PDL of the rat first maxillary molar were examined during experimental tooth movement. Changes in the number of GAL-positive nerve fibers were found in PDL at 1, 3, 5, 7, 14, and 28 days after an application of orthodontic force. Electron microscopic observation showed that these GAL-containing nerve fibers were unmyelinated.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Tooth Movement and Tissue Preparation
Thirty-six male Sprague-Dawley rats (body weight, 200–250 g) were deeply anesthetized with pentobarbital sodium (40 mg/kg, i.p.), and a piece of orthodontic elastic band (1 x 1 x 0.8 mm) was then inserted interproximally between the maxillary right first and second molars (Waldo, 1953) (Fig. 1Go). After 1, 3, 5, 7, 14, and 28 days, rats (n = 6 on each day) were re-anesthetized with ether to the level at which respiration was suppressed. They were then perfused with saline, followed by 4% formaldehyde (freshly prepared from paraformaldehyde) in 0.1 M phosphate buffer (pH 7.4). Another 6 rats that did not have the elastic placed were used as the control group. For the immunoelectron microscopic study, in addition to the experimental and the control groups, 4 rats were deeply anesthetized with pentobarbital sodium (40 mg/kg, i.p.), and a piece of orthodontic elastic band was inserted as previously described. Three days after insertion of the band, they were re-anesthetized with ether and perfused with saline followed by 0.1% glutaraldehyde and 4% formaldehyde in 0.1 M phosphate buffer (pH 7.4). Maxillae containing right molar teeth were dissected and decalcified with 4.13% ethylene diaminetetraacetic acid disodium (EDTA) in 0.1 M phosphate buffer (pH 7.4) for 1 wk at room temperature. These tissues were soaked overnight in 20% sucrose in phosphate buffer and cut sagitally into 50-µm-thick serial sections with a cryostat. The experiment was approved by the Animal Committee of the Okayama University Dental School.



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  		Figure 1. Schematic drawing indicates the method of experimental tooth movement. A piece of elastic band (E) was inserted between the upper first (M1) and second (M2) molars. GAL-ir nerve fibers were counted in the boxed area in the mesial root (MR) and distal roots (DR). Each root was divided into equal thirds perpendicular to the long axis of the tooth. The coronal extent of the root was demarcated by the adjacent alveolar crest, and the apical extent of the root was demarcated by the most apical extent of the PDL. C = coronal, I = intermediate, A = apical. Arrows indicate the direction of the force.

 
Immunohistochemistry
GAL-ir nerve fibers were visualized by means of the ABC (avidin-biotin-horseradish peroxidase complex) method. Briefly, sections were incubated with rabbit anti-galanin serum (1:5000; Peninsula Lab., Belmont, CA, USA) for 3 days at 4°C followed by 1 hr of incubation with biotinylated anti-rabbit IgG and 1 hr with ABC complex (Vector Labs., Burlingame, CA, USA) at room temperature. Immunoreactive products were visualized by use of the nickel/ammonium-sulfate-intensified diaminobenzidine reaction. For light microscopic analysis, sections were dehydrated in a graded series of alcohols, cleared in xylene, and cover-slipped with Entellan (Merck, Darmstadt, Germany). For electron microscopic analysis, GAL-stained sections were post-fixed in 1% osmium tetroxide in 0.1 M phosphate buffer (pH 7.4), dehydrated through a graded series of ethanols, and embedded in Polybed 812. Some sections were examined without further staining, whereas others were analyzed after having been stained with lead citrate for 10–40 sec, so that the diaminobenzidine reaction could be checked. The specificities of the antibodies used have been described elsewhere (Ichikawa and Helke, 1993).

Histomorphometry
For the histomorphometric analysis, we selected serial sections from each rat that included the apical foramen and the root pulp—16 sections per mesial root (MR), 9 sections per distal buccal root (DBR), and 7 sections per distal lingual root (DLR). The roots were then equally divided into 3 regions (coronal, intermediate, and apical) for description of the location of GAL-ir nerve fibers within the PDL (Fig. 1Go). The GAL-ir fibers were traced and counted in the region of interest under a Nikon light microscope. The average number of GAL-ir fibers was calculated for each rat and compared between and among groups. The difference in the numbers of GAL-ir fibers between the control and the experimental groups at each time was then examined by two-way analysis of variance and Scheffé’s F test for post hoc comparison. P < 0.05 was taken as the level of significance.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Histomorphometry of the GAL-ir Nerve Fibers
The PDL of the first molar in control rats contained only a few GAL-ir fibers. Such nerve fibers were mostly found in the intermediate region of the PDL. They had a fine and varicose appearance, and were accompanied by small blood vessels adjacent to the alveolar bone (Fig. 2aGo). In contrast, in the experimental rats, GAL-ir fibers were mainly dispersed around the apical regions, with a few in the intermediate regions, but they were rarely found in the coronal regions of the PDL. Most of the GAL-ir fibers in the experimental rats showed a varicose appearance; however, rarely, some showed a smooth appearance from 5 to 14 days after the experimental tooth movement. Those smooth-type GAL-ir fibers were mainly observed at the intermediate region. At the intermediate and the coronal regions, GAL-ir fibers were so rare that there were no significant differences between the days. Most of the GAL-ir nerve fibers were observed within nerve bundles or associated with blood vessels.



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  		Figure 2. GAL-ir nerve fibers at 0 day (a), 1 day (b,c), 3 days (d,e), 5 days (f,g), 14 days (h), and 28 days (i) after the insertion of an elastic band in the PDL of the distal buccal root (a,b,d,f,i) and the mesial root (c,e,g,h) of the first molar. Photographs a, f, and i were taken at the intermediate region, whereas the others were taken at the apical region. Arrows indicate varicosities of GAL-ir nerve fibers. Most of these fibers were observed at the apical region and were associated with the blood vessels. Marked increase of GAL-ir nerve fibers was observed after 3 days (d,e). Arrowhead indicates smooth GAL-ir nerve fibers (f). These smooth types were observed, after 5 days of treatment, predominantly in the intermediate region. Scale bars = 20 µm. AL = alveolar bone, PL = periodontal ligament, V = blood vessel.

 
In the control animals, the number of GAL-ir nerve fibers was 0.1 ± 0.1 per mm2 in the DBR, 0.1 ± 0.1 per mm2 in the DLR, and 0.1 ± 0.1 per mm2 in the MR (average ± SD, n = 6; Figs. 2aGo, 3Go). There were no significant differences between the number of GAL-ir fibers among the roots in control animals. A marked increase in the number of GAL-ir fibers was observed at 1 day (6.4 ± 1.1 per mm2 in the DBR, 4.2 ± 1.0 per mm2 in the DLR, and 1.0 ± 0.5 per mm2 in the MR; p < 0.05; Figs. 2bGo, 2cGo, 3Go) and at 3 days (11.8 ± 1.1 per mm2 in the DBR, 13.7 ± 2.3 per mm2 in the DLR, and 3.7 ± 1.4 per mm2 in the MR; p < 0.05 compared with 1 day; Figs. 2dGo, 2eGo, 3Go) of tooth movement. GAL-ir fibers in both DRs decreased rapidly from 5 days (7.7 ± 2.3 per mm2 in DBR, and 7.1 ± 2.8 per mm2 in DLR; p < 0.05 compared with 3 days; Figs. 2fGo, 2gGo, 3Go) to 28 days (Figs. 2iGo, 3Go). From 1 to 5 days after insertion of the elastic, the DRs showed significantly more GAL-ir fibers than the MR (p < 0.05). At 7 days, GAL-ir fibers were 5.7 ± 2.2 per mm2 in the DBR, 4.0 ± 0.5 per mm2 in DLR, and 2.6 ± 1.0 per mm2 in MR. The number of GAL-ir fibers in the MR decreased gradually from 3 to 28 days (Fig. 3Go). At 14 days, GAL-ir fibers were 1.9 ± 0.2 per mm2 in the DBR, 1.6 ± 0.5 per mm2 in the DLR, and 2.2 ± 0.5 per mm2 in the MR (Figs. 2hGo, 3Go). The number of GAL-ir fibers returned to the control level at 28 days (1.1 ± 0.3 per mm2 in the DBR, 0.7 ± 0.3 per mm2 in the DLR, and 0.6 ± 0.3 per mm2 in the MR; Figs. 2iGo, 3Go).



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  		Figure 3. Change in the number of GAL-ir nerve fibers in PDL at 0, 1, 3, 5, 7, 14, and 28 days during experimental tooth movement. Day 0 represents the control group. The areas evaluated for histomorphometry were 1.74 ± 0.07 mm2 for the 2 DRs and 2.28 ± 0.09 mm2 for the MR. aSignificantly different from control group (p < 0.05). bSignificantly different from the day 1 group (p < 0.05). cSignificantly different from the day 3 group (p < 0.05). dSignificant difference between the distal and mesial roots (p < 0.05). Each value indicates average ± SD (n = 6). DLR = distal lingual root, DBR = distal buccal root, MR = mesial root.

 
Immunoelectron Microscopic Observation
GAL-ir fibers were easily identified by the electron-dense granular precipitates in their axoplasm, seen under the electron microscope (Fig. 4Go). All GAL-ir fibers were unmyelinated, having the typical structure of multiple axons sharing a single sheath of Schwann cell cytoplasm. Some GAL-ir fibers were located adjacent to blood vessels. No reaction product was detected in the Schwann cell.



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  		Figure 4. Immunoelectron microscopic photographs showing GAL immunoreaction in the apical region of the distal root of the first molar at 3 days after the insertion of an elastic band. GAL-ir products (arrow) were all located in the axoplasm of unmyelinated fibers that were mostly associated with blood vessels. The Schwann sheaths were always devoid of GAL-ir (arrowhead). Scale bars = 0.5 µm. V = blood vessel, CO = collagen fibers, F = fibroblast, My = Myelinated nerve, SS = Schwann sheaths.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study demonstrated the increase in the nerve fibers expressing GAL-ir in the PDL of the maxillary first molar during experimental tooth movement in the rat. The number of GAL-ir fibers in the PDL was increased at 1 day and showed a marked increase 3 days after initiation of experimental tooth movement. From 5 days after the insertion of the elastic, the number of GAL-ir fibers tended to decrease, and returned to control levels at 28 days.

In the previous studies, the expression of neuropeptides such as CGRP-ir fibers is known to increase during experimental tooth movement (Kvinnsland and Kvinnsland, 1990; Saito et al., 1991). Saito and colleagues suggested that neuropeptides such as CGRP are directly or indirectly associated with tissue remodeling during experimental tooth movement (Saito et al., 1991). In the present study, the expression of GAL-ir in nerve fibers showed a pattern similar to that of CGRP during experimental tooth movement. Furthermore, 3 days after the placement of the elastic, the changes in the osteoclastic activity increase, persisting until 5 days and tending to decrease thereafter in the PDL (Waldo, 1953; Takano-Yamamoto et al., 1992; Yamashiro et al., 2000). Therefore, GAL-ir nerve fibers in the PDL might be involved in tissue responses during experimental tooth movement. However, further investigations are necessary to elucidate the role of GAL in tissue remodeling such as bone remodeling during experimental tooth movement.

More GAL-ir fibers were observed in the distal roots compared with those in the mesial root from 1 to 5 days after the insertion of the elastic. In a study with finite element stress analysis, it was concluded that orthodontically induced bone remodeling and locations of osteogenesis uniquely coincided with increased tension within the PDL (Katona et al., 1995). According to this study, the apical region of the distal root had the most concentrated stress distribution. The mesial root is much longer and wider than the distal roots and may have more resistance against the orthodontic force. Moreover, we observed more extrusion at the apical region of the PDL in distal roots than in the mesial root. Since the elastic was inserted between the first and second molars, the mechanical stress may have distributed more around the closer distal roots than around the mesial root. Thus, the increase in GAL-ir fibers may be related to the amount of mechanical force induced by experimental tooth movement.

During orthodontic tooth movement, patients feel pain or discomfort from the continuous pressure on the PDL (Jones and Chan, 1992). We previously demonstrated that experimental tooth movement induced c-fos expression in the superficial layers of the ipsilateral medullary dorsal horn and in the trigeminal subnucleus oralis in rats (Fujiyoshi et al., 2000). We indicated that there were two different responses during experimental movement (Fujiyoshi et al., 2000). The first response occurred at 2 hrs at the ipsilateral medullary dorsal horn level after the orthodontic force was applied and then immediately disappeared, whereas the second response appeared at the trigeminal subnucleus oralis much later, with a peak intensity on day two, and lasted for a few days. It is suggested that the trigeminal subnucleus oralis may play an important role in nociceptive information from the intra-oral receptive fields (Sugimoto et al., 1998). In our study, the number of GAL-ir fibers in the PDL showed a marked increase at day 3, lasting until 5 days after the force application. Thus, the similar time courses of the changes in the GAL-ir fibers in the PDL suggest that GAL may play a role in pain transmission, especially in delayed nociceptive response during experimental tooth movement.

The origin of the GAL-ir fibers is unclear, because GAL-ir neurons are located in the cranial sensory and autonomic ganglia (Ch’ng et al., 1985; Lindh et al., 1989). Sensory and sympathetic neurons in the trigeminal and superior cervical ganglia, respectively, are immunoreactive for GAL. The present immunoelectron microscopic observation demonstrates that the morphology of GAL-ir nerve endings was identical to that of free nerve endings. Furthermore, from previous findings, GAL-ir neurons were small in the trigeminal ganglion (Ch’ng et al., 1985; Skofitsch and Jacobowitz, 1985b), and it is known that the small sensory neurons supply their peripheral receptive fields with free nerve endings. Thus, such fibers containing GAL might at least partly originate from the sensory ganglion, i.e., the trigeminal ganglion. However, further investigation is necessary to clarify whether the change in the number of GAL-ir fibers is due to increased expression of GAL-ir in existing fibers or to increased innervation by GAL-ir fibers.

The existence and function of GAL in the PDL have never been reported previously. Neuropeptides such as CGRP and some other peptides have been suggested to play a role in sensory transmission, especially nociception (Cridland and Henry, 1988; Ryu et al., 1988). CGRP is derived from precursor proteins in the nerve cell bodies in the trigeminal ganglion, from which the peptide is transported via axonal flow to sensory branches in oral tissues (Amara et al., 1982; Silverman and Kruger, 1987). These neuropeptides, including GAL, are widely distributed in the primary sensory neurons. GAL has been shown to localize mainly in small neurons (Skofitsch and Jacobowitz, 1985b; Ju et al., 1987), whereas CGRP has been detected in small to large neurons (Ju et al., 1987). The co-existence of CGRP and GAL also has been shown in small ganglion cells (Ju et al., 1987). Intrathecal GAL selectively blocks the excitatory effect of Substance P and CGRP on spinal flexor reflex excitability (Wiesenfeld-Hallin et al., 1989), and after injury, GAL has been proposed to act as an endogenous anti-nociceptive modulator of spinal cord excitability (Wiesenfeld-Hallin et al., 1992). Thus, the increase in GAL-ir nerve fibers during experimental tooth movement may represent up-regulation of GAL for its antinociceptive effects in the spinal cord.


   ACKNOWLEDGMENTS
 
We thank Dr. Hiroyuki Ichikawa for his support and guidance, and Dr. Lawrence P. Garetto of the Indiana University School of Dentistry for his review of this manuscript. This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan (13557183).

Received April 3, 2002; Last revision April 29, 2003; Accepted May 30, 2003


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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